Molecular analysis of the diets of snakes: Changes in prey exploitation during development of the rare smooth snake Coronella austriaca

Molecular Ecology

Volumn 23, Issue 15, 2014, Pages 3734-3743

  Brown, David S ^a   Ebenezer, Katie L ^a   Symondson, William O C ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

amphibians; Coronella austriaca; dietary analysis; grass snake; molecular diagnostics; Natrix natrix; smooth snake

Indexed keywords

AMPHIBIA; ANIMALIA; CORONELLA AUSTRIACA; INVERTEBRATA; MAMMALIA; NATRIX NATRIX; REPTILIA; SERPENTES;

AMPHIBIA; ANIMAL; CLASSIFICATION; COLUBRIDAE; CONFERENCE PAPER; CORONELLA AUSTRIACA; DIET; DIETARY ANALYSIS; DNA SEQUENCE; FECES; FOOD CHAIN; GRASS SNAKE; GROWTH, DEVELOPMENT AND AGING; MAMMAL; MOLECULAR DIAGNOSTICS; NATRIX NATRIX; PHYSIOLOGY; PREDATION; REPTILE; SMOOTH SNAKE; UNITED KINGDOM;

AMPHIBIANS; CORONELLA AUSTRIACA; DIETARY ANALYSIS; GRASS SNAKE; MOLECULAR DIAGNOSTICS; NATRIX NATRIX; SMOOTH SNAKE;

ANIMALS; COLUBRIDAE; DIET; FECES; FOOD CHAIN; GREAT BRITAIN; MAMMALS; PREDATORY BEHAVIOR; REPTILES; SEQUENCE ANALYSIS, DNA;

EID: 84904660916     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12475     Document Type: Conference Paper

References (69)

