Advertisement

Behavioral Ecology and Sociobiology

, Volume 70, Issue 11, pp 1831–1841 | Cite as

Sympatric predator odour reveals a competitive relationship in size-structured mammalian carnivores

  • Georgina E. AndersenEmail author
  • Christopher N. Johnson
  • Menna E. Jones
Original Article

Abstract

Interspecific competition between sympatric carnivores can have a profound effect on the structure, function and composition of ecosystems. Interspecific competition is often asymmetrical and the smaller carnivore is usually affected the most. We investigated the behavioural responses of two native species, the larger Tasmanian devil (Sarcophilus harrisii) and the smaller spotted-tailed quoll (Dasyurus maculatus) to each other’s odour and to that of an introduced predator, the feral cat (Felis catus), in north-west Tasmania, Australia. We used an experimental array of camera traps, in which carnivore scats were added as treatments. Behavioural responses exhibited by devils and quolls are indicative of a dominant predator-mesopredator relationship and suggest the potential for interspecific competition. The larger predator, the devil, was as vigilant at quoll odour as at control camera traps, but showed decreased vigilance at cat odour and did not avoid cat or quoll odours. The smaller predator, the spotted-tailed quoll, increased its vigilance near devil odour compared to control camera traps but did not avoid it. This experiment shows that assessing the behavioural responses of sympatric carnivores to each other’s odour can help understand predator interactions and reveal the potential for interspecific competition. Understanding these interactions is crucial in managing and conserving carnivores.

Significance statement

Animals navigate through an environment full of faecal odours left by predators, competitors and conspecifics. These odours provide information on both the immediate presence and the indirect risk of encountering a predator or an aggressive competitor. Tasmania’s largest predator, the Tasmanian devil, coexists with the smaller spotted-tailed quoll and the introduced feral cat. We tested the behavioural responses of Tasmanian devils and spotted-tailed quolls to each other’s faecal odour and to cat faecal odour. Behavioural patterns exhibited by predators in this experiment are indicative of a dominant predator-mesopredator relationship and suggest the potential for interspecific competition. Knowledge of the ecological interactions amongst sympatric carnivores can aid managers in making more informed decisions when trying to achieve specific conservation goals.

Keywords

Interspecific competition Behavioural response Predator odour Predator interactions Tasmanian devil Spotted-tailed quoll 

Notes

Acknowledgments

We are grateful to Tasmanian Parks and Wildlife Service for permission to work in the Arthur-Pieman Conservation Area. We are also grateful to Van Diemen’s Land Company and Hydro Tasmania for permission to work at Woolnorth. We thank all the volunteers that assisted with field work and Leon Barmuta for statistical advice. We also thank the two anonymous reviewers for their helpful feedback.

Compliance with ethical standards

Ethical Statement

All applicable international, national and/or institutional guidelines for the care and use of animals have been followed. This research was funded by grants from the Australian Research Council Discovery Scheme grant (DP110103069), the Holsworth Wildlife Research Endowment (grant number not available) and a Dr Eric Guiler Tasmanian Devil Research grant from the Save the Tasmanian Devil Appeal (grant number not available). The authors declare that they have no competing interests. All procedures performed in this study were in accordance with the ethical standards of the Animal Ethics Committee, University of Tasmania (Approval number A12361). This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

265_2016_2189_MOESM1_ESM.docx (22 kb)
ESM 1 ᅟ (DOCX 21 kb)
265_2016_2189_MOESM2_ESM.docx (22 kb)
ESM 2 ᅟ (DOCX 21 kb)

