Auditory sensitivity of the saccule in the American toad (Bufo americanus)

Summary Single unit recordings in the posterior nerve branchlet from the saccule have shown that, in the American toad (Bufo americanus), approximately 30% of the fibers respond to airborne sounds in a way similar to fibers from the two known auditory organs, the amphibian and basilar papillae. In response to tones, saccule fibers have best excitatory frequencies which fall into two disjoint populations: units in the low-frequency-sensitive group (below 300 Hz) show tone-on-tone suppression while those in the high-frequency-sensitive group (700–1,200 Hz) show no evidence of peripheral inhibition. Saccule units have somewhat higher thresholds than those from the other auditory organs. It is suggested that the high-frequency-sensitive fibers might be useful for discriminating mating calls in an intense chorus while the low-frequency-sensitive units likely respond to other high intensity sounds in the environment.Research supported by the U.S. Public Health Service (NIH grant NS-09244).     

Spatial and spectral dependence of the auditory periphery in the northern leopard frog

We investigated directionalities of eardrum vibration and auditory nerve response in anesthetized northern leopard frogs (Rana pipiens pipiens). Simultaneous measures of eardrum velocities and firing rates from 282 auditory nerve fibers were obtained in response to free-field sounds from eight directions in the horizontal plane. Sound pressure at the external surface of the ipsilateral eardrum was kept constant for each presentation direction (± 0.5 dB). Significant effects of sound direction on eardrum velocity were shown in 90% of the cases. Maximum or minimum eardrum velocity was observed more often when sounds were presented from the lateral and posterior fields, or from the anterior and contralateral fields, respectively. Firing rates of 38% of the fibers were significantly affected by sound direction and maximum or minimum firing rate was observed more frequently when sounds were delivered from the lateral fields, or from the anterior and contralateral fields, respectively. Directionality patterns of eardrum velocity and nerve firing also vary with sound frequency. Statistically significant correlation between eardrum velocity and nerve fiber firing rate was demonstrated in only 45% of the fibers, suggesting that sound transmission to the inner ear through extratympanic pathways plays a non-trivial role in the genesis of directionality of auditory nerve responses.Abbreviations CF characteristic frequency - SVL snout-vent length - TM tympanic membrane     

Tympanic sound radiation in the bullfrog Rana catesbeiana

Members of the Rana catesbeiana clade display sexually dimorphic eardrums. In this species assemblage the eardrum of males can be 50% larger than in females of the same body size. There has been, however, no apparent functional explanation for this dimorphism. Measurements of the acoustical coupling (transfer function) of internally generated sound to the enlarged eardrum of male bullfrogs (R. catesbeiana) show distinct energy peaks coincident with those observed in the spectral envelopes of the release and mating calls. Moreover, when the tympanic membranes are artificially damped the spectrum of the release call is drastically altered and the total amount of power radiated decreases substantially. These observations point to a previously unsuspected role for the ears in the sound broadcasting process of the bullfrog and possibly other anurans with similarly modified tympanic membranes. Accepted: 19 July 1997     

Double stimulation of the inner ear organs of an anuran species (Alytes cisternasii) with simple tonal advertisement calls

Midwife toads present one of the simplest calls in anurans, with the whole energy concentrated in a single band without frequency modulation. The tuning curves of the Iberian midwife toads Alytes cisternasii show the typical bimodal pattern in anurans, with two best excitatory frequencies at 0.412 kHz (corresponding to the amphibian papilla) and at 1.358 kHz (corresponding to the basilar papilla and matching the male call frequency). In this study, the hypothesis that complex calls arose in anurans because they were inherently more attractive to females, since they provided greater acoustic stimulation, was tested. However, our results indicate that splitting the call energy to stimulate both inner ear organs simultaneously, the male call is not more attractive to female midwife toads, but sometimes renders it unattractive. The biological role of the amphibian papilla is discussed in ecological and evolutionary terms.     

Correlation between auditory evoked responses in the thalamus and species-specific call characteristics

This evoked potential study of the bullfrog's auditory thalamic area (an auditory responsive region in the posterior dorsal thalamus) shows that complex processing, distinct from that reported in lower auditory regions, occurs in this center. An acoustic stimulus consisting of two tones, one which stimulates either the low-frequency or the mid-frequency sensitive population of auditory nerve fibers from the amphibian papilla and the other the high-frequency sensitive population of fibers from the basilar papilla, evoked a maximal response. The amplitude of the response to the simultaneous stimulation of the two auditory organs was, in some locations, much larger than the linear sum of the responses to the individual tones presented separately. Bimodal spectral stimuli that had relatively long rise-times (greater than or equal to 100 ms) evoked much larger responses than similar sounds with short rise-times. The optimal rise-times were close to those occurring in the bullfrog's mating call. The response was dependent on the waveform periodicity and harmonic content, with a fundamental frequency of 200 Hz producing a larger response than those with fundamentals of 50, 100 or 300 Hz. Six of the natural calls in the bullfrog's vocal repertoire were tested and the mating call and warning call were found to evoke the best responses. Each of these calls stimulate the two auditory organs simultaneously. The evoked response had a long refractory period which could not be altered by lesioning the efferent telencephalic pathways. The type of spectral and temporal information extracted by the auditory thalamic area suggests that this center is involved in processing complex sounds and likely plays an important role in the bullfrog's detection of some of its vocal signals.     

