Ethology

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

* Department of Neurobiology Cognitive Ethology, German 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 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 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 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 421¢S7309¢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 animal was engaged in a quiet activity with little or much information available on the predator fauna of no locomotion, i.e. resting, grooming, feeding or the area, but several case studies of sightings and relaxed foraging. To avoid interfering stimuli we con- attacks report on a wide variety of preda- ducted all playback experiments when no territorial tors, such as large raptors (Heymann 1990; Overs- encounters or natural predator alarms took place. The luijs Vasquez & Heymann 2001) and snakes focal animals were chosen opportunistically when all (Bartecki & Heymann 1987; Shahuano Tello et al. the required conditions were met. Altogether, 10 2002). Attacks of terrestrial predators like cats and S. fuscicollis and 11 S. mystax individuals were tested. mustelids are of course difficult to observe, as these We aimed to test any one focal individual with all animals are strongly disturbed by the human obser- three playback types (aerial, terrestrial, and control). ver following the monkeys. Nevertheless, during this We used an ‘all combination design’, i.e. we played study, the first author had the opportunity to see S. mystax calls both to S. mystax and to S. fuscicollis sub- two (Eira barbara) and two bush dogs (prob- jects, and S. fuscicollis calls both to S. fuscicollis and ably Atelocynus microtis) in immediate proximity of S. mystax subjects. All playback experiments were con- the study groups. An (Felis pardalis) has been ducted during the two study periods (see study site seen at EBQB by a first author’s co-worker in 2001 and subjects). To avoid habituation, we attempted to (P. Lo¨ ttker, pers. comm.). For more information on conduct subsequent experiments in the same focal predator fauna see also Smith et al. (2004). There is group with at least 1 d of spacing in between. Only no data available on the predation pressure. in three cases, a subsequent experiment had to be During the study period two fully habituated carried out the following day. groups of tamarins inhabited the area. A third group was habituated by the first author and a field assist- Playback Stimuli ant starting late Oct. 2001. Each group consisted of the two species Saguinus mystax and Saguinus fuscicol- All calls used as playback stimuli were recorded in lis, which formed stable associations. Group sizes the same study groups at EBQB during 6 mo of pre- ranged from eight to 14 individuals, including liminary studies in 2000 and during the first play- between four and six S. fuscicollis and between three back study period from May to Nov. 2001. We and nine S. mystax. The number of individuals chan- adjusted the volume of the calls to that observed ged in the course of time because of migration, birth during naturally occurring predator encounters. or death. Individuals could be identified by a combi- Figure 1 shows spectrograms of the characteristic nation of natural features such as body size, body aerial and terrestrial alarm calls of S. fuscicollis and shape, and fur characteristics as well as size, color- S. mystax. The figure represents typical examples of ation, and pigmentation of genitals or other body the call series we used as playback stimuli. A call parts. At the EBQB the observers can approach any series is a unit of calls in the same sequence as nat- habituated tamarin up to a proximity of approxi- urally recorded. Note that both species’ aerial and mately 1 m (S. fuscicollis)or3m(S. mystax), which S. mystax terrestrial alarm call series consist exclusively facilitates individual recognition. By means of bin- of repetitions of one and the same call type, whereas oculars the identification is also possible from larger S. fuscicollis terrestrial alarm call series contain several distances and at greater heights. different call types. A multi-parametric acoustic ana- lysis of the various call types will be given in a sep- arate paper (J. Kirchhof & K. Hammerschmidt, Experimental Procedure unpubl. data). For the playback experiments we used a SONY TCD- We used only alarm calls of which the eliciting D100 DAT-Recorder connected to a BOSE ‘Room- predator or model type (aerial or terrestrial) was

Ethology 112 (2006) 346–354 ª 2006 The Authors 348 Journal compilation ª 2006 Blackwell Verlag, Berlin J. Kirchhof & K. Hammerschmidt Functionally Referential Alarm Calls in Tamarins

(a)

(b)

