crocodiles - biology, husbandry and diseases

Plate 1. Adult captive gharials at the Madras Crocodile Bank. Note the ghara, the nasal excrescence, of the malegharial.Plate 2. The right gonad, macroscopically undifferentiated, of a juvenile Nile crocodile can be seen between thespleen and the right kidney. The left gonad is hidden by the mesentery. The yellowish adrenals are almost completely obscured by the paler gonads.Plate 3. The dark-brown right thyroid situated laterally of the right bronchus. The pale right parathyroid is visibleslightly caudally of the thyroid on the right aortic arch, medially of the precaval vein.Plate 4. Fighting male Nile crocodiles on a crocodile farm in South Africa.Plate 5. Oral cavity, gular valve and pharynx exposed after the ventral skin has been removed and the tongue hasbeen cut loose from the mandibles.Plate 6. Cutting lines for a belly skin.

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Plate 7. Spectacled caiman hatchling with the greyish-white crusty lesions of caiman pox on the dorsal and lateralsurfaces of head, body, tail and limbs.Plate 8. Nile crocodile hatchling with ventral, dark-brown crocodile pox lesions in patterns suggesting bite marks.Plate 9. Reddening of the ventral skin of the hind legs and around the cloaca of a juvenile Nile crocodile with septicaemia.Plate 10. Right elbow joint of a juvenile Nile crocodile with exudative arthritis.Plate 11. Heart of an adult Nile crocodile with exudative epicarditis.Plate 12. Hepatozoon sp. gametocyte in a red blood cell of a Nile crocodile.

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Plate 13. Ascaridoids in the stomach of an adult wild-caught Nile crocodile.Plate 14. Juvenile Nile crocodile with fat necrosis involving the thoracic and abdominal fat deposits.Plate 15. Fat necrosis: hardened yellow fat between the tail muscles of a Nile crocodile.Plate 16. Renal gout in a juvenile Nile crocodile with deposits of uric acid in the pelvic portions of the renal folds.Plate 17. Close-up of winter sores on the ventral surface of the tail of a juvenile Nile crocodile.Plate 18. Advanced case of stress dermatitis with lesions affecting all parts of the body.

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Plate 19. Large fungal granuloma on the right hind foot of an adult captive Indo-Pacific crocodile.Plate 20. Exudative enteritis causing the intestine to be grossly distended by the fibrinous exudate.Plate 21. Haemorrhagic enteritis in a juvenile Nile crocodile.Plate 22. Tonsillitis in a juvenile Nile crocodile.Plate 23. Laryngitis in a juvenile Nile crocodile.Plate 24. Lacrimal cyst under the eye of a captive Nile crocodile (photo Marc Gansuana).

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Crocodiles

Biology, Husbandry and Diseases

Crocodiles

Biology, Husbandry and Diseases

F.W. Huchzermeyer

Onderstepoort Veterinary Institute,South Africa

CABI Publishing

CABI Publishing is a division of CAB International

CABI Publishing CABI PublishingCAB International 44 Brattle StreetWallingford 4th FloorOxon OX10 8DE Cambridge, MA 02138UK USA

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© CAB International 2003. All rights reserved. No part of this publicationmay be reproduced in any form or by any means, electronically,mechanically, by photocopying, recording or otherwise, without the priorpermission of the copyright owners.

A catalogue record for this book is available from the British Library,London, UK.

Library of Congress Cataloging-in-Publication Data

Huchzermeyer, F. W. (Fritz W.) Crocodiles : biology, husbandry and diseases / by F. W. Huchzermeyer.

p. cm.Includes bibliographical references (p. ).

ISBN 0-85199-656-61. Crocodile farming. 2. Crocodiles. 3. Captive reptiles. I. Title.

SF515.5.C75 H83 2003639.3�982--dc21

2002013734

ISBN 0 85199 656 6

Typeset in Palatino by Columns Design Ltd, Reading.Printed and bound in the UK by Biddles Ltd, Guildford and King’s Lynn.

Contents

Foreword vii

Disclaimer viii

Introduction ix

1 Crocodiles and Alligators 1The Species of Crocodilians 1Crocodilian Anatomy 6Crocodilian Physiology 32Crocodilian Biochemistry 47Crocodilian Behaviour 52

2 Examination of Crocodiles and Clinical Procedures 57Clinical Examination 57Post-mortem Examination 75Medication 86Surgical Interventions 91

3 Important Aspects of Crocodile Farming 98Nutrition 98Incubation of Crocodile Eggs 102Rearing 107Breeding 118Slaughter 123Crocodiles in Zoos and Private Collections 133Animal Welfare 136

4 Diseases of Eggs and Hatchlings 139Diseases of the Egg 139Diseases of the Yolk-sac 142Hatchling Diseases 145Congenital Malformations 148

5 Transmissible Diseases 157Viral Infections 157Bacterial Infections 163Fungal Infections 176Parasitic Protozoa 182Metazoan Endoparasites 192Ectoparasites 203

v

6 Non-transmissible Diseases 211Nutritional Diseases 211Poisoning 221Multifactorial Diseases 226

7 Organ Diseases and Miscellaneous Conditions 240Skin Diseases 240Eye Diseases 245Diseases of the Digestive System 247Diseases of the Urogenital System 263Diseases of the Nervous System 266Diseases of the Circulatory System 268Diseases of the Respiratory System 270Diseases of the Skeletal–Muscular System 272Diseases of the Endocrine System 274Miscellaneous Pathological Conditions 277

References 292

Index 323

vi Contents

Foreword

Crocodilians have been the subject of international study for hundreds of years. Research ontheir biology began appearing in the literature during the 1800s, increased considerably inthe 1920s and then really took off after the mid-1950s, when funding for academic researchbecame more readily available. These early studies concentrated on various aspects ofpopulation dynamics of the species in the wild, and of crocodilians kept in display centresand zoos.

Husbandry and diseases of crocodiles received early attention by zoo veterinarians andkeepers, but interest in these matters took a dramatic turn upwards once ranching andfarming of the species became a serious business, worth hundreds of millions of dollars.

I well remember some 25 years ago how at meetings of the Crocodile Specialist Group(CSG), someone would mention seeing blemishes on crocodile skins and how this woulddrastically decrease the value of the skins. Soon dozens of husbandry problems and diseasescame to the fore and it became imperative that the issues be looked at in a systematic anddeliberate fashion. More and more researchers became interested in the field, and by the year2000 the CSG had decided to establish, with the encouragement and leadership by Dr FritzHuchzermeyer, a veterinary group within the CSG.

I am delighted to see that Dr Huchzermeyer has put pen to paper and produced this mostimportant and valuable book on husbandry and diseases of crocodilians. It will have manyavid readers.

Professor Harry MesselChairman, CSG

vii

Disclaimer

Although every effort has been made in the collection and presentation of facts the authorcannot accept any responsibility for damages arising from actions based on informationcontained in this book.

viii

Introduction

This book has been written for veterinarians, scientists, wildlife officials, students andcrocodile farmers. The knowledge was gained mainly by my work over many years withfarmed Nile crocodiles, some work with wild and wild-caught African dwarf crocodiles inthe Congo Republic and, in addition, by the study of the available literature, which embracesmost of the other crocodilian species as well. I believe this to be the first comprehensive bookon crocodile diseases.

Being a pathologist, poultry pathologist, and not a clinician, I placed the emphasis in thisbook on the diagnosis and treatment, or rather prevention, of diseases as they occur oncrocodile farms. However, an effort has been made to cover all clinical aspects as well. Ibelieve that my avian background has helped me to grasp the peculiarities of crocodilianphysiology and pathology, while my poultry background has guided me towards a herdhealth approach.

Diseases cannot be understood without a background knowledge of normal bodyfunctions, nor without knowledge of farming conditions. These are therefore treated in asomewhat introductory fashion in the first and third part, without any claim of completeness.

Wherever possible, common names have been used as well as scientific names, in an effortto make the book more accessible. Unless emphasized specifically the term ‘crocodiles’ isused to denote all crocodilians (see Chapter 1).

Basically we know very little about crocodiles and their diseases. Research into theirbiology is carried out and funded in the course of normal biological studies and conservationefforts. However, most veterinary research is centred on domestic animals and may at bestinvolve some of the major wildlife species, possibly stimulated by a need to protect theinhabitants of national parks and zoological gardens. The crocodile farming and ranchingindustries in the various countries are in competition with each other and are most unlikelyto be able to provide funding for a concerted and specialized veterinary research effort.

There are no catastrophic crocodile diseases, and consequently veterinary research willalways be regarded as not so important. I had the good fortune that the Poultry Section of theOnderstepoort Veterinary Institute (OVI) was closed a few years before my retirement andthat I was allowed then to devote all my time to crocodile work. For some years I had somenearby crocodile farms submit practically all their mortalities. The many post-mortemscarried out during that time and the generous permission to make full use of the Institute’slibrary, even up to the present, have laid a foundation of knowledge, on which I became con-fident to tackle writing this book.

The past and present directors of the OVI, Dr D.W. Verwoerd, Dr G.R. Thomson, Dr S.T.Cornelius and Dr F.T. Potgieter, are thanked for the provision of an office for my use andcontinued access to the Institute’s infrastructure since my retirement, as well as for theircontinued interest in my work. The secretary of the now also defunct Pathology Section ofthe OVI, Mrs Mara Stoltz, has always been at hand to solve computer and program problems

ix

most speedily and efficiently, and Mr D. Swanepoel of the Institute’s library and his staffhave been most helpful in trying to procure even the most obscure items of literature.

Over the years I have been most fortunate in having been able to draw on the knowledgeof many colleagues, for which I want to express my gratitude. Many crocodile farmers insouthern Africa have welcomed me on their farms and have allowed me to study theiranimals in their environment. Dr Jenny Turton and Dr Jane Walker reviewed parts of themanuscript and helped me to overcome some of my language problems. To all go myheartfelt thanks.

And, last but not least, I have to thank my wife Hildegard, who not only put up with myperiods of withdrawal while writing, but always showed a keen interest in my work andencouraged me to carry on.

F.W. HuchzermeyerPretoria

June 2002

x Introduction

The Species of Crocodilians

The crocodilians are classified as reptiles,together with lizards, snakes, tuataras andchelonians (tortoises, terrapins and turtles –note that the Americans use the term ‘turtles’for all chelonians), because of their exother-mia and their skin architecture. However,many features, particularly behaviour(vocalizations and parental care), heart mor-phology and fat body, clearly separate themfrom the other reptiles.

All living crocodilians are grouped in thefamily Crocodylidae. They occur in a broadband around the globe in the tropics andsubtropics of the Old and New World. Atpresent the distinctions between subfamilies,genera and species are based mainly onanatomical features, particularly of the skull,and on scale patterns of the skin. DNAanalyses may, in the near future, add newinformation and cause some revisions(Densmore and Owen, 1989; Ray et al., 2001;White and Densmore, 2001). The followingdetails were taken mainly from Ross andMagnusson (1989).

Please note that several common namescan be in use for any one species. An efforthas been made in this book to use only onecommon name per species, as listed below.Many synonyms of the scientific names canbe found in the older literature. Where this

literature is cited, these synonyms have beenreplaced in most cases by the current names.

Crocodiles

The subfamily Crocodylinae contains threegenera: Crocodylus (the true crocodiles, with13 species), Osteolaemus and Tomistoma (eachwith one species).

The genus Crocodylus:C. rhombifer Cuban crocodile CubaC. moreletii Morelet’s crocodile Central AmericaC. acutus American crocodile Central AmericaC. cataphractus African slender- Africa

snouted crocodile (Fig. 1.1)

C. niloticus Nile crocodile Africa and (see Fig. 1.7) Madagascar

C. intermedius Orinoco crocodile South AmericaC. porosus Indo-Pacific Asia and

crocodile AustraliaC. johnsoni Johnston’s crocodile AustraliaC. palustris Mugger (Fig. 1.2) Indian

subcontinentC. siamensis Siamese crocodile AsiaC. mindorensis Philippine Philippines

crocodileC. novaeguineae New Guinea New Guinea

crocodileC. raninus Bornean crocodile Borneo (see

Ross, 1990; Rosset al., 1998)

Chapter 1

Crocodiles and Alligators

© CAB International 2003. Crocodiles: Biology, Husbandry and Diseases(F.W. Huchzermeyer) 1

Due to a consistent spelling error in itsoriginal description, the scientific name ofJohnston’s crocodile is C. johnsoni. As therules of nomenclature do not allow a subse-quent correction, the original spelling of thescientific name must be retained.

The wide distribution of C. porosus in the

Indo-Pacific area, C. niloticus throughoutAfrica and Madagascar, and C. acutus inCentral America is probably due to theirability to tolerate varying degrees of salinity.This has allowed them to spread to differentriver systems and even islands, unlike morelocalized species that do not have any salt

2 Chapter 1

Fig. 1.1. Captive Crocodylus cataphractus at the St Lucia Crocodile Centre.

Fig. 1.2. Captive Crocodylus palustris at the Madras Crocodile Bank.

tolerance. It therefore appears to be incorrectto use the names saltwater and freshwatercrocodiles for C. porosus and C. johnsoni,respectively, outside Australia.

The genus Osteolaemus:O. tetraspis Dwarf crocodile Africa

This has two subspecies, as follows:O. t. tetraspis from coastal West Africa (Fig. 1.3); andO. t. osborni from the Congo basin (Fig. 1.4).

The genus Tomistoma:T. schlegelii False gharial Asia

(Fig. 1.5)

Alligators

The subfamily Alligatorinae contains fourgenera: Alligator (the true alligators, withtwo species), Caiman (the caimans, with twospecies), Palaeosuchus (the dwarf caimans,

Crocodiles and Alligators 3

Fig. 1.3. Captive juvenile Osteolaemus tetraspis tetraspis at the St Lucia Crocodile Centre. Their colour-ing is yellow and black, while that of O. t. osborni hatchlings is green and black.

Fig. 1.4. Young adult wild-caught Osteolaemus tetraspis osborni trussed up for transport to the market.

with two species) and Melanosuchus (theblack caiman, with only one species).

The genus Alligator:A. mississippiensis American alligator USAA. sinensis Chinese alligator China

The genus Caiman:C. latirostris Broad-snouted South

caiman AmericaC. crocodilus Common caiman South

(Fig. 1.6) America

4 Chapter 1

Fig. 1.5. Captive Tomistoma schlegelii on a farm in Kuching, East Malaysia.

Fig. 1.6. Juvenile Caiman crocodilus on a farm in São Paulo State, Brazil.

The genus Palaeosuchus:P. palpebrosus Cuvier’s dwarf South

caiman AmericaP. trigonatus Schneider’s dwarf South

caiman America

The genus Melanosuchus:M. niger Black caiman South

America

Gharials

The subfamily Gavialinae only has onegenus, Gavialis, with a single species.

The genus Gavialis:G. gangeticus Gharial (Plate 1) Indian sub-

continent

Differences between crocodiles andalligators

This question is asked quite regularly. Thereare many anatomical and physiological dif-ferences, but for the purposes of this book itwill suffice to name only three reasonablyobvious ones:

1. Alligators are more cold resistant thancaimans and crocodiles. They can therefore

live further north than caimans and croco-diles in both North America and in China.2. In alligators and caimans the teeth of thelower jaw fit into pits in the upper jaw, con-sequently when the mouth is closed nomandibular teeth are visible. In crocodilesthe fourth mandibular tooth fits into a notchin the upper jaw and thus remains visiblewhen the mouth is closed (Fig. 1.7).3. Crocodiles and gharials have sensory pitsin the ventral scales (Fig. 1.8). These areabsent in alligators and caimans. This is oneof the important features used in the speciesidentification of goods made from crocodil-ian leather.

Wild or captive?

This refers to the description of the differentways in which the crocodiles are living orkept.

Wild

Crocodiles in the wild may be either leftentirely to their own devices or subjected toa certain degree of management. They arehardly ever seen to be suffering from disease


Fig. 1.7. Adult Nile crocodile on a farm in South Africa. Note the visible fourth mandibular tooth in itsmaxillar notch.

or dying, and often they live in such remoteareas that suitable specimens rarely reach thelaboratory (see also p. 239).

Captive

Crocodiles kept in zoos and other collectionswithout a productive goal are referred to ascaptive. They may be bred or exhibited only,but they may also be subjected to scientificstudies.

Wild-caught

Crocodiles caught in the wild and kept for ashort period restrained for the purpose ofsample collection or transported alive to amarket, where they are slaughtered. They areunder very severe stress which may affectmany of their physiological and biochemicalparameters. Such animals should be referredto as wild-caught.

Ranched

Crocodiles kept on farms for commercial(productive) purposes, but either hatchedfrom eggs collected in the wild or havingbeen collected as hatchlings, are referred toas ranched. Their diseases are substantially

the same as those of farmed crocodiles,except for their closer contact with wild pop-ulations, which may constitute a naturalreservoir of crocodile-specific infectiousagents.

Farmed

Crocodiles hatched from eggs laid by breed-ing stock kept on a farm for commercial pur-poses are called farmed crocodiles. Theon-farm breeding of these crocodiles allowsthe genetic selection for certain productiveparameters. These animals no longer have adirect link to the wild. Their only contribu-tion to the conservation of wild crocodilesmay be to keep commodity prices low,thereby lowering the incentive for poaching.However, they may also provide a substan-tial additional gene pool.

Where such crocodiles are farmed faraway from wild crocodile populations theincidence of crocodile-specific infectious dis-eases is usually very low.

Crocodilian Anatomy

The aim of this section is to provide suffi-cient information for the normal functions of

6 Chapter 1

Fig. 1.8. Sensory pits in the ventral skin of Crocodylus palustris.

the body to be understood and for the recog-nition of the organs during post-mortemexaminations. This information is basedlargely on my own experience with Nilecrocodiles. For a reasonably detailed andaccurate study of the anatomy of theAmerican alligator see Chiasson (1962). Weare still waiting for a standard textbook oncrocodilian anatomy. A dissection guide forpost-mortem examinations is given inChapter 2 (p. 75).

The skeleton

Skull

The pitted appearance of the dorsal skullsurface (Fig. 1.9) is due to its fusion with theskin. There are three pairs of foramina dor-sally on the skull: the external nares openinginto one nasal orifice, the orbits and thesupertemporal fossae (Fig. 1.9). On the ven-tral aspect, almost at the same level, are theanterior palatine foramina (foramen), theposterior palatine foramina and, partiallyhidden, the internal nares (Fig. 1.10). Thecranium, which houses the brain, lies

roughly between the orbits and thesupertemporal fossae. The articulation of thejaw is caudal to the atlanto-occipital joint,allowing the jaws to open extremely widely(Fig. 1.11).

Vertebrae

The cervical and thoracic vertebrae haveribs. The cervical ribs lie alongside the verte-bral column pointing caudally, but only thethoracic ribs connect with the sternum. Acartilaginous portion in the midrib allowsflexibility for collapsing the thorax duringdeep diving. The lumbar vertebrae do nothave ribs, but the sacral ones do. Dorsally allthe vertebrae bear neural spines; and ven-trally, chevron bones, which point in anobliquely caudal direction, are attached tothe caudal vertebrae. A fibrous membranebearing abdominal ribs (gastralia) connectsthe sternum with the os pubis and supportsthe abdominal viscera.

Legs

The pectoral girdle, consisting of the scapula,coracoid and sternum, together with the first


Fig. 1.9. Pitted appearance of the skull bones of a mature Nile crocodile, dorsal aspect.

thoracic ribs, surrounds the wide cranialaperture of the thorax. This allows largemasses to be swallowed. The bones of theforelimb (humerus, radius and ulna) areshorter than their counterparts in the hindlimb. The front feet have five digits, the firstthree carrying claws.

The pelvic girdle consists of an os ileum,an os ischium directed caudoventrally and anos pubis pointing cranially. The hind limbsare twice as long as the forelimbs, allowing

for a galloping action. Femur, tibia and fibulaare well developed. The foot has four digits,the first three carrying claws (Fig. 1.12).

The skin

Scales and osteoderms

Crocodile skin, like that of all reptiles, is cov-ered with scales or scutes and is devoid ofsweat glands. On the head the skin is fused

8 Chapter 1

Fig. 1.10. Ventral aspect of the skull of an adult Nile crocodile.

Fig. 1.11. Lateral aspect of the skull of a juvenile Nile crocodile.

to the bones of the skull. The large scales onthe back, and in some species some of theventral scales also, contain bony plates, theosteoderms. Muscles connect the ossifieddorsal scales with the vertebral column, andwhen the muscles contract this results in adorso-ventrally rigid, beam-like structurethat allows the crocodile to keep its back andtail straight when walking or running (Frey,1988a,b). In this context it is interesting tonote that recent mitochondrial DNA analy-ses, as well as studies of nuclear genes, sug-gested a close relationship betweencrocodilians and chelonians (tortoises andturtles). The latter also have osteoderms andboth dorsal and ventral armour (Hedges andPoling, 1999).

Skin glands

Crocodilians have a few holocrine skinglands. The cloacal (paracloacal) glands aresituated laterally within the lips of thecloaca. The mandibular (gular) glands are inthe skin under the tongue, between themandibles (Fig. 1.13). The septa of the gularglands are lined with melanocytes, givingthe gland tissue its black appearance(Weldon and Sampson, 1988). The paracloa-cal gland is a single secretory sac with a sin-gle duct and a single lumen. The

parenchymal cells contain lipid droplets(Weldon and Sampson, 1987). For the analy-sis of the aromatic secreta of these glands,see p. 52. In some species there are also rudi-mentary dorsal glands – in the Chinese alli-gator beneath the second row of scales fromthe dorsal midline, but in various positionsfrom the 2nd to the 15th transverse row(Chen et al., 1991).

Identification

The patterns of scales, both dorsal and ven-tral, are species specific, although someslight individual variations may occur. A keyfor the identification of tanned whole croco-dilian skins can be found in Brazaitis (1987).

Pigmentation

Hatchlings of many species have light anddark transverse striations, which in somespecies are maintained almost into adult-hood. These striations mimic rippling shad-ows in shallow water (see Fig. 1.3). Thechromatophores in the skin can contract andexpand following nervous impulses from theeyes via the brain. Blind crocodiles and thosekept in complete darkness usually displaylighter colours than those exposed to brightdaylight.


Fig. 1.12. Claws on the left hind foot of an adult Tomistoma schlegelii at Singapore Zoological Gardens(photo P. Martelli).

The muscles

There are no external muscles on the headbecause the skin adheres to the skull. Thepowerful jaw muscles are all on the medianaspect of the mandible, thus broadening theposterior skull. Sphincters close the external

nares and depressors close the auricular flapover the tympanum for diving. The long dor-sal muscles of the trunk extend into the tail.These muscles, plus the ventral tail muscles,musculus (m.) caudofemoralis medially andm. ilioischiocaudalis externally (Frey, 1988a),provide the power for swimming (Fig. 1.14).

10 Chapter 1

Fig. 1.13. Mandibular (gular) glands of a juvenile Nile crocodile.

Fig. 1.14. Schematic drawing of a cross-section of the tail of a Nile crocodile: 1, musculus (m.) longis-simus dorsi; 2, m. caudofemoralis; 3, m. ilioischiocaudalis.

The respiratory system

Respiratory tract

The external nares are slightly raised abovethe level of the upper jaw, allowing the croc-odile to surface and breathe when most of itsbody is submerged. Adult male gharialsdevelop a large nasal excrescence, the ghara(see Plate 1), which is thought to function asa vocal resonator (Whitaker and Basu, 1983).

In the long nasal passage the olfactorynerve endings are exposed to the air. Exceptwhen swallowing, bellowing or yawning,the posterior part of the mouth is closed bythe gular valve, consisting of the dorsal flapof the tongue and the palatal flap (velumpalati) extending from the soft palate(Putterill and Soley, 1998a) (Fig. 1.15). TheEustachian tubes enter the pharynx in ajoined opening just caudally of the internalnares (Colbert, 1946) (Fig. 1.16). Their func-


Fig. 1.15. Schematic drawing of the oral and pharyngeal cavities of the crocodile: 1, gular valve; 2,tongue; 3, larynx and trachea; 4, oesophagus; 5, internal nares; 6, tonsils; 7, Eustachian tubes; 8, nasalpassages.

Fig. 1.16. Tonsils of the crocodile caudally of the internal nares.

tion is to equalize the pressure on the twosides of the tympanum (the ear membrane).Close to the opening of the Eustachian tubesinto the pharynx there are two mucosalfolds, one on either side and extending cau-dally, which contain tonsillar tissue (Putterilland Soley, 2001) (Fig. 1.16).

The glottis has two soft lips (Fig. 1.17)which close when the crocodile swallows. Incrocodiles (but not in alligators) the tracheabends to the left inside the thorax before itsbifurcation, a substantial distance beforeentering the lungs (Fig. 1.18). This allowslarge chunks of prey to be swallowed with-out exerting any pressure on the trachea orbronchi.

Lungs

The lungs are multi-cameral sac-like struc-tures, highly vascularized but with thickerwalls than a mammalian lung. These thickwalls may be necessary to counteract theoutside pressure during diving. The lungs liein pleural chambers which are separated by

a complete mediastinum. The posterior partof the lungs is connected tightly to the ante-rior transverse membrane (postpulmonarymembrane). In crocodiles the remainder ofthe lungs lies loosely in the thoracic cavity,not as described by Duncker (1989), while inthe caiman the lungs are fused to the ventralwall of the thorax. For a detailed study oflung morphology of the Nile crocodile, seePerry (1988).

Respiratory muscles

The thorax is divided from the abdomen bytwo transverse membranes. The postpul-monary membrane separates the lungs fromthe liver, and its ventral third is muscular.The posthepatic (posterior transverse) mem-brane is attached to a sheet of muscle (m.diaphragmaticus) which extends to the ospubis (Van der Merwe and Kotzé, 1993).Together, the two membranes, with theirmuscular components, act like a diaphragm,pulling the liver in a caudal direction forinspiration.

12 Chapter 1

Fig. 1.17. Tongue and ventral aspect of the pharyngeal cavity with protruding glottis; juvenile Nile crocodile.

Voice organ?

Crocodiles can produce a range of sounds,but have neither vocal cords (like mammals)nor a syrinx with tympaniform membranes(like birds). It is believed that sounds areproduced by forcing the air through the com-pressed lips of the glottis (Fig. 1.17), much assounds are produced by human lips in themouthpiece of a trumpet.

The digestive system

Teeth

Crocodilian teeth are pointed, very sharp andare constantly replaced throughout life. Thereplacement rate varies with the growth rateand slows down as the animal becomes older.In small American alligators (<1.5 m) the esti-mated replacement rate varied from 3 to 4months (Erickson, 1996a). Early in life, toothreplacement occurs in waves, passing alongalternately numbered tooth series from backto front, while later in life the direction isreversed (Edmund, 1962). Although very old,toothless individuals are sometimes found,this may be due to accumulated damage tothe alveoli (Erickson, 1996b) (see p. 247).

While crocodilian teeth are homomorphic,they may be categorized by their position inthe maxilla and mandible. Kieser et al. (1993)group the teeth of the Nile crocodile as fol-lows (Fig. 1.19):

● maxilla: 5 incisors – gap – 5 canines – gap– 5 molars;

● mandible: 3 incisors – gap – 5 canines –gap – 7 molars.

The first mandibular canine is the longestand often extends above the dorsal plane ofthe snout (Fig. 1.20). This can cause damageto belly skins when frightened young croco-diles pile in the corner of their pen (see alsopp. 114 and 241). In some individuals thetwo mandibular incisors 1 on each sidesometimes penetrate the maxilla behind themaxillary incisors and produce openings inthe upper lips in front of the nostrils, whichcould be called ‘false nostrils’ (Figs 1.9 and1.21; see also p. 153).

Tongue

The tongue occupies the floor of the mouthcavity. It is not free but is held in place later-ally by a folded membrane. The dorsal sur-face of the tongue contains mucus glandswhich are associated with lymphoid tissue,


Fig. 1.18. Tracheal loop in the thorax of Crocodylus palustris.

forming ‘lingual tonsils’, while sensoryorgans are found along the sides of thetongue (Putterill and Soley, 1998b). In croco-diles the dorsal surface also contains saltglands (Taplin and Grigg, 1981; Franklin andGrigg, 1993).

Oesophagus

The oesophagus extends from the epihyalcartilage of the larynx to the clearly definedgastro-oesophageal junction. It has manylongitudinal folds, allowing distension whenthe crocodile swallows large chunks. Theentire epithelial surface contains many

goblet cells that function as an intra-epithe-lial gland (Putterill et al., 1991).

Stomach

The stomach lies to the left, immediatelybehind the left lobe of the liver and the pos-terior transverse membrane. Its junction withthe oesophagus (cardia) is defined by a well-developed sphincter muscle. The pyloric exitalso lies in the cranial aspect, slightly to theright of the cardia, and is defined by a smallbulbus, the pyloric antrum, which in turnopens into the duodenum (Figs 1.22–1.24).The entire interior surface of the stomach is

14 Chapter 1

Fig. 1.19. Dentition of a juvenile Nile crocodile.

Fig. 1.20. The protruding first mandibular canine causes scratches when the crocodiles pile up in thecorner of their pen.

lined uniformly by mucosal glands. Gastrinand somatostatin cells are found only in theglands of the pyloric antrum (Rawdon et al.,1980; Dimaline et al., 1982). The pyloric open-ing to the duodenum is very small, thus pre-venting the escape of accidentally swallowedforeign bodies (see p. 254).

The gastric wall is strongly muscularizedover the fundus, which gives the crocodilianstomach a somewhat gizzard-like appear-

ance. However, the internal glandular liningwould not be able to protect the mucosa froma strong chewing action, as the koilin layerdoes in the avian gizzard. The function of thegastroliths that are often found in crocodilianstomachs, i.e. whether they are ballast, have achewing function as in birds or have beentaken in accidentally, is the subject of anongoing debate (Steel, 1989) (see also pp. 36and 290). The fact that stomachs of crocodiles


Fig. 1.21. ‘False nostrils’ in a captive Crocodylus palustris.

Fig. 1.22. Overview of the gastrointestinal tract, oesophagus to cloaca, of a Nile crocodile hatchling.

in the Okawango swamps in Botswana con-tain increasing amounts of plant material,such as papyrus roots and palm tree seeds,with increasing body length (Blomberg, 1976)tends to indicate accidental ingestion.

Intestine

The looped duodenum starts from thepyloric antrum and extends to the end of theloop. In many crocodile species the duode-

num folds over again, forming a doubleloop, although this is apparently not the casein alligators. Both forms occur in differentpopulations of Osteolaemus tetraspis(Huchzermeyer et al., 1995; Huchzermeyer,1996b). Part of the pancreas is embeddedbetween the limbs of this loop (see Fig. 1.26).From the end of the loop the jejunum runsinitially straight along the dorsal aspect ofthe abdominal cavity, then becomes sus-pended in loose coils by the mesentery to the

16 Chapter 1

Fig. 1.23. Stomach and duodenal antrum of a Nile crocodile. The strong musculature and the centraltendinous plate create a gizzard-like impression.

Fig. 1.24. Opened stomach and duodenal antrum of a Nile crocodile. Note the clear demarcationbetween oesophageal and gastric mucosa.

point at which the cranial mesenteric arterymeets the intestine (van der Merwe andKotze, 1993). From this point the ileumextends in similar coils to the very short rec-tum, which in turn enters into the cloaca(Hunter, 1861) (Fig. 1.22). The rectum is sus-pended by a short mesentery and liesbetween, and ventral to, the two kidneys.

The internal surface of the intestine doesnot have villi, but a system of complexzigzagging, ridge-like folds, which alternatewith each other and are oriented longitudi-nally (Kotzé et al., 1992; Kotzé and Soley,1995) (Fig. 1.25).

Pancreas

The proximal (ventral) pancreas lies betweenthe limbs of the duodenal loop, while thedistal (dorsal) part surrounds the cranialaspect of the spleen (Miller and Lagios, 1970;Huchzermeyer, 1995) (Fig. 1.26).

Liver

The liver lies between the two transversemembranes in the hepatic coelom and hastwo lobes of almost equal size – the rightlobe being slightly larger than the left. The


Fig. 1.25. Zigzagging intestinal folds, adult Nile crocodile.

Fig. 1.26. The pancreas between the duodenal loops and extending towards the spleen in a juvenile Nilecrocodile.

18 Chapter 1

Fig. 1.27. Kidney of a Nile crocodile.

heart separates these two lobes. In somespecies the lobes are completely separate,while in others they are joined by a dorsalbridge of liver tissue.

Substantial collagenous trabeculae havebeen found in the liver of American alliga-tors and to a lesser extent in Caiman croco-dilus (Beresford, 1992). Storch et al. (1989)found abundant Kupffer cells, as well asfat-storing cells, in the sinusoidal lining ofthe liver of O. tetraspis. Numerous Kupffercells are also present in Nile crocodilelivers.

The gall bladder lies between the twoliver lobes within the hepatic coelom, andreceives bile from both. The bile duct entersthe intestine in the proximal duodenum (Vander Merwe and Kotzé, 1993). In most of theAmerican alligators examined by Xu et al.(1997) the right and left hepatic ducts wereinterconnected, the right duct entering thegall bladder while the left duct continuedthrough the pancreas directly into the duo-denum.

The urinary system

The two kidneys are firmly attached to thedorsal abdominal wall in the most posteriorpart of the abdomen. As in birds, they arenot embedded in perirenal fat and lack acapsule. The renal tissue, consisting of corti-cal and pelvic layers, is folded over, in a sin-

gle fold in the African dwarf crocodile and inmultiple folds in other crocodile species.These folds continue to grow as the crocodilegrows. These multiple folds give the kidneyof the Nile crocodile a triangular shape ontransverse section, while the kidney of theAfrican dwarf crocodile appears flattened.The folding patterns appear to be speciesspecific (Figs 1.27–1.29).

Crocodilians do not have a urinary blad-der. The two ureters open into the cloaca.However, urine may be stored in the rectum(Fig. 1.30).

The reproductive organs

Female

Two ovaries are attached to the dorsal bodywall cranioventrally to the kidneys, and arepartially attached to the cranial part of thekidneys. The ovaries are elongate, and in veryyoung animals they are difficult to differenti-ate macroscopically from testes. In largerjuveniles the follicular structure becomes evi-dent. In adult crocodiles all the folliclesmature at the same time (Fig. 1.31). The ovar-ian histology of the American alligator wasstudied by Uribe and Guillette (2000). In adultfemale American alligators the corpora luteaform after ovulation. Their morphology issimilar to that in birds and their size can beused to judge whether a female had laid eggsduring the preceding season, recent corpora


Fig. 1.28. Kidney of Crocodylus palustris.

Fig. 1.29. Kidney of Caiman crocodilus.

lutea having a minimum diameter of 0.4 cm(Guillette et al., 1995b).

The ostium of the oviduct lies close to thecranial apex of each ovary. The oviducts areconvoluted and increase in size with matu-rity and sexual activity. They enter the uteri(the glandular part), followed by the vagi-nae, where the eggs are stored before laying(Fig. 1.32). The vaginae join the cloaca, cau-dally to the ureters. A small clitoralappendage, which resembles the male penisin shape, is situated ventrally in the cloaca.

Male

The slightly flattened testes are situated inthe same position as the ovaries in thefemale (Plate 2). A convoluted deferent ductruns along the caudolateral border of eachtestis and enters the cloaca close to the baseof the copulatory organ. This crocodilianpenis is folded around a ventral seminalgroove (Fig. 1.33). Note that crocodiles andtortoises have only one penis, while lizardsand snakes have paired hemipenises.

20 Chapter 1

Fig. 1.30. Rectum filled with urine, juvenile Nile crocodile.

Fig. 1.31. Nile crocodile ovary, with mature follicles.

The endocrine organs

Pituitary

The pituitary gland lies on the ventral aspectof the brain, at the level of the optic lobes(Fig. 2.26) (Chiasson, 1962).

Thymus

The thymus gland consists of a series of lob-ules of varying sizes on both sides of the tra-chea along the neck and in the thorax to thebase of the heart. In well-nourished croco-diles these glands are embedded in fatty


Fig. 1.32. Ovaries, oviducts, uteri and vaginae of Osteolaemus tetraspis.

Fig. 1.33. Everted penis of an adult Nile crocodile.

tissue, which is almost the same colour. Thismakes it difficult to differentiate the individ-ual lobules. Note that Huchzermeyer’s (1995)description of the thymus glands of the Nilecrocodile was based on emaciated individualsfor improved visibility. Consequenly the lob-ules had vanished from the necks of these ani-mals. However, lobules were subsequentlyseen in the neck of healthier Nile crocodiles asdescribed previously from other crocodilespecies (Gegenbauer, 1901; Bockman, 1970).

It is believed that in crocodilians thethymus remains active throughout life. For adiscussion of the striated muscle cells occa-sionally found in the reptilian thymus, seeRaviola and Raviola (1967).

Thyroids

While some crocodilians have a single thy-roid gland with two well-defined lobes oneither side of the trachea, connected by anarrow isthmus (Lynn, 1970), other specieshave two separate lobes. They are recog-nized by their dark-brown colour. In the Nilecrocodile these are situated not on either sideof the trachea, but on the lateral side of eachof the two bronchi and medially of the com-mon carotid artery, the right one closer to theentrance of the right bronchus into the lungand the left one closer to the bifurcation ofthe trachea (Plate 3) (Huchzermeyer, 1995).

Parathyroids

The two parathyroid glands are normallyhidden by thymus tissue and difficult to see.In the Nile crocodile they are situated cau-dolaterally of the thyroid glands on eachside, between the precaval vein and the com-mon carotid artery, immediately cranially ofthe dorsal bend of the aortic arch (Plate 3and Fig. 1.35) (Huchzermeyer, 1995). The sit-uation appears to be similar in C. crocodilus,apart from the fact that additional (acces-sory) parathyroid glands occasionally occur(Oguro and Sasayama, 1976).

Adrenals

The two adrenal glands are found in theabdominal cavity adhering to the dorsal

body wall. Ventrally they partially overlapthe proximal part of the kidneys. Theyextend cranially beyond the two kidneys andsomewhat laterally of the midline (Plate 2)(Huchzermeyer, 1995).

Pancreas and intestinal tract

The topography of the pancreas has beendescribed above. In the Nile crocodile theislets of Langerhans appear to be present in the distal (dorsal) pancreas only(Huchzermeyer, 1995). A similar distributionwas found in the American alligator, inwhich smaller groups were also found in theventral (proximal) portion (Jackintell andLance, 1994).

Endocrine cells have also been found inthe pyloric part of the stomach and in theintestine of crocodiles (Rawdon et al., 1980;Dimaline et al., 1982; van Aswegen et al.,1992).

The circulatory system and blood cells

Heart

In the Nile crocodile the heart is situatedbetween the 4th and 8th thoracic ribs (Vander Merwe and Kotzé, 1993) and betweenthe two lobes of the liver (Fig. 1.34). The situ-ation is similar in the other crocodilians. Aligament at its apex, the gubernaculumcordis (Webb, 1979), connects it to the peri-cardial sac and beyond this to the postpul-monary transverse membrane. There is nofat in the coronary groove. The two auriclesstretch caudally on either side halfway alongthe ventricles, the larger right auricle some-times further. The four chambers are com-pletely separated.

Circulation

The major blood vessels leaving the heart ofthe Nile crocodile are identified in Fig. 1.35.Crocodiles have two aortic arches like otherreptiles. The left aortic arch leaves the rightventricle alongside the pulmonary arteryand becomes the coeliac artery; this supplies the digestive organs of the abdomen. The

22 Chapter 1

right aortic arch emerges from the leftventricle and runs posteriorly as the dorsalaorta.

The left and right aortic arches communi-cate in two places: the foramen of Panizzaand the anastomosis (Axelsson and Franklin,

1997). The foramen of Panizza is located atthe base of the heart within the aortic archvalves (Webb, 1979), and the anastomosis is ashort vessel connecting the two aortic arches.In American alligators of length 1–2 m, theforamen of Panizza had a diameter of


Fig. 1.34. The heart is situated between the lungs and the two lobes of the liver; juvenile Nile crocodile.

Fig. 1.35. Schematic drawing of the heart and major blood vessels of the Nile crocodile, ventral aspect.1, trachea; 2, thyroid; 3, carotid artery; 4, precaval vein; 5, parathyroid; 6, aortic arch; 7, left auricle; 8, leftventricle; 9, bifurcation of the trachea; 10, carotid artery; 11, thyroid; 12, precaval vein; 13, parathyroid;14, aortic arch; 15, right auricle; 16, right ventricle.

1–2 mm (Greenfield and Morrow, 1961).During systole it is completely covered bythe aortic valves, thus allowing an exchangeof blood during diastole only (Axelsson andFranklin, 1997).

As in all reptiles and birds, part of thevenous blood of the caudal half of the bodyis drained through the renal portal system.According to Chiasson (1962) this appears tobe bypassed partially by the ventral abdomi-nal veins which, together with the mesen-teric vein, enter the hepatic portal system.

Superficial veins

I have been unable to identify any large, eas-ily accessible superficial veins for intra-venous injections. Blood can be drawn fromthe dorsal and ventral vertebral veins of theneck and tail (see p. 64). The statement aboutdrawing blood from the temporal vein,which lies just below the temporal muscle onthe dorsal aspect of the head (Lance, quotedby Samour et al., 1984), is in error. Such atechnique has never been used or describedby Lance (personal communication, V.A.Lance, San Diego, 1999).

Tonsils

In the Nile crocodile the tonsils are situatedin the roof of the pharynx (Putterill andSoley, 2001) (see above, Fig. 1.16).

Spleen

The pear-shaped spleen lies dorsally in themesentery, close to the base of the duodenalloop (Plate 2). Its broad cranial end is embed-ded in the caudal limb of the pancreas. Thespleen is covered by a strong capsule. Thehistology and vascular architecture of thespleen of the American alligator were stud-ied by Tanaka and Elsey (1997).

Lymphatics

The lymphatic system was studied byMcCauley (1956). There are no subcutaneouslymph vessels and no lymph nodes. Lymphvessels from the head and the anterior limbs,thorax and abdomen anastomose with the

external jugular vein just proximal to thejuncture with the subclavian vein. Thelymph from the caudal and pelvic regions ispumped by the posterior lymph hearts intosmall vessels which empty into the pelvicvenous plexus. These lymph hearts are sin-gle-chambered muscular structures, measur-ing 3 � 5–7 mm in alligators 50–75 cm long.They are situated superficially at the junctionof the hind limb with the pelvis, below thesuperficial layer of the deep fascia in thetriangle formed by the m. longissimuscaudae, the crest of the ileum and the m.flexor caudae.

In the absence of lymph nodes, the thy-mus (see above), tonsils, spleen and numer-ous lymphoid masses in the walls of thedigestive tract act as reservoirs of lympho-cytes.

Blood volume

The total blood volume of one juvenileAmerican alligator was 4.2% of body mass(Coulson et al., 1950), of another two alliga-tors 5.1% and 5.5% (Andersen, 1961), andthat of 3.5-year-old Cuban crocodiles (n = 19)was 4.0 ± 0.3% for males and 3.6 ± 0.2% forfemales (Carmena-Suero et al., 1979).

Blood cells

All crocodilian blood cells are nucleated. Theerythrocytes are oval in shape with round oroval nuclei. The dimensions of the red bloodcells of some crocodilian species are given inTable 1.1.

The following descriptions of the variousblood cells were taken from Mateo et al.(1984b) and refer to the American alligator.Detailed descriptions of the blood cells ofCrocodylus porosus and Crocodylus johnsoni aregiven by Canfield (1985). See also Hawkeyand Dennett (1989). However, there is someconfusion in the literature, with differentauthors using different definitions for thedifferent leucocytes.

THROMBOCYTES. Length 14.3 �m, oval or ellip-tical with smooth cell borders, smooth paleblue or almost colourless cytoplasm thatoften contains numerous clear confluent

24 Chapter 1

vacuoles with poorly demarcated borders.The uniform oval nuclei are located central-ly and oriented longitudinally, stainingintensely dark purple, with coarsely con-densed chromatin.

A phagocytic function of avian thrombo-cytes was discovered recently (Wigley et al.,1999) and the same function may be postu-lated for reptilian thrombocytes. The func-tions of the other blood cells are presumed tobe the same as in mammals and birds.

HETEROPHILS. Heterophils, or type I granulo-cytes (Canfield, 1985), are round to oval cellswith mean diameters of 17.3 �m and distinctsmooth cytoplasmic borders. The nuclei arelenticular, oval or, rarely, bilobed, withindistinctly clumped purple chromatin,usually eccentrically located at one pole ofthe cell. The cytoplasm contains abundant,3–4 �m long, fusiform refractile granules,occasionally arranged in perinuclear radi-ally symmetrical star-like configurations(Fig. 1.36).

EOSINOPHILS. Eosinophils, or type II granulo-cytes (Canfield, 1985), are oval or occasion-ally round, with a mean diameter of 14.9 �mand smooth cytoplasmic outlines. The lentic-ular or oval nuclei are purple with promi-

nent coarsely clumped chromatin and verysharply demarcated borders, usually locatedat one pole of the cell, often causing a slightoutward bulge of the cell outline. Somenuclei are located more centrally. The pale-blue, smooth cytoplasm is visible only as athin rim surrounding the many bright pinkplump granules measuring 2–3 �m (Fig.1.37). Often a few granules are present on theface of the nucleus.

BASOPHILS. Basophils, or type III granulocytes(Canfield, 1985), are round cells with irregu-lar external ‘cobblestone’ contours and adiameter of 12.8 �m. Abundant, dark-purpleto purplish-red, round granules measuring0.1–0.5 �m pack the cell to the point wherethey frequently obscure the nucleus.Sometimes the granules are arranged in aperipheral rim with a central cluster over thenucleus.

LYMPHOCYTES. Lymphocytes are generallyround or oval, with a diameter of 10.7 �m,but irregular, polygonal forms are also seen.A large nucleus, with smooth outlines andfollowing the cell contours, almost fills thecell. The nucleus is pale violet with finelyclumped chromatin. The cytoplasm is visibleonly as a thin, slate-grey or pale-blue rim


Table 1.1. Erythrocyte dimensions (means).

Species Length (�m) Width (�m) References

Alligator mississippiensis 14.8–22.0 8.1–12.8 1A. mississippiensis 17.5 9.7 4A. mississippiensis 23.2 12.1 5A. mississippiensis 23.0 14.3 6Caiman latirostris 21.3 10.9 2C. latirostris 19.5 10.8 2Caiman crocodilus 23.8 13.3 3A. mississippiensis 20.8 11.1 3C. latirostris 17.0 9.0 7C. crocodilus 17.0 9.0 7

1, Reese (1917); 2, Gulliver (1840) (cited by Reese, 1917); 3, Milne-Edwards (1856) (cited by Reese,1917); 4, Glassman et al. (1981); 5, Wintrobe (1933); 6, Mateo et al. (1984); 7, Troiano et al. (1998).Note the nomenclature used in the older papers:Alligator lucius = Alligator mississippiensis;Alligator sclerops = Caiman crocodilus;Caiman fissipes = Caiman latirostris.

bordering the nucleus. Occasionally dust-like red granules and/or a few clear vac-uoles, 1 �m in diameter, are scatteredthrough the cytoplasm. External cell bordersrange from smooth to ragged, frequentlywith bleb-like protrusions of cytoplasm.

MONOCYTES. Monocytes are oval or roundwith a diameter of 14.3 �m, with somewhat

indistinct external cell borders and numer-ous delicate cytoplasmic projections. Theabundant grey-blue cytoplasm sometimescontains a few clear, refractile vacuoles, mea-suring 1.2 �m. Many cells have fine dust-likegranules, usually arranged in crescentic per-inuclear aggregates. The plump, ovalnucleus, measuring 7.1 �m, is usuallylocated centrally, but is sometimes eccentri-

26 Chapter 1

Fig. 1.36. Heterophil (h) of a Nile crocodile.

Fig. 1.37. Two eosinophils, Nile crocodile.

cally situated adjacent to one pole of the cell.The nucleus is homogeneous light purplewith finely stippled chromatin (Fig. 1.38). Inaddition to these typical monocytes, largecells, up to 20 �m in diameter, with undulat-ing borders, pale-blue cytoplasm with fewinclusions, and prominent, indented or evenhorseshoe-shaped nuclei are seen occasion-ally.

Details of crocodilian haematology are givenin Chapter 2.

Chromosomes

The chromosomes of 21 species of crocodil-ians were studied by Cohen and Gans (1970)and of five species and several crossings byChavananikul et al. (1994). The number ofchromosomes ranges from 30 to 42 and thefundamental number from 56 to 62, for detailssee Table 1.2. There are no sex chromosomes.

The nervous system and sensory organs

Brain

The most striking features of the crocodilianbrain are the two olfactory bulbs, whichextend anteriorly far beyond the two cerebralhemispheres. The optic lobes are exposed

between the hemispheres and the relativelysmall cerebellum. The base is formed by arelatively broad medulla oblongata.

Spinal cord

The spinal cord extends almost to the tip ofthe tail. There is no cauda equina, as eachpair of caudal nerves leaves the cord at thesite of exit from the vertebral column(Chiasson, 1962).

Peripheral nerves

The peripheral nerves exit the spinal cord inpairs. At the level of the pectoral and pelvicgirdles they are organized into a brachialand lumbo-sacral plexus, respectively. For adetailed description see Chiasson (1962).

Autonomic nervous system

Like higher vertebrates, crocodiles also havean autonomous nervous system, consistingof two components. The vagus nerve startsas the tenth cranial nerve and runs along thejugular to the thoracic and abdominal vis-cera. The sympathetic trunk runs parallel tothe spinal cord and communicates with eachspinal nerve, thickening at each site of com-munication in the form of a sympathetic gan-glion (Chiasson, 1962).


Fig. 1.38. Monocyte (m) of a Nile crocodile.

Ear

The ear has two sensory functions, hearingand spatial orientation.

HEARING. The tympanic membrane of the earis protected by a fibrous flap which closeswhen diving. In the middle ear the columellais attached to the tympanic membrane and atthe other end it has a large basal plate set inthe fenestra ovalis of the inner ear.

SPATIAL ORIENTATION. The membranouslabyrinth consists of three semicircularcanals, each with an ampulla, the utriculusand its ventral extension, the lagena, allenclosed in bone.

Both functions are served by the acousticnerve (eighth cranial nerve) (Chiasson, 1962).

Eye

The eye is protected by three eyelids. Thethird eyelid is the nictitating membrane,

which is optically clear and protects thecornea during diving. A special muscle canretract the eye into the orbital fossa. A reflect-ing layer behind the retina improves nightvision and causes crocodile eyes to light upat night in the beam of a torch (Fig. 1.39).There is no night vision in complete dark-ness without a minimum of residual light.

Fat storage

Fat body

Being exothermic, crocodiles do not need fatfor insulation. In fact, subcutaneous fatdeposits would impede thermoregulation (seep. 44). Also, crocodiles do not store fat in thecoronary groove of the heart. In mammals,there is growing evidence that the heart usesmainly fat as a source of energy (Medeirosand Wildman, 1997). It is believed that this isalso the case in crocodiles, and that the fatsupply for the heart is stored in the abdomi-nal fat body, for which I propose the anatomi-cal name the steatotheca (Greek stear = fat;

28 Chapter 1

Table 1.2. The chromosomes of crocodiles.

Cohen and Chavananikul et al. Amavet et al.Gans (1970) (1994) (2000)

Species 2n NF 2n NF 2n

Palaeosuchus trigonatus 42 58P. palpebrosus 42 58Melanosuchus niger 42 60Caiman latirostris 42 60 42C. crocodilus 42 62 42Alligator mississippiensis 32 60A. sinensis 32 60Gavialis gangeticus 32 60Crocodylus siamensis 34 58 30 58C. porosus 34 58 34 58C. moreletii 32 56C. johnsoni 32 58C. acutus 32 58C. intermedius 32 58C. niloticus 32 58 32 58C. novaeguineae 32 58 32 58C. cataphractus 30 58C. rhombifer 30 58 30 58C. palustris 30 58Osteolaemus tetraspis 38 58Tomistoma schlegelii 32 58

2n, Diploid number; NF, fundamental number.

th\k\ = container, store). This organ is locatedin a mesenteric fold close to the right abdomi-nal wall, immediately posterior to the liver(Fig. 1.40) (Vorstman, 1939; Mushonga andHorowitz, 1996). Its volume varies with thestate of nutrition, while its shape varies fromspecies to species (Fig. 1.41). The fat cells havelarge nuclei, demonstrating their ability toactivate the stored fat rapidly (Fig. 1.42).

Somatic fat

Additional fat may be stored in somatic fat cells with small nuclei: in the medi-astinum of the thorax, under the peri-toneum and between muscles, particularlyventrally in the tail between the inner(caudofemoralis) and external (ilioischio-caudalis) muscles.


Fig. 1.39. Light of the photographic flash reflected by the eyes of the juvenile Nile crocodiles on a farmin South Africa (photo A. Brieger).

Fig. 1.40. The abdominal fat body of a juvenile Nile crocodile, caudally of the right lobe of the liver andpartially hidden by the duodenal loop.

The egg

Crocodilian eggs are elongate elliptical andhave a hard shell. The size of the egg varieswith the species, with the age of the femalethat lays the egg – young females layingsmaller eggs than mature females – and indi-

vidually between females. Larger eggsproduce stronger and more viable hatch-lings, which rapidly outgrow hatchlingsfrom smaller eggs. Parameters of Americanalligator eggs were determined byCardeilhac et al. (1999b) and are summarizedin Table 1.3.

30 Chapter 1

Fig. 1.41. Abdominal fat body of Osteolaemus tetraspis.

Fig. 1.42. Histology of an almost depleted abdominal fat body of a Nile crocodile hatchling. Note thelarge nuclei of the fat cells.

Eggshell

The calcareous shell consists of an outer,densely calcified layer, in which the calcitecrystals are stacked vertically; a honeycomblayer of horizontally stacked crystals; anorganic layer, which contains a higher per-centage of organic matrix; and a mammillarylayer. Pores penetrate the shell surface andend between the mammillae. These pores aremost frequent in the opaque zone (Ferguson,1982).

A thin, organic, probably mucinous, layerwas found to cover the outer surface of somenewly laid eggs and was believed to consistof the remnants of oviductal secretions. Thislayer was no longer present after 2 weeks ofincubation. It is therefore not an equivalent

of the wax cuticle present on most avianeggs (Ferguson, 1982).

Under the calcareous shell lies theeggshell membrane, consisting of two layers,a fibrous membrane facing the shell and alimiting membrane facing the embryo. Thelimiting membrane contains a large numberof tiny pores and fewer large pores. Most ofthese pores are closed at the onset of incuba-tion and others open up as incubation pro-ceeds. Consequently, the shell membrane isless permeable to oxygen than the calcareousshell (Kern and Ferguson, 1997).

The opaque band around the lesser cir-cumference of the egg develops during incu-bation in parallel with the expansion of thechorioallantoic membrane and the mobiliza-tion of calcium out of the shell for use by theembryo (Fig. 1.43). At the same time, anextrinsic acidic degradation of the outer shelloccurs due to microbial action in the nest.This produces erosion craters around thepores and increases the permeability of theshell (Ferguson, 1982).

Unlike the avian egg, the crocodile eggdoes not have an air chamber between theshell and the shell membrane (Ferguson,1982).

Internal components

The yolk, with the embryonic disc floatingon top, is surrounded by a large quantity ofthin albumen, which in turn is contained in a


Table 1.3. Summary of mean parameters of eggsof three different populations of American alligators(after Cardeilhac et al., 1999b).

Parameter Result

Egg length (cm) 7.25–7.57Egg width (cm) 4.079–4.47Egg mass (g) 68.85–86.0Length/width ratio 1.684–1.766Shell thickness (mm) 0.43–0.45Shell density 2.10–2.14Shell mass (g) 7.39–8.89Shell mass (% of egg mass) 10.57–11.14Yolk mass (g) 31.9–36.2Yolk mass (% of egg mass) 44–48Membrane mass (% of egg mass) 1.06–1.08

Fig. 1.43. A banded Nile crocodile egg after removal of its contents.

layer of thick albumen separating it from theshell (Magnusson and Taylor, 1980). If theegg is turned during laying, gravity causesthe yolk with the embryo to rotate. Within24 h of laying, the developing vitelline mem-brane and the embryo adhere to the shellmembrane, displacing the albumen towardsthe poles of the egg (Webb et al., 1987).

The embryo

From the start of embryonic development inthe oviduct, water is drawn from the albu-men and secreted beneath the embryo on theinside of the vitelline membrane, where itforms the subembryonic fluid. After laying,the volume of subembryonic fluid increasesrapidly, causing the volume within thevitelline membrane (containing embryo,subembryonic fluid and yolk) to expand(Webb et al., 1987).

Albumen dehydration and the productionof subembryonic fluid peak at the time of theexpansion of the allantois. Along the shellthe allantois fuses with the chorion andforms the chorioallantois (Webb et al., 1987),which becomes highly vascularized andtakes on the gas-exchange function untilhatching, when the lungs are able to fill withair. The different embryonic membranes andspaces are shown schematically in Fig. 1.44.

Crocodilian Physiology

Yolk-sac resorption

Just before hatching, the yolk-sac is drawninto the abdominal cavity and the body wallcloses around the navel. At this point gasexchange can no longer take place via themembranes and the young pre-hatchling hasto start using its lungs.

The yolk-sac has already provided nutri-tion during embryonic and fetal develop-ment, and (in American alligators) has lost25% of its mass (Fischer et al., 1991), but stillcontains sufficient nutrients (75% of its con-tents in American alligators) for the first fewweeks, until the hatchling is strong enoughto find its own food (Fischer et al., 1991). Thecontents of the yolk-sac are resorbed in twodistinct ways: (i) direct resorption into thebloodstream via a capillary bed which hasdeveloped in the wall of the yolk-sac; and (ii)voiding via the vitello-intestinal duct intothe intestine, digestion there and finallyresorption through the intestinal mucosa.The open vitello-intestinal duct is also amajor pathway for infection of the yolk-sacwith intestinal bacteria, depending onintestinal colonization and peristaltic move-ments (see p. 142). The vitelline duct con-necting the yolk-sac to the intestine is shown

32 Chapter 1

Fig. 1.44. Schematic drawing of a crocodile embryo and its membranes at 45 days of incubation; ca,chorioallantois; m, shell membrane; s, shell; y, yolk-sac (after Webb et al., 1987).

in Fig. 1.45. Unlike the situation in birds, thecrocodilian yolk-sac does not appear to beanchored to the navel.

There do not appear to be any reportsabout the time it takes for the yolk-sac to becompletely resorbed under normal circum-stances. It is probably 3–4 weeks. This wouldbe temperature dependent, with a slower rateof resorption at lower (suboptimal) tempera-tures. Infection of the vitello-intestinal ductcan lead to its closure and, in this case, theyolk-sac will remain unresorbed (see p. 143).

Sex differentiation

Crocodiles do not have sex chromosomes(see above). Instead, the sex of the embryo isdetermined by the incubation temperature.Recently, Crews and Ross (1998) reviewedcurrent knowledge about the mechanismsinvolved, as follows.

At the temperature-sensitive stage earlyin embryonic development, temperatureinfluences the expression of stereogenic fac-tor 1, which in turn upregulates the expres-sion of the gene for aromatase, the critical

enzyme in the synthesis of oestrogen.Oestrogen then binds to the oestrogen recep-tor, the expression of which is also modu-lated by the incubation temperature. Via thiscascade of events low incubation tempera-tures favour the development of ovaries,while at high temperatures testes are pro-duced. However, this cascade can easily beinfluenced, or even disrupted, by the actionof external steroids (see p. 223).

Growth

Factors influencing growth

The growth of juvenile crocodiles dependsmainly on the environmental temperatureconditions and on nutrition, althoughgenetic and clutch-related factors probablyalso play a role (Garnett and Murray, 1986).The most important clutch-related factor isegg size and consequently hatchling size, assmall hatchlings are generally poor growers.Stress caused by high stocking density candepress the growth rate (Elsey et al., 1990a)(see also pp. 116 and 280).


Fig. 1.45. One-day-old gharial hatchling, showing the yolk-sac connected to the intestines by thevitelline duct. Note the double duodenal loop of this species.

Metabolic rate

The metabolic rate of crocodiles depends ontheir size and activity, and the temperature(Baldwin et al., 1995; Munns et al., 1998). At28°C a 70 kg American alligator producesabout 72 kcal day�1, i.e. about 4% of that of aperson of equal mass. At 32°C the rate dou-bles. However, a hatchling at 28°C has half thehuman metabolic rate (Coulson et al., 1989).

Stress-related reduction of the growth rate– runting – of some individuals is a commonoccurrence on crocodile farms (see p. 234). Apositive influence of sunlight on the growthrate was found by Zilber et al. (1991), but thesmall number of individuals involved, thepoor overall growth rates achieved and thehigh mortality in the experimental groupsseverely limit the usefulness and credibilityof their results. Generally, growth rates, par-ticularly weights, achieved on farms exceedthose in the wild. One-year-old wild Indo-Pacific crocodiles attained 0.73 m and0.87 kg, while farmed ones of the same ageaveraged 0.75 m and 1.36 kg (Webb et al.,1991).

Crocodiles may continue growingthroughout their life, males faster thanfemales. The growth of adult females is fur-ther reduced by reproductive demands. Withincreasing age the growth in length slowsdown and is replaced by growth in width,leading to a maximum length, at least inAmerican alligators, which might not beexceeded (Woodward et al., 1995). Youngfemales lay smaller eggs and smallerclutches than older ones. There is also someindication that, in individual females, eggsize and clutch size are inversely related.

Allometry

Allometric studies have shown that the bodyand tail grow faster than the head and legs,although at some stage the snout lengthgrows faster than any other part measured.These changes in the proportions of the dif-ferent parts of the body allow the growingcrocodiles to adjust to the different demandsmade by the environment on crocodiles ofdifferent sizes (Kramer and Medem, 1955;Junprasert and Youngprapakorn, 1994).

The correlation between myocardial mass,i.e. the mass of the two ventricles of theheart, and body length of Nile crocodileswas examined by Huchzermeyer (1994). Theventricular mass can be used as a standardfor the evaluation of other more variableorgans, particularly the fat body and spleen(see p. 85).

Bone rings

In most crocodilian species growth is sea-sonal and this is reflected by bone deposi-tion. Such growth rings can be detectedhistologically and are used to estimate theage of the crocodile in question (de Buffrénil,1980a,b; de Buffrénil and Buffetaud, 1981;Wagner et al., 1990). Experimentally, thismethod can be enhanced by feeding tetracy-cline which is deposited in the bone in theform of visible, stained rings (Roberts et al.,1988).

The growth rate of crocodilians is limitedby the slow deposition of lamellar bone. Thiswas the case even in the giant crocodileDeinosuchus of the Late Cretaceous period ofNorth America (up to 10 m in length), whichis estimated to have taken 35 years to reachadult size (Erickson and Brochu, 1999).

Age–length–weight relations

The age–length relation depends on thegrowth rate, while the length–weight rela-tion depends on the actual state of nutrition.Consequently these relations differ betweenwild and farmed crocodiles, the latter grow-ing faster and being fatter. There are alsoindividual differences. Some examples ofsuch relations in American alligators, Nilecrocodiles and African dwarf crocodiles aregiven in Tables 1.4 to 1.6. Furtherlength–weight relations for Nile crocodilescan be found in Table 2.10. Mathematicalapproaches to length–mass relationships ofcrocodilians were explored by Wilkinson etal. (1997).

Longevity

While captive American alligators may livefor up to 70 years, they do not appear to

34 Chapter 1

reach more than 50 years in the wild(Woodward et al., 1995). Similar ages may beattained by individuals of other crocodilianspecies. However, estimates may be far out.An American crocodile with an estimatedage of 100 years was mentioned by Jasminand Baucom (1967).

Locomotion

Swimming

The crocodilian body is designed primarilyfor swimming. During this action the frontlegs are held parallel to the thorax, while thehind legs are partially spread out to act asrudders. Sideways movements of the tailprovide the propelling force for both slowand rapid swimming. Rapid swimming canbe extremely fast and can catapult the croco-dile out of the water at a very high speedwhen it attacks a prey on land close to thewater.

At lower temperatures the swimmingspeed is reduced. In juvenile American alli-gators the swimming speed increased at


Table 1.4. Age–length–weight relations of marked and released American alligators (McIlhenny, 1934).

Age Sex Length (m) Weight (kg)

1 day 0.23–0.24 0.071–0.08532 days 0.34–0.3710 months 0.45 0.2412 months 0.67 1.8415 months 0.69–0.81 1.93–2.3720 months 0.75 1.4121 months 0.79–0.82 1.64–1.842 years 1 month 0.99–1.20 4.35–5.642 years 8 months 1.09–1.14 3.66–4.543 years 2 months 1.27–1.50 7.83–9.573 years 10 months 1.18–1.73 5.06–13.34 years 2 months 1.58–1.71 8.85–17.56 years Female 1.61–1.75 13.6–17.36 years Male 1.75–2.39 18.9–56.69 years Female 2.01–2.08 38.2–40.49 years Male 2.35–2.68 57.0–67.610 years Female 2.17–2.21 49.9–52.810 years Male 2.69–2.87 80.7–132.211 years Male 2.64–3.07 76.9–160.6

Table 1.5. Age–length–weight relations in farmed Nile crocodiles (Loveridge and Blake, 1972).

Age Sex N Length (m) Weight (kg)

19–20 months Female 5 0.91–1.18 1.75–5.332 months Male 4 1.18–1.33 5.5–8.932–33 months Female 4 0.98–1.40 3.2–9.746–47 months Female 2 1.18–1.75 5.9–25.451–54 months Female 2 1.91 32.6–33.5

Female 2 2.82 125Male 1 3.92 312

Table 1.6. Age–length–weight relations of twoAfrican dwarf crocodiles reared in captivity(Helfenberger, 1982).

Age Length (m) Weight (kg)

10 weeks 0.26–0.31 0.08–0.146 months 0.36–0.41 0.23–0.401 year 0.63 1.29–1.402 years 0.77–0.78 2.01–2.70

temperatures from 15°C to 20°C, but not between 20°C and 30°C (Gatten et al.,1991).

Sliding

Sliding occurs when the body is not lifted offthe ground. This kind of motion is used overshort distances on land and always whengoing into water. Sometimes referred to as‘sprawling’, it is also seen in the transitionfrom stationary to ‘high walk’ (Elias andReilley, 1996). On farms sliding can damagethe chin, the belly skin and the soles of thefeet if the floor of the pen consists of concretethat is not absolutely smooth or covered witha protective paint.

Gharials cannot walk. On land they slide,moving their body forward with all four legsacting simultaneously.

Walking

When walking the crocodile lifts its wholebody off the ground. In this way it can moveover rough terrain without getting scratchedor torn. It is a stately motion, similar to thatof a tortoise when walking. It is also referredto as ‘high walk’.

Running

A faster way of moving on land is running,which is a kind of galloping motion. This canbe quite fast, but can only be sustained overshort distances.

Jumping

Hatchlings and yearlings of the Africandwarf crocodile have an additional mode oflocomotion. They use their relatively stronghind legs to jump in a frog-like fashionwhen frightened while on land. Each jumppropels the hatchling forward by up to 1 m and it may jump several times insuccession.

Crocodiles can also jump out of deepwater to catch prey high above the water orout on land. To achieve this they gatherspeed under water before surfacing.

Digestion

Ingestion

Small prey is swallowed whole, though it isat least punctured during the act of catchingand killing. Larger prey is masticated for awhile before deglutination (Diefenbach,1975a). However, crocodiles do not reducethe size of the morsels by prolonged chew-ing. Excessively large prey is reduced byworrying and ripping off bits or limbs byrapid rotation around the longitudinal axisof the crocodile. Ripping is facilitated whenseveral crocodiles feed from the same car-cass.

Small bits are taken off the ground byholding the head sideways (see Fig. 3.20).

Reduction

In the stomach the swallowed food isexposed to the action of hydrochloric acid(HCl) and peptic proteolysis. Their secretionis stimulated by the presence of the food,while penetration into the food is facilitatedby the puncturing and chewing that hastaken place before swallowing. Gastric pHdrops as low as 1.2 and in fasting animalseven stays below 2.5 (Diefenbach, 1975a).Gastric contractions mixing the stomach con-tents take place 2–3 times per minute whenthe stomach is full (Diefenbach, 1975b). At30°C complete emptying of the stomach took99 h on average and at 15°C 315 h(Diefenbach, 1975b). However, Kanui et al.(1991) recorded gastrointestinal passagetimes in 12-week-old Nile crocodiles as 35 hat 30°C and 44 h at 25°C.

Lithophagy

Stones (gastroliths) are often found amongcrocodilian stomach contents. The questionremains whether these stones are needed togrind the ingested food, similar to the situa-tion in an avian gizzard, whether they areneeded as ballast, or whether they are swal-lowed accidentally (Sokol, 1971) (see alsop. 15). Here it should be noted that predatory(carnivorous) birds do not use stones in theirgizzards. Fitch-Snyder and Lance (1993)

36 Chapter 1

observed captive juvenile American alliga-tors actively seeking out and swallowinggravel. However, this could have been due toa behavioural disturbance similar to the fre-quently seen ingestion of foreign objects bystressed farmed or captive ostriches(Huchzermeyer, 1996a) (see also pp. 281 and290).

Regurgitation

When American alligators eat hairy prey, theindigestible hair forms hair balls, which arethen regurgitated. Smaller foreign bodiesmay also become incorporated in these hairballs and regurgitated as well. Even radiocollars attached to released juvenile alliga-tors have been found regurgitated after thebearers had been cannibalized (Chabreck,1996; Chabreck et al., 1996).

Digestion

The combined action of pepsin and HCl inthe stomach digests most of the protein inthe food and dissolves the bones of the prey.Further protein, glycogen and fats aredigested in the upper small intestine underthe action of bile and pancreatic secretions.There is some evidence that frequent fillingof the stomach reduces the digestive effi-ciency of the system (Webb et al., 1991).There is a suspicion that excess fat in the dietmight interfere with proteolytic activity andtherefore Webb et al. (1991) recommend amaximum of 9% fat in crocodile rations.

Assimilation

Assimilation is the uptake of the digestedfood from the intestine either into the venouscirculation and hence into the liver, or via thelymph directly into the general circulation.This takes place throughout the length of thesmall intestine (duodenum, jejunum andileum).

Seasonal suppression of appetite

Coulson et al. (1950) observed that captiveAmerican alligators practically stopped feed-ing during autumn and winter, although

they were kept at a constant temperature. Itis unclear whether this response was trig-gered by diminishing daylength or whetherit might be governed by a built-in bodyclock. This phenomenon has also beenobserved in captive Nile crocodiles (personalcommunication, L. Fougeirol, Pierrelatte,2002).

Normal oral flora

Identification of the oral flora of crocodiliansis important for the treatment of bitewounds. The work done on American alliga-tors can be taken as representative for allcrocodilian species. Doering et al. (1971)isolated Clostridium spp., Citrobacter,Enterococcus spp. ‘and others’ from twoAmerican alligators. Flandry et al. (1989)examined ten alligators from three differentlocations and found both aerobic and anaer-obic bacteria in all of them, but isolated fungifrom only seven individuals (Tables 1.7–1.9).

The bacterial oral flora of 19 farmed spec-tacled caimans in Brazil comprised the gen-era Citrobacter, Providencia, Escherichia,Proteus, Morganella, Serratia, Edwardsiella,Aeromonas, Acinetobacter, Staphylococcus,Streptococcus and Bacillus (Matushima andRamos, 1993).


Table 1.7. Oral anaerobic bacterial flora of tenAmerican alligators (Flandry et al., 1989).

Genus Species N

Bacteroides asaccharolyticus 2bivius 3loeschei/denticola 2oralis 3sordellii 1thetaiotamicron 1vulgatus 1

Clostridium bifermentans 3clostridioforme 1limosum 1sordellii 2tetani 1

Fusobacterium nucleatum 2varium 3

Peptococcus magnus 1prevotii 3

N, number of isolates.

Crocodiles, particularly in captive or farmsituations, tend to contaminate their aquaticenvironment with faecal bacteria and fungi.Thus it is not surprising that the oral florashould be similar to that of the intestine.

Flora of the gular and paracloacal glands

Williams et al. (1990) isolated the followingaquatic and intestinal bacteria from either orboth pairs of the exocrine skin glands of 23adult American alligators: Acinetobacter ani-tratus, A. wolffi, Aeromonas hydrophila, Bacillussp., Citrobacter amalonaticus, C. freundii,Corynebacterium sp., Enterobacter agglomerans,E. cloacae, Edwardsiella tarda, Escherichia coli,E. hermanii, Flavobacterium indoltheticum, F.gleum, F. multivorum, Hafnia alvei, Klebsiellapneumoniae, Proteus mirabilis, Pseudomonascepacia, P. maltophila, Serratia marcescens andYersinia enterocolitica.

Normal intestinal flora

The intestinal flora plays an important pro-tective role by occupying the availableattachment sites and thereby displacingpathogenic intruders, a phenomenon referredto as competitive exclusion. Intensivelyreared crocodiles often have a single-speciesflora, an abnormal situation that makes themprone to intestinal infection. Despite itsimportance, this appears to be a neglectedsubject, probably partly due to the difficultyof obtaining specimens from animals in thewild, since they are usually in remote places.Most of the published results are from cap-tive crocodiles and it is doubtful that theyare representative of a normal intestinalflora.

Campylobacter fetus subspecies jejuniserotype 23 was isolated from a captiveAfrican dwarf crocodile (Luechtefeld et al.,1981). Misra et al. (1993) examined cloacalswabs of 23 captive gharials and the resultsare shown in Table 1.10.

38 Chapter 1

Table 1.8. Oral aerobic bacterial flora of tenAmerican alligators (Flandry et al., 1989).

Genus Species N

Acinetobacter calcoaceticus var. wolffi 1Aerobacter radiobacter 3Aeromonas hydrophila 9Citrobacter freundii 4Corynebacterium sp. 1Diphtheroides sp. 2Enterobacter cloacae 2Klebsiella oxytoca 1Moraxella sp. 1Morganella morganii 1Pasteurella haemolytica 1

sp. 1Proteus vulgaris 7Pseudomonas cepacia 2

fluorescens 1pickettii 1

Serratia odorifera 1


Table 1.9. Oral fungal flora of ten Americanalligators (Flandry et al., 1989).

Genus Species N

Aspergillus flavipes 1Candida humicola 1

lipolytica 1rugosa 2zeylansides 1sp. 1

Cladosporium sp. 1Curvularia sp. 1Drechsleria sp. 1Epicoccum sp. 2Fusarium sp. 1Penicillium sp. 1Rhodotorula rubra 2Trichoderma sp. 2Trichosporon beigelii 2Torulopsis sp. 1Unidentified moulds 6

N, number of isolates.Table 1.10. Aerobic bacterial intestinal flora ofcaptive gharials, N = 23 (Misra et al., 1993).

Organism Pure Mixed

Staphylococcus sp. 4 10Aeromonas hydrophila 1 6Citrobacter sp. – 6Edwardsiella tarda 3 –Haffnia alvei 1 –Escherichia coli 2 7

Roggendorf and Müller (1976) isolatedCitrobacter sp., Escherichia coli, Proteusmirabilis, P. vulgaris and Aeromonas hydrophilafrom the faeces of one captive Nile crocodileand Citrobacter sp., Providentia rettgeri andAeromonas hydrophila from the faeces of a C.crocodilus.

Huchzermeyer and Agnagna (1994)reported the isolation of aerobic bacteriaand fungi from 21 wild-caught and severelystressed African dwarf crocodiles whichwere sampled when they were slaughteredat markets in Brazzaville, Congo Republic.These and subsequently published iso-lations from samples collected during a second expedition in 1995 (Huchzermeyer

et al., 1999) are shown in Tables 1.11 and1.12.

Respiration

Ventilation

There are two types of ventilatory move-ments, pharyngeal and thoraco-abdominal.Pharyngeal ventilation does not contribute tothe air flow to the lung. It only serves to moveair through the nasal passages for olfaction.Thoraco-abdominal movements involve thediaphragmatic muscles for inhalation and theintercostal and abdominal muscles for exhala-tion (Gans and Clark, 1976).


Table 1.11. Aerobic bacterial intestinal flora of African dwarf crocodiles (Huchzermeyer et al., 2000).

Genus Species N (1993) N (1995)

Alcaligenes faecalis 2Bacillus alvei 1

cereus 11 4circulans 1coagulans 1

Citrobacter amalonaticus 1freundii 3

Dermacoccus nishinomyaensis 1Enterobacter agglomerans 1 1

cloacae 7gergoviae 1

Enterococcus caecorum 1durans 1faecalis 1faecium 10 1pseudoavium 7solitarius 1

Escherichia coli 8Flavobacterium balustinum 1

odoratum 1Klebsiella oxytoca 2 2Kocuria varians 1Kurthia gibsonii 3Lactobacillus sp. 1Micrococcus luteus 4Proteus mirabilis 6 2Salmonella serovars 3Serratia odorifera 1Staphylococcus chromogenes 4

epidermidis 1xylosus 2

Streptococcus salivarius 1Streptomyces sp. 1


Respiratory rate

Respiration takes place in cycles of two tothree rapid movements followed by a longerpause (Gans and Clark, 1976). The respiratoryrate depends on the size of the animal,decreasing with increasing body mass (Gansand Clark, 1976). It is also influenced by tem-perature, increasing with increasing bodytemperature (Campos, 1964; Smith, 1976),with lower rates during warming than duringcooling (Smith, 1976). There appeared to be alow correlation between the metabolic rateand the respiratory rate (Huggins et al., 1971).Respiratory rates for different sized crocodilesare given in Table 1.13. The respiratory rate of123 crocodiles of 27.4 min�1 reported bySigler (1991) falls entirely outside the range ofall the other observations and may possiblyinclude pharyngeal (gular) movements.

Diving

The following is based on work with Indo-Pacific crocodiles by Wright (1987). Most vol-untary dives are short, only lasting ±5 min.During these dives the metabolism stays aero-

bic. Forced dives occur when the crocodile isdisturbed and can last for up to 1 h. Duringthese dives the metabolism slows down andbecomes anaerobic as an oxygen debt devel-ops. A crocodile disturbed during a voluntarydive immediately changes its metabolism.The diversion of the arterial blood flow awayfrom muscles during forced diving conservesoxygen reserves for the functioning of thebrain. Lactic acid accumulated in the musclesenters the circulation only after the crocodileemerges (Andersen, 1961).

Oxygen consumption

In both American alligators and Nile croco-diles, the oxygen consumption of inactiveanimals was found to increase as the temper-ature rose. However, in Nile crocodiles itwas found to decrease between 25 and 30°Cand then rise again steeply to 35°C (Brownand Loveridge, 1981; Lewis and Gatten,1985). The decrease is seen as an adaptationto nocturnal activity, which is usually atlower temperatures (Brown and Loveridge,1981). In the American alligator values rang-ing from 0.08 to 0.2 ml g�1 h�1 correspond

40 Chapter 1

Table 1.12. Fungal intestinal flora of African dwarf crocodiles (Huchzermeyer et al., 2000).

Genus Species N (1993) N (1995)

Acremonium sp. 1Arthrinium sp. 1Aspergillus clavatus 5

flavus 2niger 2

Beauveria sp. 3Candida guillermondii 2 2

krusei 1Chrysosporium sp. 3Cryptococcus lipolytica 3 3

luteolus 1Curvularia sp. 1Fusarium sp. 1Geotrichum candidum 4Paecilomyces sp. 2Penicillium sp. 7 2Phoma sp. 2Trichoderma sp. 1Trichosporon beigelii 2

capitatum 1


with those cited from a number of reports(Lewis and Gatten, 1985). Similar valueswere established for the Nile crocodile(Brown and Loveridge, 1981).

Non-respiratory CO2 excretion

A relatively low respiratory quotient in croc-odilians is explained by the excretion of largeamounts of ammonium bicarbonate in theurine (Coulson and Hernandez, 1964; Grigg,1978), while Davies (1978) suggested cuta-neous CO2 loss as an explanation (see alsobelow).

Acid–base balance

In American alligators and in Indo-Pacificcrocodiles, arterial pH decreased with risingbody temperature, while arterial PCO2increased (Davies, 1978; Davies et al., 1982;Seymour et al., 1985; Douse and Mitchell,1991).

Respiratory regulation

In progressively anaesthetized American alli-gators it was shown that central chemorecep-tors play a significant role in ventilatoryregulation (Branco and Wood, 1993).

Excretion

Fasting crocodiles and alligators produceapproximately equal quantities of ammonia

and uric acid in their urine, but when theyare fed maximally the excretion of ammoniaincreases while the proportion of uric acid inthe urine decreases. This decrease in uricacid clearance leads to increased plasma uricacid levels, predisposing the animals to gout(see p. 230). Only negligible amounts of ureaare produced (Khalil and Hagagg, 1958;Herbert, 1981). The white deposits in croco-dile urine consist mainly of uric acid crystals(Khalil and Hagagg, 1958).

The glomerular filtration rate remainsfairly constant under different conditions,and the tubules have little capacity to regu-late the osmolality of the urine. However,cloacal absorption varies with the salt load(Schmidt-Nielsen and Skadhauge, 1967).Salt lost into the freshwater environment isreplaced constantly by the salt contained inthe prey. Excess salt is excreted by special-ized salt glands, as is the case in othermarine reptiles (Schmidt-Nielsen andFange, 1958) (see also p. 14). Ammonia isthought to be excreted in the form ofNH4HCO3 which may be responsible for asubstantial deficit in respiratory CO2(Schmidt-Nielsen and Skadhauge, 1967;Grigg, 1978) (see above).

Responses to high salinity

All alligatorines and most crocodiles arefreshwater species with poor salt tolerance.However, four crocodile species (C. porosus,C. johnsoni, C. niloticus and C. acutus) have


Table 1.13. Respiratory rates of crocodiles.

Species Mass (kg) Breaths per min Temperature (°C) Reference

Caiman crocodilus 0.18 0.58 23–25 10.29 0.63 10.65 0.57 14.8 0.25 14.8 0.14 15.0 0.17 1

Alligator mississippiensis 1.15–8.78 3.3a:1.5b 20.46–1.31 0.39–4.95 23–25 3

a During cooling.b During warming.1, Gans and Clark (1976); 2, Smith (1976); 3, Huggins et al. (1971).

estuarine populations. Large specimens of C.acutus lose weight more slowly in sea waterthan small ones, and NaCl loading causes areduction in cloacal flow rate, thus conserv-ing body water (Ellis, 1981).

Alligators osmoregulate by keeping a lowbody sodium turnover, by the low perme-ability of the skin to sodium and even bykeeping a relatively low water turnover.Estuarine crocodiles add to that effect by theexcreting of excess salt through the lingualsalt glands (p. 14). Freshwater species ofcrocodiles also have these salt glands andmay use them in aestivation during droughtperiods (Mazzotti and Dunson, 1989).

Water loss through the skin when it isexposed to dry air may be considerable andthe lost water can only be replaced by drink-ing, not absorbed through the skin(Cloudesley-Thompson, 1968).