1. Andrén C, Nilson G, (1976) Hasselsnoken (Coronella austraica)-en utrotningshotad ormat!. Fauna Flora, Stockholm, 71, 61-76.
2. Andrén C, Nilson G, (1979) Hasselsnoken (Coronella austriaca)-I Norden-en isolerad och ekologiskt sarstalld ras? Fauna Flora, Stockholm, 74, 89-96.
3. Angelici FM, Luiselli L, Rugiero L, (1997) Food habits of the green lizard, Lacerta bilineata, in central Italy and a reliability test of faecal pellet analysis. Italian Journal of Zoology, 64, 267-272.
4. Baxley DL, Qualls CP, (2009) Black pine snake (Pituophis melanoleucus lodingi): spatial ecology and associations between habitat use and prey dynamics. Journal of Herpetology, 43, 284-293.
5. Beebee T, Griffiths R, (2000) Amphibians and Reptiles. HarperCollins, London.
6. Braithwaite AC, Buckley J, Corbett KF, et al,. (1989) The distribution in England of the smooth snake (C. austriaca Laurenti). Herpetological Journal, 1, 370-376.
7. Bronikowski AM, Arnold SJ, (1999) The evolutionary ecology of life-history variation in the garter snake Thamnophis elegans. Ecology, 80, 2314-2325.
8. Brown DS, (2010) Molecular analysis of the trophic interactions of British Reptiles. PhD Thesis, Cardiff University.
9. Brown DS, Jarman SN, Symonson WOC, (2012) Pyrosequencing of prey DNA in reptile faeces: analysis of earthworm consumption by slow worms. Molecular Ecology Resources, 12, 259-266.
10. van de Bund CF, (1964) De verspreiding van de reptielen en amphibieën in Nederland. Lacerta, 22, 1-72.
11. Capula M, Rugiero L, Luiselli L, (1994) Ecological observations on the Sardinian grass snake, Natrix natrix cetti. Amphibia-Reptilia, 15, 221-227.
12. Chen Y, Giles KL, Payton ME, Greenstone MH, (2000) Identifying key cereal aphid predators by molecular gut analysis. Molecular Ecology, 9, 1887-1898.
13. Clare EL, Fraser EE, Braid HE, Fenton MB, Hebert PDN, (2009) Species on the menu of a generalist predator, the eastern red bat (Lasiurus borealis): using a molecular approach to detect arthropod prey. Molecular Ecology, 18, 2532-2542.
14. Clare EL, Barber BR, Sweeney BW, Hebert PDN, Fenton MB, (2011) Eating local: influences of habitat on the diet of little brown bats (Myotis lucifugus). Molecular Ecology, 20, 1772-1780.
15. Deagle BE, Tollit DJ, (2007) Quantitative analysis of prey DNA in pinniped faeces: potential to estimate diet composition? Conservation Genetics, 8, 743-747.
16. Deagle BE, Gales NJ, Evans K, et al,. (2007) Studying seabird diet through genetic analysis of faeces: a case study on macaroni penguins (Eudyptes chrysolophus). PLoS ONE, 2, e831.
17. Dickman CR, (1988) Age-related dietary change in the European hedgehog, Erinaceus europaeus. Journal of Zoology, 215, 1-14.
18. Drobenkov SM, (1995) Comparative analysis of the feeding of sympatric snakes Vipera berus (L.), N. natrix (L.) and C. austriaca (L.). Russian Journal of Ecology, 26, 197-201.
19. Duguy R, (1961) Le cycle annuel d'activite de C. austriaca Laur.; d'aprex les observations manuscrites inedites de Ramond Rollinat. Terre Vie, 15, 401-435.
20. Filippi EM, Capula L, Luiselli L, Agrimi U, (1996) The prey spectrum of N. natrix (Linnaeus, 1758) and Natrix tessellata (Laurenti, 1768) in sympatric populations. Herpetozoa, 8, 155-164.
21. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R, (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology & Biotechnology, 3, 294-299.
22. Fretwell SD, (1972) Populations in a Seasonal Environment. Princeton University Press, Princeton, New Jersey.
23. Fretwell SD, Lucas HJ Jr, (1970) On territorial behaviour and other factors influencing habitat distribution in birds. Acta Biotheoretica, 19, 16-36.
24. Gasc J-P, Cabela A, Crnobrnja-Isailovic J, et al,. (1997) Atlas of Amphibians and Reptiles in Europe. Societas Europaea Herpetologica and Muséum National d'Histoire Naturelle, Paris.
25. Gignac A, Gregory PT, (2005) The effects of body size, age, and food intake during pregnancy on reproductive traits of a viviparous snake, Thamnophis ordinoides. Ecoscience, 12, 236-243.
26. Goddard P, (1981) Ecology of the smooth snake C. austriaca Laurenti in Britain. PhD Thesis, University of Southampton.
27. Goddard P, (1984) Morphology, growth, food habits and population characteristics of the smooth snake C. austriaca in southern Britain. Journal of Zoology (London), 204, 241-257.
28. 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.
29. Gregory PT, Isaac LA, (2004) Food habits of the grass snake in Southeastern England: is N. natrix a generalist predator? Journal of Herpetology, 38, 88-95.
30. Harper GL, King RA, Dodd CS, et al,. (2005) Rapid screening of invertebrate predators for multiple prey DNA targets. Molecular Ecology, 14, 819-827.
31. Harvey DS, Weatherhead PJ, (2006) Hibernation site selection by eastern Massasuga rattlesnakes (Sistrurus catenatus catenatus) near their northern range limit. Journal of Herpetology, 40, 66-73.
32. Harwood JD, Phillips SW, Sunderland KD, Symondson WOC, (2001) Secondary predation: quantification of food chain errors in an aphid-spider-carabid system using monoclonal antibodies. Molecular Ecology, 10, 2049-2057.
33. Heard GW, Black D, Robertson P, (2004) Habitat use by the inland carpet python (Morelia spilota metcalfei: Pythonidae): seasonal relationships with habitat structure and prey distribution in a rural landscape. Austral Ecology, 29, 446-460.
34. Herrel A, O'Reilly JC, (2006) Ontogenetic scaling of bite force in lizards and turtles. Physiological and Biochemical Zoology, 79, 31-42.
35. Huey RB, (1991) Physiological consequences of habitat selection. American Naturalist, 137, S91-S115.
36. Jarman SN, Wilson SG, (2004) DNA-based species identification of krill consumed by whale sharks. Journal of Fish Biology, 65, 586-591.
