Multiple signals and male spacing affect female preference at cocktail parties in treefrogs

Effective acoustic communication in the face of intense conspecific background noise constitutes a constant sensory challenge in chorusing and colonial species. An evolutionary approach suggests that behavioural and environmental constraints in these species should have shaped signal design and signalling behaviour to enable communication in noisy conditions. This could be attained both through the use of multicomponent signals and through short-term adjustments in the spatial separation of calling males. We investigated these two hypotheses in a chorusing anuran, the hylid Hyla arborea, through a series of phonotaxis experiments conducted within a six-speaker arena in a high background noise situation, by presenting females with male calls containing either single or multiple attractive call components, and by modifying distances between speakers. We found that female ability to discriminate attractive calls increased when several attractive call components were available, providing novel evidence that the use of multicomponent signals enhances communication in complex acoustic conditions. Signal discrimination in females also improved with speaker separation, demonstrating that within natural choruses, spatial unmasking conditioned by male density and spatial separation probably improves female discrimination of competing males. Implications of these results for the accuracy of mate choice within choruses are discussed.     

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 three main call types in common cuckoo

Acoustic signals play a key role in shaping the relationships in birds. Common cuckoos Cuculus canorus are known to produce various call types, but the function of these calls has only been studied recently. Here, we used a combination of field recordings (conducted in 2017) and playback experiments (conducted in 2018) to investigate the functional significance of common cuckoo calls. We found significant differences in the characteristics between male two‐element “cu‐coo” and three‐element “cu‐cu‐coo” calls, with these two call types being used in different contexts. The three‐element male “cu‐cu‐coo” calls were associated with females emitting their “bubbling” call. Playback experiments revealed that both males and females exhibit stronger responses to playing female “bubbling” calls than with the calls of the Eurasian sparrowhawk (Accipter nisus) serving as a control, suggesting a significant intraspecific communication function for this call type. However, we did not find any evidence to support mate attraction in male calls, as females were not stimulated by playback of male calls compared with sparrowhawk calls in the control group.     

No pre-existing biases for heterospecific call traits in the frog Physalaemus enesefae

Previous phonotaxis studies with two species of the Physalaemuspustulosus species group indicated that female preferences for several heterospecific call traits resulted from sensory biases inherited from a common ancestor. In phonotaxis experiments, we determined whether Physalaemus enesefae, a distant relative of the P. pustulosus group, showed similar preferences for call traits not present in conspecific males. We presented females with a choice between the typical conspecific advertisement call and the same call to which we digitally appended a chuck from P. pustulosus, a squawk from P. freibergi, and an amplitude-modulated prefix from P. pustulatus. In addition we presented the advertisement call in doublets, a trait peculiar to P. coloradorum. We also analysed male vocal behaviour evoked in response to the same suite of stimuli. Physalaemus enesefae females did not prefer the calls of their own males with appended heterospecific traits over unmodified calls, nor conspecific calls in doublets over single calls. The lack of preference among females was not the result of a behavioural polymorphism. Female responses to repeated presentations of the same stimulus pair were not consistent. Males also did not show an enhanced vocal response to altered calls relative to the typical conspecific call. Consequently, there are no pre-existing biases for these heterospecific call traits in P. enesefae; pre-existing preferences in the P. pustulosus group could have been inherited from an ancestor not shared with P. enesefae, but data from other closely related species are needed to confirm this conclusion. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Interspecific signalling between mutualists: food-thieving drongos use a cooperative sentinel call to manipulate foraging partners

Interspecific communication is common in nature, particularly between mutualists. However, whether signals evolved for communication with other species, or are in fact conspecific signals eavesdropped upon by partners, is often unclear. Fork-tailed drongos (Dicrurus adsimilis) associate with mixed-species groups and often produce true alarms at predators, whereupon associating species flee to cover, but also false alarms to steal associating species'' food (kleptoparasitism). Despite such deception, associating species respond to drongo non-alarm calls by increasing their foraging and decreasing vigilance. Yet, whether these calls represent interspecific sentinel signals remains unknown. We show that drongos produced a specific sentinel call when foraging with a common associate, the sociable weaver (Philetairus socius), but not when alone. Weavers increased their foraging and decreased vigilance when naturally associating with drongos, and in response to sentinel call playback. Further, drongos sentinel-called more often when weavers were moving, and weavers approached sentinel calls, suggesting a recruitment function. Finally, drongos sentinel-called when weavers fled following false alarms, thereby reducing disruption to weaver foraging time. Results therefore provide evidence of an ‘all clear’ signal that mitigates the cost of inaccurate communication. Our results suggest that drongos enhance exploitation of a foraging mutualist through coevolution of interspecific sentinel signals.     

