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Cottontop tamarin, Saguinus oedipus, alarm calls contain sufficient information for recognition of individual identity
ANIMAL BEHAVIOUR, 2006, 72, 1379e1385 doi:10.1016/j.anbehav.2006.04.006
Cottontop tamarin, Saguinus oedipus, alarm calls contain sufficient information for recognition of individual identity C ATHERI NE S PROUL* , A LBERTO PALLERONI* & MA RC D. H AU S ER*†‡
*Department of Psychology, Harvard University yDepartment of Organismic & Evolutionary Biology, Harvard University zDepartment of Biological Anthropology, Harvard University (Received 10 November 2005; initial acceptance 18 January 2006; final acceptance 7 April 2006; published online 10 October 2006; MS. number: A10298)
Most work on individual recognition has focused on signals used in the context of social contact or mate attraction. Here we present the results of a playback experiment designed to test whether cues of individual identity are encoded in alarm calls given by cottontop tamarins during encounters with a trained and flying goshawk, Accipiter gentilis. Based on a habituationediscrimination paradigm previously used with this species to show individual recognition of their long calls, subjects showed the ability to distinguish individuals by their alarm calls alone. Once subjects habituated to multiple exemplars of one individual’s alarm call, their response was renewed to the alarm calls of another individual but not to a new set of alarm calls from the same individual. We discuss the implications of these results for current theories of signal processing. Ó 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Alarm calls are potentially rich sources for passing information to conspecifics. Based on field and laboratory studies of birds and mammals, it is now understood that these calls encode information about the type of predator that is attacking or the most adaptive escape route (Seyfarth et al. 1980; Gyger et al. 1987; Macedonia & Polak ¨ hler 2001; 1989; Marler et al. 1992; Manser 2001; Zuberbu Templeton et al. 2005) as well as the level of threat presented by the predator (Owings & Morton 1998; Le Roux et al. 2001; Randall & Rogovin 2002). Access to this information can expedite an animal’s reaction to a predator and therefore increase its chances of survival. In the case of animals with functionally referential alarm calls, the call itself elicits predator-specific defensive behaviour, rather than merely drawing the animal’s attention to the presence of a possible threat (Seyfarth et al. ¨ hler et al. 1997). Urgency-based calls, in 1980; Zuberbu contrast, alert animals to the proximity of a threat, thus affecting their vigilance (Owings & Morton 1998; Randall & Rogovin 2002). The urgency or motivational component of an alarm call can relay the proximity of the threat either by a change in the physical properties of the calls produced, suggesting the internal state of the caller (Evans
Correspondence: A. Palleroni, Department of Psychology, Harvard University, Cambridge, MA 02138, U.S.A. (email: aliparti@wjh. harvard.edu). 0003e 3472/06/$30.00/0
1997), or by a change in the type of call given (Randall & Rogovin 2002). What is not yet clear is the extent to which various species encode information about individual identity in their animal alarm calls and the extent to which it is decoded by listeners. Moreover, given the function of alarm calls, it is not clear whether such information is necessary or relevant since the primary adaptive goal is to warn kin or to notify the predator that it has been detected (Hauser 1996; Caro 2005). In the case of kin warning, a group-level signature would be relevant, whereas in the case of predator warning, no such information is pertinent. However, in cases where group size is small (e.g. monogamously mated species), selection may favour encoding of individual identity. Thus, in contrast to the wealth of evidence for individual-level acoustic signatures in nonalarm calls, including calls given during territorial defence, mate attraction and the establishment of contact (Rendall et al. 1996; Karavanich & Atema 1998; Jouventin, et al. 1999; Sayigh et al. 1999), to what extent is there comparable evidence in the context of predator alarm calls? As noted above, the function of alarm calls is either to alert kin or to deter predators by indicating that they have been sighted (Marler et al. 1992; Caro 1995, 2005; Rendall, et al. 1998). In addition to the alerting function of alarm calls, however, it is reasonable to suppose that selection may have favoured cues to individual identity because
1379 Ó 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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ANIMAL BEHAVIOUR, 72, 6
such information provides one path into the assessment of caller reliability. In other words, because some individuals may be less reliable than others, perhaps because they have a higher incidence of false alarms in the signal detection sense, recognizing individuals by voice alone will enable listeners to assess the odds that a predator has been detected, especially when the caller is out of sight. Information about individual identity may be a by-product of vocal tract morphology (Rendall et al. 1998), or result from variation that arises in the course of vocal learning and maturation. The question addressed here is the extent to which listeners can extract information about individual identity from subjects’ alarm calls. Mitani et al. (1996) proposed that different selective pressures could operate on the design features of vocalizations within a species’ repertoire, with long-range calls providing more distinctive cues to individuality when contrasted with close-range calls. The idea is that longrange calls are typically given to recipients who are out of view, and thus, individuality can only be extracted from acoustic cues. In contrast, when individuals vocalize to others in close range, sensory modalities other than audition may be used to identify individuals. Mitani et al. found that the distinctiveness of individual chimpanzees’ signatures varied significantly across call types. However, cues to individual identity were more reliable in the long-distance pant hoot than in the short-range pant grunt. While individuality was better encoded in long-distance calls, further experiments revealed that chimpanzees can recognize individuals using both types of calls under the controlled conditions of captivity (Kijoma et al. 2003). One pressure on the capacity to recognize individual alarm calls comes from considering the problem of deception, and in particular, the capacity to discriminate between reliable and unreliable callers. Hare & Atkins (2001) played back squirrel alarm calls from different individuals and either paired the call with a predator model or no stimulus at all. The alarm calls of individuals who were paired with the predator model induced greater response in subjects, suggesting that these callers were perceived as more reliable in predicting the presence of a predator than others who ‘cried wolf’. Vervet monkeys, Cercopithecus aethiops, also use cues to individual identity in alarm and nonalarm calls to distinguish reliable from unreliable callers (Cheney & Seyfarth 1988). Subjects that habituated to the alarm calls of an unreliable individual transferred habituation to an acoustically different alarm call with the same referent from that individual. In contrast, subjects that habituated to one individual’s alarm calls responded to an alarm call from a novel individual even if the referent was the same. In other words, as long as the test call was from a referentially distinctive class, independently of caller identity, subjects responded following habituation. In the case of vervets, infants may be unreliable sources of predator information (Cheney & Seyfarth 1990). Detecting cheaters provides another important functional reason to identify reliable individuals (Munn 1986). This combined ability to recognize individual callers and determine reliability may result in more efficient predator defence (Yin & McCowan 2004).
