Stress Triangle: Do Introduced Predators Exert Indirect Costs on Native Predators and Prey?

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Anson, Jennifer R ^a   Dickman, Chris R ^a   Boonstra, Rudy ^b   Jessop, Tim S ^c  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID; HYDROCORTISONE;

ALERTNESS; ANIMAL BEHAVIOR; ARTICLE; AUSTRALIA; BLOOD PARASITE; CONTROLLED STUDY; EOSINOPHIL COUNT; FORAGING BEHAVIOR; GEOGRAPHICAL VARIATION (SPECIES); HAEMOGREGARINA VARANICOLA; HOST PARASITE INTERACTION; HYDROCORTISONE BLOOD LEVEL; MARSUPIAL; NONHUMAN; PARASITE IDENTIFICATION; PARASITE LOAD; PREDATOR PREY INTERACTION; PSEUDOCHEIRUS PEREGRINUS; REPTILE; REWARD; VARANUS VARIUS; VULPES VULPES;

ANIMALS; AUSTRALIA; CARNIVORY; ECOSYSTEM; ENERGY METABOLISM; FEAR; FEEDING BEHAVIOR; FOOD CHAIN; FOXES; HAEMOSPORIDA; HERBIVORY; INTRODUCED SPECIES; PHALANGERIDAE; POPULATION DYNAMICS; PREDATORY BEHAVIOR; REPTILES; STRESS, PHYSIOLOGICAL;

BASSARISCUS; CANIDAE; METATHERIA; PSEUDOCHEIRUS PEREGRINUS; REPTILIA; VARANUS VARIUS; VULPES; VULPES VULPES;

EID: 84876014550     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060916     Document Type: Article

References (92)

