Food Calls Research Articles

Cognitive Components of Vocal Communication: A Case Study.

Simple SummaryThe pygmy marmoset is the world’s smallest true monkey with a mean brain size of 4.5 g. I review the cognitive and pre-linguistic skills that these monkeys show in their vocal communication. Pygmy marmosets have several types of calls used to maintain contact with one another, and they use calls that are cryptic when they are close to group members, and calls that more easily detected when they are farther away. They take turns in contact calling. They modify their call structure when in a new social setting to match the structure of other group members or of mates. Infants display babbling behavior similar to human infants, and adult caretakers provide social reinforcement that lead infants to develop adult like calls. Thus, pygmy marmosets modify vocal structure and learn through social interactions. This contrasts sharply with the general view that most nonhuman primates do not display vocal learning or an ability to modify call structure. Pygmy marmosets signal other group members when they find food using specialized calls but inhibit these calls with living prey. These complex cognitive skills in communication indicate that brain size may not be a good predictor of cognitive ability.Communication among nonhuman animals is often presented as rigid and inflexible, reflecting emotional states rather than having any cognitive basis. Using the world’s smallest monkey, the pygmy marmoset (Cebuella pygmaea), with the smallest absolute brain size amongst simian primates as a case study, I review the role of cognition in the development and usage of vocalizations in pygmy marmosets and present new data on the instrumental use of babbling and of food associated vocalizations. Pygmy marmosets have several contact calls that differ in the psychoacoustic properties for sound localization as well as the distance at which they carry through the rainforest. Marmosets use these calls strategically based on distance from neighbors. Marmosets alter spectral and temporal aspects of call structure when exposed to new groups and when newly mated. They display population specific vocal dialects. Young pygmy marmosets engage in extensive babbling behavior rewarded by parents that helps the young develop adult vocal structures, but older monkeys also use babbling instrumentally in conflict situations. Specific food referential calls generally relate to food preferences, but food calls are suppressed in the presence of animate prey. Unmated animals systematically combine a long distance call with food calls as though advertising for mates. Taken together, these examples show that even small brained primates use their vocal signals flexibly and strategically in response to a variety of environmental and social conditions.

Food Calls in Common Marmosets, Callithrix jacchus, and Evidence That One Is Functionally Referential.

Simple SummaryWe studied the calls that are made by common marmosets when they see food and when they consume it. They were tested with two types of fruit (banana and blueberries) and two types of insect (live mealworms and crickets). All of these foods elicited Call A, described previously as a food call. Call B was softer and was given more often to crickets. Of particular interest was our discovery of Call C, which was produced when the marmosets discovered insects but not fruit. We showed that Call C has referential meaning, by playing recordings of the call to marmosets when they were eating banana, as follows: on hearing Call C, but not Call A, they stopped eating the banana and went to look in container where they had found insects before. Call C, therefore, has specific meaning, signaling the availability of insect food. All of the calls were produced more frequently when the marmosets were tested alone than when in pairs, indicating that they advertise the availability of food to companions. Call C, at least, is not merely an automatic response reflecting the marmoset’s emotional state. A meaningful call about the discovery of insect food would be essential for survival, since marmosets often forage out of sight of each other. Knowledge of their vocal communication can improve the care of marmosets held in captivity.We studied three calls of common marmosets, Callithrix jacchus, elicited in the context of food. Call A, but not B or C, had been described previously as a food call. We presented insects (live mealworms or crickets) and fruit (banana or blueberries) and used playbacks of calls. We found that Call C was produced only in response to seeing insects, and not fruit; it consistently signaled the availability of insects (includes mealworms), and more so when this food could be seen but not consumed. Playback of Call C caused the marmosets to stop feeding on a less preferred food (banana) and, instead, go to inspect a location where mealworms had been found previously, providing evidence that it has referential meaning. No such immediate response was elicited on hearing Call A or background noise. Call A differed from C in that it was produced more frequently when the marmosets were consuming the food than when they could only see it, and call A showed no specificity between insects and fruit. Call B was emitted less frequently than the A or C calls and, by the marmosets that were tested alone, most often to crickets. An audience effect occurred, in that all three calls were emitted more often when the marmosets were tested alone than when in pairs. Recognition of the functional significance of marmoset calls can lead to improved husbandry of marmosets in captivity.

