Conspecific Advertisement Calls Research Articles

Consistency in responses to conspecific advertisement calls with various signal-to-noise ratios in both sexes of the Anhui tree frog.

Environmental noise has a significant negative impact on acoustic communication in most situations, as it influences the production, transmission, and reception of acoustic signals. However, how animals respond to conspecific sounds when there is interference from environmental noise, and whether males and females display convergent behavioral responses in the face of noise masking remain poorly understood. In this study, we investigated the effects of conspecific male advertisement calls with different signal-to-noise ratios on male-male competition and female choice in the Anhui tree frog Rhacophorus zhoukaiyae using playback and phonotaxis experiments, respectively. The results showed that (1) female Anhui tree frogs preferentially selected the conspecific calls with higher SNR compared to calls with lower SNR; (2) males preferentially responded vocally to the conspecific calls with higher SNR compared to calls with lower SNR; and (3) males' competitive strategies were flexible in the face of noise interference. These results suggest that preferences of both sexes converge in outcome, and that male competitive strategies may depend on predictable female preferences. This study will provide an important basis for further research on decision-making in animals.

Neural basis of acoustic species recognition in a cryptic species complex.

Sexual traits that promote species recognition are important drivers of reproductive isolation, especially among closely related species. Identifying neural processes that shape species differences in recognition is crucial for understanding the causal mechanisms of reproductive isolation. Temporal patterns are salient features of sexual signals that are widely used in species recognition by several taxa, including anurans. Recent advances in our understanding of temporal processing by the anuran auditory system provide an opportunity to investigate the neural basis of species-specific recognition. The anuran inferior colliculus consists of neurons that are selective for temporal features of calls. Of potential relevance are auditory neurons known as interval-counting neurons (ICNs) that are often selective for the pulse rate of conspecific advertisement calls. Here, we tested the hypothesis that ICNs mediate acoustic species recognition by exploiting the known differences in temporal selectivity in two cryptic species of gray treefrog (Hyla chrysoscelis and Hyla versicolor). We examined the extent to which the threshold number of pulses required to elicit behavioral responses from females and neural responses from ICNs was similar within each species but potentially different between the two species. In support of our hypothesis, we found that a species difference in behavioral pulse number thresholds closely matched the species difference in neural pulse number thresholds. However, this relationship held only for ICNs that exhibited band-pass tuning for conspecific pulse rates. Together, these findings suggest that differences in temporal processing of a subset of ICNs provide a mechanistic explanation for reproductive isolation between two cryptic treefrog species.

Diverse patterns of responsiveness to fine temporal features of acoustic signals in a temperate austral forest frog, Batrachyla leptopus (Batrachylidae)

ABSTRACT Phonotactic female and vocal male responses of frogs to advertisement calls have been shown to encompass broader ranges than those of variation of natural mate-attracting signals. Anuran aggressive calls contribute to expand the range of sound features significant for communication. Evoked vocal responses (EVRs) of males of Batrachyla leptopus to synthetic advertisement calls and variants with different temporal features altered parametrically were studied to assess their correspondence with features of natural signals. Frogs responded to stimuli differing in note rate with vocal patterns that depended on the design of the synthetic sounds: lower call rates were obtained with stimuli composed of notes with linear rise-fall times deviating from the average of this parameter for natural calls. However, opposite results were obtained with stimuli composed of sinusoidally amplitude-modulated notes. Calls of longer duration resembling aggressive calls were emitted in response to low note rate sinusoidal stimuli. Stimuli with note durations above and below the natural average, stimuli having low pulse rates and a continuous tone also elicited longer calls of aggressive type. These patterns relate the vocal responses recorded to recognition of conspecific and heterospecific advertisement and aggressive calls, as well as to novel signal features.

Timing of the advertisement call of the common tink frog (Diasporus diastema) shifts with the acoustic behaviour of local conspecifics

ABSTRACTWe investigated the temporal dynamics of acoustically interacting common tink frogs (Diasporus diastema), a species in which advertising males maintain large inter-individual distances that may influence call timing behaviours among nearest neighbours. This species produces advertisement calls in temporally structured bouts, with decreasing inter-note intervals that culminate in a ‘burst’ sequence of rapidly emitted notes. We broadcast playbacks of unaltered and temporally manipulated conspecific advertisement calls to focal male individuals vocalizing within triads (comprised of closely neighbouring focal and non-focal males and a more distant, outsider male). Focal males demonstrated rhythmic entrainment and adjusted their calling behaviour to overlap their call sequences with those of their nearest vocalizing neighbour, including the unaltered conspecific playback. When presented with a playback of conspecific calls lacking the natural temporal sequence, focal males reduced the duration of the silent interval between call bouts and reduced the number of notes in the burst phase of their call bout, indicating the significance of the multi-element temporally complex call bout structure in mediating male–male vocal interactions.