Cottontop tamarins, the subjects of our experiments, produce a variety of acoustically distinctive vocalizations (Cleveland & Snowdon 1982). To date, the best studied vocalization is the combination long call (CLC), a multisyllabic contact call. As one would expect, previous acoustic analyses and playback experiments indicate that this contact call not only carries information about individual identity, but that subjects also readily extract this information during perceptual playback experiments using both an antiphonal calling procedure as well as the habituationediscrimination method (Weiss et al. 2001; Miller & Ghazanfar 2002; Weiss & Hauser 2002). Here we look at the problem of individual recognition using the tamarins’ alarm call to an aerial predator. This call has not been studied in the laboratory to the degree that the combination long call has, and individual recognition has not been explored. Neyman (1978) noted that the cottontop tamarins that he studied in the wild seemed to have distinct alarm calls for birds of prey and for ground predators. Furthermore, wild tamarins did not give the aerial predator call unless the bird was flying; perching birds of prey failed to elicit alarm calls until they flew off (Neyman 1978). To test the hypothesis that tamarin alarm calls carry information that can be extracted to identify individual callers, we used the habituationediscrimination paradigm that successfully identified individual discrimination in tamarin combination long calls (Weiss & Hauser 2002). In prior work (C. Sproul, unpublished data), we used a trained, flying goshawk to simulate predation events on tamarins that were housed singly or in groups. The alarm calls given in these known contexts were used as stimuli in the following playback experiments.
METHODS
Subjects Cottontop tamarins are New World monkeys, native to the rainforests of Colombia. They are cooperative breeders, with both parents and offspring involved in rearing infants (Cleveland & Snowdon 1984). Snakes, ocelots, tayras and various hawks have been observed killing tamarins, and it is clear that flying hawks elicit strong alarm responses in tamarins (Caine 1993). Predation pressure has been hypothesized to be important in shaping the cooperative social group structure in tamarins (Caine 1993). We tested 23 adult cottontop tamarins, 12 males and 11 females (see Table 1). Each subject participated in two playback sessions. Subjects were captive born at either the New England Regional Primate Center in Southborough, Massachusetts, U.S.A. or the Cognitive Evolution Laboratory at Harvard University, where they were housed during the experiment. In addition to the small treats of raisins and marshmallows that subjects received in other experiments throughout the day, the animals’ diet consisted of monkey chow supplemented with sunflower seeds, peanuts, fruit, yogurt and vitamins given once a day in the early evening. Each subject was housed with its mate and offspring or parents in one of 11 cages.
SPROUL ET AL.: TAMARIN ALARM CALLS ENCODE CALLER ID
Table 1. Experimental subject history including experience with an aerial predator
Subject ID AC AG DD DG DW EM EN ID JG JK JM KW LG LS PB PJ RA RB RJ SD SH SP UB
Age (years) Sex 11 3 13 3 3 13 9 10 9 4 4 5 3 3 5 4 3 7 8 3 10 12 17
M M M F M F F M F F M F F F M M M F M M F M F
Home cage
Experience with goshawk in isolation
Experience with goshawk in a social context
5 5 8 3 7 10 2 10 5 7 6 8 4 6 9 4 3 9 1 10 11 2 1
N Y N Y N N Y N N N Y N N Y N N Y N N N Y Y N
N N N N Y N Y N N Y Y N Y Y Y Y N Y N N Y Y N
Each cage, measuring 1.5 2.0 1.2 m, was outfitted with nestboxes, branches, ropes and ladders.
Acoustic Stimuli Alarm calls were collected during an earlier experiment in which a goshawk was presented to a subject in isolation (see Fig. 1). During this experiment, subjects were housed in a large cage at one end of a 14-m-long hallway. To simulate a predatory event, the goshawk flew towards the 12
Frequency (kHz)
10 8 6 4 2 0
0.5
1 Time (s)
1.5
2
Figure 1. Spectrogram (sample rate 50 kHz, 256-point FFT, Hanning window) of an alarm call exemplar used in the playback.
subject from a concealed area at the opposite end of the hallway. At the end of the approach, the goshawk veered away and perched out of sight of the subject. Vocalizations were recorded onto DAT tapes using an ME-66 directional Sennheiser microphone and then acquired into a MatLab program for sound analysis. The microphone was placed 0.5 m from the cage. Because subjects moved during the presentation, the recording distance ranged from 0.5 to 1.5 m, during which subjects could be facing towards or away from the microphone. Subjects had no previous experience with aerial predation before these experiments.
Playback Procedure We replicated the general habituationediscrimination procedure used in previous studies of tamarins, exploring the perceptual mechanisms underlying their ability to process human speech as well as their combination long call (Weiss et al. 2001). We first transferred each subject from its home cage to a small test cage (0.60 0.40 0.15 m; Fig. 2a) with a wire mesh front and opaque Plexiglas on all other sides; this design generally caused subjects to hang on the wire mesh front, thereby facilitating the playback procedure, which required orientation to the concealed speaker. We placed a video camera directly in front of the wire mesh front of the test cage, while the playback speaker was concealed above, behind, and to the right of the subject. All experiments were run by an experimenter sitting outside the test room. The sound intensity at the playback box was 70e75 dB. Once the subject was sitting calmly in the test cage, the session began. To habituate our subjects, we played 12e15 exemplars of one individual’s alarm calls. Calls were played when the subject was looking down and to the right (in the opposite direction from the speaker for a maximum orientation response). A response was defined as orienting up and towards the speaker during the playback or within 2 s of its termination (Fig. 2b; for video clips of the responses, see http://www.wjh.harvard.edu/ wmnkylab/prothome.htm under ‘Acoustic perception and the orienting response’). The experimenter would wait until the animal was in this position to play an alarm call. The time between calls never exceeded 60 s and was never less than 10 s. This time interval was chosen because it was consistent with playback experiments previously run in our laboratory (e.g. Weiss & Hauser 2002). If the animal failed to orient to the speaker, the trial was marked ‘no’, and after three consecutive, unambiguous no responses, the animal was considered to be habituated. If the subject jumped, called or faced the speaker during the playback, we coded the trial as ‘bad’. Trials in which a subject’s response was ambiguous were coded as such. During online coding of habituation trials, we coded all ‘bad’ and ‘ambiguous’ responses as ‘yes’ responses in order to guarantee that all subjects entered the test phase following unambiguous ‘no’ responses. We consider this a conservative approach because our goal was to ensure that each subject entered the test phase after complete habituation, defined as three consecutive no responses.
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(a)
(b)
Before playback
During and postplayback
Figure 2. (a) Diagram of the playback set-up. (b) Example of an orienting response to the playback stimuli in which the subject oriented towards the hidden speaker, which was above and to the left of the subject.
