Rev. sci. tech. Off. int. Epiz., 1994 ,13 (4), 985-1017

Ectoparasites and classification CE. HOPLA *, L.A. DURDEN ** and J.E. KEIRANS **

Summary: The authors present an introductory overview of the principal groups of ectoparasites (flukes, leeches, crustaceans, insects, arachnids, lampreys and vampire bats) associated with domestic animals. Currently-accepted higher-level classifications are outlined for these parasites. Almost all significant ectoparasites of domestic animals are invertebrates, the majority being arthropods (crustaceans, insects and arachnids). Some of these ectoparasites are of particular importance as vectors of pathogens. Many ectoparasite species are host-specific, and vector species typically transmit characteristic pathogens.

K E Y W O R D S : Classification - Domes t ic animals - Ectoparas i tes - Pa thogen transmission - Vector-borne diseases.

INTRODUCTION

E c t o p a r a s i t e s a r e o r g a n i s m s w h i c h i n h a b i t t h e s k i n o r o u t g r o w t h s of t h e sk in of a n o t h e r o r g a n i s m ( t h e h o s t ) for va r i ous p e r i o d s , a n d m a y b e d e t r i m e n t a l t o t h e la t te r . Var ious e c t o p a r a s i t e s cause signif icant in fes ta t ions in m a n y k i n d s of d o m e s t i c a n i m a l s including l ivestock, pe t s , l a b o r a t o r y an imals , poul t ry , fish a n d b e e s ( 2 8 , 3 9 , 5 5 ) . M a n y of t h e s e e c t o p a r a s i t e s ( e .g . m o s t l i ce ) a r e h o s t spec i f i c , w h i l e o t h e r s ( e .g . m a n y t i c k s ) p a r a s i t i z e a w i d e r r a n g e of h o s t s . S e v e r a l e c t o p a r a s i t e s c u r r e n t l y a s s o c i a t e d w i t h domes t i c an ima l s h a v e b e e n a c q u i r e d by the i n t r o d u c t i o n of e i the r hos t or pa r a s i t e in to n e w reg ions , as an ima l s h a v e b e c o m e d o m e s t i c a t e d t h r o u g h o u t t he wor ld . F o r e x a m p l e , cat t le , goa t s , a n d o t h e r i m p o r t a n t d o m e s t i c l ivestock species h a v e b e e n i n t r o d u c e d in to m u c h of A f r i c a , w h e r e t h e y m a y n o w fall v i c t i m to t h e r a v a g e s of n a t i v e t s e t s e flies (Glossina spp. ) a n d t icks, as wel l as p a t h o g e n s t r a n s m i t t e d by t h e s e pa ras i t e s . Re la t ive ly r a p i d i n t e r c o n t i n e n t a l t r a n s p o r t a t i o n of t h e s e a n i m a l s h a s c o m p o u n d e d t h e p r o b l e m . T h e vas t m a j o r i t y of e c t o p a r a s i t e s a r e i n v e r t e b r a t e s . M o s t i n v e r t e b r a t e e c t o p a r a s i t e s a r e a r t h r o p o d s ; insec t s a n d a r a c h n i d s typical ly pa ra s i t i z e t e r r e s t r i a l d o m e s t i c an ima l s , whi le c rus t aceans a r e assoc ia ted wi th fish.

M a n y e c t o p a r a s i t e s a r e k n o w n t o b e v e c t o r s of p a t h o g e n s , w h i c h t h e p a r a s i t e s t y p i c a l l y t r a n s m i t t o h o s t s w h i l e f e e d i n g o r ( o c c a s i o n a l l y ) d e f a e c a t i n g . H o w e v e r , ec topa ras i t e s - especial ly in la rge aggrega t ions - m a y also deb i l i t a te d o m e s t i c an ima l s in o t h e r ways , by caus ing t h e fol lowing d i so rde rs ( 3 9 , 6 5 , 6 6 , 8 8 ) :

- a n a e m i a

- d e t r i m e n t a l i m m u n e r eac t i ons (hypersensi t ivi ty , anaphy lax i s , etc.)

* Emeritus, Department of Zoology, The University of Oklahoma, 730 Van Vleet Oval, Room 314, Norman, Oklahoma 73019-0235, United States of America.

** Institute of Arthropodology and Parasitology, Georgia Southern University, Landrum, Box 8056, Statesboro, Georgia 30460-8056, United States of America.

986

- i rr i tabil i ty

- de rma t i t i s

- sk in necros i s

- low weigh t gains (par t icu lar ly i m p o r t a n t in l ives tock)

- s e c o n d a r y infect ion

- focal h a e m o r r h a g e s

- b l o c k a g e of orifices (ears , etc.)

- i nocu la t ion of toxins

- exsangu ina t ion (occas ional ly) .

S u b d e r m a l l y - l o c a t e d paras i t i c la rva l s tages of ce r t a in flies cause a cond i t i on t e r m e d 'myiasis ' , which m a y lead to significant tissue d a m a g e and secondary infection (11, 50, 100). Never the le s s , ec toparas i t e infestat ions of m a n y domes t i c an imals a r e m i n o r a n d s e e m to cause litt le h a r m to t he host .

T h i s i n t r o d u c t o r y c h a p t e r will br ief ly o u t l i n e t h e m a i n cha rac t e r i s t i c s , h igher - l eve l c l a s s i f i c a t i o n a n d e c o n o m i c i m p o r t a n c e of t h e p r i n c i p a l m e t a z o a n e c t o p a r a s i t e s a f fec t ing d o m e s t i c a n i m a l s . L e s s c o v e r a g e is g i v e n t o e c t o p a r a s i t e s a s s o c i a t e d w i t h l a b o r a t o r y a n i m a l s , a n d for f u r t h e r d e t a i l s o n th i s s u b j ec t , r e a d e r s a r e r e f e r r e d t o a p r e v i o u s r ev iew (28) . H o w e v e r , m o r e i n f o r m a t i o n is p r o v i d e d on e c t o p a r a s i t e s of b e e s a n d fish, as t he se a reas a r e no t dea l t wi th e l s ewhere in this v o l u m e , a n d also o n t hose of b i r d s , n o t ful ly c o v e r e d e l s e w h e r e . T h i s c h a p t e r a t t e m p t s t o fo l low a n a t u r a l ( p h y l o g e n e t i c ) c l a s s i f i ca t ion for t h e e c t o p a r a s i t e s d i s c u s s e d . T a b l e I is a t a x o n o m i c c o m p i l a t i o n of t h e p r i n c i p a l e c t o p a r a s i t e s of v a r i o u s d o m e s t i c a n i m a l s a n d t h e m a i n p a t h o g e n s t r a n s m i t t e d by t h e s e p a r a s i t e s . B o t h in T a b l e I a n d t h r o u g h o u t t h i s b r i e f overview, t h e va r ious t axa of e c t o p a r a s i t e s a r e c o n s i d e r e d o n an e v o l u t i o n a r y scale by sequent ia l ly address ing f lukes, l eeches , a r t h r o p o d s a n d finally v e r t e b r a t e s .

FLUKES AND LEECHES

S o m e species of flukes (P la tyhe lmin thes : T r e m a t o d a ) , such as Gyrodactylus spp. , a r e e c t o p a r a s i t e s of fish a n d c a n c a u s e s e r i o u s d a m a g e t o c u l t u r e d s p e c i e s ( 3 , 3 8 , 4 2 ) . H o w e v e r , m o s t flukes which paras i t ize fish a r e endoparas i t i c .

A l t h o u g h m a n y l e e c h e s ( A n n e l i d a : H i r u d i n e a ) a r e f r ee - l iv ing , c e r t a i n s p e c i e s p a r a s i t i z e fish a n d s o m e t i m e s a l so d o m e s t i c a n d l a b o r a t o r y a n i m a l s ( c r o c o d i l i a n s , m a c a q u e s , etc.) . S o m e leeches can t ransmi t haemof lage l la te or s p o r o z o a n p r o t o z o a n s to v e r t e b r a t e h o s t s d u r i n g b l o o d - f e e d i n g (97) . T h e fish l e e c h (Piscicola geometria) c a n t ransmi t spr ing v i raemia ca rp virus ( S V C V ) to carp (2); a n o t h e r fish p a t h o g e n , infectious h a e m a t o p o i e t i c necros is ( I H N ) virus, has also b e e n isola ted f rom this leech (63).

CRUSTACEANS

A w i d e v a r i e t y of c r u s t a c e a n s f e a t u r e p r o m i n e n t l y as fish e c t o p a r a s i t e s a n d s o m e s p e c i e s a d v e r s e l y a f fec t d o m e s t i c fish s t o c k s . F i s h c u l t u r e ( f a r m i n g ) is a b r a n c h of an ima l h u s b a n d r y which da tes back h u n d r e d s of years in A s i a a n d E u r o p e . F ish fa rming

987

prac t ices h a v e b e e n ref ined a n d p r o d u c t i o n h a s inc reased ove r t ime . Since t h e 1950s, an explos ive g r o w t h h a s b e e n w i t n e s s e d in t h e fish c u l t u r e indus t ry . His tor ica l ly , cypr in id fish species of A s i a n origin (e.g. va r ious species of ca rp , t e n c h a n d pe l eds ) w e r e a d a p t e d to fish fa rming prac t ices . Later , w a r m w a t e r species (e.g. catfish: Ictalurus) w e r e a d a p t e d t o fish f a r m i n g in t h e s o u t h e r n U n i t e d S t a t e s of A m e r i c a ( U S A ) , t h e n c e b e i n g i n t r o d u c e d t o d e v e l o p i n g c o u n t r i e s in A f r i c a , a n d t h u s b e c a m e a r e l i a b l e s o u r c e of p r o t e i n in t h e h u m a n d i e t in t h e s e r e g i o n s . F i s h f a r m i n g is c u r r e n t l y p r a c t i s e d o n all c o n t i n e n t s e x c e p t A n t a r c t i c a . T h e m o s t r e c e n t d e v e l o p m e n t h a s b e e n t h e e n o r m o u s progress in r e a r i n g a n a d r o m o u s a n d c a t a d r o n o u s fish species us ing ' n e t p e n ' t e chno logy in t e m p e r a t e r e g i o n s of t h e n o r t h e r n h e m i s p h e r e . Fac i l i t i es for s a l t w a t e r fish f a r m i n g have b e e n d e v e l o p e d e v e n in land , ad jacen t to f avourab le coas t l ines . K e n t (46) ind ica ted tha t t he use of n e t p e n p rac t i ces w o u l d i nc rea se s a l m o n p r o d u c t i o n in C a n a d a by 2 5 0 % b e t w e e n 1989 a n d t h e yea r 2000.

E c t o p a r a s i t e s a r e u sua l l y a m i n o r p r o b l e m u n d e r p o n d o r h a t c h e r y c o n d i t i o n s , as t h e y c a n b e e l i m i n a t e d q u i c k l y u s i n g e x t e r n a l l y - a p p l i e d t h e r a p e u t i c a g e n t s . B y con t r a s t , e c t o p a r a s i t e s c a n b e d e v a s t a t i n g in n e t p e n s , w h e r e it is difficult t o a p p l y a n d m a i n t a i n b a t h - a d m i n i s t e r e d d r u g s . E c t o p a r a s i t i c C r u s t a c e a c o n s t i t u t e o n e of t h e m o s t s e v e r e p r o b l e m s fac ing p e n - r e a r e d A t l a n t i c s a l m o n (46) . A s a c o n s e q u e n c e of t h e i r s h a r e d a q u a t i c h a b i t a t , C r u s t a c e a a n d f i sh w e r e t h r o w n i n t o e c o l o g i c a l p r o p i n q u i t y ( 4 1 ) . J u s t as c r u s t a c e a n s d e v e l o p e d a p a r a s i t i c r e l a t i o n s h i p w i t h f ish, a r t h r o p o d s w e r e i n e v i t a b l y a b l e t o d o s o w i t h w a r m - b l o o d e d v e r t e b r a t e s . N e v e r t h e l e s s , p a r a s i t i c c r u s t a c e a n s a r e t h e m o s t p o o r l y u n d e r s t o o d g r o u p of e c t o p a r a s i t e s , e x c e p t by a few spec ia l i s t s ( 4 1 , 42 ) , a n d t h e i r t a x o n o m i c in t r i cac ies a r e b e y o n d t h e s c o p e of th i s p a p e r . T h e r e v i e w p r e s e n t e d b e l o w is i n t e n d e d t o e x a m i n e r e p r e s e n t a t i v e t y p e s of C r u s t a c e a w h i c h a r e p a r a s i t i c o n fish spec i e s e n c o u n t e r e d in fish f a rms , a n d to e x p l o r e t h e effects of th is p a r a s i t i s m o n t h e h o s t s . T h i s is effect ively a s t u d y of c o e v o l u t i o n , w i t h t h e e c t o p a r a s i t e a n d h o s t s e r v i n g as m o d e l s . T h e m o s t r e c e n t b r e a k t h r o u g h in t h e s t u d y of p a r a s i t i c C r u s t a c e a c o n c e r n s k n o w l e d g e of t h e r o l e of t h e c r u s t a c e a n e c t o p a r a s i t e as a v e c t o r a n d / o r p o s s i b l e r e s e r v o i r i n t h e t r a n s m i s s i o n of d i s e a s e o r g a n i s m s to fish.