Brain Activation Patterns in Response to Conspecific and Heterospecific Social Acoustic Signals in Female Plainfin Midshipman Fish, Porichthys notatus

While the peripheral auditory system of fish has been well studied, less is known about how the fish’s brain and central auditory system process complex social acoustic signals. The plainfin midshipman fish, Porichthys notatus, has become a good species for investigating the neural basis of acoustic communication because the production and reception of acoustic signals is paramount for this species’ reproductive success. Nesting males produce long-duration advertisement calls that females detect and localize among the noise in the intertidal zone to successfully find mates and spawn. How female midshipman are able to discriminate male advertisement calls from environmental noise and other acoustic stimuli is unknown. Using the immediate early gene product cFos as a marker for neural activity, we quantified neural activation of the ascending auditory pathway in female midshipman exposed to conspecific advertisement calls, heterospecific white seabass calls, or ambient environment noise. We hypothesized that auditory hindbrain nuclei would be activated by general acoustic stimuli (ambient noise and other biotic acoustic stimuli) whereas auditory neurons in the midbrain and forebrain would be selectively activated by conspecific advertisement calls. We show that neural activation in two regions of the auditory hindbrain, i.e., the rostral intermediate division of the descending octaval nucleus and the ventral division of the secondary octaval nucleus, did not differ via cFos immunoreactive (cFos-ir) activity when exposed to different acoustic stimuli. In contrast, female midshipman exposed to conspecific advertisement calls showed greater cFos-ir in the nucleus centralis of the midbrain torus semicircularis compared to fish exposed only to ambient noise. No difference in cFos-ir was observed in the torus semicircularis of animals exposed to conspecific versus heterospecific calls. However, cFos-ir was greater in two forebrain structures that receive auditory input, i.e., the central posterior nucleus of the thalamus and the anterior tuberal hypothalamus, when exposed to conspecific calls versus either ambient noise or heterospecific calls. Our results suggest that higher-order neurons in the female midshipman midbrain torus semicircularis, thalamic central posterior nucleus, and hypothalamic anterior tuberal nucleus may be necessary for the discrimination of complex social acoustic signals. Furthermore, neurons in the central posterior and anterior tuberal nuclei are differentially activated by exposure to conspecific versus other acoustic stimuli.

Responses of male cricket frogs (Acris crepitans) to attenuated and degraded advertisement calls.

We examined the vocal and non-vocal responses of male cricket frogs (Acris crepitans) to conspecific advertisement calls that had been attenuated or degraded by reducing the depth of amplitude modulation (AM). Both are characteristic of changes to the call as it is transmitted through natural habitats. As stimulus calls became more intense or less degraded, male cricket frogs gradually decreased their call rate and increased the number of call groups and pulse groups in their calls, changes indicative of increased aggressive interactions. At the higher intensities and lower degradation levels, the probability that males would shift to one of two non-vocal behavioral responses, attacking the perceived intruder or ceasing calling and abandoning the call site, gradually increased. The results show that differences in signal attenuation and AM degradation levels are perceived by males and trigger both vocal and non-vocal behavioral responses consistent with their use in evaluating the distance to a challenging male. Furthermore, the results indicate that the male responses are graded, increasing as intensity rises and degradation falls, and hierarchical, with vocal responses preceding behavioral responses over the range of intensities and degradation levels presented.

How do males of Hypsiboas goianus (Hylidae: Anura) respond to conspecific acoustic stimuli?

