97354553 Crocodiles Biology Husbandry and Diseases (1)

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

1

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5

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

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

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

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Crocodiles

Biology, Husbandry and Diseases

Crocodiles

Biology, Husbandry and Diseases

F.W. Huchzermeyer

Onderstepoort Veterinary Institute,South Africa

CABI Publishing

CABI Publishing is a division of CAB International

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

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

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

Library of Congress Cataloging-in-Publication Data

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

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

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

SF515.5.C75 H83 2003639.3982--dc21

2002013734

ISBN 0 85199 656 6

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

Contents

Foreword vii

Disclaimer viii

Introduction ix

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

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

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

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

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

v

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

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

References 292

Index 323

vi Contents

Foreword

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

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

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

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

Professor Harry MesselChairman, CSG

vii

Disclaimer

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

viii

Introduction

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

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

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

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

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

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

The past and present directors of the OVI, Dr D.W. Verwoerd, Dr G.R. Thomson, Dr S.T.Cornelius and Dr F.T. Potgieter, are thanked for the provision of an ofce for my use andcontinued access to the Institutes infrastructure since my retirement, as well as for theircontinued interest in my work. The secretary of the now also defunct Pathology Section ofthe OVI, Mrs Mara Stoltz, has always been at hand to solve computer and program problems

ix

most speedily and efciently, and Mr D. Swanepoel of the Institutes library and his staffhave been most helpful in trying to procure even the most obscure items of literature.

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

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

F.W. HuchzermeyerPretoria

June 2002

x Introduction

The Species of Crocodilians

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

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

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

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

Crocodiles

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

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

snouted crocodile (Fig. 1.1)

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

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

crocodile AustraliaC. johnsoni Johnstons crocodile AustraliaC. palustris Mugger (Fig. 1.2) Indian

subcontinentC. siamensis Siamese crocodile AsiaC. mindorensis Philippine Philippines

crocodileC. novaeguineae New Guinea New Guinea

crocodileC. raninus Bornean crocodile Borneo (see

Ross, 1990; Rosset al., 1998)

Chapter 1Crocodiles and Alligators

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

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

The wide distribution of C. porosus in the

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

2 Chapter 1

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

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

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

The genus Osteolaemus:O. tetraspis Dwarf crocodile Africa

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

The genus Tomistoma:T. schlegelii False gharial Asia

(Fig. 1.5)

Alligators

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

Crocodiles and Alligators 3

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

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

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

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

The genus Caiman:C. latirostris Broad-snouted South

caiman AmericaC. crocodilus Common caiman South

(Fig. 1.6) America

4 Chapter 1

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

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

The genus Palaeosuchus:P. palpebrosus Cuviers dwarf South

caiman AmericaP. trigonatus Schneiders dwarf South

caiman America

The genus Melanosuchus:M. niger Black caiman South

America

Gharials

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

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

continent

Differences between crocodiles andalligators

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

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

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

Wild or captive?

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

Wild

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


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

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

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

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

Ranched

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

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

Farmed

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

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

Crocodilian Anatomy

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

6 Chapter 1

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

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

The skeleton

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

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

Vertebrae

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

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


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

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

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

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

The skin

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

8 Chapter 1

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

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

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

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

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

Identification

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

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


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

The muscles

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

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

10 Chapter 1

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

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

The respiratory system

Respiratory tract

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

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


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

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

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

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

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

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

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

12 Chapter 1

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

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

The digestive system

Teeth

Crocodilian teeth are pointed, very sharp andare constantly replaced throughout life. Thereplacement rate varies with the growth rateand slows down as the animal becomes older.In small American alligators (

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

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

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

StomachThe stomach lies to the left, immediatelybehind the left lobe of the liver and the pos-terior transverse membrane. Its junction withthe oesophagus (cardia) is defined by a well-developed sphincter muscle. The pyloric exitalso lies in the cranial aspect, slightly to theright of the cardia, and is defined by a smallbulbus, the pyloric antrum, which in turnopens into the duodenum (Figs 1.221.24).The entire interior surface of the stomach is

14 Chapter 1

Fig. 1.19. Dentition of a juvenile Nile crocodile.

