Evolutionary and neurobiological implications of selective phonotaxis in the spring peeper (Hyla crucifer)

Males of the spring peeper (Hyla crucifer) in central Missouri produce frequency-modulated, sinusoidal advertisement calls with a duration of 90–250 ms, and a mid-point frequency of 2800–3360 Hz. The frequency of the call is inversely correlated with body size. In playback experiments with synthetic stimuli, females did not prefer a frequency-modulated call to a call of constant frequency. Females preferred a call with a duration of 150 ms to sounds with durations of 40, 75 and 400 ms; a call of 300 ms was just as attractive as the 150-ms call. Females preferred a call of 2875 Hz to alternatives of 4000 Hz and 2600 Hz. The auditory system of H. crucifer is thus only roughly tuned to the temporal and spectral properties of the advertisement call. The female's specificity with respect to duration alone is adequate for species recognition, but intraspecific mate choice based on call frequency is extremely unlikely.     

Mating preference functions of individual female barking treefrogs, Hyla gratiosa, for two properties of male advertisement calls

Abstract.— A mating preference function describes the relationship between variation in a trait in potential mates and the strength of the preference for that trait. Few studies have measured mating preference functions either at a population level or for individuals. We used two-choice playback experiments to determine the mating preference functions of individual female barking treefrogs for two call characteristics: call-repetition rate and fundamental frequency. We tested each female four times with each pair of stimuli and with three to six pairs of stimuli. Individual females exhibited directional preferences for higher call rates and stabilizing preferences for intermediate fundamental frequency. These individual preference functions were similar to population-level preferences documented in previous studies. Within a stimulus type (call rate or fundamental frequency), nearly all females exhibited the same general preference function. However, females varied in the minimum difference between stimuli necessary to elicit a unanimous choice for the higher call rate, and they differed in both the intermediate fundamental frequency they preferred most and the minimum difference in fundamental frequency that elicited a unanimous choice for one of the two alternatives. The variation we observed among females was not repeatable; repeatabilities were in general low and statistically nonsignificant. The observed variation in the preferences of females, even if unrepeatable, should weaken selection on male traits relative to selection in the absence of such variation.     

Male Calling Behavior and Female Choice in the Neotropical Treefrog Hyla microcephala

The effect of stimulus call complexity and calling rate on the vocal responses of males and female mate choice was studied in Hyla microcephala in Panama. Males increased the number of notes in their calls in response to increases in stimulus call complexity during both playback of 1 to 8-note advertisement calls and during natural interactions. However, precise matching of the number of notes in stimuli and responses did not occur consistently. Males also increased calling rates if stimuli were presented above prestimulus rates. Two-stimulus choice experiments demonstrated that females prefer both higher calling rates and greater call complexity, indicating that the ways males change their vocal behavior during interactions increases their attractiveness to potential mates. Tests in which the relative intensity of a high and low rate stimulus was varied indicated that females prefer stimuli with higher total sound energy. In a natural chorus, it is likely that females simply approach males giving the most conspicuous calls.     

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.     

Decisions during Phonotaxis in the Bushcricket Requena verticalis (Orthoptera: Tettigoniidae): Do Females Change Direction to Alternative Male Calls?

Female bushcrickets (Requena verticalis, Listroscelidinae, Tettigoniidae) show a preference between male calls that differ in three parameters, temporal structure, frequency and intensity. In a two-choice speaker situation they prefer louder calls, songs in which the upper part of the frequency spectrum occupies higher frequencies and calls with short chirps rather than those with longer chirps. In an experiment females were offered an alternative call while orienting to a model of their conspecific song. The alternative call was demonstrably preferred by females when presented in a paired-speaker trial. Two motivational states were identified where females moved slowly or quickly to a sound source. Movement patterns were associated with the form of stimulus and slow females were discriminatory of male calls while fast females were not. Slow females changed speaker preference when the alternate speaker broadcast a call model with the higher frequency peak or the song model with the shorter chirps. By comparison fast moving females only changed course when the alternative sound source was louder.     