Following habituation, we presented four test calls consisting of two novel calls from the habituation individual and two from a novel individual, counterbalanced for order of presentation. One condition contrasted two same-sex callers, whereas the second contrasted opposite-sex callers. Previous experiments with the tamarin’s combination long calls revealed that discrimination was more difficult for same-sex callers than for opposite-sex callers (Weiss et al. 2001). We presented the alarm calls of three adult males and three adult females, all familiar members of the colony. Paralleling the habituation phase, test trials were played 10e60 s after the prior trial. We aborted a session if a subject failed to habituate after 50 trials (i.e. calls); prior studies in our laboratory suggested that subjects are too agitated to participate once they have exceeded this number of trials. As indicated in our results below, most subjects habituated in less than 30 trials. Trials were also aborted if the subject was too agitated to perform properly, or if one of the four
test trials was marked ‘bad’. Out of 56 sessions run, we aborted 10 based on these criteria. We digitized each session and coded all trials blind to the condition. Interobserver reliability was greater than 95%.
RESULTS Across all sessions, the mean SD number of trials to habituation was 15 8.06 (range 4e41, N ¼ 46). This value did not differ significantly between different caller identities (independent samples t test: t44 ¼ 0.44, P ¼ 0.67). Figure 3 plots the frequency distribution of the number of trials to habituation for the entire data set of playbacks. To test the effects of call type on response, we ran a repeated measures ANOVA. Subjects oriented significantly more to an alarm call from a novel subject than to a novel alarm call from the habituation subject (F1,22 ¼ 11.76, P ¼ 0.002; Fig. 4). We also compared
SPROUL ET AL.: TAMARIN ALARM CALLS ENCODE CALLER ID
Frequency of habituation length
5
4
3
2
1
0
3
6
9
12
15 18 21 24 27 30 33 Number of trials to habituate subject
36
39
42
Figure 3. Distribution of the number of trials (i.e. calls) needed to habituate subjects across all sessions.
subject orientation to calls when the novel individual was the same sex as the habituation individual versus the opposite sex. Using a paired t test, there was no significant difference between how subjects responded to a novel same-sex call and to a novel opposite-sex call. Contrasting two individuals of the same sex, subjects readily discriminated between habituation and novel callers (t22 ¼ 4.21, P ¼ 0.0004). However, the difference in response to habituation versus novel callers of opposite sex was not significant (t22 ¼ 1.56, P ¼ 0.134; Fig. 5). Subjects sometimes vocalized (alarm calls or combination long calls) in response to alarm call playbacks. Subjects vocalized more often after alarm calls from novel callers than after calls from the same caller (t22 ¼ 2.08, P ¼ 0.05; Fig. 6).
DISCUSSION The habituationediscrimination method enables one to assess whether subjects perceive meaningful differences between two classes of stimuli. In the case presented here,
we habituated subjects to multiple exemplars from one individual and then asked whether they detected a meaningful difference when presented with novel calls from the same individual and novel calls from a different individual. Based on the level of their responses, results suggest that subjects perceived a more meaningful difference for the novel calls of a new individual than the novel calls of the same individual presented during habituation. There are two reasons why we think that these results are important. First, tamarins can not only extract information about caller identity from their combination long calls (Weiss et al. 2001; Weiss & Hauser 2002) but also from their alarm calls. These vocalizations have different functions, different acoustic morphologies, and based on preliminary acoustic analyses, different degrees of within-call type variability. Second, our results indicate that repeated exposure to one individual’s alarm calls does not cause general habituation to this call type, but rather, habituation to a particular individual’s alarm call. 2 Habituation Novel
2 1.8 1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0
1.6 Mean response
Mean response
1.8
1.4 1.2 1 0.8 0.6 0.4 0.2 0
Habituation calls
Novel calls
Figure 4. Mean þ SE number of orienting responses to playbacks of novel calls from the habituating subject and novel calls from a novel individual.
Same sex
Opposite sex
Figure 5. Mean orienting response broken down by the contrast of caller sex. Each average takes into account two trials for each call type. Therefore, if the subject oriented to both novel calls in a session, its response was counted as two.
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Mean response over two sessions
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2 1.8 1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0
*
Habituation calls
Novel calls
Figure 6. Subjects’ mean responses (alarm calls and combination long calls, CLCs) following playback of novel test calls and habituation test calls. *P ¼ 0.05.
Although the habituationediscrimination method does not permit definitive evidence for recognition of individual identity, it suggests that the acoustic difference between call exemplars within an individual’s alarm call repertoire is less than that between individuals, and this is precisely the kind of evidence that would be necessary for individual recognition; labelling calls as belonging to a particular individual would be further supported by operant methods, such as matching to sample. From a functional perspective, hearing a novel individual alarm calling could impart added information, perhaps confirming the presence of a predator or indicating its location. An important pressure on individual recognition of tamarin alarm calls may, therefore, have been the capacity to both identify reliable callers and determine when it is important to revive a habituated response. If an individual continues to alarm call in the absence of a threat, it may be considered unreliable. In the present study, when the habituation calls of one individual were repeated, subjects no longer oriented to it. However, subjects resumed orienting when a new individual’s call was presented, suggesting that a functional explanation for individual recognition may be that of confirming the presence of a predator. In addition to the orienting response, we also found differences in vocal responses: subjects were more likely to call back with combination long calls and alarm calls to playbacks of novel individuals than to playbacks of novel calls from the habituating individual. Both call types encode information about individual identity, yet the functional reasons for responding with one or the other in this context are unclear. One unexpected result of this experiment was the apparent reversal in the subjects’ ability to discriminate between same-sex and opposite-sex callers for the combination long call and alarm call. Previous work revealed a greater capacity to discriminate combination long calls from opposite-sex versus same-sex individuals (Weiss et al. 2001). Here, in contrast, tamarins showed a greater capacity to discriminate between the alarm calls of same-sex individuals. However, other factors could bias these results (i.e. the relationships between the opposite-sex callers). This issue warrants more detailed study in order to explore the variability in these acoustic signals and the extent to
which differences between call types map onto perceptual discriminability. Cottontop tamarins, and callitrichids more generally, are noted for their close social interactions within a small family group, where caller identity is likely to influence how others interpret and respond to a call. The social system of cottontop tamarins, in which breeding pairs are monogamous and group members share in the care of young, suggests further functional explanations for individual recognition in this alarm system. The variable risk to young, mates or helpers carrying young could impart additional selective pressures on recognizing caller identity and reliability. Furthermore, knowing an individual’s location can provide more detailed information about predator location and who is at risk. If two or more callers can be identified, the likelihood of a predator’s presence increases. Conversely, if one individual repeatedly alarmcalls when no predator is sighted and other individuals do not join in, then this could lessen the alarm response. Our findings suggest that the callitrichid alarm call should be included in comparisons to other social systems with alarm calls that encode individual information. Also, within-species comparisons, such as identifying acoustic features of recognition, can now be investigated and compared with the well-studied tamarin combination long call.
