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

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

An exception to the matched filter hypothesis: A mismatch of male call frequency and female best hearing frequency in a torrent frog

The matched filter hypothesis proposes that the tuning of auditory sensitivity and the spectral character of calls will match in order to maximize auditory processing efficiency during courtship. In this study, we analyzed the acoustic structure of male calls and both male and female hearing sensitivities in the little torrent frog (Amolops torrentis), an anuran species who transmits acoustic signals across streams. The results were in striking contradiction to the matched filter hypothesis. Auditory brainstem response results showed that the best hearing range was 1.6–2 kHz consistent with the best sensitive frequency of most terrestrial lentic taxa, yet completely mismatched with the dominant frequency of conspecific calls (4.3 kHz). Moreover, phonotaxis tests show that females strongly prefer high‐frequency (4.3 kHz) over low‐frequency calls (1.6 kHz) regardless of ambient noise levels, although peripheral auditory sensitivity is highest in the 1.6–2 kHz range. These results are consistent with the idea that A. torrentis evolved from nonstreamside species and that high‐frequency calls evolved under the pressure of stream noise. Our results also suggest that female preferences based on central auditory system characteristics may evolve independently of peripheral auditory system sensitivity in order to maximize communication effectiveness in noisy environments.     

Auditory sexual difference in the large odorous frog Odorrana graminea

Acoustic communication is an important behavior in frog courtship. Male and female frogs of most species, except the concave-eared torrent frog Odorrana tormota, have largely similar audiograms. The large odorous frogs (Odorrana graminea) are sympatric with O. tormota, but have no ear canals. The difference in hearing between two sexes of the frog is unknown. We recorded auditory evoked near-field potentials and single-unit responses from the auditory midbrain (the torus semicircularis) to determine auditory frequency sensitivity and threshold. The results show that males have the upper frequency limit at 24 kHz and females have the upper limit at 16 kHz. The more sensitive frequency range is 3–15 kHz for males and 1–8 kHz for females. Males have the minimum threshold at 11 kHz (58 dB SPL), higher about 5 dB than that at 3 kHz for females. The best excitatory frequencies of single units are mostly between 3 and 5 kHz in females and at 7–8 kHz in males. The underlying mechanism of auditory sexual differences is discussed.     

Ultrasound hearing and male–male communication in Australian katydids (Tettigoniidae: Zaprochilinae) with sexually dimorphic ears

The genus Kawanaphila (Tettigoniidae: Zaprochilinae) is unusual among the Tettigoniidae in the possession of sexually dimorphic auditory organs. We examined the auditory system and acoustic behaviour of two previously unstudied species in this genus to test whether reduced hearing in males is consistently associated with reduced male–male competition. Kawanaphila yarraga (Rentz, 1993) and K. mirla (Rentz, 1993) are both sexually dimorphic with respect to their auditory system, but to different degrees. Males of both species produce songs consisting of trains of brief (< 1 ms) pure-tone sound pulses at ultrasonic frequencies (K. yarraga, 40 kHz;K. mirla, 70 kHz). In both species, female hearing is more sensitive than that of males by 10 dB. In addition, male K. mirla are most sensitive at lower frequencies than females. Male and female K. yarraga differed only in sensitivity, not in tuning. The two species also differ in their degree of sexual dimorphism in auditory anatomy. Kawanaphila mirla males lack some auditory specializations of the prothoracic tracheal system, which are present in the normal tettigoniid condition in females. In K. yarraga males these structures are present, but reduced in size relative to females. The acoustic behaviour of males of the two species is consistent with this pattern of relative auditory sensitivity. Males of both species interact acoustically by altering the timing of their sound output to synchronize with neighbouring males. However, K. mirla males only interact in this way over very short distances (< 5 m), whereas K. yarraga males interact with neighbours up to at least 10 m distant. These results indicate that, although males of the two species differ in hearing sensitivity, the nature of their responses to conspecific calls are similar to one another and to those of other acoustic insects. This suggests that acoustically mediated male–male competition may be maintained even while selection favours a reduction in male auditory sensitivity.     