Fig. 1: Spectrograms of the characteristic (a) aerial and (b) terrestrial alarm calls of S. fuscicollis and S. mystax. The call series represent typical examples of the ones we used as playback stimuli known. As it was difficult to record a sufficient repeated. Thus, the entire playback had a total dur- number of alarm calls with known stimuli, not every ation of approximately 35–40 s. The recording of the experiment could be conducted with a unique call focal animal began several seconds before the first series. Therefore, some call series were used in more call series and ended between 30 and 50 s after the than one experiment. For the 19 aerial playback second call series. experiments we used 10 different call series, which were all recorded during natural predator encoun- Behavioural Analysis ters. For the 20 terrestrial playback experiments we used 11 different call series, which were recorded All video recordings were digitised and viewed with during natural encounters and presentations of a live the program ADOBE PREMIERE 4.2 with a time dog or a stuffed toy serving as an ocelot (F. pardalis) resolution of 25 frames per second (duration of a model. For the 17 control playback experiments we single frame = 0.04 s). We measured the latency to used 11 different stimuli: nine of these were differ- the first reaction of the focal animal (mostly a turn- ent song series of common birds in the area which ing of the head) by counting the frames, beginning are known to be harmless to the tamarins (n = 5: from the start of the first call series. We then coun- Lipaugus vociferans, screaming piha, n = 4: Ramphastus ted the frames the focal animal spent looking up, spec., toucan), one was the observer’s voice and one down, and to remaining directions, ending 25 s after was ambient noise of the forest. Table 1 gives the the start of the second call series. The durations of distribution of playback experiments regarding play- all directions were summed up to build the duration back type (aerial, terrestrial, and control), focal spe- of total looking. By doing so all analysed playback cies and call origin (conspecific or heterospecific). videos had a duration of approximately 60 s All playbacks were designed as follows: an initial (x = 54.70 Æ 5.35 s, n = 64). For each playback call series with a duration of 8–9 s was followed by a experiment, we also determined the direction of the pause of 20–25 s, and then the same call series was focal animal’s first glance following the stimulus. We recorded a change of gaze direction only when the Table 1: Number of conducted playback experiments subject had turned its head in response to the call series. If the subject maintained the same gaze direc- S. fuscicollis S. mystax tion before as after the stimulus, we scored it as ‘no Conspecific Heterospecific Conspecific Heterospecific direction’. Tamarins usually make obvious head movements while scanning their environment. The Aerial 4 6 5 4 looking direction was therefore considered as ‘up’ or Terrestrial 7 3 6 4 ‘down’ when the angle of the tamarin’s head Control 10 7 reached at least 45 declination from the horizontal

Ethology 112 (2006) 346–354 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag, Berlin 349 Functionally Referential Alarm Calls in Tamarins J. Kirchhof & K. Hammerschmidt line. All smaller angles were considered as ‘straight’. found short latencies only in aerial playbacks, in ter- It was also sampled when the subject looked to the restrial playbacks S. mystax showed intermediate loudspeaker. Glances of the animals to their own latencies and the longest in control playbacks body, the body of grooming partners or glances at (Fig. 2). Therefore, we found significant differences items close by, such as hand-held food, were not in latency between the two species only after play- sampled as any looking direction. back a control call (GLM: F1,11 = 12.88, p = 0.004). We found no significant differences in latency after playback of an aerial alarm call and a terrestrial Statistical Analysis alarm call. Although we tried to test each focal animal within all three playback types and both with conspecific Looking Durations and heterospecific calls, some subjects were not available frequently enough in an appropriate test For S. fuscicollis and S. mystax, we found significant situation, and others died or disappeared before the differences in the looking directions between aerial test series was completed. Thus, the test tables inclu- and terrestrial alarm call playbacks (Fig. 3). After ded some missing values. Therefore, we were not playback of an aerial alarm call both species spent able to use a test design, which includes the different significantly more time looking up than looking playback types at the same time. We used a general- down (GLM repeated measurement: F1,16 = 51.3, ized linear model analysis (GLM, SPSS 12) to iden- p = 0.000). After playback of a terrestrial alarm call tify differences in latency related to playback type, both species spent significantly more time looking species and call origin. To test our paradigm that down than looking up (GLM repeated measure- subjects look significantly longer upwards in ment: F1,15 = 14.5, p = 0.002). After playback of a response to the playback of aerial alarm calls than in control call neither species showed stimulus signifi- response to the playback of terrestrial alarm calls we cant differences in the time looking up or down used the GLM repeated measurement procedure (GLM repeated measurement: F1,16 = 0.221, (SPSS 12). We did separate tests for the three play- p = 0.645). back types (aerial, terrestrial and control). To test the direction of the first glance, we grouped the possible directions in three categories (up, down, and other directions) and used Pearson chi-quadrate test (SPSS 12).

