Coral Reefs

, Volume 32, Issue 2, pp 527–538 | Cite as

Effects of season, sex and body size on the feeding ecology of turtle-headed sea snakes (Emydocephalus annulatus) on IndoPacific inshore coral reefs

Report

Abstract

In terrestrial snakes, many cases of intraspecific shifts in dietary habits as a function of predator sex and body size are driven by gape limitation and hence are most common in species that feed on relatively large prey and exhibit a wide body-size range. Our data on sea snakes reveal an alternative mechanism for intraspecific niche partitioning, based on sex-specific seasonal anorexia induced by reproductive activities. Turtle-headed sea snakes (Emydocephalus annulatus) on coral reefs in the New Caledonian Lagoon feed entirely on the eggs of demersal-spawning fishes. DNA sequence data (cytochrome b gene) on eggs that we palpated from stomachs of 37 snakes showed that despite this ontogenetic stage specialization, the prey comes from a taxonomically diverse array of species including damselfish (41 % of samples, at least 5 species), blennies (41 %, 4 species) and gobies (19 %, 5 species). The composition of snake diets shifted seasonally (with damselfish dominating in winter but not summer), presumably reflecting seasonality of fish reproduction. That seasonal shift affects male and female snakes differently, because reproduction is incompatible with foraging. Adult female sea snakes ceased feeding when they became heavily distended with developing embryos in late summer, and males ceased feeding while they were mate searching in winter. The sex divergence in foraging habits may be amplified by sexual size dimorphism; females grow larger than males, and larger snakes (of both sexes) feed more on damselfish (which often lay their eggs in exposed sites) than on blennies and gobies (whose eggs are hidden within narrow crevices). Specific features of reproductive biology of coral reef fish (seasonality and nest type) have generated intraspecific niche partitioning in these sea snakes, by mechanisms different from those that apply to terrestrial snakes.

Keywords

Cost of reproduction Dietary specialist Oophagy Predation Sexual dimorphism 

Supplementary material

Supplementary material 1 (MOV 28618 kb)

Video sequences of turtle-headed sea snakes foraging and feeding in the Baie des Citrons, New Caledonia. Photography by Claire Goiran. Supplementary material 2 (AVI 15978 kb)