Acoustic communication plays an important role in the social behavior of anurans. Acoustic signals, which can be used in different contexts such as mate attraction and territory defense, may mediate social interactions among individuals. Herein, we used playback experiments to test whether males of Hypsiboas goianus (Lutz, 1968) change their vocal behavior in response to conspecific advertisement calls. Specifically, we used different field playback experiments in which we modified the time interval between advertisement calls to simulate males with distinct states of motivation (Sequence A and B). We did not observe differences in the acoustic response of males of H. goianus between the two types of field playback experiments. On the other hand, we observed that H. goianus males reduce the dominant frequency of the advertisement call and increase the rate of aggressive calls in response to a conspecific competitor. Our results suggest that the acoustic plasticity observed in males of H. goianus represents an aggressive response that allows repelling conspecific individuals.

Evolutionary adaptations for the temporal processing of natural sounds by the anuran peripheral auditory system

Sensory systems function most efficiently when processing natural stimuli, such as vocalizations, and it is thought that this reflects evolutionary adaptation. Among the best-described examples of evolutionary adaptation in the auditory system are the frequent matches between spectral tuning in both the peripheral and central auditory systems of anurans (frogs and toads) and the frequency spectra of conspecific calls. Tuning to the temporal properties of conspecific calls is less well established, and in anurans has so far been documented only in the central auditory system. Using auditory-evoked potentials, we asked whether there are species-specific or sex-specific adaptations of the auditory systems of gray treefrogs (Hyla chrysoscelis) and green treefrogs (H. cinerea) to the temporal modulations present in conspecific calls. Modulation rate transfer functions (MRTFs) constructed from auditory steady-state responses revealed that each species was more sensitive than the other to the modulation rates typical of conspecific advertisement calls. In addition, auditory brainstem responses (ABRs) to paired clicks indicated relatively better temporal resolution in green treefrogs, which could represent an adaptation to the faster modulation rates present in the calls of this species. MRTFs and recovery of ABRs to paired clicks were generally similar between the sexes, and we found no evidence that males were more sensitive than females to the temporal modulation patterns characteristic of the aggressive calls used in male-male competition. Together, our results suggest that efficient processing of the temporal properties of behaviorally relevant sounds begins at potentially very early stages of the anuran auditory system that include the periphery.

Behavioral strategies and signaling in interspecific aggressive interactions in gray tree frogs

Interspecific aggression has important consequences for ecological processes and the evolution of behavioral strategies. We examined interspecific aggressive interactions in the 2 gray tree frog species, Hyla chrysoscelis and Hyla versicolor. These species call side by side in the same ponds, and acoustic interference occurs because of the similar spectral characteristics of their vocalizations. The aggressive calls of these 2 species, although very similar, were statistically distinguishable: calls of H. chrysoscelis were more strongly amplitude modulated than those of H. versicolor. We used playbacks and staged interactions to characterize the behaviors of males exposed to heterospecific competitors or their signals. Males readily responded with aggression to heterospecific individuals and playbacks of their calls. These behaviors were qualitatively similar in both intraspecific and interspecific interactions, but there were some significant differences. First, males of H. chrysoscelis were more aggressive toward playbacks of conspecific advertisement calls than toward those of H. versicolor. There were no significant differences in this respect in H. versicolor. Second, interspecific interactions were usually more escalated than intraspecific interactions and more likely to end with the loser moving away from its opponent. Although neither species had an advantage in staged interactions, behavioral responses were asymmetrical because H. versicolor was more likely than H. chrysoscelis to initiate physical contact. Previous studies showed that H. versicolor suffers from a greater reduction in attractiveness than H. chrysoscelis in the presence of heterospecific call overlap. Thus, the asymmetries in aggressive behavior between the 2 species may be related to differential costs of heterospecific competition.

Signal recognition by frogs in the presence of temporally fluctuating chorus-shaped noise

The background noise generated in large social aggregations of calling individuals is a potent source of auditory masking for animals that communicate acoustically. Despite similarities with the so-called "cocktail-party problem" in humans, few studies have explicitly investigated how non-human animals solve the perceptual task of separating biologically relevant acoustic signals from ambient background noise. Under certain conditions, humans experience a release from auditory masking when speech is presented in speech-like masking noise that fluctuates in amplitude. We tested the hypothesis that females of Cope's gray treefrog (Hyla chrysoscelis) experience masking release in artificial chorus noise that fluctuates in level at modulations rates characteristic of those present in ambient chorus noise. We estimated thresholds for recognizing conspecific advertisement calls (pulse rate=40-50 pulses/s) in the presence of unmodulated and sinusoidally amplitude modulated (SAM) chorus-shaped masking noise. We tested two rates of modulation (5 Hz and 45 Hz) because the sounds of frog choruses are modulated at low rates (e.g., less than 5-10 Hz), and because those of species with pulsatile signals are additionally modulated at higher rates typical of the pulse rate of calls (e.g., between 15-50 Hz). Recognition thresholds were similar in the unmodulated and 5-Hz SAM conditions, and 12 dB higher in the 45-Hz SAM condition. These results did not support the hypothesis that female gray treefrogs experience masking release in temporally fluctuating chorus-shaped noise. We discuss our results in terms of modulation masking, and hypothesize that natural amplitude fluctuations in ambient chorus noise may impair mating call perception.

