Temporal call changes and prior experience affect graded signalling in the cricket frog

We investigated how male cricket frogs Acris crepitans, alter their advertisement calls in response to broadcasts of synthetic calls that were either 'attractive' or 'aggressive'. The stimulus calls differed in temporal but not spectral characteristics. Male cricket frogs produced a more aggressive call when presented with the aggressive stimulus, indicating that they perceived the temporal differences between the two call categories. The direction and degree of temporal and spectral changes depended on the relative dominant frequency of the resident and opponent. If the resident's dominant frequency was initially higher than the stimulus frequency, the pattern of change in dominant frequency mirrored that seen for the temporal call characters. In contrast, if the resident's initial dominant frequency was below that of the stimulus, then the temporal and spectral changes were in opposite directions. Furthermore, stimulus order influenced whether males responded differently to playbacks of aggressive and attractive calls; males that received the aggressive call first produced more aggressive calls during the aggressive stimulus, while males that received the attractive call first produced similar calls in response to the two stimuli. This suggests that experience with different types of signals influences the subsequent calling behaviour of male cricket frogs. Copyright 1999 The Association for the Study of Animal Behaviour.     

Coevolution of Male and Female Response Preferences to Sexual Signals in Music Frogs

Male signaling influences both female choice and male-male competition. Although male signaling characteristics and female preferences have been shown to coevolve in many species, few studies have examined whether male signal characteristics and male receiver responses related to male-male competition also coevolve. The present study tested the hypothesis that male and female signal receiver preferences may coevolve in parallel for frogs in the genus Babina by comparing the acoustic structure of male advertisement calls of four closely related and geographically isolated Babina species. Then we assessed the behavioral responses of both male and female B. daunchina(Emei music frog) to male call playbacks from each of the four species. The results support the hypothesis that male and female signal receiver preferences have coevolved in this species. Specifically, both male and female B. daunchina respond strongly to the heterospecific calls of B. hainanensis, suggesting that preexisting biases exist in both females and males. Both male and female individuals showed a slight response to the calls of B. adenopleura while no response was evoked by the calls of B. lini. The manifestation of similar response profiles in male and female B. daunchina to the calls of the four species support the idea that male and female signal receiver preferences evolved in parallel and that the origin of these receiver biases reflects adaptations dependent on the same neural and cognitive systems in both sexes.     

Significance of temporal and spectral acoustic cues for sexual recognition in Xenopus laevis

As in many anurans, males of the totally aquatic species, Xenopus laevis, advertise their sexual receptivity using vocalizations. Unusually for anurans, X. laevis females also advertise producing a fertility call that results in courtship duets between partners. Although all X. laevis calls consist of repetitive click trains, male and female calls exhibit sex-specific acoustic features that might convey sexual identity. We tested the significance of the carrier frequency and the temporal pattern of calls using underwater playback experiments in which modified calls were used to evoke vocal responses in males. Since males respond differently to male and female calls, the modification of a key component of sexual identity in calls should change the male's response. We found that a female-like slow call rhythm triggers more vocal activity than a male-like fast rhythm. A call containing both a female-like temporal pattern and a female-like carrier frequency elicits higher levels of courtship display than either feature alone. In contrast, a male-like temporal pattern is sufficient to trigger typical male-male encounter vocalizations regardless of spectral cues. Thus, our evidence supports a role for temporal acoustic cues in sexual identity recognition and for spectral acoustic cues in conveying female attractiveness in X. laevis.     

The relationship between perception and production in songbird vocal imitation: what learned calls can teach us

Songbirds produce calls as well as song. This paper summarizes four studies of the zebra finch long call, used by both sexes in similar behavioral contexts. Female long calls are acoustically simpler than male long calls, which include acoustic features learned during development. Production of these male-typical features requires an intact nucleus robustus archistriatalis, the sexually-dimorphic source of the telencephalic projection to brainstem vocal effectors. In experiments that quantified the long calls produced in response to long call playbacks, intact adult zebra finch males, but not females, show a categorical preference for the long calls of females over those of males. Experiments with synthetic stimuli showed that males classify long call stimuli that they hear by gender, using both spectral and temporal information, but that females use only temporal information. Juvenile males (<45 days) did not show the categorical preference, but it emerged during the same period when the robustus archistriatalis matures anatomically and the first male-typical vocalizations are produced. Adult males with robustus archistriatalis lesions lost the categorical preference for female long calls, suggesting that the robustus archistriatalis plays a role in long call discrimination. These results demonstrate that calls complement song as a potent tool for studying the neurobiology of vocal communication.     

