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.     

Reproductive character displacement in the acoustic communication system of green tree frogs (Hyla cinerea)

Abstract Interactions between species can affect the evolution of their sexual signals, receiver selectivity, or both. One commonly expected outcome is reproductive character displacement, whereby adverse consequences of mismating select for greater differentiation of communication systems in areas of sympatry than in areas of allopatry. We found evidence of reproductive character displacement in the acoustic communication system of green tree frogs ( Hyla cinerea ). The strength of female preferences for the spectral properties of calls that distinguish conspecific calls from those of a closely related congener, H. gratiosa , was greater in areas of sympatry with H. gratiosa than in areas of allopatry. We also found subtle differences in advertisement calls and in the heights of male calling perches when we restricted our comparisons to localities in which H. gratiosa was also breeding (syntopy) with localities where this species was absent. Hyla cinerea and H. gratiosa show only weak genetic incompatibility, but the calls representative of interspecific hybrids were unattractive to females of both parental species. Hybrids might also be at an ecological disadvantage because of different habitat preferences of the two taxa. Thus, selection against production of less fit or less attractive hybrid or backcross offspring are probably the main causes responsible for the differences documented in this paper.     

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.     

Communication in a noisy environment: short-term acoustic adjustments and the underlying acoustic niche of a Neotropical stream-breeding frog

Acoustically active animals may show long- and short-term adaptations in acoustic traits for coping with ambient noise. Given the key role of calls in anurans’ life history, long- and short-term adaptations are expected in species inhabiting noisy habitats. However, to disentangle such adaptations is a difficult task, incipiently addressed for Neotropical frogs. We investigated if males of a stream-breeding frog (Crossodactylus schmidti) adjust call traits according to the background noise, and if the signal-to-noise ratio (SNR) varies between call harmonics and along call notes. We measured sound pressure levels of calls and noise in the field and used a fine-scale acoustic analysis to describe the signal and noise structure and test for noise-related call adjustments. The multi-note harmonic call of C. schmidti greatly varied in the spectral structure, including a trend for increasing note amplitude along the call, a wide frequency bandwidth of the 2nd harmonic, a minor call frequency modulation due to a trend for increasing note frequency within the same harmonic, and a major call frequency modulation due to the variable location of the dominant harmonic along the call. Calls had significantly higher frequencies than the noise at the range of the 1st and the 2nd call harmonics, and significantly louder sound pressure than the noise at the range of all harmonics. Males emitted the majority of call notes showing positive SNR, and though males also emitted some notes with negative SNR, when a given harmonic was negative the other harmonics in the same note did not tend to be SNR-negative. Our results indicate that male C. schmidti show short-term acoustic adjustments that make the advertisement call effective for coping with the interference of the stream-generated noise. We suggest that the call spectral plasticity serves for coping with temporary changes in the background noise, whilst we also discuss the possibility that the redundant, harmonic-structured call may have evolved to diminish masking interference on the acoustic signal by the background noise. This is the first study to uncouple noise-related acoustic adjustments and putative long-term acoustic adaptations for a Hylodidae, providing insights on behavioral plasticity and signal evolution of stream-breeding frogs.     

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.     

The sound of a blood meal: Acoustic ecology of frog‐biting midges (Corethrella) in lowland Pacific Costa Rica

Animal communication systems are often exploited by eavesdropping antagonists, especially predators and ectoparasites. Female frog‐biting midges (Diptera: Corethrellidae) are known to use male anuran advertisement calls to locate their blood hosts, frogs. Here, we use acoustic midge traps broadcasting synthetic and recorded calls to identify those frog call parameters that affect midge attraction. At our study site in Pacific lowland Costa Rica, we found that overall midge attraction was influenced by both spectral and temporal acoustic parameters. Low dominant frequencies (below 1 kHz) and short pulse durations (between 125 and 500 ms) attracted the highest numbers of midges in tests with synthetic sinusoidal pure tones. These preferences partially explained the relative attractiveness of the advertisement calls of ten local frog species. The advertisement calls of the common and widespread Giant Bullfrog, Leptodactylus savagei (Anura: Leptodactylidae), attracted by far the largest number of midges, suggesting that this frog species might be a key resource for frog‐biting midges in Costa Rica. Although we found that calls of different frog species attracted different midge species/morphospecies in statistically different proportions, acoustic niche differentiation among midge species appeared to be moderate, suggesting either a limited degree of host specialization or the use of additional short‐range, that is, chemical, host recognition cues.     

