Individual vocal signatures in barn owl nestlings: does individual recognition have an adaptive role in sibling vocal competition?

To compete over limited parental resources, young animals communicate with their parents and siblings by producing honest vocal signals of need. Components of begging calls that are sensitive to food deprivation may honestly signal need, whereas other components may be associated with individual‐specific attributes that do not change with time such as identity, sex, absolute age and hierarchy. In a sib–sib communication system where barn owl (Tyto alba) nestlings vocally negotiate priority access to food resources, we show that calls have individual signatures that are used by nestlings to recognize which siblings are motivated to compete, even if most vocalization features vary with hunger level. Nestlings were more identifiable when food‐deprived than food‐satiated, suggesting that vocal identity is emphasized when the benefit of winning a vocal contest is higher. In broods where siblings interact iteratively, we speculate that individual‐specific signature permits siblings to verify that the most vocal individual in the absence of parents is the one that indeed perceived the food brought by parents. Individual recognition may also allow nestlings to associate identity with individual‐specific characteristics such as position in the within‐brood dominance hierarchy. Calls indeed revealed age hierarchy and to a lower extent sex and absolute age. Using a cross‐fostering experimental design, we show that most acoustic features were related to the nest of origin (but not the nest of rearing), suggesting a genetic or an early developmental effect on the ontogeny of vocal signatures. To conclude, our study suggests that sibling competition has promoted the evolution of vocal behaviours that signal not only hunger level but also intrinsic individual characteristics such as identity, family, sex and age.     

No need to shout: Effect of signal loudness on sibling communication in barn owls Tyto alba

In animal communication, signal loudness is often ignored and seldom measured. We used a playback experiment to examine the role of vocal loudness (i.e., sound pressure level) in sibling to sibling communication of nestling barn owls Tyto alba. In this species, siblings vocally negotiate among each other for priority access to parental food resources. Call rate and call duration play key roles in this vocal communication system, with the most vocal nestlings deterring their siblings from competing for access to the food item next delivered by parents. Here, we broadcast calls at different loudness levels and call rate to live nestlings. The loudness of playback calls did not affect owlets' investment in call rate, call duration or call loudness. The rate at which playback calls were broadcast affected owlets' call rate but did not influence their response in terms of loudness. This suggests that selection for producing loud signals may be weak in this species, as loud calls may attract predators. Moreover, given that owlets do not overlap their calls and that they communicate to nearby siblings in the silence of the night, loud signals may not be necessary to convey reliable information about food need.     

Primate phonation: Anterior cingulate lesion effects on response rate and acoustical structure

Four juvenile rhesus monkeys (Macaca mulatta) that were conditioned to emit a discriminative vocal response underwent unilateral and bilateral lesions of anterior cingulate gyrus in stepwise sequence. Pre- and post-lesion measures of vocal response rate and acoustical features (call duration, amplitude, and fundamental frequency) were obtained for the conditioned task and for vocalization in the home colony (spontaneous vocalization). Unilateral lesions produced little consistent change in spontaneous “coo” vocalization rate and call duration. Conditioned vocalization of the monkeys exhibited no significant change in rate at this stage, although call duration was reduced significantly. Bilateral lesions produced no further modifications in acoustic properties of spontaneous calls, while the vocal rate decreased slightly. Conditioned calls were not significantly altered in acoustic features at this stage, although the discriminative vocalization rate was significantly decreased for all monkeys. The results indicate limited control over vocal motor systems by anterior cingulate cortex, while suggesting that this region participates in initiation of voluntary phonation.     

