Functionally Referential Alarm Calls in Tamarins (Saguinus fuscicollis and Saguinus mystax) – Evidence from Playback Experiments

Studies on primate vocalisation have revealed different types of alarm call systems ranging from graded signals based on response urgency to functionally referential alarm calls that elicit predator-specific reactions. In addition, alarm call systems that include both highly specific and other more unspecific calls have been reported. There has been consistent discussion on the possible factors leading to the evolution of different alarm call systems, among which is the need of qualitatively different escape strategies. We studied the alarm calls of free-ranging saddleback and moustached tamarins (Saguinus fuscicollis and Saguinus mystax) in northeast Peru. Both species have predator-specific alarm calls and show specific non-vocal reactions. In response to aerial predators, they look upwards and quickly move downwards, while in response to terrestrial predators, they look downwards and sometimes approach the predator. We conducted playback experiments to test if the predator-specific reactions could be elicited in the absence of the predator by the tamarins' alarm calls alone. We found that in response to aerial alarm call playbacks the subjects looked significantly longer upwards, and in response to terrestrial alarm call playbacks they looked significantly longer downwards. Thus, the tamarins reacted as if external referents, i.e. information about the predator type or the appropriate reaction, were encoded in the acoustic features of the calls. In addition, we found no differences in the responses of S. fuscicollis and S. mystax whether the alarm call stimulus was produced by a conspecific or a heterospecific caller. Furthermore, it seems that S. fuscicollis terrestrial alarm calls were less specific than either S. mystax terrestrial predator alarms or either species' aerial predator alarms, but because of the small sample size it is difficult to draw a final conclusion.

[1]  E. Greene,et al.  Red squirrels, Tamiasciurus hudsonicus , produce predator-class specific alarm calls , 1998, Animal Behaviour.

[2]  Nonconvergence in the evolution of primate life history and socio-ecology , 1996 .

[3]  P. Kappeler,et al.  Anti-predator behavior of group-living Malagasy primates: mixed evidence for a referential alarm call system , 2002, Behavioral Ecology and Sociobiology.

[4]  Christopher S. Evans,et al.  Referential Signals , 2000 .

[5]  K. Zuberbühler,et al.  Diana monkey long-distance calls: messages for conspecifics and predators , 1997, Animal Behaviour.

[6]  H. Buchanan-Smith,et al.  Responses of Captive Single- and Mixed-Species Groups of Saguinus to Novel Nonthreatening Objects , 2000, International Journal of Primatology.

[7]  D. Kramer,et al.  Response of eastern chipmunks to conspecific alarm calls , 1995, Animal Behaviour.

[8]  Peter Marler,et al.  Semantics of an avian alarm call system: the male domestic fowl , 1987 .

[9]  E. Heymann A Field observation of predation on a Moustached Tamarin(Saguinus mystax) by an Anaconda , 1987, International Journal of Primatology.

[10]  M. Huck,et al.  Boa constrictor Attack and Successful Group Defence in Moustached Tamarins, Saguinus mystax , 2002, Folia Primatologica.

[11]  R. Seyfarth,et al.  The assessment by vervet monkeys of their own and another species' alarm calls , 1990, Animal Behaviour.

[12]  R. Seyfarth,et al.  Acoustic Features of Female Chacma Baboon Barks , 2001 .

[13]  Michael E. Pereira,et al.  Ringtailed lemur anti-predator calls denote predator class, not response urgency , 1991, Animal Behaviour.

[14]  M. Manser,et al.  The information that receivers extract from alarm calls in suricates , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  C. Peres,et al.  Anti-predation benefits in a mixed-species group of Amazonian tamarins. , 1993, Folia primatologica; international journal of primatology.

[16]  Reactions of wild tamarins,Saguinus mystax andSaguinus fuscicollis to avian predators , 1990, International Journal of Primatology.

[17]  H. Buchanan-Smith Polyspecific association of two tamarin species, Saguinus labiatus and Saguinus fuscicollis, in Bolivia , 1990, American journal of primatology.

[18]  M. Norconk Mechanisms promoting stability in mixed Saguinus mystax and S. fuscicollis troops , 1990, American journal of primatology.

[19]  H. Buchanan-Smith,et al.  Factors affecting vigilance within wild mixed-species troops of saddleback (Saguinus fuscicollis) and moustached tamarins (S. mystax) , 2004, Behavioral Ecology and Sociobiology.

[20]  K. Strier Myth of the typical primate , 1994 .

[21]  E. Heymann,et al.  Field observation of snake-mobbing in a group of saddle-back tamarins, Saguinus fuscicollis nigrifrons. , 1987, Folia primatologica; international journal of primatology.

[22]  E. Heymann,et al.  Crested Eagle (Morphnus guianensis) Predation on Infant Tamarins (Saguinus mystax and Saguinus fuscicollis, Callitrichinae) , 2001, Folia Primatologica.

[23]  K. Zuberbühler Predator-specific alarm calls in Campbell's monkeys, Cercopithecus campbelli , 2001, Behavioral Ecology and Sociobiology.

[24]  P. Marler,et al.  Vervet monkey alarm calls: Semantic communication in a free-ranging primate , 1980, Animal Behaviour.

[25]  M. Manser,et al.  The acoustic structure of suricates' alarm calls varies with predator type and the level of response urgency , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  P. Marler,et al.  Effects of apparent size and speed on the response of chickens, Gallus gallus, to computer-generated simulations of aerial predators , 1993, Animal Behaviour.

[27]  P. F. Major,et al.  Predator-prey interactions in two schooling fishes, Caranx ignobilis and Stolephorus purpureus , 1978, Animal Behaviour.

[28]  Julie Gros-Louis,et al.  Alarm calls of white-faced capuchin monkeys: an acoustic analysis , 2005, Animal Behaviour.

[29]  Louise H. Emmons,et al.  Comparative feeding ecology of felids in a neotropical rainforest , 1987, Behavioral Ecology and Sociobiology.

[30]  E. Heymann Sleeping habits of tamarins, Saguinus mystax and Saguinus fuscicollis (Mammalia; Primates; Callitrichidae), in north-eastern Peru , 1995 .

[31]  F. Encarnación Introducción a la flora y vegetación de la Amazonia peruana: estado actual estudios, medio natural y ensayo de una clave de determinación de las formaciones vegetales en la llanura amazónica , 1985 .

[32]  R. Seyfarth,et al.  Signalers and receivers in animal communication. , 2003, Annual review of psychology.

[33]  P. Kappeler,et al.  Nonconvergence in the evolution of primate life history and socio-ecology , 1996 .

[34]  H. Yong,et al.  Vocalizations in response to predators in three species of Malaysian Callosciurus (Sciuridae) , 1993 .