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

Volumn 32, Issue 2, 2013, Pages 527-538

  Goiran, C ^a   Dubey, S ^b   Shine, R ^c  

^a UNIVERSITÉ DE LA NOUVELLE CALÉDONIE   (New Caledonia)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Cost of reproduction; Dietary specialist; Oophagy; Predation; Sexual dimorphism

Indexed keywords

BODY SIZE; COASTAL LAGOON; CORAL REEF; EMBRYONIC DEVELOPMENT; FEEDING ECOLOGY; MATE LOCATION; NICHE PARTITIONING; ONTOGENY; PERCIFORM; REPRODUCTIVE BIOLOGY; REPRODUCTIVE COST; SEASONALITY; SEX-RELATED DIFFERENCE; SEXUAL DIMORPHISM; SNAKE; SPECIALIST; SPECIALIZATION; TAXONOMY;

NEW CALEDONIA [MELANESIA];

ANTHOZOA; BLENNIOIDEI; EMYDOCEPHALUS ANNULATUS; GOBIIDAE; HYDROPHIIDAE; PISCES; POMACENTRIDAE; SERPENTES; TESTUDINES;

EID: 84877061216     PISSN: 07224028     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00338-012-1008-7     Document Type: Article

References (85)

1. Aars J, Ims RA (2002) Intrinsic and climatic determinants of population demography: the winter dynamics of tundra voles. Ecology 83: 3449-3456.
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: 399-407.
3. Aplin LM, Cockburn A (2012) Ecological selection and sexual dimorphism in the sooty oystercatcher, Haematopus fuliginosus. Austral Ecol 37: 248-257.
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 87-116.
5. Arnold SJ, Wassersug RJ (1978) Differential predation on metamorphic anurans by garter snakes (Thamnophis): social behavior as a possible defense. Ecology 59: 1014-1022.
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: 379-392.
7. Avolio C, Shine R, Pile AJ (2006) The adaptive significance of sexually dimorphic scale rugosity in sea snakes. Am Nat 167: 728-738.
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: 161-168.
9. Bea A, Brana F, Baron JP, Saint Girons H (1992) Régimes et cycles alimentaires des vipères européennes (Reptilia, Viperidae). Année Biologique 31: 25-44.
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: 145-151.
11. Brischoux F, Bonnet X, Shine R (2011) Conflicts between feeding and reproduction in amphibious snakes (sea kraits, Laticauda spp.). Austral Ecol 36: 46-52.
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: 235-244.
13. Brown GP, Shine R (2006) Why do most tropical animals reproduce seasonally? Testing alternative hypotheses on the snake Tropidonophis mairii (Colubridae). Ecology 87: 133-143.
14. Caughley G (1977) Analysis of vertebrate populations. John Wiley & Sons, New York.
15. Cundall D (1987) Functional morphology. In: Seigel RA, Collins JT, Novak SS (eds) Snakes: ecology and evolutionary biology. MacMillan, New York, pp 106-142.
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: 198-205.
17. Doherty PJ (1983) Diel, lunar and seasonal rhythms in the reproduction of two tropical damselfishes: Pomacentrus flavicauda and P. wardi. Mar Biol 75: 215-224.
18. Glodek GS, Voris HK (1982) Marine snake diets: prey composition, diversity and overlap. Copeia 1982: 661-666.
19. Gopalakrishnakone P, Kochva E (1990) Venom glands and some associated muscles in sea snakes. J Morphol 205: 85-96.
20. Greene HW (1983) Dietary correlates of the origin and radiation of snakes. Am Zool 23: 431-441.
21. Greene HW (1997) Snakes. The evolution of mystery in nature. University of California Press, Berkeley, CA.
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 366-395.
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: 231-241.
24. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 692-704.
25. Guinea ML (1996) Functions of the cephalic scales of the sea snake Emydocephalus annulatus. J Herpetol 30: 126-128.
26. Heatwole HF (1999) Sea snakes. University of NSW Press, Sydney.
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 493-529.
28. Hernaman V, Munday PL (2007) Evolution of mating systems in coral reef gobies and constraints on mating system plasticity. Coral Reefs 26: 585-595.
29. Hilder ML, Pankhurst NW (2003) Evidence that temperature change cues reproductive development in the spiny damselfish, Acanthochromis polyacanthus. Environ Biol Fishes 66: 187-196.
30. Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. J Mol Evol 32: 128-144.
31. Jayne BC (1985) Swimming in constricting (Elaphe g. guttata) and nonconstricting (Nerodia fasciata pictiventris) colubrid snakes. Copeia 1985: 195-208.
32. King MB, Duvall D (1990) Prairie rattlesnake seasonal migrations: episodes of movement, vernal foraging and sex differences. Anim Behav 39: 924-935.
33. Lourdais O, Shine R, Bonnet X, Guillon M, Naulleau G (2004) Climate affects offspring phenotypes in a viviparous snake. Oikos 104: 551-560.
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: 183-185.
35. Lukoschek V, Keogh JS (2006) Molecular phylogeny of sea snakes reveals a rapidly diverged adaptive radiation. Biol J Linn Soc 89: 523-539.
