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How Infant Vervet Monkeys Learn To Recognize Starling Alarm Calls: the Role of Experience

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Abstract

Natural observations and field playback experiments were conducted on five groups of free-ranging vervet monkeys to determine when infants recognize the alarm calls of starlings as general alerting signals. Results show that infants do not recognize starling alarm calls at birth. Recognition of starling calls emerges gradually and age at recognition is affected by differences in auditory environment. Infants who have heard starling alarm calls at high rates respond at an earlier age than infants who hear calls at low rates. More importantly, in those groups where infants respond at an earlier age, starlings give alarm calls to vervet predators more often than to non-vervet predators. Thus in the former groups, when adults respond to starling alarm calls, their behavior is more positively reinforcing than in the other groups where starling alarm calls are commonly given to non-vervet predators.

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... This difference in response acquisition means that the relative speed and timing of development can indirectly test for learning (Hollén & Radford, 2009). Young animals have proved useful in testing this prediction, as they initially have little exposure to heterospecifics, and evidence suggests that young can learn to eavesdrop on heterospecific alarm calls (Hauser, 1988;Fichtel, 2008;Haff & Magrath, 2012. For example, 5-day-old nestling white-browed scrubwrens ignore sympatric superb fairy-wren and New Holland honeyeater, Phylidonyris novaehollandiae, mobbing calls, which are acoustically distinct from parental alarms, but do respond by the time they are 10 days old (Haff & Magrath, 2012). ...
... Correlations between the rate of response development and the magnitude of exposure to heterospecific alarm calls provide stronger evidence for learning than temporal changes alone. In a classic example, infant vervet monkeys develop adult-like responses to superb starling, Lamprotornis superbus, mobbing alarm calls more quickly on territories where starlings are common, suggesting that those young have more opportunities to learn about the alarms than young on territories where starlings are less abundant (Hauser, 1988). Similarly, fledgling white-browed scrubwrens develop a response to New Holland honeyeater aerial alarm calls more quickly on territories where the honeyeaters are more common. ...
... Because of its inherent risks, direct learning may be most common in low-risk situations, such as predator mobbing (Caro, 2005), which combines predator presence with repetitive, easily locatable calls (Vieth et al., 1980;Klump & Shalter, 1984;Hurd, 1996;Griffin, 2004;Goodale & Kotagama, 2006;Magrath et al., 2009b;Nocera & Ratcliffe, 2010;Bradbury & Vehrencamp, 2011). Observational evidence suggests that young vervet monkeys learn to associate starling mobbing alarms directly with predators (Hauser, 1988). There has been only one experimental test of direct learning about unfamiliar alarm calls. ...
Article
Animals often gather information from other species by eavesdropping on signals intended for others. We review the extent, benefits, mechanisms, and ecological and evolutionary consequences of eavesdropping on other species’ alarm calls. Eavesdropping has been shown experimentally in about 70 vertebrate species, and can entail closely or distantly related species. The benefits of eavesdropping include prompting immediate anti-predator responses, indirect enhancement of foraging or changed habitat use, and learning about predators. Eavesdropping on heterospecifics can provide more eyes looking for danger, complementary information to that from conspecifics, and potentially information at reduced cost. The response to heterospecific calls can be unlearned or learned. Unlearned responses occur when heterospecific calls have acoustic features similar to that used to recognize conspecific calls, or acoustic properties such as harsh sounds that prompt attention and may allow recognition or facilitate learning. Learning to recognize heterospecific alarm calls is probably essential to allow recognition of the diversity of alarm calls, but the evidence is largely indirect. The value of eavesdropping on different species is affected by problems of signal interception and the relevance of heterospecific alarm calls to the listener. These constraints on eavesdropping will affect how information flows among species and thus affect community function. Some species are ‘keystone’ information producers, while others largely seek information, and these differences probably affect the formation and function of mixed-species groups. Eavesdroppers might also integrate alarm calls from multiple species to extract relevant and reliable information. Eavesdropping appears to set the stage for the evolution of interspecific deception and communication, and potentially affects communication within species. Overall, we now know that eavesdropping on heterospecific alarm calls is an important source of information for many species across the globe, and there are ample opportunities for research on mechanisms, fitness consequences and implications for community function and signalling evolution.
... A recent study on cross-fostered nestlings of reed warblers (Acrocephalus scirpaceus), dunnocks (Prunella modularis) and robins (Erithacus rubecula) also shows that although these nestlings do not develop a response to their foster species' alarm calls, learning does seem necessary to finetune the responses to their own species' alarms (Davies et al. 2004). Other evidence that learning is involved comes from numerous studies showing that both mammals and birds respond to the calls of other species (Rasa 1983;Hauser 1988;Shriner 1998;Zuberbühler 2000a;Ramakrishnan & Coss 2000a;Rainey 2004a, b). Responses to calls of others thus show a greater developmental flexibility than both call production and call usage. ...
... For example, infant vervet monkeys, Cercopithecus aethiops, of 3-4 months of age rarely responded like adults, whereas most infants older than 6 months did so ). The need for experience was further supported by Hauser (1988), who found that infant vervet monkeys exposed to superb starlings, Spreo superbus, alarm calls at a high rate responded appropriately to these calls at an earlier age than did infants exposed to these calls at a lower rate. ...
... If referential alarm calls evolve from motivational signals as proposed by , it may make sense that predator type specific calls require more learning than others and appear later in the repertoire. Moreover, the speed of learning may depend on the frequency with which different call types are heard (see Hauser 1988;. Aerial encounters occurred more frequently than terrestrial or snake encounters and aerial low urgency calls were most common amongst the predator type specific calls produced by young. ...
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Despite strong selection on young and adult prey to avoid predators, we often find obvious differences in anti-predator behaviour between them. By examining the ontogeny of antipredator behaviour, we can gain insight into how young animals come to classify predators, knowledge crucial for their survival. In this thesis, I investigated how and when young meerkats (Suricata suricatta) develop the ability to produce alarm calls with an adult-like structure, how they come to use these alarm calls in appropriate contexts, and how they respond to the alarm calls of other group members. Meerkats, which are cooperatively breeding mongooses living under a high predation pressure, have evolved a sophisticated alarm-call system consisting of calls which simultaneously encode information about specific predator types and the level of urgency, and calls not distinctively related to specific predator types. This system is therefore highly suitable to address questions regarding vocal development of alarm calls. Since captive environments often lack many of the natural predators that wild animals experience, research on captive animals can also offer additional insight into how experience with predators may influence a species’ capabilities of responding to them. I collected behavioural observations of naturally occurring predator events, and conducted playback and manipulation experiments at different stages during juvenile development in wild and captive populations. Although young meerkats were able to respond correctly to alarm calls within three months, their probability of doing so increased as they grew older. Young were also likely to gather cues from other group members by looking towards them or running to them. These results suggest that experience is needed to perfect the alarm-call responses of young. However, young showed correct responses to alarm calls signalling predators closeby at an earlier age than to those signalling predators far away, indicating that responses may also be adapted to the level of risk posed by different situations. Correct responses were not, however, contingent upon the particular predator approaching. In terms of call production, young were less likely to utter alarm calls than were adults, but also less likely to look out for predators. Since alarm calls were more likely to be given by vigilant young, the increase in alertness with age might be responsible for an age-related increase in alarm calling. Nevertheless, alarm calls which are not related to specific predator types were produced much earlier than predator type specific calls, indicating that some learning may also be involved. Experience also seems necessary to restrict alarm calling to predators belonging to particular classes. In contrast, although the alarm calls of young underwent slight modification during development, changes which are likely to reflect physical maturation, they were more or less structurally indistinguishable from those of adult calls. All alarm calls that have been documented in the wild also occurred in captivity. The acoustic structure, however, differed slightly from that observed in the wild, but may only reflect differences in arousal. Without experience of odours from predators, captive-born meerkats distinguished between faeces of potential predators and non-predators, similar to that of wild individuals. Together, these findings show that young animals come to classify predators through a mixture of innately recognised features and gradual modification as a result of experience,and provide an important contribution to the small existing literature on predator avoidanceontogeny.
... If fledglings learn to respond to heterospecific alarm calls, by contrast, young should ignore heterospecific alarm calls when they are just out of the nest, but should respond like adults later in their dependency period. Additionally, if fledgling response to heterospecific calls is learned, then the response should develop more rapidly on territories on which heterospecifics occur more frequently (Hauser 1988). ...
... These results support past studies that have found a gradual development of appropriate response to conspecific alarm calls by young (reviewed in Hollén & Radford 2009;Lea & Blumstein 2011), and strongly suggest that fledglings quickly learn to respond appropriately to heterospecific alarm calls, either through direct experience or through secondary associations with parental calls or behaviour. This result is thus consistent with other studies suggesting that learning is an important mechanism of response to heterospecific alarm calls (Hauser 1988;Hurd 1996;Mathis et al. 1996;Shriner 1999;Zuberbühler 2000a;Forsman & Monkkonen 2001;Caro 2005;Wisenden et al. 2008). ...
... This pattern shows a remarkably fine-scaled response to the presence or absence of heterospecifics, and is comparable to hosts learning to respond to brood parasites on a territory-by-territory spatial scale ). Young on territories without resident honeyeaters probably required more time to develop appropriate response because they had fewer opportunities to learn to associate honeyeater alarm calls with danger, just as young vervet monkeys, Chlorocebus pygerythrus, respond earlier to superb starling, Lamprotornis superbus, alarm calls on territories where starlings are more common (Hauser 1988). Honeyeaters are highly mobile in search of flowering trees and shrubs (Higgins et al. 2001), and so even young on territories without resident honeyeaters were likely to be exposed to the alarm calls of passing individuals. ...
Article
Young birds and mammals suffer from a high risk of predation, and should be under strong selection for early response to cues indicating danger, including the alarm calls of other species. Despite this prediction, there has been little investigation of the development of response by young animals to heterospecific alarm calls, and none on fledgling birds. Previous studies have suggested that learning is important in the recognition of heterospecific alarm calls in adult birds, but when learning occurs is unknown. We examined the responses of fledgling white-browed scrubwrens, Sericornis frontalis, at three ages to playback of the aerial alarm calls of the sympatric superb fairy-wren, Malurus cyaneus, and New Holland honeyeater, Phylidonyris novaehollandiae. Fairy-wren and scrubwren alarm calls are acoustically similar, while honeyeater alarm calls are distinct, but adult scrubwrens respond to both. Recently fledged scrubwrens responded strongly to conspecific alarm calls, but weakly to heterospecific alarm calls. By contrast, only 2 weeks after leaving the nest most fledglings responded to fairy-wren and honeyeater alarm calls similarly to conspecific alarm calls. However, fledglings in territories without honeyeaters ignored honeyeater alarm calls. Three weeks later, fledglings on all territories responded to all heterospecific alarm calls, an identical response to that of their parents. These results demonstrate that fledglings can quickly develop appropriate responses to heterospecific alarm calls, and present strong evidence that response is learned over a microgeographical scale.
... First, it is generally assumed that the production of the basic acoustic structure of vocalizations is predominately genetically determined, but subtle acoustic variation in calls between groups can arise as a result of social learning (Crockford et al. 2004; Hammerschmidt et al. 2001; Snowdon 2001; Winter et al. 1973). Second, the ability to use vocalizations in an appropriate context appears to be partly innate and partly socially learned, and thus more flexible (Hauser 1988; Seyfarth and Cheney 1997). For example, infant vervets (Chlorocebus aethiops) produce an alarm call inappropriately upon detecting nonthreatening species such as pigeons or warthogs. ...