References

  1. Abbott I (2008) The spread of the cat, Felis catus, in Australia: re-examination of the current conceptual model with additional information. Conserv Sci W Aust 7:1–17Google Scholar
  2. Albone ES, Shirley SG (1984) Mammalian semiochemistry: the investigation of chemical signals between mammals. Wiley, ChichesterGoogle Scholar
  3. 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 29:1123–1144CrossRefPubMedGoogle Scholar
  4. Australian Bureau of Meteorology (2016) Australian Bureau of Meteorology. 2016. http://www.bom.gov.au/. Accessed 2 Apr 2016
  5. Banks PB, Nordstrom M, Ahola M, Salo P, Fey K, Korpimäki E (2008) Impacts of alien mink predation on island vertebrate communities of the Baltic Sea Archipelago: review of a long-term experimental study. Boreal Environ Res 13:3–16Google Scholar
  6. Beauchamp G (2015) Animal vigilance: monitoring predators and competitors. Academic, LondonGoogle Scholar
  7. Bitterlich W (1984) The relascope idea. relative measurements in forestry. Commonwealth Agricultural Bureaux, NorwichGoogle Scholar
  8. Brown RE, Macdonald DW (1985) Social odours in mammals. Clarendon, OxfordGoogle Scholar
  9. Buchmann OLK, Guiler ER (1977) Behaviour and ecology of the Tasmanian devil, Sarcophilus harrisii. In: Stonehouse B, Gilmore D (eds) The biology of marsupials. Macmillan Education, London, pp 155–168CrossRefGoogle Scholar
  10. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  11. Bytheway JP, Carthey AJR, Banks PB (2013) Risk vs. reward: how predators and prey respond to aging olfactory cues. Behav Ecol Sociobiol 67:715–725CrossRefGoogle Scholar
  12. Carthey AJR, Banks PB (2014) Naivete in novel ecological interactions: lessons from theory and experimental evidence. Biol Rev 89:932–949CrossRefPubMedGoogle Scholar
  13. Cox TE, Murray PJ, Bengsen AJ, Hall GP, Li XH (2015) Do fecal odors from native and non-native predators cause a habitat shift among macropods? Wildl Soc Bull 39:159–164CrossRefGoogle Scholar
  14. Dickman CR (1996) Overview of the impacts of feral cats on Australian native fauna. Australian Nature Conservation Agency, CanberraGoogle Scholar
  15. Donadio E, Buskirk SW (2006) Diet, morphology, and interspecific killing in carnivora. Am Nat 167:524–536CrossRefPubMedGoogle Scholar
  16. Durant SM (2000) Living with the enemy: avoidance of hyenas and lions by cheetahs in the Serengeti. Behav Ecol 11:624–632CrossRefGoogle Scholar
  17. Estes JA, Terborgh J, Brashares JS et al (2011) Trophic downgrading of planet earth. Science 333:301–306CrossRefPubMedGoogle Scholar
  18. Fancourt BA, Hawkins CE, Cameron EZ, Jones ME, Nicol SC (2015) Devil declines and catastrophic cascades: is mesopredator release of feral cats inhibiting recovery of the eastern quoll? PLoS One 10:e0119303CrossRefPubMedPubMedCentralGoogle Scholar
  19. Garvey PM, Glen AS, Pech RP (2015) Foraging Ermine Avoid Risk: behavioural responses of a mesopredator to its interspecific competitors in a mammalian guild. Biol Invasions 17:1771–1783CrossRefGoogle Scholar
  20. Garvey PM, Glen AS, Pech RP (2016) Dominant predator odour triggers caution and eavesdropping behaviour in a mammalian mesopredator. Behav Ecol Sociobiol 70:1–12CrossRefGoogle Scholar
  21. Glen AS, Dickman CR (2005) Complex interactions among mammalian carnivores in Australia, and their implications for wildlife management. Biol Rev 80:387–401CrossRefPubMedGoogle Scholar
  22. Gosling LM, Roberts SC (2001) Scent-marking by male mammals: cheat-proof signals to competitors and mates. In: Slater PJB, Rosenblatt JS, Snowdon CT, Roper TJ (eds) Adv Stud Behav 30:169–217Google Scholar
  23. Hawkins CE, Baars C, Hesterman H et al (2006) Emerging disease and population decline of an island endemic, the Tasmanian devil Sarcophilus harrisii. Biol Conserv 131:307–324CrossRefGoogle Scholar
  24. 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
  25. Hollings T (2013) Ecological effects of disease-induced apex predator decline. Dissertation, University of TasmaniaGoogle Scholar
  26. Hollings T, Jones M, Mooney N, McCallum H (2014) Trophic cascades following the disease-induced decline of an apex predator, the Tasmanian devil. Conserv Biol 28:63–75CrossRefPubMedGoogle Scholar
  27. Hughes NK, Kelley JL, Banks PB (2012) Dangerous liaisons: the predation risks of receiving social signals. Ecol Lett 15:1326–1339CrossRefPubMedGoogle Scholar
  28. Hughes NK, Korpimäki E, Banks PB (2010) The predation risks of interspecific eavesdropping: weasel-vole interactions. Oikos 119:1210–1216CrossRefGoogle Scholar
  29. Janssen A, Sabelis MW, Magalhaes S, Montserrat M, van der Hammen T (2007) Habitat structure affects intraguild predation. Ecology 88:2713–2719CrossRefPubMedGoogle Scholar