The vocal sac as a visual cue in anuran communication: an experimental analysis using video playback

Acoustic signals produced by most anurans are accompanied by inflation of a conspicuous vocal sac. We presented female túngara frogs, Physalaemus pustulosus, with acoustic playback of the male advertisement call, synchronized with a video playback of vocal sac inflation. Females significantly preferred a stimulus combination including vocal sac inflation over an identical set of stimuli with the vocal sac inflation removed. Neither a moving rectangle bearing the gross contrast and spatiotemporal properties of the vocal sac inflation sequence, nor the image of a noncalling male significantly enhanced the attractiveness of the acoustic stimulus. Both the form and spatiotemporal properties of the vocal sac thus appear to be salient to females. The results indicate that the vocal sac can serve as a visual cue, which may account for the conspicuous pigmentation found on the vocal sacs of males in many species. Gular inflation in synchrony with a call may function to facilitate female localization of individual males in an aggregation.     

Neural mechanisms underlying acoustic behaviour of the frog Pseudophryne semimarmorata (Anura: Leptodactylidae)

Pseudophryne semimarmorata lacks a columella and tympanic membrane. However, at least males are relatively sensitive to sound. The mating call in this species can be inhibited by certain acoustic stimuli. The range of stimuli that inhibited calling was compared with that which evoked neural activity in midbrain auditory units. One of three types of unit which can be distinguished on the basis of best frequency, the high frequency unit, is presumed to be derived from the basilar papilla. High frequency units responded to the same range of sounds that inhibited calling. It is suggested that production of the mating call is initiated by a neural pacemaker, and sufficient neural input to this centre from the basilar papilla inhibits the pacemaker.     

Modality interactions alter the shape of acoustic mate preference functions in gray treefrogs

Sexual selection takes place in complex environments where females evaluating male mating signals are confronted with stimuli from multiple sources and modalities. The pattern of expression of female preferences may be influenced by interactions between modalities, changing the shape of female preference functions, and thus ultimately altering the selective landscape acting on male signal evolution. We tested the hypothesis that the responses of female gray treefrogs, Hyla versicolor, to acoustic male advertisement calls are affected by interactions with visual stimuli. We measured preference functions for several call traits under two experimental conditions: unimodal (only acoustic signals presented), and multimodal (acoustic signals presented along with a video‐animated calling male). We found that females were more responsive to multimodal stimulus presentations and, compared to unimodal playbacks, had weaker preferences for temporal call characteristics. We compared the preference functions obtained in these two treatments to the distribution of male call characteristics to make inferences on the strength and direction of selection expected to act on male calls. Modality interactions have the potential to influence the course of signal evolution and thus are an important consideration in sexual selection studies.     

Female call preferences in tree-hole frogs: why are there so many unattractive males?

In tree-hole frogs, Metaphrynella sundana, the fundamental call frequency varies widely between males. In field playback experiments, females strongly preferred calls from the lower range of frequencies found in the population. There was no correlation, however, between male size and call frequency, as is normally the case for anurans, so large males were not necessarily more attractive to females. Presence or absence of upper harmonics in the call had no effect on female choice. Tree holes with shallow air columns were more often used by calling frogs, and were presumably more common, than deep holes. Since male M. sundana actively exploit the resonant properties of tree holes for mate attraction, and high frequencies match comparatively shallow holes, the benefits of attaining acoustic matching probably select for high-frequency calls. In addition, males with high-frequency calls may be heard from a greater distance in the vicinity of torrent streams. Since the level of such noise in the forest varies in time and space, different frequencies may prove optimal in different contexts, thereby preserving the observed variation within the population. Having an ‘unattractive’ high-frequency call should be potentially beneficial only when calling males do not congregate, a condition that our data suggest is fulfilled in this system.     

Acoustically induced call modification in the white-lipped frog,Leptodactylus albilabris

The vocalization behaviour of Leptodactylus albilabris was investigated using field playback experiments. To assess the response of males to pre-recorded natural ‘chirp’ (advertisement call) and natural ‘chuckle” (aggressive call) stimuli of gradually increasing broadcast intensity, three parameters (intensity, dominant frequency and repetition rate) of the chirp call were analysed. Of the males tested, 69% showed a significant increase in chirp intensity with increased levels of both stimulus types. In response to playback of the chirp stimulus, males actively modified the dominant frequency of their chirp calls over a mean range of 91·42 Hz, and in one case as much as 400 Hz. Moreover, 12 of 17 males shifted the frequency of their call towards the dominant frequency of the chirp stimulus (2175 Hz) by either increasing or decreasing the dominant frequency of their chirp calls. In response to the natural chuckle stimulus, 83% of the males showed either a decrease or no significant change in the dominant frequency of their chirps. All eight males for which both the chirp frequency and intensity were analysed and that showed an increase in chirp intensity also showed a concomitant increase in chirp dominant frequency. These results are the first to document quantitatively the plasticity of advertisement call intensity and dominant frequency in an anuran. The possible effects of advertisement call modification on male mating success in L. albilabris is discussed.     

