Recognition of partially concealed leopards by wild bonnet macaques (Macaca radiata). The role of the spotted coat

Wild bonnet macaques (Macaca radiata) have been shown to recognize models of leopards (Panthera pardus), based on their configuration and spotted yellow coat. This study examined whether bonnet macaques could recognize the spotted and dark melanic morph when partially concealed by vegetation. Seven troops were studied at two sites in southern India, the Mudumalai Wildlife Sanctuary and the Kalakad-Mundanthurai Tiger Reserve. The forequarters and hindquarters of the two leopard morphs were presented from behind thick vegetation to individuals at feeding stations 25 m away. Flight reaction times and frequency of flight were obtained from video for only those individuals who oriented towards the models prior to hearing alarm calls. Bonnet macaques exhibited faster reaction times and greater frequency of flight after looking at the spotted morph's forequarter than after looking at either its spotted hindquarter or the dark morph's forequarter. The hindquarter of the dark morph was ignored completely. Artificial neural network modeling examined the perceptual aspects of leopard face recognition and the role of spots as camouflage. When spots were integrated into the pattern recognition process via network training, these spots contributed to leopard face recognition. When networks were not trained with spots, spots did not act as camouflage by disrupting facial features.     

Snake Species Discrimination by Wild Bonnet Macaques (Macaca radiata)

Wild bonnet macaques (Macaca radiata) were studied in southern India to assess their ability to discriminate non‐venomous, venomous and predatory snakes. Realistic snake models were presented to eight troops of bonnet macaques at feeding stations and their behavior was video‐recorded 3 min before and 3 min after snake exposure. Snakes presented were: (1) venomous Indian cobra (Naja naja) displaying an open hood with ‘eyespots’; (2) venomous common Indian krait (Bungarus caeruleus); (3) non‐venomous green keelback (Macropisthodan plumbicolor); (4) non‐venomous rat snake (Ptyas mucosus); and (5) Indian python (Python molurus) which preys on macaques. Latencies to detect and react to the snakes were evaluated to determine initial responsiveness. Longer‐term assessment was measured as the percentage of time individuals looked at the snakes and monitored the activity of nearby individuals before and after snake detection. All snake models engendered caution and maintenance of a safe distance. Alarm calling occurred only during python presentations. The cobra engendered a startle response or running in the largest percentage of individuals after its detection, whereas the rat snake and python elicited bipedal standing or ambulating to monitor the snakes. We also examined the influence of age on snake recognition. Juveniles and subadults looked at the cobra, krait, and python for a larger percentage of time than adults did; albeit, adults looked at the python substantially longer than at the other snakes. Age differences in behavior suggest that, with the exception of the python, repeated experience with snakes in the wild moderates excitability, consistent with the likely threat of envenomation.     

The Predator Deterrence Function of Primate Alarm Calls

It is generally assumed that alarm calls function in intraspecific communication, for example to warn close relatives about the presence of a predator. However, an alternative hypothesis suggests that, in some cases, signallers may also gain fitness benefits in directly communicating to the predator, for example by advertising perception and unprofitability to predators that depend on unprepared prey. In this study, we show that six monkey species in Taï forest, Ivory Coast, produce significantly more alarm calls to leopards than to chimpanzees, although both are notorious monkey predators. The conspicuously high vocalization rates to leopards had adaptive consequences for the monkeys. By following a radio-collared leopard, we found that after detection and high alarm call rates the leopard gave up its hiding location and left the group significantly faster than would be expected by chance. We discuss these data with respect to the various functional hypothesis of alarm call behaviour and conclude that the high alarm call rates to leopards are part of an anti-predator strategy in primates that may have evolved to deter predators that depend on surprise.     

