Morphology, reproduction and diet of the greater sea snake, Hydrophis major (Elapidae, Hydrophiinae)

Coral Reefs - Tập 38 - Trang 1057-1064 - 2019
R. Shine1, T. Shine1, C. Goiran2
1Department of Biological Sciences, Macquarie University, Sydney, Australia
2Labex Corail and Université de la Nouvelle-Calédonie, Nouméa Cedex, New Caledonia

Tóm tắt

Although widespread, the large Hydrophiinae sea snake Hydrophis major is poorly known ecologically. We dissected 119 preserved specimens in museum collections to quantify body sizes and proportions, sexual dimorphism, reproductive biology and diet. The sexes mature at similar snout–vent lengths (SVLs, about 75 cm) and attain similar maximum sizes (females 123 cm vs. males 122 cm SVL), but females in our sample exhibited larger mean sizes than did males (means 98.8 vs. 93.1 cm SVL). The adult sex ratio in museum specimens was highly female-biased (64:30), and the high proportion of reproductive females during the austral summer suggests annual reproduction. At the same SVL, females had shorter tails and wider bodies than did males, but sex differences in other body proportions (e.g. tail shape, head dimensions, eye diameter) were minimal. Skin rugosity increased with SVL, was greater in males than females and was greater on the dorsal than the ventral surface of the body. Litter size averaged 4.9 offspring (range 2–10) and increased with maternal body size. Neonates were approximately 33 cm SVL. The only prey items found inside dissected snakes (and also, recorded as prey in free-ranging snakes in our New Caledonia field studies) were catfish (Plotosus lineatus), whereas previous studies have suggested a more diverse diet. Although H. major resembles its terrestrial relatives in some respects, other characteristics (such as scale rugosity, low proportion of juveniles in collections, frequent production of small litters of large offspring) may reflect adaptation to marine habitats.

