Increased syllable rate during aggressive singing in a bird with complex and fast song

Sexual signals can comprise traits with multiple functions, and species with extreme phenotypes offer an opportunity to link function with signal evolution. This is the case in the serin Serinus serinus, a songbird with extremely fast syllable rate compared to related finches, and high sound frequency for its body size. Previous work on receiver responses showed that playback of artificially increased syllable rate is avoided and inhibits vocal responses, suggesting it is perceived as aggressive, while, on the contrary, higher sound frequency appears preferred by females. We tested whether senders also change these traits during aggressive singing, with a field playback experiment. Serin males responding aggressively by approaching the playback loudspeaker also increased syllable rate, while males responding less aggressively did not change syllable rate. Together with work on receiver responses, this suggests that aggressive signalling may have been an important selective pressure for the evolution of extremely fast syllable rate in this species. It is noteworthy that aggressive male serins still increase syllable rate, despite of their already elevated natural syllable rate. We found no changes in sound frequency when singing aggressively, which agrees with previous work that instead showed a female preference for high song frequency. We conclude that the evolution of extreme traits in serin song is best explained by multiple functions.     

Female presence and estrous state influence mouse ultrasonic courtship vocalizations

The laboratory mouse is an emerging model for context-dependent vocal signaling and reception. Mouse ultrasonic vocalizations are robustly produced in social contexts. In adults, male vocalization during courtship has become a model of interest for signal-receiver interactions. These vocalizations can be grouped into syllable types that are consistently produced by different subspecies and strains of mice. Vocalizations are unique to individuals, vary across development, and depend on social housing conditions. The behavioral significance of different syllable types, including the contexts in which different vocalizations are made and the responses listeners have to different types of vocalizations, is not well understood. We examined the effect of female presence and estrous state on male vocalizations by exploring the use of syllable types and the parameters of syllables during courtship. We also explored correlations between vocalizations and other behaviors. These experimental manipulations produced four main findings: 1) vocalizations varied among males, 2) the production of USVs and an increase in the use of a specific syllable type were temporally related to mounting behavior, 3) the frequency (kHz), bandwidth, and duration of syllables produced by males were influenced by the estrous phase of female partners, and 4) syllable types changed when females were removed. These findings show that mouse ultrasonic courtship vocalizations are sensitive to changes in female phase and presence, further demonstrating the context-sensitivity of these calls.     

Acoustic communication in a duetting grasshopper: receiver response variability, male strategies and signal design

In the duetting grasshopper Chorthippus biguttulus, a female's decision to reply to a conspecific male is based on the evaluation of a number of features of the male's song, which consists of uninterrupted syllables separated by pauses. Female responses are tuned to a restricted range of pause durations. However, males produce songs with noisy rather than silent pauses, which should make the measurement of pause durations more difficult for the female. We examined the adaptive value of these noisy pauses by testing female responses to (1) pairs of natural phrases, which differed only with respect to clear or noisy syllable pauses, and (2) synthetic phrases, in which the syllable onset accentuations and noise levels in the pauses were systematically varied. There was considerable variation between females, both in their preference for clear or noisy pauses in natural phrases, and in the optimal combinations of syllable onset accentuations and noise levels in pauses that they preferred in synthetic phrases. The response profiles of individual females were consistent. The experiments with synthetic phrases showed that, on average, females preferred more extreme values of syllable onset accentuations than were present in male songs. Noisy pauses increased the range of syllable pause durations accepted by females. The results suggest that noisy pauses could buffer signallers against the negative consequences of both signal degradation during transmission and extreme receiver choosiness.     

