Modelling the effects of chorus species composition and caller density on acoustic masking interference in multispecies choruses of crickets and katydids

Natural multispecies acoustic choruses such as the dusk chorus of a tropical rain forest consist of simultaneously signalling individuals of different species whose calls travel through a common shared medium before reaching their ‘intended’ receivers. This causes masking interference between signals and impedes signal detection, recognition and localization. The levels of acoustic overlap depend on a number of factors, including call structure, intensity, habitat-dependent signal attenuation and receiver tuning. In addition, acoustic overlaps should also depend on caller density and the species composition of choruses, including relative and absolute abundance of the different calling species. In this study, we used simulations to examine the effects of chorus species relative abundance and caller density on the levels of effective heterospecific acoustic overlap in multispecies choruses composed of the calls of five species of crickets and katydids that share the understorey of a rain forest in southern India. We found that on average species-even choruses resulted in higher levels of effective heterospecific acoustic overlap than choruses with strong dominance structures. This effect was found consistently across dominance levels ranging from 0.4 to 0.8 for larger choruses of forty individuals. For smaller choruses of twenty individuals, the effect was seen consistently for dominance levels of 0.6 and 0.8 but not 0.4. Effective acoustic overlap (EAO) increased with caller density but the manner and extent of increase depended both on the species' call structure and the acoustic context provided by the composition scenario. The Phaloria sp. experienced very low levels of EAO and was highly buffered to changes in acoustic context whereas other species experienced high EAO across contexts or were poorly buffered. These differences were not simply predictable from call structures. These simulation-based findings may have important implications for acoustic biodiversity monitoring and for the study of acoustic masking interference in natural environments.     

Phonotaxis to male’s calls embedded within a chorus by female gray treefrogs, Hyla versicolor

During the reproductive season, male Hyla versicolor produce advertisement calls to attract females. Females exhibit phonotaxis and approach the individual callers, resulting in amplexus. For frogs that call from dense choruses, the extent to which and the range from which a male’s advertisement call within a chorus can be heard by a receptive female leading to phonotaxis is unclear. We investigated females’ responses to natural choruses in the field and found that they were attracted and showed directed orientation to breeding choruses at distances up to 100 m. To assess the role of acoustic cues in the directed orientation, we conducted acoustic playback experiments in the laboratory using conspecific call and noise as stimuli, as well as chorus sounds (that contained calls from a focal male) recorded at various distances, all played at naturalistic intensities. Using two response metrics (females’ normalized response times and their phonotaxis trajectories) we found that, unlike the field experiments, females oriented and were attracted to chorus sounds from 1 to 32 m only, but not from >32 m, or to band-limited noise. Possible reasons for the observed difference in phonotaxis behavior in the two experimental conditions were discussed.     

Individual Distinctiveness in Call Types of Wild Western Female Gorillas

Individually distinct vocalizations play an important role in animal communication, allowing call recipients to respond differentially based on caller identity. However, which of the many calls in a species'' repertoire should have more acoustic variability and be more recognizable is less apparent. One proposed hypothesis is that calls used over long distances should be more distinct because visual cues are not available to identify the caller. An alternative hypothesis proposes that close calls should be more recognizable because of their importance in social interactions. To examine which hypothesis garners more support, the acoustic variation and individual distinctiveness of eight call types of six wild western gorilla (Gorilla gorilla) females were investigated. Acoustic recordings of gorilla calls were collected at the Mondika Research Center (Republic of Congo). Acoustic variability was high in all gorilla calls. Similar high inter-individual variation and potential for identity coding (PIC) was found for all call types. Discriminant function analyses confirmed that all call types were individually distinct (although for call types with lowest sample size - hum, grumble and scream - this result cannot be generalized), suggesting that neither the distance at which communication occurs nor the call social function alone can explain the evolution of identity signaling in western gorilla communication.     

Variability in spider monkeys' vocalizations may provide basis for individual recognition

Analysis of long-range vocalizations given by spider monkeys revealed consistent acoustic differences among the calls of individuals. Of seven acoustic measurements, four exhibited significant variation between individuals. A discriminant analysis demonstrated that two of these variables allowed correct identification of the caller 44% of the time. Including the remainder of the variables increased the percentage correctly identified to 50%. Individual identification by call structure could benefit spider monkeys, where individuals forage separately in subgroups and the interactions between specific pairs of individuals is highly variable. Acoustic recognition of callers would facilitate the choice of which subgroups to join, thus allowing individuals to manipulate the size and composition of their subgroups. In addition, the calls of mothers and offspring appeared to be similar in acoustic properties.     

