Inter-sexual multimodal communication during mating in wild geladas: the leading role of females

Female primates can emit vocalizations associated with mating that can function as honest signals of fertility. Here, we investigated the role of mating calls and visual signals in female geladas (Theropithecus gelada). Because females have a central role in the gelada society and seem to solicit sexual interactions, we answered whether they emit vocalizations in conjunction with gazing to increase mating success probability. Before and during copulations, females can emit pre-copulation calls and copulation calls. For the first time, we identified a new female vocalization emitted at the final stage of copulations (end-copulation call), possibly marking the occurrence of ejaculation. We found that longer pre-copulation call sequences were followed by both prolonged copulations and the presence of end-copulation calls, thus suggesting that females use pre-copulation calls to ensure successful copula completion. Moreover, we found that different combinations of female vocal types and gazing had different effects on male vocal behavior and motivation to complete the copula. The analysis of the vocal and visual signals revealed a complex inter-sexual multimodal chattering with the leading role of females in the signal exchange. Such chattering, led by females, modulates male sexual arousal, thus increasing the probability of the copula success.     

Ultrasonic Vocalizations in Rat Sexual Behavior

Ultrasonic vocalizations are very conspicuous during rat matingactivity. Two types of calls are produced by both sexes. Thefirst, brief complex calls with the main frequency centeredabout 50 kHz, occur primarily in conjunction with solicitationand mounting activity. The second type of call is the long,22 kHz whistle which is emitted mainly by the male during thepostejaculatory refractory period, but also by both male andfemale at other times during the copulatory sequence. The occurrenceof ultrasonic vocalizations is correlated with sexual motivationof rats. Males emit more 50 kHz calls before successful matingtests than before tests in which they fail to ejaculate. Furthermore,more vocalizations are emitted by the pair prior to intromissionsthan prior to mounts without intromission. Just before ejaculationthere is a large increase in the rate of calling and, at times,transition by the male to calling at 22 kHz. This latter eventmay represent physiological dearousal by the male. Followingejaculation, the male characteristically emits 22 kHz vocalizationsand exhibits a sleep-like EEG pattern. The function of the postejaculatoryvocalization may be to enforce separation between the matingpair, while at the same lime maintaining contact between thepartners. Fifty kHz calls, on the other hand, prime and facilitatesexual responsiveness of the female. Tape recorded vocalizationsof mating rats facilitate solicitation behavior of estrous femalesin the presence of castrated males, and such females also showa preference for these sounds in a "Y" maze. Deafening of femalesdoes not affect their normal pacing of copulatory contacts,but it drastically reduces their solicitation behavior. Thestudies summarized in this paper lead us to conclude that ultrasonicvocalizations play a major role in the integration of reproductiveactivity in the Norway rat, Rattus norvegicus.     

Assessing the Patterns of Evolution in Anuran Vocal Sexual Signals

Many animal species have evolved signalling traits to mediate various intra-specific interactions. Signals are particularly important for inter-sexual selection, where females use male signalling traits to select mates. Female preferences are therefore a major selective force in the evolution of these male signals, and these preferences can facilitate rapid changes in these traits in an evolutionary timeframe. This introduction of high levels of variation in inter-sexual signals may overshadow any phylogenetic patterns present. Such shadowing effects, however, should be dependant on the characteristics of traits (e.g. morphological, physiological and behavioural). Using male advertisement calls from 72 species of anuran amphibians, we tested the levels of phylogenetic signal present for a variety of call features in relation to trait types, and for calls as whole units using phylogenetic principal components analysis. We found that most call features displayed some level of phylogenetic autocorrelation (or signal), with traits that are dependent on morphology having much stronger phylogenetic signals than those based on behaviour. In addition, when calls were analysed as whole units, closely related species were found to be similar to each other, indicating that phylogenetic patterns had not been cancelled out by selection via female preferences. We suggest that signal functions, such as indicating male quality (e.g. mediated by body size) to potential mates, may place constraints on the amount of variation that can be introduced by female preferences. More research, particularly studies on other taxa, will be required to elucidate whether the patterns found in anurans are general across the animal kingdom.     