Hornbills can distinguish between primate alarm calls

Some mammals distinguish between and respond appropriately to the alarm calls of other mammal and bird species. However, the ability of birds to distinguish between mammal alarm calls has not been investigated. Diana monkeys (Cercopithecus diana) produce different alarm calls to two predators: crowned eagles (Stephanoaetus coronatus) and leopards (Panthera pardus). Yellow-casqued hornbills (Ceratogymna elata) are vulnerable to predation by crowned eagles but are not preyed on by leopards and might therefore be expected to respond to the Diana monkey eagle alarm call but not to the leopard alarm call. We compared responses of hornbills to playback of eagle shrieks, leopard growls, Diana monkey eagle alarm calls and Diana monkey leopard alarm calls and found that they distinguished appropriately between the two predator vocalizations as well as between the two Diana monkey alarm calls. We discuss possible mechanisms leading to these responses.     

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.     

Interspecies semantic communication in two forest primates

West African Diana monkeys (Cercopithecus diana) and Campbell's monkeys (Cercopithecus campbelli) frequently form mixed-species associations. Males of both species produce acoustically distinct alarm calls to crowned eagles (Stephanoaetus coronalus) and leopards (Panthera pardus), two of their main predators. Field playback experiments were conducted to investigate whether Diana monkeys respond to Campbell's alarm calls and whether they understand the calls' semantic content. Diana monkeys responded to playback of Campbell's leopard or eagle alarm calls as though the original predator were present. In a second experiment, Diana monkeys were primed with either Campbell's eagle or leopard alarm calls and then subsequently probed with the vocalizations of a crowned eagle or a leopard. Results showed that monkeys used the semantic information conveyed by the Campbell's alarm calls to predict the presence of a predator. The data are consistent with the hypothesis that non-human primates are able to use acoustic signals of diverse origin as labels for underlying mental representations.     

Hunting behaviour in West African forest leopards

The leopard (Panthera pardus) is a major predator of mammals within the rainforest ecosystem of West Africa. Most of the available information on leopard hunting behaviour comes from studies conducted in open savannah habitats, while little is known about forest leopards. Our radio‐tracking data and scat analysis show that forest leopards differ in various ways from the savannah populations. Forest leopards are diurnal and crepuscular hunters who follow the activity pattern of their prey species. They exhibit seasonal differences in activity patterns, and they develop highly individualized prey preferences. These findings challenge the widespread notion of leopards as opportunistic nocturnal predators.     

Low leopard populations in protected areas of Maputaland: a consequence of poaching,habitat condition,abundance of prey,and a top predator

Identifying the primary causes affecting population densities and distribution of flagship species are necessary in developing sustainable management strategies for large carnivore conservation. We modeled drivers of spatial density of the common leopard (Panthera pardus) using a spatially explicit capture–recapture—Bayesian approach to understand their population dynamics in the Maputaland Conservation Unit, South Africa. We camera‐trapped leopards in four protected areas (PAs) of varying sizes and disturbance levels covering 198 camera stations. Ours is the first study to explore the effects of poaching level, abundance of prey species (small, medium, and large), competitors (lion Panthera leo and spotted hyenas Crocuta crocuta), and habitat on the spatial distribution of common leopard density. Twenty‐six male and 41 female leopards were individually identified and estimated leopard density ranged from 1.6 ± 0.62/100 km² (smallest PA—Ndumo) to 8.4 ± 1.03/100 km² (largest PA—western shores). Although dry forest thickets and plantation habitats largely represented the western shores, the plantation areas had extremely low leopard density compared to native forest. We found that leopard density increased in areas when low poaching levels/no poaching was recorded in dry forest thickets and with high abundance of medium‐sized prey, but decreased with increasing abundance of lion. Because local leopard populations are vulnerable to extinction, particularly in smaller PAs, the long‐term sustainability of leopard populations depend on developing appropriate management strategies that consider a combination of multiple factors to maintain their optimal habitats.     

