Heart rate changes reveal that little blue penguin chicks (Eudyptula minor) can use vocal signatures to discriminate familiar from unfamiliar chicks

Researchers investigating social recognition typically measure only behavioural responses during discrimination tests - physiological changes have been largely ignored. We examined whether little blue penguin chicks (Eudyptula minor) could distinguish siblings from other chicks using auditory cues, by measuring behavioural and heart rate changes during playback experiments. Chicks were exposed to five treatments: the begging calls of siblings, neighbouring chicks and unfamiliar chicks, and two controls (heterospecific begging calls and music). We also determined if chicks developed distinctive begging calls, by using F-ratios to quantify inter- versus intra-individual variability in a range of acoustic parameters, and applying a discriminant-function analysis. Inter-individual variation was greater for pitch than for temporal or amplitude parameters, suggesting that call pitch may be important for individual recognition. The discriminant-function analysis showed each chick's calls were distinctive and could act as a vocal signature. Treatments did not instigate different behavioural responses. However, chick heart rates during playback of sibling calls were significantly higher than those recorded during stranger, but not neighbour, playback. A simple recognition system based on familiarity may allow this plesiomorphic and loosely colonial penguin to gain at least some of the benefits associated with more advanced sibling recognition systems (some highly colonial seabirds discriminate siblings from neighbouring chicks). Heart rate could be a useful measure of social recognition abilities, particularly in species where changes in behaviour are not always evident or are difficult to observe.     

Individual specific contact calls of pallid bats (<Emphasis Type="Italic">Antrozous pallidus</Emphasis>) attract conspecifics at roosting sites

Contact calls are utilized by several bird and mammal species to maintain group cohesion and coordinate group movement. From a signal design perspective, contact calls typically exhibit acoustic features that make them easily localizable and encode information about individual or group identity. Pallid bats (Antrozous pallidus) are unusual among vespertilionids in that they often emit a loud, partially audible frequency-modulated social call several times in rapid succession while in flight. This call appears to function as a contact call in that it is frequently given when bats return from foraging and perform circular flights before entering a crevice roost. However, the degree to which pallid bats respond to the calls of conspecifics and what information is provided in the call is unknown. Thus, the goal of this study was to investigate pallid bat calling behavior to determine if calls attract roostmates or elicit responses from them and provide sufficient information for individual recognition. In playback studies, we found that contact calls, elicit calls, and approaches and that free-flying bats respond more to familiar than unfamiliar calls. In addition, analysis of frequency and temporal measurements of calls collected from multiple sites and spectral cross correlation analysis of calls recorded from the same radio-tagged bats on multiple evenings revealed that the frequency pattern of contact calls is highly repeatable over time within individuals but exhibits significant differences among individuals. Thus, contact call structure appears to be unique to individuals and stable through time, which makes these calls well-suited for roostmate recognition.     

Predation affects alarm call usage in female Diana monkeys (Cercopithecus diana diana)

Diana monkeys produce acoustically distinct calls to a number of external events, including different types of predators. In a previous study, we found population-wide differences in male alarm call production in Taï Forest, Ivory Coast, and on Tiwai Island, Sierra Leone, mostly likely originating from differences in predator experience. In Taï Forest, leopards (Panthera pardus) are common but on Tiwai Island they have been absent for decades, while the predation pressure from crowned eagles (Stephanoaetus coronatus) has been similar. To further evaluate the impact of predator experience, we here analyse the vocal behaviour of female Diana monkeys in both habitats. Female Diana monkeys produce predator-specific alarm calls, alert calls and contact calls in response to predators, suggesting that their calls serve in a broader range of functions compared to males. Results showed that females produced the same call types at both sites, despite the differences in predator fauna. Regarding call usage, leopard alarm calls were extremely rare on Tiwai Island, but not in Taï Forest, whereas we found no differences in eagle alarm call production. When comparing response latencies, Tiwai females were slower to respond to both predators compared to Taï females. Finally, we found no habitat-specific acoustic differences in the alert and predator-specific alarm calls, but significant differences in frequency-based parameters of contact calls. Overall, our results suggest that ontogenetic experience can affect primate vocal behaviour in both usage and acoustic structure but that the way in which particular call types are affected may be closely linked to function.     