Barn owl (Tyto alba) siblings vocally negotiate resources

Current theory proposes that nestlings beg to signal hunger level to parents honestly, or that siblings compete by escalating begging to attract the attention of parents. Although begging is assumed to be directed at parents, barn owl (Tyto alba) nestlings vocalize in the presence but also in the absence of the parents. Applying the theory of asymmetrical contests we experimentally tested three predictions of the novel hypothesis that in the absence of the parents siblings vocally settle contests over prey items to be delivered next by a parent. This 'sibling negotiation hypothesis' proposes that offspring use each others' begging vocalization as a source of information about their relative willingness to contest the next prey item delivered. In line with the hypothesis we found that (i) a nestling barn owl refrains from vocalization when a rival is more hungry, but (ii) escalates once the rival has been fed by a parent, and (iii) nestlings refrain from and escalate vocalization in experimentally enlarged and reduced broods, respectively. Thus, when parents are not at the nest a nestling vocally refrains when the value of the next delivered prey item will be higher for its nest-mates. These findings are the exact opposite of what current models predict for begging calls produced in the presence of the parents.     

Sib‐sib communication and the risk of prey theft in the barn owl Tyto alba

Conflicts among siblings are widespread and their resolution involves complex physical and communication tools. Observations in the barn owl Tyto alba showed that siblings vocally communicate in the absence of parents to negotiate priority of access to the impending food resources that parents will bring. In the present paper, we hypothesize and provide correlative evidence that after a parent brought a food item to their progeny, sibling competition involves vocal sib‐sib communication. A food item takes a long time to be entirely consumed, and hence siblings continue to compete over prey monopolization even after parents gave a food item to a single offspring. When physical competition is pronounced and thereby the risk of prey theft is high, the individual that received a prey item consumes it in a concealed place. Concomitantly, nestlings vocalize intensely probably to indicate their motivation to siblings to not share their food item, since this vocal behaviour was particularly frequent in younger individuals for which the risk of being robbed is higher than in their older siblings. Furthermore, nestlings consumed more rapidly a food item when their siblings vocalized intensely presumably because the intensity of siblings’ vocalizations is associated with a risk of prey theft. Our correlative study suggests that sibling competition favoured the evolution of sib‐sib communication under a wide range of situations.     

Interleukin-1 induces sleep-like behavior and alters call structure in juvenile rhesus macaques

To date, there have been no investigations of the behavioral effects of interleukin-1 (IL-1) in nonhuman primates. In this study the locomotor behavior and vocalizations of juvenile rhesus monkeys were monitored for 45 minutes following intravenous injections of recombinant human IL-1 alpha. In addition, their reaction to a broadcasted recording of infant monkey distress calls was determined 20 minutes after the beginning of each test session. IL-1 induced sleep-like inactivity and significantly diminished the monkey's behavioral and vocal responses to the broadcasted calls. The coo calls uttered by the monkeys following IL-1 treatment also had a longer duration and lower fundamental frequency than calls during the control condition. As several studies have indicated that behavioral effects of IL-1 may be mediated by corticotropin-releasing hormone (CRH), a second group of rhesus monkeys was given injections of CRH. CRH did not alter behavior or call structure at the dose administered. These results extend previous research on the behavioral effects of IL-1 to include the nonhuman primate and provide the first evidence that cytokines can affect vocal communication in rhesus monkeys. © 1995 Wiley-Liss, Inc.     

Corticosterone Promotes Scramble Competition Over Sibling Negotiation in Barn Owl Nestlings (Tyto alba)

In species with parental care, siblings compete for access to food resources. Typically, they vocally signal their level of need to each other and to parents, and jostle for the position in the nest where parents deliver food. Although food shortage and social interactions are stressful, little is known about the effect of stress on the way siblings resolve the conflict over how food is shared among them. Because glucocorticoid hormones mediate physiological and behavioral responses to stressors, we tested whether corticosterone, the main glucocorticoid in birds, modulates physical and vocal signaling used by barn owl siblings (Tyto alba) to compete for food. Although corticosterone-implanted (cort-) nestlings and placebo-nestlings were similarly successful to monopolize food, they employed different behavioral strategies. Compared to placebo-nestlings, cort-individuals reduced the rate of vocally communicating with their siblings (but not with their parents) but were positioned closer to the nest-box entrance where parents predictably deliver food. Therefore, corticosterone induced nestlings to increase their effort in physical competition for the best nest position at the expense of investment in sib?Csib communication without modifying vocal begging signals directed to parents. This suggests that in the barn owl stress alters nestlings?? behavior and corticosterone could mediate the trade-off between scramble competition and vocal sib?Csib communication. We conclude that stressful environments may prevent the evolution of sib?Csib communication as a way to resolve family conflicts peacefully.     