Acoustic Properties of Long Calls Given by Flanged Male Orang‐Utans (Pongo pygmaeus wurmbii) Reflect Both Individual Identity and Context

Long calls by flanged male Bornean orang‐utans (Pongo pygmaeus wurmbii) serve as a long‐distance communication signal in this semi‐solitary species and allow individuals to adjust their ranging behavior. Long calls can be heard up to circa 1 km in dense rainforest. Only flanged males emit them, in various contexts: spontaneously (where no disturbances from the environment are perceived by human observers), when highly aroused by another male’s long call or a falling tree nearby, or right after having pushed over a dead tree themselves. In this study, acoustic analyses of orang‐utan long calls at Tuanan in Central Kalimantan not only confirm the discrimination of individual males by their long calls but also demonstrate the discrimination of context based on the long calls’ acoustic structure, which is further supported by the females’ ranging responses according to long call contexts. Females with dependent offspring move away from spontaneous long call sources but appear to ignore long calls elicited by disturbance. Hence, Bornean orang‐utan females perceive measurable differences in acoustic characteristics of long calls given in different contexts. These findings concur with vocal discrimination of contexts in other non‐human primates.     

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

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

Vocal communication in a neotropical treefrog, Hyla ebraccata: Advertisement calls

We studied the vocal communication of Hyla ebraccata in central Panama. The advertisement call of this species consists of a pulsed buzz-like primary note which may be given alone or followed by 1–4 secondary click notes. Primary notes are highly stereotyped, showing little variation within or0 among individuals in dominant frequency, duration, pulse repetition rate or rise time. Males calling in isolation give mostly single-note calls. They respond to playbacks of conspecific calls by increasing calling rates and the proportion of multi-note calls, and by giving synchronized calls 140–200 ms after the stimulus begins. Responses to conspecific advertisement calls are usually given immediately after the primary note of the leading call, but the primary note of the response often overlaps with the click notes of the leading call. Experiments with synthetic signals showed that males synchronize to any type of sound of the appropriate frequency (3 kHz), regardless of the fine structure of the stimulus. Playbacks of synthetic calls of variable duration showed that males do not synchronize well to calls less than 150 ms long, but they do to longer calls (200–600 ms). The variance in response latency increased with increasing stimulus duration, but modal response times remained at around 140–200 ms. Similar results were obtained in experiments withsynthetic calls having a variable number of click notes. Males showed no tendency to increase the number of click notes in their calls in response to increasing stimulus duration or increasing number of clicks in the stimulus. Females preferred three-note to one-note calls in two-choice playback experiments, whether these were presented in alternation, or with the one-note call leading and the three-note call following. Females showed no preference for leader or follower calls when both were one-note. When two-note calls were presented with the primary note of the follower overlapping the click note of the leader, females went to calls in which click notes were not obscured. Our results indicate that male H. ebraccata respond to other males in a chorus in ways which enhance their ability to attract mates.     

Traffic noise differentially impacts call types in a Japanese treefrog (Buergeria japonica)

Acoustic noise from automobile traffic impedes communication between signaling animals. To overcome the acoustic interference imposed by anthropogenic noise, species across taxa adjust their signaling behavior to increase signal saliency. As most of the spectral energy of anthropogenic noise is concentrated at low acoustic frequencies, species with lower frequency signals are expected to be more affected. Thus, species with low-frequency signals are under stronger pressure to adjust their signaling behaviors to avoid auditory masking than species with higher frequency signals. Similarly, for a species with multiple types of signals that differ in spectral characteristics, different signal types are expected to be differentially masked. We investigate how the different call types of a Japanese stream breeding treefrog (Buergeria japonica) are affected by automobile traffic noise. Male B. japonica produce two call types that differ in their spectral elements, a Type I call with lower dominant frequency and a Type II call with higher dominant frequency. In response to acoustic playbacks of traffic noise, B. japonica reduced the duration of their Type I calls, but not Type II calls. In addition, B. japonica increased the call effort of their Type I calls and decreased the call effort of their Type II calls. This result contrasts with prior studies in other taxa, which suggest that signalers may switch to higher frequency signal types in response to traffic noise. Furthermore, the increase in Type I call effort was only a short-term response to noise, while reduced Type II call effort persisted after the playbacks had ended. Overall, such differential effects on signal types suggest that some social functions will be disrupted more than others. By considering the effects of anthropogenic noise across multiple signal types, these results provide a more in-depth understanding of the behavioral impacts of anthropogenic noise within a species.     

