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Vocal Sound Production and Acoustic Communication in Amphibians and Reptiles

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Abstract

Most amphibians and reptiles produce sounds with a larynx containing a pair of vocal cords. Clicking and hissing are common in both groups whereas tonal sounds are found most frequently in anurans and geckos. Calls can exceed 90 dB SPL at a distance of 1 m and they can have fundamental frequencies above 20 kHz. Calling is used mostly by males for courtship and territorial displays. Offspring and females call to synchronize hatching and to mediate maternal care. Adults and juveniles in many groups produce hissing when threatened. Amphibians and reptiles include more than 17,000 species. As a result of this diversity, major advances in the field of vocalization are made through exploratory research but also through careful experimentation and the use of novel technologies. Combining the study of vocal and auditory systems is important to explain issues such as the diversity of frequency tuning in the group. Many questions can also be answered through comparative studies in amphibians and reptiles because these groups have evolved independent solutions to common communication problems.

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... In addition to the unresolved situation in anurans, the non-avian reptiles have been entirely neglected (although birds are members of Dinosauria, and therefore Reptilia, to avoid confusion, we will continue to (incorrectly) use the term reptile to refer to all members of this group except birds) leaving a critical gap in our understanding of the evolution of vocal plasticity. Although many reptiles use sound to communicate (reviewed in [19]) it remains unclear whether they possess any form of vocal flexibility to adjust their vocal signals to the environment. To trace back the evolutionary origin of the complex vocal plasticity found in birds and mammals, we investigated whether a lizard, the tokay gecko Gekko gecko (figure 1a), modifies the properties of its calls in response to changes in background noise. ...
... Vocal signalling is a less common feature in reptiles than in anurans, with many taxa producing only non-vocal sounds, such as percussive sounds or hissing, generated by forceful expiration of air without involving the vocal cords. Among the vocal reptiles (some chelonians, some lizardsmost notably geckos, and crocodilians (reviewed in [19,40])), the functional morphology of their vocal systems are quite diverse, as are the complexity of signals produced, which range from noisy grunts that require little control of glottal tension to frequency-modulated tonal sounds requiring active control of the vocal cords [19]. Basal sound production mechanisms, such as hissing or grunting are more inflexible in their production than tonal, harmonic and frequency modulated sounds, which are modified by changes in tension of the vibratory tissues, and thus the evolution of more sophisticated vocal anatomy may be a first step towards the evolution of flexible acoustic communication systems, such as those of birds, mammals, and now geckos. ...
... Vocal signalling is a less common feature in reptiles than in anurans, with many taxa producing only non-vocal sounds, such as percussive sounds or hissing, generated by forceful expiration of air without involving the vocal cords. Among the vocal reptiles (some chelonians, some lizardsmost notably geckos, and crocodilians (reviewed in [19,40])), the functional morphology of their vocal systems are quite diverse, as are the complexity of signals produced, which range from noisy grunts that require little control of glottal tension to frequency-modulated tonal sounds requiring active control of the vocal cords [19]. Basal sound production mechanisms, such as hissing or grunting are more inflexible in their production than tonal, harmonic and frequency modulated sounds, which are modified by changes in tension of the vibratory tissues, and thus the evolution of more sophisticated vocal anatomy may be a first step towards the evolution of flexible acoustic communication systems, such as those of birds, mammals, and now geckos. ...
Article
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Sophisticated vocal communication systems of birds and mammals, including human speech, are characterized by a high degree of plasticity in which signals are individually adjusted in response to changes in the environment. Here, we present, to our knowledge, the first evidence for vocal plasticity in a reptile. Like birds and mammals, tokay geckos (Gekko gecko) increased the duration of brief call notes in the presence of broadcast noise compared to quiet conditions, a behaviour that facilitates signal detection by receivers. By contrast, they did not adjust the amplitudes of their call syllables in noise (the Lombard effect), which is in line with the hypothesis that the Lombard effect has evolved independently in birds and mammals. However, the geckos used a different strategy to increase signal-to-noise ratios: instead of increasing the amplitude of a given call type when exposed to noise, the subjects produced more high-amplitude syllable types from their repertoire. Our findings demonstrate that reptile vocalizations are much more flexible than previously thought, including elaborate vocal plasticity that is also important for the complex signalling systems of birds and mammals. We suggest that signal detection constraints are one of the major forces driving the evolution of animal communication systems across different taxa. © 2017 The Author(s) Published by the Royal Society. All rights reserved.
... The Physalaemus larynges described in the present study have several of the anatomical modifications observed in other genera of the Leiuperinae subfamily (Engystomops and Edalorhina), with differences in size, shape and position of both arytenoid and cricoid cartilages that set them apart from the general anatomical pattern in Anura (Colafrancesco & Gridi-Papp, 2016;Martin, 1972;Trewavas, 1933): the larynx is of considerable relative size and closed as a capsule or box (Lagorio et al., 2019;Martin, 1972). The arytenoid has a large extension dorsally in the larynx, covering almost the entire dorsal surface. ...
... Similarly to the pattern observed in E. pustulosus (Drewry et al., 1982;. The multiple and relatively independent vibrating sources might be the cause of the nonlinear phenomena observed for some of these species, such as subharmonics, fundamental frequency jumps and acoustic chaos (noisy sounds) due to the high irregularity of the wave periods (De Carvalho et al., 2019;Colafrancesco & Gridi-Papp, 2016;Hepp & Pombal, 2020). ...
... In contrast, they are adhered to the arytenoids' internal wall and usually with a more cylindrical shape in the other species groups. They could be able to affect call production only by contributing to the total mass of set FM1 plus transverse thickening in species of P. olfersii group, whereas they should not affect this production in the other groups since they are broadly attached to a nonvibrating structure (Colafrancesco & Gridi-Papp, 2016). ...
Article
The anuran larynx is an organ of great evolutionary interest because it impacts male reproductive success in courtships. However, little is known about the diversity of the larynx's anatomy, evolutionary history and systematics importance. Here, we describe and compare the anatomy of the larynx of 10 Physalaemus species of the P. cuvieri clade, focusing on the P. olfersii species group. We also reconstructed the ancestral states and tested the phylogenetic signal for the anatomical features. In all the species, the larynx has a general globular shape with the arytenoid cartilages covering almost its entire dorsal surface, while the anterior process of the cricoid cartilages covers most of the ventral surface. The size of the secondary fibrous mass, the thickness of the vocal membrane, and the attachment position of the vocal membrane's free edge considerably differ among the species. Moreover, only four species of a single clade in the P. olfersii species group have the primary fibrous mass well-developed with a suspended region in the dorsolateral passage. We found a significant phylogenetic signal for all these characters. Ancestral reconstructions pointed to reduction tendencies in the thickness of the vocal membrane and the size of the secondary fibrous mass, and a shift of the ventral attachment of the vocal membrane, increasing the angle of its free edge along the phylogeny. This latter trait can diagnose the entire Physalaemus olfersii group, which has the ventral ends of the arytenoids positioned posteriorly, giving this group the steepest angles for the vocal membrane's free edge in relation to the frontal plane. Based on our results, the larynges can contribute to the Physalaemus olfersii species group's systematics and could be elucidative to understand the evolution of the genus. High levels of anatomical and bioacoustical complexity and diversity observed in the group support the expected correlation between vocal anatomy and bioacoustical signal.
... A rather separate, but also voluminous, literature deals with vocal signals in birds (e.g., Podos, Huber, & Taft, 2004). Anuran amphibians have also been much studied in this regard (e.g., Colafrancesco & Gridi-Papp, 2016). ...
... This has likely contributed to the absence of a comprehensive overview of vocalization in this paraphyletic assemblage. Furthermore, although reptiles are amniotes and, therefore, more closely related to mammals and birds than to amphibians, the traditional association of amphibians and reptiles within the discipline of herpetology has left the latter in the bioacoustic shadow of their much more universally vociferous anuran amphibian associates (see, e.g., the asymmetrical treatment afforded in the recent review by Colafrancesco & Gridi-Papp, 2016). We contend, however, that the multiple origins of vocalization among reptiles renders them particularly useful for the investigation of how true vocalization originates. ...
... Although not the major focus of this review, we outline below some of the main factors influencing and governing hearing in extant reptiles, thereby enabling the placement of the sounds they emit into their auditory context. In this way the diversity of frequency tuning can be more fully appreciated (Colafrancesco & Gridi-Papp, 2016). ...
Article
Among amniote vertebrates, nonavian reptiles (chelonians, crocodilians, and lepidosaurs) are regarded as using vocal signals rarely (compared to birds and mammals). In all three reptilian clades, however, certain taxa emit distress calls and advertisement calls using modifications of regions of the upper respiratory tract. There is no central tendency in either acoustic mechanisms or the structure of the vocal apparatus, and many taxa that vocalize emit only relatively simple sounds. Available evidence indicates multiple origins of true vocal abilities within these lineages. Reptiles thus provide opportunities for studying the early evolutionary stages of vocalization. The early literature on the diversity of form of the laryngotracheal apparatus of reptiles boded well for the study of form‐function relationships, but this potential was not extensively explored. Emphasis shifted away from anatomy, however, and centered instead on acoustic analysis of the sounds that are produced. New investigative techniques have provided novel ways of studying the form‐function aspects of the structures involved in phonation and have brought anatomical investigation to the forefront again. In this review we summarize what is known about hearing in reptiles in order to contextualize the vocal signals they generate and the sound‐producing mechanisms responsible for them. The diversity of form of the sound producing apparatus and the increasing evidence that reptiles are more dependent upon vocalization as a communication medium than previously thought indicates that they have a significant role to play in the understanding of the evolution of vocalization in amniotes.
