Mating Calls Research Articles

Noise constrains the evolution of call frequency contours in flowing water frogs: a comparative analysis in two clades

BackgroundThe acoustic adaptation hypothesis (AAH) states that signals should evolve towards an optimal transmission of the intended information from senders to intended receivers given the environmental constraints of the medium that they traverse. To date, most AAH studies have focused on the effect of stratified vegetation on signal propagation. These studies, based on the AAH, predict that acoustic signals should experience less attenuation and degradation where habitats are less acoustically complex. Here, we explored this effect by including an environmental noise dimension to test some AAH predictions in two clades of widespread amphibians (Bufonidae and Ranidae) that actively use acoustic signals for communication. By using data from 106 species in these clades, we focused on the characterization of the differences in dominant frequency (DF) and frequency contour (i.e., frequency modulation [FM] and harmonic performances) of mating calls and compared them between species that inhabit flowing-water or still-water environments.ResultsAfter including temperature, body size, habitat type and phylogenetic relationships, we found that DF differences among species were explained mostly by body size and habitat structure. We also showed that species living in lentic habitats tend to have advertisement calls characterized by well-defined FM and harmonics. Likewise, our results suggest that flowing-water habitats can constrain the evolutionary trajectories of the frequency-contour traits of advertisement calls in these anurans.ConclusionsOur results may support AAH predictions in frogs that vocalize in noisy habitats because flowing-water environments often produce persistent ambient noise. For instance, these anurans tend to generate vocalizations with less well-defined FM and harmonic traits. These findings may help us understand how noise in the environment can influence natural selection as it shapes acoustic signals in affected species.

Limited effects of traffic noise on behavioural responses to conspecific mating calls in the eastern sedge frog Litoria fallax.

Anthropogenic noise is a pervasive environmental feature across both urban and non-urban habitats and presents a novel challenge especially for acoustically communicating species. While it is known that some species adjust acoustic signals to communicate more effectively in noisy habitats, we know very little about how the receivers of these signals might be impacted by anthropogenic noise. Here, we investigated female and male Litoria fallax frogs’ ability to distinguish between high- and low-quality acoustic signals during the presence of background traffic noise and without. We performed a controlled behavioural experiment whereby frogs were presented with simultaneously broadcasted attractive and unattractive calls from opposing directions, once with background traffic noise and once without. We found that females in particular chose the unattractive call significantly more often (and males significantly less often) when noise was being broadcast. This indicates that anthropogenic noise potentially affects receiver responses to acoustic signals, even when calls are not acoustically masked, with potential consequences for maladaptive mating behaviours and population outcomes.Supplementary informationThe online version contains supplementary material available at 10.1007/s10211-021-00378-7.

Phenotypic and genomic diversification with isolation by environment along elevational gradients in a neotropical treefrog.

Understanding how geographic and environmental heterogeneity drive local patterns of genetic variation is a major goal of ecological genomics and a key question in evolutionary biology. The tropical Andes and inter-Andean valleys are shaped by markedly heterogeneous landscapes, where species experience strong selective processes. We examined genome-wide SNP data together with behavioural and ecological traits (mating calls and body size) known to contribute to genetic isolation in anurans in the banana tree-dwelling frog, Boana platanera, distributed across an environmental gradient in Central Colombia (northern South America). Here, we analysed the relationships between environmentally (temperature and precipitation) associated genetic and phenotypic differentiation and the potential drivers of isolation by environment along an elevation gradient. We identified candidate SNPs associated with temperature and body size, which follow a clinal pattern of genome-wide differentiation tightly coupled with phenotypic variation: as elevation increases, B. platanera exhibits larger body size and longer call duration with more pulses but lower pulse rate and frequency. Thus, the environmental landscape has rendered a scenario where isolation by environment and candidate loci show concordance with phenotypic divergence in this tropical frog along an elevation gradient in the Colombian Andes. Our study sets the basis for evaluating the role of temperature in the genetic structure and local adaptation in tropical treefrogs and its putative effect on life cycle (embryos, tadpoles, adults) along elevation gradients.

Microhabitat of Leptophryne borbonica (Tschudi, 1838) (Anura: Bufonidae) and it’s calling behaviour in Sumatera

Microhabitat use of amphibians have been widely neglected among studies on herpetofauna. The microhabitat structure is important when it served as reproduction site. Here we survey the microhabitat characteristics of Leptophryne borbonica and the mating calls. We observed 15 individuals perching on the rock in the middle of the stream and two others have been observed far from stream and other water bodies. The calling males perch on the moist and dry rocks. Interestingly, this species always calls on the rock which is located right in front of the water that fall from two intersecting rocks, creating the small-like waterfall with very noisy backsound. It might suggest the behavior of hiding from predators detection through the sound of environment.

