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.     

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.     

BIOACOUSTIC PUBLICATIONS, 1989

ABSTRACT

Coruros Spalacopus cyanus, social fossorial rodents from Chile, use a complex acoustic repertoire with eleven different true vocalisations and one mechanical sound in various behavioural contexts. The complex of contact calls is particularly well differentiated. Juvenile coruros produced six true vocalisations of which four were structurally identical to adult calls. One vocalisation had components of two adult sounds and one occurred only in juvenile animals. Certain calls from the adult repertoire were lacking. The frequencies of sounds of juveniles were considerably higher than those of adults, with many sounds reaching the ultrasonic range. Nevertheless, pure ultrasonic sounds were not recorded.

The frequencies of the analysed sounds of coruros extended from 0.17 to 20.33 kHz with dominant frequency components between 0.17 and 10 kHz. The acoustic properties of calls are suitable for transmission above and below ground, thus providing further indirect evidence that coruros are not strictly confined to an underground way of life. Indeed, the great variability of frequency ranges, with lower frequencies always being included, reflects a specialisation for communication in variable acoustic environments.

The most distinctive and unique vocalisation of coruros is the long duration musical trilling (lasting up to two minutes), which is a long-distance call emitted in alarm and arousal contexts. Recordings of this call from natural burrows in the field in Chile showed similar structural features to vocalisations from captive colonies in the laboratory.

Our findings provide a further example of matching physical properties of vocalisations to the acoustic conditions of the habitat. However, vocalisations in subterranean rodents consist almost exclusively of short-distance calls, the trilling of coruros being the notable exception. Since the selective pressure of the acoustic environment upon the evolution of short-distance vocalisations is probably minimal, we suggest that during their evolution, subterranean mammals have matched their vocalisations primarily to their hearing range and not directly to the acoustics underground. Hearing probably has been the primary target of natural selection, serving not only for communication but also for detection of predators (and, in carnivores, of prey).     

Habitat type and density influence vocal signal design in satin bowerbirds

1. This study provided a thorough test of the acoustic adaptation hypothesis using a within-species comparison of call structure involving a wide range of habitat types, an objective measure of habitat density and direct measures of habitat-related attenuation. 2. The structure of the bower advertisement call of the satin bowerbird was measured in 16 populations from throughout the species' range and related to the habitat type and density at each site. Transmission of white noise, pure tones and different bowerbird dialects was measured in five of six habitat types inhabited by satin bowerbirds. 3. Bowerbird advertisement call structure converged in similar habitats but diverged among different habitats; this pattern was apparent at both continent-wide and local geographical scales. Bowerbirds' call structures differed with changes in habitat density, consistent with the acoustic adaptation hypothesis. Lower frequencies and less frequency modulation were utilized in denser habitats such as rainforest and higher frequencies and more frequency modulation were used in the more open eucalypt-dominated habitats. 4. The white noise and pure tone transmission measurements indicated that different habitats varied in their sound transmission properties in a manner consistent with the observed variation in satin bowerbird vocalizations. 5. There was no effect of geographical proximity of recording locations, nor was there the predicted inverse relationship between frequency and body size. 6. These findings indicate that the transmission qualities of different habitats have had a major influence on variation in vocal phenotypes in this species. In addition, previously published molecular data for this species suggest that there is no effect of genetic relatedness on call similarity among satin bowerbird populations.     

Variability in the mating calls of the Lusitanian toadfish Halobatrachus didactylus: cues for potential individual recognition

The mating sounds (boatwhistles) of nesting batrachoidid Halobatrachus didactylus males were recorded in the Tagus Estuary from piers. Thirteen males with 16 boatwhistles per fish were analysed for 20 acoustic features. All variables showed larger between‐male than within‐male variation and differed significantly among individuals. Discriminant function analyses (DFA) considering seven of these variables assigned 90–100% of boatwhistles to the correct individual, depending on the number of males and number of sounds per male included in the model. The acoustic features that consistently best discriminated individuals were the dominant frequency of the middle tonal segment of the boatwhistle (P₂) and dominant frequency modulation, followed by P₂ pulse period, amplitude modulation and sound duration. These results suggest the possibility of individual recognition based on acoustic cues.     

