Development of the Avian Embryo

Development of the Avian Embryo A Behavioural and Physiological Study

B. M. FREEMAN Houghton Poultry Research Station, Houghton, Huntingdon

and

Margaret A. VINCE Psychological Laboratory, Downing Street, Cambridge

LONDON

CHAPMAN AND HALL

First published 1974 by Chapman and Hall Ltd

11 New Fetter Lane, London EC4P 4EE

© 1974 B. M. Freeman and Margaret A. Vince Soj'tcover reprint of the hardcover 1st edition 1974

All rights reserved. No part of this book may be reprinted, or reproduced or utilized in

any form or by any electronic, mechanical or other means, now known or hereafter invented,

including photocopying and recording, or in any information storage and retrieval system,

without permission in writing from the Publisher.

Distributed in the U.S.A. by Halsted Press, a Division

of John Wiley & Son, Inc., New York

Library of Congress Catalog Card Number 74-4340

ISBN -13: 978-94-009-5712-1 e-ISBN-13:978-94-009-571 0-7 DOT: 10.1007/978-94-009-5710-7

Contents

Preface Acknowledgements List of Generic and Specific Names

PART ONE: BEHAVIOUR by Margaret A. Vince

page xiii xiv xv

1. Incubation Requirements 3 1.1 Introduction 3 1.2 Requirements of the embryo of the domestic fowl 4

Heat - Humidity - The gaseous environment - Egg position and change of position

1.3 Incubation requirements of other domestic species 5 1.4 Incubation in wild birds 6

Introduction - Incubation sites - Warming of the eggs -The problem of cooling - The continuity of attentiveness -Humidity - The gaseous environment - Egg shifting or turning - Hatching success

2. General Development, Postural Changes, Activity and Relationship between the Embryo and Other Structures within the Shell 20 2.1 Changes in size, posture and position in the domestic fowl

embryo during incubation 20 2.2 Embryonic activity during incubation in the domestic fowl 25

embryo Passive movements - Active, spontaneous movements -Significance of spontaneous activity

2.3 Hatching and emergence in the fowl 30 2.4 Structural and behavioural development in species other

than the fowl 32 Structural and behavioural development during the first two­thirds of incubation - Pre-hatching and hatching behaviour in species other than the fowl

v

CONTENTS

2.5 The characterization and scoring of embryonic movements 36 Terms used to describe embryonic activity - The quantifica-tion of embryonic motility

3. Vocalization and Communication in the Natural Situation 38 3.1 Species which can vocalize before hatching 38 3.2 Prerequisites for the onset of vocalization 38 3.3 Types of stimulation followed by embryonic vocalization 39 3.4 Effects of embryonic vocalization on the parent 40 3.5 Long-term effects of embryo/parent interaction 40 3.6 The earliest stage at which embryos become responsive to

parental calls 42

4. Effects of External Stimulation on Embryonic Activity, Rate of Development and Time of Hatching 43 4.1 Introduction 43 4.2 The synchronization of hatching in quail 43

Effects of stimulation on the time of hatching - Problems arising from changes in hatching time - Signals which have accelerating or retarding effects on neighbouring eggs - Effects of accelerating and retarding signals on the rate of development

4.3 Effects of accelerating and retarding stimulation in domesticated species 55

4.4 Effects of light in the fowl 56 4.5 Embryonic interactions in wild species 57 4.6 The embryonic response to stimulation 59

5. The Nervous System 62 5.1 Introduction 62 5.2 Development of activity in different parts of the nervous

system 62 Spontaneous activity - Responses of the brain to stimulation

5.3 Neural mechanisms mediating early motility in the embryo of the domestic fowl 66 The development of motor and sensory areas in the spinal cord -The part played by the brain in controlling periodic, random motility - Independence of periodic, random motility from sensory input - Areas of the brain which influence periodic random motility

vi

6.