Acoustic Preference of Frog‐Biting Midges (Corethrella spp) Attacking Túngara Frogs in their Natural Habitat

In many animals, males aggregate to produce mating signals that attract conspecific females. These leks, however, also attract eavesdropping predators and parasites lured by the mating signal. This study investigates the acoustic preferences of eavesdroppers attracted to natural choruses in a Neotropical frog, the túngara frog (Engystomops pustulosus). In particular, we examined the responses of frog‐biting midges to natural variation in call properties and signaling rates of males in the chorus. These midges use the mating calls of the frogs to localize them and obtain a blood meal. Although it is known that the midges prefer complex over simple túngara frog calls, it is unclear how these eavesdroppers respond to natural call variation when confronted with multiple males in a chorus. We investigated the acoustic preference of the midges using calling frogs in their natural environment and thus accounted for natural variation in their call properties. We performed field recordings using a sound imaging system to quantify the temporal call properties of males in small choruses. During these recordings, we also collected frog‐biting midges attacking calling males. Our results revealed that, in a given chorus, male frogs calling at higher rates and with higher call complexity attracted a larger number of frog‐biting midges. Call rate was particularly important at increasing the number of midges attracted when males produced calls of lower complexity. Similarly, call complexity increased attractiveness to the midges especially when males produced calls at a low repetition rate. Given that female túngara frogs prefer calls produced at higher repetition rates and higher complexity, this study highlights the challenge faced by signalers when increasing attractiveness of the signal to their intended receivers.     

Stress hormone is implicated in satellite-caller associations and sexual selection in the Great Plains toad

The effects of androgens on male-typical traits suggest that variation among males in circulating levels can play a major role in sexual selection. We examined whether variation in vocal attractiveness is attributable to differences in androgen levels among Great Plains toads (Bufo cognatus). We found that noncalling "satellite" males practicing an alternative mating tactic were more likely to associate with males producing long calls. However, callers with satellites did not have higher androgen levels than callers without satellites. Rather, callers with satellites had significantly lower corticosterone (CORT) levels than callers without satellites. A CORT manipulation experiment suggested that differences in calls for males with and without satellites were related to differences in CORT levels. Furthermore, there was a negative correlation between CORT level and call duration within most nights of chorus activity. However, the correlation was weak for the pooled data (across all nights), suggesting that local environmental and/or social factors also affect call duration. Last, we show that females preferred broadcast calls of longer duration, characteristic of males with satellites and low CORT. These results imply that satellites optimize their reproductive success by associating with males producing long calls. However, this association should negatively affect the fitness of attractive callers.     

The Structure of Bonobo Copulation Calls During Reproductive and Non‐Reproductive Sex

Copulation calls in primates are usually identified as sexually selected signals that promote the reproductive success of the caller. In this study, we investigated the acoustic structure of copulation calls in bonobos (Pan paniscus), a great ape known for its heightened socio‐sexuality. Throughout their cycles, females engage in sexual relations with both males and other females and produce copulation calls with both partners. We found that calls produced during sexual interactions with male and female partners could not be reliably distinguished in terms of their acoustic structure, despite major differences in mating behaviour and social context. Call structure was equally unaffected by the size of a female’s sexual swelling and by the rank of her mating partner. Rank of the partner did affect call delivery although only with male, but not female partners. The only strong effect on call structure was because of caller identity, suggesting that these signals primarily function to broadcast individual identity during sexual interactions. This primarily social use of an evolved reproductive signal is consistent with a broader trend seen in this species, namely a transition of sexual behaviour to social functions.     

The function of loud calls (Hoot Series) in wild western gorillas (Gorilla gorilla)

The use of loud vocal signals to reduce distance among separated social partners is well documented in many species; however, the underlying mechanisms by which the reduction of spacing occurs and how they differ across species remain unclear. Western gorillas (Gorilla gorilla) offer an opportunity to investigate these issues because their vocal repertoire includes a loud, long‐distance call (i.e., hoot series) that is potentially used in within‐group communication, whereas mountain gorillas use an identical call exclusively during intergroup encounters. First, we tested whether the hoot series functions as a contact/separation call. Second, we examined which individuals were more likely to reply and which party was more responsible for decreasing distance to identify the underlying mechanisms and cognitive implications of hoot series. We collected behavioral, spatial, and acoustic data on five adult gorillas over 15 months at the Mondika Research Center (Republic of Congo and CAR). Hoot series are individually distinct calls and given by both male and female gorillas when separated from each other. Following hooting, the distance between separated group members decreased significantly; thus we concluded that western gorillas use this call to reestablish group cohesion. The way in which proximity was achieved depended upon listeners replying or not to the caller. Replies may indicate a conflict between callers about intended travel direction, with vocal interchanges serving to negotiate a consensus. Although the acoustic features of vocal signals are highly constrained in closely related species, our results demonstrate that the function and usage of particular calls can be flexible. Am J Phys Anthropol 155:379–391, 2014. © 2014 Wiley Periodicals, Inc.     