Hormone-induced vocal behavior and midbrain auditory sensitivity in the green treefrog,Hyla cinerea

Summary Twenty four castrated male, 6 intact male, and 11 intact female Hyla cinerea were injected subcutaneously with 25 g arginine-vasotocin (AVT) and induced to call 1 h later in response to the playback of a conspecific mating call. Eighteen castrated males and 8 intact females were implanted 5 mg androgen pellets for 3 weeks prior to the neuropeptide injection. Among castrated males, 6/9 testosterone (T) implanted, 4/9 dihydrotestosterone (DHT) implanted and 2/6 non implanted individuals produced calls after being administered AVT. 5/6 intact non implanted males and 6/8 T intact implanted females also called, and 3 intact non implanted females remained silent after the injection. Evoked calls had a mid-frequency spectral peak at about 1900 Hz which is absent in field-recorded mating calls of this species. Calls of implanted females and castrated non implanted males were shorter than those of castrated implanted and intact non implanted males. Audiograms measured before hormone implants showed dips of enhanced sensitivity at about 0.5, 0.9 and 3.0 kHz in males and females. After AVT injection, thresholds at frequencies within the 0.7–1.5 kHz range were increased in castrated males. Such reduction in sensitivity points to an inhibition of the auditory system during hormone induced vocal activation.Abbreviations AVT arginine-vasotocin - DHT dihydrotestosterone - T testosterone - TS torus semicircularis     

Do large bushcrickets have more sensitive ears? Natural variation in hearing thresholds within populations of the bushcricket Requena verticalis (Listroscelidinae: Tettigoniidae)

The auditory spiracle of tettigoniid Orthoptera influences hearing threshold and, for the most part, individuals with larger auditory spiracles have lower hearing thresholds; they are more sensitive. Hearing thresholds of both sexes of the bushcricket, Requena verticalis Walker (Orthoptera; Tettigoniidae; Listroscelidinae), were measured at the male call's carrier frequency and were found to correlate with spiracle dimension. In turn, spiracle dimension correlates with the size of the insect as measured by pronotum length. The best frequency of hearing is close to 16 kHz and this appears to be independent of size. Males show a higher variation in threshold than females and this was reflected in a trend toward lower variance in spiracle size in females.
To test the effects of size on sensitivity, spiracle size was manipulated by partially blocking it. Blocking the spiracle decreases sensitivity to high rather than low frequencies. As in other tettigoniids, the spiracle and associated auditory system act as a high-pass filter. Within and between sex differences in hearing sensitivity were compared with differences in male call intensity. It is argued that sensitivity to sounds associated with mating should be as much under sexual selection as the sexual calls of males.     

Changes in the Frequency Structure of a Mating Call Decrease Its Attractiveness to Females in the Cricket Frog Acris crepitans blanchardi

In many species, females often prefer male signals that are more complex than in nature or beyond the range of calls naturally produced by conspecific males in spectral, temporal and amplitude features. In this study we examined both the ability of females to recognize signals outside the normal range of spectral frequency variation seen in male advertisement calls, and the influence of increasing call complexity by adding spectral components to enhance the attractiveness of a male advertisement call in the cricket frog Acris crepitans blanchardi, while keeping its amplitude constant. We used two different natural male call groups and created the following synthetic call groups: with a dominant frequency at 3500 Hz, i.e. at the normal dominant frequency with a frequency band within the sensitivity range of the inner ear basilar papilla; with a dominant frequency at 700 Hz, i.e. outside the normal range of variation and with a frequency band outside the sensitivity range of the basilar papilla but within the range of the amphibian papilla; with two dominant frequencies, one at 700 Hz and another at 3500 Hz, stimulating the basilar and amphibian papilla simultaneously. In double choice experiments we tested all combinations of the three call groups, and we tested the 3500 Hz call groups against the same natural call groups. Additionally, we tested the 700 Hz call groups against white noise to see whether these signals are meaningful in mate choice. Females preferred 3500 Hz call groups over all other call groups. The synthetic call group was as attractive to females as the same natural call group. The 700 Hz call group was not meaningful in mate choice. The combined (700 Hz + 3500 Hz) call group was significantly less attractive to females than the 3500 Hz call group. Thus, making a call more spectrally complex without increasing its overall amplitude decreases its attractiveness to cricket frog females.     

