Adaptation or preadaptation: Why are keelback snakes (Tropidonophis mairii) less vulnerable to invasive cane toads (Bufo marinus) than are other Australian snakes?

Evolutionary Ecology

Volumn 25, Issue 1, 2011, Pages 13-24

  Llewelyn, John ^a,b,c   Phillips, Ben L ^a   Brown, Greg P ^a   Schwarzkopf, Lin ^b   Alford, Ross A ^b   Shine, Richard ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b JAMES COOK UNIVERSITY   (Australia)

^c NONE   (Australia)

Author keywords

Cane toad; Chemical defense; Introduced species; Keelback; Preadaptation

Indexed keywords

ADAPTATION; BIOGEOGRAPHICAL REGION; BIOLOGICAL INVASION; CHEMICAL DEFENSE; COEXISTENCE; FEEDING BEHAVIOR; INVASIVE SPECIES; NEONATE; PREDATOR; PREDATOR-PREY INTERACTION; SNAKE; SYMPATRY; TOAD; TOXIN;

AUSTRALIA;

ANURA; BUFO MARINUS; BUFONIDAE; SERPENTES; TROPIDONOPHIS MAIRII;

EID: 78650480042     PISSN: 02697653     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10682-010-9369-2     Document Type: Article

References (52)

1. Bernays EA (1993) Aversion learning and feeding. In: Papaj DR, Lewis AC (eds) Insect learning: ecological and evolutionary perspectives. Chapman & Hall, New York, pp 1-17.
2. Blumstein DT (2006) The multipredator hypothesis and the evolutionary persistence of antipredator behavior. Ethology 112: 209-217.
3. Breeden K (1963) Cane toad (Bufo marinus). Wildl Aust 1: 31.
4. Brodie ED, Brodie ED Jr (1990) Tetrodotoxin resistance in garter snakes: an evolutionary response of predators to dangerous prey. Evolution 44: 651-659.
5. Brodie ED, Brodie ED Jr (1999) Costs of exploiting poisonous prey: evolutionary trade-offs in a predator-prey arms race. Evolution 53: 626-631.
6. Brodie ED Jr, Ridenhour BJ, Brodie ED (2002) The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts. Evolution 56: 2067-2082.
7. Carroll SP, Loye JE, Dingle H, Mathieson M, Famula TR, Zalucki MP (2005) And the beak shall inherit-evolution in response to invasion. Ecol Lett 8: 944-951.
8. Cogger HG (2000) Reptiles and amphibians of Australia, 6th edn. Reed New Holland, Sydney.
9. Cogger H, Heatwole H (1981) The Australian reptiles: origins, biogeography, distribution patterns and island evolution. In: Keast A, Junk W (eds) Ecological biogeography of Australia. The Hague, Boston, pp 1332-1373.
10. Cooper CB, Hochachka WM, Dhondt AA (2007) Contrasting natural experiments confirm competition between house finches and house sparrows. Ecology 88: 864-870.
11. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287: 443-449.
12. Dickman CR (1992) Predation and habitat shift in the house mouse, Mus domesticus. Ecology 73: 313-322.
13. Drummond H, Garcia MC (1995) Congenital responsiveness of garter snakes to a dangerous prey abolished by learning. Anim Behav 49: 891-900.
14. Endler JA (1980) Natural selection on colour patterns in Poecilia reticulata. Evolution 34: 76-91.
15. Erspamer V, Erspamer GF, Mazzanti G, Endean R (1984) Active peptides in the skins of one hundred amphibian species from Australia and Papua New Guinea. Comp Biochem Physiol C 77: 99-108.
16. Fritts TH, Rodda GH (1998) The role of introduced species in the degradation of island ecosystems: a case history of Guam. Annu Rev Ecol Syst 29: 113-140.
17. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19: 207-233.
18. Georges A (2009) Wildlife worries spread. Canberra Times, Canberra.
19. Glenn S, Holway D (2008) Consumption of introduced prey by native predators: Argentine ants and pit-building ant lions. Biol Invasions 10: 273-280.
20. Greer AE (1997) The biology and evolution of Australian snakes. Surrey Beatty & Sons, Chipping Norton.
21. King RB, Ray JM, Stanford KM (2006) Gorging on gobies: beneficial effects of alien prey on a threatened vertebrate. Can J Zool 84: 108-115.
22. Kozubikova E, Filipova L, Kozak P, Duris Z, Martins M, Dieguez-Uribeondos J, Oidtmann B, Petrusek A (2009) Prevalence of the crayfish plague pathogen Aphanomyces astaci in invasive American crayfishes in the Czech Republic. Conserv Biol 23: 1204-1213.
23. Krueger CC, May B (1991) Ecological and genetic effects of salmonid introductions in North America. Can J Fish Aquat Sci 48: 66-77.
24. Launchbaugh KL, Provenza FD (1994) The effect of flavor concentration and toxin dose on the formation and generalization of flavor aversions in lambs. J Anim Sci 72: 10-13.