1. Preisser EL, Bolnick DI, Benard MF, (2005) Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86: 501-509.
2. Lima SL, (1998) Stress and decision making under the risk of predation: Recent developments from behavioral, reproductive, and ecological perspectives. Advances in the Study of Behavior 27: 215-290.
3. Schmitz OJ (2005) Behavior of predators and prey and links with population-level processes. In: Barbosa P, Castellanos I, editors. Ecology of Predator-Prey Interactions. New York: Oxford University Press. 256-278.
4. Creel S, Christianson D, Liley S, Winnie JA, (2007) Predation risk affects reproductive physiology and demography of elk. Science 315: 960-960.
5. Glen AS, Dickman CR, (2005) Complex interactions among mammalian carnivores in Australia, and their implications for wildlife management. Biological Reviews 80: 387-401.
6. Caro T (2005) Antipredator defenses in birds and mammals. Chicago: University of Chicago Press.
7. Sergio F, Caro T, Brown D, Clucas B, Hunter J, et al. (2008) Top predators as conservation tools: ecological rationale, assumptions, and efficacy. Annual Review of Ecology Evolution and Systematics. 1-19.
8. Salo P, Banks PB, Dickman CR, Korpimaki E, (2010) Predator manipulation experiments: impacts on populations of terrestrial vertebrate prey. Ecological Monographs 80: 531-546.
9. Salo P, Korpimaki E, Banks PB, Nordstrom M, Dickman CR, (2007) Alien predators are more dangerous than native predators to prey populations. Proceedings of the Royal Society B-Biological Sciences 274: 1237-1243.
10. Saunders GR, Gentle MN, Dickman CR, (2010) The impacts and management of foxes Vulpes vulpes in Australia. Mammal Review 40: 181-211.
11. Cox JG, Lima SL, (2006) Naivete and an aquatic-terrestrial dichotomy in the effects of introduced predators. Trends in Ecology & Evolution 21: 674-680.
12. Banks PB, Dickman CR, (2007) Alien predation and the effects of multiple levels of prey naivete. Trends in Ecology & Evolution 22: 229-230.
13. Strauss SY, Lau JA, Carroll SP, (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecology Letters 9: 354-371.
14. Kovacs EM, Crowther MS, Webb JK, Dickman CR (2012) Population and behavioural responses of native prey to alien predation. Oecologia.
15. McEwen BS, Wingfield JC, (2003) The concept of allostasis in biology and biomedicine. Hormones and Behavior 43: 2-15.
16. Wikelski M, Cooke SJ, (2006) Conservation physiology. Trends in Ecology & Evolution 21: 38-46.
17. Boonstra R, Hik D, Singleton GR, Tinnikov A, (1998) The impact of predator-induced stress on the snowshoe hare cycle. Ecological Monographs 68: 371-394.
18. Sapolsky RM, Romero LM, Munck AU, (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21: 55-89.
19. Romero LM, (2004) Physiological stress in ecology: lessons from biomedical research. Trends in Ecology & Evolution 19: 249-255.
20. Boonstra R, (2005) Equipped for life: The adaptive role of the stress axis in male mammals. Journal of Mammalogy 86: 236-247.
21. Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, et al. (1998) Ecological bases of hormone-behavior interactions: The "emergency life history stage". American Zoologist 38: 191-206.
22. Lee AK, McDonald IR, (1985) Stress and population regulation in small mammals. Oxford Reviews of Reproductive Biology 7: 261-304.
23. Krebs CJ, Boonstra R, Boutin S, Sinclair ARE, (2001) What drives the 10-year cycle of snowshoe hares? Bioscience 51: 25-35.
24. Hik DS, McColl CJ, Boonstra R, (2001) Why are Arctic ground squirrels more stressed in the boreal forest than in alpine meadows? Ecoscience 8: 275-288.
25. Lima SL, Dill LM, (1990) Behavioral decisions made under the risk of predation- a review and prospectus. Canadian Journal of Zoology-Revue Canadienne De Zoologie 68: 619-640.
26. Houston AI, McNamara JM, Hutchinson JMC, (1993) General results concerning the trade-off between gaining energy and avoiding predation. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 341: 375-397.
27. Creel S, Winnie J, Christianson D (2009) Glucocorticoid stress hormones and the effect of predation risk on elk reproduction. Proceedings of the National Academy of Sciences USA 106.
28. Creel S, Winnie J, Maxwell B, Hamlin K, Creel M, (2005) Elk alter habitat selection as an antipredator response to wolves. Ecology 86: 3387-3397.
29. Sinclair ARE, Pech RP, Dickman CR, Hik D, Mahon P, et al. (1998) Predicting effects of predation on conservation of endangered prey. Conservation Biology 12: 564-575.
30. Watson M, Aebischer NJ, Cresswell W, (2007) Vigilance and fitness in grey partridges Perdix perdix: the effects of group size and foraging-vigilance trade-offs on predation mortality. Journal of Animal Ecology 76: 211-221.
31. Koivula K, Rytkonen S, Orell M, (1995) Hunger-dependency of hiding behaviour after a predator attack in dominant and subordinate willow tits. Ardea 83: 397-404.
32. Christianson D, Creel S, (2010) A nutritionally mediated risk effect of wolves on elk. Ecology 91: 1184-1191.