Sound localization behavior of the green treefrog (Hyla cinerea) and the barking treefrog (H. gratiosa)

Summary Female treefrogs (Hyla cinerea andH. gratiosa) can accurately localize a sound source (playback of male mating calls) if both ears are intact. When the sensitivity of one eardrum is attenuated, by coating it with a thin layer of silicone grease, females no longer can locate the sound source. This study demonstrates that female anurans rely on interaural cues for localization of a calling male. The neural basis for an anuran's sound localization ability presumably involves binaural convergence on single cells in the central auditory nervous system.This work was supported by research grants from the National Science Foundation and the U.S. Public Health Service. The assistance of Anne J.M. Moffat in measuring the directional characteristics of the loudspeaker is gratefully appreciated.     

Different mate preferences by parasitized and unparasitized females potentially reduces sexual selection

Parasite‐mediated models of sexual selection predict that females should avoid parasitized mates, thereby generating selection on male traits revealing health. The strength of this selection, however, may depend on the prevalence of parasitism among females if their infection status alters their mate preferences. We evaluated the effects of a socially transmitted parasite on male traits and female behaviour in spadefoot toads. Parasitized males were larger and in better condition than unparasitized males. Moreover, better condition males produced longer calls. Unparasitized females preferred longer calls indicative of good‐condition males that are more likely parasitized. By contrast, parasitized females as a group possessed no preference for call duration. Presumably because of reduced selection by these parasitized females, male mating success was not associated with any measured traits. Thus, when females are parasitized, sexual selection on condition‐dependent traits is potentially reduced.     

Social signals increase monoamine levels in the tegmentum of juvenile Mexican spadefoot toads (Spea multiplicata)

Monoamines are important neuromodulators that respond to social cues and that can, in turn, modify social responses. Yet we know very little about the ontogeny of monoaminergic systems and whether they contribute to the development of social behavior. Anurans are an excellent model for studying the development of social behavior because one of its primary components, phonotaxis, is expressed early in life. To examine the effect of social signals on monoamines early in ontogeny, we presented juvenile Mexican spadefoot toads (Spea multiplicata) with a male mating call or no sound and measured norepinephrine, epinephrine, dopamine, serotonin, and a serotonin metabolite, across the brain using high-pressure liquid chromatography. Our results demonstrate that adult-like monoaminergic systems are in place shortly after metamorphosis. Perhaps more interestingly, we found that mating calls increased the level of monoamines in the juvenile tegmentum, a midbrain region involved in sensory-motor integration and that contributes to brain arousal and attention. We saw no such increase in the auditory midbrain or in forebrain regions. We suggest that changes in monoamine levels in the juvenile tegmentum may reflect the effects of social signals on arousal state and could contribute to context-dependent modulation of social behavior.     

Mid-frequency suppression in the green treefrog (<Emphasis Type="Italic">Hyla cinerea</Emphasis>): mechanisms and implications for the evolution of acoustic communication

Advertisement calls of green treefrogs (Hyla cinerea) have two spectral peaks centered at about 1 kHz and 3 kHz. Addition of a component of intermediate frequency (1.8 kHz) to a synthetic call reduced its attractiveness to females relative to an alternative lacking this component. This mid-frequency suppression occurred over a 20-dB range of playback levels. Addition of other intermediate frequencies had weak effects on preferences at some playback levels, in some localities, and at lower-than-normal temperatures. These effects correlate well with the response properties of a population of low-frequency-tuned auditory neurons innervating the amphibian papilla. Males of a closely related species (H. gratiosa) produce calls with emphasized frequencies within the range of suppression in H. cinerea; however, suppression also occurred in localities well outside the area of geographical overlap with this species. Thus, previous speculation that mid-frequency suppression evolved to enhance species discrimination is probably incorrect. This phenomenon is more likely to reflect a general sensory bias in anurans and other vertebrates, tone-on-tone inhibition. Such negative biases, and other inhibitory mechanisms, almost certainly play an important role in the evolution of communication systems but have received far less attention than positive biases that enhance signal attractiveness.     