CONTENTS

5.4 Neural mechanisms mediating pre-hatching and hatching

behaviour 71 Introduction - The spinal cord and pre-hatching behaviour - The midbrain and pre-hatching behaviour - The fore-brain and hatching - The cerebral EEG during hatching

5.5 Neural correlates of embryonic motility 73 Nervous activity in the spinal cord between 15 and 19 days-The polyneuronal burst discharge between days 5 and 20 -

Neural correlates of motility - Communication between different parts of the spinal cord

5.6 Inhibition 78 5.7 Sleep and arousal 80

The Development of Sensory Systems 84 6.1 Introduction 84 6.2 The non-visual response to light 85

Introduction - Evidence for a non-visual response to light in newly hatched pigeons - Evidence for a non-visual response to light in pigeon embryos

6.3 Tactile sensitivity 86 The onset of sensitivity - The type of movement evoked by tactile stimulation - Response decrements with repeated stimulation

6.4 Vestibular sensitivity 89 6.5 Proprioception 90 6.6 Hearing 91

Development of the auditory system - The age of onset of auditory sensitivity - The development of auditory sensitivity - The ontogeny of auditory discrimination

6.7 Taste 96 The sense of taste in birds - Development of a taste sense in the embryo

6.8 Vision 98 Development of the visual system - Response to light in the domestic fowl - Colour vision - The behavioural response to light - Effects of previous experience on the responsiveness of the visual system - A comparative view of the onset of visual function - Effects of light on the embryo in ovo

6.9 Olfaction 102 The olfactory sense in birds - Development of olfaction in the embryo

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CONTENTS

7. Conditioning of the Chick Embryo and Conclusions to 104 Chapters 1-7

8. The Newly Hatched Bird 108 8.1 Introduction 108 8.2 Requirements of the neonate 109

Warming and cooling - Righting and standing - Social attachments in young birds - Feeding behaviour - Oiling and preening

8.3 What is new in the life of the neonate? 113 8.4 Effects of new environmental stimuli on neural

mechanisms 114 8.5 Conclusions 116

PART TWO: PHYSIOLOGY by B. M. Freeman

9. Gaseous Exchange and Oxygenation of the Embryo 119 9.1 Gross oxygen consumption and carbon dioxide

production 119 9.2 The shell and the chorio-allantois 123

Structure of the shell - Development and structure of the chorio-allantois

9.3 Physical aspects of gaseous exchange 130 Oxygen - Carbon dioxide - The air space - Maximum gaseous flux during incubation

9.4 The blood and vascular system 138 Red blood cells - Blood volume and pressure - The heart­Haemoglobins - Oxygen affinity of haemoglobins - Blood gases

9.5 Efficiency of the chorio-allantois as a surface for gaseous exchange 154

9.6 Effects of altitude 156

10. Nutrition and Utilization of Albumen and Yolk 160 10.1 Nutrition of the developing bird 160

Essential amino acids - Carbohydrate - Essential fatty acids - Minerals, trace elements and vitamins - Energy sources

10.2 Gross composition of the egg and the changes during incubation 163

10.3 The albumen and its utilization 164 Composition - Absorption - Functions

viii

CONTENTS

10.4 The yolk and its utilization 168 Composition - The yolk sac membrane - Utilization of yolk

10.5 Energy metabolism 183 10.6 The sub-embryonic fluid 184

11. Acid-base Balance 186

12.

11.1 Blood pH and PC02 186 11.2 Plasma bicarbonate 186 11.3 The compensation of respiratory acidosis 187

The sources of bicarbonate - The possible role of the kidney in excreting bicarbonate

Excretion and Water Balance 12.1 Introduction 12.2 The development of the excretory system

The pronephros - The mesonephros - The metanephros 12.3 Synthesis of nitrogenous excretory products

Metabolism of the amino group - Urea - Uric acid 12.4 The pattern of excretion during development

Excretory products - The organs of excretion 12.5 The allantoic sac

Storage of excretory products - Active transport by the allantoic endoderm

12.6 Water balance Sources of water - Factors affecting water loss - Gross movements of water within the egg - Conservation of water

191 191 191

194

198

200

204

13. Hormones in Development 208 13.1 General introduction 208 13.2 Thyroid hormones 208

Development of the thyroid glands - Synthesis and secretion of hormones - Metabolic effects of the thyroid hormones-The thyroid and hatching

13.3 Parathyroid hormone and calcitonin 213 Introduction - Development of the parathyroids and ultimo­branchial bodies - Secretion of parathormone and calcitonin - Significance in development

