Heterospecific recognition of referential alarm calls in two species of lemur

ABSTRACT

Alarm vocalizations are a common feature of the mammalian antipredator response. The meaning and function of these calls vary between species, with some species using calls to reference-specific categories of predators. Species can also use more than just the calls of conspecifics to detect threat, ‘eavesdropping’ on other species’ signalling to avoid predation. However, the evidence to date for both referential signalling and eavesdropping within primates is limited. We investigated two sympatric populations of wild lemur, the Coquerel’s sifaka Propithecus coquereli and the common brown lemur Eulemur fulvus, presenting them with playbacks of predator calls, conspecific alarm calls and heterospecific lemur alarm calls, and recorded their behavioural responses following the playbacks. Results suggest that the Coquerel’s sifaka may have functionally referential alarm calls with high specificity for aerial predators, but there was no evidence for any referential nature of the other call investigated. Brown lemurs appear to have a mixed alarm system, with one call being specific with respect to aerial predators. The other call investigated appeared to reference terrestrial predators. However, it was also used in other contexts, so does not meet the criteria for functional reference. Both species showed evidence for heterospecific alarm call recognition, with both the Coquerel’s sifaka and the brown lemurs responding appropriately to heterospecific aerial alarm calls.     

Variation in the Meaning of Alarm Calls in Verreaux’s and Coquerel’s Sifakas (<Emphasis Type="Italic">Propithecus verreauxi,P. coquereli</Emphasis>)

The comprehension and usage of primate alarm calls appear to be influenced by social learning. Thus, alarm calls provide flexible behavioral mechanisms that may allow animals to develop appropriate responses to locally present predators. To study this potential flexibility, we compared the usage and function of 3 alarm calls common to 2 closely related sifaka species (Propithecus verreauxi and P. coquereli), in each of 2 different populations with different sets of predators. Playback studies revealed that both species in both of their respective populations emitted roaring barks in response to raptors, and playbacks of this call elicited a specific anti-raptor response (look up and climb down). However, in Verreaux’s sifakas, tchi-faks elicited anti-terrestrial predator responses (look down, climb up) in the population with a higher potential predation threat by terrestrial predators, whereas tchi-faks in the other population were associated with nonspecific flight responses. In both populations of Coquerel’s sifakas, tchi-fak playbacks elicited anti-terrestrial predator responses. More strikingly, Verreaux’s sifakas exhibited anti-terrestrial predator responses after playbacks of growls in the population with a higher threat of predation by terrestrial predators, whereas Coquerel’s sifakas in the raptor-dominated habitat seemed to associate growls with a threat by raptors; the 2 other populations of each species associated a mild disturbance with growls. We interpret this differential comprehension and usage of alarm calls as the result of social learning processes that caused changes in signal content in response to changes in the set of predators to which these populations have been exposed since they last shared a common ancestor.     

Ontogeny of conspecific and heterospecific alarm call recognition in wild Verreaux's sifakas (Propithecus verreauxi verreauxi)

The production of vocalizations in nonhuman primates is predominantly innate, whereas learning influences the usage and comprehension of vocalizations. In this study, I examined the development of alarm call recognition in free-ranging infant Verreaux's sifakas. Specifically, I investigated their ability to recognize conspecific alarm calls as well as those of sympatric redfronted lemurs (Eulemur fulvus rufus) in Kirindy forest, western Madagascar. Both species have functionally referential alarm calls for aerial predators and give general alarm calls for both aerial and general predators and also other kinds of threats, such as intergroup encounters with conspecifics. I conducted playback experiments with members of two birth cohorts (nine and ten individuals) to determine the age at which infant Verreaux's sifakas discriminate between conspecific alarm calls, heterospecific alarm calls, and non-alarm vocalizations (parrot song). Most 3-4 months old infants fled toward adults after hearing any playback stimuli, whereas 4-5-month-old infants did so only after presentation of alarm calls. Moreover, all infants of these age classes showed a longer latency to flee after the parrot song indicating their emerging ability to discriminate between alarm calls and non-alarm stimuli. At an age of about 6 months, infants switched from fleeing toward adults to performing adult-like escape responses after presentation of conspecific and heterospecific alarm calls. Thus, the ability to discriminate between alarm from non-alarm stimuli precedes the appearance of adult-like responses. The transition to adult-like escape behavior was coincident with the physical independence of infants from their mothers.     