Causal knowledge of predators' behaviour in wild Diana monkeys

Wild Diana monkeys, Cercopithecus diana, of Ta? forest, Ivory Coast, are preyed upon by leopards, Panthera pardus, and chimpanzees, Pan troglodytes. These two predators differ in their main hunting tactic and Diana monkeys attempt to avoid predation with two distinct antipredator strategies: conspicuous alarm-calling behaviour to leopards and silent, cryptic behaviour to chimpanzees. However, the Diana monkeys' choice of the appropriate antipredator strategy is complicated by the fact that chimpanzees themselves also fall prey to leopards. Chimpanzees give loud and conspicuous alarm screams when they detect a leopard. When these chimpanzees' leopard alarm calls were played back to different groups of Diana monkeys, in about half of the cases recipients switched from a chimp-specific cryptic response to a leopard-specific conspicuous response, suggesting that some individuals assumed the presence of a leopard. Groups whose home range was in the core area of the resident chimpanzee community were more likely to respond this way than more peripheral groups, indicating between-group differences in semantic knowledge. In a follow-up experiment, the monkeys' understanding of the chimpanzee alarm calls was further assessed with a prime-probe technique. Monkeys were primed with chimpanzee alarm calls and then, 5 min later, tested with leopard growls to see whether they were able to anticipate the presence of a leopard. Results were consistent with the hypothesis that monkeys responding cryptically to chimpanzee alarm calls did so because they were not able to understand the calls' meaning. Data are discussed with respect to three possible cognitive mechanisms, associative learning, specialized learning programmes, and causal reasoning, that could have led to causal knowledge in some individuals but not others. Copyright 2000 The Association for the Study of Animal Behaviour.     

Referential labelling in Diana monkeys

Animal semantic communication has received considerable theoretical and empirical attention because of its relevance to human language. Advances have been made by studies of alarm-call behaviour in nonhumans. In monkeys, for example, there is evidence that recipients have a fairly sophisticated understanding of a call's meaning; that is, the predator type usually associated with a certain alarm call. Little is known, however, about the mental mechanisms that drive call production in nonhuman primates. In some nonprimate species, it has been found that signallers do not respond to a predator's physical features but instead seem to respond to its relative threat or direction of attack. In these species, therefore, alarm calls do not denote different predator categories but simply reflect different types or levels of danger. Because different predator categories typically impose different types and degrees of threat it is entirely possible that nonhuman primates also respond to threat rather than a predator's category. This study examined how wild Diana monkeys, Cercopithecus diana, of the Ta? forest, Ivory Coast, label predation events. By altering playback stimuli and the position of a concealed speaker, I investigated whether Diana monkeys respond with acoustically different alarm calls depending on a predator's (1) distance (close versus far), (2) elevation (above versus below), or (3) category (eagle versus leopard). Analysis of male and female alarm-call behaviour showed that Diana monkeys consistently responded to predator category regardless of immediate threat or direction of attack. Data further suggested that, in addition to predator category, monkeys' alarm calls might also convey information about the predator's distance. Copyright 2000 The Association for the Study of Animal Behaviour.     

Early environment shapes the development of gaze aversion by wild bonnet macaques (<Emphasis Type="Italic">Macaca radiata</Emphasis>)

Among many species of primates, staring is perceived as a sign of aggression and averting the gaze usually serves to reduce such conflict. The current study conducted in southern India documented developmental differences among wild bonnet macaques (Macaca radiata) in their latency to gaze avert after establishing eye contact with other individuals. Feeding stations were used to gather macaques within a small area to facilitate the video recording of group dynamics and eye contact between subordinate and dominant individuals. Individuals were grouped into three age classes: juveniles, subadult males, and adult males. Comparisons were also made between urban and forest dwelling troops. In the forest, juveniles established eye contact with older males for significantly longer periods of time than did adults. A linear trend was observed in which the latency to gaze avert after establishing eye contact decreased with age. This trend was not evident in the urban troops, for which the latency to gaze avert did not change significantly with age. Urban juveniles were also more likely to be chased when they established eye contact with adults compared with their forest counterparts. These differences could be the result of increased predatory risk in the forest setting — the necessity for heightened predator vigilance in forests may reduce the frequency with which juveniles are monitored and chased or attacked as a result of their eye contact. Conversely, the rarity of predators in the city may engender more intense aggressive behavior between monkeys, accelerating the rate of learning to signal appeasement to dominant males.     