Behaviors associated with vocal communication of squirrels

AbstractVocal communication is an important method squirrels (Sciuridae) use to transfer information from one individual to others. While behaviors associated with vocal communication have been explored in individual species or single call‐types in specific groups of squirrels, no comprehensive review of these behaviors exists for Sciuridae. Herein, I review the current literature to describe behaviors associated with vocal communication in three groups of squirrels: ground squirrels, tree squirrels, and flying squirrels. I discuss the behavioral functions of squirrel vocalizations. A wide variety of behaviors are associated with particular call‐types produced by squirrels, including alarm, agonistic, discomfort, affiliative, mating, and neonatal calls. There are large knowledge gaps in cataloging the vocal repertoires and associated behaviors of many species of squirrels, including commonly studied species such as marmots and ground squirrels, as alarm calls are typically focused on and other call‐types are understudied or ignored. Since vocal communication is important to the development, reproduction, and survival of squirrels, further understanding the biological and ecological drivers behind vocal repertoires is critical to evaluating the ethology of this family as a whole.

Geographical variation in squirrel mating calls and their recognition limits in the widely distributed species complex

Geographical variation in squirrel mating calls and their recognition limits in the widely distributed species complex

Not only a listener: female frog-biting midges (Corethrellidae) also distinguish the shape of frogs

AbstractIt is well known that female adults of frog-biting midges (Corethrellidae) are attracted by anuran mating calls. However, the role of host-emitted cues other than mating calls in determining the level of attraction remains poorly understood. Here, we performed field playback experiments to test how the host-seeking behaviour of Corethrella Coquillett is influenced by different sound stimuli: mating call of a tree frog, cricket call, and no sound. Then, after long-distance host detection, we evaluated if Corethrella can distinguish landing sites by using at short distance the colour and/or shape of anurans. For that, we placed artificial models of frogs with different colours (light green and dark brown) and an artificial caterpillar model (light green colour) on the top of speakers. We found that only frog mating calls presented with the visual cue of an artificial frog were attacked by Corethrella, suggesting that frog shape, regardless of colour, is an important cue for the identification of its hosts. This is the first study providing evidence that after flying long distances guided by frog calls, Corethrella can identify their hosts using visual cues at short distances.

The rain calls of frogs and the reigning paradigm of American herpetology

American zoologists and herpetologists during the past 50 years have successfully deciphered the mating calls of frogs and toads with ever increasing precision and sophistication. However, the vocalizations most commonly termed “rain calls”, which typically occur beyond both normal breeding seasons and breeding sites, have remained a persistent puzzle. This article traces the gradual disappearance of rain calls, along with a corresponding decline in any mention of emotional states, from herpetological studies of anuran vocalizations in the United States from the middle of the twentieth century to the present and examines the historical roots of this disappearance. This evaporation of rain calls is indicative of a much larger change in the scientific climate of the times, involving the transition from traditional natural history to the neo-Darwinian, adaptationist paradigm of contemporary biology. Rain calls thus increasingly became anomalous, thereby eliminating a possibly fruitful line of inquiry in the comparative study of human–animal communication, in this case with evolution's earliest vocalizers. The contours and benefits of a more encompassing paradigm, envisioned by some leading early twentieth-century zoologists, are briefly discussed.

Multisensory modalities increase working memory for mating signals in a treefrog.

Animal choruses, such as those found in insects and frogs, are often intermittent. Thus, females sampling males in the chorus might have to remember the location of the potential mates' calls during periods of silence. Although a number of studies have shown that frogs use and prefer multimodal mating signals, usually acoustic plus visual, it is not clear why they do so. Here we tested the hypothesis that preference for multimodal signals over unimodal signals might be due to multimodal signals instantiating longer memories than unimodal signals, particularly during the inter-chorus intervals. We tested this hypothesis in serrate-legged small treefrogs Kurixalus odontotarsus whose males produce advertisement calls accompanied by conspicuous vocal sac inflation. Females were tested with acoustic and acoustic+visual (video of inflating-deflating vocal sac) mating calls. We found that females prefer multimodal calls over unimodal, audio-only calls. Furthermore, multimodal calls are still preferred after a silent period of up to 30s, a time that spans the average silent period of the chorus. This was not true of unimodal calls. Our results demonstrate that a multimodal signal can engage longer working memory than a unimodal signal, and thus female memory might favour the evolution of multimodal signals in males through sexual selection. Selection might also favour female preference for multimodal signals if longer memory facilitates mate searching and assessment. Our study does not allow us to elucidate the sequence of evolution of this trait and preference.

