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.     

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.     

Interspecific Responses of Ringtailed Lemurs to Playback of Antipredator Alarm Calls Given by Verreaux's Sifakas

The ringtailed lemur, Lemur catta, and Verreaux's sifaka, Propithecus verreauxi verreauxi, are diurnal prosimians living sympatrically in Madagascar. Species-specific alarm calls emitted by each of these two species in response to aerial and terrestrial predators differ acoustically. Behavioural responses of ringtailed lemurs evoked by playbacks of conspecific alarm calls differ when the vocalizations were produced in response to aerial predators as opposed to terrestrial predators. We conducted playback experiments on two populations of ringtailed lemurs, using two types of sifaka alarm calls. One population consisted of free-ranging groups which lived sympatrically with sifakas, the other was a colony group which had no contact with sifakas. The results illustrate that the former group of lemurs can perceive what type of predators the sifaka calls refer to, whereas the latter group was not able to recognize the difference in the calls.     

Age Differences in the Responses to Adult and Juvenile Alarm Calls by Bonnet Macaques (Macaca radiata)

This study examined the differential responses to alarm calls from juvenile and adult wild bonnet macaques ( Macaca radiata ) in two parks in southern India. Field studies of several mammalian species have reported that the alarm vocalizations of immature individuals are often treated by perceivers as less provocative than those of adults. This study documents such differences in response using field-recorded playbacks of juvenile and adult alarm vocalizations. To validate the use of playback vocalizations as proxies of natural calls, we compared the responses of bonnet macaques to playbacks of alarm vocalizations with responses engendered by natural alarm vocalizations. We found that the frequency of flight, latency to flee, and the frequency of scanning to vocalization playbacks and natural vocalizations were comparable, thus supporting the use of playbacks to compare the effects of adult and juvenile calls. Our results showed that adult alarm calls were more provocative than juvenile alarm calls, inducing greater frequencies of flight with faster reaction times. Conversely, juvenile alarm calls were more likely to engender scanning by adults, a result interpreted as reflecting the lack of reliability of juvenile calls. Finally, we found age differences in flight behavior to juvenile alarm calls and to playbacks of motorcycle engine sounds, with juveniles and subadults more likely to flee than adults after hearing such sounds. These findings might reflect an increased vulnerability to predators or a lack of experience in young bonnet macaques.     

Dual Function of Chip Calls Depending on Changing Call Rate Related to Risk Level in Territorial Pairs of White‐Eared Ground‐Sparrows

Different mechanisms have been proposed for encoding information into vocalizations: variation of frequency or temporal characteristics, variation in the rate of vocalization production, and use of different vocalization types. We analyze the effect of rate variation on the dual function of chip calls (contact and alarm) produced by White‐eared Ground‐sparrows (Melozone leucotis). We conducted an acoustic playback experiment where we played back 1 min of four chip call rates (12, 36, 60, 84 calls/min). We measured the response of territorial pairs using behavioral responses, and fine structural features of calls produced in response to those playbacks. White‐eared Ground‐sparrows showed more intense behavioral responses to higher than lower call rate playbacks. Both individuals of the pair approached the source of the playback stimulus faster, produced the first vocalization faster, produced more vocalizations, and spent more time close to the stimulus in higher call rate than in lower call rate playbacks. Frequency and duration characteristics of calls (chip and tseet) were similar in response to all call rate playbacks. Our playback experiment elicited different intensity of behavioral responses, suggesting that risk‐based information is encoded in call rate. Our results suggest that variation in the rate of chip call production serves a dual function in this species; calls are used at lower rates for pair contact and at higher rates for alarm/mobbing signals.     

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.     

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.     