Allometric escape from acoustic constraints is rare for frog calls

Allometric constraint is a product of natural selection and physical laws, particularly with respect to body size and traits constrained by properties thereof, such as metabolism, longevity, and vocal frequency. Allometric relationships are often conserved across lineages, indicating that physical constraints dictate scaling patterns in deep time, despite substantial genetic and ecological divergence among organisms. In particular, acoustic allometry (sound frequency ~ body size) is conserved across frogs, in defiance of massive variation in both body size and frequency. Here, we ask how many instances of allometric escape have occurred across the frog tree of life using a Bayesian framework that estimates the location, number, and magnitude of shifts in the adaptive landscape of acoustic allometry. Moreover, we test whether ecology in terms of calling site could affect these relationships. We find that calling site has a major influence on acoustic allometry. Despite this, we identify only four major instances of allometric escape, potentially deriving from ecomorphological adaptations to new signal modalities. In these instances of allometric escape, the optima and strength of the scaling relationship are different than expected for most other frog species, representing new adaptive regimes of body size ~ call frequency. Allometric constraints on frog calls are highly conserved and have rarely allowed escape, despite frequent invasions of new adaptive regimes and dramatic ecomorphological divergence. Our results highlight the rare instances in which natural and sexual selection combined can overcome physical constraints on sound production.     

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.     

Hearing is not necessarily believing in nocturnal anurans

The recent discovery of the use of visual cues for mate choice by nocturnal acoustic species raises the important, and to date unaddressed, question of how these signals affect the outcome of mate choice predicted by female preference for male calls. In order to address this question, we presented female Hyla arborea tree frogs with a series of choices between combinations of acoustic and visual cues of varying quality in nocturnal conditions. While females exhibited the expected preference for a combination of attractive values for visual and acoustic signals over combinations of unattractive values for both signals, when presented with conflicting acoustic and visual cues, they equally adopted one of two strategies, preferring either attractive calls or intense vocal sac coloration. This constitutes novel evidence that the outcome of mate choice, as predicted on the basis of male calling quality, can be drastically different when additional communication modalities—in this case vision—are taken into account. These results also highlight the possible existence of individual variation in female rules for cue prioritization. The implications of these results for the study of mate choice in nocturnal acoustic species are discussed.     

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.     

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.     

Polyploids with different origins and ancestors form a single sexual polyploid species

Polyploidization is one of the few mechanisms that can produce instantaneous speciation. Multiple origins of tetraploid lineages from the same two diploid progenitors are common, but here we report the first known instance of a single tetraploid species that originated repeatedly from at least three diploid ancestors. Parallel evolution of advertisement calls in tetraploid lineages of gray tree frogs has allowed these lineages to interbreed, resulting in a single sexually interacting polyploid species despite the separate origins of polyploids from different diploids. Speciation by polyploidization in these frogs has been the source of considerable debate, but the various published hypotheses have assumed that polyploids arose through either autopolyploidy or allopolyploidy of extant diploid species. We utilized molecular markers and advertisement calls to infer the origins of tetraploid gray tree frogs. Previous hypotheses did not sufficiently account for the observed data. Instead, we found that tetraploids originated multiple times from extant diploid gray tree frogs and two other, apparently extinct, lineages of tree frogs. Tetraploid lineages then merged through interbreeding to result in a single species. Thus, polyploid species may have complex origins, especially in systems in which isolating mechanisms (such as advertisement calls) are affected directly through hybridization and polyploidy.     

