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1.  Real estate ads in Emei music frog vocalizations: female preference for calls emanating from burrows 
Biology Letters  2011;8(3):337-340.
During female mate choice, both the male's phenotype and resources (e.g. his nest) contribute to the chooser's fitness. Animals other than humans are not known to advertise resource characteristics to potential mates through vocal communication; although in some species of anurans and birds, females do evaluate male qualities through vocal communication. Here, we demonstrate that calls of the male Emei music frog (Babina dauchina), vocalizing from male-built nests, reflect nest structure information that can be recognized by females. Inside-nest calls consisted of notes with energy concentrated at lower frequency ranges and longer note durations when compared with outside-nest calls. Centre frequencies and note durations of the inside calls positively correlate with the area of the burrow entrance and the depth of the burrow, respectively. When given a choice between outside and inside calls played back alternately, more than 70 per cent of the females (33/47) chose inside calls. These results demonstrate that males of this species faithfully advertise whether or not they possess a nest to potential mates by vocal communication, which probably facilitates optimal mate selection by females. These results revealed a novel function of advertisement calls, which is consistent with the wide variation in both call complexity and social behaviour within amphibians.
PMCID: PMC3367746  PMID: 22158736
sexual selection; sound communication; mate choice; burrowing frog; phonotaxis tests
2.  Bioacoustic Field Research: A Primer to Acoustic Analyses and Playback Experiments With Primates 
American Journal of Primatology  2013;75(7):643-663.
Acoustic analyses of primate vocalizations as well as playback experiments are staple methods in primatology. Acoustic analyses have been used to investigate the influence of factors such as individuality, context, sex, age, and size on variation in calls. More recent studies have expanded our knowledge on the effects of phylogenetic relatedness and the structure of primate vocal repertoires in general. Complementary playback experiments allow direct testing of hypotheses regarding the attribution of meaning to calls, the cognitive mechanisms underpinning responses, and/or the adaptive value of primate behavior. After briefly touching on the historical background of this field of research, we first provide an introduction to recording primate vocalizations and discuss different approaches to describe primate calls in terms of their temporal and spectral properties. Second, we present a tutorial regarding the preparation, execution, and interpretation of field playback experiments, including a review of studies that have used such approaches to investigate the responses to acoustic variation in calls including the integration of contextual and acoustic information, recognition of kin and social relationships, and social knowledge. Based on the review of the literature and our own experience, we make a number of recommendations regarding the most common problems and pitfalls. The power of acoustic analyses typically hinges on the quality of the recordings and the number of individuals represented in the sample. Playback experiments require profound knowledge of the natural behavior of the animals for solid interpretation; experiments should be conducted sparingly, to avoid habituation of the subjects to the occurrence of the calls; experimenter-blind designs chosen whenever possible; and researchers should brace themselves for long periods of waiting times until the appropriate moments to do the experiment arise. If all these aspects are considered, acoustic analyses and field playback experiments provide unique insights into primate communication and cognition. Am. J. Primatol. 75:643–663, 2013. © 2013 Wiley Periodicals, Inc.
PMCID: PMC3698702  PMID: 23592340
acoustic analysis; alarm calls; cognition; communication; playback experiments
3.  Whispering to the Deaf: Communication by a Frog without External Vocal Sac or Tympanum in Noisy Environments 
PLoS ONE  2011;6(7):e22080.
Atelopus franciscus is a diurnal bufonid frog that lives in South-American tropical rain forests. As in many other frogs, males produce calls to defend their territories and attract females. However, this species is a so-called “earless” frog lacking an external tympanum and is thus anatomically deaf. Moreover, A. franciscus has no external vocal sac and lives in a sound constraining environment along river banks where it competes with other calling frogs. Despite these constraints, male A. franciscus reply acoustically to the calls of conspecifics in the field. To resolve this apparent paradox, we studied the vocal apparatus and middle-ear, analysed signal content of the calls, examined sound and signal content propagation in its natural habitat, and performed playback experiments. We show that A. franciscus males can produce only low intensity calls that propagate a short distance (<8 m) as a result of the lack of an external vocal sac. The species-specific coding of the signal is based on the pulse duration, providing a simple coding that is efficient as it allows discrimination from calls of sympatric frogs. Moreover, the signal is redundant and consequently adapted to noisy environments. As such a coding system can be efficient only at short-range, territory holders established themselves at short distances from each other. Finally, we show that the middle-ear of A. franciscus does not present any particular adaptations to compensate for the lack of an external tympanum, suggesting the existence of extra-tympanic pathways for sound propagation.