Similarity in the begging calls of nestling Red‐winged Blackbirds

ABSTRACT Although individually distinct begging calls may permit parents to recognize their offspring, birds nesting in dense breeding colonies where fledglings intermingle might benefit from additional adaptations. For example, if the calls of all nestlings in a brood were similar, parents would need to recognize only one brood call instead of the identity calls of each nestling. We recorded nestling Red‐winged Blackbirds (Agelaius phoeniceus) to determine whether their calls function to identify individuals (identity call hypothesis) or broods (brood call hypothesis). We used spectrogram cross‐correlation and dynamic time warping as well as call duration, peak frequency, and frequency range to estimate the similarity of begging calls of nestling Red‐winged Blackbirds. We recorded individual nestlings on day 5 and on day 9 of the nestling period to determine whether calls of individuals were more similar than calls of different nestlings, and whether calls of broodmates were more similar than calls of nestlings from different broods. We found that calls of 8‐d‐old individuals were more similar than calls of different nestlings, but the calls of broodmates were not more similar than those of nestlings from different broods. These results were consistent with the identity call hypothesis. We then compared begging calls of pairs of nestlings recorded separately and together on day 9. We found that the calls of 8‐d‐old nestlings recorded together were more similar than when they were recorded separately. In addition, using playback of begging calls from normal broods and artificial “broods” constructed from the calls of single nestlings, we found that females returned with food sooner in response to the calls of single nestlings (with enhanced call similarity) than to those of normal broods. Our results suggest that similar begging calls may be beneficial for both nestlings and parents, with broodmates fed at higher rates when their calls are more similar and, after fledging, parents needing to recognize only one brood call instead of the identity calls of each fledgling.     

Are Tropical Highland Frog Calls Cold–adapted? The Case of the Andean Frog Hyla labialis1

Across a wide range of temperatures established in the laboratory, we tape–recorded the advertisement calls of 76 freshly caught Hyla labialis males from three elevationally separated populations in the Eastern Andes of Colombia. Each male was tested once at a single temperature and returned to his capture site after measurement of his snout–vent length. We measured and averaged three characteristics of five to ten successive calls for each individual: number of pulses per call, pulse repetition rate, and call duration. We found that calling activity occurred within temperature ranges that overlapped among frogs from different elevations, but widened and shifted downward with increasing altitude of origin. Males from all sites called at temperatures higher, but not lower, than those naturally occurring during their nightly activity period. No decline in vocal performance was apparent when frogs extended their calling activity into the range of high temperatures selected for basking. Both snout–vent length and temperature affected pulse repetition rate and call duration, while the number of pulses per call was temperature–independent. Compared to the smaller males from lower elevations, the larger, high–mountain males had calls with significandy more pulses, a lower pulse repetition rate, and longer duration. Within each population, rising temperatures caused pulse repetition rate to increase and call duration to decrease significantly, whereas the number of pulses per call remained unchanged. Pulse repetition rate of highland males was the factor least affected by temperature, and it was less sensitive to night temperatures than to day temperatures. This, together with their capacity to call at low temperatures, suggests that highland frog calls are cold adapted.     

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.     

Vocal repertoire of cooperatively breeding Smooth‐billed Anis

Calls are functionally diverse signals that mediate behavior in a wide variety of contexts in both passerines and non‐passerines. However, the call‐based acoustic communication systems of non‐passerines have received less attention from investigators than those of passerines. We examined the vocal repertoire of Smooth‐billed Anis (Crotophaga ani), cooperatively breeding cuckoos that live in groups with multiple breeding pairs. We recorded calls from 22 groups over two breeding seasons at the Cabo Rojo National Wildlife Refuge in Puerto Rico. We identified 11 call types and one group vocalization, and used an automated sound measurement program to quantify their acoustic features. Discriminant function analysis (DFA) correctly classified 74.2% of calls based on these features. The vocal repertoire of Smooth‐billed Anis is larger than that reported for the three other species in the subfamily Crotophaginae. Smooth‐billed Anis have at least two alarm calls, two nest‐specific calls, and one nest defense call. We also identified one possible signal of aggressive intent, one possible appeasement signal, and two calls that may communicate identity. The relatively large vocal repertoire of Smooth‐billed Anis and association of distinct call types with different functions and contexts supports the main prediction of the social complexity hypothesis, i.e., species with more complex social systems will have more complex communication systems.     