References Caine, N. G. 1993. Flexibility and co-operation as unifying themes in Saguinus social organization and behaviour: the role of predation pressures. In: Marmosets and Tamarins: Systemics, Behaviour and Ecology (Ed. by A. B. Rylands), pp. 201e219. New York: Oxford University Press. Caro, T. M. 1995. Pursuit-deterrence revisited. Trends in Ecology and Evolution, 10, 500e503. Caro, T. M. 2005. Antipredator Defenses in Birds and Mammals. Chicago: University of Chicago Press. Cheney, D. L. & Seyfarth, R. M. 1988. Assessment of meaning and the detection of unreliable signals by vervet monkeys. Animal Behaviour, 36, 477e486. Cheney, D. L. & Seyfarth, R. M. 1990. How Monkeys See the World: Inside the Mind of Another Species. Chicago: Chicago University Press.
SPROUL ET AL.: TAMARIN ALARM CALLS ENCODE CALLER ID
Cleveland, J. & Snowdon, C. T. 1982. The complex vocal repertoire of the adult cotton-top tamarin, Saguinus oedipus oedipus. Zeitschrift fu¨r Tierpsychologie, 58, 231e270. Cleveland, J. & Snowdon, C. T. 1984. Social development during the first twenty weeks in the cotton-top tamarin (Saguinus oedipus oedipus). Animal Behaviour, 32, 432e444. Evans, C. S. 1997. Referential signals. Perspectives in Ethology, 12, 99e143. Gyger, M., Marler, P. & Pickert, R. 1987. Semantics of an avian alarm calling system: the male domestic fowl, Gallus domesticus. Behaviour, 102, 15e40. Hare, J. F. & Atkins, B. A. 2001. The squirrel that cried wolf: reliability detection by juvenile Richardson’s ground squirrels (Spermophilus richardsonii). Behavioral Ecology and Sociobiology, 51, 108e112. Hauser, M. D. 1996. The Evolution of Communication. Cambridge, Massachusetts: MIT Press. Jouventin, P., Aubin, T. & Lengagne, T. 1999. Finding a parent in a king penguin colony: the acoustic system of individual recognition. Animal Behaviour, 57, 1175e1183. Karavanich, C. & Atema, J. 1998. Individual recognition and memory in lobster dominance. Animal Behaviour, 56, 1553e1560. Kijoma, S., Izumi, A. & Ceugniet, M. 2003. Identification of vocalizers by pant hoots, pant grunts, and screams in a chimpanzee. Primates, 44, 225e230. Le Roux, A. L., Jackson, T. P. & Cherry, M. I. 2001. Does Brants’ whistling rat (Parotomys brantsii) use an urgency-based alarm system in reaction to aerial and terrestrial predators? Behaviour, 138, 757e773. Macedonia, J. & Polak, J. F. 1989. Visual assessment of avian threat in semi-captive ringtailed lemurs (Lemur catta). Behaviour, 111, 291e304. Manser, M. B. 2001. The acoustic structure of suricates’ alarm calls varies with predator type and the level of response urgency. Proceedings of the Royal Society of London, Series B, 268, 2315e2324. Marler, P., Evans, C. S. & Hauser, M. D. 1992. Animal signals? Reference, motivation or both? In: Nonverbal Vocal Communication: Comparative and Developmental Approaches (Ed. by H. Papoucek, U. Ju ¨ rgens & M. Papoucek), pp. 66e86. Cambridge: Cambridge University Press. Miller, C. T. & Ghazanfar, A. A. 2002. Meaningful acoustic units in nonhuman primate vocal behavior. In: Cognitive Animal: Empirical and Theoretical Perspectives on Animal Cognition (Ed. by M. Bekoff, C. Allen & G. Burghardt), pp. 265e274. Cambridge, Massachusetts: MIT Press. Mitani, J., Gros-Louis, J. & Macedonia, J. 1996. Selection for acoustic individuality within the vocal repertoire of wild chimpanzees. International Journal of Primatology, 17, 569e583.
Munn, C. 1986. Birds that ‘cry wolf’. Nature, 319, 143e145. Neyman, P. F. 1978. Aspects of the ecology and social organization of free-ranging cotton-top tamarins (Saguinus oedipus) and the conservation status of the species. In: The Biology and Conservation of the Callitrichidae (Ed. by D. G. Kleiman), pp. 39e71. Washington, D.C.: Smithsonian Institution Press. Owings, D. H. & Morton, E. S. 1998. Animal Vocal Communication: a New Approach. Cambridge: Cambridge University Press. Randall, J. A. & Rogovin, K. A. 2002. Variation in and meaning of alarm calls in a social desert rodent, Rhombomys opimus. Ethology, 108, 513e527. Rendall, D., Rodman, P. S. & Emond, R. E. 1996. Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Animal Behaviour, 51, 1007e1015. Rendall, D., Owren, M. J. & Rodman, P. S. 1998. The role of vocal tract filtering in identity cueing in rhesus monkey (Macaca mulatta) vocalizations. Journal of the Acoustical Society of America, 103, 602e614. Sayigh, L. S., Tyack, P. L., Wells, R. S., Solow, A. R., Scott, M. D. & Irvine, A. B. 1999. Individual recognition in wild bottlenose dolphins: a field test using playback experiments. Animal Behaviour, 57, 41e50. Seyfarth, R. M., Cheney, D. L. & Marler, P. 1980. Vervet monkey alarm calls: semantic communication in a free-ranging primate. Animal Behaviour, 28, 1070e1094. Templeton, C. N., Greene, E. & Davis, C. 2005. Allometry of alarm calls: black-capped chickadees encode information about predator size. Science, 308, 1934e1937. Weiss, D. & Hauser, M. 2002. Perception of harmonics in the combination long call of cotton-top tamarins, Saguinus oedipus. Animal Behaviour, 64, 415e426. Weiss, D., Garibaldi, B. & Hauser, M. D. 2001. The production and perception of long calls by cotton-top tamarins (Saguinus oedipus): acoustic analyses and playback experiments. Journal of Comparative Psychology, 115, 258e271. Yin, S. & McCowan, B. 2004. Barking in domestic dogs: context specificity and individual identification. Animal Behaviour, 68, 343e355. ¨ hler, K. 2001. Predator-specific alarm calls in Campell’s Zuberbu monkeys, Ceropithecus campbelli. Behavioral Ecology and Sociobiology, 50, 414e422. ¨ hler, K., Noe¨, R. & Seyfarth, R. M. 1997. Diana monkey Zuberbu long-distance calls: messages for conspecifics and predators. Animal Behaviour, 53, 589e604.