PMCID: PMC3135622  PMID: 21779377
4.  Multimodal signaling in the Small Torrent Frog (Micrixalus saxicola) in a complex acoustic environment 
Behavioral Ecology and Sociobiology  2013;67(9):1449-1456.
Many animals use multimodal (both visual and acoustic) components in courtship signals. The acoustic communication of anuran amphibians can be masked by the presence of environmental background noise, and multimodal displays may enhance receiver detection in complex acoustic environments. In the present study, we measured sound pressure levels of concurrently calling males of the Small Torrent Frog (Micrixalus saxicola) and used acoustic playbacks and an inflatable balloon mimicking a vocal sac to investigate male responses to controlled unimodal (acoustic) and multimodal (acoustic and visual) dynamic stimuli in the frogs’ natural habitat. Our results suggest that abiotic noise of the stream does not constrain signal detection, but males are faced with acoustic interference and masking from conspecific chorus noise. Multimodal stimuli elicited greater response from males and triggered significantly more visual signal responses than unimodal stimuli. We suggest that the vocal sac acts as a visual cue and improves detection and discrimination of acoustic signals by making them more salient to receivers amidst complex biotic background noise.
PMCID: PMC3742427  PMID: 23956486
Anura; Acoustic signal; Background noise; Multimodal communication; Visual cue; Vocal sac
5.  How Noisy Does a Noisy Miner Have to Be? Amplitude Adjustments of Alarm Calls in an Avian Urban ‘Adapter’ 
PLoS ONE  2012;7(1):e29960.
Urban environments generate constant loud noise, which creates a formidable challenge for many animals relying on acoustic communication. Some birds make vocal adjustments that reduce auditory masking by altering, for example, the frequency (kHz) or timing of vocalizations. Another adjustment, well documented for birds under laboratory and natural field conditions, is a noise level-dependent change in sound signal amplitude (the ‘Lombard effect’). To date, however, field research on amplitude adjustments in urban environments has focused exclusively on bird song.
We investigated amplitude regulation of alarm calls using, as our model, a successful urban ‘adapter’ species, the Noisy miner, Manorina melanocephala. We compared several different alarm calls under contrasting noise conditions.
Individuals at noisier locations (arterial roads) alarm called significantly more loudly than those at quieter locations (residential streets). Other mechanisms known to improve sound signal transmission in ‘noise’, namely use of higher perches and in-flight calling, did not differ between site types. Intriguingly, the observed preferential use of different alarm calls by Noisy miners inhabiting arterial roads and residential streets was unlikely to have constituted a vocal modification made in response to sound-masking in the urban environment because the calls involved fell within the main frequency range of background anthropogenic noise.
The results of our study suggest that a species, which has the ability to adjust the amplitude of its signals, might have a ‘natural’ advantage in noisy urban environments.
PMCID: PMC3251594  PMID: 22238684
6.  Divergence of Acoustic Signals in a Widely Distributed Frog: Relevance of Inter-Male Interactions 
PLoS ONE  2014;9(1):e87732.
Divergence of acoustic signals in a geographic scale results from diverse evolutionary forces acting in parallel and affecting directly inter-male vocal interactions among disjunct populations. Pleurodema thaul is a frog having an extensive latitudinal distribution in Chile along which males' advertisement calls exhibit an important variation. Using the playback paradigm we studied the evoked vocal responses of males of three populations of P. thaul in Chile, from northern, central and southern distribution. In each population, males were stimulated with standard synthetic calls having the acoustic structure of local and foreign populations. Males of both northern and central populations displayed strong vocal responses when were confronted with the synthetic call of their own populations, giving weaker responses to the call of the southern population. The southern population gave stronger responses to calls of the northern population than to the local call. Furthermore, males in all populations were stimulated with synthetic calls for which the dominant frequency, pulse rate and modulation depth were varied parametrically. Individuals from the northern and central populations gave lower responses to a synthetic call devoid of amplitude modulation relative to stimuli containing modulation depths between 30–100%, whereas the southern population responded similarly to all stimuli in this series. Geographic variation in the evoked vocal responses of males of P. thaul underlines the importance of inter-male interactions in driving the divergence of the acoustic traits and contributes evidence for a role of intra-sexual selection in the evolution of the sound communication system of this anuran.
