The effects of social status on food-associated calling behaviour in captive cotton-top tamarins

We examined the effects of social environment on food-asociated calling of cotton-top tamarins, Saguinus oedipus, in two experiments. In experiment 1, we compared the food-associated calling behaviour of six juvenile tamarins living in their natal groups with their calling behaviour 9 months after being removed from family groups and paired. In experiment 2, we studied food-associated calling behaviour of nine cotton-top tamarins immediately before and after removal from their natal groups and pairing. The tamarins underwent three separate developmental processes in their calling behaviour. Animals removed from their natal groups showed an immediate reduction in vocalizations other than food-associated calls (C and D chirps). The development of precise adult forms of C and D chirps was more gradual and was a function of time since removal from their natal group rather than time since pairing. Finally, the postremoval tamarins persisted in applying C chirps to nonfood objects and showed no correlation between C-chirp rate and food preference, which is typical of immature tamarins. We conclude that social status plays an important role in the development of adult forms and usage of food-associated calls. Copyright 1999 The Association for the Study of Animal Behaviour.     

Food Transfer and Development of Feeding Behavior and Food-Associated Vocalizations in Cotton-Top Tamarins

Food transfer between adults and infants is common in many marmoset and tamarin monkeys, and is often accompanied by vocalizations. We hypothesized that vocalizations by adults in a food transfer context creates an opportunity for infants to learn not only what foods are appropriate but what vocalizations are appropriate in feeding contexts. We studied the development of feeding behavior and food-associated vocalizations in 10 infant cotton-top tamarins through the first 20 wks of life. Infants obtained solid food through transfers from older group members, primarily the adult male, beginning at weeks 5–6. Both adults and infants vocalized during food transfers with adults, producing rapid sequences of the call types adults normally give when feeding. Infants were usually successful in obtaining food primarily when the adult was vocalizing. The sooner infants were active participants in food transfers, the sooner they began to feed independently. In the early weeks, infants produced a large number of vocal types during food transfers, but with increasing age there was a steady increase in the number of adult-form food calls and a reduction in other, non-food-associated calls. Infants that fed independently at an early age produced fewer non-food-associated calls by the last month of observation. Infants called at higher rates to their most preferred food. Food transfers accompanied by vocalizations may provide an opportunity for infants to learn about appropriate foods as well as the vocalizations that accompany feeding in adults, and may represent a form of 'coaching' or information donation by adults.     

The role of social context and individual experience in novel task acquisition in cottontop tamarins, Saguinus oedipus

In socially tolerant settings, na?ve individuals may have opportunities to interact jointly with knowledgeable demonstrators and novel tasks. This process is expected to facilitate social learning. Individual experience may also be important for reinforcing and honing socially acquired behaviours. We examined the role of joint interaction and individual experience in the acquisition of a novel foraging task in captive cottontop tamarins. The task involved learning how to locate and access two hidden food rewards from among 10 differently cued forage sites. Tamarins were tested in three different conditions: (1) individually, (2) while interacting with a na?ve mate, and (3) while interacting with a mate trained as a knowledgeable demonstrator. For tamarins tested with mates present, we interspersed social input test days with exposure to the task while alone. Tamarins were tested again 17 months after their last exposure to the task, to assess long-term memory. All tamarins tested with knowledgeable demonstrators solved the task. In contrast, tamarins tested alone or with na?ve mates had similarly high levels of neophobia and low levels of task acquisition. We conclude that joint interaction occurs in mated pairs of cottontop tamarins and facilitates the spread of novel behaviour. Interspersing test days with a knowledgeable demonstrator present and test days alone with the task helped tamarins to achieve the ultimate goal of the task: obtaining food rewards. Tamarins performed similarly when tested 17 months later, regardless of their initial learning environment. Tamarins had memory deficits for the location of hidden food rewards, but retained memory of the necessary motor actions and solved the task.     

The function of food-associated calls in white-faced capuchin monkeys, Cebus capucinus, from the perspective of the signaller

In many species, call recipients respond to food-associated calls by approaching the signaller. For this reason, most studies of food-associated calls focus on the benefits to a signaller of attracting a particular audience to a food source. Although call recipients respond as if they have been informed about the location of a food source, it is not necessarily the case that the primary function of food-associated calls is to inform others. I combined naturalistic observations and food placement experiments to investigate the environmental and social influences on call production in white-faced capuchin monkeys to assess other possible functions of food-associated calls. Individuals did not call under the circumstances predicted by an information-sharing hypothesis. The quantity of food and the age-sex composition of the audience did not influence call production, but food type did. Individuals produced more food-associated calls when they discovered fruit compared with insects or eggs. Results of observations of social interactions after food discovery indicated another possible function of food-associated calls. Individuals who called when they discovered food were less likely to be approached by others who were in visual contact than individuals who remained silent. Individuals who did not call when they discovered food were more likely to call subsequently if a higher-ranking, as opposed to a lower-ranking, animal approached them. Furthermore, individuals who called when approached by higher-ranking animals were less likely to receive aggression than individuals who did not call. Therefore, food-associated calls may function to announce food ownership, thereby decreasing aggression from other individuals.     

