The Sounds of Silence as an Alarm Cue in Túngara Frogs,Physalaemus pustulosus

In many species males vocally advertise for mates in choruses and these choruses serve as acoustic beacons to conspecific females as well as to eavesdropping predators and parasites. Chorusing will often cease in response to disturbances, such as the presence of predators. In some cases the cessation is so rapid and over such a large area that it seems improbable that males are all responding directly to the same local disturbance. Here, we demonstrate experimentally in Neotropical túngara frogs, Physalaemus pustulosus, that the cessation of calling by males spreads rapidly through the chorus. The cessation of chorusing in response to the cessation of playbacks of three calling males is more effective in inducing chorus cessation than is the cessation of one male calling. When three males are calling, the cessation of complex calls is more effective in inducing chorus cessation than simple calls. There is no main effect on whether the final call of the male is complete or is interrupted. We thus conclude that the sudden lack of signals—the ‘sounds of silence’—becomes an alarm cue that can explain the rapid cessation of choruses that are common in many chorusing species.     

Precedence effects and the evolution of chorusing

The structured choruses produced by rhythmically signalling males in many species of acoustic animals have long-captured the imagination of evolutionary biologists. Though various hypotheses have been forwarded to explain the adaptive significance of such chorusing, none have withstood empirical scrutiny. We suggest instead that alternating and synchronous choruses represent collective epiphenomena resulting from individual males competing to jam each other''s signals. These competitions originate in psychoacoustic precedence effects wherein females only orient toward the first call of a sequence, thus selectively favouring males who produce leading calls. Given this perceptual bias, our modelling confirms that a resetting of signal rhythm by neighbours'' signals, which generates either alternation or synchrony, is evolutionarily stable provided that resetting includes a relativity adjustment for the velocity of signal transmission and selective attention toward only a subset of signalling neighbours. Signalling strategies in chorusing insects and anurans are consistent with these predicted features.     

Variation and Repeatability of Female Choice in a Chorusing Katydid, Ephippiger ephippiger: an Experimental Exploration of the Precedence Effect

Female choice in various species of acoustic insects and anurans entails a psychoacoustic preference for male calls that lead their neighbors by a brief time interval. This discrimination, which can be termed a precedence effect, may select for various mechanisms with which males adjust call rhythm and thus reduce their incidence of ineffective following calls. At a collective level, alternating and synchronous choruses may emerge from these call timing mechanisms. Using playback experiments, we characterized the precedence effect in females of the katydid Ephippiger ephippiger, an alternating choruser in which males use a rhythm adjustment mechanism that prevents calling during brief intervals following their neighbors’ calls. E. ephippiger females oriented toward leading male calls in >75% of trials when relatively young (<40 d old) and when playbacks were timed so that following calls began within 100–250 ms of the leading ones. However, this preference declined to below 60% as females aged and the interval separating leading and following call onsets increased. The strength of this precedence effect varied greatly between females, but within broad age classes the effect in a given female was statistically repeatable. Such repeatability indicates the possibility that additive genetic variance could be a significant component of variation in the precedence effect. We discuss the implications of our findings and inference on genetic variance for evolution of the precedence effect and for chorusing.     

Female Iberian midwife toads (Alytes cisternasii) use call order to reach particular males in dense choruses

Call-timing mechanisms among anuran males calling within choruses are frequent, and previous studies have indicated that midwife toad females respond preferentially to these mechanisms. The results of multi-speaker tests performed here with midwife toads suggest that the temporal order of male calls within a dense chorus can determine the ability of females to locate the most attractive calls (in this instance the low-frequency calls emitted by larger males). When call emission was regular in the multi-speaker tests, most females chose the most attractive option (i.e., the speaker emitting the lower-frequency call). When call emission was not regular, however, most females failed to reach the most attractive option, selecting the speaker that emitted immediately after that emitting the most attractive call. These results support the idea that there may be benefits for smaller males that emit their less attractive calls close to those of larger, more attractive males in dense choruses. Less attractive males could exploit the attractiveness of nearby larger males calls by alternating their calls in an unordered sequence to reach receptive females.     