Reproduction

Laying cycle

Crocodiles reproduce by laying eggs, as thetemperature control of sex determinationdoes not allow internal incubation (ovovi-vipary) as occurs in some snakes andlizards. Most species lay only one clutch ofeggs per year, the mugger being the excep-tion, with two cycles per year occurring reg-ularly (Whitaker and Whitaker, 1984).However, many females in the wild do notreproduce every year, probably dependingon their nutritional state (Lance, 1987;Kofron, 1990).

Clutch and egg size

Egg size and egg number per clutch arespecies dependent but increase with the sizeand age of the female, with younger femaleslaying small eggs from which fewer, smallerand more slowly growing hatchlings are pro-duced.

Hormonal control

The hormonal control of the reproductivecycle and factors influencing this control

have been described by Lance (1987). A sex-steroid-binding protein, seasonally presentin the plasma of female American alligatorsand probably other crocodiles as well, pre-vents the delivery of free steroid to targetorgans outside the breeding season (Ho et al.,1987).

Ovulation

All follicles are normally ovulated togetherover a period of a few hours (personal com-munication, V.A. Lance, San Diego, 2000),but according to Youngprapakorn (1990b)sometimes some follicles ovulate prema-turely and proceed through the oviduct tothe uterus in advance of the others.Fertilization takes place in the infundibulumor upper oviduct before the albumen andshell are secreted in the glandular part of theoviduct (uterus). The eggs are then stored inthe muscular part (vagina) until they arelaid. In the American alligator the eggs arestored in the vagina for 3–3.5 weeks beforethey are laid (Lance, 1989). During this time,before oviposition, initial embryonic devel-opment is already taking place, to the 15–17somite stage and occasionally further (per-sonal communication, V.A. Lance, San Diego,2000). Oestradiol liberated during ovulationincreases plasma calcium levels for the pro-duction of the eggshells, but, unlike birds,crocodiles do not deposit calcium in theirbones before ovulation (Elsey and Wink,1986).

Nesting and incubation

Nesting habits vary from species to species.Forest-dwelling species build nest moundsfrom leaves scooped up from the forest floorand depend on the heat produced by com-posting, rather than on the sun, to incubatethe eggs. Swamp dwellers make nest mountsfrom swamp vegetation and rely on com-posting heat as well as on the sun for theincubation of the eggs, while crocodiles liv-ing in rivers nest in the sandy banks abovethe flood level and rely on the sun for incu-bation heat. All eggs in the clutch aredeposited into the nest at the same time andcovered again with nesting material. The

42 Chapter 1

incubation period depends on the species aswell as on incubation temperature, decreas-ing with rising temperature, and rangesroughly from 60 to 90 days.

Cross-breeding

Several species of crocodiles cross-breed voluntarily, producing fertile hybrids(Youngprapakorn, 1990a; Thang, 1994). Asthese hybrids tend to be more vigorous, theyare sought after by some farmers. Escapedhybrids, however, can pollute existing wildpopulations and this constitutes a consider-able danger to the conservation of certaincrocodile populations.

Circulation

Blood flow

The flow of blood transports oxygen andnutrients to the organs and tissues, and CO2and end-products of metabolism from theorgans and tissues to the lungs and kidneys.In addition, it can speed up the transport ofheat from the skin to the internal organswhen the crocodile is basking, move whiteblood cells and antibodies to infection sites,and hormones to targeted organs. A 70 kgAmerican alligator at 28°C has a blood flowof 0.2 l min�1, a stroke volume of 6.3 ml, acirculation time of 27 min and 4% of themetabolic rate of a person of equal mass(Coulson et al., 1989).

Heart rate

The heart rate depends on the size of the ani-mal and on the temperature. In 57- to 78-cm-long American alligators at an ambienttemperature of 22–25°C it was 18.7 beats perminute (Huggins et al., 1971). In anaes-thetized American alligators from 1.5 to4.3 kg live mass it ranged from 10 beats perminute at 10°C to 30 beats per minute at30°C (Campos, 1964). At 38°C and aboveirreversible damage occurred through over-heating (Wilber, 1960).

At 28°C a 70 kg American alligator had ablood flow of 0.2 l min�1, a stroke volume of

6.3 ml and a circulation time of 27 min(Coulson et al., 1989).

Bradycardia

Diving bradycardia occurs when crocodilesdive after a sudden fright. Under these cir-cumstances the heart rate decreases fromaround 30 beats per minute to 2–5 beats perminute, but not during voluntary (short-term) dives (Gaunt and Gans, 1969; Smith etal., 1974). During bradycardia the blood pres-sure is maintained by peripheral vasocon-striction (Jones and Shelton, 1993).

Shunt

Under certain conditions, venous (deoxy-genated) blood can become mixed with arte-rial (oxygenated) blood through the foramenof Panizza, through direct release into theright aorta and through the anastomosesbetween the right and left aortas (see p. 23).This mixing of venous and arterial blood isreferred to as a left-to-right shunt. Jones andShelton (1993) described a biphasic systolicpressure curve in the right ventricle of rest-ing crocodiles in which the first phase sup-plies the pulmonary artery and the secondphase supplies the right aorta. This shuntdiverted 15–25% of the venous blood awayfrom the pulmonary circulation. They specu-lated that in addition to the respiratoryrequirements for a shunt during forced div-ing, the alkaline wave caused by the produc-tion of HCl in the stomach after a meal alsonecessitated a flow of venous (acidic) bloodto the digestive viscera.

Vasoconstriction

Vasoconstriction is mediated hormonallyand by nervous stimuli and can occur locally,e.g. as a response in thermoregulation (seebelow), or systemically. Adrenaline wasfound to produce a stronger vasoconstrictionin the American alligator than noradrenaline(Akers and Peiss, 1963). Angiotensin I of theAmerican alligator was found to be closelyrelated to that of the chicken (Takei et al.,1993).


Nervous activity

The brain of the crocodile is larger and betterorganized than that of other reptiles, but it isstill relatively small in relation to the croco-dile’s body mass. Many functions are there-fore delegated to centres in the spinal cord.During hypothermia (2–4°C) in restrainedAmerican alligators (size not stated, butprobably large as their sex was stated), theelectrical activity of cerebrum and opticlobes decreased, whereas it increased in thecerebellum (Parsons and Huggins, 1965).

Compared with that of other reptiles, aswell as with that of many birds and mam-mals, the hearing of crocodiles is very acute,particularly in the middle range but less sofor high and low tones (Wever, 1971). On thefarm, the crocodiles rely mainly on smell andhearing to recognize the person usuallyworking with them. In nature they recognizeeach other by the excretions of their skinglands (see p. 52). Therefore, captive orfarmed crocodiles may fail to recognize, andthus be disturbed by, people who occasion-ally wear perfume.

Thermoregulation

Crocodiles are exothermic reptiles, unable tomaintain a constant internal body tempera-ture independently of the environment.However, they try to achieve and then main-tain their temperature within a preferredrange, and they do this by making use ofthermogradients in the environment. Thesegradients exist between sun and shade,warm surface water and cool deep water.Some species also make use of burrows inwhich their rate of cooling during winternights would be slower than in cold water(Pooley, 1962) or which protect them fromheat and dehydration during aestivation(Christian et al., 1996).

During cooling the blood circulation tothe body surface is restricted, thus reducingthe rate of cooling. During warming theblood flow to the skin is increased and thewarmed blood transports the heat to theinternal organs (Johnson, 1974; Grigg andAlchin, 1976; Johnson et al., 1976; Drane et al.,

1977; Johnson and Voigt, 1978; Smith andAdams, 1978; Smith et al., 1978; Smith, 1979).When basking in shallow water, the bloodsupply to the submersed skin is reduced,while it is increased to the skin exposed tothe air and sun (Johnson, 1974). The osteo-derms may also play a role in thermoregula-tion as heat collectors (Seidel, 1979). Gapingincreases evaporation and thereby con-tributes to cooling, which at certain times ofthe day appears to be preferred to going intothe water. However, gaping may also beused to increase the temperature-exchangesurface. Consequently Nile crocodiles havebeen observed gaping while basking on acold African winter morning (own observa-tion).

The preferred temperature depends onthe crocodile’s activity: fasting crocodilesprefer cooler and feeding ones select highertemperatures (Lang, 1979). Endogenous(metabolic) heat plays a role only in verylarge crocodiles with a low surface area tomass ratio (Smith, 1979).

In very cold winter weather Americanalligators remain close to the surface, withonly the nostrils protruding from the water.In this position, called ‘icing’, they are safefrom suffocation when the water freezes over(Hagan et al., 1983; Lee et al., 1997). However,even such specimens do not survive if theirinternal temperature falls below 4.5°C(Brisbin et al., 1982). A released Americanalligator in a swamp in Pennsylvaniaappears to have survived at least six coldwinters before it was shot (Barton, 1955).Nile crocodiles tolerate a minimum internaltemperature of 10°C.

Exposing juvenile farmed crocodiles tovarying temperature regimes, Turton et al.(1994) found that high temperatures aremore stressful than lower ones, and that tem-perature changes are always accompaniedby increased corticosterone levels. Certainfarming conditions tend to expose the croco-diles periodically to overheating as well as towidely fluctuating day–night temperatures,a situation that is obviously to be avoided. Itis my belief that for their well-being croco-diles need to be able to thermoregulateactively along a thermogradient within therange of preferred temperatures. They

44 Chapter 1

should also be strictly protected from forcedoverheating, i.e. being exposed to high tem-peratures without any means of avoiding theheat or being able to cool down.

The growth rate of juvenile crocodiles isclosely related to the temperature at whichthey are kept, with the fastest growth seen inthose kept closest to the preferred maximumtemperature, and particularly in those withthe highest preferred temperature (Lang,1987). As the preferred temperature is influ-enced by the incubation temperature, one canactively select for a higher temperature pref-erence, and thus for faster growth, by incubat-ing at a higher temperature (Lang, 1987).

Immunity

Crocodiles can react to infections by devel-oping antibodies and thus becomingimmune to the agent in question. The whiteblood cells that play a role in this system

have been described above (p. 25). Inresponse to a stimulus, lymphocytes are pro-duced in the thymus and spleen. An activespleen increases in size very rapidly, but asthe tough fibrous capsule resists this rapidgrowth, the active tissue buds out throughthe capsule, giving the hypertrophic spleenan irregular, knobby appearance (Fig. 1.46).

Unlike other reptiles, crocodiles are capa-ble of an anamnestic response. YoungAmerican alligators immunized with 50 mghaemocyanin had antibodies in their bloodafter 20 days. However, when given a secondinjection of 2.5 mg, antibodies becamedetectable after only 2 days (Lerch at al.,1967). An immunoglobulin with two IgG-likelight chains was isolated from American alli-gators by Saluk et al. (1970). Turton et al.(1994) isolated an immunoglobulin fromjuvenile Indo-Pacific crocodiles and identi-fied it as IgG, with a molecular weight of218 kDa and heavy and light chains of 57and 27 kDa, respectively.


Fig. 1.46. ‘Budding’ hypertrophic spleens as a consequence of an immune response.

American alligators did not have any iso-haemagglutination, but their serum con-tained three agglutinins, one for all humancells, another similar to the �-agglutinin andone similar to the �-agglutinin of humanserum (Bond, 1940).

Inflammation

Exudation

Inflammation is a reaction by the body tolocalize, isolate and fight a local infection orother injury. The first step is a congestion ofthe local capillaries, allowing serum to seepinto the tissue and cause oedema. In mam-mals, the liquid from this oedema is filteredwith the lymph through lymph nodes, butcrocodiles, like birds, lack lymph nodes. Toprevent the drainage of pathogens away fromthe inflammation site directly into the generalcirculation, they exude fibrin into the inflamedsite, which immobilizes all the pathogens andprevents their escape. This is a very successfulstrategy, with the result that crocodiles andbirds rarely contract septicaemia from woundinfections. However, if the inflammatory cellsare unable to remove the invading pathogens,the exudation process continues and ulti-mately can lead to serious problems.

Abscess, fibriscess

Fibrin also inhibits the movement of leuco-cytes and prevents the liquefaction ofnecrotic tissue, with the result that trueabscesses filled with liquid pus cannot beformed. Hard swellings forming at the site ofan infected wound consist of sheets of fibrinbetween the tissues and these are extremelydifficult to remove surgically. Veterinariansoften refer to this exudate erroneously as‘inspissated pus’. Since such a fibrin-filledswelling cannot be classified as a trueabscess, it should rather be called fibriscess(Huchzermeyer and Cooper, 2000).

Cellular reactions

After subcutaneous injection of turpentineinto juvenile American alligators, Mateo et al.(1984b) observed oedema followed by gran-

ulocyte migration in the first 3 days. Latermonocytic cells predominated, includingvacuolated macrophages. From 14 daysonwards zones of necrotic debris (most likelyexudate, see above) were surrounded by pal-isades of vacuolated multinucleated giantcells and capillary-laden immature fibrousconnective tissue.

Fever

Fever results from a higher setting in an ani-mal’s thermoregulatory system in reaction toan infection or similar event. In endothermsthe increase in temperature is achieved meta-bolically, but crocodiles, as ectotherms, haveto adjust their temperature behaviourally byselecting a higher temperature on the envi-ronmental gradient (Lang, 1987) (see p. 44).

Disease

In a holistic view, a healthy animal lives in astate of balance with its natural environment.Within certain ranges it can respond to allphysical, chemical and biological challenges.These challenges may act singly or in combi-nation (Fig. 1.47). The responses are thedefences. An animal that is unable to defenditself adequately against any such single orcombined challenge slides into a state ofimbalance that is referred to as disease(Wedemeyer et al., 1976).

Captive, farming and ranching conditionsare usually different from natural conditionsand often far from ideal. Often they increasethe severity of the challenges while limitingthe animal’s ability to respond. Such condi-tions can easily cause an animal to becomeimbalanced and diseased.

From the holistic definition of disease it isclear that such a state cannot be diagnosedmerely by examining the affected animalalone, nor by the laboratory analysis of cer-tain specimens taken from the diseased ordeceased animal. In addition, all factors inthe environment, as well as nutrition, haveto be taken into consideration. Equally, allcontributing environmental and other factorsmust also be considered when formulating a

46 Chapter 1

course of treatment or a prophylactic pro-gramme. It is for this reason that chapters onbehaviour, nutrition and farming practiceshave been included in this book.

It is of little use if in a diagnosis the terms‘stress’ and ‘poor management’ are usedwithout clarifying the exact circumstancesinvolved in the particular case, nor does theisolation of a pathogen from a crocodile nec-essarily mean that this was the primary causeof disease or death. Also, none of the croco-dile-specific pathogens (viruses, bacteria, etc.)are primary pathogens. All are opportunists,waiting for a weakened or stressed animal inwhich to produce the specific disease. In allsuch cases one should always ask: Why didthis happen? One should always investigatethe circumstances of the outbreak.

In a way, it is unfortunate that in a booklike this the individual diseases have to bediscussed in relation to their causal agent,when in reality they are all influenced oreven triggered by environmental factors.

Crocodilian Biochemistry

This section concentrates on diagnostic bio-chemistry, trying to give normal values, asfar as they are known.

Blood biochemistry

Published values of the blood (serum,plasma) biochemistry of crocodilians aregiven in Tables 1.14 to 1.16. Since most ofthese values are from captive or farmed ani-mals, there may be some doubt as towhether they can be taken as normal values.Species differences may play a role and thestress involved in immobilizing the animalsfor sampling might also affect the results.However, they may still give some guidancefor the interpretation of results of clinicalinvestigations. In addition, thyroxine valuesare given in Table 1.17.

In juvenile American alligators the injec-tion of alligator, turkey or bovine insulincaused a hypoglycaemia lasting from 12 to120 h after the injection, and a much morerapid decrease in plasma amino acids lastingfrom 2 to 36 h after the injection (Lance et al.,1993).

All blood chloride, bicarbonate, pH andsodium values should be determined on ani-mals that have been fasting for at least 3days. This is because far-ranging changes arebrought about by the alkaline tide followingthe ingestion of food, with all the accompa-nying changes in blood electrolytes (Coulsonet al., 1950).


Fig. 1.47. Schematic drawing of the physical, chemical and biological challenges countered by theappropriate responses of the crocodile in a state of balance.

48 Chapter 1

Table 1.14. Blood biochemistry of farmed and captive crocodiles.

Parameter Unit A.m.a C.l.b C.m.c C.n.d T.s.e C.p.g

Total protein g dl�1 5.21 9.37 5.3 3.7 4.1–7.0Albumin g dl�1 1.87 1.9 1.4–2.3Globulin g dl�1 3.33 3.1 2.7–5Glucose mg dl�1 92.0 81.82 52.95 81.6 75.3

mmol l�1 4.5–12.1Calcium mg dl�1 10.73 10.5 2.4–2.8f 10.2

mmol dl�1 2.41–3.45Phosphorus mg dl�1 5.73 3.0 3.4

mmol dl�1 1.2–2.9Sodium mmol dl�1 144.2 155.9 143–161Potassium mmol dl�1 3.71 4.4 3.8–7.2Magnesium mmol dl�1 0.8–1.4Chloride mmol dl�1 104.2 120.0 88–127Total serum iron �mol dl�1 1–19Uric acid mg dl�1 3.03 8.17 4.1 3.2

�mol dl�1 167–988Urea mg dl�1 3.8Bilirubin mg dl�1 0.16 0.47Cholesterol mg dl�1 120.8 231.5 110.5

mmol l�1 1.1–7.2Triglyceride mmol l�1 0.1–8.8

mg dl�1 46.2Creatinine mg dl�1 1.06 0.21

�mol dl�1 20–51GOT IU l�1 16.6 18.0GPT IU l�1 13.1 20.2ALP IU l�1 30.03 17.8 31–180ALT IU l�1 46.05 11–51AST IU l�1 223.5 23–157BUN mg dl�1 0.99 1.45T4 nmol l�1 4.95T3 nmol l�1 0.2rT3 nmol l�1 0.7LDH IU l�1 426.2

A.m., Alligator mississippiensis; C.l., Caiman latirostris; C.m., Crocodylus moreletii; C.n., Crocodylusniloticus; T.s., Tomistoma schlegelii; C.p., Crocodylus porosus.a Barnett et al. (1998); b Tourn et al. (1994); c Sigler (1991); d Foggin (1987); e Siruntawineti andRatanakorn (1994); f Morpurgo et al. (1992); g Millan et al. (1997a).GOT, glutamate oxaloacetate transaminase; GPT, alkaline phosphatase; ALP, alkaline phosphatase; ALT,alanine aminotransferase; AST, alanine transaminase; BUN, blood urea nitrogen; T4, thyroxine; T3, tri-iodothyronine; rT3, reverse triiodothyroxine; LDH, lactate dehydrogenase.

Urine biochemistry

The nitrogenous wastes excreted by the kid-neys consist of uric acid, urea and ammoniain the form of ammonium bicarbonate(NH4HCO3). Crocodile urine, like that ofbirds, consists of a liquid and a solid portion.Values determined from the liquid urine offasting crocodiles are given in Table 1.18. The

urine solids of the Nile crocodile were com-posed of 6% ammonia and 88.6% uric acid; nourea was present (Khalil and Haggag, 1958).

The full composition of the urine of fastingAmerican alligators is given in Table 1.19. In acomparison between maximally fed Americanalligators (fed ad libitum five times per week)and those given a single large meal, it wasfound that uric acid excretion levels were sim-

ilar in both groups, while the excretion ofammonia was low in the single-meal group.However, uric acid clearance was also low inthe single-meal group, with high levels ofplasma uric acid (Herbert, 1981) (see p. 41).

Mineral values

Plasma

Plasma mineral values of wild and farmedmale American alligators, lengths rangingfrom 185 to 325 cm (wild) and 230–326 cm(farmed) (Lance et al., 1983), are shown inTable 1.20.

Organs

For organ mineral values of American alliga-tors and Nile crocodiles see Tables 6.1 and 6.2.

Bones

The mean mineral composition of the ribs ofthree wild Nile crocodiles from the KrugerNational Park, South Africa, was: Ca, 17.9%;P, 7.9%; Mg, 0.38%; F, 713 �g g�1 (Swanepoelet al., 2000). It is quite possible that the skulland legs of crocodiles have a higher densitythan the ribs.

Composition of crocodile fat

The fatty acid composition of the plasma andof the body fat depend on the sources of fatin the food, but also varies according to the


Table 1.15. Clinical serum biochemistry: means of2-year-old farmed Nile crocodiles (n = 5)(Thurman, 1990) and ranges of means of wild Nilecrocodiles from three different rivers in the KrugerNational Park, South Africa (Swanepoel et al.,2000).

Parameter Unit Farmed Wild

Albumin g l�1 9.8–16.38Globulin g l�1 30.7–47.35Glucose mmol l�1 5.9 3.2–11.45Na mmol l�1 153.8 141.5–154.5K mmol l�1 3.8 2.53–5.35Ca mmol l�1 2.97 2.60–3.98Mg mmol l�1 0.52 1.51–2.24SIP mmol l�1 0.88–1.96TSP g l�1 50.2LD IU l�1 301ALP IU l�1 64.2CK IU l�1 211Lactate �mol l�1 22.1Cortisol nmol l�1 <27Urea mmol l�1 0.60–2.62Creatinine mmol l�1 36.5–97.0Cl mmol l�1 88.5–120.5

SIP, serum inorganic phosphate; TSP, total serumprotein; LD, lactatedehydrogenase; ALP, alkalinephosphatase; CK, creatine kinase.

Table 1.16. Blood biochemistry of Caimanlatirostris (means only).

Troiano and Tourn et al. Parameter Unit Althaus (1993) (1993)

Calcium mg dl�1 10.12Creatinine mg dl�1 0.36Phosphate mg dl�1 5.40Glucose mg dl�1 102.2Urea mg dl�1 6.88Cholesterol g dl�1 2.315GOT IU l�1 163GPT IU l�1 19.67LDH IU l�1 1020Total protein g dl�1 5.01Albumin g dl�1 2.42Globulin g dl�1 3.10

GOT, glutamate oxaloacetate transaminase; GPT,alkaline phosphatase; LDH, lactate dehydrogenase.

Table 1.17. Mean plasma thyroxine values ofcrocodiles.

Thyroxine (ng ml�1)

Crocodylus niloticus 1.63(Morpurgo et al., 1992)Crocodylus johnsoni 2.5(Hulbert and Williams, 1988)

Table 1.18. Percentage distribution of nitrogen inthe liquid urine of fasting crocodiles.

Crocodylus niloticus (Khalil Alligator

and Haggag, mississippiensisComponent 1958) (Hopping, 1923)

Ammonia 66.8 66–81Urea 12.5 0–17Uric acid 2.3 7–19.8

species of crocodile (Tables 1.21–1.26). Thedifferent crocodilian species may, in fact,have differing nutritional requirements forsaturated and unsaturated fatty acids. Ahomeostatic mechanism may be lacking, butthere may also be an age effect (Morpurgo etal., 1993a; Gelman and Morpurgo, 1994;Morpurgo and Gelman, 1995).

Nutrient composition of crocodile eggs

Yolk

The lipid and fatty acid composition ofAmerican alligator eggs and the changesduring incubation were described by Nobleet al. (1993). The composition on day 8 ofincubation is shown in Tables 1.27 and 1.28.

50 Chapter 1

Table 1.19. Urine composition of fasting American alligators expressed per kg body mass per day(Coulson and Hernandez, 1964), unit abbreviations as used by the authors.

Parameter Unit Mean Range

Volume ml 17 6–28pH 7.81 7.6–7.93OP mOs l�1 203 157–247NH2 mEq l�1 1.77 0.67–2.4K mEq l�1 0.13 0.01–0.26Na mEq l�1 0.06 0.01–0.1Ca + Mg mEq l�1 0.03 0.02–0.05CO2 as bicarbonate mEq l�1 1.19 0.46–1.47Cl mEq l�1 0.05 Traces to 0.12P mEq l�1 0.45 0.07–0.98SO4 mEq l�1 0.17 0.1–0.26Uric acid N mM l�1 (?) 0.75 0.18–2.14Creatinine mg l�1 0.6 0.37–1.04

OP, osmotic pressure.

Table 1.20. Plasma minerals of wild (n = 24) andfarmed (n = 18–23) male American alligators(Lance et al., 1983).

Parameter Unit Wild Farmed

Calcium mmol l�1 3.12 2.87Magnesium mmol l�1 1.32 1.06Zinc �g ml�1 0.44 0.42Copper �g ml�1 0.76 0.60Iron �g ml�1 0.53 0.54Selenium �g ml�1 0.17 0.2Protein g l�1 0.564 0.553Cholesterol mg l�1 5.81 5.02Vitamin E �g ml�1 5.36 5.25

Table 1.21. Lipid composition (%) of Americanalligator fat from two farms (Peplow et al., 1990).

Triglyceride 77.2 85.1Diglyceride 2.4 2.1Monoglyceride 0.4 1.5Free fatty acids 1.9 1.2Cholesterol 1.8 0.2Phospholipid 4.8 6.7

Table 1.22. Fatty acid composition (%) ofAmerican alligator fat from different trial groupsand different farms (Peplow et al., 1990).

Fatty acid Low High

C14:0 1.3 3.3C14:1 0.00 0.19C16:0 19.9 22.1C16:1 4.4 7.7C18:0 3.1 8.4C18:1 33.2 44.4C18:2 3.4 19.3C18:3 0.9 3.4C20:1 1.1 2.8C20:2 0.01 0.17C20:5 0.1 4.0C22:1 0.00 0.98C22:6 0.7 11.1C24:1 0.00 0.14


Table 1.23. Fatty acid composition (%) in four groups of juvenile Indo-Pacific crocodiles (Garnett, 1985).

Fatty acid Newly hatched Starved Fed lean pork Fed fatty pork

C16:0 19.62 22.81 21.86 22.73C18:0 5.93 9.99 8.59 12.19C16:1 2.95 2.26 2.84 2.94C18:1 30.31 35.27 29.22 41.06C18:2 5.01 8.43 21.18 11.31C18:3 1.70 1.62 2.81 1.85C20:4 3.22 7.31 3.37 1.26C20:5 7.75 0.60 1.07 0.17C22:6 15.55 2.84 2.52 0.41

Table 1.24. Mean percentage plasma fatty acid composition in 3- and 8-year-old farmed and 3–6-year-old wild Nile crocodiles (Morpurgo et al., 1993a).

Fatty acid Farmed (3 years old) Farmed (8 years old) Wild

16:0 38.46 37.04 27.0316:1 0.60 4.95 7.4918:0 9.22 9.94 12.5418:1 19.11 23.74 27.0018:2 20.32 22.79 12.0418:3+20:1 2.79 0.69 3.4420:4 6.82 3.58 2.7120:5 1.25 0.46 2.7422:5 0.22 0.34 1.2522:6 1.50 0.31 3.91

NB: The tables in the paper by Morpurgo and Gelman (1995), referring to the same results, appear tohave been mixed up.

Table 1.25. Fatty acid composition of crocodilemeat (Crocodylus porosus and Crocodylusjohnsoni), averages of 12 samples (Mitchell et al.,1995).

C:n Name %

14:0 Myristic 1.115:0 Pentadecanoic 0.216:0 Palmitic 22.516:1 �-9 0.416:1 �-7 Palmitoleic 5.117:0 Heptadecanoic 0.518:0 Stearic 7.418:1 �-9 Oleic 33.118:2 �-6 Linoleic 15.218:3 �-3 �-Linolenic 4.818:4 �-3 0.120:0 Arachidic < 0.120:1 �-9 Gondoic 0.520:4 �-6 Arachidonic 3.620:4 �-3 0.320:5 �-3 Eicosapentaenoic 0.522:5 �-6 0.422:5 �-3 Docosapentaenoic 1.522:6 �-3 Docosahexaenoic 1.3

Table 1.26. Fat profile of boiled tail meat ofAlligator mississippiensis – means in % (Debyserand Zwart, 1991).

Total fat content 2.9Saturated fat 29.1Mono-unsaturated fat 46.5Poly-unsaturated fat 24.0Cholesterol (mg/100 g) 64.8

Table 1.27. Mean yolk lipid composition (% oftotal lipid) of American alligator eggs incubated at30°C on day 8 (Noble et al., 1993).

Cholesteryl ethers 1.48Triacylglycerols 69.5Free fatty acids 1.60Free cholesterol 7.68Phospholipids 19.8

Albumen

The albumen of avian eggs consists largelyof proteins with antibacterial properties.Crocodile egg albumen contains much fewersolids (3.6% against 12% in birds) and themain protein is a glycoprotein (Burley et al.,1987; Abrams et al., 1989; Rose et al., 1990).An �2-macroglobulin-like protease inhibitorwas identified in the albumen of eggs of theCuban crocodile (Ikai et al., 1983). The possi-bility that the proteins in crocodilian eggshave antibacterial properties has not yetbeen investigated.

Paracloacal and gular glands

The secreta of the paracloacal and gularglands are used by all crocodilians for chem-ical signalling. This is important for therecognition of individuals, of the sex of anyother individual and of conspecifics.

The paracloacal glands of C. crocodilusand Caiman latirostris contained between3.5 g and 34.5 g secreta. They consisted offatty acids, particularly myristic and palmiticacid, nitrogenous bases, glycerol, cholesterol,traces of phosphorus-containing compoundsand an eight-carbon alcohol, yacarol. Thiswas later identified as D-citronellol and wascharacterized by its distinct rose-like scent(Fester and Bertuzzi, 1934; Fester et al., 1937).Citronellol was also found in the paracloacalgland secreta of Paleosuchus palpebrosus andP. trigonatus (Shafagati et al., 1989). The diter-pene �-springene that occurs in the paracloa-cal glands of P. trigonatus is also present inthe secretions of a braconid wasp and of the

springbok antelope, as well as in tobaccoleaves (Avery et al., 1993).

Paracloacal secreta of 80 immature and 15adult American alligators contained hexade-cyl and other acetates and esters, but no freealcohols. There was a high degree of varia-tion between age classes and sexes, but alsoindividually (Weldon et al., 1988). The secretaof the gular glands of American alligatorsconsist of C14, C16 and C18 fatty acids, squa-lene and �-tocopherol, but contain nopheromone (Weldon et al., 1987).

Lipids from the paracloacal glands ofadult Chinese alligators of both sexes con-sisted of acetates, aliphatic alcohols, freefatty acids and waxes, primarily hexade-canoates. The male secretions also containedcholesterol, a diterpene hydrocarbon, cem-brene A and a diterpene ketone (Dunn et al.,1993; Mattern et al., 1997).

The secretions of the paracloacal glands ofO. tetraspis contained an aromatic ketone,dianeackerone, and several aromatic steroidalesters (Whyte et al., 1999; Yang et al., 1999).

A comparative chromatographic study ofthe secretions of gular and paracloacalglands of almost all crocodilian species,except C. novoguineae, was carried out byWeldon and Tanner (1991).

Crocodilian Behaviour

Normal behaviour is characteristic of ahealthy animal. Not to be able to act in accor-dance with its behavioural requirements in acaptive or farm situation may severely stressan animal. Non-domesticated animals, par-

52 Chapter 1

Table 1.28. Mean fatty acid composition (% of total) of the cholesteryl esters, triacylglycerols andphospholipids of the yolks of incubated American alligator eggs on day 8 (Noble et al., 1993).

Fatty acids Cholesteryl esters Triacylglycerols Phospholipids

Palmitic 60.0 29.1 32.1Palmitoleic 5.68 18.5 9.16Stearic 7.76 6.49 7.88Oleic 16.4 32.3 19.3Linoleic 4.47 6.53 4.18Linolenic 1.69 4.58 2.33Arachidonic 3.96 1.02 13.1Docosapentaenoic <1.0 <1.0 2.38Docosahexaenoic <1.0 <1.0 9.67

ticularly crocodiles, are very sensitive to thiskind of stress. It is therefore important forcrocodile farmers and veterinarians to beaware of the behaviour patterns and require-ments of their crocodiles.

Embryonic learning

It has been found that the food selection ofIndo-Pacific crocodiles can be influenced bypainting flavours on to the crocodile eggsduring incubation (Sneddon et al., 1998). Thiskind of embryonic learning may also influ-ence other aspects of hatchling behaviour. Itis possible that by urinating on the nest themother primes the hatchlings to recognizeher when they hatch.

Parental care

Parental care has been observed in manycrocodile species and it is presumably therule in all crocodilians. It includes guardingthe nest, helping the hatchlings out of theegg, carrying them from the nest to the water,guarding them there, responding to the dis-tress calls of young ones in danger and occa-sionally moving the pod to new nurseryareas. All this is done mainly by the female,but, where the adults live in pairs or wherethe female has disappeared, males have beenseen either helping or taking over the care ofthe hatchlings (Alvarez del Toro, 1968).

Imprinting

Imprinting is known from birds, which athatch are imprinted with the image of theirmother and thereby recognize their parentsand later in life choose their sexual mate intheir parents’ image. Human imprinting in intensively reared ostrich chicks can leadto behavioural disturbances, sometimes with serious consequences (Huchzermeyer,1996a).

It is difficult to explain the complex hatch-ling–parent interactions of crocodilians with-out thinking of the possibility of imprinting.A suspected case of human imprinting of

farmed Nile crocodiles in South Africa wasreported by Huchzermeyer (1998b). It is pos-tulated that when the mother drives thehatchlings away before the new broodhatches (see below), a behavioural switch isoperated, inducing the juveniles to avoidlarger crocodiles from then on. When farm-reared juvenile crocodiles are released intothe wild, often many of them are eaten byolder crocodiles. Possibly their lack ofimprinting made them unable to see the dan-ger posed by larger members of the samespecies.

Dispersal of the young

Before the new clutch hatches, in somespecies possibly long before, the juvenilesleave their mother, and there are some indi-cations that, in fact, they are being activelychased away (Hunt, 1977; Hunt andWatanabe, 1982). After leaving their parentsthey may still stay together in pods, evenpods consisting of several clutches (Allstead,1994), or they may disperse individually. Inmany species the different age groupsoccupy different habitats, primarily for age-specific prey requirements, but also keepingthe different sizes apart and thereby mini-mizing cannibalism.

Cannibalism

Cannibalism occurs quite commonly in croc-odiles and may be regarded as a populationregulatory mechanism, allowing more juve-niles to reach adulthood in a depleted adultpopulation (Hutton, 1989). However, highlosses of released juveniles (Rootes andChabreck, 1993) could also be caused by thefact that the released farm-reared animalswere non-imprinted and therefore did nothave the behavioural switch enabling themto avoid larger members of the same species(see above). Where the size classes are segre-gated in the wild, it would be important torelease juveniles into the correct habitat orniches to avoid excessive cannibalism.

The fact that many sporulated coccidiansporocysts often become sequestered in dif-


ferent organs of crocodiles (see p. 187) couldalso be an indication that cannibalism is anormal occurrence in crocodiles in the wildand that this parasite, at least, has adoptedthis as a mechanism for its transmission.

Hunting and feed selection

Crocodiles are nocturnal animals and huntor forage actively during the night.However, they will also take prey during theday if the opportunity should arise. Howmuch their behaviour is affected by diurnalfeeding in captive and farm situations is notknown. However, crocodiles might becomemore interesting for zoo visitors to observe ifthey were shown in a night display.

All crocodiles prefer live, moving food,but they easily adapt to inert feed, such asfresh or boiled mince. Under suitable stress-free conditions they also will take pelletedfeed without any problems. While small fish,tadpoles, frogs and toads were readily recog-nized as prey by Nile crocodile hatchlingspreviously fed with mince, lizards (Agamastellio) were left untouched (Morpurgo et al.,1991).

Social behaviour

Social interactions revolve around sexual,territorial and food competition, and theestablishment of a ranking hierarchy in apopulation. For this the crocodiles useacoustic and visual signalling as well asaggression. The signals vary to some extentfrom species to species, and so does aggres-siveness. In juvenile farmed Nile crocodiles,aggression was found to be linked to feedingand the type of feed, to stocking density andto size variation. Inert feed, low stockingdensity and removal of the larger individu-als were all conducive to low aggression lev-els (Morpurgo et al., 1993b).

Territoriality

Territorial behaviour varies from species tospecies and is most marked in adult croco-

diles during the breeding season. In general,one can say that swamp-inhabiting croco-diles are stricter about establishing territo-ries, while riverine species tend to be moregregarious or tolerant of a higher populationdensity in a breeding area. This may haveimplications for the establishing of breedingcolonies on crocodile farms.

Although apparently severe wounds maybe inflicted during territorial fights betweenmales, the fights are more of a ritualizednature (Plate 4) and much less severe thanthose between females over nesting sites.

Sexual behaviour

The sexual behaviour of crocodiles consistsof courtship displays, mating and defendingthe ‘harem’. Here also the details differ fromspecies to species. Often, while the dominantmale is occupied with one particular female,some of the other females of his ‘harem’ willseek out and copulate with other males. Thisleads to multiple fatherhood of particularclutches and has the benefit of a widerspread of genes.

In large breeding colonies on Nile croco-dile farms one aims to provide distinct terri-tories for several dominant males by thedisposition of islands and other visual barri-ers (Fig. 1.48).

Nesting

Depending on the characteristic habitat ofthe species, crocodiles either build nestmounds from the substrate (vegetation mat-ter or sand) or dig holes in the sand. It isbelieved that the rotting vegetation in thenest mound contributes to the creation of thecorrect incubation temperature, particularlyin dense forest, where the nest mounds can-not be exposed to the sun. In areas whereflooding occurs, crocodiles choose highground for their nesting sites. For this reasonit is important when designing breedingcolonies on Nile crocodile farms to have allthe nesting sites at the same level, to avoidcompetition for the more elevated ones(Fig. 1.49).

54 Chapter 1

Thermoregulation

All crocodiles like to maintain a constantinternal body temperature, dependingsomewhat on their activities and the time ofday. To achieve this they make use of theenvironmental thermogradient, which con-sists of sun (radiation) and shade (air tem-perature), as well as warm surface and cool

deep water. To some extent they can alsomake use of evaporative cooling, although itis unlikely that that is the only purpose ofgaping (Fig. 1.50). During gaping the gularvalve remains closed, whereas it opens dur-ing yawning.

Many species make use of burrows toescape excessive heat (aestivation) or exces-sive cold. This means of maintaining the


Fig. 1.48. Breeding colony on a Nile crocodile farm with visual barriers to allow the establishment ofseveral individual territories.

Fig. 1.49. Nesting sites all on the same level in a breeding colony for farmed Nile crocodiles.

temperature is usually not provided oncrocodile farms. In autumn, Chinese alliga-tors dig particularly elaborate burrows, withone or two openings usually facing south,one or two tunnels, one to three chambers, asleeping platform and a pool. They use theirsnout, fore limbs, body and tail for diggingand moving the soil (Bihui et al., 1990).

We also know the pleasures of thermoreg-ulatory behaviour, lying on a beach andsoaking up the warm sunshine, then divinginto the cold water to cool down, and thenback into the sun again and so on. Crocodileslying in the sun the whole morning are notjust lying there, they are busy thermoregulat-ing. We should always keep in mind that toprevent crocodiles in a captive or farm situa-tion from being able to thermoregulate andachieve their desired temperature can causevery severe stress.

Optimal core temperatures are between28 and 33°C. Temperatures above 35°C arelethal (once the internal temperature rises tothose levels), and several systems cease tofunction below 25°C. However, Americanalligators are known to survive very lowtemperatures. If, during a cold spell, theirwater freezes over, they keep their nostrilsout of the water (ice), while the rest of thebody remains submerged. This behaviour iscalled ‘icing’ (Hagan et al., 1983; Lee et al.,1997) (see also p. 44).

Vocalization

Crocodiles have a large repertoire of soundsthat they use in their various interactions.This begins with the croaking of the hatch-lings in the egg when they are ready to hatch,their frequent croaking to inform their motherand hatch mates of their whereabouts, andthe distress call of a hatchling in danger. Thesame distress call is also used by older juve-nile crocodiles. In some species vocalizationsare added to the mating displays. Growlingand bellowing are used to threaten off attack-ers or competitors. In the Congo Basin swampforests, adult African dwarf crocodiles can beheard calling each other during the night(own unpublished observation).

Britton (2001) has classified the calls ofjuvenile crocodilians as:

● hatching calls;● contact calls;● threat calls;● annoyance calls; ● distress calls.

Their vocal range includes infrasound,which may be audible to other crocodiles inthe water over very long distances. The agi-tation of the water around the thorax of anAmerican alligator producing this sound isshown in the cover photo of Volume 1 of the1990 CSG Proceedings (CSG, 1990).

56 Chapter 1

Fig. 1.50. Gaping Nile crocodile on a farm in South Africa; gaping may facilitate evaporative cooling.

Clinical Examination

Capture and physical restraint

Stress

The capture of wild crocodiles falls outsidethe scope of this book. The subject here is thehandling of captive and farmed crocodiles.All handling and physical restraint causessevere stress and should therefore be kept tothe minimum. If it is ever necessary, the leastviolent methods should be employed.

Bare hands

Hatchlings can be caught by hand directlybehind the head. Slightly larger juveniles arecaught in the same way, but the tail is heldwith the other hand. A dustpan held over thecrocodile to be caught will be accepted asshelter. The hatchling or juvenile will remainimmobile under the shelter and can easily beapprehended by the free hand (Fig. 2.1).

Specimens over 1 m in size are caughtwith a wet towel (Blake, 1993), the animal tobe caught is separated from the others and a

Chapter 2

Examination of Crocodiles and Clinical Procedures


Fig. 2.1. Holding a dustpan over the hatchling to be caught.

wet towel or sack is thrown over its head(Fig. 2.2). The handler then grabs the caudalpart of the head through the towel, whilestraddling the crocodile and holding itsbody between his knees (Fig. 2.3). Withlarger animals a second and third personmay be needed to hold down the body andtail. Another assistant then secures the jawswith insulating tape, taking care not toblock the nostrils. The muscles opening thejaws are relatively weak, so the crocodilewill be unable to break the insulating tape.

Therefore, using rubber bands or string isnot necessary and can cause needless dis-comfort. The animal can be further immobi-lized by tying it to a plank, pole or ladder(Fig. 2.3). In this way it can also be carriedto another location (Fig. 2.4). Bending thebody sideways and fastening the head tothe tail prevents the crocodile from rollingin attempts to free itself. Pressing the eyesinto the orbits and then taping the eyes shutappears to have a further calming effect(Fig. 2.5).

58 Chapter 2

Fig. 2.2. A wet sack is thrown over the head of the roped crocodile.

Fig. 2.3. The crocodile is tied to a ladder, while one assistant sits on its head.

Devices

The above methods are very stressful for theanimal and also dangerous for the handler(s)and it is better to use one of the handlingdevices described below.

● Hatchling and small juveniles (<1 m) areeasily caught with snake tongs (Fig. 2.6)or Pillstrom tongs (McDaniel and Hord,

1990). This allows one to catch them froma distance without having to enter therearing pen and thereby upsetting all theother hatchlings in the pen.

● A catching noose made from strong ropecan be handled more easily if it is passedthrough a strong PVC pipe of adequatediameter and length (Fig. 2.7) (Fletcherand Trammel, 1989).

Examination of Crocodiles and Clinical Procedures 59

Fig. 2.4. The crocodile tied to a ladder can now be moved without danger to the assistants.

Fig. 2.5. Young Nile crocodile with jaws and eyes taped closed. Note that masking tape is not a suitablematerial as it is not water resistant.

● PVC irrigation pipes of various diametersand lengths can be used to restrain andtransport crocodiles after they have beencaught with a noose around the neck anda second noose has been fitted around thebody in front of the hind legs. The frontnoose is used to pull the crocodile into thepipe and the rear noose is then used tohold it back, preventing it from escapingthrough the front of the pipe (Fig. 2.8)(Jones and Hayes-Odum, 1994). Bothropes can be fastened through holes ornotches drilled or cut into the pipe.

● A rigid PVC pipe of about 5–8 cm diame-ter is also useful for chasing away othercrocodiles while working in the pen, e.g.when collecting eggs. Such a pipe pro-duces a loud noise when hitting the

ground next to the crocodile that is to bechased away. This noise is very similar tothe jaw clap used by crocodiles as a warn-ing, and this is probably why it is so effec-tive. Being lighter than a pole of similardimensions, its impact is lighter and thereis less danger of causing pain or injurywhen hitting the crocodile.

Physical examination

Unrestrained crocodiles

An unrestrained crocodile is examined froma distance in its enclosure. Its estimatedlength is noted and its nutritional state isjudged mainly by the relative thickness of its

60 Chapter 2

Fig. 2.6. Snake tongs can be used to catch crocodile hatchlings out of their pen without causingdisturbance.

Fig. 2.7. Catching noose fitted through a PVC pipe.

neck, a severely drawn-in neck being typicalfor an animal in a poor state (Fig. 2.9).Sunken muscles in the supertemporal fossae(see p. 7) also indicate a poor state of nutri-tion (Fig. 2.10).

Nile crocodiles can be recognized individ-ually by the distribution of dark spots onboth sides of the tail, and the same probablyholds true for some of the other crocodilespecies (Swanepoel, 1996) (see p. 74). The taillying either erect or flat in a sideways posi-

tion is supposed to indicate the state ofhealth, the latter position indicating poorhealth (Fig. 2.11), but this is rather doubtful.The animal is then examined for obviousabnormalities, wounds, other skin lesions ordiscoloration and also the state of its eyes.

Restrained animals

Restrained crocodiles can be examined moreclosely. They can also be turned over for a


Fig. 2.8. Crocodile inside a large PVC pipe, held in place by two ropes which are fastened into notchesin the pipe.

Fig. 2.9. A drawn-in neck indicating a poor state of nutrition.

close examination of the belly skin and cloaca.The eyes are difficult to examine, as they areretracted as soon as the lids are touched.However, it is possible to examine the pupiland its response to light, as well as the eyelidsfor any sign of conjunctivitis. A whitish dis-

coloration of the eyelids and the area aroundthe nostrils sometimes occurs in chronicdisease conditions (Fig. 2.12) (see p. 237).

The whiteness of the teeth of hatchlingsand older crocodiles indicates the state ofcalcium nutrition. Calcium-deficient croco-

62 Chapter 2

Fig. 2.11. A tail lying flat on its side, supposedly indicating poor health.

Fig. 2.10. Sunken supertemporal fossae on a captive Nile crocodile, indicating a poor nutritional state (photo Henri Lagasse).

diles have clear, diaphanous, ‘glassy’ teeth(Fig. 2.13), and such hatchlings should betested for the rigidity of their bones by gen-tly trying to bend the upper jaw (‘rubberjaw’) (see pp. 148 and 211).

In hatchlings the mouth can also beopened, by a gentle tap on the nose, to exam-ine the gingivae, the tongue and the twoflaps of the gular valve (see p. 11).

Diagnostic imaging

While wild and farmed crocodiles can rarelybe taken to imaging apparatus, this situationmay be different in the case of captive ani-mals, as many zoos and specialized citypractices have well-equipped clinics and lab-oratories. However, the existing literature onthis subject is still very limited:


Fig. 2.12. A whitish discoloration around the nose may indicate a chronic disease condition.

Fig. 2.13. Diaphanous teeth in a calcium-deficient adult Nile crocodile.

● Radiography: radiographs were taken ofthe digital connective tissue masses of anAmerican alligator at San Diego Zoo(Ensley et al., 1979). No technical detailswere given.

● Ultrasonography: ultrasound was used toevaluate follicle development in adultfemale broad-nosed caimans (Vac et al.,1992; Verdade, 1995). The authors usedthe ultrasonograph Aloka No 210-DX2 at3.5 MHz. In larger animals the lateralapproach was preferred, due to the pres-ence of ventral osteoderms.

● EKG: an electrocardiogram was recordedfrom a 75 cm American alligator.Electrodes applied to the hide did notreceive any deflections. When pins wereinserted into both forelimbs and the lefthind limb, deflections were recorded,none in lead I, but low deflections in leadsII and III. The P waves were indistinctand the R wave in lead II measured2.5 mm. In lead III it was lower andslightly slurred. The T waves were alsopoorly defined in both leads (Blackford,1956).

● Gastric pressure: in chronically cannu-lated Caiman crocodilus, gastric pressurewas recorded with a Beckman Model RDynograph in relation to temperature and

fasting or feeding (Diefenbach, 1975b).However, this method is beyond thescope of normal clinical examination.

Sample collection

Blood

Blood can be obtained from several sites:

● The internal jugular vein runs dorsallywithin the vertebral column and can bestbe punctured at the junction of atlas andaxis. Flexing the head slightly down-wards may help in reaching the vein.Care should be taken not to injure thespinal cord (Olson et al., 1975).

● The caudal veins run ventrally and dor-sally along the vertebral column (ventraland dorsal coccygeal veins). To access theventral vein, the animal is held in dorsalrecumbency. The best place is about one-fifth of the distance from the cloaca to thetip of the tail. The needle should be longenough and inserted pointing craniad atan angle of 45° from vertical. Bending thetail slightly in the opposite direction helpsby opening the space between the longchevron bones covering the haemal canal(Fig. 2.14) (Olson et al., 1975; Gorzula

64 Chapter 2

Fig. 2.14. Taking a blood sample from the ventral tail vein.

et al., 1976; Samour et al., 1984). The dorsalvein can be reached at a similar distancefrom the base of the tail, and at a similarangle because of the dorsal spines (Fig.2.15). This is also the preferred site for alethal injection.

● Cardiac puncture: the heart can be foundby holding the crocodile lying on its backand observing the slight rise and fall ofthe ventral wall that accompanies eachheart beat (Hopping, 1923). In theAmerican alligator, the heart lies in themidline at the level of the 11th and 12throw of scutes, counting back from thebroad band above the forelimbs(Hopping, 1923; Jacobson, 1984). Becauseof differences in the size of scutes, thenumber of rows to be counted may differfrom species to species. It may, therefore,be necessary to ascertain the heart’s exactposition by first examining a dead speci-men of the same species. The animal isheld in dorsal recumbence and the needleis inserted slowly, until blood is encoun-tered.

● Small quantities of blood for smearsmay be obtained by clipping the toenails, the tips of the tail crests (Olsonet al., 1975) or the tip of the tail (Coulsonet al., 1950).

TAKING A BLOOD FILM. A small drop of blood isdeposited at one end of a slide and the edgeof a second slide or cover slip is dipped intoit. The blood is then allowed to spread side-ways right across the edge, before the slideor cover slip is pushed along the originalslide, thus spreading the blood in a thin,even film. The frosted edge or the driedblood film itself can be marked with a pencil(Fig. 2.16). Crocodile red blood cells arenucleated, and these nuclei tend to obscurethe stained blood smear if the blood film istoo thick. Therefore, care should be taken toprepare very thin blood films.

The blood film is allowed to dry in the air.It can be placed face down over two pencilsto keep flies away from the blood. When dry,it is fixed by immersing it briefly in methanoland allowing it to dry again. For the prepara-tion of permanent specimens the blood filmshould be stained with Giemsa stain.

Urine

In the coprodeum the urine is mixed withthe faeces, making it impossible to collectclean urine for clinical examination.However, clean urine can be obtained forresearch purposes by catheterization of theureters.


Fig. 2.15. Bleeding from the dorsal tail vein.

Faeces

Faeces mixed with urine can be obtainedfrom the cloaca of a crocodile held in dorsalrecumbency. They can also be collected fromthe base of a clean container, in which asmall crocodile is kept until it has defecated.For bacteriological sampling of faeces onecan simply take a cloacal swab, which is thenplaced into a sterile container (tube), or atransport medium, and kept refrigerateduntil it can be examined in the laboratory.

Sperm

During the breeding season sperm can beobtained by swabbing the seminal groove ofthe externalized penis. For this the crocodileis immobilized and held in dorsal recum-bency (see p. 70).

Stomach contents

Stomach contents can be sampled by scoop-ing or by washing (Taylor et al., 1978). For

scooping, a piece of rubber-coated metaltube is tied into the opened mouth of thecrocodile. A scoop is made from a stainless-steel or brass rod shaped into a handle, witha loop at a right angle at its end and with arubber finger, or glove, sewn on to the loop.This is lubricated with vegetable oil andpassed through the tube then, with a twist-ing motion, through the basihyal valve intothe oesophagus, and, with another twistingmotion, through the pectoral girdle. When itis in the stomach, it can be felt by externalpalpation and positioned behind a suitablepiece of food to be extracted. Throughoutthis operation the crocodile’s head is raisedat an angle of about 30° to the axis of thebody. Diameters and sizes of tubes andscoops vary with the length of the crocodilesto be sampled. These sizes are shown inTable 2.1.

For stomach washing, a clear PVC tube isinserted through the mouth and oesophagusinto the stomach. The crocodile is then heldwith its head above the level of its stomach

66 Chapter 2

Fig. 2.16. Preparing a thin blood film.

and water is poured through a funnel intothe tube until the abdomen is visibly dis-tended. The abdomen is then squeezed andmassaged gently to mix the water with thestomach contents until the water surges upin the tube. The crocodile then is turned withits head down, the free end of the tube isinserted into the collecting bottle and thetube is withdrawn from the mouth of thecrocodile. Water and food then flow into thebottle. Three to four washes suffice to clearall the food from the stomach (Taylor et al.,1978). The diameters and lengths of tubesrequired for the different sizes of crocodilesare shown in Table 2.1.

Biopsy

Taking samples of diseased tissue from a liveanimal for laboratory examination may helpto establish an accurate diagnosis. The sam-pling by excision, punches, suction needlesor biopsy forceps employs the same tech-niques as are used in other species (Cooper,1994).

Haematology

Blood sampling has been discussed above(see p. 64). The best diluent for leucocyte anderythrocyte counts for reptiles is Shaw’savian solution, which is prepared as follows(Otis, 1974):

Solution ANeutral red 25.0 mgSodium chloride 0.9 mgDistilled water 100.0 ml

Solution BCrystal violet 12.0 mgSodium citrate 3.8 gFormaldehyde 0.4 mlDistilled water 100.0 ml

Each solution is thoroughly mixed andfiltered, then the two are added to each otherand mixed again. The stain is now dividedinto 1.98 ml aliquots and can be kept frozenfor up to 3 months. Heparinized blood(20 �l) is added to one thawed aliquot andmixed gently for several minutes, resultingin a 1:100 dilution before filling the countingchamber. For the morphology of crocodilianleucocytes see Chapter 1 (p. 24).Haematological values have been reportedfrom several different crocodilian speciesand are summarized in Tables 2.2–2.7.

Individual and species values varywidely. Runting leads to the depression ofmany haematological values (Foggin, 1987).White blood cell counts in American alliga-tors infected with Aeromonas hydrophila (seep. 173) increased considerably. In differentialcounts the heterophils increased from 37.4%to 72.9%, while the lymphocytes decreasedfrom 50.6% to 16.0% (Glassman and Bennett,1978; Glassman et al., 1981). Infestation ofAmerican alligators with the leech Placobdellamultilineata (p. 203) resulted in an increase ofeosinophils to 60%. After removal of theleeches, the eosinophil levels returned tonormal within 6 weeks (Glassman andBennett, 1978; Glassman et al., 1979). In Nilecrocodiles stressed by blasting, the total leu-cocyte counts decreased, with a relativeincrease in lymphocytes (Watson, 1990) (seealso p. 280).


Table 2.1. Dimensions (in centimetres) of crocodiles (Crocodylus porosus) and recommended mouthcylinders, scoops and stomach tubes. The dimensions should be similar for other crocodile species.(After Taylor et al., 1978.)

Cylinder Rod TubeCrocodile Scoop

length Diameter Length diameter Length Diameter Diameter Length

28–35 3 2 1 4035–50 4.5 2.5 1 4050–120 5 3 2 40 0.2 1.5 60

120–130 5 3 3 60 0.4 1.5 60130–140 9.5 5 3 60 0.4 2 80140–180 9.5 5 4 80 0.4 2 80

68 Chapter 2

Table 2.2. Mean haematological values of American alligators.

Barnett et al. Mateo et al. Glassman et al.Parameter Unit (1998) (1984) (1981)

Erythrocytes � 106 �l−1 0.67 0.38 0.4Leucocytes � 103 �l−1 5.8 6.4 5.3Haemoglobin g dl−1 9.29 7.2Haematocrit % 24.4 18.6Heterophils % 57.6 54.7 37.4Lymphocytes % 11.1 23.9 50.6Monocytes % 22.3 0.7 3.0Eosinophils % 9.2 10.4 5.5Basophils % 1.2 12.7 3.5

Table 2.3. Mean haematological values of Caiman latirostris (C.l.) and Caiman crocodilus (C.c.).

Parameter Unit C.l.a C.l.b C.c.a

Haematocrit % 22 19.5 27Haemoglobin g dl�1 9.4 12Erythrocytes ×106 dl�1 0.56 0.69Leucocytes ×103 dl�1 22.7 16.4Lymphocytes % 65 60Azurophils (?) % 8 9Monocytes % 5 5Basophils % 1 0Eosinophils % 19 21Heterophils % 3 5

aTroiano et al. (1996a); b Tourn et al. (1994).

Table 2.4. Mean haematological values of Crocodylus niloticus (C.n.), C. rhombifer (C.r.) and C. moreletii (C.m.).

Parameter Unit C.n.a C.n.b C.r.c C.m.d C.n.e C.r.f

Haematocrit % 24 23–26 24.5 22 21.7Haemoglobin g dl�1 7.8 8.1–8.9 7.75 7.4 7.5Erythrocytes � 106 �l�1 0.60 2.4–2.9Leucocytes � 103 �l�1 4.0Neutrophils % 6 50Lymphocytes % 73 21Monocytes % 1 5Eosinophils % 2 2Basophils % 20?g 22

a Makinde and Alemu (1991); b Thurman (1990); c Carmena-Suero et al. (1979); d Sigler (1991); e Foggin(1987); f Moliner et al. (2000a).g Apparently left out of the paper.


Table 2.5. Mean haematological values of Crocodylus porosus (C.p.) and Tomistoma schlegelii (T.s.).

Parameter Unit C.p.a C.p.b T.s.c

Haematocrit % 19.2 24.8 15.2Haemoglobin g dl�1 4.9 7.1Erythrocytes � 106 �l�1 0.34Leucocytes � 103 �l�1 4.35Heterophils % 64.9Lymphocytes % 24.1Eosinophils % 8.5Monocytes % 3.9Basophils % 0

a Wells et al. (1991); b Grigg and Cairncross (1980); c Siruntawineti and Ratanakorn (1994).

Table 2.6. Ranges of haematological values from Crocodylus porosus yearlings (Millan et al., 1997a)and hatchlings (Turton et al., 1997).

Parameter Unit Yearlings Hatchlings

Haematocrit % 17–41Haemoglobin g dl�1 4.7–12.2Erythrocytes � 106 �l�1 0.6–1.3Leucocytes � 103 �l�1 6.4–25.7 5.33Heterophils � 103 �l�1 0.8–7.4 3.08Lymphocytes � 103 �l�1 4.5–21.6 1.69Monocytes � 103 �l�1 0.0–1.2 0.05Eosinophils � 103 �l�1 0.0–0.7 0.35Basophils � 103 �l�1 0.0–0.4 0.15Thrombocytesa � 103 �l�1 4–71

a The diagnostic value of thrombocyte counts is still undetermined. In percentage counts they tend toupset the other values.

Table 2.7. Ranges of haematological values from 2–4-year-old captive Australian crocodiles, fourCrocodylus porosus and four Crocodylus johnsoni (Canfield, 1985).

Parameter Unit C. porosus C. johnsoni

Haematocrit % 0.20–0.22 0.18–0.21Total plasma protein g l�1 48–70 33–69Erythrocytes � 1012 l�1 0.86–0.98 0.71–0.93Haemoglobin g l�1 62–77 57–75Total leucocytes � 109 l�1 39.6–44.2 26.4–48.8Thrombocytes % 72.2–95 76.5–87.7Lymphocytes % 0.6–9 4–8.5Monocytes % 0–3.0 2.2–11Type I granulocytes % 1.6–14 3–8.6Type II granulocytes % 0–0.8 0–0.5Type III granulocytes % 0–4.8 0.8–2.8Unidentified % 0.2–0.8 0.4–0.8

Sexing

Crocodiles do not show distinctive sexualbimorphism. American alligators have a dif-fering pattern of scutes around the vent,with three rows of smaller scutes around thevent in males and four rows in females(Viosca, 1939).

However, the penis and clitoris of croco-diles of all species and ages differ sufficientlyin size and shape for an experienced opera-tor to sex even hatchlings with a large mea-sure of confidence (Brazaitis, 1969; Whitaker,1973; Webb et al., 1984). In female hatchlings,the cliteropenis is small with a sharp extrem-ity, while in the male it is large and tubularwith a more bulbous extremity (Webb et al.,1984).

For the examination of hatchlings, finecurved forceps or haemostats are insertedinto the cloaca and spread, thus exposing thecliteropenis which is attached to the cranio-ventral wall of the cloaca (Webb et al., 1984).In large specimens the index finger isinserted into the cloaca, with the tip of thefinger hooked cranially. It is then possible tofeel the rigid male organ and to extrude it(Brazaitis, 1969) (see Fig. 1.33).

Cloacal examination

As in the case of rectal examination of mam-mals, larger crocodiles can be examined viathe cloaca by inserting a finger into the lowerrectum. The animal is held in dorsal recum-bency and pressure is applied to theabdomen to shift the organs to be examinedtowards the midline. In this way intestinalloops and ovarian follicles, as well as hard-and soft-shelled eggs in the uterus andvagina, could be identified by palpation inJohnston’s crocodiles (Limpus, 1984).

Immobilization

When larger crocodiles are to be handled,either for examination and other interven-tions, or to be moved, the safety of staff hasto be considered just as much as the safety ofthe animal. Being caught and handled is

very stressful for all crocodiles, and thisstress can have very deleterious conse-quences (see p. 278). While there are manyinstances where crocodiles have been han-dled and transported safely without chemi-cal immobilization, there are also many caseswhere the animals have died a few monthslater from a stress-associated disease.

If used at the correct dosage rates andhandled properly by competent persons,preferably by veterinarians, immobilizingagents are very safe. The only major cause ofmortality encountered in immobilized croco-diles is drowning, which occurs if they arereleased into water before they have fullyrecovered from immobilization or if theyhave been darted in the water (Loveridge,1979). In this context the recommendation byFlamand et al. (1992) that crocodiles shouldbe allowed access to water ‘once the immo-bilization is complete’ is misleading anddangerous. Rather, it should read, ‘oncerecovery from immobilization is complete’(Brisbin, 1966; Loveridge and Blake, 1972;Messel and Stephens, 1980). It should also benoted that the dosages found to be safe andeffective in one species may not be so inanother (McClure, 1997), for instance, theeffective dose of succinylcholine HCl inCrocodylus porosus was ten times thatrequired for Crocodylus johnsoni (Messel andStephens, 1980). Exploratory trials shouldalways be undertaken and effective dosesestablished before any of these drugs is usedon a species for the first time.

These drugs are either given by handsyringe, pole syringe or dart (Flamand et al.,1992). If a hand syringe is to be used, the ani-mal must be restrained beforehand. The pre-ferred sites of injection are the upper fore-and hind limbs. The advantages of usingthese sites are that there are no fat depositsbetween the limb muscles, which could slowdown the resorption of the drug, and that alarger quantity can be injected slowly, thuspreventing the liquid from flowing out afterwithdrawal of the needle (Flamand et al.,1992).

A pole syringe is safe for the handler, butthe injection takes place very rapidly, with therisk of reflux through the puncture wound.The preferred injection site is the side of the

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tail, close to its base. If the drug is injectedinto the fat deposits between the superficialand deep muscles (see p. 29), its resorptionwill be slow (Flamand et al., 1992).

The same site is used for darting, and thesame disadvantages apply. In addition thereis great danger if the dart should strike anosteoderm obliquely and ricochet off(Flamand et al., 1992). The neck has also beenused as a darting site in cases where thedarts tended to bounce off the tail (Klide andKlein, 1973).

Several drugs, mainly muscle relaxants,have been used for the immobilization ofcrocodiles. Those that have been reported areshown with their dosage ranges in Tables 2.8and 2.9. In several species of Crocodylus,gallamine (Flaxedil®) has been found to beeffective. Its action can be reversed rapidly bythe injection of the antidote, neostigmine.While the immobilized crocodiles recoverwithout the help of the antidote, it is essentialto have it at hand whenever Flaxedil® isused, for the treatment of accidentallyinjected people (e.g. by a ricocheting dart!). Itis also essential to use it when immobilizedcrocodiles cannot be prevented from enteringthe water before full recovery. In fact, a largenumber of transferred Nile crocodiles diedon a crocodile farm in South Africa in 1998,when the drugged crocodiles were releasedinto a pen with water, without first giving

them the antidote. The animals entered thewater before having fully recovered and werefound drowned the next morning. Many sim-ilar incidents have occurred.

Recently, exploratory work has beenundertaken on the combination of xylazineand ketamine (Seashole et al., 2000). The trialanimals were given xylazine 1.5 mg kg�1

body mass and, 20 min later, ketamine20 mg kg�1 body mass, both injected into thebrachial muscles. Immobilization was pro-found in Crocodylus moreletii and Palaeosuchuspalpebrosus, moderate in C. crocodilus, whilethere was no effect in Palaeosuchus trigonatus.

The recommended doses for Flaxedil®

and neostigmine are given in Table 2.10.However, at the time of writing, Flaxedil®

has been taken off the market. While it hasbecome available again locally in SouthAfrica, this has opened the quest worldwidefor other efficient and safe immobilizingagents for crocodiles. The names of theimmobilizing drugs and their synonyms areshown in Table 2.11.

The following precautions for crocodilehandlers have been suggested by Blake(1993):

● Do not take chances when working withcrocodiles, even small ones.

● Never work alone with crocodiles.● Never use damaged or worn equipment.


Table 2.8. Immobilizing agents that have been tried in Alligatorinae (dosages in mg kg�1 body mass).

Alligator mississippiensis Caiman crocodilus

Agent Dose Effect Dose Effect Reference

Tricaine 88–99 9 h 1110 – 2

Pentobarbitol 7.7–8.8 2–3 h 18.8 – 2

Etorphine 0.4 + 2.5–20a + 30.5 – 4

Phenylcyclidine 11–22 6–7 h 1Succinylcholine 3.0–5.0 7–9 h 1

0.33 35 min 2Diazepam + 0.22–0.62 3 h 5succinylcholine 0.14–0.37

+ Effective.– Not effective.a Hatchlings.1, Brisbin (1966); 2, Klide and Klein (1973); 3, Wallach and Hoessle (1970); 4, Hinsch and Gandal(1969); 5, Spiegel et al. (1984).

72C

hapter 2

Table 2.9. Immobilizing agents that have been tried in Crocodylinae (dosages in mg kg�1 body mass).

Crocodylus acutus Crocodylus palustris Crocodylus porosus Crocodylus johnsoni Crocodylus niloticus

Agent Dose Effect Dose Effect Dose Effect Dose Effect Dose Effect References

Succinylcholine 9.2 2 h 6 1 h 13–17 + 0.8–3.6 + 2

Tricaine * − * − 2Phenylcyclidine * − * − 2Gallamine * + * + 3

0.5–0.6 + 40.64–4.0 + 5

1–1.25 + 6Zoletil® 5.0 + 7Suxathonium * − * − 2

* No dose stated.+ Effective.− Not effective.1, Klide and Klein (1973); 2, Messels and Stephens (1980); 3, Whitaker and Andrews (1989) (quoted by McClure, 1997); 4, Bonath et al. (1990); 5, Loveridgeand Blake (1972); 6, Woodford (1972); 7, Haagner and Reynolds (1992).

● Do not leave drugged crocodiles un-attended.

● Do not forget to remove the tape from thejaws before administering the antidote.

● Do not allow large, noisy audiences at acrocodile capture exercise.

● Do not allow the nostrils of the crocodileto be occluded while it is tied up ordrugged – it will suffocate.

Pre-release screening

There is concern about the introduction orspread of diseases where farm-reared, juvenile


Table 2.10. Recommended doses for Flaxedil® and neostigmine in Nile crocodiles (Loveridge and Blake,1972; Flamand et al., 1992).

Weight (kg)

LoveridgeFlamand and Blake

Length (m) et al. (1992) (1972) Flaxedil®a (ml) Neostigmineb (ml)

0.91 2 2 0.10 0.051.07 3 3 0.15 0.051.22 5 5 0.25 0.101.37 8 8 0.40 0.201.52 12 12 0.60 0.301.68 16 16 0.80 0.401.83 21 21 1.50 0.501.98 26 26 1.70 0.602.13 35 35 2.00 0.802.29 55 42 2.50 1.002.44 65 61 3.00 1.002.59 77 77 3.50 1.002.74 95 88 4.00 1.002.90 125 99 4.50 1.003.05 135 108 5.00 1.003.20 165 135 5.50 1.003.35 185 155 6.00 1.003.51 215 179 6.50 1.003.66 230 203 7.00 1.003.81 260 239 7.50 1.003.96 280 297 8.00 2.004.12 295 338 8.50 2.004.27 320 376 9.00 2.004.42 340 415 9.00 2.004.57 350 451 9.50 2.004.72 492 492 10.00 2.004.88 532 532 10.00 2.00

a Gallamine triethiodide 40 mg ml�1.b Neostigmine methylsulphate 2.5 mg ml�1.

Table 2.11. Names and synonyms of immobilizingdrugs as used in the cited literature.

Technical Commercial

Diazepam Valium®

Etorphine M99®

Gallamine triethiodide Flaxedil®

Phenylcyclidine hydrochloride Sernylan®

Sodium pentobarbital Cap-Chur Barb®

Succinylcholine chloride Anectine®, Scoline®, Sucostrin®

Suxathonium bromide Brevidil E®

Tricaine methanosulphonate MS222®

Zolazepam hydrochloride +tiletamine hydrochloride (1:1) Zoletil®

crocodiles are to be released back into thewild. However, habitats already occupied bywild crocodiles usually already harbour allthe crocodile-specific pathogens of thatspecies. One should also bear in mind thatcrocodiles are fortunate in being free fromprimary pathogens: none of the presentlyknown crocodile-specific contagious agentscan be classified as primary pathogens, asthey all need triggering factors to precipitateoutbreaks of disease. In fact, the presence ofthese pathogens at a low level in a wild pop-ulation most likely ensures a state of immu-nity in the population. For this reason it ispossibly not a good idea to release ‘clean’juveniles into a new area, not inhabited bycrocodiles, as the later introduction of apathogen might have more serious conse-quences there.

In any case, it is not possible to recom-mend a programme of rigorous serologicalscreening, as there are no serological testsavailable for any of the crocodile-specificinfections yet, except chlamydiosis. The onlyrecommendation presently possible is tocheck the condition of the animals to bereleased, and only release healthy looking,well-nourished individuals, originating froma farm where no undue mortality hasoccurred in the preceding 12 months.

The presently known crocodile-specificpathogens are:

● crocodile poxvirus (p. 158);● caiman poxvirus (p. 157);● adenovirus (p. 160);● Mycoplasma spp. (p. 167);● Chlamydia sp. (p. 167);● coccidia (as yet unnamed) (p. 183).

The only other pathogen that one shouldpossibly consider is Mycobacterium avium(p. 170), which could be perpetuated in awild population through cannibalism.However, this pathogen does occur in wildbirds and has recently been involved inmass mortality in flamingos in Kenya (Kocket al., 1999). There may perhaps be a differ-ence in pathogenicity for crocodiles betweenM. avium strains originating from pigs andthose from birds. The mycobacteria may alsoneed stress or other triggering factors tocause disease.

Tagging and identification

Natural markings

For many purposes it is useful to be able torecognize or mark individual animals. Nilecrocodiles have dark spots on the sides oftheir tail which vary individually. Swanepoel(1996) used the markings on the last nine tailsegments with horizontal scutes that precedethe segment with the first single verticalscute (Fig. 2.17) on both sides of the tail (Rand L). By numbering the segments 1–9 fromcaudal to cranial, and by recording the seg-ments with markings, doubling the numberfor double markings, a code could be estab-lished. This could be further refined by dis-tinguishing between black and greymarkings, placing the code numbers for greyspots in brackets, and by adding a sketch ofthe side view to the record. Using nine rowsof scales on either side of the tail of almost300 crocodiles, Swanepoel (1996) found anaccuracy of 95%. The degree of accuracycould be increased by using ten or even 12rows. This method is applicable to wild pop-ulations as well as to farmed animals, e.g. ina breeding colony, and could also be appliedto other species of crocodiles.

Clipping

Several ways of marking crocodilians havebeen used. Toe clipping limits the number ofindividuals that can be marked, and the acci-dental amputation of a toe as a result of bit-ing or fighting is quite common (Dixon andYanowsky, 1993). Clipping the dorsal crest ofthe tail is difficult, if not impossible in hatch-lings. As the marked individuals grow, themark becomes smaller in relation to the over-all size of the animal (Dixon and Yanowsky,1993).

Tags

Web-tagging has been used widely, but tagsare frequently lost, and limbs are also lostoccasionally – leading to the loss of a record(Dixon and Yanowsky, 1993). Tags applied toone of the dorsal crests in adult crocodiliansare often used. However, they occasionally

74 Chapter 2

get lost, and the numbers are not easy toread (Dixon and Yanowsky, 1993). On SouthAfrican crocodile farms the colour of thesetags is used to indicate the sex of the animal.None of these markings is acceptable forzoos and other tourist exhibits.

Microchips

Transponder chips or microchips have beenused successfully in broad-snouted caimans(Dixon and Yanowsky, 1993). The chips wereinserted into the left side of the tail base, andit was found that the microchips did notmigrate from the site of implantation, norwas there any scarring of the skin. A seriousdisadvantage of this method is the fact thatthe reading device only works from a maxi-mum distance of about 20 cm, forcing theoperator to come dangerously near to theanimal to read it, or to capture and restrainthe animal first. The presence of the chip inthe tail meat may also affect its acceptabilityin certain countries.

Since 1997, the European community hasrequired all crocodilians to be microchipped(as are all Annex A listed vertebrates) if usedfor commercial purposes such as sale, dis-play, breeding, etc. (Redrobe et al., 1999). TheBritish Veterinary Zoological Society advises

injection of the microchip in crocodiliansdorsally into the neck, anterior to the nuchalcluster (Redrobe et al., 1999).

Post-mortem Examination

Storage and transport of the carcass

Dead crocodiles are usually found in a verywarm environment and, at that temperature,tend to decompose very rapidly. Therefore, itis important to collect the dead animal assoon after death as possible and cool it downto about 4–10°C. Larger bodies cool morequickly if immersed in ice water. Freezing acarcass should be avoided as the formationof ice crystals destroys the cells and rendersthe carcass unsuitable for histopathologicalexamination. However, when refrigerated,psychrophilic bacteria continue to multiplyand may overgrow those pathogens poten-tially involved in causing the mortality. Thusfreezing a few specimens purely to maintainthe microbial flora for examination in thelaboratory might be considered.

In any case, the carcass should be taken toa diagnostic laboratory as soon as possible –remember that laboratory procedures alsocause delays and that the usefulness of a


Fig. 2.17. Spots on the tail of a Nile crocodile used for identification (after Swanepoel, 1996). Readingfrom caudal to cranial, this crocodile would have the code R113346688.

diagnosis decreases with the time lapsedafter the death of the animal. The laboratoryshould be alerted and the carcass trans-ported to the laboratory, size permitting, inan insulated container and on ice. The cost ofan examination and investigation is usuallysmall compared with the value of the ani-mals lost. If there is a high mortality, severalcarcasses should be submitted, but a wholebagful of dead hatchlings may only tire thepathologist without contributing to the even-tual diagnosis.

At the laboratory the pathologist shouldbe given as complete a history as possible,including the age and number of animalsaffected, and be provided with contact num-bers (phone, fax and e-mail) and address.Most laboratories have forms for this pur-pose.

Humane killing

Live specimens that have been submitted forpost-mortem examination will have to beput down humanely. Larger crocodiles(>60 cm) are killed easily with a captive boltstunning gun, as used for the slaughter ofpigs or cattle. This destroys the brain of thecrocodile completely, rendering the animal

immediately ready for further procedures.The spot to aim at is in the middle, betweenthe orbits and the supertemporal fossae (Fig.2.18). Small specimens can be given a lethalinjection of a barbiturate either intraperi-toneally (see p. 89), into the heart, the dorsalneck vein (see p. 64) or into the dorsal orventral tail vein (Figs 2.14 and 2.15). Cattoand Amato (1994b) used intracerebral injec-tions of ethyl alcohol, but the route of injec-tion and dosage rate were not given, nor didthe authors comment on the effectiveness ofthis method.

Examination of head and skin

Before opening the carcass, the head andskin are examined. The examination of thehead includes the eyes (eyelids, nictitatingmembrane, cornea), the nostrils and themouth (gingivae, teeth, tongue and gularvalve). The skin of the whole body ischecked for injuries, ulcers, swellings, abra-sions (under the chin and the soles of thefeet, see p. 242), pox (pp. 157 and 158) orpox-like lesions (p. 236) and any other abnor-malities. Then the total length is measured,recorded and, if possible, the animal isweighed.

76 Chapter 2

Fig. 2.18. Head of a farmed Nile crocodile killed with a captive bolt stunning gun. The correct spot to aimat is in the centre, between the orbits and the supertemporal fossae.

Opening the carcass

The animal is placed on the table with itsbelly up and the skin is incised across thelower neck, just cranial to the row of largescales between the fore limbs (Fig. 2.19).From there the skin and body wall are cutalong both sides of the body, first throughthe coracoid and then through the cartilagi-nous part of the ribs. The coracoids are verytough, and in adult animals it may be easierto cut through their cartilaginous junction, inthe midline, before going to the ribs on eitherside. In larger specimens the skin is taken offprior to the removal of the ventral body wall(Fig. 2.20).

The lateral cuts are continued beyond theribs through the abdominal wall, taking carenot to cut into any of the abdominal organs,particularly into the stomach which isattached to the left body wall. The pubicbone protrudes cranially from the pelvic girdle. In hatchlings it can be removed with atransverse cut, in older specimens it becomesextremely tough and can be left in place andthe transverse cut made just cranially to it.The skin with the ventral body wall is nowlifted and all adhesions are carefully dis-sected until the whole piece can be lifted off,exposing the thoracic and some of theabdominal organs (Fig. 2.21).

Neck, pharynx and oral cavity

The lateral cuts are continued in a cranialdirection to the maxillary joints, and thenmedially of the mandibles to the tip of thetongue. This flap of skin with the tongue islifted off, exposing the hard and soft palate,with the dorsal flap of the gular valve, theinternal nares, the ventral opening of theEustachian tubes and the larynx (Plate 5) (seep. 11). Along both sides of the neck it may bepossible to see the chains of thymus glands(p. 21). However, they are no longer presentin emaciated animals.

Examination of the thoracic viscera

The thoracic part of the trachea is inspectedfirst. Then the various thoracic endocrineglands are located, which may be hidden infat deposits: the multiple lobes of the thymusgland, the thyroid(s) and the parathyroids(see p. 22) (see Plate 3).

The pericardial sac is opened, the heart istaken out, and the auricles separated fromthe ventricles. Note that crocodiles do nothave fat in the coronary groove. The twolungs are then loosened from their attach-ments to the body wall and the prehepatic


Fig. 2.19. Line of incision across the lower neck and along the sides.

transverse membrane. These attachments arenormal, but they vary in extent from speciesto species. The lungs can then be taken outfor closer examination. This leaves theoesophagus, which is situated in the medi-astinum and is attached dorsally to the bodywall.

Examination of the abdominal viscera

Before fully exposing the abdominal viscerait may be necessary to carefully remove theventral diaphragmatic muscle, which runsfrom the cranial transversal membrane to thepubic bone. Its removal exposes the two

78 Chapter 2

Fig. 2.20. In larger specimens the ventral skin is taken off before removal of the ventral body wall.

Fig. 2.21. Opened carcass with the ventral body wall deflected caudally.

lobes of the liver, the stomach on the leftside, the fat body on the right side and a fewintestinal loops (Fig. 2.22).

The duodenum is severed where itemerges from the pyloric antrum of thestomach, and the whole intestine is gentlypulled loose from the mesentery and liftedout to the left side of the body. The fat bodyis then lifted out, giving access to the spleendorsally in the mesentery (Fig. 2.23). The sizeof the fat body is a better indicator of theactual state of nutrition than any subperi-toneal fat that may be present, as such fat ispoorly metabolized, while the fat body is avery active fat storage organ, supplying thedaily needs, particularly of the heart (seep. 28). Cranially the spleen is surrounded bythe caudal pancreas, the cranial pancreas isfound between the duodenal loops.

The spleen is covered by a very strongfibrous membrane, which normally grows asthe spleen itself grows but does not stretchwhen the spleen hypertrophies in responseto an infection. In such cases, the spleen tis-sue buds through the capsule. Such a bud-ding spleen is a clear sign of hypertrophysplenomegaly, indicating infection and septi-caemia (Fig. 1.46) (Huchzermeyer, 1994).

The stomach is severed from its attachment

to the left body wall and then lifted out withparts of the oesophagus. It is then opened andinspected for normal contents, foreign bodies(p. 254), parasites (pp. 192 and 194) and ulcers(p. 251). Next, the two lobes of the liver,together with the gall bladder, can be removedand examined. The intestine is then cut off atits most caudal accessible end. It is opened forcloser examination, at least in parts. It is now possible to attempt a cut through thepubic bone towards the cloaca and excise thecloaca.

This leaves the gonads partially coveringthe adrenals, the Muellerian ducts or theoviducts and finally the kidneys, attached toeither side of the backbone in the caudalrecesses of the abdominal cavity.

Tail, legs and feet

The tail is cut across, not far from its base, toexpose the fat deposits between the superfi-cial and deep muscles (p. 10). The legs andthe joints are examined for any swellingsand, if necessary, the joints are opened toexamine them for arthritis (p. 273) and gout(pp. 230 and 264) (Fig. 2.24). Any otherswellings are also incised and examined.


Fig. 2.22. Abdominal organs exposed after removal of the diaphragmatic muscle: a, liver; b, stomach; c,fat body; d, duodenal loop; e, loops of jejunum and ileum.

Brain and spinal cord

In smaller specimens (<1.5 m) the skull canbe split longitudinally in the midline fromthe ventral aspect (the head upside down)with the help of a strong knife and a hammer(Fig. 2.25). This gives access to the nasal cavi-

ties and both halves of the brain (Fig. 2.26).For mature specimens a saw has to be usedto open the skull.

Sections of the vertebral column can alsobe opened longitudinally with a knife andhammer, to expose the spinal cord. I havenever been able to pull the spinal cord as is

80 Chapter 2

Fig. 2.23. The spleen in situ dorsally in the mesentery, cranially surrounded by the caudal pancreas.

Fig. 2.24. Opened carpal joint.


Fig. 2.25. Splitting the skull of a juvenile Nile crocodile from the ventral aspect with a strong knife and ahammer.

Fig. 2.26. The split skull, exposing the nasal passages, the halves of the brain and the pituitary gland (p. 21) at the base of the brain (arrow).

done with slaughtered dwarf crocodiles inthe Congo Republic. There, the butcherladies at the markets cut dorsally throughthe neck down to the vertebral column, bendthe head down and grip the spinal cordbetween two fingers before severing it cra-nially. Then, while gently tapping the backwith the blunt side of the machete, theyslowly pull out the entire spinal cord (Fig.2.27). They claim that the meat is inedible ifthe ‘black worm’ is left inside.