PMCID: PMC3905042  PMID: 24489957
7.  Call Transmission Efficiency in Native and Invasive Anurans: Competing Hypotheses of Divergence in Acoustic Signals 
PLoS ONE  2013;8(10):e77312.
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.
PMCID: PMC3796471  PMID: 24155940
8.  Divergent Receiver Responses to Components of Multimodal Signals in Two Foot-Flagging Frog Species 
PLoS ONE  2013;8(1):e55367.
Multimodal communication of acoustic and visual signals serves a vital role in the mating system of anuran amphibians. To understand signal evolution and function in multimodal signal design it is critical to test receiver responses to unimodal signal components versus multimodal composite signals. We investigated two anuran species displaying a conspicuous foot-flagging behavior in addition to or in combination with advertisement calls while announcing their signaling sites to conspecifics. To investigate the conspicuousness of the foot-flagging signals, we measured and compared spectral reflectance of foot webbings of Micrixalus saxicola and Staurois parvus using a spectrophotometer. We performed behavioral field experiments using a model frog including an extendable leg combined with acoustic playbacks to test receiver responses to acoustic, visual and combined audio-visual stimuli. Our results indicated that the foot webbings of S. parvus achieved a 13 times higher contrast against their visual background than feet of M. saxicola. The main response to all experimental stimuli in S. parvus was foot flagging, whereas M. saxicola responded primarily with calls but never foot flagged. Together these across-species differences suggest that in S. parvus foot-flagging behavior is applied as a salient and frequently used communicative signal during agonistic behavior, whereas we propose it constitutes an evolutionary nascent state in ritualization of the current fighting behavior in M. saxicola.
PMCID: PMC3558420  PMID: 23383168
9.  Bat echolocation calls: adaptation and convergent evolution 
Bat echolocation calls provide remarkable examples of ‘good design’ through evolution by natural selection. Theory developed from acoustics and sonar engineering permits a strong predictive basis for understanding echolocation performance. Call features, such as frequency, bandwidth, duration and pulse interval are all related to ecological niche. Recent technological breakthroughs have aided our understanding of adaptive aspects of call design in free-living bats. Stereo videogrammetry, laser scanning of habitat features and acoustic flight path tracking permit reconstruction of the flight paths of echolocating bats relative to obstacles and prey in nature. These methods show that echolocation calls are among the most intense airborne vocalizations produced by animals. Acoustic tracking has clarified how and why bats vary call structure in relation to flight speed. Bats using broadband echolocation calls adjust call design in a range-dependent manner so that nearby obstacles are localized accurately. Recent phylogenetic analyses based on gene sequences show that particular types of echolocation signals have evolved independently in several lineages of bats. Call design is often influenced more by perceptual challenges imposed by the environment than by phylogeny, and provides excellent examples of convergent evolution. Now that whole genome sequences of bats are imminent, understanding the functional genomics of echolocation will become a major challenge.
PMCID: PMC1919403  PMID: 17251105
echolocation; bats; adaptation; convergent evolution
10.  Changes in breeding phenology of eastern Ontario frogs over four decades 
Ecology and Evolution  2013;3(4):835-845.
Global climate change has been implicated in phenological shifts for a variety of taxa. Amphibian species in particular are sensitive to changes in their environment due to their biphasic life history and restricted reproductive requirements. Previous research has shown that not all temperate amphibian species respond similarly to the same suite of climatic or environmental cues, nor are individual species necessarily uniform in their responses across their range. We examined both the timing of spring emergence and calling phenology of eight anuran species in southeastern Ontario, Canada, using an approximately 40-year dataset of historical records of amphibian activity. Rana pipiens was the only species out of eight considered to emerge significantly earlier, by an estimated 22 days over four decades. Both R. pipiens and Bufo americanus have advanced initiation of calling over a four-decade span significantly earlier by an estimated 37.2 and 19.2 days, respectively. Rana sylvatica showed a trend toward earlier emergence by 19 days, whereas we did not detect changes in emergence phenology for the remaining five species. This significant shift in breeding behavior for two species correlates to significant regional increases in spring temperatures of an estimated 2.7–2.8°C overall over four decades. Our study suggests that local temperature increases have affected the timing of emergence and the onset of calling activity in some Ontario anuran species. Global decline or range shifts ultimately may be related to changes in reproductive behavior and timing mediated by shifting climate.
PMCID: PMC3631398  PMID: 23610628
Anuran; calling activity; climate change; emergence; precipitation; reproductive timing; temperature
11.  Biological invasions and the acoustic niche: the effect of bullfrog calls on the acoustic signals of white-banded tree frogs 
Biology Letters  2012;8(5):714-716.
