Quality, Quantity, Distribution and Audience Effects on Food Calling in Cotton—Top Tamarins

Despite extensive documentation in many taxa of vocalizations specific to feeding contexts, little is known of the variables leading to production of food-associated calls. We thus experimentally investigated food-associated calls in cotton-top tamarins ( Saguinus oedipus ). In one experiment, we examined the roles of food quantity, quality and distribution and of social condition of individuals on food-associated calling. Paired adults without offspring gave more vocalizations than immature individuals and adults with offspring. We observed no effects of food quantity or distribution on calling rate. Tamarins called more often to peaches, a food of intermediate preference that was also consumed the fastest. Tamarins gave more food-associated calls when in closer proximity to other group members. Low rates of moderate aggression were observed in single, but not multiple, feeder conditions. We saw no consistent evidence of dominance among adults, and all aggression in family groups was directed toward immature animals. In another experiment, we presented a tamarin with food in a separate cage, either in view of or visually isolated from its mate. Tamarins presented with food called at an equal rate whether or not their mates were visible, suggesting no effect of audience on calling. Individuals not presented with food called in response to the food calls of their mates equally often, irrespective of whether or not the mate or the food was visible. Since food calling occurs at extremely low rates in the absence of food, the food calling by tamarins that cannot see the food suggests that the calls of their mates provide representational information about food.     

Food-associated calls in rhesus macaques (Macaca mulatta): II. Costs and benefits of call production and suppression

In field experiments, free-ranging rhesus macaques (Macaca mulatto)gave food-associated calls in 45% of the trials in which theywere presented with food, either monkey chow or coconut; theydid not call in control trials when sticks were presented. Consistentwith prior naturalistic observations, adult females called ina higher proportion of trials than adult males. Coconut, oneof the most highly preferred food items in the diet, eliciteddifferent call types and a higher rate of calling from "discoverers"than did chow. The call types produced to coconut (warbles,harmonic arches, and chirps) were primarily those that, undernonexperimental conditions, were associated with relativelyrare and preferred foods. In contrast, coos and grunts wereprimarily produced in response to chow. The relative hungerlevel of the discoverer had no significant effect on the calltype produced but did affect the rate of call production; discovererscalled at higher rates when they were hungry. Upon hearing food-associatedcalls, individuals within the vicinity of the discovery respondedby rapidly approaching the caller. A larger number of individualsapproached when discoverers called than when they did not. Discovererswho failed to call received significantly more aggression fromgroup members and, in the case of females, actually consumedless food than discoverers who called. The probability of receivingaggression did not appear to be associated with the discoverer'sdominance rank. Results suggest that food-associated calls are"honest" signals reflecting food possession. Those who failto signal and are caught with food are apparently punished.     

Assessment of meaning and the detection of unreliable signals by vervet monkeys

Free-ranging vervet monkeys, Cercopithecus aethiops, who had learned to ignore playbacks of one type of call by an unreliable signaller subsequently also ignored playback of an acoustically different call by the same individual if the calls had similar referents. Such transfer did not occur if either the identity of the signaller changed or if the two calls had different referents. After repeatedly being played an intergroup call in the absence of other groups, vervets also ignored an acoustically different intergroup call given by the same individual. The monkeys did not transfer habituation, however, if the new call was given by a different individual. In tests where the referents of two calls were different, the monkeys also failed to transfer habituation across call types. Vervet monkeys who had learned to ignore an unreliable leopard alarm call did not later ignore an eagle alarm call, even when the signaller remained the same. Results suggest that vervets, like humans, process information at a semantic, and not just an acoustic, level.     