Sample collection

Blood

If the animal is still alive, blood samples canbe collected as explained above (p. 64).During post-mortem examination, blood canbe collected from the auricles of the heart.Note, though, that the cells deteriorate afterdeath, and that only the freshest carcasseswill have blood that is still suitable for someof the laboratory tests. The method for thepreparation of thin blood smears has beenexplained above (p. 65). The blood smearsare air dried and then fixed by immersingthem in methanol, or by letting methanol runover them. They are air dried again, and can

then be wrapped in tissue paper or placed ina container for dispatch to a laboratory.

Bacteriology

Samples for the isolation of bacteria shouldbe taken with sterile instruments before theorgans have been contaminated by handling,and should be placed in sterile containers. Ifthey cannot be delivered to the laboratoryimmediately, they should preferably befrozen to prevent any further growth by con-taminating bacteria. If sterilized instrumentsare not available, scissors and forceps can beimmersed in a 10% formalin solution, suchas is used for the preservation of histopathol-ogy specimens (see below).

In the case of a generalized infection, allinternal organs will contain the bacteria, ascrocodiles have no lymph nodes and aretherefore unable to localize an infection in aparticular organ system. Therefore it isunnecessary to collect bacteriological speci-mens from all the organs, normally the liversuffices. In addition, one should sample spe-cific lesions or organs that are visibly dis-eased. In cases of enteritis, either a piece ofunopened intestine is collected or a smallquantity of intestinal contents. The organ

82 Chapter 2

Fig. 2.27. Pulling the spinal cord from a slaughtered wild-caught African dwarf crocodile at a market inBrazzaville.

samples should be taken in the form of smallcubes, with a side length of 5–10 mm, andplaced in separate containers.

Viral isolation

If a viral infection is suspected, first discusswith staff at the virology laboratory whethersuch a virus can be isolated at all (see p. 157).An alternative may be to demonstrate virusparticles in fluids (intestinal contents) bynegative staining and transmission electronmicroscopy (TEM) (Huchzermeyer et al.,1994b). Virus particles can also be detectedby TEM in tissues that have been fixed inglutaraldehyde solution. The details wouldhave to be discussed with the electron micro-scopist at the laboratory. Some viruses causethe formation of typical inclusion bodies,which are detected by histopathologicalexamination (see below).

Histopathology

For histopathological examination, smallcubes of tissue (5–10 mm side length) shouldbe placed in 10% formalin solution. Formalinis normally sold as a 40% formaldehydesolution, which is regarded as 100% formalin(saturated solution). One part of this, dilutedin nine parts of water gives the 10% formalinsolution that is required. Laboratories preferto dilute the formalin in buffered distilledwater or in buffered saline solution.However, in an emergency, sufficiently goodresults can be obtained by using tap water asdiluent. Note that the formalin becomes fur-ther diluted by the water in the tissues.Therefore, it is advisible to immerse the tis-sue cubes in about ten times more formalinsolution than the actual mass of the tissues tobe preserved (e.g. 10 g of tissues in 100 ml ofsolution). Formalin penetrates the tissuesonly very slowly, and this causes large piecesto rot inside while only the outer layers arefixed by the preservative, particularly underwarm or hot climatic conditions. This is themain reason why small cubes of tissueshould be used.

It is wise to collect tissues from all organsand from all the different lesions encoun-tered, but tissues from different animals

should be kept in separate containers. Thehistopathologist can then choose whichorgans to examine in each particular case. Bylimiting the number of organs collected, theability of the pathologist to establish the cor-rect diagnosis is also limited.

Parasites

Stomach and intestine are cut open in theirwhole length and placed in a screw-cap jar,which is filled to one half with water. Thecap is tightened and the jar shaken vigorously. Then the contents are pouredthrough a strainer (coffee strainer) and thecontents of the strainer washed out into adark plastic tray, in which the parasites canbe found. Intestines from very large croco-diles may have to be processed in smallersections.

Parasites are best preserved in 70% ethylalcohol. Roundworms tend to roll up intotight balls when placed in alcohol. They arethen difficult to examine later under themicroscope. It is better to place them in a testtube with saline solution, or even tap water,which is then heated over a flame to almostboiling. At that moment the parasitestretches out, and it remains stretched whenplaced in alcohol.

Collecting specimens in the field

Required material

Field work often takes place far away fromthe nearest laboratory, under difficult cli-matic conditions and usually also withsevere restrictions regarding space andweight allowed for equipment and materials.The minimal requirements comprise the fol-lowing instruments:

● a knife;● scissors (both good quality and sharp);● forceps and razor blades;● a number of very small (2–5 ml) and

small (20–30 ml) plastic screw-cap jars;● a few larger (±200 ml) screw-cap jars;● one 500 ml screw-cap jar;● a few 10 ml plastic syringes with needles;● two test tubes;


● glass slides and cover slips;● a coffee strainer;● a small cutting plank;● a plastic tray;● a plastic measuring cylinder (±250 ml);● 500 ml of formalin (40% formaldehyde

solution – see above, p. 83), 500 ml of 70%ethanol and 500 ml of methanol, all threein sturdy plastic cool drink bottles;

● a few similar spare bottles for the solu-tions to be made up, and;

● an insulated box for the transport offrozen specimens.

Also required are masking tape, a roll of toi-let paper, a pencil, paper and a marking pen.

Bacteriology and blood samples

If there is no access to a freezer, bacteriologi-cal and serum samples cannot be taken. If afreezer is available, the bacteriological sam-ples are taken as explained on p. 82, but inthe smallest possible containers, marked onthe outside with the specimen number andplaced in the freezer as soon as possible.

For serum samples, the blood is collectedfrom the auricles, one drop of blood is placedon a glass slide for a blood smear (see p. 65)and the rest squirted gently into a 20 ml jar,marked on the outside and placed on its sidein the shade, but not refrigerated, to allow theblood to coagulate in a slope (Fig. 2.28). Oncethe blood has coagulated, the jar is stood

upright again to allow the serum to collect atthe bottom. After a few hours, the serum canbe drawn off with a syringe and needle,squirted into a very small jar, marked on theoutside again and placed in the freezer. Theair-dried blood smears are marked with apencil, either on the frosted end or on thethicker part of the smear. After fixing anddrying they can be rolled into a short lengthof toilet paper (Fig. 2.29) and secured tightlywith masking tape. Several blood smearsrolled up tightly in toilet paper are fairly wellprotected from breakage.

Histopathology samples

A 1:10 formalin solution is prepared witheither tap or other drinking-quality water,using the measuring cylinder, and pouredinto one of the spare bottles. One of the200 ml jars is roughly half-filled from thisstock for the initial fixing of the histopathol-ogy samples, which are cut as small as possi-ble and left in this jar for 24–48 h withoutrefrigeration. The specimen number is writ-ten, with a pencil, on a small square of paper,and also placed into the jar. After 1 or 2 daysof fixing, the contents of the jar are pouredthrough the coffee strainer into a second jar.The fixed organ pieces are then placed intothe plastic tray and are trimmed with a razorblade on the small cutting plank to the mini-mum size required for embedding (usually

84 Chapter 2

Fig. 2.28. Jars lying on their side to allow the blood to coagulate in a slope.

3 mm thick pieces, about 5 � 10 mm wideand long, for details consult a pathologist).These pieces, together with the square ofpaper, now fit into one of the small jars, inwhich they are covered with some recycledformalin. They are now ready for storing atambient temperature and eventual transportback to the laboratory. Do not refrigeratesamples in formalin! If necessary, the remain-der of the formalin can be used a secondtime for fixing another set of specimens.

Parasites

Stomach parasites can be picked directly outof the opened stomach, or the stomach con-tents can be poured out into the plastic tray inwhich the parasites become more visible. Theintestine is cut open along its whole lengthand placed into the 500 ml jar. This is roughlyhalf-filled with water, the cap is closed andthe jar is shaken vigorously. The intestine isthen taken out and the remaining contents ofthe jar poured through the coffee strainer. Thecontents of the strainer are then washed witha small amount of water into the tray, wherethe parasites can be collected. Fixation of theparasites with heat and in alcohol has beenexplained above (p. 83). For storing the para-sites, use the smallest possible container andplace a square of paper with the pencilledspecimen number in the jar with the sample.Store at ambient temperature. Note that

writing in pencil on paper is not washed offby immersion in the liquid, while glued-onlabels or writing with a marker pen easilycome off if there is an accidental leak.

Pentastomes (p. 205) are collected bydeeply incising the lungs. If the parasites arestill alive, they will come out into the air andcan then be picked up easily. For a thoroughsearch, the lungs should be cut into smallpieces, washed in the 500 ml jar and the con-tents then examined in the tray.

These are the absolute minimal require-ments for the collection of standard speci-mens, tried on several Congo expeditions. Ifyou can carry more, do so by all means. Ifthere are any specific requirements, e.g. sam-ples for toxicological investigations, youshould ask the laboratory for detailedinstructions.

Age determination

Crocodiles do not have any outwardly visi-ble markers that can be used to determinetheir age. Their growth also varies individu-ally, for example runted 1-year-old yearlingscan be the same size as 1-month-old hatch-lings. Unless the date of hatch is known andstated, one should not attempt to guess acrocodile’s age, but rather record its lengthand weight.

Crocodiles that are exposed to hot andcold seasons, as a rule, grow faster in the hotthan in the cold season. In such crocodilesthe bone is deposited in laminae of varyingthickness, similar to tree rings. These bonerings can be visualized and counted in histo-logical preparations (de Buffrénil, 1980a,b;de Buffrénil and Buffetaud, 1981; Hutton,1986).

Organ morphometry

In animals with very large variations in over-all body size, it is often difficult to judge therelative size of a particular organ in an indi-vidual case. However, for a pathologicaldiagnosis it is important to be able to deter-mine whether an organ is hypotrophic,hypertrophic or normal. Huchzermeyer


Fig. 2.29. Several blood smears wrapped tightly intoilet paper are fairly secure from breakage.

(1994) found a close relation in Nile croco-diles between the mass of the two ventriclesof the heart (total ventricular mass, TV) andtotal body length, so TV is used as the stan-dard against which the other organs are mea-sured (Fig. 2.30). To make this comparison,the organ in question is weighed and so is theheart, without the auricles. The weight of theorgan is then divided by the weight of theventricles, resulting in the following ratios:

● spleen :heart ratio (SHR);● fat body :heart ratio (FHR);● kidney :heart ratio (KHR).

The spleen :heart ratio indicates the stateof activity of the spleen. The SHRs of normaland diseased Nile crocodiles are shown inTable 2.12. It must be borne in mind, though,that often the affected crocodiles die veryslowly, and that after a long illness thespleen becomes hypotrophic again and couldappear normal.

The fat body :heart ratio indicates theactual state of nutrition. An FRH <0.5 indi-cates an animal in a very poor state, while anFRH >5 indicates an overfed animal (excessenergy). The kidney:heart ratio was found tobe of limited use, as there was little variationin relative kidney mass and visibly affectedkidneys could be detected without weighing.

Examination of unhatched eggs

On farms where poor hatching results areobtained, it may be necessary to open andexamine all unhatched eggs, particularlythose from nests with very poor results. Ifthe eggs are to be submitted to a laboratory,they should be kept refrigerated, but notfrozen, before and during transport.

The eggs are cut open lengthwise with asmall pair of scissors and the contentspoured into a dish. After each egg has beenexamined, the contents of the dish arepoured into a bucket for eventual disposal.

Infertile eggs usually remain clearthroughout the incubation period and nosign of banding or remains of an embryo canbe found. If any contamination has pene-trated into the egg, the contents becomeputrid, and in such an egg a small, deadembryo may have dissolved altogether.Consequently an infertile egg may be diffi-cult to differentiate from one with earlyembryonic death. A microsatellite analysisprocedure, based on parental DNA, has beendescribed for the exact differentiationbetween infertile eggs and early embryonicdeath, but may not be applicable to routinefarm investigations (Rotstein et al., 2002).

Larger embryos can, however, be foundand examined. From their state of develop-ment one can try to judge at which pointduring incubation the embryo has died. Ifcontamination is found, or is suspected to bethe problem, submit some swabs to a bacteri-ology laboratory (i.e. sterile swabs dippedinto the liquid before it has been poured outof the egg).

Medication

Administration of medication

Mass medication

Mass medication is rarely given in the water,as only a small part of the water is consumedby the crocodiles. Medication of the water issuitable for the external treatment of skininfections and for a supportive treatmentwith salt (1 g l�1). The salt is intended to

86 Chapter 2

Fig. 2.30. The relative sizes of myocardium, fatbody and spleen.

replace salt lost into the fresh water by ani-mals that have not eaten for a while, andthus have not been able to obtain salt fromtheir food (see pp. 41 and 282).

Antibacterials and anticoccidials can beadministered via the food. Medicated pel-leted rations will have to be prepared spe-cially for the purpose. When medication is tobe incorporated into wet rations based onmeat or fish, only one-quarter of the dryration dose should be used to compensatefor the high moisture content of the ration.

Mixing powders or liquids accurately intowet rations is extremely difficult and an evendistribution of the medication is rarelyachieved. If the mince is spread out in a thinlayer on a tray, a liquid can be sprayed overit. Medication in powder form should first bemixed into bonemeal to increase its bulk,and only then be mixed into the mince.

Individual dosing

Small crocodiles that can be handled easily(hatchlings) can be dosed individually bymouth, in the following way. The liquid(0.2–0.5 ml) is drawn into a 1 ml plasticsyringe. The crocodile is held in one hand,with the thumb and index finger holding thebase of the mandible (Fig. 2.31). Tapping thehatchling’s nose lightly with a pen causes it toopen its mouth, or the mouth is forced opengently with the tip of a finger of the otherhand, and the entire syringe is slowly pushedinto the mouth, past the gular valve and intothe oesophagus, to the cardia of the stomach.Then the plunger is pushed down before the

syringe is withdrawn slowly. The crocodile isstill held upright for a while, so that the liquidis not regurgitated. During the whole proce-dure care should be taken not to exert anypressure on the stomach.

Larger crocodiles can be force-fed bystomach tube in the same way as for collect-ing stomach contents (see p. 66). It may beeasier to use a flexible tube, threading itthrough a hole of appropriate size drilledthrough a long piece of wood, which can beheld still by an assistant (Fig. 2.32). Themethod described for stomach washing (p.66) can also be used for force-feeding.

Larger, even very large crocodiles, partic-ularly ones that have not eaten for a longtime and need dosing with sugar to stimu-late their hunger, can be dosed with a thicksugar syrup (e.g. treacle or honey), whichcan also be medicated with whatever isrequired. The syrup is rolled on to one end ofa long stick (broomstick), and with anotherstick or plastic pipe the crocodile is tappedon its snout until it opens its mouth. Thesyrup then is slapped into the back of itsmouth and wiped off on the tongue. Fromthere it will be swallowed slowly by the croc-odile. After dosing, the crocodile should beprevented from entering the water, so as notto wash the syrup out of its mouth (personalcommunication, P. Martelli, Singapore, 1994).

Injections

The resorption of injected medication isslower in reptiles than in mammals or birdsbecause of the slower heart rate (p. 43). It is


Table 2.12. Spleen:heart ratios (SHR) of Nile crocodiles in relation to different pathological conditions(Huchzermeyer, 1994). SHR values indicate the degree of splenomegaly.

Condition Range n See also

No apparent infection 0.19–0.72 77Conjunctivitis, mostly chlamydial 0.11–2.12 40 Chapter 5, p. 167;

Chapter 7, p. 245Septicaemia 0.24–2.57 84 Chapter 5, p. 173;

Chapter 6, p. 228Salmonellosis 0.22–2.68 70 Chapter 5, p. 164Gastritis 0.41–2.49 54 Chapter 7, p. 251Enteritis 0.34–2.71 35 Chapter 6, p. 226;

Chapter 7, p. 255

n, Number of cases.

also temperature dependent – slower at lower,and faster at higher temperatures. It is recom-mended not to inject oily solutions or emul-sions, as their resorption is even slower (Kraft,

1978). Oils and emulsions may also elicit alocal inflammatory response, and the exuda-tion of fibrin may prevent the resorption of theinjected substance entirely (see p. 46).

88 Chapter 2

Fig. 2.31. Dosing a hatchling with the help of a 1 ml syringe.

Fig. 2.32. Dosing by stomach tube.

Because of the tight adherence of the skinand the many cutaneous muscles, it is hardlypossible to give subcutaneous (sc) injectionsto crocodiles, except under the ventral skin,which is less accessible. When giving intra-muscular (im) injections, one should try toavoid injecting into accumulations of bodyfat, which would slow down the resorption.This often happens with deep injections intothe tail. The ideal sites for im injections arethe muscles of the upper limbs. An injectionwith a pole syringe is best given caudolater-ally into the junction of hind leg and tail.

Intraperitoneal (ip) injections are giveneither in the ventral midline, cranial to thepubic bone, in small crocodiles that can beheld in a belly-up position, or, in larger spec-imens, laterally on the right-hand side cra-nial to the knee. It is also possible to injectinto masses of fat here, with a consequentlyreduced speed of resorption.

The sites for intravenous (iv) injectionsare the same as those that are used for takingblood samples (see p. 64). However, itshould be noted that all these sites onlyallow the needle to be placed in a perpendic-ular position to the vein and, therefore, someor even all of the liquid could well beinjected paravenously, particularly if the ani-mal struggles during the injection. A case ofparavenous injection during an attemptedblood transfusion into the supervertebral(internal jugular) vein in an African dwarfcrocodile ended in the death of the crocodiledue to compression of the spinal cord byblood entering the subarachnoid space(Heard et al., 1988). For future attempts ofblood transfusion, the authors recommendedusing the tail veins, or the external jugularvein after surgical dissection.

Tibial puncture

An alternative to the iv route may be tibialpuncture in the middle of the proximal thirdof the tibia. This allows the needle to be placedin the venous sinuses in the head of the tibia.The injected liquid will be transported veryrapidly from this site. This may be the route ofchoice when a needle must be left in place forrepeated injections or blood sampling, e.g. forpharmacokinetic studies. This method has

been adapted from paediatrics and has beenused successfully in birds (Ritchie et al., 1990).

Drugs and dosages

Generally, the same drugs that are used inpoultry can be used in crocodiles. For a sin-gle dose, the same dosage should be used asin poultry. However, excretion is generallyslower in crocodiles and, therefore, repeatedadministrations should be spaced accord-ingly. Normally, with drugs being given inthe food, this evens out, as crocodiles tend toeat only every second day. The dosageshould also take into account the relativelylow feed intake of crocodiles. The dosagelevels given in Table 2.13 have been calcu-lated for the average feed intake.

Another point to be taken into considera-tion with mass administration of medicationis the possible effect on the environment.Many drugs are excreted unaltered and willbe washed out with the water. They have thepotential to pollute rivers or other naturalwater bodies into which the effluent from thecrocodile farm is released. Some of themetabolites of commonly used drugs arealso biologically active.

The antibiotic sensitivity of bacteria iso-lated from crocodiles varies considerably. Itis therefore recommended that antibacterialsshould be used only after the sensitivity ofthe bacteria in question has been establishedin a laboratory (see p. 91).

The prolonged or repeated prophylacticuse of antibiotics only serves to increase thelevel of resistance in all the bacteria exposedto the particular antibiotic. This resistancecan even be passed on to other species ofbacteria, creating problems when the sameantibiotic could, or should, be used in a dis-ease outbreak. This is the reason why theprophylactic use of antibiotics should bestrictly avoided (see also p. 91).

The commonly used drugs and theirdosages have been collated in Table 2.13.Note that ivermectin is toxic to crocodiles(see p. 225). It causes paralysis when used athalf the mammalian dose (personal commu-nication, C.M. Foggin, Harare, 2000).


Vaccines

Vaccines are used to stimulate antibody pro-duction against specific pathogens. For thepreparation of such vaccines it is necessaryto culture and propagate the specific diseaseagents. Few vaccines have been used in croc-odiles so far, as none of the crocodile-specific

viruses have yet been cultured. In an inacti-vated vaccine, the agent has been killed toprevent its further multiplication andspread, while a live vaccine allows the agentto multiply in the inoculated host.

An autogenous crocodile pox vaccine wasprepared and tested successfully by Horner(1988a). He macerated 1 g of pox crusts,

90 Chapter 2

Table 2.13. Drugs and dosages commonly used in crocodiles.

Drug By mouth im In feed Times Refs

Tetracyclinea 75 mg kg�1 Single dose 11.5 g kg�1 Daily for 10 days 1

10 mg kg�1 10 mg kg�1 Daily for 9 days 3, 40.5 g kg�1 For 4–10 days 5

Tetracycline long actinga 20 mg kg�1 Repeat after 3 days 5Kanamycina 20 mg kg�1 Every 2nd day for 2

8 daysGentamycina 2.5mg kg�1 Every 3rd day for 3, 4

15 days3 mg kg�1 5

Chloramphenicola 20 mg kg�1 2� per day for 3, 49 days

10–30 mg kg�1 Daily for 4 days 5Penicillinsa 0.1 MIU kg�1 Repeat after 2 days 5Danofloxacin (Advocin®)b 1 g kg�1 For 5 days 6Enrofloxacin (Baytril®)b 0.05–0.2 ml kg�1 5Sulphachloropyrazine dilute 1:5, 5

(ESB3)b 5 ml kg�1

10 g kg�1 For 4 days 5Amproliumb 2 g kg�1 Daily for 7 days 5

1 g kg�1 Continuously 5Toltrazuril (Baycox®)b 7 ml kg�1 For 3 days 5Ketaconazolea 50 mg kg�1 1� repeat after 3, 4

2 weeksFenbendazole 2 ml kg�1 For 3 days 5

(100 mg ml�1)Oxfendazole 5 ml kg�1 For 3 days 5

(22.6 mg ml�1)Thiabendazolea 50 mg kg�1 1� repeat after 4

2 weeksMebendazolea 20 mg kg�1 1� repeat after 4

2 weeksPiperazinea 50 mg kg�1 1� repeat after 4

2 weeksCa-borogluconate ip, dilute 1:2, 5

(250 mg ml�1) 3 ml kg�1

Doramectin 1% 1 ml 50 kg�1 7NaCl In water For 10 days 6

1 g l�1

a Active substance.b As product.1, Huchzermeyer et al. (1994a); 2, Huchzermeyer (1991a); 3, Verseput (1986); 4, Jacobson et al. (1983);5, Foggin (1992a); 6, own recommendation; 7, C.M. Foggin, Harare (2000), personal communication.

collected from the skin of affected crocodiles,in 10 ml of phosphate buffered saline, added1 MIU penicillin and 1 g streptomycin, andleft the suspension standing for 24 h, afterwhich it was centrifuged at 180 g for 10 min.The trial hatchlings were inoculated with0.5 ml of this vaccine sc between the hind legand the base of the tail.

Mohan et al. (1997) reported the vaccina-tion of Nile crocodiles against Mycoplasmacrocodyli. The vaccine was inactivated withformalin, and contained aluminium potas-sium sulphate as an adjuvant.

The use of an inactivated calf paratyphoidvaccine as part of a range of therapeutic andpreventive measures in an outbreak of sal-monellosis in farmed Nile crocodile hatch-lings was reported by Huchzermeyer(1991a).

Pharmacokinetics

Pharmacokinetics deals with the fate ofdrugs in the body, their absorption, distribu-tion, metabolization and, finally, their excre-tion. Hardly any work has been carried outin this field in crocodiles. We assume that,because of the slow circulation in crocodiles,the resorption, distribution and excretion ofany drug are much slower than in birds andmammals, and that they are temperaturedependent. We also assume that, because ofthe low metabolic rate of crocodiles, they aremetabolized more slowly. Drug dosage rates(p. 89) have generally been calculated on thebasis of these assumptions, and in certaincases have been corrected if and when signsof toxic effects occurred. There is no doubtthat species differences might occur amongthe crocodilians regarding pharmacokineticsand drug tolerance. This is a very wide fieldof research that urgently needs attention.

In this context, the paper by Coulson andHernandez (1953), regarding glucose,insulin, adrenaline and ACTH in theAmerican alligator, deserves particular men-tion. The authors found that injected glucoseis removed from the bloodstream at a veryslow rate. One unit of insulin per 1 g of bodymass produced an immediate state of shockdue to hyperglycaemia, which lasted for a

few hours. A second state of shock occurredmore than a day later, and was due to hypo-glycaemia. Large amounts of glucose pro-moted the formation of liver and bodyglycogen. For 2 h after the injection of adren-aline no effects on blood glucose or pupillaryresponse were observed. After 2 h the pupilscontracted to slits and blood glucose rose byseveral hundred mg ml�1. Adrenalinereduced the glycogen stores of the liver toabout one-third and the body glycogen toabout one-half of normal values within 24 h.Prolonged daily injections of cortisone,10 mg kg�1 body mass, caused a moderatehyperglycaemia. Daily injections of ACTH,5 mg kg�1 body mass, had no effect.

Antibiotic resistance

The antibiotic resistance of pathogenic bacte-ria depends on previous exposure to thesesubstances. If crocodiles are fed the meat orwhole carcases of farm mortalities, theyacquire the pathogens of these animals,which will be resistant to any antibiotics towhich they have been exposed previously.This is the case particularly if poultry or pigsare used as crocodile feed.

As not all bacteria are killed during acourse of treatment, the most resistant onesare likely to remain alive and pass on theirgenes for resistance to their progeny. Bacteriacan also transfer these genes to other bacter-ial species, thereby causing a whole popula-tion of bacteria to become resistant veryrapidly.

Continuous use of antibacterials on thecrocodiles themselves can obviously alsostimulate antibiotic resistance and shouldtherefore be avoided (see above).

Surgical Interventions

Most of the procedures described in the following were designed for experimentalsurgery, used in physiology research. Incases in which clinical surgery becomes nec-essary, they may be able to give some guid-ance on how to access a particular organ.


Anaesthesia

Anaesthesia differs from immobilization (p.70), in that it excludes the sensation of pain,which immobilization does not do. For anysurgical procedure it is necessary to employa local or general anaesthetic, possibly inaddition to immobilization. Drugs anddosages used in the anaesthesia of crocodil-ians have been reviewed by Loveridge (1979)and Bennett (1991).

Hypothermia

Lowering the body temperature by packingthe animal in ice, or even placing it in afreezer, reduces its ability to react and immo-bilizes the animal, but does not reduce itscapability to perceive pain (Kennedy andBrockman, 1965; Hartman, 1976; Ensley et al.,1979). The procedure is very stressful, andmay lead to post-recovery complications. Itshould, therefore, never be used, even inconjunction with local anaesthesia (Bonath,1979; Nichols, 1986; Bennett, 1991).

Inhalation anaesthesia

Crocodiles, like all amphibious animals, canhold their breath for prolonged periods. Thismay make it difficult to induce inhalationanaesthesia (Jones, 1977). However, this maybe overcome by removing the tape coveringthe eyes, which was found to stimulate respi-ration in a 2.2 m Crocodylus palustris (Russo,1979). For the induction of anaesthesia, theanimal’s head was placed in a clear plasticbag filled with a halothane–oxygen mixturefrom a vaporizer, operated at a 5.5%halothane concentration with a flow rate of5 l min�1. After 20 min the animal wasthought to be sufficiently anaesthetized, theplastic bag was removed and its jaws wereheld open by the insertion of a woodenblock. However, the animal started to react,so the plastic bag was replaced for another15 min. After that, a cuffed endotracheal tubewas inserted and connected to the anaes-thetic machine, which was then operated at2.5% halothane with 2 l min�1 oxygen. Aftertermination of the anaesthesia it took the ani-mal 10 min to recover fully and walk back to

its pool (Russo, 1979). Apparently, the loss ofthe skin reflex is a better indicator of thedepth of anaesthesia than the loss of otherreflexes. This reflex is provoked by applyingfirm pressure with a key, in a linear strokealong the side of the crocodile (Russo, 1979).

In juvenile American alligators of ±770 gbody mass, anaesthesia was induced by 5%halothane and 95% oxygen and maintainedwith 3% halothane and 95% oxygen (Brancoand Wood, 1993). In American alligators,Calderwood (1971) induced anaesthesia with3% halothane in oxygen via a mask, whichafter intubation was continued with 1.5%halothane.

General anaesthesia by injection

A number of general anaesthetics have beenused in crocodiles, including barbiturates,ketamine, phencyclidine and tricainemethane sulphonate. Their dosages are sum-marized in Tables 2.14–2.16. As most of thesedrugs are injected either im or ip, theirresorption may take a long time. Recoveryfrom this type of general anaesthesia mayalso be prolonged and barbiturate anaesthe-sia should be avoided, since recovery is espe-cially protracted (Nichols, 1986).

Local anaesthesia

Local anaesthetics work best when usedtogether with chemical restraint (see p. 70). Invery small hatchlings there may be a dangerof overdosing, as is the case in small birds.Lignocaine and procaine have been used forlaparotomies in C. johnsoni and Crocodylusniloticus, respectively (Limpus, 1984; Kofronand Trembath, 1987) (see also below), andprocaine, together with thiopental, inAmerican alligators (Greenfield and Morrow,1961). Xylocaine was used in conjunctionwith hypothermia in an American alligator,for the removal of fibro-granulomatousmasses (Ensley et al., 1979) (see also p. 95).

Laparoscopy

Limpus (1984) examined the ovaries of 23mature Johnston’s crocodiles by laparoscopy

92 Chapter 2

in the field. Each crocodile was strapped to aboard to prevent movement. The abdominalcavity was tightly inflated with air from acompressed air cylinder, as used for under-water diving, delivered via a Veress pneu-moperitoneum needle (10 cm) with aspring-loaded blunt stylet. This was insertedthrough the ventral body wall, two scalerows to the right of the midline and anteriorto the pubic bone. A 7 mm OE trocar and

cannula with valve was inserted through thesame incision, to provide an entry for thelaparoscope, a Storz 26031B Hopkins tele-scope (OD 6.5 mm, forward-oblique viewing,30E wide angle, incorporating fibre opticslight transmission) connected to a Storz 482Bcold light source.

The following internal structures wereseen and identified during laparoscopy:intestinal loops, hard-shelled eggs in the


Table 2.14. The use of barbiturates for general anaesthesia in crocodiles.

DoseSpecies Length (m) Mass (kg) (mg kg�1) Route References

PentabarbAlligator

mississippiensis <2.3 >43 By mouth s 1A. mississippiensis 90–180 11–14.5 By mouth s

11 ipa;b s 1A. mississippiensis 3.35 135 14.8 By mouth

14.8 ip3.7 ipa;b s 1

A. mississippiensis 9 ip s 2A. mississippiensis 7.8–8.9 im s 3Caiman crocodilus 15.5 imc u 4C. crocodilus 8.9 imd u 4A. mississippiensis 1–1.14 4.1–5.9 20–30 ip s 6

ThiopentalA. mississippiensis 1–1.2 7–30 15 ipe s 5

a + Tubocurarine ip.b + Postsurgically pentamethylene tetrazole half-hourly or hourly.c Split and given in three consecutive amounts.d During induced hyperthermia 35.6°C.e + Local anaesthesia with procaine.s, Satisfactory.u, Unsatisfactory.1, Pleuger (1950); 2, Jones (1977); 3, Brisbin (1966); 4, Klide and Klein (1973); 5, Greenfield and Morrow(1961); 6, Xu et al. (1997).

Table 2.15. The use of ketamine for general anaesthesia in crocodiles.

DoseSpecies Length (m) Mass (kg) (mg kg�1) Route Comment References

Aligator mississippiensis 2.5–3 125–150 im h 1

Crocodylus niloticus 0.07 59 d 2A. mississippiensis 0.65–2.92 0.8–100 40–100 im h, s 3C. niloticus 22–44 s, r 4

h, Fine for handling only. d, Dead after 1 h.s, Satisfactory.r, Respiratory depression.1, Jones (1977); 2, Cooper (1974); 3, Terpin and Dobson (1978); 4, Thurman (1990).

oviducts (vaginae), soft-shelled eggs in theoviducts (uteri) and the ovaries with small orlarge follicles.

Laparotomy

Limpus (1984) performed laparotomies onfive adult Johnston’s crocodiles to examinetheir ovaries. The manually restrained ani-mals were held in dorsal recumbency, theskin around the site of the incision wasscrubbed and disinfected, and the incisionsite was injected subcutaneously with a localanaesthetic (see also p. 92). The incisionswere closed with surgical catgut, and coatedwith a sterile spray-on wound dressing. Thecrocodiles were kept dry and cool for 24 hafter the surgery and then returned to thewater.

Kofron and Trembath (1987) describelaparotomies on adult female Nile crocodilesfor the examination of their ovaries. The ani-mals were restrained manually, their legswere tied together over their backs and theireyes were taped closed. Two animals wereoperated on in dorsal, and two in ventralrecumbency, and it was found that the latterstruggled less. For the animals in ventralrecumbency, the abdomen was lifted some-what on the side of the incision by placing a

block of wood underneath. The skin wasscrubbed, disinfected and a local anaestheticwas injected at several points along the lineof the intended incision, transversallybetween two rows of scales, halfwaybetween the last rib and the leg (see alsop. 92). The skin was incised ±10 cm and thedifferent muscle layers each dissectedbluntly.

After the operation the peritoneum, themuscle layers and the fat layer were closedwith continuous catgut sutures. The skinwas closed with stainless-steel or nylonsutures. The incision was then sprayed witha plastic skin sealer containing neomycinand bacitracin, and each animal was givenchloramphenicol by im injection into thebase of the tail. The animals were releasedinto the water 30 min after completion of theoperation and were recaptured 1–3 monthslater, when the skin sutures were removed.

Clinical surgery

Gastrotomy

Pleuger (1950) describes the gastrotomy ofan adult zoo ‘crocodile’ (species not indi-cated) that had been observed swallowing aCoca Cola bottle. The animal was anaes-

94 Chapter 2

Table 2.16. Other agents used for general anaesthesia in crocodiles.

DoseAgent Species Mass (kg) (mg kg�1) Route Comment References

MS222® Alligator mississippiensis 88–99 im s, l 1

Caiman crocodilus 66–110 im u 2Sernylan® A. mississippiensis 11–22 im h, l 1Viadryl® A. mississippiensis 1.4–4.3 150 s 3Saffan® A. mississippiensis Immature 0.74 iv u 4

10 0.25 iv s 4M99® Crocodylus spp. 0.3–0.5 s 5

C. crocodilus 0.112 0.5–5 im s 6A. mississippiensis 1.5–6.7 1–20 im ss 6

MS222®, Tricaine methanosulphonate; Sernylan®, phenylcyclidine; Viadryl®, hydroxidione; Saffan®,alphaxolone/alphadolone; M99®, etorphine; s, satisfactory; l, long recovery; u, unsatisfactory; h, fine forhandling only; ss, satisfactory in small individuals only.1, Brisbin (1966); 2, Klide and Klein (1973); 3, Campos (1964); 4, Calderwood and Jacobson (1979); 5,Jones (1977); 6, Wallach and Hoessle (1970).

thetized with pentobarbitol (see p. 92). Theabdominal skin was scrubbed, disinfectedand a longitudinal 25 cm incision was madein the midline, between two rows of scales.The skin was held back by retractors, and theabdominal muscle was incised down to theperitoneum and also held back by retractors.The stomach itself was palpated and broughtto the surface through a peritoneal incision.Then a 7.5 cm incision, made through thestomach wall along the line of its greatestcurvature, exposed the neck of the Coca Colabottle. This bottle, unbroken, was removedfrom the stomach, together with the majorportions of five broken bottles, 39 stones,three marbles, two firearm shells, a plasticwhistle and a porcelain elephant.

The stomach mucosa was thoroughlysponged and the gastric incision was closedwith surgical silk No. 0, which was also usedto close the abdominal muscle and the subs-cutal skin. The skin was closed with No. 1sutures, painted with collodion and coveredwith gauze sponges. The entire abdomenwas then wrapped in a heavy muslin ban-dage. The crocodile was not allowed backinto its pool for 3 weeks, after which the ban-dage was removed and the wound wasfound to have healed completely.

Pleuger’s (1950) speculation about stor-age of swallowed matter in the loweroesophagus is wide off the mark: the stom-ach takes all the swallowed matter and theoesophagus does not act as a crop, as infowls, or a proventriculus, as in the ostrich.While gastroliths are commonly found incrocodiles and their presence is regarded asnormal, it is possible that the swallowing oflarge numbers of foreign bodies might bedue to deranged, or stress, behaviour (seep. 290), similar to that commonly observedin ostriches (Huchzermeyer, 1998a). Whetherthe operation described above was in factnecessary is a debatable point; it may be thecase that the bottles would have been eitherregurgitated or ground down. Regurgitationof hair balls and foreign objects has beenobserved in American alligators (Chabreck,1996; Chabreck et al., 1996) (see p. 37). Thebandage appears to have been entirelyunnecessary, and the animal should havebeen returned to the water much earlier,

probably within 3 or 4 days, to avoid unnec-essary dehydration (see p. 283).

Oral surgery

Russo (1979) reports on the removal of agranulomatous polyp from the palatal foldin the pharynx of a 55 kg, 2.2 m C. palustris,at the New York Zoological Park. The animalwas restrained manually and anaesthetizedwith halothane (see p. 92), while the mouthwas held open by a wooden block insertedon one side, between the jaws. The polypmeasured 5 � 3 � 1.5 cm and was easilyexcised from the underlying tissue. Twosmall vessels entering the growth were lig-ated and the incision was closed with simpleinterrupted sutures of polyglycolic acid(Dexon, American Cyanamid). Ten minutesafter completion of surgery, the animalwalked back into its pool. It resumed feedingon schedule and the surgical site healedwithout complication or recurrence.

An open multiple fracture of themandible of a 1.05 m long American croco-dile was operated on under general andlocal anaesthesia (ketamine 50 mg kg�1 andlidocaine 1%). A 1 cm piece of bone wastaken out. The two ends of the fracturedjaw bone were united with the help of astainless-steel plate, stitched in place withsurgical stainless-steel wire. During recov-ery, the lower jaw deviated towards theinjured side by approximately 5° (Rubio-Delgado, 2000).

Limb surgery

Ensley et al. (1979) describe the removal ofgranulomatous masses from both forelimbs,plantar in the metacarpal area of a 128 kgAmerican alligator, at San Diego Zoo. Theanimal was restrained physically and byhypothermia, and was given a local anaes-thetic at the base of the growths. A circum-ferential incision was made at the base ofeach mass, the edge of this incision wasundermined and dense fibrous connectivetissue was excised from the centre of the sur-gical wound to facilitate its closure. Simple,interrupted sutures of 0.4 mm stainless-steelwire were used to close the skin. A gauze


dressing, covered by elastic adhesive tape(Elastakon, Johnson & Johnson), was appliedto each carpus, leaving the digits exposed.The operation lasted 2 h, and minimal bleed-ing was encountered.

After the operation, the animal washoused for 6 weeks in a shaded enclosure onconcrete. Dressings were changed each weekand wound drainage was minimal. Whenthe animal was returned to an aquaticexhibit, the stainless-steel sutures, with asmall amount of adjacent tissue, weresloughing while being replaced by regener-ating skin (Ensley et al., 1979).

Yolk-sac excision

The surgical removal of retained yolk-sacshas been described by Youngprapakorn andJunprasert (1994). For details, see Chapter 4(p. 144).

Experimental surgery

Gastric cannulation

Sixteen C. crocodilus ranging from 30.5 to96 cm total length were used in the experi-ments by Diefenbach (1975b). As repeatedcannulation of the stomach, through themouth, for the sampling of fluids was foundto be too traumatic, a polyethylene tube wasinserted via the mouth into the lumen of thestomach. The cranial end was then led out-side through an incision in the floor of thepharynx, lateral to the basihyal cartilaginousplate of the larynx. The outside of thecatheter was stoppered and strapped to theanimal’s neck with surgical adhesive tape,which resisted immersion in water. Details ofanaesthesia, if any, and suture were notgiven (Diefenbach, 1975b).

Bile fistula

Xu et al. (1997) implanted bile fistulas intoseven juvenile American alligators, between104 and 114 cm long and weighing4.1–5.9 kg, for the study of bile salts. The ani-mals were anaesthetized by the ip injectionof pentobarbital, 20–30 mg kg�1 live mass,

and deep anaesthesia followed within 1–2 h.The animals were taped to an operating tableprior to surgery. A midline incision of about8 cm was made just caudally of the rib cage.The gall bladder was mobilized from themesoduodenum and the cystic duct, dis-sected and ligated. Cholecystotomy was per-formed by inserting silicone tubing into thegall bladder and fixing it with a purse-stringsuture. The tubing was exteriorized througha dorsal subcutaneous channel to an areanear the hind legs of the animal, fixed inposition with tape and inserted into a sterile,plastic sampling bag, which was alsosecured with tape.

After three animals had been fistulated inthis manner, the method was modified whenit was found that the left hepatic duct inmost alligators had a direct connection withthe duodenum. After ligation of the cysticduct, the left hepatic duct was dissected inthe mesoduodenum, double-ligated and cutbetween the ligations. Then the procedurefor cholecystotomy and externalization ofthe bile drainage tubing was followed asbefore. The alligators were maintained in drytanks for 5–7 days postoperatively and thenplaced in environmental chambers (Xu et al.,1997).

Open-heart surgery

Heart operations were carried out on 11American alligators (1.1–1.5 m) by Kennedyand Brockman (1965). After immobilizationby hypothermia (see p. 92), and scrubbingand disinfection of the site of incision, a mid-line cut between the scales was made fromthe distal end of the sternum, extending cau-dally for about 6 cm. Beneath the scales thethin, fibrous tissue and the muscle layerwere exposed and incised to permit entryinto the pericardium, which was lifted withforceps and incised longitudinally. The peri-cardial incision was large enough to permitdelivery of the heart beyond the ventralabdominal wall. The gubernaculum cordiswas clamped, cut and tied on the side of thepericardium. Near the apex of the heart, theclamp was left on the gubernaculum cordisand used for traction when manipulating theheart. After delivery of the heart, a cardiac

96 Chapter 2

tourniquet, consisting of a heavy cottonstring looped within a glass tube, wasapplied so as to encircle all the vessels nearthe base of the heart. Once the cardiactourniquet was tightened, a time was set tomeasure the time of cardiac occlusion. Themean occlusion time for nine alligators was22.5 min (range 16–30 min). The ventriculo-tomy began just caudal to the junction of theright ventricle, with the conus arteriosus lon-gitudinally for about 1.5 cm, and avoidedmajor coronary vessels.

After completion of the experiments, theright ventriculotomy wound was closed intwo layers with a continuous suture throughthe myocardium and through the epi-cardium. Shortly before closure, the ventriclewas flooded with Ringer’s solution to reducethe risk of air embolism. The cardiac tourni-quet was released immediately after the ven-tricle had been closed. The heart wasobserved through several beats to demon-strate adequate closure and, when necessary,one or two additional sutures were applied.Clotted blood was removed from the pericar-dial cavity and the cavity was closed looselywith interrupted fine silk sutures to allow

drainage. The fibrous and muscle tissue cutduring the initial midline incision was closedwith an interrupted suture of No. 30 stain-less-steel wire. Eastman 910 Monomer or col-lodion was applied to the sutured wound tostrengthen and seal it. After the operationthe alligator was left in a dry cage for up to 2weeks to ensure that no infection or otherproblem had occurred.

Five of the operated alligators died with amean survival time of 35 days. All of themhad an acute pericarditis, which the authorsbelieved to have been due to insufficient clo-sure of the skin wound. Sutures did ruptureduring violent movements of the alligatorswhen they were caught for inspection of thewounds. Even sutures that remained intactcaused local peripheral erosion around thesuture of scales and subjacent tissue, witheventual disruption of the wound (Kennedyand Brockman, 1965). Another more likelyreason for the high incidence of pericarditisafter the operation may be stress septicaemia(p. 228) brought about by the lack of anaes-thesia during hypothermia, by the hypother-mia itself, by water deprivation or by thestress of frequent handling (p. 278).


The contents of this chapter are not intendedto be a definitive guide to crocodile farming.However, most crocodile diseases are some-how related to, or caused by, managementfactors, and this cannot be made clear in thediscussion of the diseases unless the princi-ples of crocodile farming have been spelledout somewhere. As there is, at present, notextbook on this subject, it became necessaryto collect and present the relevant facts inthis book.

Nutrition

In the wild

The study of the nutrition of crocodiles in thewild is based mainly on the analysis of theirstomach contents and only secondarily onthe observation of their behaviour.Indigestible items, such as shells and fishscales, tend to accumulate in the stomachand may skew the results of such analyses. Itis also logical to assume that prey sizeincreases as the crocodile grows. The factthat fishes are the only known intermediatehosts of the internal parasites of crocodilesfurther indicates the important role of fish inthe diet of all crocodilians.

Hatchlings start feeding on small aquaticinvertebrates such as insects, crustaceans and

snails, and later include tadpoles, small frogsand fish in their diet. As they grow, the pro-portion of fish increases and later birds andsmall mammals are also taken. Hippel (1946)examined 587 stomach contents of Nile croco-diles in Uganda, of which 141 were found tobe empty apart from stones. Of the remainingstomachs, 73.1% contained fish, 14.8%amphibians and reptiles, including crocodileremains and crocodile eggs, 8.5% birds, 1.6%mammals, 0.7% insects and 36.3% plant mate-rial, the latter probably ingested accidentally.

Stomach contents of Crocodylus porosus upto 180 cm in length consisted mainly of crus-taceans and insects, with an increasing pro-portion of vertebrates (fish, reptiles, birdsand small mammals) in animals longer than120 cm (Taylor, 1979).

Stomach contents of adult wild-caughtdwarf crocodiles Osteolaemus tetraspis sur-veyed at markets in the Congo Republiccomprised remains of beetles and otherinsects as well as spiders, scorpions and mil-lipedes, also remains of fishes, frogs, lizards,snakes, birds and small mammals (Riley andHuchzermeyer, 2000).

Energy

The metabolic rate is the rate at whichenergy is burned. In crocodiles, as in other

Chapter 3

Important Aspects of Crocodile Farming

© CAB International 2003. Crocodiles: Biology, Husbandry and Diseases98 (F.W. Huchzermeyer)

reptiles, this is dependent on the body andenvironmental temperature and on theenergy demands of certain activities. Thus itincreases sharply during the digestion of ameal (Gatten, 1980). In American alligators itwas found that acetate (from fat) was pre-ferred to glucose as a source of energy, butthe major pathways of energy utilizationwere the same as in mammals (Black et al.,1963).

Lawrence and Loveridge (1988) demon-strated that a meat diet (ox heart plus bonemeal) did not fulfil the energy requirementsof juvenile Nile crocodiles. The addition ofraw maize (corn) flour as an energy source tothe rations of spectacled caimans reducedtheir performance (Avendaño et al., 1992), ascrocodiles cannot digest raw starch. The sup-plementation of rations of American alliga-tors with precooked (extruded) starchimproved not only the growth performanceof the alligators but also the digestibility ofprotein (Staton et al., 1990a,b, 1992). Thesame authors found a similar improvementby supplementing the rations with fat.However, fat supplementation alone of C.porosus diets did not reduce the use of pro-tein as an energy source, but led to fat depo-sition instead. The digestibility of long-chainsaturated fatty acids was less than that ofunsaturated fatty acids, and C20:5 as well asC22:6 fatty acids were found to be essentialfor juvenile C. porosus (Garnett, 1985, 1988).

Protein

While protein may be used partially as asource of energy, its main purpose in nutri-tion is to provide amino acids that are usedin the synthesis of the body’s own proteinsfor the growth of body tissues. As predators,crocodiles in nature consume animal proteinalmost exclusively. However, in feed trialswith American alligators, they have beenshown to utilize isolated soybean proteinequally well when it was incorporated as40% of the total protein content of the ration(Staton et al., 1992). Total digestible proteincomprising 42.5–48.7% of the rations gavethe best performance (Staton et al., 1990b).

Minerals

There is no need to supply additionalmacrominerals if the crocodiles are fed meatwith bones. In compounded rations themacrominerals are best supplied by the addi-tion of bonemeal. Fish meal is a good sourceof many microminerals (trace elements). Thecomposition of a micromineral premix usedin South Africa (Feedmix, Johannesburg) isshown in Table 3.1. The quantities given arefor inclusion into 1 t (1000 kg) of dry mixedration. In a meat- or fish-based wet ration,only one-quarter of the amount should beused, because of the water content of theration (see also Table 3.4). A trace mineral pre-mix used in feeding trials with juvenileAmerican alligators is shown in Table 3.2.

Vitamins

There are hardly any experimental dataconcerning the vitamin requirements of

Important Aspects of Crocodile Farming 99

Table 3.1. Mineral premix used for crocodiles inSouth Africa (Feedmix, Johannesburg), quantitiesper 1 t of complete ration.

Availa-Zn 40,000 mgAvaila-Cu 5,000 mgAvaila-Mn 40,000 mgAvaila-Fe 20,000 mgCholine 600,000 mgIron 40,000 mgCopper 7,000 mgZinc 70,000 mgCobalt 500 mgManganese 60,000 mgIodine 1,500 mgSelenium 200 mgChromium 200 mg

Availa, mineral in a metabolically available form.

Table 3.2. Micromineral premix used in feedingtrials with American alligators, inclusion per 1 kg ofwet ration (Staton et al., 1992).

Manganese 240 mgZinc 200 mgIron 120 mgCopper 20 mgIodine 4.2 mgSelenium (sodium selenite) 0.1 mg

crocodiles. Most of the recommendations arebased on extrapolation from other species. Acrocodile vitamin premix used in SouthAfrica (Feedmix, Johannesburg) is shown inTable 3.3. The quantities given are for 1 t(1000 kg) of dry mixed ration. In a meat- orfish-based wet ration only one-quarter of theamount should be used. The composition ofthe vitamin supplement used by Cardeilhacet al. (1991) in breeding trials with Americanalligators is shown in Table 3.4 and the oneused in feeding trials with juvenileAmerican alligators by Staton et al. (1992) inTable 3.5.

Home-mixed rations

Home-mixed rations are often based on farmmortalities – dead horses, cows, pigs or poul-try. Meat from large animals usually is sepa-rated from the bones before mincing andthereby becomes deficient in macrominerals(see above), whereas poultry carcasses areminced usually with the bones. However, thebones in broiler carcasses may be deficient incalcium and phosphorus, as these birds arefed minimal mineral levels. Pig carcassesmay provide excessive amounts of fat. Thepolyunsaturated fatty acids in fish oil mayhave become rancid if the fish is not entirelyfresh when fed, and this can poison the

crocodiles, causing steatitis and fat necrosis(see p. 219). Mince that is kept frozen, andthawed out and refrozen repeatedly,becomes depleted of biotin, with the result-ing deficiency causing nervous symptoms(see p. 217).

All farm mortalities, and even other freshmeats, may contain large numbers of bacte-ria, including pathogenic ones. These can be

100 Chapter 3

Table 3.3. Vitamin premix for crocodiles used inSouth Africa (Feedmix, Johannesburg), quantitiesper 1 t of complete ration.

Vitamin A 12,000,000 IUVitamin D3 2,000,000 IUVitamin E 120,000 mgVitamin K3 15,000 mgFolic acid 3,000 mgNiacin 100,000 mgPantothenic acid 50,000 mgVitamin B1 15,000 mgVitamin B2 20,000 mgVitamin B6 15,000 mgVitamin B12 30 mgBiotin H2 1,000 mgVitamin C 1,000,000 mgAntioxidant 3,500 mgZinc bacitracina 80,000 mg

a Not a vitamin, but added as a growth promotor.

Table 3.4. Vitamin and micromineral supplementsused in breeding trials with American alligators;rate of inclusion not stated, probably per kg wetration (Cardeilhac et al., 1991).

Vitamin A 220,000 IUVitamin D3 55,000 IUVitamin C 300 mgVitamin E 14,500 IUMenadione 300 mgRiboflavin 132 mgNiacin 700 mgPantothenic acid 220 mgFolic acid 18 mgVitamin B12 0.22 mgBiotin 3.5 mgPyridoxine 88 mgThiamin 44 mgCopper 18 mgManganese 1,320 mgIron 176 mgSelenium 6 mgIodine 18 mg

Table 3.5. Vitamin supplement used in feedingtrials with juvenile American alligators, inclusionper 1 kg of wet ration (Staton et al., 1992).

Vitamin A, all-trans-retinyl acetate 18,000 IUVitamin D, cholecalciferol 2,000 IUVitamin E, all-rac-�-tocopheryl acetate 150 IUMenadione sodium bisulphite 25 mgThiamin 15 mgRiboflavin 15 mgPyridoxine 25 mgVitamin B12 0.042 mgNiacin 200 mgCalcium pantothenate 50 mgFolic acid 4 mgBiotin 1 mgCholine 1,500 mgInositol 50 mgp-Amino-benzoic acid 50 mgVitamin C 450 mg

eliminated by heating the mince, which isthen allowed to cool down before vitaminand mineral premixes are added and the mixis minced a second time (Huchzermeyer,1991a). The resulting food is a loose crumble,which does not compact on the floor of thepen as easily as fresh mince and thereforecan be consumed much better by the croco-diles.

Carbohydrate can be added to such acooked ration easily by cooking a stiff maize(corn) porridge (polenta) which is added inapproximately equal proportion to thecooked mince and the other ingredients (seeabove) before mincing the ration a secondtime.

Pellets

Provided the crocodiles are kept under con-trolled thermal conditions, within a narrowrange of their preferred temperature, andare protected from disturbances and otherstress (see p. 277), they will accept dry pel-lets as food and can be fed pellets exclu-sively from hatch to slaughter. Dry pelletshave the advantage that they are veryhygienic and can be picked up easily fromthe floor by the crocodiles, thereby minimiz-ing wastage.

In South Africa several crocodile farmersprepare their own pellets in different sizesdepending on the size of the young croco-diles. Other crocodile farmers have turned tocommercial trout pellets, also with accept-able results.

In the formulation of such pellets oneshould probably be guided by the results ofStaton et al. (1990b), although these authorswere feeding their rations in the form of athick paste, which led to serious wastageproblems. Their best results were obtained atlevels of 42.5–48.7% digestible protein and4367–4421 kcal kg�1 digestible energy, withthe inclusion of 6.3–18.8% precooked(extruded) maize (corn) and 15.8–27.4% fat.Note that the inclusion of such amounts offat into dry pellets would create serioustechnical problems. The same authors gave8.2–10.9 : 1 kcal g�1 protein as an optimaldigestible energy to crude protein ratio.

Influence of temperature on nutrientutilization

In Caiman crocodilus the amplitude and fre-quency of gastric contractions increases withtemperature, while complete emptying of afull stomach takes an average of 315 h at15°C and 99 h at 30°C (Diefenbach, 1975b)(see also p. 36). In the same species, pepticactivity in the stomach also increases withtemperature between 15°C and 35°C(Diefenbach, 1975a). While American alliga-tors kept at 32°C had greater feed intake andbody mass gains, their feed efficiency ratiowas poorer than that of alligators kept at28°C. However, the digestibility of proteinappeared not to be affected by temperature(Staton et al., 1992). At 25°C the digestion oflean meat by juvenile American alligatorswas found to be incomplete (Coulson andCoulson, 1986).

Effect of nutrients on reproductiveperformance

Cardeilhac et al. (1991) studied the influenceof various nutrients on the reproductive per-formance of American alligators. Theydivided reproductive performance into nestrate, clutch size, per cent banding andembryo survival, and analysed the effects ofprotein, fat, highly unsaturated fat, vitamins(see Table 3.5) and a growth promoter(‘Gatorcillin’ containing 200 mg virgini-amycin and 800 mg oxytetracycline).

Nest rate was influenced by protein con-sumption, followed by total feed intake andhighly unsaturated fat, and slightly by vita-min and antibiotic supplementation. Clutchsize was affected by total fat in the diet, fol-lowed by protein and total feed. Percentbanding was strongly correlated with vita-mins and antibiotics, followed by highlyunsaturated fat, while total fat consumptionhad a negative effect. Embryo survival wasstrongly affected by the mother’s age, andthe effect of nutrients was estimated to be inthe following order: total fat, vitamins,antibiotics, highly unsaturated fat, protein,total feed.


A high incidence of shell defects wascaused by low calcium levels in the ration ofthe breeding females. The addition of extracalcium in subsequent seasons eliminatedthe incidence of these defects almost com-pletely (Hibberd, 1996) (see p. 139).

Note that the long-term use of antibi-otics in the feed leads to bacterial resis-tance, and should therefore be avoided (seep. 91). It may also leave antibiotic residuesin the meat, which may then not be allowedto be exported to certain countries (seep. 130).

Growth stimulants

Various growth stimulants have been tried inthe different species of crocodiles. The ana-bolic steroid Laurobolin was given at a doseof 1 mg kg�1 of live mass to poorly perform-ing Morelet’s crocodiles by intramuscular(im) injection. The effect lasted for approxi-mately 21 days and there was a markedimprovement in growth and mass gains(Leon Ojeda et al., 1998). Similar results wereobtained in Caiman crocodilus yacare that wereinjected at fortnightly intervals subcuta-neously (sc) with nandrolone phenpropi-onate (Pelosi et al., 1944).

Kanui et al. (1993) treated juvenile Nilecrocodiles with weekly im injections of0.325 mg kg�1 recombinant bovine growthhormone and found that this treatment stim-ulated appetite and growth. The authors rec-ommend this treatment for poorlyperforming crocodiles kept under less thanideal conditions.

The addition of taurine, an extract of oxheart, at 0.1% to the diet of American alliga-tors resulted in greater fat digestibility andimproved weight gains (Staton et al., 1992).However, the addition of 0.025 mg day�1 ofL-thyroxine to the diet did not affect thegrowth of juvenile C. crocodilus (Avendaño etal., 1992).

Antibacterials are often used as growthstimulants. A combination of virginiamycin200 mg and oxytetracycline 800 mg is sup-plied under the name of ‘Gatorcillin’(Cardeilhac et al., 1991). Avendaño et al.(1992) used a combination of virginiamycin

84 mg kg�1 and oxytetracycline 300 mg kg�1

of the ration. The South African crocodilepremix contains 80 mg zinc bacitracin per kgof final ration (see Table 3.3).

Note that there is growing concern aboutthe stimulation of bacterial resistance due tothe widespread use of antibiotics in animalfeeds (see p. 91). Importing countriesincreasingly demand meats and meat prod-ucts to be free of growth stimulant, hormoneand antibiotic residues.

Incubation of Crocodile Eggs

Nesting behaviour and physiology

Crocodilians either lay their eggs in holes inthe sand or build nest mounds into whichthey lay their eggs. While it has been specu-lated that these two forms of nesting haveevolved during the evolution of the crocodil-ians themselves (Greer, 1970), it is also possi-ble that they represent adaptations toparticular environments. The hole nestersusually nest in sand above the flood level onriver banks, while the mound nesters ofteninhabit swamps or plains without access tohigher ground. Mounds made from plantmaterial may produce incubation heat bybacterial action, and this may be beneficial ina forest (swamp forest) environment wherethe nests cannot be exposed to direct sun-light.

Different nesting substrates differ intheir water content and in their resistance togas diffusion. American crocodile eggs insand nests were found to lose up to 15% oftheir initial mass due to evaporation duringincubation, without apparent ill effects tothe embryo (Lutz and Dunbar-Cooper,1984).

On the farm the nesting areas should allbe on the same level to avoid competition forthe higher nesting sites, and they should beseparated by walls to allow the undisturbeduse of adjacent nests (Fig. 3.1). The femalescontinue guarding their nests even when theeggs have been lifted, and remain aggressivetowards other females in the vicinity of thenest.

102 Chapter 3

Physical parameters of the egg

Crocodile eggs have an oblong ovoid shapeand a hard shell. The shell consists of anouter densely calcified layer of verticallystacked calcite crystals, a honeycomb layer ofhorizontally stacked crystals, an organiclayer containing a higher proportion oforganic matrix to calcite crystals and a mam-millary layer. The latter is more pronouncedin the central opaque region of the shell andis attached to the shell membrane, which hasnumerous pores and is separated from thealbumen by an amorphous limiting mem-brane (Ferguson, 1982) (see also p. 30).

Embryonic development starts before theeggs are laid. Within 24 h after the egg hasbeen laid, the embryo, which is floating atthe top of the yolk, attaches its membranes tothe top of the egg. By displacing the wateryalbumen towards the poles of the egg, itcauses the shell to dry out somewhat, andthis changes the optical properties of theshell and produces the visible opaque band-ing (Ferguson, 1982), the band increasing insize with the growth of the embryo (see Fig.1.43). Consequently, a banded egg can beregarded as a fertile egg and the size of thebanded area can be used to estimate the ageof the embryo (Webb et al., 1987).

During incubation, the outer crystallinelayer of the egg undergoes a degradationprocess, due to the acidic metabolic productsof the nest bacteria which cause the forma-tion of erosion craters. At the same time, cal-cite from the organic layer is mobilized forthe calcium requirements of the growingembryo. Both the extrinsic and the intrinsicaction weaken the shell, which facilitateshatching (Ferguson, 1981, 1982). However,one wonders whether this really is an evolu-tionary necessity, as most crocodile parentsassist the hatchlings to emerge from theeggs.

During the last third of incubation theoxygen uptake of Nile crocodile eggs at 32°Cis 8.11 ml h�1 (Aulie et al., 1989).

Egg collection and transport

On farms the eggs should be collected assoon after laying as possible. This is oftenimpossible if eggs are collected from thewild. Collection should be done early in themorning or late in the afternoon, not in theheat of the day, and care should be takennot to expose the eggs to direct sunlight,which would cause overheating and rapiddeath. Early in the morning the nesting


Fig. 3.1. Nesting sites all on the same level and with separating walls in a Nile crocodile breeding pen inSouth Africa.

areas are checked for signs of nightly activ-ity to determine where eggs might havebeen laid. On some farms nightly egg-lay-ing activity is recorded by an automaticvideo camera, which comes on every fewhours during the night – together withfloodlights – and does one circular sweep ofthe nesting areas. In the morning the tape isplayed back and the nests in which activityoccurred are noted.

During collection of the eggs, one personmust stand guard to fend off the female,which might want to defend the nest. Thesand is gently removed from the top of thenest until the uppermost eggs are exposed.The top of each egg then is marked with across with felt-tipped pen, crayon or penciland each egg is transferred in its position tothe transport box. Even though the embryonormally attaches itself to the uppermostpoint of the shell within 24 h after layingonly, it is good practice to mark the positionof farm-laid eggs as well, as occasionallyembryonic development has already com-menced before the eggs have been laid (seep. 30); it certainly has to be done with alleggs that have started banding.

The transport box is a styrofoam box ofthe same type as is used for incubation, withholes punched in the bottom as well as thelid (Fig. 3.2). If the eggs have to be trans-ported over long distances, they should becushioned by placing them on a layer ofmoist vermiculite. The collected eggs remainseparated by clutch, one clutch per box.

The incubator room

Crocodile eggs can be, and have been, incu-bated in boxes filled with sand or even insand mounds. This may cause hygiene prob-lems, particularly fungal infections. In thefollowing, the most successful techniquesused on crocodile farms will be described.

The incubation complex should consist ofa storage area for the egg boxes and the ver-miculite, a cleaning and packing area, theincubator room itself and a hatching room.The incubator room should be of sufficientsize to accommodate all the clutches andallow for future increase in production. Itshould be well insulated and allow the

104 Chapter 3

Fig. 3.2. Nile crocodile eggs and a styrofoam box with holes punched into lid and bottom.

required temperature and humidity to bemaintained throughout the incubationperiod.

The most even distribution of heat isachieved by under-floor heating controlledby a thermostat. Humidity of 97–99% isachieved with the help of a humidifierassisted by a fan. Covering the floor withwater to achieve the necessary level ofhumidity can cause hygiene problems andshould be avoided. Inside this room the eggboxes are stacked on stainless-steel racks,with passages between the racks for easyaccess (Fig. 3.3). Wood is prone to fungalgrowth under conditions of high humidityand the use of stainless steel is therefore rec-ommended for all structures within the incu-bator room. Ventilation of the incubatorroom is usually provided through the door,which is opened from time to time when theoperator enters and leaves. This is sufficientas the eggs consume very little oxygen (see

above) and as the air volume in the room isvery large in relation to the total mass ofeggs being incubated. When incubationfacilities on a farm in South Africa were notcompleted in time, eggs were incubated suc-cessfully in the passage between rearingpens in a space-heated rearing house (Fig.3.4).

In the cleaning and packing area, the col-lected eggs are cleaned under running tap-water and dipped in a mild disinfectantsolution (e.g. the South African product,F10®, Health and Hygiene (Pty) Ltd), beforethey are packed into the incubation boxes.This area also contains the control panelmonitoring the temperature and humidity inthe incubator room.

The hatching room should also have ther-mostatically controlled heating, should havea sink and tap for washing the hatchlingsand some basins into which the hatchlingscan be placed before they are transferred tothe rearing house (see p. 107).

Incubation temperature

The incubation temperature not only deter-mines the sex of a hatchling (see p. 32), butalso its preferred body temperature later inlife. Consequently, crocodiles that are to bereared or kept in a cooler environmentshould be incubated at a lower temperature.As the metabolic rate depends on the bodytemperature, a higher rearing temperaturewill ensure faster growth and will thereforerequire a higher incubation temperature. Thelength of the incubation period also dependson the incubation temperature. All these fac-tors have to be taken into considerationwhen choosing the temperature at which theincubator is to function, anywhere between29°C and 33°C.

In the last third of the incubation periodthe metabolic heat produced by the growingembryo can raise the temperature within thebox, and this may have to be monitored ifthe incubator room is running at a high tem-perature.


Fig. 3.3. Egg boxes stacked on racks in an incu-bator room.

Humidity

The humidity in the incubator room shouldbe held just below saturation point, 97–99%.Excessive moisture is absorbed by the eggsand leads to them swelling and bursting (seep. 139). Excessive moisture in the incubationmedium also interferes with gas permeabil-ity and can lead to the suffocation ofembryos at a fairly late stage, when theiroxygen demand is at its highest. The vermi-culite in the boxes should be soaked in waterand then squeezed out, so that it just com-pacts but does not drip.

Incubation on trays

Incubation on trays requires a particularlywell-controlled environment. In thismethod the eggs lie open on plastic eggtrays on shelves in the incubator room. Thisallows easy access to the eggs and theremoval of infertile (not banded) eggs,reducing the danger of rotting and contami-nation, and it also prevents overheatingfrom the metabolic heat produced by the

embryo. However, the eggs are exposeddirectly to fluctuations of temperature andhumidity.

Incubation in a medium

Incubation in a medium copies the situationin nature, where the egg is buried in the nest.While sand and other materials have beenused, vermiculite has been found to be supe-rior, as it is practically sterile on delivery andis capable of holding a large amount of mois-ture. However, experience has taught croco-dile farmers not to re-use vermiculite, as it isdifficult to sterilize or disinfect after it hasbeen used.

A layer of 2–3 cm moistened vermiculiteis spread on the bottom of the incubationbox. The eggs are stacked in a pyramid ontop of this layer and then more vermiculite isadded until the eggs are covered by a layer1–2 cm thick. In a different method, the eggsare stacked on the moistened vermiculite,but no further vermiculite is added, leavingthe eggs open to inspection once the lid ofthe box is lifted.

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Fig. 3.4. Incubation in the passage of a space-heated rearing house on a farm in South Africa. Theenterprise had been moved to new premises and the incubation room had not been completed beforethe beginning of the laying season.

Hatching

When the calculated hatching dateapproaches, the nest boxes are opened gentlyone by one. If the crocodiles in the eggs areready to hatch they begin croaking, callingtheir mother. The boxes containing theseeggs are taken to the hatching room, wherethe eggs are uncovered and those hatchlingsthat have hatched by themselves are takenout. The remaining eggs are examined andany further live hatchlings are assisted out ofthe shell.

As they are taken from the box, the hatch-lings are placed in a basin or bucket withclean warm water containing a mild disinfec-tant (F10®, Health and Hygiene (Pty) Ltd) fora first wash. They are then transferred to anursery basin in which they remain for 1 or 2days until their navels have closed com-pletely, after which they are transferred tothe rearing pens.

The nursery basins should have slopingfloors, allowing the hatchlings to come out ofthe water. They should also be partially cov-ered to give the hatchlings the feeling of pro-tection, as they do not realize that they areindoors and protected from predators (Fig.3.5). These basins can be glass aquaria or plas-tic or metal basins. Some farms have a smallnursery enclosure instead. However, from thepoint of view of cleaning and observation ofindividual hatchlings, smaller basins, one perclutch, are preferable. The water in the nurs-ery basins should contain a mild disinfectant,such as a quaternary ammonium or F10®

(Health and Hygiene (Pty) Ltd).

Hatchery hygiene

Before the start of the incubation season, theincubator room is cleaned thoroughly anddisinfected, and the heating and humidify-ing equipment is checked. The incubationboxes are washed, disinfected and left in thesun to be dried and irradiated. The supply ofvermiculite is also checked.

The boxes used for the collection of theeggs from the nests are kept separately. Theyare re-used for the same purpose but neverenter the incubator room. On arrival at thepacking room, the eggs are rinsed under thetap in running water and may be immersedin a mild disinfectant solution (F10®, Healthand Hygiene (Pty) Ltd), before they arestacked in the box. For the day’s clutches thevermiculite is soaked in clean water. Beforeplacing it into the box the water is squeezedout that it no longer drips from the materialheld in the hand. As soon as the eggs havebeen packed in the box it is placed on theshelf in the incubator room.

People working in the cleaning and pack-ing room, the incubator room and the hatch-ing room should wear clean gumboots andclean overalls. Visitors should not be allowedinto the incubator room during the incuba-tion season.

Rearing

Farming conditions are a compromisebetween the perceived requirements of thefarmed animals and economically feasible


Fig. 3.5. Nursery basin with sloping floor and partial cover.

solutions. Constraints are not only economic– our understanding of the requirements ofcrocodiles is still very limited.

While domesticated species have beenselected and bred to adapt to certain givenconditions, animals taken from the wild aremuch less adaptable. The closer one cancater for the actual needs of the crocodiles,the more likely it is that the farming enter-prise will be successful. Hatchlings andjuvenile crocodiles not only need food,water and space, they have very stricthygiene and other needs and a range ofbehavioural requirements. Not meetingthese needs causes stress, and stress oftencauses disease and death (see pp. 46 and278).

Rearing outside

Outdoor rearing is practised in tropicalcountries, often in the proximity of wildcrocodile populations. The crocodiles arekept in relatively small concrete-lined penswith equal water and land areas and par-tially shaded. The water is usually 15–20 cmdeep, and there are sloping sides to allow the

crocodiles to climb out of the water.Additional heating may be provided via hotwater pipes which run submerged throughthe water areas of the pens (Fig. 3.6). Whilesuch a system is relatively cheap to build, ithas several serious weaknesses.

Although the additional heating may pre-vent cooling of the water during cool nights,there is no protection against overheating.When air (shade) temperatures climb above36°C, and the sun shining on to the shallowwater heats it up to a similar temperaturewhile heating the concrete floor of the peneven more – the crocodiles have no way toescape overheating. Smaller crocodiles aremore likely to suffer than larger ones, astheir smaller mass heats up more quickly.This overheating is a very serious source ofstress (see p. 278). The lack of temperaturecontrol also depresses the appetite to thepoint that crocodiles reared outdoors gener-ally do not accept dry compound feeds (pel-lets).

Hatchlings are instinctively afraid of anymovement overhead, such as birds or eventhe shadow of a passing person. While thesefrequent disturbances could be prevented bythe provision of hide boards, this is often not

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Fig. 3.6. Partially shaded outdoor crocodile rearing pen with hot water pipes for additional heating on afarm in Zimbabwe.

done, exposing the hatchlings to a constantsuccession of stressful events. On such farmsthe alarm calls of the hatchlings can be heardfrequently, indicating the degree of stresssuffered by the animals.

Further problems encountered in outdoorrearing are flies and rats attracted by left-over feed, as well as escapees, as youngcrocodiles are very good at climbing overseparating walls and fences (Fig. 3.7).

If outdoor rearing is to be attempted dur-ing the colder months, some protectionagainst excessive cold or temperature fluctu-ations may have to be provided. Possiblemeasures include:

● deeper water (>1 m), which will not cooldown as rapidly as shallow water (butwill be more expensive to change regu-larly);

● a sheltered area, e.g. under a plasticawning (Fig. 3.8);

● a few spots heated with infrared lamps,preferably under a shelter;

● an area of underfloor heating, preferablyalso under a shelter.

Protection against overheating can beafforded in outdoor pens only by the provi-sion of deep water.

Rearing indoors

Indoor rearing aims at reducing or prevent-ing temperature fluctuations, but this is doneeffectively only if the building is insulatedsufficiently – to the same standard as arefrigerator or freezer room – with a 150 mmstyrofoam layer or similar insulation. Thisinsulation will take care of overheating,while at the same time minimizing heatingcosts.

Heating of the rearing house can be pro-vided in several ways:

● heating the air – space heating;● heating the water by means of heating

pipes;● underfloor heating, electrically or via hot-

water pipes;● infrared lamps.

Space heating needs good insulation of thebuilding. The larger such a unit, the lowerthe building cost per crocodile housed.Usually the heat is provided by oil burners(Fig. 3.9) which heat water circulated to theheat exchangers. The water for the croco-diles is brought in from a borehole at ±20°Cand provides a thermogradient for the ani-mals (see p. 44). The air in such a house is


Fig. 3.7. Potential escapees lying on top of pen walls.

relatively dry, but a disadvantage may bethe fact that the floor remains cooler thanthe air and that convection from the air tothe body may be relatively inefficient, notallowing the crocodiles to reach optimalcore temperatures, even if the air is heatedto 35°C.

Underfloor heating requires less insula-tion for the building. It should not involve

the whole floor area, and the water for thecrocodiles should remain unheated as in aspace-heated house. The air in such a unitremains relatively dry. The convection fromthe floor to the body of the crocodile is veryefficient and therefore a lower temperature isrequired, maximally 33°C. The water to becirculated through the pipes can be heatedby oil, coal or heat-pump. While coal is

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Fig. 3.8. Juvenile Nile crocodiles protected against excessive cooling by a plastic tent on a farm in SouthAfrica.

Fig. 3.9. Oil burner on a crocodile farm in South Africa.

cheaper than oil, its use is more labour inten-sive. Unfortunately the heat pump system isleast efficient in winter, when it is neededmost. Electrical underfloor heating may beeconomical on small farms. Maintenance andrepairing of underfloor heating installationsmay be difficult and costly.

Heating the water by circulating hotwater in pipes is mainly used in outdoorrearing units. If used indoors, it can causevery steamy conditions. The circulatingwater is usually heated by coal (Fig. 3.10). Ifthe house is insufficiently insulated, over-heating can occur in hot summer weather.Occasionally crocodiles become trappedunder the pipes and drown.

Infrared lamps (gas or electrical) areunsuitable for space heating, as their radia-tion cannot be controlled by thermostat.However, they can be used for heating areasin outdoor pens to provide warm spots incold winter weather.

Ventilation in insulated rearing housesmay be provided through the doors only, buta more efficient system uses large extractorfans in the wall opposite the entrance doorand these are operated once or twice a day toremove the ammonia fumes produced by theurine of the crocodiles (see p. 41). Theammonia and the humidity combined have avery corrosive action on all building materi-als. Low ceilings reduce the volume of air to

be heated but also limit the volume of airavailable to the crocodiles with regard toboth the supply of oxygen and ammoniaconcentrations.

Added advantages of a well-constructedindoor rearing unit are the absence of flies andrats and the efficient prevention of escapees.

In a semi-open rearing house, lights fittedover the pens attract insects during thenight. These fall into the water and provideadded nutrition and activity for the hatch-lings (Fig. 3.11).

Environmental chambers are insulatedboxes, 2 m � 2 m or larger, which areaccessed through a lid. The sloping bottom iscovered with water, allowing the crocodileseither to rest in the shallow water or to gointo deeper water. The water is kept at aconstant temperature, and there is no ther-mogradient allowing for active thermo-regulation. Access to these chambers forfeeding, cleaning and inspection is difficult,while their construction per unit housed isno cheaper than that of a larger insulatedrearing house. High air humidity and ammo-nia levels are common problems.

Temperature

The rearing temperature for crocodiles isdictated by their physiology. Digestion,


Fig. 3.10. Partially shaded outdoor rearing pens with the coal-burning heating unit in the background, ona farm in Zimbabwe.

metabolic rate and growth are at their best ata body temperature (core temperature) of32–33°C. A temperature of 35°C and above isstressful and may be fatal, while tempera-tures below 28°C reduce the rate of digestionand assimilation, as well as the metabolicrate and growth. Any involuntary tempera-ture change causes stress and reduces theappetite, while the provision of a thermogra-dient allows the crocodiles to adjust theirbody temperature to their own needs andcomfort (voluntary temperature change) (seep. 55).

For the crocodile itself, heating and cool-ing takes place more efficiently in the wateror from the floor of the pen than from the air.In outside rearing, the infrared radiation ofthe sun is absorbed very efficiently, while thecrocodiles may be able to counteract theeffect of hot dry air to some extent by evapo-rative cooling.

Ideal temperature conditions in an indoorrearing unit are achieved by keeping the airat 33–35°C and bringing in the water, prefer-ably from a borehole, at 20–25°C. The waterwill warm up during the 24-h cycle before itis changed again but, cooled by evaporation,it will remain below 33°C.

Water is commonly heated in poorly

insulated rearing houses, where the heatfrom the air dissipates quickly through theceiling. However, there is a serious dangeron hot sunny days, when the air temperatureinside the house rises above 35°C and theheated water does not allow the crocodiles tocool down. This affects hatchlings more seri-ously than older juveniles, as the smallerbody of the hatchlings reaches critical tem-peratures more rapidly.

Light

Although they are nocturnal animals withexcellent night vision, crocodiles cannot seein complete darkness. While they may bekept in darkness, a small, dim light sourceshould provide some residual light in therearing house.

Where rearing takes place in the open,lights over the rearing pens will attractinsects at night, which then fall into the penand provide an additional feeding stimu-lus. However, sunlight also containsinfrared radiation, which can cause over-heating if the animals are not providedwith sufficient shaded areas (Fig. 3.12) (seealso p. 108).

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Fig. 3.11. Lamps over the pens in a semi-open rearing house in South Africa attract insects, which pro-vide added nightly activity for the hatchlings.

Feeding

While crocodiles, even small ones, need atleast 36 h after a meal to empty their stom-ach, it is common practice to feed hatchlingsand juveniles daily. If some of the animalshave not been able to get at the feed on oneday, due to the high stocking density, theyshould then be able to feed on the secondday. On many farms no food is given overthe weekend, which allows all the crocodilesto empty their stomach completely.

As the crocodiles feed off the floor, the feedshould be offered after the pen has beencleaned and the water has been changed. Onlyas much feed should be given as the crocodileswill consume within 30 min. Leftover feedonly contaminates the water and encouragesbacterial growth. Throwing the feed into thewater increases the rate of contamination.Crocodiles can also be taught to take the pel-lets out of feed troughs (Fig. 3.13).

Some crocodilian species, notablyAmerican alligators, reduce their feed intakein autumn if they are kept in natural day-light, even if heating is provided. Thisshould not occur if they are kept in a closedenvironment with artificial lighting. How-ever, crocodiles reared outside should not be

fed during cool winter weather, when theycannot maintain their body temperatureabove 25°C (see p. 111).

Cleaning and disinfection

Crocodile faeces are rich in bacteria andfungi, which continue to multiply in thenutrient-rich, moist and warm environmentof the rearing pens. Not only is it necessaryto change the water every 24 h, but the cont-aminated surfaces must be washed as well.High-pressure hosing is more effective thanusing normal pressure (Fig. 3.14). The thinlayer of fat, which covers all surfaces fromleached-out and undigested fat, has to beremoved from time to time by using a deter-gent. Only after the removal of this fat layeris it possible to disinfect the rearing peneffectively.

Under normal circumstances it is recom-mended that the change of water and hosingdown of the pen be carried out daily, whiledetergent and disinfectant are used once aweek. However, during a disease outbreakdisinfection should also take place every day.

If there has been an excessive build-up offat, it may be necessary to spray the deter-


Fig. 3.12. Nile crocodile hatchlings competing for shade in the early days of crocodile farming.

gent on to the crocodiles as well, and to hosethem down afterwards, and the disinfectantshould also be sprayed over the crocodiles toremove excess bacteria from their skin. Forthis purpose a quaternary ammonium orcombination disinfectant should be used, e.g.F10® (Health and Hygiene (Pty) Ltd).

Prevention of piling

Frightened hatchlings and juvenile croco-diles tend to seek refuge by piling on top ofeach other in a corner of the pen (Fig. 3.15).This can lead to suffocation and death, butalso to scratches on the belly skin, which

114 Chapter 3

Fig. 3.13. Presenting pellets in feed troughs reduces wasting and contamination.

Fig. 3.14. High-pressure hosing removes faeces and wasted feed very efficiently (photo publishedpreviously in the OIE Review (Huchzermeyer, 2002)).

might become infected and, in the end, maycause scars to remain. It also causes unneces-sary stress (see p. 278). While rounding thecorners of the pens may somewhat alleviatethe problem, the solution lies in preventingfrightening events and in providing ade-quate cover.

Frightening events can be avoided bybeing quiet around the crocodiles and byavoiding any sudden and rash movements.One should also allow the crocodiles tobecome used to human presence, andworkers should talk quietly to the

crocodiles while cleaning the pens andfeeding them. A certain level of backgroundnoise, e.g. from a radio, also appears tohave a quietening effect on the crocodiles.

Adequate cover can be provided by hideboards which are distributed evenly in thepen (Fig. 3.16). This is of particular impor-tance for the behavioural comfort of thehatchlings, but juveniles also make use ofthem, even to age of slaughter. The hideboards should be provided indoors as wellas in outside pens.


Fig. 3.15. Frightened Nile crocodile hatchlings piling in their pen.

Fig. 3.16. Hide board providing cover to frightened Nile crocodile hatchlings and preventing piling.

Handling of hatchlings

All handling should be done as quietly aspossible. Never chase a particular hatchlingthrough the whole pen. It can be grabbedfrom a distance by using snake tongs (seealso p. 59 and Fig. 2.6). Once caught, thehatchling is held in one hand around theneck and upper part of the body with thumband forefinger securing the mandibles andpreventing sideways movements by thehead (Fig. 3.17).

Handling of yearlings and older juveniles

Yearlings are caught with two hands, onehand securing the head, as with hatchlings,while the other hand holds the tail to preventany wriggling (Fig. 3.18). Older juvenileshave to be approached much more carefully,

as they can inflict quite severe bites.Sometimes they can be distracted by pullingthem by their tail, although sometimes thiswill already elicit a snapping response. It isbest to cover their head with a towel or sack,before trying to grab head, body and tail (seealso p. 57).

Stocking density

The stocking density should allow all ani-mals free access simultaneously to the differ-ent components of the pen, land area andwater, or warm and cool areas, as well as tothe food. It depends also on the aggressive-ness of the particular species, which may fur-ther increase with age. Ideally, a pen shouldbe stocked with the number of hatchlingsthat could still be accommodated as pre-slaughter juveniles. However, a low stocking

116 Chapter 3

Fig. 3.17. Holding a hatchling in one hand.

density is costly because of the demand oncostly space, while a high stocking densitycauses stress, fighting and injuries (seep. 278).

