THE FUNCTION OF CALL ALTERNATION IN ANURAN AMPHIBIANS: A TEST OF THREE HYPOTHESES

Males of many species of anurans alternate calls with those of their neighbors in a chorus. This pattern of calling reduces signal interference and may: 1) facilitate intermale spacing because males can better gauge the intensity of neighbors' calls if these calls do not overlap with their own; 2) help preserve species-specific temporal information in calls required to attract females; and/or 3) make it easier for females to localize males in the chorus. I tested these hypotheses with three species that exhibit call alternation, Hyla crucifer, H. versicolor, and H. microcephala. Males of all three species gave more aggressive calls to high-intensity synthetic stimuli that alternated with their calls than to those that overlapped their calls. These results support the first hypothesis. Results of four-speaker female choice experiments using alternating and overlapping calls indicate that preservation of signal integrity also is important in H. versicolor and H. microcephala, species that have fine-scale temporal information in their calls. However, the third hypothesis was not supported; females failed to discriminate among alternating and overlapping calls if the problem of signal disruption was eliminated or irrelevant.     

Synchronized interdigitated calling in the Kuvangu running frog, Kassina kuvangensis

Male Kuvangu frogs show repetitive calling of pulsed advertisement calls in which up to seven calls are repeated in short succession. Recordings of pairwise interactions between males showed that calls were highly synchronized, with individual calls interdigitating with each other. Males frequently switched between the leader and follower role with neither male dominating the interaction. Interactive playback experiments using synthetic calls revealed that males slightly but significantly increased the number of calls per call group with increases in stimulus call number. Males also significantly increased call rate with the number of calls in the playback stimulus. Furthermore, when presented with shortened intercall intervals, males increased their own intercall intervals, thus ‘skipping’ a call and avoiding overlap with the playback. The low degree of call matching suggests that repetitive calling, apart from maintaining a male's attractiveness to females relative to rival males, may mediate male-male competition. In addition, synchronized interdigitated calling may serve to reduce predation, while maintaining species-specific temporal features of advertisement calls important to females. Kuvangu running frogs may have reduced the costs associated with synchrony and alternation by using a signal timing scheme that allows them to do both simultaneously.Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.       

Robust calling performance in frogs infected by a deadly fungal pathogen

Reproduction is an energetically costly behavior for many organisms, including species with mating systems in which males call to attract females. In these species, calling males can often attract more females by displaying more often, with higher intensity, or at certain frequencies. Male frogs attract females almost exclusively by calling, and we know little about how pathogens, including the globally devastating fungus, Batrachochytrium dendrobatidis, influence calling effort and call traits. A previous study demonstrated that the nightly probability of calling by male treefrogs, Litoria rheocola, is elevated when they are in good body condition and are infected by B. dendrobatidis. This suggests that infections may cause males to increase their present investment in mate attraction to compensate for potential decreases in future reproduction. However, if infection by B. dendrobatidis decreases the attractiveness of their calls, infected males might experience decreased reproductive success despite increases in calling effort. We examined whether calls emitted by L. rheocola infected by B. dendrobatidis differed from those of uninfected individuals in duration, pulse rate, dominant frequency, call rate, or intercall interval, the attributes commonly linked to mate choice. We found no effects of fungal infection status or infection intensity on any call attribute. Our results indicate that infected males produce calls similar in all the qualities we measured to those of uninfected males. It is therefore likely that the calls of infected and uninfected males should be equally attractive to females. The increased nightly probability of calling previously demonstrated for infected males in good condition may therefore lead to greater reproductive success than that of uninfected males. This could reduce the effectiveness of natural selection for resistance to infection, but could increase the effectiveness of selection for infection tolerance, the ability to limit the harm caused by infection, such as reductions in body condition.     

Female begging in European robins: do neighbors eavesdrop for extrapair copulations?

