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Reproductive Biology and Embryology of the Crocodilians

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Reproductive Biology and Embryology of the Crocodilians 32B EMBRYOLOGY OF MARINE TURTLEB bei den Seeschildkrbten, untersucht an Embryonen von Chelonia viridis. Anat. Anz, 8, 801-803. Voeltzkow, A. (1903). Beitrage zur Entwicklungsgeschichte der Reptilien. VI. Gesichtsbildung und Entwicklung der ausseren Kbrperform bei Chelone imbricala Schweigg. Abh. senckenb. naturf. Ges. 27, 179-190. CHAPTER Wassersug, R. J. (1976). A procedure for differential staining of cartilage and bone in whole formalin-fixed vertebrates. Stain Tech. 51, 131-134. Wiedersheim, R. (1890a). Uber die Entwicklung des Urogenitalapparates bei Krokodilen und 5 Schildkrbten. Anal. Anz. 5, 337-344. Wiedersheim, R. (1890b). Uber die Entwicklung des Urogenitalapparates bei Krokodilen und Schildkrbten. Arch. mikr. Anal. 36, 410-468. Will, L. (1893). Beitrage zur Entwicklungsgeschichte der Reptilien. 2. Die Anlage der Keirn­ blatter bei der menorquinischen Sumpfschildkrbte (Cistudo lutaria Gesn.). Zool. Jahrb .. Abt. Anal. 6, 529-615. Reproductive Biology and Witzell, W. N. (1983). Synopsis of biological data on the hawksbill turtle, Erelmochelys imbricata (Linnaeus, 1766). FAD Fish. Synop. 137, 1-78. Embryology of the Wood, J. R. and Wood, F. E. (1980). Reproductive biology of captive green sea turtles CIlelonia mydas. Amer. Zool. 20, 499-505. Crocodilians Yamamoto, Y. (1960). Comparative histological studies of the thyroid gland of lower verte­ brates. Folia anat. jap. 34, 353-387. Yntema, C. L. (1964). Procurement and use of turtle embryos for experimental procedures. Anal. Rec. 149, 577-586. Yntema, C. L. (1968). A series of stages in the embryonic development of Chelydra serpentina. f. Morph. 125, 219-251. MARK W. 0. FERGUSON Yntema, C. L. (1976). Effects of incubation temperatures on sexual differentiation in the turtle, Department of Basic Dental Sciences, Turner Dental School, University of Chelydra serpentina. J. Morph. 150, 453-462. Manchester, Higher Cambridge Street, Manchester, M 1 5 6FH England Yntema, C. L. (1979). Temperature levels and periods of sex determination during incubation of eggs of Chelydra serpentina. f. Morph. 159, 17-28. Yntema, C. and Mrosovsky, N. (1979). Incubation temperature and sex ratio in hatchling loggerhead turtles: a preliminary report. Mar. Turtle Newslet. 11, 9-10. Yntema, C. and Mrosovsky, N. (1980). Sexual differentiation in hatchling loggerheads (Caretta caretta) incubated at different controlled temperatures. Herpetologica 36, 33-36. Yntema, C. L. and Mrosovsky, N. (1982). Critical periods and pivotal temperatures for sexual differentiation in loggerhead sea turtles. Can. f. Zool. 60, 1012-1016. Yoshie, S. and Honma, Y. (1976). Light and scanning electron microscopic studies on the esophageal spines in the Pacific Ridley turtle, Lepidochelys olivacea. Archs. Hislol. Jap. 38, 339-346. Zanger!, R. (1969). The turtle shell. In Biology of the Reptilia (c. Gans, A. d'A. Bellairs, and T. Parsons, eds.). Volume 1, Academic Press, London and New York, pp. 311-339. Zanger!, R. (1980). Patterns of phylogenetic differentiation in the toxochelyid and cheloniid sea turtles. Amer. Zool. 20, 585-596. Zeleny, C. (1901). The ear!y development of the hypophysis in Chelonia. BioI. Bull., Stockh 2, 267-281. Zwinenberg, A. J. (1976). The olive ridley, Lepidochelys olivacea (Eschscholtz, 1829): probablY the most numerous marine turtle today. Bull. Maryland herp. Soc. 12, 75-95. Zwinenberg, A. J. (1977). Kemp's Ridley, Lepidochelys kempii (Garman, 1880), undoubtedly the most endangered marine turtle today (with notes on the current status of Lepidochel.'l' olivacea). Bull. Maryland herp. Soc. 13, 170-192. INTRODUCTION 331 P. Endocrine Glands, 445 CONTENTS Q. Thymus and Immune System, 446 R, Limbs and Tail, 446 I. INTROOUCTION 331 S, Integument and Its Glands, 450 II. REPRODUCTIVE BIOLOGY T. Caruncle, 450 333 A. General, 333 VIII. DEVELOPMENTAL ABNORMALITIES 451 B. Sexual Maturity and Adult Sex Ratios, 333 IX. SHELL·LESS, SEMI.SHELL.LESS, AND IN VITRO C. Courtship, Spermatogenesis, Ovulation, Copulation, CULTURE TECHNIGUES 460 the Breeding Season, Fertilization, and Egg Laying, 336 D. Nesting Biology, 349 X. CONCLUSIONS 462 E. Maternal Behavior, 355 REFERENCES 464 F. Captive Breeding, Egg Collection, and Artificial Incubation, 356 G. Hatching, 360 III. THE EGGSHELL AND SHELL MEMBRANES 363 A. General, 363 B. Egg Banding, 363 C. Structure, 367 D. Chemical Composition, 374 E. Water and Gas Conductance and Embryonic I. INTRODUCTION Metabolism, 376 IV. THE EGG CONTENTS AND EXTRA.EMBRYONIC The living crocodilians, represented by 26 living species placed in three MEMBRANES 377 subfamilies (see Table III later in chapter), are the end products of a rela­ V. tively conservative lineage, which arose from thecodont