Invasion of the acoustic niche: variable responses by native species to invasive American bullfrog calls

Biological invasions are a major threat to biodiversity. Invasive species that use acoustic communication can affect native species through interference in the acoustic niche. The American Bullfrog Lithobates catesbeianus is a highly invasive anuran that is widely distributed in the Brazilian Atlantic Rainforest. Adult male bullfrogs emit loud advertisement calls at frequencies that overlap with the calls of several native species of frogs. Given that spectral overlap is a major factor in acoustic masking, the purpose of this study was to test the effects of the acoustic invasion of L. catesbeianus on native frogs that have calls with and without spectral overlap with the invader. In field experiments, we exposed calling males of two overlapping species and two non-overlapping species to recorded bullfrog vocalizations, white noise, and the vocalization of another native frog species. To identify effects, we compared calls recorded before, during, and after exposure. Our results showed that native species altered their calls in response to the bullfrog calls. However, we also observed similar responses to white noise and heterospecific native calls. Both the invasive and heterospecific calls were emitted at low frequencies, which suggests that the observed responses might be specific to low-frequency calls. Our results provide evidence that the introduction of new sounds can cause native species to modify their calls, and that responses to exogenous sounds are species- and stimulus-specific.     

How the environment shapes animal signals: a test of the acoustic adaptation hypothesis in frogs

Long‐distance acoustic signals are widely used in animal communication systems and, in many cases, are essential for reproduction. The acoustic adaptation hypothesis (AAH) implies that acoustic signals should be selected for further transmission and better content integrity under the acoustic constraints of the habitat in which they are produced. In this study, we test predictions derived from the AAH in frogs. Specifically, we focus on the difference between torrent frogs and frogs calling in less noisy habitats. Torrents produce sounds that can mask frog vocalizations and constitute a major acoustic constraint on call evolution. We combine data collected in the field, material from scientific collections and the literature for a total of 79 primarily Asian species, of the families Ranidae, Rhacophoridae, Dicroglossidae and Microhylidae. Using phylogenetic comparative methods and including morphological and environmental potential confounding factors, we investigate putatively adaptive call features in torrent frogs. We use broad habitat categories as well as fine‐scale habitat measurements and test their correlation with six call characteristics. We find mixed support for the AAH. Spectral features of torrent frog calls are different from those of frogs calling in other habitats and are related to ambient noise levels, as predicted by the AAH. However, temporal call features do not seem to be shaped by the frogs’ calling habitats. Our results underline both the complexity of call evolution and the need to consider multiple factors when investigating this issue.     

Frog call transmission in forestry monocultures: Are there drawbacks?

Anuran males emit advertisement calls for the purpose of attracting females and repelling conspecific males. Call transmission is influenced by the acoustics of the propagation environment, including vegetation. Thus, forestry monocultures of non-native trees represent artificial environments that could modify call transmission. These monocultures have substituted large areas of Atlantic Forest in southern Brazil, representing a conservation challenge. Considering this context, we hypothesized that anurans have calls that are less attenuated in their native environment than in forest plantations. To test it, we performed sound transmission experiments using calls of three anuran species native to southern Brazil: Boana bischoffi, B. leptolineata, and Hylodes meridionalis. We compared sound attenuation between the native forest and forestry monocultures (Eucalyptus sp. and Pinus sp. forests), and included distance from the sound source, air temperature, humidity, and vegetation density as cofactors in linear mixed models. Our results show that the advertisement calls of the two tree frogs (Boana) attenuate less in tree plantations than in native forests, while the third species shows either no differences or less attenuation in native forests. Our results can be understood according to differences in natural history and microhabitat use among the studied species. The two tree frog species vocalize perched from vegetation so their calls become better transmitted in forestry monocultures, which have fewer trees than the native forest. On the other hand, H. meridionalis calls from rocks on streams and the propagation is finely tuned to this peculiar microhabitat. We discuss the conservation implications of our findings for anurans and for the Atlantic Forest. Abstract in Portuguese and Spanish are available with online material.     