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-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.     

Progressive parenting behavior in wild golden lion tamarins

Young primates in the family Callitrichidae (the marmosets and tamarins) receive extensive and relatively prolonged care from adults. Of particular note, callitrichid young are routinely provisioned until well after weaning by parents and helpers, which is in stark contrast to typical juvenile primates, who must acquire most of their food independently once they are weaned. Adults of some callitrichid species produce a specialized vocalization that encourages immature group members to take proffered food from the caller. Here, I report that wild adult golden lion tamarins (Leontopithecus rosalia) not only used this food-offering call to encourage young, mobile offspring to approach and take captured prey from them, but as the young began to spend significant time foraging for themselves and to acquire prey by independent means, the frequency of these vocalizations in the context of food transfer declined. Adults then began to use food-offering calls in a novel context: to direct juveniles to foraging sites that contained hidden prey that the adults had found but not captured. During the period of these most frequent adult-directed prey captures, the independent prey-capture success rates of juveniles improved. Thus, adults modified their provisioning behavior in a progressive developmentally sensitive manner that may have facilitated learning how to find food. I hypothesize that as a result of these demonstrations by adults, juveniles either may be encouraged to continue foraging despite low return rates or to learn the properties of productive prey-foraging substrates in a complex environment.     

Alarm calls of wintering great tits Parus major: warning of mate,reciprocal altruism or a message to the predator?

When a predator is not an immediate threat, a prey may produce relatively loud alarm calls because the risk is low. Since such calls could nevertheless attract acoustically oriented predators, the cost of predator attraction must be outweighed by factors beneficial to the caller. In this field study we elicited low-risk alarm calls by temporarily catching wintering adult male great tits Parus major at feeders both within and outside their territories. We tested whether the alarm calls of dominant males can be explained in terms of mate warning, reciprocal altruism or notifying the predator of detection. If alarms are intended to warn mates, males accompanied by their mates should give alarm calls both within and outside home range, even if other permanent flock members are absent. If alarms are to be explained by reciprocal altruism, male great tits should give low-risk alarm calls when accompanied by permanent flock members other than mate within and not outside of the home-range. If alarm calling is a message to a predator, males should call when foraging alone. We found that male great tits gave low-risk alarm calls when accompanied by their mates, independent of feeder location. They also gave low-risk alarm calls within home ranges in the presence of other permanent flock members when mates were absent. In contrast, only a few males gave calls when foraging alone within their home ranges, or when in the company of unfamiliar great tits outside their usual home-range. The results suggest that the utterance of alarm calls may be explained as mate protection and reciprocal altruism among familiar individuals.     

The response of adult orang-utans to flanged male long calls: inferences about their function

Flanged male orang-utans emit loud vocalizations called long calls. In this study, we examined the correlates of variation in long-calling rates among flanged male Sumatran orang-utans, as well as the ranging responses of adult females and flanged males to these long calls. Males that gave calls more often were more likely to approach calls by others. Results bolster a female attraction function of long calls. Flanged males did not significantly avoid or approach long calls. However, males called more when alone than when guarding a female mate, and adult females significantly approached long calls, especially those of the dominant male, and did so regardless of their reproductive state, allowing them to remain within earshot of calling males. The possible selective advantages of this response include avoidance of harassment and infanticide by males. These findings confirm the existence of some form of social organization above the mother-infant unit.     

Long-range call use in dominance-structured Crested Tit Parus cristatus winter groups

In this study on free-ranging Crested Tits Parus cristatus , I examine the relationship between social dominance and the frequency of use of long-range communication calls. Calling rates of trills were highest among socially dominant individuals and they gave more calls when close to the boundary of their territories. Dominant females uttered fewer calls than their mates. However, they gave significantly more calls than subordinate males and subordinate females, the latter calling least. A removal and playback experiment revealed a relationship between the utterance of trilled calls and the defence of the winter territory in the Crested Tit. Although territorial vocalizations could incur costs, territorial individuals may gain from improved winter survival by decreasing the risk of food stealing by Crested Tits from adjacent territories.     

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.     