Raven food calls indicate sender\u2019s age and sex

BackgroundAcoustic parameters of animal signals have been shown to correlate with various phenotypic characteristics of the sender. These acoustic characteristics can be learned and categorized and thus are a basis for perceivers’ recognition abilities. One of the most demanding capacities is individual recognition, achievable only after repeated interactions with the same individual. Still, class-level recognition might be potentially important to perceivers who have not previously encountered callers but can classify unknown individuals according to the already learned categories. Especially for species with high fission-fusion dynamics that repeatedly encounter unknown individuals it may be advantageous to develop class-level recognition. We tested whether frequency-, temporal-, and amplitude-related acoustic parameters of vocalizations emitted by ravens, a species showing high fission-fusion dynamics in non-breeder aggregations, are connected to phenotypic characteristics and thus have the potential for class-level recognition.ResultsThe analysis of 418 food calls revealed that some components summarizing acoustic parameters were differentiated by age-classes and sex.ConclusionsTogether, the results provide evidence for the co-variation of vocal characteristics and respective sex and age categories, a prerequisite for class-level recognition in perceivers. Perceivers that are ignorant of the caller’s identity can thus potentially recognize these class-level differences for decision-making processes in feeding contexts.

Evidence for Dialects in Three Captive Populations of Common Marmosets (Callithrix jacchus)

The vocal repertoires of nonhuman primates have long been thought to be invariable across populations and not to result from vocal learning. However, increasing evidence suggests that learning does influence vocal production in nonhuman primates, and that several species modify the structure of their calls in response to social or environmental influences. Vocal usage learning refers to the process whereby an individual learns in which circumstances to produce a certain call type, whereas vocal production learning refers to the process in which signals get modified as the result of individual experiences. Common marmosets (Callithrix jacchus) show socially mediated vocal plasticity as adults and during vocal development. This propensity to engage in simple forms of vocal production learning (accommodation) should produce population-level differences in call structure. To test this prediction, we compared the vocalizations of three captive populations of common marmosets. We analyzed the acoustic structure of 1337 phee calls, 461 trills, and 3611 food calls and compared them with a permutated discriminant function analysis. We found that all call types differed significantly between the three populations, and 76–98% of the calls were correctly classified. As physical differences in body mass and environmental differences between colonies could not explain the call differences, we conclude that vocal accommodation is the most likely explanation for the differences in call structure. This will allow us to further investigate the role and importance of vocal learning in a species increasingly used to study vocal learning and language evolution.

Hens vary their vocal repertoire and structure when anticipating different types of reward

The vocalizations of nonhuman animals are considered potential indicators of motivational or internal state. In many species, different call types, and structural variation within call types, encode information about physical characteristics such as age or sex, or about variable traits such as motivation. Domestic chickens, Gallus gallus, have an elaborate vocal repertoire, enabling investigation into whether reward-related arousal is encoded within their call type and structure. Twelve hens were given a Pavlovian conditioning paradigm using sound cues to signal the availability of two food rewards (mealworms, normal food), one nonfood reward (a container of substrate suitable for dustbathing), and a sound-neutral event (sound cue, no reward). A muted-neutral treatment (no sound cue, no reward) provided a baseline for vocal behaviour. Sound cues preceded a 15 s anticipation period during which vocalizations were recorded. Hens produced a ‘Food call’ (previously defined in other studies) in anticipation of all rewards, including the nonfood reward. ‘Food calls’ and ‘Fast clucks’ were more prevalent in anticipation of rewards, and most prevalent following the cue signalling the dustbathing substrate, suggesting that this reward induced the most arousal in hens. The peak frequency of ‘Food calls’ made in anticipation of the dustbathing substrate was significantly lower than those made in anticipation of food rewards, potentially reflecting differences in arousal. Vocalizations that reliably indicate hens' motivational state could be used as measures of welfare in on-farm assessment situations. Our study is the first to reveal variation in the frequency-related parameters of the ‘Food call’ in different contexts, and to show the prevalence of different call types in reward and nonreward contexts, which may have implications for welfare assessments.