Invasive species are known to affect native species in a variety of ways, but the effect of acoustic invaders has not been examined previously. We simulated an invasion of the acoustic niche by exposing calling native male white-banded tree frogs (Hypsiboas albomarginatus) to recorded invasive American bullfrog (Lithobates catesbeianus) calls. In response, tree frogs immediately shifted calls to significantly higher frequencies. In the post-stimulus period, they continued to use higher frequencies while also decreasing signal duration. Acoustic signals are the primary basis of mate selection in many anurans, suggesting that such changes could negatively affect the reproductive success of native species. The effects of bullfrog vocalizations on acoustic communities are expected to be especially severe due to their broad frequency band, which masks the calls of multiple species simultaneously.
PMCID: PMC3440993  PMID: 22675139
invasive species; bioacoustics; noise pollution; Anura; Amphibia; Brazil
12.  Vocal communication in a complex multi-level society: constrained acoustic structure and flexible call usage in Guinea baboons 
Frontiers in Zoology  2013;10:58.
To understand the evolution of acoustic communication in animals, it is important to distinguish between the structure and the usage of vocal signals, since both aspects are subject to different constraints. In terrestrial mammals, the structure of calls is largely innate, while individuals have a greater ability to actively initiate or withhold calls. In closely related taxa, one would therefore predict a higher flexibility in call usage compared to call structure. In the present study, we investigated the vocal repertoire of free living Guinea baboons (Papio papio) and examined the structure and usage of the animals’ vocal signals. Guinea baboons live in a complex multi-level social organization and exhibit a largely tolerant and affiliative social style, contrary to most other baboon taxa. To classify the vocal repertoire of male and female Guinea baboons, cluster analyses were used and focal observations were conducted to assess the usage of vocal signals in the particular contexts.
In general, the vocal repertoire of Guinea baboons largely corresponded to the vocal repertoire other baboon taxa. The usage of calls, however, differed considerably from other baboon taxa and corresponded with the specific characteristics of the Guinea baboons’ social behaviour. While Guinea baboons showed a diminished usage of contest and display vocalizations (a common pattern observed in chacma baboons), they frequently used vocal signals during affiliative and greeting interactions.
Our study shows that the call structure of primates is largely unaffected by the species’ social system (including grouping patterns and social interactions), while the usage of calls can be more flexibly adjusted, reflecting the quality of social interactions of the individuals. Our results support the view that the primary function of social signals is to regulate social interactions, and therefore the degree of competition and cooperation may be more important to explain variation in call usage than grouping patterns or group size.
PMCID: PMC3849383  PMID: 24059742
Evolution; Vocal communication; Call structure; Call usage; Guinea baboon; Social complexity; Competition
13.  Why do shrews twitter? Communication or simple echo-based orientation 
Biology Letters  2009;5(5):593-596.
Shrews are very vocal animals. We tested behaviourally whether the high-pitched laryngeal ‘twittering’ calls of as-yet unclear function serve for communication or echo-based orientation. We used a representative species from each of the two largest phylogenetic groups of shrews. In both species, experimental manipulation of substrate density, but not of the likelihood of conspecific presence, affected the shrews' call rate when exploring an unknown environment. This adaptation of call rate to the degree of habitat clutter parallels bat echolocation and suggests that shrews may use the echoes and reverberations of their calls for identifying routes through their habitat or for probing habitat type. To assess the acoustic feasibility of shrew echo orientation, we ensonified shrew habitats in the field with an ‘artificial shrew’ (small speaker mounted close to a sensitive microphone). The data showed that shrew-like calls can indeed yield echo scenes useful for habitat assessment at close range, but beyond the range of the shrews' vibrissae.
PMCID: PMC2781971  PMID: 19535367
vocal behaviour; echolocation; communication; habitat acoustics; Sorex; Crocidura
14.  Multi-character perspectives on the evolution of intraspecific differentiation in a neotropical hylid frog 
Multi-character empirical studies are important contributions to our understanding of the process of speciation. The relatively conserved morphology of, and importance of the mate recognition system in anurans, combined with phylogenetic tools, provide an opportunity to address predictions about the relative role of each in the process of speciation. We examine the relationship among patterns of variation in morphology, call characters, and 16S gene sequences across seven populations of a neotropical hylid frog, Hyla leucophyllata, to infer their relative importance in predicting the early stages of population differentiation.
