Elsevier

Animal Behaviour

Volume 83, Issue 2, February 2012, Pages 323-330
Animal Behaviour

Food-associated vocalizations in mammals and birds: what do these calls really mean?

We dedicate this paper to the memory of Professor Chris Evans, a scholar and friend who thought hard about the meaning of animal signals
https://doi.org/10.1016/j.anbehav.2011.12.008Get rights and content

Alarm calls and food-associated calls from a diverse range of species are said to be functionally referential, in that receivers can use these sounds to predict environmental events in the absence of other contextual cues. The evolutionary driver for referential alarm calls has been hypothesized to be the mutually incompatible escape behaviours required to avoid different predators. However, some species produce acoustically distinctive and referential alarm calls but do not show highly referential abilities in other domains. We examined whether food-associated calls in many species are likely to be functionally referential and whether they specifically communicate about characteristic features of food. Food-associated calls are given in both feeding and nonfeeding contexts, and the types of information contained vary greatly. Most species do not produce unique calls for different foods; more common is variation in the call rate, which suggests that call structure reflects the callers’ internal state rather than the food type. We also examined the ultimate function of food-associated calls to evaluate whether there is a unifying explanation for the evolution of functionally referential food calls. Based on the literature, there does not appear to be a unifying function. In conclusion, while functionally referential food-associated calls have been convincingly demonstrated in a few species, it is more common for these vocalizations to reflect arousal rather than additionally providing specific referential information about the feeding event. At this point, there is no compelling hypothesis to explain the evolution of functionally referential food-associated calls. Given the multiple functions of food-associated signals, we should not expect a unitary explanation.

Highlights

► We examined whether food-associated calls documented in birds and mammals communicate characteristic features of food. ► We explored the literature to determine whether a single unifying explanation exists for these calls. ► Variability and specificity of food-associated calls appear to be linked to social/environmental factors. ► A few species show evidence of referential calling, but in most species, food-associated calls more reflect arousal. ► Evidence of multiple functions does not support a unified explanation for food-associated calls.

Section snippets

Functionally referential food-associated calls?

To date, the most convincing cases of functional reference in the feeding context come from studies of fowl (Evans and Marler, 1994, Evans and Evans, 1999, Evans and Evans, 2007). Upon discovery of a food item in the presence of a hen, male fowl produce a specific food-associated vocalization. Consistent with the criteria described above, fowl’s food-associated calls are produced specifically within the context of food, have an acoustically distinct structure, and playback experiments have

Food-associated versus food-specific vocalizations

Acoustic specificity between stimulus and signal, such as has been demonstrated for fowl food calls, is a key prerequisite for functional reference. The notable problem for a unifying concept of functionally referential food-associated calls is that, for a considerable number of species, calls produced during feeding are also produced in nonfood contexts (e.g. toque macaque, Macaca sinica: Dittus 1984; spider monkey, Ateles geoffroyi: Chapman & Lefebvre 1990; rhesus macaque, Macaca mulatta:

What information do food-associated calls convey?

Related to the question of acoustic specificity is determining what information may be conveyed by food-associated calls. The arousal-based perspective suggests that food-associated calls most likely relate to the signaller’s level of excitement or arousal in response to the feeding event (e.g. Owren & Rendall 2001). In this sense, receivers may be responding to the signaller’s increased level of excitement, which has been triggered by the presence of food, rather than the specific expectation

Acoustic variation in food-associated calls

Although variation in call rate is the most common form of acoustic variation in food-associated signalling, some species produce food-associated calls whose acoustic structure covaries with features of the feeding event (golden-lion tamarins: Benz 1993; rhesus macaques: Hauser & Marler, 1993a; ravens: Bugnyar et al. 2001; chimpanzees: Slocombe & Zuberbühler 2006; bonobos: Clay & Zuberbühler 2009). Furthermore, playback experiments in some of these species have also demonstrated that these

What is the function of food-associated calls?

Along with the information conveyed by food-associated calls, an important related question concerns the ultimate function of these calls. Although this is a discrete question, logically separate from the meaning of food calls, an integrative Tinbergian approach to understanding the phenomena warrants some discussion of function. Indeed, by understanding the function of these calls, we may evaluate the question of whether there is a unifying explanation for the evolution of functionally

Conclusions

The widespread evidence of selective food-associated signalling suggests that, compared to other contexts in which functionally referential signals have been identified (i.e. alarm or agonistic interactions), food-associated calls may be produced or withheld in response to the signaller’s own ecological, social and reproductive pressures. The contrast between the production of alarm signals and food-associated calls may reflect the difference in the pressures that would have selected for

Acknowledgments

This paper emerged from a meeting, Vocal Communication and Social Cognition, organized by Marta Manser and Simon Townsend, and supported by the Gleichstellung, University of Zurich. Z.C. was supported by The Leverhulme Trust, with many thanks to Prof. K. Zuberbühler. D.T.B. was supported by National Science Foundation grant NSF IDBR-0754247. We thank Dorothy Cheney and two anonymous referees for their particularly insightful comments.