Mating Signals Indicating Sexual Receptiveness Induce Unique Spatio-Temporal EEG Theta Patterns in an Anuran Species

Female mate choice is of importance for individual fitness as well as a determining factor in genetic diversity and speciation. Nevertheless relatively little is known about how females process information acquired from males during mate selection. In the Emei music frog, Babina daunchina, males normally call from hidden burrows and females in the reproductive stage prefer male calls produced from inside burrows compared with ones from outside burrows. The present study evaluated changes in electroencephalogram (EEG) power output in four frequency bands induced by male courtship vocalizations on both sides of the telencephalon and mesencephalon in females. The results show that (1) both the values of left hemispheric theta relative power and global lateralization in the theta band are modulated by the sexual attractiveness of the acoustic stimulus in the reproductive stage, suggesting the theta oscillation is closely correlated with processing information associated with mate choice; (2) mean relative power in the beta band is significantly greater in the mesencephalon than the left telencephalon, regardless of reproductive status or the biological significance of signals, indicating it is associated with processing acoustic features and (3) relative power in the delta and alpha bands are not affected by reproductive status or acoustic stimuli. The results imply that EEG power in the theta and beta bands reflect different information processing mechanisms related to vocal recognition and auditory perception in anurans.     

Female greater wax moths reduce sexual display behavior in relation to the potential risk of predation by echolocating bats

Female greater wax moths Galleria mellonella display by wing fanning in response to bursts of ultrasonic calls produced bymales. The temporal and spectral characteristics of these callsshow some similarities with the echolocation calls of batsthat emit frequency-modulated (FM) signals. Female G. mellonellatherefore need to distinguish between the attractive signalsof male conspecifics, which may lead to mating opportunities,and similar sounds made by predatory bats. We therefore predictedthat (1) females would display in response to playbacks of male calls; (2) females would not display in response to playbacksof the calls of echolocating bats (we used the calls of Daubenton'sbat Myotis daubentonii as representative of a typical FM echolocatingbat); and (3) when presented with male calls and bat callsduring the same time block, females would display more whenperceived predation risk was lower. We manipulated predationrisk in two ways. First, we varied the intensity of bat callsto represent a nearby (high risk) or distant (low risk) bat.Second, we played back calls of bats searching for prey (lowrisk) and attacking prey (high risk). All predictions weresupported, suggesting that female G. mellonella are able todistinguish conspecific male mating calls from bat calls, andthat they modify display rate in relation to predation risk.The mechanism (s) by which the moths separate the calls ofbat and moth must involve temporal cues. Bat and moth signalsdiffer considerably in duration, and differences in durationcould be encoded by the moth's nervous system and used in discrimination.     

Perceptual specificity in the alarm calls of Gunnison's prairie dogs

Gunnison's prairie dogs have a complex alarm communication system. We show that the escape responses of prairie dogs to naturally occurring live predators differed depending upon the species of predator. We also show that playbacks of alarm calls that were elicited originally by the live predators produced the same escape responses as the live predators themselves. The escape responses fell into two qualitatively different categories: running to the burrow and diving inside for hawks and humans, and standing upright outside the burrow for coyotes and dogs. Within these two categories there were differences in response. For hawks, only the prairie dogs that were in the direct flight path of a stooping red-tailed hawk ran to their burrows and dove inside, while for humans and human alarm call playbacks there was a colony-wide running to the burrows and diving inside. For coyotes and coyote alarm call playbacks there was a colony-wide running to the burrows and standing alert at the burrow rims, while for domestic dogs and playbacks of alarm calls for domestic dogs the prairie dogs assumed an alert posture wherever they were feeding, but did not run to their burrows. These responses to both the live predators and to predator-elicited alarm calls suggest that the alarm calls of Gunnison's prairie dogs contain meaningful referential information about the categories of predators that approach a colony of prairie dogs.     