SPECIES RECOGNITION AND SEXUAL SELECTION AS A UNITARY PROBLEM IN ANIMAL COMMUNICATION

We investigated patterns of mating call preference and mating call recognition by examining phonotaxis of female túngara frogs, Physalaemus pustulosus, in response to conspecific and heterospecific calls. There are four results: females always prefer conspecific calls; most heterospecific calls do not elicit phonotaxis; some heterospecific calls do elicit phonotaxis and thus are effective mate recognition signals; and females prefer conspecific calls to which a component of a heterospecific call has been added to a normal conspecific call. We use these data to illustrate how concepts of species recognition and sexual selection can be understood in a unitary framework by comparing the distribution of signal traits to female preference functions.     

‘Compromise’ in Echolocation Calls between Different Colonies of the Intermediate Leaf-Nosed Bat (Hipposideros larvatus)

Each animal population has its own acoustic signature which facilitates identification, communication and reproduction. The sonar signals of bats can convey social information, such as species identity and contextual information. The goal of this study was to determine whether bats adjust their echolocation call structures to mutually recognize and communicate when they encounter the bats from different colonies. We used the intermediate leaf-nosed bats (Hipposideros larvatus) as a case study to investigate the variations of echolocation calls when bats from one colony were introduced singly into the home cage of a new colony or two bats from different colonies were cohabitated together for one month. Our experiments showed that the single bat individual altered its peak frequency of echolocation calls to approach the call of new colony members and two bats from different colonies adjusted their call frequencies toward each other to a similar frequency after being chronically cohabitated. These results indicate that the ‘compromise’ in echolocation calls might be used to ensure effective mutual communication among bats.     

Evolution of Novel Signal Traits in the Absence of Female Preferences in Neoconocephalus Katydids (Orthoptera,Tettigoniidae)

Background Significance

Communication signals that function to bring together the sexes are important for maintaining reproductive isolation in many taxa. Changes in male calls are often attributed to sexual selection, in which female preferences initiate signal divergence. Natural selection can also influence signal traits if calls attract predators or parasitoids, or if calling is energetically costly. Neutral evolution is often neglected in the context of acoustic communication.

Methodology/Principal Findings

We describe a signal trait that appears to have evolved in the absence of either sexual or natural selection. In the katydid genus Neoconocephalus, calls with a derived pattern in which pulses are grouped into pairs have evolved five times independently. We have previously shown that in three of these species, females require the double pulse pattern for call recognition, and hence the recognition system of the females is also in a derived state. Here we describe the remaining two species and find that although males produce the derived call pattern, females use the ancestral recognition mechanism in which no pulse pattern is required. Females respond equally well to the single and double pulse calls, indicating that the derived trait is selectively neutral in the context of mate recognition.

Conclusions/Significance

These results suggest that 1) neutral changes in signal traits could be important in the diversification of communication systems, and 2) males rather than females may be responsible for initiating signal divergence.     

FORMS OF CALL OVERLAP AND THEIR IMPACT ON ADVERTISEMENT CALL ATTRACTIVENESS TO FEMALES OF THE GRAY TREEFROG,HYLA VERSICOLOR

ABSTRACT

Male gray Lreefrogs, Hyla versicolor, advertise for females in choruses in which calls often overlap. Previous research has demonstrated that such acoustic interference among conspecifics can impair the ability of a male to attract a mate. However, the stimulus set used in those studies was quite limited. Here we performed single-speaker and two-speaker tests of phonotaxis with female Hyla versicolor to explore the impact of different degrees and forms of call overlap on the relative attractiveness of male signals. We found that: (1) overlapped calls are recognized as acceptable signals by females, although they are less attractive than calls that are not overlapped; (2) the relative phase of the overlapping calls matters. When calls were time-shifted by 50% of their pulse-period (180 degree offset), attractiveness of overlapped calls was reduced relative to non-overlapped calls as much as it would be by a reduction in intensity of about 12 dB SPL or a drop in call duration of between one third to one half. A 90 degree phase offset was equivalent to a 3 dB drop in SPL; (3) partial call overlap may not impair call attractiveness if one third or less of the call is overlapped; (4) if the ending portion of a call is overlapped it may impair attractiveness less than if previous segments of a call are obscured; (5) if most (three fourths or more) of a male's calls are free of interference, overlap of his remaining calls does not significantly impair his attractiveness.     