... Third, call comprehension appears to be more flexible and influenced by experience and learning than call production and usage (Seyfarth and Cheney 2010). For example, young vervets or Verreaux's sifakas (Propithecus verreauxi) need experience before they respond appropriately to their own or other species' alarm calls, and are likely to learn by observation of adult responses (Fichtel 2008; Hauser 1988; Seyfarth and Cheney 1997). Moreover, studies focusing on the acquisition of predator evasion tactics in rhesus monkeys (Macaca mulatta), as well as in birds and marsupials such as naïve blackbirds (Turdus merula) or tammar wallabies (Macropus egenii), revealed that fear responses could be conditioned to formerly novel objects by observing conspecifics showing fear or mobbing responses toward the object (Cook and Mineka 1989; Curio et al. 1978; Griffin and Evans 2003). ...
... We propose that the observed population differences in responses to tchi-faks and growls might be related to differences in the set of predators to which these sifakas are exposed. Because non-human primate's comprehension of vocalizations is highly flexible (Seyfarth and Cheney 2010) and because the appropriate categorization of alarm calls develops with age and seems to be influenced by social learning (Fichtel 2008; Hauser 1988; Seyfarth and Cheney 1997), our data suggest that sifakas of both species underwent a socially learned modification in the meaning of one of their alarm calls. However, the social and behavioral mechanisms underlying such a shift in comprehension of alarm calls remain obscure. ...
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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.
... Some of the strongest evidence that associative learning shapes signal response in wild animals comes from studies of responses of various taxa to heterospecific alarm calls (Hauser 1988;Terborgh 1990;Rainey et al. 2004;Ito and Mori 2010;Magrath and Bennett 2012; see also Mitchell and McCormick 2013). It is often assumed that such responses are due to individuals of one species learning that the production of other species' alarms is associated with the presence of a predator (Fischer 2011). ...
... However, it is also plausible that responses to the alarm calls of other species are innate, nervous system-based reactions to the physical features of the sound, given that alarm calls across taxa tend to be characterised by similar acoustic features (e.g., sudden onsets and pulses of energy) (Owren and Rendall 2001;Rendall et al. 2009). While most evidence points to a role of learning (Hauser 1988;Magrath et al. 2009;Magrath and Bennett 2012), the two hypotheses regarding the proximate basis for anti-predator responses to heterospecific alarms are not mutually exclusive (Owren and Rendall 2001;Fallow et al. 2013), and a role for acoustic features in driving responses has also received some support (Fallow et al. 2011(Fallow et al. , 2013. Despite the widespread evidence that responses to heterospecific alarm are shaped at least in part by learning, support has been largely indirect (Magrath et al. 2015a). ...
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Many vertebrate taxa respond to heterospecific alarm calls with anti-predator behaviours. While it is unclear how apparent recognition is achieved, learned associations between the occurrence of the call and the presence of a predator are considered the most likely explanation. Conclusive evidence that this behaviour is indeed underpinned by learning, however, is scarce. This study tested whether wild black capuchin monkeys (Sapajus nigritus) learn to associate novel sounds with predators through a two-phase field experiment. During an initial training phase, three study groups were each presented with a playback of one of the three novel sounds together with a simulated felid predator on four occasions over an 8- to 12-week period. This was followed by a test phase, wherein each of the three sounds was played back to individuals in all three groups, allowing each sound to serve as both a test stimulus for individuals trained with that sound, and a control stimulus for individuals trained with another sound. Antipredator responses were significantly stronger in response to test sounds than to controls. Limited observations suggest that antipredator responses persisted for at least 2 years without reinforcement of the predator–sound link. Additionally, responses to noisier sounds were typically stronger than were those to more tonal sounds, although the effect of sound type cannot be disentangled from potential effects of group. This study provides the strongest evidence to date that learning affects the responses of primates to sounds such as heterospecific alarm calls, and supports the contention that signals provide receivers with information.
... Vervets also attend to the alarm calls of other species, such as the alarm calls of the superb startling, Spreo superbus, which are given in response to ground predators such as leopards (Cheney & Seyfarth 1985). Vervet infants in an area with higher rates of starling alarm calling responded to playbacks of these calls at an earlier age than did infants living in areas with lower rates of starling alarm calling (Hauser 1988). Chacma baboon, Papio cynocephalus ursinus, infants begin to discriminate between different variants of their loud calls at an age of about six months (Fischer et al. 2000). ...
... The view that experience, and not only maturation, mediates the development of infants' responses is supported by the observations that both vervets and baboons respond to the alarm calls of birds, ungulates, and other primate species (Cheney & Seyfarth 1985, Hauser 1988Cheney & Seyfarth 1990;Zuberbühler 2000). It seems unlikely that these responses have a purely genetic basis. ...
... For example, juvenile meerkats are more likely to interact with novel tasks than adults, which is likely due to their low fear in exploring new objects and situations (Thornton and Samson 2012). Similarly, some studies have suggested that neophobia is a product of experience (Hauser 1988;Kelley and Magurran 2003;Benson-Amram and Holekamp 2012), which additionally supports the finding that older magpies, with more experience, are more hesitant to Fig. 4 The effect of age on the mean (±SE) frequency of individuals solving a novel foraging task. Data included 53 trials with a novel task to 18 individuals from four different groups Fig. 5 Relationship between the time spent interacting with a task and the proportion of individuals that solved the colour-reward association task. ...
... demonstrated higher flipping success) and displayed higher levels of learning success than juveniles. Adults are likely to possess a larger repertoire of prior experience and knowledge (Hauser 1988) from which to innovate in novel situations and may therefore succeed in learning more often where juveniles may fail Thornton and Samson 2012;Resende et al. 2014). Hauser (1999) suggested that maturity is associated with more successful learning mechanisms, as older individuals are less exploratory and have a higher capacity to reject non-beneficial options when interacting with a novel associative task. ...
Article
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Group living can present unique challenges that may require individuals to possess cognitive skills, such as the ability to recognise group members and maintain relationships with specific individuals. These skills may be particularly important for animals that live in large groups, because the intricacies of social life may become more complex when more individuals are involved. Previous research has found that species with regular social interactions tend to show elevated cognitive performance relative to those that rarely interact, yet intraspecific variation in performance among individuals in social groups of varying size is rarely explored. We investigated the relationship between the ability to solve an associative learning task and group size among individuals of a free-living, social bird, the Australian magpie (Cracticus tibicen dorsalis). Individuals varied in their likelihood of interacting with and solving the task. Individuals from larger groups were more likely to approach the associative learning task, suggesting that group size influences individual propensity to attempt a novel task. However, group size did not influence the likelihood that individuals solved the task. Rather, age had an important effect; adults were more likely to solve the association task than juveniles. Our finding that free-living individuals occurring in large social groups were more likely to interact with a novel task suggests that group size may affect differences in performance at a cognitive task within a species.
... In the present paper, voice perception will refer primarily to the processing of information in conspecific vocalizations (CV) despite evidence that primates are also able to extract information from heterospecific vocalizations [18][19][20][21][22]. CV perception is assumed to include several processing stages that are organized in a similar way to those employed to extract information from faces [23,24], from distinguishing CV among non-CV sounds (initial 'structural encoding' stage) to processing different types of information contained in CVs (e.g. ...
... From a larger perspective, we assume that the vocal exchanges of information essential to the primates' social life may have shaped their voice processing system in a similar way. As an example, similar encoding strategies in their vocalizations [149] could allow a generalization across call categories but also across the vocal repertoires of other species [18][19][20][21][22]. To what extent has social life been able to determine these similarities in voice processing among primates? ...
Article
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One can consider human language to be the Swiss army knife of the vastdomain of animal communication. There is now growing evidencesuggesting that this technology may have emerged from already operationalmaterial instead of being a sudden innovation. Sharing ideas and thoughtswith conspecifics via language constitutes an amazing ability, but whatvalue would it hold if our conspecifics were not first detected andrecognized? Conspecific voice (CV) perception is fundamental to communi-cation and widely shared across the animal kingdom. Two questions thatarise then are: is this apparently shared ability reflected in common cerebralsubstrate? And, how has this substrate evolved? The paper addresses thesequestions by examining studies on the cerebral basis of CV perception inhumans’closest relatives, non-human primates. Neuroimaging studies, inparticular, suggest the existence of a‘voice patch system’, a network of inter-connected cortical areas that can provide a common template for the cerebralprocessing of CV in primates.
... Where the use of information is acquired by learning (individual or social), the interpretation can change and become more accurate and complete as it is updated with experience. For instance, animals can learn to extract referential information from alarm calls (Hauser 1988;Zuberbühler 2000b;Hollén & Manser 2006). Where it is innate on the other hand, the interpretation is not influenced by the individual's experience. ...
... suggested that recognition is acquired by associative learning (Curio 1971;Nuechterlein 1981;Hauser 1988;Shriner 1999), or that alarm calls are recognized by acoustic properties common to alarm calls across taxa (Marler 1957;Bradbury & Vehrencamp 1998). If associative learning plays a role, the response should be correlated with the rate at which heterospecific alarms are encountered. ...
Article
Soziale Raubtiere sind für die Kognitionsforschung besonders interessant, da komplexe Sozialsysteme die Evolution von speziellen kognitiven Fähigkeiten und von Intelligenz im Allgemeinen begünstigt haben könnten (‚social intelligence’ Hypothese). Daher habe ich grundlegende kognitive Fähigkeiten von freilebenden Zebramangusten (Mungos mungo), einer kleinen sozialen Raubtierart, in ihrem natürlichen Lebensraum im Queen Elizabeth Nationalpark, Uganda studiert. Meine Dissertation zeigt, welche Informationen Zebramangusten aus ihrer Umwelt entnehmen, aber auch welche an sich verfügbare Information von ihnen nicht genutzt wird. Ich diskutiere diese Erkenntnisse hinsichtlich Grenzen des sensorischen und kognitiven Systems, und hinsichtlich der situationsabhängigen Relevanz bestimmter Informationen. Weiter diskutiere ich meine Ergebnisse im Zusammenhang von spezifischen Gegebenheiten der ökologischen und sozialen Umwelt, welche die Nutzung von Information und die dazugehörigen kognitiven Fähigkeiten fördern. Social carnivores are of particular interest in the study of cognition because complex social systems are thought to promote the evolution of specialized cognitive abilities and intelligence in general (social intelligence hypothesis). Therefore, I explored basic cognitive abilities of free-ranging banded mongooses (Mungos mungo), small social carnivores, in their natural habitat in Queen Elizabeth National Park, Uganda. My thesis shows what specific information banded mongooses extract from their environment, but it also provides examples of available information that is not used. I discuss these findings with regard to limitations of the sensory and cognitive apparatus and to the relevance of information in particular situations. I further discuss the use of information and the associated cognitive abilities in the context of demands of the ecological and social environment.
... Our present findings indicate that for alarm signals, unlike a variety of other social signals, receivers do not respond preferentially to signals emanating from their mother's or colony members. This is not particularly surprising in that receivers would benefit from displaying antipredator behavior to any signal that is reliably associated with the presence of a predatory threat (Hauser, 1988;Lind and Cresswell, 1995;Shriner, 1999;Schibler and Manser, 2007), though as Leonard et al. (2005) have argued, receivers cannot increase their responsiveness to signals without simultaneously increasing their risk of responding to inappropriate signals. Future studies of social discrimination in the context of ground squirrel alarm signaling should thus focus on documenting the active space of alarm signals and how that relates to the development of differential responsiveness to reliable versus unreliable individual signalers, along with the costs and benefits of such discrimination. ...