... Notwithstanding, as in other animal groups, lizard vocalizations might equally well serve to alarm conspecifics of impending danger (Sherman 1977) or to attract additional predators that disrupt the predator event (Högstedt 1983). Vocalizations may also play a role during intraspecific interactions or can even be vestigial and non-functional (Hibbitts et al. 2007;Colafrancesco and Gridi-Papp 2016). ...
... s) (Böhme et al. 1985). While our comprehensive acoustic analysis revealed a more complex spectral structure than previously documented for P. algirus (Böhme et al. 1985), its vocalizations are, nevertheless, far less elaborate than those of geckos, a lizard group which is known to rely strongly on acoustic signalling for intraspecific communication (Colafrancesco and Gridi-Papp 2016). Our analyses also show considerable within-species variation in call design, with each individual having a unique call signature, defined by only a few acoustic variables. ...
... In vertebrates, call amplitude is predominantly determined by the degree of subglottal pressure and vocal fold adduction, which are controlled by the respiratory and laryngeal muscles, respectively (Gans and Maderson 1973;Stein 1973;Elemans et al. 2015). Individuals with more massive respiratory and laryngeal muscles are able to produce louder vocalizations than those with less developed muscles (Colafrancesco and Gridi-Papp 2016). Although the vocal muscle architecture is anatomically independent from the jaw muscles (that are responsible for an animal's bite), it is not unlikely that individuals with welldeveloped respiratory/laryngeal muscles are those in overall good condition, hence, those that carry well-developed muscles across their whole cranial system. ...
Article
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When encountering predators, prey animals often signal their ability to fight or flee to discourage the predator from an attack or pursuit. A key requirement for evolutionary stability of these predator-deterrent signals is that they convey honest information on the prey’s fighting or fleeing performance. In this study, we investigate the enigmatic ‘distress call’ of the lacertid lizard Psammodromus algirus, and test whether it conveys reliable information on an individual’s body size, and bite and sprint performance. Our acoustic analyses revealed a complex spectral structure in the vocalization of P. algirus, showing a wide frequency bandwidth, multiple harmonics, and a marked frequency modulation. This spectral design may allow such calls to be perceived by multiple potential predators, as it was assessed by a literature search comparing the call frequency range with the hearing ranges of P. algirus’ top predators. In addition, we found considerable inter-individual variation in the call design of lizards (‘call signatures’), which was linked with inter-individual variation in body size and maximum bite force, but not with sprint speed (a proxy of escape performance). As a whole, our study supports the hypothesis that the vocalizations of P. algirus lizards have the potential to serve as honest calls to deter predators. Further research on the behavioural response of predators towards lizard calls is essential in order to unravel the true predator deterrence potential of these calls. Significance statement When eye-to-eye with a predator, prey animals may signal their ability to fight or flee to convince the predator not to attack or pursue them. Reptiles typically use visual displays to deter predators, but fascinatingly, Psammodromus algirus lizards have been observed to vocalize when encountered by predators. Here, we explored the acoustic properties of these calls and examined whether they convey honest information on a lizard’s fighting and fleeing performance. Our recordings indicate that the acoustic profile of the calls fall within the hearing sensitivity of the lizard’s top predators. Moreover, our experiments show a significant link between the acoustic profile of lizard calls and lizard fighting ability, but not with fleeing ability. Together, our results imply that these lizard calls have predator deterrence potential. Additionally, this study provides the first evidence of honest acoustic signalling of performance in a reptile.
... Frogs produce vocalizations by shuttling air from the lungs, through the larynx and into the vocal sac, and thus, the contraction of trunk muscles is the main power source of phonation. Unlike mammals and birds, anurans are considered to lack extensive neuromuscular control over the larynx (Colafrancesco & Gridi-Papp, 2016). Instead, the spectral content of calls is largely determined by the morphology of the larynx (e.g. ...
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Animals show a rich diversity of signals and displays. Among the many selective forces driving the evolution of communication between individuals, one widely recognized factor is the structure of the environment in which signals are produced, transmitted and received. In particular, animals communicating by sounds often emit acoustic signals from specific locations, such as high up in the air, from the ground or in the water. The properties of these different display sites will impose different constraints on sound production and transmission and may therefore drive signal evolution. Here, we used comparative phylogenetic analyses to assess the relationship between the display site properties and the structure of reproductive calls from 161 frog species from the frog families Ranidae, Leptodactylidae and Hylidae. Specifically, we compared the dominant frequency of species that vocalize from aquatic versus non-aquatic sites, and its relation with body size. We found that the dominant frequency of frogs calling from the water was lower than that of species calling outside of the water, a trend that was consistent across the three families studied. Furthermore, phylogenetic path analysis revealed that the call site had both direct and indirect effects on the dominant frequency. Indirect effects were mediated by call site influencing male body size, which in turn was negatively associated to call dominant frequency. Our results suggest that properties of display sites can drive signal evolution, most likely through morphological constraints, in particular the ones imposed on the sound production mechanism. Also, variation in body size between calling sites explained some of the differences we found in call frequency, highlighting the relevance of the interplay between morphological adaptation and signal evolution. Changes of display site may therefore have important evolutionary consequences, as it may influence sexual selection processes and ultimately may even promote speciation. Impact summary To attract or impress mates, animals have evolved a great diversity of communication signals, such as song and dance, or brightly colored body parts. Whether these sexual signals are successful depends to a large extent on the environment in which they are produced, transmitted and perceived. For acoustic signals, such as the mating calls of frogs, the environment is well known to influence both their transmission and perception. The impact of the environment on the production of sounds is however far less understood. Here we studied the relation between the environment and signal design across a wide range of frog species, specifically comparing calls of aquatic versus non-aquatic species. Frogs that called from water were found to call at lower pitch, which was partly explained by the fact that they were also larger. Our results point towards an important environmental driver of signal evolution, namely morphological constraints on signal production. We argue that the environment can impose limits on morphological traits that are either directly or indirectly involved in signal production. Such a mechanism would in particular be important when species move into new habitats, as rapid changes to display sites may lead to rapid changes in sexual signaling and sexual attractiveness.
... These animals have vocal sacs to help radiate sound energy effectively (like a speaker membrane) and they use an air-recycling system to pump air between the lungs and the vocal sacs across the larynx (vocal folds). This air pumping is independent of air breathing, because the nostrils and mouth are closed (Gerhardt and Huber, 2002;Kime et al., 2013;Colafrancesco and Gridi-Papp, 2016) (Fig. 3A). Among Anura, an exception to the normal tetrapod mechanism of sound production is found only in the fully aquatic pipid frogs, such as the African clawed frog Xenopus. ...
Article
Full-text available
Sound propagates much faster and over larger distances in water than in air, mainly because of differences in the density of these media. This raises the question of whether terrestrial (land mammals, birds) and (semi-)aquatic animals (frogs, fishes, cetaceans) differ fundamentally in the way they communicate acoustically. Terrestrial vertebrates primarily produce sounds by vibrating vocal tissue (folds) directly in an airflow. This mechanism has been modified in frogs and cetaceans, whereas fishes generate sounds in quite different ways mainly by utilizing the swimbladder or pectoral fins. On land, vertebrates pick up sounds with light tympana, whereas other mechanisms have had to evolve underwater. Furthermore, fishes differ from all other vertebrates by not having an inner ear end organ devoted exclusively to hearing. Comparing acoustic communication within and between aquatic and terrestrial vertebrates reveals that there is no 'aquatic way' of sound communication, as compared witha more uniform terrestrial one. Birds and mammals display rich acoustic communication behaviour, which reflects their highly developed cognitive and social capabilities. In contrast, acoustic signaling seems to be the exception in fishes, and is obviously limited to short distances and to substrate-breeding species, whereas all cetaceans communicate acoustically and, because of their predominantly pelagic lifestyle, exploit the benefits of sound propagation in a dense, obstacle-free medium that provides fast and almost lossless signal transmission.
... closed during diving, it is hypothesised that toothed whales recycle air repeatedly during long dives by forcing air from the vestibular sacs back into the lower nasal passages. A similar system that enables underwater vocalisation has been found in frogs and toads (Colafrancesco and Gridi-Papp, 2016) but experimental evidence for air recycling in odontocetes is limited (Dormer, 1979). Nevertheless, it is assumed to be the norm during echolocation in toothed whales and to take place during pauses in click sequences (Wahlberg, 2002). ...
Thesis
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Deep-diving odontocetes have a limited air supply for the production of clicks during long dives and they need to recycle it in their nasal sacs. Recordings from animal-attached tags reveal that these clicks diverge from the on-axis signals by having longer decays. Due to acoustic impedance differences at the air-tissue interface, we hypothesize that (i) long click decays are caused by nasal sacs via resonance and reverberation, and that (ii) the magnitude of decay depends on the sacs’ size thus providing hints for air recycling. We measured click decay time from DTAG acoustic data in three odontocetes with diverse nasal anatomy: sperm whales Physeter macrocephalus, short-finned pilot whales Globicephala macrorhynchus and Blainville’s beaked whales Mesoplodon densirostris. For G. macrorhynchus, we modelled click decay rate as a function of depth and number of clicks preceding from the last clicking pause. We also fitted a gas equation from swim bladders of fish to the resonant frequencies of pilot whale clicks. Results show that the right nasal passage and the vestibular sacs contribute to long click decays in P. macrocephalus and G. macrorhynchus respectively, and that clicking pauses are associated with substantial changes in the size of these sacs indicating air recycling. Depth has a positive effect on decay rate (0.0034 dB RMS/ms per metre, p<0.0001) by compressing the air in the vestibular sacs, while the effect of number of clicks is negative (-0.027 dB RMS/ms per click, p<0.0001) since air is added to these sacs after each click. Pauses are more often at depth for G. macrorhynchus, while click decay time in M. densirostris is minimal due to their thin nasal sacs. We conclude that the need to pause for air recycling forces deep-diving odontocetes to accommodate brief periods of 'blindness', which need to be managed carefully during foraging.
