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Do yellow-bellied marmots respond to predator vocalizations?

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Abstract

We conducted four experiments to determine whether yellow-bellied marmots, Marmota flaviventris, discriminate among predator vocalizations, and if so, whether the recognition mechanism is learned or experience-independent. First, we broadcast to marmots the social sounds of coyotes, Canis latrans, wolves, Canis lupus, and golden eagles, Aquila chrysaetos, as well as conspecific alarm calls. Coyotes and eagles are extant predators at our study site, while wolves have been absent since the mid-1930s. In three follow-up experiments, we reversed the eagle call and presented marmots with forward and reverse calls to control for response to general properties of call structure rather than those specifically associated with eagles, we tested for novelty by comparing responses to familiar and unfamiliar birds, and we tested for the duration of predator sounds by comparing a wolf howl (that was much longer than the coyote in the first experiment) with a long coyote howl of equal duration to the original wolf. Marmots suppressed foraging and increased looking most after presentation of the conspecific alarm call and least after that of the coyote in the first experiment, with moderate responses to wolf and eagle calls. Marmots responded more to the forward eagle call than the reverse call, a finding consistent with a recognition template. Marmots did not differentiate vocalizations from the novel and familiar birds, suggesting that novelty itself did not explain our results. Furthermore, marmots did not differentiate between a wolf howl and a coyote howl of equal duration, suggesting that the duration of the vocalizations played a role in the marmots’ response. Our results show that marmots may respond to predators based solely on acoustic stimuli. The response to currently novel wolf calls suggests that they have an experience-independent ability to identify certain predators acoustically. Marmots’ response to predator vocalizations is not unexpected because 25 of 30 species in which acoustic predator discrimination has been studied have a demonstrated ability to respond selectively to cues from their predators.

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References

  • Abramsky Z, Strauss E, Subach A, Kotler BP, Riechman A (1996) The effect of barn owls (Tyto alba) on the activity and microhabitat selection of Gerbillus allenbyi and G. pyramidum. Oecologia 105:313–319

    Article  Google Scholar 

  • Armitage KB (1982) Yellow-bellied marmot. In: Davis DE (ed) CRC handbook of census methods for terrestrial vertebrates. CRC, Boca Raton, Florida, pp 148–149

    Google Scholar 

  • Berger J (1998) Future prey: some consequences of the loss and restoration of large carnivores. In: Caro TM (ed) Behavioral ecology and conservation biology. Oxford University Press, New York, pp 80–100

    Google Scholar 

  • Berger J, Swenson JE, Persson I-L (2001) Recolonizing carnivores and naive prey: conservation lessons from Pleistocene extinctions. Science 291:1036–1039

    Article  PubMed  CAS  Google Scholar 

  • Blumstein DT (1999) The evolution of functionally referential alarm communication: multiple adaptations; multiple constraints. Evol Commun 3:135–147

    Article  Google Scholar 

  • Blumstein DT (2006) The ‘multi-predator’ hypothesis and the evolutionary persistence of antipredator behaviour. Ethology 112:209–217

    Article  Google Scholar 

  • Blumstein DT, Armitage KB (1997) Alarm calling in yellow-bellied marmots: I. The meaning of situationally-specific calls. Anim Behav 53:143–171

    Article  Google Scholar 

  • Blumstein DT, Daniel JC, Griffin AS, Evans CS (2000a) Insular tammar wallabies (Macropus eugenii) respond to visual but not acoustic cues from predators. Behav Ecol 11:528–535

    Article  Google Scholar 

  • Blumstein DT, Evans CS, Daniel JC (2000b) JWatcher 0.9. An introductory user’s guide. http://www.jwatcher.ucla.edu

  • Blumstein DT, Daniel JC, Schnell MR, Ardron JG, Evans CS (2002) Anipredator behaviour of red-necked pademelons: a factor contributing to species survival? Anim Conserv 5:325–331

    Article  Google Scholar 

  • Bouskila A, Blumstein DT (1992) Rules of thumb for predation hazard assessment: predictions from a dynamic model. Am Nat 139:161–176

    Article  Google Scholar 

  • Bshary R, Noe R (1997) Anti-predation behaviour of red colobus monkeys in the presence of chimpanzees. Behav Ecol Sociobiol 41:321–333

    Article  Google Scholar 

  • Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, Chicago

    Google Scholar 

  • Charif RA, Mitchell S, Clark CW (1995) Canary 1.2 user’s manual. Cornell Laboratory of Ornithology, Ithaca, NY

    Google Scholar 

  • Cheney DL, Seyfarth RM (1990) How monkeys see the world. University of Chicago Press, Chicago