Life cycles of t h e pa ras i t i c C r u s t a c e a h a v e b e e n r e v i e w e d e l s e w h e r e ( 1 3 , 3 7 , 46, 68) . T h e C r u s t a c e a a r e r e p r e s e n t e d h e r e b y t w o s u b c l a s s e s , C o p e p o d a a n d B r a n c h i u r a , w h i l e a t h i r d s u b c l a s s , M a l a c o s t r a c a , m a y b e of s o m e i m p o r t a n c e . T h e s e d i f f e r e n t g r o u p s of c r u s t a c e a n s h a v e b e e n v a r i o u s l y m o d i f i e d in a d a p t i n g t o t h e i r r e s p e c t i v e h o s t s . I n al l t h e c r u s t a c e a n s p e c i e s i n v o l v e d , t h i s a d a p t a t i o n h a s r e q u i r e d v a r y i n g deg rees of loss of mobi l i ty a n d flexibility, wi th a c o n c o m i t a n t gain in rigidity.

Subclass C o p e p o d a

I n p a r a s i t i c c o p e p o d s , t h e b o d y s e g m e n t s a r e o f t en fused . T h e a b d o m e n h a s f o u r s egmen t s , wh ich a r e usual ly all fused in t he paras i t ic species as a resu l t of a d a p t a t i o n t o t h e h o s t . T h e s e s p e c i e s a r e diff icul t t o r e c o g n i z e as a r t h r o p o d s , l e t a l o n e c o p e p o d s . A p p r o x i m a t e l y 8,000 spec i e s of c o p e p o d s exis t , m o s t of w h i c h a r e f ree- l iv ing . T h e s e spec i e s a r e u sua l l y c lass i f ied in s e v e n o r d e r s . H o w e v e r , m o s t p a r a s i t i c c o p e p o d s a r e f o u n d w i t h i n t h r e e o r d e r s : C y c l o p o i d a , C a l i g o i d a a n d L e r n a e o p o d o i d a . A l l ec toparas i t i c c o p e p o d s a r e k n o w n to feed o n t h e b l o o d a n d t issue fluids of t he hos t . Sites of pa ra s i t e a t t a c h m e n t c o m m o n l y b e c o m e h a e m o r r h a g i c , spongy a n d nec ro t i c .

988

T A B L E I

Principal groups of ectoparasites associated with domestic animals and their role in pathogen transmission *

Ectoparasites Hosts Pathogens transmitted

Invertebrata Platyhelminthes

Trematoda (flukes) Annelida

Hirudinea (leeches)

Arthropoda Crustacea (crustaceans)

Copepoda (copepods) Cyclopoida Caligoida Lernaeopodoida

Branchiura Arguloida

Malacostraca Isopoda

Insecta Anoplura (sucking lice)

Mallophaga (chewing lice)

Hemiptera Cimicidae (bat bugs and bed bugs) Reduviidae

Triatominae (kissing bugs)

Diptera Nematocera

Fish

Fish, livestock (mammals)

Fish Fish Fish

Fish

Fish

Livestock and pets (mammals)

Livestock and pets (mammals and birds)

Poultry

Livestock and pets (mammals)

None

Viruses, protozoa

Secondary bacterial infections Secondary bacterial infections

Viruses (?), bacteria (?)

Viruses, bacteria

Secondary bacterial infections

Viruses, rickettsiae, skin fungi, nematodes Skin fungi, cestodes**,

nematodes

None

Protozoa

Culicidae (mosquitoes) All domestic vertebrates Viruses, bacteria, protozoa, nematodes Psychodidae (sandflies) Livestock and pets Viruses, protozoa

(mammals) Simuliidae (blackflies) Livestock and pets Protozoa, nematodes

(mammals and birds) Ceratopogonidae (biting midges) Livestock and pets Viruses, protozoa, nematodes

(mammals) Viruses, protozoa, nematodes

Brachycera Tabanidae (horse and deer flies) Livestock and pets Viruses, bacteria, protozoa

(mammals) Viruses, bacteria, protozoa

Carnidae Birds None Braulidae (bee 'lice') Bees None Muscidae (house flies, etc.) All domestic vertebrates Bacteria Chloropidae (eye gnats) Livestock (mammals) Viruses, bacteria Calliphoridae (blow flies) All domestic vertebrates Secondary infection via haematophagy

Oestridae (bot flies) or myiasis

Oestridae (bot flies) Livestock (mammals) Secondary infection via myiasis Sarcophagidae (flesh flies) Livestock (mammals) Secondary infection via myiasis

989

Brachycera(contd) Glossinidae (tsetse flies) Livestock (mammals) Protozoa Hippoboscidae (louse-flies) Livestock Protozoa, nematodes

(mammals and birds) Siphonaptera (fleas) Livestock and pets Viruses, bacteria,

(mammals and birds) rickettsiae, cestodes ** ^rachnida Parasitiformes

Ixodida (ticks) Livestock and pets Viruses, bacteria, rickettsiae, Ixodida (ticks) (mammals and birds) protozoa, nematodes

Dermanyssidae Birds Viruses (?) Halarachnidae Mammals None Laelapidae Bees None Macronyssidae Poultry, pets (mammals) Nematodes Rhinonyssidae Birds None Varroidae (bee mites) Bees Secondary bacterial infections

Acariformes Analgidae (feather mites) Birds None Cheyletiellidae Livestock and pets None

(mammals and birds) Cytoditidae Birds None Demodicidae (follicle mites) Livestock (mammals) Secondary bacterial infections Dermoglyphidae (quill mites) Birds None Epidermoptidae Birds None Ereynetidae Birds None Gaudoglyphidae (quill mites) Birds None Knemidocoptidae Birds None Laminosioptidae Birds None Myobiidae (fur mites) Mammals None Psorergatidae (itch mites) Livestock and pets None

(mammals) Psoroptidae (mange mites) Livestock and pets None

(mammals) Pterolichidae (feather mites) Birds None Sarcoptidae (mange mites) Livestock and pets None

(mammals) Syringophilidae (quill mites) Birds None Tarsonemidae Bees None Trombiculidae (chigger mites) Livestock and pets Viruses (?), rickettsiae Trombiculidae (chigger mites)

(mammals and birds)

* Pathogens transmitted to humans or wild animals are excluded ** These pathogens use the listed ectoparasites as intermediate hosts

T A B L E I (contd)

Principal groups of ectoparasites associated with domestic animals and their role in pathogen transmission*

Ectoparasites Hosts Pathogens transmitted

Vertebrata Pisces

Agnatha (lampreys) Mammalia

Chiroptera (vampire bats)

Fish None

Livestock (mammals) Virases, rickettsiae, protozoa

990

Order Cyclopoida

T h e o r d e r Cyc lopo ida is mos t ly c o m p r i s e d of free-living c o p e p o d s inc luding t h e well-k n o w n free-living Cyclops spp . A few g e n e r a a r e paras i t ic , inc luding t h e fol lowing:

a) Ergasilus spp . morpho log ica l ly r e s e m b l e Cyclops spp . , excep t t h a t in Ergasilus t h e s e c o n d a n t e n n a e a r e t r a n s f o r m e d in to l a rge c lasper- l ike claws. Ergasilus s pp . a t t a c h t o t h e gill f i laments of f r e shwate r ( p o n d ) fish. C o p u l a t i o n occurs whi le b o t h sexes a r e f ree-sw imming , after wh ich t h e m a l e d ies . On ly f e m a l e ergasi l ids e n t e r t h e gill cavity of t h e fish, w h e r e they c r e e p to t h e gills a n d a t t ach us ing the i r c laws.

b) T h e g e n u s Lernaea h a s f r e q u e n t l y b e e n p l a c e d in t h e o r d e r Ca l i go ida . O n l y t h e worm-l ike females , which h a v e horn- l ike processes or anchors on t he cepha lo tho rax (38), a r e p a r a s i t i c . T h e c e p h a l i c h o r n s e n a b l e t h e p a r a s i t e t o fix i tself i n t o t h e h o s t m u s c l e t issue. Lernaea cyprinacea paras i t izes f reshwater fish, a t tach ing o n the ou t s ide surface by bor ing in to t he under ly ing musc le t issues, a l t hough t h e g r e a t e r p a r t of t h e pa ras i t e body r e m a i n s ou t s ide t he host . H e a v y infes ta t ion by Lernaea is fatal to t he hos t (13).

Order Caligoida

T h e o r d e r C a l i g o i d a is c o m p r i s e d e x c l u s i v e l y b y p a r a s i t i c g e n e r a . T h e f o l l o w i n g g e n e r a a r e f requent ly e n c o u n t e r e d :

a) Lepeophtheirus s p p . ( s e a l ice) h a v e a c i r c u l a r d o r s o v e n t r a l l y - f l a t t e n e d c e p h a l o t h o r a x , w h i c h is c o v e r e d w i t h a c a r a p a c e o r sh ie ld . T h e m o u t h is a d a p t e d for s u c k i n g , w h i l e t h e p o i n t e d m a n d i b l e s p i e r c e t h e sk in of t h e h o s t . Lepeophtheirus salmonis is e s s e n t i a l l y l i m i t e d t o s a l m o n i d fish in E u r o p e a n d N o r t h A m e r i c a . I n expe r imen ta l s tudies using At lan t i c , ch inook a n d coho sa lmon, t he la t te r species was t he m o s t r e s i s t an t t o L. salmonis whi le t h e A t l a n t i c s a l m o n was t h e m o s t suscep t ib le (40) . K e n t (46) i nd i ca t e s t h a t all spec ies of sea l ice s t u d i e d h a v e a d i r e c t life cycle ( w i t h o u t a l t e rna te or i n t e rmed ia t e hosts) with t en d e v e l o p m e n t a l s tages (Fig. 1). Var ious s tages in t he life cycle a r e parasi t ic . Sea lice h a v e b e e n r e p o r t e d t o cause ser ious d a m a g e to fish in m a n y sa l twater r ea r ing facilities, inc luding t hose loca ted in land. T h e r e l a t ionsh ip of t he n u m b e r of sea lice t o t h e sever i ty of d i s ea se is d e p e n d e n t o n t w o fac tors , n a m e l y (46) :

- size a n d age of t h e fish

- species a n d d e v e l o p m e n t a l s tages of sea lice p re sen t .

b) Caligus s pp . a r e c h a r a c t e r i z e d by t h e p r e s e n c e of t w o semic i r cu la r s t r u c t u r e s o n t h e a n t e r i o r m a r g i n of t h e h e a d ; t h e s e a r e k n o w n as ' l u n u l e s ' , a n d a r e b e l i e v e d t o b e s enso ry o rgans . Caligus has c o n e - s h a p e d , suck ing m o u t h p a r t s . U n l i k e Lepeophtheirus or mos t o t h e r paras i t ic c o p e p o d s , adu l t Caligus a r e capab le of sw imming a n d m a y leave o n e h o s t a n d a t t a c h t o a n o t h e r . S o m e spec ies of Caligus a p p e a r t o h a v e a w o r l d - w i d e d i s t r i b u t i o n a n d b r o a d h o s t a s soc ia t ions . Caligus clemensi is a n i m p o r t a n t p a r a s i t e of n e t p e n s a l m o n in t he no r th -wes t Pacific reg ion (46).

Order Lernaeopodoida

T h e l e r n a e o p o d i d s a r e m o d i f i e d m o r e m a r k e d l y f r o m t h e a n c e s t r a l f r e e - l i v i n g c o p e p o d s t h a n even t h e caligoids. T h e ancho r ing device in this o r d e r is t e r m e d t h e bul la , a n d is f o r m e d by sec re t ions f rom t h e h e a d a n d maxi l la ry g lands (13) . T h e maxi l l ae a r e u s u a l l y l a r g e a n d f u s e d t o t h e b u l l a . T h e f e m a l e b e c o m e s a f ixed p a r a s i t e a t t a c h e d i m m o v a b l y t o t h e hos t . T h e m a l e is very smal l ( d w a r f e d ) , clings t o t h e f e m a l e a n d c a n crawl o v e r h e r body. T h e o r d e r L e r n a e o p o d o i d a consis ts of a p p r o x i m a t e l y six g e n e r a , o n e of which (Salmincola) is i m p o r t a n t to t he fish cu l tu re industry.

991

Chalimus (four stages), attached to fish by

frontal filament

Fig. 1 Life cycle of the sea lice (Lepeophtheirus spp.)

(46)

I n Salmincola, t h e b o d y of t h e f e m a l e is c o m p l e t e l y w i t h o u t s e g m e n t s ; t h e max i l l ae a r e m o d i f i e d as a r m s , j o i n i n g a t t h e b u l l a . T h e m o u t h p a r t s b e a r a f i l a m e n t for a t t a c h m e n t t o fish. T h e la rva l Salmincola forces this f i lament in to t h e t i ssue of fish a n d a t t a c h e s t h e s e c o n d m a x i l l a e t o t h e f i l a m e n t , w h i c h b e c o m e s p a r t of t h e b u l l a , t h u s a t t ach ing itself p e r m a n e n t l y t o t h e hos t . Salmincola spp . cause c o n s i d e r a b l e d a m a g e in s a lmon id fish fa rming o p e r a t i o n s , especial ly in N o r t h A m e r i c a (41) .