References

  1. Aars J, Ims RA (2002) Intrinsic and climatic determinants of population demography: the winter dynamics of tundra voles. Ecology 83:3449–3456CrossRefGoogle Scholar
  2. Aldridge RD, Brown WS (1995) Male reproductive cycle, age at maturity, and cost of reproduction in the timber rattlesnake (Crotalus horridus). J Herpetol 29:399–407CrossRefGoogle Scholar
  3. Aplin LM, Cockburn A (2012) Ecological selection and sexual dimorphism in the sooty oystercatcher, Haematopus fuliginosus. Austral Ecol 37:248–257CrossRefGoogle Scholar
  4. Arnold SJ (1993) Foraging theory and prey-size-predator-size relations in snakes. In: Seigel RA, Collins JT (eds) Snakes: ecology and behaviour. McGraw-Hill, New York, pp 87–116Google Scholar
  5. Arnold SJ, Wassersug RJ (1978) Differential predation on metamorphic anurans by garter snakes (Thamnophis): social behavior as a possible defense. Ecology 59:1014–1022CrossRefGoogle Scholar
  6. Asoh K, Yoshikawa T (2002) The role of temperature and embryo development time in the diel timing of spawning in a coral-reef damselfish with high-frequency spawning synchrony. Environ Biol Fishes 64:379–392CrossRefGoogle Scholar
  7. Avolio C, Shine R, Pile AJ (2006) The adaptive significance of sexually dimorphic scale rugosity in sea snakes. Am Nat 167:728–738PubMedCrossRefGoogle Scholar
  8. Awata S, Miura S, Seki S, Sagawa T, Sato N, Sakai K (2010) Seasonal changes in reproductive and physical condition, sexual dimorphism, and male mating tactics in the jewelled blenny Salarias fasciatus. Ichthyol Res 57:161–168CrossRefGoogle Scholar
  9. Bea A, Brana F, Baron JP, Saint Girons H (1992) Régimes et cycles alimentaires des vipères européennes (Reptilia, Viperidae). Année Biologique 31:25–44Google Scholar
  10. Brischoux F, Bonnet X, Shine R (2007) Foraging ecology of sea kraits Laticauda spp. in the Neo-Caledonian Lagoon. Mar Ecol Prog Ser 350:145–151CrossRefGoogle Scholar
  11. Brischoux F, Bonnet X, Shine R (2011) Conflicts between feeding and reproduction in amphibious snakes (sea kraits, Laticauda spp.). Austral Ecol 36:46–52CrossRefGoogle Scholar
  12. Brischoux F, Rolland V, Bonnet X, Caillaud M, Shine R (2012) Effects of oceanic salinity on body condition in sea snakes. Integr Comp Biol 52:235–244PubMedCrossRefGoogle Scholar
  13. Brown GP, Shine R (2006) Why do most tropical animals reproduce seasonally? Testing alternative hypotheses on the snake Tropidonophis mairii (Colubridae). Ecology 87:133–143PubMedCrossRefGoogle Scholar
  14. Caughley G (1977) Analysis of vertebrate populations. John Wiley & Sons, New YorkGoogle Scholar
  15. Cundall D (1987) Functional morphology. In: Seigel RA, Collins JT, Novak SS (eds) Snakes: ecology and evolutionary biology. MacMillan, New York, pp 106–142Google Scholar
  16. Daltry JC, Wuster W, Thorpe RS (1998) Intraspecific variation in the feeding ecology of the crotaline snake Calloselasma rhodostoma in southeast Asia. J Herpetol 32:198–205CrossRefGoogle Scholar
  17. Doherty PJ (1983) Diel, lunar and seasonal rhythms in the reproduction of two tropical damselfishes: Pomacentrus flavicauda and P. wardi. Mar Biol 75:215–224CrossRefGoogle Scholar
  18. Glodek GS, Voris HK (1982) Marine snake diets: prey composition, diversity and overlap. Copeia 1982:661–666CrossRefGoogle Scholar
  19. Gopalakrishnakone P, Kochva E (1990) Venom glands and some associated muscles in sea snakes. J Morphol 205:85–96CrossRefGoogle Scholar
  20. Greene HW (1983) Dietary correlates of the origin and radiation of snakes. Am Zool 23:431–441Google Scholar
  21. Greene HW (1997) Snakes. The evolution of mystery in nature. University of California Press, Berkeley, CAGoogle Scholar
  22. Gregory PT, Macartney JM, Larsen KW (1987) Spatial patterns and movements. In: Seigel RA, Collins JT, Novak SS (eds) Snakes: ecology and evolutionary biology. MacMillan, New York, pp 366–395Google Scholar