Female European robins beg for food from their mates throughoutthe breeding season using far-carrying "seep" calls which resemblethe begging calls of fledglings. We investigated the possibilitythat these calls are eavesdropped by neighboring males andused as cues to target intrusions during the fertile period.Female seep calling and male courtship feeding peaked in thefertile period, and males appeared to modify provisioning rate in relation to seep calling rate. Further, there was a positivecorrelation between rate of courtship feeding and clutch size,both of which tended to be inversely related to seep callingrates. These observations imply that the seep call is a hungersignal directed at pair males. As the signal is loud and givenmost frequently during the fertile period, it must also contain information about fertility and location. Playback experimentssuggested that this information is eavesdropped by neighboringmales, who responded to rapid rates of seep calling more readilythan slow rates and to calls broadcast at the edge of territoriesrather than their center, presumably in search of extrapaircopulations. Pair males can reduce the intensity of the female's signal by courtship feeding, and thus male provisioning mayprotect paternity.     

Acoustic mimicry and disruptive alternative calling tactics in an Australian bushcricket (Caedicia; Phaneropterinae; Tettigoniidae; Orthoptera): does mating influence male calling tactic?

Abstract.  Male calling and searching tactics are described for a duetting Australian bushcricket, Caedicia sp. 12 (Phaneropterinae; Tettigoniidae; Orthoptera). The repertoire of Caedicia sp. 12 consists of the calling song and, by nonduetting males, a series of calling tactics that include short-click calling, disruptive over-singing and a call mimicking the entire duet. Nonduetting males respond to the production of a duet by another male and a female with short-click calls that mimic the female call at the conclusion of a duet. By manipulating the male's mating history, it is found that this form of calling behaviour is more likely to occur within the male's 6-day postmating refractory period; the low cost tactic allows males to re-mate during spermatophore replenishment. Males also produce disruptive calls in response to a duet, where the male may over-sing the duetting male's signal or produce a call that appears to mimic the entire duet; the male produces a calling song followed by a short signal that has the same latency as the female's reply within a duet. Males also over-sing crucial elements of the duetting-male's song that are normally critical for the female's conspecific recognition. There is no evidence that females search for the duetting male partner, but males unable to enter a duet will search for the call of a responding female. Searching by males is more common when these males are producing disruptive calls. Alternative male calling tactics are discussed as a set of conditional strategies for securing unmated females.     

Nightly calling patterns in a Neotropical gladiator frog

In anurans, vocalization is the primary communication form and acoustic parameters are influenced by climatic conditions, but also by social contexts. We investigated calling site use and within-individual variation of acoustic parameters throughout the night in the gladiator-frog Hypsiboas goianus. We expected that large males would call closer to the water and at higher perches to avoid dehydration and maximize sound propagation. Furthermore, we tested the prediction that males would emit more aggressive calls early in the night and more advertisement calls late at night. Male size was not correlated with either distance from the water or perch height. However, as expected, males of H. goianus adopted a calling strategy that consisted of emitting more aggressive calls early in the night and more advertisement calls later in the night. Furthermore, repetition rate and interval between notes of the aggressive calls and repetition rate of the advertisement calls showed within-individual variation throughout the night that agreed with our expectations. The calling strategy of H. goianus is probably related to the establishment of calling sites early in the night and an investment in female attraction in the middle of the night when males’ aggressive interactions have faded away, or due to habituation increasing the males’ aggressive thresholds. This is the first study investigating within-individual patterns of acoustic parameters of calls throughout the night for anurans.     

