Vocal Strategies in Confronting Interfering Sounds by a Frog from the Southern Temperate Forest,Batrachyla antartandica

Animals are communicating by sound face interference from biotic and abiotic sources. Contrasting strategies have been reported in different taxa in the presence of prolonged noises, but in particular, interactions among acoustically active species have been studied to a very limited extent. In addition, reactions of a single species to interferences having contrasting structural patterns have not been explored systematically. The vocal responses of 16 male frogs Batrachyla antartandica from the temperate austral forest in Chile were tested with conspecific calls and with the calls of two sympatric species: B. taeniata and B. leptopus, broadcast at amplitudes of 73, 79, 85, 91, and 97 dB peak sound pressure level (SPL). Also, the vocal activity of the subjects during exposure to a 3‐min continuous broadband noise presented at 67 dB root mean square (RMS) SPL was monitored. The subjects gave significantly higher responses to the conspecific relative to the heterospecific calls but increased their vocal output in the presence of continuous noise. The preference of vocal responses for the conspecific relative to heterospecific signals bears a general resemblance to those exhibited by B. taeniata in a previous study and potentially contributes to the typical segregation in conspecific choruses observed in areas where these frogs breed in sympatry. Such lack of vocal responses to heterospecific stimuli contrasts with the increase in vocal activity during exposure to continuous noise lacking a temporal fine structure and points to identify different strategies in confronting interferences of diverse origin.     

Restricted responsiveness to noise interference in two anurans from the southern temperate forest

Animals adopt different strategies to communicate by means of sound in noisy environments such that some species increase, while others decrease their vocal activity in the presence of interference. Anuran amphibians from diverse latitudes exhibit both kinds of responses. Recent studies have shown that males of Batrachyla taeniata and Batrachyla antartandica from the temperate austral forest do not call in response to the presentation of advertisement calls of sympatric congeneric species. In contrast, Batrachyla leptopus responds to these signals in a similar way as to conspecific calls. The responsiveness of B. taeniata to natural abiotic interference has also been tested and found that noises of such sources produce strong increases in vocal activity. To assess the diversity in responsiveness to acoustic intrusion in this group, we exposed males of B. leptopus and B. antartandica to prolonged pre‐recorded natural abiotic noises of wind, creek, rain, and to a band‐pass noise centered at 2,000 Hz, at 67 dB Sound Pressure Level (SPL). The subjects did not increase their vocal activity significantly when exposed to these sounds and to band‐pass noise at increasing intensities (55–79 dB SPL). These results contrast with the increase in vocal activity observed previously in B. taeniata to continuous abiotic noise and point to the existence of diverse strategies to confront acoustic intrusion among related species. The lack of vocal activation observed also contrasts with the responsiveness of B. leptopus to heterospecific signals, but parallels the lack of response to such sounds in B. antartandica. Furthermore, the results obtained contrast with the responsiveness of these species to synthetic prolonged sounds observed in previous studies, suggesting that the modes of responses to acoustic intrusion may depend on previous experience, rather than having a species‐specific nature.     

Heterospecific Vocal Interactions in a Frog from the Southern Temperate Forest,Batrachyla taeniata

Animals using sound communication employ different strategies to overcome interferences from biotic and abiotic sources. However, interactions among acoustically active species have been studied to a very limited extent. The evoked vocal responses of 20 male frogs Batrachyla taeniata from the temperate austral forest in Chile were tested with conspecific calls and with the calls of two sympatric species: B. antartandica and B. leptopus, broadcast at amplitudes of 73, 79, 85, 91 and 97 dB peak SPL. The subjects responded actively to the conspecific call, but only responded weakly to the call of B. leptopus at the highest intensity. The preferential responses to conspecific calls could contribute to the typical segregation in monospecific choruses observed in areas where these frogs breed in sympatry.     

