A possible phylogenetically conserved urgency response of great tits (<Emphasis Type="Italic">Parus major</Emphasis>) towards allopatric mobbing calls

Black-capped chickadees Poecile atricapillus alter the number of D notes of their chick-a-dee call to reflect urgency and threat. Here, I tested whether heterospecific responses of an allopatric species to these mobbing calls occur. Heterospecific chickadee mobbing calls and songs from North America were broadcast to European great tits (Parus major) and compared with conspecific mobbing calls. During conspecific mobbing playbacks, all great tits approached the speaker, during the heterospecific “chick-a-dee” playbacks, 63.3% individuals approached the speaker, while during the song playback, only 31.3% of the great tits approached the speaker. Minimum distances of great tits were lower during conspecific mobbing calls compared to allopatric chick-a-dee calls and to allopatric chickadee song. Also, minimum distances were lower when comparing allopatric chick-a-dee calls and chickadee song. Great tits approached the speaker on average down to (mean ± SE) 20.0 ± 1.8 m during playbacks of 1–4 D elements, to 17.7 ± 2.0 m during playbacks of 5–7 D elements and down to 11.5 ± 2.0 m during playbacks of 8–11 D elements. The number of D notes was inversely related to minimum distance. Thus, the urgency message encoded in the D notes was perceived also by an allopatric but phylogenetically related European species, suggesting that the heterospecific response is possibly phylogenetically conserved.     

Chick-a-dee call variation in the context of “flying” avian predator stimuli: a field study of Carolina chickadees (<Emphasis Type="Italic">Poecile carolinensis</Emphasis>)

Chick-a-dee calls function in social organization in Poecile (chickadee) species. Recent field and aviary studies have found that variation in chick-a-dee calls relates to the type or proximity of avian predator, or level of threat. Earlier studies on calls in the context of predator stimuli have typically used stationary and perched predator models. For chickadees and other small songbirds, more frequently detected and more dangerous avian predatory stimuli are flying predators. In the present study, we tested whether simulated flying avian predator and control models influenced chick-a-dee calling behavior of wild Carolina chickadees, Poecile carolinensis. At 20 independent field sites, chickadee subjects were presented with wooden models that were painted to resemble either a predatory sharp-shinned hawk (Accipiter striatus) or a blue jay (Cyanocitta cristata) and that were made to “fly” down a zip line near a feeding station chickadees were using. The note composition of chick-a-dee calls was affected by both the flight of stimuli and type of model. Call variation in this flying predator context suggests interesting similarities and differences with experimental findings with congeners. Finally, increased production of certain notes to the flying of both model types provides support for a “Better Safe than Sorry” strategy. When costs of alarm calling are low but costs of discriminating potentially serious threats may be extremely high, individuals should err on the side of caution, and alarm call to any potentially threatening stimulus.     

Inspection of mob-calls as sources of predator information: response of migrant and resident birds in the Neotropics

Migrating animals face numerous mortality risks, such as novel predators with which they may not be accustomed. Most animals can recognize predators innately; however, additional predator information can be collected to enhance familiarity. Because migrating birds rarely participate in mobs, they may seek alternative information sources such as cues provided by other birds that can provide information on predator location, identity, and degree of threat. We predicted that Nearctic–Neotropical migrants (hereafter, “migrants”) would react to vocal antipredator cues (e.g., mob-calls) of species residing in areas through which they migrate. To test this, we conducted experiments in Belize during spring migration, using playbacks of mob-calls of black-capped chickadees (Poecile atricapillus) and blue-gray tanagers (Thraupis episcopus); tanagers are familiar to all birds in Belize; chickadees are novel to residents but familiar to migrants. This also allowed us to assess response to novel and out-of-context antipredator signals. Resident birds did not respond to novel chickadee mob-calls, but did respond to familiar tanager calls. Birds overwintering south of our study area, which were migrating during our study, responded most strongly to chickadee playbacks. Conversely, individuals of species that include our study area in their winter range did not respond to either playback. This is the first evidence that birds react to vocal antipredator cues during migration, which may be a strategy used by migrants to learn about predators. Although residents failed to recognize a foreign cue, migrating birds responded most strongly to the out-of-context chickadee cue, associated with breeding grounds >2,000 km northward. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Predator stimuli and calling behavior of Carolina chickadees (Poecile carolinensis), tufted titmice (Baeolophus bicolor), and white-breasted nuthatches (Sitta carolinensis)