... Both tortoises and crocodiles vocalize (Colafrancesco and Gridi-Papp 2016) and if, like geckos, they do not regulate their vocal amplitudes in relation to noise, it is likely that the Lombard effect has evolved independently in birds and mammals. ...
Article
Full-text available
Signal plasticity is a building block of complex animal communication systems. A particular form of signal plasticity is the Lombard effect, in which a signaler increases its vocal amplitude in response to an increase in the background noise. The Lombard effect is a basic mechanism for communication in noise that is well-studied in human speech and which has also been reported in other mammals and several bird species. Sometimes, but not always, the Lombard effect is accompanied by additional changes in signal parameters. However, the evolution of the Lombard effect and other related vocal adjustments in birds are still unclear because so far only three major avian clades have been studied. We report the first evidence for the Lombard effect in an anseriform bird, the mallard (Anas platyrhynchos). In association with the Lombard effect, the fifteen ducklings in our experiment also increased the peak frequency of their calls in noise. However, they did not change the duration of call syllables or their call rates as has been found in other bird species. Our findings support the notion that all extant birds use the Lombard effect to solve the common problem of maintaining communication in noise, i.e. it is an ancestral trait shared among all living avian taxa, which means that it has evolved more than 70 million years ago within that group. At the same time, our data suggest that parameter changes associated with the Lombard effect follow more complex patterns, with marked differences between taxa, some of which might be related to proximate constraints.
... Wilczynski and Ryan 2010). Relatively few studies have used experimental manipulations to investigate the mechanics of anuran vocal production (Schmidt 1965;Martin 1971;Gans 1973;Gridi-Papp et al. 2006;Suthers et al. 2006;Gridi-Papp 2014;Colafrancesco and Gridi-Papp 2016), and such studies are complicated by the fact that sound production is determined by both active (neural) modulation of the vocal system and the passive dynamics of its oscillators. This is particularly true for frogs that produce complex calls. ...
Article
Relatively few studies have used experimental manipulations to investigate the mechanics of vocal production in frogs and toads, even though many frogs produce complex signals with multiple components and/or nonlinearities. Modelling approaches can add to empirical studies by illuminating how various components of the vocal system interact to produce communication signals. In this study, we use bond graphs, a lumped-element modelling technique, to explore how the combination of active modulation of vocal production and the passive dynamics of a unique laryngeal structure result in the complex calls produced by males in an anuran model system. The túngara frog (Physalaemus (= Engystomops) pustulosus) produces advertisement calls with a ‘whine’ and a facultative ‘chuck’. Whines are amplitude and frequency modulated. The chuck is characterized by its spectral complexity and appears to contain a period doubling bifurcation resulting in subharmonics. In our model, we focus on how a fibrous mass attached to the vocal cords results in subharmonics in the chuck. Our models suggest that active (neural) modulation of the fibrous mass is not necessary for the transition between the spectral characteristics of the whine and chuck. Rather, it is possible that the vibratory mode of the fibrous mass and thus the vocal cords changes passively as a result of changes in airflow through the system.
... Further Lombard experiments in Testudines and Crocodilia would be a critical test of these two alternative hypotheses. Both tortoises and crocodiles vocalize (Colafrancesco and Gridi-Papp, 2016) and if, like geckos, they do not regulate their vocal amplitudes in relation to noise, it is likely that the Lombard effect has evolved independently in birds and mammals. ...
... In the last decades, passive acoustic monitoring has become a popular tool for collecting information about biodiversity [5], population densities [6,7], animal movement and behaviour [8], and how these factors are impacted by anthropogenic activities [9]. Both in terrestrial and marine environments, acoustic data have gained in importance [9,10] across taxonomic groups from insects [11], amphibians [12], reptiles [13], fish [14,15], and birds [16] to mammals [17][18][19][20][21][22]. Alongside species identity [21,23,24] acoustic data can encode information about sex [25][26][27][28], individual identity [25,29], body size, age, and social group [28,[30][31][32] or geographic origin [33][34][35]. ...
Article
Full-text available
Population sex ratios are of high ecological relevance, but are challenging to determine in species lacking conspicuous external cues indicating their sex. Acoustic sexing is an option if vocalizations differ between sexes, but is precluded by overlapping distributions of the values of male and female vocalizations in many species. A method allowing the inference of sex ratios despite such an overlap will therefore greatly increase the information extractable from acoustic data. To meet this demand, we developed a novel approach using Approximate Bayesian Computation (ABC) to infer the sex ratio of populations from acoustic data. Additionally, parameters characterizing the male and female distribution of acoustic values (mean and standard deviation) are inferred. This information is then used to probabilistically assign a sex to a single acoustic signal. We furthermore develop a simpler means of sex ratio estimation based on the exclusion of calls from the overlap zone. Applying our methods to simulated data demonstrates that sex ratio and acoustic parameter characteristics of males and females are reliably inferred by the ABC approach. Applying both the ABC and the exclusion method to empirical datasets (echolocation calls recorded in colonies of lesser horseshoe bats, Rhinolophus hipposideros) provides similar sex ratios as molecular sexing. Our methods aim to facilitate evidence-based conservation, and to benefit scientists investigating ecological or conservation questions related to sex- or group specific behaviour across a wide range of organisms emitting acoustic signals. The developed methodology is non-invasive, low-cost and time-efficient, thus allowing the study of many sites and individuals. We provide an R-script for the easy application of the method and discuss potential future extensions and fields of applications. The script can be easily adapted to account for numerous biological systems by adjusting the type and number of groups to be distinguished (e.g. age, social rank, cryptic species) and the acoustic parameters investigated.
... What evidence we do have, however, does not appear to support this scenario. Among extant tetrapods, vocal communication may or may not be ancestral to lepidosaurs, but there is increasing evidence that it was present in many turtles, the closest outgroup of crocodilians and birds (10,11). Other behaviors in which vocal communication is deployed, such as posthatching parental care and feeding of young, have consistently been inferred to be homologous in turtles, birds, and crocodilians (12)(13)(14). ...
Article
In its most basic conception, a novelty is simply something new. However, when many previously proposed evolutionary novelties have been illuminated by genetic, developmental, and fossil data, they have refined and narrowed our concept of biological "newness." For example, they show that these novelties can occur at one or multiple levels of biological organization. Here, we review the identity of structures in the avian vocal organ, the syrinx, and bring together developmental data on airway patterning, structural data from across tetrapods, and mathematical modeling to assess what is novel. In contrast with laryngeal cartilages that support vocal folds in other vertebrates, we find no evidence that individual cartilage rings anchoring vocal folds in the syrinx have homology with any specific elements in outgroups. Further, unlike all other vertebrate vocal organs, the syrinx is not derived from a known valve precursor, and its origin involves a transition from an evolutionary "spandrel" in the respiratory tract, the site where the trachea meets the bronchi, to a target for novel selective regimes. We find that the syrinx falls into an unusual category of novel structures: those having significant functional overlap with the structures they replace. The syrinx, along with other evolutionary novelties in sensory and signaling modalities, may more commonly involve structural changes that contribute to or modify an existing function rather than those that enable new functions.
... Extremely little is also known about the function of hearing in turtles. Several studies have documented vocalizations in turtles (see Colafrancesco & Gridi-Papp, 2016 for a recent summary) that can reasonably be interpreted as calls utilized in communication, though experimental setups are still too preliminary to demonstrate their function with confidence. Additional functions of hearing are both possible and probable (i.e. ...
Article
The middle ear of turtles differs from other reptiles in being separated into two distinct compartments. Several ideas have been proposed as to why the middle ear is compartmentalized in turtles, most suggesting a relationship with underwater hearing. Extant turtle species span fully marine to strictly terrestrial habitats, and ecomorphological hypotheses of turtle hearing predict that this should correlate with variation in the structure of the middle ear due to differences in the fluid properties of water and air. We investigate the shape and size of the air-filled middle ear cavity of 56 extant turtles using 3D data and phylogenetic comparative analysis to test for correlations between habitat preferences and the shape and size of the middle ear cavity. Only weak correlations are found between middle ear cavity size and ecology, with aquatic taxa having proportionally smaller cavity volumes. The middle ear cavity of turtles exhibits high shape diversity among species, but we found no relationship between this shape variation and ecology. Surprisingly, the estimated acoustic transformer ratio, a key functional parameter of impedance-matching ears in vertebrates, also shows no relation to habitat preferences (aquatic/terrestrial) in turtles. We suggest that middle ear cavity shape may be controlled by factors unrelated to hearing, such as the spatial demands of surrounding cranial structures. A review of the fossil record suggests that the modern turtle ear evolved during the Early to Middle Jurassic in stem turtles broadly adapted to freshwater and terrestrial settings. This, combined with our finding that evolutionary transitions between habitats caused only weak evolutionary changes in middle ear structure, suggests that tympanic hearing in turtles evolved as a compromise between subaerial and underwater hearing.