Interspecific Semantic Alarm Call Recognition in the Solitary Sahamalaza Sportive Lemur,Lepilemur sahamalazensis

As alarm calls indicate the presence of predators, the correct interpretation of alarm calls, including those of other species, is essential for predator avoidance. Conversely, communication calls of other species might indicate the perceived absence of a predator and hence allow a reduction in vigilance. This “eavesdropping” was demonstrated in birds and mammals, including lemur species. Interspecific communication between taxonomic groups has so far been reported in some reptiles and mammals, including three primate species. So far, neither semantic nor interspecific communication has been tested in a solitary and nocturnal lemur species. The aim of this study was to investigate if the nocturnal and solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis, is able to access semantic information of sympatric species. During the day, this species faces the risk of falling prey to aerial and terrestrial predators and therefore shows high levels of vigilance. We presented alarm calls of the crested coua, the Madagascar magpie-robin and aerial, terrestrial and agitation alarm calls of the blue-eyed black lemur to 19 individual Sahamalaza sportive lemurs resting in tree holes. Songs of both bird species’ and contact calls of the blue-eyed black lemur were used as a control. After alarm calls of crested coua, Madagascar magpie-robin and aerial alarm of the blue-eyed black lemur, the lemurs scanned up and their vigilance increased significantly. After presentation of terrestrial alarm and agitation calls of the blue-eyed black lemur, the animals did not show significant changes in scanning direction or in the duration of vigilance. Sportive lemur vigilance decreased after playbacks of songs of the bird species and contact calls of blue-eyed black lemurs. Our results indicate that the Sahamalaza sportive lemur is capable of using information on predator presence as well as predator type of different sympatric species, using their referential signals to detect predators early, and that the lemurs’ reactions are based on experience and learning.     

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

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

Semantic Differences in Sifaka (Propithecus verreauxi) Alarm Calls: A Reflection of Genetic or Cultural Variants?

In this study, we compared the usage of alarm calls and anti‐predator strategies between a captive and a wild lemur population. The wild lemur population was studied earlier in Western Madagascar ( Fichtel & Kappeler 2002 ). The captive population was studied in outdoor enclosures of the Duke University Primate Center. Alarm calls and anti‐predator behavior were elicited by conducting experiments with both vocal and visual dummies. We scored the subjects’ immediate behavioral responses, including alarm calls, from video recordings made during the experiments. In principle, both populations have a mixed alarm call system with functionally referential alarm calls for aerial predators and general alarm calls for terrestrial and aerial predators and for situations associated with high arousal, such as group encounters. Although wild and captive sifakas exhibit the same alarm call system and use the same alarm call types, we discovered striking differences in the usage and perception of some of the alarm calls. We argue that these differences indicate either an evolutionary drift in the meaning of these calls or reflect cultural variation. The latter possibility is consistent with our understanding of the ontogeny of call usage and comprehension.     

Avoiding predators at night: antipredator strategies in red-tailed sportive lemurs (Lepilemur ruficaudatus)

Although about one-third of all primate species are nocturnal, their antipredator behavior has rarely been studied directly. Crypsis and a solitary lifestyle have traditionally been considered to be the main adaptive antipredator strategies of nocturnal primates. However, a number of recent studies have revealed that nocturnal primates are not as cryptic and solitary as previously suggested. Thus, the antipredator strategies available for diurnal primates that rely on early detection and warning of approaching predators may also be available to nocturnal species. In order to shed additional light on the antipredator strategies of nocturnal primates, I studied pair-living red-tailed sportive lemurs (Lepilemur ruficaudatus) in Western Madagascar. In an experimental field study I exposed adult sportive lemurs that lived in pairs and had offspring to playbacks of vocalizations of their main aerial and terrestrial predators, as well as to their own mobbing calls (barks) given in response to disturbances at their tree holes. I documented the subjects' immediate behavioral responses, including alarm calls, during the first minute following a playback. The sportive lemurs did not give alarm calls in response to predator call playbacks or to playbacks with barks. Other behavioral responses, such as gaze and escape directions, corresponded to the hunting strategies of the two classes of predators, suggesting that the corresponding vocalizations were correctly categorized. In response to barks, they scanned the ground and fled. Because barks do not indicate any specific threats, they are presumably general alarm calls. Thus, sportive lemurs do not rely on early warning of acoustically simulated predators; rather, they show adaptive escape strategies and use general alarm calls that are primarily directed toward the predator but may also serve to warn kin and pair-partners.     