Free-Ranging Male Koalas Use Size-Related Variation in Formant Frequencies to Assess Rival Males

Although the use of formant frequencies in nonhuman animal vocal communication systems has received considerable recent interest, only a few studies have examined the importance of these acoustic cues to body size during intra-sexual competition between males. Here we used playback experiments to present free-ranging male koalas with re-synthesised bellow vocalisations in which the formants were shifted to simulate either a large or a small adult male. We found that male looking responses did not differ according to the size variant condition played back. In contrast, male koalas produced longer bellows and spent more time bellowing when they were presented with playbacks simulating larger rivals. In addition, males were significantly slower to respond to this class of playback stimuli than they were to bellows simulating small males. Our results indicate that male koalas invest more effort into their vocal responses when they are presented with bellows that have lower formants indicative of larger rivals, but also show that males are slower to engage in vocal exchanges with larger males that represent more dangerous rivals. By demonstrating that male koalas use formants to assess rivals during the breeding season we have provided evidence that male-male competition constitutes an important selection pressure for broadcasting and attending to size-related formant information in this species. Further empirical studies should investigate the extent to which the use of formants during intra-sexual competition is widespread throughout mammals.     

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.     

Aggressive Thresholds of Male Pacific Treefrogs for Advertisement Calls Vary with Amplitude of Neighbors' Calls

In breeding choruses, male Pacific treefrogs (H. regilla) produce advertisement and encounter calls. The role of each call type in establishing intermale spacing patterns was investigated by playing back, at various amplitudes, recordings of these vocalizations to resident males. The aggressive threshold of a male for each call type was defined as the lowest amplitude of playback that elicited encounter calls. Pacific treefrogs consistently had lower aggressive thresholds to playbacks of encounter calls than to playbacks of advertisement calls. Aggressive thresholds to playbacks of advertisement calls were positively correlated with the maximum amplitude of the advertisement calls of neighboring males, as measured at the position of the focal male.     

The calling song of the field cricket,Gryllus bimaculatus (de geer): constraints on transmission and its role in intermale competition and female choice

Field studies of calling male field crickets, Gryllus bimaculatus, showed that males formed calling aggregations. Within aggregations males appeared to maintain an exclusive female-attraction zone about their burrows; calling song may thus serve as an aggressive signal to neighbouring males to maintain spacing. Calling song attenuates with distance. Furthermore, calls became degraded with distance by the loss of low frequency components and a reduction in the interval between chirps and pulses due to reverberation. Playback experiments suggested that the predictable degrading properties of the call may serve as a distance-finding mechanism maintaining observed male spacing. The intensity of calls and the repetition rate of chirps and pulses was positively correlated with male size. While information contained within the intensity parameter of calls may prove unreliable due to unpredictable attenuation and irregular amplitude fluctuations, the repetition rate of chirps and pulses was not affected by distance degradation. Playback experiments in which intensity was controlled suggested that females orientate preferentially to the calls of large males.     

Sexual selection and adult male orangutan long calls

Long calls given by adult male orangutans (Pongo pygmaeus) have been hypothesized to mediate interindividual spacing among male orangutans and to attract female orangutans, to high-ranking mates over long distances. To test these two hypotheses I conducted observations of calling behaviour and a series of experimental playbacks of recorded long calls. The findings were consistent with the male-spacing hypothesis but did not support the mate-attraction hypothesis. Experimental playbacks demonstrate that long calls regulate spacing between males through an approach-avoidance system based on dominance relationships: the highest-ranking adult male approaches calls, while lower-ranking, males avoid calls. The results of playbacks also reveal that sexually active females do not move toward long calls, and therefore do not indicate that long calls function in attracting mates. This latter finding suggests that female mate choice may not have been an important selective factor during the evolution of long calls.     

Complex Vocal Responses to Conspecific Calls in Whistling Frogs Eleutherodactylus johnstonei: Playback Experiments in the Field

We simulated the presence of an acoustic competitor by broadcasting conspecific playbacks to males of Johnstone's whistling frog, Eleutherodactylus johnstonei, in the field. We broadcast calls that differed in duration (short, typical, and long), dominant frequency (high, typical, and low), and period (short, typical, and long), and analyzed male vocal responses. We tested the hypothesis that males respond by escalating vocally when they are exposed to female‐attractive calls and by ignoring unattractive ones. At the population level, males responded to playbacks in ways that would potentially increase their attractiveness with regard to solo calling: males increased the duration, reduced the dominant frequency, and increased their calling effort (duty cycle), despite an increase in call period. The modification of call duration occurred only in response to playbacks of low‐frequency calls, long calls, and short‐period calls (selective response), while the modification of the dominant frequency was independent of the characteristic of the playback (fixed response). Contrary to the expected, males did not reduce the call period when they were exposed to attractive playbacks. At the ultimate level, the results suggest energy‐saving strategies. In addition, males seem to trade off call period for the avoidance of acoustic interference with attractive calls as calling effort was typically increased by increasing call duration but only rarely by reducing the call period. Interactive playbacks are necessary to better understand the calling strategies of males of E. johnstonei.     