燕雀丘间复合体背内侧核对叫声的调控模式

鸣禽鸟的基本发声中枢——丘间复合体背内侧核(nucleus dorsalis medialis of the intercollicular complex,DM)对叫声的调控模式是诱发单次叫声。应用电生理与声学分析相结合的方法研究鸣禽鸟燕雀(Fringilla montifringilla)DM核团对声音调控的模式。经语图和频谱图分析,结果显示：燕雀左侧DM诱发单次叫声的声长和主能量区的带宽分别为右侧DM诱发叫声的2倍和1．7～3．1倍,提示燕雀DM对叫声声长和声强的调控能力,均呈明显的左侧优势。这与高级发声中枢(high vocal center,HVC)和古纹状体粗核(nucleus robustus archistriatalis,RA)等发声控制核团在控声模式中具有左侧优势的特征相似,从而为鸣禽发声控制通路高、低级中枢具有内源投射关系提供了声学上的证据。     

Dual Function of Chip Calls Depending on Changing Call Rate Related to Risk Level in Territorial Pairs of White‐Eared Ground‐Sparrows

Different mechanisms have been proposed for encoding information into vocalizations: variation of frequency or temporal characteristics, variation in the rate of vocalization production, and use of different vocalization types. We analyze the effect of rate variation on the dual function of chip calls (contact and alarm) produced by White‐eared Ground‐sparrows (Melozone leucotis). We conducted an acoustic playback experiment where we played back 1 min of four chip call rates (12, 36, 60, 84 calls/min). We measured the response of territorial pairs using behavioral responses, and fine structural features of calls produced in response to those playbacks. White‐eared Ground‐sparrows showed more intense behavioral responses to higher than lower call rate playbacks. Both individuals of the pair approached the source of the playback stimulus faster, produced the first vocalization faster, produced more vocalizations, and spent more time close to the stimulus in higher call rate than in lower call rate playbacks. Frequency and duration characteristics of calls (chip and tseet) were similar in response to all call rate playbacks. Our playback experiment elicited different intensity of behavioral responses, suggesting that risk‐based information is encoded in call rate. Our results suggest that variation in the rate of chip call production serves a dual function in this species; calls are used at lower rates for pair contact and at higher rates for alarm/mobbing signals.     

Vocal behavior of Great Curassows,a vulnerable Neotropical bird

ABSTRACT The Cracidae rank among the most threatened families of Neotropical birds, and studies of their vocal behavior may help guide conservation and monitoring efforts. We describe the vocal behavior of Great Curassows (Crax rubra), a little‐studied Cracid species currently listed as vulnerable. From 2008 to 2010, we recorded curassows in northwest Costa Rica using both handheld and automated digital recorders. Analysis of recordings revealed that Great Curassows had a vocal repertoire of five call types. Yip and bark calls are sex‐specific alarm calls of short duration (0.12 and 0.08 s, respectively). The descending whistle is a longer duration alarm call (2.18 s) produced primarily by males. The snarl is a short call (0.67 s) associated with a threat display produced by adults with dependent young. The boom call was the most common Great Curassow vocalization, and was given only by males. Boom calls are long (8.86 s), low‐frequency (<150 Hz), multisyllable calls comprised of four stereotyped phrases. Great Curassows often uttered boom calls well before dawn, with a peak in activity at dawn and the hours following. Males produced bouts of repeated boom calls that lasted an average of 35 min, but sometimes continued for more than 5 h. Boom calls were given from February to June, with a peak in late April and early May when breeding begins. Discriminant analysis of boom calls of birds from 10 different locations revealed interindividual variation in call structure that may be useful for bioacoustic monitoring of individuals. Our results suggest that automated recorders might provide a way to monitor the abundance of male curassows because their boom calls are given frequently during the period from February to June and can be detected at distances up to 250 m.     