... Furthermore, these studies focused on a single species: the African clawed frog, Xenopus laevis (e.g., Hayes et al. 2002;Smith et al. 2005;Qin et al. 2007). Although Xenopus laevis is a model organism in development and genetics, its laryngeal morphology is atypical for anurans (Sassoon and Kelley 1986;Colafrancesco and Gridi-Papp 2016) as this species is fully aquatic and calls underwater (Yager 1992). It is also unclear how similar the physiological responses to endocrine disruptors are among Xenopus and other anuran taxa (Pattersson and Berg 2007;Tamschick et al. 2016). ...
Article
Anthropogenic factors, including the spread of endocrine-disrupting chemicals, have been linked to alterations in the reproductive physiology, morphology, and behavior of wildlife. Few studies of endocrine disruption, however, focus on secondary sexual traits that affect mating signals, despite their importance for reproductive success. The larynx of many anurans (frogs and toads), for example, is larger in males than in females and is crucial for producing mating calls. We aim to determine if wild populations of cane toads (Rhinella marina) near sugarcane fields in Florida have demasculinized larynges when compared to populations near urban areas. We find evidence of demasculinization in both primary and secondary sexual traits in male toads living near sugarcane. Relative to body size, the laryngeal mass, vocal cord length, and dilator muscle width are all reduced in males from sugarcane regions compared to their urban counterparts. Strong correlations between primary and secondary male sexual traits indicate that demasculinization occurs in concert both within and across diverse organs, including the testes, larynx, and skin. Our results show that anurans near sugarcane fields have demasculinized reproductive systems, that this disruption extends to secondary sexual traits like the larynx, and that it is likely due to anthropogenic causes.
... 2). The literature concerning lizard and snake vocalizations has been reviewed by Frankenberg and Werner (1992), Hibbits et al. (2007), Colafrancesco and Gridi-Papp (2016), Baeckens et al. (2019), Rohtla et al. (2019), and Fleischman and Font (2019) and readers are referred to these for details. ...
Chapter
Synopsis The huge structural variety in lepidosaurs ears is unique and results in substantial functional differences. The simple epithelia of snakes are restricted to low frequencies. Each lizard family has a characteristic hearing organ structure, with the largest variety in the number of hair cells and the type of tectorial membrane. Whereas the nocturnal geckos have highly sensitive and frequency selective hearing, diurnal lizard family hearing varies greatly, from poor to excellent, rivaling that of birds and mammals over the same frequency ranges.
... This indicates that sounds are produced with the mouth closed, and air stays within the vocal system of the turtles, as described for the long-necked freshwater turtle (Giles et al., 2009). The aerial and underwater vocal production mechanisms are still unknown in turtles, but they likely involve the larynx, the vocal chords, and two ventral cricoid diverticula that may act as cavity resonators (Colafrancesco and Gridi-Papp, 2016;Sacchi et al., 2004). Further investigations are needed to better understand the anatomical structures involved in the vocal production in turtles as well as the air flow during underwater vocal production in aquatic turtles. ...
Thesis
La Plateforme intergouvernementale sur la biodiversité et les services écosystémiques (IPBES) alertait en 2019 qu’un million d’espèces animales et végétales sont désormais menacées d’extinction. L’étude du comportement animal peut apporter une contribution significative à la conservation en améliorant les connaissances sur l’écologie des espèces et permettre l’élaboration de mesures de protection adaptées et effectives. Ainsi, l’objectif de cette thèse était de développer une méthode d’identification automatique des comportements à partir de bio-loggers pour des espèces menacées difficiles à observer ; les tortues marines. A partir du déploiement de caméras embarquées couplées à des accéléromètres, gyroscopes et capteurs de pression sur les tortues vertes en Martinique, un puissant réseau de neurones a été entrainé pour répondre à cet objectif. L’application de cette méthode sur cette même population via le déploiement de bio-loggers sur plusieurs jours nous a permis d’identifier des mesures de protection concrètes et adaptées aux enjeux économiques de la région.
... data), and Carothers et al. (2001) indicated that under these experimental conditions a human can hear calls from ~ 3 m. It is unclear from how far the Weeping lizard can hear these calls, as it is for species such as geckos, a taxon more vocal than lizards (Colafrancesco and Gridi-Papp 2016). For example, the determination of how far the calls of Gekko japonicas are audible is based on human perception (Jono and Inui 2012). ...
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For a prey, its best ticket to stay alive is to get early and accurate information on predation risk and so, escape from predation at low cost. Some prey species have evolved the ability to eavesdrop signals intended for others, which contain information on predation risk. This is the case for the vocalizations produced by prey species when interacting with predators. Although primarily studied in birds and mammals, eavesdropping on vocal signals has been recorded in some lizard species. Here, we explored whether the lizard Liolaemus lemniscatus eavesdrops on the distress calls of its sympatric species, the Weeping lizard (L. chiliensis). Individuals of the Weeping lizard respond to these calls by displaying antipredator behaviours (i.e., reduced movement), and individuals of L. lemniscatus may potentially display similar defences if they decode the information contained in these calls. Our playback experiments showed that individuals of L. lemniscatus responded to the sound stimuli (distress calls and white noise), reducing their activity, but they did not discriminate between these two stimuli, suggesting that L. lemniscatus does not eavesdrop on the distress calls of its sympatric lizard species. We discuss some hypotheses to explain the lack of eavesdropping by L. lemniscatus on the Weeping lizard distress calls.
... Frogs produce vocalizations by shuttling air from the lungs, through the larynx and into the vocal sac, and thus, the contraction of trunk muscles is the main power source of phonation. Unlike mammals and birds, anurans are considered to lack extensive neuromuscular control over the larynx (Colafrancesco & Gridi-Papp, 2016). Instead, the spectral content of calls is largely determined by the morphology of the larynx (e.g. ...
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Animals show a rich diversity of signals and displays. Among the many selective forces driving the evolution of communication signals, one widely recognized factor is the structure of the environment where animals communicate. In particular, animals communicating by sounds often emit acoustic signals from specific locations, such as high up in the air, from the ground or in the water. The properties of these different display sites may impose different constraints on sound production, and therefore drive signal evolution. Here, we used comparative phylogenetic analyses to assess the relationship between calling site (aquatic versus nonaquatic), body size and call dominant frequency of 160 frog species from the families Ranidae, Leptodactylidae and Hylidae. We found that the frequency of frogs calling from the water was lower than that of species calling outside of the water, a trend that was consistent across the three families studied. Furthermore, phylogenetic path analysis revealed that call site had both direct and indirect effects on call frequency. Indirect effects were mediated by call site influencing male body size, which in turn was negatively associated with call frequency. Our results suggest that properties of display sites can drive signal evolution, most likely not only through morphological constraints imposed on the sound production mechanism, but also through changes in body size, highlighting the relevance of the interplay between morphological adaptation and signal evolution. Changes in display site may therefore have important evolutionary consequences, as it may influence sexual selection processes and ultimately may even promote speciation.
... Even though most terrestrial vertebrates share this basic design, their vocal sound production is extremely varied. While frogs use a buccal pumping for sound production, lizards and snakes use their ribs and costal muscles to allow the expansion of the thoracic cavity (Colafrancesco and Gridi-Papp 2016). However, many extant non-avian reptiles do not vocalize, with a few exceptions for some turtles and tortoises, most gecko lizards, and most crocodilians (Russel and Bauer 2020;Vergne et al. 2009). ...
... Little is known about the neural and physiological basis of sound production in gymnophionans and urodeles. Courtship calls have not been observed in salamanders, but vocalizations involving clicks and hissing are used as an apparent defense mechanism [52]. Caecilian sounds have been only rarely recorded and described as soft yelps or squeaks [53]. ...
Article
Recent studies have served to emphasize the unique placement of amphibians, composed of more than 8000 species, in the evolution of the brain. We provide an overview of the three amphibian orders and their respective ecologies, behaviors, and brain anatomy. Studies have probed the origins of independently evolved parental care strategies in frogs and the biophysical principles driving species-specific differences in courtship vocalization patterns. Amphibians are also important models for studying the central control of movement, especially in the context of the vertebrate origin of limb-based locomotion. By highlighting the versatility of amphibians, we hope to see a further adoption of anurans, urodeles, and gymnophionans as model systems for the evolution and neural basis of behavior across vertebrates.
... The known frequency of sounds produced by snakes ranges from 0.2 -7.5 KHz, ranging from imperceptible sounds to humans to audible and observable squeaks. These sounds are associated with body in ation and muscle contraction to expel air and produce sound [5][6][7][8][9] . In other cases, the friction of the skin's scalloped scales (a more complex structure, such as a rattle (present in species of the genus snake can produce warning sounds audible within walking distance 4,8 . ...
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Discussions about auditory systems and sound dynamics in snakes are frequent. The known frequency of sounds produced by snakes ranges from 0.2 - 7.5 KHz, ranging from imperceptible sounds to humans to audible and observable squeaks. The hiss and whistles are the most common sound and are not considered vocalizations. During a nocturnal survey on June 13, 2021, in the northern Brazilian Amazon, we observed the first record of vocalization in a South American snake. Emitted by the individual from Dipsas catesbyi has a duration of 0.06 seconds, reaching 3036 Hz in its peak frequency, with an amplitude of 2761 to 4152 Hz of frequency in its main emission. Vocalizations were made during the exhalation of air through the larynx. The modulation differs from all patterns observed for snakes resembling the agonistic call of anuran amphibians, which could characterize an evolutionary mimicry of this behavior. Vocal emission via the larynx can generate internal vibrations perceptible to the auditory system of snakes, which, when vocalizing, vibrate the laryngeal cartilage and vocal cord. Our hypothesis is that structured vocal emission through laryngeal air exhalation may be a characteristic shared by other species of the Colubridae family.
