Reproductive Biology of the Crocodylia

By Valentine Lance

Reproductive Biology of the Crocodylia is based on over 40 years of research on global crocodiles, alligators and caimans. It brings together data and information previously scattered across publications to synthesize knowledge on the history, ecology, physiology and anatomy of crocodilians. The book provides a comprehensive look at the physiology, current taxonomy, ecology and sexual maturity factors of these reptiles. It then delves into the anatomy and cycles of both male and female reproduction systems, including nesting and incubation, temperature-dependent sex determination, and sex ratios across various species populations.

Finally, the book focuses on conservation efforts to protect the reproductive cycle, taking factors such as pollution, climate change, and human disruption into consideration. It is an ideal resource for wildlife biologists and herpetologists seeking up-to-date and thorough research data on conservation efforts. It will also be helpful for exotic animal veterinarians, zookeepers, and alligator or crocodile farmers.

• Focuses on crocodilian reproduction and how it is impacted by seasons, social interactions, pollution, and more
• Provides a thorough overview by a globally recognized expert on crocodilian reproduction and endocrinology
• Explores conservation efforts and offers insights for protecting crocodilian reproduction cycles against current factors, including pollution, environmental effects and human interference

• Language: English
• Publisher: Academic Press
• Release date: Dec 4, 2021
• ISBN: 9780128218075

Valentine Lance

Dr. Valentine Lance is a retired researcher and professor who taught in the Graduate School of Public Health at San Diego State University, California, USA. He previously served for 16 years as a senior scientist and the Head of Endocrinology in the Research Department at the San Diego Zoo. Dr. Lance received his master's degree in biology from the College of William and Mary, Virgina, USA, and later his PhD in zoology from the University of Hong Kong, Hong Kong. He has conducted decades of research on reproductive biology, specifically on the physiology and endocrinology of reptiles such as crocodiles, alligators, and turtle species. He currently serves as Vice Chairman for Science for the Crocodile Specialist Group of SSC/IUCN and Advisor to the Crocodilian Advisory Group (TAG) of the AAZPA.

Book preview

Front Cover for Reproductive Biology of the Crocodylia - 1st edition - by Valentine Lance

Reproductive Biology of the Crocodylia

Valentine Lance

Vice Chairman for Science for the Crocodile Specialist Group of SSC/IUCN and Advisor to the Crocodilian Advisory Group (TAG) of the AAZPA, California, United States