37. Jarman SN, Gales NJ, Tierney M, Gill PC, Elliott NG, (2002) A DNA-based method for identification of krill species and its application to analysing the diet of marine vertebrate predators. Molecular Ecology, 11, 2679-2690.
38. Jarman SN, Deagle BE, Gales NJ, (2004) Group-specific polymerase chain reaction for DNA-based analysis of species diversity and identity in dietary samples. Molecular Ecology, 13, 313-1322.
39. King RA, Read DS, Traugott M, Symondson WOC, (2008) Molecular analysis of predation: a review of best practice for DNA-based approaches. Molecular Ecology, 17, 947-963.
40. Lind AJ, Welsh HH Jr, (1994) Ontogenetic changes in foraging behavior and habitat use by the Oregon garter snake, Thamnophis atratus hydrophilus. Animal Behaviour, 48, 1261-1273.
41. Luiselli L, Capula M, (1997) Food habits, growth rates, and reproductive biology of grass snakes, N. natrix (Colobridae) in the Italian Alps. Journal of Zoology (London), 241, 371-380.
42. Luiselli L, Rugiero L, (1991) Food niche partitioning by water snakes (genus Natrix) at a freshwater environment in central Italy. Journal of Freshwater Ecology, 6, 439-444.
43. Madsen T, Shine R, (1996) Seasonal migration of predators and prey-a study of pythons and rats in tropical Australia. Ecology, 77, 149-156.
44. Marshall HD, Hart KA, Yaskowiak ES, Stenson GB, McKinnon D, Perry EA, (2010) Molecular identification of prey in the stomach contents of harp seals (Pagophilus groenlandicus) using species-specific oligonucleotides. Molecular Ecology Resources, 10, 181-189.
45. McCormick MI, (1998) Ontogeny of diet shifts by a microcarnivorous fish, Cheilodactylus spectabilis: relationship between feeding mechanics, microhabitat selection and growth. Marine Biology, 132, 9-20.
46. Moran S, Turner PD, O'Reilly C, (2008) Non-invasive genetic identification of small mammal species using real-time polymerase chain reaction. Molecular Ecology Resources, 8, 1267-1269.
47. Nature Conservancy Council (1983) The Ecology and Conservation of Amphibian and Reptile Species Endangered in Britain. English Nature Status (Wildlife), Peterborough.
48. Page B, McKenzie J, Goldsworthy SD, (2005) Dietary resource partitioning among sympatric New Zealand and Australian fur seals. Marine Ecology Progress Series, 293, 283-302.
49. Pernetta AP, Reading CJ, Allen JA, (2009) Chemoreception and kin discrimination by neonate smooth snakes, C. austriaca. Animal Behaviour, 77, 363-368.
50. Phelps TE, (1978) Seasonal movement of the snakes C. austriaca, V. berus and Natrxi natrix in southern England. British Journal of Herpetology, 5, 755-761.
51. Pizzatto L, Marques OAV, Facure K, (2009) Food habits of Brazilian boid snakes: overview and new data, with special reference to Corallus hortulanus. Amphibia-Reptilia, 30, 533-544.
52. Prestt I, (1971) An ecological study of the viper V. berus in Britain. Journal of Zoology (London), 164, 373-418.
53. Price TD, Grant PR, (1984) Life history traits and natural selection for small body size in a population of Darwin's finches. Evolution, 38, 483-494.
54. Prior KA, Weatherhead PJ, (1996) Habitat features of black rat snake hibernacula in Ontario. Journal of Herpetology, 30, 211-218.
55. Razgour O, Clare EL, Zeale MRK, et al,. (2011) High-throughput sequencing offers insight into mechanisms of resource partitioning in cryptic bat species. Ecology and Evolution, 1, 556-570.
56. Reinert HK, (1993) Habitat selection in snakes. In: Snakes: Ecology and Behavior (eds, Seigel RA, Collins JT,), pp. 201-240. McGraw Hill, New York.
57. Reñones O, Polunin NVC, Goni R, (2002) Size related dietary shifts of Epinephelus marginatus in a western Mediterranean littoral ecosystem: an isotope and stomach content analysis. Journal of Fish Biology, 61, 122-137.
58. Row JR, Blouin-Demers G, (2006) Thermal quality influences habitat selection at multiple spatial scales in milksnakes. Ecoscience, 13, 443-450.
59. Rugiero L, Capula M, Filippi E, Luiselli L, (1995) Food habits of Mediterranean populations of the smooth snake (C. austriaca). Herpetological Journal, 5, 316-318.
60. Rutz C, Whittingham MJ, Newton I, (2006) Age-dependent diet choice in an avian top predator. Proceedings of the Royal Society B: Biological Sciences, 273, 579-586.
61. Saitoh K, Takagaki M, Yamashita Y, (2003) Detection of Japanese flounder-specific DNA from the gut contents of potential predators in the field. Fisheries Science, 69, 473-477.
62. Secor SM, (2008) Digestive physiology of the Burmese python: broad regulation of integrated performance. Journal of Experimental Biology, 211, 3767-3774.
63. Sheppard SK, Bell JR, Sunderland KD, Fenlon J, Skirvin DJ, Symondson WOC, (2005) Detection of secondary predation by PCR analyses of the gut contents of invertebrate generalist predators. Molecular Ecology, 14, 4461-4468.
64. Shine R, Wall M, (2007) Why is intraspecific variation in foraging biology more common in snakes than in lizards? In: Lizard Ecology (eds, Reilly SM, McBrayer LB, Miles DB,), pp. 173-208. Cambridge University Press, Cambridge.
65. Spellerberg IF, (1977) Behaviour of a young smooth snake, C. austriaca Laurenti. Biological Journal of the Linnean Society, 9, 323-330.
66. Spellerberg IF, Phelps TE, (1977) Biology, general ecology and behaviour of the snake C. austriaca. Biological Journal of the Linnean Society, 9, 133-164.
67. Street D, (1979) The Reptiles of Northern and Central Europe. Batsford BT, London.
68. Symondson WOC, (2002) Molecular identification of prey in predator diets. Molecular Ecology, 11, 627-641.
69. Wilkinson JW, Arnell AP, (2011) NARRS report 2007-2009: interim results of the UK National amphibian and reptile recording scheme widespread species surveys. ARC Research Report, 11/01.