Evidence from different chickadee species (Poecile genus) indicates that birds can modify the note composition of their “chick-a-dee” calls in the presence of predator stimuli. Here, we tested the effects of predator models and the distance of those models on calls of three species foraging together at feeding stations: Carolina chickadees (Poecile carolinensis) and tufted titmice (Baeolophus bicolor), both members of the Paridae family, and white-breasted nuthatches (Sitta carolinensis), a member of the Sittidae family. Model and distance affected seed-taking rates in all three species. “Chick-a-dee” calling rates were higher in the predator context for both chickadees and titmice, but we detected no predator context effects on “quank” call rates for nuthatches. Predator and distance contexts affected acoustic parameters of notes of the “chick-a-dee” calls of chickadees and titmice; no such effects were detected for nuthatch “quank” calls. These results suggest species differences in encoding of information in the primary social calls of these three species that commonly occur in multi-species flocks. Chickadees and titmice are “nuclear” species and nuthatches are “satellite” species, and these different roles might be related to the differences in vocal signaling that we detected.     

Interspecific attraction to the mobbing calls of black-capped chickadees (Parus atricapillus)

The species and number of birds attracted to playbacks of mobbing calls and song of the black-capped chickadee, Parus atricapillus, were compared. The chickadee vocalizations were played at abandoned chickadee nests, and the numbers and species of other birds that approached the speaker were tallied. Few non-chickadees were observed in the area when the song was played. That significantly more birds approached the speaker and displayed mobbing behavior during the mobbing call playback suggests that black-capped chickadee mobbing vocalizations carry meaning for at least ten other avian species. This finding supports the idea that species subjected to the same predators in an area may benefit by recognizing each others’ predator calls. This recognition may be facilitated by the similar structure of different species’ mobbing calls and also a learned association of another species’ call with the presence of a predator. Received: 23 March 1995 /Accepted after revision: 28 October 1995     

Advertisement-call modification,male competition,and female preference in the bird-voiced treefrog <Emphasis Type="Italic">Hyla avivoca</Emphasis>

Senders and receivers influence dynamic characteristics of the signals used for mate attraction over different time scales. On a moment-to-moment basis, interactions among senders competing for a mate influence dynamic characteristics, whereas the preferences of receivers of the opposite gender exert an influence over evolutionary time. We observed and recorded the calling patterns of the bird-voiced treefrog Hyla avivoca to assess how the dynamic characters of calls vary during interactions among groups of males in a chorus. This question was also addressed using playback experiments with males. Playback experiments with females showed how changes in dynamic call properties are likely to affect male mating success. Frogs calling in pairs, groups, or in response to playbacks produced longer calls than did isolated males. During call overlap, males often increased the duration of the silent interval (gaps) between the pulses of their calls so that the pulses of the calls of two neighbors interdigitated. This change resulted in increased variability of pulse rate, a traditionally static acoustic property; however, males also produced high proportions of non-overlapped calls in which variability in pulse rate was low and had species-typical values. Females preferred long calls to short- and average-duration calls, and non-overlapped calls to overlapped calls. Given a choice between pairs of overlapped calls, females preferred pairs in which the proportion of overlap was low and pairs in which the pulses of such calls interdigitated completely. The observed patterns of vocal competition thus reflect the preferences of conspecific females, which have influenced the evolution of the calling behavior of H. avivoca. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

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     

Individual differences and within-flock convergence in chickadee calls

Summary A detailed sound analysis of the Chick-adee call of the black-capped chickadee (Parus atricapillus) was performed in order to determine a basis for individual recognition and for imitation within winter flocks. During the winter of 1978–1979 members of five free-living black-capped chickadee flocks were uniquely marked for individual identification, and their calls were recorded in the field. Nested analysis of variance of temporal call parameters measured from sonagrams and spectral parameters from frequency spectra showed that there were significant differences between individuals within flocks for every parameter measured. There were significant differences between flocks in the frequency ranges 800–2,200 Hz and 4,000–5,300 Hz, in the spectral parameters bandwidth and maximum frequency, and in the duration of the Dee syllable and total call duration.Members of four of the five flocks were captured in December 1978 and held in aviaries segregated by original flock membership. In January 1979 the memberships of the three aviaries were rearranged to form experimental flocks. After one month, there were significant differences among the experimental flocks in the duration of the Dee syllable and total call duration. Convergence, as indicated by a significant decrease in variance among members (F-test), occurred in the experimental flock in Aviary 1 and was concentrated in the frequency ranges 1,300–1,800 and 6,200–6,900 Hz. The members of this experimental flock differed from each other in the number of 100 Hz frequency intervals within which each changed its own call.The Chick-a-dee call contains sufficient information that it can potentially be used by black-capped chickadees for individual recognition. In addition, both field and aviary data suggest that flock members converge in some call characteristics. Possible explanations of the social significance of vocal convergence in chickadee flocks are discussed.     