33. Hik DS, (1995) Does risk of predation influence population dynamics- Evidence for the cyclic decline of snowshoe hares. Wildlife Research 22: 115-129.
34. Rehage JS, Barnett BK, Sih A, (2005) Foraging behaviour and invasiveness: do invasive gambusia exhibit higher feeding rates and broader diets than their noninvasive relatives? Ecology of Freshwater Fish 14: 352-360.
35. Watts HE, Holekamp KE, (2008) Interspecific competition influences reproduction in spotted hyenas. Journal of Zoology 276: 402-410.
36. Macdonald DW, Buesching CD, Stopka P, Henderson J, Ellwood SA, et al. (2004) Encounters between two sympatric carnivores: red foxes (Vulpes vulpes) and European badgers (Meles meles). Journal of Zoology 263: 385-392.
37. Trewby LD, Wilson GJ, Delahay RJ, Walker N, Young R, et al. (2008) Experimental evidence of competitive release in sympatric carnivores. Biology Letters 4: 170-172.
38. Sheriff MJ, Krebs CJ, Boonstra R, (2009) The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. Journal of Animal Ecology 78: 1249-1258.
39. Dickman CR (2011) Animal competition. In: Simberloff D, Rejmanek M, editors. Encyclopedia of Biological Invasions. Berkley and Los Angeles: University of California Press. 117-122.
40. Clinchy M, Zanette L, Boonstra R, Wingfield JC, Smith JNM, (2004) Balancing food and predator pressure induces chronic stress in songbirds. Proceedings of the Royal Society of London Series B-Biological Sciences 271: 2473-2479.
41. Burbidge AA, McKenzie NL, (1989) Patterns in the modern decline of Western Australia vertebrate fauna- causes and conservation implications. Biological Conservation 50: 143-198.
42. Guarino F, (2001) Diet of a large carnivorous lizard, Varanus varius. Wildlife Research 28: 627-630.
43. Weavers BW, (1988) Vital statistics of the lace monitor lizard (Varanus varius) in south-eastern Australia. Victorian Naturalist 105: 142-145.
44. Guarino F, (2002) Spatial ecology of a large carnivorous lizard, Varanus varius (Squamata: Varanidae). Journal of Zoology 258: 449-457.
45. Smith B, Augee M, Rose S, (2003) Radio-tracking studies of common ringtail possums, Pseudocheirus peregrinus, in Manly Dam Reserve, Sydney. Proceedings of the Linnean Society of New South Wales 124: 183-194.
46. McKay GM, Ong P (2008) Common ringtail possum. In: Van Dyck S, Strahan R, editors. Mammals of Australia. 3rd edition ed. Sydney, Australia: Reed New Holland.
47. Lindenmayer DB, MacGregor C, Welsh A, Donnelly CF, Brown D, (2008) The use of hollows and dreys by the common ringtail possum (Pseudocheirus peregrinus) in different vegetation types. Australian Journal of Zoology 56: 1-11.
48. Augee ML, Smith B, Rose S, (1996) Survival of wild and hand-reared ringtail possums (Pseudocheirus peregrinus) in bushland near Sydney. Wildlife Research 23: 99-108.
49. Russell BG, Smith B, Augee ML, (2003) Changes to a population of common ringtail possums (Pseudocheirus peregrinus) after bushfire. Wildlife Research 30: 389-396.
50. Triggs B, Brunner H, Cullen JM, (1984) The food of fox, dog and cat in Croajingalong National Park, southeastern Victoria. Australian Wildlife Research 11: 491-499.
51. Jessop TS, Urlus J, Lockwood T, Gillespie G, (2010) Preying possum: assessment of the diet of lace monitors (Varanus varius) from coastal forests in southeastern Victoria. Biawak 4: 59.
52. Sutherland DR, Glen AS, de Tores PJ, (2011) Could controlling mammalian carnivores lead to mesopredator release of carnivorous reptiles? Proceedings of the Royal Society B-Biological Sciences 278: 641-648.
53. Murray AJ, Poore RN, Dexter N (2006) Project Deliverance- the response of 'critical weight range' mammals to effective fox control in mesic forest habitats in far East Gippsland, Victoria. Melbourne: Department of Sustainability and Environment.
54. Krebs CJ, Boutin S, Boonstra R, Sinclair ARE, Smith JNM, et al. (1995) Impact of food and predation on the snowshoe hare cycle. Science 269: 1112-1115.
55. Tilman D, (1994) Competition and biodiversity in spatially structured habitats. Ecology 75: 2-16.
56. Engeman RM, (2005) Indexing principles and a widely applicable paradigm for indexing animal populations. Wildlife Research 32: 203-210.
57. Wilson GJ, Delahay RJ, (2001) A review of methods to estimate the abundance of terrestrial carnivores using field signs and observation. Wildlife Research 28: 151-164.
58. Jessop TS, Hamann M, (2005) Interplay between age class, sex and stress response in green turtles (Chelonia mydas). Australian Journal of Zoology 53: 131-136.
59. Bocking AD, McMillen IC, Harding R, Thorburn GD, (1986) Effect of reduced uterine blood flow on fetal and maternal cortisol. Journal of Developmental Physiology 8: 237-245.
60. Wingfield JC, Romero LM (2001) Adrenocortical responses to stress and their modulation in free-living vertebrates. In: McEwan BS, editor. Coping with the Environment: Neural and Endocrine Mechanisms. New York: Oxford University Press. 211-236.
