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Functionally Referential Alarm Calls in Tamarins (Saguinus Fuscicollis and Saguinus Mystax) – Evidence from Playback Experiments Janna Kirchhof* & Kurt Hammerschmidt

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Functionally Referential Alarm Calls in Tamarins (Saguinus Fuscicollis and Saguinus Mystax) – Evidence from Playback Experiments Janna Kirchhof* & Kurt Hammerschmidt Ethology Functionally Referential Alarm Calls in Tamarins (Saguinus fuscicollis and Saguinus mystax) – Evidence from Playback Experiments Janna Kirchhof* & Kurt Hammerschmidt * Department of Neurobiology Cognitive Ethology, German Primate Center, Kellnerweg 4, Go¨ ttingen, Germany Correspondence Abstract Kurt Hammerschmidt, Cognitive Ethology, German Primate Center, Kellnerweg 4, 37077 Studies on primate vocalisation have revealed different types of alarm Go¨ ttingen, Germany. call systems ranging from graded signals based on response urgency to E-mail: [email protected] functionally referential alarm calls that elicit predator-specific reactions. In addition, alarm call systems that include both highly specific and Received: December 9, 2004 other more unspecific calls have been reported. There has been consis- Initial acceptance: April 3, 2005 tent discussion on the possible factors leading to the evolution of differ- Final acceptance: June 26, 2005 (L. Sundstro¨ m) ent alarm call systems, among which is the need of qualitatively doi: 10.1111/j.1439-0310.2006.01165.x 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. example for a functionally referential alarm call sys- Introduction tem (Struhsaker 1967; Seyfarth et al. 1980; Evans Although animals do not intend to provide informa- 1997). Vervet monkeys give acoustically distinct tion for their conspecifics, there are many examples alarm calls in response to different types of predators demonstrating that listeners are able to acquire such as aerial and terrestrial predators or snakes. information from vocal signals (Seyfarth & Cheney When conspecific listeners hear these alarm calls 2003). Vervet monkey alarm calls are the classical they respond with the adequate escape strategy. In Ethology 112 (2006) 346–354 ª 2006 The Authors 346 Journal compilation ª 2006 Blackwell Verlag, Berlin J. Kirchhof & K. Hammerschmidt Functionally Referential Alarm Calls in Tamarins the case of an aerial alarm call vervet monkeys climb As former studies of alarm call systems have all down the tree and scan the sky. In the case of a ter- been carried out on lemurs or cercopithecines, some restrial alarm call they climb up into trees, and in of whom are closely related to each other, it seems the case of a snake alarm call they often stand bipe- important and useful to gain similar knowledge also dal and scan the ground. Regardless of whether or on New World monkeys. These have undergone an not the caller has an intention to communicate the independent radiation within the order primates and presence of a certain predator, evidently these calls differ in essential socio-ecological and life-history serve a referential function for the listeners. characteristics from the other primate taxa (Strier Further studies on nonhuman primate vocalisa- 1994; Kappeler & Heymann 1996). Therefore, acous- tions have revealed other types of alarm call systems, tic studies on New World monkeys cannot only fill a such as a continuum of graded signals with the usage taxonomic gap, but also lead, in comparison with based on response urgency (chacma baboons: Fischer prosimians and Old World monkeys, to a deeper et al. 2001) or mixed systems (redfronted lemurs and understanding of alarm call systems in general. white sifakas: Fichtel & Kappeler 2002) with one Tamarins of the New World genus Saguinus, and functionally referential call and other unspecific calls. most other callitrichids, suffer from a severe preda- Scientists have identified two factors that appear to tion pressure because of their small body size. Most explain the evolution of such different alarm call sys- important among their predators are large raptors, tems: the presence or absence of different types of but also felids, mustelids, and snakes have been predators and hence the presence or absence of dif- reported to prey on callitrichids (e.g. Terborgh 1983; ferent escape strategies in a certain species (Macedo- Emmons 1987; Heymann 1987). In field studies, it nia 1990; Pereira & Macedonia 1991). Following has been observed that saddleback and moustached Macedonia & Evans (1993) animals with different tamarins show distinct behavioural reactions towards escape strategies, like ring-tailed lemurs (Lemur catta), different types of predators (Heymann 1990; Peres tend to have a functionally referential alarm call sys- 1993). In response to aerial predators, they look tem, while animals with similar or only one escape upwards and quickly fall or climb downwards, while strategy, like ruffed lemurs (Varecia variegata), tend to in response to terrestrial predators, they look down- have a gradual or urgency-based system. Subsequent wards and sometimes approach the predator. Tama- studies on several Old World monkeys confirmed this rins live in dense forest habitats with limited hypothesis. Diana monkeys (Cercopithecus diana: visibility and therefore need to maximize the effi- Zuberbu¨ hler et al. 1997) and Campbell’s monkeys ciency of their acoustic communication. This is espe- (Cercopithecus campbelli: Zuberbu¨ hler 2001) show dif- cially true in the case of anti-predatory behaviour, ferent locomotive patterns towards eagles and leop- where quick and appropriate reactions are required. ards and have functionally referential call types for Hence, tamarins are very suitable subjects for the these predators. On the contrary, larger and predom- investigation of acoustic warning signals. inantly terrestrial primates like chacma baboons In this study, we conducted playback experiments seem to fulfil the prediction that primates without to test if the acoustic information of aerial and ter- specific escape strategies encode arousal or escape restrial alarm calls is sufficient to elicit the predator- urgency in their alarm calls. Field studies on chacma specific reactions in saddleback and moustached baboons in the Okavango delta in Botswana have tamarins. In accordance with the reactions observed shown that these primates have no distinct alarm call during natural predator encounters we established types in their repertoire (Fischer et al. 2001). Their the test paradigm: in response to the playback of alarm calls continuously grade into ‘lost calls’, calls aerial alarm calls the focal animal should look signi- that are uttered when an individual has lost contact ficantly longer upwards, while in response to the with other group members. Of course, the same spe- playback of terrestrial alarm calls the focal animal cies may have acoustically discrete, predator-specific should look significantly longer downwards. alarm calls that show urgency-based acoustic grada- tion within each class. Manser (2001) demonstrated Methods experimentally that suricates give acoustically dis- tinct alarm calls to terrestrial predators, avian preda- Study Site and Subjects tors, and snakes, and within each class have high urgency and low urgency variants that reflect the The study was carried out from May to Nov. 2001 immediacy of danger and elicit stronger or weaker and Oct. to Nov. 2002 at the Estacio´ n Biolo´ gica responses. Quebrada Blanco (EBQB) in northeast Peru. The Ethology 112 (2006) 346–354 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag, Berlin 347 Functionally Referential Alarm Calls in Tamarins J. Kirchhof & K. Hammerschmidt station is located at 4°21¢S73°09¢W, approximately mate II’ (BOSE Corporation, Framingham, MA, 90 km southeast of Iquitos, near the river (Quebra- USA) loudspeaker. The loudspeaker was positioned da) Blanco. The rain forest is of the ‘terra-firme’ type at approximately 8–12 m distance from the focal ani- (Encarnacio´ n 1985, 1993) and has a canopy height mal and tied to the trunk of a tree at approximately ranging from 25 to 30 m with some outstanding 1.5 m of height, presumably invisible to the mon- trees rising up to 40 m. The study site is approxi- key. The subject’s behaviour was recorded with a mately 1.5 km2 large and run through by a system CANON UC-X50 Hi 8 mm video camcorder (Canon, of parallel trails in north–south and west–east direc- Tokya, Japan). tion, with a 100 m spacing in between. For details of The playback was performed only when the focal the study site see also Heymann (1995). There is not
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