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 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 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.     

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.     

Female preference in complex acoustical environments in the midwife toads Alytes obstetricans and Alytes cisternasii

Gravid females of Alytes obstricans and Alytes cisternasii weretested with synthetic calls in seven-speaker playback tests.A first, "mean-centered" test presented calls with frequenciesrepresenting an array of different calls spanning over the rangeof the population (±2.25 SD). In this test, females ofboth species approached a synthetic call that was lower thanthe average call frequency of the male population although thedifference was significant only for A. obstetricans. The regressionbetween female weight and size and preferred frequency was notsignificant in either species. These results confirm the reportedtrends of females preferring lower frequency calls (correspondingto larger males) based on two-speaker playback tests for A.obstetricans. For A. cisternasii, the lack of significance ofthe seven-speaker test suggests that the preference trend previouslyfound in two-speaker tests may be obscured in more complex acousticalenvironments. A second "supernormal stimulus" test presentedfemales with calls ranging from the lowest frequency valuesof the male population (–2.25 SD) and lower, up to –6.75SD beyond the range. In both species females preferentiallyapproached calls higher than the mean frequency of the stimuluspresented. This result suggests that in both cases selectionfor low frequencies is not open ended, and that the preferredfrequency is within the range of the male population.     

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.     

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 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.     

Call Intensity and Female Preferences in the European Green Toad

In the present paper we study the pattern of variation in call intensity in a natural population of the European green toad (Bufo viridis), and we analyse females preferences for this property by means of playback experiments. Although call sound pressure level (SPL) shows little within‐bout variation, we found significant positive correlation between call SPL and fundamental frequency: on average, an increase of 6 dB SPL produces a 100‐Hz increase in fundamental frequency. When females were given a choice between two calls differing by 10 and 6 dB SPL, they significantly preferred the loudest call, whereas they did not discriminate between calls differing by 3 dB. To test whether a 3‐dB difference reflects a sensory or behavioural limit, we carried out three experiments where females were given a choice between two calls differing in both duration (4 s and 6 s, respectively) and SPL (3 dB). In all three experiments, the longer call attracted a larger number of females, but the 3‐dB difference did not show any significant effect. Finally, we investigated the relationships between call intensity and frequency on female preferences. Previous experiments showed size‐dependent preferences for calls with lower‐than‐average frequencies (1.3 kHz) over calls with higher‐than‐average frequencies (1.6 kHz). Here, we show that this weak preference is abruptly reversed when the highest‐pitched call is broadcast at an intensity 6 dB higher than the alternative.     

The relationship between perception and production in songbird vocal imitation: what learned calls can teach us

Songbirds produce calls as well as song. This paper summarizes four studies of the zebra finch long call, used by both sexes in similar behavioral contexts. Female long calls are acoustically simpler than male long calls, which include acoustic features learned during development. Production of these male-typical features requires an intact nucleus robustus archistriatalis, the sexually-dimorphic source of the telencephalic projection to brainstem vocal effectors. In experiments that quantified the long calls produced in response to long call playbacks, intact adult zebra finch males, but not females, show a categorical preference for the long calls of females over those of males. Experiments with synthetic stimuli showed that males classify long call stimuli that they hear by gender, using both spectral and temporal information, but that females use only temporal information. Juvenile males (<45 days) did not show the categorical preference, but it emerged during the same period when the robustus archistriatalis matures anatomically and the first male-typical vocalizations are produced. Adult males with robustus archistriatalis lesions lost the categorical preference for female long calls, suggesting that the robustus archistriatalis plays a role in long call discrimination. These results demonstrate that calls complement song as a potent tool for studying the neurobiology of vocal communication.     

The structure and usage of female and male mouse ultrasonic vocalizations reveal only minor differences

