Animal Cognition

, Volume 13, Issue 6, pp 861–870 | Cite as

Comparing responses of four ungulate species to playbacks of baboon alarm calls

  • Dawn M. KitchenEmail author
  • Thore J. Bergman
  • Dorothy L. Cheney
  • James R. Nicholson
  • Robert M. Seyfarth
Original Paper


A growing body of evidence suggests that a wide range of animals can recognize and respond appropriately to calls produced by other species. Social learning has been implicated as a possible mechanism by which heterospecific call recognition might develop. To examine whether familiarity and/or shared vulnerability with the calling species might influence the ability of sympatric species to distinguish heterospecific alarm calls, we tested whether four ungulate species (impala: Aepyceros melampus; tsessebe: Damaliscus lunatus; zebra: Equus burchelli; wildebeest: Connochaetes taurinus) could distinguish baboon (Papio hamadryas ursinus) alarm calls from other loud baboon calls produced during intra-specific aggressive interactions (‘contest’ calls). Overall, subjects’ responses were stronger following playback of alarm calls than contest calls. Of the species tested, impala showed the strongest responses and the greatest difference in composite response scores, suggesting they were best able to differentiate call types. Compared with the other ungulate species, impala are the most frequent associates of baboons. Moreover, like baboons, they are susceptible to both lion and leopard attacks, whereas leopards rarely take the larger ungulates. Although it seems possible that high rates of association and/or shared vulnerability may influence impala’s greater ability to distinguish among baboon call types, our results point to a stronger influence of familiarity. Ours is the first study to compare such abilities among several community members with variable natural histories, and we discuss future experiments that would more systematically examine development of these skills in young ungulates.


Heterospecific alarm calls Baboon Impala Tsessebe Wildebeest Zebra 



We are grateful to the Office of the President of the Republic of Botswana and the Botswana Department of Wildlife and National Parks for permission to conduct this research. We thank J. Beehner, A. Mokupi, M. Mokupi, J. Rawle, C. McAllister and M. McAllister for support and assistance in the field, and four anonymous reviewers for suggestions. We are grateful to W. Smith, C. Shaw, I. Clark and the staff at Eagle Island Camp for use of vehicles and for friendship. Research was supported by National Science Foundation grant IBN 9514001, National Institute of Health Grant MH62249, The Leakey Foundation, the University of Pennsylvania, and The Ohio State University. This research adhered to the Animal Behavior Society Guidelines for the Use of Animals in Research, the legal requirements of Republic of Botswana, and institutional guidelines.

Conflict of interest statement

The authors declare that they have no conflict of interest.


