Predatory attack on a bearded capuchin monkey by a Boa constrictor

Habitats with spatial variation in food availability, predation risk, and hunting pressure allow us to study how animals resolve the trade-off between food searching and predator avoidance. We investigated the influence of food availability, predation risk, and the perceived predation risk on habitat use by a primate living under high hunting pressure, the yellow-breasted capuchin monkeys, Sapajus xanthosternos, at Una Biological Reserve (ReBio Una). We hypothesized that the hunting pressure occurring in the capuchins' home range would favor predator avoidance to the detriment of searching for food. We characterized a set of covariates related to resource availability (fruit and invertebrate biomasses, feeding on dispersed and clumped food items, sleeping sites), perceived predation risk (alarm calls given to terrestrial and aerial predators, silent group movement, and vigilance behavior), and actual predation risk (evidence of hunting) and estimated their effects on how one group of capuchin monkeys uses its habitat. The group divides its time among three major forest types within their home range: agroforest, mature, and secondary. Our results suggest that the actual and perceived risk of hunting by humans, as well as the perceived predation risk by both terrestrial and aerial predators, were significant determinants of capuchin monkeys' space use. Yellow-breasted capuchin monkeys' space use was negatively related to the risk of hunting by humans (actual evidence and silent behavior), the perceived risk of predation by both aerial and terrestrial predators, and the presence of sleeping sites. Capuchin monkeys' use of space was not related to the biomass of fruits in the habitat, and the biomass of invertebrates had a very low positive effect. We confirmed our prediction that in a habitat with high hunting pressure, the risk of predation, both perceived and actual, had a more significant impact on how yellow-breasted capuchins used space than did food availability.

Young animals are known to direct alarm calls at a wider range of species than adults. Our field study examined age-related differences in the snake-directed antipredator behavior of infant, juvenile, and adult white-faced capuchin monkeys (Cebus capucinus) in terms of alarm calling, looking behavior, and aggressive behavior. In the first experiment, we exposed infant and juvenile white-faced capuchins to realistic-looking inflatable models of their two snake predators, the boa constrictior (Boa constrictor) and neotropical rattlesnake (Crotalus durissus) and a white airplane as a novel control. In the second experiment, infants, juveniles, and adults were presented photographic models of a coiled boa constrictor, rattlesnake, indigo snake (Drymarchon corais), a noncapuchin predator, and a white snake-like model. We found that antipredator behavior changed during the immature stage. Infants as young as 4 months old were able to recognize snakes and display antipredator behavior, but engaged in less snake-model discrimination than juveniles. All age classes exhibited a lower response to the white snake-like model, indicating that the absence of color and snake-scale patterns affected snake recognition. Infants also showed a higher level of vigilance after snake-model detection as exhibited by a higher proportion of time spent looking and head cocking at the models. Aggressive antipredator behavior was found in all age classes, but was more prevalent in juveniles and adults than infants. This study adds to the knowledge of development of antipredator behavior in primates by showing that, although alarm calling behavior and predator recognition appear at a very young age in capuchins, snake-species discrimination does not become apparent until the juvenile stage.

Inter‐ and intraspecific variation in alarm calls were compared for two species of free‐ranging capuchin monkey: the wedge‐capped capuchin (Cebus olivaceus) and the white‐faced capuchin (Cebus capuchinus). Alarm calls in each case were made in the presence of the same predator, a boa constrictor. Vocalizations (n=40) were compared for commonly examined acoustic parameters (e.g., signal duration, frequency, and amplitude variables), as well as for vocal features found to be acoustic cues to the monkeys [e.g., bandwidth of dominant formant; change in frequency of the dominant formant (see Norris, 4aAB3)]. Additionally, correlations of spectrograms were performed using CANARY. Interspecific variability was found to be significantly greater than intraspecific variability for signal duration (F=45.30;p<0.0001), maximum frequency (F=8.52; p<0.0059), and formant number (F=10.32;p<0.0027). However, interspecific variability of calls was not significant for any of the acoustic parameters found to be used as perceptual cues for the two species. The evolutionary and ecological significance of these findings will be discussed.