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

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

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

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


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

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

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

Intestine

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

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

16 Chapter 1

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

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

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

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

Pancreas

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

Liver

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


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

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

18 Chapter 1

Fig. 1.27. Kidney of a Nile crocodile.

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

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

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

The urinary system

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

gle fold in the African dwarf crocodile and inmultiple folds in other crocodile species.These folds continue to grow as the crocodilegrows. These multiple folds give the kidneyof the Nile crocodile a triangular shape ontransverse section, while the kidney of theAfrican dwarf crocodile appears flattened.The folding patterns appear to be speciesspecific (Figs 1.271.29).

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

The reproductive organs

Female

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


Fig. 1.28. Kidney of Crocodylus palustris.

Fig. 1.29. Kidney of Caiman crocodilus.

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

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

Male

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

20 Chapter 1

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

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

The endocrine organs

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

Thymus

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


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

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

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

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

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

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

Adrenals

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

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

Pancreas and intestinal tract

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

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

The circulatory system and blood cells

Heart

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

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

22 Chapter 1

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

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

1997). The foramen of Panizza is located atthe base of the heart within the aortic archvalves (Webb, 1979), and the anastomosis is ashort vessel connecting the two aortic arches.In American alligators of length 12 m, theforamen of Panizza had a diameter of


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

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

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

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

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

Tonsils

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

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

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

external jugular vein just proximal to thejuncture with the subclavian vein. Thelymph from the caudal and pelvic regions ispumped by the posterior lymph hearts intosmall vessels which empty into the pelvicvenous plexus. These lymph hearts are sin-gle-chambered muscular structures, measur-ing 3 57 mm in alligators 5075 cm long.They are situated superficially at the junctionof the hind limb with the pelvis, below thesuperficial layer of the deep fascia in thetriangle formed by the m. longissimuscaudae, the crest of the ileum and the m.flexor caudae.

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

Blood volume

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

Blood cells

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

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

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

24 Chapter 1

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

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

HETEROPHILS. Heterophils, or type I granulo-cytes (Canfield, 1985), are round to oval cellswith mean diameters of 17.3 m and distinctsmooth cytoplasmic borders. The nuclei arelenticular, oval or, rarely, bilobed, withindistinctly clumped purple chromatin,usually eccentrically located at one pole ofthe cell. The cytoplasm contains abundant,34 m long, fusiform refractile granules,occasionally arranged in perinuclear radi-ally symmetrical star-like configurations(Fig. 1.36).

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

nent coarsely clumped chromatin and verysharply demarcated borders, usually locatedat one pole of the cell, often causing a slightoutward bulge of the cell outline. Somenuclei are located more centrally. The pale-blue, smooth cytoplasm is visible only as athin rim surrounding the many bright pinkplump granules measuring 23 m (Fig.1.37). Often a few granules are present on theface of the nucleus.

BASOPHILS. Basophils, or type III granulocytes(Canfield, 1985), are round cells with irregu-lar external cobblestone contours and adiameter of 12.8 m. Abundant, dark-purpleto purplish-red, round granules measuring0.10.5 m pack the cell to the point wherethey frequently obscure the nucleus.Sometimes the granules are arranged in aperipheral rim with a central cluster over thenucleus.

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


Table 1.1. Erythrocyte dimensions (means).Species Length (m) Width (m) ReferencesAlligator mississippiensis 14.822.0 8.112.8 1A. mississippiensis 17.5 9.7 4A. mississippiensis 23.2 12.1 5A. mississippiensis 23.0 14.3 6Caiman latirostris 21.3 10.9 2C. latirostris 19.5 10.8 2Caiman crocodilus 23.8 13.3 3A. mississippiensis 20.8 11.1 3C. latirostris 17.0 9.0 7C. crocodilus 17.0 9.0 7

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

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

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

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

26 Chapter 1

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

Fig. 1.37. Two eosinophils, Nile crocodile.

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

Details of crocodilian haematology are givenin Chapter 2.

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

The nervous system and sensory organs

Brain

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

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

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

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

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


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

Ear

The ear has two sensory functions, hearingand spatial orientation.

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

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

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

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

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

Fat storage

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

28 Chapter 1

Table 1.2. The chromosomes of crocodiles.

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

Species 2n NF 2n NF 2n

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

2n, Diploid number; NF, fundamental number.

