Behavioral Ecology and Sociobiology

, Volume 62, Issue 10, pp 1551–1558

Rats on the run: removal of alien terrestrial predators affects bush rat behaviour

  • Axel Strauß
  • Katrin Y. Solmsdorff
  • Roger Pech
  • Jens Jacob
Original Paper

Abstract

Predators can strongly influence the microhabitat use and foraging behaviour of prey. In a large-scale replicated field experiment in East Gippsland, Australia, we tested the effects of reduced alien red fox (Vulpes vulpes) and alien wild dog (Canis lupus familiaris) abundance (treatment) on native bush rat (Rattus fuscipes) behaviour. Bush rats are exposed to two main guilds of predators, namely mammalian carnivores and birds of prey. Tracking rat movements using the spool-and-line technique revealed that, in treatment sites, rats used ground cover, which provides shelter from predators, less often than at unmanipulated fox and wild dog abundance (non-treatment sites). In treatment sites, rats more frequently moved on logs where they would have been exposed to hunting foxes and dogs than in non-treatment sites. Furthermore, in treatments, rats showed a preference for understorey but not in non-treatments. Hence, bush rats adapted their behaviour to removal of alien terrestrial predators. Giving-up densities (GUDs) indicated no treatment effects on the marginal feeding rate of bush rats. Interestingly, GUDs were higher in open patches than in sheltered patches, suggesting higher perceived predation risk of bush rats during foraging at low versus high cover. The lack of treatment effects on GUDs but the clear response of bush rats to cover may be explained by the impact of predators other than foxes and wild dogs.