Situational Specificity in Alpine-marmot Alarm Communication

We studied the degree to which alpine marmot (Marmota marmota L.) alarm calls function as communication about specific external stimuli. Alpine marmots emit variable alarm calls when they encounter humans, dogs, and several species of aerial predators. The first part of the study involved observations and manipulations designed to document contextual variation in alarm calls. Alarm calls varied along several acoustic parameters, but only along one that we examined, the number of notes per call, was significantly correlated with the type of external stimulus. Marmots were more likely to emit single-note alarm calls as their first or only call in response to an aerial stimulus, and multiple-note alarm calls when first calling to a terrestrial stimulus. This relationship was not without exceptions; there was considerable variation in the number of notes they emitted to both aerial and terrestrial stimuli, and a single stimulus type — humans — elicited a wide range of acoustic responses. The second part of the study involved playing back three types of alarm calls to marmots and observing their responses. Marmots did not have overtly different responses to the three types of played-back alarm calls. Our results are consistent with the hypotheses that: 1. Alarm calls do not refer to specific external stimuli; 2. Alarm calls function to communicate the degree of risk a caller experiences; and 3. Alarm calls require additional contextual cues to be properly interpreted by conspecifics.     

Alarm calls elicit predator-specific physiological responses

Glucocorticoids regulate glucose concentrations and responses to unpredictable events, while also modulating cognition. Juvenile Belding''s ground squirrels (Urocitellus beldingi) learn to respond to whistle and trill alarm calls, warning of aerial and terrestrial predators, respectively, shortly after emerging from natal burrows at one month of age. Alarm calls can cause physiological reactions and arousal, and this arousal, coupled with watching adult responses, might help juveniles learn associations between calls and behavioural responses. I studied whether young show differential cortisol responses to alarm and non-alarm calls, using playbacks of U. beldingi whistles, trills, squeals (a conspecific control vocalization) and silent controls. Trills elicited very high cortisol responses, and, using an individual''s response to the silent control as baseline, only their response to a trill was significantly higher than baseline. This cortisol increase would provide glucose for extended vigilance and escape efforts, which is appropriate for evading terrestrial predators which hunt for long periods. Although whistles do not elicit a cortisol response, previous research has shown that they do result in bradycardia, which enhances attention and information processing. This is a novel demonstration of two physiological responses to two alarm calls, each appropriate to the threats represented by the calls.     

8. CORRESPONDENCE

This paper investigates, through experiments using surrogate predators, differences in intraspecific alarm calls between familiar and unfamiliar Bronze Mannikin Spermestes cucculatus groups. Four groups of mannikins were captured with mist nets from four areas in Durban (i.e. original groups) and randomly mixed (i.e. assorted groups). These groups were exposed to latex terrestrial snakes and mounted aerial raptors, and their alarm calls and predator response behaviours recorded. The Bronze Mannikins were able to discriminate between predators of different sizes, and increased their calling rate and decreased the end frequency of the alarm call in response to larger predators. This perhaps signalled increased threat, while simultaneously decreasing the conspicuousness of the flock. When the alarm call structure of the original and assorted groups in response to both raptors and snakes was compared, birds in original groups called more often, but paused longer between calls. Anti-predator behaviour differed in that assorted groups were less vigilant and aggressive toward the predators and panicked more frequently. In these groups, a failure to transfer the predation threat information might have caused the group to stop behaving cohesively and reliably. The manipulated experiments carried out in this study indicated that Bronze Mannikins were able to communicate predator size risk to conspecifics, but not as successfully to unfamiliar group members, showing that the investment, probability through altruistic payback, is greater in stable groups.     

