Behavioral Ecology and Sociobiology

, Volume 62, Issue 4, pp 549–559 | Cite as

A forest monkey’s alarm call series to predator models

Original Paper

Abstract

Some non-human primates produce acoustically distinct alarm calls to different predators, such as eagles or leopards. Recipients respond to these calls as if they have seen the actual predator, which has led to the notion of functionally referential alarm calls. However, in a previous study with free-ranging putty-nosed monkeys (Cercopithecus nictitans martini), we demonstrated that callers produced two acoustically distinct alarm calls to eagle shrieks and leopard growls, but both alarm calls were given to both predators. We can think of two basic explanations for this surprising result, a methodological and theoretical one. Firstly, acoustic predator models may not always be suitable to test alarm call behaviour in primates, sometimes causing uncharacteristic behaviour. Secondly, referential alarm calling may not be a universal feature of primate alarm call systems. Considering the methodological and theoretical importance of these possibilities, we conducted a follow-up study using life-sized leopard, eagle, and human models on the same population and compared the resulting vocal responses to those given to acoustic predator models. We compared the alarm call series given to each of these predator model types and found a considerable degree of consistency suggesting that the mode of presentation did not affect anti-predator calling strategies. However, evidence for audience effects on calling behaviour was inconclusive. While it appears that predator class is reliably encoded by different call series types irrespective of the mode of presentation, observations of these same call series given in non-predatory contexts indicate that predator class is unlikely to be the relevant organising principle underlying the alarm-calling behaviour in this species. We conclude by offering an alternative, non-referential, account of the alarm-calling system exhibited by this species.

Keywords

Referential communication Anti-predator Call combinations Semantic Syntax Predation Evolution of language Cognition 