Multivariate analyses demonstrate that both morphological and call characteristics were significantly variable among populations, characterized by significantly lower intra-population dispersion in call space than morphological space, and significantly greater among-population variation in call structure. We found lack of concordance between a 16S DNA phylogeny of Hyla leucophyllata and the significant population-level differentiation evident in both external morphology and male advertisement call. Comparisons of the reconstructed gene trees to simulated lineages support the notion that variation in call cannot be simply explained by population history.
Discordance among traits may reflect sampling biases (e.g. single genetic marker effects), or imply a decoupling of evolution of different suites of characters. Diagnostic differences among populations in call structure possibly reflect local selection pressures presented by different heterospecific calling assemblages and may serve as a precursor of species-wide differentiation. Differentiation among populations in morphology may be due to ecophenotypic variation or to diversifying selection on body size directly, or on frequency attributes of calls (mediated by female choice) that show a strong relationship to body size.
PMCID: PMC1434785  PMID: 16539709
15.  The role of nocturnal vision in mate choice: females prefer conspicuous males in the European tree frog (Hyla arborea) 
Nocturnal frog species rely extensively on vocalization for reproduction. But recent studies provide evidence for an important, though long overlooked, role of visual communication. In many species, calling males exhibit a conspicuous pulsing vocal sac, a signal bearing visually important dynamic components. Here, we investigate female preference for male vocal sac coloration—a question hitherto unexplored—and male colour pattern in the European tree frog (Hyla arborea). Under nocturnal conditions, we conducted two-choice experiments involving video playbacks of calling males with identical calls and showing various naturally encountered colour signals, differing in their chromatic and brightness components. We adjusted video colours to match the frogs' visual perception, a crucial aspect not considered in previous experiments. Females prefer males with a colourful sac and a pronounced flank stripe. Both signals probably enhance male conspicuousness and facilitate detection and localization by females. This study provides the first experimental evidence of a preference for specific vocal sac spectral properties in a nocturnal anuran species. Vocal sac coloration is based on carotenoids and may convey information about male quality worthwhile for females to assess. The informative content of the flank stripe remains to be demonstrated.
PMCID: PMC2690462  PMID: 19324736
mate choice; coloration; nocturnal vision; multimodal signalling; vocal sac; lateral stripe
16.  The juvenile social environment introduces variation in the choice and expression of sexually selected traits 
Ecology and Evolution  2012;2(5):1036-1047.
The juvenile environment provides numerous cues of the intensity of competition and the availability of mates in the near environment. As research demonstrates that the developing individuals can use these cues to alter their developmental trajectories, and therefore, adult phenotypes, we examined whether social cues available during development can affect the expression and the preference of sexually selected traits. To examine this, we used the Australian black field cricket (Telogryllus commodus), a species where condition at maturity is known to affect both male calling effort and female choice. We mimicked different social environments by rearing juveniles in two different densities crossed with three different calling environments. We demonstrate that the social environment affected female response speed but not preference, and male age-specific calling effort (especially the rate of senescence in calling effort) but not the structural/temporal parameters of calls. These results demonstrate that the social environment can introduce variation in sexually selected traits by modifying the behavioral components of male production and female choice, suggesting that the social environment may be an overlooked source of phenotypic variation. We discuss the plasticity of trait expression and preference in reference to estimations of male quality and the concept of condition dependence.
PMCID: PMC3399168  PMID: 22837847
Adult behavior; age-specific calling effort; condition dependence; developmental plasticity; juvenile environment; social environment
17.  Tone and call responses of units in the auditory nerve and dorsal medullary nucleus of Xenopus laevis 
The clawed frog Xenopus laevis produces vocalizations consisting of distinct patterns of clicks. This study provides the first description of spontaneous, pure-tone and communication-signal evoked discharge properties of auditory nerve (n.VIII) fibers and dorsal medullary nucleus (DMN) cells in an obligatorily aquatic anuran. Responses of 297 n.VIII and 253 DMN units are analyzed for spontaneous rates (SR), frequency tuning, rate-intensity functions, and firing rate adaptation, with a view to how these basic characteristics shape responses to recorded call stimuli. Response properties generally resemble those in partially terrestrial anurans. Broad tuning exists across characteristic frequencies (CFs). Threshold minima are −101 dB re 1 mm/s at 675 Hz; −87 dB at 1,600 Hz; and −61 dB at 3,000 Hz (−90, −77, and −44 dB re 1 Pa, respectively), paralleling the peak frequency of vocalizations at 1.2–1.6 kHz with ~500 Hz in 3 dB bandwidth. SRs range from 0 to 80 (n.VIII) and 0 to 73 spikes/s (DMN). Nerve and DMN units of all CFs follow click rates in natural calls, ≤67 clicks/s and faster. Units encode clicks with a single spike, double spikes, or bursts. Spike times correlate closely with click envelopes. No temporal filtering for communicative click rates occurs in either n.VIII or the DMN.