Calling energetics of a neotropical treefrog,Hyla microcephala

Summary We investigated the calling energetics of Hyla microcephala, a neotropical treefrog with an unusually complex vocal repertoire. Males respond to the calls of other individuals by adding secondary click notes to their calls, thereby increasing the total number of notes given per minute. Rates of oxygen consumption of males calling in metabolic chambers were 0.41–2.80 ml O₂/(g·h), corresponding to calling rates of 205–6330 notes/h. Note rate explained 95% of the variance in meta-bolic rate; the effect of variation in body size and temperature was small. Data from playback experiments with males in the field showed that note rate increased as as the number of notes in a stimulus call increased, and this resulted in substantial increases in the cost of calling. Average metabolic rates for males in the field were about 1.7 ml O₂/(g·h), for a net cost of calling of about 20 J/h for an average-size male. However, estimated metabolic rates varied by more than 300% and were strongly influenced by the proximity and calling activity of other males in the chorus. Male H. microcephala appear to conserve energy by reducing calling rates when only a few males are active and increasing calling efforts only when vocal competition among males is intense.     

Effects of multiple-speaker playbacks on aggressive calling behavior in the treefrog <Emphasis Type="Italic">Dendropsophus ebraccatus</Emphasis>

In addition to producing signals, males of chorusing species also act as receivers by adjusting properties of their vocalizations in response to those of other nearby individuals. Although it is likely that males are responsive to more than one other individual, most playback studies investigating male response have involved dyads in which vocal responses are measured to stimuli presented from a single speaker. In this study, I explored changes in both the propensity to give aggressive calls and the temporal properties of those calls in response to the playback of multiple aggressive call stimuli in the treefrog Dendropsophus ebraccatus. I found that males were sensitive to both the number of simulated aggressive callers and their specific call characteristics. Males generally gave a highly aggressive response to the first stimulus presented, but their response to the modification of this stimulus by the addition or subtraction of a simulated competitor depended on the degree of aggressiveness of the stimuli. Males tended to decrease their aggressive responses when either a more aggressive call was silenced or a less aggressive call was added and to increase their aggressive responses in the opposite situation. Aggressive calling in this species is clearly affected by complex changes in the social environment and I suggest that future studies explore these issues in other species to improve the understanding of communication interactions.     

Call matching in the quacking frog (Crinia georgiana)

Males of the quacking frog Crinia georgiana produce calls consisting of 1–11 notes. Playback experiments using synthetic calls showed that males tend to match the number of notes in 2-note and 4-note stimuli; however, males tended to produce more than 1 note in response to a 1-note stimulus and fewer than 8 notes in response to an 8-note stimulus. Successive playbacks of two, 4-note calls from separate speakers indicate that males are likely to match the combined number of notes in the calls of two neighbors, even if they are not equidistant from the focal male. The results are compared with the few other studies of matching in anurans, and interpreted in terms of hypotheses developed to explain matching in songbirds. One attractive and testable hypothesis for call matching in C. georgiana is that males are attempting to produce calls that are at least as attractive to females as those of rivals, without wasting energy. Received: 14 February 2000 / Received in revised form: 11 April 2000 / Accepted: 3 May 2000     

Species-specificity and individual variation in the song of male Nathusius’ pipistrelles (<Emphasis Type="Italic">Pipistrellus nathusii</Emphasis>)

Sequences of the advertisement calls produced by male Nathusius’ pipistrelles (Pipistrellus nathusii) during the autumn mating period were recorded from individuals at two separate sites in Antrim, Northern Ireland, in August 2004. Several male roosts were found at these sites in close proximity to a single maternity roost, each containing approximately 200 adult females and their young. Analysis of measured parameters of four identified call types revealed that there were significant differences in call structure between sites and between individuals. Playback experiments, performed outside the adult female and juvenile roost sites, comprised of experimental advertisement call sequences of P. nathusii, Pipistrellus pygmaeus and Pipistrellus pipistrellus and control sound recorded without bats present (silence). Response was measured by simultaneously recording ultrasound during playbacks and counting the number of echolocation pulses identified as those of P. nathusii above a predetermined amplitude threshold. Significantly greater numbers of P. nathusii echolocation pulses were recorded during playback of male P. nathusii advertisement calls than during playback of congeners’ advertisement calls and control sound. The number of echolocation pulses recorded was similar during playback of P. pipistrellus and P. pygmaeus advertisement calls and silence. We suggest that, due to call complexity, male P. nathusii advertisement calls should be classified as ‘song’. Species-specificity and individual variation suggests that the songs of male P. nathusii have the potential to play a role in mate attraction and mate assessment.     

