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To humans, the diverse array of display behaviors that animals use for communication can easily seem peculiar or bizarre. While ample research delves into the evolutionary principles that shape these signals' effectiveness, little attention is paid to evolutionary patterning of signal design across taxa, particularly when it comes to the potential convergent evolution of many elaborate behavioral displays. By taking a mechanistic perspective, we explore the physiological and neurobiological mechanisms that likely influence the evolution of communication signals, emphasizing the utilization of pre-existing structures over novel adaptations. Central to this investigation are the concepts of perceptual bias and ritualization, which we propose contribute to the convergence of elaborate display designs across species. Perceptual bias explains a phenomenon where pre-existing perceptual systems of receivers, used for innate behaviors such as food and predator recognition, select for certain traits of a communication signal from a signaler. Ritualization occurs when traits with no functional role in communication are co-opted through selection and transformed into a new communicative signal. Importantly, susceptibility for ritualization can be brought about through physiological modifications that occurred early in evolutionary time. In this way, perceptual bias can be a selective force that causes the co-option of non-communicative traits into a new communication signal through ritualization involving pre-existing modifications to physiological systems. If the perceptual bias, non-communicative signal, and physiological modifications that increase susceptibility to ritualization are highly conserved, then we may see the convergent evolution of the new communication signal with unrelated taxa facing similar sensory constraints. We explore this idea here using the foot-flagging frog system as a theoretical case study.
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Ventilation is critical to animal life-it ensures that individuals move air/water across their respiratory surface, and thus it sustains gas exchange with the environment. Many species have evolved highly specialized (if not unusual) ventilatory mechanisms, including the use of behavior to facilitate different aspects of breathing. However, these behavioral traits are often only described anecdotally, and the ecological conditions that elicit them are typically unclear. We study one such "ventilation behavior" in Lake Titicaca frogs (Telmatobius culeus). These frogs inhabit high-altitude (i.e., low oxygen) lakes in the Andean Mountains of South America, and they have become textbook examples of cutaneous gas exchange, which is essentially breathing that occurs across the skin. Accordingly, this species has evolved large, baggy skin-folds that dangle from the body to increase the surface area for ventilation. We show that individuals exposed to acute hypoxic conditions that mirror what free-living individuals likely encounter quickly (within minutes) decrease their activity levels, and thus become very still. If oxygen levels continue to decline, the frogs soon begin to perform push-up behaviors that presumably break the low-oxygen boundary layer around skin-folds to increase the conductance of the water/skin gas exchange pathway. Altogether, we suspect that individuals rapidly adjust aspects of their behavior in response to seemingly sudden changes to the oxygen environment as a mechanism to fine tune cutaneous respiration.
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Anuros , Comportamento Animal , Animais , Anuros/fisiologia , Comportamento Animal/fisiologia , Hipóxia/fisiopatologia , Lagos , Oxigênio , Respiração , Pele , Fenômenos Fisiológicos da Pele , AltitudeRESUMO
Amphibians globally suffer from emerging infectious diseases like chytridiomycosis caused by the continuously spreading chytrid fungi. One is Batrachochytrium salamandrivorans (Bsal) and its disease â the 'salamander plague' â which is lethal to several caudate taxa. Recently introduced into Western Europe, long distance dispersal of Bsal, likely through human mediation, has been reported. Herein we study if Alpine salamanders (Salamandra atra and S. lanzai) are yet affected by the salamander plague in the wild. Members of the genus Salamandra are highly susceptible to Bsal leading to the lethal disease. Moreover, ecological modelling has shown that the Alps and Dinarides, where Alpine salamanders occur, are generally suitable for Bsal. We analysed skin swabs of 818 individuals of Alpine salamanders and syntopic amphibians at 40 sites between 2017 to 2022. Further, we compiled those with published data from 319 individuals from 13 sites concluding that Bsal infections were not detected. Our results suggest that the salamander plague so far is absent from the geographic ranges of Alpine salamanders. That means that there is still a chance to timely implement surveillance strategies. Among others, we recommend prevention measures, citizen science approaches, and ex situ conservation breeding of endemic salamandrid lineages.