Faecal glucocorticoid metabolites and alarm calling in free-living yellow-bellied marmots

When individuals of a variety of species encounter a potential predator, some, but not all, emit alarm calls. To explain the proximate basis of this variation, we compared faecal glucocorticoid metabolite concentrations in live-trapped yellow-bellied marmots (Marmota flaviventris) between occasions when they did and did not emit alarm calls. We found that marmots had significantly higher glucocorticoid levels when they called than when they did not call, suggesting that stress or arousal may play an important role in potentiating alarm calls. Marmots are sensitive to variation in the reliability of callers. The present finding provides one possible mechanism underlying caller variation: physiological arousal influences the propensity to emit alarm calls.     

Is Alarm Calling Risky? Marmots Avoid Calling from Risky Places

Alarm calling is common in many species. A prevalent assumption is that calling puts the vocalizing individual at increased risk of predation. If calling is indeed costly, we need special explanations for its evolution and maintenance. In some, but not all species, callers vocalize away from safety and thus may be exposed to an increased risk of predation. However, for species that emit bouts with one or a few calls, it is often difficult to identify the caller and find the precise location where a call was produced. We analyzed the spatial dynamics of yellow-bellied marmot (Marmota flaviventris) alarm calling using an acoustic localization system to determine the location from which calls were emitted. Marmots almost always called from positions close to the safety of their burrows, and, if they produced more than one alarm call, tended to end their calling bouts closer to safety than they started them. These results suggest that for this species, potential increased predation risk from alarm calling is greatly mitigated and indeed calling may have limited predation costs.     

Little Brown Bats (Myotis lucifugus) Recognize Individual Identity of Conspecifics Using Sonar Calls

Bats use sonar calls to locate prey and orient in their environment but they may also be used by conspecifics to obtain information about a caller. Statistical analysis of sonar calls provides evidence that variation carries social information about a caller, including individual identity. We hypothesized that little brown bats (Myotis lucifugus) would be able to recognize individuals given the potential fitness benefits of doing so. We performed playback trials using a habituation‐discrimination design to determine whether little brown bats are able to recognize the individual identity of a caller based on variation in their sonar calls. Each subject bat was played the calls of bat A until they habituated (defined as a 50% decrease from the beginning call rate), then the calls of bat B or a new call sequence of bat A (a control, referred to as bat A’) were played. Each subject received a unique pair of playback recordings (bat A and B) from adult female bats from the same colony (but a different colony from the subject) and the order of trials was randomized. The response measures were habituation time (s) and call rate (calls/s). Within a trial, subjects habituated to calls of bat A and transferred this habituation to the bat A’ sequence. In addition, they increased their call rates when played calls of bat B. Comparing between trials, subjects increased their call rate to the calls of bat B to a greater relative extent than to the calls of bat A’. These results provide the first evidence that bats recognize individual identity of conspecifics (as opposed to discrimination of groups), which has implications for the social interactions of bats.     

Call type signals caller goal: a new take on ultimate and proximate influences in vocal production

After 40 years of debate it remains unclear whether signallers produce vocalizations in order to provide receivers with information about call context or external stimuli. This has led some researchers to propose that call production is arousal‐ or affect‐based. Although arousal influences certain acoustic parameters within a call type, we argue that it cannot explain why individuals across vertebrates produce different call types. Given emerging evidence that calls are goal‐based, we argue that call type is a signal of a caller's goal to elicit a change in receiver behaviour. Using chimpanzees (Pan troglodytes) and vervet monkeys (Cercopithecus aethiops) as case studies, we demonstrate the two benefits of viewing call production as signalling both caller goal (which determines call type) and caller arousal (which affects within‐call‐type variation). Such a framework can explain first, why a single class of calls is apparently given in multiple contexts, and, second, why some species have larger call repertoires than others. Previous studies have noted links between sociality and repertoire size, but have not specified exactly why animals living in societies that are more complex might require a greater number of differentiated signals. The caller‐goal framework potentially clarifies how social complexity might favour call diversification. As social complexity increases, callers may need to elicit a larger number of distinct behaviours from a wider range of distinct audiences.     

