Provided for non-commercial research and educational use. Not for reproduction, distribution or commercial use. This chapter was originally published in Treatise on Estuarine and Coastal Science, published by Elsevier, and the attached copy is provided by Elsevier for the author's benefit and for the benefit of the author's institution, for non- commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues who you know, and providing a copy to your institution's administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution's website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier's permissions site at: http://www.elsevier.com/locate/permissionusematerial Davenport J (2011) High-Trophic-Level Consumers: Trophic Relationships of Reptiles and Amphibians of Coastal and Estuarine Ecosystems. In: Wolanski E and McLusky DS (eds.) Treatise on Estuarine and Coastal Science, Vol 6, pp. 227–249. Waltham: Academic Press. © 2011 Elsevier Inc. All rights reserved. Author's personal copy 6.09 High-Trophic-Level Consumers: Trophic Relationships of Reptiles and Amphibians of Coastal and Estuarine Ecosystems J Davenport, University College Cork, Cork, Republic of Ireland © 2011 Elsevier Inc. All rights reserved. 6.09.1 Introduction/Paleoecology 227 6.09.2 Amphibia 229 6.09.3 Reptiles 230 6.09.3.1 Lizards 230 6.09.3.2 Snakes 233 6.09.3.2.1 Sea snakes 233 6.09.3.2.2 Other snakes 236 6.09.3.3 Crocodilians 236 6.09.3.4 Turtles 237 6.09.3.4.1 Sea turtles 237 6.09.3.4.2 Other turtles 244 6.09.4 General Conclusions 246 References 246 Abstract This chapter briefly considers the trophic relationships of Mesozoic coastal reptiles (ichthyosaurs, plesiosaurs, mosasaurs, pterosaurs, and placodonts). The few amphibian species that exploit coastal/estuarine food resources are described. Coastal lizards are dealt with in detail, while there is a large section devoted to the trophic specialization and niche separation of sea snakes. The trophic biology of estuarine crocodilians is reviewed. The rest of the chapter is devoted to sea turtles plus a few other chelonian species that exploit estuaries and coastal waters. The consequences of anthropogenic depletion of reptile populations form a major theme, as do inter-ecosystem energetic subsidies. 6.09.1 Introduction/Paleoecology artifact of the bias created by the presence of indigestible belemnite hooklets in the stomachs; cf. squid diets of ele­ Amphibian ancestors were basal tetrapods, derived from fresh­ phant seals and sperm whales), coastal forms appear to have water fish, dating to the Devonian (~365 million years ago had a broader diet, some having jaws suitable for crushing (MYA)). Modern amphibians (mainly frogs, toads, newts, and shellfish and others apparently taking fish. Recently, evidence salamanders) are mostly tied to freshwater for reproduction of a truly catholic diet in a widespread coastal ichthyosaur was and there is no fossil evidence of ancestral forms from marine found in the fossilized stomach contents of a specimen of the sediments, indicating an absence of an amphibian role in Cretaceous Platypterigius, which had been eating fish, hatchl­ Devonian coastal or estuarine ecosystems. ing sea turtles, and a bird (Kear et al., 2003). Given their size Basal tetrapods (formerly known as labrynthodont amphi­ diversity (and relatively small size at birth), it is virtually bians) gave rise to reptiles in the Carboniferous (320–310 certain that members of the ichthyosaur feeding guild preyed MYA). Reptiles were truly terrestrial, laying shelled eggs and upon each other and there is some fossil evidence to support having relatively impermeable skins. During the Mesozoic this view (e.g., McGowan, 1974). (230–63 MYA), reptiles became extremely important in marine Plesiosaurs (190–65 MYA) were highly successful Mesozoic trophic biology and occupied coastal and estuarine niches that, reptiles, many of which were large and oceanic predators on since major extinctions at the end of the Mesozoic, have sub­ fish and cephalopods (e.g., belemnites). Although the best- sequently been taken over by a variety of fish and marine known species were long necked with a small head and four mammals. Some groups (notably the ichthyosaurs) were vivi­ roughly equal-sized flippers, morphological diversity was high, parous and independent of land. with short-necked, large-headed pliosaurs being apex predators Ichthyosaurs (230–90 MYA) formed a highly diverse that competed with ichthyosaurs. Many plesiosaurs were cer­ group, ranging from 2 to 20 m in overall length and occupied tainly coastal and omnivorous; McHenry et al. (2005) recently both oceanic and coastal