Interactive vocal communication at the nest by parent Great Tits Parus major

Although most bird species show monogamous pair bonds and bi‐parental care, little is known of how mated birds coordinate their activities. Whether or not partners communicate with each other to adjust their behaviour remains an open question. During incubation and the first days after hatching, one parent – generally the female – stays in the nest for extended periods, and might depend on acoustic communication to exchange information with its mate outside. The Great Tit Parus major is an interesting study system to investigate intra‐pair communication at the nest because males address songs to their mate while she is in the nest cavity, and females answer the male from the cavity with calls. However, the function of this communication remains unknown. In this study, we recorded the vocalizations and observed the resulting behaviour of Great Tit pairs around the nest at different breeding stages (laying, incubation and chick‐rearing). We observed vocal exchanges (vocalization bouts, alternated on the same tempo, between the female inside the nest and her male outside) in three contexts with different outcomes: (1) the female left the nest, (2) the male entered the box with food, and the female then used specific call types, (3) mates stopped calling but did not leave or enter the nest. The structure of vocal exchanges was globally stable between contexts, but females used calls with an up‐shifted spectrum during exchanges, at the end of which they left the nest or the male entered the nest. Birds vocalized more and at higher tempo during exchanges that ended up in feeding inside the nest. Birds also vocalized more during exchanges taking place during laying – a period of active mate guarding – than during incubation. We conclude that vocal exchanges could signal the females’ need for food and the males’ mate guarding behaviour, and discuss other possible functions of this communication.     

DOCUMENTATION STANDARDS FOR WILDLIFE SOUND RECORDINGS

ABSTRACT

Shearwaters are nocturnal seabirds that rely on olfaction and acoustics to communicate at night. Although previous studies have described the vocal repertoire of some shearwater species, there is a need for more precise experimental data investigating the biological relevance of these acoustic signals in this seabird group. The present paper focuses on the vocal behaviour of the Yelkouan shearwater Puffinus yelkouan, a poorly studied species which produces a single major call composed of two notes, a noisy note and a clear one. A quantitative analysis of the calls allowed to extract the acoustic parameters supporting both sexual and individual signatures. Playback experiments were conducted during the incubation period to test the ability of the Yelkouan shearwater (1) to vocally identify the sex of the emitter, and (2) to discriminate the mate from a non-mate. We showed that birds discriminate the sex of the emitter, calling back almost exclusively to calls of birds of the same sex. Among the few birds replying to calls of the opposite sex, females responded to calls of their partner only, whereas males responded equally to calls of the partner or to calls of a non-partner, suggesting that females are vocally more selective than males.     

Mate recognition by female zebra finch: analysis of individuality in male call and first investigations on female decoding process

Zebra finches are monogamous birds living in large assemblies, which represent a source of confusion for recognition between mates. Because the members of a pair use distance calls to remain in contact, call-based mate recognition is highly probable in this species. Whereas it had been previously demonstrated in males [Vignal, C., Mathevon, N., Mottin, S., 2004. Audience drives male songbird response to mate's voice. Nature 430, 448-451], call-based mate recognition remained to be shown in females. By analysing the acoustic structure of male calls, we investigated the existence of an individual signature and identified the involved acoustic cues. We tested to see if females can identify their mates on the basis of their calls alone, and performed preliminary experiments using modified signals to investigate the acoustic basis of this recognition. Playback tests carried on six individuals showed that a female zebra finch is able to perform the call-based recognition of its mate. Our experiments suggested that the female uses both the energy spectrum and the frequency modulation of the male signal. More experiments are now needed to decipher precisely which acoustic cues are used by females for recognition.     

