Signal Redundancy and Receiver Permissiveness in Acoustic Mate Recognition by the Tungara Frog, Physalaemus pustulosus

The tungara frog has an advertisement call with two structurallyand functionally distinct components: the whine is both necessaryand sufficient for species recognition, and addition of chucksfurther enhances call attractiveness. Only the fundamental frequencyof the whine contributes to phonotaxis; the upper harmonicsplay no role. Furthermore, only a small portion of the whine,within the first 0–100 msec, is necessary to elicit phonotaxis;there is some redundancy since either the 0–50 msec orthe 50–100 msec portion elicits a response. Most of theremainder of the whine's fundamental further enhances call attractiveness.Only the amphibian papilla in the peripheral auditory systemis involved in decoding the whine. In stark contrast, severalchuck variants, which stimulate either the amphibian papillaor the basilar papilla, and white noise are as effective inenhancing call attractiveness as is the normal chuck, showingthat either peripheral end organ can be involved in the perceptionof a more attractive call. Thus there is greater receiver specificityfor decoding stimuli in interspecific mate choice, and greaterreceiver permissiveness for decoding stimuli in intraspecificmate choice; it appears that intraspecific mate choice can takeadvantage of a greater array of neural pathways for call decodingthan can interspecific mate choice.     

Development of hearing in vertebrates with special reference to anuran acoustic communication

Amphibians, specially anurans, are excellent model systems for studying acoustic communication. After hatching, anurans exist in two forms; these have two distinct mode of sound perception. Aquatic larvae are perceptive to waterborne sound stimuli; then, following metamorphosis, as terrestrial adults, perceptive to airborne sound stimuli. Added to this, the metamorphosing tadpole presents an equally interesting study as it could recapitulate the events which occurred during the evolution of hearing in vertebrates at the lime of the transition from aquatic to terrestrial life. Metamorphosis entails the loss of a prominent aquatic sensory system—the lateral line system—and the simultaneous gain of another, the inner ear, along with the coevolution of the tympanic middle ear, a basilar papilla and a periotic labyrinth in the inner ear. Another interesting feature is that anurans are believed to be the first terrestrial vertebrates to use vocalization as a part of their reproductive behaviour. Vocal communication plays an important role in behaviour, ranging from territorial defense to reproduction, and calls are classified according to the particular behaviors that they subserve. Adult male anurans produce a species-specific mating call which is used to attract conspecific females dung their mating season, and this call serves as a mechanism in maintaining reproductive isolation from other sympatric species.     

Changes in the Frequency Structure of a Mating Call Decrease Its Attractiveness to Females in the Cricket Frog Acris crepitans blanchardi

In many species, females often prefer male signals that are more complex than in nature or beyond the range of calls naturally produced by conspecific males in spectral, temporal and amplitude features. In this study we examined both the ability of females to recognize signals outside the normal range of spectral frequency variation seen in male advertisement calls, and the influence of increasing call complexity by adding spectral components to enhance the attractiveness of a male advertisement call in the cricket frog Acris crepitans blanchardi, while keeping its amplitude constant. We used two different natural male call groups and created the following synthetic call groups: with a dominant frequency at 3500 Hz, i.e. at the normal dominant frequency with a frequency band within the sensitivity range of the inner ear basilar papilla; with a dominant frequency at 700 Hz, i.e. outside the normal range of variation and with a frequency band outside the sensitivity range of the basilar papilla but within the range of the amphibian papilla; with two dominant frequencies, one at 700 Hz and another at 3500 Hz, stimulating the basilar and amphibian papilla simultaneously. In double choice experiments we tested all combinations of the three call groups, and we tested the 3500 Hz call groups against the same natural call groups. Additionally, we tested the 700 Hz call groups against white noise to see whether these signals are meaningful in mate choice. Females preferred 3500 Hz call groups over all other call groups. The synthetic call group was as attractive to females as the same natural call group. The 700 Hz call group was not meaningful in mate choice. The combined (700 Hz + 3500 Hz) call group was significantly less attractive to females than the 3500 Hz call group. Thus, making a call more spectrally complex without increasing its overall amplitude decreases its attractiveness to cricket frog females.     