Food-Associated Calling in Gorillas (Gorilla g. gorilla) in the Wild

Many nonhuman primates produce food-associated vocalizations upon encountering or ingesting particular food. Concerning the great apes, only food-associated vocalizations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) have been studied in detail, providing evidence that these vocalizations can be produced flexibly in relation to a variety of factors, such as the quantity and quality of food and/or the type of audience. Only anecdotal evidence exists of eastern (Gorilla beringei) and western gorillas (Gorilla gorilla) producing food-associated vocalizations, termed singing or humming. To enable a better understanding of the context in which these calls are produced, we investigated and compared the vocal behavior of two free-ranging groups of western lowland gorillas (Gorilla g. gorilla) at Mondika, Republic of Congo. Our results show that (a) food-associated call production occurs only during feeding and not in other contexts; (b) calling is not uniformly distributed across age and sex classes; (c) calls are only produced during feeding on specific foods; and (d) normally just one individual gives calls during group feeding sessions, however, certain food types elicit simultaneous calling of two or more individuals. Our findings provide new insight into the vocal abilities of gorillas but also carry larger implications for questions concerning vocal variability among the great apes. Food-associated calls of nonhuman primates have been shown to be flexible in terms of when they are used and who they are directed at, making them interesting vocalizations from the viewpoint of language evolution. Food-associated vocalizations in great apes can offer new opportunities to investigate the phylogenetic development of vocal communication within the primate lineage and can possibly contribute novel insights into the origins of human language.     

Acoustic Analysis and Contextual Description of Food-Associated Calls in White-Faced Capuchin Monkeys (Cebus capucinus)

Since early studies of primates that identified vocalizations that attracted others to a food source, the assumed function of food-associated calls has been to inform others of the presence of food. The label food-associated calls and its implied function has led to a focus in research on many species of the costs/benefits for the signaler and recipient of informing others about the presence of food; however, without clearly identifying the calls contextually or acoustically, it is unclear if calls are specific to a feeding context and thus whether calls provide specific information about the presence of food. If calls occur exclusively in the context of feeding, information about individual identity would allow listeners to decide whether or not to approach a calling individual. I conducted acoustic and contextual analyses on food-associated calls in white-faced capuchins. I identified the calls as distinct vocalizations that occur almost exclusively in a feeding context. Discriminant function analyses demonstrate that information about caller sex and identity are encoded in the calls. Therefore, there is the potential for individuals to use acoustic information when responding to food-associated calls; however, playback experiments are necessary to test more explicitly the hypothesis that recipients are able to recognize the calls of specific individuals.     

Food calling in wild ravens (Corvus corax) revisited: Who is addressed?

Numerous birds and mammals use vocal signals to advertise feeding opportunities but often such signals vary with individual and contextual factors. Non-breeding ravens call at food that is difficult to access, resulting in the attraction of nearby conspecifics. Although callers may benefit from group formation in various ways, we recently found substantial individual variation in food calling. We here explored whether this variation can be partly explained by the social dynamics in raven foraging groups, together with already known effects of age class and sex. Specifically, we expected ravens to respond to the presence or absence of affiliates that could act as cooperative partners in the forthcoming feeding event, that is they should call when other ravens were present but they themselves were alone rather than when they were also in company of an affiliation partner. We observed the vocal behaviour of individually marked wild ravens and, simultaneously, categorized their affiliative behaviour with other ravens in the minutes before experimentally controlled feedings. In line with our prediction, individuals were less likely to produce food-associated calls when they were in close contact with an affiliation partner prior to feeding as compared to when they were alone. Furthermore, sex and age class influenced food calling as females called more often than males and younger birds called more often than adult ravens. In conclusion, these results suggest that ravens attempt to find support from a particular cooperative partner by broadly advertise feeding opportunities via food-associated calls, especially when they have low chances in contest competition due to their age and sex. These findings lend further support to the assumption of raven flocks being structured by social relationships and individual birds flexibly controlling their vocal signalling according to the current flock composition.     