Vocal communication in a neotropical treefrog, Hyla ebraccata: Advertisement calls

We studied the vocal communication of Hyla ebraccata in central Panama. The advertisement call of this species consists of a pulsed buzz-like primary note which may be given alone or followed by 1–4 secondary click notes. Primary notes are highly stereotyped, showing little variation within or0 among individuals in dominant frequency, duration, pulse repetition rate or rise time. Males calling in isolation give mostly single-note calls. They respond to playbacks of conspecific calls by increasing calling rates and the proportion of multi-note calls, and by giving synchronized calls 140–200 ms after the stimulus begins. Responses to conspecific advertisement calls are usually given immediately after the primary note of the leading call, but the primary note of the response often overlaps with the click notes of the leading call. Experiments with synthetic signals showed that males synchronize to any type of sound of the appropriate frequency (3 kHz), regardless of the fine structure of the stimulus. Playbacks of synthetic calls of variable duration showed that males do not synchronize well to calls less than 150 ms long, but they do to longer calls (200–600 ms). The variance in response latency increased with increasing stimulus duration, but modal response times remained at around 140–200 ms. Similar results were obtained in experiments withsynthetic calls having a variable number of click notes. Males showed no tendency to increase the number of click notes in their calls in response to increasing stimulus duration or increasing number of clicks in the stimulus. Females preferred three-note to one-note calls in two-choice playback experiments, whether these were presented in alternation, or with the one-note call leading and the three-note call following. Females showed no preference for leader or follower calls when both were one-note. When two-note calls were presented with the primary note of the follower overlapping the click note of the leader, females went to calls in which click notes were not obscured. Our results indicate that male H. ebraccata respond to other males in a chorus in ways which enhance their ability to attract mates.     

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.     

The Sounds of Silence as an Alarm Cue in Túngara Frogs,Physalaemus pustulosus

In many species males vocally advertise for mates in choruses and these choruses serve as acoustic beacons to conspecific females as well as to eavesdropping predators and parasites. Chorusing will often cease in response to disturbances, such as the presence of predators. In some cases the cessation is so rapid and over such a large area that it seems improbable that males are all responding directly to the same local disturbance. Here, we demonstrate experimentally in Neotropical túngara frogs, Physalaemus pustulosus, that the cessation of calling by males spreads rapidly through the chorus. The cessation of chorusing in response to the cessation of playbacks of three calling males is more effective in inducing chorus cessation than is the cessation of one male calling. When three males are calling, the cessation of complex calls is more effective in inducing chorus cessation than simple calls. There is no main effect on whether the final call of the male is complete or is interrupted. We thus conclude that the sudden lack of signals—the ‘sounds of silence’—becomes an alarm cue that can explain the rapid cessation of choruses that are common in many chorusing species.     

Chorusing Behaviour,a Density-dependent Alternative Mating Strategy in Male Common Toads (Bufo bufo)

Male chorusing behaviour was studied in a population of common toads (Bufo bufo) on the island of Öland south Sweden, and the functional role of male advertisement calling in this species was experimentally examined. Calling males were larger and heavier than non-calling males (t = 2.41, p < 0.025 and t = 2.36, p < 0.025, respectively). However, small males were also found to call. This indicates that large males persisted in calling for longer and/or called more often. The proportion of calling males decreased as population size increased during the breeding season, indicating that calling is a low density strategy. Females responded more readily to calls than males. There were insufficient data to determine if the dominant frequencies of advertisement calls were inversely correlated with male body size, however, this relationship was found for the similar release calls. Females were found not to discriminate between high and low frequency calls, but when given a choice between two calls of different sound pressure levels (SPL), females were attracted to the louder calls. Thus, the function of chorusing is to advertise the position of males to mate-seeking females when the population density is low.     