Food transfers in wild and reintroduced golden lion tamarins,Leontopithecus rosalia

We collected data from wild and reintroduced golden lion tamarins (Leontopithecus rosalia) to describe the behavior of donor and recipient during food transfers, evaluate the effect of supplemental feeding on food transfer behavior, and examine various hypotheses concerning the function of food transfers in primates. Behavioral observations were conducted on 12 groups of tamarins with young (N = 30) between the ages of 1 week and 1 year old. Results show that food transfers involve various behaviors, from steals by recipients to offers by donors; transfers mostly derive from adults and are directed at immature weaned young (between 3 and 9 months old); and that most items transferred were prey or fruits that require skill to process. Eleven percent of food transfers were preceded by an adult vocalization specific to that context, whereas 86% were preceded by conspicuous infant vocalizations and begging behavior. The most common vocalizations were loud and atonal (rasps) and broad banded frequency modulated (trills). Infants born to reintroduced parents vocalized less, whereas reintroduced adults vocalized more before transferring food than their wild counterparts. Reintroduced adults and young received more food transfers (4.4 per hr) than did wild‐born adults and young (2.2 per hr). Our findings suggest that food transfer in golden lion tamarins is best understood as provisioning of young that have not fully developed foraging skills to ensure they get the necessary resources for growth and survival. Am. J. Primatol. 48:305–320, 1999. © 1999 Wiley‐Liss, Inc.     

Food, audience and sex effects on pinyon jay (Gymnorhinus cyanocephalus) communication

Pinyon jays (Gymnorhinus cyanocephalus) have a complex social system that may require a complex communication system. They need to interact with multiple flock members, and they form life-long pair-bonds. We researched whether pinyon jays would selectively vocalize depending on the presence or absence of food and certain flock members. We recorded the vocalizations of nine pinyon jays (four pair-bonds and one single male) in response to different audience types. The calls of the test bird were recorded after it was given either an empty food cup or one containing 50 pinyon pine (Pinus edulis) seeds, and the bird was in the presence of one of the following audience types: (1) two males and two females including subject's mate; (2) two males and two females excluding subject's mate; (3) four males excluding mate; (4) three females excluding mate; and (5) no audience. Birds gave fewer calls when there was food. When alone, birds called in a manner that may maximize long-distance transmission. Trends indicate that birds call differently to their mate. A sex effect was also found in that males and females called in a distinct manner, possibly reflecting differences in dominance status. Overall, birds responded to the presence or absence of an audience.     

Food Transfer Among Adult Lion Tamarins: Mutualism,Reciprocity or One-Sided Relationships?

Tamarins (Callitrichidae) are cooperative breeders. Groups typically contain only two or three breeding individuals and subordinate group members are reproductively suppressed. Nonreproductive individuals, which are usually the offspring of the group's breeding members, delay dispersal while providing care to infant siblings. Callitrichid breeder-infant and helper-infant relationships have been well studied but empirical studies regarding the dynamics of breeder-helper relationships are sparse. I examined food-transfer interactions among parents and natal adults in 7 groups of captive lion tamarins, Leontopithecus spp., to test whether relationships are maintained by mutualism or reciprocity or are to the benefit of one side of a dyad. Individuals that had recently received food from a group member most frequently released food to the previous donor as their next act of transfer. Conversely, food transfer was not dependent on symmetrical relationships within groups over a time frame of several weeks. These results suggest that mutualism plays a role in the maintenance of food-transfer relationships but reciprocity does not. However, there is evidence for a reciprocal relationship between grooming and food transfer in one group. Subadults and adults living in their natal groups transferred proportionally more food to mothers than to oppositely-sexed subadult and adult siblings. Thus, individuals most likely to receive aggression preferentially released food to individuals most likely to inflict injury upon them. Although these results support the coercion hypothesis, they may suggest alternatively that food transfer by helpers to breeding adults is driven by inclusive fitness considerations.     

Captive-born cotton-top tamarins (Saguinus oedipus) respond similarly to vocalizations of predators and sympatric nonpredators

What types of cues do callitrichid primates use to detect and respond to predators? Do they respond to predator‐specific cues or to more general cues? The evidence for these questions remains conflicting. We presented captive‐born and reared cotton‐top tamarins with no previous exposure to predators (or predator cues) with vocalizations from three potential predators of cotton‐top tamarin in the wild (white hawk, jaguar, and tayra) and with vocalizations from sympatric nonpredators (black‐faced antthrush and red howler monkey). Vocalizations from predators and from nonpredator mammals elicited equivalent arousal, fear, and vocal responses. Howler monkey roars produced the strongest responses. The results suggest that predator‐naïve cotton‐top tamarins do not recognize specific predator vocalizations, but may respond to vocal qualities (low‐frequency, noisy sounds) that indicate large body size, threat, or aggression. On the other hand, tamarins responded much more strongly to the higher frequency calls from the hawk than the antthrush, suggesting another mechanism must also be involved. The failure of captive‐reared tamarins to distinguish between vocalizations of predators and nonpredator mammals has important implications for reintroduction studies. Am. J. Primatol. 70:707–710, 2008. © 2008 Wiley‐Liss, Inc.     