PMCID: PMC3493246  PMID: 17989982
Auditory nerve; Hearing; Amphibian; Dorsal medullary nucleus; Sound communication
18.  Seasonal Variation in Population Abundance and Chytrid Infection in Stream-Dwelling Frogs of the Brazilian Atlantic Forest 
PLoS ONE  2015;10(7):e0130554.
Enigmatic amphibian declines were first reported in southern and southeastern Brazil in the late 1980s and included several species of stream-dwelling anurans (families Hylodidae and Cycloramphidae). At that time, we were unaware of the amphibian-killing fungus Batrachochytrium dendrobatidis (Bd); therefore, pollution, habitat loss, fragmentation and unusual climatic events were hypothesized as primary causes of these declines. We now know that multiple lineages of Bd have infected amphibians of the Brazilian Atlantic forest for over a century, yet declines have not been associated specifically with Bd outbreaks. Because stream-dwelling anurans occupy an environmental hotspot ideal for disease transmission, we investigated temporal variation in population and infection dynamics of three stream-adapted species (Hylodes asper, H. phyllodes, and Cycloramphus boraceiensis) on the northern coast of São Paulo state, Brazil. We surveyed standardized transects along streams for four years, and show that fluctuations in the number of frogs correlate with specific climatic variables that also increase the likelihood of Bd infections. In addition, we found that Bd infection probability in C. boraceiensis, a nocturnal species, was significantly higher than in Hylodes spp., which are diurnal, suggesting that the nocturnal activity may either facilitate Bd zoospore transmission or increase susceptibility of hosts. Our findings indicate that, despite long-term persistence of Bd in Brazil, some hosts persist with seasonally variable infections, and thus future persistence in the face of climate change will depend on the relative effect of those changes on frog recruitment and pathogen proliferation.
PMCID: PMC4498819  PMID: 26161777
19.  Vocal communication between male Xenopus laevis 
Animal behaviour  2003;67(2):353-365.
This study focuses on the role of male–male vocal communication in the reproductive repertoire of the South African clawed frog, Xenopus laevis. Six male and two female call types were recorded from native ponds in the environs of Cape Town, South Africa. These include all call types previously recorded in the laboratory as well as one previously unidentified male call: chirping. The amount of calling and the number of call types increased as the breeding season progressed. Laboratory recordings indicated that all six male call types were directed to males; three of these were directed to both sexes and three were directed exclusively to males. Both female call types were directed exclusively to males. The predominant call type, in both field and laboratory recordings, was the male advertisement call. Sexual state affected male vocal behaviour. Male pairs in which at least one male was sexually active (gonadotropin injected) produced all call types, whereas pairs of uninjected males rarely called. Some call types were strongly associated with a specific behaviour and others were not. Clasped males always growled and clasping males typically produced amplectant calls or chirps; males not engaged in clasping most frequently advertised. The amount of advertising produced by one male was profoundly affected by the presence of another male. Pairing two sexually active males resulted in suppression of advertisement calling in one; suppression was released when males were isolated after pairing. Vocal dominance was achieved even in the absence of physical contact (clasping). We suggest that X. laevis males gain a reproductive advantage by competing for advertisement privileges and by vocally suppressing neighbouring males.
PMCID: PMC3583545  PMID: 23457414
20.  The Effect of Habitat Acoustics on Common Marmoset Vocal Signal Transmission 
American journal of primatology  2013;75(9):904-916.