Tài liệu tham khảo

Avolio C, Shine R, Pile A (2006a) Sexual dimorphism in scale rugosity in sea snakes (Hydrophiidae). Biol J Linn Soc 89:343–354 Avolio C, Shine R, Pile AJ (2006b) The adaptive significance of sexually dimorphic scale rugosity in sea snakes. Am Nat 167:728–738 Bonnet X, Shine R, Naulleau G, Lourdais O (1999) What is the appropriate timescale for measuring “costs of reproduction” in a typical capital breeder, the asp viper? Evol Ecol 13:485–497 Brischoux F, Bonnet X, Shine R (2007) Foraging ecology of sea kraits Laticauda spp. in the Neo-Caledonian Lagoon. Mar Ecol Prog Ser 350:145–151 Brown GP, Shine R (2004) Effects of reproduction on the antipredator tactics of snakes (Tropidonophis mairii, Colubridae). Behav Ecol Sociobiol 56:257–262 Burns GW (1985) The female reproductive cycle of the Olive Sea snake, Aipysurus laevis (Hydrophiidae). In: Grigg GC, Shine R, Ehmann H (eds) Biology of Australasian frogs and reptiles. Surrey Beatty, Sydney, pp 339–341 Burns GW, Heatwole H (2000) Growth, sexual dimorphism, and population biology of the olive sea snake, Aipysurus laevis, on the Great Barrier Reef of Australia. Amphibia-Reptilia 21:289–300 Crowe-Riddell JM, Snelling EP, Watson AP, Suh AK, Partridge JC, Sanders KL (2016) The evolution of scale sensilla in the transition from land to sea in elapid snakes. Open Biol 6:160054 Dunson WA, Dunson MK (1973) Convergent evolution of sublingual salt glands in the marine file snake and the true sea snakes. J Comp Physiol 86:193–208 Elfes CT, Livingstone SR, Lane A, Lukoschek V, Sanders KL, Courtney AJ, Gatus JL, Guinea M, Lobo AS, Milton D, Rasmussen AR (2013) Fascinating and forgotten: the conservation status of the world’s sea snakes. Herpetol Conserv Biol 8:37–52 Fry GC, Milton DA, Wassenberg TJ (2001) The reproductive biology and diet of sea snake bycatch of prawn trawling in northern Australia: characteristics important for assessing the impacts on populations. Pac Conserv Biol 7:55–73 Goiran C, Shine R (2013) Decline in sea snake abundance on a protected coral reef system in the New Caledonian Lagoon. Coral Reefs 32:281–284 Goiran C, Shine R (2014) Reaction of a sea snake (Hydrophis major) to contact with a sea anemone. Coral Reefs 33:793 Goiran C, Dubey S, Shine R (2013) Effects of season, sex and body size on the feeding ecology of turtle-headed sea snakes (Emydocephalus annulatus) on IndoPacific inshore coral reefs. Coral Reefs 32:527–538 Greer AE (1997) The biology and evolution of Australian snakes. Surrey Beatty, Sydney Heatwole H (1978) Adaptations of marine snakes: unusual physiological strategies have enabled some snakes to live in a saltwater environment. Am Sci 66:594–604 Heatwole H (1999) Sea snakes, 2nd edn. Krieger Publishing Company, Florida Heatwole H, Burns G (1987) Final Report for National Parks and Wildlife Service Consultancy on Sea snake Populations. Unpublished Report, Australian National parks and Wildlife Service, Canberra Heatwole H, Cogger HG (1994) Sea snakes of Australia. In: Gopalakrishnakone P (ed) Sea snake toxinology. Singapore University Press, Singapore, pp 167–205 Heatwole H, Minton SA Jr, Taylor R, Taylor V (1978) Underwater observations on sea snake behaviour. Rec Aust Mus 31:737–761 Ineich I, Rasmussen AR (1997) Sea snakes from New Caledonia and the Loyalty Islands (Elapidae, Laticaudinae and Hydrophiinae). Zoosystema 19:185–192 Ineich I, Laboute P (2002) Les serpents marins de Nouvelle-Calédonie. IRD éditions, Paris Keogh JS, Shine R, Donnellan S (1998) Phylogenetic relationships of terrestrial Australo-Papuan elapid snakes (subfamily Hydrophiinae) based on cytochrome b and 16S rRNA sequences. Mol Phylogenet Evol 10:67–81 Kerford M (2005) The ecology of the bar bellied sea snake (Hydrophis elegans) in Shark Bay, Western Australia. M.Sc. thesis, Biological Sciences, Simon Fraser University, p 85 Kerford M, Wirsing AJ, Heithaus MR, Dill LM (2008) Danger on the rise: diurnal tidal state mediates an exchange of food for safety by the bar-bellied sea snake Hydrophis elegans. Mar Ecol Prog Ser 358:289–294 Lee MS, Sanders KL, King B, Palci A (2016) Diversification rates and phenotypic evolution in venomous snakes (Elapidae). R Soc Open Sci 3:150277 Lemen CA, Voris HK (1981) A comparison of reproductive strategies among marine snakes. J Anim Ecol 50:89–101 Letourneur Y, Briand MJ (2012) Catfish Plotosus lineatus are prey for the rare sea snake Hydrophis major in New Caledonia. Coral Reefs 31:349–349 Lillywhite HB, Menon GK (2019) Structure and function of skin in the pelagic sea snake, Hydrophis platurus. J Morphol 280:544–554 Lukoschek V, Avise JC (2011) Genetic monandry in 6 viviparous species of true sea snakes. J Hered 102:347–351 Lukoschek V, Beger M, Ceccarelli D, Richards Z, Pratchett M (2013) Enigmatic declines of Australia’s sea snakes from a biodiversity hotspot. Biol Conserv 