Alarm calls of white-faced capuchin monkeys: an acoustic analysis

The apicomplexan parasite Toxoplasma gondii (T. gondii) has been found in more than 350 species of homoeothermic vertebrates in diverse climates and geographic areas. In most animals, T. gondii produces mild or asymptomatic infection. However, acute and hyperacute toxoplasmosis is associated with high mortality rates observed in Neotropical primates (NP) in captivity. These primates are distributed in 20 countries across the Americas, and although infection has been reported in certain countries and species, toxoplasmosis in the wild and its impact on NP population survival is unknown. Differences among species in exposure rates and disease susceptibility may be due in part to differences in host behavior and ecology. Four species of NP are found in Costa Rica, i.e., howler (Alouatta palliata), spider (Ateles geoffroyi), capuchin (Cebus imitator), and squirrel monkeys (Saimiri oerstedii). This study reports NP exposure to T. gondii using the modified agglutination test in 245 serum samples of NP (198 wild and 47 from captivity) from Costa Rica. Associations of serostatus with environmental (forest cover, annual mean temperature), anthropogenic (human population density), and biological (sex) variables in howler and capuchin monkeys were evaluated. The seroprevalence among wild NP was 11.6% (95% CI = 7.7–17.34), compared with 60% in captive monkeys (95% CI = 44.27–73.63), with significant differences between species (X2 = 20.072; df = 3, p = 0.000164), suggesting an effect of behavior and ecology. In general, antibody titers were low for wild NP (<1:128) and high for captive NP (>1:8192), suggesting higher exposure due to management factors and increased life span in captivity. Seropositivity in howler monkeys was positively related to forest cover and inversely related to annual rainfall. For capuchins, annual rainfall was inversely related to seropositivity. Surveillance of T. gondii exposure in NP in captivity and in the wild is required to understand drivers of the infection and develop novel strategies to protect them.

In many primates, the acoustic properties of alarm calls can provide information on the level of perceived predatory threat as well as influence the antipredator behavior of nearby conspecifics. The present study examined the harmonics-to-noise ratio (tonality of spectral structure) of alarm calls emitted by white-faced capuchin monkeys (Cebus capucinus) in trees directed at photographic models of a boa constrictor, neotropical rattlesnake, scorpion eater snake, and white snake-shaped control presented on the ground. The average and peak harmonics-to-noise ratios of initial alarm calls by infants, juveniles, and adults and those of nearby second callers were analyzed using PRAAT software. Averaged for age class, the peak harmonics-to-noise ratio of alarm calls directed at the boa constrictor model, characterizing a primary capuchin predator, was reliably higher than the peak harmonics-to-noise ratio of alarm calls directed at the harmless scorpion eater model. This effect was influenced by the higher harmonics-to-noise ratio of infant alarm calls and it disconfirmed our prediction, based on primate vocalization research, that snake perception would increase arousal and alarm-call noisiness. Levels of call tonality did not distinguish the boa and rattlesnake or rattlesnake and scorpion eater models for any age class. Higher alarm-call tonality appeared contagious to nearby perceivers, with focal alarm calling influencing the level of tonality of the first calls of second callers. Together, these findings suggest that the higher peak harmonics-to-noise ratio of capuchin alarm calling directed at snakes is contagious and possibly conveys information about the level of perceived predatory threat.

Animals should continuously assess the threat of predation. Alarm calls inform on predation risk and are often used as cues to shape behavioural responses in birds and mammals. Hitherto, however, the ecological consequences of alarm calls in terms of organization of animal communities have been neglected. Here, we show experimentally that calls of a resident nocturnal raptor, the little owl Athene noctua, triggered a response in terms of breeding habitat selection and investment in current reproduction in conspecifics and heterospecifics. Little owls preferred to settle in territories where calls of conspecifics, irrespective of their type (i.e. alarm versus contact calls), were broadcasted, indicating that either conspecific attraction exists or calls are interpreted as foreign calls, eliciting settlement as a mode of defence against competitors. Also, we found that little owls seemed to invest more in current reproduction in safe territories as revealed by conspecific calls. Innovatively, we reported that a second owl species, the migratory scops owl Otus scops, preferred to breed in safe territories as indicated by little owls' calls. These results evidence that the emission of alarm calls may have, apart from well-known behavioural effects, ecological consequences in natural communities by inducing species-specific biases in breeding habitat selection. This study demonstrates a previously unsuspected informative role of avian alarm calls which may modulate the spatial structure of species within communities.