Noisy acoustic environments present several challenges for the evolution of acoustic communication systems. Among the most significant is the need to limit degradation of spectro-temporal signal structure in order to maintain communicative efficacy. This can be achieved by selecting for several potentially complementary processes. Selection can act on behavioral mechanisms permitting signalers to control the timing and occurrence of signal production to avoid acoustic interference. Likewise, the signal itself may be the target of selection, biasing the evolution of its structure to comprise acoustic features that avoid interference from ambient noise or degrade minimally in the habitat. Here, we address the latter topic for common marmoset (Callithrix jacchus) long-distance contact vocalizations, known as phee calls. Our aim was to test whether this vocalization is specifically adapted for transmission in a species-typical forest habitat, the Atlantic forests of northeastern Brazil. We combined seasonal analyses of ambient habitat acoustics with experiments in which pure tones, clicks, and vocalizations were broadcast and rerecorded at different distances to characterize signal degradation in the habitat. Ambient sound was analyzed from intervals throughout the day and over rainy and dry seasons, showing temporal regularities across varied timescales. Broadcast experiment results indicated that the tone and click stimuli showed the typically inverse relationship between frequency and signaling efficacy. Although marmoset phee calls degraded over distance with marked predictability compared with artificial sounds, they did not otherwise appear to be specially designed for increased transmission efficacy or minimal interference in this habitat. We discuss these data in the context of other similar studies and evidence of potential behavioral mechanisms for avoiding acoustic interference in order to maintain effective vocal communication in common marmosets.
PMCID: PMC3787903  PMID: 23592313
Callithrix jacchus; vocal communication; behavioral ecology; sound broadcasts; sound window
21.  Driving Factors for the Evolution of Species-Specific Echolocation Call Design in New World Free-Tailed Bats (Molossidae) 
PLoS ONE  2014;9(1):e85279.
Phylogeny, ecology, and sensorial constraints are thought to be the most important factors influencing echolocation call design in bats. The Molossidae is a diverse bat family with a majority of species restricted to tropical and subtropical regions. Most molossids are specialized to forage for insects in open space, and thus share similar navigational challenges. We use an unprecedented dataset on the echolocation calls of 8 genera and 18 species of New World molossids to explore how habitat, phylogenetic relatedness, body mass, and prey perception contribute to echolocation call design. Our results confirm that, with the exception of the genus Molossops, echolocation calls of these bats show a typical design for open space foraging. Two lines of evidence point to echolocation call structure of molossids reflecting phylogenetic relatedness. First, such structure is significantly more similar within than among genera. Second, except for allometric scaling, such structure is nearly the same in congeneric species. Despite contrasting body masses, 12 of 18 species call within a relatively narrow frequency range of 20 to 35 kHz, a finding that we explain by using a modeling approach whose results suggest this frequency range to be an adaptation optimizing prey perception in open space. To conclude, we argue that the high variability in echolocation call design of molossids is an advanced evolutionary trait allowing the flexible adjustment of echolocation systems to various sensorial challenges, while conserving sender identity for social communication. Unraveling evolutionary drivers for echolocation call design in bats has so far been hampered by the lack of adequate model organisms sharing a phylogenetic origin and facing similar sensorial challenges. We thus believe that knowledge of the echolocation call diversity of New World molossid bats may prove to be landmark to understand the evolution and functionality of species-specific signal design in bats.
PMCID: PMC3891751  PMID: 24454833
22.  Individual, Contextual, and Age-Related Acoustic Variation in Simakobu (Simias concolor) Loud Calls 
PLoS ONE  2013;8(12):e83131.
Primate loud calls have the potential to encode information about the identity, arousal, age, or physical condition of the caller, even at long distances. In this study, we conducted an analysis of the acoustic features of the loud calls produced by a species of Asian colobine monkey (simakobu, Simias concolor). Adult male simakobu produce loud calls spontaneously and in response to loud sounds and other loud calls, which are audible more than 500 m. Individual differences in calling rates and durations exist, but it is unknown what these differences signal and which other acoustic features vary among individuals. We aimed to describe the structure and usage of calls and to examine acoustic features that vary within and among individuals. We determined the context of 318 loud calls and analyzed 170 loud calls recorded from 10 adult males at an undisturbed site, Pungut, Siberut Island, Indonesia. Most calls (53%) followed the loud call of another male, 31% were spontaneous, and the remaining 16% followed a loud environmental disturbance. The fundamental frequency (F0) decreased while inter-unit intervals (IUI) increased over the course of loud call bouts, possibly indicating caller fatigue. Discriminant function analysis indicated that calls were not well discriminated by context, but spontaneous calls had higher peak frequencies, suggesting a higher level of arousal. Individual calls were distinct and individuals were mainly discriminated by IUI, call duration, and F0. Loud calls of older males had shorter IUI and lower F0, while middle-aged males had the highest peak frequencies. Overall, we found that calls were individually distinct and may provide information about the age, stamina, and arousal of the calling male, and could thus be a way for males and females to assess competitors and mates from long distances.