... This indicates that the sounds are produced with the mouth closed, and air stays within the vocal system of the turtles, as described for the longnecked freshwater turtle (Giles et al. 2009). The aerial and underwater vocal production mechanisms are still unknown in turtles, but they likely involve the larynx, the vocal cords, and 2 ventral cricoid diverticula that may act as cavity resonators (Sacchi et al. 2004, Colafrancesco & Gridi-Papp 2016. Further in -vestigations are needed to better understand the anatomical structures involved in vocal production in turtles as well as the air flow during underwater vocal production in aquatic turtles. ...
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Marine turtles have long been considered to be silent, but few investigations have been performed to confirm such muteness. However, recent studies on the aerial and underwater hearing abilities of marine turtles have shown they have an ability to perceive sounds, suggesting the potential existence of acoustic communication among them. In the present study, audio-video recorders were deployed on 11 free-ranging juvenile green sea turtles Chelonia mydas at Grande Anse d’Arlet in Martinique. The recordings revealed that the turtles produced 10 different sound types that were classified into 4 main categories: pulses, low-amplitude calls (LAC), frequencymodulated sounds, and squeaks. Although other turtles were not observed in close proximity to tagged turtles during the recordings, some of the described sounds were found in most recorded individuals and their frequency characteristics ranged within the underwater hearing range of green sea turtles, suggesting that the sounds could be used for intra-specific communication. While control recordings in the study area without the presence of green sea turtles contained sounds with similar general structure (pulses, LAC), the acoustic characteristics were significantly different to those recorded for green sea turtles. The 2 types of squeaks identified for the turtles were found to be individual-specific, also suggesting they could be used for intra-species communication. Further research on sea turtles is needed to better understand the behavioral and social context of these acoustic productions, especially during the developmental period and breeding season. Thus, the vocal repertoire of green sea turtles is likely to be more diverse than that currently described.
... Within the animal kingdom, communication is a key mechanism for keeping animal societies together (SMITH, 1977), which for many species -especially insects, amphibians, birds, and some mammals -includes vocal signals (calls) (COLAFRANCESCO and GRIDI-PAPP, 2016;CHAVERRI et al., 2018;RAND et al., 2022;SOULSBURY et al., 2022). The call recipients could be either conspecifi c (e.g. to advertise reproductive status and territory of an individual; NAGUIB et al., 2022) or allospecifi c (e.g. to inform predators that they have been spotted or to alert sympatric species of danger; SABOL et al., 2022). ...
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Passive acoustic monitoring is a wildlife monitoring method used especially for the study of vocally active species which are difficult to observe directly. The tawny owl (Strix aluco, Linnaeus 1758) is such a species, and has not been previously studied in Greece. The aim of the study was to provide a first insight into the species' acoustic ecology in the Rhodope Mountains by describing its calling activity at four sites over a period of 3-6 months, and to examine possible correlation with natural and climatic parameters. Based on 24,937 calls, we report a significant increase in the number of calls per night (18:00 pm to 9:00 am) as the length of the night increased, as well as a negative relation with wind speed. We did not observe a relationship between calling frequency and the phase of the moon.
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The multifaceted ability to produce, transmit, receive, and respond to acoustic signals is widespread in animals and forms the basis of the interdisciplinary science of bioacoustics. Bioacoustics research methods, including sound recording and playback experiments, are applicable in cognitive research that centers around the processing of information from the acoustic environment. We provide an overview of bioacoustics techniques in the context of cognitive studies and make the case for the importance of bioacoustics in the study of cognition by outlining some of the major cognitive processes in which acoustic signals are involved. We also describe key considerations associated with the recording of sound and its use in cognitive applications. Based on these considerations, we provide a set of recommendations for best practices in the recording and use of acoustic signals in cognitive studies. Our aim is to demonstrate that acoustic recordings and stimuli are valuable tools for cognitive researchers when used appropriately. In doing so, we hope to stimulate opportunities for innovative cognitive research that incorporates robust recording protocols. This article is categorized under: • Neuroscience > Cognition • Psychology > Theory and Methods • Neuroscience > Behavior • Neuroscience > Cognition
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Synopsis The huge structural variety in lepidosaurs ears is unique and results in substantial functional differences. The simple epithelia of snakes are restricted to low frequencies. Each lizard family has a characteristic hearing organ structure, with the largest variety in the number of hair cells and the type of tectorial membrane. Whereas the nocturnal geckos have highly sensitive and frequency selective hearing, diurnal lizard family hearing varies greatly, from poor to excellent, rivaling that of birds and mammals over the same frequency ranges.
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Recordings were made in nests of Eretmochelys imbricata and 107 samples of 10-min recordings revealed 575 sounds that were classified manually into 4 categories. Our results show that hawksbill turtles vocalize within the nest, especially during and after eclosion, which suggests vocalizations are important for communication among hatchlings to synchronize emergence from the nest.
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Sound-producing organs generate acoustic signals that have a fundamental role in communication systems. In species exhibiting different biogeographic patterns, variations of these structures can explain a large part of interpopulation differences of their signals. Pleurodema thaul is an anuran with an extensive geographic distribution in Chile and presents an evident divergence in its acoustic signals among three genetic/bioacoustic groups (i.e. northern, central and southern). By means of classic histology and 3D-reconstructions, we study the geographic variation in the larynx of P. thaul males from these three groups. In addition, volumes of six laryngeal structures are used as predictors of acoustic characteristics of advertisement calls recorded in previous studies for the same subjects used in the current study. After removing the effect of body size, the arytenoid cartilage, dilator muscle and vocal cords show significant differences between the three bioacoustic groups. Furthermore, arytenoid cartilage and dilator muscle volumes predict some temporal parameters and also the dominant frequency of advertisement calls. Our results show important geographic variation in laryngeal morphology, which is in correspondence with acoustic, behavioural and genetic variation in this species.
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We describe for the first time the call of Rhinella festae (Peracca, 1904), recording it in captivity inside a plastic bag. The call is composed of 1 to 2 multi-pulsed notes (2–5 pulses), has an average duration of 0.72 s, and a dominant frequency of 1.40 kHz. This species is characterized by the absence of vocal slits and sacs, so the emission of this call would be considered unusual and uncommon. In addition to the purpose of improving the knowledge of species suggested as mutes, we have also compiled information from other anuran species that emit sounds with the absence of these anatomical structures.
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Sensory perception is of crucial importance for animals to interact with their biotic and abiotic environment. In amniotes, the clade including modern mammals (Synapsida), modern reptiles (Reptilia), and their fossil relatives, the evolution of sensory perception took place in a stepwise manner after amniotes appeared in the Carboniferous. Fossil evidence suggests that Paleozoic taxa had only a limited amount of sensory capacities relative to later forms, with the majority of more sophisticated types of sensing evolving during the Triassic and Jurassic. Alongside the evolution of improved sensory capacities, various types of social communication evolved across different groups. At present there is no definitive evidence for a relationship between sensory evolution and species diversification. It cannot be excluded, however, that selection for improved sensing was partially triggered by biotic interactions, e.g., in the context of niche competition, whereas ecospace expansion, especially during the Mesozoic, might also have played an important role. Expected final online publication date for the Annual Review of Earth and Planetary Sciences Volume 46 is May 30, 2018. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
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Ancestral character-state reconstruction is a powerful method in phylogenetics that can be applied to elucidate the evolutionary history of secondary sexual characters. Here, we surveyed the variation and reconstructed the ancestral states of secondary sexual characters (i.e. sexual dichromatism, vocal slits and nuptial pads) for the most species-rich genus of anurans (Pristimantis) using maximum parsimony, maximum-likelihood and Bayesian methods. This study demonstrates that at least five independent transformation series account for the occurrence of sexual dichromatism in Pristimantis: dorsum, throat, venter, groin and posterior surface of thighs. The ancestral reconstructions suggest that the most recent common ancestor of Pristimantis lacks sexual dichromatism on these five body areas. Likewise, the occurrence of vocal slits and the absence of nuptial pads were inferred as ancestral conditions. Morphological synapomorphies were identified for Yunganastes and two infrageneric units within Pristimantis (the Pristimantis devillei and Pristimantis unistrigatus species groups). Our results demonstrate that the evolutionary history of the secondary sexual characters in Pristimantis followed a rather complex pattern of multiple independent gains and losses for which this genus is a promising model to investigate the evolution of secondary sexual characters in the context of the complex interactions between natural and sexual selection.
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Acoustic communication, broadly distributed along the vertebrate phylogeny, plays a fundamental role in parental care, mate attraction and various other behaviours. Despite its importance, comparatively less is known about the evolutionary roots of acoustic communication. Phylogenetic comparative analyses can provide insights into the deep time evolutionary origin of acoustic communication, but they are often plagued by missing data from key species. Here we present evidence for 53 species of four major clades (turtles, tuatara, caecilian and lungfish) in the form of vocal recordings and contextual behavioural information accompanying sound production. This and a broad literature-based dataset evidence acoustic abilities in several groups previously considered non-vocal. Critically, phylogenetic analyses encompassing 1800 species of choanate vertebrates reconstructs acoustic communication as a homologous trait, and suggests that it is at least as old as the last common ancestor of all choanate vertebrates, that lived approx. 407 million years before present.
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Recently it was discovered that freshwater turtles communicate underwater by sound. The vocal repertoire of the Western Australian longneck turtle Chelodina colliei includes complex and percussive calls which are harmonically structured and frequency modulated, with dominant frequencies below 1 kHz and a range from around 100 to 3.5 kHz. Sounds with similar characteristics are used by the females of the South American river turtle Podocnemis expansa when migrating to nesting beaches and during communal nesting. Near term embryos inside eggs vocalize, and hatchlings emerging from nests and scampering across the beach and into the river continue to vocalize. In the water the adult females respond and the hatchlings then migrate with the females down the river, presumably to the flooded forests where they feed. Many unexplained aspects of aquatic turtles social behavior may eventually be explained when their vocalizations have been studied. © 2014 Springer Science+Business Media Dordrecht. All rights are reserved.