Acoustic Features of Female Chacma Baboon Barks

We studied variation in the loud barks of free-ranging female chacma baboons ( Papio cynocephalus ursinus ) with respect to context, predator type, and individuality over an 18-month period in the Moremi Game Reserve, Botswana. To examine acoustic differences in relation to these variables, we extracted a suite of acoustic parameters from digitized calls and applied discriminant function analyses. The barks constitute a graded continuum, ranging from a tonal, harmonically rich call into a call with a more noisy, harsh structure. Tonal barks are typically given when the signaler is at risk of losing contact with the group or when a mother and infant have become separated (contact barks). The harsher variants are given in response to large predators (alarm barks). However, there are also intermediate forms between the two subtypes which may occur in both situations. This finding is not due to an overlap of individuals' distinct distributions but can be replicated within individuals. Within the alarm bark category, there are significant differences between calls given in response to mammalian carnivores and those given in response to crocodiles. Again, there are intermediate variants. Both alarm call types are equally different from contact barks, indicating that the calls vary along different dimensions. Finally, there are consistent, significant differences among different individuals' calls. However, individual identity in one call type cannot directly be inferred from knowledge of the individuals' call characteristics in the other. In sum, the barks of female baboons potentially provide rich information to the recipients of these signals. The extent to which baboons discriminate between alarm and contact barks, and classify calls according to context and/or acoustic similarity will be described in a subsequent paper.     

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.     

Behavioral responses to species-specific warning calls in infant squirrel monkeys reared in social isolation

Six infant squirrel monkeys were reared in social isolation. They responded differentially to playbacks of two species-specific alarm calls. The reaction to the alarm peep, the warning call to bird predators, was a prompt flight to the mother surrogate and essentially resembled the respective behavior of mother-reared infants. The responses to yapping, the alarm call to terrestrial predators, were less clear-cut and habituated soon. However, when yapping was played back in connection with the presentation of a reference object, both subjects tested in this way clearly avoided the object and preferred contact with the mother surrogate while they thoroughly explored an object presented with a control tone. From this it can be concluded that the perception of both alarm calls is innate. In addition, the method of behavior-contingent playback of vocalizations simulates the learning process by which the visual perception of terrestrial predators of the habitat is acquired.     

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.     

Variation in and Meaning of Alarm Calls in a Social Desert Rodent Rhombomys opimus

The great gerbil (Rhombomys opimus), a social rodent that lives in family groups, emits three different alarm vocalizations in the presence of predators: a rhythmic call; a faster more intense call; and a single whistle. We tested the hypothesis that the alarm calls communicate risk of predation. We quantified the relationship between predator distance and type of alarm call via human approaches to gerbils. We also tested responses of focal adults in family groups to playback broadcasts of the different calls and controls of bird song and tape noise. Results showed that alarm calls were related to distance from a predator. Gerbils gave the rhythmic call when the predator was farthest away, the more intense call as the predator moved closer; and a short whistle when startled by a close approach of the predator. Gerbils stopped feeding and stood vigilant in a frozen alert posture in response to playbacks of all three alarm calls. They decreased non‐vigilant behavior to the alarm vocalizations more than to the controls and decreased non‐vigilant behavior significantly more in response to the intense alarm and whistle compared with the rhythmic alarm. We conclude that one function of gerbil alarm calls is to communicate response urgency to family members. The rhythmic alarm communicates danger at a distance, whereas the intense alarm and whistle signal the close approach of a predator.     

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.     

Asymmetrical interspecific communication of predatory threat in mixed‐species colonies of lesser kestrels (Falco naumanni) and jackdaws (Corvus monedula)

Sympatric species derive benefits by attending to information conveyed by heterospecifics. Our previous finding of reduced vigilance among jackdaws and lesser kestrels residing in mixed‐species colonies suggested a reliance on interspecific communication of information regarding predatory threats. To test for interspecific communication of threat, we first determined whether jackdaw and lesser kestrel call structure varied with perceived threat. In this call production phase of our study, free‐living birds in mixed‐species colonies were presented with models representing a potential nest predator (European magpie) or with non‐threatening stimuli (wood pigeon or wooden dowel) in proximity to nests. We recorded and subsequently analysed those calls to determine if any temporal or frequency‐related call parameters differed by model type. In a second, perceptual phase of our study, we tested whether receivers perceive threat‐related variation in both conspecific and heterospecific call structure by playing back call exemplars recorded in response to the predator model or to innocuous control stimuli, to determine whether free‐living jackdaws or lesser kestrels respond differentially to playbacks of the different call types. We detected differences in vocalizations of both jackdaws and lesser kestrels relative to the model type presented, with more broadband (lesser kestrel) or noisy calls (jackdaws) in response to magpie versus innocuous model types. We also detected differential behavioural responses to call playbacks, with both jackdaws and lesser kestrels increasing vigilance and alarm calling in response to magpie‐elicited jackdaw calls, but not to other call types. Taken together, our results suggest that jackdaw, but not lesser kestrel vocalizations, communicate enhanced threat associated with European magpies as possible nest predators. This interspecific alarm communication benefits both jackdaws and lesser kestrels, and, at least in part, explains asymmetric responses of jackdaws and lesser kestrels to magpies attending mixed‐species colonies in nature.     