Oscillating gas bubbles as the origin of bowel sounds: a combined acoustic and imaging study

Bowel sounds have been speculated to stem from the movement of gas or a mixture in the bowel lumen, with gas as the major component. The exact role and the mechanism through which gas participates have not been elucidated. Video images of actively moving bubbles under either real-time ultrasonography (RU, n = 4) or videofluoroscopy (VF, n = 4) with synchronous sound recording were studied and a total of 24 bubbling bowel sounds (BBS's) were obtained. The physical dimensions and acoustic parameters of bubbles were analyzed. Freely oscillating bubbles were demonstrated clearly in both groups. Bubble radii ranged from 1.5 to 7.2 mm and frequencies from 258.3 to 1,078 Hz. The bubble frequency correlated inversely with the radius (P < 0.01). The relevant acoustic features and parameters of bubble dynamics further supported the identification of gas bubbles. Although the acoustic features seemed to be of minor clinical significance, increased number of clustering or fixed, repetitive pattern of occurrences might suggest a poorer prognosis. In summary, oscillating gas bubbles are capable of producing BBS's and may play a central role in this newly recognized model of bowel sound genesis. The patterns of BBS's may be of prognostic value in clinical application, underlining the need for further study.     

Acoustic localization of terrestrial wildlife: Current practices and future opportunities

Autonomous acoustic recorders are an increasingly popular method for low‐disturbance, large‐scale monitoring of sound‐producing animals, such as birds, anurans, bats, and other mammals. A specialized use of autonomous recording units (ARUs) is acoustic localization, in which a vocalizing animal is located spatially, usually by quantifying the time delay of arrival of its sound at an array of time‐synchronized microphones. To describe trends in the literature, identify considerations for field biologists who wish to use these systems, and suggest advancements that will improve the field of acoustic localization, we comprehensively review published applications of wildlife localization in terrestrial environments. We describe the wide variety of methods used to complete the five steps of acoustic localization: (1) define the research question, (2) obtain or build a time‐synchronizing microphone array, (3) deploy the array to record sounds in the field, (4) process recordings captured in the field, and (5) determine animal location using position estimation algorithms. We find eight general purposes in ecology and animal behavior for localization systems: assessing individual animals' positions or movements, localizing multiple individuals simultaneously to study their interactions, determining animals' individual identities, quantifying sound amplitude or directionality, selecting subsets of sounds for further acoustic analysis, calculating species abundance, inferring territory boundaries or habitat use, and separating animal sounds from background noise to improve species classification. We find that the labor‐intensive steps of processing recordings and estimating animal positions have not yet been automated. In the near future, we expect that increased availability of recording hardware, development of automated and open‐source localization software, and improvement of automated sound classification algorithms will broaden the use of acoustic localization. With these three advances, ecologists will be better able to embrace acoustic localization, enabling low‐disturbance, large‐scale collection of animal position data.     

Auditory Sketches: Very Sparse Representations of Sounds Are Still Recognizable

Sounds in our environment like voices, animal calls or musical instruments are easily recognized by human listeners. Understanding the key features underlying this robust sound recognition is an important question in auditory science. Here, we studied the recognition by human listeners of new classes of sounds: acoustic and auditory sketches, sounds that are severely impoverished but still recognizable. Starting from a time-frequency representation, a sketch is obtained by keeping only sparse elements of the original signal, here, by means of a simple peak-picking algorithm. Two time-frequency representations were compared: a biologically grounded one, the auditory spectrogram, which simulates peripheral auditory filtering, and a simple acoustic spectrogram, based on a Fourier transform. Three degrees of sparsity were also investigated. Listeners were asked to recognize the category to which a sketch sound belongs: singing voices, bird calls, musical instruments, and vehicle engine noises. Results showed that, with the exception of voice sounds, very sparse representations of sounds (10 features, or energy peaks, per second) could be recognized above chance. No clear differences could be observed between the acoustic and the auditory sketches. For the voice sounds, however, a completely different pattern of results emerged, with at-chance or even below-chance recognition performances, suggesting that the important features of the voice, whatever they are, were removed by the sketch process. Overall, these perceptual results were well correlated with a model of auditory distances, based on spectro-temporal excitation patterns (STEPs). This study confirms the potential of these new classes of sounds, acoustic and auditory sketches, to study sound recognition.     