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Batrachochytrium , Micoses , Urodelos , Animais , Batrachochytrium/genética , Batrachochytrium/patogenicidade , Micoses/veterinária , Micoses/microbiologia , Micoses/epidemiologia , Urodelos/microbiologia , Doenças Transmissíveis Emergentes/microbiologia , Doenças Transmissíveis Emergentes/epidemiologia , Doenças Transmissíveis Emergentes/veterinária , Salamandra/microbiologia , Europa (Continente)/epidemiologia , QuitridiomicetosRESUMO
How diverse animal communication signals have arisen is a question that has fascinated many. Xenopus frogs have been a model system used for three decades to reveal insights into the neuroendocrine mechanisms and evolution of vocal diversity. Due to the ease of studying central nervous system control of the laryngeal muscles in vitro, Xenopus has helped us understand how variation in vocal communication signals between sexes and between species is produced at the molecular, cellular, and systems levels. Yet, it is becoming easier to make similar advances in non-model organisms. In this paper, we summarize our research on a group of frog species that have evolved a novel hind limb signal known as 'foot flagging.' We have previously shown that foot flagging is androgen dependent and that the evolution of foot flagging in multiple unrelated species is accompanied by the evolution of higher androgen hormone sensitivity in the leg muscles. Here, we present new preliminary data that compare patterns of androgen receptor expression and neuronal cell density in the lumbar spinal cord - the neuromotor system that controls the hind limb - between foot-flagging and non-foot-flagging frog species. We then relate our work to prior findings in Xenopus, highlighting which patterns of hormone sensitivity and neuroanatomical structure are shared between the neuromotor systems underlying Xenopus vocalizations and foot-flagging frogs' limb movement and which appear to be species-specific. Overall, we aim to illustrate the power of drawing inspiration from experiments in model organisms, in which the mechanistic details have been worked out, and then applying these ideas to a non-model species to reveal new details, further complexities, and fresh hypotheses.
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Androgênios , Comunicação Animal , Evolução Biológica , Animais , Androgênios/farmacologia , Vocalização Animal/fisiologia , Vocalização Animal/efeitos dos fármacos , Masculino , Anuros/fisiologia , Feminino , Xenopus/fisiologia , Membro Posterior/fisiologia , Receptores Androgênicos/metabolismo , Receptores Androgênicos/fisiologia , Medula Espinal/efeitos dos fármacos , Medula Espinal/fisiologia , Medula Espinal/metabolismoRESUMO
Zhao et al. recently reported results which, they claim, suggest that sexual selection produces the multimodal displays seen in little torrent frogs (Amolops torrentis) by co-opting limb movements that originally evolved to support parasite defense (Zhao et al., 2022). Here, we explain why we believe this conclusion to be premature.
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Parasitos , Animais , Masculino , Anuros , Ranidae , AcústicaRESUMO
Many animals use forms of gesture and dance to communicate with conspecifics in the breeding season, though the mechanisms of this behavior are rarely studied. Here, we investigate the hormone basis of such visual signal behavior in Bornean rocks frogs (Staurois parvus). Our results show that males aggregating at breeding waterfalls have higher testosterone (T) levels, and we speculate that this hormone increase is caused by social cues associated with sexual competition. To this end, we find that T levels in frogs at the waterfall positively predict the number waving gestures-or "foot flags"-that males perform while competing with rivals. By contrast, T does not predict differences in male calling behavior. In these frogs, vocal displays are used largely as an alert signal to direct a rival's attention to the foot flag; thus, our results are consistent with the view that factors related to reproductive context drive up T levels to mediate displays most closely linked to male-male combat, which in this case is the frog's elaborate gestural routine.
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Androgênios , Gestos , Animais , Masculino , Comportamento Sexual Animal/fisiologia , Anuros/fisiologia , Ranidae/fisiologia , Testosterona , Comportamento SocialRESUMO
Elaborate and skilled movements of the body have been selected in a variety of species as courtship and rivalry signals. One roadblock in studying these behaviors has been a lack of resources for understanding how they evolved at the genetic level. The Bornean rock frog (Staurois parvus) is an ideal species in which to address this issue. Males wave their hindlimbs in a "foot-flagging" display when competing for mates. The evolution of foot flagging in S. parvus and other species is accompanied by increases in the expression of the androgen receptor gene within its neuromuscular system, but it remains unclear what genetic or transcriptional changes are associated with this behavioral phenotype. We have now assembled the genome of S. parvus, resulting in 3.98 Gbp of 22,402 contigs with an N50 of 611,229 bp. The genome will be a resource for finding genes related to the physiology underlying foot flagging and to adaptations of the neuromuscular system. As a first application of the genome, we also began work in comparative genomics and differential gene expression analysis. We show that the androgen receptor is diverged from other anuran species, and we identify unique expression patterns of genes in the spinal cord and leg muscle that are important for axial patterning, cell specification and morphology, or muscle contraction. This genome will continue to be an important tool for future -omics studies to understand the evolution of elaborate signaling behaviors in this and potentially related species.