  30. Johnson CN (2006) Australia’s mammal extinctions: a 50,000 year history. Cambridge University Press, Port MelbourneGoogle Scholar
  31. Jones M (1995) Guild structure of the large marsupial carnivores in Tasmania. Dissertation, University of TasmaniaGoogle Scholar
  32. Jones ME, Barmuta LA (1998) Diet overlap and relative abundance of sympatric dasyurid carnivores: a hypothesis of competition. J Anim Ecol 67:410–421CrossRefGoogle Scholar
  33. Jones ME, Barmuta LA (2000) Niche differentiation among sympatric Australian dasyurid carnivores. J Mammal 81:434–447CrossRefGoogle Scholar
  34. Jones ME, Jarman PJ, Lees CM et al (2007) Conservation management of Tasmanian devils in the context of an emerging, extinction-threatening disease: Devil facial tumor disease. Ecohealth 4:326–337CrossRefGoogle Scholar
  35. Jones ME, Smith GC, Jones SM (2004) Is anti-predator behaviour in Tasmanian eastern quolls (Dasyurus viverrinus) effective against introduced predators? Anim Conserv 7:155–160CrossRefGoogle Scholar
  36. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394Google Scholar
  37. Lazenby B (2012) Do feral cats affect small mammals? A case study from the forests of southern Tasmania. Dissertation, University of SydneyGoogle Scholar
  38. Lazenby BT, Dickman CR (2013) Patterns of detection and capture are associated with cohabiting predators and prey. PLoS One 8, e59846CrossRefPubMedPubMedCentralGoogle Scholar
  39. Leo V, Reading RP, Letnic M (2015) Interference competition: odours of an apex predator and conspecifics influence resource acquisition by red foxes. Oecologia:1–8Google Scholar
  40. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation—a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  41. Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species. Invasive Species Specialist Group, AucklandGoogle Scholar
  42. Martin CW, Fodrie FJ, Heck KL, Mattila J (2010) Differential habitat use and antipredator response of juvenile roach (Rutilus rutilus) to olfactory and visual cues from multiple predators. Oecologia 162:893–902CrossRefPubMedGoogle Scholar
  43. Medina FM, Bonnaud E, Vidal E et al (2011) A global review of the impacts of invasive cats on island endangered vertebrates. Glob Change Biol 17:3503–3510CrossRefGoogle Scholar
  44. Meek PD, Ballard GA, Fleming PJS, Schaefer M, Williams W, Falzon G (2014) Camera traps can be heard and seen by animals. PLoS One 9:e11083210CrossRefGoogle Scholar
  45. Mukherjee S, Zelcer M, Kotler BP (2009) Patch use in time and space for a meso-predator in a risky world. Oecologia 159:661–668CrossRefPubMedGoogle Scholar
  46. Nudds TD (1977) Quantifying the vegetative structure of wildlife cover. Wildl Soc Bull 5:113–117Google Scholar
  47. Palomares F, Caro TM (1999) Interspecific killing among mammalian carnivores. Am Nat 153:492–508CrossRefGoogle Scholar
  48. Peacock D, Abbott I (2014) When the ‘native cat’ would ‘plague’: historical hyperabundance in the quoll (Marsupialia: Dasyuridae) and an assessment of the role of disease, cats and foxes in its curtailment. Aust J Zool 62:294–344CrossRefGoogle Scholar
  49. Pemberton D (1990) Social organisation and behaviour of the Tasmanian devil, Sarcophilus harrisii. Dissertation, University of TasmaniaGoogle Scholar
  50. Periquet S, Fritz H, Revilla E (2015) The lion king and the hyaena queen: large carnivore interactions and coexistence. Biol Rev 90:1197–1214CrossRefPubMedGoogle 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. Prugh LR, Stoner CJ, Epps CW, Bean WT, Ripple WJ, Laliberte AS, Brashares JS (2009) The rise of the mesopredator. Bioscience 59:779–791CrossRefGoogle Scholar
  53. Quenette PY (1990) Functions of vigilance behaviour in mammals—a review. Acta Oecola 11:801–818Google Scholar
  54. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. www.r-project.org/
  55. Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecol Lett 12:982–998CrossRefPubMedGoogle Scholar
  56. Ruibal M, Peakall R, Claridge A (2010) Socio-seasonal changes in scent-marking habits in the carnivorous marsupial Dasyurus maculatus at communal latrines. Aust J Zool 58:317–322CrossRefGoogle Scholar
  57. Van Dyck S, Strahan R (2008) The mammals of Australia, 3rd edn. Reed New Holland, SydneyGoogle Scholar
  58. Vazquez DP, Melian CJ, Williams NM, Bluthgen N, Krasnov BR, Poulin R (2007) Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:1120–1127CrossRefGoogle Scholar
  59. Webster H, McNutt JW, McComb K (2010) Eavesdropping and risk assessment between lions, spotted hyenas and African wild dogs. Ethology 116:233–239CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Georgina E. Andersen
    • 1
    Email author
  • Christopher N. Johnson
    • 1
  • Menna E. Jones
    • 1
  1. 1.School of Biological Sciences, University of TasmaniaHobartAustralia

Personalised recommendations