Reliability and the adaptive utility of discrimination among alarm callers

Unlike individually distinctive contact calls, or calls that aid in the recognition of young by their parents, the function or functions of individually distinctive alarm calls is less obvious. We conducted three experiments to study the importance of caller reliability in explaining individual-discriminative abilities in the alarm calls of yellow-bellied marmots (Marmota flaviventris). In our first two experiments, we found that calls from less reliable individuals and calls from individuals calling from a greater simulated distance were more evocative than calls from reliable individuals or nearby callers. These results are consistent with the hypothesis that marmots assess the reliability of callers to help them decide how much time to allocate to independent vigilance. The third experiment demonstrated that the number of callers influenced responsiveness, probably because situations where more than a single caller calls, are those when there is certain to be a predator present. Taken together, the results from all three experiments demonstrate the importance of reliability in explaining individual discrimination abilities in yellow-bellied marmots. Marmots' assessment of reliability acts by influencing the time allocated to individual assessment and thus the time not allocated to other activities.     

A comparison of individual distinctiveness in three vocalizations of the dwarf mongoose (Helogale parvula)

Individual specificity can be found in the vocalizations of many avian and mammalian species. However, it is often difficult to determine whether these vocal cues to identity rise from “unselected” individual differences in vocal morphology or whether they have been accentuated by selection for the purposes of advertising caller identity. By comparing the level of acoustic individuality of different vocalizations within the repertoire of a single species, it is possible to ascertain whether selection for individual recognition has modified the vocal cues to identity in particular contexts. We used discriminant function analyses to determine the level of accuracy with which calls could be classified to the correct individual caller, for three dwarf mongoose (Helogale parvula) vocalizations: contact, snake, and isolation calls. These calls were similar in acoustic structure but divergent in context and function. We found that all three call types showed individual specificity but levels varied with call type (increasing from snake to contact to isolation call). The individual distinctiveness of each call type appeared to be directly related to the degree of benefit that signalers were likely to accrue from advertising their identity within that call context. We conclude that dwarf mongoose signalers have undergone selection to facilitate vocal individual recognition, particularly in relation to the species’ isolation call.     

Alarm calls of the Cyprus Wheatear Oenanthe cypriaca—one for nest defence, one for parent–offspring communication?

Alarm calling has been interpreted from the viewpoint of parental investment and nest defence. Calling should increase with an increasing value of the brood to the caller or with increasing vulnerability of the brood. Parental alarm calling might also be viewed from assessment–management with callers using vocalisations to elicit affective responses in others, e.g. in silencing offspring. I examined parental alarm calling in the Cyprus Wheatear (Oenanthe cypriaca) at different developmental stages. The Cyprus Wheatear produces two alarm calls, but one is emitted only during a short period of the year (type II alarm call). The commoner alarm call (type I alarm call), however, is used year-round. Predation was simulated using consistent approach by human observers. The brood cycle was divided into (I) incubation, (II) nestling, (III) early fledging, and (IV) late fledging. Type I calls increased from phases I to III, and decreased afterwards. Type II calls were absent during incubating and occurred during nestling and early fledging stages. As a conclusion, I suggest that the type I alarm call might be used to alert the mate, deter the predator and signal strength of nest defence, while the type II alarm call is addressed to offspring.     

The communicative content of the common marmoset phee call during antiphonal calling

Vocalizations are a dominant means of communication for numerous species, including nonhuman primates. These acoustic signals are encoded with a rich array of information available to signal receivers that can be used to guide species‐typical behaviors. In this study, we examined the communicative content of common marmoset phee calls, the species‐typical long distance contact call, during antiphonal calling. This call type has a relatively stereotyped acoustic structure, consisting of a series of long tonal pulses. Analyses revealed that calls could be reliably classified based on the individual identity and social group of the caller. Our analyses did not, however, correctly classify phee calls recorded under different social contexts, although differences were evident along individual acoustic parameters. Further tests of antiphonal calling interactions showed that spontaneously produced phee calls differ from antiphonal phee calls in their peak and end frequency, which may be functionally significant. Overall, this study shows that the marmoset phee call has a rich communicative content encoded in its acoustic structure available to conspecifics during antiphonal calling exchanges. Am. J. Primatol. 72:974–980, 2010. © 2010 Wiley‐Liss, Inc.     