Referential signalling in birds: the past, present and future

Many species produce specific signals in response to environmental events. The specificity of these signals allows receivers to react appropriately to an event in the absence of other contextual cues. These functionally referential signals can be auditory, visual or multimodal and occur in antipredator, food and social cohesion contexts. In birds, acoustic signals used in antipredator defence are the most often studied. However, several species of birds produce functionally referential signals in other modalities, including gestures, and in other contexts, including food and social contact. The prevalence of functionally referential visual or multimodal signals may be underestimated. More research using innovative techniques is needed to test these signals. Food calls, particularly those produced during food provisioning, also require further study and may shed light on the ontogeny of food signals. Comparative studies across closely related species of birds may also reveal differences in the development of functionally referential versus motivational signals. Taken together, the type of research into functionally referential signals suggested herein will likely further our understanding of the ecological, social and physiological pressures that have shaped communication in birds.

Audience effects in chimpanzee food calls and their potential for recruiting others

One proposed benefit for the seemingly costly behaviour of food calling is the recruitment of social allies and mates by the signaller. In chimpanzees, food calls are only produced for approximately half of all feeding events. Therefore, we investigated the influence of social and ecological context on the probability of making a food call upon arriving to a food patch in a group of wild chimpanzees. First, we tested whether feeding events where food calls had been uttered did in fact attract more individuals to join the caller. Secondly, we examined the influence of two sources of audience effects: those who were physically present with the caller and those who were presumed nearby but out of sight, and thirdly the effect of various ecological factors. We found that when feeding on fruit species, events where food calls had been produced had a higher probability of group mates arriving, even whilst controlling for the effect of pant hoots. Furthermore, the probability of uttering a food call was motivated by social more than ecological context. Specifically, high-ranking males were more likely to make food calls when estrous females were nearby, while low-ranking males and females generally called more when more females were nearby, irrespective of their reproductive state. These effects were independent of the increase in food call probability when male callers were accompanied by more males. Our findings support the recruitment function of food calls and suggest that high-ranking males call to attract estrous females to food patches to obtain mating opportunities.

Human-Animal Relationships: The Use of Species-Typical Food Calls and Chimpanzee (Pan troglodytes) Names: Welfare-Oriented Tools to Manage Sanctuary Chimpanzees

Human-Animal Relationships: The Use of Species-Typical Food Calls and Chimpanzee (Pan troglodytes) Names: Welfare-Oriented Tools to Manage Sanctuary Chimpanzees

Come dine with me: food-associated social signalling in wild bottlenose dolphins (Tursiops truncatus).

Food-related signalling is widespread in the animal kingdom with some food-associated vocalizations considered functionally referential. Food calls can, however, vary greatly in the type of information they convey. Thus, there are a multitude of purposes for which food calls are used, including social recruitment, caller spacing, the indication of type, quantity, quality, divisibility of food, the caller's hunger level and even as tools to manipulate prey behaviour. Yet little work has focused on the social aspect of food calling in animals. We investigated the association of social signals in wild bottlenose dolphins with foraging behaviour where context-specific food-associated calls are commonly produced. Our data showed that specific social signals were significantly correlated with food call production and these calls rarely occurred in the absence of food calls. We suggest that animals are sharing additional information on the food patch itself with their social affiliates.

Wild chimpanzees modify food call structure with respect to tree size for a particular fruit species

The extent to which animal vocalizations are referential has long been debated since it reflects on the evolution of language. Our closest living relative, the chimpanzee, has been shown to have functionally referential food calls in captivity but evidence for such capabilities in the wild is lacking. We investigated the context specificity and function of West African chimpanzee, Pan troglodytes verus , food calls in the wild using all day focal follows of adult males and females of one habituated group in the Tai forest, Cote d’Ivoire. We collected over 750 h of observation and analysed 379 food calls produced for five different food species and found that higher pitched calls were produced for a single fruit species. Additionally, within this species, chimpanzees modified calls according to tree size, whereby smaller trees elicited higher pitched calls. Our results suggest that chimpanzees subtly vary the acoustic structure of food calls with respect to food patch size for a putatively highly valued fruit species, and we propose that arousal alone cannot sufficiently explain the patterns observed. Further work is needed to determine whether variation in food call pitch can influence receiver foraging behaviour. However, in light of our results, we propose that understanding the information content encoded by acoustic variation in chimpanzee food calls requires receiver knowledge about the natural ecological context, specifically spatial memory of tree locations. Therefore, this study highlights the potential significance of feeding ecology in the evolution of flexibly modulated vocal communication.