Article
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Alarm calls are emitted by Richardson's ground squirrels Urocitellus richardsonii in response to avian and terrestrial predators. Conspecifics detecting these calls respond with increased vigilance, promoting predator detection and evasion, but in doing so, lose time from foraging. That loss can be minimized if alarm call recipients discriminate among signalers, and weight their response accordingly. For juvenile ground squirrels, we predicted that the trade-off between foraging and vigilance could be optimized via selective response to alarm calls emitted by their own dam, and/or neighboring colony members over calls broadcast by less familiar conspecifics. Alarm calls of adult female Richardson's ground squirrels were elicited in the field using a predator model and recorded on digital audio tape. Free-living focal juveniles were subjected to playbacks of a call of their mother, and on a separate occasion a call from either another adult female from their own colony, or an adult female from another colony. Neither immediate postural responses and escape behavior, nor the duration of vigilance manifested by juveniles differed with exposure to alarm calls of the three adult female signaler types. Thus, juveniles did not respond preferentially to alarm calls emitted by their mothers or colony members, likely reflecting the high cost of ignoring alarm signals where receivers have had limited opportunity to establish past signaler reliability.
... In some species, effective nest-defence responses are given to a novel predator on the first encounter, indicating that the ability to recognise predators may be genetically inherited (Curio 1975, Hobson et al. 1988, Mueller & Parker 1980, Owings & Coss 1977, Riechert & Hedrick 1990, whereas in others, recognition of predators may be learned (Coleman 1987, Conover 1987, Curio et al. 1978a, 1978b, Hauser 1988, Klopfer 1957, Knight 1984, Pugesek 1983, Regelmann & Curio 1983, Thornhill 1989, Vieth et al. 1980. It may be that inheritance of predator recognition involves a mix of genetic and cultural processes, where an animal is genetically predisposed to learn defence responses. ...
... For instance, juvenile chimango caracaras (Milvago chimango) are less neophobic toward novel objects than adults (Biondi et al. 2010). In contrast, adult vervet monkeys (Chlorocebus pygerythrus) are less neophobic because of a greater variety of experiences (Hauser 1988). How neophobia changes over development is likely affected by whether individuals have positive or negative experiences with novelty throughout their life. ...
Article
For species moving into new environments, locating and using unfamiliar resources is crucial for survival. The cane toad (Rhinella marina) has been successful in many countries worldwide, persisting in both urban and rural landscapes. Given that animals exploiting urban habitats are confronted with novel feeding opportunities, individuals in those areas are expected to exhibit reduced neophobic tendencies compared with individuals in rural populations. Additionally, individuals persisting in introduced populations are expected to be less neophobic than individuals in native populations, taking advantage of novelty as their range expands. To investigate such predictions, we examined the response to novel prey and a novel object in native toads in Panama and introduced populations (urban and rural) in Florida. Toads were tested in an arena with novel or familiar prey and later with a novel object next to familiar prey. We found differences in response to novelty between cane toads in different ranges but not in different habitats. Most introduced individuals from both urban and rural habitats consumed novel prey with no difference in latency to eat between prey types. Few native toads, however, consumed any prey during trials, spending most of their time moving about the arena. When familiar prey was presented near a novel object, more than half of the introduced toads ate, but no native individuals ate. This study emphasizes the importance of behavior as a mechanism used by invasive species to exploit novel resources and successfully colonize new environments.
... 91 Alarm calls by juvenile vervet monkeys tend to get ignored because they are unreliable and at times incorrect but the same vervet monkey juveniles may learn to recognize the alarm calls issued by starlings. 92 The fact that animals may recognize signals of heterospeci cs and act on them is intriguing because, in those cases in which alarm calls are clearly not part of a species' genetic makeup, their recognition has to include some form of learning. Recognition, in this case, has to include its speci c representational value of a real event or a potential danger (warning of a predator). ...
Animal communication is first and foremost about signal transmission and aims to understand how communication occurs. It is a field that has contributed to and been inspired by other fields, from information technology to neuroscience, in finding ever better methods to eavesdrop on the actual 'message' that forms the basis of communication. Much of this review deals with vocal communication as an example of the questions that research on communication has tried to answer and it provides an historical overview of the theoretical arguments proposed. Topics covered include signal transmission in different environments and different species, referential signaling, and intentionality. The contention is that animal communication may reveal significant thought processes that enable some individuals in a small number of species so far investigated to anticipate what conspecifics might do, although some researchers think of such behavior as adaptive or worth dismissing as anthropomorphizing. The review further points out that some species are more likely than others to develop more complex communication patterns. It is a matter of asking how animals categorize their world and which concepts require cognitive processes and which are adaptive. The review concludes with questions of life history, social learning, and decision making, all criteria that have remained relatively unexplored in communication research. Long-lived, cooperative social animals have so far offered especially exciting prospects for investigation. There are ample opportunities and now very advanced technologies as well to tap further into expressions of memory of signals, be they vocal or expressed in other modalities. WIREs Cogn Sci 2014, 5:661-677. doi: 10.1002/wcs.1321 For further resources related to this article, please visit the WIREs website. The author has declared no conflicts of interest for this article. © 2014 John Wiley & Sons, Ltd.
... Several reasons have been proposed in the literature to explain mixed-species groups (Sridhar et al. 2009;Harrison & Whitehouse 2011;Farine et al. 2012). Studies have reported that many mammals and birds have learned to associate heterospecific alarm calls with the presence of a predator (Hauser 1988;Shriner 1998;Fichtel 2004;Rainey et al. 2004;Magrath et al. 2007). Moreover, species that normally form small groups can increase group size by heterospecific association and hence enhance the effectiveness of antipredator behaviour (as the dilution effect or collective detection) (Goodale et al. 2010). ...
Article
Prey can obtain valuable benefits from associating with other species if heterospecifics help to detect predators or locate good food patches. In mixed-species groups, how species respond to the presence of other species remains a poorly explored question although it might give crucial insights into mechanisms underlying the interspecific coexistence. We studied temporary mixed-species groups of large herbivores in Hwange National Park (Zimbabwe) between the common impala (Aepyceros melampus), the focal species here, and bigger species including the plains zebra (Equus quagga), the greater kudu (Tragelaphus strepsiceros) or the blue wildebeest (Connochaetes taurinus). In the Hwange savanna, the focal and smaller species are exposed to a larger range of predators than the associated species. In this context, we investigated how impalas adjusted their vigilance with group size comparing impala-only and mixed-species groups and whether the identity of heterospecifics affected vigilance of impalas. Our study showed that the time impalas spent in vigilance significantly decreased with group size when they formed impala-only groups, whereas it did not significantly vary with group size in mixed-species groups. Moreover, in mixed-species groups, impalas did not adjust their time spent in vigilance with the proportion of conspecifics and the identity of the associated species. Thus, the mechanism underlying the difference of impalas' behavioural adjustment of vigilance with group size between single- and mixed-species groups seemed to be related to the presence but not to the number and the identity of heteropecifics. Finally, we discuss the concept that larger and dominant heterospecifics were likely to increase competition for food access, thereby forcing higher vigilance of impalas, outweighing any reduction from collective vigilance.
... In humans, the identification of transitional probability cues appears to be based on a domain-general cognitive mechanism, namely statistical learning [100][101][102][103]. Furthermore, statistical learning is not a uniquely human cognitive mechanism, and also other species have been demonstrated to use it to deduce signal structure [104]. These can even apply across species; for example, many non-human animals form associations between heterospecific alarm calls and the presence of a predator [105,106]. Also, vocal learning in nonhuman animals, most notably in birds, is suggested to be supported by statistical computations, although the precise mechanisms behind it are not yet fully understood [104]. It thus seems likely that both humans and many non-human tetrapods rely on a combination of statistical learning and acoustic modulations when learning the structure of their species-specific sound sequences. ...
Article
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Voice modulatory cues such as variations in fundamental frequency, duration and pauses are key factors for structuring vocal signals in human speech and vocal communication in other tetrapods. Voice modulation physiology is highly similar in humans and other tetrapods due to shared ancestry and shared functional pressures for efficient communication. This has led to similarly structured vocalizations across humans and other tetrapods. Nonetheless, in their details, structural characteristics may vary across species and languages. Because data concerning voice modulation in non-human tetrapod vocal production and especially perception are relatively scarce compared to human vocal production and perception, this review focuses on voice modulatory cues used for speech segmentation across human languages, highlighting comparative data where available. Cues that are used similarly across many languages may help indicate which cues may result from physiological or basic cognitive constraints, and which cues may be employed more flexibly and are shaped by cultural evolution. This suggests promising candidates for future investigation of cues to structure in non-human tetrapod vocalizations. This article is part of the theme issue ‘Voice modulation: from origin and mechanism to social impact (Part I)’.
... Many respondents indicated that instinct 'kicks in' and responses to potential predators are normal, but this assumes that predationrelated behaviours are instinctive. There is evidence to suggest that some antipredator behaviours are learnt (Hauser 1988;Shier and Owings 2007), indicating that some level of training may be necessary. Training has been attempted with marsupial species, with some short-term success (McLean et al. 1996;McLean et al. 2000). ...
Article
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Wildlife rehabilitation is common in Australia, with more than 30 mainly volunteer wildlife networks caring for thousands of animals annually. Here we report on a survey of 140 Australian wildlife rehabilitators that asked questions about their motivations, their methods of rehabilitation and their methods for release and post-release assessments. Most rehabilitators were motivated by animal welfare concerns and most animals coming into care were injured or orphaned wildlife. Most rehabilitators recorded each animal’s history, conducted a medical examination and briefly quarantined new arrivals; few conducted pre-release medical testing. Animal behaviour before release was a significant concern and >50% of respondents stated that animals exhibiting stereotypic behaviours were still released. However, there were no consistent criteria for the suitability of an animal for release, its release site, or which soft-release method to use. Fewer than 60% of respondents carried out post-release monitoring, which was typically <1 month, and only 40% could identify factors that contribute to release success. Predation hampers most reintroductions and is likely to reduce survival of rehabilitated wildlife, highlighting the need for strategies to reduce predation risk; 20% of respondents carried out antipredator training, though most in an unstructured way. The ability to carry out animal training, and monitor success was perceived to be limited by poor funding, poor access to monitoring equipment, little government support and time constraints. Researchers are encouraged to collaborate with wildlife volunteer networks in order to improve this potentially valuable conservation approach.
... They responded most strongly to typical alarm barks, less strongly to intermediate alarm calls, less strongly still to intermediate contact barks, and hardly at all to typical contact barks (Fischer et al., 2000). There appears to be some flexibility, because infant vervet monkeys who were exposed to specific alarm calls frequently developed the appropriate response earlier than infants who were rarely exposed to it (Hauser, 1988). Furthermore, a study of the development of maternal recognition showed that, from as early as ten weeks of age, Barbary macaque infants responded more strongly to playbacks of their mothers' calls than to playbacks of unrelated females from the same social group (Fischer, 2004). ...
Research
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Draft manuscript of review article on communication and social learning in nonhuman primates
... For example, 29 % of respondents stated that training was required for animals to recognize palatable natural foods, highlighting the importance of providing natural food items consistently through the rehabilitation process. Animals captured as juveniles are also likely to be predator naïve as predator avoidance behaviour has been shown to be learnt (Hauser 1988;Shier and Owings 2007). This indicates that training for predator avoidance may be necessary. ...