Conspicuous calling near cryptic nests: a review of hypotheses and a field study on white‐browed scrubwrens

Predation is an important source of nest mortality in many bird species and calling near the nest can increase this risk, yet adults of many species regularly vocalize near their nests. Some of these calls serve clearly adaptive functions, such as alarm or provisioning calls. However, many species also give conspicuous ‘contact’ calls near the nest, which is puzzling because the function of these calls is unclear, and they might attract predators. Most studies of parental vocalizations near nests have focused on specific vocalizations and single hypotheses, yet there is a diversity of vocalization types and potential functions. We review the literature on the diversity and possible function of parental vocalizations near the nest, and then investigate the puzzle of conspicuous contact calling near nests by white‐browed scrubwrens Sericornis frontalis. In scrubwrens, ‘chip‐zz’ contact calls were almost always used when adults approached nests, and when they approached one another or changed location. Call composition also changed: the proportion of ‘chip’ elements increased as callers approached the nest or other adults. Neither adult sex nor nestling age affected calling. Thus, chip‐zz calls appear to be used as ongoing signals to other group members of the caller's activity and location, particularly relative to the nest. Nestlings appeared to use the calls as cues of adult arrival, and increased calling as adults approached nests. Further, adults called less after a predator was on the territory, suggesting that parents may be able to reduce the risk of chip‐zz calls betraying nest location, or possibly use the absence of calling as a signal of danger. This study thus demonstrates that calling near nests could inform both adults and nestlings about the caller's behaviour, and could serve multiple functions. Future studies will need to experimentally test these functions, as well as the other hypotheses reviewed here.     

Tutoring in Wild Golden Lion Tamarins

Among most nonhuman primates, juveniles must acquire most of their solid food independently. Information gleaned from adults results from efforts initiated by the juveniles. Donation of food or foraging information by adults to immatures is rare among apes and virtually unknown among monkeys. We report 3 observations in which wild adult golden lion tamarins appear to have directed their immature offspring to a location where a hidden prey item was located. According to the definition of Caro and Hauser (1992), the tamarins were tutoring their young.     

Not for Parents Only: Begging Calls Allow Nest‐Mate Discrimination in Juvenile Zebra Finches

The benefits of recognition of family members may range from inbreeding avoidance to cooperative and coordinated behaviors within the family group. In birds, recognition of family members has almost exclusively been studied between parents and offspring or within cooperatively breeding societies. Yet, recognition of nest‐mates could be of special importance in recently fledged birds of colonial species by helping in locating the nest, maintaining family group cohesion, or allowing detection of feeding opportunities by recognizing the begging calls nest‐mates produced on the return of a parent. Here we study nest‐mate discrimination based on begging calls in fledglings of domesticated zebra finches (Taeniopygia guttata), a gregarious songbird living in loose colonies in which juveniles may gather in crèches and are fed by parents up to 20 d after fledging. Using playback tests, we show that fledglings called more and spent more time near the loudspeaker in response to the begging calls of their nest‐mates than to the calls of other familiar individuals. Because each fledgling was exposed to the repeated association of the begging calls of its nest‐mates and the subsequent feeding of its parents, this preferential response to the nest‐mates' calls could be a conditioned response to the food reward. Whereas fledglings answered more to male fledgling calls than to female fledgling calls, response to playback was influenced neither by the sex of the subject nor by its brood size. Discriminant function analysis based on acoustic parameters showed that begging calls carried an individual signature as well as a brood signature which might account for such nest‐mate discrimination. Begging signals are major study systems of the evolution of communication in the face of conflicts of interest between signalers and receivers. Our results suggest that eavesdropping and communication networks may be other informative frameworks to understand the design of offspring solicitation signals.     

Predation as a cost of sexual communication in nocturnal seabirds: an experimental approach using acoustic signals

Conspicuous behaviour, such as sexual advertisement, exposes animals to predation; mate attraction thus often conflicts with antipredator behaviour. We investigated whether an avian predator, the brown skua, Catharacta antarctica l?nnbergi, uses the mate attraction calls of colonial seabirds, the petrels. The majority of petrels attract mates at night and vocalizations are their main way of communicating. At our study sites, skua predation on nocturnal petrels was heavy, and concentrated particularly on a single species, the blue petrel, Halobaena caerulea. Using playback experiments, we showed that skuas can use male petrel calls as a cue for prey location and selection. This listening behaviour of skuas probably imposes a major constraint on advertising petrels, and especially on single males which face a trade-off between attracting females (which respond by calling in flight) and avoiding predation. We also investigated the consequences of this predation risk on the behaviour of petrels: a second set of playback experiments showed that the most heavily preyed on petrel species could use skua territorial calls to infer predation risk and stop calling thereafter, which may reduce conspicuousness and predation risk. Copyright 2000 The Association for the Study of Animal Behaviour.