Lung mediated auditory contrast enhancement improves the Signal-to-noise ratio for communication in frogs

Environmental noise is a major source of selection on animal sensory and communication systems. The acoustic signals of other animals represent particularly potent sources of noise for chorusing insects, frogs, and birds, which contend with a multi-species analog of the human "cocktail party problem" (i.e., our difficulty following speech in crowds). However, current knowledge of the diverse adaptations that function to solve noise problems in nonhuman animals remains limited. Here, we show that a lung-to-ear sound transmission pathway in frogs serves a heretofore unknown noise-control function in vertebrate hearing and sound communication. Inflated lungs improve the signal-to-noise ratio for communication by enhancing the spectral contrast in received vocalizations in ways analogous to signal processing algorithms used in hearing aids and cochlear implants. Laser vibrometry revealed that the resonance of inflated lungs selectively reduces the tympanum's sensitivity to frequencies between the two spectral peaks present in conspecific mating calls. Social network analysis of continent-scale citizen science data on frog calling behavior revealed that the calls of other frog species in multi-species choruses can be a prominent source of environmental noise attenuated by the lungs. Physiological modeling of peripheral frequency tuning indicated that inflated lungs could reduce both auditory masking and suppression of neural responses to mating calls by environmental noise. Together, these data suggest an ancient adaptation for detecting sound via the lungs has been evolutionarily co-opted to create auditory contrast enhancement that contributes to solving a multi-species cocktail party problem.

A taxonomic revision of the genus Phrynoglossus in Indochina with the description of a new species and comments on the classification within Occidozyginae (Amphibia, Anura, Dicroglossidae)

We revise the frogs of the genusPhrynoglossusfrom Indochina based on data of external morphology, bioacoustics and molecular genetics. The results of this integrative study provide evidence for the recognition of three distinct species, one of which we describe as new.Phrynoglossus martensiihas a vast geographic distribution from central and southern Thailand across southern China to Vietnam, Laos, and Cambodia.Phrynoglossus myanhesseisp. nov.is distributed in central Myanmar whereasPhrynoglossus magnapustulosusis restricted to the Khorat Plateau, Thailand. These three species occur in allopatry and differ in their mating calls, external morphology, and in genetic distances of the 16S gene of 3.8–5.9%. Finally, we discuss and provide evolutionary evidence for the recognition ofPhrynoglossusas a genus distinct fromOccidozyga. Members of both genera form reciprocal monophyletic groups in our analyses of mtDNA data (16S) and are well differentiated from each other in morphology and ecology. Furthermore, they differ in the amplexus mode withPhrynoglossushaving an inguinal amplexus whereas it is axillary inOccidozyga. We further provide ade novodraft genome of the holotype based on short-read sequencing technology to a coverage of 25-fold. This resource will permanently link the genetic characterization of the species to the name-bearing type specimen.

A taxonomic revision of the genus Phrynoglossus in Indochina with the description of a new species and comments on the classification within Occidozyginae (Amphibia, Anura, Dicroglossidae)

We revise the frogs of the genus Phrynoglossus from Indochina based on data of external morphology, bioacoustics and molecular genetics. The results of this integrative study provide evidence for the recognition of three distinct species, one of which we describe as new. Phrynoglossus martensii has a vast geographic distribution from central and southern Thailand across southern China to Vietnam, Laos, and Cambodia. Phrynoglossus myanhesseisp. nov. is distributed in central Myanmar whereas Phrynoglossus magnapustulosus is restricted to the Khorat Plateau, Thailand. These three species occur in allopatry and differ in their mating calls, external morphology, and in genetic distances of the 16S gene of 3.8–5.9%. Finally, we discuss and provide evolutionary evidence for the recognition of Phrynoglossus as a genus distinct from Occidozyga. Members of both genera form reciprocal monophyletic groups in our analyses of mtDNA data (16S) and are well differentiated from each other in morphology and ecology. Furthermore, they differ in the amplexus mode with Phrynoglossus having an inguinal amplexus whereas it is axillary in Occidozyga. We further provide a de novo draft genome of the holotype based on short-read sequencing technology to a coverage of 25-fold. This resource will permanently link the genetic characterization of the species to the name-bearing type specimen.