While in the past authors tended to rec-ommend small groups (Pooley, 1969), experi-ence with Nile crocodiles, at least, has shownthat there need not be a limit to group size,as long as each individual animal has therequired space (Fig. 3.19).

As stocking density is a function of thesize of the animals, and since size is relatedto mass, it is probably best to relate stockingdensity to the average mass of the crocodilesin the pen. For mass–length relationships seeTables 1.4–1.6 and 2.10.

If p is the required pen size in m2, n thenumber of crocodiles in the pen and m theaverage mass of a crocodile in the pen, theformula p = (n�m)/5 should apply. Thedivisor 5 may be species specific, and in thiscase applies to the gregarious Nile crocodile.A different divisor may have to be found forother species.

Even the group with the lowest density ofAmerican alligators in the trial reported byElsey et al. (1990a) exceeded this recom-mended stocking density. However, theseauthors showed that growth performancewas inversely related to stocking density, the

lowest-density group having the fastestgrowth rate. Plasma corticosteroid levelsindicative of chronic stress were directlyrelated to stocking density (Elsey et al.,1990a) (see also p. 278).

Biosecurity

Biosecurity aims to protect valuable farmstock against the introduction of infectiousor contagious agents by erecting barriersbetween the animals and potential sources ofinfectious agents. This is common practice,particularly in the poultry industry.

The pathogens include both crocodile-specific and non-specific pathogens. Thecrocodile-specific agents – caiman and croco-dile pox viruses (p. 157), adenovirus (p. 160),chlamydiae (p. 167), mycoplasmas (p. 167),coccidia (p. 183), pentastomes (p. 205),roundworms (pp. 192 and 194) and trema-todes (p. 200) – are carried by other (wild)crocodiles and may be present in the waterof rivers and lakes inhabited by wild croco-diles. Pentastomes, roundworms and trema-todes require fish as intermediate hosts.

Non-specific (general) pathogens (seep. 172) are introduced either via the food, par-ticularly with the meat from farm mortalities,


Fig. 3.18. Holding a yearling with two hands to prevent wriggling.

carried by rats, flies and birds or via thewater (surface water). Others are part of thenormal intestinal flora (see p. 38).

The most important task is to keep thecrocodile-specific pathogens out of the farm,particularly the rearing section. To this endthe following measures should be consid-ered and, where possible, applied:

● only borehole, well or public watershould be used, particularly in the rearingsection;

● extreme care should be taken with theintroduction of new stock, particularly ifthe animals have originated from the wildor from farms with previous outbreaks ofdisease;

● wide separation of breeding and rearingsections on the farm with separate staffworking in each section, or at least differ-ent sets of gumboots should be worn ineach section;

● separation of incubation and rearing facil-ities for eggs and hatchlings from eggscollected in the wild from those producedon the farm from own breeding stock;

● separation of water and drainage systemsfor the different groups (pens) in the rear-ing section;

● use of separate brooms for the cleaning ofthe different pens; and

● disinfection of gumboots before enteringany rearing pen.

The parasitic worms are kept out by notfeeding lake or river fish, or by boiling orfreezing such fish before it can be used (Fig.3.20). The impact of general pathogens canbe reduced by not feeding farm mortalities,or at least by heat sterilizing (boiling) suchmeat before feeding. Feeding pellets is muchmore hygienic and therefore preferable tofeeding fresh meat.

The use of well, borehole or public waterwill also reduce the danger of environmentalbacteria. However, the danger posed byintestinal microbes remains a cause of con-cern. Daily water change and regular clean-ing and disinfection of the pens are the onlyways to reduce this danger.

Breeding

Sustainable use, with the collection of eggsor hatchlings from the wild and the releaseback into nature of a certain percentage ofthe reared juveniles, is regarded as the farm-ing method of choice from a conservationpoint of view. There is also a certain justifica-tion for captive breeding, particularly incountries and for species where collection of

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Fig. 3.19. Large numbers of Nile crocodiles can be reared together, provided there is enough space.

eggs or hatchlings from the wild for com-mercial purposes is not permitted. This sec-tion is based mainly on farming with Nilecrocodiles in South Africa. It should beunderstood that different crocodile speciesmay have different requirements, but certainprinciples may well apply to other crocodilespecies.

Selection of group size

Most crocodiles are polygamous, with river-ine and lake species usually being more gre-garious and swamp and forest species beingmore territorial. This may affect the choice ofsize of the breeding group. Generally thereare two systems: single male units and multi-ple male units. While the males establish aterritory for their females, the females areterritorial with regard to their nesting sites.Single male units avoid fighting betweenmales, which can be a problem in multiplemale units.

The generally accepted sex ratio for Nilecrocodiles is one male to five or six or eventen females, but this might differ for differ-ent species. Experience in South Africa

shows that the best results are obtained invery large enclosures with up to 500 femalesand the requisite number of males. Thelarger the available area, the easier the intro-duction of new individuals or groups into anestablished breeding group becomes. Insmall enclosures or single male groups,severe fighting often results from attempts tointroduce a new member into the group.

Enclosure and nesting areas

The breeding enclosure should be in a quietarea and the nesting sites, in particular,should be free of any outside disturbances.Visual barriers, in the form of islands, lowwalls or clumps of dense vegetation, shouldbe provided in multiple male units, to allowthe dominant males to establish their indi-vidual territories out of sight of each other(Fig. 3.21). The larger the enclosure, the lessfighting is experienced. Walling off the nest-ing sites prevents fighting between thefemales. All nests should be on the samelevel, as those nesting sites highest abovethe water level are regarded as the mostdesirable ones (Fig. 3.21) (see also p. 54).


Fig. 3.20. Feeding freshwater lake sardines on a farm in Zimbabwe. This practice can cause severeascaridoid infestations (see p. 192).

Fighting between females that are ready tolay can cause the oviduct to rupture, withresulting peritonitis and permanent sterility(see p. 200). Basking and shaded areas shouldalso be provided for the thermal needs of thecrocodiles.

Protection from excessive temperaturevariations

Large crocodiles are less sensitive to temper-ature variations because of their large bodymass. However, they are still affectedadversely by excessive cold and heat. As thebreeding enclosures are out in the open, themost important protection against excessiveheat and cold is deep water. While someparts of the breeding ponds should be shal-low to allow partially submerged basking, alarge part of the breeding pond should be2–3 m deep. The deep water does not cooldown rapidly during a spell of cold weathernor does it heat up during prolonged hotweather.

An alternative is the provision of artificialburrows, which provide protection againstboth heat and cold. These can be provided inthe form of a 60 cm high space of sufficientarea to fit a number of crocodiles and cov-ered by a slab of concrete and a thick layer of

soil. However, they do present difficultiesfrom the point of view of maintenance andcleaning.

Additional heating can also be providedagainst winter cold by infrared lamps inparts of the basking area. The crocodilesquickly learn to make use of the heatingrather than going into the cold water. Theprovision of infrared heating is muchcheaper than heating the water.

All this applies to crocodile farms in trop-ical and subtropical climates. Crocodiles keptin colder climates need more sophisticatedprotection, from cold in particular. However,the general principles of thermoregulationand thermal requirements apply to croco-diles everywhere (see p. 44).

Selection of breeding stock

Healthy, vigorous animals should be selectedas breeding stock. Where farm-reared croco-diles are to be kept as breeders, one shouldselect the fastest growers. Breeding groupsshould be composed of animals that arecompatible in size and age.

Wild-caught breeders are usually moreterritorial and more inclined to fight thanfarm-reared stock. Although the subspeciesof the Nile crocodile have not yet been

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Fig. 3.21. Visual barriers and walled-off nesting sites in a large breeding enclosure for Nile crocodiles inSouth Africa.

defined (awaiting DNA analysis), the inter-breeding of crocodiles from different geo-graphic regions of their distribution mightnot be a good idea, as it will render theirprogeny unsuitable for release back into thewild. Escapees from farms where such inter-breeding is practised should also beregarded as a danger to the environment. Inthis light, the breeding of hybrids from twodifferent species, e.g. C. porosus and C. sia-mensis, clearly is not acceptable.

Introduction of new stock

Two dangers are associated with the intro-duction of new stock: the introduction of dis-ease and fighting. Wild-caught crocodiles cancarry crocodile-specific diseases and theirintroduction may in future endanger the rear-ing stock on the farm (see also p. 117).

Fighting results when single crocodiles orgroups are introduced into existing breedinggroups. The larger the breeding enclosure,the less is the danger of fighting. In this con-text, one should also consider that the croco-diles to be introduced are already understress from transport and translocation, andtherefore are severely disadvantaged.

If at all necessary, such an introductionshould take place outside the breeding sea-son. It is best done in combination withanother procedure in the enclosure, such asdraining the water and cleaning the pond,which will deflect the attention of the domi-nant crocodiles from the introduced ones, atleast initially.

Feeding

The breeding crocodiles are fed once a weekduring the warm months, but not at all dur-ing cold weather (May to August in SouthAfrica), as digestion and assimilation areinhibited by the cold. While some farmersbelieve that overfeeding leads to infertility,other farmers claim that this is not the case.

Generally, breeding crocodiles are fedwhole chickens or large chunks of meat withbones. Mineral and vitamin supplements canbe applied to the surface of the meat and

multivitamin preparations can also beinjected into it. Vitamin E and zinc are twosubstances that should be supplemented toboost reproductive performance (see p. 101).

Egg collection

As soon as the eggs have been laid, the nestshould be examined and the eggs be takenout. For this purpose one person armed witha wooden pole or a strong plastic pipeshould chase the female away while theother person gently removes the soil fromthe top of the nest to expose the eggs. Even ifthe eggs are not banded, the top of eachshould be marked and the egg always bepositioned in the same way it had been lyingin the nest (see also p. 103).

Although normally eggs are not bandedby the time they are laid, some embryonicdevelopment takes place in the vagina. Iflaying has been delayed, for whatever rea-son, the embryo might just be in the processof attaching to the shell by the time the egg islifted. Any turning at that stage will causethe death of the embryo (see p. 30).

If the eggs have to be transported to thefarm over long distances, they should beprotected from severe vibration as well asfrom temperature changes, particularly over-heating.

In American alligators, Chabreck (1978)found that the best incubation results wereachieved if the egg collection was delayeduntil the fourth week after lay.

Water change and cleaning

Larger volumes of water out in the open andexposed to sunshine contain bacteria andalgae, which to some extent break down theexcreta of the crocodiles and thereby keepthe water clean. A large proportion of thenitrogenous waste from the urine escapesinto the air in the form of ammonia gas;however, the solids accumulate at the bottomof the pond in the form of mud. The amountof mud accumulating at the bottom can bereduced by the addition of suitable bacterial


cultures that digest the organic constituentsof the mud.

The mud can be removed periodically, oreven more or less continuously, by drainingfrom the bottom together with partial refill-ing or topping up. A sketch of such a bottomdrain is shown in Fig. 3.22.

The whole pond should never be drainedduring the breeding season, but this maybecome necessary once or twice a year, ifbottom drainage has not been installed orhas been found to be inadequate. A largebreeding pond can also be divided into twoparts by a shallow section in between, so thatone part can be drained at a time. This willbe much less stressful for the crocodiles (Figs3.23 and 3.24).

Productivity and fertility

Well-fed crocodiles in a suitable enclosureand under optimal conditions should be ableto produce a clutch of fertile eggs per female

every year. However, this is rarely achieved.Unsuitable weather conditions, suboptimalnutrition and various stressing incidents andinteractions affect the number of nests pro-duced in the enclosure, as well as the per-centage of fertile eggs laid. Stress seriouslyreduces male sex hormone levels and thusmale fertility (Lance and Elsey, 1986) (seep. 276). This stress may be due to outsideinterference and to fighting between males,as well as to bad weather (see p. 278). Thenutrition of the breeders normally receivesthe least attention and has been poorlyresearched. Where crocodile farmingdepends on captive breeding, but also incaptive breeding programmes of highlyendangered species, the critical importanceof the well being of the breeders is usuallygreatly underestimated or even disregarded.

The nutritional and behavioural require-ments of the different crocodilian species mayvary, but a successful breeding operationdepends on meticulous attention to detail inthe fulfilment of all these requirements.

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Fig. 3.22. Sketch of a bottom drain for a breeding pond. When water is added, the overflow is takenfrom the bottom, removing the accumulated mud.

Fig. 3.23. Schematic diagram showing the division of a large breeding pond by a shallow part or wall,allowing draining and cleaning of one part, while the crocodiles can seek refuge in the submersed part.

Artificial insemination

The only published work on artificial insemi-nation was done in American alligators,where it achieved considerable improvementover very poor results in the controls(Cardeilhac et al., 1988). It was found to beimportant that insemination into bothoviducts took place not more than 5 daysprior to ovulation. Therefore it is easier touse artificial insemination in species inwhich all the females ovulate more or less atthe same time, or within a few days of eachother, as is the case with the American alliga-tor. However, the collection of semen fromkilled males cannot be regarded as a viableprocedure (Larsen et al., 1984).

Larsen et al. (1992) reported the collectionof semen from the seminal groove of livebroad-nosed caiman by aspiration in a 3 mlsyringe, and the evaluation of various semenextenders. It is unlikely that artificial insemi-nation will become a practical crocodilefarming routine in the near future.

Slaughter

Crocodiles do not grow uniformly, and con-sequently all the crocodiles on a farm do notreach slaughter size at the same time,whereas it is preferable to market skins of a

uniform size. Skinning is a highly skilled joband this skill is honed by continuous prac-tice. In addition, the transport of live croco-diles to an abattoir is not possible because ofthe pernicious effects of pre-slaughter stress(see p. 125). For these combined reasons, theslaughter facility should be erected on thefarm and the slaughter process should bespread over most of the year. Only smallcrocodile farms should consider sendingkilled crocodiles by refrigerated transport toan abattoir of a larger farm for skinning andevisceration. This latter practice is acceptableand does not affect the quality of the meat(Rickard et al., 1995).

On some crocodile farms in the past theslaughtered animals were skinned, eviscer-ated and processed in the same room and onthe same tables that were used for the cut-ting up of cadaver meat for feeding the croc-odiles. This practice renders the crocodilemeat unfit for human consumption and isutterly unacceptable.

In view of fluctuating skin prices, theadditional income derived from the meat canprovide a stable base for any crocodile farm.

The slaughter facility

Apart from the fact that the crocodiles arekilled in the pen (see p. 124), which necessi-


Fig. 3.24. Crocodiles basking in the shallow water above the dividing wall between two parts of a largebreeding pond on a farm in South Africa.

tates the location of the slaughter house on thefarm, the crocodile slaughter facility should beof the same standard as slaughter houses usedfor other domestic species.

The floor and walls should have a smoothand impermeable finish and the interior fit-tings should be made from stainless steel. Allwater used in the abattoir should be ofpotable quality and there should be chang-ing rooms and ablution and toilet facilitiesfor employees of both sexes. The workersshould be provided with clean overalls,gumboots, impermeable aprons and caps.Hand washbasins and basins for the cleaningand disinfection of knives should be withineasy reach.

The abattoir should be divided into areasof different levels of contamination (Fig.3.25). In the arrival area (A) the shot and bledcrocodiles are hosed down. Here their skincould be cleansed by scrubbing with a chlo-rine-based sanitizer (Rickard et al., 1995) orF10® (Health and Hygiene, South Africa).They could also be immersed in ice water,although there is a risk of bacterial build-upin such a bath. From here the crocodiles aremoved to the skinning area (B). After skin-ning the skins go to the skin processing area(C), where they are scraped and then saltedand stored in a refrigerated skin room (D),which is used exclusively for storing thesalted skins. The salted skins exit via anotherdoor to the grading and packing room (E).All the above rooms are part of the dirty area.

After skinning, the body is moved fromthe skinning room (B) to the eviscerationarea (F), which is semi-dirty. The viscera andother offal exit from here via the skinningand arrival rooms (B, A), while the eviscer-ated carcass is moved to the clean meat pro-cessing room (G), where the carcass is cut upinto the different portions and the portionsare packed and sealed, before they are frozenin the meat freezing room (H), dedicated toholding crocodile meat only. The packed andfrozen meat leaves this area via a separateexit (J) without having to go through thedirty areas.

Humane killing

The crocodile farming and ranching industryalready has to overcome periodic bouts ofadverse publicity aimed at the total pro-tection of the species and opposed to theidea of sustainable use. This is a very strongreason to avoid any practices in the farmingand slaughter of crocodiles that could beinterpreted as inhumane and therefore givefurther ammunition to the anti-crocodile-farming lobby.

Destruction of the brain by the use of afirearm or a captive bolt apparatus causesimmediate loss of consciousness and there-fore clearly is the most humane method ofkilling. The shock of the explosion alsocauses an immediate cessation of spinal

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Fig. 3.25. Sketch plan of a crocodile abattoir: A, arrival; B, skinning; C, skin scraping; D, skin salting andstore; E, skin grading and packaging; F, evisceration; G, meat processing and packaging; H, meat freez-ing; J, meat exit; single arrow, dirty flow; double arrow, clean flow.

cord reflexes. A crocodile killed in this waydoes not move or struggle after death.However, in a situation where the crocodileis handled before killing and therefore hasto be held, the use of a firearm with live rounds is not practicable (Hutton,1992) while the use of a captive bolt gunstill is.

Severance of the spinal cord by neck stab-bing, using a sharp chisel and a heavy ham-mer, does not cause loss of consciousness.The brain of American alligators killed bythis method remained perceptive for morethan 1 h (Warwick, 1990). To overcome thisproblem Hutton (1992) suggests pithing thebrain with a stainless steel rod immediatelyafter neck stabbing, claiming that this couldbe done within 2 min. While this may be aconsiderable improvement over neck stab-bing without pithing, the question ariseswhether such a delay is acceptable for ahumane slaughter method. Even 2 min isquite a long time for an animal being killedby a painful method.

Any handling of the crocodiles immedi-ately prior to slaughter should be avoided inany case because of the meat hygiene conse-quences of pre-slaughter stress (see below).Where handling cannot be avoided, a captivebolt gun or the captive bolt device Zilka,driven by compressed air, should be used(Campos, 2000).

Clearly the most humane and efficientmethod is the use of a silenced small-calibrefirearm (0.22 with low load) to shoot theunsuspecting crocodile in the pen at closerange. The bullet destroys the brain andlodges below it, usually in the tongue, with-out damaging the skin of the chin. The pointto aim at is the middle between the orbits andthe supertemporal fossae (Fig. 3.26) (see alsopp. 7 and 27). Since there is no struggle, theother crocodiles in the pen are not upset bythis. The subsequent removal of the killedcrocodiles and the hosing down of the blooddoes not upset or stress the remaining croco-diles either. In the end though, after repeatedkilling sessions, some crocodiles mightbecome wary and try to hide or run away andmay have to be shot from a greater distance.

Where the skulls are to be cleaned andsold to tourists, and the hole in the frontalbone of the skull is regarded as undesirable,the crocodile can also be shot from behind,destroying the brain through the occiput(Fig. 3.27).

Pre-slaughter stress

Acute stress increases the permeability of theintestinal blood capillaries and allowsintestinal bacteria to enter the bloodstream,causing a septicaemia – stress septicaemia


Fig. 3.26. The correct spot to aim at for killing a crocodile with a small-calibre firearm.

(see p. 278). Normally the immune system ofthe animal takes care of the situation afterblood corticosteroid levels have returned tonormal. However, if the animal is slaugh-tered during the acute septicaemic stage, thebacteria may have been distributed through-out the body and may remain present in themeat. No effort at implementing strictesthygiene measures during slaughter and pro-cessing will prevent this pre-slaughter conta-mination of the meat, which contributeslargely to the high incidence of salmonellaisolates from crocodile meat – three isolatesout of six crocodile tails from one farm(Madsen, 1993), 14 out of 72 carcasses(Rickard et al., 1995).

If crocodiles have to be handled at allbefore slaughter, this handling should bekept to the barest minimum. The corticos-teroid response to acute stress is delayed bya few minutes, allowing a short and rapidhandling procedure but no restraining, livetransport or similar action. This is an impor-tant additional reason for the recommenda-tion of shooting the crocodiles in the penwithout prior handling (see above).

Skinning

The skin is the major product of crocodilefarming and therefore needs particular atten-tion. Many factors can cause skin damage.Attention to detail is very important.

Bacterial degradation begins soon afterthe skin has been removed from the body. Asa first step, this danger is reduced by wash-ing and possibly disinfecting the whole croc-odile before skinning (Fig. 3.28). At the sametime, this will also reduce the danger of bac-terial contamination of the meat (Rickard etal., 1995).

The cutting lines depend on whether horn-back or belly skins are to be produced.Hornback skins are cut along the ventral mid-line and along the median aspect of the limbs(Fig. 3.29), while the cutting lines for bellyskins are on the dorso-lateral aspect, leavingtwo rows of button scales on each side of thebelly skin, and along the lateral aspect of thelimbs. On the neck, the nuchal scales are leftout and, further cranially, the cut moves alongthe dorsal midline to the occiput, then followsthe caudal edge of the skull and mandiblesand the median aspect of the mandibles to thechin (Plate 6 and Fig. 3.30).

These cuts are performed on a table andthe skin is flayed from the dorsal and lateralparts of the body, while the body is still lyingon the table. Dorsally a web of subcutaneousmuscles connects the skin with the vertebralcolumn and ribs (see p. 8). Here the skin can-not be pulled off, but the flaying knife mustbe used sparingly and never too close to theskin. Now the crocodile is hung up, headdown, to prevent contamination of the tailmeat in particular, and the skin is pulled offthe ventral aspect. Then the skin is spread

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Fig. 3.27. A shot through the occiput destroys the brain from behind.


Fig. 3.28. Washing the killed crocodiles before skinning to remove most of the faecal contamination.

Fig. 3.29. A salted hornback skin on top of a pile of skins.

out on a table with the flesh side up and theattached muscle and fatty tissue are removedby scraping (Fig. 3.31).

As soon as possible after scraping, theskin should be salted to prevent further bac-terial growth and to start the curing (dehy-drating) process. For this purpose the skin isspread out, flesh side up, on a slatted plat-form which is slightly raised off the floor. Itis covered with high-quality coarse salt toabout 50% of its own mass. In this process

the skins are placed on top of each other,separated by the layers of salt.

The skins are left in this pile for a fewdays, but not too long to avoid excessivedehydration. Then the salt is shaken off andthe skins are rolled individually and packedfor transport.

The growth of halophilic bacteria is notinhibited by the salt. If they are present, andparticularly under warm conditions, theywill attack the protein structures of the skin.

Some of these bacteria produce a red discol-oration, referred to as red heat, while thedamage caused by others only becomesapparent during the tanning process.

Evisceration

After the skin has been pulled off, the carcassremains hanging head down. The abdominal

and thoracic cavities are opened by an inci-sion in the ventral midline continuing downthe neck, the cloaca is cut loose from the sur-rounding tissue and all the viscera are pulledout in one movement.

On many farms the viscera of the slaugh-tered crocodiles are fed to the breedingstock. This solves the problem of disposaland the viscera certainly have a high nutri-tional value. However, this practice is veryquestionable from an epidemiological pointof view, as there is a distinct danger of per-petuating the presence of certain crocodile-specific infectious agents, which can becarried by apparently healthy slaughtercrocodiles.

The meat

After evisceration, the carcasses are cut intoportions as required by the market, and the portions are vacuum packed, placed intostyrofoam containers and frozen (Fig. 3.32).

Crocodile meat is white and relatively firm.The meat of the legs is tougher than that of tailand body. Its flavour lies between chicken,veal and fish. The meat yield depends on thesize of the crocodile, with larger individualsyielding a higher percentage. While there arealso sex and species differences, the overallyield of defatted and deboned body and tailmeat can be expected to be in the region of30–40%, with a dressed carcass of approxi-mately 65% of body mass (Gutiérez El-Juri,1990; Staton et al., 1990c; Cooper, 1999).

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Fig. 3.31. Scraping the remaining flesh off the skin.

Fig. 3.30. Salted belly skin of a farmed Nile crocodile.

The meat is high in protein and low incholesterol and energy. Details of its composi-tion are shown in Table 3.6. The fat content ofthe carcass varies with the energy content ofthe nutrition and with the nutritional state ofthe individual crocodile. The tail contains thelargest intermuscular fat deposits. For thecomposition of crocodile fat see Table 1.26.

Bacterial contamination of the meat isbelieved to occur during skinning, eviscera-tion and handling of the carcass, and decon-tamination of the skin before skinning isrecommended to reduce bacterial countsobtained from the meat (Rickard et al., 1995).

Practically all the bacteria isolated fromfrozen Nile crocodile tail meat samples byMadsen (1993) (Table 3.7) commonly occurin the intestinal flora of crocodiles. It is alsopossible that bacteria are liberated into theblood circulation under severe pre-slaughterstress (stress septicaemia) (see pp. 228 and278). Three out of three tail meat samplesfrom one farm contained salmonellae(Madsen, 1993). Gamma irradiation of alli-gator and caiman meat at D values of 0.53 ±0.02 kGy and 0.37 ± 0.01 kGy, respectively,eliminated salmonellae and Staphylococcusaureus (Thayer et al., 1997).


Fig. 3.32. Vacuum-packed portions of crocodile meat frozen in styrofoam containers and ready forshipping.

Table 3.6. Composition of crocodile meat, means of different cuts.

AlligatorCrocodylus porosus mississippiensis Crocodylus porosus,

(Mitchell et al., (Debyser and Zwart, Crocodylus johnsoniComponent 1995) 1991) (Mitchell et al., 1995)

Moisture (g 100 g�1) 75.5 65.7 75.9Protein (g 100 g�1) 21.4 29.1 21.1Fat (g 100 g�1) 2.1 2.9 1.9Ash (g 100 g�1) 0.96 1.5 0.95Cholesterol (mg 100 g�1) 89.9 91.1Energy (kJ 100 g�1) 599 438

Human health risks

The human health risks of crocodile meathave been reviewed by Huchzermeyer (1997)and Millan et al. (1997b). The rate of contami-nation of crocodile meat with salmonellae (p.164) depends on housing, feed, slaughtertechniques and the hygiene practices underwhich crocodiles are reared. While chlamy-dial infections (p. 167) are common on somecrocodile farms in southern Africa, it isunclear whether the agent involved in thesecases can infect people, and no human casesof chlamydial infection originating from croc-odile meat or from contact with infected croc-odiles have been reported. Mycobacteriosis(p. 170) is very rare in crocodiles, and neitherMycobacterium tuberculosis nor M. bovis arebelieved to be able to infect crocodilesbecause of the low body temperature of thesereptiles (Huchzermeyer and Huchzermeyer,2000). Tapeworm cysts (sparganosis) havebeen found in crocodile meat in a fewinstances only (see p. 203). Trichinellosis (p.197) has been found in crocodile meat pro-duced by several farms in Zimbabwe, and the

parasite was proven to be infective to domes-tic pigs (Mukaratirwa and Foggin, 1999).However, the parasite is killed by freezingand only frozen crocodile meat is exported.

The meat of wild harvested crocodilesmay contain residues of heavy metals (p.221) and polychlorinated hydrocarbons (p.223), unlikely to be present in the meat offarmed or ranched crocodiles. However,the latter may accumulate antibioticresidues from farm animals, particularlypigs and poultry, fed to them (see p. 91).This potential problem is in urgent need ofinvestigation, if crocodile meat is to main-tain its image of being a high-qualityproduct.

Meat from healthy and hygienicallyreared and slaughtered crocodiles should beregarded as safe for human consumption.

Crocodiles in the bush meat trade in Westand Central Africa

Wild-caught O. tetraspis play an importantrole in the bush meat trade in several Westand Central African countries. This is due tothe ease with which they can be caught andkept alive until they arrive at the market,thereby providing a source of fresh meat.Conditions are inhumane, with the crocodilesremaining muzzled and tied up from captureto slaughter, and unhygienic as well. Stresssepticaemia (see p. 228) kills some of the croc-odiles before arrival at the market (Fig. 3.33),and large-scale muscular degeneration (Fig.3.34) occurs due to the long period ofrestraint from capture to slaughter (Figs 1.4and 3.35).

In the Congo Republic the crocodiles are cutup, sold and eaten with the skin (Figs 3.36 and3.37), while in other countries the skins areused for the manufacture of handbags fortourists (Brazaitis, 1987; Huchzermeyer andAgnagna, 1994; Huchzermeyer, 1998c). There isalso the question of sustainability of this trade.While the swamp forests of the Congo Basindo not produce any usable timber and do notlend themselves to transformation to agricul-ture, the dwarf crocodiles inhabit only a nar-row margin around the swamp forests (Rileyand Huchzermeyer, 1999). This places severe

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Table 3.7. Bacteria isolated from frozen crocodilemeat, nine tails from two farms in Zimbabwe(Madsen, 1993).

Genus Species

Acinetobacter wolffiAlcaligenes denitrificansBacillus lentusEnterobacter agglomeransFlavobacterium breveF. indologenesMicrococcus kristinaeM. luteusM. nishinomiyaensisM. roseusM. sedentariusMoraxella sp.Pseudomonas acidovoransP. maltophilaSalmonella serov.Staphylococcus capitisS. epidermidisS. hominisS. saprophyticusStreptococcus faeciumS. equisimilis

limits on available habitat and also makes theexisting populations accessible to hunters.

Medicinal use of crocodiles andsuperstitions

Cultural beliefs of the magic properties ofcrocodiles may be at the root of some of the

medicinal uses of crocodile organs or tissues.The uses and beliefs are enumerated hereuncritically and without any claim of com-pleteness.

Fat

In several cultures crocodile fat is appliedexternally to treat skin ulcers and burns, but


Fig. 3.33. Stomach and intestine of an African dwarf crocodile which died from enteritis and stress septi-caemia before slaughter.

Fig. 3.34. Muscle degeneration in an African dwarf crocodile slaughtered at a market in Brazzaville.

also to treat painful joints. Internally it istaken as treatment for respiratory ailments,particularly asthma (Ross, 1992).

Meat

Regular consumption of crocodile (caiman)meat is said to promote the regrowth of hairin men suffering from male-pattern baldness(Wycombe, 1992). However, the abundant

hair growth seen in many South Americantribes may be due more to genetic than nutri-tional causes.

Bile and penises

Dried crocodile gall bladders with the bileand dried crocodile penises are sometimescollected and bought up for the Chinesemarket.

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Fig. 3.35. Live African dwarf crocodiles arrive at the market in Imfondo, Congo Republic.

Fig. 3.36. African dwarf crocodile about to be slaughtered at a bush meat market in the Congo Republic.Note pieces of crocodile meat with skin lying on the table.

Spinal cord

In the Congo Republic it is believed that thepigmented spinal cord (the black worm) mustbe removed from a slaughtered crocodile,because when left it renders the meat unpalat-able. In fact, its removal can be witnessed rou-tinely on markets where crocodiles areslaughtered. After having been severed closeto the head it is pulled out cranially while thecrocodile’s back is tapped lightly with theback of the machete. A beneficial side-effect ofthis procedure is the immediate cessation ofreflex movements (see also p. 80).

Brain

In South Africa crocodile brain is regarded ashighly toxic in some rural cultures, and brainhas been said to have been given to intendedmurder victims.

A few hints for cooking crocodile meat

The unique but delicate flavour of crocodilemeat should be complemented and enhancedbut not drowned. Therefore it is important tokeep recipes simple. Tail and body meat canbe roasted, fried, grilled or deep fried, whilethe legs and some of the body parts are best

stewed, as is done in West Africa. For frying,use butter or olive oil and do not overcook.Preferably do not cook the meat in the gravy,but rather prepare the gravy separately andpour it over the meat when serving.Basically, prepare crocodile meat like anyother white meat (Page, 1996).

Crocodiles in Zoos and PrivateCollections

While zoos generally subscribe to the princi-ples of conservation and claim to play a rolein the survival of endangered species, thereare few zoos where these principles areapplied to the housing and care of their croco-diles.

Keeping crocodiles in zoos or private col-lections is subject to the same principles askeeping them on farms, with the differencethat the farming of crocodiles is ruled moreby strict economic considerations and less byaesthetic ones. In all cases, the welfare of theindividual animal should be of prime impor-tance. The CITES permit entrusts the animal’slife to the owner’s care. By providing a stress-free environment and by catering for all itsother needs, one can ensure that the animalwill stay alive for its normal life span and


Fig. 3.37. African dwarf crocodile cut into portions for sale.

possibly also reproduce, thereby actively con-tributing to the conservation of the species.

Thermal requirements

While crocodiles, particularly larger speci-mens, apparently can tolerate prolongedexposure to low temperatures, such expo-sure causes considerable stress and affectsthe immune system as well as metabolism.Tropical crocodiles are more cold-sensitivethan subtropical ones. Even in winter, thelatter must be allowed to achieve a core tem-perature of 32°C at least once a day.

A natural thermogradient, consisting ofsun and shade, warm shallow and cool deepwater, can be provided to crocodiles that arekept outdoors. Indoors there should be athermogradient between heated and non-heated environments. Radiation or under-floor heating provides the upper end of thegradient, while cooler air and cooler water(never below 20°C) constitute the lower end(see also pp. 44 and 111).

Overheating is even more stressful thanexposure to low temperatures. Althoughcrocodiles are tropical or subtropicalanimals, they have to be able to maintain acore temperature of not more than 34°C evenif the air temperature in the shade goesabove 40°C. In nature they achieve this bymaking use of deep water or of burrows. Toa limited extend they can also make use ofevaporative cooling, particularly by gaping.Prolonged exposure to excessive heat causesthe immune system to fail and encouragesthe establishment of bacterial and fungalinfections, often of faecal origin, which leadto the death of the animal 4–10 weeks later(see also p. 228).

It should be noted here that hatchlingsand small juvenile crocodiles are moreseverely affected by overheating, as theirsmall body mass heats up more quickly thanthat of larger crocodiles.

Space

Crocodiles are nocturnal animals and there-fore their activity is rarely witnessed, as for

most of the day they are seen lying still,sleeping or trying to thermoregulate. Thismay lead to the mistaken view that captivecrocodiles do not need much space.However, they do have a need to exercise, onland as well as in the water. Therefore theminimum length of an enclosure for a singlecrocodile should be equal to twice the lengthof the crocodile and its width equal to onelength of the crocodile. An enclosure for sev-eral crocodiles should be larger, although notnecessarily a multiple of the minimum for asingle crocodile. For larger groups the rulesof stocking density, formulated for the rear-ing of farm crocodiles, apply (p. 116).

The species of crocodile also needs to betaken into consideration. Gregarious species,such as the Nile crocodile, tend to be tolerantof each other and can be kept in groups,while other species prefer to inhabit a terri-tory alone or at best with one sexual partner.As a general rule, crocodile species inhabit-ing large rivers and lakes are more gregari-ous than those inhabiting forests andswamps. In all cases one should familiarizeoneself with the requirements of a particularspecies before designing the enclosure orassigning a newly acquired animal or groupto an existing exhibit.

Where larger groups are kept together inone enclosure, the space should be arrangedin such a way that a dominant animal cannotsee or survey the whole enclosure from anyone point, thus allowing other individuals tofind their own separate territories (Fig. 3.8)(see p. 119).

Different species of crocodiles shouldnever be mixed, as this may lead to stressfulsituations and fighting. It might also encour-age hybridization, which should be strictlyavoided (p. 136).

Land and water areas

The available space should be divided intoapproximately equal proportions of land andwater areas. While the land area in largeroutdoor enclosures can contain natural soiland be covered by vegetation, it is necessaryfor indoor enclosures to be covered to a largeextent by a cement floor or tiles. While

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crocodiles, with the exception of gharials,walk on land, they always slide back into thewater. This sliding over roughly finishedconcrete causes skin abrasions, particularlyunder the mandibles, the soles of all four feetand the belly, which easily become infected.It is therefore recommended to provide anextremely smoothly finished surface close tothe water, as can be achieved with a coat ofepoxy resin paint.

In outside enclosures the water is neededas part of the thermogradient. It should bedeep enough (>1.5 m) in parts to provide thetwo separate thermal environments – shal-low, warm and deep, cool water. Runningwater tends to be of even temperature andtherefore is not as suitable for outdoor enclo-sures. Indoors the water should be deepenough in part to allow submersed swim-ming, >0.60 m for adult crocodiles.

Another function of the water is theabsorption of the excreta of the crocodiles. Alarge proportion of the nitrogen in the urineis excreted in the form of ammonium car-bonate, which evaporates from the waterand can produce an unpleasant smell in anindoor exhibit. The ventilation necessary toremove this smell may adversely affect thethermal environment, particularly where

space heating is used to provide the neces-sary warmth. As ammonia is heavier thanair, it should be extracted close to theground and not through the ceiling. On theother hand, the advantage of this evapora-tion is that less of the nitrogenous wasteremains in the water. In a large volume ofwater and in the presence of sufficient light,algae and aquatic bacteria can dealefficiently with the remaining dissolvedwastes, as long as the sludge is removedregularly from the bottom (p. 121). Smallervolumes of water may have to be filteredcontinuously or changed regularly.

Cover

Where crocodiles are exposed to direct sun-light, a shaded area is necessary for them aspart of the thermogradient, just as much as abasking area. In addition, one has to considerthe fact that hatchlings and juvenile croco-diles are afraid of open skies and seek someform of cover for protection when alarmed.This cover can be provided easily by orna-mental plants with large leaves, which canbe arranged in a way that the crocodilesunder cover remain visible to the visitor,


Fig. 3.38. Ample space, division of territories and pleasing aesthetics at an indoor Nile crocodile exhibitin France.

while feeling protected from any possiblethreats from above. Crocodiles have this fearof the open both indoors and outdoors (p.114). The stress of not being able to seekcover may lead to immune failure, infectionsand deaths (pp. 228 and 278).

Feeding

Hatchlings, and possibly juveniles as well,should be fed boiled minced meat or fishwith added minerals and vitamins (seep. 99). Meat, ox heart and liver lack calciumand phosphorus, and crocodiles fed exclu-sively on them develop mineral shortagesand bone diseases, such as osteomalacia andosteoporosis (p. 211).

Feeding live food may stimulate theappetite, particularly of newly housed, dis-oriented hatchlings, but may be objection-able on ethical and aesthetical grounds.Small tropical fish (guppies) or culturedinsects (crickets and cockroaches) are suit-able as starters for hatchlings.

Feeding should take place at a time of theday when the crocodiles have attained theiroptimal core temperature – not early in themorning after a cold night. The inert feedshould always be offered on land so as not tosoil the water, and unused feed should beremoved from the pen, after the crocodileshave all eaten.

Breeding, hybridization

Where possible, breeding should be allowedor attempted, particularly in the rarer species.This entails the provision of a suitable nestingarea, either with deep sand for hole nesters orwith sufficient leaves or other substrate formound nesters. While many species usesunny places for nesting, the forest speciesgenerally build their nests in the shade.

In single-pair enclosures it is possible toallow natural incubation, climatic conditionspermitting, and even natural rearing, whileunder other conditions the eggs should beremoved from the nest as soon after lay aspossible and incubated artificially. For detailsof artificial incubation see p. 102.

Hybridization, the interbreeding of twodifferent species, happens quite easily incrocodiles but does not serve any purpose atall and should be avoided at all cost, as itruns against the principles of conservation.For this reason sexually mature crocodiles ofdifferent species should not be kept togetherin the same enclosure.

Protection of visitors

All crocodiles are dangerous and visitors canbehave stupidly. Such behaviour is basedpartially on ignorance and partially on ageneral feeling of safety in a civilized societyand environment. It is motivated by wantingto interact with the animal, which is seenlying immobile in its pen.

In the city-dweller’s mind actual dangersare relegated to entertainment and witnessedonly on television and in videos. They do nothappen in real life. A basking crocodile mayappear absolutely harmless and may temptthe visitor somehow to interact with it.Visitors also like to hold up their children togive them a better view of an animal lyingdirectly below. Rarely do they realize howfast and how high a crocodile can jump.These are possibilities that have to be takeninto account in the design of a crocodileenclosure, even in private collections towhich visitors have access only occasionally.

Animal Welfare

Climatic adaptability

As a rule of thumb, species with a wide geo-graphic distribution show a higher degree ofadaptability than those with a very limitedrange. The actual conditions in their naturalhabitat, and particularly the components ofthe thermogradient within it, will dictate theconditions under which the crocodiles willthrive in captivity. Mere survival is a poormeasurement of adaptation and well-being,as large crocodiles may take years to die aslow death of stress, malnutrition and inci-dental infections. The one point that cannotbe overstated is that the thermal require-

136 Chapter 3

ments are absolutely central to the welfare ofall crocodiles.

Behavioural requirements

The need for crocodiles to be able to ther-moregulate has been explained above (seealso p. 44). Young crocodiles want to be ableto seek visual shelter against any perceivedthreat from above (see p. 114). The require-ments for space and territory vary with ageand species. This not only affects group sizeand stocking density, but also, in breedingcolonies, the provision of adequate territoriesand nesting sites (see p. 119).

Crocodiles are stimulated to feed whenthey see other crocodiles feeding. In a farmsituation this means that all crocodiles in apen should be able to feed simultaneously.Weaker animals being bullied away from thefeed by stronger animals may later not wantto go back to the feed and eat what has beenleft over.

Farming conditions

On the farm it is in the owner’s interest tohave well-nourished and stress-free croco-diles, as many disease outbreaks are trig-gered by stress. Well cared for crocodiles aremost likely to perform to the farmer’s expec-tations.

Overcrowding, handling and sorting arecommon causes of stress (see p. 278).Handling should be kept to a minimum andshould be done as quietly as possible.Hatchlings, in particular, are afraid of beingapproached too closely. If they have to becaught, it is best done from a distance with apair of snake tongs (see p. 59).

Insufficient heating and overheating bothare important stressors. At all times the croc-odiles should be able to thermoregulate andkeep their body temperature close to the pre-ferred optimum of 32–33°C.

During egg collection the female guard-ing the nest can best be driven off with along piece of plastic piping (heavy gauge,5 cm diameter, ±3 m long). The sound of theimpact scares the female away when hit with

this pipe rather than any pain that couldpossibly be caused by such a light instru-ment (see p. 103).

Transport

Before transport, crocodiles have to be cap-tured and restrained, either physically orchemically. The details of these actions havebeen discussed in Chapter 2. Transport andall handling are very stressful and thereforeshould be carried out as quietly, efficientlyand speedily as possible.

The mouth should be taped shut, leavingthe nostrils clear, and care should be takenthat the nostrils remain clear as long as theanimal is restrained. The eyes should be cov-ered with cotton gauze swabs and also tapedclosed to avoid any visual disturbance of therestrained crocodile (Blake, 1993). Forcingthe eyes closed also has a quietening effecton the animal and prevents unnecessarystruggling.

Crocodiles should always be held andtransported in a belly-down position. Whilethey are in a belly-up position the strongrighting reflex will induce them to strain andstruggle. When moving and rolling a largecrocodile, the legs should not be used as han-dles, as they can easily be dislocated.

While being restrained, and particularlyduring transport, the crocodiles cannot ther-moregulate. Overheating can occur whenthey are left exposed to the sun, and exces-sive cooling can occur through the wind chillfactor if they are moved on an open vehicle,particularly in cold weather. If there is a dan-ger of overheating, wetting the crocodilesmay allow them to cool down by evapora-tion.

Transport stress, like any other severestress, reduces the resistance of the croco-diles against infections, and consequentlystress septicaemia always occurs (see p. 228).If the crocodile is transported under coldconditions, e.g. in winter, and after arrival isunable to reach an optimal body tempera-ture, it will not be able to fight off this septi-caemia. This is the most common cause ofpost-transport mortality in larger crocodilesafter transport in winter conditions.


Transport stress also often causes the ani-mals to stop eating. They then fall into hypo-glycaemia, which further suppresses theappetite. Such crocodiles may never starteating again (see p. 282). Stress hypogly-caemia can be prevented by dosing theimmobilized crocodiles with a sugar solutionby stomach tube before the actual transportbegins (Fig. 2.32) (personal communication,P. Watson, Maidstone, 1999).

Painful procedures

The ability to feel pain has an importantdefence function: it induces an animal toavoid pain and injuries and therefore main-tain its bodily integrity. Crocodiles havesmall brains and therefore some of the brainfunctions of mammals are delegated to reflexcentres in the spinal cord, but this does notmean that crocodiles cannot feel pain. Thereis therefore no excuse for not using anaesthe-sia for potentially painful procedures.

It should be noted that chemical immobi-lization has no anaesthetic effect. Underchemical restraint the animal remains fullyconscious of its surroundings and fully capa-ble of feeling pain. Details of anaesthesiahave been discussed in Chapter 2.

Humane slaughter

Where we take it upon ourselves to keepcrocodiles in captivity and to use (farm)

them for our own profit, we are under amoral obligation to do this in the mosthumane and enlightened way possible.Obviously, slaughter is one of the mostimportant aspects in this context. This matterhas already been dealt with in Chapter 2 andabove, but some aspects need further discus-sion.

The slaughter process potentially con-sists of two separate components, the cap-ture, restraint and transport of the animalto be slaughtered and the actual killingitself. The capture, restraint, handling andtransport of the animal to the slaughterplant cause intense fear and a high level ofstress. The effect of the stress-induced sep-ticaemia and its effect on meat hygiene andmeat quality have been explained in detailabove. From this it becomes clear that pre-slaughter handling should be kept to thebarest minimum, if it cannot be avoidedaltogether.

The only acceptable methods of killingare those that cause an immediate cessationof brain functions, ideally by the destructionof the brain. Shooting the unsuspecting croc-odile in its pen with a small-calibre fire arminto the brain is by far the best and mosthumane method. Where the animal has to behandled before slaughter, captive bolt orcompressed air devices are the next bestchoices. Neck stabbing, particularly without,but also even with, subsequent pithing of thebrain, is clearly inhumane and should not beused at all.

138 Chapter 3

Diseases of the Egg

Without going into any detailed and elabo-rate definition of disease, this chapter dealswith any defect, fault or infection that couldcause an embryo not to develop or to die.

Shell defects

The shell protects the embryo against physi-cal damage, but during embryonic develop-ment gas and water exchange also have totake place through the shell. The porosity ofthe shell determines the efficiency of thisexchange. Wink et al. (1990) found Americanalligator eggs with early embryonic mortal-ity to have a lower degree of shell porosityand the existent pores plugged with undeter-mined material when compared with theshells of eggs with normal embryonic devel-opment. The same authors also found farm-produced eggs to be less porous and oflower hatchability than eggs collected fromthe wild.

Hibberd (1996) reported the followingshell defects in Crocodylus porosus eggs: softshells, partial shell formation, completeabsence of the shell with only the membranebeing present, additional calcareous protru-sions on the external surface of the shell(pimpling), under- or oversized eggs and

eggs of deformed shape with incompletesealing. A low level of calcium in the rationof the breeding females was believed to bethe cause of these shell defects, and the sup-plementation of the pre-breeding ration withcalcium almost eliminated their incidence inthe subsequent breeding season.

Eggs incubated in a very moist environ-ment tend to absorb excessive amounts ofmoisture, which leads to a build-up of inter-nal pressure and the eventual cracking of theshell, with typically multiple, parallel, longi-tudinal cracks of the shell, but leaving themembrane intact (Fig. 4.1).

Early embryonic deaths

Early embryonic deaths in farm-bredAmerican alligator eggs were found to belinked to, and probably caused by, low shellporosity, thought to interfere with gasexchange (Wink et al., 1990) (see also above).

Early embryonic deaths can also becaused by inadvertent turning of bandedeggs during collection or inspection, whichdislodges the embryo from its attachment tothe shell and lets it sink into the yolk sac. Forthe collection of eggs from the wild, Blake(1992) recommends waiting until theembryos are at least 4 weeks old (see alsopp. 103 and 121).

Chapter 4

Diseases of Eggs and Hatchlings


Poor hatchability

Poor hatchability is the result of all thecauses of infertility and embryonic deaths.After excluding infertility and infectiouscauses, there remain incubation conditions(p. 105), the nutrition of the female croco-diles (p. 101) and possibly some genetic fac-tors relating either to a lack of adaptation toincubation conditions or to genetic defects(lethal factors).

An investigation into poor hatchabilitytherefore has to eliminate the various factorsstep by step. The seasonality of crocodilianbreeding can cause this process to be drawnout over several years. Crocodile farmersrarely submit unhatched eggs to a laboratoryfor examination. Much work remains to bedone in this field.

Infertile eggs

Infertile eggs can be recognized during incu-bation by their failure to develop banding.However, if the embryo dies before it hasattached, no banding would be visible. Onmany crocodile farms the eggs are collectedthe morning after they have been laid. Theythen show no banding and no care is takenabout keeping the egg in the same position inwhich it has been found. However, there is asuspicion that the embryo becomes sensitive

to position damage during the process ofattachment, before the first sign of bandingbecomes visible (see pp. 30, 103 and 121).

Theoretically, any egg that has been laidshould have been able to be fertilized. Inlarge multiple-female and multiple-malebreeding groups, all females should havebeen the subjects of multiple copulations. Ifall females in a single-male breeding groupwere producing infertile eggs, this wouldpoint at male sterility. However, copulationtakes place a while before ovulation. Duringthis time the sperm survives in the oviducts.If conditions in one or both oviducts are notconducive to sperm survival, fertilization ofthe ovulated eggs will not take place. Suchconditions can be created by bacterial infec-tions, either ascending from the cloaca ordescending from the infundibulum after aperitonitis, which could have been caused bytrauma (penetrating bite wound) or stress.The fighting of females for nesting sitescould be responsible for both causes ofdescending infections.

Bacterial infections of eggs and embryos

Theoretically, bacteria can infect the eggeither transovarially through an infection ofthe yolk, or after hatch, through the shell.The transovarial route can be used by veryfew bacterial species, and no cases of transo-

140 Chapter 4

Fig. 4.1. Cracked shell of a crocodile egg after excessive water absorption.

varial bacterial infection of crocodile eggshave been reported so far.

The shell and the membranes present acertain barrier to penetration by bacteria.This is further supported by an antibacterialaction of the albumen, known in bird eggsbut not yet confirmed for crocodile eggs (seep. 30). This combined action is strongenough to ward off the challenge presentedby small numbers normally present in a nat-ural incubation environment. However,slight cracks in the shell allow easy access tobacteria. Where such eggs become rotten,they can present a danger of heavy contami-nation for adjacent eggs in the nest, whichcan easily overcome the relatively weakdefences of the egg. This kind of contamina-tion is particularly important in artificialincubation, where large numbers of eggs arebeing handled.

The preventive measures are based onstrict hygiene. Only clean eggs are to be set.Washing eggs under running water preventsthe build-up of bacteria in the washing water.After washing, the eggs can be dipped in adisinfectant solution (quaternary ammoniumor F10® (Health and Hygiene, South Africa)).Cracked eggs are to be discarded and onlyclean incubation medium is to be used. A non-organic medium such as vermiculite is practi-cally sterile when unpacked. However, oneshould never attempt to sterilize it for re-use(see p. 107). The sand in the nesting sites canalso become contaminated over time, particu-larly if eggs were broken. It may thereforehave to be replaced after a few years of use.

Infected eggs may show small, brown, cir-cular lesions under the shell, on or near thechorioallantois. Schumacher and Cardeilhac(1990) isolated Enterobacter cloacae, Citrobactersp., Proteus sp. and Pseudomonas aeruginosafrom these lesions, as well as fungi (seebelow). All of these are part of the intestinalflora and point at faecal contamination as thesource of the problem (see p. 38).

Fungal infections of eggs and embryos

Fungi present in the nesting medium, on theshell or in the incubation medium can pene-trate the shell, particularly if there is a severe

challenge. Hibberd (1994) found that thepore size of C. porosus eggs was sufficient toallow hyphae and spores to pass through.She also found growth of hyphae alongminute cracks. The fungi may not kill all theaffected embryos during incubation.Consequently some infected hatchlings maydie very much later (Hibberd and Harrower,1993).

Fungi isolated from C. porosus eggs wereFusarium solani, Paecilomyces lilacinus andAspergillus sp. (Hibberd, 1994) and fromAlligator mississippiensis eggs Fusarium oxys-porum, Paeciliomyces aviotti, Penicillium fellu-canum and Aspergillus niger. However, ofthese, only Fusarium oxysporum was found toproduce lesions on the egg membrane afterinoculation of disinfected infertile eggs(Schumacher and Cardeilhac, 1990).

The danger of fungal infection is higher inmound-nesting crocodile species because ofthe plant material used in the construction ofthe nest mounds.

Protozoan infections of eggs andembryos

Coccidia were found in tissues of deadembryos of Caiman crocodilus fuscus(Villafañe et al., 1996). As certain crocodiliancoccidia have a tendency to cause general-ized infections, it is possible that in this casesome coccidia had settled in the ovary andwere transferred to the egg during ovulation(see also p. 183).

Drowning

Excessive amounts of moisture added to theincubation medium interfered with gasexchange and caused 100% mortality inalmost mature Nile crocodile embryos (ownobservations). The chorioallantois, whichdevelops inside the shell, acts as the lungs ofthe embryo (see p. 30). As the embryo grows,its demand for oxygen increases. This makesthe later stages of the embryo particularlyvulnerable. While the incubation mediumshould be moist, it should not be wet. Theincubation medium protects the eggs from

Diseases of Eggs and Hatchlings 141

temperature and humidity fluctuations, butit should not interfere with gas exchange.

Diseases of the Yolk-sac

Diseases of the yolk-sac are part of the com-plex of hatchling diseases. Here they aredealt with in a separate section as theyinclude a number of different conditions.

Yolk-sac infection

The yolk-sac of the crocodilian embryo isconnected to the intestine at the junctionbetween jejunum and ileum by the vitellineduct, which remains open for the extrusionof the non-soluble fraction of the yolk, whichis digested in the intestine (see p. 30). Thesoluble fraction of the yolk is taken up intothe blood circulation via the placenta-like tis-sue that develops on the inner surface of theyolk-sac.

A pre-hatch bacterial contamination of theegg, and the consequent infection of theembryonic membranes, can lead to a navelinfection, omphalitis, when some of theinfected membranes, together with the yolk-

sac, are drawn into the abdominal cavity justprior to hatch. From such a navel infectionthe pathogens can spread through the yolk-sac wall into the yolk. Salmonellaarizona, coliforms, Pseudomonas aeruginosaand Aeromonas hydrophila, as well as fungiincluding Fusarium sp., were isolated fromshell membranes of unhatched crocodileeggs in Zimbabwe (Foggin, 1992a).

After hatch, with the first exposure to theenvironment, the intestine is colonized bywhatever bacteria have arrived first.Potentially pathogenic bacteria can, undercertain conditions, penetrate through thepatent vitelline canal into the yolk-sac andcause its infection. As crocodile embryosdevelop at different speeds, but all hatchtogether, the navel of some of the hatchlingsmay not have healed completely at hatch,making it vulnerable to infection. If such ahatchling is placed into contaminated water,or on to a contaminated surface, a navelinfection can result, and from there the yolk-sac will become infected.

The infection of the yolk-sac and the yolktherein causes the vitelline canal to close(Fig. 4.2). This leads to the retention of theyolk-sac, and the affected hatchling does notget the nutritional boost provided by theyolk (Fig. 4.3). The bacterial degradation

142 Chapter 4

Fig. 4.2. Nile crocodile hatchling with infected yolk-sac. Note the enlargement and the coagulatedappearance of the contents due to the exudation of fibrin.

(putrefaction) of the yolk further producestoxic metabolites which are resorbed fromthe yolk-sac. The bacteria may remain alivein the yolk-sac and at a later stage some ofthese bacteria may be able to leave the yolk-sac under certain conditions and then causesepticaemia.

Omphalitis

The navel being in close contact with theyolk-sac, the infection of one invariablycauses the infection of the other. The twopossibilities of navel infection have beendiscussed above. However, a direct infectionof the open navel from a contaminated envi-ronment is the most common occurrence.The very large numbers of hatchlings han-dled on a commercial crocodile farm canlead to a rapid build-up of contamination.This calls for the strictest possible hygienicmeasures, disinfection of hands and imple-ments, and the release of the hatchlings intoa mild disinfectant (quaternary ammoniumor F10® (Health and Hygiene, South Africa))solution for the first 24 h after hatch (seep. 107).

In nature such a high build-up of contam-ination does not occur and, in addition, thehatchlings are exposed to a normal bacterialflora from the moment they are immersedinto the water of their nursery, from where

normal intestinal colonization will take placeimmediately. There is a very delicate balancebetween contamination and a normal envi-ronmental flora, which cannot be reproducedunder intensive farming conditions.

Yolk-sac retention

Inflamed yolk-sacs

Retention of the yolk-sac can be causedeither by low rearing temperatures or, morecommonly, by infection. The mechanismsinvolved in yolk-sac infection have been dis-cussed above. Infection and inflammation ofthe vitelline canal cause it to close, prevent-ing any further extrusion of yolk into theintestine for digestion. The inflammation ofthe absorptive tissue in the wall of the yolk-sac causes the exudation of fibrin, which inturn causes the contents to take on a creamyor dry, cheesy, caseous, inspissated appear-ance (see Fig. 4.2) (Jacobson, 1984; Friedland,1986; Foggin, 1992a). In such cases the yolk-sac is transformed into a typical fibriscess(Huchzermeyer and Cooper, 2000) (seep. 46). Continued inflammation and exuda-tion of fibrin may cause the yolk-sac to swellto considerable size and to rupture, withconsequent spread of the infection andinflammation to the peritoneal cavity(Friedland, 1986) (see p. 144).


Fig. 4.3. Older Nile crocodile hatchling with non-resorbed yolk-sac still attached to the intestine.

Hydropic yolk-sacs

The retention of hydropic yolk-sacs withwatery contents has been described byYoungprapakorn and Junprasert (1994). Thecause of this condition remains obscure.

Symptoms of yolk-sac retention

Retention of the yolk-sac deprives thehatchlings of essential nutrients needed for agood start. It also leaves a focus of infectioninside the body, from which bacterialmetabolites may be absorbed, leading to atoxaemia. Consequently, hatchlings withretained yolk-sacs do poorly, usually refuseto feed and become emaciated with a promi-nently swollen abdomen.

Thermal treatment

Foggin (1992a) and Youngprapakorn andJunprasert (1994) recommend keeping suchhatchlings at elevated temperatures of32–34°C, and to withhold food until theyolk-sac is resorbed. However, this treatmentpromises results only in cases where theyolk-sac has not become infected.

Surgical excision

Where the heat treatment is unsuccessful,Youngprapakorn and Junprasert (1994) rec-ommend the excision of the yolk-sac withthe following steps (quoted verbatim):

No anaesthesia is needed during a 10–20 minoperation.

1. Fix the affected hatchling on a board in thesupine position.

2. Clean thorax, abdomen and proximal hindlimbs with an antiseptic (Providine andethanol 70%).

3. Make an incision from 0.5 cm cranial to thepalpable mass along the abdominal midlineto the pubis.

4. Cut through the peritoneum to expose theyolk sac.

5. Dissect any adhesions between the yolk sacand abdominal viscera.

6. Ligate blood vessels running from theintestine to the yolk sac and cut free the yolksac.

7. Clean carefully if the yolk sac has rupturedand spilled its contents into the peritonealcavity.

8. Suture peritoneum and skin in onecontinuous suture.

9. Clean the abdominal area.

After the operation the hatchling shouldbe kept in a clean, dry and warm place on asheet of cloth and observed for any postop-erative bleeding. Also, check if defecationoccurs, which will indicate freedom fromobstructions caused by the operation. After3–4 days the hatchling is allowed to swim inclean water for a while each day, after whichthe sutures are cleaned. Once the wound hashealed completely, the hatchling can bereturned to the rearing pond. The authorsreport a success rate of 77%.

Rupture of the yolk-sac

Continued inflammation of the yolk-sac withexudation of fibrin can cause the yolk-sac toswell to such a size that it finally ruptures(Friedland, 1986) (see also p. 143). However,the fibrinous contents are no longer liquidand therefore do not spill out. Consequentlythe peritonitis caused by the rupture alsoremains localized. Affected hatchlings maycontinue to ail for a long time before dying.Because of the peritonitis and attachment toabdominal wall and intestines, surgicalremoval of the yolk-sac may not be success-ful in such cases.

Displacement of the yolk-sac

A 3-month-old hatchling Nile crocodile witha non-resorbed and semisolidified yolk-sacwas apparently stepped upon by an atten-dant and, as a consequence, suffered adiaphragmatic hernia which ruptured boththe pre-hepatic and the post-hepatic trans-verse membranes (see p. 12) and displacedthe yolk-sac into the right pleural cavity,while the fat body came to lie between theright lobe of the liver and the body wall (Fig.4.4). The case occurred at a time when therewas a high incidence of non-resorption of

144 Chapter 4

yolk-sacs on the farm (Huchzermeyer, 1993).A similar case of diaphragmatic hernia withthe yolk-sac projecting into the pleural cavityhas been reported by Youngprapakorn et al.(1994), who presumed the case to be due toincomplete closure of the transverse mem-branes.

Hatchling Diseases

Enteritis

Competitive exclusion

In a normal crocodile, even a hatchling, theintestine is protected by a normal intestinalbacterial flora (see p. 38). These bacteriaoccupy all the available attachment sites onthe inner lining of the intestine and therebyprevent pathogenic bacteria from being ableto attach. This phenomenon is known ascompetitive exclusion. In the wild, the nor-mal gut inhabitants are recruited from thenest as well as from the water in the nursery,while contamination with unwanted bacteriais kept at a low level because of the normallylow population density of crocodiles in thebreeding area.

Under the intensive production condi-tions on the farm, contamination levels are

high and necessitate hygienic measures suchas periodic cleaning and disinfection.Frequently this creates a situation whereonly one bacterial species is able to survive,or where initial colonization of the intestinetakes place only after feeding with raw meat,particularly if raw minced meat from farmmortalities is being fed, which can introducemany pathogens foreign to the normalintestinal flora.

Factors involved

The presence of such pathogenic bacteria isnecessary for an outbreak of enteritis tooccur, while the lack of a normal intestinalflora is the major predisposing factor. Inaddition, temperature stress or other stres-sors are needed to trigger the outbreak byreducing the resistance and immunity of thehatchlings. Hatchling enteritis thereforemust be regarded as a multifactorial disease(see also p. 226).

Pathophysiology

The inflammation of the intestine follows thenormal pattern of reptilian inflammationwith the exudation of fibrin. The fibrin fillsthe intestine and causes an intestinal occlu-


Fig. 4.4. Nile crocodile hatchling with diaphragmatic hernia of the yolk-sac: f, fat body; l, right liver lobe;y, yolk-sac.

sion (Figs 4.5 and 4.6). For this reason diar-rhoea is rarely seen. Sometimes sheets of fib-rinous pseudomembranes are excreted,particularly in older juveniles and if the con-dition is not so severe. Intestinal occlusionmeans that the hatchlings cannot eat anddigest any more. They lose weight andbecome emaciated with an extendedabdomen (Fig. 4.7). The diagnosis includesthe isolation of the causative bacterium andan antibiogram.

Treatment and prevention

Because of the intestinal occlusion there is noindividual treatment that could be success-ful. Antibiotic therapy based on the antibi-ogram established in the laboratory willreach those hatchlings that do not yet sufferfrom occlusion, and it will prevent thespread of the infection to other hatchlings inthe pen.

Regular (daily) water changes, as well asscrubbing and disinfection of the floor, arevery important preventive measures (seep. 113). A sealed floor surface, either epoxyresin or tiles, allows the cleaning to be moreefficient. Fat, leaching from the meat andforming a film on the surface of the water, isdeposited on the floor every time the water

is drained. Here it forms a protective layerunder which bacteria can survive ordinarycleaning and disinfection. This fat layer hasto be removed from time to time by using asuitable detergent. As the water from croco-dile farms is released back into nature, thedetergent used should be biodegradable. Theuse of probiotics and gut flora preparationsfor hatchling crocodiles has not yet beenexplored, but can be expected to be of greatbenefit.

Heat sterilizing (boiling) the minced meatgreatly reduces the challenge by food-bornepathogens (Huchzermeyer, 1991a). Feedingpelleted feeds instead of wet rations has asimilar effect. A preventive antibacterial(antibiotic) treatment regime should beavoided because of the danger of the bacteriadeveloping antibiotic resistance, as well asbecause of environmental implications as theeffluents are released back into naturalwaters (see also pp. 91 and 102).

Alligator hatchling syndrome

Alligator hatchling syndrome (AHS) hasbeen described in American alligators(Cardeilhac, 1986; Cardeilhac and Peters,1988) but is also seen in hatchlings of other

146 Chapter 4

Fig. 4.5. Intestine of a Nile crocodile hatchling filled with, and occluded by, fibrin.

crocodilian species. Under various condi-tions of stress (such as cold, overheating,overcrowding, handling and disturbance)opportunistic, normally present, but non-invasive bacteria invade the blood circula-tion and various organs and seriously affectgrowth performance and survival, produc-ing a large proportion of runts. The highestincidence is seen in hatchlings under 90 daysof age, but juvenile and older crocodiles arealso susceptible to stress septicaemia(Huchzermeyer, 2001) (see also p. 228).

Virginiamycin and oxytetracycline givencontinuously for the first 90 days of life were

both found to be effective in improving theperformance and reducing the mortality ofhatchlings from hatchling alligator syn-drome (Cardeilhac, 1986; Cardeilhac andPeters, 1988). Oxytetracycline was given at adose of 300 mg kg�1 of feed. However, thecontinuous use of antibiotics creates the dan-ger of antibiotic resistance and should there-fore be avoided if at all possible. Rather, amuch more rational approach should betaken along the line of stress prevention bymanagement measures, e.g. protection of thehatchlings against temperature fluctuationsand extremes. Another approach would be


Fig. 4.6. Cross-section of an intestine with exudative enteritis and occluded by the exudate.

Fig. 4.7. Emaciation and extended abdomen in a Nile crocodile hatchling suffering from intestinal occlu-sion due to exudative enteritis.

via the suppression of stress, e.g. by the con-tinuous use of vitamin C (see p. 278).

Anorexia

Under stress-free conditions and at an opti-mal environmental temperature, crocodilehatchlings will start eating whatever isoffered, minced meat or pellets, very soonafter hatch. However, at inadequate temper-atures, or when subjected to temperaturevariations, they will not be attracted to inertfood. If they do not start feeding by the timethe yolk-sac is resorbed, or earlier if resorp-tion of the yolk is prevented by infection (seep. 142), the animals develop a hypogly-caemia which then further depresses theappetite. Although it has been speculatedthat the affected hatchlings might involun-tarily take in some of the minced meatwashed into the water, this is unlikely tohave any effect (Peucker and Mayer, 1995).The starving hatchlings become emaciated,but may take a long time to die because oftheir low metabolic requirements. They alsodevelop a hypoproteinaemia, which pro-duces the post-mortem lesions hydroperi-cardium and ascites (Matushima and Ramos,1993) (see also pp. 234 and 282).

If treated early, the condition can beturned around. The treatment consists offorce-feeding with a nutrient-rich liquid (amix of equal parts of milk and egg yolk withsome sugar), 1 ml per animal daily for 3 days(my own formula), injecting the hatchlingswith glucose solution and possibly also witha multivitamin preparation (Peucker andMayer, 1995), or the administration of a sin-gle dose of metronidazole (Flagyl®),125–250 mg kg�1 (Thurman, 1990).

Prevention is more likely to be successful.For this the importance of a stress-free rear-ing environment and adequate temperaturecontrol must be emphasized again andagain. The appetite can be stimulated by thepresentation of live food, such as bloodworms spread over the mince or live fish(guppies) (Peucker and Mayer, 1995). Suchlive food would also serve as a source of nor-mal intestinal bacteria needed for the pre-vention of enteritis (see p. 145). In an

open-air facility, or one with open windows,an electric light suspended high above eachrearing pen will attract flying insects at nightwhich, when falling down, are caught by thehatchlings even before they hit the water (seep. 109).

Osteomalacia

If hatchlings are fed mince without bone, e.g.minced meat of large animals, and particu-larly liver and heart, they develop a calciumand phosphorus deficiency which preventsthe hardening of the growing bones.Affected hatchlings remain able to movefreely in the water, but have difficulty tomove on land and eventually will be unableto come out of the water. Contraction of thelong muscles of the back causes the vertebralcolumn to become deformed. The upper jawbecomes flexible and can be bent upwards(‘rubber jaws’) and the teeth becomediaphanous, like shards of glass (‘glassyteeth’) (Huchzermeyer, 1986). The treatmentconsists in the supplementation of the rationwith calcium and phosphorus in the form ofbone meal or calcium diphosphate, or feed-ing mince of whole small animals (poultry)minced with the bones. However, the defor-mities of the vertebral column will remain(Huchzermeyer, 1986). For a more detaileddescription of this condition and discussionof its causes see Chapter 6.

Congenital Malformations

Congenital malformations are caused fromtime to time by mishap when somethinggoes wrong in one or other of the develop-mental processes. Such a mishap will cause asingle case. Ferguson (1989) found anincreased incidence of malformations inhatchlings from very young and very oldfemales.

If there is an increased incidence of anyparticular type of malformation, one willhave to consider genetic causes, malnutritionof the parents or faulty incubation. Mutatedgenes may be recessive and remain inappar-ent until both parents in a mating carry the

148 Chapter 4

same mutated gene. Therefore one wouldexpect a low incidence of such cases butrepeatedly, year after year, and limited to oneor two clutches. A ‘blind’ gene has been sus-pected to occur in natural gharial popula-tions in Nepal (Singh and Bustard, 1982).

Malnutrition of the parents would affectthe majority of the hatchlings, and the lack ofcertain vitamins is also suspected to play arole in the causation of deformities in croco-dilian embryos. The effect of malnutrition onthe incidence of shell defects has been dealtwith above.

Incubation errors may happen only onceduring an incubation period and may affectmany clutches at different stages of incuba-tion in the same incubator in different ways,depending on the stage of incubation, thusproducing a range of malformations in dif-ferent clutches for one incubation season.Continuous incubation at the limits of theviable range of incubation temperatures (29or 34°C) has been reported to produce a highincidence of malformations in American alli-gator embryos (Ferguson, 1989). Webb andManolis (1998) state that high-temperatureincubation (35°C), particularly in the earlystages, causes various spine abnormalities,strongly curled tails, skull deformities byinducing premature ossification and alsoprotruding lower jaws in C. porosus andCrocodylus johnsoni hatchlings.

Many congenital defects are lethal,killing the embryo or the hatchling shortly

before or after hatch. Where hatchlingswith defects survive, particularly in nature,and are found later, their defects may beconfounded with healed injuries. From apractical point of view, the details of con-genital malformations are of lesser impor-tance and more of curiosity value.However, the attention of the reader isdirected to the excellent photography ofcongenital malformations in the book byYoungprapakorn et al. (1994).

Axial and tail deformities

Many different deformities of the vertebralcolumn have been reported from differentcrocodilian species, and they affect differentparts of the spine. Necks bent sideways havebeen reported from gharial hatchlings (Singhand Bustard, 1982). Scoliosis and kyphoscol-iosis (humpback formation) of the spine hasbeen reported by Ferguson (1989) andHibberd (1996). The tail can be affected by anumber of different deformities, such as apermanent sideways bending, a sharp kink(Figs 4.8 and 4.9), curling (Fig. 4.10), shorten-ing or complete absence (Figs 4.11 and 4.12)(Kar and Bustard, 1982b; Singh and Bustard,1982; Ferguson, 1989; Youngprapakorn et al.,1994; Hibberd, 1996; Troiano and Román,1996; Webb and Manolis, 1998). Tailless croc-odiles cannot swim and will drown oncethey go into deep water.


Fig. 4.8. Kinky tail in a Nile crocodile hatchling.

150 Chapter 4

Fig. 4.9. Gharial hatchling with a kinky tail.

Fig. 4.10. Nile crocodile hatchling with a curled tail.

Fig. 4.11. Juvenile Nile crocodile born without a tail.

A spina bifida has been reported byFerguson (1989).

Polydactyly and limb duplication

Functional additional toes, some with andsome without claws, three on each front footand three and four on the hind feet, werefound in an 82-cm-long wild American alli-gator in Louisiana (Giles, 1948). A case ofnon-functional polydactyly and syndactylyhas been reported by Youngprapakorn et al.(1994). Similar cases were seen in SouthAfrica in Nile crocodile hatchlings from oneparticular farm (Figs 4.13 and 4.14) (owncases).

The duplication of limbs is one of themalformations believed to be caused byincubation at extreme temperatures(Ferguson, 1989). An adult Nile crocodilewith an additional pair of hind limbs isshown in Fig. 4.15. Youngprapakorn et al.(1994) show a hatchling with one additionallimb attached to the navel and bearing a sin-gle clawed toe, which may, however, havebeen an incomplete twin (see p. 153).

Ectromelia and micromelia

The complete absence of one foreleg, on radi-ographs even the absence of the shoulderblade, was found in two wild Crocodylus


Fig. 4.12. Tailless Osteolaemus tetraspis hatchling.

Fig. 4.13. Nile crocodile hatchling with polydactyly of both left limbs as well as left anophthalmia.

moreletii, of a total length of 37 cm and 104 cm(Rainwater et al., 1999). Youngprapakorn etal. (1994) show a hatchling with both fore-limbs missing and also mention cases withshortened legs, micromelia. Missing limbs arealso listed amongst congenital malformationsof caiman hatchlings (Troiano and Román,1996).

Malformations of head, jaws and eyes

Hall (1985) reported cases of brachycephalic(shortened) skulls and dental anomalies in

New Guinea crocodiles. The dental anom-alies included supernumerary and subnu-merary dental counts, double sets of teetherupting from a single alveolus and alveolarossification, which the author did not believeto be an expression of the ageing process.Brachycephalic skulls have also been foundin other crocodilian species: A. mississippien-sis, Crocodylus niloticus and C. porosus (Kälin,1936). Unilateral anophthalmia, monoph-thalmia, causes an asymmetric developmentof the skull (Youngprapakorn et al., 1994).Bumps, tubercles, on top of the skull, asshown by Youngprapakorn et al. (1994), are

152 Chapter 4

Fig. 4.14. Polydactyly and syndactyly in a Nile crocodile hatchling.

Fig. 4.15. Adult Nile crocodile with an additional pair of hind limbs attached to its back.

believed to be caused by premature ossifica-tion of the skull in hatchlings incubated attoo high a temperature (Webb and Manolis,1998). Monorhiny, the formation of a singlenasal passage, was reported by Ferguson(1989).

The lower jaws can either be protrudingor shortened or missing completely, agnathia(Ferguson, 1989; Youngprapakorn et al., 1994;Hibberd, 1996). Protruding lower jaws com-monly occur in C. johnsoni hatchlings and arebelieved to be caused by high-temperatureincubation (Webb and Manolis, 1998). Aslightly protruding upper jaw causes the twolarge incisor teeth of the short lower jaw topenetrate through the apical maxilla, produc-ing ‘false nostrils’ (see Fig. 1.21). Sidewaysbending of the upper jaw of a monoph-thalmic gharial hatchling was reported bySingh and Bustard (1982), and upwards curv-ing of the snout in wild C. johnsoni by Webband Manolis (1983). Cleft lip, cleft palate andcleft chin are shown by Youngprapakorn et al.(1994). Sideways bending of the lower jaws(Fig. 4.16) may also be caused by injury laterin life (see also p. 95).

Reported malformations of the braininclude hydrocephalus and meningo-ence-phalocele (Ferguson, 1989; Youngprapakornet al., 1994; Hibberd, 1996; Webb and Manolis,1998). Malformed eyes can be too small

(microphthalmia), completely missing(anophthalmia) on one or both sides (see Fig.4.13), protruding (exophthalmia) or moved tothe front of the head (cyclopia) (Singh andBustard, 1982; Millichamp et al., 1983;Jacobson, 1984; Ferguson, 1989;Youngprapakorn et al., 1994; Hibberd, 1996).Defects of cornea and iris and the sealing ofthe nictitating membrane (third eyelid) havealso been reported (Singh and Bustard, 1982;Youngprapakorn et al., 1994).

Twins

Twins can be either monozygotic (identicaltwins), originating from one ovum (germ celland yolk-sac) or dizygotic, originating fromseparate ova included in one egg (double-yolked egg).

Double-yolked eggs are larger than theother eggs in the clutch. However, theembryos remain small and usually die beforehatching, or, if they hatch, fail to developnormally and remain stunted (Blomberg,1979; Hibberd, 1996; Webb and Manolis,1998). Elongated eggs containing three yolkshave also been reported (Youngprapakorn etal., 1994). This can happen when the simulta-neously ovulated yolks travel down theoviduct too closely to one another.


Fig. 4.16. Adult captive Crocodylus porosus with skewed jaws.

Monozygotic twins occur more frequentlythan dizygotic ones (Youngprapakorn et al.,1994). They share one yolk-sac and thereforeeither die when they both fail to internalizethe yolk-sac or become attached to eachother at the navel. The surgical separation ofsuch omphalopagous twins may be very dif-ficult because of the shared yolk-sac(Larriera and Imhof, 1994; Youngprapakornet al., 1994).

Incomplete twinning occurs when the sep-arate development of the two monozygousembryos has occurred at a slightly later stageand one of the twins has remained incom-plete. Such incomplete twins may have twoheads on one body or may be joined at vari-ous parts of the body, as Siamese twins(Ferguson, 1989; Youngprapakorn et al, 1994;Troiano and Roman, 1996), or the incompletetwin may consist of a limb or even incom-plete limb only, which is attached to the navelof the other twin (Fig. 4.17).

Albinism and other colour variations

Albinism consists of the complete absence ofpigment in skin and eyes, producing a whiteskin and red eyes. Sometimes the transversemarkings can be seen as faint shadows.Crocodile farmers often refer to any white orlight-coloured crocodiles as albinos, but this

is incorrect. True albino crocodiles are quiterare but have been found in caiman andAmerican alligators (Allen and Neill, 1956;Troiano and Román, 1996). True Nile croco-dile albinos have also hatched from time totime on a particular farm in South Africa.

White crocodiles with dark markings arenot albinos and the condition is not partialalbinism but rather leucotism. Such animals,also called leucystic, have pigmented eyeswhich are blue-grey, and a white skin withdarker markings when young, but the skinbecomes darker as the animals mature (Karand Bustard, 1982a; Barnett et al., 1999).Unfortunately Bezuijen (1996) does notdescribe the eye colour of the ‘albino’ croco-diles in Cambodia. Their dark markings sug-gest that they are merely white.

A melanistic (black) spectacled caimanhatchling from Colombia had black eyes andonly a narrow greyish area along its ventralmidline (Allen and Neill, 1956). An erythrys-tic (red) American alligator had reddish-brown cross bars over a normally colouredbackground (Allen and Neill, 1956).

American alligator embryos incubated atan elevated temperature (33°C) develop oneextra transversal stripe. This is due to thelarge size of the embryo at the stage whenthe wave-like pattern of pigmentation initia-tion passes down the body of the embryo(Ferguson, 1989).

154 Chapter 4

Fig. 4.17. Incompletely formed homozygous twin attached to the navel of the completely formed Nilecrocodile hatchling.

Abdominal wall defects

Several defects of the walls of thorax andabdomen have been described byYoungprapakorn et al. (1994). These includenon-closure of the thorax with ectopic heart,non-closure of the abdominal wall withectopic yolk-sac and intestines, and non-clo-sure of the abdominal wall between naveland cloaca. Ectopia cordis has also beenfound in an American alligator hatchling(Elsey et al., 1994).

Malformation of internal organs

The reported congenital defects of internalorgans include oesophageal stenosis, duode-nal atresia and atresia of the bile duct(Youngprapakorn et al., 1994). In all these casesthe closure of the important passages eventu-

ally led to the death of the hatchling. My ownobservations in farmed Nile crocodiles includeextra loops on the duodenal loop (Figs 4.18and 4.19), which appears to be relatively com-mon, doubling of the gall bladder, one in eachliver lobe and each with a separate duct lead-ing into the duodenum (Fig. 4.20), and a two-lobed fat body (Fig. 4.21). None of these lattermalformations appeared to have any seriouseffects on the crocodiles.

Congenital gout

Non-formation of one kidney has been seenin our own post-mortem material. In suchcases, the remaining kidney showed com-pensatory growth. It is not clear whether thecongenital gout described by Foggin (1992a)was cause by an absence of kidney formationor by non-functional kidneys.


Fig. 4.18. Malformed duodenal loop in a juvenile Nile crocodile: extra twist.

156 Chapter 4

Fig. 4.19. Malformed duodenal loop in a juvenile Nile crocodile: extra arm.

Fig. 4.20. Double gall bladder in a juvenile Nile crocodile, the right liver lobe has been removed.

Fig. 4.21. A two-lobed fat body in a Nile crocodile.

Transmissible diseases are those caused byinfectious or parasitic agents, including para-sitic infestations. There are several crocodile-specific viral and bacterial infections, someof which may even be species or genus spe-cific. However, their present distributionmay also be due purely to geographical lim-its. The specificity of parasites also varies. Inaddition, there are many non-specific infec-tions, particularly bacterial and fungal.

Contamination and infection have to beseen in quantitative terms. While a low infec-tion pressure may not suffice to overcome thedefences of the host, the build-up of contami-nation in an intensive rearing unit may reachsuch proportions as to be able to overcomeeven high levels of immunity. In addition, theimmune-suppressive action of stress may infact trigger outbreaks of infectious diseases, ifthe infectious agent is already present in therearing pens. In other words, the presence ofpoxvirus, chlamydiae or coccidia alone is notenough to start an outbreak of the disease, oneor more triggering factors may be needed toallow the infection to manifest itself as disease.

Viral Infections

Unlike ostriches, crocodiles have their ownspecific infectious diseases, amongst them poxand adenoviral hepatitis, but they can alsoacquire infections from other animal species.

The diagnosis of viral infections shouldbe based on the presence of specific patho-logical and histopathological lesions, possi-bly with typical inclusion bodies, on electronmicroscopy, on serological tests and on theisolation and characterization of the virus.With regard to crocodile viruses, there is aserious problem. None of them can be iso-lated in embryonated chicken eggs, the mostcommon tool in veterinary virology laborato-ries, nor can they be grown in any of the cellculture lines presently in use. Nobody hasyet isolated or established crocodile embry-onic cell lines that could be used for thiswork (see Notes Added at Proof, p. 210).Such viral cultures are also necessary for thepreparation of antigens for serological tests,as well as for the manufacture of specificvaccines. Without the ability to grow croco-dile viruses in cell culture, we still are lack-ing some very important tools.

It is amazing that a book on reptile medi-cine and surgery published as recently as1996 by a reputable publishing house cancontain a statement to the effect that the onlyknown viral disease of crocodiles wascaiman pox (Lane, 1996).

Caiman pox

Caiman pox is the infection with aParapoxvirus and is characterized by grey or

Chapter 5

Transmissible Diseases


greyish-white lesions in the mouth and onthe dorsal skin of the head, body and legs ofhatchling and juvenile spectacled caimans.Outbreaks have been reported from the USA(Jacobson et al., 1979), Hungary (Vetési et al.,1981), South Africa (Penrith et al., 1991),Brazil (Matushima and Ramos, 1993, 1995;Cubas 1996) and Colombia (Villafañe et al.,1996). The colour and distribution of lesionsand the limitation of the disease to probablyone single species of Caiman indicate thatthis is a separate disease entity.