Do nestling Tree Swallows (Tachycineta bicolor) respond to parental alarm calls?

ABSTRACT Nestling birds use a conspicuous begging display, which includes loud begging calls, to solicit food from their parents. Although these calls are important in communicating offspring need, predators can use begging calls to locate nests. Parents may, however, counteract nestling vulnerability by giving alarm calls to silence calling nestlings when predators are nearby. This defense has been observed in grass- and reed-nesting species, whose nestlings beg to vibrational cues of a parent's arrival, even in the absence of the parents. It is considered less likely to occur, however, in cavity-nesting species, because the rigid substrate of the nest does not provide vibrational cues, and nestlings instead wait for a parental food call before begging. Cavity-nesting Tree Swallows (Tachycineta bicolor) use food calls to solicit begging, which suggests that parental alarm calls are not required to silence them. Older nestling Tree Swallows, however, beg in the absence of their parents, which suggests tha...

Jackdaw nestlings can discriminate between conspecific calls but do not beg specifically to their parents

The ability to recognize other individuals may provide substantial benefits to young birds, allowing them to target their begging efforts appropriately, follow caregivers after fledging, and establish social relationships later in life. Individual recognition using vocal cues is likely to play an important role in the social lives of birds such as corvids that provision their young postfledging and form stable social bonds, but the early development of vocal recognition has received little attention. We used playback experiments on jackdaws, a colonial corvid species, to test whether nestlings begin to recognize their parents’ calls before fledging. Although the food calls made by adults when provisioning nestlings were individually distinctive, nestlings did not beg preferentially to their parents’ calls. Ten-dayold nestlings not only responded equally to the calls of their parents, neighboring jackdaws whose calls they were likely to overhear regularly and unfamiliar jackdaws from distant nest boxes, but also to the calls of rooks, a sympatric corvid species. Responses to rooks declined substantially with age, but 20- and 28-day-old nestlings were still equally likely to produce vocal and postural begging responses to parental and nonparental calls. This is unlikely to be due to an inability to discriminate between calls, as older nestlings did respond more quickly and with greater vocal intensity to familiar calls, with some indication of discrimination between parents and neighbors. These results suggest that jackdaws develop the perceptual and cognitive resources to discriminate between conspecific calls before fledging but may not benefit from selective begging responses. Key words: begging, Corvidae, Corvus monedula, food calls, parental care, social cognition, vocal recognition.

Chimpanzee food calls are directed at specific individuals

If primates were capable of vocalizing to inform a receiver about an external entity, it would represent an important element of continuity with human language. We tested experimentally whether chimpanzee rough grunts, which function to refer to food, are produced selectively, indicating voluntary control, and whether they are directed at specific individuals. These are prerequisites for a system capable of actively informing others about external events. We conducted a field playback experiment in which we presented silently feeding male chimpanzees, Pan troglodytes , with arrival pant hoots of a familiar group member. We found that subjects were significantly more likely to respond with food calls to the simulated arrival of an individual with whom the caller had a high rather than low level of friendship and where there was a large rather than small positive dominance rank difference between the individuals (i.e. caller was lower ranking). We concluded that chimpanzee food calls are not simply reflexive responses to food, but can be selectively directed at socially important individuals. Our findings are thus inconsistent with traditional views of primate vocalizations as inflexibly and indiscriminately produced. Instead, our results indicate that great apes can produce semantically meaningful calls in a highly selective, recipient-directed manner. Further research is needed to test whether chimpanzees use this flexible system to inform ignorant individuals about food, but the prerequisites to support this type of communication seem to be present. • Field playback experiment shows chimpanzees direct food calls to specific recipients. • Male chimpanzees selectively produce calls for the arrival of high-ranking friends. • Functionally referential chimpanzee food calls are not reflexive responses to food. • Chimpanzees produce referential calls in a voluntary recipient-directed manner. • Challenges view that primate vocal production is inflexible and indiscriminate.