Bioacoustic characterization of mating calls of a freshwater fish (Prochilodus magdalenae) for passive acoustic monitoring

Fish produce sounds that are usually species-specific and associated with particular behaviors and contexts. Acoustic characterization enables the use of sounds as natural acoustic labels for species identification. Males of Prochilodus magdalenae produce mating sounds. We characterized these sounds and tested their use in natural habitats, to use passive acoustic monitoring for spawning ground identification. We identified two types of acoustic signals: simple pulses and pulse trains. Simple pulses were 13.7 ms long, with peak frequency of 365 Hz, whereas pulse train were 2.3 s long, had peak frequency of 399 Hz, 48.6 pulses and its pulses lasted 12.2 ms, with interpulse interval of 49.0 ms long and 22.3 Hz pulse rate. We did not detect spawning in absence of male calls nor differences in male sounds at different female densities. We found differences in train duration, pulse rate, and pulse duration in trains, according to the fish's source sites, but these sites were not well discriminated based on bioacoustical variables. In rivers, we located two P. magdalenae spawning grounds and recognized calls from another fish species (Megaleporinus muyscorum). We did not find a significant relationship between fish size and call peak frequency for P. magdalenae.

Eurasian Pygmy-owl Glaucidium passerinum in Ukrainian Polissia

Background. The Eurasian Pygmy-owl Glaucidium passerinum (Linnaeus, 1758) is a rare and poorly studied species in Ukraine. It is listed in the Red Data book of Ukraine [2]. Its breeding locations can be found in the Carpathians, Roztochia and Polissia. There are insufficient data the on distribution and current state of abundance of Eurasian Pygmy-owl as well as breeding biology of the species on the territory of Polissia. Materials and Methods. The published data, internet sources, and unpublished materials of colleagues were used in addition to our own observations. Special studies were conducted on permanent study sites in Polissia Nature Reserve (Olevsk and Ovruch districts, Zhytomyr region) and Desniansko-Starohutskyi National Nature Park (Seredyno-Buda district, Sumy region). Small expeditions were organized to other locations within Polissia. Studies of this species were conducted in conjunction with the study of other owl species. They included surveys, behavioral observations, and eco­logy studies. During the surveys, the registrations on the routes of natural voca­lization of adult owls were made at twilight and at night; in cases when natural vocali­za­tion was absent, the recordings of mating calls of males and females were played [1]. The maximum distance of species registration by calling (500 m) was used for breeding density estimation. Results. During the breeding period, the Eurasian Pygmy-owl was found in all regions of Polissia. The southern boundary of that area lies near the villages Perebrody, Dubrovytsia district [12] – Karasyn, Sarny district [12] – Kochychyne, Yemilchyn district – Lypnyky, Luhyny district – Velyki Klishchi, Narodychi district – Stavrovka, Ivankiv district. The second site of regular breeding is the territory of Desniansko-Starohutskyi National Nature Park, where the species has been detected since 1996 [13]. For the first time, on the territory of Polissia, two nests in Zhytomyr and Sumy regions were found. For the first time in Ukraine, the clutch was measured. Behavioral observations of owls in breeding sites were conducted. Food remains were collected and identified. Conclusions. The Eurasian Pygmy-owl is a breeding species in Ukrainian Polissia. The average breeding density in Polissia is 5.8 pairs/100 sq. km. The permanent bree­ding range was identified; it covers the northeastern part of Rivne region, the northern part of Zhytomyr and Kyiv regions, the northeastern part of Chernihiv region and the northern part of Sumy region, on the area of 18.1 thousand sq. km. The estimated bree­ding population of this species is 330 pairs. During the mating season, there are two peaks of natural 24-hour vocalization activity: in the evening and morning twilight. In the evening, males often begin to call 30 min after sunset, in the morning – 30 min before sunrise. In the autumn-winter period, birds either stay within their breeding areas or migrate, flying outside the breeding habitats. The increase in the number of registrations is due to special surveys taking into account the narrow interval of 24-hour natural vocalization acti­vity in the twilight period and the use of phonogram reproduction techniques. Keywords: Eurasian Pygmy-owl, breeding, abundance, behavior, Polissia, Ukraine