Article
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Mammal rehabilitation is carried out in hundreds of centres worldwide, requiring a large investment of time, personnel and funds. Although there are numerous published studies focusing on post-release outcomes, few have discussed the methods employed in rehabilitation. As an important first step toward addressing this, data were collected directly from rehabilitation centres about their aims, methods employed and assessment of outcomes. A survey of mammal rehabilitation centres was conducted with data collected in the form of responses to multiple-choice questions and written responses. Our results indicated a number of challenges, including: problems surrounding social group formation, lack of predator avoidance training, limited or no pre-release medical screening, release of animals exhibiting stereotypic behaviours, frequently short-term (<6 months) post-release monitoring, with only a third of centres assessing the success of releases. Although many factors may influence the success of rehabilitation, improvements to monitoring and assessment are needed before the effects of any changes to protocols could be determined. Extended post-release monitoring and thorough assessment should be a part of any future mammal rehabilitation projects. With a view to improving the rehabilitation phase, we have developed a decision tree to assist the assessment of mammals at each stage of the rehabilitation process. This could be easily adapted to create detailed species-specific models in the future.
... For example, golden-mantled ground squirrels (Spermophilus lateralis) that respond to yellow-bellied marmot (Marmota flaviventris) alarm calls [Shriner 1998] could be trained to associate a new sound with the appearance of a model predator [Shriner 1999]. Similarly, young vervet monkeys (Cercopithecus aethiops) acquired the ability to respond to the alarm calls of superb starlings (Spreo superbus) faster if they were exposed to a higher level of starling alarm calls, suggesting learning [Hauser 1988]. Several studies have also demonstrated that species respond to the alarm calls produced by sympatric but not allopatric species [Fichtel 2004;Magrath et al. 2009;Nocera et al. 2008;Ramakrishnan and Coss 2000]. ...
Thesis
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Habitat destruction and fragmentation are the main threats to the lemurs of Madagascar. The extent of impact of habitat alteration on a species is manifold and not clearly predictable without knowing the species’ ecology and habitat preferences. This study examined baseline aspects of the ecology and behaviour of the Critically Endangered Sahamalaza sportive lemur (Lepilemur sahamalazensis). Study aims were to identify the lemurs’ requirements regarding home ranges and sleeping sites, to investigate the influence of habitat degradation on the lemurs’ ecology and behaviour, to describe its’ vocal repertoire and to develop a non-invasive acoustic tool for rapid species identification. Data collection was conducted in the Ankarafa Forest, Sahamalaza, during three successive field seasons, amounting to twelve months of fieldwork from 2009 to 2011. For habitat descriptions of fragments and microhabitats I used the quarter point sampling method, for home range habitat descriptions a plot-based method. Focal animal sampling was used to create a 24-hour activity budget, and for night follows individuals were radio-tagged. Vocalisations were recorded during night follows using continuous sampling. Playback-experiments with predator calls as well as alarm calls of syntopic bird and lemur species were conducted during the day and with sportive lemur calls during the nocturnal focal animal sampling. The forest structure and tree species composition differed significantly between the five forest fragments, and differences in species composition suggested a lack of seed exchange, indicating that the Ankarafa Forest has been exposed to anthropogenic influences for several decades. Irrespective of the differences in overall structure and habitat parameters of the forest fragments, the microhabitat around sportive lemurs sleeping sites was similar in all measured habitat parameters, as were all measured parameters for the different sleeping trees. The abundance of sleeping sites and feeding tree species was an important factor for home range choice. Tree density was a critical factor for home range and sleeping site choice as a larger amount of canopy cover provided better protection from aerial predators. Results indicate that habitat requirements of the species can still be met by all of the forest fragments, regardless of their differing levels of degradation. The observed lemurs were highly folivorous and fed on 42 different tree species. Insects and fruits were added to the diet occasionally. Individuals had home ranges of 1.4. ha, but used only 0.5 ha of it during one night. They rested for prolonged times during their activity period. Based on low frequencies of social behaviour and the solitary use of sleeping sites, I concluded that the Sahamalaza sportive lemur is a solitary species. I could identify seven loud call classes for the Sahamalaza sportive lemur, most of which were structurally related to call classes described for other sportive lemur species, but differed in frequency and duration. Vocal parameters of the species’ loud calls could thus be used for future non- invasive species monitoring and species identification for range boundary studies. The studied lemurs had high levels of active behaviour during the day, and higher diurnal levels of activity in tree hole compared to tree tangle sleeping sites, suggesting a higher predation risk in tree holes. Resting Sahamalaza sportive lemurs recognised predator vocalisations as indicators of increased predation risk, discerned vocalisations of different predators, and employed species-specific anti-predator behaviours. Furthermore, the studied Sahamalaza sportive lemurs were able to use information on predator presence and predator type in referential signals of different surrounding species, thereby taking advantage of the possibility of early predator detection through cross-species communication. This study highlights the need for effective protection of the few remaining intact forest fragments on the Sahamalaza Peninsula with their old trees and high tree diversity, which will be crucial for the long-term survival of the Sahamalaza sportive lemur.
... This seasonal difference in territory occupancy did not lead to a difference in the number of jays attracted to CAs, since the mean number of aggregating birds did not differ substantially between the two experiments (Table 3). But the presence of fledglings on territories may have influenced the duration of CAs in other ways, for example, if the benefit to prolonged antipredator behaviour by parents is higher when their fledglings are nearby, or if CAs provide an opportunity for fledglings to learn about dangers and cues of risk, and if this learning is facilitated by a prolonged alarm response (Seyfarth & Cheney 1986;Hauser 1988;Griffin 2004;Hollén & Manser 2006;Hollén & Radford 2009). Carmen (2004) found that many vocal behaviours of scrub-jays decrease during March through early June (when experiment 2 was performed), when parents are busy with nesting, brooding and feeding nestlings, which may further contribute to seasonal differences. ...
Article
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All organisms must contend with the risk of injury or death; many animals reduce this danger by assessing environmental cues to avoid areas of elevated risk. However, little is known about how organisms respond to one of the most salient visual cues of risk: a dead conspecific. Here we show that the sight of a dead conspecific is sufficient to induce alarm calling and subsequent risk-reducing behavioural modification in western scrub-jays, Aphelocoma californica, and is similar to the response to a predator (a great horned owl, Bubo virginianus, model). Discovery of a dead conspecific elicits vocalizations that are effective at attracting conspecifics, which then also vocalize, thereby resulting in a cacophonous aggregation. Presentations of prostrate dead conspecifics and predator mounts elicited aggregations and hundreds of long-range communication vocalizations, while novel objects did not. In contrast to presentations of prostrate dead conspecifics, presentations of a jay skin mounted in an upright, life-like pose elicited aggressive responses, suggesting the mounted scrub-jay was perceived to be alive and the prostrate jay was not. There was a decrease of foraging in the area during presentations of prostrate dead conspecifics and predator mounts, which was still detectable 24 h later. Foraging returned to baseline levels 48 h after presentations. Novel objects and mounted jays did not affect foraging. Our results show that without witnessing the struggle and manner of death, the sight of a dead conspecific is used as public information and that this information is actively shared with conspecifics and used to reduce exposure to risk.
... Functional effects of pheromones can best be seen in male and female mating behaviors of rodents (Buck 2000). Animals use acoustic vocalizations for a variety of purposes, including individual recognition (Rendall et al. 1996), courtship and mating (Bosch et al. 2000), predator avoidance (Hauser 1988), and navigation and foraging . Although acoustic communication signals have their disadvantages (i.e., they may reveal location of sender to a predator, they may be energetically expensive to produce, and they rapidly attenuate), they have the advantage of high information content (i.e. a result of signal variation in form, function, and complexity) and are not limited by environmental barriers. ...
Article
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Communication signals are important regulators of mating behavior in many animals. Various pre- and post-copulatory mechanisms have been suggested to play a role in the reproductive success and mating strategies of many mammals. Recent studies have cited sperm competition as a possible post-copulatory mechanism of selection in bats, but few studies have examined which pre-copulatory mechanisms influence mate selection. Although it is generally accepted that bats emit vocalizations that function for communication purposes as well as the more universally recognized echolocation function, there is lack of actual empirical support for this idea. In this dissertation, I test the hypothesis that ultrasonic vocalizations of big brown bats are sexually dimorphic and differ contextually in the mating season. I used playback experiments to test the response of male and female big brown bats to variations in ultrasonic vocalizations of the opposite sex and to determine if ultrasonic vocalizations are used for mate selection. My data suggest that males were likely to select ultrasonic vocalization of frequently copulating females, but females did not select ultrasonic vocalizations of frequently copulating males over infrequently copulating males. These results suggest that mate selection of male big brown bats is influenced by ultrasonic vocalizations of females.
... Whereas cross-fostered individuals showed almost no change in vocal production, both they and the animals in their adoptive groups learned to recognize and respond appropriately to each others' vocalizations (Seyfarth and Cheney 1997). Similarly, young vervet monkeys must learn to distinguish and respond appropriately to the different alarm calls given by both their own species and nearby ungulates and birds (Seyfarth and Cheney 1990;Hauser 1988). Probably because they cannot recognize ignorance in others, adults do not actively instruct their offspring in this process. ...
Article
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If we accept the view that language first evolved from the conceptual struc- ture of our pre-linguistic ancestors, several questions arise, including: What kind of structure? Concepts about what? Here we review research on the vocal communication and cognition of nonhuman primates, focusing on results that may be relevant to the earliest stages of language evolution. From these data we conclude, first, that nonhuman primates' inability to represent the mental states of others makes their communication fundamentally different from hu- man language. Second, while nonhuman primates' production of vocalizations is highly constrained, their ability to extract complex information from sounds is not. Upon hearing vocalizations, listeners acquire information about their social companions that is referential, discretely coded, hierarchically struc- tured, rule-governed, and propositional. We therefore suggest that, in the ear- liest stages of language evolution, communication had a formal structure that grew out of its speakers' knowledge of social relations.
... Once learned, these relations do not require much flexibility on behalf of the recipient, since the same utterance always refers to the same external event. However, in their natural habitats, monkeys encounter numerous signals that have more vague and ambiguous referents which require them to take into account additional information before being able to respond adaptively (Hauser, 1988; Seyfarth and Cheney, 1990). The predator alarm calls of the ground-dwelling crested guinea fowl (Guttera pulcheri) provide a good example. ...
Article
Recent evidence suggests that our hominid ancestors did not have speech until very recently, indicating that many of the cognitive skills required for linguistic competence must have been present in the primate lineage long before the advent of language. These pre-adaptations might have evolved to function in communication as part of a general social or ecological intelligence, or as mere byproducts of other traits, calling for an empirical investigation of the functional significance of these abilities. The natural referential and combinatorial capacities in extant primates in their natural habitats are of particular interest. The empirical evidence reviewed in this chapter suggests that various cognitive capacities required for understanding language, including the ability to take into account semantic, syntactic, and pragmatic cues, are present in non-human primates. As signalers, however, non-human primates are curiously limited, showing little evidence of cognitive flexibility and creativity. These expressive limitations seem to be rooted in at least two deficiencies: a lack of sophisticated control over the articulators in the supra-laryngeal vocal tract and a remarkable shortcoming in social cognition. Non-human primates have consistently failed to show evidence of perceiving others as beings that possess mental states, such as beliefs or desires, suggesting that mind-blindness has impeded the evolution of sophisticated communication in situations that go beyond evolutionarily urgent events.
... Such an associative learning ability by experience can explain why (1) juvenile vervet monkeys are less successful than adults in associating the corresponding predator with the distinct conspecific alarm calls (Hauser, 1988(Hauser, , 1989Seyfarth and Cheney, 1986;reviewed in: Cheney and Seyfarth, 1990b) and that (2) nonhuman primates are able to extract meaningful information from the vocalizations of other animal species. Diana monkeys understand the causes of chimpanzees' screams (Zuberbühler, 2000b) and infer the type of predator from the Campbell's monkeys' and guinea fowls', Numida meleagris, alarm calls (Zuberbühler, 2000c(Zuberbühler, , 2000a. ...