ecological niches. Coastal species described the gut contents of elasmosaurs (extremely long- appear to have been smaller and rather less streamlined than necked plesiosaurs) from early Cretaceous deposits of the well-known highly streamlined tuna-like forms with large Australia. They found remains of fish and belemnites – and eyes (e.g., Opthalmosaurus) that probably foraged offshore in also remains of gastropod and bivalve mollusks as well as deep water. Whereas oceanic forms seem to have specialized crinoid echinoderms and crustacean exoskeletons. They noted in feeding on belemnite cephalopods (though this may be an that the elasmosaurs had conical teeth like modern fish and 227 Treatise on Estuarine and Coastal Science, 2011, Vol.6, 227-249, DOI: 10.1016/B978-0-12-374711-2.00618-5 Author's personal copy 228 High-Trophic-Level Consumers: Trophic Relationships of Reptiles and Amphibians of Coastal and Estuarine Ecosystems Placodus Cyamodus Henodus Figure 1 Placodont diversity. Reproduced with permission from Naish, D., 2004. Fossils explained 48. Placodonts. Geology Today 20, 153–158. squid eaters, but that the stomachs contained gastroliths (as do there is plentiful evidence that they also ate ammonites and modern crocodilians) which would have allowed hard-shelled nautiloids, besides preying on other mosasaurs, small plesio­ prey to be triturated, even though the animals had first to be saurs, sea turtles, and seabirds. Mosasaur anatomy was not swallowed whole. compatible with high swimming speeds, so it seems likely Triassic (230–63 MYA) placodonts (see Naish (2004) for that they were ambush, rather than pursuit predators (except review; Figure 1) were modest-sized (1–3 m overall length), when preying on slow-moving groups such as nautiloids). As shallow water durophagous benthic predators that appear to early mosasaurs had highly kinetic skulls (like snakes), they have subsisted predominantly upon bivalve mollusks, crushed were able to ingest relatively large prey items (e.g., large teleost by palatine teeth, although crustaceans and even brachiopods fish). With increasing study, it has become clear that mosasaurs have been suggested as possible food items. Many placodonts were extremely diverse in form, and occupied a variety of were heavily armored and superficially resembled turtles, being trophic niches, exploiting pelagic and benthic food resources. short-legged and often with carapaces (Figure 1). They prob­ For example, Martin (2007) confirmed that a mosasaur ably foraged predominantly on sandy and muddy bottoms, (Globidens) with rounded crusher teeth had bivalve remains in digging into the substratum with limbs and/or snouts to extract its stomach. Whereas juvenile mosasaurs probably fell prey to a bivalves. However, most placodonts had robust, spatulate teeth range of pterosaurs, birds, and fish, it seems likely that adult at the front of the jaws, so appear to have been capable of mosasaurs were only preyed upon by other mosasaurs, by plucking prey from rocky substrata; again, bivalve mollusks marine crocodiles, or by sharks. Healed bite marks on mosa­ may have been the most important prey, though gastropods saur skeletons are evidence of shark predation (rather than and even large barnacles are other likely candidates. Placodonts scavenging) (Rothschild et al., 2005). were slow moving and it has been suggested that adults were In recent years, paleontological studies have revealed that preyed upon by sharks or larger coastal marine reptiles such as flying pterosaurs (which arose in the Triassic 225 MYA and crocodilian phytosaurs (Mazin and Pinna, 1993). Certainly disappeared about 65 MYA, but coexisted with birds for 100 juveniles are known to have fallen prey to the small (1 m) million years) predominantly occupied coastal niches, nothosaur (plesiosaur precursor) Lariosaurus (Tschanz, 1989) whereas birds dominated in terrestrial and inland habitats and, by analogy with bird predation, it has been suggested that (Wang et al., 2005). Pterosaurs formed a highly diverse pterosaurs may have preyed upon them (Mazin and Pinna, group anatomically and ecologically; old ideas of weak, lim­ 1993). It seems probable that placodonts were egg layers like ited fliers that were nearly helpless on land have been replaced sea turtles, and that eggs and hatchlings would therefore have by concepts of powerful, agile flying and running animals provided a marine energetic subsidy for coastal terrestrial (probably endothermic) that filled ecological niches currently predators. occupied by albatrosses, pelicans, gulls, waders, etc. It is evi­ Mosasaurs made up the last great group