No evidence of eavesdropping on heterospecific alarm calls by captive zebra finches recently descended from wild birds

Alarm calls are vocalisations animals give in response to predators which mainly function to alert conspecifics of danger. Studies show that numerous species eavesdrop on heterospecific calls to gain information about predator presence. Responding to heterospecific calls may be a learned or innate response, determined by whether the response occurs with or without prior exposure to the call. In this study, we investigated the presence of eavesdropping behaviour in zebra finches Taeniopygia guttata. This species is not known to possess a distinct alarm call to warn adult conspecifics of a threat, and could be relying on alarm calls of nearby heterospecifics for predator information. We used a playback experiment to expose captive zebra finches to three heterospecific sounds: an unfamiliar alarm call (from the chestnut‐rumped thornbill Acanthiza uropygialis), a familiar alarm call, and a familiar control (both from the noisy miner Manorina melanocephala). These calls were chosen to test if the birds had learnt to distinguish between the function of the two familiar calls, and if the acoustic properties of the unfamiliar alarm indicated presence of a threat to the finches. Our results showed that in response to the thornbill alarm, the birds reduced the rate of production of short calls. However, this decrease was also seen when considering both short and distance calls in response to the control sound. An increase in latency to call was also seen after the control stimulus when compared to the miner alarm. The time spent scanning increased in response to all three stimuli, but this did not differ between stimuli. There were no significant differences when considering the stimulus by time interaction for any of the three vigilance measures. Overall, no strong evidence was found to indicate that the captive zebra finches were responding to the heterospecific alarm stimuli with anti‐predator behaviour.     

Predation increases acoustic complexity in primate alarm calls

According to most accounts, alarm calling in non-human primates is a biologically hardwired behaviour with signallers having little control over the acoustic structure of their calls. In this study, we compared the alarm calling behaviour of two adjacent populations of Diana monkeys at Taï forest (Ivory Coast) and Tiwai Island (Sierra Leone), which differ significantly in predation pressure. At Taï, monkeys regularly interact with two major predators, crowned eagles and leopards, while at Tiwai, monkeys are only hunted by crowned eagles. We monitored the alarm call responses of adult male Diana monkeys to acoustic predator models. We found no site-specific differences in the types of calls given to eagles, leopards and general disturbances, but there were consistent differences in how callers assembled calls into sequences. At Tiwai, males responded to leopards and general disturbances in the same way, while at Taï, males discriminated by giving call sequences that differed in the number of component calls. Responses to eagles were identical at both sites. We concluded that Diana monkeys are predisposed to use their repertoire in context-specific ways, but that ontogenetic experience determines how individual calls are assembled into meaningful sequences.     

Ravens adjust their antipredatory responses to con‐ and hetero‐specific alarms to the perceived threat

Heterospecific alarm calls are typically found in situations where multiple species have a common predator. In birds, they are particularly common in mixed mixed‐species flocks. In species with highly developed social and cognitive abilities like corvids, there is the potential for differential responses to heterospecific vs. conspecific calls according to the riskiness of the habitat. We tested the responses of free‐ranging ravens (Corvus corax) to conspecific alarm calls and compared them to heterospecific alarm calls of jackdaws (Corvus monedula). We observed the proportion of ravens leaving the feeding site after the con‐ or hetero‐specific playback was presented in a situation of low threat (wild boar—Sus scrofa enclosure) and high threat of predation (wolf—Canis lupus enclosure). We show that ravens responded to conspecific calls more intensively at the wolves than at the wild boar, but the response to conspecific calls was in both enclosures stronger than to the control (great tit—Parus major song). The response to the heterospecific alarm was also stronger in the wolves’ enclosure, but it did not differ from control in the wild boar enclosure. These findings suggest that ravens are aware of the meaning of the jackdaw alarm calls, but they respond to it only in a situation of high predatory threat (wolves are present). In the wild boar enclosure, the ravens probably consider jackdaws warning against some other predator, very probably harmless to ravens. This interpretation requires further testing, as both enclosures differ also in respect to other parameters like food quality and shelter availability.     