Sensory ecology of the frog-eating bat, Trachops cirrhosus, from DNA metabarcoding and behavior

Abstract Metabarcoding of prey DNA from fecal samples can be used to design behavioral experiments to study the foraging behavior and sensory ecology of predators. The frog-eating bat, Trachops cirrhosus, eavesdrops on the mating calls of its anuran prey. We captured wild T. cirrhosus and identified prey remains in the bats’ fecal samples using DNA metabarcoding of two gene regions (CO1 and 16S). Bats were preying on frogs previously unknown in their diet, such as species in the genus Pristimantis, which occurred in 29% of T. cirrhosus samples. Twenty-three percent of samples also contained DNA of Anolis lizards. We additionally report apparently rare predation events on hummingbirds and heterospecific bats. We used results from metabarcoding to design acoustic and 3D model stimuli to present to bats in behavioral experiments. We show predatory responses by T. cirrhosus to the calls of the frog Pristimantis taeniatus and to the rustling sounds of anoles moving through leaf-litter, as well as attacks on a stuffed hummingbird and a plastic anole model. The combination of species-specific dietary information from metabarcoding analyses with behavioral responses to prey cues provides a unique window into the foraging ecology of predators that are difficult to observe in the wild.

Acoustic signals induce egg laying in túngara frogs

Male mating calls generally attract mates and deter competitors. In some vertebrates, however, mating calls can also influence ovarian development. Stimulation of the auditory system shifts the endocrine control of the female gonads but little is known about the underlying mechanisms. We studied túngara frogs because their mate choice responses to sound are well known. We stimulated isolated females with sound and monitored their egg laying to answer three questions: (1) Can egg laying be triggered by sound? (2) Is their response to sound specific? (3) Among conspecific male calls, are the most attractive ones also more likely to elicit egg laying? The results showed that egg laying in isolated females could be elicited by male advertisement calls in the presence of a pool of water. This response occurred within hours but it was abolished if the calls were modified. Among conspecific calls, complex ones known to have enhanced attractiveness to females did not differ significantly from simple ones in their ability to stimulate egg laying. The reproductive state response of the female to sound can therefore match or depart from her mate choice response indicating a complex neuroendocrine coordination with the auditory system.

Singing in the suburbs: point count surveys efficiently reveal habitat associations for nocturnal Orthoptera across an urban-to-rural gradient

As evidence for global insect population declines continues to amass, several studies have indicated that Orthoptera (grasshoppers, crickets, and katydids) are among the most threatened insect groups. Understanding Orthoptera populations across large spatial extents requires efficient survey protocols, however, many previously established methods are expensive and/or labor-intensive. One survey method widely employed in wildlife biology, the aural point count, may work well for crickets and katydids (suborder: Ensifera) because males produce conspicuous, species-specific mating calls. We conducted repeated point count surveys across an urban-to-rural gradient in central Pennsylvania. Occupancy analyses of ten focal species indicated that, although detection probability rates varied by species from 0.43 to 0.98, detection rates compounded over five visits such that all focal species achieved cumulative > 0.90. Factors associated with site occupancy varied among species with some positively associated with urbanization (e.g., Greater Anglewing, Microcentrum rhombifolium), some negatively associated with urbanization (e.g., Sword-bearing Conehead, Neoconocephalus ensiger), and others exhibiting constant occupancy across a habitat gradient (e.g., Common True Katydid, Pterophylla camellifolia). Our community-level analysis revealed that different species’ habitat associations interacted such that intermediate levels of urbanization (i.e., suburbs) hosted the highest number of species.Implications for insect conservationUltimately, our analyses clearly support the concept that aural point counts paired with static occupancy modeling can serve as an important tool for monitoring night-singing Orthoptera populations. Applications of point count surveys by both researchers and citizen scientists may improve our understanding Ensifera populations and help in the global conservation of these threatened insects.

Effect of temperature on life-history traits and mating calls of a field cricket, Acanthogryllus asiaticus.