Diets of Two Lemur Species in Different Microhabitats in Beza Mahafaly Special Reserve,Madagascar

Studies of primate diets usually focus on differences that distinguish species or populations. However, variation in diet can occur at a more local level of groups within a population, especially in a non-homogeneous habitat. I compared dietary variation in food composition and toughness across groups of 2 lemur species in Beza Mahafaly special reserve, Madagascar. Beza Mahafaly contains an 80-ha reserve (Parcel 1) that, while small, hosts a dense population of Lemur catta (ring-tailed lemurs) and Propithecus verreauxi verreauxi (sifakas). Microhabitats in the eastern vs. western sides of the parcel are structurally and floristically distinct. Sifakas in this parcel have small, discrete home ranges and are morphological folivores. For these reasons, I expected that the 6 groups studied would eat a different menu of food plants but with similar toughness values. Ring-tailed lemurs have comparatively large, overlapping home ranges, and I expected that the 5 study groups would eat similar foods. Despite living in different microhabitats across the parcel, sifakas exhibit high dietary uniformity both in dietary plant species composition and the toughness of the foods. Food selection in sifakas operates on two distinct levels. Sifaka groups share many key food species that appear independent of local abundances, but the ranking of the foods within each group appears related to availability. Ring-tailed lemur groups are more heterogeneous in the composition of their diets relative to sifakas, though the time spent feeding on individual foods reveals a marked preference for the fruits of Tamarindus indica by all groups. Food toughness is consistent across the parcel with the exception of the most western group. Ring-tailed lemurs are highly specific feeders, but indiscriminate nibblers. Sifakas are targeted, balanced feeders. There does not appear to be a consistent microhabitat effect operating across species. Differences within sifaka and ring-tailed lemur populations in food composition and toughness, however, correspond to an east-west microhabitat gradient. Measures of dietary flexibility must take into account not only the plant species consumed and the different parts eaten but also their associated food properties and proportion of time spent feeding on them.     

Interspecific audience effects on the alarm-calling behaviour of a kleptoparasitic bird

Audience effects are increasingly recognized as an important aspect of intraspecific communication. Yet despite the common occurrence of interspecific interactions and considerable evidence that individuals respond to the calls of heterospecifics, empirical evidence for interspecific audience effects on signalling behaviour is lacking. Here we present evidence of an interspecific audience effect on the alarm-calling behaviour of the kleptoparasitic fork-tailed drongo (Dicrurus adsimilis). When foraging solitarily, drongos regularly alarm at aerial predators, but rarely alarm at terrestrial predators. In contrast, when drongos are following terrestrially foraging pied babblers (Turdoides bicolor) for kleptoparasitic opportunities, they consistently give alarm calls to both aerial and terrestrial predators. This change occurs despite no difference in the amount of time that drongos spend foraging terrestrially. Babblers respond to drongo alarm calls by fleeing to cover, providing drongos with opportunities to steal babbler food items by occasionally giving false alarm calls. This provides an example of an interspecific audience effect on alarm-calling behaviour that may be explained by the benefits received from audience response.     

Responses of Redfronted Lemurs to Experimentally Modified Alarm Calls: Evidence for Urgency-Based Changes in Call Structure

Abstract The aim of this study was to investigate how information about the affective state is expressed in vocalizations. Alarm calls can serve as model systems with which to study this general question. Therefore, we examined the information content of terrestrial predator alarm calls of redfronted lemurs ( Eulemur fulvus rufus ), group-living Malagasy primates. Redfronted lemurs give specific alarm calls only towards raptors, whereas calls given in response to terrestrial predators (woofs) are also used in other situations characterized by high arousal. Woofs may therefore have the potential to express the perceived risk of a given threat. In order to examine whether different levels of arousal are expressed in call structure, we analysed woofs given during inter-group encounters or in response to playbacks of a barking dog, assuming that animals engaged in inter-group encounters experience higher arousal than during the playbacks of dog barks. A multivariate acoustic analysis revealed that calls given during group encounters were characterized by higher frequencies than calls given in response to playbacks of dog barks. In order to examine whether this change in call structure is salient to conspecifics, we conducted playback experiments with woofs, modified in either amplitude or frequencies. Playbacks of calls with increased frequency or amplitude elicited a longer orienting response, suggesting that different levels of arousal are expressed in call structure and provide meaningful information for listeners. In conclusion, the results of our study indicate that the information about the sender's affective state is expressed in the structure of vocalizations.     

