Singing in the Face of Danger: the Anomalous Type II Vocalization of the Splendid Fairy-Wren

Males of certain species of fairy-wrens (Aves: Maluridae) emit a unique vocalization, the Type II vocalization, in response to the calls of potential predators. We conducted field observations and playback experiments to identify the contexts in which the Type II vocalization is emitted by splendid fairy-wren ( Malurus splendens ) males, and to examine social and genetic factors that influence its occurrence. In field observations and controlled playback experiments, Type II vocalizations were elicited most consistently by calls of the predatory gray butcherbird ( Cracticus torquatus ). Some vocalizations from other avian species also elicited Type II vocalizations, and the majority of these were vocalizations from avian predators. Splendid fairy-wrens are cooperative breeders, and males that responded with Type II vocalizations to playbacks of butcherbird calls tended to be primary rather than secondary males, had larger cloacal protuberances, and were older than those that did not respond. In addition, secondary males that were sons of resident females were more likely than non-sons to respond with a Type II vocalization. In another playback experiment, females responded similarly to the Type I song and Type II vocalizations of their mates. Although the Type II vocalization is emitted primarily in response to predator calls, it is inconsistent with an alarm call explanation. Patterns of reproductive success among Type II calling males suggest that it does not function as an honest signal of male quality. At present, the function of the vocalization remains anomalous, but indirect fitness benefits may play a role in its explanation.     

Female preference for temporal features of vocalization in the Japanese treefrog,Rhacophorus arboreus

Female preference for the different temporal features of advertisement calls by males was studied in the foam-nesting treefrog,Rhacophorus arboreus. Field observations showed that females were attracted to males making more calls, calling in more bouts of vocalization and leading choruses. In phonotactic experiments in the laboratory, however, females were attracted to vocalizations with more total notes while they were not attracted to chorus leaders. alphabetical order     

The orangutan long call and snag crashing at Tanjung Puting Reserve

The long call, which is only given by adult males, is the most frequently uttered orangutan vocalization and the only one which can be heard over long distances. At the Orangutan Research and Conservation Project study area in the Tanjung Puting Reserve, Central Indonesian Borneo, adult males were calling more regularly and frequently than reported from other areas in Borneo. Adult males also exhibited a behavior, not reported elsewhere, sometimes associated with the vocalization of long calls: the pushing over of large snags (branchless dead trees) to the ground. At Tanjung Puting long calls functioned primarily to mediate dominance relationships among adult males who rarely came into direct contact with one another. In addition, long calls may have been helping sexually receptive females locate males.     

The use of low-frequency vocalizations in African elephant(Loxodonta africana) reproductive strategies

Fertility-advertisement calls in females are predicted to occur in nonmonogamous species where males and females are widely separated in space. In African elephants, low-frequency vocalizations have thus been suggested as a reproductive strategy used by fertile females to attract mates. This study examined the use of low-frequency vocalizations with respect to different phases of the estrous cycle in African elephants by simultaneously monitoring vocalizations, behavior, and hormonal profiles. Subjects were one male and six female African elephants housed at Disney's Animal Kingdom. No acoustically distinct vocalizations were restricted to the ovulatory follicular phase. However, overall rate of low-frequency vocalization as well as the rate of one acoustically distinct vocalization changed over the estrous cycle, with highest rates of calling related to the first period of follicular growth, or anovulatory follicular phase. Elevated rates of vocalization thus were not restricted to behavioral estrus and occurred much earlier in the estrous cycle than in most species that produce fertility-advertisement calls. Both herd composition and elephant identity also affected rates of vocalization. Vocalizations therefore may not be reliable signals of actual fertility. However, the increase in vocalizations in advance of estrus may attract males to the herd prior to ovulation, facilitating both male-male competition and female choice. Once present in the herd, males may then switch strategies to use more reliable chemical and visual cues to detect ovulating females.     

Male Calling Behavior and Female Choice in the Neotropical Treefrog Hyla microcephala

The effect of stimulus call complexity and calling rate on the vocal responses of males and female mate choice was studied in Hyla microcephala in Panama. Males increased the number of notes in their calls in response to increases in stimulus call complexity during both playback of 1 to 8-note advertisement calls and during natural interactions. However, precise matching of the number of notes in stimuli and responses did not occur consistently. Males also increased calling rates if stimuli were presented above prestimulus rates. Two-stimulus choice experiments demonstrated that females prefer both higher calling rates and greater call complexity, indicating that the ways males change their vocal behavior during interactions increases their attractiveness to potential mates. Tests in which the relative intensity of a high and low rate stimulus was varied indicated that females prefer stimuli with higher total sound energy. In a natural chorus, it is likely that females simply approach males giving the most conspicuous calls.     

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.     

黄山短尾猴交配叫声及其影响因素

哺乳动物在交配过程中经常会发出独特且有节奏的交配叫声(Copulation call),这通常被认为是雌雄双方交配策略的一种体现.交配叫声的发生及其影响因素在不同物种间差异较大,对其深入研究有助于比较和揭示不同动物交配策略的差异及其适应性功能.为了阐明交配叫声的生物学和社会学因素,我们在安徽黄山记录了野生黄山短尾猴(M...     