The acoustic repertoire of the Southern right whale,a quantitative analysis

Some 1274 southern right whale sounds were randomly selected and each sound was described by 10 acoustic variables. Two hundred and fifty of these sounds were also ‘labelled’ by the activity, size and sexual composition o the group producing them. Principal components analysis was performed on all the sounds' variables (1274×10) and on the variables for a subset of 823 sounds referred to as calls. Results of the principal components analyses indicate that the sounds can be divided into three major classes: blow sounds, slaps, and calls; and that the repertoire of calls is a continuum with certain types more common than others. The distribution of the ‘labelled’ sounds in the principal components analyses patterns revealed general associations between whale activities and the types of sounds produced.     

Acoustic indicators for mapping infestation probabilities of soil invertebrates

Acoustic and traditional excavation methods were used in consecutive summers to conduct two geospatial surveys of distributions of white grubs and other soil invertebrates in two forage fields. Indicator variables were constructed from listener- and computer-based assessments of sounds detected at each recording site and then applied in geostatistical analysis, contingency analysis, and spatial analysis of distance indices (SADIE) of soil invertebrate distributions. Significant relationships were identified between the acoustic indicators and the counts of sound-producing soil invertebrates in a majority of the geostatistical and contingency analyses. Significant clusterings and overall spatial associations were identified also in most of the SADIE analyses. In addition, significant local spatial associations were identified between acoustic indicators and counts of sound-producing soil invertebrates that could be of potential value in selection of specific sites as targets for treatment or for untreated reserves in integrated pest management programs. An example is presented of the relative efficiency of acoustic surveys for targeting of white grub treatments.     

The utility of a long‐term acoustic recording system for detecting white seabass Atractoscion nobilis spawning sounds

This study reports the use of a long‐term acoustic recording system (LARS) to remotely monitor white seabass Atractoscion nobilis spawning sounds at three sites along the southern California coastline, adjacent to Camp Pendleton. On the basis of previous studies of A. nobilis sound production relative to periods of known spawning activity, LARS were set to continuously record ambient sounds for a 2 h period around sunset from April to June 2009. Acoustic analyses identified A. nobilis courtship sounds on 89, 28 and 45% of the days at the three locations, respectively. From 474 h of acoustic data, spawning‐related sounds (chants) were detected on 19 occasions in 2009 with an additional 11 spawning chants recorded during a 2007 validation period. Most spawning chants occurred within 30 min of sunset during the months of May and June at a mean ±s.d . surface temperature of 18·2 ± 1·2° C. Consecutive daily spawning activity was not apparent at any sites in 2009. Atractoscion nobilis spawning chants were recorded at all three sites, suggesting that shallow rocky reefs which support kelp forests provide suitable A. nobilis spawning habitat. Results confirm the utility of passive acoustic recorders for identifying A. nobilis spawning periods and locations.     

Call Transmission Efficiency in Native and Invasive Anurans: Competing Hypotheses of Divergence in Acoustic Signals

Invasive species are a leading cause of the current biodiversity decline, and hence examining the major traits favouring invasion is a key and long-standing goal of invasion biology. Despite the prominent role of the advertisement calls in sexual selection and reproduction, very little attention has been paid to the features of acoustic communication of invasive species in nonindigenous habitats and their potential impacts on native species. Here we compare for the first time the transmission efficiency of the advertisement calls of native and invasive species, searching for competitive advantages for acoustic communication and reproduction of introduced taxa, and providing insights into competing hypotheses in evolutionary divergence of acoustic signals: acoustic adaptation vs. morphological constraints. Using sound propagation experiments, we measured the attenuation rates of pure tones (0.2–5 kHz) and playback calls (Lithobates catesbeianus and Pelophylax perezi) across four distances (1, 2, 4, and 8 m) and over two substrates (water and soil) in seven Iberian localities. All factors considered (signal type, distance, substrate, and locality) affected transmission efficiency of acoustic signals, which was maximized with lower frequency sounds, shorter distances, and over water surface. Despite being broadcast in nonindigenous habitats, the advertisement calls of invasive L. catesbeianus were propagated more efficiently than those of the native species, in both aquatic and terrestrial substrates, and in most of the study sites. This implies absence of optimal relationship between native environments and propagation of acoustic signals in anurans, in contrast to what predicted by the acoustic adaptation hypothesis, and it might render these vertebrates particularly vulnerable to intrusion of invasive species producing low frequency signals, such as L. catesbeianus. Our findings suggest that mechanisms optimizing sound transmission in native habitat can play a less significant role than other selective forces or biological constraints in evolutionary design of anuran acoustic signals.     