Outbreaks of clinical disease usually occurin hatchlings and juveniles under 1 year ofage and may affect a large proportion of theanimals being reared together. The infectionappears to be limited to Caiman crocodilus.Some authors state that the animals recoverafter a prolonged period without apparent illeffects (Cubas, 1996), while others reportsevere clinical problems, including retardedgrowth and eventual death (Vetési et al.,1981). This may depend on conditions in therearing environment. Complete recoverymay take 6 weeks or longer.

The lesions in the oral mucosa and on thedorsal skin of head, body and legs begin assmall, round, whitish papular lesions 1 mmin size and usually situated between scales.Later they become covered with greyish-white crusts, increase in size, become conflu-ent, assume irregular shapes and cover oneor even several scales (Plate 7).

Microscopically the lesions are character-ized by epithelial hyperplasia, acanthosis,hyperkeratosis and necrosis. Enlargedepithelial cells contain large, deeplyeosinophilic cytoplasmic inclusions, whichare typical Bollinger bodies or smaller inclu-sions (Borrel bodies). Transmission electronmicroscopy reveals these inclusions to con-tain large numbers of dumb-bell-shaped viri-ons (Jacobson et al., 1979). Negatively stainedpreparations of the caiman poxvirusrevealed the regular criss-cross surface pat-tern characteristic of the genus Parapoxvirus,similar to those of the crocodile poxvirus (p.160) (Gerdes, 1991). Attempts to isolate thevirus on various reptile cell lines have failed(Jacobson et al., 1979).

It is believed that individual caimans cancarry and shed the virus without being clini-

cally affected. This shedding can take placeeither on the farm or in a natural populationin the vicinity of the farm, from which thevirus can be introduced into the rearing facil-ity by the use of water from the river or lakeinhabited by the wild population. There isalso evidence that stress may play a role intriggering actual outbreaks, if the virus ispresent already.

There is no specific treatment. Providingoptimal rearing conditions and good foodwill help to speed up the recovery. There isno further experimental evidence that nat-ural or artificial sunlight will improvechances of recovery as stated by Penrith et al.(1991). Prevention consists of providing astress-free rearing environment, stricthygiene, including the regular scrubbing anddisinfection of the rearing pens, and the useof borehole or well water for the rearingunits, instead of river water.

Crocodile pox

Crocodile pox is an infection of hatchlingand juvenile crocodiles with a Parapoxvirus,characterized by brown crusty lesions in theoral cavity, on the head and on the ventraland lateral surfaces of the body and tail.Outbreaks of the disease have been reportedin Nile crocodiles (Foggin, 1987; Horner,1988a; Pandey et al., 1990; Huchzermeyer etal., 1991; Buoro, 1992) and individual cases inC. porosus and C. johnsoni (Buenviaje et al.,1992, 1998b; Turton et al., 1996). The colour ofthe lesions, their distribution on the ventraland lateral aspects of the body and theapparent limitation of the infection to a smallrange of Crocodylus species indicate that thisis a separate disease entity.

Outbreaks of clinical disease occur inhatchlings as well as juveniles under 2 yearsof age. Small (1–3 mm) sunken or prominentand crusty brown lesions appear on the headand on the ventral and lateral surfaces ofbody and tail, often apparently associatedwith bite marks (Plate 8) (Huchzermeyer etal., 1991). Lesions on the eyelids may causeblindness, and lesions on the head maycause a shrinking of the skin, leading to

158 Chapter 5

deformities (Foggin, 1987; Horner, 1988a).While the morbidity is high, mortality usu-ally remains low, unless the disease becomescomplicated by opportunistic bacterial andfungal infection of the lesions. Recovery isnormally spontaneous within a few weeks ormonths.

The pathology is limited to the skinlesions as described above. Microscopicallythe lesions are characterized by hyperkerato-sis and parakeratosis with ballooningepithelial cells containing single large intra-cytoplasmic inclusions (Bollinger bodies) orseveral small inclusions (Borrel bodies) (Fig.5.1). Unlike avipox lesions, the inclusions ofcrocodilian pox cannot be stained with a fatstain. By electron microscopy numerousdumb-bell-shaped virions can be demon-strated, which have been identified innegatively stained preparations, by their criss-cross striations, as belonging to the genusParapoxvirus (Fig. 5.2) (Gerdes, 1991). Attemptsto grow the virus in embryonated chickeneggs and on chicken cell lines have failed(Horner, 1988a).

It is presumed that the virus can be car-ried and shed by clinically healthy carriers.In one case, the disease was introduced pre-sumably with the acquisition of hatchlingsfrom a farm where the disease had occurredpreviously (Horner, 1988a). Wild crocodiles

in the vicinity of a crocodile farm probablyare the most common source of infection,which can enter the farm with the waterfrom the river or lake harbouring a wildpopulation. Adult breeding stock on thefarm also are a possible source of the virus.While the virus could possibly be transmit-ted by mosquito bite, it is much more likelyto be transmitted by contaminated water.Stress must be seen as the major factor trig-gering outbreaks in the presence of the infec-tion.

There is no specific treatment againstcrocodile pox infection, although secondaryinfections may warrant therapeutic interven-tion. Attempts at individual treatment andthe associated handling may cause stress andnegatively affect the individual animals(Horner, 1988a). A crude autogenous vaccineprepared from scabs from affected animalsreduced the recovery time (Horner, 1988a),but there is the danger of causing general-ized infection amongst unvaccinated indi-viduals, when the live vaccine virus isintroduced into the rearing environment(Foggin, 1992a).

The prevention of crocodile pox infectionis based on avoiding the use of potentiallycontaminated water – rather use borehole orwell water in the rearing section – and theavoidance of stress, particularly heat stress.

Transmissible Diseases 159

Fig. 5.1. Crocodile pox lesion with intracytoplasmic inclusions.

Adenoviral infection

Adenoviral infection most commonly affectsthe liver of Nile crocodile hatchlings under 5months of age, less often the intestines andpancreas, and sometimes the lungs as well,but rarely all in the same animal (Jacobson etal., 1984; Foggin, 1987, 1992a,b). The diseaseoccurs mainly in Zimbabwe but has beendiagnosed in South Africa as well.Adenoviral particles were found by trans-mission electron microscopy in negativelystained faeces of three Nile crocodile (length31–47 cm), which had been imported toSouth Africa from Mozambique (Fig. 5.3)(Huchzermeyer et al., 1994b). In experimen-

tal transmission trials by oral administrationof naturally infected liver, the incubationperiod was 2–18 weeks (Foggin, 1992a).There is a suspicion that it may also be trans-mitted vertically via the egg from mother tohatchling, although horizontal transmissionappears to be more common (Foggin, 1992a).Successful isolation of the crocodile aden-ovirus virus has never been reported.

Apart from lethargy and anorexia, thereare no clinical symptoms. Sometimes theinfection is associated with the occurrence ofmassive mortality, particularly during thewinter months. However, other factors maybe involved in these outbreaks (Foggin,1987). The virus frequently causes a chronic

160 Chapter 5

Fig. 5.2. Transmission electron micrograph of crocodile pox virus particles, showing the criss-crosssurface striations (micrograph G.H. Gerdes).

hepatitis which, in Zimbabwe, is seen as amajor cause of runting (Foggin, 1992b).

On post-mortem examination, there maybe slight icterus. The liver is markedlyswollen and pale (Fig. 5.4) and the bile ispale yellow instead of the normal dark-greencolour (Foggin, 1992a). The intestine may beswollen and congested, and is sometimesfilled with fibrinous exudate. The infection isconfirmed histopathologically by the demon-stration of the typical intranuclear inclusionbodies in the hepatocytes of the liver, theintestinal or pulmonary epithelium, or theacinar cells of the pancreas (Fig. 5.5)(Jacobson et al., 1984; Foggin, 1992a).Common findings in chronic adenoviral

hepatitis are fibrosis of the portal tracts andbile duct hyperplasia (Foggin, 1992a).

There is no treatment for the infection,although antibiotic treatment of the sec-ondary bacterial infections may have a bene-ficial effect in serious outbreaks. In theabsence of a suitable medium for the isola-tion of the virus, it is impossible to produce avaccine. Prevention should be based on stricthygienic measures aimed at preventing thehorizontal spread of the virus, including notusing water from rivers inhabited by wildcrocodiles, and preventing stress, particu-larly thermal stress caused by wide tempera-ture fluctuations in open-air rearing pens inwinter.


Fig. 5.3. Transmission electron micrograph of a crocodile adenovirus particle (micrograph J.F. Putterill).

Fig. 5.4. Nile crocodile hatchling with adenoviral hepatitis.

Newcastle disease – paramyxovirus

The Newcastle disease virus does not causeclinical disease in crocodiles, but Nile croco-diles fed fowls that had died from Newcastledisease were found to seroconvert (Thomson,1972). Paramyxovirus particles, believed to beNewcastle disease virus, were found by trans-mission electron microscopy in negativelystained faeces of crocodiles (length from 32 to144 cm) from a farm where the crocodiles hadbeen fed with dead chickens from a poultryfarm on which an outbreak of Newcastle dis-

ease had occurred (Fig. 5.6). A paramyxoviruswas also found in the faeces of a single croco-dile from a farm where no poultry had beenfed (Huchzermeyer et al., 1994b).

Seroconversion takes place only if thevirus multiplies within the host. Excretion ofthe virus in the faeces could mean that croco-diles can act as carriers and a possible sourceof infection for wild waterbirds. In a recentserological survey, wild waterbirds werefound to be a potential reservoir ofNewcastle disease virus in South Africa(Pfitzer et al., 2000).

162 Chapter 5

Fig. 5.5. Intranuclear adenoviral inclusion bodies in the pancreas of a Nile crocodile hatchling.

Fig. 5.6. Paramyxovirus in negatively stained faeces of a farmed Nile crocodile that had been fed deadchickens from an outbreak of Newcastle disease (micrograph J.F. Putterill).

In the light of the above, there is a strongsuspicion that the outbreaks of conjunctivitisand encephalitis reported from farmedcaimans in Colombia (Villafañe et al., 1996)could also be caused by a paramyxovirus(see also p. 245).

Eastern encephalitis virus

Antibodies to the virus of eastern equineencephalitis (EEE) were found in the blood ofa single American alligator, adding thisspecies to the list of possible reptile carriersof the virus (Karstad, 1961; Lunger and Clark,1978; Jacobson, 1984). The carrier reptiles arenot affected clinically by the infection.

Influenza C virus

Filamentous forms of influenza C virus werefound by transmission electron microscopy innegatively stained faeces of eight Nile croco-diles (length 31–81 cm) from one farm associ-ated with high mortality over a period of 1month (Fig. 5.7). The animals had beenexposed to severe stress caused by overstock-ing, handling and fluctuating temperatures,which could have rendered the animals moresusceptible to the infection, which may or

may not have contributed to the high mortal-ity rate (Huchzermeyer et al., 1994b).

Coronavirus

Coronavirus-like particles were found bytransmission electron microscopy in nega-tively stained faeces of four 2–3-year-oldcrocodiles from a farm with severe mortalityin that age group (Fig. 5.8). They were pre-sent in very high concentrations in two of thefour specimens (Huchzermeyer et al., 1994b).It is not possible to say whether this agentwas pathogenic and contributed to the highmortality, or whether it was only opportunis-tic and able to multiply in severely compro-mised animals.

See Notes Added at Proof, p. 210.

Bacterial Infections

Only a few bacteria cause specific diseasesin crocodiles, and even fewer of these arecrocodile-specific. However, very many dif-ferent species of bacteria can cause non-specific septicaemias. These bacteria arerecruited either from the aquatic environ-ment, the intestinal flora or from food con-taminants, particularly where raw meat isused as feed.


Fig. 5.7. Influenza C virus in negatively stained Nile crocodile faeces (micrograph J.F. Putterill).

All septicaemias, specific and non-spe-cific, are triggered, if not caused, by stress.Bacteria are allowed to escape under severestress from the intestine into the blood circu-lation (see p. 228), and if the stress continues,the resultant immune suppression preventsthe crocodile from overcoming the initialescape and allows the bacteria to gain afoothold. Infections in septic woundsnormally are contained by fibriscess for-mation, the exudation of fibrin into the septicarea, which immobilizes the invading bacte-ria (see p. 46) (Huchzermeyer and Cooper,2000).

Identifying and eliminating the source ofstress that has triggered an outbreak of septi-caemia is the most important part of thetreatment in an outbreak of bacterial infec-tions, as antibacterial treatment alone israrely successful. The elimination of poten-tial stressors and the identification of poten-tial sources of infection play a major role inall prophylaxis programmes.

Salmonellosis

Salmonellosis is caused by bacteria of thegenus Salmonella and manifests itself eitheras enteritis, particularly in hatchlings (seep. 145), or as septicaemia. This is not a croco-dile-specific disease, as the agents can infectmany different animal species, and some ofthe salmonellae, particularly S. enteritidis and

S. typhimurium, are also human pathogens.Crocodiles, like other reptiles, harboursalmonellae in their intestines as part of theirnormal gut flora. Bacteriologists and veteri-narians become excited whenever salmonel-lae are found. However, the danger of any ofthese salmonellae spreading to people isminimal. How many records are there ofhuman salmonella infections originatingfrom crocodiles? Species and serovars ofSalmonella that have been isolated fromcrocodiles are listed in Table 5.1.

Bacterial septicaemia is often precipitatedby severe stress, particularly temperaturestress such as overheating or frequent tem-perature changes (pp. 228 and 278). In thesecases the salmonellae act only as opportunis-tic invaders, similarly to many other bacte-ria. The ongoing infection may causedepression and anorexia. In advanced casesthe bacteria may attack the joints, taking theform of polyarthritis, which renders theaffected crocodiles unable to move (seep. 273). The enteritic form of the disease mayeither cause fibrinous exudation and occlu-sion of the intestine (see p. 145) or diarrhoea,sometimes with portions of fibrinous casts(pseudomembranes) in the faeces. A haemor-rhagic enteritis due to S. choleraesuis has alsobeen described (Ocholi and Enurah, 1989).

The clinical diagnosis can be establishedonly on the strength of bacterial cultures ofblood, faeces or synovial aspirate. The post-mortem findings are non-specific and need

164 Chapter 5

Fig. 5.8. Coronavirus-like particles in negatively stained faeces of a farmed Nile crocodile (micrographJ.F. Putterill).


Table 5.1. Salmonella serovars isolated from crocodiles.

Serovar Reference Serovar Reference

Salmonella IRough 1Untypeable 1, 4, 99,12:1; v:- 217:Z4Z23Z32 1Aarhus 1Aberdeen 1Abony 2Adelaide 1, 2, 4, 9Agama 1Agodi 1Agona 2Agoueve 1Alamo 1Albany 1Anatum 1, 2, 4, 17Antarctica 1Arechavaleta 1Bahrenfeld 17Banana 2Bangui 1Binza 4Blockley 1Bonn 10Bovis-morbificans 17Braenderup 1Brancaster 1Brazos 1Bredeny 2Brisbane 1Bron 1Budapest 1California 1Cerro 4Chester 4, 17Chicago 2Choleraesuis 7Cullingworth 2Dabou 1Derby 11Diguel 1Duesseldorf 1Duval 1Eastbourne 2Edinburgh 2Emek 2Enteritidis 4Farsta 1Good 1Haardt 1Havana 4Herston 1

Salmonella I (continued)Infantis 2, 4Israel 1Javiana 1Johannesburg 2, 5, 6, 17Kinondoni 4Kingston 1Kisangani 1Kottbus 2Koumra 9Livingstone 4Montevideo 2Muenchen 2, 4, 14Naestved 1Ndolo 1Newport 2Newlands 1Onderstepoort 17Oranienburg 2Orion 2, 4Os 1Oslo 1Othmarschen 1Phaliron 1Plymouth 2Poona 4, 15, 17Ried 1Saint-Paul 2, 4, 15Sandiego 1Schwarzengrund 1Schwerin 1Senftenberg 2, 4Shamba 13Simi 1Singapore 4, 17Sofia 4Somone 1Tallahassee 1Tanger 1Tennessee 4Thompson 4Tinda 1Tsevie 1Tshiongwe 1Typhimurium 1, 2, 4, 5, 6,

9, 12, 16, 17

Urbana 17Virchow 17Wagenia 1Wangata 1Waycross 5

Continued

to be confirmed by bacterial isolation. Thetreatment of clinical cases comprises oral orparenteral administration of an antibioticselected by antibiogram and the eliminationof the precipitating stressor(s). If the animalstill eats, the oral route should be chosen, asparenteral administration may need furtherphysical immobilization of the animal andthereby further stress.

On farms, treatment should be aimed atcontaining the outbreak rather than at savingaffected individuals. Administration of asuitable antibiotic in the feed, eliminating thestressor(s) and eliminating the source ofinfection are of equal importance. However,it should be noted that the salmonellae mayhave been present in the intestines of someof the animals for a considerable time beforethe outbreak, and have only become activewhen stress reduced the resistance of the

crocodiles. Since the spread occurs by thefaecal–oral route, water changes, scrubbingand disinfection of the pens are of primeimportance (see p. 113).

The prevention of salmonellosis must bebased on the use of sanitary feed (pellets orboiled mince), a strict hygiene programme(smooth surfaces free of cracks, washing witha detergent to remove protective layers of fat,thorough disinfection with each change ofwater; see p. 113), and the elimination of allstressors, in particular the protection fromvarying and excessive temperatures. While theuse of a calf paratyphoid vaccine in an out-break of salmonellosis due to S. typhimuriumhas been reported (Huchzermeyer, 1991a), it isdoubtful whether such a vaccination wouldhave any prophylactic value, particularly inview of the plethora of immunologically dif-ferent Salmonella isolates listed in Table 5.1.

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Table 5.1. Continued.

Serovar Reference Serovar Reference

Salmonella I (continued)Weltevreden 4Westhampton 1Yaba 1Yoruba 1

Salmonella IIRough 16,8; eh; enz15 19,12; gz62; - 116; gt; z42 116; z; enx 139; mt; enx 140; b; - 148; k; enxz15 155; -; - 1

Salmonella IIIUntypeable 116:z10:e,n,x,z15 1448:1;v; z35 250; -; - 150; k; z 17

Salmonella IIIa48; k; z53 1

Salmonella IIIb28; -; - 130; k; enx 138; k; z35 148; k; z53 148; r; enxz15 150; r; z35 150; r; z53 150; z52; z35 160,65; k; z 1

Salmonella IV50; z4z23 1

Group C 9Group D 9Group E 9, 10Group 5 8, 9

S. arizona 3, 4, 5, 8, 9, 11, 17

References: 1, Van der Walt et al. (1997); 2, Greenberg and Sechter (1992); 3, Ippen (1965); 4, Manoliset al. (1991); 5, Ladds and Sims (1990); 6, Hibberd et al. (1996); 7, Ocholi and Enurah (1989); 8, Obwoloand Zwart (1993); 9, Foggin (1992a); 10, Madsen (1993); 11, Foggin (1987); 12, Shotts et al. (1972); 13,Rudat et al. (1966); 14, Habermalz and Pietzsch (1973); 15, Cope et al. (1955); 16, Huchzermeyer(1991a); 17, Millan et al. (1997b).

Mycoplasmosis

Cases of polyarthritis in 1–3-year-old Nilecrocodiles have occurred on several farms inZimbabwe (Mohan et al., 1995) and similarcases have been reported from Israel andSpain (Levisohn and Bernstein, and Oros,both quoted by Mohan et al., 1997).Mycoplasmas were isolated from lungs andsynovial fluid of the Zimbabwean crocodilesand the isolates were identified as Mycoplasmacrocodyli (Kirchhoff et al., 1997). The sick ani-mals had swollen joints and were progres-sively unable to move. The joints were filledwith excessive quantities of turbid fluid, inchronic cases with dry fibrinous exudate, andsome of the animals were found to havelesions of pneumonia (Mohan et al., 1995).

In an outbreak of mortality in adult maleAmerican alligators, Mycoplasma sp. was iso-lated from lungs and synovial fluid fromseven out of eight of the euthanized animals(Clippinger et al., 1996). Clinically the ani-mals had been in poor condition, withanorexia, lethargy, muscle weakness, para-paresis, bilateral white ocular discharge and varying degrees of periocular, facial, cer-vical and limb oedema. The authors referredto the state of these 30-year-old animals as ‘geriatric’ (Clippinger et al., 1996).Intramuscular treatment with oxytetracy-cline (10 mg kg�1 estimated body mass)every 7 days for 1 month and every 14 daysthereafter for 5 months appeared to have hadbeneficial results. The agent was identified asMycoplasma alligatoris (Brown et al., 2001a).Experimental infection of American alliga-tors produced fatal disease, with fibrinouspolyserositis, polyarthritis, myocarditis andmeningitis (Brown et al., 2001b). Broad-nosedcaimans were also susceptible to fatal experi-mental infection, while Siamese crocodileswere not affected clinically but reacted sero-logically (Brown et al., 2001b,c).

Treatment of the Zimbabwean cases withtetracycline by injection, followed by admin-istration of the same antibiotic in the feed,ameliorated clinical signs but did not pre-vent relapses (Mohan et al., 1997). A vaccinemade from M. crocodyli gave a certain degreeof protection (six out of eight) to animals thathad received a booster 21 days after the firstvaccination (Mohan et al., 1997).

The epidemiology of this disease stillremains unresolved. It is to be presumed thatwild crocodiles act as reservoirs of infection.Vertical transmission has been suggested tobe the major mode of transmission and thisis likely to affect farms with hatchlings fromeggs collected from the wild (Mohan et al.,1996). Limited trials in Zimbabwe could notdemonstrate the horizontal transmission ofthe disease to in-contact animals from a farmknown to be free from mycoplasmosis(Mohan et al., 1996). However, unidentifiedmycoplasmas (Fig. 5.9) were found in thefaeces of crocodiles from two farms in SouthAfrica, and this finding could demonstratethe mode of excretion for horizontal trans-mission (Huchzermeyer et al., 1994b).

There is no doubt that stress serves as atriggering factor for outbreaks of mycoplas-mosis, as with other bacterial infections.Blood cultures from the American alligatorsyielded a range of bacteria but ‘different bac-teria were isolated from different individuals’(Clippinger et al., 1996). This is typical foroutbreaks of stress septicaemia (see p. 228).

Specific enzyme-linked immunosorbentassays (ELISA) for M. alligatoris and M. croco-dyli could be used to screen crocodiles beforeexport or import, or before their release backinto nature (Huchzermeyer, 2001).

Chlamydiosis

Chlamydiosis is a disease in farmed Nilecrocodiles caused by chlamydiae closelyrelated to Chlamydia psittaci, but probably adifferent species. There are two forms: anacute hepatitis and a chronic conjunctivitis(Huchzermeyer et al., 1994a). Chlamydiaewere isolated together with mycoplasmasfrom cases of polyarthritis in Nile crocodilesin Israel (Levisohn, 1995, quoted by Mohanet al., 1996). In Zimbabwe acute chlamydiosisoften is found associated with adenoviralhepatitis (Foggin, 1992b).

In outbreaks of the acute form, the affectedhatchlings die without having shown anysigns of illness. On post-mortem examinationthe liver is found to be pale, mottled andenlarged (Fig. 5.10) and the spleen slightlyenlarged (see also p. 270). There is a mildascites and a severe hydropericardium


(Fig. 5.10). The most severe histopathologicalchanges are found in the liver: a severe portalto diffuse lymphoplasmocytic hepatitis withcongestion, mild bile duct proliferation, vac-uolar degeneration of the hepatocytes andmultifocal to coalescing necrosis. Numerouscolonies of intracytoplasmic organisms arepresent in the hepatocytes (Fig. 5.11). The

chlamydiae in the liver tissue can be stainedwith special stains or demonstrated in liverimpression smears stained with Giemsa stain.The organisms can be isolated in embryonatedchicken eggs as well as in tissue culture.

The chronic cases, which are more com-mon in South Africa, occur in the form of abilateral blepharo-conjunctivitis with swelling

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Fig. 5.9. Electron micrograph of a mycoplasma found in negatively stained faeces of farmed Nilecrocodiles in South Africa (micrograph J.F. Putterill). Previously published in the OIE Bulletin(Huchzermeyer, 2002).

Fig. 5.10. Nile crocodile hatchling with chlamydial hepatitis and hydropericardium.

and increasing opacity of the third eyelid,and finally the accumulation of fibrinousexudate under the third eyelid, leading toblindness (Fig. 5.12). Such outbreaks canaffect up to 50% of the hatchlings or juve-niles in a pen. In these cases demonstrationof the presence of chlamydiae by microscopyis much more difficult, almost impossible, asonly very few are present, but the isolationof the agent in tissue culture or embryonatedeggs is more likely to be successful.

The agent is sensitive to oxytetracyclineand this is administered via the feed:

Terramycin soluble powder (Pfizer, oxytetra-cycline 55 mg g�1) 10 g kg�1 (Foggin, 1992b),or pure oxytetracycline 1 g kg�1 of feed (wetration, four times as much in dry pellets).

Wild crocodiles, and possibly carrier croc-odiles on the farm, are believed to be the nat-ural reservoir of infection. From the wildcrocodiles the infection might be brought onto the farm by the use of river water in therearing pens, while the spread from carrieranimals on the farm might occur on theshoes of staff and the manager when movingfrom enclosure to enclosure or pen to pen.


Fig. 5.11. Chlamydial hepatitis in a Nile crocodile hatchling, intracellular chlamydial colonies in the hepa-tocytes (haematoxylin and eosin).

Fig. 5.12. Chlamydial conjunctivitis with fibrinous exudate behind the third eyelid, Nile crocodile hatchling.

Stress is suspected to play a role in triggeringthe outbreaks.

The prevention of chlamydiosis must bebased on stress prevention as well as onstrict hygienic measures, such as the use ofborehole or well water in the rearing section,as well as the disinfection of footwear whenmoving from section to section. It should bepossible to prepare a diagnostic antigenwhich then could be used for screening croc-odiles due to be sold or released, particularlyNile crocodiles from southern Africa.

Mycobacteriosis

Mycobacteriosis is the disease caused by dif-ferent species of Mycobacterium. Only theinfection with the obligatory pathogens M.tuberculosis and M. bovis should be calledtuberculosis. However, it is believed thatthese obligatory pathogens cannot infectcrocodiles because of their very specific tem-perature requirements (Huchzermeyer andHuchzermeyer, 2000), although they can beadapted to growth at lower temperaturesand thereby able to infect poikilothermic ani-mals (Vogel, 1958).

Only a few cases of mycobacterial infec-tions in crocodilians have been reported, andthese mostly from zoos and other collections:Mycobacterium marinum was isolated fromfour spectacled caimans, C. crocodilus, fromLondon Zoo (Griffith, 1928); a case of renal‘tuberculosis’ was reported from a spectacledcaiman without culture results (Zwart, 1964);a non-typeable strain of M. avium complexwas isolated from a ‘crocodile’ (Thoen andSchliesser, 1984); and acid-fast bacteria,which did not grow on culture media, werefound associated with granulomatouslesions in a captive Chinese alligator (Blahak,1998). Mycobacterium fortuitum was isolatedfrom generalized granulomatous lesions of acaptive spectacled caiman (Huchzermeyerand Huchzermeyer, 2000).

The reported cases of farmed crocodilesare: a number of crocodilian cases with gran-ulomatous lesions in lungs, trachea andintestines associated with mycobacteria, butwithout culture results (Youngprapakorn etal., 1994); generalized mycobacteriosis in 12

juvenile C. johnsoni, in which the agent wasidentified by a polymerase chain reaction(PCR) probe as M. ulcerans (Ariel et al.,1997b); granulomatous mycobacterial der-matitis in five C. porosus, but without identi-fication of the agent (Buenviaje et al., 1998b);and acid-fast bacteria found in a granuloma-tous lesion with giant cells in the foot of afarmed C. porosus hatchling (Turton et al.,1996). In addition, Huchzermeyer andHuchzermeyer (2000) reported several casesof generalized mycobacteriosis in farmedNile crocodiles in South Africa caused by M.avium complex, while M. terrae, M. trivialeand an atypical Mycobacterium were found tobe environmental contaminants of granulo-matous lesions caused by fungal infections.

The infection usually takes place via theoral–intestinal route and spreads from theintestine by septicaemia to all organ systems(see p. 228). The fat body appears to be par-ticularly sensitive to mycobacterial infection,probably because of a lack of cells of theimmune system (Fig. 5.13) (see also p. 262).

The granulomatous lesions of crocodilesare non-specific and their presence does notindicate the presence of mycobacteria per se(Fig. 5.14). Mycobacteria have to be shown tobe present by the use of a special stain(Ziehl–Neelsen) (Fig. 5.15), by PCR or by cul-ture. Note that the culture of mycobacteriafrom crocodiles can only be done in a spe-cialized laboratory, as the media and proce-dures used for the culture of M. tuberculosisin medical pathology laboratories are notsuitable for their isolation.

The source of infection is either the food,e.g. pork infected with M. avium complex(Huchzermeyer and Huchzermeyer, 2000)and fish infected with M. fortuitum or M.marinum, or the environment. There is notreatment. For some cases the careful appli-cation of heat should be investigated, as M.ulcerans, for example, does not survive at33°C (Glynn, 1972). However, it is believedthat high levels of vitamin C in the food mayhelp to control the infection in the face ofenvironmental contamination, as it does infish (Chávez de Martínez and Richards,1991). Strict hygiene comprising scrubbingand disinfection of the rearing pens withevery water change, the boiling of raw meat

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or fish from suspect sources and the provi-sion of a stress-free environment are furtherprophylactic measures that can be taken.

Erysipelothrix infection

Only one outbreak of Erysipelothrix insidiosainfection has been described, in a zoologicalexhibit in Florida, USA, where it caused gen-

eralized disease associated with mortality in6–8-week-old spectacled caiman hatchlings,and dark-brown, crusty skin lesions, 2–4 cmin diameter, on the back of a very oldAmerican crocodile (estimated to be 100years old). Treatment with penicillin in thefeed and locally with an iodine spray led tothe cessation of losses in the caimans andclinical improvement of the adult crocodile(Jasmin and Baucom, 1967).


Fig. 5.13. Mycobacterial steatothecitis in a case of generalized mycobacteriosis in a juvenile Nile crocodile.

Fig. 5.14. Mycobacterial granuloma in the fat body of a juvenile Nile crocodile (haematoxylin and eosin).

Clostridiosis

Clostridial infections most likely are alsoprecipitated by stress. It is only because oftheir apparent rarity that they are treatedhere under a separate heading.

A Clostridium sp. was isolated from oede-matous fluid from four gharials that had‘oedematous swelling in all limbs and partialswelling of the abdomens’. On palpationthese swellings appeared to be painful(Misra et al., 1993). This description fits thecommon picture of polyarthritis following asepticaemia (see p. 228). A ‘critically’ lowwater level in the pond housing the affectedgharials (Misra et al., 1993) may have led tothermal stress and precipitated the disease.Clostridium septicum was isolated from a caseof bacterial hepatitis/septicaemia from afarmed crocodile in Australia (Buenviaje etal., 1994).

Clostridium limosum was isolated inFlorida from the livers and kidneys ofAmerican alligators that died ‘with symp-toms of paralysis’ (Cato et al., 1970). Mostlikely the ‘paralysis’, in these cases, was dueto polyarthritis, which often originates fromstress-related septicaemias (p. 228).

Clostridium spp. were reported to havebeen the second most important bacterial

isolates from 131 cases of hatchling alligatorsyndrome over 15 years on 25 farms insouth-eastern USA (Barnett and Cardeilhac,1995). A haemorrhagic enteritis associatedwith a clostridial infection is described inChapter 7 (p. 257).

Dermatophilosis

A Dermatophilus sp. was isolated from skinlesions referred to as ‘brown spot’ in farmedAmerican alligators in Louisiana. Thelesions, in the form of a small discolorationbetween the abdominal scales, were reportedto lower drastically the value of the hides(Bounds and Normand, 1991). However,Barnett and Cardeilhac (1998) failed to findfilamentous organisms in similar ‘brownspot’ lesions in an alligator skin fromFlorida. Filamentous organisms have alsobeen seen in histopathological preparationsof skin lesions in Zimbabwe (Foggin, 1992b)and South Africa (the author’s own cases)(Fig. 5.16), but they have never been isolatedon culture media.

The disease has been described in moredetail from Australian crocodiles, where aDermatophilus sp. was isolated from thelesions and the disease was transmitted

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Fig. 5.15. Masses of mycobacteria in a granuloma in the spleen of a juvenile Nile crocodile(Ziehl–Neelsen stain).

experimentally by the application of brothcultures to the skin of the trial crocodiles(Buenviaje et al., 1997, 1998a,b). The initiallesion consists of a lifting of the keratinaccompanied by some accumulation ofdebris. This is followed by an indentation ofthe epidermis because of the continuousreplacement of the necrotic cells and byhyperplasia of cells of the stratum basale. Inthe third stage the erosion of the epidermisresults in ulceration with increased amountsof debris and the extension of the filamen-tous organisms into the subcutis (Buenviajeet al., 1998b).

Broadly similar lesions are seen in a con-dition in Nile crocodiles called ‘winter sores’,which occurs in farmed crocodiles kept atsuboptimal temperatures (Huchzermeyer,1996c) (see pp. 236 and 241).

Dermatophilus spp. are environmentalorganisms. Treatment of the infection can betried by including tetracycline into the ration(1 g active substance per kg of food) for 10days and by spraying the crocodiles them-selves with a disinfectant such as F10®

(Health and Hygiene, South Africa) or a 0.5%solution of copper sulphate or zinc sulphate(Van Tonder and Horner, 1994). The infectioncan be prevented by the application of verystrict hygienic measures, such as regularthorough cleaning and disinfection of therearing pens (see p. 113).

Non-specific septicaemias

The non-specific septicaemias of crocodilesare caused by a large variety of bacteria ofenteric or environmental origin, many ofwhich are opportunistic rather than obliga-tory pathogens, mostly part of the normalintestinal flora (see p. 38), although theintestinal flora of farmed crocodiles may bemodified by antibacterial treatments and theintroduction of potential pathogens whenfeeding meat, particularly from farm mortal-ities. Septic wounds rarely lead to septi-caemias (Huchzermeyer and Cooper, 2000)and this adds support to the hypothesis ofthe enteric origin of septicaemia in croco-diles. The infections usually are precipitatedby stress (Jacobson, 1984) and may be exacer-bated by suboptimal temperature regimes orby the inability of the affected crocodiles tothermoregulate effectively. As all these infec-tions produce the same disease, there is noneed to create a separate disease entity foreach bacterium.

There follows a list of bacteria isolatedfrom cases of crocodilian septicaemias:

● Aeromonas hydrophila and A. shigel-loides. In adult American alligators(Shotts et al., 1972; Gorden et al., 1979), inzoo crocodiles (Mayer and Frank, 1974),from the eyes of American alligators(Jacobson, 1984), in Nile crocodiles


Fig. 5.16. Dermatophilus-like organisms in a skin lesion in a juvenile Nile crocodile.

(Foggin, 1987, 1992a), in American alliga-tor hatchlings (Peters and Cardeilhac,1988; Barnett and Cardeilhac, 1995), infarm-reared C. porosus, C. johnsoni andCrocodylus novaeguineae (Ladds and Sims,1990; Buenviaje et al., 1994).

● Bacillus sp. In American alligator hatch-lings (Barnett and Cardeilhac, 1995).

● Campylobacter fetus subsp. jejuni. Froma West African dwarf crocodile at DenverZoological Gardens (Luechtefeld et al.,1981).

● Chromobacterium sp. In farmed NewGuinea and Indo-Pacific crocodiles (Laddsand Sims, 1990).

● Citrobacter sp. and C. freundii. InAmerican alligators (Novak and Seigel,1986), in farmed Nile crocodiles (Foggin,1992a), in American alligator hatchlings(Barnett and Cardeilhac, 1995).

● Corynebacterium sp. and C. pyogenes. Infarmed Nile crocodiles (Foggin, 1992a), inAmerican alligator hatchlings (Barnettand Cardeilhac, 1995).

● Edwardsiella sp. and E. tarda. In farmedNile crocodiles (Foggin, 1992a), inAmerican alligator hatchlings (Barnett andCardeilhac, 1995) and from an adultfemale American alligator in a zoo(Wallace et al., 1966), in farmed C. porosus(Buenviaje et al., 1994; Hibberd et al., 1996).

● Enterobacter agglomerans. In Americanalligators (Novak and Seigel, 1986), infarmed Nile crocodiles (Foggin, 1992a), infarmed C. porosus (Hibberd et al., 1996).

● Escherichia coli. In an adult captiveAmerican alligator (Russell and Herman,1970), in juvenile captive Crocodylus palus-tris (Sinha et al., 1988), in farmed Nilecrocodiles (Foggin, 1992a).

● Klebsiella oxytoca and Klebsiella sp. InAmerican alligators (Novak and Seigel,1986) and in farmed crocodiles inAustralia (Buenviaje et al., 1994).

● Morganella morgani. In a captive WestAfrican dwarf crocodile with subsequentarthritis (Heard et al., 1988), in Americanalligators (Novak and Seigel, 1986), infarmed Nile crocodiles (Foggin, 1992a), infarmed C. porosus (Hibberd et al., 1996).

● Pasteurella multocida. In captiveAmerican alligators that had been stoned

by trespassing persons (Mainster et al.,1972), in farmed Nile crocodiles (Mohanet al., 1994; Dziva and Mohan, 2000), infarmed C. porosus (Hibberd et al., 1996).

● Planococcus sp. In captive gharials (Misraet al., 1993).

● Proteus sp. In captive crocodiles (Mayerand Frank, 1974), in American alligators(Novak and Seigel, 1986), in a crocodile(Chakraborty et al., 1988).

● Providencia rettgeri. In farmed Nile croc-odiles (Foggin, 1992a), in an adult femalemugger from a zoo (Sinha et al., 1987), infarmed C. porosus (Buenviaje et al., 1994;Hibberd et al., 1996).

● Pseudomonas sp. and P. aeruginosa. Infarmed Nile crocodiles (Foggin, 1992a), infarmed American alligator hatchlings(Barnett and Cardeilhac, 1995), in farmedspectacled caimans (Villafañe et al., 1996),in farmed C. porosus (Hibberd et al., 1996).Pseudomonas putida in farmed C. porosus(Turton et al., 1996).

● Serratia sp., S. marcescens and S. liquefa-ciens. In American alligators (Novak andSeigel, 1986; Barnett and Cardeilhac, 1995)and in farmed crocodiles in Australia(Buenviaje et al., 1994).

● Staphylococcus sp. and S. aureus. InAmerican alligators (Mainster et al., 1972),in a captive West African dwarf crocodilewith subsequent septic arthritis (Heard etal., 1988), in American alligator hatchlings(Barnett and Cardeilhac, 1995).

● Streptococcus sp. In American alligatorhatchlings (Barnett and Cardeilhac, 1995).

Clinical signs

The course of the disease depends on theenvironmental temperature and the size ofthe affected crocodiles. It is fast in hatchlingskept at 32–34°C, but slow in juveniles at lowtemperatures, while it can take severalmonths in adults. Hatchlings may die with-out showing any clinical signs. Juveniles andadults may refuse to feed, become lethargicand show a reddish discoloration of the ven-tral skin (Plate 9). In some chronic cases theaffected animals develop white patchesaround the nostrils and eyes, as well as on

174 Chapter 5

the dorsal surface of body and limbs (Fig.5.17) (see also p. 241). Even extreme emacia-tion is seen in some cases.

In other instances the infection settles inthe joints and other serous cavities, causing apolyarthritis or polyserositis (Plate 10). Thecrocodiles appear to be ‘paralysed’ or ratherunwilling or unable to move. The inflamma-tion of the joints may cause painful swellingof the legs (see p. 287).

Pathology

The findings vary with the age of the animaland the course of the disease. In acute casesthere may be no lesions at all. Diffuse orfocal hepatitis, excess serous fluid in bodycavities, subcutaneous oedema, sometimeshaemorrhagic, myocarditis and/or acute fib-rinous epicarditis (Plate 11), as well as pneu-monia, have been described (Mainster et al.,1972; Ladds and Sims, 1990; Foggin, 1992a).Splenomegaly is also a common feature(Huchzermeyer, 1994) (see p. 270).

Treatment

In advanced cases, the likelihood of a treat-ment being successful is minimal. If under-taken on a group basis, the treatment should

be based on the results of bacterial culturesand an antibiogram of the isolated agent,and should be administered via the food.Individual handling and injecting only addsto the stress that originally triggered the out-break. At the same time, the environmentaltemperature should be adjusted to the opti-mal range and all stresses avoided. Onlyhatchlings can be caught and dosed orinjected individually, as they appear to bestressed less by individual handling.Transferring sick animals to a hospital penalso causes further stress, and the necessityand consequences of such a move should beassessed beforehand.

Prevention

For the prevention of septicaemias it is nec-essary to maintain optimal temperature con-ditions and to keep handling and otherstressful events to an absolute minimum.Since low temperatures do not allow thebody to overcome a stress septicaemia,because of the inactivation of the immunesystem, crocodiles should not be handled,caught or transported in cold weather (win-ter) conditions, and during air transport thetemperature should not be allowed to fallbelow 25°C.


Fig. 5.17. White patches on the dorsal aspect of a juvenile Nile crocodile suffering from a chronicsepticaemia.

Fungal Infections

Opportunistic infections

Most fungal infections are opportunistic.Many of the fungi involved in these infectionsare part of the normal intestinal flora and areexcreted daily with the faeces into the water.They and the environmental fungi can thrivein the warm and humid conditions in the rear-ing house. However, they can also escape fromthe intestine and enter the blood circulationunder severe stress (p. 278). This route ofinfection has been demonstrated in ostriches(Walker, 1912) and it is probably the mostcommon origin of cases of generalized myco-sis. Normally the fungi are inhibited in theintestine by the bacterial flora. If the latter issuppressed by prolonged antibacterial treat-ment, the fungi can multiply more freely(Silberman et al., 1977). Once a systemic infec-tion has occurred, it depends on the suppres-sion of the host’s immune system by cold orchronic stress to be able to fully establish itself.It is to be noted here that some of the fungiinvolved in these cases can multiply evenunder very cold conditions, exactly when thedefenses of the host are immobilized by cold.

Pathology

The tissue reaction to fungal infections isgranulomatous, and not exudative as it is inmost localized bacterial infections. The gran-ulomata are characterized by the presence ofmultinucleated giant cells.

Fungal agents

The following fungi have been isolated fromcrocodilians:

● Aspergillus flavus. From farmed C. poro-sus (Hibberd et al., 1996) and from theskin of a farmed C. porosus (Buenviaje etal., 1998b).

● Aspergillus fumigatus. From skin lesionsof farmed caimans (Troiano and Román,1996) and from the lungs of captiveAmerican alligators (Jasmin et al., 1968).

● Aspergillus niger. From farmed C. porosus(Buenviaje et al., 1994; Hibberd et al., 1996)

and from the skin of a farmed C. porosus(Buenviaje et al., 1998b).

● Aspergillus ustus. From the lungs of cap-tive American alligators (Jasmin et al.,1968).

● Aspergillus versicolor. From farmed C.porosus (Hibberd et al., 1996).

● Beauveria bassiana. From the lungs of acaptive American alligator (Fromtling etal., 1979a,b) and from the lungs of a cap-tive Nile crocodile (Keymer, 1974).

● Candida albicans. From the oral cavity of acaptive caiman (Debyser and Zwart, 1991).

● Candida parasilosis. From the skin of afarmed C. porosus (Buenviaje et al., 1998b).

● Candida sp. From the skin of two farmedC. porosus (Buenviaje et al., 1998b).

● Cephalosporium sp. From small whitemuscle lesions of a captive C. crocodilus(Debyser and Zwart, 1991) and from thelungs of captive juvenile caimans(Trevino, 1972).

● Cladosporium sp. From skin lesions offarmed caimans (Troiano and Román,1996).

● Curvularia lunata varaeria. From the skinof farmed C. porosus (Buenviaje et al., 1994).

● Fusarium moniliforme. From the lungs ofa captive American alligator (Frelier et al.,1985).

● Fusarium solani. From internal organs offarmed C. porosus (Hibberd and Harrower,1993; Buenviaje et al., 1994).

● Fusarium sp. From farmed C. porosus(Hibberd et al., 1996), from gingivae of acaptive C. crocodilus fuscus (Kuttin et al.,1978) and from the skin of farmed C. poro-sus (Buenviaje et al., 1998b).

● Geotrichum candidum. From farmed C.porosus (Hibberd et al., 1996).

● Geotrichum sp. From farmed C. porosus(Hibberd et al., 1996).

● Metarhizium anisopliae. From the lungsof a captive crocodile (species not indi-cated) (Debyser and Zwart, 1991), fromthe lungs of a captive African dwarf croco-dile (Keymer, 1974) and from the lungs ofa captive American alligator (Jones, 1978).

● Mucor circinelloides. From the skin of acaptive caiman (Debyser and Zwart, 1991)and from gastric ulcers of a captive croco-dilian (Jones, 1978).

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● Mucor sp. From the lungs of four captivecrocodiles (Silberman et al., 1977).

● Paecilomyces farinosus. From the lungs ofa captive American alligator (Jones, 1978).

● Paecilomyces sp. From farmed C. porosus(Hibberd et al., 1996).

● Penicillium lilacinum. From the lungs offive captive crocodiles and alligators(Keymer, 1974).

● Penicillium oxalicum. From the skin of afarmed C. porosus (Buenviaje et al., 1994).

● Penicillium sp. From farmed C. porosus(Hibberd et al., 1996).

● Syncephalastrum sp. From the skin oftwo farmed C. porosus (Buenviaje et al.,1998b).

● Trichoderma sp. From the skin surface ofa wild-caught American alligator (Foreytet al., 1985).

● Trichophyton sp. From the skin of anAmerican alligator (Jacobson, 1980, 1984).

● Trichosporon cutaneum. From the skin ofone farmed C. porosus (Buenviaje et al.,1998b).

● Trichosporon sp. From tongue and gingi-vae of a captive Nile crocodile and a cap-tive Caiman crocodilus fuscus (Kuttin et al.,1978).

Treatment

Systemic and respiratory infections are oftendiagnosed too late for treatment to be con-sidered, while oral infections and dermato-mycoses may be diagnosed early. In all casesof attempted treatment it is of utmost impor-tance to rectify the triggering (environmen-tal) circumstances, such as temperature andhygiene. The fungal load in the pens can bereduced by washing the surfaces with CuSO4(1:1000) or a fungicidal disinfectant (F10®,Health and Hygiene, South Africa). Theactual topical treatment also depends on thesensitivity spectrum of the fungal isolate(s)from the particular case.

Prevention

It is important to avoid excessive fungalbuild-up in the intestines as well as in theenvironment. Prolonged antibacterial treat-

ment is dangerous in this context. Regularchanges of water, as well as scrubbing anddisinfection of the pens, are essential mea-sures. The crocodiles also have to be pro-tected from prolonged exposure tosuboptimal temperatures. Many fungi arepsychrophilic, able to multiply at low tem-peratures. Simulating hibernation conditionsfor captive crocodiles kept in high-densitysituations is fraught with danger. Similarly,transporting crocodiles in winter regularlyleads to high losses from generalized fungalinfections. Crocodiles kept in a clean,hygienic and stress-free environment, at closeto optimal temperatures at all times, are leastlikely to succumb to fungal infections.

Fungal dermatitis

Fungal infections of the skin usually origi-nate from infected wounds and abrasions.Stress, particularly thermal stress, may playan aggravating role. Debyser and Zwart(1991) report the isolation of Mucor circinel-loides from the scales of a caiman. A superfi-cial fungal dermatitis has been described byFoggin (1987), in which the dorsal skinappears dry and has a fine white coating,while in the mouth a more proliferative reac-tion can be seen. On histopathological exam-ination, fungal hyphae and spores can bedemonstrated in the superficial epidermis.

Infections by Aspergillus, Penicillium andCurvularia spp. in C. porosus hatchlingscaused a pale, gelatinous change in theaffected skin of head, belly and tail, as wellas between the scutes. The affected skin wassometimes ulcerated and sloughed easily(Buenviaje et al., 1994). Similar lesions wereassociated with Fusarium sp. and other fungi(Buenviaje et al., 1998b).

Superficial growth of fungi on the skinmay be facilitated by the deposition of nutri-ents on the skin from water which may becontaminated by food wastes. Histopatho-logically, the underlying skin is not affected.However, it appears that the dense fungalgrowth has a deleterious effect on the vari-ous functions of the skin, particularly inhatchlings. Foreyt et al. (1985) describe sucha case in an American alligator. A similar


case was seen in intensively reared Nile croc-odile hatchlings on a farm where very fatmeat was fed. We called this condition‘greasy skin’ (Fig. 5.18). Spraying the penand crocodiles with a detergent and hosingthem down led to a speedy recovery(author’s own unpublished findings).

Deep granulomatous lesions causingsevere swellings are produced by fungal infec-tion of skin abrasions and bite wounds on thefeet of captive and farmed crocodiles (Figs5.19–5.21). Jacobson (1984) describes theselesions as resembling bumblefoot in birds.However, these local infections in crocodilesdo not provoke an exudative reaction (fib-riscess) characteristic of bacterial infections(see p. 46), but are purely granulomatous.Ailing crocodiles often develop a fungal der-matitis at the tip of the tail (Figs 5.22 and 5.23).

Respiratory mycosis

Fungal lesions in the lungs usually are ofenteric origin and develop after severe stressor during prolonged exposure to cold(Frelier et al., 1985). A lung infection withBeauveria bassiana developed in a captiveAmerican alligator after exposure to coldtemperatures (Fromtling et al., 1979a,b).Although the authors regarded this fungus

as an insect pathogen, it was found to be partof the normal intestinal flora of wild-caughtAfrican dwarf crocodiles (Huchzermeyerand Agnagna, 1994; Huchzermeyer et al.,2000) (see also Table 1.12). In the above casethe fungal colonies spread to the serosal sur-face of the lung.

Fungi isolated from lesions in the lungsinclude: Metarhizium anisopliae (Jones, 1978;Debyser and Zwart, 1991), Cephalosporium sp.(Trevino, 1972), Mucor sp. (Silberman et al.,1977), Aspergillus fumigatus and A. ustus(Jasmin et al., 1968), Beauveria bassiana,Metarhizium anisopliae and Penicillium lilac-inum (Keymer, 1974), Paecilomyces farinosus(Jones, 1978), Fusarium moniliforme (Frelier etal., 1985) and Fusarium solani (Hibberd andHarrower, 1993).

The lesions can either be small granulo-mata resembling tuberculous lesions (Figs 5.24and 5.25) (Keymer, 1974), large granulomata,or confluent lesions with solidification of partsof the lung tissue (Fig. 5.26). Dilatation of thebronchi and the formation of emphysematousbullae have also been reported (Fig. 5.26)(Frelier et al., 1985) (see also p. 272).

Treatment with systemic antifungalscould be tried, but normally the condition isdiagnosed post-mortem. The prevention isbased on avoiding severe stress and pro-longed exposure to cold.

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Fig. 5.18. Nile crocodile hatchling covered in superficial fungal growth, ‘greasy crocodile’.


Fig. 5.19. Small fungal granulomata betweenthe toes of a juvenile Nile crocodile.

Fig. 5.20. Large fungal granuloma on the plantarsurface of the left forelimb of a juvenile Nile crocodile.

Fig. 5.21. Large fungal granuloma on the dorsal aspect of the left hind limb of a juvenile Nile crocodile.

Gastrointestinal mycosis

A case of gastric mycosis in a captive Nilecrocodile was described by Kuttin et al. (1978).The crocodile also had gingival and tonguelesions (see below). Clearly circumscribedlesions of up to 3 cm diameter were present inthe gastric mucosa, and fungal elements were

found in the lesions, superficially as well aspenetrating deep into the muscular layer. ATrichosporon sp. was isolated from the orallesions. Mucor circinelloides was isolated fromlarge chronic gastric ulcers of a captive croco-dilian (species not stated) (Jones, 1978).

Intestinal lesions with fungal hyphaewere found in generalized Fusarium solani

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Fig. 5.22. Dermatomycosis of the tail tip of a juvenile Nile crocodile.

Fig. 5.23. Fungal hyphae in a section of a mycotic skin lesion of a juvenile Nile crocodile.

Fig. 5.24. Small mycotic granulomata on the pleural surface of the lung of an adult Nile crocodile.

infections in farmed C. porosus in Australia(Hibberd and Harrower, 1993), as well as incrocodiles with Mucor sp. infections in addi-tion to pulmonary lesions (Silberman et al.,1977). Gastric fungal lesions were found inan adult Nile crocodile as part of a general-ized mycosis (Fig. 5.27) (author’s own case).

Oral mycosis

Mixed bacterial and fungal oral infectionscommonly occur in stressed and anorexiccrocodiles (see p. 249). Candida albicans is fre-quently isolated from these lesions (Debyserand Zwart, 1991). Kuttin et al. (1978) found


Fig. 5.25. Small mycotic granulomata in the lung of an adult Nile crocodile.

Fig. 5.26. Confluent mycotic lesion at the caudal tip of the left lung and widespread emphysema in ajuvenile Nile crocodile.

Trichosporon sp. in tongue lesions of a captiveNile crocodile, and Fusarium sp. andTrichosporon sp. associated with gingivallesions in a captive Caiman crocodilus fuscusthat had shared the same basin. The lesionscan be confluent or well-circumscribedulcers.

Generalized mycosis

Generalized fungal infections usually are ofenteric origin and commonly develop instressed and anorexic animals, particularlyin combination with prolonged exposure tosuboptimal temperatures (Huchzermeyer,1991b). An outbreak of generalized mycosisin juvenile farmed C. porosus was associatedwith abnormally low winter temperatures,and fungal lesions were found in livers andlungs (Buenviaje et al., 1994).

Different organs and tissues may beaffected. Debyser and Zwart (1991) reportthe isolation of Cephalosporium sp. fromsmall, white muscle lesions in a C. crocodilus.In the case of pulmonary infection withBeauveria bassiana in a captive American alli-gator, there had been ‘dissemination’ to liverand spleen (Fromtling et al., 1979a). How-

ever, more likely all the lesions originatedfrom a fungaemia. Similarly, the cases of fun-gal infections in crocodiles and alligatorsdescribed by Keymer (1974) were respiratoryand systemic. Fusarium solani caused sys-temic infection in farmed C. porosus, affectinglivers, lungs and intestines (Hibberd andHarrower, 1993).

It is worth mentioning here that theinflammatory response in reptiles is less spe-cific than in mammals. In crocodiles, multin-ucleated giant cells are commonly present ingranulomas and not limited to mycobacterialinfections.

Parasitic Protozoa

Most parasitic protozoa, including some ofthe coccidia, are harmless commensals.Finding them is interesting from an ecologi-cal point of view. Parasites are an integralpart of an ecosystem and of biodiversity.The extinction of a host causes the extinctionof its parasites at the same time. Rescue andcaptive breeding of an endangered crocodilespecies may still not prevent the extinctionof its specific parasites, particularly wherethe latter require intermediate hosts that are

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Fig. 5.27. Mycotic ulcers in the pyloric region of the stomach of an adult Nile crocodile with generalizedmycosis.

not present in the captive environment. Thepositive role of parasites in the evolution ofthe immune system, e.g. spleen size, hasbeen demonstrated for birds (Morand andPoulin, 2000) and probably applies to allvertebrates.

Coccidiosis

Species of coccidia

Coccidiosis is caused by several species ofcoccidia. A number of coccidian parasites ofcrocodiles have been described from faecalsuspensions according to their oocyst mor-phology (see Tables 5.2 and 5.3), but in mostcases without reference to any pathology,while, on the other hand, cases and severeoutbreaks of coccidiosis, often involvinginternal organs as well as the intestine, havebeen described from many crocodilianspecies without definitive identification ofthe coccidian species involved (Table 5.4).Much further research is needed in this field.Since sporozoites within the sporocysts areoften the only stage found in cases of coc-cidiosis, it might be interesting to study themorphology of the sporozoites to determinewhich species are involved in causing out-breaks of disease.

Some of the described species of Eimeriaand Isospora may be very host specific, whileothers may be able to infect a wider range of

species. However, it must be stated categori-cally that avian and mammalian coccidiafrom the animals fed to the crocodiles do notpose any threat. However, it is possible thatGoussia sp. can be transmitted by fishes usedto feed the crocodiles.

Life cycle

The coccidia of the genera Eimeria andIsospora have a complex life cycle but do notrequire intermediate hosts. The oocysts areeither excreted with the faeces and sporulateoutside in the environment (exogenoussporulation) or sporulate while still in theintestine (endogenous sporulation). Thesporulated oocysts of Eimeria contain foursporocysts with two sporozoites in eachsporocyst (Figs 5.28 and 5.29), while those ofIsospora contain two sporocysts with foursporozoites each. The sporozoites are liber-ated when the sporulated oocyst (or sporo-cyst) is ingested by a new host. However, incases of endogenous sporulation, the sporo-zoites may be liberated within the same hostand the development may continue withoutpassing on to a new host.

The sporozoites invade epithelial cells inthe intestine, usually deep in the crypts, andthere they develop into schizonts (Fig. 5.30).This process is called schizogony. Themature schizonts break up, at the sametime destroying the host cell, and liberatemerozoites, which, in turn, invade further


Table 5.2. The coccidia of crocodiles.

Host Parasite Pathology References

Alligator mississippiensis Eimeria alligatori – McAllister and Upton (1990)A. mississippiensis Eimeria hatcheri – McAllister and Upton (1990)‘Caiman’ Eimeria pintoi – Carini (1933)Caiman yacare Eimeria caimani – Aquino-Shuster and

Duszynski (1989)C. yacare Eimeria paraguayensis – Aquino-Shuster and

Duszynski (1989)Caiman latirostris Isospora jacarei – Carini and Biocca (1940)Crocodylus acutus Eimeria crocodyli – Lainson (1968)Crocodylus acutus Isospora wilkei – Lainson (1968)C. niloticus Eimeria sp. undescribed – Own materialC. niloticus Eimeria sp. – Thiroux (1916); Hoare (1932)C. niloticus Goussia sp. +++ Gardiner et al. (1986)Gavialis gangeticus Eimeria kermoganti – Simond (1901b)

+++, Only species with which pathology was associated.

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Table 5.3. Characteristic features of the oocysts of crocodilian coccidia.

Species Size (�m) Shape Shell Sporulation

Eimeria alligatori 25.3 � 20 Ovoid Pitted ExogenousEimeria caimani 19–29 Spheroid PittedEimeria crocodyli 14.25 � 15.7 Spheroid SmoothEimeria hatcheri 13.7 � 16.1 Sub-spheroid Smooth ExogenousEimeria kermoganti 20–22 Spherical EndogenousEimeria parasuayeusis 23.6 � 34 Ellipsoid EndogenousEimeria pintoi 33 � 22 Ovoid Micropyle ExogenousEimeria sp. of Crocodylus 13 � 12.6 Spheroid Pitted Endogenous

niloticus, undescribedGoussia sp. 20 Spherical EndogenousIsospora jacarei 13 � 15 Sub-spherical SmoothIsospora wilkei 22.8 � 33 Ovoid Smooth

Table 5.4. Crocodilian species from which cases of coccidiosis have been reported.

Host Intestinal Generalized References

Caiman crocodilus x x 1Crocodylus niloticus x x 2, 3, 4, 5Crocodylus novaeguineae x x 6, 7Crocodylus palustris x 8Crocodylus porosus x x 6, 7Gavialis gangeticus x 8G. gangeticus x 9

1, Villafañe et al. (1996); 2, Foggin (1987); 3, Foggin (1992a); 4, Foggin (1992b); 5, Obwolo and Zwart(1992); 6, Ladds and Sims (1990); 7, Ladds et al. (1995); 8, Jacobson (1984); 9, Griner (1983).

Fig. 5.28. Oocyst of an Eimeria sp. from a Nile crocodile; stained intestinal smear. Note the pitted sur-face of the oocyst shell.

epithelial cells. After several cycles of schizo-gony, the merozoites invading epithelial cellsdevelop into macrogametocytes (female) andmicrogametocytes (male), and the latterliberate a large number of microgametes,which fertilize the female macrogametes.Subsequently these develop into oocysts,which can start a new cycle of infection(Fig. 5.31).

Sources of infection

Infected crocodiles are the only source of theinfection. This is of particular importancewhere the crocodile farm is situated in anarea inhabited by wild crocodiles and whereriver or lake water is used on the crocodilefarm. Adult breeding crocodiles can alsocarry the infection without being affected


Fig. 5.29. Four sporulated sporocysts of the Nile crocodile Eimeria sp.; stained intestinal smear.

Fig. 5.30. Crocodile coccidia schizonts in a section of the intestinal mucosa.

themselves in any way. Attendants who havebeen working in the breeding enclosure cancarry the oocysts or sporocysts on their feetor shoes into the rearing houses, and thusstart an outbreak of coccidiosis in the hatch-lings or juveniles. Feeding the intestines andinternal organs of slaughtered crocodilesback to juvenile or even breeding crocodiles,a common practice on many crococile farms(see p. 128), may help to perpetuate theinfection on the farm.

It is possible that the Goussia sp., whichappears to be responsible for outbreaks ofgeneralized coccidiosis, uses fishes as inter-mediate hosts, although it has been shown tobe capable of direct transmission from croco-dile to crocodile as well (Foggin, 1987).

Clinical signs

Acute infections do not produce any clinicalsigns. However, as the infection progresses,the inflammatory reaction to the presence ofthe coccidia, and possible secondary bacter-ial infections, produces masses of fibrinousexudate, which completely block theintestines. This causes the animal to becomebloated first and later to become lethargic.Some infected animals with blockedintestines may be able to survive for months,with a runted and emaciated appearance.

Pathology

In early cases there may only be a congestionof the intestinal mucosa with a serous

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Fig. 5.31. Schematic drawing of the eimerian life cycle: 1, oocyst; 2, sporulated oocyst with foursporocysts containing two sporozoites each; 3, liberated sporocysts and sporozoites; 4, sporozoiteinfecting epithelial cell; 5, developing into a schizont; 6, schizont breaking up into merozoites, destroyingthe host cell and infecting further epithelial cells, either to form new schizonts (schizogony) or to begingametogony; 7, merozoite infecting new cell; 8, to develop into a macrogametocyte (female) or into 9, amicrogametocyte (male); 10, microgametocyte breaking up and liberating microgametes; 11, microgametes fertilizing the macrogamete, which develops into an oocyst → 1.

exudate. Probably, the presence of secondarybacterial infections stimulates the prolificexudation of fibrin, once the intestinal bacte-ria have penetrated the epithelial barrierwhere the epithelial cells have beendestroyed by the coccidia. Frequently thisfibrinous exudate blocks the intestinallumen. In early cases schizonts may be pre-sent in the epithelial cells of the crypts, whilein advanced cases sporulated oocysts or lib-erated sporocysts may be found in themucosa surrounded by intensive inflamma-tory reaction and abundant fibrinous exu-date (Fig. 5.32).

In some cases, some of the sporulatedoocysts and sporocysts may be transportedby the lymph to the general circulation andlodge in various internal organs (Fig. 5.33);however, in many cases without any notice-able inflammatory response.

Generalized coccidiosis

In a particular form of coccidiosis, probablycaused by Goussia sp., the developmentalstages are seen to invade other internalorgans, where they continue to multiply andcause a severe inflammatory response


Fig. 5.32. Eimerian sporocysts with sporozoites deep in the intestinal mucosa of a juvenile Nile crocodile.

Fig. 5.33. Eimerian sporocysts with sporozoites in the pancreas of a wild-caught Osteolaemus tetraspis.

(Gardiner et al., 1986; Foggin, 1987, 1992a,b).A similar case has been reported from a cap-tive gharial (Griner, 1983). This generalizedform of coccidiosis may even lead to thetransovarial infection of crocodile embryos(Villafañe et al., 1996) (see also p. 141).

Therapy

It is not possible to treat advanced cases of crocodilian coccidiosis because of theblockage of the intestine by the fibrinousexudate. However, as a herd treatment,sulphachloropyrazine (ESB3®, Ciba Geigy)has been found to be particularly effectivebecause of its simultaneous antibacterialactivity (10 g of the water-soluble powderper 1 kg of food for 4 days, or dilute 1 g in5 ml of water and dose by stomach tube atthe rate of 0.2 ml per 100 g of body mass;Foggin, 1992a). Amprolium (Amprol 20%®

Logos Agvet; 2 g in 1 kg of food for 7 days)and Toltrazuril (Baycox®, Bayer; 7 ml in 1 kgof food for 3 days) have also been found tobe effective (Foggin, 1992a).

Prevention

The most important prophylactic measureconsists in not allowing infected oocysts toenter the rearing section of the farm. Wherethe farm is situated close to waters inhabitedby wild crocodiles, it is absolutely essentialto avoid the use of surface water in the rear-ing pens. Note that chlorination of the waterdoes not kill the oocysts. Separate shoes orrubber boots should be used for work in thebreeding and rearing pens. Again, it must bestressed that disinfectant dips do not kill theoocysts that are carried on the shoes orboots.

The continuous inclusion of a coccidiostatin the food does not seem to be practisedanywhere, at least it has not been reported.However, on farms where outbreaks occurfrequently, one could consider the prophy-lactic use of Toltrazuril in the food atmonthly intervals. Foggin (1992a) recom-mends for such farms a prophylactic treat-ment with sulphachlorpyrazine (ESB3®, CibaGeigy), 10 g kg�1 food for 4 days, every 3–4weeks.

Where generalized coccidiosis is a prob-lem, one might also have to consider the pos-sibility of food fish harbouring the parasiteand introducing it into the farm.

Cryptosporidia

Cryptosporidia are very small coccidian par-asites of the intestinal epithelium. Theiroocysts are approximately 4 � 5 �m in size.They are mainly found in mammals andbirds and are not very host specific. Becauseof their size, they are rarely found in directfaecal smears. Staining preparations withperiodic acid–Schiff (PAS) or Mayer’shaematoxylin improves chances of findingthe oocysts (Lane and Mader, 1996).Histopathological examination of the intesti-nal mucosa is another way to detect cryp-tosporidial infections. At present there is notreatment for these infections.

Cryptosporidia were found in the faecesof one out of nine captive Nile crocodiles inEgypt. The infection may have originatedfrom infected attendants or from rats, whichwere fed to the crocodiles. The experimentalinfection of mice with cryptosporidia fromthe attendants, as well as from the crocodile,was successful (Siam et al., 1994). Theinfected crocodile did not show any clinicalsigns. This appears to be the first and onlyreport of cryptosporidia in crocodiles.

Hepatozoon (‘haemogregarines’)

A certain degree of confusion exists aroundthese blood parasites, which originally werecalled haemogregarines, then split into thegenera Haemogregarina and Hepatozoon, untilall the crocodilian parasites of this groupwere finally transferred to the latter genus(Siddall, 1995; Smith, 1996). These belong toone of two groups of coccidian blood para-sites of crocodilians, the other one belongingto the genus Progarnia (see p. 190), whilePlasmodium spp., the true agents of malaria,have never been found in crocodiles.

Members of the genus Hepatozoon aretransmitted by arthropods – in the case ofthe crocodilians, biting flies and mosquitoes,

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in which the sexual multiplication takesplace (Chatton and Roubaud, 1913; Hoare,1932; Pessôa et al., 1972; Khan et al., 1980).Asexual schizonts are found in the liver ofthe infected crocodiles (Fig. 5.34), whilegametocytes are found either in the redblood cells, typically folded over (Plate 12),or free in the blood as elongated vermiformbodies (Fig. 5.35). While developmentalstages have also been found in leeches, it hasnot been possible to transmit the infectionexperimentally via these ectoparasites (Khanet al., 1980).

Confusion still surrounds the naming ofindividual Hepatozoon spp. of crocodiles.Some of the original descriptions gave insuf-ficient detail and others were based on theassumption that each host species had itsown ‘haemogregarine’ parasite species. A listof the presently known named species isgiven in Table 5.5. However, a revision of thestatus of these species is required.

The Hepatozoon spp. of crocodiles are ableto sustain a high level of parasitaemia formany years, but do not appear to cause anyharm to the host. However, it is possible that


Fig. 5.34. Hepatozoon sp. schizont in the liver of a wild-caught Osteolaemus tetraspis.

Fig. 5.35. Hepatozoon sp. free gametocyte in the blood of a wild-caught Osteolaemus tetraspis.

chronically or terminally ill crocodiles maylose the ability to control the parasite, andthis may lead to very high parasitaemias,which in turn could be falsely interpreted ascause of death.

Progarnia sp.

Progarnia archosauriae (Haemosporina:Garniidae) is a parasite of red and whiteblood cells of C. crocodilus in northern Brazil(Lainson, 1995). Merogony takes place inlymphocytes and monocytes, less frequentlyin thrombocytes and even less frequently inimmature and mature erythrocytes. Thegamonts are found also in lymphocytes,monocytes and thrombocytes. The nuclearmaterial of microgamonts is scattered dif-fusely, while the macrogamonts have a well-defined nucleus and the characteristicblue-staining cytoplasm of female malarialparasites.

The infection was found in very young,wild-caught animals. Nothing is known aboutthe transmission of the parasite, presumablyby biting insects, nor is anything knownabout a possible pathogenicity of the parasite.

Intestinal flagellates

Trichomonas spp.

Trichomonas prowazeki Alexeieff, 1909 hasfour anterior flagellae and parasitizes sala-

manders and newts. It was found in acaptive juvenile C. palustris (Parisi, 1910).Heavy trichomonad infections have beenfound in captive American alligators thatdied from colibacillosis (Russell andHerman, 1970) and in juvenile farmed C.crocodilus in a feeding trial (Avendaño et al.,1992). While all these cases were associatedwith either mortality or poor performance, itremains unclear whether these parasiteswere the cause of death or poor perfor-mance, or were able to thrive in otherwisesuppressed or stressed animals.

Giardia sp.

Giardias are binucleated flagellates with anadhesive disk, which enables them to adhereto the intestinal epithelium. A Giardia sp.,morphologically different from other knownreptilian parasites of the same genus, wasfound repeatedly in farmed Nile crocodileson several farms in South Africa, but did notappear to be associated with any pathology(author’s own findings). The trophozoitesoccur deep in the crypts of the intestinalmucosa and their cysts are excreted with thefaeces (Figs 5.36 and 5.37).

Leishmania (?) sp.

Cases of severe giant cell enteritis in juvenilefarmed C. porosus, usually under 1 year ofage, with severely thickened walls of theupper intestine and associated with signs ofchronic illness and runting, occurred in

190 Chapter 5

Table 5.5. Hepatozoon spp. described from crocodiles. Note that the nomenclature is in need ofrevision.

Alligator mississippiensis H. crocodilinorum Börner (1901)a

Caiman crocodilus H. brasiliensis Di Primio (1925)C. latirostris H. caimani Carini (1909)‘Crocodilus frontatus’ H. crocodilinorum Börner (1901)Crocodylus cataphractus H. sp. Dutton et al. (1907)C. niloticus H. pettiti Thiroux (1910)C. niloticus H. sheppardi Travassos Santos Dias (1952)C. novaeguineae H. sp. Ladds and Sims (1990)C. porosus H. hankini Simond (1901a)Gavialis gangeticus H. hankini Simond (1901a)Osteolaemus tetraspis H. sp. Theiler (1930)

a Redescribed by Khan et al. (1980).

Australia and Papua New Guinea (Ladds etal., 1994). The giant cells contained intracyto-plasmic bodies, which bore some resem-blance to amastigotes of Leishmania spp. inmammalian histiocytes.

Trypanosomes

The trypanosomes of crocodiles are harmlessflagellate blood parasites transmitted by

biting flies and possibly also mosquitoes.The life cycle of Trypanosoma grayi of the Nilecrocodile in the tsetse fly Glossina palpalis andits mode of transmission were studied byHoare (1929, 1931). Trypanosomes areknown from crocodiles and from caimans(Table 5.6). Normally the parasitaemia is solow that one rarely finds a trypanosome on ablood slide, even from infected crocodiles.However, one can improve the chances offinding the parasites by taking a larger blood


Fig. 5.36. Binucleated Giardia sp. trophozoite in a faecal smear from a farmed Nile crocodile.

Fig. 5.37. Giardia sp. trophozoites between the folds of the intestinal mucosa of a farmed Nile crocodile.

sample, centrifuging it and making thesmear from the buffy coat, the layer of whiteblood cells above the erythrocytes.

Entamoeba sp.

A single case of amoebic enteritis in a captivecrocodile (no species given) has beenreported, which happened in the course of anoutbreak of amoebiasis in snakes and otherreptiles in the affected collection (Ippen,1965). This was associated with an exudativeand necrotizing colitis (see also p. 257).

Blastocystis sp.

Blastocysts are intestinal parasites of uncer-tain taxonomic position of mammals, birdsand reptiles. They have a typical cyst-likeshape, 10–15 �m in diameter, with 2–4, oreven more, nuclei (Fig. 5.38). In a survey of

reptiles at Singapore Zoological Gardens,Blastocystis sp. was found in almost one-thirdof the species, including one C. porosus. Allindications are that these parasites are harm-less commensals (Teow et al., 1992).

Metazoan Endoparasites

In contrast to the protozoa, the single-cellorganisms of the preceding chapter, the meta-zoa are multicelled, with a variety of organsconsisting of different tissues. The endopara-sites in this group are the roundworms (nema-todes) and the flatworms, namely thetrematodes (flukes) and cestodes (tapeworms).

Ascaridoids

The ascaridoid species

A very large number of ascaridoid specieshave been described from crocodilians,demonstrating the rich and interesting biodi-versity of crocodilian parasites. The speciesare listed below in alphabetical order,together with their hosts:

● Brevimulticaecum baylisi. Found inAlligator mississippiensis, C. crocodilus andMelanosuchus niger (Sprent, 1979b;Goldberg et al., 1991; Catto and Amato,1994b).

● B. gibsoni. Found in M. niger (Sprent,1979b).

● B. pintoi. Found in Caiman latirostris andC. crocodilus (Sprent, 1979b).

● B. stekhoveni. Found in M. niger and C.crocodilus (Sprent, 1979b; Goldberg et al.,1991; Catto and Amato, 1994b).

● B. tenuicolle. Found in A. mississippiensis(Hazen et al., 1978; Sprent, 1979b).

192 Chapter 5

Table 5.6. Crocodile species in which trypanosomes have been found.

Host Parasite Length (�m) a References

Crocodylus niloticus T. grayi 61.6 Hoare (1928, 1929, 1931)C. cataphractus T. sp. 35 Dutton et al. (1907)Caiman crocodilus T. cecili 71.3 Lainson (1977)C. crocodilus T. sp. 50.1 Nunes and Oshiro (1990)

a Mean length without flagella.

Fig. 5.38. Schematic drawing of a Blastocystis sp.

● Dujardinascaris angusae. Found in C.porosus (Sprent et al., 1998).

● D. antipini. Found in Crocodylus rhombifer(Groschaft and Barus, 1970).

● D. blairi. Found in C. johnsoni (Sprent etal., 1998).

● D. chabaudi. Found in C. johnsoni (Sprent,1977).

● D. dujardini. Found in Crocodylus niloticus,Crocodylus cataphractus and C. porosus (?) inIndia (Bayliss, 1947; Sprent, 1977).

● D. gedoelsti. Found in C. niloticus (Sprent,1977).

● D. harrisae. Found in C. porosus (?) and C.novaeguineae (Sprent et al., 1998).

● D. helicina. Found in Crocodylus acutus(Sprent, 1977).

● D. longispicula. Found in C. crocodilus(Sprent, 1977).

● D. madagascarensis. Found in C. niloticusand C. cataphractus (Sprent, 1977).

● D. mawsonae. Found in C. novaeguineae,C. porosus and C. johnsoni (?) (Sprent, 1977;Ladds and Sims, 1990; Sprent et al., 1998).

● D. paulista. Found in C. crocodilus(Sprent, 1977; Goldberg et al., 1991).

● D. philippinensis. Found in C. porosus(Machida et al., 1992; Sprent et al., 1998).

● D. petterae. Found in Osteolaemus tetraspis(Sprent et al., 1998).

● D. puylaerti. Found in C. niloticus (Sprent,1977; Graber, 1981).

● D. salomonis. Found in C. porosus(Bayliss, 1947).

● D. tasmani. Found in C. niloticus(Ortlepp, 1932).

● D. taylorae. Found in C. porosus and C.novaeguineae (Sprent, 1977).

● D. waltonae. Found in A. mississippiensis(Sprent, 1977; Hazen et al., 1978; Cherryand Ager, 1982).

● D. westonae. Found in C. porosus (Sprentet al., 1998).

● D. woodlandi. Found in Gavialis gangeti-cus (Sprent, 1977).

● Gedoelstascaris australiensis. Found inC. johnsoni and C. porosus (Sprent, 1978a;Machida et al., 1992).

● G. vandenbrandeni. Found in C. niloticusand C. cataphractus (Sprent, 1978a).

● Goezia gavialidis. Found in G. gangeticus(Sprent, 1978b).

● G. holmesi. Found in C. porosus (Sprent,1978b).

● G. lacerticola. Found in A. mississippiensis(Deardorff and Overstreet, 1979).

● Hartwichia rousseloti. Found in C. niloti-cus and C. cataphractus (Graber, 1981;Sprent, 1983).

● Multicaecum agile. Found in C. niloticus,C. cataphractus, C. palustris, C. johnsoni, G.gangeticus and O. tetraspis (Sprent, 1979b;Graber, 1981).

● Ortleppascaris alata. Found in Crocodylusintermedius, C. crocodilus and probably M.niger (Sprent 1978a; Goldberg et al., 1991;Catto and Amato, 1994b).

● O. antipini. Found in A. mississippiensisand C. rhombifer (Sprent, 1978a).

● O. nigra. Found in C. niloticus, C. cat-aphractus and O. tetraspis (Sprent, 1978a;Graber, 1981).

● Terranova lanceolata (syn. braziliensis).Found in M. niger (Sprent, 1979a).

● T. crocodili. Found in C. niloticus, C. poro-sus, C. johnsoni (Sprent, 1983; Machida etal., 1992).

● Trispiculascaris assymmetrica. Found inC. niloticus (Sprent, 1983).

● T. trispiculascaris. Found in C. niloticus(Sprent, 1983).

● Typhlophorus lamellaris. Found in G.gangeticus (Sprent, 1983).

● T. spratti. Found in C. johnsoni (Sprent,1999).

Life cycle

Probably all ascaridoids of crocodiles requireintermediate hosts, although this has beenverified in only a few species. Larval formstaken from the amphibians Rana catesbiana,R. sphenocephala and Siren lacertina maturedinto adult examples of Brevimulticaecumtenuicolle when dosed to Alligator mississippi-ensis (Walton, 1936). It is likely that the lifecycle of Dujardinascaris involves an encystedstage in fish, frogs or possibly other food ani-mals. When swallowed by the crocodile, thethird-stage larvae emerge in the stomach,where the fourth-stage larvae and adults alsoremain, usually attached to the stomachmucosa (Sprent, 1977). Dujardinascaris


gedoelsti and D. dujardini were found inyoung farmed crocodiles in Zimbabwe afterthey had been fed with the lake sardineLimnothrissa miodon from Lake Kariba(Foggin, 1987, 1992a).

Clinical signs and pathology

Most ascaridoid infestations remain withoutclinical signs. Only in cases of very severeinfestations will there be a certain degree ofunderperformance and runting (Foggin,1992a). In subclinical cases the parasitesremain in the stomach (Plate 13), but insevere infestations they may be found fromthe oesophagus to the cloaca. Often theascaridoids are found associated with gastriculcers, to which they attach (Figs 5.39 and5.40) (Ortlepp, 1932; Ladds and Sims, 1990;Huchzermeyer and Agnagna, 1994; Ladds etal., 1995). However, it is not clear whetherthey can cause these ulcers or whether theyonly prefer to attach to mucosal lesions, oncethese exist. These mucosal lesions are sur-rounded by an intensive inflammatory reac-tion (see also p. 25).

Treatment

Severe ascaridoid infestations can be treatedby individual dosing with piperazine,

150–200 mg kg�1 of body mass. For masstreatment, the vermifuge is given in the food:Fenbendazole (100 mg ml�1), 2 ml kg�1 offood, or Oxfendazole (22.6 mg ml�1),5 ml kg�1 of food, both for 2–3 consecutivefeeds (Foggin, 1992a). For better mixing, thedrugs should be diluted in a small quantityof water.

Prevention

Crocodiles reared indoors and fed pelletedrations always are free of metazoan para-sites. Therefore the best preventive measureagainst ascaridoid infestations is not to feedinfected intermediate hosts to the crocodilesand not to allow live fish in the rearingponds. Where the feeding of locally caughtfish cannot be avoided, the larvae should bekilled by freezing the fish for 72 h and thaw-ing before feeding (Foggin, 1992a).

Capillarioids

Crocodilocapillaria longiovata

This is an apparently harmless parasite inthe stomach of C. porosus, C. johnsoni and C.novaeguineae (Ladds and Sims, 1990; Laddset al., 1995; Moravec and Spratt, 1998). The

194 Chapter 5

Fig. 5.39. Stomach of a wild-caught African dwarf crocodile, with ulcers inhabited by ascaridoids.

larvae, as well as adults, were found coiledin the gastric glands without apparent tissuereactions (Ladds et al., 1995). Similar nema-todes were found in the gastric glands ofwild-caught O. tetraspis (Fig. 5.41) (author’sown findings). At our present state of knowl-edge preventative action and treatment donot appear to be necessary.

Paratrichosoma spp.

These capillarioid parasites are found inzigzagging burrows in the ventral skin of

crocodiles (Fig. 5.42). Two species are knownso far: Paratrichosoma recurvum from C. acu-tus (Solger, 1877) and from Crocodylusmorelettii (Moravec and Vargas-Vásquez,1998), and P. crocodylus from C. novaeguineae(Ashford and Muller, 1978; Spratt, 1985) andC. porosus (Buenviaje et al., 1998). It is pre-sumed that similar worm trails commonlyfound in wild-caught C. johnsoni are causedby the same parasite (Webb and Manolis,1983).

These zigzagging cutaneous trails arefound in the skin of many crocodile species:


Fig. 5.40. Section of the gastric mucosa of a wild-caught African dwarf crocodile with ascaridoids pene-trating deep into the mucosa and surrounded by a strong inflammatory reaction.

Fig. 5.41. Section of the gastric mucosa of a wild-caught African dwarf crocodile with capillarioidnematodes in the mucosal glands.

● C. acutus (Solger, 1877);● C. intermedius (King and Brazaitis, 1971);● C. johnsoni (Webb and Manolis, 1983);● C. moreletii (Moravec and Vargas-

Vásquez, 1998);● C. niloticus (Foggin, 1987);● C. novaeguineae (Ashford and Muller,

1978);● C. palustris (Whitaker and Andrews, 1989);● C. porosus (Buenviaje et al., 1998).

In view of the wide range of affected croco-dile species and of their geographic distribu-tion, it is possible that more hithertoundescribed Paratrichosoma spp. might exist(Moravec and Vargas-Vásquez, 1998).