The Ability of Three Species of Tadpoles to Differentiate among Potential Fish Predators

The ability of prey to respond to novel predator cues may depend on the generality or specificity of the response to predator cues. We used laboratory behavioral experiments to examine the ability of tadpoles of three species of anurans (American toad, Bufo americanus ; bullfrog, Rana catesbeiana ; and green frog, R. clamitans ) to respond to the presence of two native potential predators (bluegill, Lepomis macrochirus ; and largemouth bass, Micropterus salmoides ) and one non-native potential predator (goldfish, Carassius auratus ). We also examined the effect of tadpole size on the behavioral responses of American toads and green frogs to predator cues. All three species of tadpoles responded to the presence of predator cues, although the specific responses varied among species. American toads and green frogs reduced activity in the presence of at least some fish cues, but bullfrog tadpoles did not change their activity. Bullfrogs decreased use of vegetation in the presence of some predator cues, whereas American toads and green frogs did not. American toads only responded to the presence of bluegill cues but not the other fish predator cues, whereas bullfrogs and green frogs responded more generally to the fish predators. In both American toads and green frogs, tadpole size affected behavior. For American toads, activity increased, as did the use of the vegetated side of the aquarium, in larger tadpoles. Not only did size affect American toad behavior, but it also influenced the responses of the tadpoles to predator cues. For green frogs, activity decreased in larger tadpoles. Our results suggest that behavioral responses of tadpoles to predator cues can be influenced by both the identity of the predator and the prey, as well as the size of the potential prey.     

Antipredator Behavioral Responses of Native and Exotic Tadpoles to Novel Predator

Factors related to the invasion process, such as high abundance of invaders, residence time, and functional distinctiveness, are well documented, but less attention has been given to the effects of antipredator strategy of invasive species during colonization. In this study, we explored the antipredator strategy of an introduced species by comparing the predator avoidance behaviors of two native anuran species and one introduced("exotic") species in the presence of different predators. The two native anuran species used in the study were Black-spotted Pond Frog Rana nigromaculata and Terrestrial Frog Rana limnocharis. The introduced(invasive) species used was American bullfrog Lithobates catesbeianus. Chinese pond turtle Chinemys reevesii, Red-backed rat snake Elaphe rufodorsata, and Big-headed turtle Platysternon megacephalum were used as predator species. Chinese pond turtles and Red-backed rat snakes are native predators of Black-spotted Pond Frogs and Terrestrial Frogs, while Big-headed turtles are novel("unfamiliar") to the two frogs. All three predator species are novel("unfamiliar") to the American bullfrog. The results show that tadpoles of the two native species displayed behaviors of recognizing the two native predators, but did not display the capability of identifying the novel predator. Results from our study also suggest that American bullfrog tadpoles exhibited strong antipredator behavioral responses by displaying the capability of identifying "unfamiliar" predators without cohabitation history and prior exposure to them. Such antipredator behavioral responses could have resulted in more favorable outcomes for an invading species during the invasive introductory process.     

Variation in anti-parasite behaviour and infection among larval amphibian species

Along with immune defences, many animals exhibit effective anti-parasite behaviours such as parasite avoidance and removal that influence their susceptibility to infection. Host ecology and life history influence investment into comparatively fixed defences such as innate immunity but may affect the strength of anti-parasite behaviours as well. We investigated activity levels in five different species of larval amphibian with varying life histories and ecology in control, novel food stimulus, and trematode parasite (Echinoparyphium sp.) threat conditions. There was a significant interaction of species and treatment given that American toad (Bufo americanus), wood frog (Lithobates sylvaticus), and bullfrog (Lithobates catesbeianus) tadpoles generally increased their activity when parasite infectious stages were present while grey tree frogs (Hyla versicolor) and northern leopard frogs (Lithobates pipiens) did not, even though activity was negatively related to infection. In addition, there was considerable variation among species in their susceptibility to parasitism, with infection prevalence ranging from 17 % in bullfrog tadpoles to 70 % in wood frogs. However, amphibian life history (larval and adult traits) was not related to parasitism or level of anti-parasite behaviour at the species level. Consequently, we suggest that future investigations include more species with a range of life history traits and also consider host ecology, particularly if conspicuous anti-parasite behaviours are more likely in amphibian species that experience a relatively low risk of predation.     