Conspicuous calling near cryptic nests: a review of hypotheses and a field study on white‐browed scrubwrens

Predation is an important source of nest mortality in many bird species and calling near the nest can increase this risk, yet adults of many species regularly vocalize near their nests. Some of these calls serve clearly adaptive functions, such as alarm or provisioning calls. However, many species also give conspicuous ‘contact’ calls near the nest, which is puzzling because the function of these calls is unclear, and they might attract predators. Most studies of parental vocalizations near nests have focused on specific vocalizations and single hypotheses, yet there is a diversity of vocalization types and potential functions. We review the literature on the diversity and possible function of parental vocalizations near the nest, and then investigate the puzzle of conspicuous contact calling near nests by white‐browed scrubwrens Sericornis frontalis. In scrubwrens, ‘chip‐zz’ contact calls were almost always used when adults approached nests, and when they approached one another or changed location. Call composition also changed: the proportion of ‘chip’ elements increased as callers approached the nest or other adults. Neither adult sex nor nestling age affected calling. Thus, chip‐zz calls appear to be used as ongoing signals to other group members of the caller's activity and location, particularly relative to the nest. Nestlings appeared to use the calls as cues of adult arrival, and increased calling as adults approached nests. Further, adults called less after a predator was on the territory, suggesting that parents may be able to reduce the risk of chip‐zz calls betraying nest location, or possibly use the absence of calling as a signal of danger. This study thus demonstrates that calling near nests could inform both adults and nestlings about the caller's behaviour, and could serve multiple functions. Future studies will need to experimentally test these functions, as well as the other hypotheses reviewed here.     

Regulation of Chorusing in the Vibrational Communication System of the Leafhopper Graminella nigrifrons

Male Graminella nigrifrons participate in alternating choruses.Vibrational calls emitted by males consist of three sections(S1, S2, and S3) that differ in pattern of amplitude modulation.In this study we examined the response of single males to syntheticchoruses and to isolated call components to gain insight intothe regulation of chorus structure. Males initiated calls primarilyduring the silent periods within synthetic choruses. In all15 trials the number of overlapping calls and the duration ofoverlap was significantly less than expected if males call atrandom. Playback of S2, S3, or random noise while males emittedS1 caused males to interrupt calling, whereas males continuedto call when S1 or no signal was played. In a related experiment,we played S2 or no signal while males were beginning to emitthe S1, S2, or S3 phase of their calls. In response to thisplayback the duration of S1 and S3 was reduced, but the durationof S2 was not affected. These results suggest that an inhibitory-resettingmechanism may result in alternation of calls in this leafhopper.     

Evolution of Novel Signal Traits in the Absence of Female Preferences in Neoconocephalus Katydids (Orthoptera,Tettigoniidae)

Background Significance

Communication signals that function to bring together the sexes are important for maintaining reproductive isolation in many taxa. Changes in male calls are often attributed to sexual selection, in which female preferences initiate signal divergence. Natural selection can also influence signal traits if calls attract predators or parasitoids, or if calling is energetically costly. Neutral evolution is often neglected in the context of acoustic communication.

Methodology/Principal Findings

We describe a signal trait that appears to have evolved in the absence of either sexual or natural selection. In the katydid genus Neoconocephalus, calls with a derived pattern in which pulses are grouped into pairs have evolved five times independently. We have previously shown that in three of these species, females require the double pulse pattern for call recognition, and hence the recognition system of the females is also in a derived state. Here we describe the remaining two species and find that although males produce the derived call pattern, females use the ancestral recognition mechanism in which no pulse pattern is required. Females respond equally well to the single and double pulse calls, indicating that the derived trait is selectively neutral in the context of mate recognition.

Conclusions/Significance

These results suggest that 1) neutral changes in signal traits could be important in the diversification of communication systems, and 2) males rather than females may be responsible for initiating signal divergence.     