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In anurans, male clasps can elicit release calls from either sex. Male release calls have been observed in many anuran genera and this vocal response is thus highly conserved. Female release calls, however, are not as prevalent, suggesting that evolutionary trajectories for anuran release calls differ by sex. We analyzed male and female release calls in all available species of Xenopus, a fully aquatic African genus. Phylogenetic relationships in this genus include three species groups, two of which are clades and one of which is characterized by a reticulated phylogeny due in part to hybridizations between species with different ploidy levels (Evans et al., 2004; Evans, 2008). In all species, males produce release calls when clasped by another male. Females in the reticulated group do not produce release calls, but females in the rest of the genus do. Release calls consist of click trains of variable durations and inter-call intervals. In both sexes, inter-click interval divides the genus into groups with different click rates and these groups are phylogenetically related. In general, inter-click interval is shorter in male than in female release calls. Across species and sexes, release calls are characterized by a single, low (∼1000 Hz) dominant frequency. In X. laevis Congo and X. borealis, clasp duration is longer for male–female than for male–male pairs and clasp duration is correlated with the number, but not the duration, of release calls in male–male pairs. We discuss evolutionary scenarios for release call traits as well as the sex difference in occurrence.
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The social behavior of turtles during the nesting season can be attributed to a series of functions such as reducing predation, increasing hatchling survivorship, and information exchange between nesting females. However, the mechanism(s) used to remain in a group during the different phases of nesting behavior has yet to be explained. The objective of this study is to document the sounds produced by Giant South American River Turtle, Podocnemis expansa, during the nesting period, and identify how acoustic mechanisms might facilitate social behavior and group aggregation during this period. From September 2009 to October 2011, the sound repertoire of P. expansa was identified during the nesting period, which begins with the migration of the turtles from the flooded forests to the nesting beaches and terminates when the hatchlings emerge and the females migrate with the hatchlings to the flooded forests. Sounds were recorded when the turtles were active in different behavioral patterns (1) migrating; (2) aggregating in front of the nesting beaches before basking; (3) nesting at night; (4) waiting in the water without nesting or after they have nested; and (5) waiting for the arrival of the hatchlings. We observed six types of sound in the recordings of turtles made during the nesting period. These data indicate that this species is social, and that sound plays an important role in the synchronization of the activities of groups during the nesting season.
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Background: Two species of frog are currently known to produce high-frequency or even partly ultrasonic vocalizations, Odorrana tormota and Huia cavitympanum. Both possess special adaptations to their hearing system that extend their hearing into the high-frequency range. Typical stream-dwelling species of frog are not known to use high frequencies. Goal: To investigate the environmental conditions that may have led to the evolution of very high-frequency communication in some frog species. Method: Study auditory communication in Huia masonii, a frog of habitats next to fast-flowing streams on the island of Java, Indonesia. Study the tympanums of all members of the genus Huia. Measure the acoustic characteristics of fast-flowing water. Calculate water noise levels (amplitudes) at different distances from streamside. Results: All four members of the genus Huia possess a modified tympanal membrane, suggesting that high-frequency communication is present in all members. All frogs using high-frequency communication live along turbulent perennial streams. They all appear to be solitary callers and experience low encounter rates between partners. The high frequencies used by Huia improve signal detection and discrimination but only within 103 m of a noisy river; they are unsuited for long-range detection. Beyond 103 m of noisy rivers, communication using normal (low) frequencies is more advantageous.
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The rate of oxygen consumption (VO"2) of male Physalaemus pustulosus (mean mass 1.51 g) during 30 min of forced activity was 1.76 mL/h. The VO"2 sustained by males (mean mass 1.84 g) during @?3 min of intense activity was 3.34 mL/h. Formation of a foam nest by a pair, which includes oviposition and fertilization, involved consumption of 2.64 mL O"2. In terms of ATP yield, the energy contributions of anaerobiosis account for only 2-7% of the total energy expended during calling, nest building, and sustained forced activity. The energy content of nests plus eggs averaged 3.96 kJ. By combining the metabolic data with data on the reproductive pattern of the species, we estimate the total aerobically supported energy expenditure for reproduction by each sex over a breeding season. Females expend an order of magnitude more energy for reproduction than do males: 40.96 vs. 3.25 kJ. There are few comparative data available, but female Physalaemus expend slightly more energy per gram than do female lizards (Uta stansburiana) but slightly less energy than the lizards when energy expenditure is adjusted for the length of the breeding season. Male Physalaemus use much less energy for reproduction than male lizards (Uta stansburiana). Male Physalaemus also use less energy for reproduction per gram than do males of two speices of Australian frogs (Ranidella signifera and R. parinsignifera).
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We examined variation in calls and calling behavior in two populations of Bufo valliceps in south-central Texas. Both pulse rate of advertisement calls and call rate were positively related to body temperature, whereas call duration was negatively correlated with body temperature. Advertisement call frequency was not significantly correlated with toad temperature, but was negatively correlated with SVL. Of the temporal advertisement call variables, only call duration was significantly correlated (positively) with SVL. Release call frequency was negatively correlated with SVL. Field observations revealed significantly greater variation among than within males for call rate, call duration, and calling effort. However, despite the consistency of individual calling behavior, calling activity varied with social context. Calling effort was weakly, positively correlated with male density. Call rate and calling effort varied nonlinearly with nearest neighbor distance. Both variables were highest at intermediate distances (2.5-7.5 m), decreasing as nearest neighbors became very close (7.5 m).
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A high diversity of mating calls is found among frogs. The calls of most species, however, are simple, in comparison to those of mammals and birds. In order to determine if the mechanics of the larynx could explain the simplicity of treefrog calls, the larynges of euthanized males were activated with airflow. Laryngeal airflow, sound frequency, and sound intensity showed a positive direct relationship with the driving air pressure. While the natural calls of the studied species exhibit minimal frequency modulation, their larynges produced about an octave of frequency modulation in response to varying pulmonary pressure. Natural advertisement calls are produced near the higher extreme of frequency obtained in the laboratory and at a slightly higher intensity (6 dB). Natural calls also exhibit fewer harmonics than artificial ones, because the larynges were activated with the mouth of the animal open. The results revealed that treefrog larynges allow them to produce calls spanning a much greater range of frequencies than observed in nature; therefore, the simplicity of the calls is not due to a limited frequency range of laryngeal output. Low frequencies are produced at low intensities, however, and this could explain why treefrogs concentrate their calling at the high frequencies.
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Many sexual displays contain multiple components that are received through a variety of sensory modalities. Primary and secondary signal components can interact to induce novel receiver responses and become targets of sexual selection as complex signals. However, predators can also use these complex signals for prey assessment, which may limit the evolution of elaborate sexual signals. We tested whether a multimodal sexual display of the male túngara frog (Physalaemus pustulosus) increases predation risk from the fringe-lipped bat (Trachops cirrhosus) when compared with a unimodal display. We gave bats a choice to attack one of two frog models: a model with a vocal sac moving in synchrony with a mating call (multisensory cue), or a control model with the call but no vocal sac movement (unimodal cue). Bats preferred to attack the model associated with the multimodal display. Furthermore, we determined that bats perceive the vocal sac using echolocation rather than visual cues. Our data illustrate the costs associated with multimodal signaling and that sexual and natural selection pressures on the same trait are not always mediated through the same sensory modalities. These data are important when considering the role of environmental fluctuations on signal evolution as different sensory modalities will be differentially affected.
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Vocalizations of Boophis madagascariensis (Rhacophoridae) males were recorded in a mid-elevation rain forest in eastern Madagascar. Call notes made by males of this species were classi®ed into 28 types. This represents the largest known call repertoire of any amphibian. The calls range widely in spectral characteristics from a narrowband, nearly pure-tone to broadband `rip' notes, to even broader band, pulsatile `iambic' notes consisting of up to 23 pulses. Even considering all `iambic' notes as variants of one type, there remain eight distinct call notes produced by this species. Morphological analysis of the vocal musculature of B. madagascariensis revealed no obvious adaptations for unusual glottal ¯exibility or function. Playback studies using a subset of the call notes as stimuli were carried out in the animals' natural habitat to determine the functional signi®cance of several of the call notes. At the lowest playback levels, there was a signi®cant tendency for males to produce rip notes in immediate response to either rip or iambic note stimuli. At the higher playback levels, we identi®ed one sequence of iambic notes that consistently evoked a signi®cant iambic note response from males. A permutation test on call note transitions during spontaneous calling revealed that call note pairs occurred inconsistently and unpredictably. The evolutionary signi®cance of an extended vocal repertoire, matched counter-calling and a random call note production scheme is discussed.
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Mule white-lipped frogs exhibit conspicuous behavioral responses to culling conspecijk males that are nearby but out of view. Since the calls often are accompanied by strong seismic signals (thumps), and since the mule white-lipped frog exhibits the most acute sensitivity to seismic stimuli yet observed in any animal, these animals may use seismic signals us well as auditory signals fbr intraspeciJic communication.