Development of social vocalizations in mice

Adult mice are highly vocal animals, with both males and females vocalizing in same sex and cross sex social encounters. Mouse pups are also highly vocal, producing isolation vocalizations when they are cold or removed from the nest. This study examined patterns in the development of pup isolation vocalizations, and compared these to adult vocalizations. In three litters of CBA/CaJ mice, we recorded isolation vocalizations at ages postnatal day 5 (p5), p7, p9, p11, and p13. Adult vocalizations were obtained in a variety of social situations. Altogether, 28,384 discrete vocal signals were recorded using high-frequency-sensitive equipment and analyzed for syllable type, spectral and temporal features, and the temporal sequencing within bouts. We found that pups produced all but one of the 11 syllable types recorded from adults. The proportions of syllable types changed developmentally, but even the youngest pups produced complex syllables with frequency-time variations. When all syllable types were pooled together for analysis, changes in the peak frequency or the duration of syllables were small, although significant, from p5 through p13. However, individual syllable types showed different, large patterns of change over development, requiring analysis of each syllable type separately. Most adult syllables were substantially lower in frequency and shorter in duration. As pups aged, the complexity of vocal bouts increased, with a greater tendency to switch between syllable types. Vocal bouts from older animals, p13 and adult, had significantly more sequential structure than those from younger mice. Overall, these results demonstrate substantial changes in social vocalizations with age. Future studies are required to identify whether these changes result from developmental processes affecting the vocal tract or control of vocalization, or from vocal learning. To provide a tool for further research, we developed a MATLAB program that generates bouts of vocalizations that correspond to mice of different ages.     

Temperature coupling in cricket acoustic communication

Acoustic communication in Gryllus firmus is temperature-coupled: temperature induces parallel changes in male calling song temporal pattern, and in female preference for song. Temperature effects on song production and recognition networks were localized by selectively warming head or thorax or both head and thorax of intact crickets, then eliciting aggression song production (males) or phonotaxis to synthetic calling song (females). Because male song is produced by a thoracic central pattern generator (CPG), and because head ganglia are necessary for female song recognition, measurements of female phonotaxis under such conditions may be used to test the following competing hypotheses about organization of the song recognition network: 1. A set of neurons homologous to the male song CPG exist in the female, and are used as a template that determines preferred values of song temporal parameters for song pattern recognition (the common neural elements hypothesis), and 2. temporal pattern preference is determined entirely within the head ganglia. Neither selective warming of the head nor of the thorax was effective in changing female song preference, but simultaneous warming of head and thorax shifted preference toward a faster song in most preparations, as did warming the whole animal by raising ambient temperature. These results suggest that phonotactic preference for song temporal pattern is plurisegmentally determined in field crickets. Selective warming experiments during aggression song production in males revealed that syllable period is influenced but not completely determined by thoracic temperature; head temperature is irrelevant. The song CPG appears to receive some rate-setting information from outside the thoracic central nervous system.     

Responses of Male and Female Black Grouse to Male Vocal Display

The evolution of leks may be explained by several hypotheses. The ‘female preference’ hypothesis, which states that females favour males that have aggregated, has recently gained some empirical support. Low-quality, unattractive males may, however, settle near attractive males, as predicted by the ‘hotshot’ hypothesis. We tested whether black grouse Tetrao tetrix females use auditory cues to find the preferred leks, and whether males respond to vocal display emitted on leks. We conducted a playback experiment with male vocal display (rookooing) on leks, where the visiting females and displaying males were counted. The number of males tended to increase more on playback leks. Specifically, the number of 1-year-old males was greater on playback sites than on control sites. Also, the number of females, in relation to the lek size before the start of the experiment tended to increase. In addition, we used aviary playback trials to test whether females distinguish between single-male and multi-male displays. In a choice test, females showed greater preference for the ‘multi-male’ tape. The tendency for increased male numbers on playback leks resulted from increased visits of young, mobile males which were attracted to leks that they perceived to be large. This suggests a ‘hotshot’-type mechanism in the settlement of young males. Because females also responded to the supplemented auditory advertisement, or directly to the increased number of males, the ‘female preference’ hypothesis is also supported. Females may, at least in part, base their decision of which lek to visit on auditory cues, but visual contact to males may be also needed.     