Anti-predator behavior of group-living Malagasy primates: mixed evidence for a referential alarm call system

Many mammals warn conspecifics with alarm calls about detected predators. These alarm calls are either functionally referential, urgency based, or they can have multiple functions, including predator deterrence. The taxonomic distribution of these alarm call systems is uneven, with primates providing the best-known examples for a functionally referential system and rodents most examples of an urgency-based system. Reports of different alarm call systems in lemurid primates prompted us to examine the anti-predator behavior of two additional lemur species. In an experimental field study we exposed adult redfronted lemurs (Eulemur fulvus rufus) and white sifakas (Propithecus verreauxi verreauxi) to playbacks of vocalizations of their main aerial and terrestrial predators, as well as to their own alarm calls given in response to the presentation of these predators. We scored the subjects' immediate behavioral responses, including alarm calls, from video recordings made during the first minute following a playback. We found that both species gave specific alarm calls only in response to raptor playbacks and the corresponding alarm calls, whereas calls given in response to carnivores and the corresponding alarm calls were also observed in other situations characterized by high arousal. Other behavioral responses, such as gaze and escape directions, corresponded to the hunting strategies of the two predator classes, suggesting that the corresponding vocalizations were categorized correctly. These two lemur species, which represent different families, have therefore independently evolved a mixed alarm call system, characterized by functionally referential calls for diurnal raptors, but not for carnivores. Electronic supplementary material to this paper can be obtained by using the Springer LINK server located at http://dx.doi.org/10.1007/s00265-001-0436-0 Electronic Publication     

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.     

Diphasy in the advertisement calls of Geocrinia laevis (Anura: Leptodactylidae): vocal responses of males during field playback experiments

Summary The advertisement calls of Geocrinia laevis are diphasic, and consist of a single introductory note, followed by a series of repeated notes; diphasy is based on differentiation in the temporal structure of the two phases. In a series of field playback tests used to investigate the functional significance of diphasy, calling males were presented with one of three types of acoustic stimulus: complete calls (introductory and repeated notes), introductory notes only, or repeated notes only. There were no marked differences in the effects of these stimuli, and all resulted in a reduction in the rates of production of introductory notes and of repeated notes. Playback at levels of 110 dB PSPL and above caused virtual cessation of calling. The results suggest that one of the functions of the advertisement call, the communication of territoriality between males, does not reside in either the introductory note or the repeated notes, so that diphasy in the advertisement call has no apparent functional basis in this context. Whether the attraction of reproductively ripe females is a particular function of either phase remains untested. The advertisement calls of G. laevis are much less diphasic than those of a closely related species, G. victoriana, for which there is a clear partitioning of the functions of communication of territoriality and the attraction of conspecific mates between the introductory notes and the repeated notes, respectively. Furthermore, the acoustic repertoire of G. laevis is less complex than that of G. victoriana in lacking a vocalisation which functions specifically in close-range aggressive encounters between males.     

Behavioral responses to echolocation calls from sympatric heterospecific bats: implications for interspecific competition

Mutual recognition is the product of species coexistence, and has direct effects on survival and reproduction of animals. Bats are able to discriminate between sympatric different heterospecifics based on their echolocation calls, which has been shown both in free-flying and captive bats. To date, however, the factors that may determine the behavioral responses of bats to echolocation calls from sympatric heterospecifics have rarely been tested, especially under well-controlled conditions in captive bats. Hence, we aimed at tackling this question by performing playback experiments (habituation–dishabituation) with three horseshoe bat species within the constant-frequency bat guild, which included big-eared horseshoe bats (Rhinolophus macrotis), Blyth’s horseshoe bats (Rhinolophus lepidus), and Chinese horseshoe bats (Rhinolophus sinicus). We studied the behavioral responses of these three species to echolocation calls of conspecifics, to other two species, and to another heterospecifics bat, Stoliczka’s trident bat (Asellisus stoliczkanus), which also belongs to this guild. We found that the three rhinolophid species displayed a series of distinct behaviors to heterospecific echolocation but few to conspecific calls after habituation, suggesting that they may have been able to discriminate sympatric heterospecific echolocation calls from those of conspecifics. Interestingly, the behavioral responses to heterospecific calls were positively correlated with the interspecific overlap index in trophic niche, whereas call design had only a minor effect. This implies that the behavioral responses of these bats to heterospecific echolocation calls may be related to the degree of interspecific food competition.     

