Sound source perception in anuran amphibians

Sound source perception refers to the auditory system's ability to parse incoming sensory information into coherent representations of distinct sound sources in the environment. Such abilities are no doubt key to successful communication in many taxa, but we know little about their function in animal communication systems. For anuran amphibians (frogs and toads), social and reproductive behaviors depend on a listener's ability to hear and identify sound signals amid high levels of background noise in acoustically cluttered environments. Recent neuroethological studies are revealing how frogs parse these complex acoustic scenes to identify individual calls in noisy breeding choruses. Current evidence highlights some interesting similarities and differences in how the auditory systems of frogs and other vertebrates (most notably birds and mammals) perform auditory scene analysis.     

Control of breathing in anuran amphibians

The primary role of the respiratory system is to ensure adequate tissue oxygenation, eliminate carbon dioxide and help to regulate acid-base status. To maintain this homeostasis, amphibians possess an array of receptors located at peripheral and central chemoreceptive sites that sense respiration-related variables in both internal and external environments. As in mammals, input from these receptors is integrated at central rhythmogenic and pattern-forming elements in the medulla in a manner that meets the demands determined by the environment within the constraints of the behavior and breathing pattern of the animal. Also as in mammals, while outputs from areas in the midbrain may modulate respiration directly, they do not play a significant role in the production of the normal respiratory rhythm. However, despite these similarities, the breathing patterns of the two classes are different: mammals maintain homeostasis of arterial blood gases through rhythmic and continuous breathing, whereas amphibians display an intermittent pattern of aerial respiration. While the latter is also often rhythmic, it allows a degree of fluctuation in key respiratory variables that has led some to suggest that control is not as tight in these animals. In this review we will focus specifically on recent advances in studies of the control of ventilation in anuran amphibians. This is the group of amphibians that has attracted the most recent attention from respiratory physiologists.     

Evolutionary transformations of ontogenesis in anuran amphibians

A review of the recent published data on ontogenesis of direct developing and marsupial frogs. The development of these representatives of anuran amphibians seems to be evolutionary advanced and considerably differs from the development of species traditionally used in amphibian embryology.     

Retina and lens regeneration in anuran amphibians

Anuran amphibians can regenerate the retina through differentiation of stem cells in the ciliary marginal zone and through transdifferentiation of the retinal pigmented epithelium. By contrast, the regeneration of the lens has been demonstrated only in larvae of species belonging to the Xenopus genus, where the lens regenerates through transdifferentiation of the outer cornea. Retinal pigmented epithelium to neural retina and outer cornea to lens transdifferentiation processes are triggered and sustained by signaling molecules belonging to the family of the fibroblast growth factor. Both during retina and lens regeneration there is a re-activation of many of the genes which are activated during development of the eye, even though the spatial and temporal pattern of gene expression is not a simple repetition of that found in development.     

Hormones and acoustic communication in anuran amphibians

Circulating hormone levels can mediate changes in the quality of courtship signals by males and/or mate choice by females and may thus play an important role in the evolution of courtship signals. Costs associated with shifts in hormone levels of males, for example, could effectively stabilize directional selection by females on male signals. Alternatively, if hormone levels affect the selection of mates by females, then variation in hormone levels among females could contribute to the maintenance of variability in the quality of males' signals. Here, I review what is known regarding the effects of hormone levels on the quality of acoustic signals produced by males and on the choice of mates by females in anuran amphibians. Surprisingly, despite the long history of anuran amphibians as model organisms for studying acoustic communication and physiology, we know very little about how variation in circulating hormone levels contributes to variation in the vocal quality of males. Proposed relationships between androgen levels and vocal quality depicted in recent models, for example, are subject to the same criticisms raised for similar models proposed in relation to birds, namely that the evidence for graded effects of androgens on vocal performance is often weak or not rigorously tested and responses seen in one species are often not observed in other species. Although several studies offer intriguing support for graded effects of hormones on calling behavior, additional comparative studies will be required to understand these relationships. Recent studies indicate that hormones may also mediate changes in anuran females' choice of mates, suggesting that the hormone levels of females can influence the evolution of males' mating signals. No studies to date have concurrently addressed the potential complexity of hormone-behavior relationships from the perspective of sender as well as receiver, nor have any studies addressed the costs that are potentially associated with changes in circulating hormone levels in anurans (i.e., life-history tradeoffs associated with elevations in circulating androgens in males). The mechanisms involved in hormonally induced changes in signal production and selectivity also require further investigation. Anuran amphibians are, in many ways, conducive to investigating such questions.     