Integration of sensory and motor processing underlying social behaviour in túngara frogs

Social decision making involves the perception and processing of social stimuli, the subsequent evaluation of that information in the context of the individual's internal and external milieus to produce a decision, and then culminates in behavioural output informed by that decision. We examined brain networks in an anuran communication system that relies on acoustic signals to guide simple, stereotyped motor output. We used egr-1 mRNA expression to measure neural activation in male túngara frogs, Physalaemus pustulosus, following exposure to conspecific and heterospecific calls that evoke competitive or aggressive behaviour. We found that acoustically driven activation in auditory brainstem nuclei is transformed into activation related to sensory-motor interactions in the diencephalon, followed by motor-related activation in the telencephalon. Furthermore, under baseline conditions, brain nuclei typically have correlated egr-1 mRNA levels within brain divisions. Hearing conspecific advertisement calls increases correlations between anatomically distant brain divisions; no such effect was observed in response to calls that elicit aggressive behaviour. Neural correlates of social decision making thus take multiple forms: (i) a progressive shift from sensory to motor encoding from lower to higher stages of neural processing and (ii) the emergence of correlated activation patterns among sensory and motor regions in response to behaviourally relevant social cues.

Effects of heterospecific call overlap on the phonotactic behaviour of grey treefrogs

We investigated the effects of overlap between the advertisement calls of two closely related and often-sympatric species of grey treefrogs on female phonotactic behaviour and signal selectivity. The tetraploid H. versicolor and the diploid H. chrysoscelis have advertisement calls consisting of trains of stereotyped pulses that are similar in their spectral composition. All females of H. versicolor from a population sympatric with H. chrysoscelis approached a speaker broadcasting synthetic advertisement calls modelled after conspecific calls when the calls of the two species alternated from speakers with a 90° angular separation with respect to the release point. Surprisingly, the same females almost exclusively approached the source of synthetic calls modelled after the heterospecific advertisement calls when these calls completely overlapped the conspecific stimuli. Female H. chrysoscelis from the same sympatric population approached the source of synthetic conspecific calls even when these calls were overlapped by the heterospecific stimuli, indicating that females in these closely related species may differ in their susceptibility to the negative consequences of call overlap. When female H. versicolor were presented with conspecific advertisement calls that were completely overlapped by those of H. chrysoscelis, many females failed to approach either signal source. Response times of females that did respond were also longer, and the direction of phonotaxis was shifted in the direction of the heterospecific signal source. These negative influences of acoustic interference were reduced or eliminated as the degree of overlap between the calls of the two species was reduced. The results demonstrate that the effects of signal overlap on female phonotactic behaviour may be complex.

Courtship Calls and Behavior in Two Species of Chorus Frogs, Genus Pseudacris (anura: Hylidae)

We studied the courtship behavior of two species of chorus frogs, Pseudacris illinoensis and P. triseriata, in western Illinois. We report observations of courtship behavior and describe courtship calls for each species. These calls were given in response to both male and female conspecifics entering the calling spaces of resident males. Courtship calls given in response to an intruder were never followed by aggressive behaviors from the resident or the intruder, and courtship calls were never given in response to playbacks of conspecific advertisement calls. Thus, these calls do not appear to be used in an aggressive context. Courtship calls of P. illinoensis are longer in duration than advertisement calls. Courtship calls in P. triseriata consist of multiple notes compared to single note advertisement calls. These courtship calls have higher pulse rates and lower dominant frequencies, and they are given at faster calling rates than advertisement calls. Courtship calls of both species are more variable in structure within males than advertisement calls. Like two other species of chorus frogs for which courtship calls have been reported, courtship calls in P. illinoensis and P. triseriata are modifications of the advertisement call. Courtship calls in the genus that have been described so far do not appear to share a common structure. The recognition of courtship calls in a chorus may play a useful role in long-term monitoring of anuran breeding activity, especially in remotely determining the presence of gravid females.