Young animals are known to direct alarm calls at a wider range of animals than adults. If social cues are safer and/or more reliable to use than asocial cues for learning about predators, then it is expected that the development of this behavior will be affected by the social environment. Our study examined the influence of the social environment on antipredator behavior in infant, juvenile, and adult wild white-faced capuchin monkeys (Cebus capucinus) at Lomas Barbudal Biological Reserve in Costa Rica during presentations of different species of model snakes and novel models. We examined (a) the alarm calling behavior of the focal animal when alone versus in the vicinity of conspecific alarm callers and (b) the latency of conspecifics to alarm call once the focal animal alarm called. Focal animals alarm called more when alone than after hearing a conspecific alarm call. No reliable differences were found in the latencies of conspecifics to alarm call based on age or model type. Conspecifics were more likely to alarm call when focal individuals alarm called at snake models than when they alarm called at novel models. Results indicate (a) that alarm calling may serve to attract others to the predator's location and (b) that learning about specific predators may begin with a generalized response to a wide variety of species, including some nonthreatening ones, that is winnowed down via Pavlovian conditioned inhibition into a response directed toward specific dangerous species. This study reveals that conspecifics play a role in the development of antipredator behavior in white-faced capuchins.

A long‐standing question in animal communication is whether signals reveal intrinsic properties of the signaller or extrinsic properties of its environment. Alarm calls, one of the most conspicuous components of antipredator behaviour, intuitively would appear to reflect internal states of the signaller. Pioneering research in primates and fowl, however, demonstrated that signallers may produce unique alarm calls during encounters with different types of predators, suggesting that signallers through selective production of alarm calls provide to conspecific receivers information about predators in the environment. In this article, we review evidence for such ‘functional reference’ in the alarm calls of birds based on explicit tests of two criteria proposed in Macedonia &amp; Evans’ (Ethology 93, 1993, 177) influential conceptual framework: (1) that unique alarm calls are given to specific predator categories, and (2) that alarm calls isolated from contextual information elicit antipredator responses from receivers similar to those produced during actual predator encounters. Despite the importance of research on birds in development of the conceptual framework and the ubiquity of alarm calls in birds, evidence for functionally referential alarm calls in this clade is limited to six species. In these species, alarm calls are associated with the type of predator encountered as well as variation in hunting behaviour; with defence of reproductive effort in addition to predators of adults; with age‐related changes in predation risk; and with strong fitness benefits. Our review likely underestimates the occurrence of functional reference in avian alarm calls, as incomplete application and testing of the conceptual framework has limited our understanding. Throughout, therefore, we suggest avian taxa for future studies, as well as additional questions and experimental approaches that would strengthen our understanding of the meaning of functional reference in avian alarm calls.

Vocally signaling a predator’s presence through alarm calls creates public information regarding risk in the environment. If having this information confers an advantage, eavesdropping behavior, the use of information in signals by individuals other than the primary target, is expected to evolve. Thus, eavesdropping for information on predation risk to avoid predators may be common. We describe the first study to quantify an effect of avian alarm calling on the perceived cost of predation in a mammalian receiver/eavesdropper using the eastern tufted titmouse–eastern chipmunk dyad. We used the technique of giving-up densities to quantify changes in chipmunks’ perceived risk of predation while foraging under experimental playbacks of titmouse vocalizations (seet, mobbing, and contact calls), hawk calls, and wood thrush song (control). Titmouse mobbing calls significantly increased chipmunk’s perceived risk of predation. Chipmunks also appeared to divert attention (i.e., cost of multitasking) to monitoring alarm call playbacks/assessing predation risk as shown by the absence of density-dependent foraging. In contrast, when foraging during hawk calls (a direct cue of predation risk), chipmunks showed no differences in foraging relative to controls. These results support other published studies that prey respond more strongly to indirect source of information about predation risk than to direct sources. Key words: alarm calls, eastern tufted titmouse, eavesdropping, information, predation risk. [Behav Ecol]