The versatility of graded acoustic measures in classification of predation threats by the tufted titmouse Baeolophus bicolor: exploring a mixed framework for threat communication

Many mammal and bird species respond to predator encounters with alarm vocalizations that generate risk‐appropriate responses in listeners. Two conceptual frameworks are typically applied to the information encoded in alarm calls and to associated anti‐predator behaviors. ‘Functionally referential’ alarm systems encode nominal classes or categories of risk in distinct call types that refer to distinct predation‐risk situations. ‘Risk‐based’ alarms encode graded or ranked threat‐levels by varying the production patterns of the same call types as the urgency of predation threat changes. Recent work suggests that viewing alarm‐response interactions as either referential or risk‐based may oversimplify how animals use information in decision‐making. Specifically, we explore whether graded alarm cues may be useful in classifying risks, supporting a referential decision‐making framework. We presented predator (hawk, owl, cat, snake) and control treatments to captive adult tufted titmice Baeolophus bicolor and recorded their vocalizations, which included ‘chick‐a‐dee’ mobbing calls (composed of chick and D notes), ‘seet’ notes, two types of contact notes (‘chip’, ‘chink’), and song. No single call type was uniquely associated with any treatment and the majority of acoustic measures varied significantly among treatments (46 of 60). The strongest models (ANOVA and classification tree analysis) grouped hawk with cat and owl, and control with snake, and were based on the number or proportion of a) chick and D notes per chick‐a‐dee call, b) chip versus chink notes produced following treatment exposure, and c) the frequency metrics of other note types. We conclude that (1) the predation‐threat information available in complex titmouse alarm calls was largely encoded in graded acoustic measures that were (2) numerous and variable across treatments and (3) could be used singly or in combinations for either ranking or classification of threats. We call attention to the potential use of mixed threat identification strategies, where risk‐based signal information may be used in referential decision‐making contexts.     

Male blue monkeys alarm call in response to danger experienced by others

Male blue monkeys (Cercopithecus mitis stuhlmanni) of Budongo Forest, Uganda, produce two acoustically distinct alarm calls: hacks to crowned eagles (Stephanoaetus coronatus) and pyows to leopards (Panthera pardus) and a range of other disturbances. In playback experiments, males responded to leopard growls exclusively with a series of pyows and to eagle shrieks predominantly with hacks. Responses to playbacks of these alarm call series matched the responses to the corresponding predators, suggesting that the calls conveyed something about the nature of the threat. When responding to a series of hacks, indicating an eagle, males responded predominately with hacks, but produced significantly more calls if their group members were close to the playback stimulus than far away, regardless of their own position. When responding to a series of pyows, indicating a range of disturbances, males responded with pyows, but call rates were independent of the distance of other group members. The results suggest that males took into account the degree of danger experienced by other group members.     

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.     

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.     

Outcast males and social structure among bonnet macaques (Macaca radiata)

Outcast males are a regular feature of rhesus (Macaca mulatta) and Japanese (M. fuscata) macaque societies but are rare among bonnet macaques (M. radiata). Apparently bonnets have other solutions than ostracism for their social problems. For example, in many troops the male-female ratio ranges from 0.7?1.0+; and, as the young adult males grow to full social and physical maturity, they remain in the troop and participate actively in social relationships. A few troops of bonnet macaques, however, have a network of social relationships which prevents the young males from being integrated into the social system; in some of these cases, male isolation occurs. A comparison of the social relations between males in bonnet macaque societies of both types suggests that societies with strong male-male bonds accommodate their growing males better than those with highly individual males.