Greater spear-nosed bats give group-distinctive calls

Individually distinctive vocalizations are ubiquitous; however, group distinctive calls have rarely been demonstrated. Under some conditions, selection should favor calls indicating social group membership in animals that forage in groups. Greater spear-nosed bats (Phyllostomus hastatus) give calls that appear to facilitate recognition of social group mates who are unrelated. Females give loud broadband (4–18 kHz) vocalizations termed screech calls when departing on foraging trips and at foraging sites. Screech calls help to establish foraging groups among social group members, and to maintain contact over the long distances they travel while foraging. I test two hypotheses about how screech calls may be structured to convey caller identity. Individual calls may be distinct and group members may learn to recognize each individual's calls and to associate the individual with the social group. Alternatively, groups may give distinct calls and individuals within groups may share call characteristics. To test these hypotheses I conducted multivariate acoustic analysis of multiple calls from 28 bats from three social groups. Although the ubiquity of individually distinctive calls in other taxa makes this result more likely, the results reveal that group calls are highly distinctive. Individual bats within groups are statistically indistinguishable. Calls appear to decrease slightly in frequency as bats age. Call convergence among unrelated group mates implies vocal learning in this species. Received: 28 March 1996 / Accepted after revision: 6 October 1996     

Incest avoidance and bonding between siblings in gerbils

Summary Social and sexual preferences for siblings versus non-siblings have been investigated in Mongolian gerbils (Meriones unguiculatus) in a series of laboratory and outdoor enclosure (100 m²) studies. When first social contact took place at pairing in adulthood full siblings and nonsiblings did not differ with respect to onset of reproduction. Correspondingly, both siblings and non-siblings paired at weaning age had a delayed onset of reproduction. Thus, no effect could be established in either case, related to the individuals' relatedness, but the importance of social exposure was clear. Non-siblings paired when 2 months old had a delayed onset of reproduction, which did not differ statistically from the onset in siblings, raised together, and housed pairwise since the same age. When sexually mature animals were paired at 3 months of age, siblings were found to start reproducing later than non-siblings (Ågren 1981). Following an initial delay in both siblings and nonsiblings paired when 5 months old, all non-sibling pairs reproduced before any sibling pair. At pair formation, at least the females in both groups were known to be sexually immature. These results indicate that for sibling-bonding to occur social exposure may be delayed until the animals are old enough, or somatically developed, to mature sexually. Thus, social exposure before weaning age during the period for primary socialization seem not to be crucial, nor the actual maturational state, sexually, in older females. To study the stability of the social bonds between siblings and non-siblings, animals kept pairwise in the laboratory were released in large outdoor enclosures. Pairs brought together before the age of sexual maturity did not remain stable, whether or not the former cagemates were siblings. Non-sibling pairs formed after this age, which had also reproduced successfully in the laboratory, did remain stable. Social and sexual interactions were studied within and between two mixed-sex sibling groups of four. The sibling groups had the possibility to establish group territories before being exposed to each other. Although the sibling groups remained stable, the females still preferred non-sibling males as sexual partners. However, socially dominant brothers copulated more frequently than subordinant brothers. This rank difference was not evident in non-siblings.     