Bottlenose dolphins can use learned vocal labels to address each other

In animal communication research, vocal labeling refers to incidents in which an animal consistently uses a specific acoustic signal when presented with a specific object or class of objects. Labeling with learned signals is a foundation of human language but is notably rare in nonhuman communication systems. In natural animal systems, labeling often occurs with signals that are not influenced by learning, such as in alarm and food calling. There is a suggestion, however, that some species use learned signals to label conspecific individuals in their own communication system when mimicking individually distinctive calls. Bottlenose dolphins (Tursiops truncatus) are a promising animal for exploration in this area because they are capable of vocal production learning and can learn to use arbitrary signals to report the presence or absence of objects. Bottlenose dolphins develop their own unique identity signal, the signature whistle. This whistle encodes individual identity independently of voice features. The copying of signature whistles may therefore allow animals to label or address one another. Here, we show that wild bottlenose dolphins respond to hearing a copy of their own signature whistle by calling back. Animals did not respond to whistles that were not their own signature. This study provides compelling evidence that a dolphin's learned identity signal is used as a label when addressing conspecifics. Bottlenose dolphins therefore appear to be unique as nonhuman mammals to use learned signals as individually specific labels for different social companions in their own natural communication system.

The Social Function of Food‐Associated Calls in Male Chimpanzees

There is an ongoing debate about the adaptive function of chimpanzee's food-associated calls. Here, we tested a new hypothesis that food-associated calls in male chimpanzees function to signal that the calling individual is likely to initiate or prolong feeding. We propose that the signal functions to coordinate activities between individuals and that its ultimate function is to retain the nearby individuals in proximity. To test this hypothesis, we collected data on social and ecological correlates of food-associates calls in male chimpanzees. The results of this study, which was conducted on the Kanyawara community in the Kibale National Park, Uganda, show that males tended to feed for significantly longer after giving food-associated calls upon initiating feeding than after remaining silent. The type of audience had a significant effect on food calling, with males producing food-associated calls more often when males rather than females and preferred rather than neutral male social partners were in close proximity. However, the total party or male party size did not correlate with food calling behaviors, suggesting that the signal "targets" those in close proximity. Finally, a male feeding partner was more likely to remain with the focal until the end of a feeding bout after the focal gave a food-associated call at the beginning of the feeding bout than when he was silent. These results support our hypothesis and suggest that one of the functions of food calling in chimpanzees might be signaling that the caller is likely to initiate and prolong a feeding bout. This information might be used by receivers to make the decision whether or not to stay with the calling individual on a feeding patch or leave him (fission). The study suggests therefore that ultimately the function of food calling might be to coordinate feeding behaviors between males.

Who wants food? Individual characteristics in raven yells

Discriminating between different individuals is considered as prerequisite for any forms of social knowledge. In birds, discriminating between conspecifics based on individual characteristics has been tested mainly in the auditory domain with territorial calls and songs for neighbour and kin discrimination but little is known about discriminating between signallers in food calls. Ravens utilize a large set of calls and show individually distinctive call repertoires. Moreover, they show advanced social tactics during foraging, suggesting that they are capable of dealing with conspecifics on an individual basis. When confronted with food that is difficult to access, ravens produce particular calls (‘haa’, yells); these calls attract other ravens and, thus, have been hypothesized to serve as ‘functionally referential signals’. We here examined whether ravens are able to differentiate between individuals on the basis of these food calls. We first analysed individual differences in call parameters, using 424 food calls recorded from 18 individually marked wild ravens in the Austrian Alps. We then tested 18 captive ravens for recognition of individual differences in food calls with playbacks, using a habituation-dishabituation design. We found evidence that food calls show individual call characteristics in fundamental frequency and intensity-related measurements providing ravens with the opportunity to respond according to these individually distinct features. Furthermore, ravens discriminated between unfamiliar ravens in the habituation-dishabituation experiment, indicating that they may discern individual differences. Our results suggest that raven food calls are individually distinct and that the birds may be capable of differentiating between food-calling individuals.