Subclass Branchiura

M e m b e r s of t h e s u b c l a s s B r a n c h i u r a a r e s m a l l c r u s t a c e a n s s i m i l a r t o c o p e p o d s which, a t o n e t i m e , w e r e c o n s i d e r e d t o r e p r e s e n t a n o r d e r wi th in t h e C o p e p o d a . T h e y a r e c o m m o n l y k n o w n as ' f i sh l i c e ' ; a l l a r e p l a c e d in t h e o r d e r A r g u l o i d a . T h e m o r p h o l o g y s h o w s f e w e r v a r i a t i o n s t h a n t h a t of o t h e r p a r a s i t i c C r u s t a c e a . T h e

Nauplius (two stages), free-swimming,

non-feeding

Eggs

Adult (one stage), free-moving on

fish, able to swim

Pre-adult (two stages), free-moving on fish,

able to swim

Copepodid (one stage), free-swimming,

non-feeding, infective

992

A r g u l o i d a a r e a d a p t e d for a t t a c h m e n t by t h e p r e s e n c e of h o o k s a n d suc t ion cups o n t h e ven t ra l sur face of t h e body. T h e r e is n o la rva l s t age (naup l ius ) a n d d e v e l o p m e n t in to a juven i le is d i rect . T h e m o u t h p a r t s a r e grea t ly r e d u c e d .

A s t r iking f ea tu re of Argulus spp . is t h e modi f ica t ion of t h e s econd maxi l l ae in to t w o suc t ion cups wh ich e n a b l e t h e p a r a s i t e t o r e m a i n a t t a c h e d to t h e hos t . T h e m a n d i b l e s a r e modi f ied , fo rming a p r e -o r a l ' s t ing ' wi th which t h e fish louse p ie rces t he skin of t h e fish t o ob t a in a b l o o d m e a l . Argulus foliaceus is t h e m o s t c o m m o n ca rp louse in E u r a s i a a n d h a s b e e n i n a d v e r t e n t l y i n t r o d u c e d t o o t h e r c o n t i n e n t s a l o n g w i t h i ts h o s t . A. foliaceus occas iona l ly p a r a s i t i z e s t r o u t a n d o t h e r spec i e s of fish. O t h e r i m p o r t a n t p a r a s i t i c s p e c i e s of t h i s g e n u s a r e A. pellucidus ( a s s o c i a t e d w i t h s e v e r a l s p e c i e s of cypr in id fish) a n d A. coregoni ( assoc ia ted wi th sa lmon ids a n d perc ids ) .

Subclass Malacostraca

M e m b e r s of t h e o r d e r I s o p o d a (e .g . Livoneca s pp . ) h a v e b e e n m e n t i o n e d (41) as causing ser ious losses in t he fishing industry, bu t the i r i m p o r t a n c e to species utilized in fish fa rming r e m a i n s unc lea r ; t hey paras i t i ze f reshwate r fish in C e n t r a l a n d S o u t h A m e r i c a . A n o t h e r m e m b e r of this subclass , t he d e c a p o d crayfish (Astacus astacus), is involved in t h e t r a n s m i s s i o n of in fec t ious p a n c r e a t i c n e c r o s i s v i rus t o r a i n b o w t r o u t ( see b e l o w ) .

E F F E C T S O F P A R A S I T I S M

T h e d i r e c t ef fects of e c t o p a r a s i t i c i n f e s t a t i o n o n t h e h o s t s h a v e b e e n ca re fu l ly r ev iewed (3 , 7, 41) . F o r in fo rma t ion o n pa ras i t e s a n d diseases of fish species cu l tu red in t he t ropics , t he r e a d e r is re fe r red to K a b a t a (42). K e n t (46) p re sen t s de ta i led in format ion o n t h e e c t o p a r a s i t e s a f fec t ing n e t p e n - r e a r e d s a l m o n i d fish in t h e n o r t h - w e s t Paci f ic region, especial ly L. salmonis a n d C. clemensi. K e n t (46) also discusses cu r r en t m e t h o d s of cont ro l . In cont ras t to t h e sensitivity of t he cyprinids a n d sa lmonids t o ec toparas i tes in aquacu l tu r e ope ra t i ons , t h e Ic ta lu r idae (catfish) f a rmed in t he w a r m e r reg ions of N o r t h A m e r i c a a n d p a r t s of E u r o p e s e e m p o t to d e v e l o p s e v e r e p r o b l e m s d u e t o c r u s t a c e a n ec toparas i tes . F o r example , Hof fman (38) impl ica ted six species of t he g e n e r a Achtheres, Argulus, Ergasilus a n d Lernaea o c c u r r i n g in n a t u r e o n t h e c h a n n e l cat f ish (Ictalurus punctatus). H o w e v e r , n o a c t u a l r e p o r t s ex i s t in t h e l i t e r a t u r e of d i s e a s e - r e l a t e d condi t ions induced by these ec toparas i t es in fish fa rming ope ra t ions .

P A T H O G E N T R A N S M I S S I O N

T h e exis tence of bac ter ia l o rgan i sms associa ted wi th fish species in fa rming prac t ices h a s b e e n d o c u m e n t e d ( 3 , 7, 7 0 ) ; for e x a m p l e , Aeromonas salmonicida, Vibrio salmonicida, Yersinia ruckeri, i n f e c t i o u s p a n c r e a t i c n e c r o s i s ( I P N ) v i ru s a n d t h e infect ious s a l m o n a n a e m i a ( I S A ) agen t h a v e b e e n r e p o r t e d . T h e m e a n s by which t h e s e o r g a n i s m s i n v a d e t h e h o s t a r e n o t k n o w n in d e t a i l . H e a v y i n f e c t i o n by p a r a s i t i c c rus taceans m a y cause genera l debi l i ta t ion of t he fish, leading to g r e a t e r susceptibil i ty t o such o r g a n i s m s . In a d d i t i o n , t h e i n t e g u m e n t a r y w o u n d s m a d e by t h e s e e c t o p a r a s i t e s of ten p e n e t r a t e d e e p in to t h e s u b c u t a n e o u s t issue. Such p u n c t u r e w o u n d s u n d o u b t e d l y aid secondary mic roorgan i sms in establ ishing infection in t he host . K a b a t a (41) ind ica ted t h a t t h e r e was l i t t le c o n c r e t e e v i d e n c e of c r u s t a c e a n pa ra s i t e s t r a n s m i t t i n g p a t h o g e n i c o rgan isms to fish, b u t cited D o m b r o w s k i (20), w h o r e p o r t e d Argulus spp . as t ransmi t t ing t h e b a c t e r i u m Aeromonas punctata ( c a u s i n g ' r e d d i s e a s e ' ) t o c a r p . A. punctata w a s injected in to t h e skin of ca rp in t he course of feeding by Argulus.

993

Recen t ly , s ignif icant a d v a n c e s h a v e b e e n m a d e in k n o w l e d g e of t h e pos s ib l e v e c t o r re la t ionships of t he parasi t ic Crus tacea t ransmi t t ing disease organisms to fish. A h n e ( 1 , 2) r e p o r t e d Argulus foliaceus to b e a m e c h a n i c a l vec to r of SVCV. U n i n f e c t e d A. foliaceus b e c a m e i n f e c t e d w h e n f ed u p o n i n f e c t e d c a r p , a n d S V C V ( n o w c la s s i f i ed as Rhabdovirus carpia) w a s t r a n s m i t t e d t o u n i n f e c t e d c a r p by t h e s e e c t o p a r a s i t e s . T h e vi rus in fec t ion in Argulus was cons i s t en t ly of a l o w e r t i t r e t h a n t h a t m a i n t a i n e d in t h e carp . M u l c a h y et al. (63) i so la ted I H N virus f rom Salmincola sp. , a c o p e p o d ec topa ra s i t e of t he sockeye s a lmon (Oncorhynchus nerka). T h e significance of t h e s e r e p o r t s was t he isolat ion of S V C V a n d I H N viruses f rom a n a n i m a l o t h e r t h a n a fish.

F i s h t h e m s e l v e s h a v e b e e n r e g a r d e d as t h e m a i n v e c t o r s in t h e t r a n s m i s s i o n of b a c t e r i a l a n d v i ra l d i s e a s e s i m p o r t a n t t o fish s p e c i e s . H o w e v e r , N e s e a n d E n g e r (67) i so la ted Aeromonas salmonicida ( causa l a g e n t of fu runcu los i s ) f rom t h e s a l m o n louse (L. salmonis) a n d f r o m u n s p e c i f i e d m a r i n e p l a n k t o n . S a l m o n l ice r e m a i n e d i n f e c t e d after app ly ing 7 0 % e t h a n o l t o t h e o u t e r su r faces of t h e p a r a s i t e s , s u g g e s t i n g t o t h e s e a u t h o r s t h a t A. salmonicida was r e s i d i n g i n s i d e L. salmonis, p r o b a b l y in t h e gu t (67) . Nylund et al. (70) p r e s e n t e d da t a indicat ing tha t L. salmonis cou ld funct ion as a vec to r of t he I S A agent , a p r e s u m e d vi rus which h a s n o t ye t b e e n fully charac te r ized . T h e y found the I S A agent t o b e p r e s e n t in t he gut of t h e s a lmon lice.

F r e s h w a t e r c r a y f i s h (Astacus astacus) h a v e b e c o m e a n i n c r e a s i n g l y i m p o r t a n t c o m p o n e n t in a q u a c u l t u r e , d u e t o m o r e f r equen t i n t e rna t i on a l s h i p m e n t of this species . H a i d e r a n d A h n e (34) e x p e r i m e n t a l l y i n f e c t e d A . astacus w i t h I P N v i r u s b y t h r e e rou tes : i m m e r s i o n in a w a t e r b a t h c o n t a i n i n g t h e virus , a d m i n i s t r a t i o n of v i rus in food, a n d e x p o s u r e t o v i r a e m i c fry of r a i n b o w t r o u t (Oncorhynchus mykiss ; f o r m e r l y Salmo gairdneri). I n f ec t ed crayfish exc re t ed I P N vi rus , a n d virus was i so la ted f rom t h e h a e m o l y m p h u p to o n e y e a r a f t e r in i t i a l i n f ec t i on . T h e f i nd ing t h a t t h e eggs a n d fry of r a i n b o w t r o u t b e c a m e in fec ted af ter e x p o s u r e t o w a t e r i n fec t ed w i t h I P N v i rus d u e t o e x c r e t i o n of t h e v i rus b y crayf ish is i m p o r t a n t , as r a i n b o w t r o u t a n d A. astacus a r e o f t en f a r m e d t o g e t h e r in t h e s a m e b i o t o p e . T h e s e d a t a i m p l i c a t e A. astacus a s a p o t e n t i a l l y i m p o r t a n t r e s e r v o i r of I P N v i r u s , a n d c l ea r ly i l l u s t r a t e t h e h e t e r o l o g o u s e p i z o o t i o l o g y of d i s e a s e s of fish a n d t h e c o m p l i c a t i o n s of r e a r i n g l a r g e n u m b e r s of an imals in conf ined spaces .

LICE

Lice a r e wingless insects wh ich a r e classified e i the r as a single o r d e r ( P h t h i r a p t e r a ) or as t w o o r d e r s ( A n o p l u r a [ s u c k i n g l ice] a n d M a l l o p h a g a [ c h e w i n g / b i t i n g l i c e ] ) . A p p r o x i m a t e l y 540 va l id spec i e s of s u c k i n g lice a r e r e c o g n i z e d (24) , all of w h i c h a r e ob l iga te h a e m a t o p h a g o u s e c t o p a r a s i t e s of m a m m a l s . A l t h o u g h on ly a b o u t 20 of t h e s e species a r e pes t s of d o m e s t i c an imals , t hey can occur in h u g e n u m b e r s which m a y resu l t in hos t i r r i t a t ion , a n a e m i a o r de rma t i t i s (23) . T w o suck ing louse g e n e r a , Haematopinus a n d Linognathus, f e a t u r e p r o m i n e n t l y as e c t o p a r a s i t e s of l i v e s t o c k . H o r s e s , c a t t l e , sheep , goa ts a n d pigs m a y b e heavi ly infes ted wi th sucking lice. Came l s , l l amas , a lpacas and g u a n a c o e s a r e all pa ras i t i zed by sucking lice be long ing t o t h e genus Microthoracius, w h i c h c a n d a m a g e t h e p e l a g e o r c a u s e d e r m a t i t i s ( 5 1 ) . L a b o r a t o r y r o d e n t s m a y b e infes ted wi th v a r i o u s spec ies of Hoplopleura o r Polyplax, wh i l e l a b o r a t o r y r a b b i t s a r e s o m e t i m e s p a r a s i t i z e d by Haemodipsus spp . , a n d p r i m a t e s by Pedicinus o r Pediculus. S o m e s u c k i n g l ice of l i v e s t o c k a r e k n o w n t o t r a n s m i t p a t h o g e n s . E x a m p l e s i n c l u d e s w i n e p o x v i r u s t r a n s m i s s i o n t o p ig s b y Haematopinus suis, a n d t r a n s m i s s i o n of Anaplasma marginale (57) a n d t h e sk in fungus Trichophyton verrucosum by v a r i o u s

994

spec ie s of ca t t l e l ice (23) . B y v i r t u e of b l o o d - f e e d i n g , s u c k i n g l ice a r e g e n e r a l l y m o r e a d e p t a t t r a n s m i t t i n g p a t h o g e n s t o d o m e s t i c a n i m a l s t h a n a r e c h e w i n g l ice , a l t h o u g h chewing lice o n ca t t le can also t r a n s m i t T. verrucosum (43) .