Advertisement calls of Guenther’s frog Hylarana guentheri (Anura: Ranidae) during the breeding season

Acoustic signalling is the most important form of communication in anuran amphibians. Here we recorded and analysed the calls of 18 male Guenther’s frogs (Hylarana guentheri) from the wild during the breeding season. The advertisement calls of H. guentheri were composed of from a single note to five notes, with three-note calls the most recorded. All individuals produced calls around 600 Hz but calls ranged from 470 to 2600 Hz. Comparing the differences between individuals calls, we found within-male coefficients of variation (CV_w) of call intensity, the fundamental frequency, the first formant, the second formant, the third formant and the fourth formant were static (less than 5% variation), whereas those of note duration, call duration, call interval, numbers of pulses and dominant frequency were dynamic (larger than 15% variation). Comparisons of the call characteristics of H. guentheri in this study with other studies from China, Singapore and Vietnam found call characteristics varied greatly between the five different locations.     

Male orientation on vocalization perches could optimize acoustic signal transmission in anurans

Acoustic signals are distorted by vegetation, wind currents, or other sounds when transmitted through the environment. Consequently, vocalizations with features that optimize sound transmission or behaviors that improve the efficacy of communication have evolved in many animal species. Among behavioral strategies, some species call from perches above the ground to increase the propagation distance of their acoustic signals. However, the orientation in the perch also influences the transmission of the vocalizations, so that frogs calling from different orientations (i.e., horizontal, upward, or downward) may affect differently the quality and efficacy of sound transmission. We implemented a sound transmission experiment to test for the effect of calling orientation (upward, downward, and horizontal) and distance on the attenuation and degradation of advertisement calls in the common dink frog Diasporus diastema. We broadcasted and re‐recorded advertisement calls at 2 m height, setting the speaker in three directions (upward, downward, and horizontal) to simulate different signaler orientations. We found that attenuation of the advertisement calls is significantly reduced when the speaker was directed either upward or downward, rather than horizontally. However, the degradation of call is lower when the speaker is direct horizontally. Since calls produced from either upward or downward orientations could travel farther, they could be used to signal male spatial location, while calls produced from a horizontal position could provide information on male quality at shorter distances at advanced phases of courtship.     

ADVERTISEMENT CALLS OF THE TREE FROGS,HYLA ARBOREA AND HYLA SAVIGNYI (ANURA: HYLIDAE) IN TURKEY

ABSTRACT

The systematic classification of tree frogs (Hyla) inhabiting different regions of the country of Turkey is unclear. Recordings of natural advertisement calls of individual male tree frogs in different locations in Turkey were analyzed to determine variation in acoustic features that may be related to taxonomic status. Multivariate analysis of covariance showed that call duration, intercali interval and number of pulses per call varied significantly between frogs in different locales. Call duration, intercall interval, and number of pulses per call were related to air temperature. Dominant frequency differed significantly between different groups of frogs, and was temperature-independent. These data are consistent with the hypothesis that tree frogs in Turkey represent two distinct species, Hyla arborea and Hyla savignyi.     

Are Tropical Highland Frog Calls Cold–adapted? The Case of the Andean Frog Hyla labialis1

Across a wide range of temperatures established in the laboratory, we tape–recorded the advertisement calls of 76 freshly caught Hyla labialis males from three elevationally separated populations in the Eastern Andes of Colombia. Each male was tested once at a single temperature and returned to his capture site after measurement of his snout–vent length. We measured and averaged three characteristics of five to ten successive calls for each individual: number of pulses per call, pulse repetition rate, and call duration. We found that calling activity occurred within temperature ranges that overlapped among frogs from different elevations, but widened and shifted downward with increasing altitude of origin. Males from all sites called at temperatures higher, but not lower, than those naturally occurring during their nightly activity period. No decline in vocal performance was apparent when frogs extended their calling activity into the range of high temperatures selected for basking. Both snout–vent length and temperature affected pulse repetition rate and call duration, while the number of pulses per call was temperature–independent. Compared to the smaller males from lower elevations, the larger, high–mountain males had calls with significandy more pulses, a lower pulse repetition rate, and longer duration. Within each population, rising temperatures caused pulse repetition rate to increase and call duration to decrease significantly, whereas the number of pulses per call remained unchanged. Pulse repetition rate of highland males was the factor least affected by temperature, and it was less sensitive to night temperatures than to day temperatures. This, together with their capacity to call at low temperatures, suggests that highland frog calls are cold adapted.     