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

Somatic fat

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


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

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

The egg

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

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

30 Chapter 1

Fig. 1.41. Abdominal fat body of Osteolaemus tetraspis.

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

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

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

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

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

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

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

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


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

Egg length (cm) 7.257.57Egg width (cm) 4.0794.47Egg mass (g) 68.8586.0Length/width ratio 1.6841.766Shell thickness (mm) 0.430.45Shell density 2.102.14Shell mass (g) 7.398.89Shell mass (% of egg mass) 10.5711.14Yolk mass (g) 31.936.2Yolk mass (% of egg mass) 4448Membrane mass (% of egg mass) 1.061.08

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

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

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

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

Crocodilian Physiology

Yolk-sac resorption

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

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

32 Chapter 1

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

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

There do not appear to be any reportsabout the time it takes for the yolk-sac to becompletely resorbed under normal circum-stances. It is probably 34 weeks. This wouldbe temperature dependent, with a slower rateof resorption at lower (suboptimal) tempera-tures. Infection of the vitello-intestinal ductcan lead to its closure and, in this case, theyolk-sac will remain unresorbed (see p. 143).

Sex differentiation

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

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

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

Growth

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


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

Metabolic rate

The metabolic rate of crocodiles depends ontheir size and activity, and the temperature(Baldwin et al., 1995; Munns et al., 1998). At28C a 70 kg American alligator producesabout 72 kcal day1, i.e. about 4% of that of aperson of equal mass. At 32C the rate dou-bles. However, a hatchling at 28C has half thehuman metabolic rate (Coulson et al., 1989).

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

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

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

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

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

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

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

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

34 Chapter 1

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

Locomotion

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

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


Table 1.4. Agelengthweight relations of marked and released American alligators (McIlhenny, 1934).Age Sex Length (m) Weight (kg)1 day 0.230.24 0.0710.08532 days 0.340.3710 months 0.45 0.2412 months 0.67 1.8415 months 0.690.81 1.932.3720 months 0.75 1.4121 months 0.790.82 1.641.842 years 1 month 0.991.20 4.355.642 years 8 months 1.091.14 3.664.543 years 2 months 1.271.50 7.839.573 years 10 months 1.181.73 5.0613.34 years 2 months 1.581.71 8.8517.56 years Female 1.611.75 13.617.36 years Male 1.752.39 18.956.69 years Female 2.012.08 38.240.49 years Male 2.352.68 57.067.610 years Female 2.172.21 49.952.810 years Male 2.692.87 80.7132.211 years Male 2.643.07 76.9160.6

Table 1.5. Agelengthweight relations in farmed Nile crocodiles (Loveridge and Blake, 1972).Age Sex N Length (m) Weight (kg)1920 months Female 5 0.911.18 1.755.332 months Male 4 1.181.33 5.58.93233 months Female 4 0.981.40 3.29.74647 months Female 2 1.181.75 5.925.45154 months Female 2 1.91 32.633.5

Female 2 2.82 125Male 1 3.92 312

Table 1.6. Agelengthweight relations of twoAfrican dwarf crocodiles reared in captivity(Helfenberger, 1982).Age Length (m) Weight (kg)10 weeks 0.260.31 0.080.146 months 0.360.41 0.230.401 year 0.63 1.291.402 years 0.770.78 2.012.70

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

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

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

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

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

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

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

Digestion

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

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

Reduction

In the stomach the swallowed food isexposed to the action of hydrochloric acid(HCl) and peptic proteolysis. Their secretionis stimulated by the presence of the food,while penetration into the food is facilitatedby the puncturing and chewing that hastaken place before swallowing. Gastric pHdrops as low as 1.2 and in fasting animalseven stays below 2.5 (Diefenbach, 1975a).Gastric contractions mixing the stomach con-tents take place 23 times per minute whenthe stomach is full (Diefenbach, 1975b). At30C complete emptying of the stomach took99 h on average and at 15C 315 h(Diefenbach, 1975b). However, Kanui et al.(1991) recorded gastrointestinal passagetimes in 12-week-old Nile crocodiles as 35 hat 30C and 44 h at 25C.