Parent–offspring resource allocation in domestic pigs

Behavioural research on domestic pigs has included parent–offspring conflict, sibling competition, and the use of signals which influence resource allocation. In this paper, we review key sow–piglet behavioural studies and discuss their relevance to resource allocation theory. Sibling competition begins in the uterus and continues after birth, as piglets compete directly for access to the sow’s teats. This competition is made more severe by a unique dentition, which newborn piglets use to lacerate the faces of siblings during teat disputes. Competition often leads to the death of some littermates, especially those of low birth weight. Piglets also compete indirectly for milk, apparently by stimulating milk production at the teats that they habitually use at the expense of milk production by other teats. The complex nursing behavior of the sow appears designed to prevent the more vigorous piglets from monopolizing the milk. Sows give vocal signals which both attract piglets to suckle and synchronize their behavior during nursing episodes. Piglets give loud vocal signals when separated from the sow; calls which vary in intensity and appear to be honest signals of need. Udder massage by piglets may also serve as an honest signal of need. Parent–offspring conflict has been demonstrated experimentally in pigs. Specifically, when given the opportunity to control contact with their piglets, sows nurse less frequently, provide less milk, and lose less weight during lactation than sows that cannot control their level of contact. Because of this interesting natural history and because they are so amenable to experimentation, domestic pigs provide a rich system for testing ideas drawn from resource allocation theory. This contribution is part of the special issue “Sibling competition and cooperation in mammals” (guest editors: Robyn Hudson and Fritz Trillmich).     

Crimson-breasted Shrike females with extra pair offspring contributed more to duets

Many socially monogamous bird species follow a genetically promiscuous reproductive strategy. Duetting birds may be an exception, as they appear to exhibit very low levels of extra pair paternity—which is thought to be connected to duetting. Duets are predicted to function either in paternity guarding or as signals of commitment to the pair bond, reciprocally reducing extra pair mating in both sexes. In this study, we used four microsatellites to document paternity loss in the Crimson-breasted Shrike (Laniarius atrococcineus), a socially monogamous subtropical duetting species. Extra pair paternity was surprisingly high, with extra pair males siring 20 % of young in 30 % of broods. Furthermore, we compared the levels of extra pair paternity of each pair to certain characteristics of their duets to test the paternity guard and the commitment hypotheses. Our results offered no support that duets function in paternity guarding, although the fact that males which had been cuckolded answered more of their female’s calls could represent an adaptation to avoid future cuckoldry. We also found no evidence for duets functioning as signal of commitment. Female vocal behaviour was in fact the reverse of that predicted: Levels of infidelity amongst social females were positively related to female answer rate of their mates’ songs. These results indicate that females may use increased answer rates as a form of manipulation, in an attempt to avoid potential costs associated with their extra pair matings.     

Loud calls as a mechanism of social coordination in a fission–fusion taxon, the white-bellied spider monkey (Ateles belzebuth)

Spider monkeys (Ateles spp.) live in social groups that exhibit high levels of fission–fusion dynamics, in which group members form subgroups of varying sizes and compositions. Within these fluid societies, how individuals establish contact with dispersed group members with whom they might choose to associate remains unclear. Long-range vocalizations might facilitate interactions between group members and provide a means of social coordination in fission–fusion societies. We evaluated this possibility for one spider monkey vocalization, the loud call, by examining calling behavior, the relationship between loud calls and changes in subgroup size, and the response of individuals to distant calls and playback experiments in a single study group. We found that 82 % of loud calls were emitted within 30 min of a call from a different location, suggesting that individuals frequently emit loud calls in response to the calls of distant group members. Subgroups that emitted loud calls, especially those that responded to distant calls, were much more likely to experience an increase in subgroup size within an hour after calling than those that did not. Animals also approached distant loud calls more than they avoided or ignored these calls. Finally, playbacks of male calls demonstrated that females respond preferentially to the calls of some individuals over others. Taken together, these results provide support for the hypothesis that spider monkey loud calls function to facilitate and initiate interactions between dispersed group members and suggest that vocal signals can play an important role in influencing social interactions in fission–fusion societies.     