36. Lukoschek V, Shine R (2012) Sea snakes rarely venture far from home. Ecol Evol 2: 1113-1121.
37. Madsen T, Shine R (1993) Costs of reproduction in a population of European adders. Oecologia 94: 488-495.
38. Madsen T, Shine R (2000) Energy versus risk: costs of reproduction in free-ranging pythons in tropical Australia. Austral Ecol 25: 670-675.
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 307-328.
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: 1119-1128.
41. McCosker JE (1975) Feeding behaviour of Indo-Australian Hydrophiidae. In: Dunson WA (ed) The biology of sea snakes. University Park Press, Baltimore, pp 217-232.
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: 41-52.
43. Mushinsky HR (1987) Foraging ecology. In: Seigel RA, Ford NB, Novak SS (eds) Snakes: ecology and evolutionary biology. Macmillan, New York, pp 302-334.
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 249-278.
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: 455-459.
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: 85-95.
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: 387-396.
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, Honolulu.
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. 14.
50. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25: 1253-1256.
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: 66-88.
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 356-386.
53. Ruckstuhl KE, Neuhaus P (2005) Sexual segregation in vertebrates. Cambridge University Press, Cambridge.
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: 682-695.
55. Shaffer SA, Costa DP, Weimerskirch H (2003) Foraging effort in relation to the constraints of reproduction in free-ranging albatrosses. Funct Ecol 17: 66-74.
56. Sherry DF, Mrosovsky N, Hogan JA (1980) Weight loss and anorexia during incubation in birds. J Comp Physiol Psychol 94: 89-98.
57. Shine R (1977) Habitats, diets and sympatry in snakes: a study from Australia. Can J Zool 55: 1118-1128.
58. Shine R (1980) 'Costs' of reproduction in reptiles. Oecologia 46: 92-100.
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 297-303.
60. Shine R (1988) Constraints on reproductive investment: a comparison between aquatic and terrestrial snakes. Evolution 42: 17-27.
61. Shine R (1989) Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q Rev Biol 64: 419-464.
62. Shine R (1991) Why do larger snakes eat larger prey? Funct Ecol 5: 493-502.
63. Shine R (2005) All at sea: aquatic life modifies mate-recognition modalities in sea snakes (Emydocephalus annulatus, Hydrophiidae). Behav Ecol Sociobiol 57: 591-598.
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 221-253.
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 173-208.
66. Shine R, Webb J (1990) Natural history of Australian typhlopid snakes. J Herpetol 24: 357-363.
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: 248-258.
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: 1-10.
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: 16-24.
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: 805-811.
71. Shine R, Brischoux F, Pile A (2010) A seasnake's colour affects its susceptibility to algal fouling. Proc R Soc B 277: 2459-2464.
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: 824-832.
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-Champaign.
74. Srinivasan M, Jones GP (2006) Extended breeding and recruitment periods of fishes on a low latitude coral reef. Coral Reefs 25: 673-682.
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: 387-398.
76. Taberlet P, Meyer A, Bouvet J (1992) Unusually large mitochondrial variation in populations of the blue tit, Parus caeruleus. Mol Ecol 1: 27-36.
77. Thresher RE (1984) Reproduction in reef fishes. TFH Publications, Neptune City, NJ.
78. Vincent SE, Herrel A (2007) Functional and ecological correlates of ecologically-based dimorphisms in squamate reptiles. Integr Comp Biol 47: 172-188.
79. Vitt LJ, Pianka ER (1994) Lizard ecology. Historical and experimental perspectives. Princeton University Press, Princeton, New Jersey.
80. Voris HK (1966) Fish eggs as the apparent sole food item for a genus of sea snake, Emydocephalus (Krefft). Ecology 47: 152-154.
81. Warkentin KM (1995) Adaptive plasticity in hatching age-a response to predation risk trade-offs. Proc Natl Acad Sci USA 92: 3507-3510.
82. Webb JK (2004) Pregnancy decreases swimming performance of female northern death adders (Acanthophis praelongus). Copeia 2004: 357-363.
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: 321-327.
84. Weeks SC (1996) The hidden cost of reproduction: reduced food intake caused by spatial constraints in the body cavity. Oikos 75: 345-349.
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: 1054-1061.