13.4 Adrenal hormones 216 Development of the adrenal glands - Synthesis and secretion of adrenal hormones - Significance of adrenal cortical hor­mones in development - Significance of adrenal medullary hormones in development

* ~

CONTENTS

13.5 Pancreatic hormones 223 Introduction - Development of the endocrine pancreas -Structure and secretion of insulin and glucagon - Role of insulin in development - Role of glucagon in development

13.6 Gonadal hormones 226 Development of the genital system - Synthesis and secretion of gonadal hormones - Significance in development

13.7 Hypophyseal hormones 232 Introduction - Development of the hypophysis - Secretion of hormones by the pars distalis - Significance of hypo-physeal hormones in development

13.8 Glands of uncertain endocrine status 235 Introduction - Bursa of Fabricius - The pineal gland

14. Mobilization and Utilization of Calcium Stores 237 14.1 Physiological aspects of calcium transport 237 14.2 The sources of calcium and gross changes during

incubation 237 14.3 The role of the chorio-allantois in calcium transport 239

Solubilization of calcium - Active transport by the chorionic ectoderm

14.4 Changes following calcium resorption 246 The shell - Plasma calcium

14.5 Mineralization of the bones 247

15. Physiology of Hatching 249 15.1 General introduction 249 15.2 Pulmonary respiration 249

Introduction - The respiratory system - The onset of breathing: the pulmonary stimulus - The development of the breathing pattern

15.3 Circulatory and associated changes 254 15.4 Pipping 256 15.5 Active hatching 257 15.6 Withdrawal and fate of the yolk sac 258 15.7 Oxygenation and energy metabolism during hatching 258

16. The Neonate 261 16.1 Introduction 261 16.2 Thermoregulation 261

Ontogeny of thermoregulation - Mechanisms of thermo­regulation

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CONTENTS

16.3 The alimentary tract 16.4 Immunological competence 16.5 Concluding remarks

263 264 265

Appendix 1: Chronology of development in the domestic fowl 269 Appendix 2: Development of the chick embryo in relation to the

References

Index

shell, yolk, albumen and extra-embryonic membranes by Beryl Tolhurst 277

xi

295

351

Preface

In this book we have described the major events of embryonic development and considered the underlying mechanisms which result in the production of a viable hatchling. We have, as the subtitle of the book indicates, con­centrated on behavioural and physiological topics: it is not our purpose to consider the early embryology of the bird - which is adequately covered by other texts - but we have included morphogenetic information where appropriate.

The form of the book was dictated by a belief that interest in this aspect of development is not confined to embryologists, biochemists and physiolo­gists. Therefore after describing the conditions in which the egg normally develops we have considered first the whole embryo: what it is like at different stages, what it does, how it gets from one position to another within the shell and how, later, it comes to interact with the wider environ­ment of the nest. Only after this have we considered the development of the nervous and sensory mechanisms on which this transformation depends and on the problem of the level of behavioural maturity with which the chick emerges from the egg.

With the main lines of development described we have, in the second part of the book, turned to a detailed consideration of the physiology of development: ranging from what may be conveniently described as the 'life-support' systems - gaseous exchange, provision of energy, etc. - to the role of hormones in avian development.

Our approach, then, has followed the lines most frequently taken in research: to present first the problem in simple everyday language and then to consider at increasing levels of complexity the solution of that problem. We have indicated where the explanation of the solution remains incomplete in the hope of encouraging further research.

The book ends with two appendices highlighting and illustrating the major points in avian development as exemplified by the domestic fowl. We are greatly indebted to Mrs. Beryl Tolhurst for undertaking the prepara­tion of the second appendix.

Finally readers may find it helpful to know that the literature survey was completed in the late autumn of 1973.

February 1974 xiii

M.A.V. B.M.F.