Ultrasonic vocalizations (USV) of mice are increasingly recognized as informative dependent variables in studies using mouse models of human diseases. While pup vocalizations primarily serve to re-establish contact with the mother, adult male "songs" were considered to be courtship signals. Alternatively, mouse USVs may generally function as territorial signals. To distinguish between these two hypotheses, we compared the structure and usage of adult male and female USVs in staged resident-intruder encounters. If calls function primarily as courtship signals, males should respond stronger than females, specifically when presented with a female intruder. Refuting this hypothesis, we found that in response to female intruders, females called more than males (228±32 calls/min vs. 71±15 calls/min), and males called more to female than to male intruders (14±7.5 calls/min). There were no significant differences in the acoustic characteristics of the calls given by females and males. To control for the influence of the intruder's behavior on calling, we repeated the experiments using anaesthetized intruders. Again, females produced more calls to female than male intruders (173±17 calls/min vs. 71±15 calls/min), while males called more in response to female than male intruders (39±17 calls/min), and there were no acoustic differences in female and male calls. The vocal activity did not differ significantly with regard to intruder state (awake or anaesthetized), while the acoustic structure exhibited significant differences. Taken together, our findings support the view that calls do not mainly function as courtship signals, although they might serve both a territorial (sex-independent) and a courtship function. The comparison of responses to awake vs. anaesthetized intruders suggests that the latter are sufficient to elicit vocal activity. The subtle acoustic differences, however, indicate that the subject differentiates between intruder states.     

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.     

Contexts and behavioral correlates of trill vocalizations in wild white-faced capuchin monkeys (Cebus capucinus)

Primate vocalizations that appear to occur independently of specific contexts typically are considered to be contact calls. However, results from several recent studies indicate that these calls function to facilitate social interactions. White-faced capuchin monkeys (Cebus capucinus) emit a high-frequency vocalization, termed a "trill," in social interactions and during travel. In this study, immatures emitted most trills, but adult females also trilled; by contrast, adult males rarely trilled. Infants emitted the majority of trills, and they trilled at significantly higher rates than adult females. Infants trilled most when approaching other individuals. Furthermore, infants emitted proportionately more trills than other age classes when approaching other individuals. I therefore focused on the detailed context and immediate behavioral correlates of trilling by infants. Infants that trilled when approaching others tended to interact affiliatively with them subsequently (i.e., climbing on, touching, receiving grooming, and performing food inspection) more than infants that did not trill when approaching. Therefore, infant trilling may have had an immediate effect on the recipient's behavior.     

Responses to natural and synthetic phee calls by common marmosets (Callithrix jacchus)

Captive adult common marmosets (Callithrix jacchus) produce whistlelike “phee” calls in two contexts: in the home cage, where phee calls may function as part of territorial marking behavior, and when separated from social companions, where phee calls may function to reunite conspecifics. Natural and synthesized calls representing the acoustic structure of male and female calls in each context were presented to adult marmosets in a playback paradigm. Marmosets demonstrated discriminative abilities according to the context of the call and the caller's sex. Vocal and behavioral responses indicated increased vigilance and territorial behavior, following playbacks of naturally produced calls as well as synthetic calls. All animals scanned more frequently following produced calls as well as synthetic calls. All animals scanned more frequently following natural home cage as well as isolation calls, but only increased contact behavior (trills) in response to home cage calls. The responses were dimorphic according to the sex of the caller, where adult males scanned more following male calls, and adult females were more aggressive following male and female calls. The differential behavioral responses to playbacks of marmoset phee calls suggest a biological relevance to subtle differences found in the acoustic parameters of the phee call. © 1994 Wiley-Liss, Inc.

1 This article is a US Government work and, as such, in the public domain in the United States of America.

     

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.     

Reproductive isolation inProkelisia planthoppers (Homoptera: Delphacidae): Acoustic differentiation and hybridization failure

Males and females of Prokelisia marginata (Van Duzee) and Prokelisia dolusWilson communicate through substrate-transmitted vibrations. The acoustic signals (attraction and courtship calls) of these planthoppers are effective in mate location, attraction, and mate choice. Attraction calls are structurally distinct for both species and differ in pulse type, pulse repetition rate, and pulse duration. Using playback of prerecorded calls, individuals discriminated between conspecific and heterospecific signals. Depending on the sex and species, response calls were produced three to eight times more frequently to conspecifics than to heterospecifics. However, acoustic signals alone did not explain reproductive isolation and hybridization failure in these two congeners. Some heterospecific pairs called, courted, and attempted to join genitalia, but no connections were successful and no progeny were produced. Thus, acoustic behavior is not a guaranteed premating isolating mechanism in no-choice situations. Other courtship behaviors and possibly morphological differences in genitalia also contributed to their isolation. Females displayed a variety of rejection behaviors to conspecific and heterospecific males, suggesting that sexual selection (female choice), in addition to species recognition, may be an important force in the evolution of the acoustic signals of planthoppers. Although signal structure was not dependent on wing form (planthoppers exhibit wing dimorphism), the age when females first began to call was related to wing form. Brachypterous (flightless) females of both species began calling early in adult life (day 2), whereas macropterous (migratory) females began calling later in adult life (day 6). This pattern is consistent with the oogenesis-flight syndrome, in which reproductive maturity is delayed until after migration occurs.     