Evolutionary diversification of the auditory organ sensilla in Neoconocephalus katydids (Orthoptera: Tettigoniidae) correlates with acoustic signal diversification over phylogenetic relatedness and life history

Neoconocephalus Tettigoniidae are a model for the evolution of acoustic signals as male calls have diversified in temporal structure during the radiation of the genus. The call divergence and phylogeny in Neoconocephalus are established, but in tettigoniids in general, accompanying evolutionary changes in hearing organs are not studied. We investigated anatomical changes of the tympanal hearing organs during the evolutionary radiation and divergence of intraspecific acoustic signals. We compared the neuroanatomy of auditory sensilla (crista acustica) from nine Neoconocephalus species for the number of auditory sensilla and the crista acustica length. These parameters were correlated with differences in temporal call features, body size, life histories and different phylogenetic positions. By this, adaptive responses to shifting frequencies of male calls and changes in their temporal patterns can be evaluated against phylogenetic constraints and allometry. All species showed well‐developed auditory sensilla, on average 32–35 between species. Crista acustica length and sensillum numbers correlated with body size, but not with phylogenetic position or life history. Statistically significant correlations existed also with specific call patterns: a higher number of auditory sensilla occurred in species with continuous calls or slow pulse rates, and a longer crista acustica occurred in species with double pulses or slow pulse rates. The auditory sensilla show significant differences between species despite their recent radiation, and morphological and ecological similarities. This indicates the responses to natural and sexual selection, including divergence of temporal and spectral signal properties. Phylogenetic constraints are unlikely to limit these changes of the auditory systems.     

Geographical variation in male advertisement calls and female preference of the wide‐ranging canyon treefrog,Hyla arenicolor

We surveyed the geographical variation in male advertisement calls of the wide‐ranging canyon treefrog, Hyla arenicolor, and found large call differences among geographically distant lineages that had been characterized by a recent phylogeographical study. To test whether these call differences were biologically relevant and could allow reproductive isolation of different lineages should they come into secondary contact, we assessed female preference in a lineage occurring in southern Utah and north‐western Arizona, USA. These females exhibited a strong preference for their own lineage's call type over the calls of two Mexican lineages, but not over the calls from the geographically nearest lineage. We also identified traits that female frogs probably use to discriminate between lineage‐specific advertisement calls. Our behavioural results, together with recent molecular estimates of phylogenetic relationships among lineages, will guide future work addressing the evolutionary forces that have led to this biologically significant variation in male sexual signals. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

Exposure to Advertisement Calls of Reproductive Competitors Activates Vocal-Acoustic and Catecholaminergic Neurons in the Plainfin Midshipman Fish,Porichthys notatus

While the neural circuitry and physiology of the auditory system is well studied among vertebrates, far less is known about how the auditory system interacts with other neural substrates to mediate behavioral responses to social acoustic signals. One species that has been the subject of intensive neuroethological investigation with regard to the production and perception of social acoustic signals is the plainfin midshipman fish, Porichthys notatus, in part because acoustic communication is essential to their reproductive behavior. Nesting male midshipman vocally court females by producing a long duration advertisement call. Females localize males by their advertisement call, spawn and deposit all their eggs in their mate’s nest. As multiple courting males establish nests in close proximity to one another, the perception of another male’s call may modulate individual calling behavior in competition for females. We tested the hypothesis that nesting males exposed to advertisement calls of other males would show elevated neural activity in auditory and vocal-acoustic brain centers as well as differential activation of catecholaminergic neurons compared to males exposed only to ambient noise. Experimental brains were then double labeled by immunofluorescence (-ir) for tyrosine hydroxylase (TH), an enzyme necessary for catecholamine synthesis, and cFos, an immediate-early gene product used as a marker for neural activation. Males exposed to other advertisement calls showed a significantly greater percentage of TH-ir cells colocalized with cFos-ir in the noradrenergic locus coeruleus and the dopaminergic periventricular posterior tuberculum, as well as increased numbers of cFos-ir neurons in several levels of the auditory and vocal-acoustic pathway. Increased activation of catecholaminergic neurons may serve to coordinate appropriate behavioral responses to male competitors. Additionally, these results implicate a role for specific catecholaminergic neuronal groups in auditory-driven social behavior in fishes, consistent with a conserved function in social acoustic behavior across vertebrates.     