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Cottontop tamarin, Saguinus oedipus, alarm calls contain sufficient information for recognition of individual identity C ATHERI NE S PROUL* , A LBERTO PALLERONI* & MA RC D. H AU S ER*†‡
*Department of Psychology, Harvard University yDepartment of Organismic & Evolutionary Biology, Harvard University zDepartment of Biological Anthropology, Harvard University (Received 10 November 2005; initial acceptance 18 January 2006; final acceptance 7 April 2006; published online 10 October 2006; MS. number: A10298)
Most work on individual recognition has focused on signals used in the context of social contact or mate attraction. Here we present the results of a playback experiment designed to test whether cues of individual identity are encoded in alarm calls given by cottontop tamarins during encounters with a trained and flying goshawk, Accipiter gentilis. Based on a habituationediscrimination paradigm previously used with this species to show individual recognition of their long calls, subjects showed the ability to distinguish individuals by their alarm calls alone. Once subjects habituated to multiple exemplars of one individual’s alarm call, their response was renewed to the alarm calls of another individual but not to a new set of alarm calls from the same individual. We discuss the implications of these results for current theories of signal processing. Ó 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Alarm calls are potentially rich sources for passing information to conspecifics. Based on field and laboratory studies of birds and mammals, it is now understood that these calls encode information about the type of predator that is attacking or the most adaptive escape route (Seyfarth et al. 1980; Gyger et al. 1987; Macedonia & Polak ¨ hler 2001; 1989; Marler et al. 1992; Manser 2001; Zuberbu Templeton et al. 2005) as well as the level of threat presented by the predator (Owings & Morton 1998; Le Roux et al. 2001; Randall & Rogovin 2002). Access to this information can expedite an animal’s reaction to a predator and therefore increase its chances of survival. In the case of animals with functionally referential alarm calls, the call itself elicits predator-specific defensive behaviour, rather than merely drawing the animal’s attention to the presence of a possible threat (Seyfarth et al. ¨ hler et al. 1997). Urgency-based calls, in 1980; Zuberbu contrast, alert animals to the proximity of a threat, thus affecting their vigilance (Owings & Morton 1998; Randall & Rogovin 2002). The urgency or motivational component of an alarm call can relay the proximity of the threat either by a change in the physical properties of the calls produced, suggesting the internal state of the caller (Evans
Correspondence: A. Palleroni, Department of Psychology, Harvard University, Cambridge, MA 02138, U.S.A. (email: aliparti@wjh. harvard.edu). 0003e 3472/06/$30.00/0
1997), or by a change in the type of call given (Randall & Rogovin 2002). What is not yet clear is the extent to which various species encode information about individual identity in their animal alarm calls and the extent to which it is decoded by listeners. Moreover, given the function of alarm calls, it is not clear whether such information is necessary or relevant since the primary adaptive goal is to warn kin or to notify the predator that it has been detected (Hauser 1996; Caro 2005). In the case of kin warning, a group-level signature would be relevant, whereas in the case of predator warning, no such information is pertinent. However, in cases where group size is small (e.g. monogamously mated species), selection may favour encoding of individual identity. Thus, in contrast to the wealth of evidence for individual-level acoustic signatures in nonalarm calls, including calls given during territorial defence, mate attraction and the establishment of contact (Rendall et al. 1996; Karavanich & Atema 1998; Jouventin, et al. 1999; Sayigh et al. 1999), to what extent is there comparable evidence in the context of predator alarm calls? As noted above, the function of alarm calls is either to alert kin or to deter predators by indicating that they have been sighted (Marler et al. 1992; Caro 1995, 2005; Rendall, et al. 1998). In addition to the alerting function of alarm calls, however, it is reasonable to suppose that selection may have favoured cues to individual identity because
1379 Ó 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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ANIMAL BEHAVIOUR, 72, 6
such information provides one path into the assessment of caller reliability. In other words, because some individuals may be less reliable than others, perhaps because they have a higher incidence of false alarms in the signal detection sense, recognizing individuals by voice alone will enable listeners to assess the odds that a predator has been detected, especially when the caller is out of sight. Information about individual identity may be a by-product of vocal tract morphology (Rendall et al. 1998), or result from variation that arises in the course of vocal learning and maturation. The question addressed here is the extent to which listeners can extract information about individual identity from subjects’ alarm calls. Mitani et al. (1996) proposed that different selective pressures could operate on the design features of vocalizations within a species’ repertoire, with long-range calls providing more distinctive cues to individuality when contrasted with close-range calls. The idea is that longrange calls are typically given to recipients who are out of view, and thus, individuality can only be extracted from acoustic cues. In contrast, when individuals vocalize to others in close range, sensory modalities other than audition may be used to identify individuals. Mitani et al. found that the distinctiveness of individual chimpanzees’ signatures varied significantly across call types. However, cues to individual identity were more reliable in the long-distance pant hoot than in the short-range pant grunt. While individuality was better encoded in long-distance calls, further experiments revealed that chimpanzees can recognize individuals using both types of calls under the controlled conditions of captivity (Kijoma et al. 2003). One pressure on the capacity to recognize individual alarm calls comes from considering the problem of deception, and in particular, the capacity to discriminate between reliable and unreliable callers. Hare & Atkins (2001) played back squirrel alarm calls from different individuals and either paired the call with a predator model or no stimulus at all. The alarm calls of individuals who were paired with the predator model induced greater response in subjects, suggesting that these callers were perceived as more reliable in predicting the presence of a predator than others who ‘cried wolf’. Vervet monkeys, Cercopithecus aethiops, also use cues to individual identity in alarm and nonalarm calls to distinguish reliable from unreliable callers (Cheney & Seyfarth 1988). Subjects that habituated to the alarm calls of an unreliable individual transferred habituation to an acoustically different alarm call with the same referent from that individual. In contrast, subjects that habituated to one individual’s alarm calls responded to an alarm call from a novel individual even if the referent was the same. In other words, as long as the test call was from a referentially distinctive class, independently of caller identity, subjects responded following habituation. In the case of vervets, infants may be unreliable sources of predator information (Cheney & Seyfarth 1990). Detecting cheaters provides another important functional reason to identify reliable individuals (Munn 1986). This combined ability to recognize individual callers and determine reliability may result in more efficient predator defence (Yin & McCowan 2004).