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Anuros , Receptores Androgênicos , Animais , Masculino , Receptores Androgênicos/genética , Anuros/genética , Genômica , GenomaRESUMO
Many animals communicate by rapidly (within minutes or seconds) changing their body coloration; however, we know little about the physiology of this behaviour. Here we study how catecholaminergic hormones regulate rapid colour change in explosive breeding toads (Duttaphrynus melanostictus), where large groups of males gather and quickly change their colour from brown to bright yellow during reproduction. We find that both epinephrine (EP) and/or norepinephrine (NE) cause the toads' skin to become yellow in minutes, even in the absence of social and environmental cues associated with explosive breeding. We hypothesize that natural selection drives the evolution of rapid colour change by co-opting the functional effects of catecholaminergic action. If so, then hormones involved in 'fight or flight' responses may mechanistically facilitate the emergence of dynamic visual signals that mediate communication in a sexual context.
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Substâncias Explosivas , Masculino , Animais , Cor , Bufonidae , Epinefrina , Norepinefrina , HormôniosRESUMO
Sex steroids play an important role in regulation of the vertebrate reproductive phenotype. This is because sex steroids not only activate sexual behaviors that mediate copulation, courtship, and aggression, but they also help guide the development of neural and muscular systems that underlie these traits. Many biologists have therefore described the effects of sex steroid action on reproductive behavior as both "activational" and "organizational," respectively. Here, we focus on these phenomena from an evolutionary standpoint, highlighting that we know relatively little about the way that organizational effects evolve in the natural world to support the adaptation and diversification of reproductive behavior. We first review the evidence that such effects do in fact evolve to mediate the evolution of sexual behavior. We then introduce an emerging animal model - the foot-flagging frog, Staurois parvus - that will be useful to study how sex hormones shape neuromotor development necessary for sexual displays. The foot flag is nothing more than a waving display that males use to compete for access to female mates, and thus the neural circuits that control its production are likely laid down when limb control systems arise during the developmental transition from tadpole to frog. We provide data that highlights how sex steroids might organize foot-flagging behavior through its putative underlying mechanisms. Overall, we anticipate that future studies of foot-flagging frogs will open a powerful window from which to see how sex steroids influence the neuromotor systems to help germinate circuits that drive signaling behavior. In this way, our aim is to bring attention to the important frontier of endocrinological regulation of evolutionary developmental biology (endo-evo-devo) and its relationship to behavior.
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Comportamento Reprodutivo , Comportamento Sexual Animal , Animais , Masculino , Feminino , Comportamento Sexual Animal/fisiologia , Anuros , Hormônios Esteroides Gonadais/farmacologia , Hormônios Esteroides Gonadais/fisiologia , EsteroidesRESUMO
Many animals communicate by performing elaborate displays that are incredibly extravagant and wildly bizarre. So, how do these displays evolve? One idea is that innate sensory biases arbitrarily favour the emergence of certain display traits over others, leading to the design of an unusual display. Here, we study how physiological factors associated with signal production influence this process, a topic that has received almost no attention. We focus on a tropical frog, whose males compete for access to females by performing an elaborate waving display. Our results show that sex hormones like testosterone regulate specific display gestures that exploit a highly conserved perceptual system, evolved originally to detect 'dangerous' stimuli in the environment. Accordingly, testosterone makes certain gestures likely to appear more perilous to rivals during combat. This suggests that hormone action can interact with effects of sensory bias to create an evolutionary optimum that guides how display exaggeration unfolds.