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 African cichlid fish Astatotilapia burtoni uses acoustic communication for reproduction: sound production, hearing, and behavioral significance

Sexual reproduction in all animals depends on effective communication between signalers and receivers. Many fish species, especially the African cichlids, are well known for their bright coloration and the importance of visual signaling during courtship and mate choice, but little is known about what role acoustic communication plays during mating and how it contributes to sexual selection in this phenotypically diverse group of vertebrates. Here we examined acoustic communication during reproduction in the social cichlid fish, Astatotilapia burtoni. We characterized the sounds and associated behaviors produced by dominant males during courtship, tested for differences in hearing ability associated with female reproductive state and male social status, and then tested the hypothesis that female mate preference is influenced by male sound production. We show that dominant males produce intentional courtship sounds in close proximity to females, and that sounds are spectrally similar to their hearing abilities. Females were 2-5-fold more sensitive to low frequency sounds in the spectral range of male courtship sounds when they were sexually-receptive compared to during the mouthbrooding parental phase. Hearing thresholds were also negatively correlated with circulating sex-steroid levels in females but positively correlated in males, suggesting a potential role for steroids in reproductive-state auditory plasticity. Behavioral experiments showed that receptive females preferred to affiliate with males that were associated with playback of courtship sounds compared to noise controls, indicating that acoustic information is likely important for female mate choice. These data show for the first time in a Tanganyikan cichlid that acoustic communication is important during reproduction as part of a multimodal signaling repertoire, and that perception of auditory information changes depending on the animal's internal physiological state. Our results highlight the importance of examining non-visual sensory modalities as potential substrates for sexual selection contributing to the incredible phenotypic diversity of African cichlid fishes.     

Sex-specific territorial responses in Tawny Owls Strix aluco

A territorial intruder often poses more of a threat to the territory holder of the same sex as itself. As territorial aggression is associated with costs, aggression shown by birds towards territorial intruders of the opposite sex deserves investigation. This behaviour could arise due to the reproductive value of a mate or through mutualism between members of a pair. We investigated these hypotheses by presenting mated pairs of Tawny Owls Strix aluco with playback of male calls, female calls and a male and female duetting, and recording the number and intensity of responses by the male and female territory holders. Females responded significantly more often to female than to male calls. Males responded equally often to male and female playback. Males which had previously bred successfully with their mate were significantly more likely to respond to female playback in the spring, which suggested males were responding to female playback due to the reproductive value of their mate. There was no evidence of mutualism between members of a pair.     

The acoustic expression of stress in a songbird: Does corticosterone drive isolation-induced modifications of zebra finch calls?

Animal vocalizations convey multiple pieces of information about the sender. Some of them are stable, such as identity or sex, but others are labile like the emotional or motivational state. Only a few studies have examined the acoustic expression of emotional state in non-human animals and related vocal cues to physiological parameters. In this paper, we examined the vocal expression of isolation-induced stress in a songbird, the zebra finch (Taeniopygia guttata). Although songbirds use acoustic communication extensively, nothing is known to date on how they might encode physiological states in their vocalizations. We tested the hypothesis that social isolation in zebra finches induces a rise of plasma corticosterone that modifies the vocal behavior. We monitored plasma corticosterone, as well as call rate and acoustic structure of calls of males in response to the playback of female calls of varied saliences (familiar versus stranger) in two situations: social isolation and social housing. Social isolation induced both a rise in plasma corticosterone, and a range of modifications in males' vocal behavior. Isolated birds showed a lower vocal activity, an abolition of the difference of response between the two stimuli, and evoked calls with longer duration and higher pitch. Because some of these effects were mimicked after oral administration of corticosterone in socially housed subjects, we conclude that corticosterone could be partly responsible for the isolation-related modifications of calls in male zebra finches. To our knowledge, this is the first demonstration of the direct implication of glucocorticoids in the modulation of the structure of vocal sounds.     

The Structure of Bonobo Copulation Calls During Reproductive and Non‐Reproductive Sex

Copulation calls in primates are usually identified as sexually selected signals that promote the reproductive success of the caller. In this study, we investigated the acoustic structure of copulation calls in bonobos (Pan paniscus), a great ape known for its heightened socio‐sexuality. Throughout their cycles, females engage in sexual relations with both males and other females and produce copulation calls with both partners. We found that calls produced during sexual interactions with male and female partners could not be reliably distinguished in terms of their acoustic structure, despite major differences in mating behaviour and social context. Call structure was equally unaffected by the size of a female’s sexual swelling and by the rank of her mating partner. Rank of the partner did affect call delivery although only with male, but not female partners. The only strong effect on call structure was because of caller identity, suggesting that these signals primarily function to broadcast individual identity during sexual interactions. This primarily social use of an evolved reproductive signal is consistent with a broader trend seen in this species, namely a transition of sexual behaviour to social functions.     