Hopeless solicitation? Host-absent vocalization in the common cuckoo has no effect on feeding rate of reed warblers

Begging behavior of nestlings can signal both hunger and competitive ability. Studies of begging in evicting avian brood parasites exclude the influence of nestling competition and may provide new insights into the host–parasite conflict and the evolution of signaling. Apart from the begging call, common cuckoo Cuculus canorus nestlings use special vocal displays in the absence of their hosts, termed here host-absent vocalization (HAV). Since these conspicuous calls can increase the risk of predation and require energy, their costs should be balanced by some benefits, such as increased food provisioning. However, there has been no evidence that chicks convey information about their hunger by HAV. We therefore tested experimentally whether cuckoo chicks use HAV as an additional signal to enhance food-delivery rate by their hosts. We used playback of HAV recorded from cuckoo nestlings to determine whether their hosts, reed warblers Acrocephalus scirpaceus, increase their provisioning in response to an apparent increase in HAV. Older chicks spent more time in HAV than younger chicks, suggesting that HAV is not caused by inaccurate discrimination of host arrival stimuli. Negative correlation of HAV with feeding rate and mass gain between the two experiments suggested that hunger was the motivation of HAV. The playback experiment, however, did not prove that HAV affects host provisioning rate. We discuss possible reasons for this result and provide alternative explanations for HAV, such as creating a bond between the hosts and the parasitic young used later in the postfledging care.     

IBERIAN AZURE-WINGED MAGPIE CYANOPICA (CYANA) COOKI NESTLINGS BEGGING CALLS: CALL CHARACTERIZATION AND HUNGER SIGNALLING

ABSTRACT

Nestling begging behaviour has long been seen as a signal by which nestlings solicit care from parents and most of the existing evidence provides some support for it being an honest signal. Begging is a multicomponent signal in which both sound and vision components are usually important. Although it is known that begging encodes information about nestling hunger the present knowledge about the specific behavioural features that convey the information is still scarce. The aim of this study was to describe begging calls of Iberian Azure-winged Magpie Cyanopica (cyana) cooki nestlings and examine how information on nestling hunger might be encoded in the begging calls. Nestlings were experimentally submitted to different periods of food deprivation and the call variation within individuals was studied. The young were individually tested and stimulated to beg by simulating parental visits. When subject to increasing food deprivation periods, nestlings increased the response level to simulated parental visits. The study also found that for the studied size differences, nestlings did not differ in their response level. Results confirmed that information on nestlings' hunger might be encoded in parameters of the calling behaviour. When the food deprivation periods increased, nestlings tended to start begging earlier, begged more often, extended their calling bout and increased the call duration, changing both at the level of the call and vocal begging bout. Overall the results support the view of begging as an honest signal, namely that begging should reflect nestling hunger and that only some call features might encode information about hunger.     

Bonobos extract meaning from call sequences

Studies on language-trained bonobos have revealed their remarkable abilities in representational and communication tasks. Surprisingly, however, corresponding research into their natural communication has largely been neglected. We address this issue with a first playback study on the natural vocal behaviour of bonobos. Bonobos produce five acoustically distinct call types when finding food, which they regularly mix together into longer call sequences. We found that individual call types were relatively poor indicators of food quality, while context specificity was much greater at the call sequence level. We therefore investigated whether receivers could extract meaning about the quality of food encountered by the caller by integrating across different call sequences. We first trained four captive individuals to find two types of foods, kiwi (preferred) and apples (less preferred) at two different locations. We then conducted naturalistic playback experiments during which we broadcasted sequences of four calls, originally produced by a familiar individual responding to either kiwi or apples. All sequences contained the same number of calls but varied in the composition of call types. Following playbacks, we found that subjects devoted significantly more search effort to the field indicated by the call sequence. Rather than attending to individual calls, bonobos attended to the entire sequences to make inferences about the food encountered by a caller. These results provide the first empirical evidence that bonobos are able to extract information about external events by attending to vocal sequences of other individuals and highlight the importance of call combinations in their natural communication system.     