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.     

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.     

Anuran mating calling circuits: inhibition by prostaglandin

Male American toads (Bufo americanus) were induced to mating call in response to electronically simulated, conspecific mating calls. The injection of prostaglandin (PG) F2 alpha caused suppression of mating call answering. Neural correlates of mating calling were triggered by electrical stimulation of the anterior preoptic nucleus in the isolated brainstem of male, Northern leopard frogs (Rana p. pipiens). The addition of PGF2 alpha to the bath completely abolished the correlates of mating calling without changing the correlates of pulmonary respiration. The suppression of mating calling shown here, along with the suppression of release signalling described by Diakow and Nemiroff (1981), supports the hypothesis of a close interrelation between the neural circuits of these two calls. The suppression of the neural correlates of mating calling in an isolated preparation shows a central site of action of the PG. The retention of normal correlates of pulmonary respiration, even after suppression of mating calling correlates, suggests that the generation of mating calling patterns involves the extension and pulsing of the expiratory phase of breathing.     

The Energetics of Male Mating Strategies in Field Crickets (Orthoptera: Gryllinae: Gryllidae)

Male field crickets (Gryllinae: Gryllidae: Orthoptera) vary in their mating strategies, particularly in whether they call from defended sites to attract phonotactic females or roam silently in search of potential mates. To better understand the economics underlying these alternative strategies, respirometry was employed to examine the energetic costs of each strategy's component behaviors for a representative species, Acheta domesticus. Advertisement calling in this species, composed of low pulse rate chirps, is an order of magnitude less energetically costly than walking per unit time. However, for gryllids that advertise call with higher pulse rate trills, calling and walking appear to be of equivalent energetic cost. Thus, if energetic costs are important in determining grylline mating strategies, trillers and chirpers should have different sensitivities to change in factors affecting the relative payoffs of each strategy. Field studies of changes in mating behavior with increased population density support this argument. This study also determined that courtship calling by A. domesticus was over twice as energetically costly as advertisement calling per unit time, suggesting its importance as a more reliable indicator of signaler, or mate, quality.     

THE SENSORY BASIS OF SEXUAL SELECTION FOR COMPLEX CALLS IN THE TÚNGARA FROG,PHYSALAEMUS PUSTULOSUS (SEXUAL SELECTION FOR SENSORY EXPLOITATION)

Male túngara frogs (Physalaemus pustulosus) vocalize to attract females, and enhance the attractiveness of their simple, whine-only call by adding chucks to produce complex calls. Complex calls contain more total energy and are of longer duration. By virtue of the greater frequency range of the chuck, complex calls also simultaneously stimulate both the amphibian papilla and the basilar papilla of the frog's inner ear. Female phonotaxis experiments using synthetic stimuli demonstrate that an increase in the call's acoustic energy is not sufficient to account for the enhanced attractiveness of the complex call. However, the stimulation of either or both of the female's sound-sensitive inner-ear organs is sufficient to elicit her preference. We suggest that the female's sensory system generates selection that equally favors at least three evolutionary alternatives for enhancing call attractiveness and that historical constraints imposed by the male's morphology determined which of the alternatives was more likely to evolve. These data are consistent with our hypothesis of sensory exploitation, which states that selection favors those traits that elicit greater stimulation from the female's sensory system and which emphasizes the nonadaptive nature of female preference.     