... But these phenomena are not limited to birds. Mothers of rhesus macaques or Japanese macaques that have been raised together respond to the calls of their adopted children; vervets are attuned to the alarm calls of Sprea superbus (Hauser, 1988), and male and female white-cheeked gibbons co-ordinate their singing in an elaborate fashion (Deputte, 1982). ...
Article
The question of animal cultures has once again become a subject of debate in ethology, and is now one of its most active and problematic areas. One surprising feature of this research, however, is the lack of attention paid to the communications that go on in these complex animal societies, with the exception of mechanisms of social learning. This neglect of communications is all the more troubling because many ethologists are unwilling to acknowledge that animals have cultures precisely because they do not possess language, a refusal therefore on semiotic grounds. In the present article, I show that the biosemiotic approach to animal cultures is, on the contrary, essential to their understanding, even if the complexity of animal communications is far from being well enough understood. I consider that some of the consequences of this approach are very important, in particular the question of whether we can talk about subjects in the case of animals. Alternatively, I suggest that the semiotic approach to animal cultures leads to a discussion of some of the most serious limitations of biosemiotics, particularly when it comes to investigating the status of the interlocutors in a social community, or to taking into account interspecific communications and the social dimension of any biosemiotic interaction - which biosemiotics has for the moment failed to do. Finally I call attention to the importance of animals living in human communities and suggest that this be studied so as to better apprehend the capacities for culture in non-human living organisms.
... Some species may also benefit from an ability to recognize and use the information coded into the auditory signals of other species. Many animals, for example, do respond appropriately to the alarm calls of other species, whether closely (e.g., rodents : Shriner 1998;passerines: Magrath et al. 2009; African savannah herbivores: Meise et al. 2018;primates: Fichtel 2004;Zuberbühler 2000) or distantly related (e.g., mammal and birds : Hauser 1988;Muller and Manser 2008;Rainey et al. 2004;Seiler et al. 2013), with some species even learning to recognize the differing external referents encoded in heterospecific alarm signals (e.g., Fallow and Magrath 2010;Seyfarth and Cheney 1990;Zuberbühler 2000). ...
Article
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The ability to recognize conspecifics by their acoustic signals is of crucial importance to social animals, especially where visibility is limited, because it allows for discrimination between familiar and unfamiliar individuals and facilitates associations with and the avoidance of particular conspecifics. Animals may also benefit from an ability to recognize and use the information coded into the auditory signals of other species. Companion species such as dogs, cats, and horses are able to discriminate between familiar and unfamiliar human voices; however, whether this ability is widespread across vertebrates is still unknown. Using playback experiments, we tested whether western gorillas living at Zoo Atlanta were able to discriminate between the voices of subgroups of people: i.e., unfamiliar individuals, familiar individuals with whom the gorillas had positive interactions, and familiar individuals with whom they had negative interactions. Gorillas responded significantly more often (longer gazing duration, higher gazing frequency, shorter latency, and larger number of distress behaviors) to the voices of unfamiliar and familiar-negative individuals than to those of familiar-positive individuals, indicating that they recognized the voices of subgroup of people based on familiarity and possibly the nature of the relationship with them. Future studies should determine whether this is also the case in the wild, where interspecific associations with humans are less intense than they are in captive settings.
... Given the vast array of challenges that developing primates must successfully overcome, it is perhaps not surprising that juveniles may be especially susceptible to mortality (Ross & Jones, 1999). While several studies have explored how young primates learn foraging and predator avoidance strategies (Hauser, 1988;Rapaport & Brown, 2008; Van de Waal, Claidiére, & Whiten, 2013), investigations on how infants develop their social skills to better integrate into the group's social networks are still scant (Barale, Rubenstein, & Beehner, 2015;Kulik, Amici, Langos, & Widdig, 2015). ...
Article
Social network analysis is increasingly common in studying complex interactions among individuals. Across a range of primates, high‐ranking adults are generally more socially connected, which results in better fitness outcomes. However, it still remains unclear whether this relationship between social network position and dominance rank emerges in infancy and whether, in species with a social transmission of dominance rank, social network positions are driven by the presence of the mother. To fill this gap, we first explored whether dominance ranks were related to social network position, measured via eigenvector centrality, in infants, juveniles, and adults in a troop of semi‐free‐ranging rhesus macaques (Macaca mulatta). We then examined relationships between dominance rank and eigenvector centrality in a peer‐only group of yearlings who were reared with their mothers in either a rich, socially complex environment of multigenerational (MG) kin support or a unigenerational group of mothers and their infants from birth through 8 months. In Experiment 1, we found that mother's network position predicted offspring network position and that dominants across all age categories were more central in affiliative networks (social contact, social grooming, and social play). Experiment 2 showed that high‐ranking yearlings in a peer‐only group were more central only in the social contact network. Moreover, yearlings reared in a socially complex environment of MG kin support were more central. Our findings suggest that the relationship between dominance rank and social network position begins early in life, and that complex early social environments can promote later social competency. Our data add to the growing body of evidence that the presence/absence of the mother and kin influence how dominance rank affects social network position. These findings have important implications for the role of caregivers in the social status of developing primates, which ultimately ties to health and fitness outcomes. Across all age categories (infancy, juvenility, and adulthood), high‐ranking rhesus macaques were more central in affiliative social networks. These results indicate that even at an early age, high‐ranking individuals may be preferred social partners. However, in a peer‐only group of one year old rhesus macaques, dominance rank was not a good predictor of social network position, but rather was explained by complex early social experiences. These results suggest that the influence of multigenerational kin support can be key to the transmission of social network position via dominance rank. Rank predicts network centrality in macaques across the lifespan. Rank predicts network centrality in macaques across the lifespan. Early social experience predicts network centrality in a peer‐only group. Early social experience predicts network centrality in a peer‐only group. Maternal presence influences the impact of dominance rank on developing primates’ social network position. Maternal presence influences the impact of dominance rank on developing primates’ social network position.
... They responded most strongly to typical alarm barks, less strongly to intermediate alarm calls, still less strongly to intermediate contact barks, and hardly at all to typical contact barks (Fischer et al., 2000). There appears to be some flexibility, because infant vervet monkeys who were exposed to specific alarm calls frequently developed the appropriate response earlier than infants who were rarely exposed to it (Hauser, 1988). Furthermore, a study of the development of maternal recognition showed that, from as early as 10 weeks of age, Barbary macaque infants responded more strongly to playbacks of their mothers' calls than to playbacks of unrelated females from the same social group (Fischer, 2004). ...
Chapter
Humans have the capacity to transmit information via language as well as through extensive social learning, giving rise to cumulative culture. How does information flow among nonhuman primates and what does this tell us about the origins of culture? This chapter reviews two main modes of information transmission, namely signaling about events in the environment and social learning. While nonhuman primates use others as sources of information, there is little evidence for active alteration of others' knowledge states or skills indicating that the latter is a derived trait of our own species.
... However, species commonly expand their eavesdropping networks to heterospecifics that share similar resource requirements or are faced with common predators (Goodale et al., 2010;Shriner, 1998). In any system where two species share a common predator, and one produces a reliable warning signal detectable by the other species, eavesdropping should arise (Shriner, 1998;Hauser, 1988). Similarly, we would expect organisms to be selected to respond to the signals or cues of heterospecifics that are associated with resources relevant to an animal's fitness. ...
Article
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Organisms often eavesdrop on the cues and signals produced by other species to obtain information about their environment. Blue jays have dietary overlap with red squirrels, and learn to associate novel stimuli with food rewards in an experimental setting. Red squirrels produce "squeals" when contesting food resources with conspecifics. We tested whether blue jays eavesdrop on red squirrels by playing back red squirrel squeals, red squirrel rattles, white noise, and chick-a-dee calls to blue jays in Winnipeg, Manitoba. Additionally we examined the response of passerine birds in general to the playbacks, and attempted to condition free-living blue jays to respond to the playback of the squeal treatments. Results of the playbacks suggested that neither blue jays nor other passerines eavesdrop on vocalizations emitted in the context of red squirrel disputes over food. Conditioning trials did not produce any conditioned responses from blue jays; however, the limited number of trials performed does not constitute a robust test of the possible acquisition of a classically-conditioned response. Blue jays may also refrain from eavesdropping on red squirrel squeals as they are not reliable indicators of food resources, or because in an urban environment, blue jays readily learn the locations of bird feeders or other reliable food sources without eavesdropping on red squirrels.
... In other cases, listeners respond appropriately to calls that are acoustically different from their own (Templeton et al. 2005;Lea et al. 2008;Fallow and Magrath 2010), suggesting that responses are biologically rooted, or, in the case of species living in close territories, learned. For example, juvenile vervet monkeys' Cercopithecus aethiops pygerthyrus appropriate responses to playback of alarm calls given by superb starlings Spreo superbus vary depending on the rates of exposure to these alarm calls (Hauser 1988). Generally, the ability to respond appropriately to heterospecific calls, which may presuppose the ability to recognize their level of emotional arousal and valence (Mendl et al. 2010), is the result of a signaling system that affords interspecific beneficial outcomes in dangerous contexts. ...
Article
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The ability to identify emotional arousal in heterospecific vocalizations may facilitate behaviors that increase survival opportunities. Crucially, this ability may orient inter-species interactions, particularly between humans and other species. Research shows that humans identify emotional arousal in vocalizations across multiple species, such as cats, dogs and piglets. However, no previous study has addressed humans’ ability to identify emotional arousal in silver foxes. Here, we adopted low and high arousal calls emitted by three strains of silver fox - Tame, Aggressive and Unselected - in response to human approach. Tame and Aggressive foxes are genetically selected for friendly and attacking behaviors toward humans, respectively. Unselected foxes show aggressive and fearful behaviors toward humans. These three strains show similar levels of emotional arousal, but different levels of emotional valence in relation to humans. This emotional information is reflected in the acoustic features of the calls. Our data suggest that humans can identify high arousal calls of Aggressive and Unselected foxes, but not of Tame foxes. Further analyses revealed that, although within each strain different acoustic parameters affect human accuracy in identifying high arousal calls, spectral center of gravity, harmonic-to-noise ratio and F0 predict humans’ ability to discriminate high arousal calls and that spectral center of gravity across all strains. Furthermore, we identified in spectral center of gravity and fundamental frequency the best predictors for humans’ absolute ratings of arousal in each call. Implications for research on the adaptive value of interspecific eavesdropping are discussed.
... From an evolutionary standpoint, this perceptual ability provides a critical complement to the encoding of emotion in vocal production. Importantly, research suggests that animals actually use this information at a heterospecific level, integrating information gained from heterospecific vocalizations with information gained from conspecifics to determine appropriate behavioural reactions in response to potential environmental dangers [41][42][43][44][45]. Therefore, the investigation of vocal emotional communication in animals across all classes is key to enhance our understanding of the link between vocal signals and their adaptive nature, shedding light on the evolution of acoustic communication. ...