Spatially-mediated call pattern recognition and the cocktail party problem in treefrog choruses: can call frequency differences help during signal overlap?

Male gray treefrogs, Hyla versicolor, advertise for mates in dense assemblages characterized by high levels of noise and acoustic clutter. In pairwise interactions, males alternate pulsatile advertisement calls and so reduce call overlap to levels below that expected by chance. However, in choruses consisting of more than two males, acoustic interference increases dramatically. Moreover, males do not seem to exhibit selective attention in a way that reduces call interference among nearest neighbours. Previous research has also demonstrated that although females discriminate strongly against overlapped calls, negative effects of call overlap can be attenuated by a large angular separation between signal sources. However, call stimuli employed were identical in spectrum and so this situation differs from that likely in nature. Based on studies of ‘auditory stream segregation’ with other taxa, we hypothesized that realistic differences in the frequencies of overlapping calls could improve the ability of females to discern critical call features during overlap of separated call sources. We found that, although, under some circumstances, differences in call frequency may help females distinguish among neighbouring males giving temporally proximate calls, naturalistic spectral differences do not seem to help females perceptually separate the overlapping calls of neighbouring conspecific males.     

A function of synchronous chorusing and a novel female preference shift in an anuran

Many chorusing insects and anurans acoustically compete for females under conditions of high background noise produced by conspecifics and have developed a variety of strategies for improving their conspicuousness in a chorus. In this study, I present a novel female preference shift that can explain the synchronous chorusing of males. In the running frog Kassina fusca the median degree of overlap found in pairwise interactions between males (20.8%) and in response to playbacks of conspecific calls (21.4%) corresponded remarkably well with the preference function of females. Although preferring follower male calls when the degree of call overlap was low (10 and 25%), females shifted their preference towards leader male calls when the degree of call overlap was high (75 and 90%). Males were physiologically capable of calling with short latencies and, thus, high degrees of overlap. This suggests that follower males can control the degree of overlap with neighbours and do so to their advantage. These results stand in contrast to recent findings in insects and anurans in which chorusing structure has been described as an epiphenomenon.     

Inter-male Spacing and Aggression in African Painted Reed Frogs,Hyperolius marmoratus

Inter-male spacing and the role of aggression in the maintenance of spatial organization was examined in choruses of Hyperolius marmoratus males housed in a semi-natural enclosure. The effects of chorus size on spacing patterns, nearest neighbour distances and male aggressive behaviour were examined. Males were found to reduce nearest neighbour distances as chorus size increased. This was accompanied by a shift in spacing pattern from even in small choruses (5–9 males) to random in choruses of 10 to 13 males. In choruses of 14, spacing patterns were once again even. The reason for these shifts is unclear but may reflect a sudden, rather than gradual increased tolerance by individuals to high neighbour call intensity as space to call from becomes more limited. The level of male aggression was influenced by chorus size and the time of night. In general, more aggressive interactions occurred in high density choruses. However, this did not translate into higher levels of individual male aggression as density increased. Individual male aggression was high in early evening choruses and declined to a minimum at peak chorusing time. High levels of aggression during early evening may reflect the establishment of calling sites by males, while the drop in aggression at peak chorusing time may occur in response to the presence of females in the chorus at this time or as a consequence of masking of neighbours calls.     