Geographical variation in sound production in the anemonefish Amphiprion akallopisos

Because of pelagic-larval dispersal, coral-reef fishes are distributed widely with minimal genetic differentiation between populations. Amphiprion akallopisos, a clownfish that uses sound production to defend its anemone territory, has a wide but disjunct distribution in the Indian Ocean. We compared sounds produced by these fishes from populations in Madagascar and Indonesia, a distance of 6500 km. Differentiation of agonistic calls into distinct types indicates a complexity not previously recorded in fishes' acoustic communication. Moreover, various acoustic parameters, including peak frequency, pulse duration, number of peaks per pulse, differed between the two populations. The geographic comparison is the first to demonstrate 'dialects' in a marine fish species, and these differences in sound parameters suggest genetic divergence between these two populations. These results highlight the possible approach for investigating the role of sounds in fish behaviour in reproductive divergence and speciation.     

Comparison of manual and automated methods for identifying target sounds in audio recordings of Pileated, Pale-billed, and putative Ivory-billed woodpeckers

ABSTRACT.   Although offering many benefits over manual recording and survey techniques for avian field studies, automated sound recording systems produce large datasets that must be carefully examined to locate sounds of interest. We compared two methods for locating target sounds in continuous sound recordings: (1) a manual method using computer software to provide a visual representation of the recording as a sound spectrogram and (2) an automated method using sound analysis software preprogrammed to identify specific target sounds. For both methods, we examined the time required to process a 24-h recording, scanning accuracy, and scanning comprehensiveness using four different target sounds of Pileated Woodpeckers ( Dryocopus pileatus ), Pale-billed Woodpeckers ( Campephilus guatemalensis ), and putative Ivory-billed Woodpeckers ( Campehilus principalis ). We collected recordings from the bottomland forests of Florida and the Neotropical dry forests of Costa Rica, and compared manual versus automated cross-correlation scanning techniques. The automated scanning method required less time to process sound recordings, but made more false positive identifications and was less comprehensive than the manual method, identifying significantly fewer target sounds. Although the automated scanning method offers a fast and economic alternative to traditional manual efforts, our results indicate that manual scanning is best for studies requiring an accurate account of temporal patterns in call frequency and for those involving birds with low vocalization rates.     

Contributions of MIR to Soundscape Ecology. Part 2: Spectral timbral analysis for discriminating soundscape components

Soundscape ecology evaluates biodiversity and environmental disturbances by investigating the interaction among soundscape components (biological, geophysical, and human-produced sounds) using data collected with autonomous recording units. Current analyses consider the acoustic properties of frequency and amplitude resulting in varied metrics, but rarely focus on the discrimination of soundscape components. Computational musicologists analyze similar data but consider a third acoustic property, timbre.Here, we investigated the effectiveness of spectral timbral analysis to distinguish among dominant soundscape components. This process included manually labeling and extracting spectral timbral features for each recording. Then, we tested classification accuracy with linear and quadratic discriminant analyses on combinations of spectral timbral features.Different spectral timbral feature groups distinguished between biological, geophysical, and manmade sounds in a single field recording. Furthermore, as we tested different combinations of spectral timbral features that resulted in both high and very low accuracy results, we found that they could be ordered to “sift” out field recordings by individual dominant soundscape component.By using timbre as a new acoustic property in soundscape analyses, we could classify dominant soundscape components effectively. We propose further investigation into a sifting scheme that may allow researchers to focus on more specific research questions such as understanding changes in biodiversity, discriminating by taxonomic class, or to inspect weather-related events.     

Probing real sensory worlds of receivers with unsupervised clustering

The task of an organism to extract information about the external environment from sensory signals is based entirely on the analysis of ongoing afferent spike activity provided by the sense organs. We investigate the processing of auditory stimuli by an acoustic interneuron of insects. In contrast to most previous work we do this by using stimuli and neurophysiological recordings directly in the nocturnal tropical rainforest, where the insect communicates. Different from typical recordings in sound proof laboratories, strong environmental noise from multiple sound sources interferes with the perception of acoustic signals in these realistic scenarios. We apply a recently developed unsupervised machine learning algorithm based on probabilistic inference to find frequently occurring firing patterns in the response of the acoustic interneuron. We can thus ask how much information the central nervous system of the receiver can extract from bursts without ever being told which type and which variants of bursts are characteristic for particular stimuli. Our results show that the reliability of burst coding in the time domain is so high that identical stimuli lead to extremely similar spike pattern responses, even for different preparations on different dates, and even if one of the preparations is recorded outdoors and the other one in the sound proof lab. Simultaneous recordings in two preparations exposed to the same acoustic environment reveal that characteristics of burst patterns are largely preserved among individuals of the same species. Our study shows that burst coding can provide a reliable mechanism for acoustic insects to classify and discriminate signals under very noisy real-world conditions. This gives new insights into the neural mechanisms potentially used by bushcrickets to discriminate conspecific songs from sounds of predators in similar carrier frequency bands.     