    Google Scholar 

  • Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum Assoc., Hillsdale, NJ

    Google Scholar 

  • Colorado Division of Wildlife (2004) Species conservation: gray wolf management. http://www.wildlife.state.co.us/species_cons/graywolf/index.asp

  • Coss RG (1999) Effects of relaxed natural selection on the evolution of behavior. In: Foster SA, Endler JA (eds) Geographic variation in behavior: perspectives on evolutionary mechanisms. Oxford University Press, Oxford, pp 180–208

    Google Scholar 

  • Crafford D, Ferguson J, Kemp A (1999) Why do grass owls (Tyto capensis) produce clicking calls? Raptor Res 33:134–142

    Google Scholar 

  • Deecke VB, Slater PJB, Ford JKB (2002) Selective habituation shapes acoustic predator recognition in harbour seals. Nature 420:171–173

    Article  PubMed  CAS  Google Scholar 

  • Durant SM (2000) Living with the enemy: avoidance of hyenas and lions by cheetahs in the Serengeti. Behav Ecol 11:624

    Article  Google Scholar 

  • Eilam D, Dayan T, Ben-Eliyahu S, Schulman I, Shefer G, Hendrie CA (1999) Differential behavioural and hormonal responses of voles and spiny mice to owl calls. Anim Behav 58:1085–1093

    Article  PubMed  Google Scholar 

  • Elliott D (2004) Yellowstone wolf found dead near Denver. Casper Star Tribune, Casper, WY

    Google Scholar 

  • Gebo DL, Chapman CA, Chapman LJ, Lambert J (1994) Locomotor response to predator threat in red-colobus monkeys. Primates 35:219–223

    Article  Google Scholar 

  • Gil-da-costa R, Palleroni A, Hauser MD, Touchton J, Kelley JP (2003) Rapid acquisition of an alarm response by a neotropical primate to a newly introduced avian predator. Proc R Soc Lond B 270:605–610

    Article  Google Scholar 

  • Griffin AS, Blumstein DT, Evans CS (2000) Training captive-bred or translocated animals to avoid predators. Conserv Biol 14:1317–1326

    Article  Google Scholar 

  • Griffin AS, Evans CS, Blumstein DT (2001) Learning specificity in acquired predator recognition. Anim Behav 62:577–589

    Article  Google Scholar 

  • Gursky S (2002) Determinants of gregariousness in the spectral tarsier (Prosimian: Tarsius spectrum). J Zool Lond 256:401–410

    Article  Google Scholar 

  • Gursky S (2003) Predation experiments on infant spectral tarsiers (Tarsius spectrum). Folia Primatol 74:272–284

    Article  PubMed  Google Scholar 

  • Hauser MD, Caffrey C (1994) Anti-predator response to raptor calls in wild crows, Corvus brachyrhynchos hesperis. Anim Behav 48:1469–1471

    Article  Google Scholar 

  • Hauser MD, Wrangham RW (1990) Recognition of predator and competitor calls in non-human primates and birds: a preliminary report. Ethology 86:116–130

    Article  Google Scholar 

  • Hendrie CA, Weiss SM, Eilam D (1998) Behavioural response of wild rodents to the calls of an owl: a comparative study. J Zool Lond 245:439–446

    Article  Google Scholar 

  • Jones ME, Smith GC, Jones SM (2004) Is anti-predator behaviour in Tasmanian eastern quolls (Dasyurus viverrinus) effective against introduced predators? Anim Conserv 7:155–160

    Article  Google Scholar 

  • Karpanty SM, Grella R (2001) Lemur responses to diurnal raptor calls in Ranomafana National Park, Madagascar. Folia Primatol 72:100–103

    Article  PubMed  CAS  Google Scholar 

  • Kelley JL, Magurran AE (2003) Learned predator recognition and antipredator responses in fishes. Fish Fish 5:216–226

    Google Scholar 

  • Keppel GL (1991) Design and analysis: a researcher’s handbook, 3rd edn. Prentice Hall, Englewood Cliffs, NJ

    Google Scholar 

  • Kristensen EA, Closs GP (2004) Anti-predator response of naive and experienced common bully to chemical alarm cues. J Fish Biol 64:643–652

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • Macedonia JM, Yount PL (1991) Auditory assessment of avian predator threat in semi-captive ringtailed lemurs (Lemur catta). Primates 32:169–182

    Article  Google Scholar 

  • Macromedia (1995) SoundEdit 16. Macromedia, Inc., San Francisco

  • Maddison WP, Maddison DR (2001) MacClade: analysis of phylogeny and character evolution. Version 4.03. Sinauer Associates, Sunderland, MA