Predation increases acoustic complexity in primate alarm calls

According to most accounts, alarm calling in non-human primates is a biologically hardwired behaviour with signallers having little control over the acoustic structure of their calls. In this study, we compared the alarm calling behaviour of two adjacent populations of Diana monkeys at Taï forest (Ivory Coast) and Tiwai Island (Sierra Leone), which differ significantly in predation pressure. At Taï, monkeys regularly interact with two major predators, crowned eagles and leopards, while at Tiwai, monkeys are only hunted by crowned eagles. We monitored the alarm call responses of adult male Diana monkeys to acoustic predator models. We found no site-specific differences in the types of calls given to eagles, leopards and general disturbances, but there were consistent differences in how callers assembled calls into sequences. At Tiwai, males responded to leopards and general disturbances in the same way, while at Taï, males discriminated by giving call sequences that differed in the number of component calls. Responses to eagles were identical at both sites. We concluded that Diana monkeys are predisposed to use their repertoire in context-specific ways, but that ontogenetic experience determines how individual calls are assembled into meaningful sequences.     

Production and perception of sex differences in vocalizations of Wied's black‐tufted‐ear marmosets (Callithrix kuhlii)

Males and females from many species produce distinct acoustic variations of functionally identical call types. Social behavior may be primed by sex‐specific variation in acoustic features of calls. We present a series of acoustic analyses and playback experiments as methods for investigating this subject. Acoustic parameters of phee calls produced by Wied's black‐tufted‐ear marmosets (Callithrix kuhlii) were analyzed for sex differences. Discriminant function analyses showed that calls contained sufficient acoustic variation to predict the sex of the caller. Several frequency variables differed significantly between the sexes. Natural and synthesized calls were presented to male–female pairs. Calls elicited differential behavioral responses based on the sex of the caller. Marmosets became significantly more vigilant following the playback of male phee calls (both natural and synthetic) than following female phee calls. In a second playback experiment, synthesized calls were modified by independently manipulating three parameters that were known to differ between the sexes (low‐, peak‐, and end‐frequency). When end‐frequency‐modified calls were presented, responsiveness was differentiable by sex of caller but did not differ from responses to natural calls. This suggests that marmosets did not use end‐frequency to determine the sex of the caller. Manipulation of peak‐and low‐frequency parameters eliminated the discrete behavioral responses to male and female calls. Together, these parameters may be important features that encode for the sex‐specific signal. Recognition of sex by acoustic cues seems to be a multivariate process that depends on the congruency of acoustic features. Am. J. Primatol. 71:324–332, 2009. © 2008 Wiley‐Liss, Inc.     

Female preference function related to precedence effect in an amphibian anuran (Alytes cisternasii): tests with non-overlapping calls

We quantified precedence effect (measured as female preferencefor the leading calls in an acoustic interaction between twomales) with non-overlapping, simulated male calls presentedwith various phase relationships to female Iberian midwifetoads (Alytes cisternasii) in two-speaker phonotaxis playbacktests. The resulting information determines the shape of thefemale preference function for intercall delays. Females preferentiallyapproached leading callers for most tested phase angles. We found a gradation in the degree to which females selected theleader. They tended to exert a strong preference for the leaderin 30° test, and at higher phase angles, the overall preferencewas weaker and graded (the higher the phase angle, the lowerthe preference). Other parameters of female preference (latencyand repeatability) also had a graded relationship with phaseangle value. The sharp difference in probability of approachbetween 30° and 60° is consistent with a mechanismof male calling inhibition immediately after hearing a competitor'scall previously described in other taxa. In natural interactions,male A. cisternasii adjust the timing of their calls to a phaseangle that provides a slight but significant advantage to theleading caller.     

The Acoustic Properties of Low Intensity Vocalizations Match Hearing Sensitivity in the Webbed-Toed Gecko,Gekko subpalmatus

The design of acoustic signals and hearing sensitivity in socially communicating species would normally be expected to closely match in order to minimize signal degradation and attenuation during signal propagation. Nevertheless, other factors such as sensory biases as well as morphological and physiological constraints may affect strict correspondence between signal features and hearing sensitivity. Thus study of the relationships between sender and receiver characteristics in species utilizing acoustic communication can provide information about how acoustic communication systems evolve. The genus Gekko includes species emitting high-amplitude vocalizations for long-range communication (loud callers) as well as species producing only low-amplitude vocalizations when in close contact with conspecifics (quiet callers) which have rarely been investigated. In order to investigate relationships between auditory physiology and the frequency characteristics of acoustic signals in a quiet caller, Gekko subpalmatus we measured the subjects’ vocal signal characteristics as well as auditory brainstem responses (ABRs) to assess auditory sensitivity. The results show that G. subpalmatus males emit low amplitude calls when encountering females, ranging in dominant frequency from 2.47 to 4.17 kHz with an average at 3.35 kHz. The auditory range with highest sensitivity closely matches the dominant frequency of the vocalizations. This correspondence is consistent with the notion that quiet and loud calling species are under similar selection pressures for matching auditory sensitivity with spectral characteristics of vocalizations.