The rôle of call frequency and the auditory papillae in phonotactic behavior in male Dart-poison frogs <Emphasis Type="Italic">Epipedobates femoralis</Emphasis> (Dendrobatidae)

Territorial males of the pan-Amazonian Dart-poison frog, Epipedobates femoralis, are known to present stereotypic phonotactic responses to the playback of conspecific and synthetic calls. Fixed site attachment and a long calling period within an environment of little temperature change render this terrestrial and diurnal pan-Amazonian frog a rewarding species for field bioacoustics. In experiments at the field station Aratai, French Guiana, we tested whether the prominent frequency modulation of the advertisement-call notes is critical for eliciting phonotactic responses. Substitution of the natural upward sweep by either a pure tone within the species frequency range or a reverse sweep did not alter the males' phonotactic behavior. Playbacks with artificial advertisement calls embedded in high levels of either low-pass or high-pass masking noise designed to saturate nerve fibers from either the amphibian papilla or basilar papilla showed that male phonotactic behavior in this species is subserved by activation of the basilar papilla of the inner ear.     

Call differences and calling site segregation in anuran species from central Amazonian floating meadows

Summary The acoustic behaviour of 15 sympatric and synchronically breeding species of frogs in an area of floating meadows near Manaus (Brazil) was studied for a period of 8 months. The calling positions of each species can be identified with certain physiognomic types of vegetation.Sound analyses were used to compare the mating calls. The main variables are dominant frequency, call duration and pulse repetition rate. Each of the 15 species has a distinct mating call and differs from the acoustic behaviour of each other one. Eleven species are separated in their dominant frequency ranges within their specific calling sites. Species sharing emphasised frequency ranges within identical calling sites differ greatly in at least two temporal variables.The roles of calling position, spectral, and temporal features of mating calls in species recognition and premating reproductive isolation are discussed.     

Variation in Male Calling Behaviour and Relation to Male Mating Success in the Strawberry Poison Frog (Dendrobates pumilio)

Calling behaviour and the characteristics of the males’ call are important for mate attraction, female mate choice and male mating success in anurans. In this study I investigated the variation in calling activity and the variation in one spectral (dominant frequency) and four temporal properties (call rate, call duration, duty cycle and pulse rate) of the advertisement call of strawberry poison frogs, Dendrobates pumilio, in two Costa Rican populations during two study periods. Regarding all call properties, no differences were found between populations or years, but between‐male variation was significantly higher than within‐recording and within‐male variation. Dominant frequency was less variable within and among males than temporal call properties and I classified the former as static and the latter as intermediate properties of the call. No call property seemed to be strongly affected by body length or weight. Moreover, I used behavioural observations to relate male calling behaviour to mating success. Calling activity was more variable between males and accounted for more variability in mating success in multiple regression models than any call property. Some call properties (call rate, dominant frequency and pulse rate) were also related to male mating success in one or two study periods. These call properties are probably important for females during courtship to assess their prospective mate and/or for competitive male–male interactions. Furthermore, I compared call properties and mating success of some males for which data were available for both study periods. Pulse rate was lower in the second than in the first year, suggesting age‐related changes in this call property. Moreover, male D. pumilio increased their relative mating success from the first to the second study year. Together with other studies, the data of this study suggest that, in anurans, endurance rivalry contributes more to variation in male mating success than does female choice based on male characteristics.     

Analysis of acoustically evoked call suppression behaviour in a neotropical treefrog

We broadcast synthetic call notes to male Eleutherodactylus coqui treefrogs in their natural habitat. The frogs avoided acoustic overlap with relatively long duration tone stimuli by calling only within the short silent interval between tones. We also observed a temporal change in call pattern in response to tone stimuli of various frequencies and intensities. This response is the basis for construction of a behavioural auditory threshold function for this species. This function does not show a sensitivity maximum at frequencies corresponding to those in the advertisement call, and demonstrates that the frogs are capable of behaviourally responding to sounds over a frequency range which is greater than that required for detection of the species-specific vocalizations and sufficient for detection of at least one sympatric anuran species.     

Bird calls: just emotional displays or something more?