Playbacks of food-associated calls attract chimpanzees towards known food patches in a captive setting

Food-associated calls have received much research attention due to their potential to refer to discovered food in a word-like manner. Studies have found that in many species, food-associated calls attract receivers to the food patch, suggesting these calls play roles in food sharing, cooperation and competition. Additionally, in various species, these calls play a role that has received much less attention: mediating social interactions among foragers that are already nearby or within the food patch, independently of whether they attract outside foragers. In order to increase understanding of the function of the chimpanzee (Pan troglodytes) food-associated rough grunt, we conducted captive playback studies testing whether rough grunt playbacks attract, repel or have no effect on the proximity of foragers already familiarized with the presence of food. We tested how acoustic playbacks of rough grunts (or control calls) from one of two known, identical feeding sites affected receivers’ approach and feeding behaviors. More often than expected, participants first approached the feeding site from which rough grunts, but not control calls, were broadcast. However, neither condition increased the likelihood that participants fed first from a given site. Our results support the hypothesis that rough grunts elicit an approach response in receivers, while providing no evidence that they repel. In addition, our study provides evidence that receivers may approach rough grunts even if they do not intend to feed. We discuss the information rough grunts may convey to receivers beyond information about discovered food and the potential benefits signalers may gain from this calling behavior.

     

Marmoset (Callithrix geoffroyi) Food-Associated Calls are Functionally Referential

Signals that are functionally referential provide listeners with information about a signaler's external environment, such as the presence of a nearby predator. Just as alarm calls may signal the presence of a predator, food-associated calls may signal the presence of food. To date, however, the only conclusive evidence that conspecifics perceive information about food from food-associated calls comes from a single species, the domestic chicken. Geoffroy's marmosets, small, arboreal New World primates, often emit food-associated calls when finding or consuming food. We presented playbacks of food calls and control sounds to two groups of naturalistically housed marmosets and observed the frequency of food-related behaviors (FRBs) during the 20-min post-playback period. Relative to the control playbacks, food call playbacks elicited an increase in the frequency of two FRBs (foraging and feeding), lasting throughout the post-playback observations. Moreover, the effect of food call playbacks was robust, occurring without regard to the type of food eliciting the food calls, the rate of food calling, or whether the signaler was a member of the receiver's group. To our knowledge, this research is the first to demonstrate that the food-associated calls of a primate species, like the food-associated calls of domestic chickens, meet the perception criterion for functionally referential communication. The results are discussed in light of the affective and cognitive mechanisms that may underlie the responses of receivers to hearing food-associated calls given by marmoset conspecifics.     

Recruitment calling: a novel form of extended parental care in an altricial species

In many altricial birds, fledglings disperse when they are no longer fed, and this dispersal marks the end of parental care. In some species, however, young remain in close association with their parents after nutritional independence. Because juveniles are still inferior foragers at this stage, they might benefit from parental assistance in locating good feeding sites, but this possibility remains largely unexplored. Here, we show that parents and helpers in pied babbler (Turdoides bicolor) societies use a recruitment call to direct nutritionally independent, but inexperienced, foragers to particular food patches. Observations and a playback experiment indicated that adult babblers use a "purr" call to recruit group members to a foraging patch. Creation of experimental foraging patches supported observations that individuals tend to give the call when they are foraging on abundant, divisible food sources and when their group contains independent fledglings (youngsters who are no longer fed directly). Fledglings responded to calls more often than adults, who frequently encountered aggression from the caller if they did, and the fledglings gained significant foraging benefits. This is the first study to demonstrate that altricial birds may use recruitment calls to extend parental care past the period of direct provisioning.     

Food-associated calls in rhesus macaques (Macaca mulatta): I. Socioecological factors