Acoustic preferences and localization performance of blood-sucking flies (Corethrella Coquillett) to tungara frog calls

Mating signals that increase attractiveness of males to femalescan also increase conspicuousness of the signaler to predatorsand parasites. We investigated the acoustic preference of speciesof blood-sucking flies of the genus Corethrella (Diptera: Corethrellidae),which eavesdrop on the sexual advertisement signals of túngarafrogs (Physalaemus pustulosus). Male frogs of this species facultativelyproduce 2 types of mating calls: simple (whines alone) and complex(whines and chucks). We tested the acoustic preference of theflies and their ability to locate their host when the frogsproduce simple or complex calls. The flies exhibited phonotaxisto both types of calls but were preferentially attracted tocomplex calls. We show that acoustic information alone is sufficientfor the flies' accurate localization of calling frogs. Complexcalls, however, were not approached at closer distance or withdecreased landing error (i.e., proportion of landings outsidethe target) than simple calls, suggesting that call structuredoes not influence localization performance. Female túngarafrogs and frog-eating bats (Trachops cirrhosus) also prefercomplex to simple túngara frog calls. Thus, intendedand unintended receivers with different ear morphologies exhibitthe same preference for a specific túngara frog calltype. This result is discussed in the context of the evolutionof call attractiveness in a communication network.     

Flexibility as a Strategy for Avoiding Call Overlap in Male Anhui Treefrogs

Male-male vocal competition is critical for mating success in anuran species; however, it remains unknown that how males regulate their competitive strategies dynamically during competition because calling is highly time-consuming, energetically demanding and likely to increase predation risks. Since different parts of calls will encode different information for vocal communication, we hypothesized that competitive strategies of male frogs may be modulated by the temporal and spectral features of different call notes. To test this hypothesis, the natural advertisement calls(OC), its modified versions with the first call note replaced by white noise(WN) or other notes and with the fifth call note replaced by WN, were played back to the Anhui tree frogs(Rhacophorus zhoukaiyae). Results showed that 1) males produced more competitive calls in response to acoustic stimuli compared to their baseline calling during silence; and 2) males emitted more non-overlapping calls compared to overlapping calls in response to the acoustic stimuli. These results are consistent with the idea that males are flexible to acoustic signals and their competition strategies are modulated dynamically by social contexts.     

Call differences and calling site segregation in anuran species from central Amazonian floating meadows

Summary The acoustic behaviour of 15 sympatric and synchronically breeding species of frogs in an area of floating meadows near Manaus (Brazil) was studied for a period of 8 months. The calling positions of each species can be identified with certain physiognomic types of vegetation.Sound analyses were used to compare the mating calls. The main variables are dominant frequency, call duration and pulse repetition rate. Each of the 15 species has a distinct mating call and differs from the acoustic behaviour of each other one. Eleven species are separated in their dominant frequency ranges within their specific calling sites. Species sharing emphasised frequency ranges within identical calling sites differ greatly in at least two temporal variables.The roles of calling position, spectral, and temporal features of mating calls in species recognition and premating reproductive isolation are discussed.     

Nightly calling patterns in a Neotropical gladiator frog

In anurans, vocalization is the primary communication form and acoustic parameters are influenced by climatic conditions, but also by social contexts. We investigated calling site use and within-individual variation of acoustic parameters throughout the night in the gladiator-frog Hypsiboas goianus. We expected that large males would call closer to the water and at higher perches to avoid dehydration and maximize sound propagation. Furthermore, we tested the prediction that males would emit more aggressive calls early in the night and more advertisement calls late at night. Male size was not correlated with either distance from the water or perch height. However, as expected, males of H. goianus adopted a calling strategy that consisted of emitting more aggressive calls early in the night and more advertisement calls later in the night. Furthermore, repetition rate and interval between notes of the aggressive calls and repetition rate of the advertisement calls showed within-individual variation throughout the night that agreed with our expectations. The calling strategy of H. goianus is probably related to the establishment of calling sites early in the night and an investment in female attraction in the middle of the night when males’ aggressive interactions have faded away, or due to habituation increasing the males’ aggressive thresholds. This is the first study investigating within-individual patterns of acoustic parameters of calls throughout the night for anurans.     