Vocal Plasticity – are Pied Flycatchers,Ficedula Hypoleuca,Open‐Ended Learners?

In some songbird species, large song repertoires are advantageous in female attraction, whereas song sharing with neighbours may give an advantage in male–male competition. Open‐ended learners, with the ability to memorize new song elements throughout their lives, may learn from territorial neighbours and thus benefit from increasing both repertoire size and song sharing. A distinction needs to be made between true adult song learning, i.e. memorization of novel song elements, and vocal plasticity resulting in changes in the use of previously memorized elements, such as the use of hidden repertoires or increased production of previously rare syllable types. We assessed the ability of adult pied flycatcher Ficedula hypoleuca males to learn previously unheard song elements and to change their song production in response to playback of unfamiliar, conspecific song, emulating a singing neighbour. After a 1‐week playback treatment, three out of 20 subjects had learned foreign song elements, providing evidence from the wild that pied flycatchers are true open‐ended learners. However, the syllable sharing with the playback stimulus repertoires had not changed, and the males’ repertoires had decreased rather than increased. Hence, we did not find support for increased syllable sharing with neighbours or increased repertoire size as functions of adult song learning in pied flycatchers. Because pied flycatcher song seems to serve mainly for mate attraction, copying of attractive syllable types is a possible alternative function of adult song learning in this species.     

体征对灰眉岩鹀鸣唱特征的影响

声信号是鸟类交流的重要方式。鸟类的鸣声特征受到生境的塑造和性选择,也受到发声器官的影响,如种间的比较研究发现,体重大的鸟类鸣声频率低,喙短的鸟类鸣声频宽大。在种内是否也存在类似的规律,目前的结论还不一致。2012年6月,在北京小龙门地区(40°00'N,115°26'E)测量了17只灰眉岩鹀(Emberiza godlewskii)的形态参数以及鸣声的频率特征,未发现体重或喙长与鸣声的最高频率、最低频率、峰频或频宽存在显著的相关性。本研究的结果支持在小型雀形目鸟类中,体型对繁殖期鸣唱频率特征的影响不显著。     

MATE CHOICE IN THE SAILFIN MOLLY,POECILIA LATIPINNA

We examined both female and male mate choice in the sailfín molly, Poecilia latipinna. Female mollies preferred larger males over smaller ones when comparing males from their own populations. Although the expression of this preference depends on a female's receptive state, the level of female preference does not appear to be associated with any other attribute of the female or of the males. When presented with males of the same size from different populations, females preferred native over foreign males in some but not all population combinations. These results cannot be explained by a bias for higher size-specific rates of courtship displays that is shared by all females. Males preferred larger over smaller females; larger males exhibited stronger preferences, and preference for the larger female also increased as the disparity in size between the two object females increased. We found no evidence that males preferred native over foreign females when encountered singly or in size-matched combinations. These results indicate that discrimination among populations arises because females exercise divergent directional preferences for size-specific trait values that are associated with differences among males in these values. This result implies an active role for sexual selection in contributing to the maintenance of the behavioral or morphological distinctions among males observed within and among populations.     

EQUIPMENT REVIEWS

ABSTRACT

Research on African elephant (Loxodonta africana) vocal communication has increased in recent years, yet there has been very little data collected on the vocal production of infant African elephants. Vocalizations were recorded from a group of five adult female African elephants and 3 dependent offspring (1 male and 2 female) at Disney's Animal Kingdom, Florida, U.S.A., using custom-designed audio-recording collars worn by the adult females. We measured both source and filter features of infant ‘rumble’ vocalizations made during affiliative social interactions and after cessation of nursing from adult females. Rumble vocalizations produced in the ‘nurse cessation’ context exhibited an upward shift in formant frequency locations, compared to rumbles produced during the ‘affiliation’ context. Additionally, call duration increased and fundamental frequencies decreased after nurse cessations for the male, but both females showed the opposite acoustic response. When infant rumbles accompanied nurse cessations, nursing was more likely to resume within 30 seconds compared to nurse cessations without vocalizations. These results suggest that infant rumbles associated with cessation of nursing reflect the motivational state of infants and may influence maternal responsiveness.     