Cytogenetics of Batrachyla species (Anura: Neobatrachia: Ceratophryidae) of southern South America,with phylogenetics comments

Abstract

A comparative cytogenetic analysis showed that B. antartandica, B. leptopus, B. nibaldoi and B. taeniata share the same diploid number 2n = 26, but not the same fundamental number (FN), which was 52 in B. leptopus and 50 in the other three species. The karyotype of B. nibaldoi, including C‐band patterns and locations of the NORs, are described for the first time. The C‐band patterns were species‐specific and were helpful in distinguishing taxa. Batrachyla leptopus can be distinguished from its congeners by the absence of telocentric chromosomes and by secondary constrictions in the long arms of pair 6 and short arms of pairs 7 and 11. The chromosomal data suggest that Batrachyla might be a paraphyletic genus.     

Ample active acoustic space of a frog from the South American temperate forest

The efficiency of acoustic communication depends on the power generated by the sound source, the attributes of the environment across which signals propagate, the environmental noise and the sensitivity of the intended receivers. Eupsophus emiliopugini, an anuran from the temperate austral forest communicates by means of an advertisement call of moderate intensity within the range for anurans. To estimate the range over which these frogs communicate effectively, we conducted measurements of call sound levels and of auditory thresholds to pure tones and to synthetic conspecific calls. The results show that E. emiliopugini produces advertisement calls of about 84 dB SPL at 0.25 m from the caller. The signals are affected by attenuation as they propagate, reaching average values of about 47 dB SPL at 8 m from the sound source. Midbrain multi-unit recordings show quite sensitive audiograms within the anuran range, with thresholds of about 44 dB SPL for synthetic imitations of conspecific calls, which would allow communication at distances beyond 8 m. This is an extended range as compared to E. calcaratus, a related syntopic species for which a previous study has shown to be restricted to active acoustic spaces shorter than 2 m. The comparison reveals divergent strategies for related taxa communicating amid the same environment.     

Severe constraints for sound communication in a frog from the South American temperate forest

The efficiency of acoustic communication depends on the power generated by the sound source, the quality of the environment across which signals propagate, the environmental noise and the sensitivity of the intended receivers. Eupsophus calcaratus, an anuran from the temperate austral forest, communicates by means of an advertisement call of weak intensity in a sound-attenuating environment. To estimate the range over which these frogs communicate effectively, we conducted measurements of sound level and degradation patterns of propagating advertisement calls in the field, and measurements of auditory thresholds to pure tones and to natural calls in laboratory conditions. The results show that E. calcaratus produces weak advertisement calls of about 72 dB sound pressure level (SPL) at 0.25 m from the caller. The signals are affected by attenuation and degradation patterns as they propagate in their native environment, reaching average values of 61 and 51 dB SPL at 1 and 2 m from the sound source, respectively. Midbrain multi-unit recordings show a relatively low auditory sensitivity, with thresholds of about 58 dB SPL for conspecific calls, which are likely to restrict communication to distances shorter than 2 m, a remarkably short range as compared to other anurans.     

Behavioural response evoked by conspecific distress calls in two neotropical treefrogs

Anurans emit distress calls when attacked by predators as a defensive mechanism. As distress calls may trigger antipredator behaviour even in individuals that are not under attack, we tested whether this defensive behaviour induced behavioural changes in neighbouring conspecifics. We compared the behavioural responses of two species of Neotropical hylid frogs (genus Boana) to conspecific distress calls and white noise. Individuals of both species interrupted their vocal activity and decreased call rate after hearing the distress call. Natural variation on signal intensity calibrated among the nearest neighbours did not influence the response and we did not observe negative phonotaxis after any acoustic stimulus. Despite the fact that many predators are acoustically oriented, we could not determine if such response (reduced call rate) was induced by risk assessment or by the masking effect on advertisement calls. Boana faber responded similarly to white noise and distress calls, while B. bischoffi responded more intensely to distress calls. Duration of silence after playbacks in B. faber was longer than B. bischoffi. We suggest that, if the signals are interpreted as a risk cue by neighbouring conspecifics, each species may be preyed upon by different predators, as they may have led to distinct defensive strategies and different responses to distress calls. If risk assessment information is included in distress calls, it triggers behavioural responses only in the nearest neighbours, as we did not observe responses on the vocal activity of the interspecific chorus. Our results add relevant data about acoustic communication and interpretations by anurans, highlighting the importance of considering cues within common and widespread signals.     