  1. Aubin T (1991) Why do distress calls evoke interspecific responses? An experimental study applied to some species of birds. Behav Process 23:103–111CrossRefGoogle Scholar
  2. Blumstein DT, Armitage KB (1997) Alarm calling in yellow-bellied marmots. I. The meaning of situationally variable alarm calls. Anim Behav 53:143–171CrossRefGoogle Scholar
  3. Brown GE, Adrian JC, Smyth E, Leet H, Brennan S (2000) Ostariophysan alarm pheromones: laboratory and field tests of the functional significance of nitrogen oxides. J Chem Ecol 26:139–154CrossRefGoogle Scholar
  4. Busse C (1982) Leopard and lion predation upon chacma baboons living in the Moremi Wildlife Reserve. Botswana Notes Rec 12:15–21Google Scholar
  5. Caro TM (1995) Pursuit-deterrence revisited. Trends Ecol Evol 10:500–503CrossRefGoogle Scholar
  6. Caro TM, Graham CM, Stoner CJ, Vargas JK (2004) Adaptive significance of antipredator behaviour in artiodactyls. Anim Behav 67:205–228. doi: 10.1016/j.anbehav.2002.12.007 CrossRefGoogle Scholar
  7. Cheney DL, Seyfarth RM, Fischer J, Beehner J, Bergman T, Johnson SE, Kitchen DM, Palombit RA, Rendall D, Silk JB (2004) Factors affecting reproduction and mortality among baboons in the Okavango Delta, Botswana. Int J Primatol 25:401–428CrossRefGoogle Scholar
  8. Codron D, Codron J (2009) Reliability of δ13C and δ15N in faeces for reconstructing savanna herbivore diet. Mamm Biol 74:36–48CrossRefGoogle Scholar
  9. Codron D, Lee-Thorp JA, Sponheimer M, de Ruiter D, Codron J (2006) Inter- and intrahabitat dietary variability of chacma baboons (Papio ursinus) in South African savannas based on fecal δ13C, δ15N, and %N. Am J Phys Anthropol 129:204–214CrossRefPubMedGoogle Scholar
  10. Codron D, Codron J, Lee-Thorp JA, Sponheimer M, de Ruiter D, Sealy J, Grant R, Fourie N (2007) Diets of savanna ungulates from stable carbon isotope composition of faeces. J Zool 273:21–29CrossRefGoogle Scholar
  11. Coe R (2000) Effect size calculator. Durham University, Durham. Available via Accessed 9 Sept 2009
  12. Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Erlbaum, HillsdaleGoogle Scholar
  13. Cook M, Mineka S, Wolkenstein B, Laitsch K (1985) Observational conditioning of snake fear in unrelated rhesus monkeys. J Abnorm Psychol 94:591–610CrossRefPubMedGoogle Scholar
  14. Cowlishaw G (1994) Vulnerability to predation in baboon populations. Behaviour 131:293–304CrossRefGoogle Scholar
  15. de Kort SR, ten Cate C (2001) Response to interspecific vocalizations is affected by degree of phylogenetic relatedness in Streptopelia doves. Anim Behav 61:239–247. doi: 10.1006/anbe.2000.1552 CrossRefPubMedGoogle Scholar
  16. Ellery WN, Ellery K, McCarthy TS (1993) Plant distribution in island of the Okavango Delta, Botswana: determinants and feedback interactions. Afr J Ecol 31:118–134CrossRefGoogle Scholar
  17. Estes RD (1991) The behavior guide to African mammals. University of California Press, BerkeleyGoogle Scholar
  18. Fichtel C (2004) Reciprocal recognition of sifakas (Propithecus verreauxi verreauxi) and redfronted lemur (Eulemur fulvus rufus) alarm calls. Anim Cogn 7:45–52. doi: 10.1007/s10071-003-0180-0 CrossRefPubMedGoogle Scholar
  19. Fischer J, Hammerschmidt K, Cheney DL, Seyfarth RM (2001) Acoustic features of female chacma baboon barks. Ethology 107:33–54CrossRefGoogle Scholar
  20. Fischer J, Hammerschmidt K, Cheney DL, Seyfarth RM (2002) Acoustic features of male baboon loud calls: influences of context, age, and individuality. J Acoust Soc Am 111:1465–1474CrossRefPubMedGoogle Scholar
  21. Fischhoff IR, Sundaresan SR, Cordingley J, Rubenstein DI (2007) Habitat use and movements of plains zebra (Equus burchelli) in response to predation danger from lions. Behav Ecol 18:725–729CrossRefGoogle Scholar
  22. Forsman JT, Monkkonen M (2001) Responses by breeding birds to heterospecific song and mobbing call playbacks under varying predation risk. Anim Behav 62:1067–1073. doi: 10.1006/anbe.2001.1856 CrossRefGoogle Scholar
  23. Griffin AS (2004) Social learning about predators: a review and prospectus. Learn Behav 32:131–140PubMedGoogle Scholar
  24. Hamilton WJ, Buskirk RE, Buskirk WH (1976) Defense of space and resources by chacma (Papio ursinus) baboon troops in an African desert and swamp. Ecology 57:1264–1272CrossRefGoogle Scholar