Calling is an honest indicator of paternal genetic quality in poison frogs

Several competing hypotheses have been put forward to explain why females of many species mate preferentially with males possessing the most conspicuous signals (e.g., ornaments, displays, or songs). We performed a laboratory experiment using two species of poison frogs, Dendrobates leucomelas and Epipedobates tricolor, to test the hypothesis that male calling performance is an honest indicator of parental quality. Our analyses are based on data from behavioral observations of mating activities of captive-reared individuals (and their offspring) that were housed in terraria for four consecutive breeding seasons. Male mating success increased with male calling rate and chirp duration in both species, suggesting that females preferred males with more elaborate calls. Because calling performance improved with age in D. leucomelas, female poison frogs that prefer males with more elaborate calls in the wild may end up mating with older males that have already proven their ability to survive. Females that mated with good callers obtained higher quality offspring. Eggs fertilized by males with high calling rates and long chirp durations had higher hatching success and produced tadpoles that were more likely to metamorphose into surviving frogs. As a consequence, females that mated with males with high calling performance obtained more surviving offspring per egg, compared to females that mated with poor callers. Collectively, our findings comply with the notion that female poison frogs prefer to mate with good callers because calling performance is a reliable predictor of offspring quality. The possible influence of maternal allocation and reasons for the strong effect size compared to previous studies are discussed.     

Males of <Emphasis Type="Italic">Hypsiboas goianus</Emphasis> (Anura; Hylidae) do not assess neighbor fighting ability through acoustic interactions

In frogs, acoustic signals are the most important communication mechanism, since they may be used in several social contexts. In many anurans, the dominant frequency of calls is negatively related to body size, and in such species, this spectral parameter may be considered a good predictor of fighting ability. We experimentally investigated the vocal behavior of 30 male Hypsiboas goianus in central Brazil to answer the following questions: (1) Do males change the acoustic parameters of their calls in response to conspecific intruders? and (2) Does the acoustic behavior of H. goianus depend on the simulated body size of their opponent? We used playback of synthesized calls with high (3573 Hz) and low (3123 Hz) dominant frequency to simulate small and large males, respectively. Males reduced the rate of advertisement calling in response to playback but did not change vocal behavior in response to low-frequency and high-frequency playback. So, while males adjust their calling activity in response to simulated conspecifics, there was no evidence that they assess the fighting ability of their opponents through acoustic interactions.     

Invasion of the acoustic niche: variable responses by native species to invasive American bullfrog calls

Biological invasions are a major threat to biodiversity. Invasive species that use acoustic communication can affect native species through interference in the acoustic niche. The American Bullfrog Lithobates catesbeianus is a highly invasive anuran that is widely distributed in the Brazilian Atlantic Rainforest. Adult male bullfrogs emit loud advertisement calls at frequencies that overlap with the calls of several native species of frogs. Given that spectral overlap is a major factor in acoustic masking, the purpose of this study was to test the effects of the acoustic invasion of L. catesbeianus on native frogs that have calls with and without spectral overlap with the invader. In field experiments, we exposed calling males of two overlapping species and two non-overlapping species to recorded bullfrog vocalizations, white noise, and the vocalization of another native frog species. To identify effects, we compared calls recorded before, during, and after exposure. Our results showed that native species altered their calls in response to the bullfrog calls. However, we also observed similar responses to white noise and heterospecific native calls. Both the invasive and heterospecific calls were emitted at low frequencies, which suggests that the observed responses might be specific to low-frequency calls. Our results provide evidence that the introduction of new sounds can cause native species to modify their calls, and that responses to exogenous sounds are species- and stimulus-specific.     

Patterns of Vocal Interactions in a Bullfrog (Rana catesbeiana) Chorus: Preferential Responding to Far Neighbors

In chorusing species, males seem to be spaced non-randomly, and their vocal interactions may be governed by particular behavioral rules. We monitored patterns of vocal interactions in a natural bullfrog ( Rana catesbeiana ) chorus to determine the probability with which calls of individual frogs would follow each other's in dyadic sequences. Expected probabilities of responses in a dyad were calculated based upon the joint probabilities of calling (relative calling rates) of the individual frogs; observed probabilities of response reflected the actual number of following responses in each dyad. Results of statistical tests comparing observed and expected probabilities of responding revealed that, when dyads were closely spaced, observed probabilities of a following response were significantly less than the expected probabilities. Conversely, when dyads were composed of more distant males, observed probabilities of responding were significantly greater than expected. Observed probabilities of response were correlated with inter-male distances; males called more frequently than expected following calls of far neighbors, and less frequently than expected following calls of near neighbors. These data suggest that males attend to both nearby and distant callers, and adjust the onset of their own vocalizations appropriately. Males may be actively inhibited by calls of their near neighbors, and their calling may be actively elicited by the calls of their far neighbors.     