25. Llewelyn J, Phillips BL, Shine R (2009a) Sublethal costs associated with the consumption of toxic prey by snakes. Aust Ecol 34: 179-184.
26. Llewelyn J, Schwarzkopf L, Alford R, Shine R (2009b) Something different for dinner? Responses of a native Australian predator (the keelback snake) to an invasive prey species (the cane toad). Biol Invasions, published online July 14th 2009.
27. Llewelyn J, Webb JK, Schwarzkopf L, Alford R, Shine R (in press) Behavioural responses of carnivorous marsupials (Planigale maculata) to toxic invasive cane toads (Bufo marinus). Aust Ecol. doi: 10. 1111/j. 1442-9993. 2009. 02067. x.
28. Maerz JC, Karuzas JM, Madison DM, Blossey B (2005) Introduced invertebrates are important prey for a generalist predator. Divers Distrib 11: 83-90.
29. Malnate EV, Underwood G (1988) Australasian snakes of the genus Tropidonophis. Proc Acad Natl Sci Phila 140: 59-201.
30. Meyer K, Linde H (1971) Collection of toad venoms and chemistry of toad venom steroids. In: Bucherl W, Buckley EE (eds) Venomous animals and their venoms. Academic Press, New York, pp 521-556.
31. Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98: 5446-5451.
32. Phillips BL, Shine R (2004) Adapting to an invasive species: toxic cane toads induce morphological change in Australian snakes. Proc Natl Acad Sci USA 101: 17150-17155.
33. Phillips BL, Shine R (2006) An invasive species induces rapid adaptive change in a native predator: cane toads and black snakes in Australia. Proc R Soc Lond B Biol Sci 273: 1545-1550.
34. Phillips BL, Brown GP, Shine R (2003) Assessing the potential impact of cane toads on Australian snakes. Conserv Biol 17: 1738-1747.
35. Phillips BL, Brown GP, Webb JK, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439: 803.
36. Phillips BL, Greenlees MJ, Brown GP, Shine R (2009) Predator behaviour and morphology mediates the impact of an invasive species: cane toads and death adders in Australia. Anim Conserv, published online July 29th 2009.
37. Pockley D (1965) The free and the caged. Blackwoods Mag 1965: 439-466.
38. Rayward A (1974) Giant toads: a threat to Australian wildlife. Wildlife 17: 506-507.
39. Schoonhoven LM, Meerman J (1978) Metabolic cost of changes in diet and neutralization of allelochemics. Entomol Exp Appl 24: 489-493.
40. Shettleworth SJ (1998) Cognition, evolution, and behavior. Oxford University Press, New York.
41. Shine R (1989) Constraints, allometry, and adaptation: food habits and reproductive biology of Australian brownsnakes (Preudonaja: Elapidae). Herpetologica 45: 195-207.
42. Shine R (1991) Strangers in a strange land: ecology of the Australian colubrid snakes. Copeia 1991: 120-131.
43. Shine R, Brown GP (2008) Adapting to the unpredictable: reproductive biology of vertebrates in the Australian wet-dry tropics. Philos Trans R Soc Lond B Biol Sci 363: 363-373.
44. Short J, Kinnear JE, Robley A (2002) Surplus killing by introduced predators in Australia-evidence for ineffective anti-predator adaptations in native prey species? Biol Conserv 103: 283-301.
45. Skelhorn J, Rowe C (2006) Predator avoidance learning of prey with secreted or stored defences and the evolution of insect defences. Anim Behav 72: 827-834.
46. Straughan IR (1969) The Hyla bicolor complex (Anura, Hylidae) in north Queensland. Proc R Soc Queensland 80: 43-54.
47. Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9: 357-374.
48. Tyler MJ (1987) Frog and cane toad skin secretions. In: Covacevich J, Davie P, Pearn J (eds) Toxic plants and animals: a guide for Australia. Queensland Museum, Brisbane, pp 329-339.
49. Tyler MJ, Davies M (1978) Species-groups within the Australopapuan hylid frog genus Litoria Tschudi. Aust J Zool 26: 619.
50. Urban MC, Phillips BL, Skelly DK, Shine R (2007) The cane toad's (Chaunus [Bufo] marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proc R Soc Lond B Biol Sci 274: 1413-1419.
51. Webb JK, Brown GP, Child T, Greenlees MJ, Phillips BL, Shine R (2008) A native dasyurid predator (common planigale, Planigale maculata) rapidly learns to avoid a toxic invader. Aust Ecol 33: 821-829.
52. Yoshida T, Jones LE, Ellner SP, Fussmann GF, Hairston JNG (2003) Rapid evolution drives ecological dynamics in a predator-prey system. Nature 424: 303-306.