166:191–202 Lynch TP (1999) The behavioural ecology of the Olive Sea snake, Aipysurus laevis. Ph.D. thesis, James Cook University, Townsville Marcos LA, Lanyon JM (2004) Dietary and morphometric analysis of three sea snake species caught as a single trawl by-catch assemblage around the Swain’s Reefs, Southern Great Barrier Reef, Queensland. Proc R Soc Qld 111:63–71 Pfaller JB, Frick MG, Brischoux F, Sheehy CM III, Lillywhite HB (2012) Marine snake epibiosis: a review and first report of decapods associated with Pelamis platurus. Integr Comp Biol 52:296–310 Sanders KL, Lee MS, Leys R, Foster R, Keogh SJ (2008) Molecular phylogeny and divergence dates for Australasian elapids and sea snakes (Hydrophiinae): evidence from seven genes for rapid evolutionary radiations. J Evol Biol 21:682–695 Sanders KL, Lee MS, Bertozzi T, Rasmussen AR (2013a) Multilocus phylogeny and recent rapid radiation of the viviparous sea snakes (Elapidae: Hydrophiinae). Mol Phylogenet Evol 66:575–591 Sanders KL, Rasmussen AR, Elmberg J, De Silva A, Guinea ML, Lee MS (2013b) Recent rapid speciation and ecomorph divergence in Indo-Australian sea snakes. Mol Ecol 22:2742–2759 Seymour RS (1982) Physiological adaptations to aquatic life. In: Gans C, Pough FH (eds) Biology of the Reptilia, vol 13. Academic Press, New York, pp 1–51 Sherratt E, Rasmussen AR, Sanders KL (2018) Trophic specialization drives morphological evolution in sea snakes. R Soc Open Sci 5:172141 Shine R (1980) Reproduction, feeding and growth in the Australian burrowing snake Vermicella annulata. J Herpetol 14:71–77 Shine R (1981) Venomous snakes in cold climates: ecology of the Australian genus Drysdalia (Serpentes: Elapidae). Copeia 1981:14–25 Shine R (1986) Ecology of a low-energy specialist: food habits and reproductive biology of the arafura filesnake (Acrochordidae). Copeia 1986:424–437 Shine R (1987) Food habits and reproductive biology of Australian snakes of the genus Hemiaspis (Elapidae). J Herpetol 21:71–74 Shine R (1988) Constraints on reproductive investment: a comparison between aquatic and terrestrial snakes. Evolution 42:17–27 Shine R (1991) Intersexual dietary divergence and the evolution of sexual dimorphism in snakes. Am Nat 138:103–122 Shine R (1993) Sexual dimorphism in snakes. In: Collins JT, Seigel RA (eds) Snakes: ecology and behavior. McGraw-Hill, New York, pp 49–86 Shine R (1994a) Sexual size dimorphism in snakes revisited. Copeia 1994:326–346 Shine R (1994b) Allometric patterns in the ecology of Australian snakes. Copeia 1994:851–867 Shine R (1995) Australian snakes: a natural history. Cornell University Press, Ithaca Shine R, Bull JJ (1977) Skewed sex ratios in snakes. Copeia 1977:228–234 Udyawer V, Simpfendorfer CA, Heupel MR (2015) Diel patterns in three-dimensional use of space by sea snakes. Animal Biotelemetry 3:29 Udyawer V, Simpfendorfer CA, Read M, Hamann M, Heupel MR (2016a) Exploring habitat selection in sea snakes using passive acoustic monitoring and Bayesian hierarchical models. Mar Ecol Prog Ser 546:249–262 Udyawer V, Read M, Hamann M, Heupel MR, Simpfendorfer CA (2016b) Importance of shallow tidal habitats as refugia from trawl fishing for sea snakes. J Herpetol 50:527–533 Ukuwela KD, Lee MS, Rasmussen AR, De Silva A, Sanders KL (2017) Biogeographic origins of the viviparous sea snake assemblage (Elapidae) of the Indian Ocean. Ceylon J Sci 46:101–110 Voris HK (1972) The role of sea snakes (Hydrophiidae) in the trophic structure of coastal ocean communities. J Mar Biol Assoc India 14:429–442 Voris HK, Voris HH (1983) Feeding strategies in marine snakes: an analysis of evolutionary, morphological, behavioral and ecological relationships. Am Zool 23:411–425 Ward TM (1996a) Sea snake by-catch of fish trawlers on the northern Australian continental shelf. Mar Freshw Res 47:625–630 Ward TM (1996b) Sea snake by-catch of prawn trawlers on the northern Australian continental shelf. Mar Freshw Res 47:631–635 Ward TM (2000) Factors affecting the catch rates and relative abundance of sea snakes in the by-catch of trawlers targeting tiger and endeavour prawns on the northern Australian continental shelf. Mar Freshw Res 51:155–164 Ward TM (2001) Age structures and reproductive patterns of two species of sea snake, Lapemis hardwickii Grey (1836) and Hydrophis elegans (Grey 1842), incidentally captured by prawn trawlers in northern Australia. Mar Freshw Res 52:193–203 Wassenberg TJ, Salini JP, Heatwole H, Kerr JD (1994) Incidental capture of sea-snakes (Hydrophiidae) by prawn trawlers in the Gulf of Carpentaria, Australia. Mar Freshw Res 45:429–443 Wirsing AJ, Heithaus MR (2009) Olive-headed sea snakes Disteria major shift seagrass microhabitats to avoid shark predation. Mar Ecol Progr Ser 387:287–293 Zimmerman K, Heatwole H (1990) Cutaneous photoreception: a new sensory mechanism for reptiles. Copeia 1990:860–862