Acoustic Image of Yellow-Breasted Bunting Emberiza aureola Pall

Sonographic analysis of conspecific advertisement calls of yellow-breasted bunting (Emberiza aureola) was carried out. Calls of nine individuals living in the same range were compared. Particular elements responsible for individual differences were recognized in the calls. At the same time, the elements defining conspecific characters were recognized in all individuals. Individual differences were based on temporal indices: durations of individual syllables and intervals and even fusion of two syllables.

Alternate tactics in male bladder grasshoppers Bullacris membracioides (Orthoptera: Pneumoridae)

Summary Bladder grasshoppers (Orthoptera, Pneumoridae) are a unique group of nocturnal, specialized herbivores, endemic to coastal regions of Southern Africa. Adult males are characterized by an inflated abdomen, which develops at the final molt, and a signaling system capable of producing high intensity calls detectable by conspecifics at distances of up to 2 km. Female response to male calls leads to reciprocal duetting and pair formation. We have found an alternative form to the dominant inflated male tactic in three pneumorid species. These alternate males are incapable of flight and lack the air-filled abdominal bladder used in long-range acoustic communication; but may be found in copula with mature females in the field. Here we address the issue of neoteny/paedogenesis in the alternate male by comparing the morphology of inflated and uninflated adult male Bullacris membracioides with that of ultimate and penultimate nymphal instars, to determine whether these forms follow a common developmental trajectory. We then compare the behavioral responsiveness of inflated and noninflated morphs to conspecific advertisement calls, to ascertain whether alternate males have the potential to actively exploit the mate location system of duetting pairs. Morphometric analyses indicate that alternate males are a distinctly divergent form from the primary male developmental tactic. We conclude that males following the alternate tactic eavesdrop on the duets of inflated males and females to exploit the acoustic mate location system. This satellite tactic has potential impact on several aspects of pneumorid biology contributing to biasing sexual selection, sensory drive, and ultimately speciation events.

Signal discrimination by female Iberian midwife toads (Alytes cisternasii)

Coevolution between signaller and receiver is critical in signal evolution. Midwife toads produce simple calls that are similar among species. I conducted phonotaxis experiments with female midwife toads to study their tolerance to alteration of conspecific advertisement calls. Large alterations in amplitude and frequency modulation rendered the typical call unattractive while smaller alterations in both amplitude and frequency modulation did not influence call attractiveness. Frequency modulations appear to be weighted more heavily in discrimination tests. The evolutionary significance of female tolerance is discussed.

Social Influences on Androgen Levels in the Southern Leopard Frog, Rana sphenocephala

Social cues play an important role in modulating neuroendocrine and hormonal states in many vertebrates. Social cues in the form of conspecific advertisement calls have been demonstrated to modulate plasma androgen levels in male Rana sphenocephala, the Southern leopard frog. Male R. sphenocephala were captured and brought to the laboratory for testing. Animals were exposed to one of two acoustical environments: a recording of an active conspecific breeding chorus or a recording of the same chorus in which all the spectral frequencies had been digitally shifted 500 Hz higher. Following 12 nights of exposure to either stimulus, plasma androgen levels were assessed by radioimmunoassay and gonadal morphology was examined to compare group differences. Plasma levels of dihydrotestosterone were significantly higher in males exposed to the conspecific chorus, compared with males exposed to the altered version of the chorus. Gonadal morphology did not differ between the two groups. These results suggest that in addition to environmental cues such as rainfall and other seasonal changes, social cues may also serve as environmental synchronizers among anurans to coordinate reproductive effort.

Male green frogs lower the pitch of acoustic signals in defense of territories: a possible dishonest signal of size?