Upon discovering food, free-living rhesus macaques (Macaca mulatta)on the island of Cayo Santiago, Puerto Rico, produce a complexof vocal signals consisting of five acoustically distinguishablecalls. This report examines the socioecological factors elicitingcall production and the information protentially conveyed toothers. The primary contexts for three vocalizations ("warbles," "harmonicarches, " and "chirps") are encounters with rareand highly preferred foods (e.g., coconut). Two other vocalizations("coos" and "grunts") are produced both in food (primarily provisionedchow) and in nonfood contexts, such as during mother-infantseparation and grooming interactions. Grunts given upon encounteringfood are acoustically distinct from those given in nonfood contexts.In contrast, coos associated with food are statistically indistinguishablefrom coos given in other contexts. When conspecitics hear thesefood-associated calls, they typically approach the caller. Coosare less likely to lead to approach than other food-associatedcalls, Results from all-day follows on adult males and adultfemales reveal that changes in hunger level influence call ratebut not call type; the different call types are produced throughoutthe day. We infer that the structure of food-associated callsprovides information about the quality of the food discovered,whereas call rate conveys information about the relative hungerlevel of the caller. In this population, adult males give fewerfood-associated calls than adult females. In addition, femaleswithin large matrilines call more than females within smallermatrilines, and males who are resident in a group are more vocalthan peripheral males.     

The influence of kinship and dominance hierarchy on grooming partner choice in free-ranging <Emphasis Type="Italic">Macaca mulatta brevicaudus</Emphasis>

In group-living animals, individuals do not interact uniformly with their conspecifics. Among primates, such heterogeneity in partner choice can be discerned from affiliative grooming patterns. While the preference for selecting close kin as grooming partners is ubiquitous across the primate order, the selection of higher-ranking non-kin individuals as grooming partners is less common. We studied a group of provisioned rhesus macaques (Macaca mulatta brevicaudus) on Hainan Island, China, to examine rank-related benefits of grooming exchanges and the influence of kin relationships. We tested four hypotheses based on Seyfarth’s model: (1) there will be kin preference in grooming relationships; (2) grooming between non-kin individuals will be directed up the dominance rank; (3) grooming between non-kin individuals will reduce aggression from higher-ranking ones; and (4) non-kin individuals will spend more time grooming with adjacent ranked ones. We found that grooming relationships between kin individuals were stronger than those between non-kin individuals. For non-kin relationships, lower-ranking individuals received less aggression from higher-ranking ones through grooming; a benefit they could not derive through grooming exchanges with individuals related by kinship. Individuals spent more time grooming adjacent higher-ranking non-kin individuals and higher-ranking individuals also received more grooming from non-kin individuals. Our results supported Seyfarth’s model for predicting partner choice between non-kin individuals. For relationships between kin individuals, we found results that were not consistent with prediction for the exchanges of aggression and grooming, indicating the importance to control for the influence of kinship in future studies.     

Calls during agonistic interactions vary with arousal and raise audience attention in ravens

Background

Acoustic properties of vocalizations can vary with the internal state of the caller, and may serve as reliable indicators for a caller’s emotional state, for example to prevent conflicts. Thus, individuals may associate distinct characteristics in acoustic signals of conspecifics with specific social contexts, and adjust their behaviour accordingly to prevent escalation of conflicts. Common ravens (Corvus corax) crowd-forage with individuals of different age classes, sex, and rank, assemble at feeding sites, and engage in agonistic interactions of varying intensity. Attacked individuals frequently utter defensive calls in order to appease the aggressor. Here, we investigated if acoustic properties of defensive calls change with varying levels of aggression, and if bystanders respond to these changes.

Results

Individuals were more likely to utter defensive calls when the attack involved contact aggression, and when the attacker was higher in rank than the victim. Defensive calls produced during intense conflicts were longer and uttered at higher rates, and showed higher fundamental frequency- and amplitude-related measures than calls uttered during low-intensity aggression, indicating arousal-based changes in defensive calls. Playback experiments showed that ravens were more likely to react in response to defensive calls with higher fundamental frequency by orientating towards the speakers as compared to original calls and calls manipulated in duration.

Conclusions

Arousal-based changes are encoded in acoustic parameters of defensive calls in attacked ravens, and bystanders in the audience pay attention to the degree of arousal in attacked conspecifics. Our findings imply that common ravens can regulate conflicts with conspecifics by means of vocalizations, and are able to gather social knowledge from conspecific calls.