Keywords

Predation risk Microhabitat use Foraging behaviour GUD Alien predator 

References

  1. Abramsky Z, Rosenzweig ML, Belmaker J, Bar A (2004) The impact of long-term continuous risk of predation on two species of gerbils. Can J Zool 82:464–474CrossRefGoogle Scholar
  2. Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29:1123–1144PubMedCrossRefGoogle Scholar
  3. Arthur AD, Pech RP, Dickman CR (2004a) Habitat structure mediates the non-lethal effects of predation on enclosed populations of house mice. J Anim Ecol 73:867–877CrossRefGoogle Scholar
  4. Arthur AD, Pech RP, Dickman CR (2004b) Effects of predation and habitat structure on the population dynamics of house mice in large outdoor enclosures. Oikos 108:562–572CrossRefGoogle Scholar
  5. Banks PB (1998) Responses of Australian bush rats, Rattus fuscipes, to the odour on introduced Vulpes vulpes. J Mammal 79:1260–1264CrossRefGoogle Scholar
  6. Banks PB (1999) Predation by introduced foxes on native bush rats in Australia: do foxes take the doomed surplus? J Appl Ecol 36:1063–1071CrossRefGoogle Scholar
  7. Banks PB (2001) Predation sensitive grouping and habitat use by eastern grey kangaroos: a field experiment. Anim Behav 61:1013–1021CrossRefGoogle Scholar
  8. Banks PB, Hughes N, Rose T (2003) Do native Australian small mammals avoid faeces of domestic dogs? Responses of Rattus fuscipes and Antechinus stuartii. Aust Zool 32:406–409Google Scholar
  9. Bilney RJ, Cooke R, White J (2006) Change in the diet of sooty owls (Tyto tenebricosa) since European settlement: from terrestrial to arboreal prey and increased overlap with powerful owls. Wildl Res 33:17–24CrossRefGoogle Scholar
  10. Bouskila A (2001) A habitat selection game of interactions between rodents and their predators. Ann Zool Fenn 38:55–70Google Scholar
  11. Breder RB (1927) Turtle trailing: a new technique for studying the life habits of certain Testudinata. Zoologica 9:231–243Google Scholar
  12. Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22:37–47CrossRefGoogle Scholar
  13. Brown JS (1992) Patch use under predation risk: I. models and predictions. Ann Zool Fenn 29:301–309Google Scholar
  14. Brown JS, Kotler BP, Smith RJ, Wirtz WO II (1988) The effects of owl predation on the foraging behavior of heteromyid rodents. Oecologia 76:408–415Google Scholar
  15. Brown JS, Morgan RA, Dow BD (1992) Patch use under predation risk: II. A test with fox squirrels, Sciurus niger. Ann Zool Fenn 29:311–318Google Scholar
  16. Charnov EL (1976) Optimal foraging, marginal value theorem. Theor Popul Biol 9:129–136PubMedCrossRefGoogle Scholar
  17. Cheal DC (1987) The diets and dietary preferences of Rattus fuscipes and Rattus lutreolus at Walkerville in Victoria. Aust Wildl Res 14:35–44CrossRefGoogle Scholar
  18. Dickman CR (1996) Impact of exotic generalist predators on the native fauna of Australia. Wildl Biol 2:185–195Google Scholar
  19. Edmunds M (1974) Defence in animals. A survey of antipredator defenses. Longman Group, New YorkGoogle Scholar
  20. Edwards GP, Preu ND, Crealy IV, Shakeshaft BJ (2002) Habitat selection by feral cats and dingoes in a semi-arid woodland environment in central Australia. Austral Ecology 27:26–31CrossRefGoogle Scholar
  21. Fey K, Banks PB, Korpimäki E (2006) Different microhabitat preferences of field and bank voles under manipulated predation risk from an alien predator. Ann Zool Fenn 43:9–16Google Scholar
  22. Fitzgerald M, Shine R, Lemckert F (2004) Life history attributes of the threatened Australian snake (Stephen’s banded snake Hoplocephalus stephensii, Elapidae). Biol Conserv 119:121–128CrossRefGoogle Scholar
  23. Fleming P, Corbett L, Harden R, Thomson P (2001) Managing the impacts of dingoes and other wild dogs. Bureau of Rural Sciences, CanberraGoogle Scholar
  24. Green K (2003) Altitudinal and temporal differences in the food of foxes (Vulpes vulpes) at alpine and subalpine altitudes in the Snowy Mountains. Wildl Res 30:245–253CrossRefGoogle Scholar
  25. Griffin PC, Griffin SC, Waroquiers C, Mills LS (2005) Mortality by moonlight: predation risk and the snowshoe hare. Behav Ecol 16:938–944CrossRefGoogle Scholar
  26. Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Evol Ecol 19:470–474CrossRefGoogle Scholar
  27. Hayes RA, Nahrung HF, Wilson JC (2006) The response of native Australian rodents to predator odours varies seasonally: a by-product of life history variation? Anim Behav 71:1307–1314CrossRefGoogle Scholar
  28. Henry JD (1996) Red fox: the catlike canine. Smithsonian Books, WashingtonGoogle Scholar
  29. Hutchings SD (1996) The effects of a fox removal program on small and medium sized mammal population dynamics within the Anglesea Heathlands, Victoria. Masters thesis, Deakin University, MelbourneGoogle Scholar
  30. Ivlev VS (1961) Experimental ecology of the feeding of fishes. Yale University Press, New HavenGoogle Scholar
  31. Jacob J, Brown JS (2000) Microhabitat use, giving-up densities and temporal activity as short and long term anti-predator behaviors in common voles. Oikos 91:131–138CrossRefGoogle Scholar
  32. Jedrzejewski W, Rychlik L, Jedrzejewska B (1993) Responses of bank voles to odours of 7 species of predators—experimental data and their relevance to natural predator–vole relationships. Oikos 68:251–257CrossRefGoogle Scholar
  33. Kearney N, Handasyde K, Ward S, Kearney M (2007) Fine-scale microhabitat selection for dense vegetation in a heathland rodent, Rattus lutreolus: insights from intraspecific and temporal patterns. Austral Ecology 32:315–325CrossRefGoogle Scholar
  34. Kinnear J, Sumner N, Onus M (2002) The red fox in Australia: an exotic predator turned biocontrol agent. Biol Conserv 108:335–359CrossRefGoogle Scholar
  35. Koivisto E, Pusenius J (2003) Effects of temporal variation in the risk of predation by least weasel (Mustela nivalis) on feeding behavior of field vole (Microtus agrestis). Evol Ecol 17:477–489CrossRefGoogle Scholar
  36. Korpimäki E, Krebs CJ (1996) Predation and population cycles of small mammals. BioScience 46:754–764CrossRefGoogle Scholar