T h e c h e w i n g l ice ( M a l l o p h a g a ) m a y b e c lass i f i ed i n t o t h r e e g r o u p s ( I s c h n o c e r a , A m b l y c e r a a n d R h y n c h o p h t h i r i n a ) , e a c h usual ly i n t e r p r e t e d as a suborde r . Whi l e s o m e chewing lice a r e h a e m a t o p h a g o u s , m o s t species a p p e a r t o subsis t o n hos t skin scrapings , e x u d a t e s , fur o r f ea the r s (55) . Col lect ively , t h e c h e w i n g lice a r e m o r e d ive r se t h a n t h e s u c k i n g l ice , w i t h a p p r o x i m a t e l y 2 ,600 s p e c i e s d e s c r i b e d w o r l d - w i d e (55 ) . D i f f e r e n t s p e c i e s of c h e w i n g l ice p a r a s i t i z e e i t h e r b i r d s o r m a m m a l s , a n d m o s t s p e c i e s ( a p p r o x i m a t e l y 2,200) a r e a s soc ia ted wi th b i rds . A s wi th t h e A n o p l u r a , t h e major i ty of t h e b iod ive r s i ty i n h e r e n t in t h e c h e w i n g lice is a s s o c i a t e d w i t h fera l h o s t s , b u t a smal l n u m b e r of i m p o r t a n t s p e c i e s ( a p p r o x i m a t e l y 50 ) p a r a s i t i z e d o m e s t i c h o s t s . A g a i n , p r e s e n c e of p a r a s i t e s in l a r g e n u m b e r s c a n b e e x t r e m e l y d e t r i m e n t a l t o t h e h o s t s , especial ly l ives tock or poul t ry . T h e g e n u s Bovicola i nc ludes severa l species of chewing lice wh ich a r e a s soc i a t ed wi th l ives tock, wh i l e Felicola subrostrata occurs o n d o m e s t i c c a t s a n d Trichodectes canis o c c u r s o n d o g s . T. canis is a n i n t e r m e d i a t e h o s t of t h e t a p e w o r m Dipylidium caninum, a n e n d o p a r a s i t e of d o g s (55 ) . H o r s e s , c a t t l e , s h e e p , goats and pou l t ry m a y b e heavi ly infes ted wi th chewing lice.

S e v e r a l g e n e r a of c h e w i n g lice o c c u r o n d o m e s t i c b i r d s , a n d l a rge i n f e s t a t i ons c a n cause irritability, p o o r weight gains o r a n a e m i a in t h e s e species . Chelopistes meleagridis a n d Oxylipeurus polytrapezius a r e c o m m o n l ice of t u r k e y s , w h i l e Cuclutogaster heterographus, Goniocotes gallinae, Goniodes dissimilis, Goniodes gigas, Lipeurus caponis, Menacanthus stramineus a n d Menopon gallinae pa ras i t i ze d o m e s t i c ch ickens in m a n y pa r t s of t he wor ld . Guinea- fowl , peafowl a n d p h e a s a n t s a r e pa ras i t i zed by s o m e of t h e s a m e spec ies of l ice w h i c h o c c u r o n c h i c k e n s . G e e s e a r e p a r a s i t i z e d by Anaticola anseris a n d Trinoton anserinum, a n d d u c k s b y Anaticola crassicornis a n d Trinoton querquedulae. C e r t a i n l ice of w a t e r fowl , i n c l u d i n g t h o s e of d u c k s a n d s w a n s , a r e c apab l e of h a r b o u r i n g a n d t r ansmi t t i ng p a t h o g e n i c n e m a t o d e s ( inc luding h e a r t w o r m s ) t o the i r hos ts (14).

T h e t h r e e m e m b e r s of t h e O l d W o r l d R h y n c h o p h t h i r i n a p a r a s i t i z e e i t h e r e l e p h a n t s o r wi ld p i g s . Haematomyzus elephantis, t h e s p e c i e s f o u n d o n e l e p h a n t s ( b o t h A f r i c a n a n d I n d i a n ) , c a n o c c u r in l a r g e n u m b e r s a n d s o m e t i m e s c a u s e s d e r m a t i t i s in hos t s (76) .

TRUE BUGS

T h e la rge insect o r d e r H e m i p t e r a c o n t a i n s s eve ra l h a e m a t o p h a g o u s e c t o p a r a s i t e s , i n c l u d i n g a p p r o x i m a t e l y 115 s p e c i e s of k i s s i n g ( ' c o n e - n o s e ' ) b u g s ( R e d u v i i d a e : T r i a t o m i n a e ) a n d a p p r o x i m a t e l y 74 s p e c i e s of b e d b u g s a n d b a t b u g s ( C i m i c i d a e ) (83 , 94, 99) . T h e s e re la t ive ly l a rge (5-44 m m in l e n g t h ) e c t o p a r a s i t e s s p e n d e x t e n d e d p e r i o d s away f rom t h e hos t (usual ly c o n c e a l e d in c rev ices ) a n d m a k e phys ica l c o n t a c t w i t h t h e h o s t p r i nc ipa l l y w h e n t a k i n g a b l o o d m e a l . M o s t k i s s ing b u g s (102 s p e c i e s ) a r e c o n f i n e d t o t h e N e w W o r l d , a n d s o m e s p e c i e s wi l l f e e d o n a v a r i e t y of h o s t s i n c l u d i n g a v a i l a b l e d o m e s t i c a n i m a l s , w h e r e r e l a t i v e l y l a r g e b l o o d v o l u m e s m a y b e i m b i b e d . S e v e r a l s p e c i e s of k i s s i n g b u g s ( c e r t a i n s p e c i e s in t h e g e n e r a Triatoma, Rhodnius a n d Panstrongylus) s e r v e as v e c t o r s of Trypanosoma cruzi, t h e c a u s a t i v e a g e n t of C h a g a s ' d i s e a s e ( A m e r i c a n t r y p a n o s o m o s i s ) , w h i c h c a n b e d e b i l i t a t i n g t o h u m a n s ( 9 9 ) . A l t h o u g h i n f e c t e d d o g s m a y s h o w s igns of C h a g a s ' d i s e a s e , m o s t

995

p a r a s i t i z e d d o m e s t i c a n d s y l v a t i c h o s t s of t h i s t r y p a n o s o m e s h o w i n a p p a r e n t in fec t ions a n d s e r v e as r e s e r v o i r hos t s (84) .

Cimicid bugs can b e deb i l i t a t ing pes t s of poul t ry , a n d e v e n re la t ive ly smal l n u m b e r s of t h e M e x i c a n c h i c k e n b u g Haematosiphon inodorus, a d e n i z e n of w e s t e r n N o r t h A m e r i c a a n d M e x i c o , c a n c a u s e i r r i t ab i l i ty o r a n a e m i a in t h e s e h o s t s w i t h o c c a s i o n a l de a th s of y o u n g b i rds . O t h e r c imids - such as Cimex lectularius (a c o s m o p o l i t a n species) a n d C. hemipterus (a t r op i copo l i t an species) - wh ich n o r m a l l y feed o n h u m a n s m a y also feed on d o m e s t i c an imals , especial ly ch ickens (94) .

MOSQUITOES AND RELATIVES

T h e t r u e flies ( o r d e r D i p t e r a ) e n c o m p a s s a d iverse a r ray of species which a r e pes t s of domes t i c an imals . S o m e g r o u p s , such as t h e k e d s or louse-fl ies ( H i p p o b o s c i d a e ) , s p e n d m u c h of t h e i r a d u l t l ives o n t h e h o s t a n d a r e c l e a r l y a d a p t e d m o r p h o l o g i c a l l y a n d p h y s i o l o g i c a l l y fo r a n e c t o p a r a s i t i c l i f e s ty l e . H o w e v e r , m o s t o t h e r g r o u p s , s u c h as m o s q u i t o e s a n d tse tse flies, can at bes t b e ca t egor i zed as i n t e r m i t t e n t ec topa ra s i t e s , d u e t o t h e t yp i ca l ly s h o r t - t e r m p h y s i c a l c o n t a c t w i t h t h e h o s t ( 5 5 ) . T h i s s y n o p s i s of t h e D i p t e r a fo l lows t h e p h y l o g e n e t i c c lass i f ica t ion of M c A l p i n e et al. ( 54 ) , w h o t r e a t t h e N e m a t o c e r a a n d B r a c h y c e r a as s u b o r d e r s , a n d recogn ize t h e M u s c o m o r p h a ( equ iva len t t o the s u b o r d e r C y c l o r r h a p h a auct.) as a n in f rao rde r of t h e B r a c h y c e r a .

R e p r e s e n t a t i v e s of severa l famil ies of D i p t e r a wi th in t h e s u b o r d e r N e m a t o c e r a feed on domes t i c an imals , ut i l izing t he i r s tylet- l ike m o u t h p a r t s t o ob t a in a b l o o d - m e a l . M o s t i m p o r t a n t a m o n g t h e s e a r e t h e m o s q u i t o e s ( C u l i c i d a e ) . T h i s b r i e f s u r v e y c a n o n l y h i g h l i g h t t h e i m p o r t a n c e of t h e s e a n d r e l a t e d f l ies . O f t h e a p p r o x i m a t e l y 3 ,200 d e s c r i b e d s p e c i e s of m o s q u i t o e s , h u n d r e d s c a n b e p e s t s of l i v e s t o ck , p e t s o r pou l t ry . L a r g e n u m b e r s of m o s q u i t o e s can cause irri tabili ty, hos t a n a e m i a , a l lergic r e s p o n s e s a n d r e l a t ed s e q u e l a e . H o w e v e r , in m a n y a r ea s , m o s q u i t o e s a r e m o r e i m p o r t a n t as vec to rs of p a t h o g e n s t o d o m e s t i c a n i m a l s . P a t h o g e n i c v i ruses (e .g. t h e e n c e p h a l i t i d e s ) , b a c t e r i a ( e .g . Bacillus anthracis), p r o t o z o a ( e .g . m a l a r i a l p a r a s i t e s ) a n d t h e n e m a t o d e s (e.g. f i lar iae) of s eve ra l d i seases a r e all t r a n s m i t t e d to d o m e s t i c b i rds a n d / o r m a m m a l s by mosqu i t oe s . M a n y o f t h e s e p a t h o g e n s u n d e r g o d e v e l o p m e n t a l cycles in t h e m o s q u i t o vec to r ref lec t ing t r u e b io logica l t r ansmiss ion , whi le o t h e r p a t h o g e n s (e.g. B. anthracis) a re t r a n s m i t t e d mechan ica l ly via c o n t a m i n a t e d m o s q u i t o m o u t h p a r t s (39) .

O t h e r n e m a t o c e r a n fl ies b e l o n g i n g t o t h e f a m i l i e s P s y c h o d i d a e ( s a n d f l i e s : a p p r o x i m a t e l y 600 s p e c i e s w o r l d - w i d e ) , S i m u l i i d a e ( b l a c k f l i e s , b u f f a l o f l ies : a p p r o x i m a t e l y 1,500 s p e c i e s ) a n d C e r a t o p o g o n i d a e ( b i t i n g m i d g e s , ' n o s e e - u m s ' , ' p u n k i e s ' : a p p r o x i m a t e l y 4 ,200 s p e c i e s ) a l s o a d v e r s e l y affect d o m e s t i c a n i m a l s , especial ly l ivestock, in m o s t p a r t s of t h e wor ld . I n l a rge p o p u l a t i o n s , r e p r e s e n t a t i v e s of all t h e s e fami l ies m a y c a u s e i r r i tab i l i ty , a n a e m i a , d e b i l i t a t i n g i m m u n e r e s p o n s e s a n d r e l a t e d m a n i f e s t a t i o n s i n h o s t s ( 3 9 ) . I n t h e N e w W o r l d , t h e s a n d f l y Lutzomyia ylephiletrix is a vec to r of t h e virus which causes ves icular s tomat i t i s in ho r ses , mu le s a n d o c c a s i o n a l l y in c a t t l e a n d p i g s . C e r t a i n s a n d f l i e s a l so t r a n s m i t Leishmania s p p . p r o t o z o a n s , wh ich c a u s e l e i s h m a n i o s e s in dogs (as wel l as in h u m a n s ) in b o t h t h e O l d a n d N e w W o r l d (53) . Sa l ivary s e c r e t i o n s of s o m e b lackf l ies c o n t a i n t ox in s wh ich m a y d e b i l i t a t e o r k i l l l i v e s t o c k . C e r t a i n b l a c k f l i e s a l s o t r a n s m i t Leucocytozoon s p p . p r o t o z o a n s t o b i rds , caus ing an infect ion which is of ten p a t h o g e n i c to tu rkeys , ch ickens , ducks a n d geese . O t h e r blackfl ies t r a n s m i t n e m a t o d e s (Onchocerca ochengi in Afr ica , a n d O. gutturosa a n d O. lienalis in t e m p e r a t e l a t i t u d e s ) w h i c h c a n b e p a t h o g e n i c t o

996

d o m e s t i c ungu la t e s , especial ly ca t t le . M o s t adu l t c e r a t o p o g o n i d s a r e tiny, a n d s o m e a re efficient vec to rs of g loba l ly-d is t r ibu ted p a t h o g e n i c a rbov i ruses (e.g. b l u e t o n g u e vi rus of u n g u l a t e s , e s p e c i a l l y s h e e p ) , a n d f i l a r i id n e m a t o d e s (e .g . Onchocerca cervicalis of h o r s e s ) (30, 36) . M u l t i p l e b i t e s by c e r t a i n spec ies of c e r a t o p o g o n i d s can a lso c a u s e a n al lergic r e s p o n s e k n o w n as ' swee t i t ch ' or ' Q u e e n s l a n d i tch ' in hyper sens i t ive h o r s e s in m a n y p a r t s of t h e wor ld (30) .