Little is known about the life cycle ofthese nematodes. The adult females arefound burrowing in the cellular layer of theepidermis where the eggs are laid. With theconstant formation of keratin, the old bur-rows containing the embryonating andembryonated eggs are slowly moved to thesurface of the keratin layer, where, eventu-ally, through abrasion, the eggs are voidedinto the environment (Elkan, 1974). On croc-odile farms the parasites are found only ifthe crocodiles are kept in earth ponds, possi-bly indicating a requirement for the larvae tospend some time outside the host (Foggin,1987).

It was assumed that after ingestion byanother crocodile the larvae undergo theirfirst development in the stomach beforemigrating to the skin (Solger, 1877; Elkan,1974). However, no signs of such migrationhave ever been described. Alternatively, it ispossible that the freed larvae penetrate theskin directly from outside through the softparts between the scales. In this they mightperhaps be assisted by leeches (personalcommunication, C.M. Foggin, Harare, 1999).Ashford and Muller (1978) found fourth-stage larvae already in the skin, andMoravec and Vargas-Vásquez (1998) foundmales and young females in deeper tissuesof the skin, where fertilization is likely totake place.

While not causing any inflammatory reac-tion and pathology, the parasites cause con-siderable damage to the skin and itscommercial value. However, no successfultreatment of the lesions or elimination of theworms have yet been described. The benzimi-dazole drugs could be tried for treating thecondition (personal communication, C.M.Foggin, Harare, 1999). If treatment is under-taken early enough and no re-infestationtakes place, the skin should be able to recover.The most important preventive measure isnot to rear the crocodiles in earth ponds.

196 Chapter 5

Fig. 5.42. Zigzag trails caused by Paratrichosoma sp. in the belly skin of a farmed Nile crocodile(specimen brought from Malawi by P. Watson).

Trichinellae

A Trichinella sp. morphologically identified asTrichinella spiralis was found in the meat offarmed crocodiles from 11 out of 17 farms inZimbabwe, mainly in the pterygoid, mandibu-lar and intercostal muscles (Fig. 5.43) (Fogginand Widdowson, 1996; Foggin et al., 1997).Larvae from affected crocodiles were infectiveto Zimbabwean domestic pigs (Mukaratirwaand Foggin, 1999) as well as to laboratory ratsand baboons (Foggin et al., 1997). However, inanother study, nine different Trichinella spp.isolates were found not to infect very youngcaimans (C. crocodilus) (Kapel et al., 1998).

The infestation of the farmed crocodilesmay have originated from infected venisonor from scavenging rodents caught by thecrocodiles. Treatment of infected crocodilesin the laboratory with albendazole,50 mg kg�1 live mass, by oral dosing twice at4-day intervals, removed the larvae from twocrocodiles, while in the third crocodile onlyvery few larvae could be detected in thepterygoid muscle after the treatment (Fogginet al., 1997). After freezing infected crocodilemeat at −18°C for 7 days it was no longerinfective to rats (Foggin et al., 1997).

The infestation of crocodiles can be pre-vented by feeding cooked meat or pelletedrations, in addition to strict rodent control.

See Notes Added at Proof, p. 210.

Gnathostoma

Third-stage larvae of Gnathostoma procyoniswere found in the muscles of two Americanalligators in Louisiana. The definitive host ofthis hookworm is the racoon (Ash, 1962) (seep. 199). This finding may have some implica-tions for the human consumption of alligatormeat.

Filariae

Parasite species

Several species of filariae have been found incrocodiles:

● Micropleura vazii free in the abdominalcavity of C. crocodilus (Travassos, 1933;Troiano et al., 1998b; Goldberg et al., 1991).

● M. vivipara from G. gangeticus (vonLinstow, 1906) and from C. niloticus(Foggin, 1987) – although the latter authormay not have been aware of Oswaldofilariaversterae of the Nile crocodile (see below).

● Oswaldofilaria bacillaris from the thoraxwall of C. crocodilus (Molin, 1858 – cited byTravassos, 1933; Prod’hon and Bain, 1972).

● O. kanbaya from connective tissues andserous membranes of the body cavity ofC. porosus (Manzanell, 1986).


Fig. 5.43. Trichinella sp. in the muscle of a farmed Nile crocodile (section sent from Zimbabwe by C.M. Foggin).

● O. medemi from Palaeosuchus trigonatus(Marinkelle, 1981).

● O. versterae from C. niloticus (Bain et al.,1982).

Unidentified filariae have been found free inthe abdominal cavity and under the pleuraof the lung in C. novaeguineae (Ladds andSims, 1990; Ladds et al., 1995).

Life cycle

The first-stage larvae, microfilariae, appearin the blood of the crocodilian host and areoccasionally found in blood smears (Fig.5.44) (Migone, 1916). They are ingested by amosquito intermediate host with a bloodmeal. The morphology and development ofthe microfilariae of O. bacillaris in the adiposetissue of the mosquito Anopheles stephensihave been described by Prod’hon and Bain(1972). The third-stage larvae are retransmit-ted to a crocodilian host by a subsequent biteby the mosquito.

Pathology

No lesions have ever been found associatedwith the presence of adult filariae in croco-diles. Possibly the larvae are more patho-genic for the mosquito, when they invade its

optical lobes and ommatids (Prod’hon andBain, 1972).

Eustrongylids

Immature specimens of Eustrongylides sp.have been found on the gastric serosa of C.porosus and C. novaeguineae (Ladds and Sims,1990; Ladds et al., 1995) as well as in C. croco-dilus, together with Contracaecum sp.(Goldberg et al., 1991). It is believed that bothare parasites of piscivorous birds, with fishesas intermediate hosts, and that the crocodilesare paratenic hosts only (Goldberg et al.,1991).

Rhabditids

Large numbers of rhabditids (Caenorhabditissp.) were found in bile ducts in the liver of acaptive O. tetraspis, provoking an intensiveinflammatory reaction (Figs 5.45 and 5.46).Only a piece of liver in formalin had beensubmitted for examination (Huchzermeyer etal., 1993). Rhabditids are not very special-ized, have a direct life cycle and can multiplyrapidly in captive situations. It is possiblethat the unidentified small nematodes

198 Chapter 5

Fig. 5.44. Microfilaria in crocodile blood (photograph M.A. Peirce).

(5 mm) found in the inflamed kidneys of agharial hatchling by Maskey et al. (1998)were also rhabditids.

Hookworm

There are only few reports of hookworms(Acanthocephala) in crocodilians. Polyacan-thorhynchus rhopalorhynchus was found aspart of the dominant helminth fauna para-sitizing C. crocodilus yacare in the BrazilianPantanal (Catto and Amato, 1994b), and

one juvenile specimen of Polymorphus muta-bilis, a parasite of fish-eating birds, wasfound in 1 out of 21 examined Cuban croco-diles (Groschaft and Barus, 1970). Oneadult unidentified hookworm was found ina survey of parasites of wild-caughtAfrican dwarf crocodiles (author’s ownmaterial).

In a survey of reptiles in Louisiana, twoout of four American alligators were foundto have Gnathostoma procyonis larvae in theirmuscles (Ash, 1962). This is a parasite of rac-coons in south-eastern USA. The alligators in


Fig. 5.45. Rhabditid in a bile duct in the liver of a captive Osteolaemus tetraspis surrounded by aninflammatory reaction.

Fig. 5.46. Rhabditid from the liver of a captive Afrian dwarf crocodile.

this case were acting as second intermediaryhosts (see also p. 197).

Trematodes

Crocodiles harbour a rich and varied faunaof digenetic trematodes, which have beenused to illustrate the co-evolution of thecrocodiles with their parasites (Brooks, 1979;Brooks and O’Grady, 1989). Monogenetictrematodes have been found as ectoparasites(see p. 209). The digenetic trematodes havetwo suckers with which they adhere to theintestinal wall (Fig. 5.47).

The species

The following host–parasite list is organizedfirst according to the site of the adult trema-tode in the host and secondarily in alpha-betical order irrespective of trematodesystematics, which should allow easy accessto names and references. This list is certainlyincomplete and not all quoted authors arenecessarily the ones who first discovered ordescribed the parasites. Also, the nomencla-ture of some of the parasites may havechanged in the course of ongoing revisions.As said before, the list is meant for easyaccess to references as a starting point forfurther research.

Trematodes found in the upper digestivetract (oral cavity, pharynx and oesophagus):

● Odhneriotrema incommodum in A. missis-sippiensis (Leigh, 1978).

● O. microcephala in C. crocodilus (Hugheset al., 1941; Catto and Amato, 1993a).

Trematodes found in intestine and cloaca:

● Acanthostomum atae in C. porosus(Tubangui and Masiluñgan, 1936).

● A. caballeroi in C. crocodilus (Caballero,1955).

● A. coronarium in A. mississippiensis(Hazen et al., 1978) and in C. acutus(Hughes et al., 1941).

● A. diploporum in A. mississippiensis(Hughes et al., 1941).

● A. elongatum in C. porosus (Tubangui andMasiluñgan, 1936).

● A. loossi in C. rhombifer (Groschaft andBarus, 1970; Brooks and Overstreet,1977) and C. acutus (Pérez Benítez et al.,1980).

● A. marajoarum in C. crocodilus (Hughes etal., 1941).

● A. pavidum in A. mississippiensis (Brooksand Overstreet, 1977).

● A. productum in C. niloticus (Hughes et al.,1941).

● A. quaesitum in C. johnsoni (Hughes et al.,1941; Brooks and Blair, 1978).

200 Chapter 5

Fig. 5.47. Digenetic trematode from a Nile crocodile, the position of the two suckers indicated by arrows.

● A. scyphocephalum in C. crocodilus(Caballero, 1955).

● A. vicinum in C. niloticus (Hughes et al.,1941).

● Allechinostomum crocodili in C. niloticusand in Crocodylus siamensis (Hughes et al.,1941).

● Archaeodiplostomum acetabulatum in A.mississippiensis (Brooks et al., 1977; Hazenet al., 1978).

● Atrophocaecum acuti in C. rhombifer(Groschaft and Barus, 1970).

● A. americanum in C. rhombifer (Groschaftand Barus, 1970).

● A. caballeroi in C. rhombifer (Groschaftand Barus, 1970).

● Caimanicola marajoira in C. crocodilus(Catto and Amato, 1993a, 1994b).

● Capsulodiplostomum crocodilinum in C.palustris (Dwivedi, 1966).

● Crocodilicola caimanicola in C. latirostris(Dollfus, 1935).

● C. gavialis in G. gangeticus (Hughes et al.,1941).

● C. pseudostoma in A. mississippiensis(Byrd and Reiber, 1942; Brooks et al., 1977)and in Crocodylus sp. (Hughes et al., 1941).

● Cyatocotyle brasiliensis in C. crocodilus(Catto and Amato, 1994b).

● C. crocodili in C. johnsoni (Ladds andSims, 1990) and C. porosus (Ladds et al.,1995).

● C. fraternae (fraterna?) in C. niloticus(Hughes et al., 1941; Bisseru, 1957).

● Cystodiplostomum hollyi in C. latirostris(Dubois, 1948) and C. crocodilus (Hugheset al., 1941; Catto and Amato, 1994a,b).

● ‘Diplostome’ medusae in C. crocodilus(Hughes et al., 1941).

● Distoma pyxidatum in C. crocodilus(Hughes et al., 1941).

● Echinostoma jacaretinga in C. crocodilus(Hughes et al., 1941).

● Exotidendrium gharialii in G. gangeticus(Hughes et al., 1941).

● Harmotrema nicollii in G. gangeticus(Hughes et al., 1941).

● H. rudolphii in C. porosus (Tubangui andMasiluñgan, 1936).

● Herpetodiplostomum caimanicola in C.crocodilus (Hughes et al., 1941; Catto andAmato, 1994a,b), in C. latirostris (Hughes

et al., 1941) and in M. niger (Hughes et al.,1941).

● Mesodiplostomum gladiolum in C. croco-dilus (Catto and Amato, 1994a) and in M.niger (Hughes et al., 1941).

● Neodiplostomum crocodilorum in C. poro-sus (Tubangui and Masiluñgan, 1936).

● N. gavialis in G. gangeticus (Narain, 1930).● Neodiplostomum sp. in C. cataphractus

(Hughes et al., 1941).● Neoparadiplostomum kafuensis in C.

niloticus (Bisseru, 1956).● N. magnitesticulatum in C. niloticus

(Bisseru, 1956).● Neostrigea africana in C. niloticus

(Bisseru, 1956).● N. leiperi in C. niloticus (Bisseru, 1956).● Nephrocephalus sessilis in C. niloticus

(Hughes et al., 1941).● Oistosomum caduceus in a ‘Krokodil’

(Hughes et al., 1941).● Pachypsolus constrictus in C. crocodilus

(Hughes et al., 1941).● P. sclerops in C. crocodilus (Catto and

Amato, 1993a).● Paradiplostomum abbreviatum in C. croc-

odilus (Hughes et al., 1941; Catto andAmato, 1994a,b) and in Crocodylus sp.(Hughes et al., 1941).

● Polycotyle ornata in A. mississippiensis(Byrd and Reiber, 1942; Brooks et al., 1977;Hazen et al., 1978).

● Proctocaecum dorsale in C. crocodilus(Catto and Amato, 1993a,b).

● Prolectithidiplostomum cavum in C. croc-odilus (Hughes et al., 1941).

● P. constrictum in C. crocodilus (Brooks etal., 1977; Catto and Amato, 1994a,b).

● Prostrigea arcuata in C. niloticus (Bisseru,1956).

● Proterodiplostomum breve in C. crocodilus(Catto and Amato, 1994a,b).

● P. globulare in C. crocodilus (Catto andAmato, 1994a,b).

● P. longum in C. crocodilus (Catto andAmato, 1993a, 1994a), in Crocodylus sp.(Hughes et al., 1941) and in M. niger(Hughes et al., 1941).

● P. medusae in C. crocodilus (Brooks et al.,1977; Catto and Amato, 1994a,b).

● P. tumidilum (tumidulum?) in C. crocodilus(Hughes et al., 1941; Catto and Amato,1994a,b).


● Pseudocrocodilicola americana in A. mis-sissippiensis (Byrd and Reiber, 1942; Hazenet al., 1978).

● P. georgiana in A. mississippiensis (Byrdand Reiber, 1942; Brooks et al., 1977).

● Pseudoneodiplostomum acetabulata in A.mississippiensis (Byrd and Reiber, 1942).

● P. bifurcatum in C. niloticus (Dubois, 1948)and O. tetraspis (Huchzermeyer andAgnagna, 1994) (Fig. 5.48).

● P. dollfusi in C. siamensis (Dubois, 1948).● P. siamense in C. siamensis (Hughes et al.,

1941).● P. thomasi in C. cataphractus and O.

tetraspis (Dubois, 1948).● Pseudoneodiplostomum sp. in C. rhomb-

ifer (Groschaft and Barus, 1970).● Pseudotelorchis caimanis in C. crocodilus

(Catto and Amato, 1993b, 1994b).● P. yacarei in C. crocodilus (Catto and

Amato, 1993b, 1994b).● Stephanoprora jacaretinga in C. crocodilus

(Catto and Amato, 1994b).● S. ornata in C. niloticus (Hughes et al.,

1941).● Timoniella absita in C. porosus (Blair et al.,

1988).

Trematodes found in the kidneys:

● Deurithitrema gingae in C. porosus (Blair,1985).

● Deurithitrema sp. in C. porosus or C.novaeguineae (Ladds and Sims, 1990).

● Exotidendrium sp. in Nile crocodiles(Foggin, 1992a).

● Plagiorchid flukes, previously unde-scribed, in C. novaeguineae (Ladds et al.,1995).

● Renivermis crocodyli in C. porosus (Blairet al., 1989).

Trematodes found in blood vessels:

● Griphobilharzia amoena in C. johnsoni(Platt et al., 1991).

● Undetermined ‘blood flukes’ in C. poro-sus and C. novaeguineae (Lads and Sims,1990; Ladds et al., 1995).

Trematodes found in the lungs:

● Undetermined trematodes and ova foundin a granuloma in the lungs of a captiveG. gangeticus (Griner, 1983).

Life cycle

All the above trematodes probably needtwo intermediate hosts, one invertebrate,such as small crustaceans or snails, and thesecond one a fish. However, the completedetails have not been worked out for any ofthem.

Pathogenicity and pathology

There does not appear to be any pathologyassociated with infestations of intestinal

202 Chapter 5

Fig. 5.48. Pseudoneodiplostomum bifurcatum from a wild-caught African Dwarf crocodile in the CongoRepublic.

flukes. While Pérez Benítez et al. (1980)report high infestations with Acanthostomumloossi, associated with poor growth and highmortality, in farmed Cuban crocodiles, it islikely that other factors related to farmingconditions and nutrition played a decisiverole in the poor performance. No histopatho-logical lesions were reported. Unless infestedfish are fed, there is no possibility for highinfestations to establish themselves incaptive or farmed crocodiles.

Leigh (1978) studied the modifiedhost–parasite junction at the attachment siteof Odhneriotrema incommodum in the oralmucosa. However, the nodule of fibrous con-nective tissue sloughs off after re-attachmentof the parasite. Usually, the presence ofblood and renal flukes was not accompaniedby marked tissue reactions, although cases ofpyelonephritis may have been caused by thelatter (Ladds and Sims, 1990; Ladds et al.,1995). The unidentified trematode found inthe lung of a captive crocodile (species notstated) was surrounded by a granulomatousreaction (Griner, 1983).

Treatment and prophylaxis

In the absence of severe pathogenicity, thereshould be no need for treatment. Captive andfarmed crocodilians can be protected frominfestation by not feeding fresh intermediatehosts, river fish from waters inhabited bywild crocodiles. If such fish are to be fed, theyshould be frozen thoroughly to kill larvae.

Tapeworm cysts

There are no published reports of adulttapeworms having been found in croco-diles, although Telford (1971) states that‘cestodes are commonly found in all groupsof reptiles’. Corrected later (Telford andCampbell, 1981), this fact remains unex-plained, as tapeworms occur in fish, inother reptiles, in birds and in mammals.One reason suggested is the very lowgastric pH of crocodiles, similar to thatfound in sharks, which also have notapeworms (personal communication, M.Penrith, Pretoria, 2002).

Larvae (plerocercoids) of the tapewormSpirometra erinacei were found in the meat offarmed C. johnsoni slaughtered in theNorthern Territory in Australia. The croco-diles had been reared in earth ponds. Sincehousing them in concrete pens the problemhas disappeared (Melville, 1988; Millan et al.,1997b). A single cestode larva was found deepin the gastric muscularis of a New Guinea orIndo-Pacific crocodile (Ladds and Sims, 1990).

A cestode larva was also found in a frag-ment of muscle attached to a piece of skin ofan African dwarf crocodile during a 1996survey of wild-caught crocodiles slaughteredat markets in the Congo Republic (Fig. 5.49)(author’s own unpublished finding). Anysuch survey in the future should include theexamination of muscle tissue.

Cestode larvae are killed by freezing themeat at −10°C for 24 h (Millan et al., 1997b).

Ectoparasites

Leeches

Leeches are oligochaete annelid worms withsuckers at both ends, allowing them a ‘head-over-tail’ motion while remaining attachedto the surface with alternate suckers. Theycan also swim freely with a slow undulatingmotion. The parasitic leeches bite throughthe skin or mucosa at the attachment site ontheir host and suck blood.

The species

The following species of leeches have beenfound on crocodiles; please note that thenames quoted may have been revised inmore recent taxonomic work (see NotesAdded at Proof, p. 210):

● Haementeria lutzi fed experimentally onC. crocodilus (Pessôa et al., 1972).

● Helobdella sp. on juvenile (<1 m totallength) C. latirostris (personal communica-tion, A. Larriera, Santa Fe, 2002).

● Hirudinaria manillensis, the buffaloleech, from larynx and lung of an Indo-Pacific crocodile (Jeffery et al., 1990).

● Philobdella gracilis from American alli-gators (Viosca, 1962).


● Placobdella multilineata from theAmerican alligator (Forrester and Sawyer,1974; Glassman et al., 1979; Khan et al.,1980; Cherry and Ager, 1982) and a cap-tive Indo-Pacific crocodile in China (Yangand Davies, 1985).

● Placobdella papillifera from Americanalligators (Smith et al., 1976).

● Placobdelloides multistriatus from theNile crocodile (Johansson, 1909; Moore,1938; Oosthuizen, 1991), apparently aquite common parasite throughout Africa(Hippel, 1946; Flamand et al., 1992).

Pathogenicity

The parasites attach to the oral mucosa, par-ticularly the upper pits made by the croco-diles’ lower teeth (Smith et al., 1976) and tothe skin: eyelids, external ears under the earflaps, ventral aspect of the neck, axillaryregion. Only Hirudinaria manillensis, the buf-falo leech, was found in the respiratory tract(Jeffery et al., 1990), and may cause suffoca-tion due to its size.

At one stage it was believed thatPlacobdella multilineata was able to transmithaemogregarine infections (see p. 188).However, Khan et al. (1980) could not provethis mode of transmission. The buffalo leech

has been shown to be able to transmit rinder-pest to water buffalos (Wharton, 1913).Similarly, leeches could play a role in thetransmission of crocodile-specific viral andbacterial infections.

American alligators infested with leecheshad significantly elevated eosinophil levels,which returned to normal within 6 weeksafter the removal of the leeches (Glassman etal., 1979). On C. johnsoni, leeches were foundcongregating in skin punctures in the axil-lary region and, as there were no such der-mal punctures in crocodiles without leeches,it was concluded that the leeches might becausing these dermal lesions (Webb andManolis, 1983).


Leeches are very sensitive to salinity (Telfordand Campbell, 1981). Adding common salt(NaCl) to the water, probably 0.5%, shouldhelp to eliminate most leeches from aninfested pond. Flamand et al. (1992) recom-mend dabbing attached leeches with alcoholor methylated spirits on a cotton swab.

A variety of treatments for use againstleeches on fishes are given by Burreson(1995). Most of these are for short-timeimmersion, as used on fish farms, and nonehas actually been tried on crocodiles:

204 Chapter 5

Fig. 5.49. Cestode larva in the nuchal muscle of a wild-caught African dwarf crocodile slaughtered at amarket in the Congo Republic.

● NaCl 2.5% for 1 h;● 200 g quicklime per 100 l for 5 s;● a 0.2% solution of Lysol or 0.4% solution

of Priasol for 5–15 s;● a 0.005% solution of cupric chloride for

15 min;● a 0.1% solution of Dylox 10 kills leech

embryos but is toxic to fish (crocodiles?);● Masoten 1 g in 4 m3 of water.

All new acquisitions of captive crocodilesshould be checked very carefully beforereleasing them into their new enclosures,and the same applies to terrapins (freshwaterturtles), which frequently carry the samespecies of leeches, if they are to be kept with,or in close proximity to, the crocodiles. Theintroduction of Placobdella multilineata toChina with the importation of American alli-gators (Yang and Davies, 1985) demonstratesthis danger.

Biting insects

Diptera

Many biting flies and mosquitos may befeeding on crocodiles. However, few of thesehave been studied, mainly as vectors of otherparasites:

● The mosquito Anopheles stephensi wasfound to act as intermediate host forOswaldofilaria bacillaris of C. crocodilus(Prod’hon and Bain, 1972) (see p. 197).

● The mosquito Culex dolosus transmitsHepatozoon caimani (see p. 188) (Pessôa etal., 1972).

● The tsetse fly Glossina palpalis transmitsHepatozoon pettiti (see p. 188) as well asTrypanosoma grayi (see p. 191) (Chattonand Roubaud, 1913; Hoare, 1931, 1932).

Other insects

In failed experiments to transmit Hepatozooncaimani, 25 nymphs of the bug Triatoma infes-tans were placed into the caiman enclosureand two of them actually did feed on thecaimans (Pessôa et al., 1972). The bug trans-mits Chagas disease to people (Schofield,2001) but is unlikely to parasitize crocodil-ians in the wild.

Ticks and mites

Ticks

Ticks are found occasionally on crocodiles,but no ticks habitually feed on crocodiles.Therefore they are unlikely to play a role inthe transmission of infectious agents, as theydo so commonly in birds and mammals. Thefollowing summarizes the few publishedreports of ticks found on crocodiles:

● Amblyomma dissimile on C. moreletii(Rainwater et al., 2001).

● Amblyomma (?) grossum on crocodiles(species not given) in Surinam(Neumann, 1899).

● Amblyomma sp. on C. johnsoni (Tucker,1995).

● Amblyomma sp. on C. moreletii(Rainwater et al., 2001).

● Aponomma exornatum. Two male speci-mens found on a crocodile (species notgiven) in the Katanga Province of theCongo (now Democratic Republic of theCongo) (Schwetz, 1927a,b).

Mites

While mites are common ectoparasites onother reptiles, there are no published reportsof mites on crocodiles.

Pentastomes

Classification and biology

Pentastomes are worm-like arthropods, afew millimetres to a few centimetres long,parasites of the respiratory system of rep-tiles, birds and mammals. An outline of theclassification of the Pentastomida preparedby J. Riley of the University of Dundee,Scotland, is shown in Table 5.7.

All crocodilian pentastomes have fishes as intermediate hosts, and in their finalcrocodilian hosts most inhabit the lungs,except Leiperia, which is found in the trachea,and Subtriquetra, which inhabits the nasalpassages.


206C

hapter 5

Table 5.7. Outline of the classification of the phylum Pentastomida.

Order Family Genus No. of species Definitive host Intermediate host

Cephalobaenida Cephalobaenidae Cephalobaena 1 Snakes ?Raillietiella >35 Snakes, lizards, Direct (?), insects, amphibians,

amphisbaeniens, amphibians lizardsReighardiidae Reighardia 2 Marine birds Direct (1 sp.)

Porocephalida Sebekidae Sebekia 12 Crocodilians (Chelonians) Fish (snakes, lizards?)Alofia 5 Crocodilians FishLeiperia 2 Crocodilians FishDiesingia 1 Chelonians ?Selfia 1 Crocodilians FishAgema 1 Crocodilians Fish

Subtriquetridae Subtriquetra 3 (?) Crocodilians FishSambonidae Sambonia 4 Monitor lizards Direct (1 sp.)

Elenia 2 Monitor lizards Amphibians, mammalsWaddycephalus 10 Snakes Amphibians, reptiles, mammalsParasambonia 2 Snakes Amphibians, reptiles, mammals

Porocephalida Porocephalus 8 Snakes Snakes, mammalsKiricephalus 5 Snakes Amphibians, lizards, mammals,

snakesArmilliferidae Armillifer 7 Snakes Mammals

Cubirea 2 Snakes ?Gigliolella 1 Snakes Mammals

Linguatulidae Linguatula 6 Mammals Direct (1 sp.), mammals

Host–parasite list

The following host–parasite list of crocodil-ian pentastomes was prepared by John Rileyof the University of Dundee, Scotland.

ALLIGATOR MISSISSIPPIENSIS

● Sebekia mississippiensis (Overstreet et al.,1985).

CAIMAN CROCODILUS

● Alofia platycephala (Lohrmann, 1889;Giglioli, 1922).

● Sebekia trinitatis (Riley et al., 1990).● Sebekia microhamus (Self and Rego, 1985).● Subtriquetra subtriquetra (Diesing, 1835;

Sambon, 1922).

CAIMAN LATIROSTRIS

● A. platycephala.

MELANOSUCHUS NIGER

● S. subtriquetra.

CROCODYLUS ACUTUS

● Sebekia divestei (Giglioli, in Sambon, 1922).

CROCODYLUS NILOTICUS

● Alofia nilotici (Riley and Huchzermeyer,1995a).

● Leiperia cincinnalis (Sambon, 1922).● Sebekia wedli (Giglioli, in Sambon, 1922).● Sebekia cesarisi (Giglioli, in Sambon, 1922).● Sebekia okavangoensis (Riley and Huch-

zermeyer, 1995a).● Subtriquetra rileyi (Junker et al., 1998).

CROCODYLUS CATAPHRACTUS

● Agema silvaepalustris (Riley et al., 1997).● S. okavangoensis.

CROCODYLUS POROSUS

● Alofia ginae (Giglioli, 1922).● Alofia merki (Riley, 1994).● Leiperia australiensis (Riley and Huch-

zermeyer, 1996).● Sebekia multiannulata (Riley et al., 1990).

● Sebekia purdiae (Riley et al., 1990).● Selfia porosus (Riley, 1994).

CROCODYLUS PALUSTRIS

● Subtriquetra megacephala (Baird, 1853;Sambon, 1922).

CROCODYLUS JOHNSONI

● L. australiensis.● Sebekia johnstoni (Riley et al., 1990).● S. multiannulata.● S. purdiae.

CROCODYLUS NOVAEGUINEAE

● Sebekia novaeguineae (Riley et al., 1990).

CROCODYLUS SIAMENSIS

● Sebekia jubini (Vaney and Sambon, 1910;Sambon, 1922) (species inquirenda).

OSTEOLAEMUS TETRASPIS

● S. okavangoensis.● A. silvaepalustris.● Alofia parva (Riley and Huchzermeyer,

1995b).

GAVIALIS GANGETICUS

● Alofia indica (Hett, 1924) or ● Sebekia indica (Heymons, 1941).

PENTASTOMID SPECIES FROM UNDETERMINED

CROCODILE SPECIES

● Alofia simpsoni (Riley, 1994) from anunknown crocodile in Ghana.

● Sebekia acuminata (Travassos, 1924) froman unknown crocodile in Brazil.

● Sebekia samboni (Travassos, 1924) from anunknown crocodile in Brazil.

● Subtriquetra shipleyi (Hett, 1924) from thepharynx of an unknown Indian crocodile.

Pathogenicity and pathology

In the lungs the parasites suck blood andthereby can cause infection and inflamma-tion. Sometimes large numbers of these para-


sites can be found in crocodile lungs withoutany signs of tissue reaction (Fig. 5.50), whilein other cases large lung abscesses are foundassociated with their presence. This is proba-bly due to the state of nutrition and the gen-eral state of health of the host, as well asfreedom from stress. In cases of stress septi-caemia (see p. 228), the bacteria present inthe blood can invade the lung tissue in thelesions caused by the pentastomes, and thuscreate the abscesses found associated withpentastome infestations. The frontal and sub-parietal glands of the pentastomes continu-ously secrete a surface membrane that coversvital areas of the host–parasite interface, andthis is believed to protect the parasites fromthe host’s strong immune response (Riley etal., 1979).

No lung lesions were found in 21 wild-caught O. tetraspis in the Congo Republic,which all had various numbers of pentas-tomes in their lungs (Huchzermeyer andAgnagna, 1994). Even high numbers of Alofiaplatycephala were not associated with anylung lesions in captive C. crocodilus nor infarmed caimans in Argentina (Troiano andRomán, 1996; Troiano et al., 1996b).

In C. johnsoni and C. novaeguineae, thelesions associated with pentastomes con-sisted either of consolidation of the lungs orsmall, dark foci beneath the pleura (Laddsand Sims, 1990; Ladds et al., 1995). The

histopathological lesions consisted of exten-sive interstitial pneumonia, bronchiectasisand hyperplasia of the bronchiolar epithe-lium (Ladds and Sims, 1990).

Wild-caught American alligators sufferingfrom steatitis (see p. 219) appeared to havedied from massive lung haemorrhage, withblood also in the stomach and intestines,apparently caused by the migration of theadult Sebekia oxycephala through the lungserosa (Deakins, 1971). Farmed Americanalligator hatchlings fed with live mosquitofish (Gambusia affinis) developed respiratoryproblems and began dying within 2 weeks.On post-mortem examination they hadsevere haemorrhages into the lungs, andlarge numbers of S. oxycephala were found inthe lungs (Boyce et al., 1984).

The fact that no pentastomes were foundin wild American alligators under 40 cmlength, and increasing numbers of the para-sites with increasing length (Moreland et al.,1989), may be due to the initial prevalenceof insectivorous behaviour in crocodilianhatchlings, with a gradual change-over topiscivory. It is possible that a slow build-upof parasite numbers with age allows theestablishment of a balance between hostand parasites (Moreland et al., 1989), but itcould also be that sick and dying juvenilealligators are removed from the scene bycannibalism.

208 Chapter 5

Fig. 5.50. Lung section of a Nile crocodile with a pentastome in an air passage. Note the absence of anytissue reaction.

Diagnosis

In severe infestations, pentastome eggs maybe found in the host’s faeces. On post-mortemexamination the parasites are found in thelarger air passages of the lungs. In a fresh,dead crocodile, the suffocating pentastomeswill come crawling out of cuts that have beenmade into the lung tissue (Figs 5.51 and 5.52).The high oxygen requirements and conse-quent air-seeking behaviour of pentastomeswere described by Self and Kuntz (1967).

Treatment

Groups of captive crocodiles with knownsevere pentastome infestation may have tobe treated. One problem here consists of thefact that few drugs have actually been testedon crocodiles, and that there may well bespecies differences in the sensitivity of croco-diles to various drugs. The antiparasiticDectomax® (doramectin 1%) has been triedout on Nile crocodiles, and the dose of 1 mlper 50 kg of body mass was found safe andeffective (personal communication, C.M.Foggin, Harare, 2001), while ivermectin ateffective doses is toxic (see pp. 89 and 225).

Prevention

For the prevention of pentastome infesta-tions, one has to bear in mind that fish arethe intermediate hosts. Where fish from croc-odile waters are to be fed to farmed or cap-tive crocodiles, such fish should be frozensolid or boiled to kill the parasite larvae.Keeping live food fish in a crocodile breed-ing pond or exhibit should also be avoided,unless in such a case the crocodiles receivean antiparasitic treatment from time to time,say once a year.

The prevention of stress is of majorimportance for allowing the crocodiles toovercome occasional bacterial infectionscaused by the pentastomes, and thereby pre-venting the formation of lung abscesses.

Monogenetic trematodes

Monogenetic trematodes have been foundwithin green slimy masses attached to theinterdigital web and between the scales on the hind limbs of farmed crocodiles. The species was not determined(Youngprapakorn et al., 1994). Monogenetic


Fig. 5.51. Pentastomes crawling out of an incised lung of a Nile crocodile.

trematodes are common ectoparasites onfishes, feeding on the mucus covering thepiscine skin. It is possible that the specimensfound in these cases were fish parasites find-ing a suitable medium in the slimy matter onthe skin of the crocodiles, as the crocodile’sepidermis normally would offer little attrac-tion to these trematodes. The ‘long flagellae’of the protozoa present in the same slimemass were most likely the polar filaments ofMyxobolus sp. which are protozoan ectopara-sites of fishes.

Notes Added at Proof

Embryonic cell lines (page 157)

Several crocodilian fibroblast cell lines havebeen established recently at San Diego Zoo(personal communication, V.A. Lance, SanDiego, 2002).

West Nile virus (page 163)

An outbreak of West Nile virus infection hasbeen diagnosed in american alligators in theUSA (personal communication, E.R.Jacobson, Gainesville, 2003).

Trichinella (page 197)

The crocodile parasite has been identified asTrichinella zimbabwensis by Pozio et al. (paperin press, International Journal of Parasitology)(personal communication, E. Pozio, Rome,2003).

Leeches (page 203)

Placobdelloides stellapapillosa was found onCrocodylus porosus and Tomistoma schlegelii inSingapore Zoological Gardens (Govedich etal., 2002).

210 Chapter 5

Fig. 5.52. Pentastomes collected from the lungs of a Nile crocodile.

Nutritional Diseases

In the wild, crocodiles eat a varied diet thatsupplies their nutritional needs but usuallysustains a slow growth rate (see p. 98).Captive crocodiles frequently are given amonotonous diet, which may be deficient inone or more essential constituents. Farmedcrocodiles usually are pushed for a fastgrowth rate, and this can further accentuatepotential imbalances in their artificial nutri-tion. This may lead to deficiencies of certainminerals and vitamins, and consequent dis-ease and mortality.

Nutritional bone disease

Synonyms

Nutritional bone disease is an umbrella termthat covers a range of related conditions andnames, such as osteomalacia, rickets, sec-ondary hyperparathyroidism, metabolicbone disease, fibrous osteodystrophy andosteoporosis. The umbrella term ‘nutritionalbone disease’ indicates the importance ofnutritional factors in this condition.Metabolic bone disease shifts the emphasisto calcium (Ca) and phosphorus (P) metabo-lism. Secondary hyperparathyroidism placesthe accent on the role of the parathyroids in

Ca and P metabolism. Osteomalacia andfibrous osteodystrophy are the terms for thecondition in young hatchlings where theirbones fail to harden due to the lack of cal-cium. Rickets applies to malformations of thegrowing bone when due to the lack of vita-min D3, the bones also fail to harden andbecome bent. Osteoporosis occurs in olderjuvenile and adults, where the already hard-ened bone structure becomes weakened bythe withdrawal of calcium for metabolicneeds. See Note Added at Proof, p. 239.

Causes

The most common cause of metabolic bonedisease in young crocodiles is feeding withred meat without bone, or with an insuffi-cient calcium supplement. This may beaggravated by a lack of vitamin D if the croc-odiles are kept indoors. Vitamin D3 levels inthe ration or in supplements can also deteri-orate during prolonged storage under tropi-cal conditions (Foggin, 1992a). However, animbalance between calcium and phosphorusin any kind of ration can cause metabolicbone disease, although at a much slowerrate. Malabsorption of calcium due to exces-sive phosphorus levels, or due to the pres-ence of other minerals, can also cause thesame condition.

Chapter 6

Non-transmissible Diseases


Symptoms

In affected hatchlings the first signs seen area weakness and sluggishness. The animalsbecome unable to walk on land, while theystill can swim. Soon the contractions of thelong back muscles cause distortions of thevertebral column, kyphoscoliosis (Fig. 6.1)(Cardeilhac, 1981; Tulasi Rao et al., 1984;Huchzermeyer, 1986; Matushima andRamos, 1995; Troiano and Román, 1996;Boede, 2000). On examination the bonesare found to be pliable, particularly thejaw bones – ‘rubber jaws’ (Fig. 6.2)(Huchzermeyer, 1986; Foggin, 1992a). Theteeth may fall out (Cardeilhac, 1981;Matushima and Ramos, 1995) or, more fre-quently, become diaphanous, like shards ofglass – ‘glassy teeth’ (Huchzermeyer, 1986) –and they may be pushed sideways into ahorizontal position (Fig. 6.3) (Jacobson, 1984)(see also p. 247). The underlying hypocal-caemia may cause tremors or seizures, par-ticularly when the crocodiles are beingdisturbed (Foggin, 1992a), and such seizuresmay lead to drowning, if they occur in thewater. In older juveniles with less pliant ver-tebrae, these seizures may cause fractures ofthe spinal column (Figs 6.4 and 6.5), withconsequent posterior paralysis (Foggin,1987).

Osteoporosis in older juveniles is clini-cally associated with poor calcification of theteeth (see Fig. 6.9), but locomotion of theaffected individuals does not appear to beadversely affected.

Pathology

On post-mortem examination, the bones ofaffected hatchlings are found to be very softand they are easily cut with a scalpel. Thecurvature of the spine will be obvious (Fig.6.6), as will be fractures of thoracic vertebrae(Figs 6.4 and 6.5), which may be associatedwith urine retention in the distended colondue to the posterior paralysis (Fig. 6.7). Alongitudinal cut through the vertebral col-umn may reveal compression of the spinalcord (Foggin, 1992a). Histopathology of theparathyroid glands may show proliferationand cystic degeneration (Fig. 6.8) (see alsop. 275).

Diaphanous teeth have also beenobserved in juvenile and even adult farmedNile crocodiles (Fig. 6.9). Concomitant lesionson the long limb bones were found inciden-tally in slaughter crocodiles, and are clearlyindicative of osteoporosis. The bones are verylight and show marked areas of erosion, par-ticularly close to the heads (Fig. 6.10). The

212 Chapter 6

Fig. 6.1. Persisting kyphoskoliosis in a juvenile Nile crocodile after recovery from osteomalacia.

Non-transmissible Diseases 213

Fig. 6.2. ‘Rubber jaws’ and ‘glassy teeth’ in a Nile crocodile hatchling with osteomalacia.

Fig. 6.3. Horizontal displacement of the teeth in a juvenile Nile crocodile that had suffered fromosteomalacia.

condition occurs on many crocodile farms inSouth Africa (author’s own cases) and hasalso been reported from Colombia (Blanco,1997).


For the treatment of nutritional bone disease,it is necessary to rectify the diagnosed defi-ciency, usually that of calcium. If the affectedhatchlings are too weak to feed by them-selves, they can initially be dosed or injected

intraperitoneally (ip) with calcium boroglu-conate (250 mg ml�1), 1.5 ml kg�1 body mass.The corrected ration should contain addi-tional calcium carbonate, dicalcium phos-phate or sterilized bonemeal, to give a finalcomposition containing 1.5–2% calcium and aCa:P ratio of 1.5:1.

For individual crocodile hatchlings keptby hobbyists, a good source of calcium andphosphorus is found in the scrapings from abutcher’s saw, while calcium alone can beobtained from ground eggshells (hens’ eggs).

214 Chapter 6

Fig. 6.4. Fractured spine in a juvenile Nile crocodile which suffered from seizures due to acute hypocal-caemia.

Fig. 6.5. Fractured thoracic vertebra, indicated by a subpleural haemorrhage, in a juvenile Nile crocodilewith acute hypocalcaemia.

Recovery takes place within a few daysfrom the start of dosing with extra calcium.The hatchlings become active again and thebones harden. However, deformities of the

spinal column and of the jaws (teeth grow-ing horizontally) will persist (Tulasi Rao etal., 1984; Huchzermeyer, 1986) (see alsop. 247).


Fig. 6.6. Deformed vertebral column in a Nile crocodile hatchling with osteomalacia.

Fig. 6.7. Urine-filled rectum in a juvenile Nile crocodile with fractured spine and posterior paralysis.

Parturition hypocalcaemia

During the production of the eggshells, thefemale mobilizes calcium from her bones. If,for some reason, this process does not func-tion perfectly, she may suffer from a hypocal-caemia, which in turn may interfere with thelaying process, cause unnecessary straining

and a prolapse of the uterus. This conditionmay not necessarily be caused by a latentcalcium deficiency and could rather be pre-cipitated by unusual weather conditions (seealso p. 265).

Treatment of the prolapse consists inimmobilizing the female with Flaxedil® orother muscle relaxant (see p. 70), cleaning

216 Chapter 6

Fig. 6.8. Parathyroid gland with cystic degeneration in a juvenile Nile crocodile hatchling suffering fromnutritional bone disease.

Fig. 6.9. Diaphanous teeth due to insufficient calcium deposition in an adult farmed Nile crocodile.

the prolapsed uterus, pushing it backthrough the cloaca and securing it with atobacco pouch suture, which is left in placefor 2–3 days (see also p. 265).

Vitamin A deficiency

Vitamin deficiencies occur when insufficientquantities of the various vitamins are present

in the bulk constituents of the ration, wheninsufficient levels of vitamins have beenadded to the ration, when the vitamins in thepremix have deteriorated during prolongedstorage on the farm or when the affected ani-mals are eating very small quantities ornothing at all. In most of these cases morethan one vitamin will be deficient, leading tomore complex symptoms. Hatchlings may beprotected from vitamin deficiencies by yolk-

derived stores in their liver, until these storeshave been used up (Ariel et al., 1997a). Allvitamin deficiencies can be treated by cor-recting the vitamin levels in the ration. Insevere cases individual crocodiles can beinjected with a specific vitamin preparationor a multivitamin suspension. Hatchlingscan also be dosed with a nutrient fluidenriched with the required vitamin(s) (seepp. 86 and 148).

Vitamin A deficiency has caused squa-mous metaplasia of the epithelium of thedorsal glands on the tongue of older croco-dile hatchlings. Macroscopically theselesions appeared as pale to whitish nodularlesions (Foggin, 1987, 1992a; Ariel et al.,1997a). Squamous metaplasia of the epithe-lium of the kidney tubules was seen in thesame hatchlings, together with an accumula-tion of uric acid crystals – gout (see p. 230)(Foggin, 1987, 1992a; Ariel et al., 1997a).Squamous metaplasia has also been found inthe conjunctivae (Foggin, 1987), althoughmuch of the conjunctivitis seen in Nile croco-dile hatchlings may, in fact, be due to, oraggravated by, chlamydiosis (see p. 167).Grossly deficient animals may develop

anasarca, generalized oedema (Foggin, 1987;Debyser and Zwart, 1991).

Thiamin deficiency

Thiamin (vitamin B1) is normally producedin sufficient quantities by the bacterialintestinal flora. Destruction of the intestinalflora by the unnecessary use of oral antibi-otics may remove this source of vitamins(Thurman, 1990). Low quantities of thiaminare normally present in meats and fish, butthe requirements for a fast growth rate mayoutstrip the naturally available vitamin sup-plies (Jubb, 1992). In addition, fish may con-tain a thiaminase that destroys the availablethiamin. Repeated thawing and re-freezingof the minced meat may also destroy the thi-amin present in the mince (Horner, 1988b;Jubb, 1992).

Outbreaks of thiamin deficiency havebeen reported in farmed Nile and Indo-Pacific crocodiles (Horner, 1988b; Jubb,1992). In both cases frozen and thawed horseor donkey meat was fed to the hatchlings.The Nile crocodiles showed depression, lack


Fig. 6.10. Osteoporosis: erosions on the articular head of a leg bone of a juvenile Nile crocodile.

of vocalization, paresis and quiveringspasms, with the head and neck stretchedout and lifted upwards (Horner, 1988b),while the Indo-Pacific hatchlings mainlyshowed a loss of righting reflex and slug-gishness, but with normal papillary reflexes(Jubb, 1992). Both cases may have been com-plicated by a Ca:P imbalance due to the feed-ing of horse or donkey meat, particularly thecase involving the Nile crocodiles, sinceHorner (1988b) also describes ‘softened anddegenerated lumbar vertebrae’ (see p. 211).

In suspected cases of thiamin deficiencyYoungprapakorn et al. (1994) saw a paralysisand inward twisting of the lower forelimbs,with the hands lying palm up.

The introduction of a more varied diet,and the supplementation with an appropri-ate vitamin premix, led to complete recoveryin all cases.

Vitamin C deficiency

Crocodiles, like most animals, can synthesizetheir own vitamin C, ascorbic acid, andtherefore symptoms of classical scurvy-likevitamin C deficiency are unlikely to be seen.However, under certain circumstances, suchas stress and infection, the vitamin C require-ments may exceed the body’s own produc-

tion. As a powerful scavenger of oxygen rad-icals, vitamin C, together with vitamin E,supports the function of leucocytes in therespiratory bursts during phagocytosis (thedestruction of invading bacteria) (Bendich,1990; Boxer, 1990). A direct protective actionof vitamin C against specific bacterial andprotozoan infections has been demonstratedin several fish species (Li and Lovell, 1985;Wahli et al., 1986; Chávez de Martínez andRichards, 1991) as well as in poultry (Gross,1992).

Ascorbic acid also supports the action ofnitric oxide in vascular endothelial cells andthereby helps to protect vascular integrity(Heller et al., 1999). Furthermore, ascorbicacid plays a role in the synthesis of corticos-teroids in the adrenal glands, and stress canlead to the depletion of ascorbic acid in theadrenals (Perek and Eckstein, 1959).Consequently, supplementary vitamin C canhelp to protect the animals against the conse-quences of stress.

Cases of ulcerative gingivitis, with bacter-ial and fungal complications, in farmed juve-nile Nile crocodiles (Fig. 6.11), which wererefractory to antibacterial treatment,responded rapidly to intramuscular (im)injections with vitamin C (± 25 mg per kglive mass, repeated after 48 h) and/or contin-uous feeding of vitamin C in the ration at

218 Chapter 6

Fig. 6.11. Nile crocodile hatchling with ulcerative gingivitis.

1 g kg�1 of feed (Huchzermeyer andHuchzermeyer, 2001) (see also p. 249). Thesupplementation of crocodile rations withascorbic acid at the above level is now a rou-tine recommendation in South Africa.

Vitamin K deficiency

Vitamin K plays a role in blood coagulationand a deficiency may cause prolonged bleed-ing from minor wounds or when replacingteeth (Thurman, 1990). The vitamin is nor-mally taken in with the intestinal contents ofthe prey. An exclusively meat diet, particu-larly horse or donkey, could lead to a vita-min K deficiency, and in all cases of severeinternal or external haemorrhage, the possi-bility of such a deficiency should be takeninto account. However, rodenticide (war-farin) poisoning should also be considered(see p. 224).

Vitamin E deficiency

In addition to its role in gonadal develop-ment and function, and to its vitamin C-likeoxygen radical scavenging function in theimmune response (see p. 218), vitamin E asantioxidant also protects against the toxiceffects of rancid fats, particularly fish oils. Insome of these functions vitamin E is sup-ported by selenium.

Steatitis – fat necrosis

Fat necrosis is due primarily to the toxicaction of rancid fish oils, which are oftenconsumed by farmed crocodiles fed fishwhich is not quite fresh any more, such asmarket left-overs. In the crocodile this causesthe fatty tissue to die and to undergo saponi-fication, to harden. The saponified fat isregarded by the body as foreign substanceand consequently elicits an inflammatoryreaction – steatitis. The hardened fat reducesthe motility of the animal. Saponification ofthe large intermuscular fat deposits in thetail may render the tail entirely immobileand the affected crocodile unable to swim,while the hardening of abdominal fat may

interfere with the motility of the intestines.Also, the saponified fat is no longer availableas source of energy. There may be acute mor-tality, but in other cases the affected croco-diles may be able to survive and continuegrowing until their slaughter. The inflamma-tion and necrosis of all fat deposits is called‘pansteatitis’.

Cases of fat necrosis have been reportedfrom American alligators (Wallach andHoessle, 1968; Wallach, 1970; Larsen et al.,1983), Caiman crocodilus (Wallach andHoessle, 1968; Frye and Schelling, 1973), Nilecrocodiles (Foggin, 1992a,b), a crocodile(unspecified) in Irian Jaya (Ladds et al., 1995)and Cuban crocodiles (Moliner et al., 2000b).

Clinically, the affected crocodiles mayappear sluggish. The strips of hardened fatin the tail can be palpated. On post-mortemexamination the hardened yellow or brown-ish fat surrounded by inflamed tissue cannotbe overlooked (Plates 14 and 15, and Fig.6.12). If fat necrosis is found at slaughter, thewhole carcases should be condemned.

There is no effective treatment to reversethe saponification of the fat. High doses ofvitamin E may help to arrest the process. Asprevention, only fresh fish should be given,if fish is the main source of nutrition for thecaptive or farmed crocodiles. Fatty fishesshould be avoided. In addition, a supple-ment containing adequate levels of vitamin Eshould be mixed into the ration (see p. 99).

White muscle disease

Inadequate amounts of vitamin E and sele-nium in the diet may cause certain musclesto degenerate – Zenker’s degeneration. Themuscles take on a white appearance – whitemuscle disease – and are unable to contract,causing the affected animal to be paralysed.Zenker’s degeneration (Fig. 6.13) was foundin a group of 1-year-old farmed Nile croco-diles in Botswana, which were unable towalk and presented with swollen upperarms and thighs. However, it was not possi-ble to pinpoint the cause of the deficiency,nor did injections with vitamin E and sele-nium lead to a rapid recovery (author’s ownunpublished findings). However, in a limitedtrial in Zimbabwe, Nile crocodile hatchlings


injected im with a selenium and vitamin Epreparation gained more weight during the2-month observation period than theuntreated controls (Foggin, 1987). Zenker’sdegeneration may have been the cause ofmuscular calcification described byYoungprapakorn et al. (1994). Degeneration

of the heart muscle was seen in one captivejuvenile gharial and thought to have beencaused by feeding fish that were not entirelyfresh (Maskey et al., 1998). White muscle dis-ease, together with pansteatitis, occurred infarmed Cuban crocodiles (Moliner et al.,2000b).

220 Chapter 6

Fig. 6.12. Fat body of a juvenile Nile crocodile with pansteatitis.

Fig. 6.13. Section of leg muscle of a farmed Nile crocodile with white muscle disease, Zenker’sdegeneration.

Cloacal ulcerations

Linear ulcerations of the cloaca, filled withyellow keratinized debris, encountered incrocodilians may also be caused by vitaminE deficiency (Wallach, 1971).

Poor reproductive performance

Fish-fed female alligators had significantlylower plasma vitamin E levels than nutria-fed and wild female alligators, and this maybe partially responsible for the lower rate offertility of the eggs of the fish-fed females,and generally for reproductive failure in fish-fed captive crocodiles (Lance et al., 1983).

Nutritional hypoproteinaemia

Matushima and Ramos (1995) describe anutritional hypoproteinaemia caused by alow protein diet in farmed caimans, but didnot specify the ingredients of such a diet.Clinically they saw paleness, muscularweakness, depression and anorexia, and, onpost-mortem, watery blood, generalizedoedema, hydropericardium, ascites anddiminished spleen size. In cases of prolongedanaemia they also saw necrosis of the liver.

All these symptoms and lesions are com-monly found in runting (see p. 234), whichdoes occur in spite of adequate rations beingoffered, rather being due to insufficientnutrient intake. In general it is quite unlikelythat crocodilians could be given a ration defi-cient in protein.

Zinc deficiency

Superficial erosion of the skin and decoloriza-tion often are seen in chronically ailing juve-nile crocodiles (see p. 241). Youngprapakornet al. (1994) suspect these cases to be causedby combined zinc and biotin deficiencies.

Poisoning

Poisoning occurs not only through the delib-erate or accidental ingestion of toxic sub-

stances, but also much more insidiouslythrough the slow accumulation of low levelsof agricultural and industrial pollutants fromupstream human activities. Being in anaquatic environment and at the top of thefood chain makes crocodiles particularly vul-nerable to the effects of pollution.Unfortunately, cases of mortality in wildcrocodiles often go unnoticed for long times,and it is usually not easy to collect adequatespecimens. The chemical analysis requiredfor the investigation of such cases needssophisticated laboratory facilities, which arelacking in many tropical countries. Theanalyses themselves are costly and funds arescarce anywhere in the crocodile world.

However, in a well-planned and fundedprogramme, crocodilian populations can beused to monitor levels of pollution(Cardeilhac et al., 1999a,b). Some of thereports below are rather about levels of cont-aminants found, sometimes multiple, thanactual cases of toxicity.

Heavy metals

Heavy metals may be naturally present inthe environment, or may originate fromindustrial activities. Both mercury and leadhave a tendency to bio-accumulate. The tol-erance of crocodilians to lead and mercurymay be very high. Only one case has beendocumented of an adult American alligator(total length 3.92 m), life-long resident in acontaminated reservoir, which was founddead and emaciated and had wet-mass mer-cury levels of 3.48 �g g�1 in the muscle,33.55 �g g�1 in the kidney and 158.85 �g g�1

in the liver (Brisbin et al., 1998).Levels of various elements found in the

tissues of wild American alligators and Nilecrocodiles are presented in Tables 6.1 and 6.2,and mercury levels in tissues of Americanalligators in Tables 6.3 and 6.4. Mercury wasalso found in the eggs of Morelet’s crocodilesin Belize (Rainwater et al., 1997).

Mercury levels in the meat are also ofconcern from a public health point of view(Hord et al., 1990; Brazaitis et al., 1996;Brisbin et al., 1998). From the tissue levelsin Tables 6.3 and 6.4 it becomes clear that,


222 Chapter 6

Table 6.1. Ranges of mean metal levels in alligator meat (Delaney et al., 1988), eggs (Heinz et al.,1991), embryos (Van Heeckeren et al., 1988) and liver, fat and tail muscle (Burger et al., 2000) fromdifferent lakes in Florida, USA, in �g g�1 wet basis.

Metal Meat Eggs Embryos Liver Fat Tail muscle

Aluminium 1.3–2.0 BDArsenic BD 0.041 0.0351 0.0241Beryllium BDCadmium 0.01–0.06 BD BD 0.127 0.0738 0.078Chromium 0.03–0.11 0.08–0.09 0.133 0.113 0.252Copper 0.28–6.03 0.32–0.78 0.29–0.53Iron 4.56–22.76 11–13 8.76–16.42Lead 0.04–0.12 BD–0.22 BD 0.00986 0.0196 0.0267Manganese 0.14–0.15 1.380 0.369 0.802Mercury 0.04–0.61 BD 0.108 0.010 0.057Molybdenum BDNickel 1.18–12.76Selenium 0.30–0.37 0.429 0.256 0.187Thallium BDVanadium BDZinc 14.20–36.0 5.6–7.6Tin 0.231 0.165 0.726

BD, below detection.Note that in their paper Burger et al. (2000) mistakenly equate p.p.b. with �g g�1.

Table 6.2. Ranges of mean metal levels in �g g�1 in frozen Nile crocodile tissues from three differentrivers in the Kruger National Park, South Africa (Swanepoel et al., 2000).

Metal Muscle Liver Kidney Fat

Al 73.5–367.8 175.2–487.6 40.8–360.6 55.6–367.6Cu 7.9–12.6 23.2–30.6 3.5–13.9 6.1–7.6Cr 9.8–90.5 5.1–69.0 0.7–82.0 14.6–105.4Fe 156.0–615.0 690.8–12,851.3 131.3–520.0 188.1–297.7Mn 0.1–17.8 0.1–15.5 0.12–17.6 0.1–18.7Ni 9.1–24.9 7.3–23.0 BD–28.9 12.8–31.2Pb BD–3.7 0–19.85 BD–9.7 BD–8.5Sr 6.7–26.7 6.6–24.4 8.0–32.5 6.9–23.2Zn 39.4–109.7 61.5–122.5 54.2–94.4 7.6–11.2

BD, below detection.

Table 6.3. Ranges of mean mercury levels in tissues of American alligators from different sites, in �g g�1

dry mass.

Tissue Yanochko et al. (1997) Jagoe et al. (1998) Hord et al. (1990)

Tail scute 5.12–6.33 0.29–5.83Claw 1.67–2.69Muscle 4.08–5.69 0.80–5.57 0.46–2.88Liver 17.73–42.15 4.30–41.03Kidney 35.00–38.46 4.82–36.42

contrary to feathers and hair, mercury doesnot appear to be concentrating in crocodilescales. Accordingly, there is no possibility ofnon-invasive sampling. Mercury may be pre-sent normally in aquatic environments ormay originate from agricultural, mining andgold extracting (amalgamate process) activi-ties (Brazaitis et al., 1996).

Lead levels in the blood of two clinicallynormal adult female false gharials and aCuban crocodile at New York ZoologicalPark were 147, 178 and 247 �g dl�1, respec-tively. The crocodiles had been fed withurban feral pigeons (Cook et al., 1988, 1989).The pollution of the urban environment withlead is mainly due to the exhaust fumes frommotor vehicles using leaded fuels.

An elevated serum zinc level of45.3 �g ml�1 was found in a Cuban crocodilethat had swallowed a number of coins. Afterremoval of the coins, with the help of acolonofibrescope fitted with retrieval forceps,the animal was treated with CaEDTA at40 mg kg�1 live mass every second day, sixtreatments in all. Thirty-nine days later, thezinc level had dropped to 4.88 �g ml�1

(Cook et al., 1989).Nothing is known of the toxicity of other

metals in crocodiles. Metal levels found inthe shells and soft contents of eggs ofCrocodylus acutus by Stoneburner andKushlan (1984) are presented in Table 6.5.

Pesticides

Some pesticides and similar industrialorganic compounds are very stable, or breakdown into stable compounds which can per-

sist in the environment for a very long time.They have a tendency to bio-accumulate andtherefore the crocodile, at the top of the foodchain, is particularly vulnerable. These cont-aminants have been found in crocodiliansamples from various populations in Africa,as well as in North and Central America(Hall et al., 1979; Wessels et al., 1980; Delaneyet al., 1988; Phelps et al., 1989; Heinz et al.,1991; Skaare et al., 1991; Cobb et al., 1997;Rainwater et al., 1997). Fatty fish, in particu-lar, have been blamed for being able to carryhigh loads of pesticides (Joanen andMcNease, 1979). Levels of polychlorinatedbiphenyls in the chorioallantoic membranesof neonatal American alligator hatchlingswere significantly correlated with concentra-tions in fat and yolk (Bargar et al., 1999).Accumulation of these compounds in the tis-sues may render the meat from such croco-diles unsuitable for human consumption.

After baiting with 10–5 bait (Mirex®)against fire ants, Solenopsis spp., residueswere found in tissues of American alligators.Two years later the levels were significantlyreduced (Wheeler et al., 1977). While grossdirect poisoning of crocodiles has not beendescribed, a most insidious effect of some ofthese compounds was discovered morerecently:

Endocrine disruption

Some of these compounds can mimic sexhormones and, at very low levels, can affect


Table 6.4. Mean tissue mercury levels ofAmerican alligators, wild from contaminated anduncontaminated habitats and farm-raised (in�g g�1 wet mass) (Heaton-Jones et al., 1997).

Non- Farm-Tissue Everglades Everglades raised

Liver 39.99 2.52 0.10Kidney 25.85 1.58 0.09Tail muscle 2.61 0.33 0.10Brain 1.37 0.16 0.08Leg scales 0.82 0.35 0.08

Table 6.5. Mean values of metals found in theshells and soft contents of Crocodylus acutuseggs (�g g�1 dry mass) (Stoneburner andKushlan, 1984).

Metal Shell Soft contents

Aluminium 52.36 10.86Cadmium 1.36 0.13Cobalt 1.70 1.12Chromium 20.46 2.64Copper 17.17 6.21Lead 16.42 3.35Mercury 0.21 0.66Molybdenum 25.43 2.37Nickel 22.04 2.35Strontium 529.50 45.65

the sex ratio of hatchlings, interfere with thedevelopment of sexual organs and generallyaffect the reproductive success of a crocodilepopulation in a contaminated environment.This effect has been documented for severallakes in Florida, USA (Woodward et al., 1993;Guillette et al., 1994, 1995a, 1996, 1999; Vonieret al., 1996; Crain et al., 1997, 1998; Cardeilhacet al., 1998; Crews and Ross, 1998; Matter etal., 1998). The most worrying fact here is thatthere is no safe level, that no threshold doseexists, as the mimicked substance already ispresent and the slightest addition to it is ableto affect the balance (Crews and Ross, 1998;Guillette and Milnes, 2001).

Radionuclides

Radioactive contaminants may accumulatein the vicinity of atomic power stations. Noill effects have been documented concerningcrocodilians living in contaminated reser-voirs, but the accumulation of radiocaesiumlevels in crocodile tissues could be of con-cern as far as human consumption of croco-dile meat is concerned (Brisbin et al., 1998).

Algicides

A captive spectacled caiman developed vis-ceral gout and died after its tank had beentreated with an algicide containing strepto-mycin (Jacobson, 1984) (see also below).

Rodenticides

No cases of rodenticide poisoning haveapparently been reported. However, mostrodenticides contain anticoagulants, whichremain active in the killed rats and can sub-sequently affect the predator catching andeating the poisoned rats. A monitor lizardresiding in the roof of our house died in thisway. Since rats are attracted into the croco-dile pens by left-overs of food, and are possi-bly eaten by crocodiles, there is the danger ofaccidentally poisoning young crocodiles,which most likely would die from massiveinternal haemorrhages (see p. 219).

Algal toxins

Algal toxins are released by blue algae,which tend to produce blooms under condi-tions of eutrophication, and in marine envi-ronments by marine algae causing ‘redtides’. No published reports could be foundof crocodiles having been affected by theseevents. However, the possibility exists ofcrocodiles being poisoned under such cir-cumstances, and this should be borne inmind when investigating deaths of croco-diles in the wild.

Fire ants

The fire ant, Solenopsis invicta, has, since itsintroduction into the USA, established itselfthroughout the south-eastern states, oftennesting in alligator nests. The effects of fireants on alligator eggs and hatchlings havebeen investigated by Allen et al. (1997). Assoon as eggs begin to crack, the ants canpenetrate the shell and consume the con-tents. Hatching alligators are bitten duringhatching, until they are taken by themother and placed into the water. Whenthe hatching process was fast, the effects ofthe bites were not too severe. Swellingsoccurred mainly around the eyes and onthe extremities.

Botulism

Botulism is caused by the toxins ofClostridium botulinum. The agent growsunder anaerobic conditions in the mud ofeutrophicated water bodies or in cadavers. Itremains active in animals that have diedfrom botulism. In the mud the toxin is accu-mulated by invertebrates and, when takenup by water fowl, can produce heavy mortal-ity amongst these birds. The toxins cause aflaccid paralysis of all limbs as well as theneck. If the type of toxin can be determined,the patient can be treated with the appropri-ate antitoxin.

A case of suspected botulism in 8 out of800 juvenile Indo-Pacific crocodiles wasreported by Youngprapakorn et al. (1994).

224 Chapter 6

The animals were paralysed and lackedpupillar reflexes, but they also sufferedfrom spasms, causing the limbs to becomerigid. The report therefore has to be treatedwith some caution. One of the photographsshows an animal with very diaphanousteeth, indicating that this might, in fact,have been a case of hypocalcaemia (seep. 211).

Vitamin D

With on-farm mixing of rations by manycrocodile farmers there is the possibility ofinadvertantly adding too much vitamin pre-mix. Usually no mixing records are held.

Excessive vitamin D consumption byNorth Pole explorers who ate the livers ofpolar bears caused severe problems, withabnormal bone formation in soft organs andexostoses. Vitamin D is also used to poisonwarfarin-resistant rats.

In green iguanas, hypervitaminosis Dcaused calcification of the aorta and pul-monary arteries (Pallaske, 1961; Wallach,1966), as well as degeneration of the kidneys,with a hyaline to ground-glass appearanceon the cut surface (Wallach, 1966). Such casesof hyaline degeneration of the kidneys wereseen in adult farmed Nile crocodiles that haddied from stress septicaemia (see p. 228) afterhaving been translocated to a new breedingenclosure during winter (Fig. 7.29) (author’sown case). The muscular ossification seen byYoungprapakorn et al. (1994) most likely iscaused by displaced embryonic tissue, whilethe muscular calcification described in thesame publication could have been a sequel ofZenker’s degeneration (see p. 219). Thereport of suspected vitamin D poisoning infarmed Nile crocodiles by Huchzermeyer(1999) was in error; it was a case of osteo-porosis (see p. 211).

To prevent any possible toxic effects, vita-min supplements should be given accordingto recommendations and not be overdosed.Since this vitamin is stored in fat, it may alsobe necessary to take into consideration thevitamin D status of dead poultry fed to thecrocodiles.

Antibiotics

Resistance

Antibiotics are used to suppress bacterialgrowth in infections. However, a prolongedexposure selects for resistance in the surviv-ing bacteria to the specific antibiotic or to aclass of antibiotics. This resistance can bepassed on to other species of bacteria as well.While this is not a toxic effect in the strictsense of the word, it is a deleterious effect,which needs mentioning. Crocodiles are notonly exposed to the antibiotics that are givento them prophylactically or therapeutically,but also to those present in carcasses andorgans of farm animals fed to the crocodiles.Residues of antibiotics may render crocodilemeat unfit for human consumption.

Gentamycin

Gentamycin is known to be nephrotoxic andreptiles are particularly vulnerable to over-dosing with this antibiotic because of theirslow metabolism (Montali et al., 1979; Knox,1980). Structural damage to the kidneytubules reduces the ability of the kidneys toeliminate uric acid and causes gout, theaccumulation of uric acid crystals (seep. 230). As Aeromonas hydrophila often is sen-sitive to gentamycin, veterinarians aretempted to use it in cases of septicaemia (seepp. 173 and 228), and this author admitshaving unintentionally killed juvenile croco-diles with repeated gentamycin injections.

Streptomycin

Streptomycin has been blamed for causingthe death of a captive spectacled caiman fol-lowing treatment of its tank with an algicidecontaining this antibiotic (see also above)(Jacobson, 1984).

Ivermectin

At one-half of the mammalian dose, iver-mectin causes paralysis in Nile crocodiles(personal communication, C.M. Foggin,Harare, 2000). There is a suspicion that it isalso toxic to other crocodilian species.


Anti-inflammatories

Probenecid, phenylbutazone and salicylatesinhibit the secretion of urates and cause gout(see pp. 230 and 264) (Cardeilhac, 1981).

Mycotoxins

Mycotoxins, and possibly also a vitamin B1deficiency (see p. 217), were suspected to beresponsible for cases of severe fatty degener-ation of the liver in farmed juvenile andadult spectacled caimans (Villafañe et al.,1996) (see also p. 261). However, fatty degen-eration of the liver is commonly present inanorectic and runting crocodile hatchlings(p. 234).

Multifactorial Diseases

Multifactorial diseases are man-made dis-eases, typical of intensive husbandry condi-tions and, in crocodiles, also of conditions ofcaptivity. These diseases are caused by thecombined actions of several factors, and inmany instances it is difficult, or even impos-sible, to assign a leading role to any of thefactors involved. Since the concept of multi-factorial diseases is relatively new, they donot fit into the traditional way of describingdiseases, which are classified by their only,or main, cause. This leaves the multifactorialdiseases to be dealt with somewhere towardsthe end of the book, whereas according totheir importance they should have theirplace right in front. It is hoped, though, thatthe reader will find this section, and will notstudy it less than the preceding ones.

The factors involved in multifactorial dis-eases are all the ones commonly associatedwith captive or intensive farming conditions.Without doubt, the single most importantfactor in all the conditions in this section isstress, and since stress does not fit into thestandard classification either, it will be dis-cussed in detail in Chapter 7 (p. 278). Otherfactors playing an important role are malnu-trition, accumulation of microorganisms inthe immediate environment and immunesuppression by unsuitable temperatures.

In very simple terms, one can also try toexplain this concept as interactions betweenthe environment (physical, chemical and bio-logical) and the organism (in our case thecrocodile with its defences) (see p. 46).

Among the physical factors are tempera-ture and sources of heat, as well as humidity,light and noise. Important chemical factorsare water and air quality, disinfectants andother chemicals used on the farm, as well ascontaminants. Biological factors range frommicroorganisms in environment and food,via the food itself, to intraspecies interactionsand the human presence.

The different factors in the environmentexert a pressure on the crocodile, whichresponds to these pressures with its defences(see Fig. 1.47). As long as the defences areadequate, there is a balance, and a crocodilein balance with its environment is healthy. Ifa single, or the combined, pressures becometoo strong for the defences of the crocodile,there will be an imbalance, and this imbal-ance will cause disease.

In the sense of the discussion above, thedefences of the crocodile do not only consistof the physical barriers of skin and mucosaeand of the immune system, but of the wholegamut of physiological, biochemical andbehavioural adaptations of the crocodile tolife in its specific ecological niche. The suc-cess of keeping crocodiles in captivity, or inan intensive farming system, depends on thedegree to which we are able to cater for thesespecific adaptations.

Enteritis

Aspects of this subject have already beendealt with under hatchling diseases (seep. 145). In the following the emphasis will beon the multifactorial aspects of the disease.

The factors involved in causing enteritisare:

● intestinal flora;● inadequate temperature;● stress;● bacterial infection from unhygienic meat;● bacterial build-up in the environment;● viruses.

226 Chapter 6

Intestinal flora

Very little is known about the normal intesti-nal flora of crocodiles living in the wild. Ourlimited knowledge is summarized inChapter 1 (p. 38). In all animals the normalintestinal bacteria occupy the availableattachment sites on the epithelial surface ofthe intestine and, with their metabolism, pro-duce an environment not conducive for theestablishment of pathogenic bacteria. Thisprocess is known as competitive exclusion.Fungi also are part of the normal intestinalflora.

In nature, the intestinal flora derives fromthe nest, from the water in the nursery conta-minated with the faeces of the mother andalso from the live food eaten.

In the sterile environment of the hatchery,and under severe hygienic conditions in therearing house, a hatchling may not beexposed to the normal intestinal bacteria itrequires and may therefore not be able toestablish the required intestinal flora.Antibacterial treatment during this periodmay further limit the range of available bac-teria, and may strongly favour fungi. Thebacteria available under these circumstancesare either highly resistant to antibacterialtreatment and hygiene measures (e.g.Pseudomonas spp.), or they derive from thefood, raw minced meat, particularly if it isprepared from livestock farm mortalities(e.g. salmonellae and pathogenic Escherichiacoli). This obviously opens the door to out-breaks of enteritis.

Cultures of intestinal bacteria suitable forthe initial colonization of the gut are calledprobiotics. Probiotics based on a singlespecies are less effective than those contain-ing several bacterial species. No crocodile-specific probiotics are presently available,but several poultry products are, and thesecould be used to treat hatchlings. However,included under the name of probiotics arealso preparations made from dead bacteria,which are used only for their enzyme action.These preparations usually contain vitaminsas well. Only probiotics based on live bacter-ial cultures should be used for the purposeof gut colonization of hatchlings, or of olderjuveniles after antibacterial treatment.

The individual bacterial and fungalspecies also have temperature optima, whichallow them to function well. It is thereforepossible that keeping crocodiles at constanthigh or low temperatures already limits thenumber of bacterial species able to thrive inthe intestinal environment.

Inadequate temperature

Crocodiles have certain temperaturerequirements, depending on their activity,and they try to adjust their body tempera-ture accordingly (see pp. 44 and 55).Inability to achieve the desired temperaturecauses stress (see below), as do overheatingor excessive temperature fluctuations. Lowtemperatures reduce the activity of theimmune system. Any of these conditions cancontribute to lowering the resistance of thecrocodiles and to triggering an outbreak ofenteritis.

Stress

Repeated, ongoing and/or severe stressreduces the functions of the immune system(see p. 278). Temperature stress has been dis-cussed above. A further source of stress com-monly found on crocodile farms is fear, theinability of hatchlings or juveniles to findcover. Even in a closed rearing house, thecrocodiles do not recognize the ceiling ascover. To feel secure they need somethingmuch lower to creep under, e.g. hide boards(see p. 114). Any disturbance, handling, etc.can also cause stress, as does overstocking(see p. 116).

Bacteria

The main source of bacterial contaminationand infection is the feed. Even pelleted feedis not sterile and can contain salmonellae.However, raw meat, particularly mincedmeat, of farm fatalities is the most importantsource of pathogenic bacteria. Initially, thesemay infect one single crocodile and multiplyin its gut. Excreted with the faeces, they thencontaminate the environment. The warmand nutrient-rich water in the rearing house


allows further multiplication of the bacteriain the periods between water changes. A thinlayer of fat on the surface of the watercollapses on the floor, when the water isdrained. This fat is not removed by normalscrubbing. Under it, bacteria find protectionfrom superficial cleaning and disinfection. Inthis manner the bacterial contamination ofthe rearing house can build up.

Further sources of bacterial contamina-tion are the faeces of rats and flies attractedto the crocodile feed in open rearingfacilities.

Other organisms

Coccidia cause a specific enteritis, dealt withelsewhere (see p. 183), but coccidial enteritiscan be complicated by bacterial infection.The other presently known intestinal proto-zoa can mostly be regarded as harmless (seep. 190). Adenovirus can cause enteritis, andthis infection can also be complicated by, orpredispose to, bacterial enteritis (Foggin,1987). It is presently unknown whetherParamyxovirus can cause enteritis in croco-diles (see p. 162).

Clinical symptoms and pathology

Diarrhoea is rarely seen because of theprevalently exudative reaction, which fre-quently leads to an occlusion of the intestine– the affected hatchlings lose condition andhave a bloated appearance (see also p. 145).The different pathological manifestations aredescribed in Chapter 7 (p. 255).

Treatment

On the one hand, the treatment of enteritismust be based on the diagnosis of the bacter-ial agent involved and its antibiogram, but,on the other hand, one has to consider theother factors as well. Correct the tempera-tures, reduce other sources of stress, reducecontamination of feed and environment andinstigate a cleaning and disinfection pro-gramme that will prevent a recurrence ofbacterial build-up in the immediate environ-ment of the crocodiles.

Prevention

The prevention of enteritis is fourfold:

● establishment and maintenance of a nor-mal and protective intestinal flora;

● optimal temperature conditions;● stress-free rearing conditions; and ● a hygiene programme preventing bacter-

ial build-up.

Septicaemia

Crocodiles, not having any lymph nodes, areprone to the rapid spread of bacteria into theblood circulation – septicaemia. The dangeris somewhat limited by the peculiarity of theprevailing inflammatory response, exuda-tion, which tends to immobilize invadingorganisms in localized infections, preventingthem from draining into the blood circula-tion and causing septicaemia (p. 46)(Huchzermeyer and Cooper, 2000). Thisleaves the intestine as the main source ofinfection and port of entry to the general cir-culation.

The bacteria that have been found incases of septicaemia have been listed inChapter 5 (p. 173). The factors involved arestress, temperature and the intestinal flora.

Bacterial translocation

Individual bacteria of the intestinal flora aretransported through the intestinal mucosa atthe sites of gut-associated lymphatic tissue,and presented as antigen for the productionof local antibodies; or are transported bymacrophages into the circulation and pre-sented as antigen for the production ofhumoral antibodies (Neutra, 1998; Vasquez-Torres et al., 1999). Apart from this, the bar-rier between the intestinal flora and theblood, the mucosal barrier, remains intact ina healthy animal. However, at least inostriches and crocodiles, this barrier canbreak down under conditions of severestress, allowing a few bacteria access to theblood circulation (author’s own unpublishedobservations). In human patients it has beenestablished that bacterial translocation from

228 Chapter 6

the gut occurs after trauma or burn shock(Deitch et al., 1996) and nitric oxide plays arole in the regulation of this process (Nadlerand Ford, 2000).

Chance or opportunity determines whichbacterial species is translocated, and conse-quently there are no bacterial species that areparticularly selected by this process. Underfavourable conditions, and if the stress doesnot persist, the immune system quickly elim-inates the invaders.

If stress conditions prevail over a longertime, suppressing the activity of the immunesystem, or if the immune system is incapaci-tated by cold, the invading bacteria can thriveand multiply. As the liver filters the bloodreturning from the intestine through the por-tal system, the bacteria may provoke varyingdegrees of cellular reaction and even a severehepatitis. The bacteria may also invade thejoints or serous cavities, causing arthritis(Huchzermeyer, 2002) (see also p. 273), peri-carditis and polyserositis (see p. 269).

Clinical signs

At first the affected crocodile(s) may behaveand feed normally. In the longer run, as vari-ous organs become affected, symptoms maydevelop accordingly. This may take weeks.Crocodiles that have been stressed during aperiod of cold weather (capture and translo-cation in winter) may not regain their appetitewith the onset of warmer weather. Inadvanced stages, juvenile crocodiles oftenshow a reddish discoloration of the ventralskin (see Plate 9). Subadult crocodiles oftenpresent with whitish patches on the facialskin, particularly around the nostrils and theeyes (see Fig. 5.17). We used to call this ‘whitenose disease’ and in conjunction with gastriculcers ‘rhinogastritis’ (Huchzermeyer andPenrith, 1992) (see also p. 237). In the finalstage, all affected crocodiles become lethargic,often refusing to go into the water (see p. 290).

Pathology

In acute cases, the animals will be in goodnutritional condition, while the lesions maydepend on the bacterial species involved andon the localization of the infection. They

include severe diffuse or focal hepatitis (seep. 259), subcutaneous haemorrhagic oedema,myocarditis and acute fibrinous epicarditis(see p. 269) (Ladds and Sims, 1990).Splenomegaly is commonly seen in chroniccases, except in emaciated individuals(Huchzermeyer, 1994) (see also p. 270), as aregranulomatous lesions in the liver. Because ofthe continuous perfusion of liver and kidneys,there is always some degree of lymphocyticreaction in these organs. Gastric ulcers may bepresent, and in some cases these may be colo-nized by ascaridoids (p. 192) (Huchzermeyerand Penrith, 1992; Huchzermeyer andAgnagna, 1994; Ladds et al., 1995).

Treatment

Any antibacterial treatment will have to bebased on bacterial isolation and an antibi-ogram, in individual cases from a blood sam-ple. However, any handling of the affectedcrocodile(s) may cause further stress and fur-ther aggravate the problem. Small hatchlingsappear to be more tolerant of handling andcan be dosed orally with a nutrient fluid con-taining the chosen antibiotic (see pp. 86 and148).

Prevention

It is most important to avoid severe, continu-ous stress, particularly if the animal will beunable subsequently to maintain an optimalbody temperature. Crocodiles should neverbe captured and transferred in winter. Wheresuch an action is unavoidable, the crocodileshould be given a prophylactic treatmentwith a broad-spectrum antibiotic. Because ofthe suspected role of nitric oxide in the bacte-rial translocation, and because of the oxygenscavenging action of vitamin C and its role insupporting phagocytosing macrophages, pro-phylactic treatment with ascorbic acid mayalso be appropriate (see also p. 218).

Generalized fungal infections

The mechanisms causing stress septicaemiaseem to apply to generalized fungal infec-tions as well (see p. 182). They also are seen


frequently after severe stress, and particu-larly in association with cold. Some fungi areknown to be able to multiply under coldconditions, when many bacteria become dor-mant. Consequently, generalized mycosis istypically a spring disease. It develops duringwinter and finally kills the crocodile inspring.

Gout

Uric acid is one of the end-products of pro-tein metabolism (see p. 48). Its solubility islimited. As soon as plasma uric acid levelsrise beyond saturation, uric acid crystalsbegin to form. Gout is therefore character-ized by the deposition of urate crystals in thekidneys, on serous surfaces of the internalorgans, in the joints, throughout the muscu-lature and even in the stomach, due to theinability of the kidneys to excrete all, or theexcess, urates. The localization of thedeposits varies from case to case. Factorsinvolved in causing gout are nutrition, dehy-dration, cold, stress, infection and toxic sub-stances.

Nutrition

The natural diet of crocodiles is rich in pro-tein, and under normal circumstances thekidneys should be able to cope with the out-put of uric acid from protein metabolism.However, if protein has to serve as source ofenergy as well, there may be an excess pro-duction of end-products of nitrogen metabo-lism. Nitrogen excretion in the form ofammonia, as well as uric acid, was higher inAmerican alligator hatchlings fed maximallyon five meals per week than in those fed asingle meal after a fast, with lower uric acidclearance and higher uric acid plasma levelsin the latter group (Herbert, 1981). Thisappears to be in contrast to the commonassumption that overfeeding is one of thecauses of gout in farmed crocodilians(McNease and Joanen, 1981). As mentionedabove, the energy value of the ration mayplay a role in this.

Kidney pathology caused by vitamin Adeficiency was found to be responsible for

outbreaks of gout in farmed crocodiles(Foggin, 1987; Ariel et al., 1997a) (see alsop. 216). High calcium supplementation hasalso been mentioned as a suspected cause(Foggin, 1992a). However, it seems unlikelythat the feeding of fatty fish or meat couldcause gout (Pooley, 1986). Intermittent feed-ing, as discussed above (Herbert, 1981) andas it may occur in captive situations, particu-larly in association with lower temperatures(see below), may well be more importantthan the composition of the feed itself.

Dehydration

Dehydration not only decreases the flowthrough the kidneys and thereby their output,but also leads to a certain concentration of theplasma (Cardeilhac, 1981). Because of the lowsolubility of uric acid, this can then trigger theformation and deposition of uric acid crystals.Dehydration may occur during prolongedtransport. Fed animals are more susceptible tothe effect of dehydration than fasting ones.All farming operations should be run in sucha way that dehydration cannot occur.