  23. Gregory PT, Crampton LH, Skebo KM (1999) Conflicts and interactions among reproduction, thermoregulation and feeding in viviparous reptiles: are gravid snakes anorexic? J Zool 248:231–241CrossRefGoogle Scholar
  24. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:692–704CrossRefGoogle Scholar
  25. Guinea ML (1996) Functions of the cephalic scales of the sea snake Emydocephalus annulatus. J Herpetol 30:126–128CrossRefGoogle Scholar
  26. Heatwole HF (1999) Sea snakes. University of NSW Press, SydneyGoogle Scholar
  27. Herler J, Munday P, Hernaman V (2011) Gobies on coral reefs. In: Patzner RA, Van Tassell JL, Kovacic M, Kappor BG (eds) The biology of gobies. Science Publishers, Boca Raton, FL, pp 493–529CrossRefGoogle Scholar
  28. Hernaman V, Munday PL (2007) Evolution of mating systems in coral reef gobies and constraints on mating system plasticity. Coral Reefs 26:585–595CrossRefGoogle Scholar
  29. Hilder ML, Pankhurst NW (2003) Evidence that temperature change cues reproductive development in the spiny damselfish, Acanthochromis polyacanthus. Environ Biol Fishes 66:187–196CrossRefGoogle Scholar
  30. Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. J Mol Evol 32:128–144PubMedCrossRefGoogle Scholar
  31. Jayne BC (1985) Swimming in constricting (Elaphe g. guttata) and nonconstricting (Nerodia fasciata pictiventris) colubrid snakes. Copeia 1985:195–208CrossRefGoogle Scholar
  32. King MB, Duvall D (1990) Prairie rattlesnake seasonal migrations: episodes of movement, vernal foraging and sex differences. Anim Behav 39:924–935CrossRefGoogle Scholar
  33. Lourdais O, Shine R, Bonnet X, Guillon M, Naulleau G (2004) Climate affects offspring phenotypes in a viviparous snake. Oikos 104:551–560CrossRefGoogle Scholar
  34. Luiselli L, Angelici FM (1998) Sexual size dimorphism and natural history traits are correlated with intersexual dietary divergence in royal pythons (Python regius) from the rainforests of southeastern Nigeria. Ital J Zool 65:183–185CrossRefGoogle Scholar
  35. Lukoschek V, Keogh JS (2006) Molecular phylogeny of sea snakes reveals a rapidly diverged adaptive radiation. Biol J Linn Soc 89:523–539CrossRefGoogle Scholar
  36. Lukoschek V, Shine R (2012) Sea snakes rarely venture far from home. Ecol Evol 2:1113–1121PubMedCrossRefGoogle Scholar
  37. Madsen T, Shine R (1993) Costs of reproduction in a population of European adders. Oecologia 94:488–495CrossRefGoogle Scholar
  38. Madsen T, Shine R (2000) Energy versus risk: costs of reproduction in free-ranging pythons in tropical Australia. Austral Ecol 25:670–675CrossRefGoogle Scholar
  39. Martins M, Marques OAV, Sazima I (2002) Ecological and phylogenetic correlates of feeding habits in Neotropical pitvipers of the genus Bothrops. In: Schuett GW, Höggren M, Douglas ME, Greene HW (eds) Biology of the vipers. Eagle Mountain Publishing, Utah, pp 307–328Google Scholar
  40. McCarthy CJ (1987) Adaptations of sea snakes that eat fish eggs; with a note on the throat musculature of Aipysurus eydouxii (Gray, 1849). J Nat Hist 21:1119–1128CrossRefGoogle Scholar
  41. McCosker JE (1975) Feeding behaviour of Indo-Australian Hydrophiidae. In: Dunson WA (ed) The biology of sea snakes. University Park Press, Baltimore, pp 217–232Google Scholar
  42. Mori A, Toda M (2011) Feeding characteristics of a Japanese pitviper, Ovophis okinavensis, on Okinawa Island: seasonally biased but ontogenetically stable exploitation on small frogs. Curr Herpetol 30:41–52CrossRefGoogle Scholar
  43. Mushinsky HR (1987) Foraging ecology. In: Seigel RA, Ford NB, Novak SS (eds) Snakes: ecology and evolutionary biology. Macmillan, New York, pp 302–334Google Scholar
  44. Neat F, Lengkeek W (2009) Sexual selection in blennies. In: Patzner RA, Goncalves EJ, Hastings PA, Kapoor BG (eds) The biology of blennies. Science Publishers, Enfield, NH, pp 249–278CrossRefGoogle Scholar