     

A community context for aggression? Multi‐species audience effects on territorial aggression in two species of Paridae

1. Territorial aggression in birds is widely observed and is commonly linked to sex, age, body size, physiology, seasonal cues, food resource, urbanization, and a variety of social contexts including conspecific audience effects. However, little is known about the heterospecific audience effects on territorial aggression.
2. Here, we address an emerging idea that heterospecific audience effects may be pervasive influences in the social lives of free‐living birds. We tested the hypothesis that the composition, number, and relative body size of heterospecific audiences observing an aggressive contest will influence the response probability and intensity of aggression displayed.
3. We subjected two Paridae species, tufted titmouse (TUTI, Baeolophus bicolor) and Carolina chickadee (CACH, Poecile carolinensis), to playbacks of aggressive calls during a breeding season in north‐central Florida. At widely spaced playback sites (N = 134) in woodland habitats, we characterized the makeup of heterospecific audiences, aggression type (intra vs. interspecific territoriality), local population density, and various environmental factors (tree density, wind speed, and noise level) that are likely to influence territorial aggression.
4. We found that the presence of heterospecific audiences increased TUTI aggression levels and that both parids were more likely to respond to playback stimuli when their audiences had higher heterospecific diversity (more heterospecific individuals and species). We also found TUTI were more likely to respond when CACH were present but not vice versa.
5. In conclusion, we found evidence that heterospecific audiences significantly influenced the metrics of territorial aggression of free‐living animals and we suggest that the definition of audience effects on the behavior of free‐living animals be expanded to incorporate heterospecific audiences.

     

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

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

Adult Richardson's Ground Squirrels (Spermophilus richardsonii) Ignore Rate Changes in Juvenile Alarm Calls: Age‐Differential Response Urgency Perception?

Juvenile Richardson's ground squirrels (RGS; Spermophilus richardsonii) communicate response urgency by modulating the rate of syllable production in repetitive alarm calls, although longer call bouts do not promote more pronounced or longer‐lasting (tonic) vigilance in juvenile call recipients. We exposed free‐living adult RGS to playbacks of alarm calls differing in rate and length to determine whether adult receivers respond to the same alarm parameters as juveniles. Adult squirrels did not respond differentially to differences in call rate or length, suggesting that adult RGS do not attend to call rate as do juveniles. This difference in response may be attributable to a developmental change in the perceptual mechanisms by which individuals extract information regarding response urgency, but could also be a product of adult receivers devaluing information encoded in alarm calls emitted by relatively inexperienced juvenile signalers.     

Decrease in Alarm Call Response Among Tufted Capuchins in Competitive Feeding Contexts: Possible Evidence for Counterdeception

Animal signals function to elicit behaviors in receivers that ultimately benefit the signaler, while receivers should respond in a way that maximizes their own fitness. However, the best response may be difficult for receivers to determine when unreliable signaling is common. “Deceptive” alarm calling is common among tufted capuchins (Cebus apella nigritus) in competitive feeding contexts, and responding to these calls is costly. Receivers should thus vary their responses based on whether a call is likely to be reliable. If capuchins are indeed able to assess reliability, I predicted that receivers will be less likely to respond to alarms that are given during competitive feeding contexts than in noncompetitive contexts, and, within feeding contexts, that individuals inside or adjacent to a food patch will be less likely to respond to alarms than those further from the resource. I tested these predictions in a group of wild capuchins by observing the reactions of focal animals to alarm calls in both noncompetitive contexts and experimental feeding contexts. Antipredator escape reactions, but not vigilance reactions, occurred significantly less often in competitive feeding contexts than in noncompetitive contexts and individuals adjacent to food patches were more likely to respond to alarm calls than were those inside or further from food patches. Although not all predictions were fully supported, the findings demonstrate that receivers vary their behavior in a way that minimizes the costs associated with “deceptive” alarms, but further research is needed to determine whether or not this can be attributed to counterdeception.     