Cold

Gout occurs more commonly during thewinter months (Pooley, 1986). This has to donot only with an inability to metabolizedigested food at lowered temperatures, butalso with the lower solubility of uric acid atlower temperatures. Under certain farmingor captive conditions, crocodiles that havebeen warm during the day and have eatentheir fill and then have started to digest andmetabolize, raising uric acid plasma levels,will be forced to cool down during the night,causing uric acid crystals to form. Americanalligators may be protected from this effectof cold by the seasonal suppression ofappetite (see p. 37).

Stress

There is only an indirect action of stress inthe aetiology of gout, via stress septicaemia(see p. 228) causing kidney infection andnephritis (see below). There could possiblybe another action, via disturbed behaviour

230 Chapter 6

interfering with thermoregulation and nor-mal water intake (see p. 289).

Infection

The continuous high rate of perfusion makesthe kidneys vulnerable to bacterial infectionsin cases of septicaemia (see p. 228). Infectionand inflammation interfere with the functionof the kidneys, causing uric acid crystaldeposition, often in the affected kidneysthemselves. Cases of pyelonephritis inCrocodylus novaeguineae (Ladds et al., 1995)and in C. johnsoni (Buenviaje et al., 1994)could also have been triggered by an ascend-ing infection. The latter case was compli-cated by a vitamin A deficiency (see above).

Toxic substances

One case of gout in a captive crocodile wasapparently caused by the use of an algicidecontaining streptomycin (Jacobson, 1984)(see also p. 224). Other nephrotoxic sub-stances are the antibiotic gentamycin (Knox,1980) (see also p. 225) and certain anti-inflammatories such as phenylbutazone,probenecid and salicylates (Cardeilhac, 1981)(see also p. 226).

The experimental ip injection of theamino acid D-serine caused renal failure withthe production of small quantities of paleurine, plasma uric acid concentrations of70 mg per 100 ml and massive deposition ofuric acid crystals throughout the body(Coulson and Hernandez, 1964).

Birth defects

Congenital gout occurred in two subsequentyears in a number of Nile crocodile hatch-lings from eggs collected from an area onLake Malawi. The hatchlings lived a shorttime only and showed gout deposits aroundtheir joints (Foggin, 1992a) (see also p. 155).

Kidney aplasia: occasionally only one kid-ney develops and, although it is larger than anormal paired one, it may reach a stagewhen it can no longer cope with the highmetabolic demands placed on it in a farm sit-uation, and consequently gout develops (seealso p. 155).

Species involved

While one would presume that all crocodil-ian species would be equally susceptible togout, it has to be noted that, in mixed farm-ing operations, Crocodylus porosus were notaffected, whereas C. novaeguineae and C. john-soni suffered cases of gout (Buenviaje et al.,1994; Ladds et al., 1995).

Other species from which cases of gouthave been reported are:

● farmed American alligators (Cardeilhac,1981; McNease and Joanen, 1981);

● a captive spectacled caiman (Jacobson,1984);

● farmed Nile crocodiles (Pooley, 1986;Foggin, 1987);

● a wild adult Indo-Pacific crocodile(Buenviaje et al., 1994);

● a captive false gharial (Frank, 1965);● a captive gharial (Frank, 1965).

Clinical signs

In all cases of gout there is a general depres-sion. In renal gout, the swollen kidneys exertpressure on the sciatic nerves, causing a hindlimb paralysis; while in arthritic gout, theaffected leg joints become painful and theanimal is reluctant to move. In advancedcases of arthritic gout, the swollen joints canbe seen or palpated. A needle aspirate fromsuch a joint will contain the white paste ofuric acid crystals, and analysis of a bloodsample will show elevated uric acid levels(see p. 47).

Pathology

Macroscopically, the most obvious lesionsare the gout deposits on the serous surfaces,particularly the pericardium and epi-cardium, in the joints, throughout the mus-culature, in the stomach and in the kidneys,the localization varying from case to case(Figs 6.14–6.17, Plate 16). The actual distribu-tion of these deposits may depend on a num-ber of factors: in cases of nephritis andpyelonephritis the deposits are mainly in thekidneys. The somatic distribution maydepend on thermal conditions. Cold, lower-


ing the solubility of uric acid, may cause itsprecipitation in the leg joints, when in fluctu-ating temperatures the legs cool down morerapidly than the body.

The uric acid crystals can best be recog-nized in a direct smear under a polarizingmicroscope. Often the formalin used for fix-

ing the histopathology specimen dissolvesthe crystals, leaving only the urate clefts inthe tissue. Tophi (the collection of urate crys-tals) may be surrounded by an inflammatoryreaction with multinucleated giant cells(Youngprapakorn et al., 1994; Ariel et al.,1997a).

232 Chapter 6

Fig. 6.14. Gout in a farmed Nile crocodile: uric acid deposits on the epicardium.

Fig. 6.15. Gout in a farmed Nile crocodile: uric acid deposits in the joints of the four legs.

Squamous metaplasia and hyperkeratosisof the large collecting ducts in the kidneywere found in gout cases caused by vitaminA deficiency (see above) (Foggin, 1987;Ladds et al., 1995; Ariel et al., 1997a) (see alsop. 216).

Treatment

Only early cases of gout can be treated, andthe possibilities of treatment are limited torehydration in cases of dehydration (Knox,

1980) and fasting for 1 week to 10 days incases of overfeeding (Cardeilhac, 1981;McNease and Joanen, 1981).

Prevention

For the prevention of gout it is important toavoid all the factors contributing to its aetiol-ogy, but particularly not to feed when lowtemperatures are expected, and also not 48 hbefore capture and transport. Dehydrationhas to be avoided under all circumstances.


Fig. 6.16. Gout in a farmed Nile crocodile: uric acid deposits in the musculature.

Fig. 6.17. Gout in a farmed Nile crocodile: uric acid deposits in gastric ulcers.

Runting

Runting is the failure of some crocodiles in agroup to grow. This can be seen in hatchlingsand in juveniles, and it can be caused by alarge number of factors. Under certain condi-tions runting can be the cause of a major pro-portion of farm mortalities (Buenviaje et al.,1994).

Factors involved

Primary anorexia occurs in hatchlings thatnever learn to feed, while secondaryanorexia may be caused by certain rations,e.g. fish (Foggin, 1992a) or unpalatablerations in general (McInerney, 1994).However, anorexia is a special case (seepp. 283 and 289), as anorexic hatchlings donot recover and therefore starve to death in aslow, protracted process, while true runtscontinue to eat but fail to grow or grow onlyvery slowly.

There may be genetic causes in somecases of runting, and poor incubation condi-tions may also play a role (Peucker andMayer, 1995). Hatchlings from small eggslaid by young females will be smaller thanaverage and may be disadvantaged from thestart.

Of the environmental factors, temperatureis probably of major importance. Nile croco-dile hatchlings kept at 25°C lost weightalthough they continued to feed (Kanui et al.,1991). Generally, the inability to maintain anadequate temperature on a thermogradient,exposure to severely fluctuating tempera-tures and overheating are very stressful (seep. 278).

Other sources of stress are a high stockingdensity, bullying by larger individuals andthe inability to hide, and fear. As a majorcause of runting, these have been summa-rized as adaptation failure (Buenviaje et al.,1994).

Some of the runts appear to be afraid togo into the water and, rather, try to hide in acorner of the pen, where they dehydrate(Foggin, 1992a) (see also p. 289). This dehy-dration further aggravates their condition.

Poor yolk-sac absorption may be linked topoor incubation conditions but also to inade-

quate temperatures or even yolk-sac infec-tion (see p. 147).

Nutritional factors may either have some-thing to do with the palatability of the food(see above) thereby limiting feed intake, itscomposition or with poor protein assimila-tion and prolonged stomach clearance(Davenport et al., 1990). The latter may alsobe the case in hatchlings recovering from anadenovirus infection (Foggin, 1987, 1992b) orother intestinal infections, such as coccidiosis(see p. 183), while a complete intestinalocclusion by exudate after coccidiosis or sal-monellosis (see p. 164) will lead to death bystarvation. An immune deficiency suggestedby Foggin (1987) may well be caused nutri-tionally by a poor feed intake.

Clinical signs

The most obvious sign of runting is the fail-ure to grow in comparison to other individu-als in the same group. The neck becomesdrawn in, while the abdomen may or maynot appear distended against the emaciatedbody (Fig. 6.18).

Blood taken from runted Nile crocodileshad lower haemoglobin and packed cell vol-ume values than blood from normal ones,and elevated alanine transaminase and alka-line phosphatase values (Foggin, 1987).Runted C. porosus hatchlings had elevatedalanine A-transferase, aspartate A-trans-ferase and alkaline phosphatase values(McInerney, 1994) (see also p. 47).

Pathology

The pathology findings are non-specific,with emaciation, depletion of the abdominalfat body (see p. 28), atrophy of liver andintestine and sometimes ascites. The liverhas a greyish colour, with fatty and vacuolardegeneration and increased numbers ofmelanomacrophages histopathologically. Inthe pancreas there is an atrophy of the acinarcells (Foggin, 1992a).

Treatment

First of all it must be realized that runting ismainly due to conditions on the farm, not so

234 Chapter 6

much ‘maladaptation’ (Buenviaje et al., 1994),but rather a failure to provide suitable condi-tions (see above). Unless the factors involvedon the particular farm are diagnosed cor-rectly and subsequently rectified, any possi-ble treatment will be of rather limited value.This should be the work of the consultingveterinarian. As long as the veterinarian’srole remains restricted to the laboratory andto prescribing antibiotics, no solutions willbe possible for any of the multifactorial dis-eases.

Runts should be separated from largerhatch mates to prevent further bullying.They can then be force-fed by stomach tube(see p. 86) with a nutrient liquid twice aweek at 20 ml kg�1 body mass. Such a liquidcould be made by homogenizing 250 g offresh fish in 250 ml water with the additionof 1 ml concentrated multivitamin drops(Foggin, 1987) or, my own formula, by mix-ing one egg yolk with 10 ml milk and 5 g ofsugar. A single im multivitamin injectionappeared to have a beneficial effect (Peuckerand Mayer, 1995), while the treatment of nor-mal Nile crocodile hatchlings with a recom-binant human growth hormone had atemporary effect only, with cessation of feed-

ing a week after the treatment was haltedand subsequently even loss of weight(Andersen et al., 1990).

Rehydration of dehydrated animals maybe problematical. Simply forcing them intowater and preventing them from comingout on to land may cause further stress and,furthermore, interfere with their thermalrequirements. Force feeding dehydratedrunts with a very dilute nutrient liquid(equal parts of water and of one ofthe above formulas) may be a betterapproach.

Unless treatment is given early, theprospect of success is rather limited.Survivors may resume growing but at a veryreduced rate, never reaching a suitable sizefor slaughter.

Prevention

The large-scale incidence of runting isentirely preventable. All the factors citedabove should be examined carefully, but ofparticular importance are stocking density,the provision of a suitable temperatureregime and a stress-free environment. Eventhe palatability of the ration becomes less


Fig. 6.18. Runted Nile crocodile hatchling with distended abdomen.

important when all the other factors havebeen corrected.

Winter sores

Winter sores occur in older juvenile croco-diles that are exposed to cold winter condi-tions. Under such conditions, the blood flowto the skin is reduced and the immune sys-tem is functioning only suboptimally. Thisallows bacteria from a contaminated envi-ronment, mainly of faecal origin, to take ahold in minor scratches, particularly in thesoft tissue between the scales. The lesionscaused by these local infections are coveredby yellow-brownish crusts (Plate 17 and Fig.6.19). Winter sores typically occur on farmswhere the hatchlings have been reared fortheir first year in a heated environment but,due to lack of space, are placed in outsidepens in their second year.

Factors involved

The two main factors are insufficient tempera-tures for the local and humoral immune sys-tem to function optimally, and unhygienicconditions. Outside ponds used for accommo-dating juvenile crocodiles in winter are usu-ally deeper, to protect the crocodiles against

excessive cooling. However, the water in sucha deep pond is not changed daily, nor arecleaning and disinfection carried out on adaily basis, and this can lead to a severe accu-mulation of faecal matter in the water.

Since the crocodiles are not fed during thecold months, latent vitamin deficiencies mayalso develop. Overcrowding is often seenunder these conditions as well, as during thesummer the crocodiles may already have out-grown the available space. This causes stress,which further depresses the immune system.

Clinical signs

Affected crocodiles have yellow-brownishcrusts between the scales, particularly on theventral skin. These crusts usually are nolarger than c. 5 � 10 mm. They are larger andlighter in colour than those seen in cases ofcrocodile pox (see p. 158), but similar tothose seen in dermatophilosis (see p. 172).

Pathology

Macroscopically, there are superficial lesionscovered by yellow-brownish crusts. Histo-pathologically, there is a destruction of the epi-dermis and an accumulation of round cells inthe dermis. The crusts are formed by necroticcells and bacteria (Huchzermeyer, 1996c).

236 Chapter 6

Fig. 6.19. Winter sores on the ventral surface of the neck and thorax of a juvenile Nile crocodile.

Permanent scarring can cause the skins ofaffected crocodiles to be downgraded.

Bacteriology

Bacterial cultures from the lesions produce alarge variety of non-pathogenic, potentiallypathogenic and known pathogenic bacteriain mixed culture from every single specimen(Huchzermeyer, 1996c).

Treatment

The treatment of winter sores is based pri-marily on rectifying the conditions that ini-tially caused them, particularly temperatureand hygiene. For possible technical solutionsto the problems caused by cold in outsiderearing see Chapter 3 (p. 108).

Once these conditions have been rectified,the healing process will start by itself. It canbe assisted by daily spraying of the croco-diles, best at the time of water change, with amild but effective disinfectant, such as F10®

(Health and Hygiene, South Africa) at a dilu-tion of 1:250.

Prevention

Winter sores can be prevented only by pro-viding protection from cold in conjunctionwith adequate hygiene, consisting of regularwater changes, scrubbing and disinfection,and the avoidance of overcrowding.

Chronic stress dermatitis

Chronic stress dermatitis is characterized bythe appearance of patches of whitish skindiscoloration, particularly around the nos-trils and eyes, but occasionally anywhere onthe body. It is also referred to as ‘white nosedisease’. It affects mainly older juveniles andsubadults held in crowded indoor condi-tions, often involving the largest specimensin the group and particularly males. It isaccompanied by steady deterioration, even-tually leading to the death of the animal.Outbreaks occurring in conjunction withgastric ulcers have also been termed ‘rhino-gastritis’ (Huchzermeyer and Penrith, 1992).

Factors involved

Overcrowding of animals that are at thestage of developing their territorial behav-iour is the most important factor. An unsuit-able temperature regime and insufficienthygiene may also play a role. As the animalsbecome anorexic, secondary nutritional deficiencies further aggravate the condition,possibly causing a biotin deficiency(Youngprapakorn et al., 1994).

Clinical signs

Affected crocodiles are listless and anorexicand develop the typical skin lesions, consist-ing of patches of white discoloration, startingaround the nostrils, then spreading to theeyelids and, in advanced cases, affecting thewhole body (Plate 18, Figs 6.20 and 6.21).

Pathology

Usually the affected animals become emaci-ated. The skin lesions range from superficialerosion and discoloration of the epidermis,to ulceration, accompanied by cellular infil-tration in the dermis (Fig. 6.22). There mayalso be an inflammation of the apical parts ofthe nasal passages. Gastric ulcers, when pre-sent, are associated with polyarteritis(Huchzermeyer and Penrith, 1992). They aredealt with in detail in Chapter 7 (p. 251). Alarge variety of non-pathogenic and patho-genic bacteria can be isolated from the skinlesions.

Treatment

There is no successful treatment, unless theaffected animals can be released into largerholding pens with suitable temperature con-ditions. For the treatment of anorexia, seeChapter 7 (p. 282). Improving hygienic mea-sures and spraying the animals at least oncea day with a suitable disinfectant (F10®,Health and Hygiene, South Africa, diluted1:250) may help to improve the condition ofthe skin. On valuable individual animals, amore intensive treatment could be tried,such as the one described in Chapter 7(p. 253).


238 Chapter 6

Fig. 6.20. Stress dermatitis: discrete erosions around the nostrils of a juvenile Nile crocodile.

Fig. 6.21. Stress dermatitis: lesions spreading to the eyelids of a juvenile Nile crocodile.

Fig. 6.22. Stress dermatitis: skin section showing cellular infiltration in the dermis.

Prevention

Overstocking of larger juveniles and subadultsoften occurs when the construction of facilitiesfor their eventual release has been fallingbehind schedule. This should be avoided at allcost. In the event of such delays, arrangementsfor alternative accommodation should bemade in good time, and the crocodiles bemoved before any losses occur.

Incidents of high mortality in wildcrocodiles

Incidents of high mortality in wild crocodilesappear to be rare. Adult crocodiles are veryresistant, while many juvenile crocodilesrather fall prey to cannibalism. In any event,it is rare to encounter dead crocodiles in thewild. By the time a dead crocodile is found,the state of the carcass may have deterio-rated to the point that it may no longer bepossible to collect suitable laboratory speci-mens. The remoteness of most crocodilehabitats also plays a role here.

Specimens from a single carcass may notbe representative of the entire outbreak ofmortality, as was the case of an outbreak ofhigh mortality in adult crocodiles with respi-ratory distress in Lake Rukwa in Tanzania in1943, when only a few nodular skin lesions,presumably fibriscesses (see p. 46) were col-lected in formalin (Thomas, 1946).

A less drastic, but very insidious, problemis posed by declining crocodile numbers inpopulations that otherwise may appear to benormal (Cardeilhac et al., 1998; Swanepoel etal., 2000). In such cases, environmental pollu-tion has been suspected (for further detailssee pp. 221 and 223).

With increasing human encroachment,the wild crocodile populations become lessremote, but also more vulnerable. In theelectronic age, communication becomesrapid and is available almost everywhere. Itis therefore recommended that, in the event

of an outbreak of mortality in wild croco-diles, the advice of specialist veterinariansshould be sought immediately and, if possi-ble, a specialist veterinarian should take partin the field investigation. He is best qualifiedto carry out the post-mortem examinationsand to decide on which specimens to takefor further laboratory studies. For details ofthe necessary equipment for such a fieldinvestigation see Chapter 2 (p. 83).

The multifactorial aspect of any such out-break of high mortality should not beneglected in the investigation. Just to findone particular pathogen may not be suffi-cient. The Aeromonas hydrophila and otherbacteria found in dead alligators and otherreptiles and fish in Lake Apopka in 1971(Shotts et al., 1972) were not the primarypathogens. Rather, the infections were pre-cipitated by environmental conditions,including eutrophication.

If the multiple fibriscesses found in theone crocodile from the 1943 outbreak of mor-tality in Lake Rukwa (Thomas, 1946) wereindeed representative of the situation, onepossible explanation could be that soldiersstationed in the vicinity of the lake had beenattracted by the excellent fish in the lake andhad indulged in some ‘grenade fishing’,which could have caused the multipleinjuries, or even that an object in the lakehad been used for artillery or bombing targetpractice.

Note Added at Proof

Osteoporosis (pages 211 and 281)

More evidence has come to light linkingosteoporosis and poor dental calcification tostress via lucocorticoids causing calciumdepletion (author’s own observations). Thisallows diaphanous teeth to be used as clini-cal indicator of chronic stress in captive andfarmed crocodiles.


Many of the conditions in this chapter havebeen dealt with in great detail in other chap-ters of this book, according to the causativeagent(s). In all such cases the reader will bereferred to the relevant chapters. This chap-ter should therefore be regarded as an aid tocorrelate clinical and pathological findingswith the specific diseases described in thepreceding chapters.

Skin Diseases

Pox

Pox is a viral infection of the skin. There aretwo different entities: caiman pox, withwhitish crusty lesions (p. 157) and crocodilepox, with dark-brown crusty lesions (p. 158).Similar lesions, but rather yellow-brownishand slightly larger, have been found in der-matophilosis and ‘brown spot’ (p. 172) aswell as in ‘winter sores’ (pp. 236 and 241).The diagnosis is based on the histopathologyof the skin lesions, finding the typical intra-cytoplasmic inclusion bodies. There is nospecific treatment. All one can do is try toreduce the impact of concurrent bacterialinfections by giving a course of antibiotictreatment in the feed.

Bacterial dermatitis

There are several forms of bacterial derma-titis. Dermatophilosis is one of the two specific bacterial skin infections and hasbeen diagnosed in Australian crocodiles aswell as in American alligators (p. 172). AnErysipelothrix dermatitis occurred in a cap-tive American crocodile (Jasmin andBaucom, 1967) (see p. 171). The other twoknown forms, ‘winter sores’, with yellow-brownish crusty lesions (pp. 236 and 241),and chronic stress dermatitis, with patches ofwhite discoloration, particularly on the headaround eyes and nostrils (pp. 237 and 241),are non-specific and many bacterial speciescan be involved. These latter two forms ofdermatitis are multifactorial (see p. 226) andtheir treatment must be based primarily onthe removal of the various causative factors.

Fungal dermatitis

Fungal infections of the skin occur eitherlocally or generalized under unhygienic con-ditions in animals with a reduced immunecapacity due to stress or cold (see alsop. 278). The different forms have beendescribed on p. 177. Superficial infections in

Chapter 7

Organ Diseases and Miscellaneous Conditions

© CAB International 2003. Crocodiles: Biology, Husbandry and Diseases240 (F.W. Huchzermeyer)

the epidermis do not provoke much of aninflammatory response. Deeper infectionscause a granulomatous reaction (Plate 19)and not an exudative one (fibriscess), as inthe case of bacterial infections (p. 46). Thetreatment has, first of all, to be based on animprovement of hygienic conditions, thereduction of stress and an improvement oftemperature conditions. Superficial lesionsrespond very well to repeated spraying withthe combination disinfectant F10® (Healthand Hygiene, South Africa).

The treatment of deep granulomatouslesions may need the application of systemicfungicides, such as ketaconazole. The provi-sion of a hygienic, stress-free environmentwith a suitable temperature regime is mostimportant for the prevention of fungal der-matitis. Furthermore, it must be emphasizedthat frequent or prolonged use of antibioticsin the feed destroys the balance of the intesti-nal flora and allows fungi to multiply out ofcontrol, which may lead to an abundance offungal spores in the faeces and in the envi-ronment (see p. 176).

Parasitic dermatitis

The most important skin parasites causingvisible lesions, although not really an inflam-mation, are the capillarid wormsParatrichosoma spp. (see p. 194), which bur-row in the epidermis and cause visiblemeandering tracts that lead to downgradingof the affected skins. Fortunately, these para-sites need earth ponds and cannot surviveon crocodile farms and ranches where hatch-lings and juveniles are kept in concrete-linedpens.

Leeches congregating in the axillarylesions of Crocodylus johnsoni were believedto have caused puncture wounds in the axil-lary skin (Webb and Manolis, 1983) (seep. 203).

Degenerative skin disease

Nutritional and environmental factors, possi-bly also stress, may be involved in causingcertain forms of degenerative skin disease,

such as the reduction of scale numbers in theareas of the ventral skin where fore- andhind legs join the body, and ‘double scaling’.For obtaining a healthy skin it is necessary toadd suitable vitamin and mineral premixesto the farm rations (see p. 99) and to avoidexcessive temperature fluctuations (seep. 111).

Winter sores

Juvenile crocodiles exposed to cold tempera-tures for prolonged periods while heldunder unhygienic conditions are prone tobacterial skin infections which cause small toconfluent yellow-brownish lesions betweenthe scales (see p. 236). These lesions cancause permanent damage to the skin andwill not heal unless environmental condi-tions are improved.

Chronic stress dermatitis – ‘white nose’

Larger juvenile crocodiles, and particularlysubadults kept in cramped quarters, becomelistless and develop patches of white discol-oration of the skin, particularly around thenostrils – ‘white nose’ – and the eyes (Fig.7.1). The lesions are caused by a superficialerosion of the epidermis (Youngprapakorn etal., 1994). This multifactorial disease hasbeen described in detail on p. 237.

Skin injuries

Scratches

In older juvenile crocodiles, the largemandibular canine teeth often protrudeabove the level of the nose (see Fig. 1.20).When frightened crocodiles pile in the cornerof a pen and one of the lower ones then pullsout, it scratches the belly skin of the croco-dile above. Infection of these scratches canlead to permanent damage. Solutions to thisproblem have been sought by breaking offthese canines, which quickly regrow, andeven by trying somehow to repress theexcessive growth of the teeth, the latter with-

Organ Diseases and Miscellaneous Conditions 241

out results as yet. The problem lies with pil-ing, and this can be prevented by reducingfearful events and, even more importantly,by the provision of hide boards even up toslaughter (see p. 114). Strict hygiene, the fre-quent disinfection of the pens, will reducethe danger of scratches becoming infected.

Superficial punctures

Fighting in hatchlings may produce punc-ture wounds in the skin, which normallyheal without even being detected. However,they can serve as point of entry of infectiousagents, and in crocodile pox (see p. 158)lesions often are aligned in rows, indicativeof an infection of puncture wounds (Plate8).

Abrasions

While crocodiles walk out of the water, theyalways slide back into the water (see p. 35).This sliding on rough concrete may causeabrasions, particularly of the skin coveringthe ventral aspect of the mandibles and onthe plantar surface of the feet (Figs 7.2 and7.3). The plantar abrasions frequentlybecome infected by fungi, causing granulo-matous swellings (see below).

All concrete surfaces in crocodile pensshould have as smooth a finish as possible.Frequent cleaning and disinfection of all con-crete surfaces is also necessary to reduce therisk of infection.

Deeper skin wounds

Bites and other wounds penetrating the der-mis often become infected. Bacterial infectionwill elicit an exudative inflammation and fib-riscess formation (p. 46). These fibriscessesmay continue to grow, eventually causinglarge swellings. They do not respond toantibacterial therapy. The only possible treat-ment would be radical excision of the fib-riscess.

Fungal infection of skin wounds elicits agranulomatous response. The excision ofsuch granulomatous masses is a possibility(Ensley et al., 1979) (see also pp. 95 and 240).Systemic treatment with an antifungal agentsuch as ketaconazole might be an option.However, most important is the preventionof abrasions by having very smooth surfacesin the crocodile pen. An infection of the abra-sions can be prevented by frequent cleaningand disinfection of all the concrete surfacesin the pen.

242 Chapter 7

Fig. 7.1. ‘White nose’: erosions of the facial epidermis of a chronically stressed juvenile Nile crocodile.

Greasy skin

When fatty meat is fed to crocodile hatch-lings, a thin layer of fat forms on the surfaceof the water. When the water is drained, thissurface layer is deposited on exposed sur-faces, including the skin of the hatchlings. It

also traps traces of the nutrient-rich water.With time, a multilayered deposit is formedin this way. On the concrete surfaces thisdeposit resists being washed down andforms a protective layer above bacteria andfungi, which are trapped between the layers.On the skin of the hatchlings the fungi start


Fig. 7.2. Abrasions on the ventral surface of the mandible of a juvenile farmed Nile crocodile.

Fig. 7.3. Abrasions on the foot pad of the left forelimb of a juvenile farmed Nile crocodile.

multiplying, either in the fatty layers only orpenetrating into the upper layers of the epi-dermis. The affected hatchlings loose condi-tion and become visibly ailing (see alsop. 177). A whitish layer can be seen coveringthe dorsal skin of the affected hatchlings (seeFig. 5.18).

The treatment of this condition consistsof spraying greasy surfaces in the drainedpen, and the crocodiles as well, with adetergent, hosing them down and thenspraying surfaces and hatchlings with a dis-infectant with strong fungicidal action(F10®, Health and Hygiene, South Africa,diluted 1:250). This treatment should berepeated daily for 1 week. For the preven-tion of this condition it is important to mon-itor the build-up of a fatty layer on theconcrete, simply by scraping with a finger-nail, and to use detergents and disinfectantsas often as necessary.

Mycobacterial dermatitis

Cases of granulomatous mycobacterial der-matitis in farmed Indo-Pacific crocodileswere described by Buenviaje et al. (1998b)(see p. 170). There is no treatment formycobacterial infections in crocodiles.

Dermatophilosis

Dermatophilus spp. have been isolated fromcrusty lesions of the ventral skin fromfarmed American alligators and Indo-Pacificcrocodiles (Bounds and Normand, 1991;Buenviaje et al., 1997, 1998a,b) (see p. 172).The latter author also confirmed the trans-missibility of the infection. Similar crustylesions are found in a common conditionassociated with cold, called ‘winter sores’(see p. 236).

Dermatophilus spp. do not respond toantibacterial treatment. The prevention ofthe infection must be based on the applica-tion of strict hygiene, particularly regular,thorough cleaning and disinfection of all sur-faces in the rearing facility.

Skin necrosis

A case of necrotic dermatitis was describedfrom a juvenile Crocodylus porosus that hadnot eaten for a while, and which died fromgeneralized bacterial infection. Whole scaleswere lifting off, and underneath there was asubcutaneous oedema. In addition to lesionsin the internal organs indicative of septi-caemia, there was diffuse necrosis of the sub-cutis and the underlying muscle, with nestsof Gram-positive coccoid bacteria (Buenviajeet al., 1998b).

Ulcerative dermatitis

Deep skin ulcers were found in crocodilessuffering from severe chronic cases of fatnecrosis (Youngprapakorn et al., 1994) (seep. 219).

Factors affecting skin quality

Crocodile farming is aimed at producinghigh-quality products. By identifying vari-ous factors that can affect the quality of theskin, one can try to avoid some of the morecommon causes of downgrading. However,the post-slaughter treatment of the skins fallsoutside the scope of this book. The in vivofactors can be classified as: genetic, environ-mental, behavioural, nutritional and micro-biological.

Genetics

Abnormal scale patterns are rare, but are notacceptable to the market. Their most likelycause is genetics. Adult or future breedingcrocodiles showing such patterns should notbe used for breeding. It may pay to submitthe breeding crocodiles to a certain degree ofgenetic selection.

Environment

A cold environment predisposes crocodiles toskin infections, e.g. ‘winter sores’ (see pp. 236and 241); cold or excessive temperature fluc-tuations may also be one of the possible

244 Chapter 7

causes of ‘double scaling’. Overheating isprobably the main cause for the loss of scalesin the axillary and inguinal regions of theventral skin. Rough surfaces may damage theskin directly (see p. 241), they may also pro-tect infectious agents from the effects ofcleaning and disinfection (see p. 243). Near-ideal environmental conditions are necessaryfor the production of top-class skins.

Behaviour

Fear-induced piling can cause scratches onthe ventral skins of the piled crocodiles (seep. 241). Overcrowding may induce fighting,and also may cause severe stress leading tochronic stress dermatitis (see p. 237). It isimportant to pay attention to the behaviouralrequirements of the growing crocodiles.

Nutrition

No particular vitamin or mineral deficiencieshave been proven to cause skin defects incrocodiles, but this is due to the lack ofexperimentation. As in other livestockspecies, the requirements for supplementa-tion certainly exist. It is safest to provide anutrition supplemented with vitamin andmineral premixes designed for use in croco-diles (see p. 99). Using poultry premixes maynot be sufficient, as the requirements of poul-try are believed to differ from those of croco-diles.

Overfeeding may lead to excessive fat inthe abdomen, causing the skin to bestretched, with wide gaps between thescales. It is the energy portion of the ration,particularly the fat, that causes excessivedeposition of abdominal fat. A fat body:heartratio of more than 5:1 indicates that the croc-odiles are fed a ration with an excessiveenergy level (see p. 85). A lean crocodile pro-duces a better skin.

Infection

There are many infections, including at leastone form of parasitism, capable of causingpermanent damage to crocodile skins. Theseconditions have been dealt with above. Theirprevention is of the utmost importance. The

role of thorough cleaning and disinfectioncannot be overemphasized.

Factors unknown

There has been an increasing incidence ofpitting in tanned American alligator skins.These pits cannot be detected on untannedskins. Consequently their later downgrad-ing constitutes a loss to the trade. The causeof this pitting is still unknown (Haire,1997).

A no-no

In spite of all the emphasis on skin quality,there is one action that has to be avoided, anabsolute no-no: the examination of the ven-tral skin of the live crocodile before slaughter!It is immaterial in any case, as the crocodile isgoing to be slaughtered sooner or later any-how and any visible defects are not going toheal before then. However, catching and han-dling the crocodile before slaughter causessevere stress, inducing stress septicaemia,where intestinal bacteria enter the blood cir-culation, leading to contamination of themeat with these very same intestinal bacteria,including salmonellae (Huchzermeyer, 2000)(see pp. 125, 164, 228 and 278).

Crocodile meat should be marketed as ahigh-quality product and this must be con-sidered in the overall production process.

Eye Diseases

Conjunctivitis

Conjunctivitis is the inflammation of theconjunctivae, the mucosal lining of theinternal surface of the two external eyelidsand both surfaces of the third eyelid, as wellas the conjunctival sac. The inflammationcan be serous, with increased lacrimation(Villafañe et al., 1996), or exudative (seep. 46). The serous inflammation may extendinto the nasal passages, causing rhinitis(Villafañe et al., 1996). An exudative con-junctivitis causes blindness due to the accu-mulation of fibrinous exudate behind theeyelids.


One-eyed

Conjunctivitis affecting one single eye may becaused by injury or by a foreign body lodgingin the conjunctival sac or behind one of theeyelids. A non-spreading infection, particu-larly a fungal infection, can also be limited toa single eye. A few cases of one-sided con-junctivitis were seen in outbreaks of meningi-tis (see p. 267) caused by Providentia rettgeri(see p. 174) in farmed C. porosus (Ladds et al.,1996). Repeated cases of one-sided conjunc-tivitis in captive juvenile American alligators(Fig. 7.4) have been ascribed to ant bites, or tothe irritation caused by ant bites and subse-quent scratching (S. Martin, Pierrelatte, 2002,personal communication).

Two-eyed

Conjunctivitis affecting both eyes, but onlyin individual animals, is caused most likelyby non-specific bacterial infection. Suchcases have been seen in farmed crocodiles inIrian Jaya with fibrinous exudation (Ladds etal., 1995) and also in Australia (Hibberd et al.,1996).

Outbreaks of conjunctivitis are due eitherto exposure to an irritant substance in the

environment or, more likely, to specific infec-tion. Outbreaks of serous conjunctivitis,associated with rhinitis and encephalitis, infarmed caimans in Colombia have beenreported by Villafañe et al. (1996), who sus-pected an unknown virus to be the causativeagent. In view of the described symptomsand pathology, this agent might very well bea paramyxovirus (see p. 162).

A whitish ocular discharge was seen in anoutbreak of mycoplasmosis in captiveAmerican alligators (Clippinger et al., 1996)(see also p. 167).

Severe outbreaks of exudative conjunc-tivitis affecting a high percentage of hatch-lings or juveniles in a pen and spreadingrapidly to other pens, occur frequently onNile crocodile farms in South Africa and arecaused by Chlamydia sp. (Huchzermeyer etal., 1994a) (see also p. 167). The conditionreferred to as ‘ophthalmia’ by Foggin (1987,1992a) may, in fact, also be chlamydial con-junctivitis. Some outbreaks of this eye condi-tion appear to have been triggered byoutbreaks of crocodile pox (Foggin, 1992a)(see also p. 158). The case of highly conta-gious keratoconjunctivitis described byYoungprapakorn et al. (1994) may also havebeen due to chlamydial infection.

246 Chapter 7

Fig. 7.4. One-sided exudative conjunctivitis in a juvenile captive American alligator.

Treatment

In individual cases the fibrinous exudate mayhave to be removed from behind the eyelids.After this an antibacterial eye ointment canbe administered. In addition, chlorampheni-col or another antibiotic can be injected sub-cutaneously (sc) into the eyelid (Foggin,1987). Outbreaks of chlamydial conjunctivitisare treated with tetracycline, 1.5 g activeingredient per kg in the feed for 10 days (seeTable 2.13). This treatment should be accom-panied by thorough cleaning and disinfectionof the pens, including spraying the crocodileswith a disinfectant such as F10® (Health andHygiene, South Africa) at a dilution of 1:250.

Opacification of the third eyelid

Opacification of the third eyelid has beenobserved in aged captive American alliga-tors, but the nature of the deposit was notdetermined (Millichamp et al., 1983).

Cataract

Cataract, the opacification of the lens of theeye, has been observed in farmed Americanalligators, probably caused by trauma andinfection, as well as in an American crocodile(Millichamp et al., 1983).

Chorioretinitis

Adult captive American alligators in a road-side show were found to have chorioretinitis,with areas of depigmentation and pigmentclumping within the tapetal fundus(Millichamp et al., 1983).

Ophthalmia

The cases and outbreaks of ophthalmiadescribed by Foggin (1987, 1992a) were prob-ably exudative (chlamydial?) conjunctivitis(see above). A case of panophthalmitis, withthe infection extending into the eye from aretrobulbar abscess, was reported byYoungprapakorn et al. (1994).

Eye injuries

Eye injuries can be caused during handlingand fighting and may easily become infected.In farmed American alligators several suchinjuries have been observed, includingcorneal perforation, uveitis, cataract (seeabove) and phthisis bulbi (Millichamp et al.,1983). A superficial scratch on the cornea maycause partial opacification (Fig. 7.5), whichwill disappear once the scratch has healed.Destruction and enucleation of eyes due toinjury have been reported from Orinoco croc-odiles (Boede, 2000).

Periocular abscess

A periocular abscess was found in one of theAmerican alligators autopsied during anoutbreak of mycoplasmosis (Clippinger et al.,1996) (see also p. 167).

Blindness

Occasionally crocodiles are blind from birth(see p. 152). In farming and captive situa-tions blind crocodiles can cope quite well,helped by their acute senses of smell andhearing. Blind Nile crocodiles often are dis-tinguished by a lighter skin colour than thatof their pen mates.

Cases of congenital glaucoma, withenlarged and protruding eyes and almostcomplete blindness, occurred in the progenyof a pair of captive African dwarf crocodiles(Fig. 7.6) (author’s case). Blindness can alsobe caused by eye injuries (see above) andtemporarily by the fibrinous exudate pro-duced in cases of conjunctivitis (see above).

Diseases of the Digestive System

Tooth abnormalities

Toothlessness

Crocodiles replace their teeth regularly (seep. 13). Teeth broken off in fights will there-fore regrow eventually. However, toothless


crocodiles are found or seen occasionally. Inold crocodiles this may be due to accumu-lated damage to the alveoli. Fracturing of atooth during fighting, or ripping on a preyitem, may damage the dental lamina(Erickson, 1996b). The affected alveoli maybecome permanently edentulous, and, dur-

ing a long life, toothlessness may affectincreasingly more alveoli in some individu-als. Some such toothless alveoli may becomecalcified (Hall, 1985).

On a Nile crocodile farm where adultbreeding crocodiles were dying from stresssepticaemia, after having been transferred

248 Chapter 7

Fig. 7.5. Partial opacity of the cornea of a captive Nile crocodile, probably due to a superficial scratch(photograph M. Gansuana).

Fig. 7.6. The bulging cornea of the right eye in a captive-bred African dwarf crocodile with congenitalglaucoma.

during winter to a new breeding dam (seep. 228), several specimens were seen to haveno, or only very small teeth (Fig. 7.7)(author’s case). The cause of this conditioncould not be determined. There is a possibil-ity that in this case there was no permanentdamage and that, instead, the teeth were inthe process of regrowing.

An adult captive mugger, which lost apiece of maxillary bone including parts offive alveoli and one tooth, regenerated thebone, including the alveoli and the missingtooth (Brazaitis, 1981).

Poor mineralization

Poor dental mineralization, or a completelack of mineralization of the teeth, is seen incases of nutritional osteomalacia (see p. 211).The condition has been dubbed ‘glassy teeth’(Huchzermeyer, 1986). In older juveniles,and even in adults, poor mineralization ofthe teeth is seen from time to time withoutassociated clinical problems, although thepresence of osteoporosis in such cases hasrecently been confirmed (author’s cases).The teeth are not completely glassy, butrather opaquely diaphanous (see Fig. 6.9).The underlying cause has not yet been deter-mined. It appeared that the affected animalshad received adequate supplies of calcium intheir diet. A Ca:P imbalance in the nutritionis a more likely cause.

Protruding incisors

Occasionally the long incisors penetratethrough the premaxilla and protrudethrough ‘false nostrils’ (Fig. 1.21) (see alsop. 153). This condition has been seen bymyself in captive Crocodylus palustris andCrocodylus niloticus, and appears to be quitecommon in wild C. johnsoni (Webb andManolis, 1983).

Horizontal orientation

A horizontal, sideways, orientation of theteeth is seen in juvenile crocodiles after theyhave recovered from nutritional osteomala-cia (Fig. 6.3) (see p. 211). After the diet hasbeen corrected, the jawbones harden but theteeth remain in their sideways position. In acaptive and farmed situation they are able tocope with these non-functional teeth.

For congenital defects of dentition see p. 152.

Gingivitis – stomatitis

Bite-wound gingivitis

Cases of gingivitis, sometimes spreading fur-ther into the oral cavity (stomatitis), arecaused by fighting injuries which becomeinfected (Fig. 6.11). The infection involves a


Fig. 7.7. Lack of fully grown teeth in an adult farmed Nile crocodile.

variety of bacterial and fungal agents andantibacterial treatment usually does not helpto clear the condition, particularly when theantibiotic is given in the ration, as theaffected animals may be anorexic. In thesecases, injection of vitamin C as well as sup-plementation of the ration with the same vit-amin has cleared up the condition veryrapidly (Huchzermeyer and Huchzermeyer,2001) (see also p. 218). The recommendedtreatment consists of injecting the badlyaffected animals individually twice at 48-hintervals with 50 mg ascorbic acid intramus-cularly (im), while at the same time supple-menting the wet ration with ascorbic acid,1 g kg�1 continuously. In addition, the pensshould be cleaned and disinfected thor-oughly. The crocodiles in the affected penscan also be sprayed with a well-tolerateddisinfectant, such as F10® (Health andHygiene, South Africa) at a dilution of 1:250.

Greasy gingivitis

Gingivitis can also be caused in a fashionsimilar to ‘greasy skin’ (see p. 243) by theaccumulation of fat and protein from the wetration, causing dark deposits between theteeth. These deposits are then colonized bybacteria and fungi, which attack the underly-ing gingival and oral mucosa, causing theaffected hatchlings to become anorexic. Thetreatment is the same as for bite-wound gin-givitis (see above).

Pox

The crusty lesions of caiman, as well as croc-odile, pox can be found in the oral cavity,either on the gingivae or on the palate (seepp. 157 and 158). Pox lesions on the gingivaeare prone to become infected secondarily bybacteria and fungi. The treatment is the sameas that recommended for bite-wound gin-givitis.

Ulcerative stomatitis

A proliferative ulcerative haemorrhagicstomatitis affecting the tongue containedGram-negative bacteria in the granulomas(Youngprapakorn et al., 1994). Such a lesion

could be the sequel to an injury produced bythe sharp point of a bone fragment.

Glossitis

An inflammation of the dorsal surface of thetongue was seen in some of the cases ofchronic stress dermatitis described byHuchzermeyer and Penrith (1992) (seepp. 237 and 241).

Hyperkeratosis of the oral mucosa

Anorexic animals, or animals suffering fromsepticaemia (see p. 228), often have largeareas of the oral mucosa, both tongue andpalate, covered with a brownish layer (Fig.7.8) which, on microscopical examination, isdue to hyperkeratosis of the oral mucosa.This is probably caused by latent vitamindeficiencies, and cannot be treated unless theunderlying condition has been diagnosedand treated.

Oral mycobacterial abscesses

Mycobacterial abscesses, species undeter-mined, were seen in the caudal part of theoral cavity, on the tongue and on the gularvalve, in a juvenile captive Chinese alligator(Blahak, 1998) (see also p. 170).

Inflammation of the gular valve

The gular valve serves to separate the oralcavity from the upper respiratory tract (seep. 11) and normally remains tightly closedexcept during swallowing, yawning andsome of the vocalizations. It does not containany tonsils or tonsil-like tissue. However, aninflammation of both velums (flaps) of thegular valve, with moderate lymphocytic andround cell infiltration, is seen occasionally injuvenile farmed Nile crocodiles (Huch-zermeyer and Penrith, 1992) (Fig. 7.9).

At the time, the authors speculated thatlymphatic cells normally present in the flapsof the valve might serve a tonsil-like func-tion. However, the first case in the reportwas from a specimen that had been trans-

250 Chapter 7

ported a long distance overland, and there-fore one might also speculate that the inflam-mation could have been caused by mucosalirritation due to dehydration during the pro-longed forced stay out of water. Cases seensubsequently, single deaths, may again havebeen ailing animals that had also stayed outof the water for a long time, as is common instressed and anorexic crocodiles (see pp. 278,282 and 289).

True tonsillar tissue has recently beenidentified in the roof of the pharynx in Nilecrocodiles (Putterill and Soley, 2001) (seep. 24).

Gastric ulcers

Gastric ulcers in crocodiles appear to becaused by stress (see p. 278). Many cases


Fig. 7.8. Hyperkeratosis of the palate in a juvenile farmed Nile crocodile.

Fig. 7.9. Inflammation of the dorsal flap of the gular valve in a juvenile farmed Nile crocodile.

were seen in juvenile Nile crocodiles associated with chronic stress derma-titis (Huchzermeyer and Penrith, 1992) (see p. 237) as well as in wild-caughtOsteolaemus tetraspis after prolonged trans-port (Huchzermeyer and Agnagna, 1994).Usually, the ulcers are small, with diametersof 2–4 mm, and are spread throughout theentire surface, or they are concentrated in thepyloric area and the duodenal pouch (Figs7.10 and 7.11). However, larger ulcers havealso been observed. Ulcers infested by ascari-doid nematodes (p. 192) are larger, withdiameters up to 10 mm and more (Fig. 5.39).

A striking feature accompanying the ulcersis a severe polyarteritis (see p. 269), which issuggestive of a severe autoimmune reaction(Fig. 7.12) (Huchzermeyer and Penrith, 1992;Huchzermeyer and Agnagna, 1994).

Gastric ulcers with a diameter of0.3–0.7 cm were seen in a captive Africandwarf crocodile suffering from septicaemiaand arthritis (Heard et al., 1988). Gastriculcers were found frequently in slow-grow-ing farmed spectacled caimans (Villafañe etal., 1996). Very small gastric ulcers filled withfibrinous exudate and containing bacterialnests were described by Youngprapakorn etal. (1994) as bacterial gastritis.

In the presence of ascaridoids, the para-sites will attach to the ulcerated surface andeven penetrate into the mucosa (see Fig.5.40), aggravating the condition (Ladds andSims, 1990; Foggin, 1992a; Buenviaje et al.,1994; Huchzermeyer and Agnagna, 1994;Ladds et al., 1995) (see also p. 192). Althoughthe gastric ascaridoids colonize the ulcersopportunistically, they do not appear tocause them. It is therefore most likely that allstomach ulcers are stress related, as no otherprimary pathogens have been found in asso-ciation with the ulcers.

The fungus Mucor circinelloides was iso-lated from gastric ulcers of a captive croco-dilian (Jones, 1978) (see pp. 176 and 179).

Bloating

Overeating may be the cause of bloating.Affected crocodiles die suddenly, and theirstomach is found to be filled with largepieces of meat (Fig. 7.13). This condition isthought to be caused when hungry animalsingest excessive amounts of insufficiently cutmeat. Bacterial decomposition continues inthe stomach before the gastric acid has beenable to penetrate the meat. Gas and bacterial

252 Chapter 7

Fig. 7.10. Small fibrin-covered ulcers in the stomach of a juvenile farmed Nile crocodile.

toxins are believed to be responsible for thedeath (Foggin, 1992a).

Gastroenteritis

A case of stress-related gastroenteritis in anadult wild-caught C. palustris was reportedby Sinha et al. (1987). The animal became list-

less and anorexic, had an offensive smellfrom the opened mouth and regurgitatedwhen force-fed with pieces of meat and fish.Proteus rettgeri was isolated from the faeces(see p. 174).

Treatment of the condition consisted of:

● Twice-daily dosing for 5 days with gluco-glycelect (sodium chloride, 11.4 g; calciumgluconate, 2.2 g; magnesium sulphate,


Fig. 7.11. Ulcers of different sizes in the gastric mucosa of a juvenile farmed Nile crocodile.

Fig. 7.12. Arteritis found in association with ulcerative gastritis.

0.61 g; potassium dihydrogen phosphate,8.68 g; glycine, 21.2 g; and dextrose,55.67 g), two tablespoons in 250 ml water.

● Daily dosing for 8 days with vinegar 60ml.

● Daily dosing for 8 days with tetracycline500 mg in 1 l cow’s milk after bacteriologyresults became available.

● Daily dosing for another fortnight with 1 lcow’s milk with 30 ml vitamin B complexsyrup.

● Continuation for another fortnight ofdaily dosing with 1 l cow’s milk.

● Continuation of daily dosing for anotherfortnight with meat soup.

After this the animal started eating by itself.

Gastric foreign bodies

Foreign bodies may be swallowed acciden-tally or may be part of the food. In a surveyof stomach contents of wild American alliga-tors, the following non-food items werefound: shotgun shells, dog tags, sinkers,buckshot, fishing line, gastroliths (see alsop. 36), pieces of wood and coal, nuts andsteel nails (Hazen et al., 1978). A wild-caughtAfrican dwarf crocodile in poor conditionhad its stomach distended with large wingfeathers (Fig. 7.14) (Huchzermeyer andAgnagna, 1994). Trichobezoars caused gas-

tric blockage in Mexican crocodile hatchlingsthat had been fed rats. The hatchlingsstopped growing, became thin and showedtorticollis. A change of diet to mincedchicken and fish led to a recovery of thehatchlings (Sigler, 1996). In many cases theanimals appear to be unable to regurgitatethe unwanted matter.

Sharp or pointed objects may penetratethe stomach wall and can damage otherinternal organs. However, infection is oftencontained by the inflammatory process typi-cal for crocodiles, in the form of fibriscessformation (see p. 46). A wooden toothpickswallowed by an adult captive Americanalligator penetrated the stomach wall andcaused a subserosal granuloma (Russell andHerman, 1970). Wire mesh, used to block thedrain pipes in the rearing pens on a crocodilefarm in South Africa, was eaten by a numberof juvenile Nile crocodiles (Friedland, 1986).In several of the animals the pieces of wirepenetrated the stomach wall and causedlocalized peritonitis, and in one case severeliver damage. In captive crocodiles the inges-tion of foreign bodies may perhaps not beaccidental but caused by disturbed behav-iour (see p. 289). The surgical removal of gas-tric foreign bodies, gastrotomy, is describedin Chapter 2 (p. 94). Gastric foreign bodieshave also been suspected to have caused cir-rhosis of the liver (see p. 261).

254 Chapter 7

Fig. 7.13. Nile crocodile hatchling which died after having consumed a large meal.

Sticks are embedded into fish or frogsused as bait and tied by a length of string toa tree at the edge of the water. When the baitis swallowed by a crocodile the string oftenbreaks, allowing the crocodile to escape.However the stick remains in the stomachand often works its way through the stom-ach wall and into other organs (Figs 7.15 and7.16). This is one of the common huntingmethods used to catch African dwarf croco-

diles in the Congo Republic, and severalsuch cases were found in our material(Agnagna et al., 1996).

Enteritis

The multifactorial aspect of enteritis hasbeen discussed in Chapter 6 (p. 226). Here,the emphasis is on the different forms and


Fig. 7.14. Stomach that had been distended by large feathers; wild-caught African dwarf crocodile.

Fig. 7.15. Bait stick attached to the outside of the stomach of a wild-caught African dwarf crocodile, afterhaving penetrated the stomach wall.

manifestations of enteritis which have beenseen in crocodiles. These different formsdepend on the pathogenic agent causing theenteritis and on the inflammatory responseelicited by the infection.

Necrotic

Severe necrotic and exudative enteritis isseen in cases of coccidiosis (see p. 183), aswell as in cases of adenovirus infection(Foggin, 1992a) (see p. 160), and in bothinstances is probably caused by secondarybacterial infection of the mucosal lesionscaused by the primary agents. In these cases,the necrosis penetrates deep into the muscu-lar layer of the intestine, while the exudatefills the intestinal lumen, causing occlusionof the intestine (see also p. 258). Because ofthe occlusion there is no possibility of deliv-ering a drug to the affected parts of theintestine. Any treatment must be aimed atsaving the less-affected animals (see p. 183).

Exudative

Bacterial enteritis, in hatchlings caused fre-quently by Salmonella serovars and patho-genic serotypes of Escherichia coli (see p. 145,164 and 174), usually manifests itself in theform of a severe exudative enteritis with dis-

tension of the intestine by the fibrinous mass(Plate 20). With a blocked intestine, thehatchlings are unable to digest and loseweight, while the abdomen becomes dis-tended with the fibrinous material accumu-lating in the intestine (see Fig. 4.7). Theaffected animals die slowly of starvation.Once the intestine is blocked by the fibrinousexudate, there is no possibility of treating theaffected animals.

In older juveniles, the exudate does notnecessarily cause an intestinal occlusion, andsuch animals pass pieces and strands of fibrinin their faeces. On occasion these have beenmistaken for tapeworm segments. Note thatcrocodiles do not have tapeworms (see p. 203).

Ulcerative

A case of ulcerative enteritis was found asso-ciated with an encephalitis of suspected viralorigin (author’s case) (see p. 266).

Nodular

A form of chronic enteritis characterized bysevere lymphoproliferation in the form ofdistinct nodules was seen several times inNile crocodiles (author’s cases) (Figs 7.17and 7.18). However, we were not able todetermine the cause of this condition.

256 Chapter 7

Fig. 7.16. Section of the stomach wall of a wild-caught African dwarf crocodile with a subserosalgranuloma around a remaining piece of a bait stick.

Haemorrhagic

Damage to the intestinal epithelium and thecapillaries can, in very acute cases of enteri-tis, lead to haemorrhage into the intestine. Incrocodiles this is relatively rare, as theexudative response usually prevents anybleeding. A case of haemorrhagic enteritiswas seen in juvenile farmed Nile crocodilesin South Africa, associated with a clostridialsepticaemia (Plate 21) (author’s case).Coronavirus-like particles were found in the

faeces of a healthy pen mate of the affectedcrocodiles (see p. 163). A haemorrhagicenteritis in a 2-month-old crocodile hatchlingwith non-resorbed yolk-sac was described byYoungprapakorn et al. (1994).

Colitis

A fibrinonecrotic colitis has been seen repeat-edly in juvenile farmed Nile crocodiles inSouth Africa (author’s cases). The colon wasdistended (Fig. 7.19) and the mucosa covered


Fig. 7.17. ‘Nodular enteritis’ in a Nile crocodile hatchling.

Fig. 7.18. Section of the intestine of a Nile crocodile hatchling with ‘nodular enteritis’: lymphoproliferativelesion penetrating through the intestinal muscularis.

by a fibrinous exudate (Fig. 7.20). The causecould not be determined. It is to be notedthat in chronic cases the causative agent mayno longer be present when death occurs. Acase of amoebic colitis occurred in a croco-dile (species not given), when snakes in thesame collection suffered from an outbreak ofamoebiasis (Ippen, 1965) (see p. 192).

Intestinal occlusion

Intestinal occlusion may be congenital(Youngprapakorn et al., 1994) (see alsop. 155), due to exudative enteritis (see

above), injury or torsio. A penetrating bitewound in an adult captive Nile crocodilecaused the closure of the ileum, with theslow accumulation of faecal masses craniadof the lesion (Fig. 7.21). The animal was seenlosing condition while the abdomen becamedistended, and in the end the animal had tobe euthanized (author’s case).

Several cases of intestinal occlusion areshown by Youngprapakorn et al. (1994)under the name of ‘diphtheritic massobstruction’. The ‘onion peel’ architecture istypical of the successive layers of fibrindeposited in cases of chronic exudativeinflammation (see p. 46).

258 Chapter 7

Fig. 7.19. Distended rectum in a juvenile Nile crocodile with colitis.

Fig. 7.20. Colitis: the mucosal surface of the colon is covered by a layer of fibrinous exudate.

A case of torsio intestinalis was seen in aNile crocodile hatchling (author’s case). Thesevere congestion normally seen in avianand mammalian intestinal strangulation wasnot present in this case (Fig. 7.22).

Cloacitis

Overfed American alligators tended to pro-trude the cloaca by as much as 5 cm. If theanimals spent much time on rough concrete,the protruded cloaca received abrasions andbecame inflamed. Keeping the animals in thewater and fasting them led to an improve-ment of the condition within a few days(Coulson et al., 1973). Histopathologically, acloacitis was found in one of the wild-caughtand severely stressed African dwarf croco-diles sampled on markets in the CongoRepublic (Fig. 7.23) (author’s case).

Linear ulcerations of the cloaca filled withyellow keratinized debris have beendescribed from cases of steatitis (Wallach,1971) (see p. 219).

Pancreatitis

Pancreatitis sometimes occurs as part of asepticaemia, occasionally seen as an accumu-

lation of lymphocytes in the tissue (Fig. 7.24)(author’s cases). In some cases of adenovirusinfection, intranuclear inclusion bodies arefound in the acinar cells (Foggin, 1992a) (seealso p. 160, Fig. 5.5).

Pancreatic thrombosis

A case of pancreatic thrombosis was seen ina crocodile with haemorrhagic enteritiscaused by Clostridium perfringens (author’scase) (see also pp. 172 and 257).

Involution of the pancreas

Chronically ailing juvenile Nile crocodileswere found to suffer from an involution ofthe pancreas, which appeared to be replacedby fat tissue between the duodenal loops(Fig. 7.25) (author’s cases). The cause of thiscondition remained undetermined.

Hepatitis

Adenoviral hepatitis

Hepatitis is a common manifestation of ade-novirus infection in Nile crocodiles (seep. 160). The liver is swollen and pale and thebile of light brown colour. Adenoviral inclu-


Fig. 7.21. Large faecal mass in the ileum of an adult captive Nile crocodile craniad of the healed bitewound that caused the intestinal occlusion (photograph H. Lagasse).

sion bodies are found in the hepatocytes.Chronic changes include fibrosis of the por-tal tracts and bile duct hyperplasia (Foggin,1992a).

Chlamydial hepatitis

Chlamydial hepatitis is the acute form ofcrocodile chlamydiosis (see p. 167). The liveris pale and enlarged. The histopathologicallesions are severe portal to diffuse lympho-plasmocytic hepatitis, with congestion, mild

bile duct proliferation, vacuolar degenera-tion of hepatocytes and multifocal to coalesc-ing necrosis. Chlamydial colonies are presentin many hepatocytes (Huchzermeyer et al.,1994a).

Non-specific bacterial hepatitis

Bacterial hepatitis is part of the septicaemiacomplex (see p. 228). It can range from thepresence of small granulomas with bacterialnests to multifocal and confluent necrosis

260 Chapter 7

Fig. 7.22. Juvenile Nile crocodile with torsio of the intestinal loops; the strangled loops are filled with gas.

Fig. 7.23. Section of the cloaca of a wild-caught African dwarf crocodile with cloacitis.

(Villafañe et al., 1996). A chronic hepatitiswith cirrhosis in a captive American alligatorwas interpreted as being of toxic originbecause of the presence of coins in the stom-ach (Will, 1975). However, crocodiles havebeen found to tolerate very high metal levels(see p. 221).

Degeneration of the liver

Degeneration of the liver can be caused bytoxic and nutritional factors. It can also occurdue to infection as part of the inflammatoryprocess (see above).

A fatty degeneration of the liver is seen instarving crocodile hatchlings, part of therunting syndrome (see p. 234). Fatty degener-ation with mild fibrosis and bile duct prolif-eration was seen in juvenile and adult farmedcaimans and interpreted as probably causedby mycotoxins (see p. 236) or vitamin B1 defi-ciency (see p. 217) (Villafañe et al., 1996).

Liver parasites

Rhabditid nematodes were found in the liverof a captive African dwarf crocodile from aSouth African zoo (Huchzermeyer et al.,


Fig. 7.24. Lymphocytic infiltration in the pancreas of a farmed juvenile Nile crocodile.

Fig. 7.25. Involution of the pancreas in a juvenile Nile crocodile; large portions of the pancreas betweenthe duodenal loops are replaced by fat tissue.

1993) (see p. 198). Coccidial stages are foundin the liver in cases of generalized coccidiosis(see p. 183) with severe inflammatory reac-tion, and schizonts of the blood parasiteHepatozoon are also found in the liver (seep. 188), but without any tissue reaction.

Cholecystitis

Infections of the gall bladder usually ascendfrom the intestine. Exudative cholecystitiscaused by coccidia was described by Foggin(1992a) (see also p. 183). An exudative andhaemorrhagic bacterial cholecystitis wasseen in an adult crocodile that had sufferedfrom anorexia, weakness and emaciation(Youngprapakorn et al., 1994). Similar caseshave been seen in juvenile farmed Nile croc-odiles (author’s cases), including one with aseverely distended bile duct due to anexudative inflammation (Fig. 7.26).

An apparently common haemorrhagicsyndrome has been described byYoungprapakorn et al. (1994), in whichhaemorrhages occur into the inflamed gallbladder. The affected 3–4-month-old farmedcrocodiles become anorexic, anaemic andemaciated, and die. The liver has a pale greycolour and the blood is very watery.

Inflammation and haemorrhage are found inthe gall bladder. Small emphysema lesionsare seen in the lungs. The cause of this dis-ease has not yet been determined.

Choleliths – gall bladder stones – proba-bly form in the altered environment causedby a mild infection. Such stones havebeen found in farmed crocodiles(Youngprapakorn et al., 1994) and in an adultcaptive American alligator (Clippinger et al.,1996).

Two functioning gall bladders were foundin a farmed Nile crocodile hatchling(author’s case) (see p. 155).

Steatothecitis

The inflammation of the abdominal fat body– steatotheca – occurs in cases of septicaemia(see p. 228) (Fig. 7.27) and in cases ofpansteatitis, fat necrosis (see p. 219).

In the cases of chlamydiosis (see p. 167)described by Huchzermeyer et al. (1994a),multiple small foci of necrosis were seen inthe fat body. In some cases of generalizedmycobacteriosis (see p. 170) in juvenilefarmed Nile crocodiles, granulomas contain-ing acid-fast rods were found in the fat body(see Fig. 5.13) (author’s cases).

262 Chapter 7

Fig. 7.26. Choleangitis in a juvenile farmed Nile crocodile; the distended bile duct lies across theduodenal loops; part of the liver has been removed.

Injuries to the fat body can occur frompenetrating gastric foreign bodies (Fig. 7.28)(see p. 254). A two-lobed fat body was foundin a juvenile farmed Nile crocodile (author’scase) (see p. 155).

Diseases of the Urogenital System

Infections of the organs of the urogenital sys-tem can either originate from septicaemias(see p. 228) or ascend from the cloaca. Theexact diagnosis of many kidney conditions

depends on the absolute freshness of thespecimens, as post-mortem changes mimicmany of the degenerative changes. Thismay explain the sparseness of reports onkidney affections in the veterinary crocodileliterature.

Pyelonephritis

A one-sided pyelonephritis caused theenlargement of the affected kidney, with exu-date filling the ducts, which were lined by an


Fig. 7.27. Steatothecitis; note the dark colour of the fat body and the small necrotic foci.

Fig. 7.28. Fat body of a wild-caught African dwarf crocodile pierced by a bait stick which had migratedout of the stomach.

epithelium showing squamous metaplasia(see also pp. 216 and 230) and a granuloma-tous response (Ladds et al., 1995). In the renaltissue there was a diffuse chronic interstitialnephritis with foci of intense infiltration bygranulocytes. Most likely an ascending infec-tion had been facilitated by a latent vitaminA deficiency (see p. 216). In farmed Nilecrocodiles, a gross enlargement of thekidneys was seen in cases of pyelonephritis(Huchzermeyer, 1994). Pyelonephritis as aresult of fluke infestation (see pp. 200 and265) was seen in juvenile farmed crocodiles inPapua New Guinea (Ladds and Sims, 1990).

Kidney aplasia

Occasionally only one kidney develops, andin such cases the remaining kidney is largerthan normal (Huchzermeyer, 1994). Theenlargement serves to compensate for themissing kidney.

Gout

Gout is caused by the deposition of urate crys-tals in the kidneys, in the joints of the limbs,on serosal surfaces, particularly the peri- and

epicardium, a well as throughout the muscula-ture. This occurs when, for one or other rea-son, the kidneys cannot excrete the urates inthe urine. This may, or may not, be associatedwith histopathological lesions in the kidneys.For a detailed discussion of the multifactorialaspect of gout in crocodiles see p. 230.

Dehydration is one of the predisposingfactors, and in these cases a hyaline dropletdegeneration of the tubular epithelial cells isseen (Foggin, 1992a).

Vitamin A deficiency

Vitamin A deficiency (see p. 216) causessquamous metaplasia of the epithelium ofthe collecting ducts of the kidneys of croco-diles, and this may predispose the kidneys toascending infections (see above) and to gout(see above and p. 230) (Foggin, 1992a;Buenviaje et al., 1994).

Hyaline degeneration

Hyaline degeneration of the kidneys (Fig.7.29) was found in an adult farmed Nilecrocodile that had been translocated to a newbreeding enclosure during winter and had

264 Chapter 7

Fig. 7.29. Macroscopically visible hyaline degeneration of parts of the kidney (arrow) of an adult farmedNile crocodile; the still functioning renal folds are dark.

died from stress septicaemia (p. 228). Ingreen iguanas the macroscopically visiblehyaline degeneration has been linked to vita-min D toxicity, hypervitaminosis D (Wallach,1966) (see also p. 225).

Kidney parasites

Two kidney flukes are known from croco-diles, Deurithrema gingae and Renivermis crocodyli (Blair, 1985; Blair et al., 1989) (seealso p. 260), both from C. porosus, but the former also from C. novaeguineae (Ladds and Sims, 1990). These latter authors alsofound numerous blood flukes, probablyGriphobilharzia amoena (Platt et al., 1991) (seealso p. 200) in the parenchyma of the kid-neys, some encapsulated and surrounded by severe tissue reaction. In addition,Exotidendrium sp. has been found in the kid-neys of Nile crocodiles (Foggin, 1992a).

Unidentified nematodes, 5 mm long, werefound in the severely swollen kidneys of ajuvenile captive gharial (Maskey et al., 1998).

Infection of oviduct and uterus

Infection and inflammation of the oviduct,oophoritis, and of the uterus, endometritis,can be caused by ascending infections origi-nating from intestine or cloaca, but also orig-inate from penetrating bite wounds. If, forsome reason, hormonal or metabolic, not alleggs are laid, the eggs remaining in theuterus may act as foreign bodies and alsoelicit an inflammatory response.

In all cases there is an exudative response(see p. 46), the fibrin often deposited in suc-cessive layers, onion-peel fashion, frequentlyforming large masses. Usually there are noclinical signs and the condition is diagnosedon post-mortem examination only.

Prolapse of the uterus

Prolapse of the uterus can occur during egglaying, due to excessive straining. It is possi-ble that unusual weather conditions, a sud-

den warm spell after a prolonged coolperiod, can play a role in triggering such anevent. A disturbed calcium metabolism afterthe depletion of Ca reserves for the produc-tion of the eggshells could also be consid-ered. Malformation of the cloaca in a taillesscrocodile has been cited as another cause(Youngprapakorn et al., 1994).

If such a case is seen early, before anydamage has occurred to the everted uterus,repositioning of the uterus may beattempted. For this the crocodile is immobi-lized (see p. 70) and the everted uteruswashed to remove any sand particles, best ina mild disinfectant solution. After cleaning,the size of the, often swollen, uterus isreduced by either gently massaging it withice cubes, by sprinkling tetracycline powderon it, or gently dabbing it with a dimethyl-sulphoxide (DMSO) solution. Once theuterus has shrunken to a smaller size, it canbe replaced in its correct position via thecloaca. Note that there are two uteri and thateach one has to be replaced into its own side.

Ectopic eggs

Mature follicles or whole eggs sometimesfind their way into the peritoneal cavity,where they cause a foreign-body peritonitis(egg peritonitis), often with a pronouncedexudative response, particularly if accompa-nied by a bacterial infection. A case ofchronic diffuse proliferative serositis, causedby the presence of egg yolk in the abdominalcavity, was found in a wild American alliga-tor (McDonald and Taylor, 1988).

Mature follicles can fall into the peri-toneal cavity when, during ovulation, theinfundibulum of the oviduct fails to catchthe follicle as it comes loose from the ovary.A severe disturbance at the moment of ovu-lation, as caused by fighting or capture, cancause this failure. Whole eggs with shellleave the uterus either through a rupture(Youngprapakorn et al., 1994), or they aremoved by antiperistalsis back up the oviductand out through the infundibulum. A severedisturbance, probably also fighting, maycause this antiperistalsis. The rupture may be


due to prolonged presence of the eggs in theuterus after the female, for some reason,failed to lay her eggs.

In many of these cases the affected croco-dile may live and appear normal for a longtime after the event, but eventually willbecome ill and die.

Orchitis

A case of necro-granulomatous orchitis wasfound in an adult farmed Nile crocodile thathad died from septicaemia (author’s case)(see also p. 228).

Impaired penis development

Juvenile male American alligators living inLake Apopka, Florida, showed a 24% reduc-tion in penis size when compared with ani-mals of the same body length from anotherlake in Florida. This reduction was caused byendocrine disruption due to exposure to ele-vated concentrations of the DDT breakdownproduct p,p’-DDE, which is known for itsanti-androgenic properties (Guillette et al.,1996) (see also p. 223).

Ovarian haemorrhage

Before ovulation there is a strong supply ofblood to the ovum, needed for the depositionof nutrients in the yolk. At the time of ovula-tion the blood supply to the ovum needs to becut off, otherwise haemorrhage may occur. Ifthere is a failure of the blood clotting system,due to low calcium levels or lack of vitaminK, for example, the haemorrhage may becomefatal. This is believed to have occurred with acaptive female mugger, which was founddead with a massive internal haemorrhage.The ovulated eggs had reached the shell-gland portion of the oviduct (uterus), but onlya thin layer of shell had been deposited(Whitaker and Huchzermeyer, 2000). The cal-cium demand for the production of the shellsmust have reduced the calcium level in theblood to such an extent that coagulation was

delayed. Delayed clotting was found indomestic laying hens during routine bloodsampling, when the samples were taken inthe morning at the time when the shell wasbeing deposited (author’s unpublished obser-vation).

Cystic gonads

Occasionally, cysts have been found inciden-tally in the immature gonads of juvenile Nilecrocodiles (Fig. 7.30). The cysts are probablydue to harmless malformations (author’scases).

Diseases of the Nervous System

Some of the conditions dealt with in this sec-tion are not nervous disorders in a strictsense, but rather they mimic nervous prob-lems. This grouping by symptoms has beendone to facilitate diagnosis.

Encephalitis

Encephalitis can be caused by bacteria as thesequel of a septicaemia (see p. 228) or byviral infections. A case of granulomatousencephalitis, probably of parasitic origin,was presented by Youngprapakorn et al.(1994). Cases of presumably viral encephali-tis with lymphocytic perivascular cuffingwere diagnosed in farmed crocodiles inPapua New Guinea (Ladds and Sims, 1990).A lymphocytic and plasmocytic encephalitisin very young juvenile farmed caimansoccurred in association with conjunctivitisand rhinitis (Villafañe et al., 1996) (see alsopp. 245 and 270). It is suggested that aparamyxovirus might be involved in thesecases (see p. 162). This needs further investi-gation.

My own cases in farmed Nile crocodileswere as follows. A small juvenile in goodnutritional state and without noticeable clini-cal symptoms. Brain lesions includedperivascular cuffing, glial proliferation, vac-uolization of the nerve cells in the cerebel-

266 Chapter 7

lum and demyelinization. This case wasassociated with small ulcers in the ileum (seep. 255). The second case involved a crocodileof length 1.2 m in good nutritional state withpetechiae in the brain (Fig. 7.31) and foci oflymphocytic infiltration.

Symptoms of encephalitis may vary withthe location of the lesions in the brain.Excitability, incoordination, opisthotonus,convulsions and weakness were seen byYoungprapakorn et al. (1994). Other symp-toms may be circular movements and inabil-ity to swim in an upright position.

Meningitis

Outbreaks of meningitis occurred in farmed4-month-old C. porosus. The outbreaks wereassociated with septicaemia caused byProvidentia rettgeri (Ladds et al., 1996) (seealso pp. 172 and 228).

Meningitis was also present in cases ofexperimental infection of American alliga-tors with Mycoplasma alligatoris (Brown et al.,2001b) (see also p. 167).

Encephalomalacia

Villafañe et al. (1996) describe a conditionwith nervous symptoms in juvenile andadult farmed caimans, leading to episodes ofmortality, in which they find encephalomala-cia, but with perivascular cuffing (seeabove), and also fatty degeneration of theliver. The authors suspect either mycotoxico-sis (see p. 226) or thiamin deficiency (seep. 217). In poultry, encephalomalacia iscaused by rancid fish oil in a syndrome simi-lar to fat necrosis in crocodiles (see p. 219),but the perivascular cuffing could be indica-tive of a viral infection.

Posterior paralysis

Fractures of the spine are caused by violentspasms in calcium-deficient juvenile farmedcrocodiles fed red meat exclusively (seep. 211) (Figs 6.4 and 6.5). Affected animalshave paralysed hind limbs. There is notreatment.


Fig. 7.30. Testicular cyst in a juvenile Nile crocodile.

Star gazing

The main symptom of thiamin deficiency isstar gazing – opisthotonus (see p. 217). Thisoccurs mainly in crocodile hatchlings andjuveniles fed fish exclusively (Santos et al.,1993). In the case described byYoungprapakorn et al. (1994) there was also adistinct forelimb paralysis.

Leg weakness

Leg weakness is often the first noticeablesymptom in cases of nutritional bone disease(osteomalacia) in crocodile hatchlings fed ared meat diet (see p. 211). This occurs evenbefore deformation of the vertebral columntakes place. Often the affected hatchlings canbe seen swimming normally, but they can nolonger crawl out on to the dry parts of the pen.

Brain parasites

Stages of the blood-vessel parasite,Griphobilharzia amoena (see p. 200 and below),have been found in the brain of farmed croc-

odiles in Papua New Guinea, with and with-out granulomatous tissue reaction (Laddsand Sims, 1990). The eosinophilic granulo-mata found in a crocodile brain byYoungprapakorn et al. (1994) may also havebeen elicited by parasites.

Diseases of the Circulatory System

Metazoan parasites of blood and bloodvessels

Griphobilharzia amoena has been found in theblood vessels of Crocodylus johnsoni, C.novaeguineae and C. porosus (Ladds and Sims,1990; Platt et al., 1991; Ladds et al., 1995) (seealso p. 200). The male is ± 2.5 mm long andcontains the smaller female entirely in agynecophoric chamber. When trapped in thecapillaries of internal organs, the parasite cancause localized inflammatory reactions.

Larvae and nymphae of the pentastomeLeiperia cincinnalis are found in the aorta ofthe Nile crocodile (Rodhain and Vuylsteke,1932) (see also p. 205), while the adults arefound in the trachea and the two bronchi(see p. 271).

268 Chapter 7

Fig. 7.31. Petechiae on the cut surface of the brain of a juvenile farmed Nile crocodile with encephalitis.

Microfilariae, the larvae of filarial worms(see p. 197), can be found in blood smears ofcrocodiles harbouring these parasites (seeFig. 5.44).

Protozoan blood parasites

The protozoan blood parasites of crocodilesbelong to the genera Hepatozoon (see p. 188),Progarnia (see p. 190) and Trypanosoma (seep. 191). None of these are regarded as patho-genic.

Endocarditis

The inflammation of the endothelium of theheart, particularly the valves, is caused bynon-specific bacterial infections during septi-caemia (see p. 228). It interferes with thefunctioning of the heart, eventually causingdeath (Youngprapakorn et al., 1994).

Pericarditis

Pericarditis, epicarditis (both exudative) andmyocarditis may be found associated withacute septicaemia (see Plate 11) (Ladds andSims, 1990) (see pp. 173 and 228). In cases ofpericarditis, there may be a considerableaccumulation of fibrinous exudate in thepericardial sac, which may, in fact, stranglethe heart. Pericarditis and myocarditis werefound in experimental infection of Americanalligators with Mycoplasma alligatoris (Brownet al., 2001b) (see also p. 167).

Cardiac hypertrophy

Enlargement of the heart has been describedas one of the lesions associated with thiamindeficiency (Youngprapakorn et al., 1994) (seep. 217).

Using data from 453 routine post-mortemcases (Nile crocodiles) Huchzermeyer (1994)found a strong correlation between bodylength and heart mass, and, on a smallersample (n = 36), a reasonably narrow range

of values for the relative mass of the rightventricle (right ventricular mass divided bytotal ventricular mass) of 0.22–0.36, with amean of 0.286. Chronic hypoxia, as in alti-tude disease, causes a hypertrophy of theright ventricle in certain birds and mam-mals. However, diving animals appear to bemore resistant against hypoxia. Most of thecrocodiles examined in the survey had beenkept at an altitude of >1200 m above sealevel. The mean right ventricular mass of thecrocodile hearts was higher than that of nor-mal domestic fowls kept at the same alti-tude, but there was no case of outright rightventricular hypertrophy in the surveyedgroup.

Arteritis

Severe arteritis with intima proliferation andlymphocytic infiltration of the adventitia(Fig. 7.32) was found in association with gas-tric ulcers (see p. 251) in juvenile farmed Nilecrocodiles (Huchzermeyer and Penrith, 1992)and in adult wild-caught African dwarf croc-odiles (Huchzermeyer and Agnagna, 1994).The gastric lesions appeared to be stress-related (see p. 278). The vascular lesionswere not limited to the stomach wall, butcould be found in various organs and partsof the body, suggesting a severe chronicautoimmune reaction. The mechanismsinvolved in this syndrome need furtherinvestigation.

Anaemia

Anaemia can be caused by severe or chronicbleeding, or by malnutrition. It is also associ-ated either with chronic disease or runting.Haemorrhage can occur through wounds orin the form of a haemorrhagic enteritis (seep. 255). It could also be associated with a vit-amin K deficiency (see p. 219) or rodenticidepoisoning (see p. 224). Youngprapakorn et al.(1994) mention anaemia as one of the symp-toms of thiamin deficiency (see p. 217). For adetailed discussion of runting see Chapter 6(p. 234).


Splenomegaly

A hypertrophy of the spleen is caused by theproliferation of the white pulp when the ani-mal is challenged by certain infectious agents.The crocodile spleen has a very strong fibrouscapsule, which cannot quickly accommodatethe increase of spleen tissue. Consequentlythe spleen tissue breaks through the capsulein the form of buds (Fig. 1.46) (Huchzermeyer,1994). For an exact measurement of the rela-tive mass of the spleen, the spleen:heart ratio(SHR) should be established by weighing thespleen as well as the ventricles of the heartand dividing spleen mass by ventricular mass(Huchzermeyer, 1994) (see p. 85). Ranges ofSHR values from normal crocodiles and croc-odiles suffering from various infections aregiven in Table 2.12. These values were estab-lished during post-mortem examinations car-ried out between January 1991 and December1993. The very low values at the low end ofthe ranges are due to the fact that chronic dis-ease causes an involution (shrinking) of thespleen. Normal SHR values lie between 0.3and 0.5.

Interventricular septal defect

A juvenile captive American alligator,approximately 18 months old and appar-ently clinically normal, had a hole in the cra-

nial portion of the septum between the twoventricles of the heart. It is not known howthis could have affected its ability to dive(Brockman and Kennedy, 1962).

Diseases of the Respiratory System

Rhinitis

A rhinitis–conjunctivitis–encephalitis syn-drome of suspected viral origin occurs infarmed spectacled caimans, 3 months of ageand older (Villafañe et al., 1996) (see alsopp. 162, 245 and 266).

A chronic syndrome, chronic stress der-matitis, involving the skin of the head, partic-ularly around the nostrils, a rhinitis in thenostrils, but not involving the deep nasal pas-sages, ulcerative gastritis and severe arteritis,occurs in older juvenile and subadult Nilecrocodiles (Huchzermeyer and Penrith, 1992)and appears to be associated with chronicstress (see pp. 237, 241, 251, 269 and 278).

Pharyngitis and rhinopharyngitis

Pharyngitis has been seen occasionally infarmed Nile crocodiles in association withsepticaemia (see p. 228). The inflammationinvolves the tonsillar tissue in the roof of thepharynx, the dorsal flap of the gular valve

270 Chapter 7

Fig. 7.32. Arteritis in a juvenile Nile crocodile with ulcerative gastritis.

and sometimes also the glottis (Plates 22 and23). Pharyngitis has also been found in a cap-tive C. palustris which suffered from granulo-matous pneumonia (see below) (Rahman,2000).

A disease referred to as rhinopharyngitisoccurs in crocodile hatchlings in Thailand.The affected animals have a runny nose withan accumulation of discharge around thenostrils, as well as a congestion of the roof ofthe pharynx in the tonsillar area (see p. 11),and severe oedema of the larynx(Youngprapakorn et al., 1994). The cause ofthis disease has not yet been determined.

Bronchopneumonia

A chronic proliferative bronchopneumoniawas found in a juvenile farmed Nile croco-dile, which also had ulcerations of the lin-gual mucosa, chronic hepatitis andinterstitial nephritis, all suspected to be man-ifestations of a chronic septicaemia (author’scase) (see also p. 228).

Fungal pneumonia

Fungal pneumonia is usually focal or multi-focal, with the formation of large granulo-mas with diameters ranging from <5 mm to20 mm and more (see Fig. 5.26). Predisposingfactors and the species of fungi isolated fromsuch lesions have been discussed in Chapter5 (p. 178). A case of granulomatous pneumo-nia was reported from a captive C. palustris(Rahman, 2000).

Mycoplasmosis

Pneumonia was seen in cases of mycoplas-mosis in farmed Nile crocodiles (Mohan etal., 1995) (see p. 167).

Parasites of the respiratory system

Nasal passages and pharynx

Pentastomids (see p. 205) of the genusSubtriquetra as well as Sebekia jubini are foundin the nasal passages and pharynx of croco-

dilians (Vargas, 1971, 1975; Riley et al., 1990).As it is difficult to open the nasal passages ofan adult crocodile, one can rather try to flushout the parasites by injecting a quantity ofwater into the nostrils (Vargas, 1971, 1975).

Trachea and bronchi

The adults of the pentastomid Leiperia cincin-nalis are found in the trachea and the twobronchi of the Nile crocodile, firmly attachedwith one-third of their anterior end bur-rowed in the tracheal mucosa, and sur-rounded by a friable substance, probablyfibrinous exudate (Rodhain and Vuylsteke,1932; Junker et al., 2000) (see also p. 205).

Lungs

All other pentastomids occur in the lungs(see p. 205), often without eliciting anyinflammatory response. However, localizedfoci of inflammation may occur in the lungsdue to bacterial infection, possibly triggeredby stress and/or septicaemia (Ladds andSims, 1990). Four-week-old American alliga-tor hatchlings fed with infested fish becameanorectic, lethargic, dyspnoeic and died. Onpost-mortem examination they had multifo-cal haemorrhages in the alveoli and bronchi(Boyce et al., 1984).