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Gestos , Testosterona , Animais , Anuros , Viés , Evolução Biológica , Feminino , Masculino , Testosterona/farmacologiaRESUMO
AbstractUnrelated species often evolve similar phenotypic solutions to the same environmental problem, a phenomenon known as convergent evolution. But how do these common traits arise? We address this question from a physiological perspective by assessing how convergence of an elaborate gestural display in frogs (foot-flagging) is linked to changes in the androgenic hormone systems that underlie it. We show that the emergence of this rare display in unrelated anuran taxa is marked by a robust increase in the expression of androgen receptor (AR) messenger RNA in the musculature that actuates leg and foot movements, but we find no evidence of changes in the abundance of AR expression in these frogs' central nervous systems. Meanwhile, the magnitude of the evolutionary change in muscular AR and its association with the origin of foot-flagging differ among clades, suggesting that these variables evolve together in a mosaic fashion. Finally, while gestural displays do differ between species, variation in the complexity of a foot-flagging routine does not predict differences in muscular AR. Altogether, these findings suggest that androgen-muscle interactions provide a conduit for convergence in sexual display behavior, potentially providing a path of least resistance for the evolution of motor performance.
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Comportamento Sexual Animal , Animais , Anuros/genética , Evolução Biológica , Expressão Gênica , FenótipoRESUMO
Multimodal communication is common in the animal kingdom. It occurs when animals display by stimulating two or more receiver sensory systems, and often arises when selection favors multiple ways to send messages to conspecifics. Mechanisms of multimodal display behavior are poorly understood, particularly with respect to how animals coordinate the production of different signals. One important question is whether all components in a multimodal display share an underlying physiological basis, or whether different components are regulated independently. We investigated the influence of androgen receptors (ARs) on the production of both visual and vocal signal components in the multimodal display repertoire of the Bornean rock frog (Staurois parvus). To assess the role of AR in signal production, we treated reproductively active adult males with the antiandrogen flutamide (FLUT) and measured the performance of each component signal in the multimodal display. Our results show that blocking AR inhibited the production of multiple visual signals, including a conspicuous visual signal known as the "foot flag," which is produced by rotating the hind limb above the body. However, FLUT treatment caused no measurable change in vocal signaling behavior, or in the frequency or fine temporal properties of males' calls. Our study, therefore, suggests that activation of AR is not a physiological prerequisite to the coordination of multiple signals, in that it either does not regulate all signaling behaviors in a male's display repertoire or it does so only in a context-dependent manner.
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Comunicação Animal , Ranidae/fisiologia , Receptores Androgênicos , Comportamento Sexual Animal , Animais , Membro Posterior , Masculino , Receptores Androgênicos/fisiologiaRESUMO
Indian fruit bats, flying fox Pteropus medius was identified as an asymptomatic natural host of recently emerged Nipah virus, which is known to induce a severe infectious disease in humans. The absence of P. medius genome sequence presents an important obstacle for further studies of virus-host interactions and better understanding of mechanisms of zoonotic viral emergence. Generation of the high-quality genome sequence is often linked to a considerable effort associated to elevated costs. Although secondary scaffolding methods have reduced sequencing expenses, they imply the development of new tools for the integration of different data sources to achieve more reliable sequencing results. We initially sequenced the P. medius genome using the combination of Illumina paired-end and Nanopore sequencing, with a depth of 57.4x and 6.1x, respectively. Then, we introduced the novel scaff2link software to integrate multiple sources of information for secondary scaffolding, allowing to remove the association with discordant information among two sources. Different quality metrics were next produced to validate the benefits from secondary scaffolding. The P. medius genome, assembled by this method, has a length of 1,985 Mb and consists of 33,613 contigs and 16,113 scaffolds with an NG50 of 19 Mb. At least 22.5% of the assembled sequences is covered by interspersed repeats already described in other species and 19,823 coding genes are annotated. Phylogenetic analysis demonstrated the clustering of P. medius genome with two other Pteropus bat species, P. alecto and P. vampyrus, for which genome sequences are currently available. SARS-CoV entry receptor ACE2 sequence of P. medius was 82.7% identical with ACE2 of Rhinolophus sinicus bats, thought to be the natural host of SARS-CoV. Altogether, our results confirm that a lower depth of sequencing is enough to obtain a valuable genome sequence, using secondary scaffolding approaches and demonstrate the benefits of the scaff2link application. The genome sequence is now available to the scientific community to (i) proceed with further genomic analysis of P. medius, (ii) to characterize the underlying mechanism allowing Nipah virus maintenance and perpetuation in its bat host, and (iii) to monitor their evolutionary pathways toward a better understanding of bats' ability to control viral infections.