The Energetics of Acoustic Signaling in Anurans and Insects

SYNOPSIS. This review focuses on the energetics of advertisementcalls in frogs and insects (mostly ensiferans). I also reviewa number of methodological questions relating to the most appropriateways to normalize metabolic rates for calling animals and tocalculate efficiency of sound production Although the mechanism of sound production is very differentin these groups (vocalization vs. stridulation), net metaboliccosts normalized to mass are similar among species producingthe most conspicuous calls. Features of the call that interactto determine energetic cost include repetition rate, call duration,and intensity (sound pressure level). Anurans tend to producelouder (more intense) calls while ensiferans tend to producesound during a greater proportion of the calling bout. All evidencesuggests that advertisement calls are produced aerobically andthe aerobic costs are similar or exceed the aerobic (but notnecessarily total costs) of terrestrial locomotion The pattern of radiated sound tends to be constant within aspecies and can be predicted to some degree from characteristicsof an animal's acoustic radiator. Efficiency of sound production(acoustic power/net metabolic power) is low (0.05 to 6%) andvariable when compared to locomotion ({small tilde} 10–20%).From the present sample it appears that frogs are more efficientthan ensiferans, but as more katydids are studied this trendmay not hold. Of the factors that have been identified as determiningefficiency the most important are the match between the sizeof the radiator and wavelength radiated, the absorption propertiesof the environment immediately around the animal, and the presenceor absence of structures such as baffles and acoustic burrows     

Reduced geographic variation in roars in different habitats rejects the acoustic adaptation hypothesis in the black-and-gold howler monkey (Alouatta caraya)

Vocalizations used for long-range communication must disperse without significant structural changes to be decoded by receivers. The acoustic adaptation hypothesis (AAH) holds that, since acoustic signals are influenced by the habitat in which they disperse, sounds will possess specific structural characteristics to diminish sound degradation. Additionally, vocalizations can also be influenced by genetics, anatomy, and/or cultural aspects. Here, we tested the AAH through quantitative comparisons of roars in four allopatric populations of the black-and-gold howler monkey (Alouatta caraya) across an environmental gradient from open to closed, in northeastern Argentina. At each site, we obtained good-quality recordings from three adult males, also between July and November 2013, conducted vegetation surveys (measuring tree density, canopy closure, and vertical structure), evaluated potential masking of roars by gathering environmental sound samples, and assessed sound attenuation of a synthetic tone at three different distances: 10 m (landmark reference distance), 50, and 100 m. We also tested the alternative hypothesis that acoustic properties of roars could be explained by population genetic divergence. Our results did not support the AAH. Although our four study sites were significantly different in vegetation structure, conforming to an open-to-closed gradient, roars of A. caraya were not different among populations. Likewise, although environmental sound differed between sites, we found no evidence of environmental sound affecting the acoustic properties of roars. The attenuation of the synthetic tone was only near significant at 100 m distance between both extreme sites from the environmental gradient. The four A. caraya study populations grouped into three genetically differentiated clusters. Since roar features were independent from population genetic clustering, we reject the genetic hypothesis too. The combination of high amplitude and low peak frequency of roars, coupled to small home range size and extensive overlap between neighboring groups, allows roars to keep their communication value across habitats without need of specific environmental tuning.     

A continental assessment of diurnality in frog calling behaviour

Acoustic signalling is evolutionarily important, influencing sexual selection and serving as a premating isolation mechanism. There is a strong evolutionary basis for acoustic signalling to occur nocturnally across many terrestrial vertebrate groups including mammals, reptiles and amphibians. Within some of these groups, there is a general assumption that ‘most taxa are nocturnal’ in their acoustic signalling, and this is a particularly strongly held view for most frogs. Here we challenge this well-accepted notion by quantifying diurnal calling behaviour in Australian frogs, leveraging a continental-wide citizen science dataset. Of 196 species present in the citizen science dataset, 140 (71%) were recorded at least once during the day. Of the most commonly observed species (i.e. species with at least 150 calls recorded in the database), there were surprisingly high rates of diurnal calling: 14 species had >25% of their calls recorded during the day. We also found that the relative rate of diurnal calling in frogs showed a strong phylogenetic signal, suggesting that the plasticity in calling behaviour as it relates to time of the day is strongly evolutionarily conserved. Our results highlight a suite of ecological and evolutionary questions that are worthy of further investigation.     