Results

Latency For S. fuscicollis, we found similar short latencies in all three playback types (Fig. 2). For S. mystax we

Fig. 2: Mean and SEM of latencies in response to the different play- Fig. 3: Durations (mean and SEM) of looking up (a) and looking down back types (b) given in percent of the total looking (TL)

Ethology 112 (2006) 346–354 ª 2006 The Authors 350 Journal compilation ª 2006 Blackwell Verlag, Berlin J. Kirchhof & K. Hammerschmidt Functionally Referential Alarm Calls in Tamarins

After playback of an aerial alarm call we found no subjects maintained the same gaze direction as prior significant differences between the two species (GLM to the playback. repeated measurement: F1,16 = 2.33, p = 0.146), or origin of the alarm calls (GLM repeated measure- Discussion ment: F1,16 = 1.88, p = 0.19). We also found no sig- nificant interactions between looking direction and Saddleback and moustached tamarins looked signifi- species or call origin (looking duration · species: cantly longer upwards in response to aerial alarm

F1,16 = 2.83, p = 0.111; looking duration · call ori- calls and significantly longer downwards in response gin: F1,16 = 0.89, p = 0.361). We also found no signi- to terrestrial alarm calls. Thus, they reacted as if ficant differences between the two species after external referents, i.e. information about the pred- playback of a terrestrial alarm call (GLM repeated ator type or the appropriate reaction, were encoded measurement: F1,15 = 3.63, p = 0.076), but because in the acoustic features of the calls. This conclusion of the small sample size this result should be taken is supported by the fact that none of the two species with caution. We found no significant difference showed any preference after playback of control related to call origin (GLM repeated measurement: calls. In addition, we found no differences in the

F1,16 = 0.198, p = 0.863) and no significant interac- responses of S. fuscicollis and S. mystax whether the tions (looking duration · species: F1,16 = 0.52, alarm call stimulus was produced by a conspecific or p = 0.481; looking duration · call origin: F1,16 = a heterospecific caller. This finding indicates that the 2.43, p = 0.14). In a similar way, we found neither call origin had no influence on the response of significant differences between species after playback either species. of a control stimulus (GLM repeated measurement: The direction of the first glance corresponded in

F1,16 = 0.01, p = 0.92), nor a significant interac- most cases to the direction from which the simulated tion between looking duration and species (looking predator would have attacked. The only exception duration · species: F1,16 = 0.007, p = 0.936). was the response of S. fuscicollis to the terrestrial alarm calls. Here, we found no preference of the first glance. This could correspond to an apparently more Direction of the First Glance general usage of their terrestrial alarm calls: while all Table 2 shows the directions of the subjects’ first the other calls, i.e. both species’ aerial alarm calls glances after hearing the playback stimulus. Saguinus and S. mystax terrestrial alarm calls, were exclusively mystax never looked immediately down after aerial used in the predator-specific situation, calls acoustic- playbacks, and never immediately up after terrestrial ally similar to S. fuscicollis terrestrial alarm calls were playbacks (chi-square two-tailed: df = 4, p = 0.025, also given in other contexts, such as aggressive n = 19). Likewise, S. fuscicollis never looked immedi- inter-group encounters. There are other studies in ately down after aerial playbacks, but by contrast, nonhuman primates (Fichtel & Kappeler 2002; Fich- showed no clear tendency in the first glances after tel et al. 2005) and birds (Seyfarth & Cheney 1990) terrestrial playbacks (Table 2). Corresponding to that, that also suggest a more general usage of terrestrial the chi-quadrate test revealed no significant differ- alarm calls in comparison with aerial alarm calls. ences comparing the direction of the first glance This is in line with our observation that aerial and (chi-square two-tailed: df = 4, p = 0.181, n = 26). In terrestrial alarm vocalisation of S. mystax and aerial control experiments, both species’ first glances were alarm vocalisation of S. fuscicollis contained only one into various directions and in three cases the call type, whereas the terrestrial alarm vocalisation of S. fuscicollis consisted of several different call types (see Fig. 1). Table 2: Direction of the first glance. The table indicates the frequen- As far as we know, this study is the first to dem- cies of the different looking directions immediately after hearing the onstrate functionally referential alarm calls in New playback stimulus World primates. Functionally referential alarm call S. fuscicollis Playback type S. mystax Playback type systems have been found among primates in three Looking cercopithecine species (Cercopithecus aethiops: Seyfarth direction Aerial Terrestrial Control Aerial Terrestrial Control et al. 1980; C. diana and C. campbelli: Zuberbu¨ hler Up 6 2 4 5 0 1 et al. 1997; Zuberbu¨ hler 2001) and in ring-tailed Down 0 2 0 0 5 1 lemurs (L. catta: Macedonia 1990). Furthermore, Straight/to 35 4 32 2 functionally referential alarm call systems also exist loudspeaker among carnivores (Suricata suricatta: Manser 2001;