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.     

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.     

Dynamic properties of the advertisement calls of gray tree frogs: patterns of variability and female choice

We assessed the potential for several acoustic properties ofthe advertisement calls of male gray tree frogs to affect relativemating success by relating patterns of variation in these propertiesto minimum differences required to elicit female choice. Dynamicproperties (pulse number, PN; call rate, CR; and duty cycle,DC, the ratio of call duration to call period) varied much morewithin bouts of calling than a static property (dominant frequency,DF) but nevertheless exhibited significant between male variationin three of four breeding seasons. Many multiply recorded malesconsistently produced calls with values substantially aboveor below mean values of males recorded on the same nights. Nightlyranges of variation in PN and CR were often greater than theminimum differences required to elicit female preferences inthe laboratory. In most experiments, females chose high-PN orfast-CR calls over low-PN or slow-CR alternatives, respectively,even if the preferred stimuli were farther away or 6-10 dB lowerin sound pressure level (SPL), provided that differences inPN or CR were 100%. Consistent with these results, females didnot always choose the closer of two calling males in the field.Nightly ranges of variation in DF rarely equaled the minimumdifference required to elicit SPL independent preferences. Femalespreferred a stimulus of high-PN and slow-CR over an alternativeof low-PN or fast-CR with the same acoustic on-time; in twoexperiments, females chose calls of high-PN over low-PN alternativeseven though the playback of the high-PN call was interruptedand the low-PN call was broadcast continuously. Thus, femalepreferences were not merely based on the total time of acousticstimulation. Responses of females tested twice in the same experimentsuggest that phenotypic variation in preference was limitedin our study populations.     

Divergence of Acoustic Signals in a Widely Distributed Frog: Relevance of Inter-Male Interactions

Divergence of acoustic signals in a geographic scale results from diverse evolutionary forces acting in parallel and affecting directly inter-male vocal interactions among disjunct populations. Pleurodema thaul is a frog having an extensive latitudinal distribution in Chile along which males'' advertisement calls exhibit an important variation. Using the playback paradigm we studied the evoked vocal responses of males of three populations of P. thaul in Chile, from northern, central and southern distribution. In each population, males were stimulated with standard synthetic calls having the acoustic structure of local and foreign populations. Males of both northern and central populations displayed strong vocal responses when were confronted with the synthetic call of their own populations, giving weaker responses to the call of the southern population. The southern population gave stronger responses to calls of the northern population than to the local call. Furthermore, males in all populations were stimulated with synthetic calls for which the dominant frequency, pulse rate and modulation depth were varied parametrically. Individuals from the northern and central populations gave lower responses to a synthetic call devoid of amplitude modulation relative to stimuli containing modulation depths between 30–100%, whereas the southern population responded similarly to all stimuli in this series. Geographic variation in the evoked vocal responses of males of P. thaul underlines the importance of inter-male interactions in driving the divergence of the acoustic traits and contributes evidence for a role of intra-sexual selection in the evolution of the sound communication system of this anuran.     

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.     

Variation in female guppy preference for male olfactory and visual traits

Animals often use different sensory systems to assess different sexually selected signals from potential mates. However, the relative importance of different signals on mate choice is not well understood in many animal species. In this study, we examined the relative importance of male olfactory and visual cues on female preference in the guppy Poecilia reticulata. We used digitally modified male images to standardize visual stimuli. We found that, regardless of whether females were presented without male visual stimuli or with identical male visual stimuli, they preferred stimuli with the odor of males to those without. However, when females were allowed to choose between dull male visual stimuli with male odor, and brightly colored male visual stimuli without male odor, there was no clear preference for either. Some females preferred the dull male visual stimuli with male odor, whereas some other females preferred the brightly colored male visual stimuli without male odor. These results indicate that the relative importance of olfactory and visual cues in female mate preference varied between individuals.     