Steroid hormone profiles and relative body condition of calling and satellite toads: implications for proximate regulation of behavior in anurans

Males of most anuran species (frogs and toads) vocalize to attractmates. However, individuals of many vocal species may also adoptalternative noncalling "satellite" tactics. Satellite malescharacteristically remain in close proximity to calling conspecificsand attempt to intercept incoming females attracted to advertisingmales. Emerson proposed that alternation between calling andnoncalling behavior in anurans is mediated by a reciprocal interactionbetween circulating levels of corticosterone and androgens thatis driven by depletion of energy reserves during vocalization.We tested this hypothesis by examining steroid hormone profilesand the relative body condition of calling and satellite Woodhouse'stoads (Bufo woodhousii) and Great Plains toads (B. cognatus).Consistent with Emerson's hypothesis, callers had significantlyhigher circulating corticosterone levels and were in bettercondition than satellites. However, levels of testosterone anddihydrotestosterone did not differ significantly between satellitesand callers, and we found no evidence that high levels of corticosteronehad an inhibitory effect on androgen production in either species.These data thus support a relationship between corticosteronelevels and depletion of energy reserves during bouts of vocalizationbut suggest that alternation between calling and satellite behaviormay be associated with direct effects of corticosterone on brainvocal control centers. We propose a model that incorporatesrelationships among energy reserves, androgens, corticosterone,and arginine vasotocin-producing neurons in the telencephalonto explain transitions between calling and satellite tacticsin toads.     

Alarm calls of wintering great tits Parus major: warning of mate,reciprocal altruism or a message to the predator?

When a predator is not an immediate threat, a prey may produce relatively loud alarm calls because the risk is low. Since such calls could nevertheless attract acoustically oriented predators, the cost of predator attraction must be outweighed by factors beneficial to the caller. In this field study we elicited low-risk alarm calls by temporarily catching wintering adult male great tits Parus major at feeders both within and outside their territories. We tested whether the alarm calls of dominant males can be explained in terms of mate warning, reciprocal altruism or notifying the predator of detection. If alarms are intended to warn mates, males accompanied by their mates should give alarm calls both within and outside home range, even if other permanent flock members are absent. If alarms are to be explained by reciprocal altruism, male great tits should give low-risk alarm calls when accompanied by permanent flock members other than mate within and not outside of the home-range. If alarm calling is a message to a predator, males should call when foraging alone. We found that male great tits gave low-risk alarm calls when accompanied by their mates, independent of feeder location. They also gave low-risk alarm calls within home ranges in the presence of other permanent flock members when mates were absent. In contrast, only a few males gave calls when foraging alone within their home ranges, or when in the company of unfamiliar great tits outside their usual home-range. The results suggest that the utterance of alarm calls may be explained as mate protection and reciprocal altruism among familiar individuals.     

Possible audience effect in Thomas langurs (Primates; Presbytis thomasi): an experimental study on male loud calls in response to a tiger model

Recent research indicates that animal vocalizations can refer to objects in the outside world, and that call production may be controlled by the sender depending on the type of audience involved. Our research on wild male Thomas langurs (Primates: Presbytis thomasi) shows that these males call as a response to a tiger model when they are in a group, but do not call when they are solitary. This is the first experimental study on wild primates to demonstrate that the presence or absence of an audience influences calling behavior. Our results indicate that males in mixed-sex groups give more loud calls than solitary males when exposed to a predator model. This suggests that giving loud calls in response to predators is not purely a reflex and may be controlled in some way by the sender.