Auditory processing in anurans.

Anurans (frogs and toads) represent an example of peripheral specialization of the auditory systems. Their inner ear contains two distinct auditory organs: the amphibian papilla and the basilar papilla. Each organ is tuned to different species-specific frequency ranges. Because of this peripheral specialization, anurans offer an excellent opportunity to explore neural decoding of complex sounds in the central auditory system.     

Intergrading between members of the "regularis group" of toads in South Africa

The mating calls of three members of the " regularis group" of toads (Anura: Bufonidae) that are sympatric in part of South Africa are examined. A naturally occurring population of hybrid toads from Pretoria (South Africa) has previously been described as representing an intergrading between Bufo garmani Meek and Bufo rangeri Hewitt. Examination of the mating calls of these toads provides little evidence of intergrading between Bufo rangeri and Bufo garmani , and indicates the involvement of Bufo regularis Reuss in the hybridization. The mating calls of the hybrids are varied, and are structurally intermediate between those of the parental species. Mating call parameters are found to be useful in separating forms that are difficult to distinguish on morphological grounds alone. They are further found to be a sensitive non-morphological means of ascertaining the affinities of naturally occurring hybrid toads.     

Reproductive stage and history affect the phonotactic preferences of female midwife toads, Alytes muletensis

We investigated whether the reproductive stage or reproductive history of females affects their preferences for male calls that differ in frequency. We repeatedly tested gravid female midwife toads prior to and immediately after mating, and during ovulation. When females were ovulating they were much more consistent in their choice of call than when they were gravid but not ovulating. When females had recently mated they still showed positive phonotaxis, but did not reliably discriminate between alternative calls. This study is the first to test gravid female anurans repeatedly at different stages in their reproductive cycle (ovulating or not; pre- and postmating). It highlights the need to treat with caution the results from population-based preference studies in which individuals are tested only once, and in which variation in reproductive state is not taken into account. Copyright 2000 The Association for the Study of Animal Behaviour.     

Independence of Evoked Vocal Responses from Stimulus Direction in Burrowing Frogs Eupsophus (Leptodactylidae)

Localization of a sound source is important for animals in mating contexts: females generally orient towards signalling males, and males can estimate the position and quality of potential rivals. In anurans, the effect of sound direction on evoked vocal responses has been studied in males of Rana catesbeiana, which alter their vocal responses depending on the location of the stimulus. The current study explored the effects of sound direction in Eupsophus calcaratus, a frog that calls from inside burrows having resonance that would hinder the localization of incoming sounds. The vocal responses of 11 males to synthetic imitations of the conspecific advertisement call broadcast from loudspeakers positioned in front, to the right and left from the burrow openings were similar in terms of call rate, duration and latency. The invariance of the vocal responses indicates that for burrowing male frogs engaged in chorusing behaviour, the specific location of an opponent does not alter the persistence of vocal activity.     

Character Displacement in Frogs

Additional evidence has accumulated over the past 20 years regardingthe significance of the anuran mating call and regarding reinforcementof this premating isolating mechanism when hybridization occursin zones of symnatry. No two sympatric species have the samecall. That the mating call is a home-specific mate attractanthas been demonstrated in five major anuran families. Discriminationagainst hybrid calls versus homospecific calls has been demonstratedin Bufo and Hyla. Principal examples of presumed reinforcementcontinue to be in Gastrophryne, Acris, and the Australian Hylaewingi group. Reinforcement may be the basis for striking differentiationof some populations of Scaphiopus bombifrons. Sympatric speciespairs of anurans show greater differentiation in call than doallopatric pairs in the same group. One hybridizing situationin Bufo appears to have changed over 30 years to discrete populationswithout intermediate calls. Effective call differences can evolvewithout sympatry, and there are sympatric situations in whichno reinforcement is evident.     

Selective Responsiveness to Long-Range Acoustic Signals in Insects and Anurans

SYNOPSIS. Insects and anurans show various patterns of selectiveresponsiveness to playbacks of natural and synthetic sounds.Preferences and tuning of the auditory system most often matchone or more strongly emphasized frequency components in long-range,mate-attracting signals typical of conspecific individuals,but exceptions, in which frequencies lower or higher than themean are preferred, occur in some species. In some insects themost preferred frequencies may correspond to regions that maximizelocalizability of signals rather than regions of maximum sensitivity.Patterns of preference for fine-temporal properties are typicallystabilizing within a population; females prefer values nearthe mean and few males produce calls with values that deviatesufficiently to make them less attractive than calls with averagevalues. Preferences for gross temporal properties {e.g., therate and duration of signaling) are usually highly directional,with much higher than mean values preferred. In anurans, callrate is a better predictor of male mating success than dominantfrequency. Nevertheless, a variety of factors, especially close-rangeassessments that are common in insects, may modify or negatethe advantages of producing long-range signals of high relativeattractiveness. The evolutionary consequences of selective responsivenessin anurans and insects are discussed     