Cottontop tamarins, the subjects of our experiments, produce a variety of acoustically distinctive vocalizations (Cleveland & Snowdon 1982). To date, the best studied vocalization is the combination long call (CLC), a multisyllabic contact call. As one would expect, previous acoustic analyses and playback experiments indicate that this contact call not only carries information about individual identity, but that subjects also readily extract this information during perceptual playback experiments using both an antiphonal calling procedure as well as the habituationediscrimination method (Weiss et al. 2001; Miller & Ghazanfar 2002; Weiss & Hauser 2002). Here we look at the problem of individual recognition using the tamarins’ alarm call to an aerial predator. This call has not been studied in the laboratory to the degree that the combination long call has, and individual recognition has not been explored. Neyman (1978) noted that the cottontop tamarins that he studied in the wild seemed to have distinct alarm calls for birds of prey and for ground predators. Furthermore, wild tamarins did not give the aerial predator call unless the bird was flying; perching birds of prey failed to elicit alarm calls until they flew off (Neyman 1978). To test the hypothesis that tamarin alarm calls carry information that can be extracted to identify individual callers, we used the habituationediscrimination paradigm that successfully identified individual discrimination in tamarin combination long calls (Weiss & Hauser 2002). In prior work (C. Sproul, unpublished data), we used a trained, flying goshawk to simulate predation events on tamarins that were housed singly or in groups. The alarm calls given in these known contexts were used as stimuli in the following playback experiments.
METHODS
Subjects Cottontop tamarins are New World monkeys, native to the rainforests of Colombia. They are cooperative breeders, with both parents and offspring involved in rearing infants (Cleveland & Snowdon 1984). Snakes, ocelots, tayras and various hawks have been observed killing tamarins, and it is clear that flying hawks elicit strong alarm responses in tamarins (Caine 1993). Predation pressure has been hypothesized to be important in shaping the cooperative social group structure in tamarins (Caine 1993). We tested 23 adult cottontop tamarins, 12 males and 11 females (see Table 1). Each subject participated in two playback sessions. Subjects were captive born at either the New England Regional Primate Center in Southborough, Massachusetts, U.S.A. or the Cognitive Evolution Laboratory at Harvard University, where they were housed during the experiment. In addition to the small treats of raisins and marshmallows that subjects received in other experiments throughout the day, the animals’ diet consisted of monkey chow supplemented with sunflower seeds, peanuts, fruit, yogurt and vitamins given once a day in the early evening. Each subject was housed with its mate and offspring or parents in one of 11 cages.
SPROUL ET AL.: TAMARIN ALARM CALLS ENCODE CALLER ID
Table 1. Experimental subject history including experience with an aerial predator
Subject ID AC AG DD DG DW EM EN ID JG JK JM KW LG LS PB PJ RA RB RJ SD SH SP UB
Age (years) Sex 11 3 13 3 3 13 9 10 9 4 4 5 3 3 5 4 3 7 8 3 10 12 17
M M M F M F F M F F M F F F M M M F M M F M F
Home cage
Experience with goshawk in isolation
Experience with goshawk in a social context
5 5 8 3 7 10 2 10 5 7 6 8 4 6 9 4 3 9 1 10 11 2 1
N Y N Y N N Y N N N Y N N Y N N Y N N N Y Y N
N N N N Y N Y N N Y Y N Y Y Y Y N Y N N Y Y N
Each cage, measuring 1.5 2.0 1.2 m, was outfitted with nestboxes, branches, ropes and ladders.
Acoustic Stimuli Alarm calls were collected during an earlier experiment in which a goshawk was presented to a subject in isolation (see Fig. 1). During this experiment, subjects were housed in a large cage at one end of a 14-m-long hallway. To simulate a predatory event, the goshawk flew towards the 12
Frequency (kHz)
10 8 6 4 2 0
0.5
1 Time (s)
1.5
2
Figure 1. Spectrogram (sample rate 50 kHz, 256-point FFT, Hanning window) of an alarm call exemplar used in the playback.
subject from a concealed area at the opposite end of the hallway. At the end of the approach, the goshawk veered away and perched out of sight of the subject. Vocalizations were recorded onto DAT tapes using an ME-66 directional Sennheiser microphone and then acquired into a MatLab program for sound analysis. The microphone was placed 0.5 m from the cage. Because subjects moved during the presentation, the recording distance ranged from 0.5 to 1.5 m, during which subjects could be facing towards or away from the microphone. Subjects had no previous experience with aerial predation before these experiments.
Playback Procedure We replicated the general habituationediscrimination procedure used in previous studies of tamarins, exploring the perceptual mechanisms underlying their ability to process human speech as well as their combination long call (Weiss et al. 2001). We first transferred each subject from its home cage to a small test cage (0.60 0.40 0.15 m; Fig. 2a) with a wire mesh front and opaque Plexiglas on all other sides; this design generally caused subjects to hang on the wire mesh front, thereby facilitating the playback procedure, which required orientation to the concealed speaker. We placed a video camera directly in front of the wire mesh front of the test cage, while the playback speaker was concealed above, behind, and to the right of the subject. All experiments were run by an experimenter sitting outside the test room. The sound intensity at the playback box was 70e75 dB. Once the subject was sitting calmly in the test cage, the session began. To habituate our subjects, we played 12e15 exemplars of one individual’s alarm calls. Calls were played when the subject was looking down and to the right (in the opposite direction from the speaker for a maximum orientation response). A response was defined as orienting up and towards the speaker during the playback or within 2 s of its termination (Fig. 2b; for video clips of the responses, see http://www.wjh.harvard.edu/ wmnkylab/prothome.htm under ‘Acoustic perception and the orienting response’). The experimenter would wait until the animal was in this position to play an alarm call. The time between calls never exceeded 60 s and was never less than 10 s. This time interval was chosen because it was consistent with playback experiments previously run in our laboratory (e.g. Weiss & Hauser 2002). If the animal failed to orient to the speaker, the trial was marked ‘no’, and after three consecutive, unambiguous no responses, the animal was considered to be habituated. If the subject jumped, called or faced the speaker during the playback, we coded the trial as ‘bad’. Trials in which a subject’s response was ambiguous were coded as such. During online coding of habituation trials, we coded all ‘bad’ and ‘ambiguous’ responses as ‘yes’ responses in order to guarantee that all subjects entered the test phase following unambiguous ‘no’ responses. We consider this a conservative approach because our goal was to ensure that each subject entered the test phase after complete habituation, defined as three consecutive no responses.
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(a)
(b)
Before playback
During and postplayback
Figure 2. (a) Diagram of the playback set-up. (b) Example of an orienting response to the playback stimuli in which the subject oriented towards the hidden speaker, which was above and to the left of the subject.