T h e r e m a i n i n g flies t o b e a d d r e s s e d in th i s o v e r v i e w a r e c u r r e n t l y a s s i g n e d to t h e s u b o r d e r B r a c h y c e r a (54) , wh ich i nc ludes m a n y fami l ies c o n t a i n i n g spec ies adve r se ly affect ing d o m e s t i c a n i m a l s . A m o n g t h e m o s t p e s t i f e r o u s of t h e s e a r e m e m b e r s of t h e family T a b a n i d a e ( h o r s e a n d d e e r flies); a d u l t f ema le s of m o s t of t h e ( a p p r o x i m a t e l y ) 3,600 d e s c r i b e d t a b a n i d s p e c i e s a r e o b l i g a t e h a e m a t o p h a g e s . S e v e r a l s p e c i e s in t h e g e n e r a Chrysops, Tabanus, Hybomitra a n d Haematopota a t t ack d o m e s t i c an imals , of ten with litt le hos t specificity. L a r g e p o p u l a t i o n s of these flies m a y s w a r m a r o u n d l ivestock, e spec i a l l y c a t t l e a n d h o r s e s , c a u s i n g s ign i f i can t i r r i t a t i o n ( a n d s o m e t i m e s a n a e m i a ) t h r o u g h pers i s t en t , painful b i t e s infl icted t o o b t a i n b l o o d mea l s . Mu l t i p l e t a b a n i d b i t e s c a n a lso c a u s e low w e i g h t g a i n s , d e c r e a s e d mi lk y ie ld a n d d a m a g e t o h i d e s in c a t t l e . S o m e h o r s e a n d d e e r f l ies a r e v e c t o r s of i m p o r t a n t p a t h o g e n s a f f ec t i ng d o m e s t i c an imals . Trypanosoma evansi, t h e causa t ive agen t of sur ra , a se r ious l ivestock d isease in t h e O l d W o r l d a n d in S o u t h a n d C e n t r a l A m e r i c a , is t r a n s m i t t e d m e c h a n i c a l l y b y seve ra l t a b a n i d s . C a m e l s , h o r s e s , dogs a n d e l e p h a n t s a r e of ten s eve re ly i n fec t ed wi th su r r a , w h e r e a s ca t t l e a n d buffa lo a r e o f t en mi ld ly a f fec ted a n d c a n s e r v e as r e s e r v o i r h o s t s . A few a d d i t i o n a l t r y p a n o s o m e s of l e s s e r s i gn i f i c ance a r e a l so t r a n s m i t t e d t o d o m e s t i c a n i m a l s by t a b a n i d s . T h e c a u s a t i v e v i r u s of e q u i n e i n f e c t i o u s a n a e m i a , a debi l i ta t ing d isease of equ ids in m a n y pa r t s of t h e wor ld , is t r a n s m i t t e d mechan ica l ly by t a b a n i d s . O t h e r p a t h o g e n s t r a n s m i t t e d t o d o m e s t i c a n i m a l s by t a b a n i d s i n c l u d e t h e r i cke t t s i a Anaplasma marginale (wh ich c a u s e s a n a p l a s m o s i s in ca t t l e ) a n d t h e fi larial n e m a t o d e Elaeophora schneiden ( a n a r t e r i a l w o r m of s h e e p a n d wild r u m i n a n t s ) (29) .

MUSCID FLIES AND RELATIVES

T h e small d i p t e r a n family C a r n i d a e inc ludes o n e species , Carnus hemapterus, which (as a n a d u l t ) b r e a k s off i ts d e c i d u o u s w ings a n d l ives as a n e c t o p a r a s i t e of b i r d s , e s p e c i a l l y n e s t l i n g s ( 8 0 ) . A l t h o u g h wi ld b i r d s a r e m o r e p r o n e t o a t t a c k b y th i s fly, domes t i c b i rds a re occasional ly paras i t ized .

T h e b e e l o u s e b e l o n g s t o t h e f ami ly B r a u l i d a e , g e n u s Braula. T h e r e is o n l y o n e s p e c i e s w i t h i n t h e family, Braula caeca (= coeca). T h e b e e l o u s e is a t iny, m i t e - l i k e , wingless insec t w i t h a r o u n d e d h e a v y body , s t r o n g legs a n d smal l eyes . A d u l t b e e l ice c l ing t o t h e b o d y of a d u l t h o n e y b e e s , m o s t l y a t t h e j u n c t i o n of t h e t h o r a x a n d t h e a b d o m e n . W h e n r e a d y t o f eed , t h e b e e l o u s e m o v e s t o w a r d s t h e h e a d a n d r e m o v e s p o l l e n a n d sa l iva f r o m t h e m o u t h p a r t s of t h e a d u l t b e e . T h e eggs d r o p i n t o b r o o d c h a m b e r s a n d h a t c h . T h e y o u n g l a rvae t h e n t u n n e l i n t o t h e w a x c a p of t h e h o n e y cell . L a r v a e inges t wax gra ins a n d po l l en (71) , a p p a r e n t l y d iges t ing t h e w a x wi th t h e a id of i n t e s t i n a l m i c r o o r g a n i s m s . T h i s m a y d i s f i g u r e h o n e y t o b e s o l d in t h e c o m b . M a t h e s o n (56) s t a t e s t h a t t h e b e e l o u s e is n o t a p a r a s i t e a n d is r e g a r d e d by m a n y as h a v i n g n o e c o n o m i c s i g n i f i c a n c e . T h e l o u s e is w o r l d - w i d e in d i s t r i b u t i o n a n d m a y c o n g r e g a t e o n t h e q u e e n in a u t u m n . S h i m a n u k i et al. (86) c o n c l u d e t h a t t h e g r e a t e s t p r o b l e m assoc ia ted wi th t he b e e louse is t he fact t ha t it m a y b e m i s t a k e n for a m i t e w h e n found on bees . T h e b e e louse is still an issue for s o m e certifying au thor i t i e s .

997

T h e f ami ly M u s c i d a e i n c l u d e s s e v e r a l i m p o r t a n t p e s t s of d o m e s t i c a n i m a l s . T h e h o u s e fly (Musca domestica) is a c o s m o p o l i t a n m e n a c e , c a p a b l e of m e c h a n i c a l l y t r ansmi t t i ng severa l p a t h o g e n s . La rge - sca l e l ives tock a n d p o u l t r y o p e r a t i o n s a r e of ten p l a g u e d w i t h t h o u s a n d s o r m i l l i o n s of h o u s e f l ies o r r e l a t e d ' f i l th f l i e s ' ( e s p e c i a l l y Fannia canicularis a n d F. scalaris [ d i s t r i bu t ed w o r l d - w i d e ] , Musca Sorbens [in t h e O l d W o r l d ] a n d M. vetustissima [in A u s t r a l i a ] ) w h i c h feed o n a n i m a l w a s t e as i m m a t u r e s . O t h e r s p e c i e s i n t h e g e n u s Musca c a u s e m o r e d i r e c t d i s t r e s s t o d o m e s t i c a n i m a l s . M. crassirostris is an ob l iga te h a e m a t o p h a g e which feeds o n l ivestock (especial ly ca t t le ) in t he O l d Wor ld , a n d M. autumnalis ( t he face fly) is a c o s m o p o l i t a n species which m a y s w a r m o n l i v e s t o c k h e a d s a n d c a n t r a n s m i t t h e c a u s a t i v e b a c t e r i u m of ' p i n k e y e ' (Moraxella bovis) in c a t t l e . T h e s h e e p h e a d fly (Hydrotaea irritans) is p e s t i f e r o u s in Br i t a in , w h e r e it is a t t r a c t e d t o s e r o u s e x u d a t e s f rom t h e eyes a n d nost r i l s ; this species c a n c a u s e d e b i l i t a t i n g l e s i o n s in s h e e p . O t h e r i m p o r t a n t m u s c i d s i n c l u d e t h e h a e m a t o p h a g o u s a n d c o s m o p o l i t a n s tab le fly (Stomoxys calcitrans) a n d r e l a t e d species (S. sitiens a n d S. nigra of t h e O l d W o r l d ) , wh ich a r e v ic ious b i t e r s of e q u i d s , ca t t l e a n d o t h e r d o m e s t i c an imals . Lastly, t h e h o r n fly (Haematobia irritans) is a h a e m a t o p h a g o u s species d i s t r ibu ted widely t h r o u g h o u t t h e wor ld , wh ich s w a r m s a r o u n d ca t t le a n d ho r ses and m a y cause significant i r r i t a t ion to t h e s e an imals , of ten resu l t ing in p o o r we igh t gains or low milk yields (30, 36) .

A l t h o u g h m o s t c h l o r o p i d fl ies a r e a s s o c i a t e d w i t h p l a n t s , a few s p e c i e s ( t h e ' e y e gna ts ' ) a r e a t t r ac t ed t o b o d y open ings , sores or w o u n d s of d o m e s t i c an imals . T h e g e n e r a Hippelates in t h e N e w W o r l d a n d Siphunculina in A s i a a r e espec ia l ly pe s t i f e rous a n d , a l t h o u g h n o t h a e m a t o p h a g o u s , flies of t h e s e g e n e r a can m e c h a n i c a l l y t r a n s m i t ce r t a in p a t h o g e n s (e.g. t h e causa t ive agen t s of b o v i n e mast i t i s a n d p ink eye) (36).

MYIASIS-CAUSING FLIES

T h e families Ca l l iphor idae (b low flies) a n d S a r c o p h a g i d a e (flesh flies) inc lude severa l species wh ich adverse ly affect d o m e s t i c an ima l s . W h i l e t he l a rvae (maggo t s ) of m o s t of t he se flies feed o n a n i m a l ca rcasses , t h o s e of s eve ra l spec ies a r e facu l ta t ive o r ob l iga te paras i tes in living t issues. Such paras i t i sm of live an imals by fly l a rvae is t e r m e d 'myiasis ' . Similarly, l a r v a e of m e m b e r s of t h e family O e s t r i d a e (bo t flies) c a u s e ob l iga t e myias is . D i f f e r e n t b o d y r e g i o n s a r e t y p i c a l l y a t t a c k e d by d i f f e r e n t fly l a r v a e , a n d g a s t r o intest inal , u rogen i ta l , ocular, n a s o p h a r y n g e a l , aur icular or c u t a n e o u s myiasis m a y resul t .

Ca l l iphor ids which cause facul ta t ive myias is inc lude Phaenicia serricata, P. pallescens a n d Phormia regina ( w h i c h c a u s e ' s h e e p s t r i k e ' ) a n d Cochliomyia macellaria ( t h e s e c o n d a r y s c r e w w o r m of t h e N e w W o r l d ) . S e v e r a l flesh flies (Sarcophaga s pp . ) a l so cause facul ta t ive myias is in d o m e s t i c an ima l s . T h e l a r v a e of re la t ive ly few ca l l iphor ids o r s a r c o p h a g i d s h a v e p r o g r e s s e d t o o b l i g a t e m y i a s i s . N e v e r t h e l e s s , s o m e i m p o r t a n t ob l iga t e myias i s - caus ing pes t s of d o m e s t i c a n i m a l s a r e i n c l u d e d in t h e s e t w o famil ies . A m o n g t h e c a l l i p h o r i d s , t h e p r i m a r y s c r e w w o r m (Cochliomyia hominivorax) is of m a j o r s ign i f i cance in t h e N e w W o r l d . A l t h o u g h C. hominivorax h a s e s sen t i a l l y b e e n e r ad i ca t ed f rom t h e U S A a n d C a n a d a , this species con t i nues t o cause ser ious p r o b l e m s in l i v e s t o c k ( e s p e c i a l l y c a t t l e ) in t h e r e m a i n d e r of t h e N e w W o r l d , a n d it w a s acc iden ta l ly i n t r o d u c e d i n t o ( b u t l a t e r e x t i r p a t e d f r o m ) L i b y a (96) . U n t r e a t e d les ions d u e t o C. hominivorax en l a rge as m o r e m a g g o t s b e c o m e involved in t h e infes ta t ion , a n d s e c o n d a r y myias is a g e n t s (e.g. Cochliomyia macellaria) o r s e c o n d a r y w o u n d infec t ion of ten resu l t in hos t d e a t h . Chrysomyia bezziana ( t he O l d Wor ld s c r e w w o r m ) is a n o t h e r

998

i m p o r t a n t m y i a s i s - c a u s i n g c a l l i p h o r i d s p e c i e s a s s o c i a t e d w i t h l i v e s t o c k ( 9 6 ) , w h i l e m e m b e r s of t h e g e n e r a Pachychoeromyia a n d Neocuterebra p a r a s i t i z e A f r i c a n e l e p h a n t s , a n d Protocalliphora s pp . p a r a s i t i z e ne s t l i ng b i r d s ( 1 1 , 100) . T h e t u m b u fly, Cordylobia anthropophaga ( C a l l i p h o r i d a e ) , o f ten causes myias is in h u m a n s in Afr ica , b u t th i s spec i e s will a l so p a r a s i t i z e r a t s , m o n k e y s , ca t s , d o g s a n d a n t e l o p e (100) . T h e H o l a r c t i c s a r cophag id g e n u s Wohlfahrtia i nc ludes four species (W. magnifica, W. nuba, W. opaca a n d W. vigil) which cause ob l iga te myiasis in d o m e s t i c an imals (36) .