Sex differences in the ontogeny of social behavior in pikas: possible relationships to dispersal and territoriality

Summary A laboratory study on the ontogeny of social behavior in pikas (Ochotona princeps), an alpine lagomorph, was conducted to determine the role of early relationships between adult females and young and among siblings in the development of territorial and dispersal behaviors. Sex differences during development were examined because field studies have reported greater dispersal distances in young females than young males. At birth, females were significantly heavier than males. There were no sex differences in nursing frequency until after the 2nd week of age, when males initiated more nursing attempts than females. By the end of the weaning period (weeks 5 and 6), adult females became non-interactive with young, but aggression of young toward littermates and the mother increased until the eighth week. At this time, young males outweighed their sibling females. Young were dominant over their mothers by the age of 5 weeks, and young males were dominant over their sibling females.Sex differences were observed in aggression, scent-marking, exploratory activity, and submissive vocalizations, with higher rates in young males, except for submissive vocalizations, which were higher in females (Table 2). Vocalizations and scent-marking behavior increased over time, and were positively correlated with interaction rates.These data support the hypothesis that female young disperse farther than male young largely as the result of unsuccessful competition with male siblings for available territories close to the birthplance. A dispersal strategy for pkkas is proposed.     

Early learning of discrete call variants in red crossbills: implications for reliable signaling

The identification of appropriate companions and mates is essential to both speciation and the maintenance of species through prezygotic isolation. In many birds, social assortment is mediated by vocalizations learned through imitation. When imitative vocal learning occurs throughout life, emergent shared signals reflect current social associations. However, when vocal and genetic variation arises among populations, shared learned signal variants have a potential to reflect cultural or genetic origin and to limit social and reproductive intermixing, provided that signal learning occurs prior to dispersal. The red crossbill (Loxia curvirostra) is a bird species in which discrete contact call variants are associated with morphological variation, raising the possibility that learned calls play a role in limiting intermixing. I examined the process of early call learning to determine if contact call variants have a potential to limit intermixing in crossbills. I conducted a captive playback study to nestlings to evaluate potential learning predispositions. I also cross-fostered nestlings to adoptive adult pairs of either their own or a different call variant than their biological parents to assess the degree of vocal learning plasticity. Results show that young crossbills imitate the call structures of adoptive parents, generating shared family-specific calls, which could facilitate family cohesion. Learning processes that generate family-specific calls could also ensure that discrete call variants are transmitted across generations, making call variants reliable signals of crossbills’ morphological and genetic backgrounds.     

Male Scudderia pistillata katydids defend their acoustic duet against eavesdroppers

Acoustic duets—in which the female reveals herself to the advertising male—are a common means of establishing a temporary, pre-mating pair bond within Phaneropterinae katydids. Such duets, however, are especially susceptible to eavesdropping males that orient to signaling females and interrupt the established duet. It would therefore be advantageous for an advertising male to protect his investment in a duet from eavesdroppers. Male Scudderia pistillata katydids produce acoustic advertisement calls after which a conspecific female enters the duet by responding during a specific time-window with her own call, one or more acoustic ticks. We demonstrate here that when a duet is occurring in the presence of other calling males, the focal male produces a single acoustic tick that has a spectrum similar to that of the female’s tick and occurs during the time-window in which the female would respond to his advertisement call within the duet. The male acoustic tick may confound eavesdropping males if they have difficulty performing accurate phonotaxis to a female sound source when sounds arrive from two locations. We tested this hypothesis in laboratory arenas and determined that silent males eavesdrop on advertising male’s duets and accurately locate his female. Moreover, we found that the added acoustic tick produced by advertising males serves to mimic the female response and reduces the accuracy of eavesdropping males to localize the female. Therefore, male ticks appear to act as a form of pre-copulatory acoustic mate guarding of the calling male’s temporary pair bond with the female.     

