The scent of your enemy is my friend? The acquisition of large carnivore scent by a smaller carnivore

Abstract

Scent marking is critical to intraspecific communication in many mammal species, but little is known regarding its role in communication among different species. We used 4 years of motion-triggered video to document the use of scent marking areas—termed “community scrapes”—by pumas (Puma concolor) (http://www.momo-p.com/showdetail-e.php?movieid=momo160812pc01a) and other carnivore species. We found that gray foxes (Urocyon cinereoargenteus) routinely rubbed their cheeks on puma scrapes (http://www.momo-p.com/showdetail-e.php?movieid=momo160812uc01a), and tested a series of hypotheses to determine its function. We found that gray foxes selected puma scrapes over other objects, and cheek rubbing by foxes was also correlated with how recently a puma had visited the scrape, suggesting that foxes were intent upon accumulating fresh puma scent. Cheek rubbing by foxes was not correlated with their breeding season or with how recently another fox had visited the site. Finally we found a cascading pattern in the occurrence of pumas, coyotes (Canis latrans) and gray foxes at community scrapes, suggesting that gray foxes may use puma scent to deter predation. This is the first published study to find evidence of a subordinate species using the scent of a dominant species to communicate with heterospecifics. The behavioral cascade we found in scent marking patterns also suggests that scent marking could be a mechanism that impacts the distribution and abundance of species. Additional videos pertaining to this article include http://www.momo-p.com/showdetail-e.php?movieid=momo160812uc02a, and http://www.momo-p.com/showdetail-e.php?movieid=momo160812uc03a.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Allen ML, Wittmer HU, Wilmers CC (2014) Puma scrape and communication behaviors: understanding functional use and variation by sex and age. Behaviour 151:819–840

    Article  Google Scholar 

  2. Allen ML, Wittmer HU, Houghtaling P, Smith J, Elbroch LM, Wilmers CC (2015a) The role of scent marking in mate selection by female pumas (Puma concolor). PLoS One 10:e0139087

    Article  PubMed  PubMed Central  Google Scholar 

  3. Allen ML, Elbroch LM, Wilmers CC, Wittmer HU (2015b) The comparative effects of large carnivores on the acquisition of carrion by scavengers. Am Nat 185:822–833

    Article  PubMed  Google Scholar 

  4. Allen ML, Yovovich V, Wilmers CC (2016) Evaluating the responses of a territorial solitary carnivore to potential mates and competitors. Sci Rep 6:27257

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. 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. Neuro Biobehav Rev 29:1123–1144

    Article  Google Scholar 

  6. Bel MC, Coulon J, Sreng L, Allaine D, Bagneres AG, Clement JL (1999) Social signals involved in scent-marking behavior by cheek-rubbing in Alpine marmots (Marmota marmota). J Chem Ecol 25:2267–2283

    CAS  Article  Google Scholar 

  7. Bytheway JP, Carthey AJR, Banks PB (2013) Risk vs. reward: how predators and prey respond to aging olfactory cues. Behav Ecol Sociobiol 67:715–725

    Article  Google Scholar 

  8. Darnell AM, Graf JA, Somers MJ, Slotow R, Gunther MS (2014) Space use of African wild dogs in relation to other large carnivores. PLoS One 9:e98846

    Article  PubMed  PubMed Central  Google Scholar 

  9. Fritzell EK, Haroldson KJ (1982) Urocyon cinereoargenteus. Mamm Spec 189:1–8

    Article  Google Scholar 

  10. Garvey PM, Glen AS, Pech RP (2016) Dominant predator odour triggers caution and eavesdropping behavior in a mammalian mesopredator. Behav Ecol Sociobiol 70:481–492

    Article  Google Scholar 

  11. Goodale E, Beauchamp G, Magrath RD, Nieh JC, Ruxton GD (2010) Interspecific information transfer influences animal community structure. Trends Ecol Evol 25:354–361

    Article  PubMed  Google Scholar 

  12. Gosling LM, McKay HV (1990) Scent-rubbing and status signaling by male mammals. Chemoecology 1:92–95

    Article  Google Scholar 

  13. Henry JD (1977) The use of urine marking in the scavenging behavior of the red fox (Vulpes vulpes). Behaviour 61:82–105

    CAS  Article  PubMed  Google Scholar 

  14. Hughes NK, Kelley JL, Banks PB (2012) Dangerous liaisons: the predation risks of receiving social signals. Ecol Lett 15:1326–1339