Following habituation, we presented four test calls consisting of two novel calls from the habituation individual and two from a novel individual, counterbalanced for order of presentation. One condition contrasted two same-sex callers, whereas the second contrasted opposite-sex callers. Previous experiments with the tamarin’s combination long calls revealed that discrimination was more difficult for same-sex callers than for opposite-sex callers (Weiss et al. 2001). We presented the alarm calls of three adult males and three adult females, all familiar members of the colony. Paralleling the habituation phase, test trials were played 10e60 s after the prior trial. We aborted a session if a subject failed to habituate after 50 trials (i.e. calls); prior studies in our laboratory suggested that subjects are too agitated to participate once they have exceeded this number of trials. As indicated in our results below, most subjects habituated in less than 30 trials. Trials were also aborted if the subject was too agitated to perform properly, or if one of the four
test trials was marked ‘bad’. Out of 56 sessions run, we aborted 10 based on these criteria. We digitized each session and coded all trials blind to the condition. Interobserver reliability was greater than 95%.
RESULTS Across all sessions, the mean SD number of trials to habituation was 15 8.06 (range 4e41, N ¼ 46). This value did not differ significantly between different caller identities (independent samples t test: t44 ¼ 0.44, P ¼ 0.67). Figure 3 plots the frequency distribution of the number of trials to habituation for the entire data set of playbacks. To test the effects of call type on response, we ran a repeated measures ANOVA. Subjects oriented significantly more to an alarm call from a novel subject than to a novel alarm call from the habituation subject (F1,22 ¼ 11.76, P ¼ 0.002; Fig. 4). We also compared
SPROUL ET AL.: TAMARIN ALARM CALLS ENCODE CALLER ID
Frequency of habituation length
5
4
3
2
1
0
3
6
9
12
15 18 21 24 27 30 33 Number of trials to habituate subject
36
39
42
Figure 3. Distribution of the number of trials (i.e. calls) needed to habituate subjects across all sessions.
subject orientation to calls when the novel individual was the same sex as the habituation individual versus the opposite sex. Using a paired t test, there was no significant difference between how subjects responded to a novel same-sex call and to a novel opposite-sex call. Contrasting two individuals of the same sex, subjects readily discriminated between habituation and novel callers (t22 ¼ 4.21, P ¼ 0.0004). However, the difference in response to habituation versus novel callers of opposite sex was not significant (t22 ¼ 1.56, P ¼ 0.134; Fig. 5). Subjects sometimes vocalized (alarm calls or combination long calls) in response to alarm call playbacks. Subjects vocalized more often after alarm calls from novel callers than after calls from the same caller (t22 ¼ 2.08, P ¼ 0.05; Fig. 6).
DISCUSSION The habituationediscrimination method enables one to assess whether subjects perceive meaningful differences between two classes of stimuli. In the case presented here,
we habituated subjects to multiple exemplars from one individual and then asked whether they detected a meaningful difference when presented with novel calls from the same individual and novel calls from a different individual. Based on the level of their responses, results suggest that subjects perceived a more meaningful difference for the novel calls of a new individual than the novel calls of the same individual presented during habituation. There are two reasons why we think that these results are important. First, tamarins can not only extract information about caller identity from their combination long calls (Weiss et al. 2001; Weiss & Hauser 2002) but also from their alarm calls. These vocalizations have different functions, different acoustic morphologies, and based on preliminary acoustic analyses, different degrees of within-call type variability. Second, our results indicate that repeated exposure to one individual’s alarm calls does not cause general habituation to this call type, but rather, habituation to a particular individual’s alarm call. 2 Habituation Novel
2 1.8 1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0
1.6 Mean response
Mean response
1.8
1.4 1.2 1 0.8 0.6 0.4 0.2 0
Habituation calls
Novel calls
Figure 4. Mean þ SE number of orienting responses to playbacks of novel calls from the habituating subject and novel calls from a novel individual.
Same sex
Opposite sex
Figure 5. Mean orienting response broken down by the contrast of caller sex. Each average takes into account two trials for each call type. Therefore, if the subject oriented to both novel calls in a session, its response was counted as two.
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Mean response over two sessions
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2 1.8 1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0
*
Habituation calls
Novel calls
Figure 6. Subjects’ mean responses (alarm calls and combination long calls, CLCs) following playback of novel test calls and habituation test calls. *P ¼ 0.05.
Although the habituationediscrimination method does not permit definitive evidence for recognition of individual identity, it suggests that the acoustic difference between call exemplars within an individual’s alarm call repertoire is less than that between individuals, and this is precisely the kind of evidence that would be necessary for individual recognition; labelling calls as belonging to a particular individual would be further supported by operant methods, such as matching to sample. From a functional perspective, hearing a novel individual alarm calling could impart added information, perhaps confirming the presence of a predator or indicating its location. An important pressure on individual recognition of tamarin alarm calls may, therefore, have been the capacity to both identify reliable callers and determine when it is important to revive a habituated response. If an individual continues to alarm call in the absence of a threat, it may be considered unreliable. In the present study, when the habituation calls of one individual were repeated, subjects no longer oriented to it. However, subjects resumed orienting when a new individual’s call was presented, suggesting that a functional explanation for individual recognition may be that of confirming the presence of a predator. In addition to the orienting response, we also found differences in vocal responses: subjects were more likely to call back with combination long calls and alarm calls to playbacks of novel individuals than to playbacks of novel calls from the habituating individual. Both call types encode information about individual identity, yet the functional reasons for responding with one or the other in this context are unclear. One unexpected result of this experiment was the apparent reversal in the subjects’ ability to discriminate between same-sex and opposite-sex callers for the combination long call and alarm call. Previous work revealed a greater capacity to discriminate combination long calls from opposite-sex versus same-sex individuals (Weiss et al. 2001). Here, in contrast, tamarins showed a greater capacity to discriminate between the alarm calls of same-sex individuals. However, other factors could bias these results (i.e. the relationships between the opposite-sex callers). This issue warrants more detailed study in order to explore the variability in these acoustic signals and the extent to
which differences between call types map onto perceptual discriminability. Cottontop tamarins, and callitrichids more generally, are noted for their close social interactions within a small family group, where caller identity is likely to influence how others interpret and respond to a call. The social system of cottontop tamarins, in which breeding pairs are monogamous and group members share in the care of young, suggests further functional explanations for individual recognition in this alarm system. The variable risk to young, mates or helpers carrying young could impart additional selective pressures on recognizing caller identity and reliability. Furthermore, knowing an individual’s location can provide more detailed information about predator location and who is at risk. If two or more callers can be identified, the likelihood of a predator’s presence increases. Conversely, if one individual repeatedly alarmcalls when no predator is sighted and other individuals do not join in, then this could lessen the alarm response. Our findings suggest that the callitrichid alarm call should be included in comparisons to other social systems with alarm calls that encode individual information. Also, within-species comparisons, such as identifying acoustic features of recognition, can now be investigated and compared with the well-studied tamarin combination long call.