Alarm calls produced by basal prey have a well-known informative value. In multi-predator communities, mesopredators, when faced with top predators, may emit alarm calls that could inform basal prey about their lowered predation risk. To test this unexplored possibility, we conducted one field and one mesocosm experiment in which we simulated alarm and non-alarm calls from little owls (Athene noctua) as mesopredators and measured their effects on grasshoppers as prey of little owls but not of top predators. In the field experiment, we found that grasshopper species were significantly more abundant in patches where we simulated either the presence of scared little owls (alarm treatment) or no owls (control treatment) compared to patches where the presence of non-scared little owls (non-alarm treatment) was simulated. In the mesocosm experiment, locusts (Locusta migratoria) moved significantly more to exposed areas when we simulated the presence of scared little owls (alarm treatment) or of a granivorous bird (control treatment), while they moved to sheltered areas when we simulated the presence of non-scared owls (non-alarm treatment). These results show that prey could cue on predators' calls to assess their predation risk and make decisions, revealing unprecedented potential ecological consequences of alarm calls in invertebrate communities.

Nepotistic alarm calling in the Siberian jay, Perisoreus infaustus

Many mammalian and avian species produce conspicuous vocalizations upon encountering a predator, but vary their calling based on risk urgency and/or predator type. Calls falling into the latter category are termed “functionally referential” if they also elicit predator-appropriate reactions in listeners. Functionally referential alarm calling has been well documented in a number of Old World monkeys and lemurs, but evidence among Neotropical primates is limited. This study investigates the alarm call system of tufted capuchin monkeys (Cebus apella nigritus) by examining responses to predator and snake decoys encountered at various distances (reflecting differences in risk urgency). Observations in natural situations were conducted to determine if predator-associated calls were given in additional contexts. Results indicate the use of three call types. “Barks” are elicited exclusively by aerial threats, but the call most commonly given to terrestrial threats (the “hiccup”) is given in nonpredatory contexts. The rate in which this latter call is produced reflects risk urgency. Playbacks of these two call types indicate that each elicits appropriate antipredator behaviors. The third call type, the “peep,” seems to be specific to terrestrial threats, but it is unknown if the call elicits predator-specific responses. “Barks” are thus functionally referential aerial predator calls, while “hiccups” are better seen as generalized disturbance calls which reflect risk urgency. Further evidence is needed to draw conclusions regarding the “peep.” These results add to the evidence that functionally referential aerial predator alarm calls are ubiquitous in primates, but that noncatarrhine primates use generalized disturbance calls in response to terrestrial threats.

Sentinel dwarf mongooses, Helogale parvula, exhibit flexible decision making in relation to predation risk

Alarm signals have evolved to communicate imminent threats to conspecifics but animals may also perceive other species' alarm displays to obtain adaptive information. In birds, mixed‐species foraging flocks are often structured around a focal sentinel species, which produces reliable alarm calls that inform eavesdropping non‐sentinel heterospecifics about predation risk. Ongoing work has revealed that several species can recognize the alarm calls of certain sentinel species even without prior encounters, including when these are from distant biogeographic regions. Similar work has yet to examine whether naive subjects' responses to unfamiliar sentinel alarm calls differ from responses to non‐sentinel alarm calls. Here we played the alarm calls of three subtropical Asian bird species that participate in mixed species flocks, to temperate North American birds. Birds responded most to the alarm call of an allopatric core sentinel and a local sympatric sentinel control species, less so to an allopatric non‐core sentinel, and least so to an allopatric non‐sentinel and a negative control stimulus. These patterns provide evidence that broad phylogenetic and geographic recognition is a pertinent aspect of sentinel alarm calls in general.