    Article  PubMed  Google Scholar 

  15. Johnson RP (1973) Scent marking in mammals. Anim Behav 21:521–535

    Article  Google Scholar 

  16. King SRB, Gurnell J (2007) Scent-marking behaviour by stallions: an assessment of function in a reintroduced population of Przewalski horses (Equus ferus przewalskii). J Zool 272:30–36

    Article  Google Scholar 

  17. Levi T, Wilmers CC (2012) Wolves-coyotes-foxes: a cascade among carnivores. Ecology 93:921–929

    Article  PubMed  Google Scholar 

  18. Li J, Schaller GB, McCarthy TM, Wang D, Jiagong Z, Cai P, Basang L, Lu Z (2013) A communal signpost of snow leopards (Panthera uncia) and other species on the Tibetan Plateau, China. Int J Biodivers 2013:370905

    Article  Google Scholar 

  19. Magrath RD, Haff TM, Fallow PM, Radford AN (2015) Eavesdropping on heterospecific alarm calls: from mechanisms to consequences. Biol Rev 90:560–586

    Article  PubMed  Google Scholar 

  20. Mellen JD (1993) A comparative analysis of scent–marking, social and reproductive behavior in 20 species of small cats. Am Zool 33:151–166

    Article  Google Scholar 

  21. Mykytowycz R (1965) Further observations on the territorial function and histology of the submandibular cutaneous (chin) glands in the rabbit, Oryctolagus cuniculus (L.). Anim Behav 13:400–412

    CAS  Article  PubMed  Google Scholar 

  22. Ordiz A, Stoen OG, Saebo S, Kindberg J, Delibes M, Swenson JE (2012) Do bears know they are being hunted? Biol Conserv 152:21–28

    Article  Google Scholar 

  23. Pineiro A, Barja I (2015) Evaluating the function of wildcat faecal marks in relation to the defence of favourable hunting areas. Ethol Ecol Evol 27:161–172

    Article  Google Scholar 

  24. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, ISBN 3-900051-07-0. http://www.R-project.org/. Accessed 25 Sept 2015

  25. Ralls K (1971) Mammalian scent marking. Science 171:443–449

    CAS  Article  PubMed  Google Scholar 

  26. Reiger I (1979) Scent rubbing in carnivores. Carnivore 2:17–25

    Google Scholar 

  27. Roper TJ, Conradt L, Butler J, Christian S, Ostler J, Schmid TK (1993) Territorial marking with faeces in badgers (Meles meles): a comparison of boundary and hinterland latrine use. Behaviour 127:289–307

    Article  Google Scholar 

  28. Rostain R, Ben-David M, Groves P, Randall JA (2004) Why do river otters scent-mark? An experimental test of several hypotheses. Anim Behav 68:703–711

    Article  Google Scholar 

  29. Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39

    CAS  Article  PubMed  Google Scholar 

  30. Shriner WM (1998) Yellow-bellied marmot and golden-mantled ground squirrel responses to heterospecific alarm calls. Anim Behav 55:529–536

    CAS  Article  PubMed  Google Scholar 

  31. Sokal RS, Rohlf FJ (1987) Introduction to biostatistics. W.H. Freeman and Company, New York

    Google Scholar 

  32. Wang Y, Allen ML, Wilmers CC (2015) Mesopredator spatial and temporal responses to large predators and human development in the Santa Cruz Mountains of California. Biol Conserv 190:23–33

    Article  Google Scholar 

  33. Wilmers CC, Wang Y, Nickel B, Houghtaling P, Shakeri Y, Allen ML, Kermish-Wells J, Yovovich V, Williams T (2013) Scale dependent behavioral responses to human development by a large predator, the puma. PLoS One 8:e60590

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

Funding was provided by NSF Grants 0963022 and 1255913, the Gordon and Betty Moore Foundation, and the University of California at Santa Cruz. We thank P. Houghtaling, Y. Shakeri, R. Peterson, and numerous technicians and volunteers for their help on the project.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Maximilian L. Allen.

About this article

Verify currency and authenticity via CrossMark

Cite this article

Allen, M.L., Gunther, M.S. & Wilmers, C.C. The scent of your enemy is my friend? The acquisition of large carnivore scent by a smaller carnivore. J Ethol 35, 13–19 (2017). https://doi.org/10.1007/s10164-016-0492-6

Download citation

Keywords

  • Cheek rubbing
  • Communication
  • Interspecific interactions
  • Puma concolor
  • Scent marking
  • Urocyon cinereoargenteus