  45. Olsson M, Madsen T, Shine R (1997) Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proc R Soc B 264:455–459CrossRefGoogle Scholar
  46. Ormond R, Roberts J, Jan R (1996) Behavioral differences in microhabitat use by damselfishes (Pomacentridae): implications for reef fish biodiversity. J Exp Mar Biol Ecol 202:85–95CrossRefGoogle Scholar
  47. Oro D, Cam E, Pradel R, Martinez-Abrain A (2004) Influence of food availability on demography and local population dynamics in a long-lived seabird. Proc R Soc B 271:387–396PubMedCrossRefGoogle Scholar
  48. Palumbi S, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. Department of Zoology and Kewalo Marine Laboratory, University of Hawaii, HonoluluGoogle Scholar
  49. Posada D (2003) Using Modeltest and PAUP* to select a model of nucleotide substitution. In: Baxevanis AD, Davison DB, Page RDM, Petsko GA, Stein LD, Stormo GD (eds) Current protocols in bioinformatics. John Wiley & Sons, New York, pp 6.5.1–6.5.14Google Scholar
  50. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256PubMedCrossRefGoogle Scholar
  51. Quenouille B, Bermingham E, Planes S (2004) Molecular systematics of the damselfishes (Teleostei: Pomacentridae): Bayesian phylogenetic analysis of mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol 31:66–88PubMedCrossRefGoogle Scholar
  52. Robertson R (1991) The role of adult biology in the timing of spawning of tropical reef fishes. In: Sale PA (ed) The ecology of fishes on coral reefs. Academic Press, New York, pp 356–386Google Scholar
  53. Ruckstuhl KE, Neuhaus P (2005) Sexual segregation in vertebrates. Cambridge University Press, CambridgeGoogle Scholar
  54. Sanders KL, Lee MSY, Leys R, Foster R, Keogh JS (2008) Molecular phylogeny and divergence dates for Australasian elapids and sea snakes (Hydrophiinae): evidence from seven genes for rapid evolutionary radiations. J Evol Biol 21:682–695PubMedCrossRefGoogle Scholar
  55. Shaffer SA, Costa DP, Weimerskirch H (2003) Foraging effort in relation to the constraints of reproduction in free-ranging albatrosses. Funct Ecol 17:66–74CrossRefGoogle Scholar
  56. Sherry DF, Mrosovsky N, Hogan JA (1980) Weight loss and anorexia during incubation in birds. J Comp Physiol Psychol 94:89–98CrossRefGoogle Scholar
  57. Shine R (1977) Habitats, diets and sympatry in snakes: a study from Australia. Can J Zool 55:1118–1128CrossRefGoogle Scholar
  58. Shine R (1980) ‘Costs’ of reproduction in reptiles. Oecologia 46:92–100CrossRefGoogle Scholar
  59. Shine R (1985) Reproductive biology of Australian reptiles: a search for general patterns. In: Grigg GC, Shine R, Ehmann H (eds) Biology of Australasian frogs and reptiles. Royal Zoological Society of New South Wales, Sydney, pp 297–303Google Scholar
  60. Shine R (1988) Constraints on reproductive investment: a comparison between aquatic and terrestrial snakes. Evolution 42:17–27CrossRefGoogle Scholar
  61. Shine R (1989) Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q Rev Biol 64:419–464PubMedCrossRefGoogle Scholar
  62. Shine R (1991) Why do larger snakes eat larger prey? Funct Ecol 5:493–502CrossRefGoogle Scholar
  63. Shine R (2005) All at sea: aquatic life modifies mate-recognition modalities in sea snakes (Emydocephalus annulatus, Hydrophiidae). Behav Ecol Sociobiol 57:591–598CrossRefGoogle Scholar
  64. Shine R, Wall M (2005) Ecological divergence between the sexes in reptiles. In: Ruckstuhl KE, Neuhaus P (eds) Sexual segregation in vertebrates. Cambridge University Press, Cambridge, pp 221–253Google Scholar
  65. Shine R, Wall M (2007) Why is intraspecific variation in foraging biology more common in snakes than in lizards? In: Reilly SM, McBrayer LB, Miles DB (eds) Lizard ecology. Cambridge University Press, Cambridge, pp 173–208CrossRefGoogle Scholar
  66. Shine R, Webb J (1990) Natural history of Australian typhlopid snakes. J Herpetol 24:357–363CrossRefGoogle Scholar