Advertisement Call Variation in the Golden Rocket Frog (Anomaloglossus beebei): Evidence for Individual Distinctiveness

Individual distinctiveness in acoustic signals can allow receivers to respond appropriately to different individuals. The aim of this research was to examine signal variation and to investigate the relative importance of different acoustic properties for coding individual distinctiveness in the advertisement calls of male golden rocket frogs (Anomaloglossus beebei). We examined patterns of within‐individual and among‐individual variability in 760 advertisement calls of 40 males as well as repeatability in 16 additional males that were recorded on two different occasions. We examined eight call properties, and all properties exhibited significant among‐individual variation and moderate to high repeatability across days. We employed discriminant function analysis to examine individual distinctiveness statistically. These analyses assigned 79% of calls to the correct individual. Fine temporal properties, including pulse duration, pulse rate, and pulse interval, as well as the spectral property of dominant frequency, contributed most toward discrimination among individuals. These results indicate that individual male golden rocket frogs can be distinguished statistically by their advertisement calls. We use these findings to evaluate results of previous playback studies in A. beebei and to generate testable predictions regarding the potential for specific call properties to function in mate selection and social recognition.     

Acoustic Preference of Frog‐Biting Midges (Corethrella spp) Attacking Túngara Frogs in their Natural Habitat

In many animals, males aggregate to produce mating signals that attract conspecific females. These leks, however, also attract eavesdropping predators and parasites lured by the mating signal. This study investigates the acoustic preferences of eavesdroppers attracted to natural choruses in a Neotropical frog, the túngara frog (Engystomops pustulosus). In particular, we examined the responses of frog‐biting midges to natural variation in call properties and signaling rates of males in the chorus. These midges use the mating calls of the frogs to localize them and obtain a blood meal. Although it is known that the midges prefer complex over simple túngara frog calls, it is unclear how these eavesdroppers respond to natural call variation when confronted with multiple males in a chorus. We investigated the acoustic preference of the midges using calling frogs in their natural environment and thus accounted for natural variation in their call properties. We performed field recordings using a sound imaging system to quantify the temporal call properties of males in small choruses. During these recordings, we also collected frog‐biting midges attacking calling males. Our results revealed that, in a given chorus, male frogs calling at higher rates and with higher call complexity attracted a larger number of frog‐biting midges. Call rate was particularly important at increasing the number of midges attracted when males produced calls of lower complexity. Similarly, call complexity increased attractiveness to the midges especially when males produced calls at a low repetition rate. Given that female túngara frogs prefer calls produced at higher repetition rates and higher complexity, this study highlights the challenge faced by signalers when increasing attractiveness of the signal to their intended receivers.     

Intraspecific variation in advertisement call characteristics and acoustic strategies among male forest green tree frogs

Frogs are a representative taxon that use advertisement calls to aid in reproduction. In most frog species, calls vary with body size, and allometric constraints between body size and call frequency have been widely reported among anuran species. Although this variation is an important driver of sexual selection in frogs, male advertisement call strategies may also vary according to body size. In this study, we conducted playback experiments on the male forest green tree frog (Zhangixalus arboreus) to determine whether male advertisement call characteristics and strategies vary according to body size and the amplitude of intraspecific chorus noise. The results indicated that the calls of larger individuals are louder and lower than those of smaller ones, who call more frequently; moreover, the calls become lower, and the number of calls decreases, as noise levels increase. These findings suggest that forest green tree frog emits lower calls or refrains from calling when chorus noise increases, and that intraspecific variation in advertisement call characteristics can induce different strategies in response to chorus noise. Because advertisement call variation with body size is common among frog species, intraspecific variation in male advertisement call strategies may also be a common phenomenon.     

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.     

Synchronized interdigitated calling in the Kuvangu running frog, Kassina kuvangensis

Male Kuvangu frogs show repetitive calling of pulsed advertisement calls in which up to seven calls are repeated in short succession. Recordings of pairwise interactions between males showed that calls were highly synchronized, with individual calls interdigitating with each other. Males frequently switched between the leader and follower role with neither male dominating the interaction. Interactive playback experiments using synthetic calls revealed that males slightly but significantly increased the number of calls per call group with increases in stimulus call number. Males also significantly increased call rate with the number of calls in the playback stimulus. Furthermore, when presented with shortened intercall intervals, males increased their own intercall intervals, thus ‘skipping’ a call and avoiding overlap with the playback. The low degree of call matching suggests that repetitive calling, apart from maintaining a male's attractiveness to females relative to rival males, may mediate male-male competition. In addition, synchronized interdigitated calling may serve to reduce predation, while maintaining species-specific temporal features of advertisement calls important to females. Kuvangu running frogs may have reduced the costs associated with synchrony and alternation by using a signal timing scheme that allows them to do both simultaneously.Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.