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.     

Differential Response to Interspecific and Intraspecific Signals Amongst Chickadees

Black‐capped chickadees (Poecile atricapillus) and mountain chickadees (P. gambeli) have a similar vocal repertoire and share many other life history traits; yet, black‐capped chickadees are socially dominant to mountain chickadees where populations overlap. Previous research suggested that in contact zones, both species respond weakly to heterospecific songs during the breeding season, and have suggested minimal interspecific competition. However, both black‐capped and mountain chickadees discriminate between conspecific and heterospecific chick‐a‐dee calls, suggesting attention is paid to interspecific signals. We compared the responses of both black‐capped and mountain chickadees to conspecific and heterospecific chick‐a‐dee calls during the winter, when both species compete for the same food resources. We conducted an aviary playback experiment exposing both species to playback composed of heterospecific and conspecific chick‐a‐dee calls, which had been recorded in the context of finding food sources. Responses from the tested birds were measured by recording vocalizations and behaviour. Black‐capped chickadees responded significantly more to conspecific than to heterospecific stimuli, whereas the subordinate mountain chickadees responded to both mountain and black‐capped chickadee calls. Based upon the reactions to playbacks, our results suggest these two closely related species may differ in their perception of the relative threat associated with intra‐ versus interspecific competitors.     

Dissimilarities in auditory tuning in midwife toads of the genus Alytes (Amphibia: Anura)

The auditory sensitivity in three species of the anuran genus Alytes (Alytidae) was examined to determine patterns of intra‐ and interspecific variation, relating these measurements to behavioural preferences measured in previous studies and to the adaptive and evolutionary significance of this sensory function. The audiograms obtained with multi‐unit recordings in the torus semicircularis of 13 Alytes cisternasii, 10 Alytes obstetricans, and eight Alytes dickhilleni show two regions of enhanced sensitivity, between approximately 100–500 and 1200–2400 Hz, with minimum thresholds at approximately 40 and 45 dB SPL, respectively. The mean and range of the high‐frequency region differed among species, although the sensitivity, measured as minimum thresholds, was similar. The region of high‐frequency sensitivity was centred at approximately the frequency of the advertisement call in A. cisternasii but, in A. obstetricans and A. dickhilleni, was centred at frequencies higher than the conspecific calls. These results contrast with preferences for lower frequencies exhibited by Alytes in female phonotactic and in male evoked vocal responses. Such loose relationships between signals and receivers suggest that the divergence of the sound communication system in Alytes has implied environmental and phylogenetic factors in addition to sexual selection processes.     

Context-dependent effects of noise on echolocation pulse characteristics in free-tailed bats

Background noise evokes a similar suite of adaptations in the acoustic structure of communication calls across a diverse range of vertebrates. Echolocating bats may have evolved specialized vocal strategies for echolocating in noise, but also seem to exhibit generic vertebrate responses such as the ubiquitous Lombard response. We wondered how bats balance generic and echolocation-specific vocal responses to noise. To address this question, we first characterized the vocal responses of flying free-tailed bats (Tadarida brasiliensis) to broadband noises varying in amplitude. Secondly, we measured the bats’ responses to band-limited noises that varied in the extent of overlap with their echolocation pulse bandwidth. We hypothesized that the bats’ generic responses to noise would be graded proportionally with noise amplitude, total bandwidth and frequency content, and consequently that more selective responses to band-limited noise such as the jamming avoidance response could be explained by a linear decomposition of the response to broadband noise. Instead, the results showed that both the nature and the magnitude of the vocal responses varied with the acoustic structure of the outgoing pulse as well as non-linearly with noise parameters. We conclude that free-tailed bats utilize separate generic and specialized vocal responses to noise in a context-dependent fashion.     