References (82)

  • W.P. Dittus

    Toque macaque food calls: semantic communication concerning food distribution in the environment

    Animal Behaviour

    (1984)
  • M. Elgar

    House sparrows establish foraging flocks by giving chirrup calls if the resources are divisible

    Animal Behaviour

    (1986)
  • A.M. Elowson et al.

    Food-associated calls correlate with food preferences in cotton-top tamarins

    Animal Behaviour

    (1991)
  • C.S. Evans et al.

    Chicken food calls are functionally referential

    Animal Behaviour

    (1999)
  • C.S. Evans et al.

    Food calling and audience effects in male chickens, Gallus gallus: their relationships to food availability, courtship and social facilitation

    Animal Behaviour

    (1994)
  • C.S. Evans et al.

    On the meaning of alarm calls: functional reference in an avian vocal system

    Animal Behaviour

    (1993)
  • J. Gros-Louis

    The function of food-associated calls in white-faced capuchin monkeys, Cebus capucinus, from the perspective of the signaller

    Animal Behaviour

    (2004)
  • B. Hare et al.

    Do chimpanzees know what conspecifics know?

    Animal Behaviour

    (2001)
  • M.D. Hauser

    Functional referents and acoustic similarity: field playback experiments with rhesus monkeys

    Animal Behaviour

    (1998)
  • M.D. Hauser et al.

    Food-elicited calls in chimpanzees: effects of food quantity and divisibility?

    Animal Behaviour

    (1993)
  • T. Judd et al.

    Naked mole-rats recruit colony mates to food sources

    Animal Behaviour

    (1996)
  • A.J. Leavesley et al.

    Communicating about danger: urgency alarm calling in a bird

    Animal Behaviour

    (2005)
  • P. Marler et al.

    Vocal communication in the domestic chicken: I. Does a sender communicate information about the quality of a food referent to a receiver?

    Animal Behaviour

    (1986)
  • J. Newman et al.

    Co-operative and non-co-operative bases of food-calling

    Journal of Theoretical Biology

    (1989)
  • A.S. Pollick et al.

    Audience effects on food calls in captive brown capuchin monkeys, Cebus apella

    Animal Behaviour

    (2005)
  • D. Rendall et al.

    What do animal signals mean?

    Animal Behaviour

    (2009)
  • R.S. Roush et al.

    The effects of social status on food-associated calling behaviour in captive cotton-top tamarins

    Animal Behaviour

    (1999)
  • R.M. Seyfarth et al.

    Production, usage and comprehension in animal vocalizations

    Brain and Language

    (2010)
  • R.M. Seyfarth et al.

    The central importance of information in studies of animal communication

    Animal Behaviour

    (2010)
  • K.E. Slocombe et al.

    Functionally referential communication in a chimpanzee

    Current Biology

    (2005)
  • K.E. Slocombe et al.

    Food-associated calls in chimpanzees: responses to food types or reative food value?

    Animal Behaviour

    (2006)
  • H. Sridhar et al.

    Why do birds participate in mixed-species foraging flocks? A large-scale synthesis

    Animal Behaviour

    (2009)
  • B.C. Wheeler

    Selfish or altruistic? An analysis of alarm call function in wild capuchin monkeys, Cebus apella nigritus

    Animal Behaviour

    (2008)
  • G. Wilkinson et al.

    Social calls coordinate foraging in greater spear-nosed bats

    Animal Behaviour

    (1998)
  • K. Zuberbühler

    Referential signalling in non-human primates: cognitive precursors and limitations for the evolution of language

    Advances in the Study of Behavior

    (2003)
  • K. Zuberbühler

    Survivor signals: the biology and psychology of animal alarm calling

    Advances in the Study of Behavior

    (2009)
  • J.J. Benz et al.

    Relation between food preference and food-elicited vocalizations in golden lion tamarins (Leontopithecus rosalia)

    Journal of Comparative Psychology

    (1992)
  • D.T. Blumstein

    The evolution of functionally referential alarm communication: multiple adaptations, multiple constraints

    Evolution of Communication

    (1999)
  • S. Boinski et al.

    The huh vocalization of white-faced capuchins: a spacing call disguised as a food call?

    Ethology

    (1996)
  • D.L. Cheney et al.

    Function and intention in the calls of nonhuman primates

    Proceedings of the British Academy

    (1996)
  • D.L. Cheney et al.

    Mechanisms underlying the vocalizations of nonhuman primates

  • Cited by (94)

    View all citing articles on Scopus
    View full text