ancestors approxi­ EARLY EMBRYONIC DEVELOPMENT [BEFORE EGG LAYING) mately 230 million years ago (Carroll, 1969; Walker, 1972). The evolution 381 and taxonomy of the order have been the subject of considerable debate VI. STAGES OF EMBRYONIC DEVELOPMENT [AFTER EGG involving paleontological (Steel, 1973), neontological (Wermuth and Mer­ LAYING) 390 tens, 1977; Groombridge, 1982), immunological, and biochemical ap­ VII. ORGANOGENESIS proaches (Perutz et al., 1981; Le Clercq et al., 1981; Densmore, 1981; Coul­ 416 son and Hernandez, 1983). Densmore's and Groombridge's classifications A. Branchial Arches, 41 6 are used here. All types of data indicate that birds are the closest living B. Face and Nose, 41 9 relatives of crocodilians. However, several aspects of crocodilian embryo­ C. Palate and Nasopharyngeal Duct, 421 D. Tongue, 427 genesis, for example, palatogenesis (Section VII, VIII), resemble mamma­ lian phenomena, and variations in hemoglobin amino acid sequences place E. Ear, 428 I" F. Eye, 428 t crocodilians closer to mammals than to snakes (Perutz et al., 1981; Le G. Chondrocranium and Osteocranium, 431 I' Clercq et al., 1981; Densmore, 1981). Thus, further studies of crocodilian H. Teeth, 431 embryogenesis not only may shed light on fundamental aspects of or­ I. Central Nervous System, 432 ganogenesis, but also exploit the potential of these vertebrates as models ..J. Vertebrae and Ribs, 435 for experimental investigations, which are difficult or impossible to per­ K. Respiratory System, 436 form in other amniotes (Ferguson, 1981a, b, 1984a). L. Cardiovascular System, 436 Crocodilian embryology has received very little attention. Some general M. Diaphragm, 438 accounts are available for Crocodylus niloticus (Rathke, 1866; Voeltzkow, N. Gastrointestinal System, 438 O. 1899, 1901, 1903a), Alligator mississippiensis (Clarke, 1891; Reese, 1908, Urogenital System and Sex Determination, 440 1910a-c, 1912, 1915a, b, 1921, 1936), C. palustris, and C. porosus (Derani­ 330 332 REPRODUCTIVE BIOLOGY AND EMBRYOLOGY OF CROCODILIANS REPRODUCTIVE BIOLOGY 333 yagala, 1934, 1936, 1939), whereas Wettstein (1937, 1954) included some factors influencing egg laying. Therefore this chapter begins with a se­ embryological data in his general review of crocodilian biology. The pres­ lected review of relevant data on these topics. This is not intended to be a ent chapter reviews the older, incomplete data and a special effort is made comprehensive review; rather it is intended to highlight areas of interest to correct ambiguous or misleading statements or concepts. My studies on common to ecologists, conservationists, and farmers, as well as to develop­ shell structure (Ferguson, 1981c, 1982a), sex determination (Ferguson and mental biologists. Insights into life history facilitate appreciation of some of Joanen, 1982, 1983), and craniofacial development (Ferguson, 1979a, b, the embryological events described later. They may also stimulate develop­ 1981a, b, 1982b, 1984a) tend to give the chapter a bias, but an attempt has mental biologists to investigate some of the mechanisms which underlie been made to review all available data in the hope that neglected topics will numerous observations of natural history, for example, embryonic dia­ be pursued by others. pause, the relation of maternal age to the incidence of birth defects, the Many of the studies on which the present chapter is based have been gaseous, aqueous, and metabolic physiology of embryos, the hatching carried out on the population of Alligator mississippiensis at the Rockefeller trigger, and the transition from chorioallantoic to pulmonary respiration. Wildlife Refuge in Louisiana, and it might be argued that these animals are The aim is also to provide the biologist or farmer with a literature review not representative of all alligator populations nor of crocodilians in general. and to stimulate collection of data on numerous unanswered but intriguing However, observations on other populations have revealed no significant questions. The difference of format of this chapter from others in this differences with respect to basic reproductive biology and embryology. volume was dictated by the nature of the available information. My objec­ Furthermore, analyses of protein electrophoretic patterns have shown that tive is to stimulate future studies in those areas for which data are currently A. mississippiensis is one of the most genetically homogeneous vertebrate unavailable. I hope that progress in the field will permit extensive revision species; protein variations are so low that animals from populations sepa­ of much of what is said here in a few years' time! rated by more than 1000 miles cannot be identified as to their geographic source (Gartside et al. 1977; Menzies et al. 1979; Adams et al. 1980). In addition, I have made limited observations
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