Acoustic communication in the Bocon toadfish (<Emphasis Type="Italic">Amphichthys cryptocentrus</Emphasis>)

The soundscapes of many coastal habitats include vocalizations produced by species of the family Batrachoididae (toadfish and midshipman). We describe the calling and grunting behavior of male Amphichthys cryptocentrus, a tropical toadfish, and predict how these vocalizations are influenced by conspecifics. We recorded individual males, which produced broadband grunts and multi-note, harmonic “boatwhistle” calls. Grunts were either in combination with calls or stand-alone. We used a null model to test if these latter grunts were produced at random or in response to calls from conspecifics. The model supports the hypothesis that grunts were in response to calls from neighboring males, suggesting acoustic competition. Using the most conservative estimate of hearing abilities we predict that males responded to the second harmonic of neighbor’s calls (230 Hz) at amplitudes of approximately 100–125 dB re 1μPa²/Hz. We also observed that call and grunt rates increased when males were exposed to higher rates of acoustic activity from neighboring fish. Fish used grunts to respond to background calls that occurred at different amplitudes, suggesting they responded to the calls of multiple neighboring fish and not just the highest amplitude neighbor. This communication with multiple fish within hearing range suggests a communication network in which the spatial distribution of individual toadfish relative to one another will impact their vocal behavior. Thus, the density and distribution, and not just abundance, of these toadfish at a given site will influence the characteristics of the chorus and the role of this species in the local soundscape.     

Perception of female reproductive state from vocal cues in a mammal species

While acoustic signalling by males is known to affect male-male competition, mate attraction and the timing of ovulation, the extent to which sexual selection has shaped the evolution of female acoustic signals is poorly understood. Among mammals, experimental evidence indicates that females attract mating partners by using olfactory and visual signals to advertise their reproductive state. Whether or not males ascertain female reproductive state from vocal signals has, however, never been systematically tested. In this study, we use playbacks of recorded vocalizations to demonstrate that male Barbary macaques, Macaca sylvanus, can discriminate between female copulation calls given at different stages of the oestrous cycle, responding more strongly to those given around the time when conception is most likely to occur. Acoustic analysis suggests that the mean dominant frequency of call units and a number of temporal parameters could provide males with the information necessary to discern the proximity of ovulation in this way Our results provide the first experimental evidence that the calls of female mammals may contain information on reproductive state, which males can perceive and use in such a way as to increase their reproductive success.     

The function of Barbary macaque copulation calls.

In a wide variety of animal species, females produce vocalizations specific to mating contexts. It has been proposed that these copulation calls function to incite males to compete for access to the calling female. Two separate advantages of inciting male-male competition in this way have been put forward. The first suggests that as a result of calling, females are only mated by the highest ranking male in the vicinity (indirect mate choice hypothesis). The second proposes that copulation calling results in a female being mated by many males, thus promoting competition at the level of sperm (sperm competition hypothesis). In this paper, I give results from the first experimental study to test these hypotheses. Playback was used to examine the function of copulation calls of female Barbary macaques (Macaca sylvanus) in Gibraltar. Although rank did not affect lone males'' likelihood of approaching copulation calls, when playbacks were given to pairs of males only the higher ranking individual approached. Moreover, females were mated significantly sooner after playback of their copulation call than after playback of a control stimulus. These results suggest that the copulation calls of female Barbary macaques play a key role in affecting patterns of male reproductive behaviour, not only providing an indirect mechanism of female choice, but also promoting sperm competition by reducing the interval between copulations. Potential fitness benefits of inciting male-male competition at these two levels are discussed.     