Early estrogen treatment alone causes female zebra finches to produce learned, male-like vocalizations.

The male zebra finch produces learned song and long calls while the female does not. This difference in behavior is believed to result from the action of sex steroids on brain areas responsible for vocal production and learning. In this study, the female zebra finch was used to explore further the specific role sex steroids play in vocal masculinization. We show that estradiol (E2) treatment at birth was sufficient to masculinize the vocal behavior of female zebra finches. Thirteen of 18 females treated with E2 as nestlings produced song-like vocalizations. Fifteen of 18 produced long calls with male-typical features. The degree of masculinization varied between individuals. Of the 15 early E2 females that produced at least one type of male-like vocalization, 7 showed evidence of vocal learning from their tutors. The ability of E2 to cause masculinization of vocal behavior was age dependent: treatment from birth was most effective, treatment at 20 days of age was partially effective, and treatment in adulthood was ineffective. The effect of subsequent testosterone exposure in adulthood differed depending on the quality of the vocalization produced after E2 treatment alone. These results suggest that E2 may play a more important role than previously thought in the development of sex differences in vocal behavior. Furthermore, this study demonstrates that exogenous E2 treatment alone can induce vocal learning.     

The vocal sac increases call rate in the Tungara frog Physalaemus pustulosus

In most anurans, the production of advertisement calls is accompanied by the inflation of a vocal sac. Current functions of the vocal sac, however, are not fully understood, although several hypotheses have been proposed. One hypothesis suggests that the vocal sac decreases the intercall interval (i.e., increases call rate) by reinflating the lungs more rapidly than is possible with the buccal pump. We investigate this hypothesis by analyzing audio and video recordings of calling tungara frogs. We compare the first two call bouts emitted by an originally uninflated male. The first call bout requires lung inflation via buccal pumping, but in the second, the male is already inflated because of capture of air and reinflation of the lungs by the vocal sac. Lung inflation to typical field levels requires 26-51 buccal pumps, which takes at least 4.4 s. This estimate is more than 2.5 times the typical intercall interval with lung reinflation via a vocal sac (ca. 1.7 s). Evidence from phonotaxis tests demonstrates that these differences in intercall intervals are salient to females and that female Physalaemus pustulosus prefer the shorter intercall interval/higher call rate. Acoustic analyses demonstrate that the first call of bout 1, which requires buccal pumping, is usually shorter, of lower amplitude, and spans a smaller frequency range than the first call of bout 2, which does not require buccal pumping. Because females prefer longer, more intense calls, these results suggest that the vocal sac not only increases call rate but also allows males to produce more calls of increased attractiveness to females.     

Early estrogen treatment alone causes female zebra finches to produce learned,male-like vocalizations

The male zebra finch produces learned song and long calls while the female does not. This difference in behavior is believed to result from the action of sex steroids on brain areas responsible for vocal production and learning. In this study, the female zebra finch was used to explore further the specific role sex steroids play in vocal masculinization. We show that estradiol (E2) treatment at birth was sufficient to masculinize the vocal behavior of female zebra finches. Thirteen of 18 females treated with E2 as nestlings produced song-like vocalizations. Fifteen of 18 produced long calls with male-typical features. The degree of masculinization varied between individuals. Of the 15 early E2 females that produced at least one type of male-like vocalization, 7 showed evidence of vocal learning from their tutors. The ability of E2 to cause masculinization of vocal behavior was age dependent: treatment from birth was most effective, treatment at 20 days of age was partially effective, and treatment in adulthood was ineffective. The effect of subsequent testosterone exposure in adulthood differed depending on the quality of the vocalization produced after E2 treatment alone. These results suggest that E2 may play a more important role than previously thought in the development of sex differences in vocal behavior. Further-more, this study demonstrates that exogenous E2 treatment alone can induce vocal learning.