Developmental changes in interrenal responsiveness in anuran amphibians

Basal activity of the hypothalamo-pituitary-interrenal (HPI)axis changes over development in larval amphibians, but developmentof the responsiveness of this axis to an external stressor hasnot been studied. We compared developmental changes in whole-bodycorticosterone content of two anuran amphibian species, Ranapipiens (family Ranidae) and Xenopus laevis (family Pipidae).We also examined developmental changes in the responsivenessof the HPI axis by subjecting tadpoles of different developmentalstages to a laboratory shaking/confinement stress and to ACTHinjection. We measured whole-body corticosterone content asan indicator of the activity of the HPI axis. Whole-body corticosteronecontent of R. pipiens remained low during premetamorphosis andprometamorphosis but increased dramatically at metamorphic climaxand remained elevated in juvenile frogs. By contrast, whole-bodycorticosterone content of X. laevis was highest during premetamorphosis,declined at the onset of prometamorphosis, increased at metamorphicclimax and remained at climax levels in juvenile frogs. Premetamorphicand prometamorphic tadpoles of both species showed strong corticosteroneresponses to both shaking stress and ACTH injection. The magnitudeand pattern of response differed among developmental stages,with premetamorphic tadpoles of both species showing greaterresponsiveness to stress and ACTH. Our results show that interrenalresponsiveness is developed in premetamorphic tadpoles, suggestingthat at these stages tadpoles are capable of mounting an increasein stress hormone production in response to changes in the externalenvironment. Our results also highlight the importance of comparativestudies in understanding the development of the stress axis.     

Morphometric relationships of take-off speed in anuran amphibians

Locomotory speed correlates with muscle mass (determining force and stride rate), limb length (stride rate and distance), and laterally compressed body trunk (force and stride distance). To delineate generalization of the locomotory-morphometric relationships specifically in anuran amphibians, we investigated take-off speed and the three morphological variables from seven species, Rana nigromaculata, R. rugosa, and Bombina orientalis, Eleuthrodectilus fitzingeri, E. diastema, Bufo typhonius, Colostethus flotator and Physalaemus pustulosus. The fastest jumper E. fitzingeri (3.41 m s(-1)) showed 2.49-fold greater speed than the slowest B. typhonius. Take-off speed correlated well with both thigh muscle mass relative to body mass and hindlimb length relative to snout-vent length (HL/SVL), but poorly correlated with the inter-ilial width relative to SVL. The best morphological predictor was HL/SVL (speed=-3.28+3.916 HL/SVL, r=0.968, P<0.0001), suggesting that anuran take-off speed is portrayed well with high gear and acceleration distance characterized by hindlimbs.     

Thermal dependence of behavioural performance of anuran amphibians

The thermal dependence of performance capacity was assessed in two anuran amphibians: Bufo boreas (western toad) and Rana pipiens (leopard frog). Quantitative measurements of performance showed that Bufo could sustain slow rates of walking for 10 min and cover greater distances than Rana, which initially jumped more vigorously but fatigued within 5 min. Changes in performance with changes in body temperature were virtually instantaneous, and performance exhibited no acclimation over 7 days. Within the range of temperatures studied, performance capacity increased with increasing body temperature and reached a maximum at 28 C in Bufo and 20 to 29 C in Rana. Performance capacity and the underlying metabolic processes had a similar thermal dependence within a species. The behavioural capacity for activity is apparently maximal for both species at body temperatures normally encountered in the field. Anuran behaviours requiring sustained activity (migration to breeding sites, mating, foraging) must therefore be markedly temperature-sensitive.     