  25. Hansen RM, Mugambi MM, Bauni SM (1985) Diets and trophic ranking of ungulates of the northern Serengeti Kenya. J Wildl Manag 49:823–829CrossRefGoogle Scholar
  26. Hasson O (1991) Pursuit-deterrent signals- communication between prey and predator. Trends Ecol Evol 6:325–329CrossRefGoogle Scholar
  27. Hauser MD (1988) How infant vervet monkeys learn to recognize starling alarm calls: the role of experience. Behaviour 105:187–201CrossRefGoogle Scholar
  28. Hayward MW, Kerley GIH (2008) Prey preferences and dietary overlap amongst Africa’s large predators. South Afr J Wildl Res 38:93–108CrossRefGoogle Scholar
  29. Hedges L, Olkin I (1985) Statistical methods for meta-analysis. Academic Press, New YorkGoogle Scholar
  30. Holm S (1979) A simple sequential rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  31. Johnson FR, McNaughton EJ, Shelley CP, Blumstein DT (2003) Mechanisms of heterospecific recognition in avian mobbing calls. Aust J Zool 51:577–585CrossRefGoogle Scholar
  32. Jurisevic MA, Sanderson KJ (1998) A comparative analysis of distress call structure in Australian passerine and non-passerine species: influence of size and phylogeny. J Avian Biol 29:61–71CrossRefGoogle Scholar
  33. Kingdon J (1988) East African mammals: an atlas of evolution in Africa. University of Chicago Press, ChicagoGoogle Scholar
  34. Kitchen DM, Cheney DL, Seyfarth RM (2003) Female baboons’ responses to male loud calls. Ethology 109:401–412CrossRefGoogle Scholar
  35. Lea AJ, Barrera JP, Tom LM, Blumstein DT (2008) Heterospecific eavesdropping in a nonsocial species. Behav Ecol 19:1041–1046. doi: 10.1093/beheco/arn064 CrossRefGoogle Scholar
  36. Lehmann MB, Funston PJ, Owen CR, Slotow R (2008) Feeding behaviour of lions (Panthera leo) on a small reserve. South Afr J Wildl Res 38:66–78CrossRefGoogle Scholar
  37. Magrath RD, Pitcher BJ, Gardner JL (2007) A mutual understanding? Interspecific responses by birds to each other’s aerial alarm calls. Behav Ecol 18:944–951. doi: 10.1093/beheco/arm063 CrossRefGoogle Scholar
  38. Magrath RD, Pitcher BJ, Gardner JL (2009) Recognition of other species’ aerial alarm calls: speaking the same language or learning another? Proc R Soc B 276:769–774. doi: 10.1098/rspb.2008.1368 CrossRefPubMedGoogle Scholar
  39. Marler P (1957) Specific distinctiveness in the communication signals of birds. Behaviour 11:13–39CrossRefGoogle Scholar
  40. Mathis A, Chivers DP, Smith RJF (1996) Cultural transmission of predator recognition in fishes: intraspecific and interspecific learning. Anim Behav 51:185–201CrossRefGoogle Scholar
  41. McCulloch CE, Searle SR (2001) Generalized, linear and mixed models. Wiley, New YorkGoogle Scholar
  42. McDonald JH (2009) Handbook of biological statistics (2nd ed.). Sparky House Publishing, Baltimore. Available via Accessed 18 Aug 2009
  43. McGregor PK (1992) Quantifying responses to playback: one, many, or composite multivariate measures? In: McGregor PK (ed) Playback and studies of animal communication. Plenum Press, New York, pp 79–96Google Scholar
  44. McGregor PK, Dabelsteen T (1996) Communication networks. In: Kroodsma DE, Miller EH (eds) Ecology and evolution of acoustic communication in birds. Cornell University Press, Ithaca, pp 409–425Google Scholar
  45. Mineka S, Cook M (1993) Mechanisms involved in the observational conditioning of fear. J Exp Psychol 122:23–38Google Scholar
  46. Mirza RS, Chivers DP (2001) Are chemical alarm cues conserved within salmonid fishes? J Chem Ecol 27:1641–1655CrossRefPubMedGoogle Scholar
  47. Müller CA, Manser MB (2008) The information banded mongooses extract from heterospecific alarms. Anim Behav 75:897–904. doi: 10.1016/j.anbehav.2007.07.012 CrossRefGoogle Scholar
  48. Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605CrossRefPubMedGoogle Scholar
  49. Newton PN (1989) Associations between langur monkeys (Presbytis entellus) and chital deer (Axis axis): chance encounter or a mutualism? Ethology 83:89–120CrossRefGoogle Scholar
  50. Nocera JJ, Taylor PD, Ratcliffe LM (2008) Inspection of mob-calls as sources of predator information: response of migrant and resident birds in the Neotropics. Behav Ecol Sociobiol 62:1769–1777. doi: 10.1007/s00265-008-0605-5 CrossRefGoogle Scholar