Two widely held assumptions about the sounds of birds and other animals are (1) they are impulsive and involuntary, and cannot be controlled, and (2) they are based only on emotion, apparently because the stimuli eliciting them are thought to be very generalized. The validity of these assumptions has been tested in studies of the alarm calling and food calling behavior of domestic chickens. Videotapes of aerial and ground predators–a hawk overhead and a raccoon on the ground–were effective in eliciting the two major classes of alarm calls. The frequency of aerial alarm calling was strongly affected by presence or absence of a companion, while other aspects of antipredator behavior were unchanged. This so-called "audience effect" on calling is not found with the ground predator call, apparently because this call is addressed to the predator as well as companions. The rules for audience effects are different again with food calling. Evidently calling is not completely impulsive, but can be controlled. By varying the attributes of digitized video images of predators we have shown that stimuli eliciting the aerial predator alarm call are quite specific, encoding different information than the ground predator call. Playback experiments demonstrate that another chicken can decode this information, and react adaptively. Although emotion is undoubtedly involved in bird calling, we conclude that simple emotion-based models of bird calls are inadequate as the sole basis for explaining the vocal behavior of birds.     

Bird calls: just emotional displays or something more?

Two widely held assumptions about the sounds of birds and other animals are (1) they are impulsive and involuntary, and cannot be controlled, and (2) they are based only on emotion, apparently because the stimuli eliciting them are thought to be very generalized. The validity of these assumptions has been tested in studies of the alarm calling and food calling behavior of domestic chickens. Videotapes of aerial and ground predators–a hawk overhead and a raccoon on the ground–were effective in eliciting the two major classes of alarm calls. The frequency of aerial alarm calling was strongly affected by presence or absence of a companion, while other aspects of antipredator behavior were unchanged. This so-called "audience effect" on calling is not found with the ground predator call, apparently because this call is addressed to the predator as well as companions. The rules for audience effects are different again with food calling. Evidently calling is not completely impulsive, but can be controlled. By varying the attributes of digitized video images of predators we have shown that stimuli eliciting the aerial predator alarm call are quite specific, encoding different information than the ground predator call. Playback experiments demonstrate that another chicken can decode this information, and react adaptively. Although emotion is undoubtedly involved in bird calling, we conclude that simple emotion-based models of bird calls are inadequate as the sole basis for explaining the vocal behavior of birds.     

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.     

Mating behaviour and male mating success in the green treefrog

Green treefrogs, Hyla cinerea, at a study site in eastern Georgia behaved as prolonged breeders: there were many more males present each night than females, the arrival of which was unpredictable. Individual males were usually consistent in their behaviour during a single night, and were most often observed calling. There was a weak, negative correlation between male size (snout-vent length, unless otherwise stated) and the frequency of satellite behaviour, defined as a non-calling male's being situated near a calling male. In 2 of 3 years, the mean size of males observed as satellites was less than that of the calling males with which they were associated on a given night; however, many satellites were the same size or larger than calling males. The distributions of matings per male during three seasons were not significantly different than Poisson distributions with the same means. Individual mating success was best predicted by attendance at the breeding site; mating success was negatively related to the frequency of satellite behaviour in some analyses, but very little of the variance was explained. An exhaustive series of analyses failed to show any pattern of size-dependent mating, including weight-assortative mating, even when males that were frequently satellites were excluded. The relative sizes of males and females in amplexus had little effect on fertilization success. On a seasonal basis, males were clumped in their spatial distribution, and matings tended to occur where male density was highest. Individual males were highly variable in their patterns of movement, which were not correlated with size or mating success. Mating success was also unrelated to the frequency (Hz) of the low-frequency spectral peak in the advertisement call of the male; male size and weight were negatively correlated with the frequency of the low-frequency peak.     

Flexibility as a Strategy for Avoiding Call Overlap in Male Anhui Treefrogs

Male-male vocal competition is critical for mating success in anuran species; however, it remains unknown that how males regulate their competitive strategies dynamically during competition because calling is highly time-consuming, energetically demanding and likely to increase predation risks. Since different parts of calls will encode different information for vocal communication, we hypothesized that competitive strategies of male frogs may be modulated by the temporal and spectral features of different call notes. To test this hypothesis, the natural advertisement calls(OC), its modified versions with the first call note replaced by white noise(WN) or other notes and with the fifth call note replaced by WN, were played back to the Anhui tree frogs(Rhacophorus zhoukaiyae). Results showed that 1) males produced more competitive calls in response to acoustic stimuli compared to their baseline calling during silence; and 2) males emitted more non-overlapping calls compared to overlapping calls in response to the acoustic stimuli. These results are consistent with the idea that males are flexible to acoustic signals and their competition strategies are modulated dynamically by social contexts.     