Triadic interactions among Macaca radiata: Passports and buffers

Male members of a group of captive Macaca radiata at the California Primate Research Center held and carried infants as they approached or were approached by higher-ranking males and as they were threatened by other males. Male infants between the ages of 25 and 84 weeks were involved in triadic interactions more frequently than were female infants of any age or male infants of other ages. That males were less likely to be harassed while huddling with or embracing infants suggested that infants provided an effective buffer against aggression.     

Development in the Usage and Comprehension of Greeting Calls in a Free‐Ranging Group of Japanese Macaques (Macaca fuscata)

The main objective of this study is to clarify the developmental process involved in both the usage of greeting calls and the response to greeting calls by Japanese macaques. These greeting calls facilitate affiliative interactions by communicating benign intent. Specifically, individuals frequently emit greeting calls when interacting with less‐predictable individuals. Here, we examined whether the targets at which greeting calls are directed, along with associated behavioral responses, differed among the age classes, by conducting a cross‐sectional observation of females aged 0–5 yr and their mothers. We found that infant females showed a weak tendency to emit greeting calls at no specific receivers, unlike that by older females. Adult females emitted greeting calls more frequently when approaching unrelated females than related females. In contrast, young adult or juvenile females exhibited no significant difference in the proportion of the calls with related and unrelated conspecifics. Adult and young adult females were more likely to respond affiliatively to other individuals that approached using greeting calls compared with silent approaches, whereas juveniles did not exhibit different responses to the two types of approaches. This study showed that the target‐specific usage and affiliative response to greeting calls emerge with changes in the developmental stage. Furthermore, the fact that even young adults did not use greeting calls as adults indicates that the usage of greeting calls is modified in conjunction with the expansion of social relationships.     

Monotony and the Information Content of Richardson's Ground Squirrel (Spermophilus richardsonii) Repeated calls: Tonic Communication or Signal Certainty?

The repetition of elements within an alarm signal is commonly thought to ensure that receivers have detected that signal, or to promote residual vigilance in light of the dangerous circumstances prompting the signal's initial production (tonic communication). Beyond alerting others and maintaining that state of alertness, however, repetitive signal elements may be parsed so as to encode information about the nature of potential threats. To determine how call length and variation in intersyllable latency might prove informative in the repetitive alarm vocalizations of Richardson's ground squirrels (Spermophilus richardsonii), we conducted a field‐based playback experiment quantifying antipredator responses to manipulated alarm calls. Free‐living juvenile squirrels were exposed to playbacks of 12 syllable (long) and six syllable (short) calls with a constant (monotonous) or changing (variable) call rate. The length of calls had no significant effect on the behaviour of call recipients during and immediately after call production; however, call recipients showed greater vigilance after the playback of monotonous calls than after variable calls. The absence of a call length effect is not consistent with tonic communication in the strict sense; rather, enhanced responsiveness to monotonous relative to variable calls suggests that multiple syllables, and the emergent patterns of intersyllable latency, communicate information about response urgency or the distance to a predatory threat. Only monotonous calls convey those aspects with any certainty on the part of the signaller and hence are selectively attended to by receivers.     

Representational signalling in birds

Some animals give specific calls when they discover food or detect a particular type of predator. Companions respond with food-searching behaviour or by adopting appropriate escape responses. These signals thus seem to denote objects in the environment, but this specific mechanism has only been demonstrated for monkey alarm calls. We manipulated whether fowl (Gallus gallus) had recently found a small quantity of preferred food and then tested for a specific interaction between this event and their subsequent response to playback of food calls. In one treatment, food calls thus potentially provided information about the immediate environment, while in the other the putative message was redundant with individual experience. Food calls evoked substrate searching, but only if the hens had not recently discovered food. An identical manipulation had no effect on responses to an acoustically matched control call. These results show that chicken food calls are representational signals: they stimulate retrieval of information about a class of external events. This is the first such demonstration for any non-primate species. Representational signalling is hence more taxonomically widespread than has previously been thought, suggesting that it may be the product of common social factors, rather than an attribute of a particular phylogenetic lineage.