Hearing is not necessarily believing in nocturnal anurans

The recent discovery of the use of visual cues for mate choice by nocturnal acoustic species raises the important, and to date unaddressed, question of how these signals affect the outcome of mate choice predicted by female preference for male calls. In order to address this question, we presented female Hyla arborea tree frogs with a series of choices between combinations of acoustic and visual cues of varying quality in nocturnal conditions. While females exhibited the expected preference for a combination of attractive values for visual and acoustic signals over combinations of unattractive values for both signals, when presented with conflicting acoustic and visual cues, they equally adopted one of two strategies, preferring either attractive calls or intense vocal sac coloration. This constitutes novel evidence that the outcome of mate choice, as predicted on the basis of male calling quality, can be drastically different when additional communication modalities—in this case vision—are taken into account. These results also highlight the possible existence of individual variation in female rules for cue prioritization. The implications of these results for the study of mate choice in nocturnal acoustic species are discussed.     

Zebra Finch Mates Use Their Forebrain Song System in Unlearned Call Communication

Unlearned calls are produced by all birds whereas learned songs are only found in three avian taxa, most notably in songbirds. The neural basis for song learning and production is formed by interconnected song nuclei: the song control system. In addition to song, zebra finches produce large numbers of soft, unlearned calls, among which “stack” calls are uttered frequently. To determine unequivocally the calls produced by each member of a group, we mounted miniature wireless microphones on each zebra finch. We find that group living paired males and females communicate using bilateral stack calling. To investigate the role of the song control system in call-based male female communication, we recorded the electrical activity in a premotor nucleus of the song control system in freely behaving male birds. The unique combination of acoustic monitoring together with wireless brain recording of individual zebra finches in groups shows that the neuronal activity of the song system correlates with the production of unlearned stack calls. The results suggest that the song system evolved from a brain circuit controlling simple unlearned calls to a system capable of producing acoustically rich, learned vocalizations.     

Vocal Behavior During Territorial Intrusions in the Lusitanian Toadfish: Boatwhistles Also Function as Territorial ‘Keep‐Out’ Signals

Male signals are frequently studied in a single behavioral context, but in some cases they may assist multiple functions, namely for both male–male competition and female mate choice. Boatwhistles are known as the mate attraction calls of toadfishes typically produced during the breeding season. However, recent observations with the Lusitanian toadfish Halobatrachus didactylus (Batrachoididae) indicate that the emission of boatwhistles is not restricted to this period, which suggests a function in other behavioral contexts such as agonistic territorial interactions. We experimentally manipulated the social context of toadfish males to investigate whether boatwhistles are produced during territorial defense, by introducing ‘intruders’ in an experimental tank containing nesting ‘resident’ males. Furthermore, we examined whether parental care (eggs in the nest) affected the behavioral responses of resident males during territorial defense. Resident males defended their shelters producing sounds, mostly boatwhistles, towards intruders. Parental males revealed higher aggression levels, exhibiting additional threatening and attack behaviors. Boatwhistles registered during agonistic events were compared with the mate advertising boatwhistles recorded from small aggregations of nesting males in a natural breeding intertidal area. Agonistic boatwhistles were produced in lower and variable calling rates comparing with the advertising ones that were typically emitted in long series of calls. Agonistic boatwhistles were similar in duration and frequency harmonic structure (with a middle tonal phase) to the advertising calls, but presented less amplitude modulation, and lower dominant and fundamental frequencies. These acoustic differences were probably related to differences in calling rates and broadcast demands associated to the distance to the intended receiver. We provide first evidence that, apart from attracting mates, the toadfish boatwhistles also function as active ‘keep‐out’ signals during territorial defense.     