Spatio-Temporal Dynamics of Field Cricket Calling Behaviour: Implications for Female Mate Search and Mate Choice

Amount of calling activity (calling effort) is a strong determinant of male mating success in species such as orthopterans and anurans that use acoustic communication in the context of mating behaviour. While many studies in crickets have investigated the determinants of calling effort, patterns of variability in male calling effort in natural choruses remain largely unexplored. Within-individual variability in calling activity across multiple nights of calling can influence female mate search and mate choice strategies. Moreover, calling site fidelity across multiple nights of calling can also affect the female mate sampling strategy. We therefore investigated the spatio-temporal dynamics of acoustic signaling behaviour in a wild population of the field cricket species Plebeiogryllus guttiventris. We first studied the consistency of calling activity by quantifying variation in male calling effort across multiple nights of calling using repeatability analysis. Callers were inconsistent in their calling effort across nights and did not optimize nightly calling effort to increase their total number of nights spent calling. We also estimated calling site fidelity of males across multiple nights by quantifying movement of callers. Callers frequently changed their calling sites across calling nights with substantial displacement but without any significant directionality. Finally, we investigated trade-offs between within-night calling effort and energetically expensive calling song features such as call intensity and chirp rate. Calling effort was not correlated with any of the calling song features, suggesting that energetically expensive song features do not constrain male calling effort. The two key features of signaling behaviour, calling effort and call intensity, which determine the duration and spatial coverage of the sexual signal, are therefore uncorrelated and function independently.     

A comparative study of auditory sensitivity in the genus Bufo (amphibia)

Multi-unit response from the torus semicircularis were recorded to obtain neural audiograms for five different species, subspecies and races of the genus Bufo:Bufo b.bufo, Bufo b. spinosus, two races of Bufo viridis, and Bufo americanus.All of the audiograms were clearly bimodal, with a low frequency peak and a high frequency peak. A less pronounced but distinguishable intermediate peak seems to be an indication of trimodality. In the low-frequency range, the audiograms of the five groups differed little or not at all. There were pronounced differences, however, in the high-frequency range. This frequency band includes the frequencies of the conspecific mating calls. The best matching between call frequency and auditory best frequency was found in the Bufo viridis group.While it is likely that factors other than the signal characteristics in the vocal repertoire may shape the sensitivity of the auditory system, it is notable that those anuran species in which the mating call clearly facilitates reproduction have a more pronounced sensitivity peak at the frequencies in their mating calls.     

The separate and combined effects of harmonic structure, phase, and FM on female preferences in the barking treefrog (Hyla gratiosa)

In natural advertisement calls of the barking treefrog, Hyla gratiosa, a small amount of incoherent frequency modulation (FM) is present. Incoherency in the FM of a call creates inharmonicity and phase changes between its frequency components. In this study, the combined and separate effects of the harmonic structure, phase spectrum, and FM of an advertisement call on female choice were tested. The harmonic structure of a call can have a direct effect on female preference; females showed a significant preference for static-inharmonic calls over static-harmonic calls. Neither differences in phase or FM alone conferred a preference in two choice tests. However, when FM is present in both calls it does influence female preference for harmonic structure -namely harmonic calls become preferable to inharmonic calls. This reversal of female preference for inharmonicity in a call by the presence of FM suggests that call parameters may interact, and thereby effect mate choice.Abbreviations AP amphibian papilla - BP basilar papilla - FM frequency modulation - PM phase modulation - HS harmonic structure - GB Gaussian Band