A field test of the effects of familiarity and relatedness on social associations and reproduction in prairie voles

Inbreeding depression is a well-documented phenomenon. In animals, one means of avoiding the costs of inbreeding is through the recognition and avoidance of kin as mates. Prairie voles (Microtus ochrogaster) are short-lived, socially monogamous rodents that demonstrate inbreeding depression in the laboratory. Field data indicate that pair formation in nature is opportunistic but pairing among close relatives seems uncommon. We examined the role of relatedness and familiarity on prairie vole social associations and reproduction by placing adult voles into 0.1-ha enclosures with familiar siblings, unfamiliar siblings, and unrelated, unfamiliar conspecifics. Live-trapping data indicated that indices of social pair bonding were random with respect to relatedness and familiarity. Among females whose litters were sired by a single male, litters were significantly more likely to be sired by unfamiliar than familiar males, but the number of litters sired by males that were unrelated to their partner was not different from the number of litters sired by males that were related to their partner. Additionally, females that produced offspring with familiar siblings were significantly more likely to have litters with multiple paternity than females not producing offspring with familiar siblings. However, multiple paternity was not influenced by relatedness of sires. Finally, older individuals were more likely to produce offspring with each other than with younger individuals. Our findings suggest that prior association is a more important mechanism of inbreeding avoidance than phenotype matching for prairie voles mating under ecologically relevant conditions.     

Individual recognition and potential recognition errors in parent–offspring communication

The recognition of food-provisioning parents is crucial for fledglings of many bird species. Vocalizations are the most commonly used cues in avian parent–offspring communication, and it has been shown in several species that fledglings respond specifically to their parents' contact calls. However, fledglings occasionally also react to unrelated adults. Such responses may reflect recognition errors or alternatively a strategy of fledglings to obtain food or other direct benefits from unrelated adult birds. In a playback experiment, we tested whether zebra finch Taeniopygia guttata fledglings perceive variation in adult call signatures to recognize their parents and whether the propensity to respond to unrelated individuals is related to the gender of adults and to signal properties of male and female calls. Male calls are learnt and show high intra-sexual variation, which may improve the accurate recognition of the father's individual signature. In contrast, calls of adult females are innate, show lower intra-sexual variation such that the mother's call is more likely to be confused with another female call. We demonstrate that fledglings are able to recognize their parents. In addition, fledglings reacted more strongly to unrelated females compared with unrelated males. Our findings suggest that responses to unrelated adults may reflect recognition errors and indicate the importance of variation in identity signals for individual recognition processes in parent–offspring communication.     

Do echolocation calls of wild colony-living Bechstein's bats (Myotis bechsteinii) provide individual-specific signatures?

Social animals often use vocal communication signals that contain individual signatures. As bats emit echolocation calls several times per second to orient in space, these might seem ideal candidates for conveying the caller's individual identity as a free by-product. From a proximate perspective, however, coding of caller identity is hampered by the simple acoustic structure of echolocation signals, by their task-specific design and by propagation loss. We investigated the occurrence of individual signatures in echolocation calls in individually marked, free-living Bechstein's bats (Myotis bechsteinii) in a situation with defined social context in the field. The bats belonged to two different colonies, for both of which genetic data on relatedness structure was available. While our data clearly demonstrate situation specificity of call structure, the evidence for individual-specific signatures was relatively weak. We could not identify a robust and simple parameter that would convey the caller's identity despite the situation-specific call variability. Discriminant function analysis assigned calls to call sequences with good performance, but worsened drastically when tested with other sequences from the same bats. Therefore, we caution against concluding from a satisfactory discrimination performance with identical training and test sequences that individual bats can reliably be told apart by echolocation calls. At least the information contained in a single call sequence seems not to be sufficient for that purpose. Starting frequencies did give the best discrimination between individuals, and it was also this parameter that was correlated with genetic relatedness in one of our two study colonies. Echolocation calls could serve as an additional source of information for individual recognition in Bechstein's bats societies, while it is unlikely that a large number of individuals could be reliably identified in different situations based on echolocation alone.     