Indirect partner choice through manipulation of male behaviour by female fowl, Gallus gallus domesticus

The direct and indirect consequences of female copulatory behaviour for copulation success have seldom been quantified. In feral fowl, most copulations were forced by males and copulation success was determined by two factors. First, female differential resistance and solicitation directly affected copulation success and were displayed non-randomly with respect to male social status. Second, another female copulatory behaviour, the distress call, had an indirect effect on both copulation success and the quality of copulation partners. Distress calls triggered male attention to a copulation, which increased the probability of higher-ranking males than the copulating male disrupting the copulation and inseminating the calling female. Females preferentially uttered distress calls when mounted by low-ranking males. Both copulation resistance and distress calling influenced copulation success, but only distress calling increased the probability of copulation disruption by other males. Consistent with the effect of direct selection, differential distress calling indirectly biased copulation success in favour of dominant males. Female fowl may thus ameliorate the effect of male sexual coercion by manipulating male behaviour.     

Territorial vocalization in sympatric damselfish: acoustic characteristics and intruder discrimination

Damselfishes are well known for their aggressive, territorial behaviour during which the use of vocalization behaviour has been well documented. However, agonistic acoustic signalling has been understudied in particular when the vocalizations are interspecific. In this study, we characterize and compare the previously undescribed vocalization behaviour of longfin damselfish (Stegastes diencaeus), in an agonistic context, with the closely related and sympatric dusky damselfish (Stegastes adustus). Next, we examined if these congeneric species modulate their vocalizations in a similar pattern to previously described aggressive behaviour patterns. Audio field recordings of territorial males were obtained in response to three separate stimuli: (1) conspecific male damselfish, (2) heterospecific male damselfish and (3) a common intruder, the slippery dick wrasse (Halichoeres bivittatus). The vocal repertoires of both longfin and dusky damselfish comprised the same three distinct call types: chirps, pops and pulse trains. However, temporal measures of the calls showed significant differences between species. Additionally, dusky damselfish were more vocal overall, producing more calls and spending more time calling than longfin damselfish. These responses were stimulus and species dependent, as the two species modulated acoustic response by modulating pulse number based on intruder species. These results suggest that these closely related species of damselfish use vocalization behaviours that are both unique and context dependent.     

Subharmonics increase the auditory impact of female koala rejection calls

Although non‐linear phenomena are common in human and non‐human animal vocalisations, their functional relevance remains poorly understood. One theory posits that non‐linear phenomena generate unpredictability in vocalisations, which increases the auditory impact of vocal signals, and makes animals less likely to habituate to call repetition. Female koalas (Phascolarctos cinereus) produce vocal signals when they reject male copulation attempts that contain relatively high levels of non‐linear phenomena, and thus may function as attention grabbing vocal signals during the breeding season. To test this hypothesis, we used playback experiments: firstly, to determine whether female rejection calls induce heightened behavioural responses in free‐ranging male koalas during the breeding season, and secondly, to examine how the relative amount of non‐linear phenomena in rejection calls influences male behavioural response. The results show that male koalas look for longer towards speakers broadcasting playback sequences of male bellows followed by a series of female rejection calls than those broadcasting only male bellows. In addition, female rejection call sequences with more subharmonics, higher harmonics‐to‐noise ratios, and less biphonation produced the greatest male looking responses. Our findings support the hypothesis that female koala rejection calls function to grab male attention during the breeding season, and indicate that subharmonics are the main acoustic feature that increases the auditory impact of these vocal signals.     

The function of Barbary macaque copulation calls.