Assortative Pairing Based on Contact Call Similarity in Budgerigars, Melopsittacus undulatus

A trait typical of parrots, but rare in other groups of birds, is the acquisition of new learned calls (acquired by copying conspecifics) throughout an individual's lifetime. The significance of this distinctive psittacid trait is not understood. In budgerigars, females preferentially affiliate with unfamiliar males whose contact calls resemble their own during brief dyadic choice trials; also, in forced‐pair situations, contact call similarity of members of pairs increases as a result of a male tendency to imitate his mate's call type. The functions of budgerigar call imitation and preference for pre‐pairing similarity are currently unknown. Moreover, as budgerigar pair formation occurs over a span of days or weeks, it is important to determine whether birds in breeding colonies assort and proceed to breed on the basis of pre‐pairing contact call similarity, and whether high levels of call similarity are maintained after pair formation is complete. To explore these questions, we recorded contact calls of male and female budgerigars before and after they were placed into an aviary equipped for breeding. As predicted, birds paired assortatively based on pre‐pairing call similarity. Once birds had paired, their calls converged further in acoustic structure, as previous work had led us to expect. However, after eggs were laid and the males began to feed their mates, the calls of mated birds diverged, suggesting that there might be some cost to maintenance of shared calls. Male care‐giving correlated with the degree to which his pre‐pairing calls resembled those of his mate, but not with the similarity achieved through convergence. These results suggest that female budgerigars may use a male's pre‐pairing call similarity as a predictor of paternal investment. The questions of why such similarity predicts male care‐giving, and why calls converge following initial pairing activities, require further work.     

Factors influencing mate guarding and territory defence in the stitchbird (hihi)

Socially monogamous male birds are predicted to maximise their reproductive success by pursuing extra-pair copulations (EPCs) while engaging in anti-cuckoldry behaviour such as mate guarding. In the stitchbird, Notiomystis cincta, high levels of forced EPCs and a high proportion of nestlings resulting from extra- pair fertilisations lead to the prediction that males of this species should exhibit intense paternity guarding behaviours. While studying an isolated stitchbird population on Tiritiri Matangi Island New Zealand (3636'S, 17453'E), I collected daily behavioural data throughout the breeding season from 15 males in 2000/01 and 27 males in 2001/02. In this study, male stitchbirds demonstrated clear paternity guarding by exhibiting: (1) an increased likelihood of being close to their mate during her fertile period, (2) an increased initiation of mate contact during her fertile period, (3) switching from site-specific territorial defence during the pre-fertile period to defending an area centring on the their female partners location during her fertile period, and (4) an increased following of the female to communal feeding sites outside the territory during her fertile period. For polygynous males, mate guarding and territorial defence were conditional on which of their females was fertile. Additional evidence supporting the hypothesis that mate guarding in this species is a form of paternity assurance, rather than protection from harassment, is that males protected their partner from harassment by other stitchbird males but did not intervene when females were harassed by male bellbirds, Anthornis melanura. While mate-guarding intensity in many species is conditional on the stage of female fertility, male stitchbirds also modified their behaviour depending on the location of the female and the rate of intrusions by extra-pair males. Resident males adopted a best-of-a-bad-job tactic when they were unable to locate their female by defending an area around her last known location. Furthermore, when the rate of intrusions by extra-pair males increased they traded-off the area they could defend within their territory against their ability to guard the female. Territory takeovers were uncommon, but when they did occur older males displaced younger males and healthy birds displaced sick ones. Contrary to the prevailing view that mate guarding is a male response to female infidelity, male stitchbirds appear to use mate guarding primarily to prevent paternity losses from forced EPCs. Future assessments of mate guarding function should consider the possibility that mate guarding involves a combination of conflict and co-operation between the sexes.     