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.     

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.     

For whom the male calls: an effect of audience on contact call rate and repertoire in budgerigars, Melopsittacus undulatus

Budgerigars are well known for their ability to imitate sounds, but little is known about the functional contexts in which they use these imitations. Recently, we have shown that male budgerigars consistently imitate the contact calls of the females with whom they are paired. Here we investigate whether males produce these imitations more frequently when they are with their mates than when they are with other females. In one experiment, we established seven budgerigar pairs and then tested each male with his mate and with an unfamiliar female. In the second experiment, we allowed pairs to form freely in an aviary and then tested the males with their mate and with a familiar mated female. In both experiments, the males produced significantly more imitations of their mate's call (defined as calls that were more than 75% similar to the mate's predominant contact call) when they were with their mate than when they were recorded with another female. Under aviary conditions, this difference was due to both a general increase in the males' rate of calling and to an increase in the percentage of the males' calls that were imitations. These data show that male budgerigars modify their contact call rates and repertoires in an audience-specific manner. This audience effect is unusual because it involves a learned vocalization and is extremely specific to a particular audience, namely the mate. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

INBREEDING AND ADVERTISEMENT CALLING IN THE CRICKET TELEOGRYLLUS COMMODUS: LABORATORY AND FIELD EXPERIMENTS

If sexually selected traits reveal a male's heterozygosity or condition to females, then such traits should exhibit declines with inbreeding. We tested this by examining the effect of inbreeding on advertisement calling in male crickets Teleogryllus commodus. We investigated the effect of one generation of full‐sibling mating on calling effort and fine‐scale call structure. Inbreeding reduced calling effort but had no effect on call structure. We then compared the attractiveness of inbred and outbred calls in the field by monitoring how many wild females were attracted to each call type. From the field data, we conducted a selection analysis to identify the major axes of linear and nonlinear multivariate sexual selection on call structure. A comparison of multivariate attractiveness of inbred and outbred calls along each major axis of selection revealed no difference in attractiveness. Our results suggest that inbred male calls have a fine‐scale structure that is no less attractive to females than that of outbred calls. However, because inbred males call less often, and female T. commodus prefer males with a higher calling effort, inbred males will suffer reductions in mating success. Females who base mate choice on call rate are therefore using a signal correlated with male heterozygosity and/or condition.     

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.     

Rhesus macaque copulation calls: Re-evaluating the “honest signal” hypothesis

Male rhesus macaques sometimes give loud calls while thrusting or dismounting during multi-mount copulations.Hauser (1993) has proposed that these calls (1) impose a cost (increased risk of aggression) on calling males, and (2) increase callers' copulation frequencies, supporting the hypothesis that calls function as honest signals (handicaps) that females use to evaluate male quality during mate choice. This hypothesis was re-examined using data collected at Cayo Santiago, Puerto Rico on 40 focal females and their 56 observed copulatory partners. Although attacks by males against copulating pairs were frequent, they were usually directed only against the female of the pair. Males that called were no more likely than silent males to suffer male escalated attack during or immediately following mount series. Male-female dyads in which the male called during copulation were significantly more likely than non-calling dyads to complete the most copulations observed for any given female. Males that called at least once were significantly more likely than non-calling males to complete at least one copulation with a peri-ovulatory female. A log-linear model revealed that male rank and calling were both associated with likelihood of experiencing at least one peri-ovulatory copulation. However, calling was not associated with reception of demonstrated female mate choice behaviors. Controlling for dominance rank, callers did not experience more female proximity maintenance than non-callers. Nor were callers' hip-grasps refused less frequently than non-callers' hip-grasps. These results cast doubt on the hypothesis that rhesus macaque copulation calls are costly, honest indicators of intrinsic male quality. A contrasting alternative hypothesis, that a male's copulatory calls advertise relative immunity from attacks against his copulatory partners, was not supported either. Thus, the function of rhesus macaque copulatory calls remains unknown. The unusually high rate of copulations amongHauser's (1993) subjects may explain the discrepancy in results, but it is unclear how high copulation rates would increase the cost of copulatory calling to males.     

Sexual differences in hormonal control of release calls in bullfrogs

Release calls in anuran amphibians are given when animals are inappropriately clasped by others. Since other call types, such as mate calls, are sexually dimorphic in frogs and toads, sonogram analysis was used to determine whether release call characteristics might also be sexually dimorphic in bullfrogs (Rana catesbeiana). Only intercall intervals differed significantly between males and females. Call duration, dominant frequency characteristics, and the display of secondary or tertiary harmonic frequencies were similar in both sexes. In the spring, but not the fall, calling rates were significantly lower in female bullfrogs, compared to males. Females also had significantly lower plasma androgen concentrations and higher plasma estrogen in the spring, compared to males. In both sexes, plasma androgen and estrogen were significantly higher in the spring, compared to the fall. The neuropeptide arginine vasotocin significantly decreased release call rates in females in the spring while it significantly increased rates in males. Vasotocin had no significant effect in the fall. Prostaglandin E2 significantly inhibited release calling in both males and females. On the other hand, prolactin significantly inhibited calling in female bullfrogs, but had no affect in males. Thus, although acoustic characteristics of release calls were similar in male and female bullfrogs, hormonal control of call rates was sexually dimorphic and seasonally variable.     