M e m b e r s of t h e fami ly O e s t r i d a e c a u s e o b l i g a t e myias i s a n d a r e r e p r e s e n t e d by a d i v e r s e a r r a y of spec ie s w h i c h p a r a s i t i z e d o m e s t i c a n i m a l s a c ro s s t h e w o r l d . C u r r e n t d i p t e r a n c l a s s i f i c a t i o n r e c o g n i z e s f o u r d i s t i n c t s u b f a m i l i e s w i t h i n t h e O e s t r i d a e : C u t e r e b r i n a e ( N e w W o r l d sk in b o t flies), H y p o d e r m a t i n a e ( O l d Wor ld skin b o t flies), O e s t r i n a e (nose a n d t h r o a t b o t flies) a n d G a s t e r o p h i l i n a e ( s t o m a c h b o t flies) (54) . T h e subfamily C u t e r e b r i n a e inc ludes m a n y species of N e w Wor ld r o d e n t a n d r a b b i t b o t flies. O n e c u t e r e b r i n e , t he to r sa lo (Dermatobia hominis), a t t acks h u m a n s a n d l ivestock, a n d a small n u m b e r of species in t h e g e n u s Alouattamyia pa ras i t i ze m o n k e y s (12, 81).

T h e s u b f a m i l y H y p o d e r m a t i n a e i n c l u d e s t h e c o m m o n c a t t l e g r u b (Hypoderma lineatim) a n d t h e n o r t h e r n ca t t l e g r u b (H. bovis), wh ich a r e n o w wide ly d i s t r i b u t e d in t h e n o r t h e r n h e m i s p h e r e , e spec ia l ly in t e m p e r a t e r e g i o n s . B o t h of t h e a b o v e spec i e s c a u s e m a j o r e c o n o m i c losses t o t h e ca t t l e indus t ry . D a m a g e occu r s w h e n ca t t l e in ju re t h e m s e l v e s as t h e y f lee f r o m o v i p o s i t i n g f e m a l e f l ies ( t e r m e d ' g a d d i n g ' ) a n d a f t e r s laughter , w h e n warb le b lemishes m u s t b e t r i m m e d ; h ides a r e also found to b e pe r fo ra t ed by t h e a c t i o n of t h e g r u b (85 ) . C a t t l e g r u b eggs a r e l a id d i r e c t l y o n c a t t l e a n d , a f t e r ha tch ing , t h e y o u n g la rvae crawl t o t h e ha i r bases a n d p e n e t r a t e t h e hos t skin t o beg in a four- to s ix-month migra t ion pe r iod wi thin the connec t ive t issue, before cluster ing a long t h e m i d l i n e o r o e s o p h a g u s a n d fo rming a w a r b l e p o r e t o t h e e x t e r i o r (8 , 85) . A n o t h e r h y p o d e r m a t i n e , H. tarandi, p r o d u c e s similar warb les in r e i n d e e r ra ised as l ivestock (11) .

M e m b e r s of t he subfamily O e s t r i n a e principal ly paras i t ize ungu la te s in t h e O l d Wor ld a n d Aus t ra l i a . Eggs of these flies d e v e l o p in utero, a n d first ins ta r l a rvae a r e squ i r t ed by hove r ing gravid females in to t he eye or muzz le of t h e hos t . D e v e l o p i n g l a rvae r e s ide in t he nasal s inuses o r pha ryngea l regions . T h e s h e e p n o s e bo t (Oestris ovis) is an i m p o r t a n t p e s t of d o m e s t i c s h e e p a n d g o a t s , w h i l e t h e h o r s e n o s e b o t (Rhinoestrus purpureus) parasi t izes horses and the r e i n d e e r t h r o a t b o t (Cephenemyia trompe) occurs in r e i n d e e r a n d car ibou. L a r v a e of all t h r e e species can cause ser ious p r o b l e m s w h e n p re sen t in large n u m b e r s , wi th occasional hos t dea th s be ing r e c o r d e d (36).

M a g g o t s of s t o m a c h b o t flies ( G a s t e r o p h i l i n a e ) d e v e l o p in t h e gu t o r p h a r y n g e a l r eg ion of equ id s , e l e p h a n t s a n d rh inoce rose s . A d u l t females ovipos i t o n t o hos t p e l a g e , w h e r e t h e eggs a r e l i cked a n d i n g e s t e d o r h a t c h s p o n t a n e o u s l y i n t o first i n s t a r l a r v a e w h i c h b u r r o w i n t o t h e m o u t h t i s s u e a n d a r e e v e n t u a l l y s w a l l o w e d , a t t a c h i n g t o t h e pha rynx , s t o m a c h o r in tes t inal wall; t h e si te of a t t a c h m e n t differs for each species . A f t e r d e v e l o p i n g in t h e s e s i t e s , m a t u r e l a r v a e r e l e a s e t h e i r h o l d a n d a r e v o i d e d w i t h h o s t f a e c e s t o s u b s e q u e n t l y p u p a t e in t h e so i l . N i n e s p e c i e s of Gasterophilus p a r a s i t i z e d o m e s t i c e q u i d s t h r o u g h o u t t h e w o r l d , w h i l e t h r e e s p e c i e s of Cobboldia i n f e s t e l e p h a n t s . I m p o r t a n t , w i d e s p r e a d spec ies a s soc ia t ed wi th d o m e s t i c e q u i d s i nc lude t h e c o m m o n h o r s e s t o m a c h bo t (G. intestinalis), t h e p r e d o m i n a n t species in N o r t h A m e r i c a , a n d t h e d a r k - w i n g e d h o r s e b o t (G. pecorum), t h e m o s t c o m m o n spec ies in Afr ica a n d E u r a s i a . M o s t d o m e s t i c e q u i d s a r e pa r a s i t i z ed by in t e s t i na l b o t s d u r i n g t h e i r l i fe t ime, wi th smal l infes ta t ions caus ing little a p p a r e n t morb id i t y (11 , 50).

999

TSETSE FLIES AND LOUSE FLIES

T h e s m a l l f ami ly G l o s s i n i d a e c o n s i s t s of 23 k n o w n s p e c i e s of t s e t s e f l ies ( g e n u s Glossina) which inhab i t var ious pa r t s of t h e Afr ican con t inen t . T h e ro le of m a n y of t he se p e s t i f e r o u s flies in t r a n s m i t t i n g t h e t r y p a n o s o m e s w h i c h c a u s e s l e e p i n g s i c k n e s s in h u m a n s a n d n a g a n a in d o m e s t i c a n i m a l s is we l l d o c u m e n t e d . A t l e a s t five spec i e s of t r y p a n o s o m e s a r e t r a n s m i t t e d t o wild a n d d o m e s t i c an imals in Afr ica by va r ious species of Glossina. W h i l e m o s t wi ld h o s t s a r e i m m u n e o r h a v e i n a p p a r e n t i n f e c t i o n s , m a n y d o m e s t i c a n i m a l s d e v e l o p t h e d i s e a s e s y m p t o m s of n a g a n a . Trypanosoma brucei, T. congolense a n d T. vivax a r e t h e m o s t i m p o r t a n t a g e n t s of n a g a n a . S e v e r a l d o m e s t i c an imals inc lud ing came l s , h o r s e s , m u l e s , ca t t l e , s h e e p , goa t s a n d pigs a r e suscep t ib le to th i s d i s e a s e , w h i c h o f t e n m a n i f e s t s as a n a e m i a , w e a k n e s s , r e d u c e d m u s c l e m a s s , e n l a r g e m e n t of i n t e r n a l o r g a n s a n d l y m p h n o d e s , f e v e r a n d d i a r r h o e a . M o s t o r g a n systems can b e c o m e infected, a n d d e a t h is c o m m o n in infected d o m e s t i c s tock (36).

T h e f ami ly H i p p o b o s c i d a e b e l o n g s t o t h e s u b o r d e r B r a c h y c e r a , s u p e r f a m i l y H i p p o b o s c o i d e a . T h e r e a r e a p p r o x i m a t e l y 20 g e n e r a a n d 150-200 spec ies in t h e w o r l d f a u n a (52 , 5 6 ) . T h e f ami ly is c o s m o p o l i t a n b u t p r i m a r i l y t r o p i c a l a n d s u b - t r o p i c a l . M e m b e r s of t h e H i p p o b o s c i d a e h a v e b e e n g iven severa l c o m m o n n a m e s , such as louse flies, k e d s , flat flies, s h e e p ' t i cks ' o r fores t flies. In t h e adu l t s tage , all species a r e ob l iga te ec topa ra s i t e s , f eed ing o n t h e b l o o d of b i rds a n d m a m m a l s . F e m a l e s p r o d u c e on ly o n e m a t u r e o v u m a t a t i m e , w h i c h d e v e l o p s i n t o a s ing l e l a r v a w i t h i n t h e f e m a l e . W h e n m a t u r e , t h e l a r v a is d e p o s i t e d e i t h e r o n a s p e c i e s - s p e c i f i c s i t e o r r a n d o m l y o n t h e g round . A s s o m e spec ies a t t a c k d o m e s t i c m a m m a l s , especia l ly u n g u l a t e s , t h e s e insec ts can b e of cons ide rab l e e c o n o m i c i m p o r t a n c e .

T h e m o s t i m p o r t a n t m e m b e r of th i s f ami ly is Melophagus ovinus ( t h e s h e e p k e d ) , which is found on s h e e p t h r o u g h o u t t h e wor ld . L a r v a e a r e a t t a ched to t h e f leece of s h e e p and, as this fly is wingless , t h e en t i r e life cycle is spen t o n t h e host . D u e to t h e g rega r ious n a t u r e of s h e e p , t ransfer of k e d s f rom o n e hos t to a n o t h e r is easily accompl i shed . T h e s e flies i r r i ta te s h e e p , caus ing t h e m to sc ra tch a n d r u b themse lves , t hus d a m a g i n g t h e w o o l and foul ing it w i t h k e d faeces . F e e d i n g les ions c a n also r e n d e r s h e e p h i d e s u n s a l e a b l e . H e a v y i n f e s t a t i o n s c a n c a u s e a n a e m i a , a n d M. ovinus is t h e v e c t o r of Trypanosoma melophagium, a n o n - p a t h o g e n i c p r o t o z o a n found in sheep .

A n e m a t o d e e n d o p a r a s i t e of d o g s , Dipetalonema dracunculoides, u n d e r g o e s d e v e l o p m e n t in, a n d is t r a n s m i t t e d by Hippobosca longipennis, a c o m m o n e c t o p a r a s i t e of dogs a n d wild ca rn ivo res in t h e O l d W o r l d (33, 64) .

A l t h o u g h a p p r o x i m a t e l y 7 5 % of all h i p p o b o s c i d s a t t ack b i rds , t h e p i g e o n (Columba livia) is t h e only d o m e s t i c a t e d b i rd pa ras i t i zed by a h ippobosc id , n a m e l y Pseudolynchia canariensis. P. canariensis is t h e v e c t o r of Haemoproteus columbae in p i g e o n s ( 4 7 ) . O t h e r infect ious agen t s t r a n s m i t t e d by m e m b e r s of t h e family H i p p o b o s c i d a e h a v e b e e n r ev iewed by B a k e r (6) .

FLEAS

Of t h e a p p r o x i m a t e l y 2 ,200 r e c o g n i z e d s p e c i e s a n d s u b s p e c i e s of f l eas ( S i p h o n a p t e r a ) , on ly a b o u t 20 species typical ly pa ras i t i ze d o m e s t i c b i rds a n d m a m m a l s (90, 91) . H o w e v e r , a d u l t s of t h e s e h a e m a t o p h a g o u s e c t o p a r a s i t e s ( w h i c h a r e u sua l l y

1000

h i g h l y m o b i l e ) c a n c a u s e s i gn i f i c an t p r o b l e m s , s u c h as a n a e m i a , d e r m a t i t i s , hypersens i t iv i ty a n d p a t h o g e n t r ansmiss ion t o d o m e s t i c hos t s (9, 90) .