Female Preferences for Male Song Characters in the Bush-Cricket Isophya camptoxypha (Orthoptera, Tettigonioidea)

Female preferences for two male song characters (duration of syllables [DS], syllable repetition period [SRP]) have been studied in Isophya camptoxypha, an Eastern European duetting bush-cricket. Songs with modified DS or SRP were presented to virgin females and their response songs were recorded and counted. Female preference functions were unimodal for both characters. But while in the case of SRP the obtained female preference function reached its maximum at the mean value of that character, in the case of DS females preferred modified songs with a DS slightly higher than the natural range of that character. A comparison between the obtained preference functions and the DS and SRP values measured in sympatric Isophya species (with similar song structure) suggests that the two examined characters and female preferences for them may be effective components of the species-specific mate recognition system of I. camptoxypha. Moreover DS values may also convey information about the quality of the singing male.     

Song complexity and song structure in the Moustached Warbler Acrocephalus melanopogon

We examined different song parameters leading to a complex song configuration, and song output (production), and their relation in male Moustached Warblers and discuss them with reference to female choice. With more than 120 different syllables per two minutes of song, male Moustached Warblers can be regarded as one of the most complex singers within the genus Acrocephalus . We found significant differences between males for almost all song parameters investigated (repertoire size, switching and repetition rate, song speed and strophe length) but not for time spent singing per 20 minutes. This individual variation probably is an important cue for female mate choice. Male Moustached Warblers achieve song complexity mainly via frequent syllable switching. Song complexity seems to be consistent throughout the song and our results suggest that females could assess the overall song complexity of a singer by examining even very short song bouts. Furthermore, a high proportion of motifs – clusters of syllables with the same sequence – occurs within the song of each male which would also facilitate assessment of song complexity by females. However, repertoire size and strophe length were positively related, thus it remains to be investigated which song feature, if any, females actually use.     

Female swamp sparrows do not show evidence of discriminating between the songs of peak‐aged and senescent males

Sexual selection theory predicts that females face contrasting selection pressures when choosing the age of their mate. On the one hand, older males have demonstrated their ability to survive and they may be more experienced than younger males. At the same time, however, younger males are expected to have accumulated fewer deleterious mutations in their germline as compared to older males. These contrasting pressures on female preference may result in a preference for intermediate‐aged males. A preference for males of a particular age can only be expressed, however, if females are able to identify males of different ages. We have previously shown that male swamp sparrows display age‐related changes in vocal quality, such that males display sharp increases in vocal quality in early adulthood, followed by gradual senescent declines thereafter. We have also shown that territorial males discriminate these within‐individual differences, giving stronger aggressive responses to songs of peak‐aged males than to those of senescent males. Here, we use a copulation solicitation assay to test whether females also discriminate these within‐signaler markers of senescence in song. Contrary to our prediction, females did not show any evidence of discriminating between songs recorded from peak‐aged males as compared to songs from the same males following song senescence. We suggest that this difference in demonstrated discrimination between males and females may be the result of the two sexes attending to different song characteristics.     

Negative impact of urban noise on sexual receptivity and clutch size in female domestic canaries

In oscines, male song stimulates female reproduction and females are known to adjust both their sexual preferences and their maternal investment according to song quality. Female domestic canaries are especially responsive to wide frequency bandwidth (4 kHz) male songs emitted with a high‐repetition syllable rate and low minimal frequencies (1 kHz). We previously showed that low‐frequency urban noise decreases female sexual responsiveness for these low‐frequency songs (1–5 kHz) through auditory masking. Based on the differential allocation hypothesis, we predicted that urban noise exposure will equally affect female maternal investment. Using a crossover design, we broadcast low‐frequency songs to females either in an overlapping noise condition or in an alternating noise condition. Females decreased both their sexual responsiveness and their clutch size in the overlapping noise treatment relative to the alternative noise treatment. No differences were found concerning egg size or egg composition (yolk and albumen mass, testosterone concentration). Due to our experimental design, we can exclude a general impact of noisy conditions and thereby provide evidence for a detrimental effect through masking on avian courtship and reproductive output. These results suggest that noisy conditions may also affect avian communication in outdoor conditions, which may partly explain field reports on noise‐dependent breeding success and reduced breeding densities at noisy sites.     