The information that receivers extract from alarm calls in suricates.

Field observations and acoustic analyses have shown that suricate (Suricata suricatta) alarm calls vary in their acoustic structure depending on predator type. In this study, we tested whether receivers respond appropriately when hearing a call in the absence of a predator. Although the only way for suricates to escape from predators is to retreat to boltholes, responses to playbacks could be divided into distinct categories. The subjects responded differently to alarm calls given in response to aerial or terrestrial predators and to recruitment calls emitted in response to snakes and deposits on the ground. Suricates also showed rather distinct responses to low, medium and high urgency aerial calls. Differences in the responses were less obvious for different levels of urgency in the terrestrial and recruitment calls. Suricate receivers thus gain information about both the predator type and level of urgency from the acoustic structures of their calls.     

What is Communicated in the Antipredator Calls of Lemurs: Evidence from Playback Experiments with Ringtailed and Ruffed Lemurs

Two hypotheses of signal specificity in antipredator calls (“referential signalling” and “response urgency”) are discussed in light of prior research on ground squirrels and vervet monkeys. These hypotheses then are examined with data on responses of semi-captive ringtailed and ruffed lemurs to antipredator call playbacks. Although the responses of ringtailed lemurs support a referential-signalling interpretation of their antipredator calls, those of ruffed lemurs do not conform well to either hypothesis. Rather, ruffed lemur antipredator calls seem best viewed as “affective” signals that may only reflect underlying emotional/motivational states.     

Evidence of Invasive Felis silvestris Predation on Propithecus verreauxi at Beza Mahafaly Special Reserve, Madagascar

Increasing evidence supports the idea that endemic avian and mammalian predators have profoundly impacted primate populations in Madagascar (Goodman, S. M. Predation on lemurs. In S. M. Goodman, & J. P. Benstead (Eds.), The natural history of Madagascar (pp. 1221–1228). Chicago: University of Chicago Press, (2003).). The role in regulating lemur populations of the 3 introduced mammalian carnivorans —small Indian civets (Viverricula indica, Desmarest 1804), domestic dogs (Canis lupus familiaris, Linnaeus 1758), and invasive wildcats (Felis silvestris, Schreber 1775)— is less clear, but recent evidence suggests that the latter 2 are becoming important predators of diurnal lemurs. We report evidence for invasive wildcat predation on sifaka (Propithecus verreauxi verreauxi) in Parcel 1 at Beza Mahafaly Special Reserve, Madagascar, including skeletal remains of apparent Propithecus sifaka victims, observations of wildcat predatory behavior, and behavioral responses of the lemurs in the presence of wildcats.     

Demography, life history, and social structure in Propithecus diadema edwardsi from 1986-2000 in Ranomafana National Park, Madagascar

Prosimian lemurs differ fundamentally from anthropoid primates in many traits related to social structure. By exploring the demography of Milne-Edwards' sifakas (Propithecus diadema edwardsi), and comparing it to other well-studied primates, we explore the effect of demographic and life-history factors on social structure. Specifically, we compare lemur survivorship and fertility patterns to two published composite models: one created for New World and another created for Old World monkeys. Using longitudinal data collected on individual Propithecus diadema edwardsi from four study groups from 1986-2000 in Ranomafana National Park, Madagascar, we quantify 1) group composition, 2) birth seasonality, 3) interbirth interval, 4) life-table values, and 5) population growth estimates. The mortality, survivorship, and life-expectancy schedules indicate high infant and juvenile mortality. Fertility remains high until death. The intrinsic rate of increase and net reproductive rate indicate a shrinking population. We suggest that high mortality rather than low fertility causes the observed population decline. While sifaka survivorship closely resembles New World patterns, fertility resembles Old World patterns, i.e., like New World monkeys, few sifakas survive to reproductive age, and those that do, reproduce at a slow rate resembling the Old World pattern. This necessarily impacts social structure. An adult sifaka at the end of her lifespan will have one only daughter who survives to reproductive age, compared to 3.4 for New World or 2.7 for Old World monkeys. Demography limits the formation of large kin-based groups for sifakas, and survivorship and fertility patterns do not easily permit sifakas to form large same-sex family groups.     