Males of <Emphasis Type="Italic">Hypsiboas goianus</Emphasis> (Anura; Hylidae) do not assess neighbor fighting ability through acoustic interactions

In frogs, acoustic signals are the most important communication mechanism, since they may be used in several social contexts. In many anurans, the dominant frequency of calls is negatively related to body size, and in such species, this spectral parameter may be considered a good predictor of fighting ability. We experimentally investigated the vocal behavior of 30 male Hypsiboas goianus in central Brazil to answer the following questions: (1) Do males change the acoustic parameters of their calls in response to conspecific intruders? and (2) Does the acoustic behavior of H. goianus depend on the simulated body size of their opponent? We used playback of synthesized calls with high (3573 Hz) and low (3123 Hz) dominant frequency to simulate small and large males, respectively. Males reduced the rate of advertisement calling in response to playback but did not change vocal behavior in response to low-frequency and high-frequency playback. So, while males adjust their calling activity in response to simulated conspecifics, there was no evidence that they assess the fighting ability of their opponents through acoustic interactions.     

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.     

Stream Noise,Hybridization, and Uncoupled Evolution of Call Traits in Two Lineages of Poison Frogs: Oophaga histrionica and Oophaga lehmanni

According to the acoustic adaptation hypothesis, communication signals are evolutionary shaped in a way that minimizes its degradation and maximizes its contrast against the background noise. To compare the importance for call divergence of acoustic adaptation and hybridization, an evolutionary force allegedly promoting phenotypic variation, we compared the mate recognition signal of two species of poison frogs (Oophaga histrionica and O. lehmanni) at five localities: two (one per species) alongside noisy streams, two away from streams, and one interspecific hybrid. We recorded the calls of 47 males and characterized the microgeographic variation in their spectral and temporal features, measuring ambient noise level, body size, and body temperature as covariates. As predicted, frogs living in noisy habitats uttered high frequency calls and, in one species, were much smaller in size. These results support a previously unconsidered role of noise on streams as a selective force promoting an increase in call frequency and pleiotropic effects in body size. Regarding hybrid frogs, their calls overlapped in the signal space with the calls of one of the parental lineages. Our data support acoustic adaptation following two evolutionary routes but do not support the presumed role of hybridization in promoting phenotypic diversity.     

中国43种蛙类鸣声特征数据集

无尾两栖动物的鸣声通常具有物种特异性,了解其鸣声特征信息,是利用生物声学进行物种多样性调查及物种监测的前提。本文汇总、整理了2012–2020年间利用高保真录音设备在野外记录的43种(隶属于7科26属)无尾两栖动物的鸣声数据,以及相应的鸣声采集信息。对音频文件进行降噪处理后,提供了由61个鸣声的波形图及语图组成的鸣声特征数据集。本数据集展示了鸣声的多种时域和频域信息,如单音节或多音节、音节数、音节时长、音节间隔、鸣声时长、主频、基频、谐波等,为我国无尾两栖类的声学研究、物种多样性调查及鸣声监测提供了数据支持。     

Beyond the river: underlying determinants of population acoustic signal variability in Amazonian direct-developing Allobates (Anura: Dendrobatoidea)

The multidimensional nature of animal signals makes acoustic traits potentially subject to different determinants. The Amazonian frogs Allobates nidicola and Allobates masniger have an allopatric distribution, occurring along the left and right sides of the Madeira River, respectively. These are two sister, phenotypically similar species whose eggs are deposited and develop entirely in a terrestrial nest. In this study, we analyzed 2,000 advertisement calls recorded from ten localities across Central Amazonia, in order to understand the role of determinants of acoustic signal variability at the population and species levels. We assessed, through nested analyses of variance, the differentiation of six characters of this sexual signal among populations and between interfluves. Moreover, we measured the degree of variability and the extent of temperature- and body size-induced plasticity in call traits. We also tested for isolation-by-distance effects in phenotypic differentiation through Mantel tests. Coefficients of variation were higher among than within populations for all call measurements. Spectral call properties were more distinctive than temporal traits among populations and species. Advertisement call traits showed strong temperature-induced plasticity (e.g., 45?% of the variation in note duration). In contrast, the effects of body size were restricted to frequency-related characters. The river barrier effect was significant among all the acoustic variables analyzed even after controlling for male body size. Geography (sampling locality) and body size also jointly affected call variability. No correlation between geographical and acoustic distances among populations was observed, suggesting that local stabilizing selective pressures have an important role in the evolution of call differentiation.