Rufous‐capped Warblers Basileuterus rufifrons show seasonal,temporal and annual variation in song use

In the majority of songbird species, males have repertoires of multiple song types used for mate attraction and territory defence. The wood‐warblers (family Parulidae) are a diverse family of songbirds in which males of many migratory species use different song types or patterns of song delivery (known as ‘singing modes’) depending on context. The vocal behaviour of most tropical resident warblers remains undescribed, although these species differ ecologically and behaviourally from migratory species, and may therefore differ in their vocal behaviour. We test whether male Rufous‐capped Warblers Basileuterus rufifrons use distinct singing modes by examining song structure and context‐dependent variation in their songs. We recorded multiple song bouts from 50 male Warblers in a Costa Rican population over 3 years to describe seasonal, diel and annual variation in song structure and vocal behaviour. We found that Rufous‐capped Warbler songs are complex, with many syllable types shared both within and between males’ repertoires. Males varied their song output depending on context: they sang long songs at a high rate at dawn and during the breeding season, and shortened songs in the presence of a vocalizing female mate. Unlike many migratory species, Rufous‐capped Warblers do not appear to have different singing modes; they did not change the song variants used or the pattern of song delivery according to time of day, season or female vocal activity. Our research provides the first detailed vocal analysis of any Basileuterus warbler species, and enhances our understanding of the evolution of repertoire specialization in tropical resident songbirds.     

Song pattern recognition in the grasshopper Chorthippus biguttulus: the mechanism of syllable onset and offset detection

The male song of the duetting grasshopper Chorthippus biguttulus consists of syllables alternating with noisy pauses. The syllable-pause structure is important for song recognition by the female. Using playback experiments we investigated the mechanism by which intensity modulations within the song pattern are used to detect syllable onsets and offsets. We varied the relative onset level (level of the syllable beginning relative to the noisy pause) and the relative offset level (level of the noisy pause relative to the syllable end) independently in different experiments. For all females, an increase in intensity defining the syllable onset was necessary to evoke responses. Syllable offset cues were not always necessary: some females responded to continuous noise stimuli wherein only syllable onsets were marked by short pulses of high intensity. Those females that did not require syllable offset cues did not, however, lack a functional pause detection mechanism, since their responses to model songs containing silent pauses were restricted to a given range of pause durations. We propose that syllable-pause detection involves two independent processes: (1) syllable onset detection by a phasic neuronal unit that can be re-activated only after a short pause, and (2) the rejection of unacceptably long pauses by a second unit.     

Dangerous love? Predation risk does not affect female mate choice in blue‐black grassquits

Predation risk may be an important factor affecting female mate choice. Hypothetically, females could choose extravagantly ornamented males that survive in high predation risk environments. However, this decision could be different if choosing a conspicuous male under high predation risk is costly for females or results in reduced offspring survival. In such contexts, females could become indifferent to male quality or prefer inconspicuous males. We tested this idea using captive blue‐black grassquits (Volatinia jacarina, Linnaeus, 1766), a species in which males perform conspicuous leap displays coupled with songs during the breeding season, which presumably subjects females and offspring to higher predation risk. Females were placed in an arena with speakers on opposite sides emitting male courtship songs. One speaker emitted songs at a high rate (proxy for a conspicuous male) while the other speaker broadcast songs at a low rate (proxy for a less conspicuous male). While the female evaluated the two male songs, a third speaker emitted vocalizations characterizing three levels of risk: adult predator, nest predator, and no‐risk control. Females showed no preference for either male stimuli across the predation risk treatments. This lack of preference relative to frequency of male vocal displays suggests that leap‐song frequency is not used by females during mate choice. We suggest that in addition to its role in courtship, male grassquit displays also signal status to other males when competing for territories. Thus, we propose that predation risk does not directly influence blue‐black grassquit intersexual selection and that females in this species may exercise indirect mate choice, choosing social mates based on male ability to establish and defend a territory, and relying secondarily upon other aspects of male display attributes, such as its visual components.     