Male territoriality,fighting and assessment of fighting ability in the Australian frog Uperoleia rugosa

Males of Uperoleia rugosa form aggregations around the breeding pond. Within the aggregations, each calling male maintains an exclusive zone in which it does not tolerate another calling male. However, attacks on silent intruders, satellite males or females were never observed. Territorial males warned calling intruders by changing from advertisement calls to encounter calls (a display); if the intruder persisted in calling the resident would either attack or retreat and call elsewhere. Fights were usually won by the heavier males, and males of similar weight were more likely to fight, whereas males retreated from opponents that were substantially heavier. Calling was energetically costly and territorial males lost weight and thus their fighting abilities declined, whereas silent satellite males gained weight and were able to oust lighter territorial males. There was thus a dynamic interchange between territorial and satellite males depending on their relative weights. The playback of recorded advertisement calls showed that males can assess each others' fighting abilities on the basis of their vocalizations. Males retreated from a loudspeaker broadcasting the calls of a larger male but they attacked the loudspeaker if the calls of smaller or similar sized males were played (N=39, P<0·001, one-tailed binomial test). Dominant frequency was probably the call parameter used in assessment as it was correlated with the weight (r=−0·71, P<0·001, N=100) and hence the fighting ability of the caller, but this hypothesis needs further testing.     

Territoriality and Male Mating Success in the Dart-poison Frog,Epipedobates femoralis (Dendrobatidae,Anura)

The social and reproductive behaviour of the dart-poison frog, Epipedobates femoralis, was studied in Amazonian Peru for 14 months. Males defended territories with advertisement calls and, ultimately, fighting. Territory size ranged from 0.25 to 26 m² and was positively correlated with duration of residence and calling activity of the owner. Females were not territorial and were never attacked when approaching calling males. Males and females only mated once and females sampled calling males before mating. Male mating success was closely correlated with territory size and calling activity. No correlation was found between male body size and mating success. Territories provide residents with sufficient space for mate attraction and reproduction without interference from rivals. Since territory size is dependent on calling activity which involves high energetic costs, it is suggested that territory size reveals male quality.     

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.       

An environmentally relevant endocrine-disrupting antiandrogen, vinclozolin, affects calling behavior of male Xenopus laevis

Vinclozolin (VIN) is an antiandrogenic model substance as well as a common fungicide that can affect the endocrine system of vertebrates. The objective of this study was to investigate how VIN affects mate calling behavior of South African clawed frogs (Xenopus laevis) and whether it is effective at environmentally relevant concentrations. Male X. laevis were injected with human chorionic gonadotropin (hCG) to stimulate their androgen-controlled mate calling behavior and were treated with VIN at concentrations of 10⁻⁶, 10⁻⁸ and 10⁻¹⁰ M. VIN at 10⁻⁶ M reduced calling activity. Furthermore, the vocalization composition of VIN-treated X. laevis was altered. The call types advertisement calls and chirping are uttered by reproductively active males, whereas the call types growling, ticking, and rasping indicate a sexually unaroused state of a male. VIN at any of the tested concentrations led to a decrease in utterance of calls, which indicate a sexually aroused state of the males, and an increase in relative proportions of calls, indicating a sexually unaroused state of the males. Additionally, the mean duration of clicks and the number of accentuated clicks during the advertisement calls decreased at all concentrations of VIN. No significant differences were observed in any other temporal or spectral calling parameters between the treatments. This study illustrates that exposure to the antiandrogen VIN might result in a reduced reproductive success by altering mate calling behavior of X. laevis. Moreover, it suggests that the behavioral parameters examined in this study can be used as sensitive biomarkers for detecting antiandrogenic endocrine disrupting compounds in amphibians.     

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.     

The role of nocturnal vision in mate choice: females prefer conspicuous males in the European tree frog (Hyla arborea)

Nocturnal frog species rely extensively on vocalization for reproduction. But recent studies provide evidence for an important, though long overlooked, role of visual communication. In many species, calling males exhibit a conspicuous pulsing vocal sac, a signal bearing visually important dynamic components. Here, we investigate female preference for male vocal sac coloration—a question hitherto unexplored—and male colour pattern in the European tree frog (Hyla arborea). Under nocturnal conditions, we conducted two-choice experiments involving video playbacks of calling males with identical calls and showing various naturally encountered colour signals, differing in their chromatic and brightness components. We adjusted video colours to match the frogs'' visual perception, a crucial aspect not considered in previous experiments. Females prefer males with a colourful sac and a pronounced flank stripe. Both signals probably enhance male conspicuousness and facilitate detection and localization by females. This study provides the first experimental evidence of a preference for specific vocal sac spectral properties in a nocturnal anuran species. Vocal sac coloration is based on carotenoids and may convey information about male quality worthwhile for females to assess. The informative content of the flank stripe remains to be demonstrated.