A test of the matched filter hypothesis in two sympatric frogs,Chiromantis doriae and Feihyla vittata

The matched filter hypothesis proposes that the auditory sensitivity of receivers should match the spectral energy distribution of the senders’ signals. If so, receivers should be able to distinguish between species-specific and hetero-specific signals. We tested the matched filter hypothesis in two sympatric species, Chiromantis doriae and Feihyla vittata, whose calls exhibit similar frequency characters and that overlap in the breeding season and microenvironment. For both species, we recorded male calls and measured the auditory sensitivity of both sexes using the auditory brainstem response (ABR). We compared the auditory sensitivity with the spectral energy distribution of the calls of each species and found that (1) auditory sensitivity matched the signal spectrogram in C. doriae and F. vittata; (2) the concordance conformed better to the conspecific signal versus the hetero-specific signal. In addition, our results show that species differences are larger than sex differences for ABR audiograms.     

Correspondence between evoked vocal responses and auditory thresholds in Pleurodema thaul (Amphibia; Leptodactylidae)

Thresholds for evoked vocal responses and thresholds of multiunit midbrain auditory responses to pure tones and synthetic calls were investigated in males of Pleurodema thaul, as behavioral thresholds well above auditory sensitivity have been reported for other anurans. Thresholds for evoked vocal responses to synthetic advertisement calls played back at increasing intensity averaged 43 dB RMS SPL (range 31–52 dB RMS SPL), measured at the subjects’ position. Number of pulses increased with stimulus intensities, reaching a plateau at about 18–39 dB above threshold and decreased at higher intensities. Latency to call followed inverse trends relative to number of pulses. Neural audiograms yielded an average best threshold in the high frequency range of 46.6 dB RMS SPL (range 41–51 dB RMS SPL) and a center frequency of 1.9 kHz (range 1.7–2.6 kHz). Auditory thresholds for a synthetic call having a carrier frequency of 2.1 kHz averaged 44 dB RMS SPL (range 39–47 dB RMS SPL). The similarity between thresholds for advertisement calling and auditory thresholds for the advertisement call indicates that male P. thaul use the full extent of their auditory sensitivity in acoustic interactions, likely an evolutionary adaptation allowing chorusing activity in low-density aggregations.     

Frequency sensitivity in the auditory periphery of male and female black-capped chickadees (Poecile atricapillus)

The black-capped chickadee is a songbird that has been used extensively as a model of animal communication in field and laboratory settings. Although many studies have focused on the complex call and song systems of the black-capped chickadee, relatively fewer studies have focused on chickadee audition. However, we do know from behavioral and molecular work that chickadees (and auditory processing areas in their brains) discriminate between artificially generated tones, between conspecific and heterospecific vocalizations, and among different types of conspecific vocalizations. In this paper we investigate peripheral auditory processing of frequency in the black-capped chickadee and the potential influence of sex on frequency sensitivity using a technique called auditory evoked potentials. We found that male and female black-capped chickadees did not differ in any measure of frequency sensitivity. Both sexes had the greatest sensitivity to frequencies between 2 and 4 kHz. This range of frequencies is well represented in black-capped chickadee song, partially supporting the idea that sender and receiver coevolve. Finally, we suggest that the call and song system of North American parids make them an ideal taxonomic group for comparative work exploring the relationship between call systems and the evolution of auditory processing.     

Acoustic Competition in Male Midwife Toads Alytes obstetricans and Alytes cisternasii: Response to Neighbor Size and Calling Rate. Implications for Female Choice

Effects of neighbor on male calling behavior was studied through playback experiments of synthetic calls to males of two species of midwife toads. The responses of resident males were scored considering two temporal parameters (call duration and calling rate) and one spectral parameter (dominant frequency). The sounds used for the playback tests included two levels of fundamental frequency (correlated with male size) and two levels of call repetition rate. In both species, resident males only changed their calling rate in the presence of an intruder, and the response was different for synthetic calls with two levels of dominant frequencies and with two calling rates. Resident size was not significantly correlated with the magnitude of the change in the calling rate. On the other hand, resident calling rate was significantly and positively correlated with the magnitude of the increase in calling rate of the stimulus. The maximum relative increase in calling rate was observed in A. cisternasii. In phonotaxis tests, females are preferentially attracted to calls emitted at a higher rate confirming the importance of changes in calling rate for female attraction.     

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.     