P e r h a p s t h e m o s t w i d e s p r e a d a n d pes t i f e rous flea, a s soc ia t ed wi th severa l d o m e s t i c m a m m a l s , is t h e cat flea (Ctenocephalides felis) (21) . A l t h o u g h this flea is m o s t c o m m o n o n cats a n d dogs , w h e r e levels of infes ta t ion can b e e x t r e m e l y high, C. felis will also feed o n h u m a n s , g o a t s , s h e e p , e q u i d s a n d o t h e r h o s t s . C. felis is a n u i s a n c e m a i n l y d u e t o pe r s i s t en t bi t ing, b u t this species can also cause de rma t i t i s , hypersens i t iv i ty o r a n a e m i a , a n d is a v e c t o r of Rickettsia typhi ( t h e causa t i ve a g e n t of m u r i n e t y p h u s ) . T h e closely-r e l a t e d d o g flea (Ctenocephalides canis) is n o w r a r e in m o s t p a r t s of t h e w o r l d , a n d is p e r h a p s be ing d i sp laced by t h e cat flea. B o t h cat a n d d o g fleas a r e i n t e r m e d i a t e hos t s of t h e t a p e w o r m Dipylidium caninum, a c o m m o n pa ra s i t e of cats a n d dogs (55).

Seve ra l o t h e r fleas a r e n u i s a n c e b i t e r s of d o m e s t i c m a m m a l s . T h e E u r o p e a n r a b b i t f lea (Spilopsyllus cuniculi) is a ' s t i ck - t igh t ' spec ies wh ich e m b e d s its m o u t h p a r t s i n t o h o s t sk in for e x t e n d e d p e r i o d s , a n d is a s s o c i a t e d wi th l a b o r a t o r y a n d b r e e d i n g r a b b i t ins ta l la t ions wor ld -wide . Th i s flea is a vec to r of t h e virus which causes m y x o m a t o s i s in E u r o p e a n r a b b i t s ( 5 5 ) . T h e ' a l a k u r t ' f l eas Dorcadia ioffi a n d Vermipsylla alakurt p a r a s i t i z e u n g u l a t e s in C e n t r a l A s i a , e s p e c i a l l y h o r s e s , s h e e p a n d y a k s ( 2 5 ) . L a r g e n u m b e r s of a l a k u r t fleas can cause a n a e m i a , ha i r loss, r e t a r d e d g rowth , unthr i f t iness o r d e a t h , e s p e c i a l l y in n e w - b o r n l a m b s . Tunga penetrans ( t h e c h i g o e o r j i g g e r f l ea ) paras i t i zes h u m a n s , pigs a n d occas ional ly dogs . F e m a l e s of this flea e m b e d t h e m s e l v e s d e e p l y i n t o h o s t sk in a n d d e r m i s t i s sue , a n d c a u s e pa in fu l l e s ions w h i c h a r e p r o n e t o s econda ry infect ion (39). In pigs , t h e s e les ions occur in t h e feet , snou t , s c r o t u m or t ea t s ; i n v o l v e m e n t of t he t ea t s of ten res t r ic ts milk flow, resu l t ing in s t a rva t ion of piglets (25) . T w o f leas in t h e g e n u s Pulex, n a m e l y P. irritans a n d P. simulans, c a n b e i m p o r t a n t e c t o p a r a s i t e s of d o m e s t i c m a m m a l s , e s p e c i a l l y p ig s , d o g s a n d c a t s . T h e s o - c a l l e d ' h u m a n flea' (P. irritans) is d i s t r ibu ted patchi ly across t h e g lobe , whi le P. simulans occurs in N o r t h A m e r i c a ( 9 1 ) . M a n y o t h e r f lea s p e c i e s a r e o c c a s i o n a l b i t e r s of d o m e s t i c a n i m a l s . S o m e of t h e s e f leas - s u c h as c e r t a i n m e m b e r s of t h e g e n e r a Citellophilus, Ctenocephalides, Ctenophthalmus, Nosopsyllus, Oropsylla, Pulex a n d e s p e c i a l l y Xenopsylla - c a n t r a n s m i t t h e a g e n t s of m u r i n e t y p h u s a n d / o r p l a g u e t o d o m e s t i c an ima l s (9, 90, 93) . W h i l e s o m e d o m e s t i c an imals a r e re f rac tory t o t he se p a t h o g e n s a n d s e rve as r e se rvo i r s of in fec t ion , o t h e r s a r e s eve re ly in fec ted a n d m a y d ie (e .g. p l a g u e -infected ca ts) .

B i r d s a r e p a r a s i t i z e d by a smal l n u m b e r of flea spec ies w h i c h m a y c a u s e deb i l i t i e s . T h e s t i c k - t i g h t f lea Echidnophaga gallinacea is a s e d e n t a r y s p e c i e s w h i c h f e e d s o n p o u l t r y in m o s t t r op i ca l a n d s u b - t r o p i c a l p a r t s of t h e w o r l d . T h e s e smal l f leas usua l ly a t t a ch for e x t e n d e d p e r i o d s t o u n f e a t h e r e d hos t s i tes (e .g. t h e h e a d , c o m b , w a t t l e a n d p e r i a n a l r e g i o n ) . L a r g e p o p u l a t i o n s of E. gallinacea c a n c a u s e a n a e m i a , a n d f e e d i n g sites can b e c o m e u lce ra ted . Such les ions a r e p r o n e to s e c o n d a r y infect ion, a n d b l indness m a y re su l t if u l c e r a t i o n s a b u t t t h e eyes , effect ively p r e v e n t i n g t h e b i r d f r o m feed ing . T h e h e n flea o r E u r o p e a n ch icken flea (Ceratophyllus gallinae) feeds o n severa l species of b i r d s , i nc lud ing pou l t ry , in m a n y p a r t s of t h e w o r l d . A r e l a t e d spec ie s , t h e w e s t e r n ch i cken flea (Ceratophyllus niger) is a pes t of p o u l t r y in w e s t e r n N o r t h A m e r i c a . B o t h Ceratophyllus species a r e n o n - s e d e n t a r y a n d a r e f r equen t ly f o u n d a w a y f rom t h e hos t . I n g e n e r a l , t h e s e f l eas c a u s e l ess d a m a g e t o t h e h o s t t h a n E. gallinacea, b u t l a r g e infes ta t ions can resul t in a n a e m i a a n d inefficient g rowth , especial ly in chicks (25).

1001

TICKS

Ticks b e l o n g to t h e class A r a c h n i d a , o r d e r A c a r i a n d s u b o r d e r I x o d i d a . T i c k s a r e classified in t h r e e famil ies , as follows:

- A r g a s i d a e (soft t icks) , compr i s ing five g e n e r a a n d a p p r o x i m a t e l y 170 species

- I x o d i d a e ( h a r d t icks) , compr i s ing 14 g e n e r a a n d a p p r o x i m a t e l y 680 species

- t he m o n o t y p i c family Nut ta l l i e l l idae , con t a in ing t h e species Nuttalliella namaqua.

All t icks a r e o b l i g a t e h a e m a t o p h a g o u s e c t o p a r a s i t e s of a m p h i b i a n s , r ep t i l e s , b i r d s , a n d / o r m a m m a l s d u r i n g s o m e o r all p h a s e s of t h e i r life cycle . F o r r e c e n t o v e r v i e w s of the Ixodida , see Ol iver (72) a n d K e i r a n s (44).

A few soft t icks (e.g. Ornithodoros lahorensis, O. tholozani a n d o r g a s persicus [ the fowl t i ck ] ) in fes t l i v e s t o c k o r fowl a n d c a n c a u s e d i s e a s e p r o b l e m s , i n c l u d i n g fowl s p i r o c h a e t o s i s . Ornithodoros moubata porcinus a n d O. erraticus a r e a l so i m p o r t a n t v e c t o r s of A f r i c a n s w i n e f e v e r v i r u s . O t h e r i m p o r t a n t a r g a s i d s o n l i v e s t o c k a r e Ornithodoros savignyi a n d Otobius megnini. T h e l a t t e r tick, or iginal ly a pa r a s i t e of la rge w a n d e r i n g a r t i o d a c t y l s of w e s t e r n N o r t h A m e r i c a , h a s b e c o m e a d a p t e d t o c a t t l e a n d ho r ses a n d h a s b e e n i n t r o d u c e d i n t o S o u t h A m e r i c a , S o u t h Af r i ca , I n d i a a n d s e v e r a l o the r a reas of t h e wor ld . A d u l t O. megnini a r e non-paras i t i c . H o w e v e r , a l t h o u g h severa l argasids a r e i m p o r t a n t pes t s , t h e vas t major i ty of t icks infes t ing l ives tock a n d d o m e s t i c animals be long to t h e family I x o d i d a e .

A c c o r d i n g to s o m e e s t ima te s , 8 0 % of t h e 1.23 bi l l ion cat t le in t h e w o r l d a r e infes ted with t icks (31) , a n d t icks a r e r e s p o n s i b l e for s eve re losses d u e t o t ick worry , b l o o d loss, d a m a g e t o h i d e s a n d u d d e r s , i n j e c t i o n of t o x i n s , o r m o r t a l i t y a n d d e b i l i t y c a u s e d b y t r ansmi t t ed d i sease o rgan i sms . M u k h e b i et al. (62) e s t i m a t e d t h e loss in 1989 f rom E a s t C o a s t f e v e r - a c a t t l e d i s e a s e in E a s t e r n a n d S o u t h e r n A f r i c a t r a n s m i t t e d b y Rhipicephalus appendiculatus ( t h e b r o w n e a r t i c k ) a n d R. zambeziensis - t o b e US$168 mil l ion. Th i s f igure inc luded t h e loss of 1.1 mil l ion h e a d of ca t t le .

O f t h e 14 g e n e r a of I x o d i d a e , s p e c i e s in t h e g e n e r a Amblyomma, Anocentor, Boophilus, Dermacentor, Haemaphysalis, Hyalomma, Ixodes, Nosomma a n d Rhipicephalus h a v e a c h i e v e d a s t a t u s as p e s t s t o l i v e s t o c k a n d o t h e r d o m e s t i c a t e d animals , p r imar i ly in t h e t rop ica l a n d sub- t rop ica l r eg ions of t h e wor ld .

In s u b - S a h a r a n Afr ica , s even Amblyomma species a r e c o m m o n l y found o n l ivestock, a n d al l a r e p r o v e n o r s t r o n g c a n d i d a t e v e c t o r s of Cowdria ruminantium, Theileria mutans, Coxiella burnetii a n d / o r Rickettsia conori. T h e s e t icks a r e a lso r e s p o n s i b l e for s e v e r a l v i r a l d i s e a s e s in u n g u l a t e s . T h e t i ck s p e c i e s i n v o l v e d a r e A. astrion, A. cohaerens, A. gemma, A. hebraeum, A. lepidum, A. pomposum a n d A. variegatum. This last spec ies is a l so a s e r ious p e s t a n d v e c t o r of t h e a g e n t of h e a r t w a t e r d i s ea se o n several C a r i b b e a n is lands , hav ing b e e n i n t r o d u c e d to t h e a r e a in t h e 19th century. F o r a s u m m a r y of t h e hos t s a n d d i s t r ibu t ions of t h e Af r i can Amblyomma spp . , t o g e t h e r wi th excel lent i l lus t ra t ions , t h e r e a d e r is r e f e r r ed to W a l k e r (95) .

T h r e e A s i a n a m b l y o m m a s a r e i m p o r t a n t p e s t s of d o m e s t i c a n i m a l s . T h e m o s t i m p o r t a n t is A. testudinarium, a d u l t s of wh ich feed o n d o m e s t i c p igs , ca t t l e a n d o t h e r l ivestock, a n d h u m a n s . T h i s spec ies is d i s t r i b u t e d o v e r a n a r e a r a n g i n g f rom I n d i a a n d Sri L a n k a t o I n d o n e s i a , B o r n e o , t h e P h i l i p p i n e s , T a i w a n a n d t h e s o u t h e r n i s l ands of J a p a n . A. integrum in I n d i a a n d S r i L a n k a a n d A. mudlairi in I n d i a f e e d o n w i ld ungu la te s a n d l ivestock.

1002

In t h e A m e r i c a s , four i m p o r t a n t Amblyomma spp . a r e p r e s e n t on l ivestock, a l t h o u g h t h e s e i n d i s c r i m i n a t e e c t o p a r a s i t e s c a n b e f o u n d o n m a n y o t h e r a n i m a l s . T h e m o s t i m p o r t a n t s p e c i e s is A. americanum ( t h e l o n e s t a r t i c k ) , w h i c h o c c u r s in S o u t h a n d C e n t r a l A m e r i c a , a n d in p a r t s of N o r t h A m e r i c a . A. cajennense ( t h e c a y e n n e t i ck ) is f o u n d f rom S o u t h A m e r i c a t o s o u t h e r n Texas , a n d h a s a lso b e e n r e p o r t e d f rom C u b a . A. maculatum ( t he Gulf C o a s t t ick) r anges f rom n o r t h e r n S o u t h A m e r i c a to t he coas ta l a reas of t he Gulf of Mex ico , hav ing also b e e n found o n t h e s o u t h - e a s t e r n A t l an t i c coas t of t h e U S A a n d in O k l a h o m a . A. maculatum has also b e e n r e c o r d e d f rom Jama ica . T h e four th species, A. imitator, occurs in Cen t r a l A m e r i c a a n d n o r t h w a r d s t o s o u t h e r n Texas .