饲养状态真鲂(鱼弗)发声的昼夜与季节变化

本文研究了受水温和光周期等自然变化影响的饲养状态真鲂鮄发声的昼夜与季节变化,并研究了实验鱼活动(鱼类游泳次数)的日变化。声音信号的昼夜节律记录发声活动的日常水平(摄食之外的时期),但是每月变化的记录(季节性式型)则在摄食期间进行,因为摄食时声音信号增加,而日常发声活动较不频繁。实验鱼包括雌雄两性,且未达性成熟。真鲂鮄在白天发声多一些,也更活跃。声音为阵发式的,较不频繁(平均值=0.04发声/min每鱼每天)。最少的发声活动出现在晚上,凌晨和黄昏居中(声音的阵发更频繁,但是声音更少),最多的发声活动出现在白天(声音的阵发更频繁,并且含更多数目的声音)。竞争摄食时声音信号的比率不呈现季节性变化(平均值=3.98发声/min每鱼),与温度也不相关,显示出竞争摄食时声音的发出以最大比率进行。敲击声和呼噜声的某些声学特征与温度相关,特别是在较高的温度下呼噜声的节拍间隔急剧下降。敲击声和呼噜声的声音参数中的季节性变化,多数可以解释为发声肌肉和中央声音控制回路的温度效应。     

A test of the Acoustic Adaptation Hypothesis in three types of tropical forest: degradation of male and female Rufous-and-white Wren songs

Many animals produce complex vocalizations that show pronounced variation between populations. The Acoustic Adaptation Hypothesis helps to explain this variation, suggesting that acoustic signals are optimized for transmission through different environments. Little is known about the transmission properties of female vocalizations because most studies of the Acoustic Adaptation Hypothesis have focused on male vocalizations of organisms living at temperate latitudes. We explored the relationship between environmental variation and the transmission properties of songs of Rufous-and-white Wrens, resident Neotropical songbirds where both sexes sing. Using playback, we broadcast and re-recorded elements of male and female songs from three populations of wrens living in three different forest habitats in Costa Rica. We measured four variables of the re-recorded sounds: signal-to-noise ratio, excess attenuation, tail-to-signal ratio and blur ratio. Our results show a significant difference between transmission characteristics of both male and female song elements across the three habitats, indicating that sounds transmit differently through different types of tropical forest. The population from which the broadcast sounds were recorded (source population) had little effect on sound transmission, however, suggesting that acoustic differences between these populations may not arise through acoustic adaptation to these habitats. Male and female elements showed similar transmission properties overall, although signal-to-noise ratio of male elements was influenced by source population, whereas blur ratio and excess attenuation of female elements were influenced by source population. Our study highlights the differences in transmission characteristics of animal sounds through different habitats, and reveals some sex differences in transmission properties.     

Sound transmission and directional hearing in field crickets: neurophysiological studies outdoors

Many studies provide detailed behavioural and neurophysiological information on the ability of crickets to localize a sound source under ideal acoustic conditions, but very little is known about how they perform in real habitats. We investigated directional hearing of crickets in the field using a neurophysiological approach, by recording the activity of the two prominent, bilaterally homologous AN1 neurons simultaneously in a cricket’s habitat. The discharge and latency differences of the pair of neurons in response to conspecific chirps presented at different distances and directions were taken as a measure of directional information. The maximum hearing distance differed between individuals and weather conditions from 1 to 15 m (mean 9.2 m). Although the AN1 activity generally decreased with increasing distance, large fluctuations in the magnitude of responses occurred with distance, indicating that the intensity gradient over distance is often irregular. The directional information provided in the discharge differences of the two neurons also varied with distance. Again, there was no simple directional gradient on the transmission channel; rather, with decreasing distance to the source there were receiver locations providing suprathreshold responses, but no directional information. The consequences for the ability of field crickets to communicate acoustically close to the ground are discussed.