The functional significance of the diphasic advertisement call of Geocrinia victoriana (Anura: Leptodactylidae)

Summary The advertisement call of Geocrinia victoriana is markedly diphasic and consists of one introcuctory note (rarely two or three), followed by a series of repeated notes of similar carrier frequency, but much shorter duration and higher pulse rate. In two-choice field discrimination experiments with the two phases of the advertisement call presented as alternative stimuli, reproductively ripe females were attracted only to the repeated notes and contacted the source of these signals (a loudspeaker). Field playback experiments were carried out on residential males, with a complete call, an introductory note, or a series of repeated notes being used as the stimulus, and intensity varied upwards in 10 dB increments. With the complete call or the introductory note as the stimulus, calling behaviour of subjects altered significantly from the pre-stimulatory pattern, with a great reduction in output of repeated notes, and an increase in duration and decrease in pulse rate of introductory notes. The threshold intensity (lowest level for a significant change in calling behaviour) with the introductory note as the stimulus, 90–99.9 dB peak sound pressure level (PSPL), was at least 10 dB lower than that with the complete call as the stimulus (110–125 dB, PSPL). Playback of repeated notes had little effect on calling behaviour until the intensity exceeded 120 dB, PSPL. Playback of all three classes of stimulus at constant intensities below and above the threshold for the complete call (i.e. 99–99.9, and 110–125 dB, PSPL) indicated that changes in calling behaviour were due to the intensity of stimulus rather than to a cumulative effect based on the number of stimuli. Measurements of intensities of advertisement calls of nearest neighbours in natural breeding assemblages (modal class=104–106 dB, PSPL) were consistent with the experimental results. It was thus demonstrated that in G. victoriana the two functions of the advertisement call are partitioned: the repeated notes attract breeding females (hence are equivalent to the mating call), and the introductory notes are directed at other males in a territorial context. The increase in duration of the introductory note is graded rather than discrete, so that this phase of the advertisement call changes progressively from the equivalent of a long-range (first-order) to a short-range (second-order) territorial call, then to an encounter call.     

The structural significance of a vocalization that stimulates gaping in black-capped chickadees

In a variety of avian species, vocalizations used to stimulate gaping in nestlings during feeding share similar features such as broad frequency range, multiple spectral components, and sudden onset. It is currently not understood what functional significance, if any, these acoustic features have for close-range communication. One example of such a vocalization is the “squawk” of the black-capped chickadees (Parus atricapillus). The present study analyzes the significant features of the squawk by observing the response of chickadee nestlings to field playbacks of natural and computer-modified squawks. Of the features tested, frequency range appears most critical, but responses to frequency ranges change with age, such that low frequencies are most stimulating around the time of hatching but cease to elicit gaping after 5 days posthatch. Aperiodic stimuli and computer-modified squawks with gradual onsets tend to be less stimulating than natural squawks at some ages, but these differences are not significant at any age. The functional significance of the broad frequency range of the squawk is discussed, including the possible role of accommodating shifting frequency preferences related to ontogenetic changes in auditory sensitivity and elaboration of the vocal repertoire. Received: 16 January 1996 / Accepted after revision: 28 December 1996     

The effect of social interactions on calling energetics in the gray treefrog (Hyla versicolor)

Summary The vocal behavior of Hyla versicolor was studied in the field by means of behavioral observations and playback experiments, and these data were coupled with measurements of oxygen consumption in calling frogs to estimate the effect of social interactions on calling energetics. Male gray treefrogs have intense calls (median peak SPL=109 dB, fast RMS SPL=100 dB at 50 cm). At an air temperature of 23° C, males produced an average of 1,200–1,300 calls/h for 2–4 h per night. Calling rates and call durations differed among individuals, but were relatively constant for each male during periods of sustained calling. Males in dense choruses gave calls about twice as long as isolated males, but produced calls at about half the rate. Consequently, total calling effort and estimated aerobic costs were largely independent of chorus density. Playbacks of recorded calls to males in the field elicited increases in call duration and decreases in calling rate, regardless of the rate or duration of the stimulus. Males gave longer calls in response to long calls or to stimuli presented at high rates, but they did not precisely match either stimulus rate or duration. Calling effort and estimated oxygen consumption changed only slightly during stimulus playbacks. These results indicate that male-male competition elicits pro-found changes in the vocal behavior of calling males, but these changes have little effect on energy expenditure. We estimated that most calling males had metabolic rates of about 1.7–1.8 ml O₂/(g\h), or about 280 J/h for an average size (8.6 g) male at 20° C. Although changes in call duration and calling rate did not affect aerobic costs of calling, males producing long calls at slow rates called for fewer hours per night than males producing shorter calls at higher rates. This suggests that calling time may be limited by the rate at which muscle glycogen reserves are depleted.