Development of infant baboons' responses to graded bark variants.

We studied the development of infant baboons' (Papio cynocephalus ursinus) responses to conspecific 'barks' in a free-ranging population in the Okavango Delta, Botswana. These barks grade from tonal, harmonically rich calls into calls with a more noisy, harsh structure. Typically, tonal variants are given when the signaller is at risk of losing contact with the group or a particular individual ('contact barks'), whereas harsh variants are given in response to predators ('alarm barks'). We conducted focal observations and playback experiments in which we presented variants of barks recorded from resident adult females. By six months of age, infants reliably discriminated between typical alarm and contact barks and they responded more strongly to intermediate alarm calls than to typical contact barks. Infants of six months and older also recognized their mothers by voice. The ability to discriminate between different call variants developed with increasing age. At two and a half months of age, infants failed to respond at all, whereas at four months they responded irrespective of the call type that was presented. At six months, infants showed adult-like responses by responding strongly to alarm barks but ignoring contact barks. We concluded that infants gradually learn to attach the appropriate meaning to alarm and contact barks.     

Acoustic structure of alarm calls in Indian sambar (<Emphasis Type="Italic">Rusa unicolor</Emphasis>) and Indian muntjac (<Emphasis Type="Italic">Muntiacus vaginalis</Emphasis>) in South Vietnam

The alarm call acoustic structure and nonlinear vocal phenomena of the Indian sambar (Rusa unicolor) and northern Indian muntjac (Muntiacus vaginalis) have been analyzed in detail as well as their vocal behavior in response to mobbing humans under natural conditions of southern Vietnam. The alarm calls of sambars, tonal barks separated by large intervals, were produced by animals standing on the place and gazing at a potentially dangerous object. Muntjacs flee off in danger and produced a series of dull barks interrupted with short intervals from a distance. The alarm call frequencies were characterized for sambars and muntjacs. The results of our study have been compared with the published data on alarm calls of other Cervidae species.     

Anti‐Predator Behaviour in a Nocturnal Primate,the Grey Mouse Lemur (Microcebus murinus)

Although one‐third of all primates are nocturnal, their anti‐predator behaviour has rarely been studied. Because of their small body size, in combination with their solitary and nocturnal life style, it has been suggested that they mainly rely on crypsis to evade predators. However, recent studies revealed that nocturnal primates are not generally cryptic and that they exhibit predator‐specific escape strategies as well as alarm calls. In order to add to this new body of research, we studied anti‐predator strategies of nocturnal grey mouse lemurs experimentally. In order to elicit anti‐predator behaviour and alarm calls, we conducted experiments with a carnivore‐, snake‐ and raptor model. We also conducted playback experiments with mouse lemur alarm calls to characterize their function. In response to predator models, they exhibited a combination of anti‐predator strategies: in response to carnivore and snake models, mouse lemurs monitored the predator, probably to assess the potential risk that emanates from the predator. In response to raptor models they behaved cryptically and exhibited freezing behaviour. All mouse lemurs, except one individual, did not alarm call in response to predator models. In addition, during playback experiments with alarm calls, recorded during real predator encounters, mouse lemurs did not emit alarm calls nor did they show any escape behaviour. Thus, as in other nocturnal primates/mammals, mouse lemurs do not seem to rely on routinely warning of conspecifics against nearby predators.     

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.