Article
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Writing over a century ago, Darwin hypothesized that vocal expression of emotion dates back to our earliest terrestrial ancestors. If this hypothesis is true, we should expect to find cross-species acoustic universals in emotional vocalizations. Studies suggest that acoustic attributes of aroused vocalizations are shared across many mammalian species, and that humans can use these attributes to infer emotional content. But do these acoustic attributes extend to non-mammalian vertebrates? In this study, we asked human participants to judge the emotional content of vocalizations of nine vertebrate species representing three different biological classes—Amphibia, Reptilia (non-aves and aves) and Mammalia. We found that humans are able to identify higher levels of arousal in vocalizations across all species. This result was consistent across different language groups (English, German and Mandarin native speakers), suggesting that this ability is biologically rooted in humans. Our findings indicate that h
... Interestingly, there are no convinc ing observations of such 'referential vocal signals' in any ape species, the closest possibility being the way chimpanzees adjust calling rate for food grunts used in the context of sharable and unsharable foods . In general, it may be said that the learning skills used in call compre hension show almost unlimited flexibility because a number of primate species can learn to effectively use the calls of other species, including some nonprimate species (Hauser, 1988;. ...
... Learning allows individuals to tailor their responses to the most relevant alarm calls in the current community (Nocera and Ratcliffe 2010), as well as to ignore non-alarm calls and the alarm calls of species that do not share similar predators (Magrath et al. 2009a). Studies of both geographic and temporal patterns of response to heterospecific alarm calls provide indirect but compelling evidence for learning (Hauser 1988 Himalayan bird communities respond more strongly to familiar than to unfamiliar heterospecific alarm calls, regardless of acoustic similarity (Wheatcroft and Price 2013); and fledgling white-browed scrubwrens, respond to aerial alarm calls of New Holland honeyeaters at a younger age where their territories overlap (Haff and Magrath 2013). Experimental evidence demonstrates that individuals can learn to respond to unfamiliar heterospecific alarm calls (Shriner 1999;Magrath et al. 2015b;Potvin et al. 2018;Dutour et al. 2019). ...
Chapter
Many birds and mammals give alarm calls when they detect predators or other threats, and these calls have been used as classic models for understanding signal design. Here we consider signal design and usage, and how individuals acquire and use information from the alarm calls of other species. Alarm calls often encode detailed information on danger, such as the type of predator, its current behavior, size, or proximity. Alarm calls are sometimes very similar among species or can share generic acoustic features, and both help to explain recognition of heterospecific alarms. However, alarm calls can vary greatly among species, and taxonomically widespread eavesdropping also requires learning the association between calls and danger. Once heterospecifics eavesdrop on alarm calls, there is potentially selection on callers to modify their alarm calls or usage. If callers benefit from eavesdroppers’ responses to their alarm calls, they may be selected to enhance signal efficacy, leading to interspecific communication and mutual benefit. Alternatively, callers can be selected to manipulate eavesdroppers, using deceptive signaling, including mimicry, causing the eavesdropper to suffer a cost. If callers suffer a cost from eavesdroppers’ responses, their signaling can be modified to make eavesdropping harder, leading to cue denial. Overall, alarm signals provide an insight into the evolution of signal design, and the complex flow of information within and among species in natural communities.
... It is unknown how much previous exposure is required to learn these associations, however superb fairy-wrens were able to learn the association between a novel sound and a predator model after only two days of exposure (Magrath et al. 2015b). Young vervet monkeys learn to respond to the mobbing alarm call of superb starlings Lamprotornis superbus quicker when starlings are more abundant (Hauser 1988), indicating that increased exposure is beneficial to learning. Although the presence of aerial threats and ensuing alarm calls by noisy miners has been witnessed at the location of this study (N. ...
Article
Alarm calls are vocalisations animals give in response to predators and mainly function to alert conspecifics of danger. Studies show that numerous species eavesdrop on the 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. This article is protected by copyright. All rights reserved.
... In the context of predation risk, warning of imminent danger is often made available to nearby individuals via visual (e.g., Caro 1986), auditory (e.g., Goodale & Kotagama 2008), or chemical (e.g., Blum 1985) alarm cues. Natural selection should favor interspecies eavesdropping on alarm cues for species that share the same predators and co-occur both spatially and temporally (Hauser 1988;Shriner 1998;Pays et al. 2014); such species are said to be are members of a 'prey guild' (Chivers et al. 1997). Most examples of cross-taxa detection of alarm cues occur within aggregates of similar species-e.g., schools of fish, choruses of frogs, flocks of birds (Mathis & Smith 1993;Phelps et al. 2007;Magrath et al. 2015). ...
Article
Many aquatic species produce chemical alarm cues that serve as a warning to nearby conspecifics. In mixed-species aggregations, individuals may also benefit by ‘eavesdropping’ on the chemical alarm cues of other species that are in the same prey guild. Rainbow Darters (Etheostoma caeruleum) are benthic fish that co-occur with native Ozark Minnows (Notropis nubilus), recently introduced Western Mosquitofish (Gambusia affinis), and native Oklahoma Salamanders (Eurycea tyrnerensis), all of whom are vulnerable to the same predators. We tested the responses of darters to the damage-released alarm cues of conspecifics (positive control), minnows, and mosquitofish; alarm cues from Bumblebee Gobies (Brachygobius doriae) served as a negative (allopatric) control. We also tested the response of sympatric and allopatric darters to the damage-released alarm cues of Oklahoma Salamander. Darters exhibited a fright response to conspecific and minnow alarm cues, but not to cues from mosquitofish or gobies. Lack of response to mosquitofish cues could be because they are introduced or because they typically occur higher in the water column than darters. Darters that were sympatric with the salamander exhibited a fright response to the alarm cues of the salamander, while allopatric darters did not. Rainbow Darters can develop responses to the alarm cues of syntopic species (minnows and Oklahoma Salamander) within their prey guild.
... Animals in natural communities gain information from members of other species facing similar ecological challenges [1][2][3][4][5], including many verte- brates that recognize the alarm calls of heterospe- cifics vulnerable to the same predators [6]. Learning is critical in explaining this widespread recognition [7][8][9][10][11][12][13], but there has been no test of the role of social learning in alarm-call recognition, despite the fact that it is predicted to be important in this context [14,15]. We show experimentally that wild superb fairy-wrens, Malurus cyaneus, learn socially to recognize new alarm calls and can do so through the previously undemonstrated mechanism of acoustic-acoustic association of unfamiliar with known alarm calls. ...
Article
Animals in natural communities gain information from members of other species facing similar ecological challenges [1-5], including many vertebrates that recognize the alarm calls of heterospecifics vulnerable to the same predators [6]. Learning is critical in explaining this widespread recognition [7-13], but there has been no test of the role of social learning in alarm-call recognition, despite the fact that it is predicted to be important in this context [14, 15]. We show experimentally that wild superb fairy-wrens, Malurus cyaneus, learn socially to recognize new alarm calls and can do so through the previously undemonstrated mechanism of acoustic-acoustic association of unfamiliar with known alarm calls. Birds were trained in the absence of any predator by broadcasting unfamiliar sounds, to which they did not originally flee, in combination with a chorus of conspecific and heterospecific aerial alarm calls (typically given to hawks in flight). The fairy-wrens responded to the new sounds after training, usually by fleeing to cover, and responded equally as strongly in repeated tests over a week. Control playbacks showed that the response was not due simply to greater wariness. Fairy-wrens therefore learnt to associate new calls with known alarm calls, without having to see the callers or a predator. This acoustic-acoustic association mechanism of social learning could result in the rapid spread of alarm-call recognition in natural communities, even when callers or predators are difficult to observe. Moreover, this mechanism offers potential for use in conservation by enhancing training of captive-bred individuals before release into the wild.
... Positive correlation between the rate of response development and the magnitude of exposure to heterospecific alarm calls suggests a learning process. For instance, infant vervet monkeys (Cercopithecus aethiops pygerythrus) develop responses to superb starling (Lamprotornis superbus) mobbing calls more quickly on territories where these birds are common, suggesting that these young have more opportunities to learn about the calls than young on territories where starlings are less common (Hauser 1988). Concerning adults, they can associate novel sounds with a chorus of conspecific and heterospecific aerial alarm calls (Potvin et al. 2018). ...
Article
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When they detect a predator, many species emit anti-predator vocalizations. In some cases, they emit mobbing calls, which are associated with the caller approaching and harassing the predator while attracting others to join it. Surprisingly, although mobbing has been widely reported in adults of numerous species, there has been no test of the role of learning in mobbing call recognition, especially during ontogeny. Here, we exposed wild great tit (Parus major) nestlings to playbacks of an unthreatening novel sound either associated with conspecific mobbing calls (experimental treatment) or with another unthreatening novel sound (control treatment). We then tested them as nestlings and fledglings to see how they respond to the novel sound compared to conspecific mobbing calls. Results revealed that fledglings in the experimental treatment behaved similarly to conspecific mobbing calls and the novel sound associated with conspecific mobbing calls. Because mobbing efficiency is often linked to interspecific communication, associative learning should be used by heterospecifics as mobbing calls recognition mechanism. Regardless of treatment during the nestling phase, fledglings always were sensitive to the playback of conspecific mobbing calls. However, fledglings from the control group were more likely to approach the loudspeaker than those from the experimental group when mobbing calls were played suggesting that overexposure during the nestling phase altered mobbing learning. Overall, these results suggest that learning could play a role in the recognition of calls, like heterospecific mobbing calls, when paired with conspecific mobbing, and that mobbing is perceived as a threatening stimulus from a very young age.
... Regarding the comprehension of calls and other sounds in the environment, it is highly adaptive for an animal to be able to use sounds as predictors of ongoing or upcoming events to adjust its responses accordingly [27][28][29] . Indeed, non-human primates are able to associate the alarm calls of other species with respective threatening situations 30,31 . Nevertheless, it remains unclear how much experience is necessary to establish such associations. ...
Article
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To evaluate the flexibility in vocal production and comprehension in a non-human primate, we presented a drone to West African green monkeys, Chlorocebus sabaeus. Calls given in response to the drone were clearly distinct from those given to other predators, but highly similar to the aerial alarm calls of the East African vervet monkey, Chlorocebuspygerythrus, suggesting that call structure is conserved. To probe how rapidly the animals attached meaning to the sound of the drone, we played back the drone sound after one to three exposures. Subjects immediately scanned the sky and ran for cover. In contrast to vocal production, comprehension learning was rapid and open-ended.
Article
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Numerical competence—the ability to represent, discriminate, and process numerical quantity information—is a widespread cognitive ability in animals that influences survival and reproductive success. Little is known about the role of numerical competence during predator mobbing—when a prey moves toward and harasses a predator. Since being in a larger group dilutes the risk of injury or death during a mobbing event and large groups are more efficient than small groups at repelling predators, the capacity to evaluate the number of mobbers before joining the mobbing flock may be highly beneficial for individuals. We tested whether the strength of the mobbing response of great tits (Parus major), a songbird that frequently mobs predators, is related to the number of callers. The minimum distance to the loudspeaker tended to be lower, and the number of calls produced by great tits was higher during playbacks simulating several callers than during the playbacks of one caller. These results suggest that numerical competence plays a central role during mobbing and that great tits reduce uncertainty of information by collating information from several individuals. We suggest further studies testing whether birds use individual vocal discrimination to assess the number of heterospecifics during mobbing. Significance statement Can animals count? Although historically the ability to count has distinguished humans apart from the rest of the animal kingdom, studies in the last decades have shown that numerical competence, the ability to represent, discriminate, and process numerical quantity information, is a widespread cognitive ability in animals. While this competence influences an individual’s survival success, little is known about the role of numerical competence during predator mobbing. Using a field-based playback experiment on a population of wild great tits (Parus major), we demonstrate that great tit responses to mobbing calls were affected by the number of individuals calling. The minimum distance to the loudspeaker tended to be lower and the number of calls produced by great tits tended to be higher during playbacks simulating multiple callers than during the playbacks of one caller. Thus, numerical assessments are used to decide whether or not to participate in mobbing responses.