Multisensory signals trigger approach behaviour in the fire-bellied toad Bombina orientalis: sex differences and call specificity

Animal communication often involves multimodal signals, and interactions between sensory modalities can trigger unique responses in receivers. Response to social signals was investigated in fire-bellied toads by exposing them to playback of male calls (advertisement and release calls) and a video clip of a male conspecific in the laboratory. The cues were presented in isolation and as a combined bimodal stimulus, and approach frequency, latency to approach and time spent around the stimulus source were measured. No positive phonotaxis was observed toward the advertisement call, both during the day and during a phonotaxis trial performed at night. However, females, but not males, approached with greater frequency, lower latency, and spent more time near the source of the bimodal stimulus in an experiment involving the advertisement call. Female response was specific to the advertisement call, as approach was not increased when the release call was used. Males, on the other hand, did not show increased approach in the advertisement call experiment, but approached with greater frequency the bimodal stimulus involving the release call within the first minute of stimulus presentation. The findings suggest that females orient toward calling males and that males eavesdrop on release calls, but in both cases a visual stimulus is also needed to trigger a response. Social approach in Bombina orientalis is thus dependent on multisensory cues, and the nature of the interaction between sensory modalities depends on receiver sex and call type.     

Male orientation on vocalization perches could optimize acoustic signal transmission in anurans

Acoustic signals are distorted by vegetation, wind currents, or other sounds when transmitted through the environment. Consequently, vocalizations with features that optimize sound transmission or behaviors that improve the efficacy of communication have evolved in many animal species. Among behavioral strategies, some species call from perches above the ground to increase the propagation distance of their acoustic signals. However, the orientation in the perch also influences the transmission of the vocalizations, so that frogs calling from different orientations (i.e., horizontal, upward, or downward) may affect differently the quality and efficacy of sound transmission. We implemented a sound transmission experiment to test for the effect of calling orientation (upward, downward, and horizontal) and distance on the attenuation and degradation of advertisement calls in the common dink frog Diasporus diastema. We broadcasted and re‐recorded advertisement calls at 2 m height, setting the speaker in three directions (upward, downward, and horizontal) to simulate different signaler orientations. We found that attenuation of the advertisement calls is significantly reduced when the speaker was directed either upward or downward, rather than horizontally. However, the degradation of call is lower when the speaker is direct horizontally. Since calls produced from either upward or downward orientations could travel farther, they could be used to signal male spatial location, while calls produced from a horizontal position could provide information on male quality at shorter distances at advanced phases of courtship.     

Matching and Symmetry in the Frequency Recognition Curve of the Poison Frog Epipedobates trivittatus

In territorial species, males use signals to advertise territory ownership to other males. In species with acoustic communication, masking interference by heterospecific signals may impede male–male communication and affect the reproductive success of males. Frogs are thought to minimize masking interference by using species‐specific frequency channels for communication. For this strategy to work, a frequency match is expected between the advertisement call and the auditory sensitivity. A previous field study on the Amazonian frog Epipedobates femoralis supported this prediction, but also revealed an asymmetric decrease in the probability of male reaction towards synthetic calls. That males of E. femoralis reacted less towards low‐frequency (compared with high‐frequency) calls was interpreted as a mechanism that reduces masking interference by E. trivittatus, a species calling within a lower, partially overlapping, frequency range. If this hypothesis holds, then males of E. trivittatus should exhibit the opposite asymmetry pattern, i.e. react less towards high‐frequency (compared with low‐frequency) calls. We tested this prediction by conducting 25 playback experiments on 22 males of E. trivittatus. Male phonotactic reaction towards synthetic calls of various frequency values was evaluated as a binary variable (the male either approached or not the loudspeaker), by measuring the latency until first jump, and by calculating the linear approaching speed. As in E. femoralis, the maximum probability of positive reaction was matched to the call frequency. Against our expectations, the response curve was symmetric. We discuss whether these results reflect a lack of selective pressures, or a compromise between natural selection and physiological constraints on the shape of the frequency recognition curves.