  67. Shine R, Harlow PS, Keogh JS, Boeadi (1998) The influence of sex and body size on food habits of a giant tropical snake, Python reticulatus. Funct Ecol 12:248–258Google Scholar
  68. Shine R, Shine T, Shine B (2003) Intraspecific habitat partitioning by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae): the effects of sex, body size, and colour pattern. Biol J Linn Soc 80:1–10CrossRefGoogle Scholar
  69. Shine R, Bonnet X, Elphick M, Barrott E (2004) A novel foraging mode in snakes: browsing by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae). Funct Ecol 18:16–24CrossRefGoogle Scholar
  70. Shine R, Shine T, Shine JM, Shine BG (2005) Synchrony in capture dates suggests cryptic social organization in sea snakes (Emydocephalus annulatus, Hydrophiidae). Austral Ecol 30:805–811CrossRefGoogle Scholar
  71. Shine R, Brischoux F, Pile A (2010) A seasnake’s colour affects its susceptibility to algal fouling. Proc R Soc B 277:2459–2464PubMedCrossRefGoogle Scholar
  72. Shine R, Goiran C, Shine T, Fauvel T, Brischoux F (2012) Phenotypic divergence between seasnake (Emydocephalus annulatus) populations from adjacent bays of the New Caledonian Lagoon. Biol J Linn Soc 107:824–832Google Scholar
  73. Song CB (1994) Molecular evolution of the cytochrome b gene among percid fishes. Ph.D. thesis, Department of Biology, University of Illinois at Urbana-ChampaignGoogle Scholar
  74. Srinivasan M, Jones GP (2006) Extended breeding and recruitment periods of fishes on a low latitude coral reef. Coral Reefs 25:673–682CrossRefGoogle Scholar
  75. Sun L, Shine R, Zhao D, Tang Z (2001) Biotic and abiotic influences on activity patterns of insular pit-vipers (Gloydius shedaoensis, Viperidae) from north-eastern China. Biol Conserv 97:387–398CrossRefGoogle Scholar
  76. Taberlet P, Meyer A, Bouvet J (1992) Unusually large mitochondrial variation in populations of the blue tit, Parus caeruleus. Mol Ecol 1:27–36PubMedCrossRefGoogle Scholar
  77. Thresher RE (1984) Reproduction in reef fishes. TFH Publications, Neptune City, NJGoogle Scholar
  78. Vincent SE, Herrel A (2007) Functional and ecological correlates of ecologically-based dimorphisms in squamate reptiles. Integr Comp Biol 47:172–188PubMedCrossRefGoogle Scholar
  79. Vitt LJ, Pianka ER (1994) Lizard ecology. Historical and experimental perspectives. Princeton University Press, Princeton, New JerseyGoogle Scholar
  80. Voris HK (1966) Fish eggs as the apparent sole food item for a genus of sea snake, Emydocephalus (Krefft). Ecology 47:152–154CrossRefGoogle Scholar
  81. Warkentin KM (1995) Adaptive plasticity in hatching age—a response to predation risk trade-offs. Proc Natl Acad Sci USA 92:3507–3510PubMedCrossRefGoogle Scholar
  82. Webb JK (2004) Pregnancy decreases swimming performance of female northern death adders (Acanthophis praelongus). Copeia 2004:357–363CrossRefGoogle Scholar
  83. Webb JK, Shine R, Branch WR, Harlow PS (2000) Life-history strategies in basal snakes: reproduction and dietary habits of the African threadsnake, Leptotyphlops scutifrons (Serpentes, Leptotyphlopidae). J Zool 250:321–327CrossRefGoogle Scholar
  84. Weeks SC (1996) The hidden cost of reproduction: reduced food intake caused by spatial constraints in the body cavity. Oikos 75:345–349CrossRefGoogle Scholar
  85. Winne CT, Hopkins WA (2006) Influence of sex and reproductive condition on terrestrial and aquatic locomotor performance in the semi-aquatic snake Seminatrix pygaea. Funct Ecol 20:1054–1061CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Laboratoire LIVE and Laboratoire d’excellence CORAILUniversité de la Nouvelle-CalédonieNouméa CedexNew Caledonia
  2. 2.Department of Ecology and EvolutionUniversity of LausanneLausanneSwitzerland
  3. 3.School of Biological Sciences A08University of SydneySydneyAustralia

Personalised recommendations