Territorial vocal behavior in hybrid smooth froglets, Geocrinia laevis complex (Anura: Myobatrachidae)

Males of the parapatically distributed myobatrachid frogs Geocrinia laevis and G. victoriana have highly divergent advertisement calls. Furthermore, the two species differ strongly in the complexity of their vocal repertoires, with males of G. victoriana possessing, and those of G. laevis lacking, a distinct territorial vocalization (encounter call). We investigated the territorial vocal behavior of males in a persistent natural hybrid population. Most hybrid males possessed encounter calls functionally equivalent to those of G. victoriana, that were produced following exposure to playback of recorded advertisement calls presented at >110 dB peak sound pressure level. The territorial acoustic responses were not associated with an index of hybridity derived from the structure of the advertisement call, suggesting genetic and functional decoupling of the two components of the vocal repertoire; i.e., advertisement calls and encounter calls. This decoupling may be the result of sexual selection favouring those hybrids with pronounced territorial behavior and the associated vocalization, regardless of the structure of their advertisement calls.Communicated by A. Mathis     

Female and male behavioral response to advertisement calls of graded complexity in túngara frogs, <Emphasis Type="Italic">Physalaemus pustulosus</Emphasis>

We investigated the natural dynamics in a sexual signal that combines different call components and explored the role of call complexity in sexual selection using a neotropical frog. Male túngara frogs, Physalaemus pustulosus, facultatively add up to seven short, multi-harmonic components (chucks) to the simple form of their calls (whines). Female túngara frogs are preferentially attracted to whines with chucks over whines without chucks, and males also call more in response to calls containing chucks. Because acoustic predators prefer complex calls, in the context of simple (no chucks) versus complex (any number of chucks) calls, the variably complex call appears to have evolved in response to the opposing selective forces of natural and sexual selection. There is no evidence, however, for the function of increasing the number of chucks within complex calls. We tested two aspects of increasing call complexity: natural patterns of use of call types in males and how both sexes respond to variation in multi-chuck calls. Males incrementally change call complexity by the addition or subtraction of a single chuck and usually do not produce more than two chucks. Variation in call complexity, for calls with at least one chuck, does not influence response calling in males or phonotaxis in females. Our results suggest that one reason for not increasing call complexity beyond a single chuck is the diminishing effectiveness on the responses of both sexes. This is a posthumous publication for A. Stanley Rand     

Do yellow-bellied marmots respond to predator vocalizations?

We conducted four experiments to determine whether yellow-bellied marmots, Marmota flaviventris, discriminate among predator vocalizations, and if so, whether the recognition mechanism is learned or experience-independent. First, we broadcast to marmots the social sounds of coyotes, Canis latrans, wolves, Canis lupus, and golden eagles, Aquila chrysaetos, as well as conspecific alarm calls. Coyotes and eagles are extant predators at our study site, while wolves have been absent since the mid-1930s. In three follow-up experiments, we reversed the eagle call and presented marmots with forward and reverse calls to control for response to general properties of call structure rather than those specifically associated with eagles, we tested for novelty by comparing responses to familiar and unfamiliar birds, and we tested for the duration of predator sounds by comparing a wolf howl (that was much longer than the coyote in the first experiment) with a long coyote howl of equal duration to the original wolf. Marmots suppressed foraging and increased looking most after presentation of the conspecific alarm call and least after that of the coyote in the first experiment, with moderate responses to wolf and eagle calls. Marmots responded more to the forward eagle call than the reverse call, a finding consistent with a recognition template. Marmots did not differentiate vocalizations from the novel and familiar birds, suggesting that novelty itself did not explain our results. Furthermore, marmots did not differentiate between a wolf howl and a coyote howl of equal duration, suggesting that the duration of the vocalizations played a role in the marmots’ response. Our results show that marmots may respond to predators based solely on acoustic stimuli. The response to currently novel wolf calls suggests that they have an experience-independent ability to identify certain predators acoustically. Marmots’ response to predator vocalizations is not unexpected because 25 of 30 species in which acoustic predator discrimination has been studied have a demonstrated ability to respond selectively to cues from their predators.     