Underground mating in the fiddler crab Uca tetragonon: the association between female life history traits and male mating tactics

Brood size and other life-history traits of females affect male investment in mating. Female Uca tetragonon, producing relatively small broods, were attracted to the burrows of males for underground mating (UM) while carrying eggs. Most UM females released larvae and ovulated new broods during the pairing, averaging 3.9 days. While a female was incubating one brood, another brood was developing within the ovaries because the females were feeding adequately during incubation. These findings suggest that in U. tetragonon, a small-brood species, females increase the total number of broods produced by breeding continually. In contrast, in large-brood species, feeding by ovigerous females is relatively brief and not enough to prepare the next brood during incubation, inducing temporal separation between incubation and brood production. Unlike females in other ocypodids where females with large broods remain in the breeding burrows of males, most female U. tetragonon left the male after UM. Wandering in female U. tetragonon after the pairs separate may occur because their small broods are adequately protected by an abdominal flap. Relative brood size probably determines the vulnerability of the incubated broods to the females' surface behavior. Hence, male reproductive success in large-brood species may decrease greatly if males expel their mates after ovulation, although this is not necessarily so in small-brood species. Whether the male drives away the female or not may depend on which behavior within either small- or large-brood species yields the greater male reproductive success. In U. tetragonon some females extruded eggs in their own burrows after surface mating as well as in males' burrows after UM. It was unclear whether females chose a male with a larger burrow as an UM mate unlike several large-brood species. Burrows of both UM males and ovigerous females in U. tetragonon were relatively smaller than those in some large-brood species, indicating that incubation of small broods does not require large burrows. Rather than benefits of UM by female choice, wandering resulting from intersexual conflict, and sperm competition may explain why some females mate in males' burrows in this small-brood species.     

Individual and Species Differences in Quail Calls (Coturnix c. japonica,c. c. coturnix and a Hybrid)

Male European and Japanese male quail have very stereotyped calls. This study examined which parameters best discriminated between individuals, and which between the two sub-species and a hybrid of the two (European father x Japanese mother). Recordings were made of several calls from individual Japanese, European and hybrid quail, from which sonograms were made and analyzed. We found that parameters describing the time structure of the call discriminated best between individuals. Time structure also showed the greatest differences between the two sub-species and the hybrid. Hybrid calls were extremely variable, individual hybrids often producing more than one call type, occasionally of both sub-species types. However, individuals could still be identified from the call parameters. In addition, we investigated responses of males to playbacks of calls from all three quail types. European and Japanese males responded most strongly, with calling, to the playbacks of the calls of their own sub-species, intermediately to playbacks of the hybrid and least to those of the other sub-species.     

Calling Patterns in Male Responses to Conspecific Playbacks in the Johnstone's Whistling Frog Eleutherodactylus johnstonei

Vocal interactions are common in chorusing frogs. Changes in the calling patterns of Eleutherodactylus johnstonei males were analyzed by recording their responses to playbacks of conspecific calls repeated at fixed periods (long: 1.7 s, short: 0.98 s). The call period and timing, estimated through the onset response time, were determined for each male. Males reduced and regularized the period of their calls in response to both stimuli, regardless of their absolute and relative period (i.e., the difference between the male's period and the stimulus period). Males avoided initiating their calls during ongoing stimuli, but did not time their calls in the silent gap between successive stimuli in ways that reduced the probability of overlap: the proportion of calls without overlap did not depart from random expectations when the silent gap was long, and was smaller than expected when the gap was short. This result indicated that males react to the presence of the virtual competitor but not to its particular characteristics. Fixed responses have been described in other anurans, and often relate to trade-offs between female attraction, male competition, predator attraction, and depletion of energy reserves. Lack of coordination with the stimuli, beyond inhibition of calling during an ongoing stimulus, also indicates somewhat rigid vocal strategies, at least under the experimental conditions. Results from the short period trials suggested a compromise between maintaining a call period and avoiding call overlap. Whether female behavior is influenced by call interference and whether males pay selective attention to distant males instead of to close neighbors must be investigated to better understand the vocal behavior of E. johnstonei .     

Mating Call Discrimination in Female European (Coturnix c. coturnix) and Japanese Quail (Coturnix c. japonica)

Each year, thousands of domestic Japanese and hybrid quails are released within the breeding range of the European quail. We showed recently that no post‐zygotic isolating mechanisms have yet been established between these subspecies. The aim of this study was to investigate whether pre‐zygotic mechanisms are strong enough to prevent hybridization. We tested the level of subspecies selectivity in females of European and Japanese quail respectively using playbacks of European, hybrid and Japanese male mating calls. European quail females emitted the greatest number of rally calls in response to mating calls by conspecific males. Their responses were the weakest to mating calls produced by males of the other subspecies and intermediate to mating calls by hybrid males. In contrast, Japanese quails produced similar responses to all types of mating calls. These results suggest that mixed pairs could form in the wild. The European quail could thus become one of the most endangered galliforms of the Western Palearctic.