Table of Contents

Cover image

Title page

Copyright

Acknowledgments

Introduction

Chapter 1. Phylogeny and fossil history

Abstract

Chapter 2. History and growth of knowledge

Abstract

Content

Early anatomical studies

Chapter 3. Life history and ecology

Abstract

Contents

Multiple paternity

Nest-site fidelity

Some unique and unusual features of crocodylians or some crocodilian oddities

Chapter 4. Growth, sexual maturity, and senescence

Abstract

Contents

Senescence

Sexual maturity

Chapter 5. Anatomy of the male reproductive tract

Abstract

Chapter 6. Male reproductive cycle

Abstract

Chapter 7. Anatomy of the female reproductive tract

Abstract

Contents

The ovary

The oviducts

Sperm storage

Chapter 8. Female reproductive cycle

Abstract

Contents

Courtship behavior

Vitellogenesis

Nesting

Eggs

Clutch size

Chapter 9. Sex determination, embryos, and teratology

Abstract

Chapter 10. Captive breeding, farming, and ranching

Abstract

Content

Double clutches

Chapter 11. Environmental contamination

Abstract

Content

Heavy metals

Chapter 12. Conservation

Abstract

References

Index

Copyright

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Acknowledgments

A large number of colleagues have helped me at many different times, in many different ways, and in many different locations, to collect the information included in this book. Crocodile researchers are, in my experience, the friendliest group of people I have ever had the pleasure to work with, and who are more than happy to share any information (maybe everyone else thinks they are a little strange and so are happy to find someone who will listen to them). First, late Prof. Roland Coulson, for his friendship, unstinting help, and advice, and for the example of his clear and elegant prose: anyone with even the slightest interest in alligator biology who was fortunate enough to visit with the Prof in his laboratory in New Orleans was given a warm welcome and invited to share whatever meal he was cooking at the time (often red beans and rice), and to listen to his yarns—a wonderful story-teller, an unrepentant anglophile, and a true gentleman in every sense of the word. He knew London (the city of my birth, better than I did), where he lived during World War II and completed PhD in biochemistry from the University of London while in the British military (for a brief biography, see Dessauer, 1989); Ted Joanen, a pioneer in field research on alligators, alligator farming, and alligator biology, and the individual who first introduced the then-controversial concept of the harvesting of wild alligators as a renewable resource. His support and help when I first ventured into this area of research were critical. Without the long hours, he volunteered to help catch alligators when he could have been home in bed, the work described in the pages that follow would not have been possible; Dr. Ruth Elsey, formerly my student and now one of the world’s experts on alligator management and biology, a long-term collaborator on some pioneering experiments, an exacting editor, and a good and true friend; Dr. Kent Vliet, a friend for more than 40 years (has it really been that long), a crocodilophile extraordinaire. Kent’s unrelenting pursuit of every last possible piece of information on crocodilians has resulted in a superb collection of more than 10,000 articles that have some mention of caimans, alligators, crocodiles, and fossil crocodilians. In addition, I would like to thank Dr. Brandon Moore for access to his published and unpublished materials on the detailed functional anatomy of the crocodilian intromittent organ, or phallus. A number of his photographs are included in this book.

I would also like to thank Jeff Lang, a friend for many years, for keeping me honest—a rigorous and exacting scientist, a superb field biologist, a world authority on crocodiles, and especially the gharial (Gavialis gangeticus), a crocodilian he has studied in India for many years, and a crocodile that he discovered does not behave as other crocodiles. My visit with him on the Chambal River (a tributary of the river Ganges) in Uttar Pradesh, India, where he has established a research post in an isolated village that seems little changed from some hundreds of years ago, is an experience I treasure.

In the years of working with alligators I have been fortunate to meet with, and establish lasting friendships, with an extraordinary group of people, namely, the Crocodile Specialist Group, or CSG, of the IUCN (International Union for the Conservation of Nature). The CSG is a group of volunteers with a passion for crocodiles that meets every 2 years, usually in a country with healthy crocodilian populations, to discuss the latest information on the management of wild populations, farming, research, veterinary science, and trade in crocodile products (their parties are famous). A simple e-mail will get an instant response to any odd question on crocodilians. Among those whom I pester with frequent questions is Dr. Chris Brochu, paleontologist and world expert on crocodiles in the fossil record. He must live attached to his computer, for it seems that any time day or night I send a question, I get an instant response. Charlie Manolis, who has worked with the notorious man-eater (Crocodylus porosus) and the Freshwater Australian crocodile (Crocodylus johnstoni) of northern Australia for more than 30 years and is a great source of information, always freely given. Grahame Webb, chairman of the CSG, who, despite his almost incomprehensible Australian accent, has advocated strongly and diplomatically (and successfully) on the international stage for the conservation and sustainable use of crocodiles. In addition, my colleagues of Proyecto Yacare, Carlos Piña, Alba and Alejandro Larriera, Pablo Siroski, and Melina Simonici, in Sante Fe, Argentina, have taken me along on their field research with the gauchos and have welcomed me into their homes. My Brazilian colleagues, especially Luciano Verdade and the indefatigable Zilca Campos—both of whom have taken care of me during my many trips to Brazil. An additional and heartfelt thanks is due to Zilca for nursing me through a bout of pneumonia I contracted in the tropics of Brazil (I think it was due to the extreme air-conditioning at a crocodile meeting in Manaus I attended shortly after I got off the plane from the United States).

A large number of students and volunteers helped both in the laboratory and the field, among whom, Lori Jackintell, Willow Gabriel, and Lisa Morici completed master’s degrees on alligators.

I would also like to thank Dr. Victoria Mattey for a superb translation from the Russian of the paper by Sovienski (1889), and my daughter Kio for her help in making my translations from papers published in Spanish a little more accurate. Also, thanks to Drs. Sterling Nesbitt and Michele Stocker, professional paleontologists, for their advice on crocodiles in the fossil record and on the evolution of the Crocodylia.

Introduction

It is probably true that any treatise on the nature and habits of an animal will reflect the prejudices of the author to the partial exclusion of the opinions of others. In a sense that is proper for it represents the authors’ experience rather than hearsay.