Mate sampling by female barking treefrogs (Hyla gratiosa)

Despite intense interest in mate choice, relatively little isknown about how individuals sample prospective mates. Indeed,a key issue is whether females sample males or simply matewith the first male encountered. We investigated mate samplingby female barking treefrogs (Hyla gratiosa). Females choosingmates in natural choruses did not move between males but insteadmated with the first male they approached closely. Most femalesmated with the male closest to them at the start of their mate-choiceprocess, and females were more likely to mate with the closest male when the distance to other males was large. These observationsare consistent with the hypothesis that females do not samplepotential mates but instead mate with the first male they distinguishfrom the rest of the chorus. To test this initial detectionhypothesis, we conducted a playback experiment in which weoffered females a choice between two calls, one of which was detectable above the background chorus sound at the female'srelease point, and one of which became detectable only as femalesmoved toward the initially detectable call. Females did notprefer the initially detectable call, thus ruling out the initialdetection hypothesis and implicating sampling of potentialmates by females. Based on the behavior of females in natural choruses, we hypothesize that females approach the chorus, moveto locations where they are able to detect the calls of severalmales simultaneously, and choose a mate from among these malesat some distance from the males. Such simultaneous samplingmay be common in lekking and chorusing species, which havebeen the subjects of many studies of sexual selection.     

Arginine Vasotocin Injection Increases Probability of Calling in Cricket Frogs, but Causes Call Changes Characteristic of Less Aggressive Males

Male cricket frogs,Acris crepitanscommunicate to males and females using advertisement calls, which are arranged into call groups. Calls at the middle and end, but not beginning of the call group, are modified in response to male–male aggressive interactions. We found in this field study of male cricket frogs in natural breeding choruses that the peptide hormone arginine vasotocin (AVT) not only increased the probability that males called after injections, but also caused modifications in middle and end calls to produce calls characteristic of less aggressive males. Moreover, AVT-injected males showed significantly greater increases in call dominant frequency than saline-injected males, again, a characteristic of less aggressive males. Cricket frog calls are used to both repel males and attract females, thus call changes may relate to male–male and/or male–female interactions. Saline-injected males also demonstrated significant changes in several call traits, including changes that occurred in the beginning and middle calls of the call groups, but not the end calls. AVT appeared to block some call changes produced through handling. These data suggest that AVT can influence acoustic communication in frogs in several ways, including effects on call characteristics and dominant frequency, as well as potentially blocking some handling effects.     

XII SYMPOSIUM OF THE INTERNATIONAL BIOACOUSTICS COUNCIL

ABSTRACT

Phonemic restoration, a form of temporal induction, occurs when the human brain compensates for masked or missing portions of speech by filling in obscured or nonexistent sounds. We tested for temporal induction and related abilities in females of the Gray Treefrog Hyla versicolor. The number of pulses in calls is used by females for assessment of males. Accordingly, an ability to “restore” or interpolate between masked or otherwise sonically degraded portions of calls could help females during mate choice in noisy choruses. In phonotaxis experiments, we employed unmodified calls and those that had a centrally placed gap, a region overlapped by a portion of another call or filtered noise, or replaced with filtered noise. When offered call alternatives with equivalent numbers of clear pulses, we found that females discriminated against calls with gaps two or more times greater than the natural 25 ms interpulse interval. When a gap was replaced with a zone of call overlap or noise (so, again the call durations of the alternatives were unequal), females discriminated either in favour (overlap) of the modified stimuli or failed to discriminate (noise). However, when the unmodified and modified stimuli were the same duration, females discriminated against the latter. Normal calls were also chosen when paired against calls with multiple noise sections. Pulses formed from noise bursts were attractive, but less so than normal pulses. In single speaker tests, standardized rates of movement did not differ between calls containing noise segments of different duration. Our results therefore do not indicate that females of the Gray Treefrog employ a form of temporal induction that is fully restorative. However, the data indicate that acoustically anomalous sections of calls can retain attractive potential provided acoustic energy and pulses are present.     