Ectotherms are sensitive to changes in ambient temperature that impact their physiology and development. To compensate for the effects of variation in temperature, ectotherms exhibit short or long-term physiological plasticity. An extensive body of literature exists towards understanding these effects and the solutions ectotherms have evolved. However, to what extent rearing temperature during early life stages impacts the behaviour expressed in adulthood is less clearly understood. In the present study, we aimed to examine the effects of developmental temperature on life-history traits and mating call features in a tropical field cricket, Acanthogryllus asiaticus. We raised A. asiaticus at two different developmental conditions: 25°C and 30°C. We found developmental time and adult lifespan of individuals reared at 30°C to be shorter than those reared at 25°C. Increased developmental temperature influenced various body size parameters differentially. Males raised at 30°C were found to be larger and heavier than those raised at 25°C, making A. asiaticus an exception to the temperature-size rule. We found a significant effect of change in immediate ambient temperature on different call features of both field-caught and lab-bred individuals. Developmental temperature also affected mating call features wherein individuals raised at higher temperature produced faster calls with a higher peak frequency compared to those raised at lower temperature. In addition, an interactive effect of both developmental and immediate temperature was found on mating call features. Our study highlights the importance of understanding how environmental temperature shapes life-history and sexual communication in crickets.

Acoustic enrichment in wildlife passages under railways improves their use by amphibians

Linear transport infrastructure can impact wildlife directly or indirectly, and amphibians are particularly affected. In some cases, mitigation measures – such as tunnels below the linear transport infrastructure – are implemented, but an evaluation of their effectiveness is often lacking, especially for small animals such as amphibians. Few studies have focused on crossing behaviour in underpasses, yet this information may be crucial to improve mitigation measures. In this study, we conducted experiments in three tunnels below a high-speed railway with individually marked amphibians (great crested newt Triturus cristatus, marbled newt Triturus marmoratus, alpine newt Ichthyosaura alpestris, fire salamander Salamandra salamandra, spined toad Bufo spinosus, agile frog Rana dalmatina and edible/pool frog Pelophylax kl. esculentus/lessonae) which were released at the entrance of tunnels varying in length. Behaviours (e.g. completed crossing, U-turn, not moving, and stay) and crossing speed were recorded. R. dalmatina, S. salamandra and T. cristatus (but not B. spinosus) exhibited crossing rate differences between tunnels 21 m and 40 m in length. More individuals performed “complete crossing” through the shorter tunnel. The crossing speed of the S. salamandra and T. cristatus did not differ between the tunnels of different lengths. In a second experiment, we evaluated the effect of acoustic enrichment on the crossing behaviour of one frog and three newt species by broadcasting a soundtrack of mating calls of syntopic anuran species in the tunnels. Pelophylax kl exhibited a large increase in complete crossings and in speed. T. cristatus showed an increase in tunnel complete crossings (but not speed) in one of the acoustically enhanced tunnels. These results indicate that acoustic enrichment can improve the crossing of underpasses. This low cost and easily implementable method could help to inform the design of wildlife passages as mitigation measures for impacted amphibian populations, though more experiments on the effect of tunnel characteristics on amphibian behaviour would be valuable.

The Specific Molecular Composition and Structural Arrangement of Eleutherodactylus Coqui Gular Skin Tissue Provide Its High Mechanical Compliance.

A male Eleutherodactylus Coqui (EC, a frog) expands and contracts its gular skin to a great extent during mating calls, displaying its extraordinarily compliant organ. There are striking similarities between frog gular skin and the human bladder as both organs expand and contract significantly. While the high extensibility of the urinary bladder is attributed to the unique helical ultrastructure of collagen type III, the mechanism behind the gular skin of EC is unknown. We therefore aim to understand the structure–property relationship of gular skin tissues of EC. Our findings demonstrate that the male EC gular tissue can elongate up to 400%, with an ultimate tensile strength (UTS) of 1.7 MPa. Species without vocal sacs, Xenopus Laevis (XL) and Xenopus Muelleri (XM), elongate only up to 80% and 350% with UTS~6.3 MPa and ~4.5 MPa, respectively. Transmission electron microscopy (TEM) and histological staining further show that EC tissues’ collagen fibers exhibit a layer-by-layer arrangement with an uninterrupted, knot-free, and continuous structure. The collagen bundles alternate between a circular and longitudinal shape, suggesting an out-of-plane zig-zag structure, which likely provides the tissue with greater extensibility. In contrast, control species contain a nearly linear collagen structure interrupted by thicker muscle bundles and mucous glands. Meanwhile, in the rat bladder, the collagen is arranged in a helical structure. The bladder-like high extensibility of EC gular skin tissue arises despite it having eight-fold lesser elastin and five times more collagen than the rat bladder. To our knowledge, this is the first study to report the structural and molecular mechanisms behind the high compliance of EC gular skin. We believe that these findings can lead us to develop more compliant biomaterials for applications in regenerative medicine.