References Caine, N. G. 1993. Flexibility and co-operation as unifying themes in Saguinus social organization and behaviour: the role of predation pressures. In: Marmosets and Tamarins: Systemics, Behaviour and Ecology (Ed. by A. B. Rylands), pp. 201e219. New York: Oxford University Press. Caro, T. M. 1995. Pursuit-deterrence revisited. Trends in Ecology and Evolution, 10, 500e503. Caro, T. M. 2005. Antipredator Defenses in Birds and Mammals. Chicago: University of Chicago Press. Cheney, D. L. & Seyfarth, R. M. 1988. Assessment of meaning and the detection of unreliable signals by vervet monkeys. Animal Behaviour, 36, 477e486. Cheney, D. L. & Seyfarth, R. M. 1990. How Monkeys See the World: Inside the Mind of Another Species. Chicago: Chicago University Press.
SPROUL ET AL.: TAMARIN ALARM CALLS ENCODE CALLER ID
Cleveland, J. & Snowdon, C. T. 1982. The complex vocal repertoire of the adult cotton-top tamarin, Saguinus oedipus oedipus. Zeitschrift fu¨r Tierpsychologie, 58, 231e270. Cleveland, J. & Snowdon, C. T. 1984. Social development during the first twenty weeks in the cotton-top tamarin (Saguinus oedipus oedipus). Animal Behaviour, 32, 432e444. Evans, C. S. 1997. Referential signals. Perspectives in Ethology, 12, 99e143. Gyger, M., Marler, P. & Pickert, R. 1987. Semantics of an avian alarm calling system: the male domestic fowl, Gallus domesticus. Behaviour, 102, 15e40. Hare, J. F. & Atkins, B. A. 2001. The squirrel that cried wolf: reliability detection by juvenile Richardson’s ground squirrels (Spermophilus richardsonii). Behavioral Ecology and Sociobiology, 51, 108e112. Hauser, M. D. 1996. The Evolution of Communication. Cambridge, Massachusetts: MIT Press. Jouventin, P., Aubin, T. & Lengagne, T. 1999. Finding a parent in a king penguin colony: the acoustic system of individual recognition. Animal Behaviour, 57, 1175e1183. Karavanich, C. & Atema, J. 1998. Individual recognition and memory in lobster dominance. Animal Behaviour, 56, 1553e1560. Kijoma, S., Izumi, A. & Ceugniet, M. 2003. Identification of vocalizers by pant hoots, pant grunts, and screams in a chimpanzee. Primates, 44, 225e230. Le Roux, A. L., Jackson, T. P. & Cherry, M. I. 2001. Does Brants’ whistling rat (Parotomys brantsii) use an urgency-based alarm system in reaction to aerial and terrestrial predators? Behaviour, 138, 757e773. Macedonia, J. & Polak, J. F. 1989. Visual assessment of avian threat in semi-captive ringtailed lemurs (Lemur catta). Behaviour, 111, 291e304. Manser, M. B. 2001. The acoustic structure of suricates’ alarm calls varies with predator type and the level of response urgency. Proceedings of the Royal Society of London, Series B, 268, 2315e2324. Marler, P., Evans, C. S. & Hauser, M. D. 1992. Animal signals? Reference, motivation or both? In: Nonverbal Vocal Communication: Comparative and Developmental Approaches (Ed. by H. Papoucek, U. Ju ¨ rgens & M. Papoucek), pp. 66e86. Cambridge: Cambridge University Press. Miller, C. T. & Ghazanfar, A. A. 2002. Meaningful acoustic units in nonhuman primate vocal behavior. In: Cognitive Animal: Empirical and Theoretical Perspectives on Animal Cognition (Ed. by M. Bekoff, C. Allen & G. Burghardt), pp. 265e274. Cambridge, Massachusetts: MIT Press. Mitani, J., Gros-Louis, J. & Macedonia, J. 1996. Selection for acoustic individuality within the vocal repertoire of wild chimpanzees. International Journal of Primatology, 17, 569e583.
Munn, C. 1986. Birds that ‘cry wolf’. Nature, 319, 143e145. Neyman, P. F. 1978. Aspects of the ecology and social organization of free-ranging cotton-top tamarins (Saguinus oedipus) and the conservation status of the species. In: The Biology and Conservation of the Callitrichidae (Ed. by D. G. Kleiman), pp. 39e71. Washington, D.C.: Smithsonian Institution Press. Owings, D. H. & Morton, E. S. 1998. Animal Vocal Communication: a New Approach. Cambridge: Cambridge University Press. Randall, J. A. & Rogovin, K. A. 2002. Variation in and meaning of alarm calls in a social desert rodent, Rhombomys opimus. Ethology, 108, 513e527. Rendall, D., Rodman, P. S. & Emond, R. E. 1996. Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Animal Behaviour, 51, 1007e1015. Rendall, D., Owren, M. J. & Rodman, P. S. 1998. The role of vocal tract filtering in identity cueing in rhesus monkey (Macaca mulatta) vocalizations. Journal of the Acoustical Society of America, 103, 602e614. Sayigh, L. S., Tyack, P. L., Wells, R. S., Solow, A. R., Scott, M. D. & Irvine, A. B. 1999. Individual recognition in wild bottlenose dolphins: a field test using playback experiments. Animal Behaviour, 57, 41e50. Seyfarth, R. M., Cheney, D. L. & Marler, P. 1980. Vervet monkey alarm calls: semantic communication in a free-ranging primate. Animal Behaviour, 28, 1070e1094. Templeton, C. N., Greene, E. & Davis, C. 2005. Allometry of alarm calls: black-capped chickadees encode information about predator size. Science, 308, 1934e1937. Weiss, D. & Hauser, M. 2002. Perception of harmonics in the combination long call of cotton-top tamarins, Saguinus oedipus. Animal Behaviour, 64, 415e426. Weiss, D., Garibaldi, B. & Hauser, M. D. 2001. The production and perception of long calls by cotton-top tamarins (Saguinus oedipus): acoustic analyses and playback experiments. Journal of Comparative Psychology, 115, 258e271. Yin, S. & McCowan, B. 2004. Barking in domestic dogs: context specificity and individual identification. Animal Behaviour, 68, 343e355. ¨ hler, K. 2001. Predator-specific alarm calls in Campell’s Zuberbu monkeys, Ceropithecus campbelli. Behavioral Ecology and Sociobiology, 50, 414e422. ¨ hler, K., Noe¨, R. & Seyfarth, R. M. 1997. Diana monkey Zuberbu long-distance calls: messages for conspecifics and predators. Animal Behaviour, 53, 589e604.
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