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Undeniably, acoustic signals are the predominant mode of communication in frogs and toads. Acoustically active species are found throughout the vast diversity of anuran families. However, additional or alternative signal modalities have gained increasing attention. In several anurans, seismic, visual and chemical communications have convergently evolved due to ecological constraints such as noisy environments. The production of a visual cue, like the inevitably moving vocal sac of acoustically advertising males, is emphasized by conspicuously coloured throats. Limb movements accompanied by dynamic displays of bright colours are additional examples of striking visual signals independent of vocalizations. In some multimodal anuran communication systems, the acoustic component acts as an alert signal, which alters the receiver attention to the following visual display. Recent findings of colourful glands on vocal sacs, producing volatile species-specific scent bouquets suggest the possibility of integration of acoustic, visual and chemical cues in species recognition and mate choice. The combination of signal components facilitates a broadened display repertoire in challenging environmental conditions. Thus, the complexity of the communication systems of frogs and toads may have been underestimated.
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For most frogs, advertisement calls are essential for reproductive success, conveying information on species identity, male quality, sexual state and location. While the evolutionary divergence of call characters has been examined in a number of species, the relative impacts of genetic drift or natural and sexual selection remain unclear. Insights into the evolutionary trajectory of vocal signals can be gained by examining how advertisement calls vary in a phylogenetic context. Evolution by genetic drift would be supported if more closely related species express more similar songs. Conversely, a poor correlation between evolutionary history and song expression would suggest evolution shaped by natural or sexual selection. Here, we measure seven song characters in 20 described and two undescribed species of African clawed frogs (genera Xenopus and Silurana) and four populations of X. laevis. We identify three call types - click, burst and trill - that can be distinguished by click number, call rate and intensity modulation. A fourth type is biphasic, consisting of two of the above. Call types vary in complexity from the simplest, a click, to the most complex, a biphasic call. Maximum parsimony analysis of variation in call type suggests that the ancestral type was of intermediate complexity. Each call type evolved independently more than once and call type is typically not shared by closely related species. These results indicate that call type is homoplasious and has low phylogenetic signal. We conclude that the evolution of call type is not due to genetic drift, but is under selective pressure.
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Female mate choice preferences may be the result of innate factors, experience, or an interaction between the two mechanisms. Understanding the relative contribution and possible interaction between these mechanisms is important for identifying sources of variation in behaviors under sexual selection. In this study, we evaluate the contribution of early experience on the development of mate choice preferences in the Neotropical Túngara Frog, Physalaemus pustulosus. We reared frogs from tadpole stage through sexual maturity in four acoustic treatments: the first group heard a conspecific chorus of Túngara Frogs, the second group heard a heterospecific chorus of the closely related sympatric congener P. enesefae, the third group heard no frog sounds, and the fourth group heard only broadband white noise. At sexual maturity, we tested each female's preferences for conspecific complex vs simple calls and discrimination against calls of the sympatric congener. Female choices in all of these tests were consistent with those in previous studies of wild-caught and laboratory-reared specimens of this species. The acoustic rearing environments in this study did not alter the preferences of females for complex conspecific calls or the discrimination of females against the sympatric congener. This study supports the hypothesis that early experience does not alter the mate choice preferences of female P. pustulosus.
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Animal displays are often perceived by intended and unintended receivers in more than one sensory system. In addition, cues that are an incidental consequence of signal production can also be perceived by different receivers, even when the receivers use different sensory systems to perceive them. Here we show that the vocal responses of male túngara frogs (Physalaemus pustulosus) increase twofold when call-induced water ripples are added to the acoustic component of a rival’s call. Hunting bats (Trachops cirrhosus) can echolocate this signal by-product and prefer to attack model frogs when ripples are added to the acoustic component of the call. This study illustrates how the perception of a signal by-product by intended and unintended receivers through different sensory systems generates both costs and benefits for the signaler.
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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.
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The structural variation of the gekkonid larynx and trachea is examined within a representative subset of 17 species of Afro-Madagascan gekkonines to determine if there are underlying morphological correlates of vocalization. The documented morphology is compared to that of the tokay (Gekko gecko), which has previously been described. Data were obtained from gross anatomical observations, scanning electron microscopy, histological examinations and computer-generated, three-dimensional, skeletal reconstructions. Although there is limited variation among most Afro-Malagasy gekkonids, the larynges of Ptenopus garrulus and Uroplatus fimbriatus exhibit marked degrees of differentiation, suggesting that laryngeal and tracheal morphology may account for the documented vocal variability of gekkonid lizards. Cladistic analyses indicated that parallel adaptive trends characterize the laryngeal morphology of the examined taxa. Alternate designs and refinements to a model of gekkonid phonation are presented, and the evolution of acoustic communication in the Gekkonidae is considered. J. Morphol. 245:241–268, 2000 © 2000 Wiley-Liss, Inc.
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The fourth edition of the textbook Herpetology covers the basic biology of amphibians and reptiles, with updates in nearly every conceptual area. Not only does it serve as a solid foundation for modern herpetology courses, but it is also relevant to courses in ecology, behavior, evolution, systematics, and morphology. Examples taken from amphibians and reptiles throughout the world make this book a useful herpetology textbook in several countries. Naturalists, amateur herpetologists, herpetoculturists, zoo professionals, and many others will find this book readable and full of relevant natural history and distributional information. Amphibians and reptiles have assumed a central role in research because of the diversity of ecological, physiological, morphological, behavioral, and evolutionary patterns they exhibit. This fully revised edition brings the latest research to the reader, ranging over topics in evolution, reproduction, behavior and more, allowing students and professionals to keep current with a quickly moving field.
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We studied the signaling, territorial, and courtship behaviors of the diurnal frog Hylodes asper. Visual and acoustic communication were used during intraspecific interactions involving males, females, and subadults. Hylodes asper has a complex visual communication system, of which foot-flagging is the most distinctive display observed in the repertoire of visual signals. The splash zone produced by the waterfalls and torrents creates a high, nearly constant, humidity near the streams, reducing the risk of desiccation which enables the diurnal activity of H. asper. Although the ambient sound pressure levels (SPL), measured at the calling sites, are similar to the SPL of the advertisement calls, the high-pitched calls of H. asper are spectrally different from the noise produced by the water current. Thus, the ambient noise produced by the water current may not interfere significantly with the acoustic communication of this species. The noise and the nearly constant and high humidity produced by the torrents and waterfalls, along with the availability of light, probably favored the evolution of contrasting colors and visual communication in H. asper. Males of H. asper excavate underwater chambers that are probably used to shelter the eggs and to prevent the clutch from being drifted downstream.
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The authors have collected specimens of Geotrypetes grandisonae Taylor (Amphibia Gymnophiona Caeciliidae) from additional localities within the area from which the species was described by TAYLOR (1970a). The distinctive characters of the species are here described in greater detail together with some observations on its behaviour and ecology. The authors agree with TAYLOR that G. grandisonae is a very distinctive member of the genus.
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Males (mean mass 1.7 g) called and amplexing pairs built foam nests in respirometer chambers. Mean oxygen consumption () of resting males during the day was 0.26 ml h⁻¹, and at night it was 0.53 ml h⁻¹. Mean of males that could hear other males calling but that were not themselves calling was 0.70 ml h⁻¹. Mean of calling males was 1.13 ml h⁻¹. The energy cost per call (whine) decreases as whine rate increases. Mean per frog during nest building was 2.03 ml h⁻¹. The individual energy cost incurred by male and female during nest building could not be separated. The data on oxygen consumption during sustained calling and nest building offer an opportunity for measuring voluntarily sustained elevated levels of aerobic metabolism in anurans. During calling and nest building mean aerobic metabolic scope was 1.23 and 1.67 ml h⁻¹, respectively. The corresponding factorial scope of about 5.7 is within the range of published values for anurans undergoing forced activity. Because there is a high energy cost associated with reproductive activities in Physalaemus, and presumably in other anurans, any interpretations of aerobic and anaerobic metabolic patterns in frogs and toads should take into account reproductive, as well as predatory and escape, behavior.
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Results do not support the hypothesis that differences in the behavior of males in a chorus are due to differences in their physiological capacities to use energy. -from Authors
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The advertisement call of Dermatonotus muelleri was originally described by Nelson (1973) in a brief section of a review on the mating calls of the Microhylinae. He used two calls from São Leopoldo, state of Minas Gerais, in Brazil to determine that they have i) dominant frequency between 1.500-2.200 kHz (mean 1.854 + 0.216 kHz), and ii) harmonic intervals between 0.140 and 0.150 kHz (0.146 +/- 0.005 kHz). Nelson (1973) based his description on an audiospectrogram produced with high frequency resolution and did not quantify the pulse structure of the calls. More recently, Giaretta and colleagues (2013) expanded on the original description using a larger set of calls recorded from Gurinhat, state of Minas Gerais, in Brazil. They quantified the temporal structure of the call and confirmed that the dominant frequency is around 1.8 kHz. In addition, they identified a secondary low frequency band at 667 Hz.
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Males of Physalaemus pustulosus are capable of producing two sounds simultaneously. All other known cases of complex frog calls are instances of the different sounds being produced serially. Comparison of call analyses and laryngeal morphology among Physalaemus gracilis, P. olfersi and P. pustulosus leads to the conclusion that the two sounds are produced by separate vibrating structures in the larynx. Lateral passageways bypassing the median free edges of the vocal cords in all three of these species are described, a feature not previously reported for any anuran larynx. A mechanism is suggested that integrates the available knowledge into a hypothesis of call production in P. pustulosus.