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The external morphology of two molecularly identified tadpoles of the genus Staurois, S. parvus and S. tuberilinguis is described. These tadpoles display a typical fossorial morphology characterized by a strongly depressed body, small subcutaneous eyes, a vermiform appearance with a long tail and reduced fins, a nearly pigmentless skin, a KRF of 1:1+1 on the upper labium and numerous keratodont rows on the lower one. The two species can be distinguished by several morphological differences, the most conspicuous are the eye condition (not bulging and covered by skin in S. tuberilinguis) and the presence of numerous white isolated acini on the body and tail in S. parvus. These differences support the specific status of S. parvus relatively to S. tuberilinguis despite low genetic divergence between these two taxa. The morphology of these tadpoles, as well as the buccopharyngeal anatomy of S. parvus, are compared to those of the tadpoles in the family Centrolenidae and the definition of the fossorial ecomorphological guild is updated.
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Ranidae , Animais , Bornéu , LarvaRESUMO
In cities and densely populated areas, several corvid species are considered nuisance animals. In Austria, particularly carrion (Corvus corone) and hooded crows (C. cornix) are regarded as pests by the general public that frequently cause damage to crops, feed on human waste, and thus spread trash. We conducted a detailed one-year field survey to estimate the abundance of carrion crows in relation to potential anthropogenic food sources and reference sites in the Austrian Rhine valley. Our results demonstrated that the number and proximity of waste management facilities, animal feeding areas, and agricultural areas, and the productive capacity of agricultural areas, predominantly influenced habitat choice and abundance of carrion crows. In the current study, the probability of observing more than two carrion crows at a survey site decreased with increasing human population density. Moreover, the abundance of crows increased despite a continuous increase in crow hunting kills registered during the past 25 years. Our study suggests a regionally comprehensive waste management plan could serve as a promising strategy to manage nuisance birds. A reduction in anthropogenic food supply through improved waste management practices is required for long-term, sustainable management to limit the abundance of crow populations in and close to urban environments.
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The giant pandas' (Ailuropoda melanoleuca) reproductive strategy is unique among mammals. Yet there are characteristics of giant panda behaviour we do not fully understand. Probably one of the least understood is the assumption that in captivity virtually all giant panda females rear only one cub when twins are born and abandon the other if given the chance. So far, only two females have raised twins simultaneously, but just with intensive human assistance. This case-study marks the first successful rearing of giant panda twins in captivity entirely by the mother. Using video data for detailed behavioural observations, we provide the first behavioural assessment of a giant panda female raising two cubs simultaneously without direct human assistance or disturbance. We compared the maternal behaviour during the denning period of twin cubs raised in 2016 with two singleton cubs born 2007 and 2010. YANG YANG, the dam, rested less and interacted more with the twins than with the singletons in the first month postpartum and invested a greater part of her daily time budget on rearing the twins. We discuss potential favourable factors for the autonomous twin-rearing of a female giant panda, which could serve as a model for similar efforts elsewhere.
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Animais de Zoológico/fisiologia , Reprodução/fisiologia , Ursidae/fisiologia , Animais , Áustria , Feminino , MasculinoRESUMO
In the majority of anuran species, acoustic signals are the dominant mode of inter- and intrasexual communication. Male calls are always accompanied by the movement of a more or less conspicuous vocal sac-a potential visual cue. Reed frogs possess a striking vocal sac with a colorful patch of gland tissue clearly visible once the vocal sac is inflated during acoustic signaling. To investigate the visual signal function of vocal sac and gular gland, we presented male Spotted Reed Frogs (Hyperolius puncticulatus) with unimodal and multimodal signal playbacks of conspecific rivals in their natural habitat and recorded their behavioral responses. We found no difference in receiver response to unimodal advertisement call stimuli and to multimodal stimulus presentations of calls combined with visual signals of an artificial vocal sac with or without a gular patch, moving synchronously or asynchronously with the call playback. The inflations of a vocal sac with a colorful gular patch did not alter receiver response and neither increase nor decrease signal salience during male-male communication. Interestingly, males frequently displayed a novel hind and front foot-tapping behavior in response to all playbacks. Comparison of male responses to advertisement and aggressive call playbacks showed that Spotted Reed Frogs approached the sound source less during aggressive call presentations. Tapping behavior was not influenced by either call playback. We suggest that the gestural tapping behavior might act as vibrational signal and discuss its potential signal function in male contests and courtship for females.