Development of Early Vocalizations and the Chick-a-dee Call in the Black-capped Chickadee,Parus atricapillus

The chick-a-dee call of the black-capped chickadee (Parus atricapillus) is composed of discrete elements, or notes, that are combined to form hundreds of different calls. To investigate the development of this complex call, 12 families of color-marked chickadees were observed and recorded in the wild. Vocalizations were monitored for 18 d in the nest and 14–18 d postfledging. Most vocalizations of nestlings and fledglings were associated with feeding. At hatching, vocalizations consisted of a structurally simple note type that became more complex and variable with age. Around 9–12 d, the development of the call occurred, when single notes became organized into a multiple-note unit. Notes within the call differentiated into higher frequency, rapidly modulated initial note types and a lower frequency, moderately modulated terminal note type, features also present in adult chick-a-dee calls. Several adult-like calls including chick-a-dee calls, fee-bee songs, and a subsong-like vocalization developed prior to fledgling dispersal. Based on resemblances of note structure and general call structure, the chick-a-dee call appeared to develop from calls of nestlings and fledglings, although not necessarily in a chronologically linear progression. Some features of the chick-a-dee call closely resembled features of older nestling and fledgling calls, while other features more closely resembled the sounds of very young nestlings. Vocal development in the chickadee is compared with song and call development in other species, and the possible significance of acoustic resemblances between chick-a-dee calls and the food-associated calls of nestlings and fledglings is discussed.     

Feeding experience and relative size modify the begging strategies of nestlings

The offspring of birds and mammals use a combination of movementsand vocalizations, known as begging, to solicit food from theirparents. A widespread interpretation of begging is that itconstitutes an honest signal of offspring need. But we knowthat in the house sparrow (Passer domesticus) the intensityof begging calls reflects the past experience of offspringin addition to their need. Here we show that this result generalizesto other species. An experiment with hand-reared magpies (Pica pica) and great spotted cuckoos (Clamator glandarius) indicates that the begging strategies depend on the past experience ofchicks and the composition of their brood. In asynchronoustwo-magpie broods, both chicks begged at the same intensitywhen the large chick obtained food more easily than its sibling,but the large chick begged at higher intensity when it was easier for the smaller chick to obtain food. Cuckoo chicks beggedat higher intensity than magpies.     

Differences in preference for species-specific female calls between acoustically experienced and acoustically naive maleRibautodelphax planthoppers (Homoptera: Delphacidae)

Males of the planthopper Ribautodelphax imitanswere exposed to playbacks of either conspecific or heterospecific (R. imitantoides)female calls during their development from egg to adult, and thereafter these, as well as naive males,were offered a two- way choice between these calls. Males of all treatments approached the conspecific call significantly more often. However, males primed by the conspecific call chose the heterospecific call almost four times less often than did males primed by heterospecific calls or naive males, thus showing that the preference for conspecific calls can be partly learned. Males primed by heterospecific calls performed very similarly to completely naive males, suggesting that the signal recognition mechanism is much less sensitive to heterospecific calls than to conspecific calls. Males with experience of the conspecific female call tended to take more time to reach the call source in the trials than both other types of males. The evolutionary implications of these findings are discussed.     

Preferred males are not always good providers: female choice and male investment in tree crickets

Female tree crickets (Oecanthus nigricornis) prefer large malesbut do not receive larger glandular courtship gifts from thesemales. This finding is puzzling from both the male and femaleperspectives, because females should prefer males providingmore direct benefits, and because males who provide larger giftsachieve higher insemination success. We tested for differencesin the quality of male secretions and found that larger malesprovided more proteinaceous food gifts than did rivals, whichcould explain why they are preferred by females. The preferencein turn could cause depletion of food gift reserves in favoredmales, because natural remating rates are high and because evena single feeding bout negatively affects glandular stores. Mostintriguingly, we showed that preferred males can adaptivelydecrease the size of courtship food-gifts provided (in orderto conserve gifts for future mating events) when they perceivethat the probability of multiple future mating opportunitiesis high. Thus, the elevated mating rates of preferred males(both before and after a focal mating event) could account forthe small size of their courtship food-gifts.