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

36 Chapter 1

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

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

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

Assimilation

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

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

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

Normal oral flora

Identification of the oral flora of crocodiliansis important for the treatment of bitewounds. The work done on American alliga-tors can be taken as representative for allcrocodilian species. Doering et al. (1971)isolated Clostridium spp., Citrobacter,Enterococcus spp. and others from twoAmerican alligators. Flandry et al. (1989)examined ten alligators from three differentlocations and found both aerobic and anaer-obic bacteria in all of them, but isolated fungifrom only seven individuals (Tables 1.71.9).

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


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

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

Clostridium bifermentans 3clostridioforme 1limosum 1sordellii 2tetani 1

Fusobacterium nucleatum 2varium 3

Peptococcus magnus 1prevotii 3

N, number of isolates.

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

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

Normal intestinal flora

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

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

38 Chapter 1

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

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

sp. 1Proteus vulgaris 7Pseudomonas cepacia 2

fluorescens 1pickettii 1

Serratia odorifera 1


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

Aspergillus flavipes 1Candida humicola 1

lipolytica 1rugosa 2zeylansides 1sp. 1

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

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

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

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

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

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

Respiration

Ventilation

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


Table 1.11. Aerobic bacterial intestinal flora of African dwarf crocodiles (Huchzermeyer et al., 2000).Genus Species N (1993) N (1995)Alcaligenes faecalis 2Bacillus alvei 1

cereus 11 4circulans 1coagulans 1

Citrobacter amalonaticus 1freundii 3

Dermacoccus nishinomyaensis 1Enterobacter agglomerans 1 1

cloacae 7gergoviae 1

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

Escherichia coli 8Flavobacterium balustinum 1

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

epidermidis 1xylosus 2

Streptococcus salivarius 1Streptomyces sp. 1


Respiratory rateRespiration takes place in cycles of two tothree rapid movements followed by a longerpause (Gans and Clark, 1976). The respiratoryrate depends on the size of the animal,decreasing with increasing body mass (Gansand Clark, 1976). It is also influenced by tem-perature, increasing with increasing bodytemperature (Campos, 1964; Smith, 1976),with lower rates during warming than duringcooling (Smith, 1976). There appeared to be alow correlation between the metabolic rateand the respiratory rate (Huggins et al., 1971).Respiratory rates for different sized crocodilesare given in Table 1.13. The respiratory rate of123 crocodiles of 27.4 min1 reported bySigler (1991) falls entirely outside the range ofall the other observations and may possiblyinclude pharyngeal (gular) movements.

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

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

Oxygen consumptionIn both American alligators and Nile croco-diles, the oxygen consumption of inactiveanimals was found to increase as the temper-ature rose. However, in Nile crocodiles itwas found to decrease between 25 and 30Cand then rise again steeply to 35C (Brownand Loveridge, 1981; Lewis and Gatten,1985). The decrease is seen as an adaptationto nocturnal activity, which is usually atlower temperatures (Brown and Loveridge,1981). In the American alligator values rang-ing from 0.08 to 0.2 ml g1 h1 correspond

40 Chapter 1

Table 1.12. Fungal intestinal flora of African dwarf crocodiles (Huchzermeyer et al., 2000).Genus Species N (1993) N (1995)Acremonium sp. 1Arthrinium sp. 1Aspergillus clavatus 5

flavus 2niger 2

Beauveria sp. 3Candida guillermondii 2 2

krusei 1Chrysosporium sp. 3Cryptococcus lipolytica 3 3

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

capitatum 1


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

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

Acidbase balance

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

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

Excretion

Fasting crocodiles and alligators produceapproximately equal quantities of ammonia

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

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

Responses to high salinity

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


Table 1.13. Respiratory rates of crocodiles.

Species Mass (kg) Breaths per min Temperature (C) ReferenceCaiman crocodilus 0.18 0.58 2325 1

0.29 0.63 10.65 0.57 14.8 0.25 14.8 0.14 15.0 0.17 1

Alligator mississippiensis 1.158.78 3.3a:1.5b 20.461.31 0.394.95 2325 3

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

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

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

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

Reproduction

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

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

Hormonal control

The hormonal control of the reproductivecycle and factors influencing this control

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

OvulationAll follicles are normally ovulated togetherover a period of a few hours (personal com-munication, V.A. Lance, San Diego, 2000),but acc

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97354553 Crocodiles Biology Husbandry and Diseases (1)