Sexual Differences in the Behavioral Response of Túngara Frogs, Physalaemus pustulosus, to Cues Associated with Increased Predation Risk

Engaging in mating behaviors usually increases exposure to predators for both males and females. Anti‐predator strategies during reproduction may have important fitness consequences for prey. Previous studies have shown that individuals of several species adjust their reproductive behavior according to their assessment of predation risk, but few studies have explored potential sexual differences in these strategies. In this study, we investigate whether the acoustic cues associated with predatory attacks or those associated with predators themselves affect the mating behavior of female and male túngara frogs, Physalaemus pustulosus. We compared the responses of females approaching a mate and those of calling males when exposed to mating calls associated with sounds representing increased hazard. When presented with mating calls that differed only in whether or not they were followed by a predation‐related sound, females preferentially approached the call without predation‐related sounds. In contrast to females, calling males showed greater vocal response to calls associated with increased risk than to a call by itself. We found significant differences in the responses of females and males to several sounds associated with increased hazard. Females behaved more cautiously than males, suggesting that the sexes balance the risk of predation and the cost of cautious mating strategies differently.     

Has the evolution of complexity in the amphibian papilla influenced anuran speciation rates?

For anurans, increasing complexity of the inner ear has been correlated with speciation rates. The evolution of a complex amphibian papilla (AP) is thought to have facilitated speciation by extending the range of frequencies over which mating calls may diverge. Although this example has been proposed to represent a key innovation, the mechanism by which the AP is thought to promote speciation makes the questionable assumption that anurans generally use the AP for detection of their mating calls. This study uses mating calls from 852 species to test this assumption. Surprisingly, the calls of most species are not detected by the AP but by a second organ, the basilar papilla (BP). This refutes the role of AP complexity in facilitating call divergence and hence, speciation. Future research into the evolution of acoustically mediated reproductive isolation should focus instead on the BP as it may play a more critical role in anuran speciation.     

Non‐Selective and Time‐Dependent Behavioural Responses of Common Toads (Bufo bufo) to Predator Acoustic Cues

Acoustic predator recognition has rarely been studied in anurans, in spite of the fact that hearing is widespread in these animals and that it has been demonstrated to play an important role in both arthropods and other vertebrates. Using field playback experiments, we tested the hypothesis that adult common toads (Bufo bufo) are capable of recognizing natural vocalizations of a common predator, the Eurasian otter (Lutra lutra), and show antipredator responses. We found that toads exposed to both natural (two types of otter sounds) and synthetic stimuli [white noise (WN) and otter sound‐based amplitude modulated WN] increased time allocated to locomotion and escape behaviour. These responses were correlated with time elapsed from sunset to the onset of testing and were independent from the type of acoustic signal, toad features and other environmental factors monitored. We conclude that B. bufo has not developed a selective recognition of predator vocalizations, suggesting that low‐frequency or seismic sounds associated with predator movements may provide anurans with better cues about an approaching risk. We propose that the time‐dependent response to acoustic stimuli of common toads represents a case of threat‐sensitivity and demonstrates that it can occur even when the response to the threat is not predator specific.     

Genome size rather than content might affect call properties in toads of three ploidy levels (Anura: Bufonidae: Bufo viridis subgroup)

In vertebrates, genome size has been shown to correlate with nuclear and cell sizes, and influences phenotypic features, such as brain complexity. In three different anuran families, advertisement calls of polyploids exhibit longer notes and intervals than diploids, and difference in cellular dimensions have been hypothesized to cause these modifications. We investigated this phenomenon in green toads (Bufo viridis subgroup) of three ploidy levels, in a different call type (release calls) that may evolve independently from advertisement calls, examining 1205 calls, from ten species, subspecies, and hybrid forms. Significant differences between pulse rates of six diploid and four polyploid (3n, 4n) green toad forms across a range of temperatures from 7 to 27 °C were found. Laboratory data supported differences in pulse rates of triploids vs. tetraploids, but failed to reach significance when including field recordings. This study supports the idea that genome size, irrespective of call type, phylogenetic context, and geographical background, might affect call properties in anurans and suggests a common principle governing this relationship. The nuclear‐cell size ratio, affected by genome size, seems the most plausible explanation. However, we cannot rule out hypotheses under which call‐influencing genes from an unexamined diploid ancestral species might also affect call properties in the hybrid‐origin polyploids. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 584–590.