  • McKenna MC, Bell SK (1997) Classification of mammals above the species level. Columbia University Press, New York

    Google Scholar 

  • Noë R, Bshary R (1997) The formation of red colobus-diana monkey associations under predation pressure from chimpanzees. Proc R Soc Lond B 264:253–259

    Article  Google Scholar 

  • Petrzelkova K, Zukal J (2001) Emergence behaviour of the serotine bat (Eptesicus serotinus) under predation risk. Neth J Zool 51:395–414

    Article  Google Scholar 

  • Pusenius J, Ostfeld RS (2000) Effects of stoat’s presence and auditory cues indicating its presence on tree seedling predation by meadow voles. Oikos 91:123–130

    Article  Google Scholar 

  • Pyare S, Cain S, Moody D, Schwartz C, Berger J (2004) Carnivore re-colonisation: reality, possibility and a non-equilibrium century for grizzly bears in the southern Yellowstone ecosystem. Anim Conserv 7:71–77

    Article  Google Scholar 

  • Rainey HJ, Zuberbühler K, Slater PJB (2004) Hornbills can distinguish between primate alarm calls. Proc R Soc Lond B 271:755–759

    Article  Google Scholar 

  • Searcy YM, Caine NG (2003) Hawk calls elicit alarm and defensive reactions in captive Geoffroy’s Marmosets (Callithrix geoffroyi). Folia Primatologica 74:115–125

    Article  Google Scholar 

  • Stewart D (2000) Australian bird calls favourites. Nature Sound, Mullumbimby, NSW

    Google Scholar 

  • SPSS, Inc. (2002) SPSS-11 for the Macintosh. SPSS Inc., Chicago, IL

  • Swaisgood RR, Rowe MP, Owings DH (1999) Assessment of rattlesnake dangerousness by California ground squirrels: exploitation of cues from rattling sounds. Anim Behav 57:1301–1310

    Article  PubMed  Google Scholar 

  • Treves A (1999) Has predation shaped the social systems of arboreal primates? Int J Primatol 20:35–67

    Article  Google Scholar 

  • Van Vuren D (2001) Predation on yellow-bellied marmots (Marmota flaviventris). Am Midl Nat 145:94–100

    Article  Google Scholar 

  • Warren ER (1942) The mammals of Colorado: their habits and distribution, 2 edn. University of Oklahoma Press, Norman

    Google Scholar 

  • Wilson DE, Reeder DM (1993) Mammal species of the world: a taxonomic and geographic reference, 2nd edn. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • Zuberbühler K (2000) Causal knowledge of predators’ behaviour in wild Diana monkeys. Anim Behav 59:209–220

    Article  PubMed  Google Scholar 

  • Zuberbühler K (2001) Predator-specific alarm calls in Campbell’s monkeys, Cercopithecus campbelli. Behav Ecol Sociobiol 50:414–422

    Article  Google Scholar 

  • Zuberbühler K, Cheney DL, Seyfarth RM (1999) Conceptual semantics in a nonhuman primate. J Comp Psychol 113:33–42

    Article  Google Scholar 

Download references

Acknowledgments

Louise Cooley was an NSF-REU fellow during this research. We thank Dan Jones for fast Ethernet, and for help trapping marmots, Esa Crumb, Louise Lochhead, Mark Luterra, Lucas Moyer-Horner, Amanda Nicodemus, Lucretia Olsen, Arpat Ozgul, David Pelletier, Weiwei Shen, Brian Smith, Tricia Stark, Ryan Trojan, Tyler Van Fleet, Thea Wang, Tina Wey, and Veronica Yovovich. Research protocols were approved by both the Rocky Mountain Biological Laboratory (RMBL) and by the University of California Los Angeles (UCLA) Animal Research Committee (No. 2001-191-03 approved on 3/8/04). Marmots were trapped under permits issued by the Colorado Division of Wildlife. Partial support for this research came from NSF-DBI-0242960 (to RMBL), the UCLA Faculty Senate Faculty Research Grants, a UCLA Assistant Professor’s Initiative grant, and the UCLA Division of Life Sciences Dean’s recruitment and retention funds (to DTB). We are extremely grateful to Peter Bednekoff and two anonymous reviewers whose comments helped us shorten the paper and improve its clarity.

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Correspondence to Daniel T. Blumstein.

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Communicated by P. Bednekoff

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Blumstein, D.T., Cooley, L., Winternitz, J. et al. Do yellow-bellied marmots respond to predator vocalizations?. Behav Ecol Sociobiol 62, 457–468 (2008). https://doi.org/10.1007/s00265-007-0473-4

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