Multiple signals and male spacing affect female preference at cocktail parties in treefrogs

Effective acoustic communication in the face of intense conspecific background noise constitutes a constant sensory challenge in chorusing and colonial species. An evolutionary approach suggests that behavioural and environmental constraints in these species should have shaped signal design and signalling behaviour to enable communication in noisy conditions. This could be attained both through the use of multicomponent signals and through short-term adjustments in the spatial separation of calling males. We investigated these two hypotheses in a chorusing anuran, the hylid Hyla arborea, through a series of phonotaxis experiments conducted within a six-speaker arena in a high background noise situation, by presenting females with male calls containing either single or multiple attractive call components, and by modifying distances between speakers. We found that female ability to discriminate attractive calls increased when several attractive call components were available, providing novel evidence that the use of multicomponent signals enhances communication in complex acoustic conditions. Signal discrimination in females also improved with speaker separation, demonstrating that within natural choruses, spatial unmasking conditioned by male density and spatial separation probably improves female discrimination of competing males. Implications of these results for the accuracy of mate choice within choruses are discussed.     

Vocalisation and its association with androgens and corticosterone in a night frog (Nyctibatrachus humayuni) with unique breeding behaviour

In anurans, vocalisation is used to communicate within and between the sexes during reproduction. Knowledge of vocal repertoire and its diversity is essential in understanding its significance in sexual selection. In this context, we studied the vocal behaviour of Nyctibatrachus humayuni and quantified the urinary metabolites of androgens and corticosterone to understand the associations among hormones, body condition index and vocalisation. Our results show that males of N. humayuni produce an amplitude‐modulated call consisting of a train of pulses. Interestingly, a high degree of inter‐individual variation was observed in the call parameters. The dominant frequency and pulse interval were negatively correlated with male body size, whereas pulse duration and pulse duty cycle were positively correlated with it. Dominant frequency was negatively correlated with androgens and corticosterone, whereas pulse interval was negatively correlated with corticosterone. Further, pulse duty cycle, pulse duration and pulses per call were positively associated with corticosterone. Surprisingly, none of the acoustic parameters was associated with male body temperature and body condition. A significant variation was evident in the vocal effort, dominant frequency and amplitude of advertisement calls produced under different social situations. Calls produced during territory establishment had lower dominant frequency but higher vocal effort, whereas those produced during courtship had higher amplitude and vocal effort than the calls produced in the absence of a competitor/female. Our results suggest that greater inter‐male variability in the advertisement call of N. humayuni could be important in female choice as it may help females to assess the quality of a male. Further, androgens and corticosterone could be important in modulating crucial parameters of the advertisement call.     

The structure and usage of female and male mouse ultrasonic vocalizations reveal only minor differences

Ultrasonic vocalizations (USV) of mice are increasingly recognized as informative dependent variables in studies using mouse models of human diseases. While pup vocalizations primarily serve to re-establish contact with the mother, adult male "songs" were considered to be courtship signals. Alternatively, mouse USVs may generally function as territorial signals. To distinguish between these two hypotheses, we compared the structure and usage of adult male and female USVs in staged resident-intruder encounters. If calls function primarily as courtship signals, males should respond stronger than females, specifically when presented with a female intruder. Refuting this hypothesis, we found that in response to female intruders, females called more than males (228±32 calls/min vs. 71±15 calls/min), and males called more to female than to male intruders (14±7.5 calls/min). There were no significant differences in the acoustic characteristics of the calls given by females and males. To control for the influence of the intruder's behavior on calling, we repeated the experiments using anaesthetized intruders. Again, females produced more calls to female than male intruders (173±17 calls/min vs. 71±15 calls/min), while males called more in response to female than male intruders (39±17 calls/min), and there were no acoustic differences in female and male calls. The vocal activity did not differ significantly with regard to intruder state (awake or anaesthetized), while the acoustic structure exhibited significant differences. Taken together, our findings support the view that calls do not mainly function as courtship signals, although they might serve both a territorial (sex-independent) and a courtship function. The comparison of responses to awake vs. anaesthetized intruders suggests that the latter are sufficient to elicit vocal activity. The subtle acoustic differences, however, indicate that the subject differentiates between intruder states.     

Information content of female copulation calls in yellow baboons.