Acknowledgements

Many individuals have variously helped us in the preparation of this book. We particularly wish to acknowledge our immediate colleagues R. E. Adkins, Mrs. J. Bellis, Mrs. F. Benson, S. Hodgson, Mrs. M. Kelly, Mrs. M. Reader, Mrs. M. G. Tebbit and Mrs. B. Tolhurst. Several people have read parts of the manuscript and have made valuable suggestions for its improvement whilst others have, with great generosity, specially pre­pared material. These include Dr. P. P. G. Bateson, Dr. J. R. Coleman, Dr. M. A. Corner, Miss J. R. Crooks, Dr. G. Gottlieb, Dr. M. Harth, Dr. R. P. Heckey, Dr. D. R. Langslow, Dr. A. Owczarzak, Dr. R. P. Oppenheim, Dr. R. R. Provine, Dr. P. C. M. Simons, Professor K. Simkiss and Dr. D. Tolhurst.

In addition we are indebted for encouragement and support to the Director and Governing Body of the Houghton Poultry Research Station (B.M.F.) and to the Medical Research Council and also Professor O. L. Zangwill of the Cambridge Psychological Laboratory (M.A.V.)

xiv

List of Generic and Specific Names

In the text the various avian species are referred to only by their common names: their generic and specific names are recorded here.

Albatross, royal Blackbird Blackbird, red-winged Booby, red-footed Bulbul Bullfinch Coot, European Coot, American Cormorant Courser, double-banded Cuckoo Dove, ring Duck, mallard} Duck, Pekin Duck, pintail Duck, redhead Duck, runner Duck, wood Emu Fowl, Burmese red jungle Fowl, domestic Fowl, guinea Fowl, Mallee Fowl, pea Gannet Godwit, black-tailed Goose, domestic

xv

Diomedia epomophora Turdus merula Agelaius phoeniceus Sula sula Pycnonotus cafer Pyrrhula pyrrhula Fulica atra Fulica americana Phalacrocorax carbo Rhinoptilus africanus Eudunamys scolopacea Streptopelia risoria

Anas platyrhynchos

Anas acuta Aytha americana Anas platyrhynchos Aix sponsa Dromaius novaehollandiae Gallus gallus Gallus domesticus Numida meleagris Leipoa ocellata Pavo cristatus Sula bassana Limosa limosa Anser anser

LIST OF GENERIC AND SPECIFIC NAMES

Grackle Grebe, greater crested Guillemot Guillemot, pigeon Gull, blackheaded Gull, Franklin's Gull, herring Gull, laughing Gull, western Hawks Heron, grey Kittiwake Kiwi, common Lapwing Lapwing, yellow-wattled Magpie Ostrich Owl, tawny Owl, Ural Partridge Partridge, chukar Penguin Penguin, Adele Pheasant, ring-necked Pigeon Puffin Quail, bobwhite Quail, Japanese Rails Redstart Rhea Shearwater, slender-billed Sparrow, house Sparrow, song Sparrow, tree Sparrow, white-crowned Starling Swan, mute Swift, palm Teal

Quiscalus quiscala Podiceps cristatus Uria aalge Cepphus columba Larus ridibundus Larus pipixcan Larus argentatus Larus atricilla Larus occidentalis wymani Accipiter spp Ardea cinerea Larus tridactylus Apteryx australis Vanellus vanellus Vanellus malabaricus Pica pica Struthio camelus Strix aluco Strix uralensis Perdix perdix Alectoris graeca Spheniscus spp or Aptenodytes spp Pygoscelis adeliae Phasianus colchicus Columba livia Fratercula arctica Colinus virginianus Coturnix coturnix japonica Rallus spp Phoenicurus phoenicurus Rhea americana Puffinus tenuirostris Passer domesticus Melospiza melodia Passer montanus Zonotrichia leucophrys gambelii Sturnus vulgaris Cygnus olor Cypsiurus parvus Anas crecca

xvi

LIST OF GENERIC AND SPECIFIC NAMES

Teal, blue-winged Tern Tern, least Thrush, song Titmouse, blue Titmouse, coal Titmouse, great Titmouse, marsh Turkey, brush Turkey, domestic Turnstone Turtle dove, ringed Woodcock, American Wren Wren, Eastern house

xvii

Anas discors Sterna cas pia Sterna albifrons Turdus philomelos Parus caeruleus Parus ater Parus major . Parus palustris Alectura lathami Meleagris gallopavo Arenaria inter pres Streptopelia risoria Philohela minor Troglodytes troglodytes Troglodytes aedon