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

Vocal and Optical Indicators of Individual Quality in a Social Seabird,the Crested Auklet (Aethia cristatella)

Indicators of individual quality in ornamentation or in vocalizations have been reported for different animal species. However, no studies have jointly investigated ornamentation and vocalizations in one species. The crested auklet (Aethia cristatella, Alcidae) is a small colonial seabird of the North Pacific and is unusual for a bird in using optical, vocal, and olfactory signals. We estimated the potential for coding individual quality in vocalizations and plumage ornamentation and the relationship between vocal and optical traits in crested auklets. During the summer seasons of 2008–2009, we recorded 359 trumpet calls from 28 individually marked males and measured indices of body size, condition, and plumage patterns of 58 male and 48 female crested auklets from a breeding colony on Talan Island, Sea of Okhotsk. We found strong interindividual differences in trumpet call characteristics. Furthermore, we found that the maximum fundamental frequency of the loudest notes of the trumpet call is negatively correlated with body condition, and head crest length is positively correlated with body size. However, we found no relationship between vocal and ornamental traits. The results suggest that advertising calls of crested auklets signal caller individuality and quality, but future experimental studies should test whether or not this is indeed case.     

Call-based species recognition in black-capped chickadees

Species recognition is essential for efficient communication between conspecifics. For this to occur, species information must be unambiguously encoded in the repertoire of each species’ vocalizations. Until now, the study of species recognition in songbirds has been focused mainly on male songs and male territorial behaviour. Species recognition of other learned vocalizations, such as calls, have not been explored, and could prove useful as calls are used in a wider range of contexts. Here, we present an experimental field study investigating the coding of species information in a learned vocalization, the ‘chick-a-dee’ call of the black-capped chickadee (Poecile atricapillus). By modifying natural calls in both temporal and spectral domains and by observing the vocal responses of black-capped chickadees following the playback of these modified calls, we demonstrate that species recognition in chickadees relies on several acoustic features including syntax, frequency modulation, amplitude modulation, and to a lesser extent, call rhythmicity and frequency range.     

Social Factors Influence the Acoustic Variability in the Long-distance Calls of Male Chimpanzees

Acoustic variability in the species-typical long-distance calls of male chimpanzees was investigated. Analysis of 13 acoustic features revealed that calls varied more within than between individuals. Although only a limited amount of acoustic variability was attributable to different populations, discriminant-function analysis confirmed that males from two populations produce acoustically distinguishable calls. Additional investigation suggested that social factors may contribute to the patterns of acoustic variation both between and within individuals. Matrix-permutation tests revealed a positive association between the amount of time males spent together and a measure of call similarity. Vocal similarities between individuals appeared to result from a dynamic process involving chorusing behaviour: males matched the acoustic characteristics of each other's vocalizations when calling together. Chorusing may also affect the degree of within-individual acoustic variation in calls. Males who chorused often with others produced more variable calls than individuals who chorused less often or called alone.     

Female bonobos use copulation calls as social signals

During mating events, females of many primate species produce loud and distinct vocalizations known as 'copulation calls'. The adaptive significance of these signals is considered to be in promoting the caller's direct reproductive success. Here, we investigated copulation calling in bonobos (Pan paniscus), a species in which females produce these vocalizations during sexual interactions with partners of both sexes. Females were more likely to call when mating with males than with females. We also observed a positive relationship between the likelihood of calling and partner rank, regardless of partner sex. Sexual activity generally increased with swelling size (an indicator of reproductive state) and, during their peak swelling, females called more with male than with female partners. Female bonobos are unusual among the non-human primates in terms of their heightened socio-sexuality. Our results suggest that in this species, copulation calls have undergone an evolutionary transition from a purely reproductive to a more general social function, reflecting the intrinsic evolutionary links between vocal behaviour and social cognition.     

Vocal individual discrimination in Japanese monkeys

The present study determines which features of the coo call are used by Japanese monkeys Macaca fuscata for vocal individual discrimination. First, two female Japanese monkeys were trained to discriminate conspecific individuals vocally, using an operant conditioning. Using as stimuli three unknown individuals with 30 calls per individual, the two monkeys succeeded in discriminating new call exemplars from the three stimulus individuals. A discriminant analysis performed on calls used as stimuli indicated that start frequency of the fundamental and call duration were variables that can differentiate individuals efficiently. Then, playbacks of acoustically modified signals were used to indicate which vocal features are used by monkeys for the individual discrimination. Stimuli signals containing modified pitch or duration, or filtered so as to keep only the fundamental component, were tested. Results indicated that Japanese monkeys use multiple acoustical cues to perform vocal individual discrimination, including at least pitch, call duration, and harmonics. However, harmonics seem to be less important for discrimination than pitch and call duration.     