Possible use of heterospecific food-associated calls of macaques by sika deer for foraging efficiency

Heterospecific communication signals sometimes convey relevant information for animal survival. For example, animals use or eavesdrop on heterospecific alarm calls concerning common predators. Indeed, most observations have been reported regarding anti-predator strategies. Use of heterospecific signals has rarely been observed as part of a foraging strategy. Here, I report empirical evidence, collected using playback experiments, showing that Japanese sika deer, Cevus nippon, use heterospecific food calls of Japanese macaques, Macaca fuscata yakui, for foraging efficiency. The deer and macaques both inhabit the wild forest of Yakushima Island with high population densities and share many food items. Anecdotal observations suggest that deer often wait to browse fruit falls under the tree where a macaque group is foraging. Furthermore, macaques frequently produce food calls during their foraging. If deer effectively obtain fruit from the leftovers of macaques, browsing fruit fall would provide a potential benefit to the deer, and, further, deer are likely to associate macaque food calls with feeding activity. The results showed that playback of macaque food calls under trees gathered significantly more deer than silence control periods. These results suggest that deer can associate macaque food calls with foraging activities and use heterospecific calls for foraging efficiency.

Acoustic variability and individual distinctiveness in the vocal repertoire of red-capped mangabeys (Cercocebus torquatus).

Acoustic variability and individual distinctiveness of vocal signals are expected to vary with both their communicative function and the need for individual recognition during social interactions. So far, few attempts have been made to comparatively study these features across the different call types within a species' vocal repertoire. We collected recordings of the six most common call types from 14 red-capped mangabeys (Cercocebus torquatus) to assess intra- and interindividual acoustic variability, using a range of temporal and frequency parameters. Acoustic variability was highest in contact and threat calls, intermediate in food calls, and lowest in loud and alarm calls. Individual distinctiveness was high in contact, threat, loud and alarm calls, and low in food calls. In sum, calls mediating intragroup social interactions were structurally most variable and individually most distinctive, highlighting the key role that social factors must have played in the evolution of the vocal repertoire in this species. We discuss these findings in light of existing hypotheses of acoustic variability in primate vocal behavior.

The central importance of information in studies of animal communication

The concept of information plays a central role in studies of animal communication. Animals’ responses to the calls of different individuals, to food calls, alarm calls, and to signals that predict behaviour, all suggest that recipients acquire information from signals and that this information affects their response. Some scientists, however, want to replace the concept of information with one based on the ‘manipulation’ of recipients by signallers through the induction of nervous-system responses. Here we review both theory and data that argue against hypotheses based exclusively on manipulation or on a fixed, obligatory link between a signal’s physical features and the responses it elicits. Results from dozens of studies indicate that calls with ‘arousing’ or ‘aversive’ features may also contain information that affects receivers’ responses; that acoustically similar calls can elicit different responses; acoustically different calls can elicit similar responses; and ‘eavesdropping’ animals respond to the relationship instantiated by signal sequences. Animal signals encode a surprisingly rich amount of information. The content of this information can be studied scientifically.

Influence of Nest Deprivation on Behaviour, Hormonal Concentrations and on the Ability to Resume Incubation in Domestic Hens (Gallus domesticus)

In this study, we investigated the influence of the length of nest deprivation period (3 vs. 6 d) on the ability to renest of incubating hens. We focused on the hens' behaviour, particularly on nesting and calls, on their prolactin, luteinizing hormone (LH) and oestradiol concentrations. Nest deprivation induced a drop of prolactin and an increase of LH plasmatic concentrations in hens. These changes in circulating pituitary hormones were followed by changes in ovarian function: the persistent rise of plasmatic oestradiol gave evidence of the resumption of ovarian activity. After nest deprivation, the number of clucks increased significantly and food calls appeared; these results demonstrate that ‘maternal’ calls can be emitted outside the maternal context. Our results suggest that the onset of typical maternal calling is strongly controlled by internal state such as plasmatic hormonal concentrations, independently of social stimulation. None of the 10 hens deprived for 6 d resumed incubation when given the opportunity, whereas, after a 3 d deprivation period, three out of 10 hens renested and two hens incubated sporadically and then gradually abandoned their nests. Long periods of nest deprivation appear to disrupt the habits of sitting and nesting. Before nest reopening, all the hens presented low levels of plasmatic prolactin. Plasma prolactin concentrations of the renesting hens increased after nest boxes were reopened and returned to levels found in incubating hens. We suggest that pituitary prolactin rather than plasmatic prolactin is responsible for the maintenance of incubating potential in hens deprived of their nests.