61. Hellgren EC, Lochmiller RL, Amoss MS, Grant WE, (1985) Endocrine and metabolic responses of the collared peccary (Tayassu tajacu) to immobilization with ketamine-hydrochloride. Journal of Wildlife Diseases 21: 417-425.
62. Reeder DM, Kosteczko NS, Kunz TH, Widmaier EP, (2004) Changes in baseline and stress-induced glucocorticold levels during the active period in free-ranging male and female little brown myotis, Myotis lucifugus (Chiroptera: Vespertilionidae). General and Comparative Endocrinology 136: 260-269.
63. Romero LM, Romero RC, (2002) Corticosterone responses in wild birds: the importance of rapid initial sampling. Condor 104: 129-135.
64. Cohen J (1988) Statistical Power Analysis for the Behavioral Sciences. New Jersey: Lawrence Erlbaum Associates.
65. Amarasekare P, (2002) Interference competition and species coexistence. Proceedings of the Royal Society of London Series B-Biological Sciences 269: 2541-2550.
66. Moseby K, Neilly H, Read J, Crisp H (2012) Interactions between a top order predator and exotic mesopredators in the Australian rangelands. International Journal of Ecology in press.
67. Dickman CR, (1992) Predation and habitat shift in the house mouse, Mus domesticus. Ecology 73: 313-322.
68. Molsher RL (1999) The ecology of feral cats (Felis catus) in open forest in New South Wales: interactions with food resources and foxes: University of Sydney.
69. Diment AN (2010) Monitoring the ecological impacts of invasive predator control [PhD thesis]: University of Sydney.
70. Jones M, Mandelik Y, Dayan T, (2001) Coexistence of temporally partitioned spiny mice: roles of habitat structure and foraging behavior. Ecology 82: 2164-2176.
71. Harrington LA, Harrington AL, Yamaguchi N, Thom MD, Ferreras P, et al. (2009) The impact of native competitors on an alien invasive: temporal niche shifts to avoid interspecific aggression? Ecology 90: 1207-1216.
72. Byers JE, (2000) Competition between two estuarine snails: Implications for invasions of exotic species. Ecology 81: 1225-1239.
73. Holway DA, (1999) Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecology 80: 238-251.
74. Risbey DA, Calver MC, Short J, Bradley JS, Wright IW, (2000) The impact of cats and foxes on the small vertebrate fauna of Heirisson Prong, Western Australia. II. A field experiment. Wildlife Research 27: 223-235.
75. Buckmaster T (2011) Ecology and management of feral cats in Far East Gippsland, Victoria. [PhD thesis]: University of Sydney.
76. McLean IG, Lundie-Jenkins G, Jarman PJ, (1996) Teaching an endangered mammal to recognise predators. Biological Conservation 75: 51-62.
77. Banks PB, Dickman CR, Newsome AE, (1998) Ecological costs of feral predator control: Foxes and rabbits. Journal of Wildlife Management 62: 766-772.
78. Griffin AS, Evans CS, Blumstein DT, (2001) Learning specificity in acquired predator recognition. Animal Behaviour 62: 577-589.
79. Russell BG, Banks PB, (2007) Do Australian small mammals respond to native and introduced predator odours? Austral Ecology 32: 277-286.
80. Banks PB, (1998) Responses of Australian bush rats, Rattus fuscipes, to the odor of introduced Vulpes vulpes. Journal of Mammalogy 79: 1260-1264.
81. McEvoy J, Sinn DL, Wapstra E, (2008) Know thy enemy: Behavioural response of a native mammal (Rattus lutreolus velutinus) to predators of different coexistence histories. Austral Ecology 33: 922-931.
82. Jones ME, Smith GC, Jones SM, (2004) Is anti-predator behaviour in Tasmanian eastern quolls (Dasyurus viverrinus) effective against introduced predators? Animal Conservation 7: 155-160.
83. Short J, Kinnear JE, Robley A, (2002) Surplus killing by introduced predators in Australia- evidence for ineffective anti-predator adaptations in native prey species? Biological Conservation 103: 283-301.
84. Sih A, Bolnick DI, Luttbeg B, Orrock JL, Peacor SD, et al. (2010) Predator-prey naivete, antipredator behavior, and the ecology of predator invasions. Oikos 119: 610-621.
85. Mateo JM, (2007) Ecological and hormonal correlates of antipredator behavior in adult Belding's ground squirrels (Spermophilus beldingi). Behavioral Ecology and Sociobiology 62: 37-49.
86. Berger S, Wikelski M, Romero LM, Kalko EK, Roedl T, (2007) Behavioral and physiological adjustments to new predators in an endemic island species, the Galapagos marine iguana. Hormones and Behavior 52: 653-663.
87. Banks PB, (1999) Predation by introduced foxes on native bush rats in Australia: do foxes take the doomed surplus? Journal of Applied Ecology 36: 1063-1071.
88. Gould J (1863) The mammals of Australia London: J. Gould.
89. Lydekker R (1896) A Hand-book to the Marsupialia and Monotremata. London: Edward Lloyd.
90. Hawlena D, Hughes KM, Schmitz OJ, (2011) Trophic trait plasticity in response to changes in resource availability and predation risk. Functional Ecology 25: 1223-1231.
91. Kats LB, Dill LM, (1998) The scent of death: Chemosensory assessment of predation risk by prey animals. Ecoscience 5: 361-394.
92. Anson JR, Dickman CR (2012) Behavioral responses of native prey to disparate predators: naiveté and predator recognition. Oecologia.