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The vocal communication of Hyla microcephala was studied in central Panama. We recorded natural interactions between males and conducted playback experiments using conspecific and heterospecific calls. Males employ both advertisement and aggressive calls which consist of a buzz-like introductory note often followed by secondary click notes. Advertisement calls show little variation in temporal features, whereas aggressive calls are quite variable. Playback of both conspecific advertisement calls and aggressive calls at high intensity elicited a significant increase in aggressive calling. Males increased the duration of aggressive call introductory notes in response to increasing playback intensity. Aggressive calls with long introductory notes were also used during close vocal or physical encounters with both conspecific males and H. ebraccata. In most cases, playback of heterospecific calls were ineffective in eliciting increased aggressive calling. Males synchronized and often added click notes to advertisement calls in response to conspecific and heterospecific calls. Call playbacks also elicited an increase in calling rate. When interrupted, males often abruptly terminated calls or added secondary notes to them. Males typically alternate individual notes in overlapping calls. Internote intervals in overlapping multi-note calls are longer than those in non-overlapping calls, reducing the probability of note overlap.
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Biting acocmpanied by the exhibition of white mouth lining and audible snapping of the jaws by Desmognathus quadramaculatus effectively repels predatory attacks by the shrew Blarina brevicauda. In other species of terrestrial salamanders vocalizations are present in species which also have noxious or toxic skin secretions. A predator that relies on hearing to locate prey could learn to avoid these vocalizations.
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Laryngeal movements were observed directly in Rana pipiens during release calling. Electromyograms from the intrinsic muscles of the larynx were recorded in Rana pipiens during release calling and Hyla cinerea and Hyla versicolor during mating calling. Laryngeal call movements consist of a vocal phase followed by a respiratory phase. Glottal opening during calling is regulated actively by central nervous control of the intrinsic laryngeal muscles and not passively by air pressure from the lungs. One method of trill production involves glottal opening due to contraction of the dilator muscles with simultaneous, periodic contraction of the constrictor muscles, causing glottal closures that break the call into trills.
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Foraging success of Eleutherodactylus coqui was estimated from stomach contents. Stomach content volume increased with frog body size as a result of the selection of larger prey by larger frogs. Number of prey per stomach was inversely related to body size. Non-calling frogs had eaten most of their night's food by 2400 h. Males called mainly before midnight and did not forage while calling. Calling males had eaten only 18% of their night's food by 2400 h. Calling males ate prey that did not differ in size from those of non-calling animals. However, they ate fewer prey items and ended the night with less food volume in their stomachs than expected for their body sizes. Foraging success of all groups was reduced during the dry season. The reduction was less pronounced for calling males because they spend less time calling in the dry season than in the wet season. On a yearly basis, males appear to lose 16% of their potential food intake because of calling activity.
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Calling male Physalaemus pustulosus (Leptodactylidae) and a synchronously displayed oscilloscope trace of the call were filmed with a video camera. Simultaneous records of vocal sac inflation and the waveform of the advertisement call were obtained. Abdominal dimensions decrease and vocal sac dimensions increase continuously through a call. The sac deflates much more rapidly than it inflates, and may be recoiling elastically. Vocal sacs increase in volume by an estimated factor of 20-40 during the course of a call. During the initial portion of the call (the whine), the rate of volumetric increase of the expanding vocal sac decreases concurrently with a drop in call frequency and amplitude. Amplitude and frequency modulation of the whine may thus arise from a decreased flow rate past the vocal cords, in addition to previously postulated changes in vocal cord tension. The dynamic characteristics of vocal sacs must be accounted for in future acoustic, behavioral, and physiological interpretations of vocal sac function.
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Tape-recorded advertisement calls of Gastrophryne carolinensis and G. olivacea, obmined in Texas and southern Louisiana, were analyzed by means of an analogue andiospectrograph. Samples were grouped into four areas: allopatric and sympatric for G. carolinensis, and combined adjacent allopatric/shallow sympatric, and sympatric for G. olivacea. Three attributes of the advertisement call (call duration, pulse rate, and dominant frequency) were investigated, with water temperature at the calling site as the independent variable. Values for dominant frequency do not overlap between species, across the full range of recording temperatures, and those of sympatric G. carolinensis are displaced away from those of both groups of G. olivacea (which are very similar) -thus indicating a pattern of geographic variation consistent with reproductive character displacement. There ts considerable overlap in the values for duration and for pulse rate of each species when considered alone, but there is only slight overlap of the scatters of points for the pairs of values. For both species, no consistent patterns of correlation were detected between the three attributes of the call and the snout-vent length of the emitter, thus reducing the likelihood that the divergence in calls is due to pleiotropic effects of body size.
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Vocal repertoire and associated behavior of geckos in captivity were observed, recorded and analysed. Juveniles, females and males vocalized. Calls varied with the type of interaction. Juveniles made three types of escape squeaks. Females had four types of squeaks emitted in various kinds of interactions with other individuals and so did males. The structure and context of the squeaks of males differed from those of females. The advertisement multiple click call of males to other males differed from those produced to females.
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The mechanism and pattern of ventilation in unrestrained Rana pipiens were investigated by simultaneous measurements of pulmonary pressure, buccal pressure and air flow at the nostrils. The buccal cavity was ventilated continuously at a rate of 90±3.2oscillations min" 1 by low-amplitude pressure swings above and below atmospheric. The lungs were ventilated intermittently by the buccal pump at a rate of 6.3±0.8breathsmin~ 1 . Expiration of gas from the nostrils occurred on two occasions during a lung ventilation. Ventilation of the lungs was achieved by precise timing of two valves, the nostrils and glottis. The timing of the valves determined the volume of expiratory flow on these two occasions and its relationship to inspiratory flow. Thus, the breathing movements could cause inflation, deflation, or no change in the lung volume. Periodically the lung was inflated by a sequence of successive breaths. During inflations the nostrils closed simultaneously with glottal opening and almost no gas was expired during the first expiratory phase. This caused a complete mixing of buccal contents and pulmonary gas and this mixture was pumped back into the lung. Deflations were characterized by a delay in nostril closing that resulted in a large outflow of gas from the lung and buccal cavity during the first phase of expiration. More gas left the system than was pumped into the lungs. The results suggest that coherent air flow from glottis to nostrils, as required by the 'jet stream' hypothesis of Gans etal. (1969), is not likely to occur.
Article
A widely cited yet unproven function for anuran vocal sacs is that of cavity resonance and call tuning during vocalization. Because resonant frequency is influenced by the speed of sound within the cavity, we replaced a substantial proportion of the air in the anuran vocal tract with heliox (80% He/20% O₂), a medium in which the speed of sound is approximately 75% faster than in a normal atmosphere. Such a manipulation will increase energy in higher call frequencies, provided that cavity resonance is present. In a heliox atmosphere, no consistent or predictable change in the frequency distribution of sound energy was observed in the advertisement calls of two hylids and one leptodactylid or in the release call of a bufonid. Therefore, the call characteristics of the anurans in this study do not arise from cavity resonance in the vocal sac or other supralaryngeal structures. The anuran vocal sac may have a variety of acoustic and nonacoustic functions, but that of cavity resonator can now be excluded in the species examined here and is unlikely to be found in other anurans.
Article
This work presents a comparison across selected species of several aspects of the mechanism of sound broadcasting in anuran amphibians. These studies indicate that all anuran species studied to date broadcast their calls through structures that resonate at the dominant frequency in their calls. Measurements of the magnitude of the transfer function of the radiating structures show that the structures responsible for radiating the bulk of the energy present in the call vary depending on the species considered. Bullfrogs (Rana catesbeiana) radiate most of the energy (89% sound level) present in their calls through their eardrums. In this species the transfer function of the eardrum displays several peaks coincident in frequency and amplitude with the energy distribution observed in the mating and release call of the species. The vocal sac and gular area contribute energy only in the lower band (150 to 400 Hz) of the call. The ears are responsible for radiating additional frequency bands to the ones being radiated through the gular area and vocal sacs. This condition appears to be derived. In Rana pipiens the ears also broadcast a significant portion of the energy present in the call (63% sound level) but the frequencies of the aural emissions are a subset of those frequencies radiated through the vocal sac and gular area. Character optimization suggests that this is the primitive condition for ranid frogs. Finally, the barking treefrog (Hyla gratiosa) appears to use two different structures to radiate different portions of the call. The low frequency band appears to be preferentially radiated through the lungs while the high frequency components of the call are radiated through the vocal sac.
Article
This paper summarises evidence for low rates of annual reproductive output (no. of offspring or eggs/female/yr) in New Zealand reptiles. Tuatara (Sphenodon spp.) and the geckos Hoplodactylus maculatus and H. duvaucelii are cold‐adapted, nocturnal, and long‐lived, with evidence in at least some populations of less‐than‐annual reproduction. Annual reproductive output estimated for three tuatara populations ranges from 1.27 to 2.28 eggs/ female/yr. New Zealand geckos produce ≤2 offspring/female/yr. Hoplodactylus maculatus in the Macraes‐Middlemarch region of Central Otago produces only about 0.85 offspring/female/yr, as a consequence of biennial reproduction and clutch sizes that are often less than two. The diurnal skinks Leiolopisma grande and L. otagense from the same region breed annually and have larger clutch sizes, so their annual reproductive output is higher (2.17 and 2.34 offspring/female/yr, respectively). Other wild populations of New Zealand skinks typically produce 1–5 offspring/female/yr. Unlike many species of oviparous geckos overseas, the viviparous New Zealand geckos do not produce multiple clutches per year, and this contributes to relatively low annual reproductive output in some species. Viviparous New Zealand skinks have similar annual reproductive output to viviparous skinks of similar body size from other parts of the world. Low annual reproductive output in New Zealand lizards thus appears to reflect, in part, responses to cool summer temperatures in association with a viviparous reproductive mode (geckos), as well as phylogenetic effects (colonisation by lineages of small clutch and body size, in geckos and skinks).