Ravens adjust their antipredatory responses to con‐ and hetero‐specific alarms to the perceived threat

Heterospecific alarm calls are typically found in situations where multiple species have a common predator. In birds, they are particularly common in mixed mixed‐species flocks. In species with highly developed social and cognitive abilities like corvids, there is the potential for differential responses to heterospecific vs. conspecific calls according to the riskiness of the habitat. We tested the responses of free‐ranging ravens (Corvus corax) to conspecific alarm calls and compared them to heterospecific alarm calls of jackdaws (Corvus monedula). We observed the proportion of ravens leaving the feeding site after the con‐ or hetero‐specific playback was presented in a situation of low threat (wild boar—Sus scrofa enclosure) and high threat of predation (wolf—Canis lupus enclosure). We show that ravens responded to conspecific calls more intensively at the wolves than at the wild boar, but the response to conspecific calls was in both enclosures stronger than to the control (great tit—Parus major song). The response to the heterospecific alarm was also stronger in the wolves’ enclosure, but it did not differ from control in the wild boar enclosure. These findings suggest that ravens are aware of the meaning of the jackdaw alarm calls, but they respond to it only in a situation of high predatory threat (wolves are present). In the wild boar enclosure, the ravens probably consider jackdaws warning against some other predator, very probably harmless to ravens. This interpretation requires further testing, as both enclosures differ also in respect to other parameters like food quality and shelter availability.     

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.     

Independence of Evoked Vocal Responses from Stimulus Direction in Burrowing Frogs Eupsophus (Leptodactylidae)

Localization of a sound source is important for animals in mating contexts: females generally orient towards signalling males, and males can estimate the position and quality of potential rivals. In anurans, the effect of sound direction on evoked vocal responses has been studied in males of Rana catesbeiana, which alter their vocal responses depending on the location of the stimulus. The current study explored the effects of sound direction in Eupsophus calcaratus, a frog that calls from inside burrows having resonance that would hinder the localization of incoming sounds. The vocal responses of 11 males to synthetic imitations of the conspecific advertisement call broadcast from loudspeakers positioned in front, to the right and left from the burrow openings were similar in terms of call rate, duration and latency. The invariance of the vocal responses indicates that for burrowing male frogs engaged in chorusing behaviour, the specific location of an opponent does not alter the persistence of vocal activity.     

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.     

Phylogeography of a Patagonian lizard and frog: Congruent signature of southern glacial refuges

Pleistocene glaciations produced significant increases in continental ice cover in polar and mid‐latitude temperate areas, sea‐level declines and shifts and reshuffling of biomes, all of which promote either isolation, coalescence or fragmentation in the distribution of land biota. If populations of several taxa have been co‐distributed for a prolonged time, and if the periods between perturbation or vicariance processes have been more or less stable, it is expected that divergence patterns of closely related and ecologically similar species will be congruent because of their similar biological and demographic characteristics. Based on this premise, we analysed the phylogeographic structure (cytochrome b) of Liolaemus pictus and Batrachyla leptopus, two widely co‐distributed lizard and frog species, respectively, in the Chiloé Archipelago of southern Chile, to decipher their genetic structure in response to a common climatic and environmental history. Haplotype network analysis and Bayesian inference suggest an evolutionary pattern of genetic diversity for the two species that is consistent with the Quaternary glacial history of southern Chile, and suggests a complex phylogeographic history in the Liolaemus and Batrachyla species. High‐divergence levels among haplotypes in some island populations of the archipelago also suggest genetic connectivity between putative refuges from Chiloé Island and the mainland along the exposed continental shelf during sea level minima associated with the most recent Quaternary glaciations. Our results are consistent with our hypothesis that two species have responded to parallel historical events in which the historical process during the last glacial maximum (approximately 41°S) has been sufficient to influence their phylogeographic structure.     