  37. Kotler BP, Holt RD (1989) Predation and competition—the interaction of two types of species interactions. Oikos 54:256–260CrossRefGoogle Scholar
  38. Kotler BP, Brown JS, Hasson O (1991) Factors affecting gerbil foraging behavior and rates of owl predation. Ecology 72:2249–2260CrossRefGoogle Scholar
  39. Kotler BP, Blaustein L, Brown JS (1992) Predator facilitation: the combined effect of snakes and owls on the foraging behavior of gerbils. Ann Zool Fenn 29:199–206Google Scholar
  40. Kotler BP, Brown JS, Oldfield A, Thorson J, Cohen D (2001) Foraging substrate and escape substrate: patch use by three species of gerbils. Ecology 82:1781–1790CrossRefGoogle Scholar
  41. Lima SL (1998) Nonlethal effects in the ecology of predator–prey interactions—what are the ecological effects of anti-predator decision-making? BioScience 48:25–34CrossRefGoogle Scholar
  42. Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behaviour: the predation risk allocation hypothesis. Am Nat 153:649–659CrossRefGoogle Scholar
  43. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation—a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  44. Mappes T, Koskela E, Ylönen H (1998) Breeding suppression in voles under predation risk of small mustelids: laboratory or methodological artefact? Oikos 82:365–369CrossRefGoogle Scholar
  45. Meek PD, Saunders G (2000) Home range and movement of foxes (Vulpes vulpes) in coastal New South Wales, Australia. Wildl Res 27:663–668CrossRefGoogle Scholar
  46. Meyer MD, Valone TJ (1999) Foraging under multiple costs: the importance of predation, energetic, and assessment error costs to a desert forager. Oikos 87:571–579CrossRefGoogle Scholar
  47. Mitchell BD, Banks PB (2005) Do wild dogs exclude foxes? Evidence for competition from dietary and spatial overlaps. Austral Ecology 30:581–591CrossRefGoogle Scholar
  48. Newsome AE (1991) Dingo. In: Strahan R (ed) Complete book of Australian mammals. Collins Angus & Robertson, Sydney, pp 483–485Google Scholar
  49. Olszewski JL (1968) Role of uprooted trees in movements of rodents in forests. Oikos 19:99–104CrossRefGoogle Scholar
  50. Parsons GJ, Bondrup-Nielsen S (1996) Experimental analysis of behaviour of meadow voles (Microtus pennsylvanicus) to odours of the short-tailed weasel (Mustela erminea). Ecoscience 3:63–69Google Scholar
  51. Pickett KN, Hik DS, Newsome AE, Pech RP (2005) The influence of predation risk on foraging behaviour of brushtail possums in Australian woodlands. Wildl Res 32:121–130CrossRefGoogle Scholar
  52. 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. Wildl Res 27:223–235CrossRefGoogle Scholar
  53. Robinson AC (1987) The ecology of the bush rat, Rattus fuscipes (Rodentia: Muridae), in Sherbrook Forest, Victoria. Aust Mammal 11:35–49Google Scholar
  54. Robley A, Wright J (2004) Adaptive experimental management of foxes. Annual Report July 2003–June 2004. Parks Victoria Technical Series No. 20, Parks Victoria, MelbourneGoogle Scholar
  55. Rosenzweig ML, MacArthur RH (1963) Graphical representation and stability conditions of predator-prey interactions. Am Nat 97:209–223CrossRefGoogle Scholar
  56. Russell BG, Banks PB (2007) Do Australian small mammals respond to native and introduced predator odours. Austral Ecology 32:277–286CrossRefGoogle Scholar
  57. S-Plus (2002) S-PLUS 6.1 Professional. Insightful Corp., SeattleGoogle Scholar
  58. Salo P, Korpimäki E, Banks PB, Nordström M, Dickman CR (2007) Alien predators are more dangerous than native predators to prey population. Proc R Soc B 274:1237–1243 (See also appendixes 2 and 3)PubMedCrossRefGoogle Scholar
  59. Seebeck JH (1978) Diet of fox Vulpes vulpes in a western Victorian forest. Aust J Ecol 3:105–108CrossRefGoogle Scholar
  60. Seebeck J, Menkhorst P (2000) Status and conservation of the rodents of Victoria. Wildl Res 27:357–369CrossRefGoogle Scholar
  61. SPSS (2001) SPSS for Windows, release 11.0.1. SPSS, ChicagoGoogle Scholar
  62. Stapley J (2003) Differential avoidance of snake odours by a lizard: evidence for prioritized avoidance based on risk. Ethology 109:785–796CrossRefGoogle Scholar
  63. Stapley J (2004) Do mountain log skinks (Pseudemoia entrecasteauxii) modify their behaviour in the presence of two predators? Behav Ecol Sociobiol 56:185–189CrossRefGoogle Scholar
  64. Stickel LF (1950) Populations and home range relationships of the box turtle, Terrapene c. carolina (Linnaeus). Ecol Monogr 20:353–378CrossRefGoogle Scholar
  65. Stokes VL, Pech RP, Banks PB, Arthur AD (2004) Foraging behaviour and habitat use by Antechinus flavipes and Sminthopsis murina (Marsupialia: Dasyuridae) in response to predation risk in eucalypt woodland. Biol Conserv 117:331–342CrossRefGoogle Scholar
  66. Sutherland DR, Predavec M (1999) The effects of moonlight on microhabitat use by Antechinus agilis (Marsupialia: Dasyuridae). Aust J Zool 47:1–17CrossRefGoogle Scholar
  67. Taylor JM, Calaby JH (1988) Rattus fuscipes. Mamm Species 298:1–3Google Scholar
  68. White JG, Gubiani R, Smallman N, Snell K, Morton A (2006) Home range, habitat selection and diet of foxes (Vulpes vulpes) in a semi-urban riparian environment. Wildl Res 33:175–180CrossRefGoogle Scholar
  69. Ylönen H, Jacob J, Davies M, Singleton G (2002) Predation risk and habitat selection of Australian house mice (Mus domesticus) during an incipient plague: desperate behaviour during food depletion. Oikos 99:284–289CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Axel Strauß
    • 1
    • 2
    • 3
  • Katrin Y. Solmsdorff
    • 1
    • 4
  • Roger Pech
    • 1
    • 5
  • Jens Jacob
    • 1
    • 6
  1. 1.CSIRO Sustainable EcosystemsCanberraAustralia
  2. 2.Institute of EcologyFriedrich-Schiller-University JenaJenaGermany
  3. 3.Division of Evolutionary Biology, Zoological InstituteTechnical University of BraunschweigBraunschweigGermany
  4. 4.HamelnGermany
  5. 5.Landcare ResearchLincolnNew Zealand
  6. 6.Federal Biological Research Centre for Agriculture and ForestryInstitute for Nematology and Vertebrate ResearchMünsterGermany

Personalised recommendations