T h e g e n u s Anocentor c o n t a i n s a s ingle spec ies , A. nitens ( t h e t rop ica l h o r s e t i ck ) , a one -hos t tick of l ivestock, especial ly ho r ses , m u l e s a n d d o n k e y s . This tick is found f rom S o u t h A m e r i c a n o r t h w a r d s t o F l o r i d a a n d T e x a s . A. nitens is c o m m o n l y c a l l e d t h e t r o p i c a l h o r s e t i ck , a n d f e e d s in t h e e a r s a n d in h e a v y i n f e s t a t i o n s in t h e n a r e s a n d m a n e s of t he se an imals . Th i s species is also t h e vec to r of Babesia caballi t o hor ses .

T h e g e n u s Boophilus c o m p r i s e s f ive s p e c i e s , al l of w h i c h a r e i m p o r t a n t p e s t s of c a t t l e , s h e e p a n d g o a t s . T h e g e n u s is d i s t r i b u t e d w o r l d - w i d e , u s u a l l y s o u t h of 4 0 ° N . B. kohlsi is a pa ras i t e of s h e e p a n d goa ts in Is rael , J o r d a n , Syria, I r a q a n d Saud i A r a b i a . T h e r ema in ing four species a r e ca t t le pa ras i t es . B. geigyi is found in h u m i d Wes t Afr ica , b e i n g o c c a s i o n a l l y r e c o r d e d ( d u e t o m o v e m e n t of a n i m a l s ) as far e a s t as s o u t h e r n S u d a n . B. decoloratus is f o u n d in s a v a n n a a r e a s f rom t h e S a h a r a t o S o u t h e r n Af r i ca . T h e r e m a i n i n g t w o s p e c i e s a r e v e r y w i d e s p r e a d , a n d r e p r e s e n t t h e m o s t d a n g e r o u s m e m b e r s of t h e g e n u s . B. annulatus is f o u n d in t h e M e d i t e r r a n e a n b a s i n ( S o u t h e r n E u r o p e and N o r t h Afr ica) , s o u t h e r n Russ i a a n d t h e M i d d l e E as t , a n d is also es tab l i shed in s u b - S a h a r a n A f r i c a as f a r s o u t h as S u d a n a n d E t h i o p i a . T h i s s p e c i e s h a s b e e n i n t r o d u c e d in to M e x i c o , a n d at o n e t i m e s p r e a d t h r o u g h o u t t h e s o u t h e r n U S A b e f o r e b e i n g v i r t u a l l y e r a d i c a t e d . C o n t i n u e d s u r v e i l l a n c e is e m p l o y e d t o p r e v e n t r e in t roduc t ion of B. annulatus in to t h e U S A . B. microplus was originally a na t ive of t h e I n d i a n s u b c o n t i n e n t , b u t is n o w f o u n d in A u s t r a l i a , S o u t h - E a s t e r n Afr ica , a n d S o u t h a n d C e n t r a l A m e r i c a . B o t h B. microplus a n d B. annulatus a r e e f f i c i en t v e c t o r s of Babesia spp . a n d Anaplasma marginale. F e l d m a n - M u h s a m a n d Schech te r (26) p r o v i d e d a s u m m a r y of t he se species , t o g e t h e r wi th d i s t r ibu t ion m a p s and keys for adul t s .

T h e genus Dermacentor compr i s e s a p p r o x i m a t e l y 30 species , t h e major i ty of wh ich a r e found in t h e N e w Wor ld . T h r e e species a r e of i m p o r t a n c e in this p a r t of t h e wor ld . D. albipictus ( t h e w i n t e r t i ck ) is a o n e - h o s t t i ck w h i c h c a n o c c u r in h u g e n u m b e r s o n c a t t l e o r h o r s e s , c a u s i n g s e v e r e deb i l i t y o r e v e n d e a t h . T h i s t i ck is a c t i v e in fall a n d win te r , a n d can b e f o u n d f rom C a n a d a to M e x i c o . D. andersoni ( t h e R o c k y M o u n t a i n w o o d t ick) is o n e of t he m o s t i m p o r t a n t t icks in t he wor ld . In t h e adu l t s tage , this species thr ives o n l ivestock ( including b ison) a n d is found f rom w e s t e r n C a n a d a s o u t h w a r d s t o N e w Mex ico . D. andersoni causes tick para lys is in wild a n d d o m e s t i c a r t iodac ty l s , dogs a n d h u m a n s , a lso t r a n s m i t t i n g t h e agen t s of a n a p l a s m o s i s , Q fever, t u l a r a e m i a , R o c k y M o u n t a i n s p o t t e d fever a n d C o l o r a d o t ick fever. D. variabilis ( t he A m e r i c a n d o g t ick) r e p l a c e s D. andersoni in t h e e a s t e r n half of t h e U S A wi th foci a l so in n o r t h e r n I d a h o , e a s t e rn Wash ing ton , O r e g o n a n d California. This species h a s a m o r e u r b a n d i s t r ibu t ion t h a n D. andersoni, a n d a l t h o u g h adul t s feed on a var ie ty of large m a m m a l s , D. variabilis s e e m s t o p r e f e r wi ld c a r n i v o r e s a n d d o m e s t i c d o g s . T h e d i s e a s e r e l a t i o n s h i p s of D. variabilis a re s imilar to t hose of D. andersoni.

I n Asia , five species of Dermacentor c an b e found , usual ly paras i t iz ing wild pigs , b u t occas ional ly d o m e s t i c pigs a n d o t h e r l ivestock. T h e species a r e D. auratus ( found f rom Ind ia a n d N e p a l t o Malays ia ) , D. atrosignatus, D. compactus a n d D. steini (in S o u t h - E a s t

1003

A s i a , i n c l u d i n g I n d o n e s i a a n d B o r n e o , a n d D. taiwanensis ( i n T a i w a n a n d s o u t h e r n J a p a n ) . I n m o u n t a i n o u s a r e a s of A s i a , D. raskemensis, D. everestianus, D. pavlovskyi a n d D. montanus c an also b e f o u n d feeding o n wild a n d d o m e s t i c s h e e p a n d goa t s , yak , ca t t le a n d horses . In C e n t r a l A s i a a n d M o n g o l i a , D. sinicus a n d D. nuttalli a r e a s soc ia ted wi th c a m e l s , ca t t l e a n d h o r s e s . D. nuttalli is a n i m p o r t a n t v e c t o r of Rickettsia siberica. D. reticulatus, a pa r a s i t e of ho r se s , ca t t le , buffalo, s h e e p , goa t s , pigs , dogs a n d d o n k e y s , is found f rom I r e l a n d to Russ i a . D. marginatus, wh ich has s imi lar hos t p r ed i l ec t i ons , is found f rom F r a n c e a n d t h e I b e r i a n pen in su l a t o Afghan i s t an .

M o s t of t h e 147 Haemaphysalis s p e c i e s p r e s e n t w o r l d - w i d e d o n o t p a r a s i t i z e d o m e s t i c a n i m a l s . H o w e v e r , s o m e e x c e p t i o n s occur . I n t h e N e a r c t i c a n d N e o t r o p i c a l f auna l r e g i o n s , H. leporispalustris is a p a r a s i t e of b o t h wi ld a n d d o m e s t i c r a b b i t s . I n A f r i c a , H. silacea ( S o u t h A f r i c a ) , H. aciculifer ( f r o m C a m e r o o n t o E t h i o p i a a n d Z i m b a b w e ) a n d H. parmata ( f rom E t h i o p i a a n d K e n y a t h r o u g h to C e n t r a l Af r ica ) a r e all paras i tes of ca t t le . T h r o u g h o u t t h e Af ro - t rop ica l r eg ion , excep t in a r ea s wi th a n n u a l rainfall of less t h a n 500 m m , H. leachi pa ras i t i zes dogs a n d occas iona l ly cats , as wel l as larger ca rn ivores .

T h e n u m b e r of Haemaphysalis s p e c i e s p r e s e n t o n t h e I n d i a n s u b c o n t i n e n t a n d in A s i a is t o o n u m e r o u s fo r t h e s e t o b e d i s c u s s e d h e r e , b u t t w o s p e c i e s s h o u l d b e m e n t i o n e d . H. longicornis r e p r o d u c e s b isexual ly in t h e s o u t h e r n i s lands of J a p a n a n d in K o r e a . A p a r t h e n o g e n e t i c s t ra in of this species or ig ina t ing in t h e R u s s i a n P r i m o r ' y e a n d e a s t e r n C h i n a h a s b e e n i n t r o d u c e d i n t o A u s t r a l i a , t h e n o r t h i s l a n d of N e w Z e a l a n d , V a n u a t u , Fiji a n d o t h e r Paci f ic i s l ands . T h i s spec i e s is a s igni f icant p e s t of c a t t l e a n d h o r s e s , a n d is t h e ch ie f v e c t o r of Theileria orientalis. H. bispinosa is f o u n d in I n d i a , Sri L a n k a , N e p a l , B h u t a n a n d w e s t e r n B a n g l a d e s h , a n d feeds o n all f o rms of l ives tock. I m m a t u r e s will f e e d o n g o a t s , d o g s a n d c h i c k e n s . T h i s t i ck t r a n s m i t s Babesia s p p . t o cat t le , and B. gibsoni a n d B. motasi t o dogs a n d s h e e p , respect ively.

I n E u r o p e , i n c l u d i n g E n g l a n d a n d W a l e s , H. punctata is a p a r a s i t e of c a t t l e a n d sheep , a n d less f r equen t ly of goa t s , ho r se s , buffalo, d o n k e y s , c ame l s a n d pigs.

T h e g e n u s Hyalomma is d i s t r ibu ted ove r a n a r e a s t re tch ing f rom t h e M e d i t e r r a n e a n bas in e a s t w a r d s t o t h e I n d i a n s u b c o n t i n e n t a n d s o u t h w a r d s t h r o u g h o u t Afr ica . T h e s e ticks a re typical ly f o u n d a t low a l t i tudes in zones wi th long, h o t d ry seasons . O v e r half of t h e a p p r o x i m a t e l y 30 Hyalomma species feed o n camels , a n d four species (H. asiaticum, H. dromedarii, H. franchimi a n d H. schulzei) s u rv ive o n l y w h e r e c a m e l s a r e p r e s e n t , a l t h o u g h a d u l t s m a y a l s o b e f o u n d o n o t h e r l i v e s t o c k . W i t h t h e e x c e p t i o n of H. aegyptium, typical ly a p a r a s i t e of t o r t o i s e s , all t h e r e m a i n i n g spec ies of Hyalomma can b e seve re pa ras i t e s of l ivestock. In add i t i on t o t r ansmiss ion of d i sease agen t s such as b o v i n e a n d e q u i n e b a b e s i o s i s , a n d C r i m e a n - C o n g o h a e m o r r h a g i c fever , t h e l o n g m o u t h p a r t s of Hyalomma s pp . cause i n t ense w o u n d s a n d l amenes s . S o m e species cause paralys is , a n d s o m e p o p u l a t i o n s of H. truncatum cause swea t ing s ickness .

M o s t spec ie s of t h e g e n u s Ixodes a r e q u i t e specif ic in t h e i r f e e d i n g h a b i t s , u sua l l y paras i t iz ing b u r r o w - o r den - inhab i t i ng m a m m a l s . H o w e v e r , severa l non-specif ic feeders in t h e s u b g e n u s Ixodes of t h e Ixodes ricinus c o m p l e x of t icks h a v e g a i n e d i m p o r t a n c e recently, d u e t o t h e p o t e n t i a l for t h e s e t icks to t r a n s m i t t h e s p i r o c h e t e of L y m e d i sease . This d i sease in d o m e s t i c an ima l s was recen t ly r e v i e w e d by B u s h m i c h (10) .

I n N o r t h A m e r i c a , t h e s p e c i e s p r e s e n t a r e I. affinis, I. jellisoni, I. pacificus a n d I. scapularis ( t he b lack- legged t ick) . T h e s e last t w o species will feed o n a w ide var ie ty of l ivestock, as wel l as dogs a n d ca ts . I n S o u t h A m e r i c a , I. pararicinus is a ca t t l e f eede r in n o r t h e r n A r g e n t i n a a n d C o l o m b i a . T h e E u r a s i a n m e m b e r s of t h e I. ricinus g r o u p

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inc lude t h e n o m i n a t e species , of ten cal led t h e s h e e p t ick, I. persulcatus ( t he ta iga t ick) , I. gibbosus, I. kazakhstani, I. kashmiricus, I. pavlovskyi, I. nuttallianus, I. nipponensis a n d p e r h a p s I. sinensis. M e m b e r s of th is c o m p l e x t r a n s m i t a v a r i e t y of v i ruses ( t h o s e wh ich c a u s e louping- i l l , t i c k - b o r n e e n c e p h a l i t i s , C r i m e