In a wide variety of animal species, females produce vocalizations just before, during, or immediately after copulation. Observational and experimental evidence indicates that these copulation calls are sexually selected traits, functioning to promote competition between males for access to the calling female. In this paper, we present an acoustic analysis of variation in the form of copulation calls of female yellow baboons, Papio cynocephalus cynocephalus. In particular, we examine whether information about three factors-the calling female's reproductive state, the occurrence or absence of ejaculation, and the dominance rank of the mating male-is encoded in call structure and hence is potentially available to male receivers attending to the signal. Although several features of copulation calls were correlated with each of these factors, when all three were included in multiple regressions only reproductive state and rank of the mating male had independent effects on call form. These findings indicate that female copulation calls in this species signal information about the proximity to ovulation of the calling female and also the relative competitive strength of her mating partner.     

Acoustic and Temporal Variation in Gelada (<Emphasis Type="Italic">Theropithecus gelada</Emphasis>) Loud Calls Advertise Male Quality

Many animals rely on information from vocal signals to assess potential competitors and mates. For example, in primates, males use loud calls to assess rivals when the acoustic properties of the calls reliably indicate the condition or quality of the sender. Here, we investigate whether the loud calls of male geladas (Theropithecus gelada) function as a quality signal. Gelada males produce loud calls during ritualistic chases with rival males. Given the physically taxing nature of these displays, we hypothesize that variation in the acoustic properties of loud calls reliably signal male stamina or competitive ability. To test this hypothesis, we examined whether the acoustic properties of the gelada loud call varied in relation to individual, age, status, and exhaustion. Specifically, we examined 12 call parameters (e.g., fundamental frequency) and 3 bout parameters (e.g., number of calls per bout), that have been previously shown to vary across condition in male primates. We found that several acoustic features varied consistently across age and status such that males deemed higher quality in gelada society (e.g., high status) produced more calls per bout, produced calls that were lower in overall frequency measures, and exhibited a greater vocal range. In addition, we found that similar acoustic features varied with exhaustion; after a long chase event, males produced both fewer calls per bout and calls with higher spectral measures. Results from this study are consistent with the hypothesis that gelada loud calls are quality signals, contributing to the growing evidence that primates may use acoustic information to assess the quality of a rival or a potential mate.     

猫蚤的交配习性及雄蚤对雌蚤提取物的反应

在人工饲喂系统上研究了猫蚤的交配习性及雄蚤对雌蚤化学提取物的反应,结果表明,当5雌1雄在饲养盒内时,该雄虫可与其他雌虫进行多次交配,连续8小时内交配达48次,交配时间平均持续6．6分钟,两次交配的间隔时间平均为2．5分钟,当1雌5雄时,交配时间平均持续11．1分钟,交配间隔时间为12．1分钟,连续7小时内,该雌虫与雄虫交配27次,新羽化的雌雄虫吸血前不能交配,当把用雌虫提取物处理过的黑色滤纸片放进只有雄虫的饲养盒时,雄虫接触纸片的次数及雄－雄交配企图明显增加。     

The hormonal response of female European Stonechats to a territorial intrusion: the role of the male partner

In many bird species, the female participates in defending a pair's breeding territory, however, the endocrine control mechanism of female aggressive behavior is largely unknown. The general statement that androgens are involved in the regulation of aggressive behavior is based on studies conducted only in males. Here, we tested whether paired female stonechats show a hormonal response to a simulated male territorial intruder. Since in males of territorial bird species androgen levels usually increase following a male-male encounter, we measured androgen-levels before and after a simulated male intrusion. In addition, we measured estradiol, the main gonadal hormone in females, and corticosterone, a stress hormone. The results show that a male intruder does not affect any of the measured hormones in females. In a second experiment, we also tested whether the endocrine state of the male partner affects the hormonal response of females to a male intruder by comparing the hormonal response of females paired with pharmacologically castrated males and females paired with control males. Females paired with pharmacologically castrated males had lower corticosterone levels both before and after the intrusion than females paired with control males. Additionally, in both groups, female corticosterone levels were increased following a male intrusion. We suggest that the differences found between females paired with pharmacologically castrated males and females paired with control males are due to differences in intra-pair interactions.