Harmonic calls and indifferent females: no preference for human consonance in an anuran

The human music faculty might have evolved from rudimentary components that occur in non-human animals. The evolutionary history of these rudimentary perceptual features is not well understood and rarely extends beyond a consideration of vertebrates that possess a cochlea. One such antecedent is a preferential response to what humans perceive as consonant harmonic sounds, which are common in many animal vocal repertoires. We tested the phonotactic response of female túngara frogs (Physalaemus pustulosus) to variations in the frequency ratios of their harmonically structured mating call to determine whether frequency ratio influences attraction to acoustic stimuli in this vertebrate that lacks a cochlea. We found that the ratio of frequencies present in acoustic stimuli did not influence female response. Instead, the amount of inner ear stimulation predicted female preference behaviour. We conclude that the harmonic relationships that characterize the vocalizations of these frogs did not evolve in response to a preference for frequency intervals with low-integer ratios. Instead, the presence of harmonics in their mating call, and perhaps in the vocalizations of many other animals, is more likely due to the biomechanics of sound production rather than any preference for ‘more musical’ sounds.     

Analysis of acoustically evoked call suppression behaviour in a neotropical treefrog

We broadcast synthetic call notes to male Eleutherodactylus coqui treefrogs in their natural habitat. The frogs avoided acoustic overlap with relatively long duration tone stimuli by calling only within the short silent interval between tones. We also observed a temporal change in call pattern in response to tone stimuli of various frequencies and intensities. This response is the basis for construction of a behavioural auditory threshold function for this species. This function does not show a sensitivity maximum at frequencies corresponding to those in the advertisement call, and demonstrates that the frogs are capable of behaviourally responding to sounds over a frequency range which is greater than that required for detection of the species-specific vocalizations and sufficient for detection of at least one sympatric anuran species.     

Discrimination of sinusoidally frequency-modulated sound signals mimicking species-specific communication calls in the FM-bat Phyllostomus discolor

In the lesser spear-nosed bat, Phyllostomus discolor, maternal directive calls are characterized by an individual type of sinusoidal frequency modulation (= SFM) pattern. Beside modulation frequency, modulation depth, carrier frequency, and number of modulation cycles per call contribute to the mother's vocal signature. Since juvenile P. discolor learn to adapt their isolation calls to the corresponding call characteristics of the own mother or even to playback of a computer-stored directive call, if hand-reared in the absence of conspecifics, the bats' auditory system ought to be able to resolve interindividual differences in communication call structure. However, quantitative psychoacoustic data on the discrimination of SFM signals in this species are not available. Thus, in the present study, lesser spear-nosed bats were trained in a two-alternative forced-choice procedure to discriminate between two alternatingly presented SFM sound signals differing in modulation frequency. Other characteristics of acoustic stimuli were identical and designed to mimick the fundamental of species-specific calls. By gradually reducing the difference in modulation frequency between both stimuli within the behavioural relevant range until the animals' performance dropped below the 75%-correct level, a considerable auditory spectro-temporal resolution has been revealed. Particularly in comparison to the overall interindividual variation of this call parameter (minimal modulation frequency = 49 Hz, maximum = 100 Hz), the determined average difference limen for modulation frequency of 2.42 ± 0.29 Hz seems substantial and sufficient for labelling individuals. Accepted: 30 November 1996     

Commensal auditory communication in two species of Neoconocephalus (Orthoptera)

Auditory communication in Neoconcephalus ensiger and Neoconocephalus robustus, two stridulating tettigoniids that inhabit the same geographical area, was examined to determine how these two species interact. Computer and electrophysiological techniques were used to analyze sound production and reception. Although similar in appearance, the males of these species produce easily distinguishable acoustic communication signals (call songs) that serve to attract conspecific females. Both wave form and spectral analyses were done on selected segments of the species-specific call songs by using discrete Fourier transform techniques. Sound production and reception capacities were measured by octave-band analyzers and extracellular electrode techniques. The results show that each of these species has a distinct, primary carrier frequency band. Secondly, the log magnitude spectra revealed a significant secondary component in the call song of N. robustus which corresponds to the primary energy band in the call song of N. ensiger. This overlap in acoustic signals and other findings suggest that males of N. ensiger might use the louder stridulation of the more metabolically active N. robustus to attract conspecific females over great distances. N. ensiger males have a sound production capacity like N. robustus, but conserve energy for soft, near-field signaling. The audiogram representing sensitivity of the tympano-receptor in the foreleg showed sound reception to be matched precisely with sound production curves.