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

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

Female frog auditory sensitivity,male calls,and background noise: potential influences on the evolution of a peculiar matched filter

The matched filter hypothesis proposes that the tuning of females' auditory sensitivity matches the spectral energy distribution of males' signals. Such correspondence is expected to arise over evolutionary time, as it promotes conspecific information transfer and reduces interference from other sound sources. Our main objective was to determine the correspondence between the acoustic sensitivity of female frogs of Eupsophus roseus and the spectral characteristics of advertisement vocalizations produced by conspecific males. We also aimed to determine how auditory sensitivity is related to the characteristics of background noise. We analysed data on the auditory sensitivity of E. roseus females, and recordings of conspecific male vocalizations and of the acoustic environment during the breeding period of this species. Our results indicate a concordance between the auditory sensitivity of females and call spectra that would provide an appropriate detection of these signals. In addition, this matching is large relative to the correspondence between auditory sensitivity with the spectra of the abiotic and biotic background noise, with the last component being associated with calls of the related species Eupsophus vertebralis. This may be an adaptation of receivers confronting sound interference, which improves the capability of E. roseus to communicate sexually by means of acoustic signals. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 814–827.     

Acoustic communication in spring peepers

Summary In the previous study (Wilczynski et al. 1984) we found that neurons in the auditory nerve of female spring peepers (Hyla crucifer) are tuned to frequencies in the male advertisement call, whereas auditory units in male peepers are mismatched in spectral sensitivity to their call. We investigated, in the present report, behavioral consequences of this sexual dimorphism in auditory sensitivity. Call amplitude, rate of call attenuation with environmental transmission, and the amplitude of ambient noise were measured and used to compute the active space of this signal for males and females. The effect of calling height upon active space was considered. Measurements of active space were compared with intermale distances within breeding choruses.Results indicate that active space of the advertisement call for females is as much as 6 times greater than that for males, and varies directly with the height above ground from which males call. Observed maximum intermale distances correspond closely to the active space of the call for this sex. This suggests that males space themselves so that the amplitude of a neighbor's calls approximates their auditory neural threshold to call frequencies. By this proximal mechanism, peepers maximize intermale distance but ensure that they remain within a chorus.Abbreviation dB SPL decibels sound pressure levelre: 20 Pa     

Listening for males and bats: spectral processing in the hearing organ of <Emphasis Type="Italic">Neoconocephalus bivocatus</Emphasis> (Orthoptera: Tettigoniidae)

Tettigoniids use hearing for mate finding and the avoidance of predators (mainly bats). Using intracellular recordings, we studied the response properties of auditory receptor cells of Neoconocephalus bivocatus to different sound frequencies, with a special focus on the frequency ranges representative of male calls and bat cries. We found several response properties that may represent adaptations for hearing in both contexts. Receptor cells with characteristic frequencies close to the dominant frequency of the communication signal were more broadly tuned, thus extending their range of high sensitivity. This increases the number of cells responding to the dominant frequency of the male call at low signal amplitudes, which should improve long distance call localization. Many cells tuned to audio frequencies had intermediate thresholds for ultrasound. As a consequence, a large number of receptors should be recruited at intermediate amplitudes of bat cries. This collective response of many receptors may function to emphasize predator information in the sensory system, and correlates with the amplitude range at which ultrasound elicits evasive behavior in tettigoniids. We compare our results with spectral processing in crickets, and discuss that both groups evolved different adaptations for the perceptual tasks of mate and predator detection.     

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.     

Temporal call changes and prior experience affect graded signalling in the cricket frog

We investigated how male cricket frogs Acris crepitans, alter their advertisement calls in response to broadcasts of synthetic calls that were either 'attractive' or 'aggressive'. The stimulus calls differed in temporal but not spectral characteristics. Male cricket frogs produced a more aggressive call when presented with the aggressive stimulus, indicating that they perceived the temporal differences between the two call categories. The direction and degree of temporal and spectral changes depended on the relative dominant frequency of the resident and opponent. If the resident's dominant frequency was initially higher than the stimulus frequency, the pattern of change in dominant frequency mirrored that seen for the temporal call characters. In contrast, if the resident's initial dominant frequency was below that of the stimulus, then the temporal and spectral changes were in opposite directions. Furthermore, stimulus order influenced whether males responded differently to playbacks of aggressive and attractive calls; males that received the aggressive call first produced more aggressive calls during the aggressive stimulus, while males that received the attractive call first produced similar calls in response to the two stimuli. This suggests that experience with different types of signals influences the subsequent calling behaviour of male cricket frogs. Copyright 1999 The Association for the Study of Animal Behaviour.     

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

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