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Physical gestures are prominent features of many species' multimodal displays, yet how evolution incorporates body and leg movements into animal signaling repertoires is unclear. Androgenic hormones modulate the production of reproductive signals and sexual motor skills in many vertebrates; therefore, one possibility is that selection for physical signals drives the evolution of androgenic sensitivity in select neuromotor pathways. We examined this issue in the Bornean rock frog (Staurois parvus, family: Ranidae). Males court females and compete with rivals by performing both vocalizations and hind limb gestural signals, called "foot flags." Foot flagging is a derived display that emerged in the ranids after vocal signaling. Here, we show that administration of testosterone (T) increases foot flagging behavior under seminatural conditions. Moreover, using quantitative PCR, we also find that adult male S. parvus maintain a unique androgenic phenotype, in which androgen receptor (AR) in the hind limb musculature is expressed at levels â¼10× greater than in two other anuran species, which do not produce foot flags (Rana pipiens and Xenopus laevis). Finally, because males of all three of these species solicit mates with calls, we accordingly detect no differences in AR expression in the vocal apparatus (larynx) among taxa. The results show that foot flagging is an androgen-dependent gestural signal, and its emergence is associated with increased androgenic sensitivity within the hind limb musculature. Selection for this novel gestural signal may therefore drive the evolution of increased AR expression in key muscles that control signal production to support adaptive motor performance.
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Evolução Biológica , Gestos , Membro Posterior/fisiologia , Músculo Esquelético/efeitos dos fármacos , Ranidae/fisiologia , Testosterona/farmacologia , Animais , Feminino , Masculino , Músculo Esquelético/fisiologia , Receptores Androgênicos/análise , Receptores Androgênicos/fisiologia , Comportamento Sexual Animal , Vocalização AnimalRESUMO
Adult individuals of several anuran species exhibit conspicuous visual displays during intraspecific communication. While signal properties in adults have been subject to an increasing number of studies, little is known about the variation of visual signals in juveniles and during ontogenetic changes. Foot-flagging signals of the Bornean frogs Staurois guttatus and S. parvus were observed in juveniles a few days after metamorphosis. We investigated color parameters of foot webbings and body coloration of individuals bred at the Vienna Zoo, and their relation to age and body size using spectrophotometry. Our results indicate that the brightness of foot webbings of S. guttatus and S. parvus increased with increasing age. Additionally, we compared the results with measurements of adult individuals from a population in Brunei and discuss possible differences related to diet and age as well as the habitat use of juveniles and adults. We suggest that the ontogenetic increase in foot-webbing brightness enhances visual conspicuousness and the signal-to-noise ratio of the visual signal with sexual maturity and potentially functions as cue to the age of the signaler.
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Although in anurans the predominant mode of intra- and intersexual communication is vocalization, modalities used in addition to or instead of acoustic signals range from seismic and visual to chemical. In some cases, signals of more than one modality are produced through or by the anuran vocal sac. However, its role beyond acoustics has been neglected for some time and nonacoustic cues such as vocal sac movement have traditionally been seen as an epiphenomenon of sound production. The diversity in vocal sac coloration and shape found in different species is striking and recently its visual properties have been given a more important role in signalling. Chemosignals seem to be the dominant communication mode in newts, salamanders and caecilians and certainly play a role in the aquatic life phase of anurans, but airborne chemical signalling has received less attention. There is, however, increasing evidence that at least some terrestrial anuran species integrate acoustic, visual and chemical cues in species recognition and mate choice and a few secondarily mute anuran species seem to fully rely on volatile chemical cues produced in glands on the vocal sac. Within vertebrates, frogs in particular are suitable organisms for investigating multimodal communication by means of experiments, since they are tolerant of disturbance by observers and can be easily manipulated under natural conditions. Thus, the anuran vocal sac might be of great interest not only to herpetologists, but also to behavioural biologists studying communication systems.