Loud calls ofGalago crassicaudatus andG. garnettii and their relation to habitat structure

Long distance vocalizations have been shown to be good indicators of genetic species in primates. Here the loud calls of two recently identified greater galago taxa —Galago crassicaudatus andG. garnettii — are compared and analyzed statistically. Observed differences in call structures are investigated further as potential indicators of differences in the structures of habitats frequented by the two species. Although the calls share a repetitive structure, and show similar dominant frequency bands (1,000 – 1,500 Hz), they differ significantly in the number of units per call, unit duration, inter-unit interval, highest frequency, lowest frequency, dominant frequency band, first harmonic, and call duration. The duration of theG. crassicaudatus call is more than twice that ofG. garnettii. Strong intraspecific consistency is seen in the most energetic frequency bands (dominant frequency band and first harmonic), and durations of the individual units and inter-unit intervals. Information important to species recognition is thus most likely to be contained in these features. Individual recognition may be encoded in the relative emphasis of higher level harmonics. The frequency structures of the calls will reflect requirements for acoustical transmission in a forest environment, as well as structural constraints imposed by body size. Higher frequencies detected in theG. garnettii call (up to 8,500 Hz) may have a functional significance related to distance estimation, or may simply be a reflection of smaller body size. The greater modulation of theG. garnettii call suggests that its habitat constitutes a denser or more turbulent medium for sound transmission than does the habitat ofG. crassicaudatus.     

Copulatory behaviour of the bank voleMyodes glareolus: matings with one and two males do not make a difference

In promiscuous species in which females mate with more than one male during oestrus, males may increase their sperm expenditure or change their copulatory behaviour in response to the risk of sperm competition. I used an experimental approach to investigate the pattern of copulatory behaviour of the bank voleMyodes glareolus Schreber, 1780 depending on whether the female mated with one or two males. The work showed that the copulatory period of the bank vole lasted about 80 minutes and consisted of 4–5 ejaculatory series, with multiple intromissions preceding ejaculation. There were no significant changes in number of intromissions across the first four ejaculatory series, but I did find a relationship between number of intromissions and first ejaculation latency; also, ejaculation latencies grew shorter as the ejaculatory series proceeded. Litter size did not differ significantly between females that mated with one male and those mating with two, nor did the reproductive success of males that mated with the same female. Mating with an oestrus female appears to be advantageous for bank vole males even if they mate as the second one, and the risk of sperm competition did not trigger changes in male copulatory behaviour. The similar durations of the copulatory period and patterns of change of ejaculation latencies during copulations with one and two males point to the role of the female in temporal copulatory behaviour of the bank vole.     

The post-copulation withdrawal response in female baboons: A functional analysis

Rapid withdrawal of females from males at the end of the copulatory sequence (prior to male dismounting) characterizes several primate species. The purpose of this paper is to make a preliminary investigation into possible functional aspects of these “copulatory darts.” Two hypotheses are proposed; (1) females use darts to aid competing males to locate the source of copulation calls; and (2) females dart in order to promote re-mating with the same male. Both hypotheses postulate that darts may thus enhance male-male competition, although acquisition of other benefits may be the primary drive to darting according to the re-mating hypothesis. Using data from 157 copulations collected from six females spread across four groups in a wild population of chacma baboonsPapio cynocephalus ursinus, darting behaviour is described. Within females, darting distance is highly variable. Darting distance is greatest at the time of ovulation (and maximal sexual swelling), and there is some evidence that darting may also be more frequent, and cover greater distances, when the mating male is adult rather than juvenile. While darting behaviour appears unrelated to the presence or absence of ejaculation, it tends to correlate positively with the duration of the female copulation call. These preliminary results are consistent with a mediating role in male-male competition and therefore provide support for both hypotheses.     

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.     

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.     

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

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