Background noise from a natural chorus alters female discrimination of male calls in a Neotropical frog

Many animals communicate in environments with high levels of background noise. Although it is a fundamental prediction of signal detection theory that noise should reduce both detection and discrimination of signals, little is known about these effects in animal communication. Female treefrogs, Hyla ebraccata, in Costa Rica choose mates in large noisy multispecies choruses. We tested gravid females for preferences between computer-synthesized calls with carrier frequencies of 3240 and 2960 Hz (values near the mode and the fifth percentile of the population, respectively) in four levels of background noise from a natural chorus. In the absence of noise (signal/noise ratio >25 dB), females preferred the lower frequency. With moderate signal/noise ratios (6 and 9 dB), they did not discriminate between these frequencies. With low signal/noise ratios (3 dB), females preferred the frequency near the mode for the population. Similar experiments had previously demonstrated that females can detect the presence of a male's calls with signal/noise ratios of 3 dB or greater. Thus moderate levels of natural background sound reduced a female's ability to discriminate between males' calls even when she could detect them. In high levels of background sound, females abandoned discrimination for low-frequency calls and reverted to the task of detecting signals with modal properties for the population. These results justify recent theoretical analyses of the importance of receivers' errors in the evolution of communication.     

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.     

Sexual selection in female perceptual space: how female túngara frogs perceive and respond to complex population variation in acoustic mating signals

Female preferences for male mating signals are often evaluated on single parameters in isolation or small suites of characters. Most signals, however, are composites of many individual parameters. In this study we quantified multivariate traits in the advertisement call of the túngara frog, Physalaemus pustulosus. We represented the calls in multidimensional scaling space and chose nine test calls to represent the range of population variation. We then tested females for phonotactic preference between calls in each pair of the nine test calls. We used statistics developed for paired comparisons in such "round robin" competitions to evaluate the null hypothesis of equal attractiveness, and to examine the degree to which females responded to calls as being different from or similar to one another in attractiveness. We then examined the attractiveness of each test call relative to all other test calls as a function of their location in multivariate acoustic space (the acoustic landscape) to visualize sexual selection on calls. Finally, we used methods from cognitive psychology to illustrate the females' perception of call attractiveness in multivariate space, and compared this perceptual landscape to the acoustic landscape of quantitative call variation. We show that correlations between individual call characters are not strong and thus there are few biomechanical constraints on their independent evolution. Most call variables differed among males, and there was high repeatability of call characters within males. Females often discriminated between pairs of calls from the population, and there were significant differences among calls in their attractiveness. Female preferences for calls were not stabilizing. The region of the acoustic landscape that was most attractive to females included the mean call but was not centered around it. The females' perceptual or preference landscape did not correlate with the call's acoustic landscape, and female perception of calls decreased rather than enhanced call differences.     

Sexual Selection in Insect Choruses: Influences of Call Power and Relative Timing

Female preference for male song in acoustic insects is primarily influenced by call energy or power, but nonenergy features such as the relative timing of male calls may also be critical in preference. Preferences for leading calls, which may be a type of precedence effect, are an example of the latter factor. In various species, females preferentially orient toward the leading of two or more spatially separated calls presented in controlled playback experiments, however the importance of this effect on mate choice in actual choruses and natural populations is generally unknown. We studied the determinants of mate choice in reenacted choruses of the tettigoniid Ephippiger ephippiger, a species in which females prefer leading calls in two-choice experiments, and neighboring males adjust their relative call timing in a way that reduces the incidence of following calls. We found that mate choice, as indicated by the pattern of female settlement, largely reflects call rate and call constancy. But, we also found suggestions that female choice is influenced by the acoustic neighborhood in which a male sings, males in neighborhoods with more overall singing being preferred, and by a males incidence of leading calls relative to his neighbors. Although statistically inconclusive owing to few relevant samples, we note that the level of preference for leading calls observed in E. ephippiger choruses is comparable to that found in controlled playback experiments.     

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.     