Ethology 112 (2006) 346–354 ª 2006 The Authors Journal compilation ª 2006 Blackwell Verlag, Berlin 351 Functionally Referential Alarm Calls in Tamarins J. Kirchhof & K. Hammerschmidt

Manser et al. 2001), and among birds (Gallus gallus: behaviour (Kirchhof, personal observation). It Gyger et al. 1987; Evans et al. 1993a), and are sup- remains open to which extent an impeded visual posed to exist in some species of rodents (e.g. Tam- contact to the predator can shape the structure of an ura & Young 1993; Weary & Kramer 1995; Greene alarm call system, but these data suggest a certain & Meagher 1998). Functionally referential alarm call connection. systems hence have evolved independently in sev- Another noteworthy aspect is that functionally eral different , and taxonomic affiliation is referential systems can also develop in species with unlikely to be a major selective factor to develop only small differences in their ways of escaping from such systems. Mixed alarm call systems so far have aerial and terrestrial predators. Diana and Campbell’s been described by Fichtel & Kappeler (2002) for red- monkeys approach the predator in natural encoun- fronted lemurs (Eulemur fulvus rufus) and white sifa- ters with both eagles and leopards. The subtle differ- kas (Propithecus verreauxi verreauxi). The assumption ence between the two situations is that in response of a mixed system in a callitrichid species, a group to aerial predators typically only adult males quite distantly related to prosimians, adds further approach and the rest of the group stays behind, support that a species’ taxonomic classification is not while in response to leopards often the whole group the only predictor for its alarm call system. This is approaches the predator (Zuberbu¨ hler et al. 1997; further enhanced by the fact that saddleback and Zuberbu¨ hler 2001). Nevertheless, both species have moustached tamarins are closely related to each evolved functionally referential alarm calls for the other, but still seem to exhibit differences in their two predator types. The same phenomenon can be alarm call systems. seen in the suricate (S. suricatta), a social mongoose, Although S. fuscicollis and S. mystax both show inhabiting the dry plains of southern Africa. predator-specific reactions which is in line with the Although these animals do not show strongly dis- hypothesis of Macedonia & Evans (1993) that differ- tinct predator-specific reactions, they give function- ent escape strategies are the main selective force for ally referential alarm calls to aerial and terrestrial the evolution of referential signalling, the difference predators (Manser et al. 2001). In natural encoun- between the alarm call behaviour of S. fuscicollis and ters with both aerial and terrestrial predators, they S. mystax found in the present study suggests there scan the area and move to a shelter, but in response might be more factors involved. One obvious differ- to aerial predators they sometimes additionally scan ence between S. fuscicollis and S. mystax is that they the sky, while in response to terrestrial predators use different height levels in the forest. S. fuscicollis they often gather and move away after looking usually range lower in the forest than S. mystax and around (Manser et al. 2001). This fine-tuned adjust- even sometimes come down to the ground (Norconk ment of reactions hints at the possibility that for 1990; Smith et al. 2004). Therefore, they generally them it might be useful enough to know where the seem to be more vulnerable to terrestrial predators predator approaches from, to look into the respective than S. mystax. In this context, it is interesting to direction, and to decide then what to do. More gen- note that S. fuscicollis mobbed terrestrial predator erally spoken, it may not be necessary to have models significantly longer than S. mystax did (Kir- clearly distinct escape strategies, like vervets, but the chhof 2003). On the other hand, S. fuscicollis, closer mere need of a fast predator recognition and, accord- proximity to the ground might also imply that for ingly, an appropriate scanning response might well them terrestrial predators are easier to recognize be sufficient to develop a referential signalling than aerial predators. Hardie & Buchanan-Smith system. (2000) studied mixed-species groups of S. fuscicollis In this study, we found evidence for a functionally and S. labiatus, which exhibit a similar height divi- referential alarm call system in S. mystax and a com- sion as associated S. fuscicollis and S. mystax (S. fusci- bined system of one functionally referential aerial collis in lower strata and S. labiatus in higher strata: alarm call and more non-specific terrestrial alarm Buchanan-Smith 1990). They found that S. fuscicollis calls in S. fuscicollis. It has been suggested that the detected novel non-threatening objects faster when type of alarm call system might be shaped on the those objects were on the ground, while S. labiatus one hand by certain ecological key factors, such as detected objects faster that were at greater heights. the body size, a terrestrial or arboreal habitat, and In the present study, it could sometimes be seen that the density of a habitat, and on the other hand in terrestrial playback experiments S. fuscicollis only by the presence or absence of different escape modes shortly checked the ground visually, whereas S. mys- from predators (e.g. Evans et al. 1993b; Macedonia tax often exhibited a rather conspicuous searching & Evans 1993; Evans 1997). However, saddleback