Female Sexual Preferences Toward Conspecific and Hybrid Male Mating Calls in Two Species of Polygynous Deer, <Emphasis Type="Italic">Cervus elaphu</Emphasis>s and <Emphasis Type="Italic">C. nippon</Emphasis>

The behavioral processes at the basis of hybridization and introgression are understudied in terrestrial mammals. We use a unique model to test the role of sexual signals as a reproductive barrier to introgression by investigating behavioral responses to male sexual calls in estrous females of two naturally allopatric but reproductively compatible deer species, red deer and sika deer. Previous studies demonstrated asymmetries in acoustic species discrimination between these species: most but not all female red deer prefer conspecific over sika deer male calls while female sika deer exhibit no preference differences. Here, we extend this examination of acoustic species discrimination to the role of male sexual calls in introgression between parent species and hybrids. Using two-speaker playback experiments, we compared the preference responses of estrous female red and sika deer to male sexual calls from conspecifics versus red × sika hybrids. These playbacks simulate early secondary contact between previously allopatric species after hybridization has occurred. Based on previous conspecific versus heterospecific playbacks, we predicted that most female red deer would prefer conspecific calls while female sika deer would show no difference in their preference behaviors toward conspecific and hybrid calls. However, results show that previous asymmetries did not persist as neither species exhibited more preferences for conspecific over hybrid calls. Thus, vocal behavior is not likely to deter introgression between these species during the early stages of sympatry. On a wider scale, weak discrimination against hybrid sexual signals could substantially contribute to this important evolutionary process in mammals and other taxa.     

Early singers attend to conspecific but not heterospecific behavioural cues at dawn

During the dawn chorus songbirds initiate singing activities just prior to sunrise. Environmental factors affect the timing of the dawn chorus, but relatively little is known about how behavioural cues influence chorus timing. We assessed whether early playback of conspecific and heterospecific song influenced chorus start times in two early‐singing temperate species, hermit thrush Catharus guttatus and veery C. fuscescens. We used arrays of GPS time‐synchronized recorders to record the dawn chorus at 30 locations. In each location, thirty minutes prior to natural chorus initiation, we broadcast: 1) an early singing species (hermit thrush or veery), 2) a late singing species (black‐throated green warbler Setophaga virens or Nashville warbler Oreothlypis ruficapilla), 3) a noise control, and 4) also recorded without playback (silent control). Playback treatments were separated by two‐three days at each location. Both hermit thrush and veery sang significantly earlier in response to conspecific playback compared to noise or silent controls. Both species also sang earlier in response to conspecific playback compared to the day before or the day after playback. Neither species sang earlier in response to heterospecific playback (regardless of whether the broadcast species was a naturally early or late song initiator) compared to noise or silent controls. Our results support the theory that the dawn chorus is a communication network where individuals attend primarily to conspecific cues; heterospecific song appears to have minimal impacts on the chorus start times of the two early‐singing species we investigated.     

An endangered bird calls less when invasive birds are calling

Novel noises can affect various animal behaviours, and changes to vocal behaviour are some of the most documented. The calls of invasive species are an important source of novel noise, yet their effects on native species are poorly understood. We examined the effects of invasive bird calls on the vocal activity of an endangered Australian finch to investigate whether: 1) native finch calling behaviour was affected by novel invasive bird calls, and 2) the calls of the finches overlapped in frequency with those of invasive birds. We exposed a wild population of black‐throated finch southern subspecies Poephila cincta cincta to the vocalisations of two invasive birds, nutmeg mannikins Lonchura punctulata and common mynas Acridotheres tristis, a synthetic ‘pink' noise, and a silent control. To determine whether the amount of black‐throated finch calling differed in response to treatments, we recorded and quantified black‐throated finch vocalisations, and assessed the amount of calling using a generalised linear mixed model followed by pairwise comparisons. We also measured, for both black‐throated finches and the stimulus noises: dominant, minimum and maximum frequency, and assessed the degree of frequency overlap between black‐throated finch calls and stimulus noises. Compared to silent controls, black‐throated finches called less when exposed to common myna calls and pink noise, but not to nutmeg mannikin calls. We also found that pink noise overlapped most in frequency with black‐throated finch calls. Common myna calls also somewhat overlapped the frequency range of black‐throated finch calls, whereas nutmeg mannikin calls overlapped the least. It is possible that masking interference is the mechanism behind the reduction in calling in response to common myna calls and pink noise, but more work is needed to resolve this. Regardless, these results indicate that the calls of invasive species can affect the behaviour of native species, and future research should aim to understand the scope and severity of this issue.