Roland A. Coulson (Metabolic Rate, Nutrition, and Growth of the Alligator, unpublished report)

I first encountered alligators in 1979 on my first visit to the Rockefeller Wildlife Refuge in Southwest Louisiana, like most who have never seen an alligator up close, was intimidated by the sheer size of the animal and, like most, knew nothing of its anatomy. My first dissection was an embarrassment. A colleague who asked for some pancreatic tissue told me I had sent him fat. What I had identified as the pancreas turned out to be the abdominal fat body. To me, this unique abdominal organ, found only in crocodilians, looked like the pancreas of a shark. Later a colleague, Dr. Alison Buchan, came to the Rockefeller Refuge and corrected me as to the correct location of the alligator pancreas (Buchan et al., 1882). In time I was able to collect sufficient pancreatic tissue to isolate and sequence alligator insulin and pancreatic polypeptide (Lance et al., 1984). Thanks to Google Books I was later able to examine a digital copy of Duverney’s (1734) anatomy of the crocodile; the dissection was actually done in 1681, according to Cole (1949), in which he accurately shows the pancreas, gall bladder and the bile ducts (see Fig. 1). In 1767 John Hunter also gave a detailed description of the pancreas of the crocodile (published in Owen, 1831). I was only 300 years behind the times.

Figure 1 Duverney’s anatomical drawing.

This book is based on my more than 40 years of research into the reproductive biology and physiology of the American alligator in Louisiana. The American alligator is the best known of the crocodilians for a number of reasons: It occurs in great abundance in one of the most industrialized countries in the world, is easily accessible, and, compared to some of the crocodiles, relatively easy to handle, but a 14-ft (426 cm) alligator weighing in excess of 1000 lb (over 450 kg) is clearly not easy to handle and requires skilled help. Where there is information on other species of crocodiles and caiman, comparative data is included.

When I first started researching the literature for this book, I was overwhelmed by how much material had actually been published on the American alligator. In 1986 Brisbin et al. listed 2711 publications in their Bibliography of the American Alligator. Today I have no doubt that this number is more than quadrupled. For an animal considered unknown or neglected (Science, September 2002), the amount of published information is staggering. A simple search using the word alligator will get more than 1500 references on PubMed, the U.S. National Library of Medicine website. A search of books with the word alligator or crocodile in the title on the Amazon.com website produces an astounding list of more than 3000 titles, many of which are books for children (children’s books on alligators or crocodiles continue to be very popular). A search for masters’ theses and doctoral dissertations that used crocodilian or alligator tissue in some parts of the research revealed more than 100 of each. These lists are obviously incomplete, but they do reveal how popular crocodilians have become as a research animal. For paleontologists, they are the exemplar of the dinosaur (Brochu, 2000; Brusatte et al., 2010; Dodson, 2003), for behaviorists a difficult, but in the long run, rewarding study animal (Vliet, 1987, 1989; Lang, 1987; Lang and Kumar, 2013), for physiologists, an excellent and sturdy lab animal (Hicks and Wang, 1996; Franklin and Seebacher, 2003), for developmental biologists an excellent model to study brain development (Pritz, 1999, 2003, 2019), cardiovascular development (Crossley and Altimras, 2005), cardiac shunting (Hicks and Wang, 1996), lung function (Farmer and Carrier, 2000), and sex determination, an animal in which the sex of the embryo can be manipulated by the temperature at which the eggs are incubated (Lang et al., 1989; Lance and Bogart, 1994; Lang and Andrews, 1994), and for ecologists, a long-lived apex predator that can be monitored for many years (Joanen and McNease, 1980; Wilkinson and Rhodes, 1997; Wilkinson et al., 2016).

Sifting through this rich and varied literature for information on the reproductive biology of the Crocodylia has been a difficult but rewarding task. Internet has truly revolutionized literature searches: The Biodiversity Heritage Library, the Hathi Trust digital library, Gallica (the French National Library), and Google Books have been remarkable resources. Many rare books that one cannot even touch (let alone make copies) are now available in digital versions free of charge.