Experience Plays a Role in Female Preference for Symmetry in the Swordtail Fish Xiphophorus malinche

Variation in female mating preferences was previously detected in wild-caught Xiphophorus cortezi and Xiphophorus malinche females: smaller (presumed younger) females preferred symmetrical males, while larger (presumed older) females preferred asymmetrical males. We examined the influence of experience on this variation in female preference by determining if X. malinche females would express a preference for symmetry as virgins, shift their preferences for bar symmetry as they got larger (older) and if experience with males of different bar number symmetry could explain the variation in female preference previously detected. Virgin females exhibited no preference for vertical bar number symmetry when tested in the young- or old-age classes. However, young virgins spent more time with the opposite treatment in the second when compared with first test, indicating an ability to detect the difference between symmetry and asymmetry, and potentially a preference to mate with multiple males. When females were reared in one of three treatments, housed with symmetrical, barless or both symmetrical and asymmetrical males, we detected both a treatment and tank effect on strength of preference for symmetry, suggesting that barring pattern and some other aspect of the social environment influenced the development of this mating preference. Finally, we detected no effect of age class on mean strength of preference for symmetry; however, there was a statistically different relationship between female size and strength of preference for symmetry across the two age classes, suggesting that the preference function for symmetry may not be linear in relation to female size.     

Dissecting the repeatability of female choice in the grasshopper Chorthippus biguttulus

Repeatable differences in preference between females are a prerequisite for the evolution of female choice. Existing studies have concentrated on the repeatability of female preference for the male trait eliciting the highest female response but have rarely dealt with female choosiness and response rate, which are also important traits for the evolution of female choice and can mimic repeatable variation in preference. We used a method devised to disentangle the effects of preference, choosiness and response rate to examine the repeatability of female choice for acoustic signals in the grasshopperChorthippus biguttulus . We stimulated females with artificial courtship signals that varied in one signal trait and recorded the number of acoustic responses of the females in two sessions separated by several days. Using a normal distribution function within a nonlinear regression between signalling trait and female response rate, we independently calculated values for female preference, choosiness and maximum response rate for the two sessions. All three aspects of female choice showed significant repeatability indicating large differences between females. This method will also be suitable for measuring the heritability of female preference, a crucial question regarding the evolution of female choice. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Vocal performance influences female response to male bird song: an experimental test

Female songbirds are thought to assess males based on aspectsof song, such as repertoire size or amount of singing, thatcould potentially provide information about male quality. Arelatively unexplored aspect of song that also might serve asan assessment signal is a male's ability to perform physicallychallenging songs. Trilled songs, such as those produced byswamp sparrows (Melospiza georgiana), present males with a performancechallenge because trills require rapid and precise coordinationof vocal tract movements, resulting in a trade-off between trillrate and frequency bandwidth. This trade-off defines a constrainton song production observed as a triangular distribution inacoustic space of trill rate by frequency bandwidth, with anupper boundary that represents a performance limit. Given thisbackground on song production constraints, we are able to identifya priori which songs are performed with a higher degree of proficiencyand, thus, which songs should be more attractive to females.We determined the performance limit for a population of swampsparrows and measured how well individual males performed songsrelative to this limit ("vocal performance"). We then comparedfemale solicitation responses to high-performance versus low-performanceversions of the same song type produced by different males.Females displayed significantly more to high-performance songsthan to low-performance songs, supporting the hypothesis thatfemales use vocal performance to assess males.