PMCID: PMC3871870  PMID: 24376651
23.  Timing matters: sonar call groups facilitate target localization in bats 
To successfully negotiate a cluttered environment, an echolocating bat must control the timing of motor behaviors in response to dynamic sensory information. Here we detail the big brown bat's adaptive temporal control over sonar call production for tracking prey, moving predictably or unpredictably, under different experimental conditions. We studied the adaptive control of vocal-motor behaviors in free-flying big brown bats, Eptesicus fuscus, as they captured tethered and free-flying insects, in open and cluttered environments. We also studied adaptive sonar behavior in bats trained to track moving targets from a resting position. In each of these experiments, bats adjusted the features of their calls to separate target and clutter. Under many task conditions, flying bats produced prominent sonar sound groups identified as clusters of echolocation pulses with relatively stable intervals, surrounded by longer pulse intervals. In experiments where bats tracked approaching targets from a resting position, bats also produced sonar sound groups, and the prevalence of these sonar sound groups increased when motion of the target was unpredictable. We hypothesize that sonar sound groups produced during flight, and the sonar call doublets produced by a bat tracking a target from a resting position, help the animal resolve dynamic target location and represent the echo scene in greater detail. Collectively, our data reveal adaptive temporal control over sonar call production that allows the bat to negotiate a complex and dynamic environment.
PMCID: PMC4026696  PMID: 24860509
echolocation behavior; sonar call timing; active sensing; spatial perception; target tracking
24.  Limited plasticity in the phenotypic variance-covariance matrix for male advertisement calls in the black field cricket, Teleogryllus commodus 
Journal of evolutionary biology  2013;26(5):1060-1078.
Phenotypic integration and plasticity are central to our understanding of how complex phenotypic traits evolve. Evolutionary change in complex quantitative traits can be predicted using the multivariate breeders’ equation, but such predictions are only accurate if the matrices involved are stable over evolutionary time. Recent work, however, suggests that these matrices are temporally plastic, spatially variable and themselves evolvable. The data available on phenotypic variance-covariance matrix (P) stability is sparse, and largely focused on morphological traits. Here we compared P for the structure of the complex sexual advertisement call of six divergent allopatric populations of the Australian black field cricket, Teleogryllus commodus. We measured a subset of calls from wild-caught crickets from each of the populations and then a second subset after rearing crickets under common-garden conditions for three generations. In a second experiment, crickets from each population were reared in the laboratory on high- and low-nutrient diets and their calls recorded. In both experiments, we estimated P for call traits and used multiple methods to compare them statistically (Flury hierarchy, geometric subspace comparisons and random skewers). Despite considerable variation in means and variances of individual call traits, the structure of P was largely conserved among populations, across generations and between our rearing diets. Our finding that P remains largely stable, among populations and between environmental conditions, suggests that selection has preserved the structure of call traits in order that they can function as an integrated unit.
PMCID: PMC3641675  PMID: 23530814
sexual selection; advertisement call; P matrix; phenotypic plasticity; phenotypic integration; common garden; diet; matrix comparison; field cricket
25.  Sexual Hearing: The influence of sex hormones on acoustic communication in frogs 
Hearing research  2009;252(1-2):15-20.
The majority of anuran amphibians (frogs and toads) use acoustic communication to mediate sexual behavior and reproduction. Generally, females find and select their mates using acoustic cues provided by males in the form of conspicuous advertisement calls. In these species, vocal signal production and reception are intimately tied to successful reproduction. Research with anurans has demonstrated that acoustic communication is modulated by reproductive hormones, including gonadal steroids and peptide neuromodulators. Most of these studies have focused on the ways in which hormonal systems influence vocal signal production; however, here we will concentrate on a growing body of literature that examines hormonal modulation of call reception. This literature suggests that reproductive hormones contribute to the coordination of reproductive behaviors between signaler and receiver by modulating sensitivity and spectral filtering of the anuran auditory system. It has become evident that the hormonal systems that influence reproductive behaviors are highly conserved among vertebrate taxa, thus studying the endocrine and neuromodulatory bases of acoustic communication in frogs and toads can lead to insights of broader applicability to hormonal modulation of vertebrate sensory physiology and behavior.
PMCID: PMC2722832  PMID: 19272318
anurans; arginine vasotocin; auditory system; gonadal steroids; sensory physiology

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