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One can consider human language to be the Swiss army knife of the vast domain of animal communication. There is now growing evidence suggesting that this technology may have emerged from already operational material instead of being a sudden innovation. Sharing ideas and thoughts with conspecifics via language constitutes an amazing ability, but what value would it hold if our conspecifics were not first detected and recognized? Conspecific voice (CV) perception is fundamental to communication and widely shared across the animal kingdom. Two questions that arise then are: is this apparently shared ability reflected in common cerebral substrate? And, how has this substrate evolved? The paper addresses these questions by examining studies on the cerebral basis of CV perception in humans' closest relatives, non-human primates. Neuroimaging studies, in particular, suggest the existence of a ‘voice patch system’, a network of interconnected cortical areas that can provide a common template for the cerebral processing of CV in primates. This article is part of the theme issue ‘What can animal communication teach us about human language?’
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In four experiments conducted over a 6-year period, we investigated whether fathead minnows, Pimephales promelas, could acquire the ability to recognize chemical alarm cues of introduced brook stickleback, Culaea inconstans. A laboratory experiment documented that stickleback-naïve minnows did not exhibit an anti-predator response when exposed to the chemical alarm cues of stickleback. In a laboratory experiment conducted 5 years after the introduction of stickleback to the pond, minnows exhibited an antipredator response to stickleback cues. Moreover, in a field experiment the minnows exhibited avoidance of areas labelled with stickleback alarm cues. Minnows raised from eggs taken from the test pond did not exhibit an anti-predator response to stickleback cues while minnows from the test pond that had experience with stickleback cues did respond to stickleback cues. Our results provide clear evidence that cross-species responses to chemical alarm cues of fishes can be learned. Learned recognition of alarm cues has important implications for predator/prey interactions.
Article
Many nestling birds go silent in response to parental alarm calls, potentially lowering their risk of being overheard by predators. Parents are not always nearby, however, and so offspring could also benefit if they respond to the alarm calls of other species. Response could be innate, particularly if heterospecific alarm calls are acoustically similar to conspecific alarms, or learned through experience or association with parental behaviour. We investigated the responses of both young (5-6 days old) and older (10-11 days old, close to fledging) nestling white-browed scrubwrens, Sericornis frontalis, to the mobbing alarm calls of three heterospecifics whose nests are vulnerable to similar predators. Brown thornbills, Acanthiza pusilla, produce the most similar alarm calls to scrubwrens, while superb fairy-wren, Malurus cyaneus, and New Holland honeyeater, Phylidonyris novaehollandiae, produce alarm calls that are distinct. Heterospecific mobbing assays demonstrated that nestlings were likely to overhear the alarm calls of all three species. In support of innate response, even young nestlings suppressed calling after hearing both thornbill and parental alarms. However, young nestlings ignored or increased calling to fairy-wren and honeyeater alarms. Older nestlings continued to suppress calling to thornbill and parental alarm calls, but also suppressed calling to honeyeater and fairy-wren alarms, suggesting that they could have learnt to recognize those calls. This study thus demonstrates that nestlings can respond to the alarm calls of other species, and that these responses are likely to be enabled through both innate mechanisms and learning.
Chapter
Nicht nur Menschen, auch Tiere kommunizieren. Und dennoch: die Sprache unterscheidet den Menschen vom Tier, wie der aufrechte Gang, einige anatomische Aspekte des Aufbaus der Hand und der konventionelle Gebrauch von Werkzeugen. Die evolutionäre Anthropologie ist ein Paradigma, welches das menschliche Verhalten aus der evolutionären Perspektive zu verstehen versucht. Ziel ist es, auf der Basis von vergleichender Forschung diejenigen Aspekte des menschlichen Verhaltens herauszukristallisieren, die auch bei Tieren zu finden sind, respektive, die im Tierreich nicht zu finden und somit spezifisch für den Menschen sind.
Book
Man the Hunted argues that primates, including the earliest members of the human family, have evolved as the prey of any number of predators, including wild cats and dogs, hyenas, snakes, crocodiles, and even birds. The authors’ studies of predators on monkeys and apes are supplemented here with the observations of naturalists in the field and revealing interpretations of the fossil record. Eyewitness accounts of the ‘man the hunted’ drama being played out even now give vivid evidence of its prehistoric significance. This provocative view of human evolution suggests that countless adaptations that have allowed our species to survive (from larger brains to speech), stem from a considerably more vulnerable position on the food chain than we might like to imagine. The myth of early humans as fearless hunters dominating the earth obscures our origins as just one of many species that had to be cautious, depend on other group members, communicate danger, and come to terms with being merely one cog in the complex cycle of life.
Article
The question: are humans the only animals endowed with language? must be preceded by the question: what makes language a unique communication system? The American linguist Charles F. Hockett answers the second question by listing what he considers the criteria that differentiate language from other communication systems. His ‘design-feature’ approach, first presented in 1958, has become a popular tool by which the communication systems of non-human animals are guaranteed a priori exclusion from the notion of language. However, the results of interspecific communication research and the discovery of language-like qualities in the natural communication systems of non-human animals (as opposed to the artificial systems devised to further language research) demonstrate that language capabilities have evolved in parallel in many species. Thus Hockett’s approach is thoroughly undermined, and in need of revision. The more fundamental question that must be faced by the design-feature approach is: are its features essential for language as a distinct and vivid phenomenon, or merely applied to language as an object of linguistic investigation? This paper offers a detailed overview of Hockett’s design-features and emphasizes the problematic nature of certain characteristics. Following Slobodchikoff and Segerdahl et al., the paper shows that language cannot be defined as an exclusive quality of a single species.
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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.
Thesis
Belugas (Delphinapterus leucas) are highly vocal cetaceans, but the function of their calls, repertoire ontogeny, and role of learning in vocal behavior are poorly understood. This dissertation examines these issues, focusing on a captive beluga group at the Vancouver Aquarium. First, I investigated vocal development in a beluga calf, longitudinally throughout his first year of life, and later opportunistically. The first sounds after birth were low energy, broadband pulse-trains, which increased in pulse repetition rate with age. He incorporated rudimentary whistles at two weeks. His mixed calls, which became consistent at four months, became progressively stereotyped, increasingly like his mother’s “Type-A” call, a presumed contact call. Six months after he was first exposed to his father’s calls, he developed a call type similar to one of his father’s. I discuss these findings in light of theories of sound production mechanisms, developmental stages of vocal acquisition, and vocal learning. Secondly, I examined context-specific use of call types recorded from the beluga group, with particular focus on the Type-A call. This signal constituted 24-97% of the vocalizations during isolation, births, deaths, presence of external stressors, and re-union of animals after separation. In contrast, it represented 4.4% of the vocalizations during regular sessions. I identified five Type-A variants subjectively and quantitatively. I used these findings to generate hypotheses about the usage of these signals by wild belugas, verified the existence of A-calls in the repertoire of St. Lawrence herds, and documented their usage by two wild individuals from different populations in contexts that supported their contact function. Finally, I investigated contextual vocal learning in trained tasks in adult belugas, focusing on the ability of a female beluga to respond to playbacks of two categories of beluga calls with matching vocalizations; pulse-trains are a natural category, and screams an artificial class shaped by training. The subject successfully matched only pulse-trains, the class that is part of this species’ natural repertoire. Her poor performance on matching screams might be partly explained by a difficulty to perceive categorically a signal that lacks a function in the natural repertoire of belugas.
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Urban animals and birds in particular are able to cope with diverse novel threats in a city environment such as avoiding novel, unfamiliar predators. Predator avoidance often includes alarm signals that can be used also by hetero-specifics, which is mainly the case in mixed-species flocks. It can also occur when species do not form flocks but co-occur together. In this study we tested whether urban crows use alarm calls of conspecifics and hetero-specifics (jackdaws, Corvus monedula) differently in a predator and a non-predator context with partly novel and unfamiliar zoo animal species. Birds were tested at the Tiergarten Schönbrunn in the city of Vienna by playing back con- and hetero-specific alarm calls and control stimuli (great tit song and no stimuli) at predator (wolf, polar bear) and non-predator (eland antelope and cranes, peccaries) enclosures. We recorded responses of crows as the percentage of birds flying away after hearing the playback (out of those present before the playback) and as the number of vocalizations given by the present birds. A significantly higher percentage of crows flew away after hearing either con- or hetero-specific alarm calls, but it did not significantly differ between the predator and the non-predator context. Crows treated jackdaw calls just as crow calls, indicating that they make proper use of hetero-specific alarm calls. Responding similarly in both contexts may suggest that the crows were uncertain about the threat a particular zoo animal represents and were generally cautious. In the predator context, however, a high percentage of crows also flew away upon hearing the great tit control song which suggests that they may still evaluate those species which occasionally killed crows as more dangerous and respond to any conspicuous sound.
Chapter
To shed light on the evolution of human language, many studies have been made on the vocal communication of nonhuman primates. These studies have revealed that some rudimentary properties of human language can be seen in nonhuman primate vocal communication. In particular, much knowledge about the natural vocal communication of primates has accumulated since the method of playback experiments was established. For example, referential signaling (Zuberbuhler et al. 1999), categorical perception of vocalization (Masataka 1983), acoustic “rules” regulating vocal exchange (Sugiura 1993), and flexibility of vocal production (Sugiura 1998) have been found in some primate species in natural habitats. However, most of these studies have been conducted on the anthropoid primates. There have been relatively few studies on vocal communication in prosimians, including the lemurs of Madagascar, which are indigenous to the island and have evolved separately. Because of their uniqueness, the lemurs are important species as subjects for comparative studies of primate vocal communication.
Article
Aspects of the ecology of vervet monkeys (Ceropithecus aethiops) are described on the basis of a 21 month field study in East Africa. Analysis of home range utilization demonstrated differences between 4 groups. The smallest group distributed its time over a greater area than did the other groups. For 3 of the groups there appeared to be a strong relationship between group size and the amount of optimal habitat defended. The smallest group defended more optimal habitat than expected. However, this same group spent only 60% of its time in this habitat, whereas the other groups all spent more than 95% of their time in it. The smallest group may have avoided the optimal habitat of its territory as an area of frequent intergroup aggression, and as a result utilized a larger and less productive area. Sleeping-tree preferences of groups and individuals are described and discussed. The minimal distance traveled each day by vervet groups varied from 148 to 2,797 yd. In comparing the mean daily distance covered by 2 groups of equal size it was found that one moved significantly further than the other. More trips were made to permanent water holes between 1300 and 1500 hr and during the dry season than at other times. The frequency of group progressions was greatest at 0700 to 1000 and 1600 to 1900 hr. Study of food habits shows that they were opportunistic omnivores. Elephants were the greatest food competitors of the vervets. The monkeys had at least 16 potential predators. Outside of parks and reserves the greatest predator was the European commercial trapper. Ecological characteristics of vervets and their niche separation from baboons are discussed.
Article
The social knowledge of East African vervet monkeys is striking. Within a local population the monkeys recognize individuals, and associate each individual with its particular group. Within groups, the monkeys recognize dominance relations, rank orders, and matrilineal kinship, and they remember who has behaved affinitively towards them in the past. Outside the social domain, however, vervets appear to know surprisingly little about other aspects of their environment. Although they do distinguish the different alarm calls given by birds, vervets do not seem to recognize the fresh tracks of a python, or indirect evidence that a leopard is nearby. Similarly, although cooperation and reciprocity seem common in social interactions, comparable behaviour has apparently not evolved to deal with ecological problems. Results support the view that primate intelligence has evolved mainly to solve social problems. As a result, vervet monkeys make excellent primatologists but poor naturalists.