Evidence for convergent evolution in the antimicrobial peptide system in anuran amphibians

Amphibians are characterized in part by their highly specialized and glandular skin that enables key physiological functions such as cutaneous respiration and defense against a variety of micro- and macroscopic predators via toxic components (e.g., alkaloids and bufodienolids), biogenic amines, neuropeptides and antimicrobial peptides (AMPs). To date, DNA sequence information regarding AMP genes in anurans is restricted to only a few anuran families and largely to “higher frogs” (Neobatrachia). Here, we analyze the DNA information for the signal sequences of the AMP precursors in anuran amphibians available to the end of 2009 in an explicit phylogenetic framework to characterize the evolution of this large, diverse gene family. Comparison of cDNA sequences suggests that there are at least three different motifs within the signal peptide sequence of the AMP-precursor corresponding to the evolutionary lineages Neobatrachia, Bombinatoridae (Bombina spp.) and Pipidae (Xenopus laevis). The signal sequences are strongly conserved within each lineage (as previously noted for Neobatrachia), but highly divergent between them. Together with the lack of a linear relationship between the degree of sequence divergence and evolutionary time, we hypothesize that the anuran AMP system has evolved convergently on at least three occasions. However, additional sampling, especially among the largely poorly sampled non-neobatrachian lineages, is required to confirm this hypothesis and could reveal the existence of additional signal sequence motifs.     

Control and interaction of the cardiovascular and respiratory systems in anuran amphibians

In anuran amphibians, respiratory rhythm is generated within the central nervous system (CNS) and is modulated by chemo- and mechanoreceptors located in the vascular system and within the CNS. The site for central respiratory rhythmogenesis and the role of various neurotransmitters and neuromodulators is described. Ventilatory air flow is generated by a positive pressure, buccal force pump driven by efferent motor output from cranial nerves. The vagus (cranial nerve X) also controls heart rate and pulmocutaneous arterial resistance that, in turn, affect cardiac shunts within the undivided anuran ventricle; however, little is known about the control of central vagal motor outflow to the heart and pulmocutaneous artery. Anatomical evidence indicates a close proximity of the centers responsible for respiratory rhythmogenesis and the vagal motoneurons involved in cardiovascular regulation. Furthermore, anurans in which phasic feedback from chemo- and mechanoreceptors is prevented by artificial ventilation exhibit cardiorespiratory interactions that appear similar to those of conscious animals. These observations indicate interactions between respiratory and cardiovascular centers within the CNS. Thus, like mammals and other air-breathing vertebrates, the cardio-respiratory interactions in anurans result from both feedback and feed-forward mechanisms.     

Diversity of opsin immunoreactivities in the extraretinal tissues of four anuran amphibians

The pineal complex, deep brain, and skin have been known to function as extraretinal photoreceptors in non-mammalian vertebrates. To see the diversity of localization of extraretinal photoreceptors in lower vertebrates having different habitats, we analyzed the opsin-like immunoreactivities in anuran amphibians, Xenopus laevis, Rana catesbeiana, Rana nigromaculata, and Bufo japonicus. An antiserum (toad Rh-AS) was raised against rhodopsin purified from the retinas of Japanese toad, B. japonicus. In the retina of all the anurans examined, the outer segments of rods were immunopositive to toad Rh-AS. The outer segments of most pinealocytes were immunopositive in R. catesbeiana, R. nigromaculata, and B. japonicus. The outer segments of photoreceptor-like cells within the frontal organ of R. nigromaculata were immunostained. Interestingly, toad Rh-AS immunostained many secretory cells of mucous glands in the head skin of B. japonicus, implying the presence of a novel photoreceptive molecule. Within the hypothalamus, toad Rh-AS immunostained many cells in the magnocellular preoptic nucleus of R. catesbeiana and B. japonicus. Toad Rh-AS also labeled cerebrospinal fluid (CSF)-contacting cells in the anterior preoptic nucleus of R. nigromaculata and those adjacent to the lateral ventricle within the septum of R. catesbeiana. Thus the distribution patterns of the rhodopsin-like immunoreactivities among the anurans were highly diverged, and there was no relationship between the distribution patterns and their habitats. J. Exp. Zool. 286:136-142, 2000.     

Advertisement calls of two anuran amphibians,Rana tigrina andTomopterna breviceps

Rana tigrina andTomopterna breviceps occur as sympatric species at Dharwad, India. Sexually mature males produce advertisement calls. The advertisement call of both the species consist of a number of calls produced in series forming a call group. Each call group ofRana tigrina comprises 10–40 calls, whereas that ofTomopterna breviceps consists 13–141 calls. Each call consists of a pulse group with variable number of pulses which lack pulse interval. Calls of both the species exhibit similarities in (i) call consisting of series of calls with a pulse group in each call, (ii) absence of pulse interval within the pulse group, (iii) the amplitude of the first pulse being always small, and (iv) the frequency spectrum beginning from 200 Hz. Based on the similarities in the spectral features of the calls, it is suggested that the two species may be closely related to each other.