There are many books on crocodiles and alligators and a steadily increasing number of publications in the scientific literature. While working on this book Dr. Gordon Grigg, with David Kirshner published a beautifully illustrated tome, Biology and Evolution of Crocodylians in 2015 that covers much, and I hope not all, of what is included in this attempt of mine. In addition, a beautifully produced book, Alligators by Kent Vliet that covers the biology, behavior, and conservation of Alligator mississippiensis was published in 2020. Let us hope that this book is not redundant, but as we all know, crocodilophiles can never get enough books on their favorite animal. I have done my best to find everything available on the ecology, anatomy, and reproductive biology of the crocodiles, caimans, and alligators and have tried my best to give a critical review of this material. All mistakes, errors, or omissions are mine.

Chapter 1

Phylogeny and fossil history

Abstract

Crocodilians belong to the clade known as the Archosauria or ruling reptiles. The clade Archosauria represents one of the fundamental divisions of vertebrate phylogeny and has been a successful and at times dominant group ever since it originated in the Late Permian or Early Triassic. Today, the extant Archosauria consists of only the birds and crocodilians. This chapter explores the fossil history and categorization of crocodilians.

Keywords

Archosauria; Crocodylians; Mesozoic; vertebrate phylogeny; fossil history

One way to grasp the main perspectives of environment and biodiversity is to understand the origins and precious nature of a single living form, a single manifestation of the miracle of existence; if one has truly understood a crane—or a leaf or a cloud or a frog—one has understood everything.

Matthiessen (2001).

Crocodilians belong to the clade known as the Archosauria, or ruling reptiles. Brussate et al. (2010) define the group as follows, The archosaurs (Cope, 1869) are a speciose and diverse group that includes birds, dinosaurs, and crocodylomorphs, as well as a range of extinct taxa restricted to the Mesozoic. The clade Archosauria represents one of the fundamental divisions of vertebrate phylogeny, and has been a successful and at times dominant group ever since its origination in the Late Permian or Early Triassic. See also the extensive review of the Archosauria by Nesbitt (2011). Today the extant Archosauria consists of only the birds and crocodilians.

Long before Cope (1869) had erected the taxon Archeosauria to include dinosaurs and birds, the great comparative anatomist, physiologist, and surgeon, John Hunter (1728–93), see Owen (1861), who had dissected more than 5000 fish, reptiles, birds, and mammals made this succinct observation, The crocodile comes nearest to the fowl in the structure of its internal parts, of any animal that I know: it is the nearest of any of this class.Du Vernay (1688, 1734) also noted similarities in the internal aatomy of the crocodile and the bird, and, in addition, Voeltzkow (1891) remarked, the development of the crocodile closely resembles that of the bird.

In the popular press, crocodiles and alligators have often been referred to as living dinosaurs, but birds, not crocodilians, are the true living dinosaurs (Varrichio et al., 2008). Padian and Chiappe (1998) wrote, There is no longer reasonable scientific doubt that birds evolved from small theropod dinosaurs sometime during or shortly before the Middle to Late Jurassic, over 150 million years ago.

According to Brochu (2003), Extant crocodylian diversity is low, but the group has a rich fossil record going back to the Campanian (84–70 million years ago). Known fossil crocodilians outnumber their living relatives five to one. They are found on every continent, and during the Eocene (56–35 million years ago) their range extended from Antarctica to Ellesmere Island (the Canadian arctic)…They are ubiquitous in continental deposits throughout the Cenozoic (65 million years ago to the present) (my additions for the time scale of the Campanian, Cenozoic and Eocene, and the location of Ellesmere Island).

Although in the fossil record, birds, not crocodilians, are known to be descended from the dinosaurs, it is now agreed among paleontologists that both crocodilians and birds evolved from the Archosaurs (Benton and Clark, 1988; Brusatte et al., 2010; Nesbitt, 2011). The crocodilian lineage evolved from a little-known group of extinct Archosaurs with the clumsy and unfortunate (but probably descriptive) name, Crurotarsi. The word crurotarsi refers to the specialized articulation between the crus (lower leg) and tarsus (the bones of the foot) that first appeared during the early Triassic, 250–200 million years ago (Sereno and Arucci, 1990; Brusatte et al., 2010b). Thus birds and crocodilians evolved from different ancestral stocks, but within the Archosaurian clade. There were, however, a few taxonomists, using cladistic analysis, who came up with unusual heterodox arguments.