Ethology 112 (2006) 346–354 ª 2006 The Authors 352 Journal compilation ª 2006 Blackwell Verlag, Berlin J. Kirchhof & K. Hammerschmidt Functionally Referential Alarm Calls in Tamarins and moustached tamarins are of more or less the Evans, C. S., Evans, L. & Marler, P. 1993a: On the mean- same body size, live both highly arboreal in the ing of alarm calls: functional reference in an avian same dense forest habitat, and respond both in dis- vocal system. Anim. Behav. 46, 23—38. tinct ways to aerial and terrestrial predators. Never- Evans, C. S., Macedonia, J. M. & Marler, P. 1993b: theless, they vary considerably in the degree of their Effects of apparent size and speed on the response of call specificity. Thus it seems that, although ecologi- chickens, Gallus gallus, to computer-generated simula- cal conditions and predator-specific reactions appar- tions of aerial predators. Anim. Behav. 46, 1—11. ently are important, they may not be sufficient to Fichtel, C. & Kappeler, P. M. 2002: Anti-predator beha- explain the evolution of a certain type of alarm call vior of group-living Malagasy primates: mixed evidence for a referential alarm call system. Behav. Ecol. Socio- system. It would be interesting to investigate more biol. 51, 262—275. species that are as similar as S. fuscicollis and S. mystax Fichtel, C., Perry, S. & Gros-Louis, J. 2005: Alarm calls of and exhibit different alarm call systems. white-faced capuchin monkeys: an acoustic analysis. Anim. Behav. 70, 165—176. Acknowledgements Fischer, J., Hammerschmidt, K., Cheney, D. L. & Sey- farth, R. M. 2001: Acoustic features of female chacma We are grateful to Eckhard Heymann for the permis- baboon barks. Ethology 107, 33—54. sion to conduct the study at the EBQB field station Greene, E. & Meagher, T. 1998: Red squirrels, Tamias- and for his essential support throughout the study. ciurus hudsonicus, produce predator-class specific alarm We thank Dietmar Todt and Uwe Ju¨ rgens for sup- calls. Anim. Behav. 55, 511—518. port and discussion. In addition, we thank Roger Gyger, M., Marler, P. & Pickert, R. 1987: Semantics of an Mundry for improving an earlier version of the avian alarm call system: the male domestic fowl, Gallus manuscript and Julia Fischer, Elisabeth Scheiner and domesticus. Behaviour 102, 15—20. Eckhard Heymann for helpful comments and discus- Hardie, S. M. & Buchanan-Smith, H. M. 2000: Responses sion. The study would not have been possible with- of captive single- and mixed-species groups of Saguinus out the invaluable help of our field assistants Jeisen to novel nonthreatening objects. Int. J. Primatol. 21, Shahuano Tello and Camilo Flores Amasifue´n. This 629—648. research was supported by the DAAD and the Evan- Heymann, E. W. 1987: A field observation of predation gelisches Studienwerk Villigst e.V. on a moustached tamarin (Saguinus mystax) by an ana- conda. Int. J. Primatol. 8, 193—195. Heymann, E. 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Ethology 112 (2006) 346–354 ª 2006 The Authors 354 Journal compilation ª 2006 Blackwell Verlag, Berlin