Article
The predator-evoked calling of California ground squirrels (Spermophilus beecheyi) was studied in the field during the reproductive season. Three different sources of data indicated that adults call more after, than before their young have reached the age of first emergence from natal burrows. During exposure to a tethered rattlesnake (Crotalus viridis oreganus) and to a freely-moving dog (Canis familiaris), and in natural encounters with a coyote (Canis latrans) or bobcat (Lynx rufus), calling was more frequent after than before young first emerged. We concluded that California ground squirrels call in order to warn their offspring about predators, like other ground squirrel species do. In order to see the increase in mammalian predator evoked calling after pup emergence, we had to separate calling on the basis of its temporal organization. Nonrepetitive calling involved spacing a few vocalizations irregularly in time. Calls patterned in this way were more common early in an encounter, became more frequent after pup emergence, and more consistently elicited immediate reactions. Such calling was probably used to warn pups. Repetitive calling comprised rhythmic emission of a series of vocalizations. Calls organized repetitively were more common later in an encounter, were not emitted more frequently after pup emergence, and less consistently evoked immediate reactions. These and other differences between the two temporal patterns of vocalizing led us to propose that repetitive calling represented a
Article
Seven major types of sampling for observational studies of social behavior have been found in the literature. These methods differ considerably in their suitability for providing unbiased data of various kinds. Below is a summary of the major recommended uses of each technique: In this paper, I have tried to point out the major strengths and weaknesses of each sampling method. Some methods are intrinsically biased with respect to many variables, others to fewer. In choosing a sampling method the main question is whether the procedure results in a biased sample of the variables under study. A method can produce a biased sample directly, as a result of intrinsic bias with respect to a study variable, or secondarily due to some degree of dependence (correlation) between the study variable and a directly-biased variable. In order to choose a sampling technique, the observer needs to consider carefully the characteristics of behavior and social interactions that are relevant to the study population and the research questions at hand. In most studies one will not have adequate empirical knowledge of the dependencies between relevant variables. Under the circumstances, the observer should avoid intrinsic biases to whatever extent possible, in particular those that direcly affect the variables under study. Finally, it will often be possible to use more than one sampling method in a study. Such samples can be taken successively or, under favorable conditions, even concurrently. For example, we have found it possible to take Instantaneous Samples of the identities and distances of nearest neighbors of a focal individual at five or ten minute intervals during Focal-Animal (behavior) Samples on that individual. Often during Focal-Animal Sampling one can also record All Occurrences of Some Behaviors, for the whole social group, for categories of conspicuous behavior, such as predation, intergroup contact, drinking, and so on. The extent to which concurrent multiple sampling is feasible will depend very much on the behavior categories and rate of occurrence, the observational conditions, etc. Where feasible, such multiple sampling can greatly aid in the efficient use of research time.
Article
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.
Article
I. 7 vocalizations emitted in the predator context are defined in terms of their function. The physical and physiological constraints on the evolution of the physical structure of alarm calls with respect to detectability and localizability are discussed. Detection of various calls depends on signal amplitude, environmental attenuation, signal-to-noise ratio, discrimination of the receiver against background noise, and absolute auditory sensitivity of the receiver. The combined effect of these factors is discussed for an exemplary predator-prey system, in which the hearing of both, predator and prey is known. Localizability of an alarm call is determined by its frequency, bandwidth, and possibly its amplitude relative to the auditory threshold of the receiver. Crude differentiation between localizable and non-localizable signals is not possible, and localizability of particular sounds varies between species. In some cases the question of detectability may render the problem of localizability unimportant. Besides detectability and localizability, other factors such as the acoustic background formed by the alarm calls of sympatric species and by the species' own repertoire of calls are discussed. II. Requisite conditions and available evidence for the evolution of alarm calls through individual selection and kin selection are described. Five types of alarm calls are discussed individually: Although the different functions of various alarm calls are treated individually, certain of the calls may have more than one function and may be employed in nonpredator contexts as well.
Article
Adult vervet monkeys effectively classify animals in the world around them by giving alarm calls to some species but not to others, and by giving acoustically different alarms to leopards, martial eagles, pythons, and baboons. When compared to adults, infant vervet monkeys give alarm calls to a significantly wider variety of species. Even for infants, however, the relation between eliciting stimulus and alarm call type is not arbitrary. Infants restrict leopard alarms to terrestrial mammals, eagle alarms to birds, snake alarms to snakes, and baboon alarms to baboons. The mechanisms by which infants come, during development, to sharpen the association between predator species and alarm call type are discussed.
Article
When a complement of vertebrate predators was exposed in an experimental field situation to a Batesian mimicry system involving the tenebrionid beetle Eleodes longicollis as the noxious model, and the cerambycid beetle, Moneilema appressum as the edible mimic, the predator complement quickly became conditioned to avoid both models and mimics. Meanwhile, predation on familiar prey (the scarab beetle Polyphilla decemlineata) remained high, indicating that the experimental design did not prevent the predators from eating acceptable prey. Models and mimics were individually placed at risk in plastic buckets in a proportion of six: one; approximately the same proportions that they are found in the field. The model-mimic system was initially sampled by the predators at a relatively high rate, but sampling dropped off within 4 days of exposure of the models and mimics to predation risk. By day 4 of the experiments, sampling had ceased. During the sampling period, models and mimics were eaten in the same proportions as they occurred in the field, suggesting that the predators did not discriminate between the edible mimic and the noxious model. These results suggest that the selective advantage of mimicry may be very high if the model is noxious enough and the predator complement is not able to distinguish between the model and the mimic.
Article
Playback experiments were conducted of five groups of free-ranging vervet monkeys (Cercopithecus aethiops) to determine whether an adult male's responsiveness to infant distress calls was a function of (1) paternal certainty, (2) dominance rank, (3) predator presence, (4) number of males, (5) number of infants, (6) infant's mother's rank and/or (7) infant's age. Results from these experiments reveal that paternal certainty was the only factor that could directly explain the differences between males in the duration of response to distress calls.
Article
Dwarf mongooses in the Taru desert region of Kenya form foraging communities with a variety of endemic bird species, especially hornbills. The prey spectra of the mongooses and hornbills overlap almost completely. For the other bird species forming the foraging community only partial overlap exists. The association between the birds and mongooses is actively sought by both parties. The birds wait in tress around the termite mound where the monogooses are sleeping for them to emerge and the mongooses delay their foraging departure if no birds are present. There is a positive relationship between the number of mongooses in the group and the number of birds accompanying them. A true mutualism only exists between the mongooses and the two hornbill species Tockus deckeni and T. flavirostris since their presence or arrival affects the subsequent start of foraging. These two hornbill species have also been observed to influence the start of foraging actively by means of two behaviour patterns termed chivvying and waking. Both the mongooses and birds are exposed to a high predator pressure from raptors with an overlap in the birds of prey predating the various species. This predator pressure is counteracted behaviourally by the mongooses by means of an altruistic behaviour pattern, guarding. Both mongooses and birds warn vocally and flee when a raptor is sighted. The mongooses modify their guarding behaviour to compensate for the warning behaviour of the birds in two ways: (a) fewer mongooses guard when large numbers of birds are present and vice versa, (b) the frequency of the mongooses' intraspecific warning calls is significantly reduced in cases where birds are present in comparison with those where they are absent. The birds also sight and respond to the raptor first on significantly more occasions than the mongooses. In addition, the birds also warn for raptor species which do not predate them but which are mongoose predators, not, however, for raptors which are not mongoose predators. This mutualistic association with its high degree of compensatory behaviour by both parties appears to be unique for free-living vertebrates and has its closest parallel in the trophobiosis described for ants and aphids.
Article
Belding's ground squirrels (Spermophilus beldingi) give acoustically distinct alarm calls to aerial and terrestrial predators. The animals typically give multiple-note trills to predatory mammals, and single-note whistles to flying hawks. During a 9-year study of free-living S. beldingi at Tioga Pass, California, the adaptive significance of the whistle call was investigated. Data were gathered on 664 ground squirrel-hawk interactions, most of which were induced by flying trained raptors over individually marked study animals of known sex and age. The sight of a flying hawk and the sound of whistles stimulated widespread calling and running to shelter by the ground squirrels (Fig. 1). Wild raptors were rarely successful at capturing the rodents once a whistle had been given, and fewer callers than noncallers were killed (Table 1). Individuals of both sexes and all ages whistled equally often (Fig. 4), and females' tendencies to whistle were not affected by the presence of relatives, including offspring (Fig. 5). The most frequent callers were animals in exposed positions: far from cover and close to the predatory bird (Table 2). Taken together the data suggest that unlike trills, which increase vulnerability to terrestrial predators (Table 1) and function to warn relatives, whistle directly benefit callers by increasing their chances of escaping from hawks.
Article
The Gurtin and Levine model5 is studied in this paper under the assumption that the fecundity of prey depends on age as well as on the total population sizes of prey and predators. The purpose of this study is to see the effect of this density dependence on the stability criteria for the equilibria of the model equations. It is shown that there are cases when, due to density dependence, the model which is originally neutrally stable becomes stable.
Article
Vervet monkeys (Cercopithecus aethiops) at Amboseli, Kenya, give acoustically different alarm calls to different predators. Each alarm evokes contrasting, seemingly adaptive, responses. Animals on the ground respond to leopard alarms by running into trees, to eagle alarms by looking up, and to snake alarms by looking down. In a 14-month field study examining the semantic properties of alarm calls, we played tape-recorded alarms to vervets in the absence of actual predators and filmed the monkeys' responses. Playbacks confirmed observations and showed that (1) alarm length, amplitude and alarmist's age/sex class had little effect on response quality, and (2) context was not a systematic determinant of response. We conclude that vervet alarm calls function to designate different classes of external danger.
Article
Eleven, non-mutually exclusive hypotheses have been proposed for the function of stotting. After, examining the possible time, energy and survivorship costs of stotting, I review each hypothesis in turn, discussing theoretical objections to them and data that are found to support each one. The Pursuit Invitation hypothesis, Pursuit Deterrence hypothesis, Confusion Effect hypothesis and Stotting-as-play hypothesis are unlikely to be correct on theoretical grounds. There are too few data to support or refute a startle effect of stotting, prey signalling its health, the Social Cohesion hypothesis or alarm function of stotting but all require caveats concerning design features or costs of stotting in order to be strong candidates. There are insufficient data to determine the merits of the Anti-ambush hypothesis of stotting or whether it attracts a mother to her fawn. Circumstantial evidence indicates that mothers may invite predators to pursue them instead of their fawns. The Predator Detection hypothesis remains the strongest candidate for the function of stotting and this is supported by evidence concerning related forms of antipredator behaviour. For each hypothesis, predictions are made concerning the stotting individual, its conspecifics, and the predator.
Article
Observations and playback experiments were used to study the development of grunts and alarm calls among free-ranging vervet monkeys. Results indicate that the production of vocalizations, their use in appropriate circumstances, and the response to the vocalizations of others emerge gradually during an individual's first 4 years. Particularly in the case of grunts, different acoustic components develop at different rates. Immatures respond appropriately to the calls of others before they produce appropriate vocalizations themselves. Finally, immature vocal development may be aided by cues received from adults. If an infant gives an alarm call to a genuine predator (as opposed to a non-predator), adults respond more strongly. When infants hear a playback of an alarm, they are more likely to respond appropriately if they first look at an adult.
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Updated and corrected, 2010
Article
Thesis (Ph. D.)--University of California, Los Angeles, 1987. Vita. Includes bibliographies.
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