Sex-specific costs of hatching last: an experimental study on herring gulls (<Emphasis Type="Italic">Larus argentatus</Emphasis>)

An organism’s pattern of development can have important long-term fitness effects. In species where the sexes differ in size or other phenotypic traits, they may also have different optimal developmental rates. This influences both parental sex allocation strategies and susceptibility of the sexes to early developmental conditions. However, sex differences in developmental rate and vulnerability to environment during the embryonic period are not well understood. In birds, sibling competition and hatching asynchrony may select for accelerated embryonic development of the last offspring in order to reduce their competitive disadvantage after hatching. They may advance their hatching in response to vocal stimuli by the older siblings. It is, however, unclear whether this flexibility in developmental rates is sex specific. In this study, we experimentally manipulated between-embryo contact and tested whether this affected the pre-natal developmental rate and post-hatching performance of male and female offspring from last-laid eggs in the herring gull. Post-hatching performance was measured both in competitive and non-competitive situations. Among young incubated in isolation, males hatched faster than females, but both sexes fledged in similar, relatively good condition. Among young incubated with normal between-embryo contact, hatching time did not differ between sexes, but males fledged in poorer condition than females, regardless of whether they were reared singly or in a brood. These results suggest that male and female offspring differ in their ability to mitigate the costs of hatching asynchrony.     

A forest monkey’s alarm call series to predator models

Some non-human primates produce acoustically distinct alarm calls to different predators, such as eagles or leopards. Recipients respond to these calls as if they have seen the actual predator, which has led to the notion of functionally referential alarm calls. However, in a previous study with free-ranging putty-nosed monkeys (Cercopithecus nictitans martini), we demonstrated that callers produced two acoustically distinct alarm calls to eagle shrieks and leopard growls, but both alarm calls were given to both predators. We can think of two basic explanations for this surprising result, a methodological and theoretical one. Firstly, acoustic predator models may not always be suitable to test alarm call behaviour in primates, sometimes causing uncharacteristic behaviour. Secondly, referential alarm calling may not be a universal feature of primate alarm call systems. Considering the methodological and theoretical importance of these possibilities, we conducted a follow-up study using life-sized leopard, eagle, and human models on the same population and compared the resulting vocal responses to those given to acoustic predator models. We compared the alarm call series given to each of these predator model types and found a considerable degree of consistency suggesting that the mode of presentation did not affect anti-predator calling strategies. However, evidence for audience effects on calling behaviour was inconclusive. While it appears that predator class is reliably encoded by different call series types irrespective of the mode of presentation, observations of these same call series given in non-predatory contexts indicate that predator class is unlikely to be the relevant organising principle underlying the alarm-calling behaviour in this species. We conclude by offering an alternative, non-referential, account of the alarm-calling system exhibited by this species. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Chick-a-dee call syntax,social context,and season affect vocal responses of Carolina chickadees (<Emphasis Type="Italic">Poecile carolinensis</Emphasis>)

Chick-a-dee calls in many chickadee (Poecile) species are common vocal signals used in a diversity of social contacts. The calls consist of four notes, A, B, C, and D, which follow simple rules of syntax (note ordering and composition) to generate many unique call types. We used field playbacks with Carolina chickadees, P. carolinensis, to ask whether violations of a syntactical rule affected their vocal responses. We show that chickadee responses to typical calls (e.g. AAAACCCC and CCCCDDDD) differ from responses to atypical calls (e.g. CACACACA and DCDCDCDC) depending on playback note composition, season, and social context (presence of heterospecifics). In the fall/winter, playbacks of typical calls with A and C notes elicited the greatest number of A and B notes in chick-a-dee call responses and typical calls with D notes elicited the greatest number of C notes, when in the presence of heterospecifics. In contrast, the corresponding atypical calls did not elicit similar responses. This suggests communicative significance is lost in calls that violate a rule of syntax in the fall/winter. In the spring, neither chickadee feebeefeebay song rate nor chick-a-dee calls responses differed by playback type. We suggest that call syntax is less salient for mated pairs in the spring than it is for fall/winter flocks that rely more on conspecific communication for foraging success and flock cohesion. This study represents the first experimental evidence that chickadees attend to both note composition and ordering in chick-a-dee calls.Communicated by W.A. Searcy