In responses to broadcasts of conspecific advertisement calls, male green frogs (Rana clamitans) lower the dominant frequency of their calls. Because dominant frequency is negatively correlated with male body size in green frogs, frequency alteration provides a means of potentially exaggerating size during territorial contests. In field playback experiments, we broadcast synthetic stimuli representing small, medium, or large intruders to territorial residents. We tested the hypotheses that males use frequency alteration to provide honest signals of their size or their size-independent fighting ability, or to dishonestly signal size. Dominant frequency did not better predict male size in response calls than in unsolicited calls. The magnitude of frequency alteration was not related to body size, general condition, or an indirect measure of fighting ability. Thus, males did not use frequency alteration to provide honest information about body size or size-independent fighting ability. However, males significantly increased their apparent size by producing lower frequency calls. Small males produced relatively lower frequency calls in response to the large-male stimulus (compared to the small-male and medium-male stimuli), but large males did not. Further, the magnitudes of frequency alteration were significantly greater in responses to the large-male stimulus, primarily because small males responded with a greater decrease in frequency to the large-male stimulus than to the small-male and medium-male stimuli. These results support several predictions of the dishonest signal hypothesis and suggest that dishonesty may be a conditional strategy used by small males. Key words: bluffing, dishonesty, frequency alteration, green frogs, Rana clamitans, territoriality. [Behav Ecol 11:169–177 (2000)]

Selectivity of Evoked Vocal Responses in the Time Domain by Frogs of the Genus Batrachyla

The leptodactylid frogs Batrachyla taeniata, B. antartandica and B. leptopus in southern Chile produce advertisement calls composed of short pulses, repeated in species-specific patterns. Batrachyla lep- topus has a call with a complex structure relative to the other species, with pulses grouped in notes. Male frogs were presented with synthetic imitations of conspecific advertisement calls and variants for which different temporal components were varied systematically. Males of B. taeniata responded with fewer calls to synthetic stimuli having a low pulse rate (12.5 pul- ses/sec) relative to a standard stimulus imitating the natural advertisement call (50 pulses/sec). In contrast, males of B. antartandica gave fewer responses to stimuli having a high pulse rate (8 pulses/sec) relative to the standard call of this species (2 pulses/sec). Batrachyla taeniata gave weaker responses to continuous tones of the same duration as the standard call (500 msec) and B. antartandica also decreased significantly their responses to stimuli composed of pulses of long duration (48 msec) relative to the standard call (6 msec). Males of B. leptopus gave fewer responses to stimuli of extremely short (5 msec) or long (80 msec) notes, relative to the standard call, comprising notes of 40 msec duration. The evoked vocal responses of males of Batrachyla denote preferences that are in correspondence with the divergent pulse repetition patterns in their advertisement calls and with a selective processing of tem- poral features by the anuran auditory system. Such mechanisms of recognition may regulate vocal interac- tions in frog calling assemblages.

The function of call alternation in the African reed frog ( Hyperolius marmoratus ): precise call timing prevents auditory masking

The function of call alternation in the African painted reed frog, Hyperolius marmoratus was studied. Males actively avoided call overlap with neighboring males in their natural habitat. Advertisement calls produced by groups of two or three males showed less overlap than expected if they called at random. In addition, isolated males significantly reduced their calling rate to match the periodicity of a playback of periodic tone pulses, with vocalizations given during the silent intervals between tones. Gap-detection experiments showed that males suppressed vocalizations during playbacks of constant-frequency tone bursts and gave more calls during silent periods than expected by chance. Females discriminated against conspecific advertisement calls with many pulses in favor of calls with few or no pulses. This suggests that there would be little selection pressure on males to alternate calls so that pulses are not obscured. To test if call alternation functions to make calls more conspicuous, females were presented with identical conspecific advertisement calls from two speakers in four different temporal patterns: simultaneous, overlapping, abutting, and alternating. Females did not discriminate when calls were presented in a simultaneous, abutting, or alternating time pattern. When calls overlapped with the trailing call delayed from 0.5 to 70 ms females discriminated in favor of the leading call. When the intensity of the leading call was reduced by 6 dB the preference for the leading call was maintained when calls overlapped by 2 and 40 ms but was abolished or reversed at 0.5 and 70 ms, respectively. These results support the notion that the second of two partially overlapping calls was acoustically masked, rendering female painted reed frogs unwilling to approach or unable to locate such calls. It is suggested that either simultaneous masking or the precedence effect are responsible for the observed behavior. Acoustic masking of the second call by the first when calls overlapped was maintained even when the frequency of the first call was altered by 150 Hz above and below the more preferred frequency of the second call.