The parasites themselves are protectedfrom the strong immune response of the hostby constantly renewed surface membranes,excreted by the parietal glands and coveringall sensitive areas of the pentastomids (Rileyet al., 1979).

Stages of the blood-vessel parasiteGriphobilharzia amoena (see pp. 200 and 268)have been found in the lungs of farmed croc-odiles in Papua New Guinea, with and with-out granulomatous tissue reaction (Laddsand Sims, 1990).

In cases of generalized coccidiosis (seep. 183), sporulated oocysts are found in thelungs as well as in other organs (Ladds andSims, 1990; Foggin, 1992a).

Adenoviral pneumonia

While adenoviral infections (see p. 160) nor-mally affect liver, intestine and pancreas,


cases of adenoviral pneumonia have alsobeen seen (Foggin, 1992a). The diagnosis isbased on detection of the intranuclear inclu-sion bodies in histopathological sections ofthe lungs.

Foreign-body pneumonia

A 4-month-old farmed Nile crocodile hatch-ling with non-resorbed yolk-sac had, onpost-mortem examination, greyish nodulesin both lungs. On histopathological examina-tion the lesions were found to be air spacesfilled with granular material, probablyaspired proteinaceous liquid (author’s case).

Lung haemorrhage

Alveolar and bronchial haemorrhagesoccurred in young American alligator hatch-lings which became infected with pentas-tomes (see pp. 205 and 271). Occasionallylung haemorrhage has been seen on post-mortem examination of juvenile farmed Nilecrocodiles, but the cause of the haemorrhagecould not be established (Fig. 7.33) (author’scases).

Lung emphysema

Emphysematous bullae form in the lungwhen the air passages are obstructed, as inthe case of multifocal granulomatous pneu-monia in a captive American alligatorinfected with Fusarium moniliforme (Frelier etal., 1985) (see also pp. 176 and 178), in associ-ation with fungal granulomata in farmedNile crocodiles (see Fig. 5.26) (author’s cases)and also in farmed crocodile hatchlings inThailand with mucus obstructing the tracheain cases of cholecystitis (Youngprapakorn etal., 1994) (see also p. 262).

Diseases of the Skeletal–MuscularSystem

Osteomalacia

Lack of calcium and phosphorus in therations of captive and farmed crocodilehatchlings is the most common cause ofosteomalacia, particularly if the hatchlingsare fed red meat exclusively. The first symp-tom noticed is leg weakness (see p. 268), theaffected animals being unable to move onland but capable of swimming. This isfollowed by deformation of the vertebral

272 Chapter 7

Fig. 7.33. Focal disseminated haemorrhages in the lung of a juvenile Nile crocodile.

column. Further signs are ‘rubber jaws’ and‘glassy teeth’ (see p. 211). In juvenile croco-diles the teeth may be bent into a horizontalposition (see p. 247) and fractures of the ver-tebral column may cause hind-limb paralysis(see p. 267).

Osteoporosis

Many cases of mild to moderate osteoporosisoccur on crocodile farms in South Africa(author’s cases) (see p. 211). The function ofthe limbs does not appear to be affected, andfor that reason the farmers do not see this asa problem. The outstanding clinical symp-tom is poor dental mineralization,diaphanous teeth (see Fig. 6.9), which stillremain sharp and functional. The cases occuron farms with on-farm feed mixing.However, the actual causes of this conditionhave not yet been identified.

Three cases of combined fibrous osteody-strophy, osteochondrosis and osteoporosis incaptive adult or subadult Crocodylus inter-medius and C. acutus, with luxation of one ormore limbs and subsequent articularchanges, were described by Blanco (1997).The causes were probably a combination ofmalnutrition and injuries.

Limb abnormalities

Extra limbs

The presence of extra limbs is due to birthdefects (see p. 151). They always are non-functional, but may not interfere with thefunction of the four normal limbs.

Missing limbs

Missing limbs may be due to birth defects(see p. 151), to injuries (see p. 284) or toinflammatory and necrotic processes, as in acase of digital emphysema (see p. 288).While captive and farmed crocodilians maybe able to cope with one or two limbs miss-ing, certain reproductory functions, such ascopulation and nesting, may not be possiblewithout the use of the limbs.

Polydactyly

The presence of supernumerary toes on thefeet on one side, or on all four feet, is a rela-tively common birth defect (see p. 151) andusually has no deleterious effect on the func-tioning of the limbs.

Claw abnormalities

Sideways bending of the claws on all four feetis probably caused by a birth defect. However,laterally or dorsally curved or malformedindividual claws are believed to be due tohealed injuries (Webb and Manolis, 1983).

Occasionally crocodiles of any speciesmay have one or more white claws.However, all the specimens of Tomistomaschlegelii in the Singapore ZoologicalGardens have white claws (Fig. 7.34). If thiswas caused by any external factors, such aswater quality or chemicals in the water, allthe other crocodiles in the collection shouldalso have white claws, but this is not so. It istherefore suggested that the false gharials inthis collection all derive from the same wildpopulation, which is characterized by thisparticular trait. However, these crocodileswere obtained from a trader and their originis unknown (personal communication, P.Martelli, Singapore, 1996).

Arthritis

Arthritis affecting a single joint can becaused by a septic injury (see p. 284).Polyarthritis can be the sequel of a specificinfection like mycoplasmosis (see p. 167) orof a non-specific septicaemia (see pp. 173and 228). There may a visible swelling andan unwillingness, or inability, to move theaffected limb(s). Similar signs can also beseen in some forms of gout (see pp. 230 and264). No successful treatment of arthritis incrocodiles has ever been reported. Anattempt to treat a case of septic arthritis in agreen sea turtle using antibiotic-impregnatedpolymethyl methacrylate beads in a localapplication, in addition to systemic antibi-otics, was not successful (Helmick et al.,1999).


Myositis

A case of skeletal muscle myositis was men-tioned by Hibberd et al. (1996) in a survey ofdiseases in farmed juvenile C. porosus, but nofurther details were given. Debyser andZwart (1991) isolated the fungusCephalosporium sp. from small white musclelesions of a spectacled caiman (see p. 182).

White muscle disease

An outbreak of white muscle diseaseoccurred in juvenile farmed Nile crocodiles.The cause was presumed to be a vitamin Eand selenium deficiency (author’s case) (seealso p. 219).

Muscle parasites

A Trichinella sp. was found in the meat ofcrocodiles from several farms in Zimbabwe(Foggin and Widdowson, 1996; Foggin et al.,1997; Mukaratirwa and Foggin, 1999) (seep. 197) and third-stage larvae of Gnathostomaprocyonis in the meat of American alligators

in Louisiana (Ash, 1962) (see pp. 197 and199). Cestode larvae, plerocercoids, werefound in the muscle tissue of farmed C. john-soni kept in earth ponds (Melville, 1988;Millan et al., 1997b) and of a wild-caughtAfrican dwarf crocodile slaughtered at amarket in the Congo Republic (author’scase) (see p. 203). The possible presence of allthe muscle parasites should be taken intoconsideration when crocodilian meat is des-tined for human consumption (see alsop. 130).

Diseases of the Endocrine System

Thymic necrosis

In the thymus of crocodiles, small lympho-cyte-free groups of medullary stromal cellsare frequently observed, some of which are inthe process of necrosis. These are believed tobe the equivalent of Hassal’s corpuscles ofmammals. Granulomas surrounding a centralmass of necrotic heterophils and consisting,in acute cases, of large macrophages, inchronic cases mainly of multinucleated giantcells (Fig. 7.35), were found in the thymus of

274 Chapter 7

Fig. 7.34. White claws on a false gharial in Singapore Zoological Gardens.

a large number of slaughtered crocodilesfrom four different farms (Penrith andHuchzermeyer, 1993), as well as in routinepost-mortem material (author’s cases). Thesegranulomas appeared to be associated withthe above-mentioned non-inflammatorylesions thought to be equivalents of Hassal’scorpuscles. They differ morphologically fromthe thymic cysts of other reptiles, which char-acteristically are lined by an epithelium(Bockman, 1970). The possible causes of theinflammation could not be established andthe question remains whether these granulo-mas are a pathological phenomenon or partof the physiological processes in the thymusof crocodiles. Foci of colliquation necrosissurrounded by multinucleated giant cellshave also been observed in farmed Nile croc-odiles (Fig. 7.36) (author’s own material). Athymic cyst (Fig. 7.37) found in a routinepost-mortem case in a juvenile farmed Nilecrocodile was thought to have been a congen-ital malformation (author’s own material).

Parathyroidosis

The parathyroid gland is surrounded bylobes of the thymus and embedded in fattissue and therefore difficult to find (Fig. 7.38)

(see p. 21). The normal histological structureof the parathyroid glands consists ofparenchymal cellular cords associated withstrands of connective tissue and blood capil-laries (Clark, 1970; Oguro and Sasayama,1976). In cases of nutritional bone disease, inparticular osteomalacia and osteoporosis (seep. 211), a transformation and degeneration ofthe parenchyma is seen, often with the for-mation of cysts (Fig. 7.39) (author’s cases).Parenchymal degeneration and cyst forma-tion were also found in a parathyroid of aseverely stressed wild-caught African dwarfcrocodile (p. 130) (author’s case). This obser-vation raises the question as to whethersevere stress can affect parathyroid function,and thus also play a role in the aetiology ofbone disease.

Thyroid pathology

Occasionally inflammation, degenerativechanges and cysts were found in crocodilethyroids during routine post-mortem andhistopathological examinations of juvenilefarmed crocodiles (Figs 7.40–7.44) (author’scases). These changes did not appear to beassociated with any particular clinical mani-festation, nor could their causes be estab-


Fig. 7.35. Thymic necrosis: necrotic focus surrounded by multinucleated giant cells in a juvenile farmedNile crocodile.

276 Chapter 7

Fig. 7.36. Focus of colliquation necrosis surrounded by multinucleated giant cells, juvenile farmed Nilecrocodile.

Fig. 7.37. Thymic cyst in a juvenile farmed Nile crocodile.

lished, except possibly for a case of C-cellhyperplasia in the thyroid of a severelystressed wild-caught African dwarf crocodile,which might have been due to prolongedsevere stress (see p. 130) (author’s case). Casesof goitre have been found in snakes, also with-out determined causes (Topper et al., 1994).

Stress

Stress is one of the defensive functions of thebody and is regulated by the central nervous

and endocrine systems. The defensive reac-tion is in direct proportion to the intensity ofthe insult, the stressor. As the two, the stres-sor and the response, are practically insepa-rable, they are commonly both referred to asstress.

The defensive reactions may exert negativeinfluences on certain other systems. Failure tocope, particularly in captive and farming situ-ations, where crocodiles may be subjected toexcessive, continuous or repetitive levels ofstress, may lead to a breakdown, with conse-quent disease and mortality. In this sense


Fig. 7.38. Cystic Nile crocodile parathyroid gland surrounded by lobes of the thymus.

Fig. 7.39. Cystic degeneration of the parathyroid gland of a juvenile farmed Nile crocodile suffering fromnutritional bone disease.

stress can also be regarded as a disease condi-tion of the endocrine systems involved in it,particularly the adrenal glands.

The consequences of stress reactions andtheir implications for the course of certaindiseases, but also on the management of cap-tive and farmed crocodiles, are discussed inthe following section. They also play a majorrole in all of the multifactorial diseases (seep. 226).

Foci of necrosis were found in the adren-als of a wild-caught African dwarf crocodile

which had been subjected to severe and pro-longed stress (see p. 130) (author’s material).

Miscellaneous PathologicalConditions

Some of the conditions dealt with in this sec-tion are quite unimportant, but wereincluded for the sake of completeness.Others are important but have been insertedhere as they did not seem to fit into any of

the preceding sections. While some logic wasinvolved in deciding names, sequence andcontents of sections, there also was a certainamount of arbitrariness.

Stress

Physiology

The physiology of stress in crocodiles hasbeen researched extensively (Lance and

Lauren, 1984; De Roos et al., 1989; Elsey et al.,1990a,b, 1991; Mahmoud et al., 1996; Moriciet al., 1997; Turton et al., 1997; Lance andElsey, 1999a,b). To a large extent the reactionsare similar to those in other reptile, avianand mammalian species, with an increasedproduction of adrenaline and corticosteroids.

Stressors

Some of the stressors important for croco-diles have been identified. They are:

278 Chapter 7

Fig. 7.40. Thyroiditis in a farmed Nile crocodile.

Fig. 7.41. Goitre in a farmed Nile crocodile.

● Capture and restraint (Elsey et al., 1991;Mahmoud et al., 1996; Lance and Elsey,1999b). This includes handling, takingblood samples, giving injections, force-feeding and other such actions, all placingthe crocodile in a situation from which itcannot escape. It appears, though, that

young hatchlings are more tolerant ofhandling, provided it is done gently. Thismay have to do with the observation thatcrocodile mothers will occasionally carrytheir hatchlings in their mouths.

● Transport (Elad et al., 1987). While this isalso part of restraint, it may further entail


Fig. 7.42. C-cell hyperplasia in the thyroid of a severely stressed wild-caught African dwarf crocodile.

Fig. 7.43. Large cyst on the right thyroid of a farmed Nile crocodile.

disorientation in the new location, withthe necessity to establish a new territory,as well as possibly having to cope with asudden climatic change. All this is part ofan inability of the crocodile to move freelyand choose its own territory.

● Cold and sudden change in temperature(Turton et al., 1997; Lance and Elsey,1999a). The major factor here is an inabil-ity to thermoregulate. Captive and farm-ing conditions often restrict or limit thethermogradient available to the crocodilesand which is necessary for an active ther-moregulatory behaviour.

● Overheating (Turton et al., 1997). Herealso there is an inability to escape the heatand to thermoregulate actively followingan environmental thermogradient, non-existent in this case.

● High stocking density (Elsey et al.,1990a,b; Morpurgo et al., 1992).Overstocking causes an inability to moveaway from other individuals. Whilehatchlings in the wild live in shoals forsome time, juveniles tend to movearound, away from adult crocodiles, butalso away from other juveniles. Thedegree of territorial tolerance is differentin different species, but in general thesame principle applies to all crocodilianspecies. Adult breeding crocodiles ofsome species may need fairly large indi-

vidual territories, particularly species thatlive in pairs. However, it appears thatadult farm-reared crocodiles are less terri-torial than wild-caught breeding stock ofthe same species.

● Fear (Watson, 1990). This is an inability toget away from frightening experiences orexpected events. Capture and handling ofsome of the crocodiles on a farm causesthe other crocodiles in the same pen tofear that the same might happen to them,and from this they cannot escape.Hatchlings are afraid of birds flying over-head. To escape them, they want to gounder cover. Even inside a rearing house,the ceiling or roof above is not perceivedby them as cover. Such a cover must beclose to the ground. Consequently fear iscaused by certain events, but the stressfulpart is the inability to escape or take cover.

The inability to do what is instinctivelydemanded in any of the above situations canalso be translated as frustration, and thisleads to the simple equation: frustration =stress. It follows that stress, at least initially,is a psychological problem. Several eventscausing frustration can happen concurrentlyand thereby have an additive effect. Thiseffect does not only depend on the severityof the stress or stresses, but also on theirduration.

280 Chapter 7

Fig. 7.44. Section of a cystic thyroid of a farmed Nile crocodile.

Effects

Short-term stress, with its adrenaline surge,can have a stimulating effect, but of impor-tance are the nefarious effects of longer orsevere exposure to stress. Not all the effectsbelow have been confirmed experimentallyin crocodiles. However, they occur widely inall higher vertebrates and most of them haveat least been observed in crocodiles in realsituations.

● Immune suppression is caused byincreased levels of corticosteroids in thecirculation. It does not only affect specificimmunity, but also the short-term, non-specific immunity, which in domesticfowls occurs between 6 and 72 h afterstimulation with an antigen (Matsumotoand Huang, 2000). Immune suppressionby stress can be compounded by the sup-pression of the immune system at lowbody temperatures. Consequently, expo-sure to stress (capture, transport) duringwinter can have more serious conse-quences than during summer. Blood corti-costeroid levels and white blood cellcounts depend on a number of extraneousfactors (Turton et al., 1997). While theirdetermination in experimental work isvaluable, there appears to be a limit totheir usefulness as clinical tools.

● Disturbance of the mucosal barrier of theintestine. Normally, intestinal bacteria aretransported across the mucosal barrier forpresentation to the immune system andthe production of specific antibodies.Several mechanisms have been studied inmammals (Fields et al., 1986; Neutra et al.,1996; Neutra, 1998; Nadler and Ford, 2000)and they are believed to apply to croco-diles as well. Gut translocation is knownto occur in human patients suffering fromtrauma and shock, resulting in septi-caemia (Deitch et al., 1996). Cases of septi-caemia involving intestinal bacteria havebeen seen in crocodiles suffering fromsevere stress (Huchzermeyer, 2000). Thisphenomenon has been given the namestress septicaemia (see also p. 228) and itappears to play a major role in the pathol-ogy of captive and farmed crocodiles.Fungi can also be translocated across the

mucosal barrier and cause fungaemia.Many of the intestinal fungi of crocodilesare cryophilic and will thrive at low tem-peratures, at which bacteria may not beable to multiply (see p. 182). CaptiveAmerican alligators that had been translo-cated to a hibernation grotto and acciden-tally subjected to very cold temperaturesdeveloped generalized fungal infections(Fromtling et al., 1979a,b). Fungal infectionof the lungs does not need the inhalationof fungal spores, but can also take placevia the blood circulation, proven at least inostriches (Walker, 1912).

● Substance depletion. Certain substancesnecessary for the metabolism of the hostbecome depleted under stress. Studies inthe domestic fowl have demonstratedstress-induced vitamin C depletion in theadrenal glands (Perek and Eckstein, 1959).The lowering of plasma zinc levels understress conditions in domestic species hasbeen reviewed by Hambridge et al. (1986).No such work has yet been carried out incrocodiles. In some cases it may be possi-ble to counteract the deleterious conse-quences of stress by supplementing thedepleted substances. See Note Added atProof, p. 239.

● Disturbed behaviour. In ostriches thedisturbance of normal behaviour patternsis a major consequence of exposure tostress (Huchzermeyer, 1998a). To someextent this appears to happen in stressedcrocodiles as well. Three disturbed behav-iours can be identified: anorexia,hydrophobia and excessive lithophagy (p.289). Anorexia may be complete orinvolve the refusal to eat less palatablefeeds (p. 282). It is a major cause of runt-ing (p. 234). Hydrophobia is the refusal ofstressed crocodiles to go into the water. Itis one of the causes of dehydration (p.283) and gout (p. 230). While lithophagyis seen as part of the normal behaviourspectrum of crocodiles, excessivelithophagy, involving stones as well asmany other foreign objects, must be seenas pathological and may necessitate surgi-cal intervention (pp. 36, 94 and 254). Thedisturbed behaviour of crocodiles can beused to diagnose stress.


Treatment

The most important aspect of the treatmentof stress-related conditions is the recognitionand removal of the stressor. This cannot bedone in the laboratory. The consulting veteri-narian may have to visit the farm to investi-gate present and past conditions andoccurrences that could have precipitated theproblem. The time scale of stress-relatedprocesses depends on the size of the croco-dile, as well as on environmental tempera-tures. Juvenile crocodiles in a heated housemay show signs of stress septicaemia within10 days, while adult crocodiles translocatedduring winter may die several months afterthe event.

Depleted substances can be supple-mented. The beneficial effect of supplemen-tation with vitamin C to stressed poultry hasbeen documented (Gross, 1992) as well as itseffects on the immune system (Bendich,1990). It prevents the slide in heterophil/lymphocyte ratios and also increasesresistance against infection.

Some adrenal-blocking agents may wellwarrant further investigation and experi-mentation in crocodiles. Substances thathave been tried in poultry are ketoconazole(Pont et al., 1982), as well as dichloro-phenyldichloroethane (Rothane®, ICNPharmaceuticals) and Metyrapone® (CibaGeigy) (Gross, 1990). However, in most casessuch chemotherapy will come too late, ifmortality from stress-related conditions hasoccurred already.

Fungal and bacterial infections precipi-tated by stress may warrant specific treat-ment, depending on the agent. For thetreatment of anorexia see below.

Prevention

The prevention of stress must primarily bebased on the prevention of stressful condi-tions and occurrences. These have been dis-cussed above in detail, and this knowledgeshould be applied to all captive and farminginstallations and their management. All han-dling of crocodiles should be done with min-imum fuss, quietly and as gently as possible.Where stressful situations or events cannot

be avoided, there may be several courses ofaction, such as tranquillization/immobiliza-tion (see p. 70), which not only reduces thelevel of stress in the animal to be capturedand handled, but also in the other crocodileswitnessing the event. When environmentalstressors are involved, prophylactic supple-mentation with ascorbic acid (vitamin C)should be considered.

Anorexia

While it has been reported that anorexia inhatchlings may be caused by an unsuitablediet, e.g. minced fish (Foggin, 1992a), all evi-dence points at stress as the main cause (seeabove), with stressed animals being lesslikely to accept an unpalatable diet, such asminced fish or pelleted feed (see also p. 289).Hatchlings most commonly become stressedby fear and fluctuating temperatures, includ-ing occasional overheating. In older croco-diles anorexia is often triggered by handlingand transport.

Once a crocodile has stopped feeding, itbecomes hypoglycaemic, and the hypogly-caemia further suppresses the appetite. Suchanimals may simply starve to death, if theyare not killed earlier by a concomitant stresssepticaemia (see p. 228). The only way tobreak this slide towards death is by stimulat-ing the appetite in one way or another, whileat the same time optimizing environmentalconditions. This must be done without dras-tic changes that could further stress the ani-mal.

One can try moving food in front of theanimal’s head, enticing it to snap, or, forhatchlings, some insects (cockroaches orcrickets) can be released into their pen. Onone Nile crocodile farm with semi-open rear-ing pens, a light was suspended high aboveeach rearing pen and the hatchlings jumpedat the insects which fell down after flyinginto the light (see Fig. 3.11).

If these attempts fail in larger crocodiles,one can tap the crocodile on the snout with astick. The crocodile then will open its mouthand one can place a morsel of food, possiblyinjected with a multivitamin preparation,into its mouth and wait for the morsel to be

282 Chapter 7

swallowed. If the morsel is rejected and themouth is opened after another tap on thenose, an amount of thick sugar solution orhoney is smeared on to the base of thetongue. Most of this sugar or honey will beswallowed slowly and absorbed. It willcause the blood sugar level to rise, and afterpossibly two or three such applications, oneeach day, normal feeding may resume.Alternatively, subcutaneous injections (seep. 89) of a glucose solution, and possibly alsomultivitamins, can be given.

Small hatchlings tolerate handling moreeasily and can be force-fed (see p. 87) a sugaror glucose solution, or a more complex nutri-ent fluid, e.g. one cup of milk with one hen’segg yolk and a tablespoon of sugar or glu-cose.

Stimulation of the appetite by oral dosingwith metronidazole (Flagyl®) 125–250 mg kg�1

has also been suggested (Thurman, 1990).Gastric function in ostrich chicks sufferingfrom gastric stasis, also a stress-related con-dition, is restimulated by the injection ofmetaclopramide 0.1 mg kg�1 live mass(Huchzermeyer, 1998a).

The loss of salt into the water (p. 41) canbe counteracted by adding salt to the water1 g l�1 (p. 86) or by dosing with a liquid con-taining salt, e.g. meat broth (Sinha et al.,1987) (see p. 253).

Dehydration

While dehydration can occur during a longperiod of transport, rehydration will occurwhen the transported animals are releasedinto the water. However, care must be takenthat they have fully recovered from chemicalimmobilization (see p. 70) before they aregiven access to water, because otherwisethey might drown (see also p. 290).

Refusal to go into the water, hydrophobia,is one of the manifestations of stress andshould be seen as a behavioural disturbance(see pp. 278 and 289). It is the most commoncause of dehydration. Severe dehydrationcan cause a malfunctioning of the kidney,leading to gout (see pp. 230 and 264).

As stress-induced dehydration is alwaysassociated with anorexia, its treatment

should be combined with the treatment forthat condition (see above). The same consid-erations also apply to optimizing environ-mental conditions. In addition, physiologicalsaline solution can be given by injection, andhatchlings can be dosed with fluids bymouth (see p. 86).

Neoplasms

Not all swellings found on or in crocodilesare true neoplasms. ‘Pseudotumours’ arecaused by the inflammatory process nowcalled fibriscess, which takes place aroundlocalized bacterial infections, particularlyseptic wounds (Huchzermeyer and Cooper,2000) (see also pp. 46 and 287). All of the‘growths’ recorded in C. johnsoni (Webb andManolis, 1983) apparently fall into this cate-gory.

Granulomata are caused by localized fun-gal infections, commonly seen externally inskin abrasions and internally in cases ofstress-associated generalized mycoses (seepp. 182 and 281). The surgical removal ofsuch a granuloma from the palatal fold of thebasihyal valve of a captive C. palustris andthe removal of digital granulomata from acaptive American alligator have beenreported (Ensley et al., 1979; Russo, 1979).Smaller digital granulomata could have beenmisdiagnosed as warts, which were reportedduring a discussion at a meeting without anyfurther details (Schlumberger and Lucké,1948). A wart-like structure on the dorsumnasi was found in a captive male Americanalligator (Wadsworth and Hill, 1956). Thewart-like appearance of such granulomas isshown in Fig. 7.45.

True warts, papillomas, have not beendescribed from crocodiles and there are onlyvery few reports of other neoplasms in croc-odiles:

● A captive male American alligator diedfrom a very large seminoma attached tothe dorsal wall of the abdominal cavity(Wadsworth and Hill, 1956).

● A round cell tumour was found in theliver with metastases in the cerebellumand heart in a captive C. porosus (Scott


and Beattie, 1927). Later this tumour was re-interpreted as lymphosarcoma(Schlumberger and Lucké, 1948).

● A polycystic ovarian mesothelioma wasfound in an adult captive Crocodylus acu-tus (Obaldia et al., 1990).

● A fibrosarcoma was found to obstruct theoropharynx of a captive adult maleCrocodylus siamensis (Janert, 1998).

● A chondroma was excised from a juvenilecaptive Caiman latirostris (personal com-munication, J.C. Troiano, Buenos Aires,1999).

● A stalked mass attached to the left hindfoot of an adult crocodile was diagnosedas fibroma and a bulging mass on theback of the thorax of an adult crocodile aslipoma (Youngprapakorn et al., 1994).

● Bone tumours of undetermined naturewere found on museum skeletons of twoCaiman crocodilus (Kälin, 1936).

Cysts were found on the skin of hatchlingcrocodiles, as well as in the mesentery and inthe salivary glands of adult crocodiles(Youngprapakorn et al., 1994), also under theeye (Plate 24) and near the nostrils (Fig.7.46). They are probably due to blockages ofglandular ducts. See also gonad cysts (p. 266), thymic cyst (p. 274) and thyroid cyst(p. 275).

Injuries

Crocodiles are prone to injuries throughintraspecies aggression in the wild as well asin captive and farming systems. In juvenilefarmed Nile crocodiles, aggression wasrelated to body size, stocking density andfood preference, and directed mainly bylarger towards smaller individuals(Morpurgo et al., 1993b). Sexually maturecrocodiles may fight for territory, the posses-sion of a female or over a nesting site. In cap-tive and farming situations, where there isno escape for the loser, hierarchical fightsmay take place again and again (see p. 54).

Injuries sustained may be series of skinpunctures, raking wounds across an area ofthe skin, deep gashes, amputations of toes, ofpart of the tail and even whole limbs. Part ofthe upper or lower jaw may be broken or sev-ered (Figs 7.47–7.49) and deep penetratingbite wounds may injure the internal organs,leading to further complications, such asintestinal occlusion (see p. 258) or peritonitis(Schoeb, 1999). Most likely this latter case hadresulted from a bite wound as well.

Interspecies interactions are far lessimportant and, with the exception of othercrocodile species, mainly involve huntinginjuries caused by man, such as a nativespear imbedded in the back of a Nile croco-

284 Chapter 7

Fig. 7.45. Wart-like appearance of fungal granulomas on the toes of a juvenile farmed Nile crocodile.

dile and penetrating its stomach (Hippel,1946), but also gunshot wounds and injuriescaused by rough handling during capture.

All injuries occur in a septic environmentand penetrate the skin, which often is colo-nized by intestinal bacteria. Consequently,all these injuries can be regarded as septic.However, cases of septicaemia contracted

from such wounds are extremely rare. This isdue to the immobilization of the bacteria inthe wound by the exudation of fibrin (fib-riscess formation, see pp. 46 and 287), whichprevents the draining of infected lymph intothe general circulation.

Healing usually is rapid, but fibriscessesin deep wounds, or damage to internal


Fig. 7.46. Cyst near the nostrils of a captive Nile crocodile (photo Marc Gansuana).

Fig. 7.47. Nile crocodile hatchling with amputated upper jaw and broken lower jaw.

organs, may have more serious conse-quences. However, regeneration is limitedand recorded only for parts of the upper jaw(Brazaitis, 1981) and the tip of the tail (Kälin,1936). The regenerated tail tip may be cov-ered by a uniform layer of keratin. The tailabnormality depicted by Troiano and Román

(1996) also appears to be a regenerated tailtip.

Where the treatment of a wound necessi-tates the capture and immobilization of theanimal, one must consider the stress causedby such an action and weigh the danger of alocalized wound infection against the possi-

286 Chapter 7

Fig. 7.48. Adult farmed Nile crocodile with amputated upper jaw.

Fig. 7.49. Captive gharial with amputated upper jaw.

bility of causing stress and septicaemia (seepp. 228 and 278) by the necessary use of force.

Where the wound is accessible, it shouldbe cleaned out with a cotton swab and a 10%solution of hydrogen peroxide, and allnecrotic tissue and fibrin should be removed.The cleaned wound should be treated liber-ally with a proteolytic enzyme spray, left fora few minutes and than sprayed with a gen-tian violet spray (Flamand et al., 1992). If atall, only absolutely clean wounds should besutured, and local anaesthesia should beused for this procedure (see p. 92).

Abscesses

Infected local swellings have, in the past,been referred to as abscesses. However, theydo not contain pus but fibrin, and in croco-diles they are not encapsulated, nor are theyassociated with necrotic processes (Fig. 7.50).The term ‘fibriscess’ has been proposed todifferentiate this type of swelling or pseudo-tumour from true abscesses (Huchzermeyer,1999; Huchzermeyer and Cooper, 2000) (seealso p. 46). A persistent infection may causethe continuation of fibrin exudation andthereby a slowly increasing growth of afibriscess.

Where such a swelling does not interferewith the normal functions of the body, it isbest to leave it alone. However, if a surgicalintervention does become necessary, caremust be taken to remove all traces of fibrin,disinfect well, use a proteolytic enzymespray and also an antibacterial powder orspray before closing the wound.

Handling and immobilizing the crocodile,as well as transferring it to a clinic for theoperation, may already cause stress (seep. 278). Keeping the treated crocodile out ofthe water to prevent re-infection of thewound may cause further stress, as well asdehydration (see p. 283). These pointsshould be taken into account when a surgicalintervention is considered.

Arthritis

Arthritis limited to one joint can be causedby a septic injury penetrating the joint (seealso p. 284). However, much more commonin crocodiles is polyarthritis, the inflamma-tion of many joints at the same time, which isa common sequel to non-specific septi-caemias (see pp. 173 and 228). The onlyspecific disease associated with polyarthritisis mycoplasmosis (see p. 167).


Fig. 7.50. Juvenile farmed Nile crocodile with fibriscess formation under the sternum as the conse-quence of a penetrating bite wound.

Usually the area around the joint becomesswollen and the animal is unwilling to usethe affected legs. Note that in poikilothermicanimals the temperature of the affected jointis not elevated.

An inability to move can also be causedby nervous disorders, such as encephalitis(see p. 266) and meningitis (see p. 267), bythe fracture of a vertebra (see p. 267) or bywhite muscle disease (see pp. 219 and 274).

On post-mortem examination of cases ofarthritis, one finds either increased quantitiesof synovial fluid, clear yellowish or turbid inearly cases, or dry deposits of fibrin.Bacterial culture will reveal the presence ofthe causative organism.

There is no treatment. Note that some ofthe anti-inflammatory drugs, which onemight be tempted to use, are nephrotoxic (seep. 226). The prevention of arthritis is based onthe prevention of stress, as stress is the onefactor that triggers septicaemia (see p. 278).

Interdigital emphysema: bubble foot

Gas bubbles forming in the interdigital skinfolds (web) on the feet of crocodile hatch-lings have been seen in C. porosus hatchlingson two farms in Australia (Turton et al., 1996)

and in C. niloticus hatchlings on one farm inZimbabwe (Fig. 7.51) (author’s case). In theAustralian case, the bubbles appeared toform in lymphatic spaces and elicited a mildinflammatory response. Various bacteriawere isolated from the lesions and poxviruswas found on the skin surface, but acausative agent could not be determined.The Zimbabwean farm used water from ahot spring and it is surmised that the watercontained gas under pressure which, whendrunk by the hatchlings, caused gas to bub-ble out in the feet, in a fashion similar to gasbubble disease in fishes (Wedemeyer et al.,1976). This could be prevented by storing thewater in an insulated tank and allowing thegas pressure to equalize, before using thewater in the rearing pens.

Frostbite

When juvenile American alligators wereplaced in bags into a freezer to achieve abody temperature of 2.5–8°C in preparationfor heart surgery, the extremities of some thealligators were outside the bag and exposedto the extreme cold. In one case this led tofrostbite, with the stratum corneum slough-

288 Chapter 7

Fig. 7.51. Interdigital emphysema, bubble foot, in a farmed Nile crocodile hatchling.

ing off where the scales had been frozen(Kennedy and Brockman, 1965). (Note thatthe cool room and freezer temperaturesstated in this paper (40°C and −48°C respec-tively) probably were calculated incorrectlywhen converting °F to °C.)

Overheating

The optimal body temperature of crocodilesof 31–33°C is very close to the toleratedupper range of 35–36°C. The upper-rangetemperatures can cause severe stress (seep. 278), while a body temperature of 37°Ccan be lethal. The smaller the crocodile, thequicker its body reaches the temperature ofthe environment. Consequently, hatchlingsare more sensitive to overheating than largerjuvenile or adult crocodiles. On farms withopen or semi-open rearing facilities, the dan-ger of overheating exists as soon as air tem-peratures rise above 36°C, even if thehatchlings can escape into the shade. If shal-low water is exposed to the sun, its tempera-ture can rise above 36°C as well. This thencreates an inevitably lethal situation for thehatchlings.

Crocodiles exposed to extreme tempera-tures cannot sweat to cool down their body.While they are losing some moisture throughthe skin, this is not used as a thermoregula-tory mechanism to any extent. They have touse the thermogradient in their environmentto maintain their preferred body temperature(see p. 55). In many captive and farming sys-tems the range of possibilities for active ther-moregulatory behaviour is inadequate (Fig.7.52).

The consequence of overheating stress inhatchlings is anorexia, and in older juvenilesan unwillingness to eat unpalatable food (seep. 282). In all age groups there is anincreased sensitivity to specific and non-spe-cific infections (see p. 278). In extremeevents, mortality, even mass mortality, mayoccur.

Disturbed behaviour

Organic diseases

Seemingly disturbed behaviour may becaused by central nervous pathology, as instar gazing – thiamin deficiency (see pp. 217and 268), and circular movements or loss of


Fig. 7.52. Nile crocodile hatchlings in a small semi-open pen, potentially unable to escape overheatingon a hot day.

balance in cases of encephalitis (see p. 266) ormeningitis (see p. 267), by pain as in cases ofarthritis (see p. 287) and arthritic gout (seep. 230), as well as by muscular disorders suchas myositis and white muscle disease (seep. 274) and also by osteomalacia (see p. 211).

Stress

True behavioural disturbances are caused bystress (see p. 278). Three forms of behaviourare seen in this category: anorexia or therefusal to accept all or certain foods (see alsop. 282); hydrophobia, the refusal to go intowater with consequent dehydration (see alsop. 283); and excessive lithophagy (see pp. 36,94 and 278).

Fear – piling

A frightened crocodile will try to seek refugeeither in deep water or under shelter. Theyounger the crocodile, the more serious is itsneed to escape perceived danger. Piling in acorner of the pen is a normal reaction to fear,sudden fright, but it is aggravated by shal-low water, which is not seen as a sufficientlysafe refuge, and the lack of hide boards,under which the animals would normallyseek shelter. Piling is worse under highstocking densities. In this sense piling is nota behavioural problem of the crocodiles butrather a design problem of the rearing facil-ity, a problem of management.

While animals used to human presenceare less likely to take fright and to pile, thebest solution to the problem lies in the provi-sion of hide boards under which the croco-diles will feel safe (see also p. 114). Pilingmay cause death by suffocation and it canalso cause severe damage to the belly skinsby scratches caused by the protruding longcanine teeth (see p. 241).

Good management

The stressed-induced behaviour problemsdiscussed above, anorexia, hydrophobia,excessive lithophagy and piling, should notonly be seen as problems by themselves butalso as indicators of stress on the farm, andtheir absence as a sign of good management.

Drowning

Drowning is diagnosed either when the deadcrocodile is found in the water, floating orlying on the bottom, or when on post-mortem examination the lungs are found tobe filled with water. There are several possi-ble circumstances under which crocodilesmay drown, particularly in captive or farm-ing conditions.

Mechanical

The pen design may be such that hatchlingscan get trapped under a heating pipe anddrown (see Fig. 7.52), or under any otherunderwater structure.

Tetany

Crocodiles suffering from seizures due tohypocalcaemia (see pp. 211 and 267) havebeen known to drown (Foggin, 1992a).

Nervous abnormality

Crocodiles suffering from brain disease, suchas encephalitis (see p. 266) and meningitis(see p. 267), may not be able to control theirmovements sufficiently to come to the sur-face for breathing, and consequently maydrown.

Drugged

While recovering from the effects of immobi-lization (see p. 70), crocodiles may go intothe water, before being able to swim to thesurface for breathing, and consequentlydrown. It is important, therefore, that theyare denied access to water, even if in dangerof dehydration, until they have recoveredfully.

Weakness

Weakness may prevent crocodiles fromclimbing out of the water area in their penon to land. If this weakness is caused byosteomalacia (see p. 211), an affected hatch-ling may be able to swim around for a longtime. If the pen design allows, the animal

290 Chapter 7

may remain on the shallow slope with itshead out of the water. However, generalweakness of a sick animal may in the endcause it to drown.

Agonal

Any sudden death may cause a last agonalbreath to be taken. If sudden death occurs inthe water, such a movement will cause the

lungs to fill with water. In this case the post-mortem appearance will be that of drown-ing, and the true cause of death may remainhidden.

Deformities

Tailless crocodiles are unable to swim anddrown in deep water when they are unableto swim to the surface (see also p. 149).


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Williams, P.A., Mitchell, W., Wilson, G.R. and Weldon, P.J. (1990) Bacteria in the gular and paracloacalglands of the American alligator (Alligator mississippiensis; Reptilia, Crocodilia). Letters in AppliedMicrobiology 10, 73–76.

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Wintrobe, M.M. (1933) Variations in the size and hemoglobin content of erythrocytes in the blood of vari-ous vertebrates. Folia Haematologica 51, 32–49.

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320 References

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References 321

Abattoir 123–124Abdominal wall defects 155Abrasions see SkinAbscess see FibriscessAcanthocephala see HookwormAcanthostomum

atae 200caballeroi 200coronarium 200diploporum 200elongatum 200loossi 200, 203marajoarum 200pavidum 200productum 200quaesitum 200scyphocephalum 201vicinum 201

Acid–base balance 41, 43, 47Acinetobacter 37

anitratus 38calcoaceticus 38wolffi 38, 130

Acremonium sp. 40ACTH 91Adenovirus 74, 117, 157, 160–161, 167, 228, 234, 256,

259, 271–272Adrenal 22, 79, 218, 277

blocking agents 282necrosis 277

Adrenaline 43, 91, 278Advocin® see DanofloxacinAerobacter radiobacter 38Aeromonas 37

hydrophila 38, 39, 67, 142, 173, 225, 239shigelloides 173

Aestivation 41, 44, 55African dwarf crocodile see Osteolaemus

tetraspisAfrican slender-snouted crocodile see Crocodylus

cataphractusAge 101, 116

determination see Bone rings–length–weight relations 34–35

Agema silvaepalustris 207Aggression see FightingAlbendazole 197Albinism 154Albumin 48, 49Alcaligenes

denitrificans 130faecalis 39

Algal toxins 224Algicides 224, 225, 231Alkaline tide see Acid–base balanceAllechinostomum crocodili 201Alligator

mississippiensis 4, 7, 18, 22, 24, 25, 28, 30, 34,35, 37–38, 40, 42, 43, 44, 45–46, 47, 48,49, 50, 51, 52, 56, 67, 68, 70, 71, 91, 92,93, 94, 95, 96, 99, 100, 101, 102, 113,117, 121, 123, 125, 129, 139, 141,146–148, 149, 151, 154, 155, 163, 167,172, 173, 174, 176, 177, 178, 183, 190,192, 193, 197, 199, 200, 201, 202, 203,204, 207, 208, 219, 221, 222, 223, 224,230, 231, 239, 240, 244, 245, 246, 247,254, 259, 262, 265, 266, 267, 269, 270,271, 272, 274, 281, 283, 288

sinensis 4, 9, 28, 52, 56, 170Alligator hatchling syndrome 146–148, 172Allometry 34

Index

323

Alofia ginae 207indica 207merki 207nilotici 207parva 207platycephala 207, 208simpsoni 207

Alphaxolone/alphadolone 94Aluminium 222, 223Amblyomma

dissimile 205grossum 205sp. 205

American alligator see Alligator mississippiensisAmerican crocodile see Crocodylus rhombiferAmmonia 41, 48, 49, 50, 111, 121, 135, 230Amoebae 192 , 258Amprolium 90, 188Anabolic steroids 102Anaemia 221, 269Anaesthesia 92, 93, 95, 138, 287Anasarca 217Anastomosis 23Anectine® see SuccinylcholineAngiotensin 43Anopheles stephensi 198, 205Anophthalmia 152, 153Anorexia 148, 160, 164, 167, 181, 182, 221, 226, 234,

237, 250, 251, 253, 262, 281, 282, 289, 290Antibiotics 91, 101, 146, 161, 166, 217, 225, 241,

273residues 102, 130resistance 89, 91, 102, 146, 225

Anti-inflammatories 226, 231, 288Antioxidant 100Ants see SolenopsisAponomma exornatum 205Appetite 112, 136

suppression 138, 282seasonal 37, 113, 230

Archaeodiplostomum acetabulatum 201Arsenic 222Arteritis 237, 252, 269, 270Arthrinium sp. 40Arthritis 79, 174, 229, 231, 252, 273, 287–288,

290Artificial insemination 123Ascaridoids 192–194, 229, 252Ascites 148, 167, 221, 234Ascorbic acid see Vitamins, CAspergillus 141, 177

clavatus 40flavus 40, 176flavipes 38fumigatus 176, 178niger 40, 141, 176

ustus 176, 178versicolor 176

Atresiabile duct 155intestine 155

Atrophocaecum acuti 201americanum 201caballeroi 201

Axial deformities 149–151

Bacillusalvei 39cereus 39circulans 39coagulans 39lentus 130sp. 37, 38, 174

Bacterial resistance see Antibiotics, resistanceBacterial translocation 228–229Bacteriology sampling 82, 84, 86Bacteroides

asaccharolyticus 37bivius 37denticola 37loeschei 37oralis 37sordellii 37thetaiotamicron 37vulgatus 37

Banding see EggBarbiturates 92, 93Basking 44Basophils 25Baycox® see ToltrazurilBaytril® see EnrofloxacinBeauveria 40

bassiana 176, 178, 182Behaviour 52–56, 245

disturbed 95, 230, 254, 281, 283, 289–290requirements 137

Beryllium 222Bilirubin 48Bile 161

fistula 96medicinal use 132

Biochemistry 47–52blood 47–49fat 49–51minerals 49–50skin glands 52urine 48–49

Biodiversity 182, 192Biopsy 67Biosecurity 117–118Biotin deficiency 100, 221, 237

324 Index

Black caiman see Melanosuchus nigerBlastocystis sp. 192Blepharo-conjunctivitis see ConjunctivitisBlindness 149, 169, 245, 247Bloating 252Blood

biochemistry see Biochemistry bloodcells 24circulation 43enzymes 48, 49film 64–65, 82, 84flow 43, 44parasites 188, 190, 191, 202, 203, 268–269pressure 43sampling 24, 64–65, 82, 84shunt 43volume 24

Bollinger bodies 158, 159Bone

minerals 49rings 34, 85tumours 284

Bornean crocodile see Crocodylus raninusBorrel bodies 158, 159 Botulism 224–225Brachycephaly 152Bradycardia 43Brain 27, 44, 80, 124, 133, 223, 283, 290

malformations 153parasites 268petechiae 267

Breeding 118–123, 136Brevidi E® see SuxathoniumBrevimulticaecum

baylisi 192gibsoni 192pintoi 192stekhoveni 192tenuicolle 192

Broad-snouted caiman see Caiman latirostrisBronchopneumonia 271Brown spot 172, 240Burrowing 44, 55–56Bush meat 130

Cadmium 222, 223Caenorhabditis sp. 198Caesium 224Caiman

crocodilus 4, 18, 19, 22, 25, 28, 37, 39, 52, 68,71, 93, 94, 96, 99, 101, 102, 129, 141,152, 154, 158, 163, 170, 171, 174, 176,177, 182, 183, 184, 190, 192, 193, 196,197, 198, 199, 200, 201, 202, 203, 205,207, 208, 219, 221, 224, 226, 231, 246,252, 266, 267, 270, 284

latirostris 4, 25, 28, 48, 49, 52, 68, 123, 167, 183,190, 192, 201, 203, 207, 284

Caimanicola marajoira 201Calcium 100, 103, 136, 139, 148, 211, 213, 230, 249,

265deficiency 62–63, 102, 148, 267, 272EDTA 223plasma 42, 48, 49, 50, 266urine 50

Calcium-borogluconate 90, 213, 253Calls see VocalizationCampylobacter fetus 38, 174Candida 38, 176

albicans 176, 181guillermondii 40humicola 38krusei 40lipolytica 38parasilosis 176rugosa 38zeylansides 38

Cannibalism 37, 53–54, 74Cap-Chur Barb® see PentobarbitalCapillarioids 194–196Capsulodiplostomum crocodilinum 201Captive bolt gun 76, 124, 125, 138Capture 57–60, 137, 138, 229, 245, 279, 285, 286Carbohydrate 101Carcass yield 128Cardiac hypertrophy 269Cataract 247Cephalosporium sp. 176, 178, 182, 274Cestode 192, 203, 256

larvae 130, 203, 274Chinese alligator see Alligator sinensisChlamydia 74, 117, 130, 157, 167–170, 246, 247, 260,

262psittaci 167

Chlamydiosis see ChlamydiaChloramphenicol 90, 247Chloride 48, 49, 50Cholecystitis 262, 272Cholecystotomy 96Choleliths 262Cholesterol 48, 49, 50, 51, 129Choline 99Chondroma 284Chorioretinitis 247Chromium 99, 222, 223Chromobacterium sp. 174Chromosomes 27, 33Chronic stress dermatitis 173, 237–239, 240, 241,

245, 250, 252, 270Chrysosporium sp. 40Circulation see BloodCitrobacter 37, 38, 39, 141, 174

amalonaticus 38, 39freundii 38, 39, 174

Index 325

Cladosporium sp. 38, 176Claw abnormalities 273Clitoral appendage see ClitorisClitoris 19, 70Clitoropenis see ClitorisCloaca 17, 62, 70, 79, 128, 140, 200, 263, 265

examination 70glands see Skin glandsulceration 221, 259

Cloacitis 259Clostridiosis 172Clostridium 37, 172

bifermentans 37botulinum 224clostridioforme 37limosum 37, 172perfringens 259septicum 172sordellii 37tetani 37

CO2 excretion 41Cobalt 99, 223Coccidia 53, 74, 117, 141, 157, 182, 228Coccidiosis 183–188, 234, 256, 262, 271Colibacillosis 190Coliform bacteria 142Colitis 257–258Common caiman see Caiman crocodilusCompetitive exclusion 38, 145, 227Conjunctivitis 62, 87, 163, 245–247, 266, 270

chlamydial 87, 167–170, 217Contracaecum sp. 198Copper 50, 99, 100, 222, 223

sulphate 173, 177Coracoid 7, 77Corneal perforation 247Coronavirus 163, 257Corpora lutea 18Cortisone 49, 91Corticosteroids 117, 126, 218, 278, 281Corynebacterium 38, 174

pyogenes 174Creatinine 48, 49, 50Crocodilicola

caimanicola 201gavialis 201pseudostoma 201

Crocodilocapillaria longiovata 194Crocodylus 1

acutus 1, 28, 41, 72, 95, 171, 183, 193, 195, 196,200, 207, 223, 240, 247, 273, 284

cataphractus 1, 28, 190, 192, 193, 201, 202, 207intermedius 1, 28, 193, 196, 247, 273johnsoni 1, 2, 24, 28, 41, 49, 51, 69, 70, 72, 92,

94, 129, 149, 153, 158, 170, 174, 193,194, 195, 196, 200, 201, 202, 203, 204,205, 207, 208, 231, 241, 249, 268, 274

mindorensis 1moreletii 1, 28, 48, 71, 102, 151, 195, 196, 205,

221, 254niloticus 1, 18, 28, 35, 39, 40, 41, 44, 48, 49, 51,

61, 68, 72, 73, 74, 91, 92, 93, 94, 98, 99,102, 117, 119, 120, 134, 141, 151, 152,154, 158, 160, 162, 163, 167, 170, 173,174, 176, 177, 178, 179, 181, 182, 183,184, 188, 190, 192, 193, 196, 197, 198,200, 201, 202, 204, 207, 217, 218, 219,221, 222, 225, 231, 234, 235, 238, 241,243, 246, 247, 248, 249, 250, 251, 252,254, 256, 257, 258, 259, 262, 264, 265,266, 268, 269, 270, 271, 272, 274, 282,284, 288

novaeguineae 1, 28, 52, 152, 174, 184, 190, 193,194, 195, 196, 198, 202, 203, 207, 208,231, 265, 268

palustris 1, 19, 28, 72, 92, 95, 174, 184, 190,193, 196, 201, 207, 249, 253, 266, 271,283

porosus 1, 24, 28, 34, 40, 41, 45, 48, 51, 67, 69,70, 72, 98, 99, 129, 141, 149, 152, 158,170, 174, 176, 177, 181, 182, 184, 190,192, 193, 194, 195, 196, 197, 198, 200,201, 202, 203, 204, 207, 217, 224, 231,234, 244, 246, 265, 267, 268, 274, 284,288

raninus 1rhombifer 1, 24, 28, 52, 68, 193, 199, 200, 201,

202, 203, 219, 220, 223siamensis 1, 28, 167, 201, 202, 207, 284

Cross-breeding 43, 134, 136Cryptococcus

lipolytica 40luteolus 40

Cryptosporidia 188Cuban crocodile see Crocodylus rhombiferCulex dolosus 205Curvularia 38, 40, 177

lunata 176Cuvier’s dwarf caiman see Palaeosuchus

palpebrosusCyatocotyle

brasiliensis 201crocodili 201fraternae 201

Cyclopia 153Cysts 266, 275, 284Cystodiplostomum hollyi 201

Danofloxacin 90Darting 71Dectomax see DoramectinDehydration 95, 230, 233, 234, 235, 251, 264, 281,

283, 287, 290

326 Index

Dental anomalies 152, 247–249, 273mineralization 249, 273

Dermacoccus nishinomyaensis 39Dermatitis 170, 177, 237–239, 240

fungal 177–178, 240–241Dermatophilosis see DermatophilusDermatophilus sp. 172–173, 236, 240, 244Deuritrema 202

gingae 202, 265Diarrhoea 164, 228Diazepam 71, 72Digenetic trematodes see TrematodesDigestion 36–37, 101Diphtheroides sp. 38Diplostome 201Disease 46Disinfection 105, 107, 113–114, 118, 124, 126, 141,

143, 145, 146, 158, 166, 170, 173, 177, 186,226, 228, 237, 241, 242, 244, 245, 247, 250

Dislocation 137Dispersal of juveniles 53Distoma pyxidatum 201Diving 40DNA 1, 121Doramectin 90, 209Dosing 87Double scaling 241, 245Drechsleria sp. 38Drinking 42Drowning 70, 71, 111, 212, 290–291Dujardinascaris

angusae 193antipini 193blairi 193chabaudi 193dujardini 193, 194gedoelsti 193, 194harrisae 193helicina 193longispicula 193madagascarensis 193mawsonae 193paulista 193petterae 193philippinensis 193puylaerti 193salomonis 193tasmani 193taylorae 193waltonae 193westonae 193woodlandi 193

Duodenal loop 16, 79malformation 155

Duodenum 16, 37, 79

Ear 28, 204Eastern equine encephalitis virus 163Echinostoma jacaretinga 201Ectopia cordis 155Ectopic eggs 265–266Ectromelia 151Edwardsiella 37, 174

tarda 38, 174Egg 30–32, 93, 103, 139–142, 221, 223

albumen 32, 141composition 52

banding 31, 101, 103, 121, 139, 140cleaning 105collection 60, 103–104, 118, 121, 137, 139,

140examination 86infertility 86, 140laying 42, 265metals 222, 223shell 31, 103, 141, 223

cracking 106, 139, 141defects 102, 139, 149porosity 139

size 33, 34, 42yolk 31

composition 51–52EKG 64Eimeria 183, 184

alligatori 183, 184caimani 183, 184crocodyli 183, 184hatcheri 183, 184kermoganti 183, 184paraguayensis 183pintoi 183, 184

Electrocardiogram see EKGEmbryo 32, 42, 86, 103, 139, 222Embryonic

death 139, 140learning 53

Emphysemainterdigital 273, 288lung 178, 262, 272

Encephalitis 163, 246, 256, 266–267, 270, 290Encephalomalacia 267Endocarditis 269Endocrine disruption 223–244, 266Endometritis 265Energy 98–99, 101, 129Enrofloxacin 90Entamoeba sp. see AmoebaeEnteritis 82, 87, 145–146, 148, 164, 172, 190,

226–228, 255–258, 266Enterobacter

agglomerans 38, 39, 130, 174cloacae 38, 39, 141gergoviae 39

Index 327

Enterococcus 37caecorum 39durans 39faecalis 39faecium 39pseudoavium 39solitarius 39

Eosinophils 25, 67, 204Epicarditis see PericarditisEpicoccum sp. 38Erysipelothrix insidiosa 171, 240Erythrocytes 24, 189, 190ESB3® see SulphachloropyrazineEscaping 109, 111Escherichia 37

coli 38, 39, 174, 227, 256hermani 38

Etorphine 71, 73, 94Eustachian tubes 11–12, 77Eustrongylides sp. 198Evisceration 124, 128Excretion see UrineExophthalmia 153Exotidendrium 202, 265

gharialii 201Exudation see FibrinEye 28, 62, 76, 173, 245–247

defects 153Eyelids 28, 62, 76, 204, 237, 245, 247

F10® see DisinfectionFaeces sampling 66False gharial see Tomistoma schlegeliiFalse nostrils 13, 153, 249Fat 99, 100, 101, 113, 129, 131, 146, 178, 222, 225,

228, 230, 243, 245, 250, 259composition 49–51digestion 37medicinal use 131necrosis see Steatitis

somatic 29, 245Fat body 28–29, 79, 144, 155, 170, 234Fat body:heart ratio 86, 245Fatty acids 49–52, 99, 100Fear 114, 227, 234, 241, 245, 280, 282, 290Feed

efficiency 101selection 53

Feeding 113, 121, 138Fenbendazole 90, 194Fever 46Fibrin 46, 88, 143, 144, 145, 161, 164, 167, 169, 186,

187, 188, 228, 245, 246, 247, 252, 256, 258,262, 263, 265, 269, 271, 285, 287, 288

Fibriscess 46, 143, 164, 208, 239, 241, 242, 254, 283,285, 287

Fibroma 284Fibrosarcoma 284Fighting 54, 116, 117, 119, 120, 121, 122, 140, 242,

245, 247, 248, 249, 265, 284Filariae 197Fire ants see SolenopsisFlagellates 190–191Flavobacterium

balustinum 39breve 130gleum 38indologenes 130indoltheticum 38multivorum 38odoratum 39

Flaxedil® see GallamineFlies 109, 111, 118, 188, 191, 205, 228Flora

intestinal 32, 38, 118, 129, 141, 148, 163, 164,173, 176, 217, 226, 227, 228

oral 37 skin glands 38

Flukes see TrematodesFolic acid 100Foraging 54Foramen of Panizza 23, 43Force feeding 87, 148, 235, 253–254, 282–283Foreign bodies, gastric see StomachFracture, mandible 95

spinal column 212, 267, 273Frost bite 288–289Frustration 280Fungaemia 182, 281Fungal infection 104, 134, 176–182Fusarium 38, 40, 142, 176, 177, 182

moniliforme 176, 178, 272oxysporum 141solani 141, 176, 178, 179, 182

Fusobacteriumnucleatum 37varium 37

Gall bladder 18, 79, 96Gallamine 71, 72, 73Gambusia affinis 208Gamma irradiation 129Gaping 44, 55Gastralia see Ribs, abdominalGastric cannulation 96Gastric pressure 64Gastrin 15Gastritis 87Gastroenteritis 253–254Gastroliths 15, 36, 95, 254Gastrotomy 94–95, 254

328 Index

Gavialis gangeticus 5, 28, 38, 135, 149, 153, 172, 174,183, 184, 188, 190, 193, 197, 199, 201, 202,207, 220, 231, 265

Gedoelstascaris australiensis 193vandenbrandeni 193

Genetic defects 140, 148, 234, 244Gentamycin 90, 225, 231Geotrichum 176

candidum 40, 176Ghara 11Gharial see Gavialis gangeticusGiardia sp. 190, 191Giemsa’s stain 168Gingivae 63, 76, 176, 179, 182Gingivitis 218, 249–250Glassy teeth 63, 148, 212, 249, 273Glaucoma 247Globulin 48, 49Glomerular filtration Glossina palpalis 191, 205Glossitis 250Glottis 12, 13Glucose 48, 49, 91, 99Gnathostoma procyonis 197, 199, 274Goezia

gavialidis 193holmesi 193lacerticola 193

Goitre 276Gonads 18–19, 79

cysts 266Goussia sp. 183, 184, 186, 187Gout 41, 79, 217, 224, 225, 226, 230–233, 264, 273,

283congenital 155, 231

Granuloma 95, 170, 176, 178, 179, 182, 203, 229,241, 242, 244, 250, 254, 260, 262, 264, 268,271, 283

Greasy skin 178, 243–244, 250Griphobilharzia amoena 202, 265, 268, 271Growth 33–34, 45, 105, 112, 117, 147, 158, 203, 211,

234hormone 102promoter 101, 102

Gular gland see Skin glandsGular valve 11, 55, 63, 76, 77, 87, 250–251,

270Gynecophoric chamber 269

Haematology 67–69, 234Haementeria lutzi 203Haemogregarines see HepatozoonHaffnia alvei 38Halophilic bacteria 128Halothane 92, 95

Handling 116, 137, 138, 147, 163, 227, 247, 282Harmotrema

nicollii 201rudolphii 201

Hartwichia rousseloti 193Hatching 103, 107Hearing 44Heart 77, 82, 86, 284

anatomy 22ectopic 155rate 43, 87septal defect 270stroke volume 43surgery 96–97

Heating 104–105, 109–111Heavy metals 130, 221–223Helobdella sp. 203Hepatitis 161, 167, 175, 229, 259–261Hepatozoon 188–190, 204, 262, 269

brasiliensis 190caimani 190, 205crocodilinorum 190hankini 190pettiti 190, 205sheppardi 190

Hernia, diaphragmatic 144Herpetodiplostomum caimanicola 201Heterophils 25, 67, 274Hibernation 177, 281Hide boards 109, 115, 227, 242, 290High walk see WalkingHirudinaria manillensis 203, 204Histopathology sampling 83, 84Hookworm 197, 199–200Humane killing 76, 124, 138Humidity 105, 106Hunting see ForagingHybridization see Cross breedingHydrocephalus 153Hydropericardium 148, 167, 221Hydrophobia 281, 283, 290Hydroxidione 94Hyperglycaemia 91Hyperkeratosis 233, 250Hyperparathyroidism see ParathyroidosisHyperthermia 93Hypervitaminosis D 225, 265 Hypocalcaemia 212, 215, 225Hypoglycaemia 47, 91, 138, 148, 282Hypoproteinaemia 148, 221Hypothermia 44, 92, 96, 97

Icing 44, 56Identification 61, 74–75Ileum 17, 37

ulcers 267

Index 329

Immobilization 70, 92, 138, 166, 215, 265, 282, 283,286, 290

Immunoglobulin 45 Immunity 45–46, 74, 126, 136, 145, 157, 164, 175,

176, 183, 207, 219, 226, 227, 229, 234, 236,240, 252, 271, 281, 282

Imprinting 53Inclusion bodies 157, 158, 159, 161, 240, 259, 272Incubation 102–107, 136, 140, 148, 149, 234

period 43room 104temperature see Temperature, incubation

Indo-Pacific crocodile see Crocodylus porosusInfertility 121Inflammation 46, 283Influenza C virus 163Injection 87–89Injury 46, 76, 117, 138, 140, 149, 153, 241–242, 246,

247, 250, 258, 265, 269, 273, 284–287Inositol 100Insulin 47, 91Intestine 93, 200

anatomy 16–17flora see Flora mycosis 179occlusion 146, 164, 234, 256, 258, 284

Iodine 99, 100, 171Iron 48, 50, 99, 100, 222Islets of Langerhans 22Isosospora 183

jacarei 183, 184wilkei 183, 184

Ivermectin 89, 209, 225

Jaw malformations 153Jejunum 16, 37Johnston’s crocodile see Crocodylus johnsoniJumping 36

Kanamycin 90Keratoconjunctivitis 246Ketaconazole 90, 241, 242, 282Ketamine 71, 92, 93, 95Kidney 18, 79, 199, 202, 203, 217, 221, 223, 229, 230,

231, 263–265, 283aplasia 155, 231, 264hyaline degeneration 225, 264–265parasites 265

Kidney:heart ratio 86Klebsiella 174

oxytoca 38, 39, 174pneumoniae 38

Kocuria varians 39Kurthia gibsonii 39Kyphoscoliosis see Scoliosis

Labyrinth see EarLactate 49Lactobacillus sp. 39Laparoscopy 92–94Laparotomy 94Larynx 77, 96Laurobolin see Anabolic steroidsLead 221–223Leeches 67, 189, 196, 203–205, 241Leg weakness 212, 268, 272, 290Leiperia 205

australiensis 207cincinnalis 207, 268, 271

Leishmania sp. 190–191Lethal injection 76Leucocyte counts 67–69Lidocaine 95Light 111, 112, 148, 282Lignocaine 92Limb duplication 151, 273

missing 273Limnothrissa miodon lake sardine 119, 193Lipids see FatLipoma 284Lithophagy 36, 95, 254, 281, 290Liver 17, 79, 82, 182, 189, 198, 221, 222, 223, 226,

229, 234cirrhosis 254, 261fatty degeneration 226, 261parasites 261–262

Locomotion 35Longevity 34–35Lung 77, 167, 176, 177, 178, 182, 202, 203, 205,

207–208anatomy 12, emphysema 262haemorrhage 208, 272

Lymphhearts 24nodes 24, 46, 82vessels 24

Lymphocytes 24, 25, 45, 57, 190, 229, 259, 266, 274Lymphosarcoma 284

M99® see EtorphineMagnesium 48, 49, 50

sulphate 253Maladaptation 235Malnutrition 136, 148, 226Manganese 99, 222Meat 51, 128, 221, 223, 224, 225, 245, 274

cooking hints 133medicinal use 132

Mebendazol 90Medication 86–91Medicinal uses 131

330 Index

Melanosuchus niger 5, 28, 192, 193, 201, 207Menadione 100Meningitis 167, 246, 267, 290Mercury 221–223 Mesodiplostomum gladiolum 201Mesothelioma 284Metabolic rate 34, 40, 43, 91, 98, 105, 112, 148Metarhizium anisopliae 176, 178Metronidazole 148, 283Microchips 75Micrococcus

kristinae 130luteus 39, 130nishinomiyaensis 130roseus 130sedentarius 130

Microfilariae 198, 269Micromelia 151Microphthalmia 153Micropleura

vazii 197vivpara 197

Minerals 99, 136premix 99–100, 121, 241, 245trace 99

Mirex® 223Mites 205Molybdenum 222, 223Monocytes 26, 190Monogenetic trematodes 200, 209–210Monophthalmia 152Monorhiny 153Moraxella sp. 38, 130Morelet’s crocodile see Crocodylus moreletiiMorganella 37

morgani 38, 174Morphometry 85, 269, 270Mosquitos 159, 188, 191, 198, 205MS222® see TricaineMucor 177, 178, 181

circinelloides 176, 177, 179, 252Mugger see Crocodylus palustrisMulticaecum agile 193Muscle 221, 222, 223, 231

anatomy 10respiratory 12tail 10

calcification 220, 225degeneration 130, 219–220lesions 176, 182ossification 225parasites 197, 199, 274

Mycobacterial abscess 250 Mycobacteriosis 73, 130, 170–171, 182, 244, 250,

262Mycobacterium

avium 74, 170

bovis 130, 170fortuitum 170marinum 170 terrae 170triviale 170tuberculosis 130, 170ulcerans 170

Mycoplasma 74, 117alligatoris 167, 267, 269crocodyli 91, 167

Mycoplasmosis 167, 246, 247, 271, 273, 287Mycotoxins 226, 261, 267Myocarditis 167, 175, 229, 269Myositis 274, 290Myxobolus sp. 210

Nandrolone see Anabolic steroidsNavel 33

infection see OmphalitisNecrosis 46, 158, 168, 277Nematodes 192–200Neodiplostomum 201

crocodilorum 201gavialis 201

Neoparadiplostomum kafuensis 201magnitesticulatum 201

Neoplasms 283–284Neostigmine 71Neostrigea

africana 201leiperi 201

Nephritis 230interstitial 271

Nephrocephalus sessilis 201Nesting 42, 54, 102, 119

substrates 102 Newcastle disease 162–163New Guinea crocodile see Crocodylus novaeguineaeNiacin 100Nickel 222, 223Nictitating membrane 28, 153, 169, 245, 247Nile crocodile see Crocodylus niloticusNutrition 98–102, 230, 234, 241

state of 60–62, 86Nutritional bone disease 63, 211–216, 249, 268, 272

Odneriotrema incommodum 200, 203microcephala 200

Oedema 46, 167, 172, 175, 217, 221, 229, 244Oesophagus 14, 78, 87, 95, 200

stenosis 155Oistosomum caduceus 201Olfaction 44

Index 331

Omphalitis 142, 143Oophoritis 265Opacification

cornea 2473rd eyelid 247

Ophthalmia 246, 247Opisthotonus see Star gazingOrchitis 266Organ minerals 49, 222Orinoco crocodile see Crocodylus intermediusOrtleppascaris

alata 193antipini 193nigra 193

Osmoregulation 42Osteoderms 9, 44, 71Osteodystrophy 211, 273Osteolaemus tetraspis 3, 16, 18, 28, 35, 36, 38, 39–40,

52, 56, 82, 89, 98, 130, 174, 176, 187, 190,193, 195, 198, 199, 202, 203, 207, 208, 247,252, 254, 255, 259, 261, 263, 269, 274, 275,276, 277

Osteomalacia 136, 148, 211, 249, 268, 272–273, 275,290, 291

Osteoporosis 136, 211, 212, 249, 273, 275Oswaldofilaria

bacillaris 197, 198, 205kanbaya 197medemi 198versterae 197, 198

Ovary 18, 94, 266haemorrhage 266

Overcrowding 137, 147, 163, 227, 234, 236, 237,239, 245, 280

Overfeeding 245Overheating 44–45, 108, 111, 112, 134, 137, 147,

164, 227, 245, 280, 282, 289Overstocking see OvercrowdingOviduct 19, 79, 94, 140, 153, 265

rupture 120Ovulation 42, 123, 140, 141, 153, 265Oxfendazol 90, 194Oxygen consumption 40, 103, 105Oxytetracyclin see Tetracycline

Pachypsolus constrictus 201sclerops 201

Paecilomyces 40, 177aviotti 141farinosus 177, 178lilacinus 141

Pain 92, 138, 290Palaeosuchus

palpebrosus 5, 28, 52, 71trigonatus 5, 28, 52, 71, 198

Pancreas 16, 17, 18, 22, 79, 234, 259Pancreatic involution 259Pancreatitis 259Panophthalmitis 247Pansteatitis see SteatitisPantothenic acid 100Papilloma 283Paradiplostomum abbreviatum 201Paralysis 172, 212, 218, 219, 224, 225, 231, 267, 268,

273Paramyxovirus 162–163, 228, 246, 266Parasitaemia 189Parasites

gastric 79sampling 82, 85

Parathyroids 22, 77, 211, 212, 275cysts 212

Parathyroidosis 211, 275Paratrichosoma 195–196, 241

crocodylus 195recurvum 195

Parental care 53Pasteurella 38

haemolytica 38multocida 174

Pectoral girdle 7Pellets 101, 118, 194, 227Pelvic girdle 8, 77Penicillin 90, 91, 171Penicillium 38, 40, 177

felucanum 141lilacinum 177, 178oxalicum 177

Penis 19, 21, 66, 70, 132, 266Pentobarbital 71, 73, 93, 95, 96Pentamethylene tetrazol 93Pentastomes 117, 205–209, 271, 272

sampling 85, 271Peptococcus

magnus 37prevotii 37

Pericarditis 97, 175, 229, 269Periocular abscess 247Peritonitis 120, 140, 144, 254, 265, 284Pesticides 223–224Pharmacokinetics 91Pharyngitis 270–271Phenylbutazone 226, 231Phenylcyclidine 71, 72, 73, 92, 94Philippine crocodile see Crocodylus mindorensisPhilobdella gracilis 203Phoma sp. 40Phosphorus 100, 136, 148, 211, 272

blood/serum 48, 49urine 50

Phthisis bulbi 247Physical restraint 57–60

332 Index

Pigmentation 9Piling 114–115, 242, 245, 290Piperazine 90, 194Pithing 125, 138Pituitary 21Placobdella

multilineata 67, 204, 205papillifera 204

Placobdelloides multistriatus 204Plagiorchid flukes 202Planococcus sp. 174Plasma minerals 49, 50Plasmodium sp. 188Plerocercoids see Cestode larvaePneumonia 167, 175, 271

foreign body 272fungal 271, 272

Pole syringe 70, 89Polyacanthorhynchus rhopalorhynchus 199Polyarteritis see ArteritisPolyarthritis 164, 167, 172, 175, 287Polychlorinated hydrocarbons 130, 223,

266Polycotyle ornata 201Polydactyly 151, 273Polymerase chain reaction (PCR) 170Polymorphus mutabilis 199Polyp 95Polyserositis 167, 175, 229Poor dental mineralization see Glassy teethPotassium 48, 49, 50Pox

lesions 76, 158, 159virus 157, 288

caiman 74, 117, 157–158, 240, 250crocodile 74, 90, 117, 158–159, 236, 240, 242,

246, 250Pre-release screening 73–74Probenecid 226, 231Probiotics 227Procaine 92, 93Proctocaecum dorsale 201Progarnia 188, 190, 269

archosauriae 190Prolapse of the uterus 215, 265Prolectithidiplostomum

cavum 201constrictum 201

Prostrigea arcuata 201Protein 99, 101, 129, 230

blood/serum 48, 49, 50Proterodiplostomum

breve 201globulare 201longum 201medusae 201tumidilum 201

Proteus 37, 141, 174mirabilis 38, 39rettgeri 253vulgaris 38, 39

Providencia 37rettgeri 39, 174 , 246, 267

Pseudocrocodilicolaamericana 202georgiana 202

Pseudomonas 174, 227acidivorans 130aeruginosa 141, 142, 174cepacia 38fluorescens 38maltophila 38, 130pickettii 38putida 174

Pseudoneodiplostomum 202acetabulata 202bifurcatum 202dollfusi 202siamense 202thomasi 202

Pseudotelorchis caimanis 202yacarei 202

Pseudotumour see FibriscessPus 46, 287Pyelonephritis 203, 231, 263–264Pyloric antrum 14, 79Pyridoxine 100

Radiography 64Radionuclides 224Rana catesbiana 193Rana sphenocephala 193 Rats see RodentsRearing 107–112Rectal examination 70Rectum 17Red blood cells see ErythrocytesRed heat 128Regeneration 249, 286Regurgitation 37, 95, 253, 254Renal portal system 24Renivermis crocodyli 202, 265Reproductive performance 101–102, 221, 224Respiratory rate 40, 41Respiratory tract, anatomy 11Restraint 57–60, 137, 138, 279Retrobulbar abscess 247Rhabditids 198, 261Rhinitis 237, 245, 246, 266, 270Rhinopharyngitis 271Rhodotorula rubra 38Riboflavin 100

Index 333

Ribs 77, 126abdominal 7cervical 7thoracic 7, 8

Rickets 211Rodenticides 219, 224, 269Rodents 109, 111, 118, 188, 197, 228Round cell tumour 283Roundworms 117, 192–200Rubber jaws 63, 148, 212 Running 9, 36Runting 34, 67, 85, 147, 161, 186, 191, 194, 221, 226,

234–236, 269, 281

Saffan see Alphaxolone/alphadoloneSalicylates 226, 231Salmonella

arizona 142, 166choleraesuis 164, 165enteritidis 164, 165serovars 39, 130, 164, 165–166typhimurium 164, 165, 166

Salmonellae 126, 129, 130, 227, 245, 256Salmonellosis 87, 91, 164, 234Salpingitis 265Salt 41, 90, 204, 205, 253, 283

glands 14, 41–42tolerance 41–42

Scapula 7Schneider’s dwarf caiman see Palaeosuchus trigona-

tusScoline® see SuccinylcholineScoliosis 149, 212Scratches see SkinSebekia

acuminata 207cesarisi 207divestei 207indica 207johnstoni 207jubini 207, 271microhamus 207mississippiensis 207multiannulata 207novaeguineae 207okavangoensis 207oxycephala 208purdiae 207samboni 207trinitatis 207wedli 207

Selenium 50, 99, 100, 219, 220, 222, 274Selfia porosus 207Seminal groove 19, 66, 123Seminoma 283Sensory pits 5, 6

Septicaemia 46, 79, 87, 97, 126, 129, 130, 137, 138,143, 147, 163, 164, 167, 170, 172, 173–175,208, 225, 228–229, 230, 231, 244, 245, 248,250, 252, 259, 260, 262, 263, 265, 266, 267,269, 270, 271, 273, 281, 282, 285, 287, 288

Serine 231Sernylan® see PhenylcyclidineSerratia 37, 174

liquefaciens 174marscescens 38, 174odorifera 38, 39

Serum biochemistry 47–50Sex differentiation 3, 42, 105Sex hormones 122Sexing 70Sexual behaviour 54Shock 91Siamese crocodile see Crocodylus siamensisSiren lacertina 193Skeleton 7Skin 240–245

abrasions 76, 135, 177, 178, 242anatomy 8discolouration 174, 221, 229, 237, 240erosion 221, 237glands 9, 44

dorsal 9gular 9paracloacal 9secreta 52

lesions 176, 177, 195–196, 204, 236, 239 necrosis 244pitting 245puncture 241, 242quality 244–245reflex 92scratches 114, 236, 241, 245, 290ulcers 76, 173, 237, 244wounds 242

Skinning 124, 126–128Skull deformities 149, 152–153Slaughter 123–133, 138, 245Sliding 36, 135, 242Snake tongs 59–60, 116, 137Social interactions 54Sodium 48, 49, 50Solenopsis 223, 246

invicta 224Somatostatin 15Sparganosis see Cestode larvaeSpectacled caiman see Caiman crocodilusSperm 140

collection 66, 123Spina bifida 151Spinal cord 27, 80–82, 89, 124, 125, 133, 138, 212

compression 89Spirometra erinacei 203

334 Index

Spleen 24, 45, 79, 182, 183Spleen:heart ratio 86, 87, 270Splenomegaly 45, 79, 175, 229, 270Squamous metaplasia 217, 233, 264 Staphylococcus 37, 38, 174

aureus 129, 174capitis 130chromogenes 39epidermidis 39, 130hominis 130saprophyticus 130xylosus 39

Star gazing 268, 289Starch 99Steatitis 100, 208, 219, 244, 259, 257Steatotheca see Fat bodySteatothecitis 262–263Stephanoprora

jacaretinga 202ornata 202

Sterility 120Sternum 7, 287Stocking density 33, 54, 113, 116–117, 134, 137, 235,

280, 284Stomach 79, 87, 231

anatomy 14–16contents 36, 79, 98

collection 66–67contractions 101foreign bodies 79, 95, 254–255, 263mycosis 179pH 36secretions 36ulcers 79, 176, 194, 229, 237, 251–252, 269

Stomatitis 249–250Streptococcus 37, 174

equisimilis 130faecium 130salivarius 39

Streptomyces sp. 39Streptomycin 224, 225, 231Stress 33, 34, 37, 44, 47, 52–53, 54, 57, 67, 70, 74, 92,

95, 97, 101, 108, 109, 112, 115, 117, 121, 122,125–126, 130, 134, 136, 137, 138, 140, 145,147, 148, 157, 158, 159, 161, 163, 164, 166,167, 170, 171, 172, 173, 175, 176, 177, 178,181, 182, 190, 208, 209, 218, 225, 226, 227,228, 229, 230, 234, 235, 236, 240, 244, 245,248, 251, 259, 265, 269, 270, 271, 275,276–277, 278–282, 283, 287, 288, 289, 290

pre-slaughter 123, 125, 129, 245Stressor 137, 164, 166Strontium 222, 223Stunning gun see Captive bolt gunStyrofoam 104, 109, 126Substance depletion 281

Subtriquetra 205, 271megacephala 207rileyi 207shipleyi 207subtriquetra 207

Succinylcholine 70, 71, 72, 73Sucostrin® see SuccinlylcholineSuffocation 114Sulphachloropyrazine 90, 188Superstition 131Supertemporal fossae 7, 62, 76, 125Surgery 91, 92–97, 287, 288Suxathonium 72, 73Swimming 35, 135, 219, 268Syncephalastrum sp. 177Syndactyly 151

Tagging 74–75Tail deformities 149–151Taillessness 149–151, 265, 291Tapeworm see CestodesTaurine 102Teeth 13, 62, 63, 76, 204, 212, 241, 247–249, 273Temperature

body 34, 36, 40, 41, 43, 44–45, 56, 88, 101, 105,112, 130, 134, 137, 227, 230, 281, 288,289

tolerated minimum 44environmental 33, 35–36, 44, 91, 99, 101, 108,

109, 134, 148, 173, 174, 177, 178, 182,226, 227, 228, 229, 231, 233, 234, 235,236, 237, 240, 241, 244, 289

fluctuations 106, 109, 120, 121, 142, 148, 161,163, 164, 166, 227, 232, 234, 241, 244,280, 282

incubation 33, 42, 43, 45, 54, 104, 105–106,149, 151, 153, 154

rearing 109–110, 111–112Terranova

crocodili 193lanceolata 193

Territoriality 54, 284Testis 19Tetany 290Tetracycline 34, 90, 101, 102, 147, 167, 169, 173,

247, 254Thallium 222Thermogradient 44, 55, 109, 112, 120, 134, 135, 136,

234, 289Thermoregulation 43, 44–45, 55–56, 120, 134, 137,

173, 231, 280, 289Thiabendazol 90Thiaminase 217Thiamin 100

deficiency 217–218, 268, 269, 289Thiopental 92, 93

Index 335

Third eye lid see Nictitating membraneThrombocytes 24, 190Thymus 21–22, 24, 45, 77, 274–275

cyst 275necrosis 274–275

Thyroid 22, 77, 275–276cysts 275, 284

Thyroxine 47, 49, 102Tibial puncture 89Ticks 205Tiletamine see Zoletil®

Timoniella absita 202Tin 222Toltrazuril 90, 188Tomistoma schlegelii 3, 9, 28, 48, 223, 231,

273Tongue 13, 63, 76, 77, 179, 182, 217Tonsils 11, 12, 24, 251, 270Tooth replacement 13, 247Toothlessness 247Torsio intestinalis 258, 259Torticollis 254Torulopsis sp. 38Toxaemia 143Transovarial infection 140, 141, 160, 188Transport 121, 126, 137–138, 175, 177, 229, 230,

252, 279, 281, 282, 283Trauma see InjuryTrematodes 117, 192, 200–203, 264Triatoma infestans 205Tricaine 71, 72, 73, 92, 94Trichinella 197, 274

spiralis 197Trichinellosis 130, 196Trichoderma sp. 38, 40, 177Trichomonas 190

prowazeki 190Trichophyton sp. 177Trichosporon 177, 179, 182

beigelii 38, 40capitatum 40cutaneum 177

Triglyceride 48Trispiculascaris

asymmetrica 193trispiculascaris 193

Trypanosoma 191–192, 269cecili 192grayi 191, 192, 205

Trypanosomes see TrypanosomaTuberculosis see MycobacteriosisTubocurarine 93Twins 151, 153–154Tympanic membrane see EarTyphlophorus

lamellaris 193spratti 193

Ultrasonography 64Urea 41, 48, 49Uric acid 41, 48, 49, 50, 225, 230Urine 41, 121, 135

biochemistry 48–49collection 65pH 50retention 212

Uterus 19, 42, 70, 265Uveitis 247

Vaccine 90, 157, 159, 161, 166, 167Valium® see DiazepamVanadium 222Vasoconstriction 43Vermiculite 104, 106–107, 141Viadril® see HydroxidioneVinegar 254Virginiamycin 101, 102, 147Virus

isolation 83, 157particles 83, 157, 158, 159, 160, 162, 163

Vitamins 101, 121, 136, 149A 100, 216–217, 230, 231, 233, 264B 100, 217–218, 226, 254, 261C 100, 147, 170, 218–219, 229, 250, 281,

282D 100, 211, 225, 265E 50, 100, 121, 218, 219–221, 274K 100, 266, 269premix 99–100, 241, 245

Vitello-intestinal duct 32, 142, 143Vocalization 56

Walking 9, 36, 135, 242Warfarin see RodenticidesWarts 283White claws 9, 273, 274 White muscle disease 219–220, 274, 288, 290 White nose 229, 237–239, 241Winter sores 173, 236–237, 240, 241, 244

Xylazine 71Xylocaine 92

Yawning 55Yersinia enterocolitica 38Yolk-sac

anatomy 32–33, 142excision 96, 144hydropic 144infection 142, 148, 234resorption 32, 142, 148, 234

336 Index

retention 142, 143–145, 257rupture 143

Zenker’s degeneration see White muscle diseaseZiehl–Neelsen stain 170Zilka 125Zinc 99, 121, 281

bacitracin 100, 102deficiency 221plasma 50, 223sulphate 173

Zolazepam see Zoletil®

Zoletil® 72, 73

Index 337

crocodiles - biology, husbandry and diseases

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