Premating Behavior in the Subgenus Limia (Pisces: Poeciliidae): Sexual Selection and the Evolution of Courtship

A three-year field-study of Richardson's ground squirrels was conducted to assess whether alarm calling functions to warn close relatives (“kin selection” hypothesis) or manipulate conspecifics (a “selfish” hypothesis). S. richardsonii had distinct calls for terrestrial and aerial predators, and the responses of squirrels varied appropriately according to the context of calls, implying that calling conveyed correct information concerning the nature of the danger. Alarm calling elicited by naturally occurring encounters with potential predators during 454 h of observation, and by a thrown frisbee in 70 experimental trials, was not equally probable for all age/sex classes. Squirrels were most likely to call when they had offspring or siblings nearby, which is supportive of the hypothesis that alarm calling is maintained by kin selection. Adult males, residing in the vicinity of either their probable progeny or their nonlittermate half-siblings, were the most likely age/sex class to call during the lactation period when young were below ground and were most vulnerable. I conclude that alarm calling by Richardson's ground squirrels is nepotistic rather than manipulative.     

Alarm Calls of Marmosets (Callithrix geoffroyi) to Snakes and Perched Raptors

Communication about the presence of predators is an important benefit of group living. Critical information about the nature of danger can be conveyed through referential alarm calls. Raptors pose a significant predatory threat to callitrichid species. Unlike a raptor in flight, a perched raptor cannot attack suddenly at great speed, and it can be monitored from a safe distance. In this sense a perched bird may pose a threat more similar to that of a terrestrial predator such as a snake. Here we compare predatory contexts by addressing these two questions: 1) Do marmosets produce acoustically distinct alarm calls to snake models and perched raptor models? 2) Do the visual responses of the marmosets to the playbacks of perched raptor–elicited calls differ from those given to the playbacks of calls given in response to snakes? We recorded alarm calls from two groups of outdoor-housed Geoffroy’s marmosets (Callithrix geoffroyi) in response to predator models. Later, we played back stimuli created from these recordings to the marmosets and scored their gaze direction. Results show that calls given to models of perched raptors are acoustically distinct from those given to models of snakes. Further, the relative number of upward to downward looks while listening to the playbacks of perched raptor–elicited calls was significantly greater than it was for snake-elicited calls. Reactions to airborne raptors are known to elicit freezing or rapid flight, neither of which occurred in response to our playbacks. Our data suggest a greater complexity in the alarm call repertoire of marmosets than previously demonstrated.     

Y chromosome evidence of earliest modern human settlement in East Asia and multiple origins of Tibetan and Japanese populations

Background

A central question in evolutionary biology is how cryptic species maintain species cohesiveness in an area of sympatry. The coexistence of sympatrically living cryptic species requires the evolution of species-specific signalling and recognition systems. In nocturnal, dispersed living species, specific vocalisations have been suggested to act as an ideal premating isolation mechanism. We studied the structure and perception of male advertisement calls of three nocturnal, dispersed living mouse lemur species, the grey mouse lemur (Microcebus murinus), the golden brown mouse lemur (M. ravelobensis) and the Goodman's mouse lemur (M. lehilahytsara). The first two species occur sympatrically, the latter lives allopatrically to them.

Results

A multi-parameter sound analysis revealed prominent differences in the frequency contour and in the duration of advertisement calls. To test whether mouse lemurs respond specifically to calls of the different species, we conducted a playback experiment with M. murinus from the field using advertisement calls and alarm whistle calls of all three species. Individuals responded significantly stronger to conspecific than to heterospecific advertisement calls but there were no differences in response behaviour towards statistically similar whistle calls of the three species. Furthermore, sympatric calls evoked weaker interest than allopatric advertisement calls.

Conclusion

Our results provide the first evidence for a specific relevance of social calls for speciation in cryptic primates. They furthermore support that specific differences in signalling and recognition systems represent an efficient premating isolation mechanism contributing to species cohesiveness in sympatrically living species.