Call recognition and female choice in a treefrog with a multicomponent call

Acoustic mating signals are typically species‐specific, and often additionally are subject to directional female preferences. Male executioner treefrogs, Dendropsophus carnifex, produce a multicomponent advertisement call composed of an introductory screech note followed by two or more click notes. Here, we tested (i) call recognition by comparing female directed phonotaxis towards individual and combined call components: screech vs. clicks vs. screech + clicks, (ii) female preferences for greater numbers of click notes and (iii) female preferences for faster call rates. The results demonstrated that screeches and clicks, presented either separately or together as a complete call, evoke similar female responses, suggesting that either note was sufficient to elicit a mate‐recognition response. Additionally, females preferred calls with greater numbers of click notes and with faster call rates. We interpret these results within the context of female mate selection in natural choruses.     

Multimodal communication in a noisy environment: a case study of the Bornean rock frog Staurois parvus

High background noise is an impediment to signal detection and perception. We report the use of multiple solutions to improve signal perception in the acoustic and visual modality by the Bornean rock frog, Staurois parvus. We discovered that vocal communication was not impaired by continuous abiotic background noise characterised by fast-flowing water. Males modified amplitude, pitch, repetition rate and duration of notes within their advertisement call. The difference in sound pressure between advertisement calls and background noise at the call dominant frequency of 5578 Hz was 8 dB, a difference sufficient for receiver detection. In addition, males used several visual signals to communicate with conspecifics with foot flagging and foot flashing being the most common and conspicuous visual displays, followed by arm waving, upright posture, crouching, and an open-mouth display. We used acoustic playback experiments to test the efficacy-based alerting signal hypothesis of multimodal communication. In support of the alerting hypothesis, we found that acoustic signals and foot flagging are functionally linked with advertisement calling preceding foot flagging. We conclude that S. parvus has solved the problem of continuous broadband low-frequency noise by both modifying its advertisement call in multiple ways and by using numerous visual signals. This is the first example of a frog using multiple acoustic and visual solutions to communicate in an environment characterised by continuous noise.     

Mechanisms and evolution of inter-male spacing in the painted reedfrog (Hyperolius marmoratus)

Inter-male spacing in Hyperolius marmoratus choruses was studied at a natural breeding site. Calling males maintain minimum inter-individual distances of 50 cm. Agonistic behaviour and encounter calling appear to help maintain spacing. Males wrestle with one another by grappsling with their forelimbs and attempt to displace each other with powerful kicks from the hindlimbs. Acoustic playback experiments demonstrated that inter-male spacing was vocally mediated and that signal intensity provides cues regarding the proximity of near neighbours. When given a choice of three identical calls, differing only in their spatial separation, females displayed selective phonotaxis to the most widely spaced call. Such discrimination by females must generate strong selective pressure for males to maintain adquate spacing if they are to attract mates successfully.     

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.     

Female Mate Choice Can Drive the Evolution of High Frequency Echolocation in Bats: A Case Study with Rhinolophus mehelyi

Animals employ an array of signals (i.e. visual, acoustic, olfactory) for communication. Natural selection favours signals, receptors, and signalling behaviour that optimise the received signal relative to background noise. When the signal is used for more than one function, antagonisms amongst the different signalling functions may constrain the optimisation of the signal for any one function. Sexual selection through mate choice can strongly modify the effects of natural selection on signalling systems ultimately causing maladaptive signals to evolve. Echolocating bats represent a fascinating group in which to study the evolution of signalling systems as unlike bird songs or frog calls, echolocation has a dual role in foraging and communication. The function of bat echolocation is to generate echoes that the calling bat uses for orientation and food detection with call characteristics being directly related to the exploitation of particular ecological niches. Therefore, it is commonly assumed that echolocation has been shaped by ecology via natural selection. Here we demonstrate for the first time using a novel combined behavioural, ecological and genetic approach that in a bat species, Rhinolophus mehelyi: (1) echolocation peak frequency is an honest signal of body size; (2) females preferentially select males with high frequency calls during the mating season; (3) high frequency males sire more off-spring, providing evidence that echolocation calls may play a role in female mate choice. Our data refute the sole role of ecology in the evolution of echolocation and highlight the antagonistic interplay between natural and sexual selection in shaping acoustic signals.