  51. Oda R (1998) The responses of Verreaux’s sifakas to anti-predator alarm calls given by sympatric ring-tailed lemurs. Folia Primatol 69:357–360. doi: 10.1159/000021651 CrossRefPubMedGoogle Scholar
  52. Oda R, Masataka N (1996) Interspecific responses of ringtailed lemurs to playback of antipredator alarm calls given by Verreaux’s sifakas. Ethology 102:441–453CrossRefGoogle Scholar
  53. Radloff FGT, DuToit JT (2004) Large predators and their prey in a southern African savanna: a predator’s size determines its prey size range. J Anim Ecol 73:410–423CrossRefGoogle Scholar
  54. Rainey HJ, Zuberbuhler K, Slater PJB (2004a) Hornbills can distinguish between primate alarm calls. Proc R Soc Lond B 271:755–759. doi: 10.1098/rspb.2003.2619 CrossRefGoogle Scholar
  55. Rainey HJ, Zuberbuhler K, Slater PJB (2004b) The responses of black-casqued hornbills to predator vocalisations and primate alarm calls. Behaviour 141:1263–1277. doi: 10.1163/1568539042729658 CrossRefGoogle Scholar
  56. Ramakrishnan R, Coss RG (2000) Recognition of heterospecific alarm vocalizations by bonnet macaques (Macaca radiata). J Comp Psychol 114:3–12. doi: 10.1037//0735-7036.114.1.3 CrossRefPubMedGoogle Scholar
  57. Randler C (2006) Red squirrels (Sciurus vulgaris) respond to alarm calls of Eurasian jays (Garrulus glandarius). Ethology 112:411–416CrossRefGoogle Scholar
  58. Seyfarth RM, Cheney DL (1986) The assessment by vervet monkeys of their own and another species alarm calls. Anim Behav 34:754–764CrossRefGoogle Scholar
  59. Shriner WM (1998) Yellow-bellied marmot and golden-mantled ground squirrel responses to heterospecific alarm calls. Anim Behav 55:529–536CrossRefPubMedGoogle Scholar
  60. Shriner WM (1999) Antipredator response to a previously neutral sound by free-living adult golden-mantled ground squirrels, Spermophilus lateralis (Sciuridae). Ethology 105:747–757CrossRefGoogle Scholar
  61. Sokal RR, Rohlf FJ (1981) Biometry. WH Freeman and Company, New YorkGoogle Scholar
  62. SYSTAT (2007) SYSTAT version 12.0. SPSS Incorporated, ChicagoGoogle Scholar
  63. Templeton CN, Greene E (2007) Nuthatches eavesdrop on variations in heterospecific chickadee mobbing alarm calls. Proc Natl Acad Sci 104:5479–5482CrossRefPubMedGoogle Scholar
  64. Underwood R (1982) Vigilance behavior in grazing African antelopes. Behaviour 79:8–107CrossRefGoogle Scholar
  65. Valone J (2007) From eavesdropping on performance to copying the behavior of others: a review of public information use. Behav Ecol Sociobiol 62:1–14. doi: 10.1007/s00265-007-0439-6 CrossRefGoogle Scholar
  66. van Bommel FPJ, Heitkönig IMA, Epema GF, Ringrose S, Bonyongo C, Veenendaal EM (2006) Remotely sensed habitat indicators for predicting distribution of impala (Aepyceros melampus) in the Okavango Delta, Botswana. J Trop Ecol 22:101–110CrossRefGoogle Scholar
  67. Vitousek MN, Adelman JS, Gregory NC, St Clair JJH (2007) Heterospecific alarm call recognition in a non-vocal reptile. Biol Lett 3:632–634. doi: 10.1098/rsbl.2007.0443 CrossRefPubMedGoogle Scholar
  68. Washburn SL, DeVore I (1961) The social life of baboons. Sci Am 204:62–72CrossRefGoogle Scholar
  69. White C (1952) The use of ranks in a test of significance for comparing two treatments. Biometrics 8:37–38CrossRefGoogle Scholar
  70. Zuberbühler K (2000) Interspecies semantic communication in two forest primates. Proc Roy Soc Lond B 267:713–718CrossRefGoogle Scholar
  71. Zuberbühler K, Jenny D, Bishary R (1999) The predator deterrence function of primate alarm calls. Ethology 105:477–490Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Dawn M. Kitchen
    • 1
    • 2
    Email author
  • Thore J. Bergman
    • 3
    • 4
  • Dorothy L. Cheney
    • 5
  • James R. Nicholson
    • 2
  • Robert M. Seyfarth
    • 6
  1. 1.Department of AnthropologyThe Ohio State UniversityColumbusUSA
  2. 2.The Ohio State UniversityMansfieldUSA
  3. 3.Department of PsychologyUniversity of MichiganAnn ArborUSA
  4. 4.Department of Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA
  5. 5.Department of BiologyUniversity of PennsylvaniaPhiladelphiaUSA
  6. 6.Department of PsychologyUniversity of PennsylvaniaPhiladelphiaUSA

Personalised recommendations