Supplementary material

References

  1. Arnold K, Zuberbühler K (2006a) The alarm calling system of adult male putty-nosed monkeys, Cercopithecus nictitans martini. Anim Behav 72:643–653CrossRefGoogle Scholar
  2. Arnold K, Zuberbühler K (2006b) Semantic combinations in primate calls. Nature 441:303PubMedCrossRefGoogle Scholar
  3. Brown MM, Kreiter NA, Maple JT, Sinnott JM (1992) Silhouettes elicit alarm calls from captive vervet monkeys (Cercopithecus aethiops). J Comp Psychol 106:350–359PubMedCrossRefGoogle Scholar
  4. Cheney DL, Seyfarth R (1985) Vervet monkey alarm calls: manipulation through shared information? Behaviour 93:150–166Google Scholar
  5. Cheney DL, Seyfarth R (1990) How monkeys see the world. University of Chicago Press, ChicagoGoogle Scholar
  6. Digweed SM, Fedigan LM, Rendall D (2005) Variable specificity in the antipredator vocalizations and behavior of the white-faced capuchin, Cebus capuchinus. Behaviour 142:997–1021CrossRefGoogle Scholar
  7. Dunn A (1993) The large mammals of Gashaka Gumpti National Park, Nigeria. Unpublished report to NCF, WWW-UKGoogle Scholar
  8. Eckhardt W, Zuberbühler K (2004) Cooperation and competition in two forest monkeys. Behav Ecol 15:400–411CrossRefGoogle Scholar
  9. Fichtel C, Kappeler PM (2002) Anti-predator behavior of group-living Malagasy primates: mixed evidence for a referential alarm call system. Behav Ecol Sociobiol 51:262–275CrossRefGoogle Scholar
  10. Fichtel C, van Schaik CP (2006) Semantic differences in sifaka (Propithecus verreauxi) alarm calls: a reflection of genetic or cultural variants? Ethology 112:839–849CrossRefGoogle Scholar
  11. Fichtel C, Perry S, Gros-Louis J (2005) Alarm calls of white faced capuchin monkeys: an acoustic analysis. Anim Behav 70:165–176CrossRefGoogle Scholar
  12. Gautier JP, Gautier A (1977) Communication in old world monkeys. In: Sebeok TA (ed) How animals communicate. Indiana University Press, Bloomington, Indiana, pp890–964Google Scholar
  13. Gautier-Hion A, Colyn M, Gautier JP (1999) Histoire naturelle des primates d’Afrique centrale. Ecofac, Libreville, GabonGoogle Scholar
  14. Grice HP (1969) Utterers’ meaning and intentions. Philos Rev 78:147–177CrossRefGoogle Scholar
  15. Jenny D, Zuberbühler K (2005) Hunting behaviour in West African forest leopards. Afr J Ecol 43:197–200CrossRefGoogle Scholar
  16. Kirchhof J, Hammerschmidt K (2006) Functionally referential alarm calls in tamarins (Sanguinus fuscicollis and Sanguinus mystax)—evidence from playback experiments. Ethology 112:346–354CrossRefGoogle Scholar
  17. Macedonia JM, Polak JF (1989) Visual assessment of avian threat in semi-captive ringtailed lemurs (Lemur catta). Behaviour 111:291–304Google Scholar
  18. Macedonia JM, Yount PL (1991) Auditory assessment of avian predator threat in semi-captive ringtailed lemurs (Lemur catta). Primates 32:169–182CrossRefGoogle Scholar
  19. Palleroni A, Hauser M, Marler P (2005) Do responses of galliform birds vary adaptively with predator size? Anim Cogn 8:200–210PubMedCrossRefGoogle Scholar
  20. Pereira ME, Macedonia JM (1991) Ringtailed lemur anti-predator calls denote predator class, not response urgency. Anim Behav 41:543–544CrossRefGoogle Scholar
  21. Rainey HJ, Zuberbühler K, Slater PJB (2004) Hornbills can distinguish between primate alarm calls. Proc R Soc Lond B 271:755–759CrossRefGoogle Scholar
  22. Ramakrishnan U, Coss RG (2000) Age differences in the response to adult and juvenile alarm calls by bonnet macaques (Macaca radiata). Ethology 106:131–144CrossRefGoogle Scholar
  23. Riede T, Zuberbühler K (2003a) Pulse register phonation in Diana monkey alarm calls. J Acoust Soc Am 113:2919–2926PubMedCrossRefGoogle Scholar
  24. Riede T, Zuberbühler K (2003b) The relationship between acoustic structure and semantic information in Diana monkey alarm calls. J Acoust Soc Am 114:1132–1142PubMedCrossRefGoogle Scholar
  25. Riede T, Bronson E, Hatzikirou H, Zuberbühler K (2005) Vocal production mechanisms in a non-human primate: morphological data and a model. J Human Evol 48:85–96Google Scholar
  26. Seyfarth RM, Cheney DL (2003) Signalers and receivers in animal communication. Annu Rev Psychol 54:145–173PubMedCrossRefGoogle Scholar
  27. Seyfarth RM, Cheney DL, Marler P (1980) Monkey responses to three different alarm calls: Evidence of predator classification and semantic communication. Science 210:801–803PubMedCrossRefGoogle Scholar
  28. Shultz S, Thomsett S (2007) Interactions between African crowned eagles and their primate prey community. In: McGraw WS, Zuberbühler K, Noë R (eds) Monkeys of the Taï forest: an African monkey community. Cambridge Univ. Press, Cambridge, pp 171–193Google Scholar
  29. Smith WJ (1965) Message, meaning, and context in ethology. Am Nat 99:405–409CrossRefGoogle Scholar
  30. Struhsaker TT (1967) Ecology of vervet monkeys (Cercopithecus aethiops) in the Masai-Amboseli Game Reserve, Kenya. Ecology 48:891–904CrossRefGoogle Scholar
  31. Struhsaker TT (1970) Phylogenetic implications of some vocalisations of Cercopithecus monkeys. In Napier JR, Napier PH (eds) Old world monkeys: evolution, systematics and behaviour. Academic Press, London, pp 365–407Google Scholar
  32. Wich SA, Sterck EHM (2003) Possible audience effect in Thomas langurs (Primates; Presbytis thomasi): an experimental study on male loud calls in response to a tiger model. Am J Primatol 60:155–159PubMedCrossRefGoogle Scholar
  33. Zuberbühler K (2000a) Referential labelling in Diana monkeys. Anim Behav 59:917–927PubMedCrossRefGoogle Scholar
  34. Zuberbühler K (2000b) Causal cognition in a non-human primate: field playback experiments with Diana monkeys. Cognition 76:195–207PubMedCrossRefGoogle Scholar
  35. Zuberbühler K (2000c) Causal knowledge of predators’ behaviour in wild Diana monkeys. Anim Behav 59:209–220PubMedCrossRefGoogle Scholar
  36. Zuberbühler K (2001) Predator specific alarm calls in Campbell’s guenons. Behav Ecol Sociobiol 50:414–422Google Scholar
  37. Zuberbühler K (2002) A syntactic rule in forest monkey communication. Anim Behav 63:293–299CrossRefGoogle Scholar
  38. Zuberbühler K (2003) Referential signalling in non-human primates: cognitive precursors and limitations for the evolution of language. Adv Study Behav 33:265–307CrossRefGoogle Scholar
  39. Zuberbühler K, Noë R, Seyfarth RM (1997) Diana monkey long-distance calls: messages for conspecifics and predators. Anim Behav 53:589–604CrossRefGoogle Scholar
  40. Zuberbühler K, Cheney DL, Seyfarth RM (1999a) Conceptual semantics in a nonhuman primate. J Comp Psychol 113:33–42CrossRefGoogle Scholar
  41. Zuberbühler K, Jenny D, Bshary R (1999b) The predator deterrence function of primate alarm calls. Ethology 105:477–490Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Kate Arnold
    • 1
  • Yvonne Pohlner
    • 2
  • Klaus Zuberbühler
    • 1
  1. 1.School of PsychologyUniversity of St AndrewsSt AndrewsUK
  2. 2.Institut für Biologie IAlbert Ludwigs UniversitätFreiburgGermany

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