Copulation Solicitation Displays Research Articles

Mating success follows duet dancing in the Java sparrow.

Mutual interactions between sexes have multiple signalling functions. Duet singing in songbirds is related to mutual mate guarding, joint resource defence, and signalling commitment. Coordinated visual displays of mating pairs are thought to perform similar functions, but are less well understood. The current study evaluated mutual interactions in an Estrildid species to explore the relative importance of duet dancing and male singing in mating success of pairs in a first encounter. When Java sparrows (Lonchura oryzivora) court prospective mates, only males sing. However, both males and females perform courtship dances, often in a duet-like manner. These dances are typically terminated by female copulation solicitation displays (CSDs). In the current study, we observed higher mating success when courtship dances were mutually exchanged, and when males sang. However, the sex initiating the courtship did not affect mating success. Most females produced CSDs after duet dancing but before hearing the entire song, indicating that duet dancing played a crucial role in mating. This finding highlights an unexplored aspect of duetting behaviour in the process of mutual mate choice. These results conflict with the majority of past songbird research, which has interpreted songs as primary behavioural sexual signals.

Urban noise undermines female sexual preferences for low-frequency songs in domestic canaries

Increasing levels of anthropogenic noise represent a challenge for animals living in urban areas and birds, especially, may suffer from noisy conditions as they use singing to attract mates. Most anthropogenic noise is low in frequency and singing at high frequencies under noisy urban conditions may avoid masking and thus be a good strategy for breeding success in cities. Despite comparative, correlational and some experimental studies supporting this hypothesis, empirical studies on the impact of noise on sexual behaviour are largely lacking. Domestic canaries, Serinus canaria, provide an excellent model system to test unequivocal sexual responsiveness as receptive females perform copulation solicitation displays (CSD) to male song. We have previously shown that CSD rate was higher for low- than for high-frequency songs. In the current study, we tested whether a typical urban noise spectrum, with a bias towards low frequencies, could undermine sexual preferences. Using overlapping and alternating noise exposure regimes while broadcasting male songs we found that masking by urban noise reduced female responsiveness to low-frequency attractive songs. Under the same conditions the responsiveness to high-frequency songs remained unaffected and, consequently, the sexual preference for low- over high-frequency songs had faded because of the urban noise. We discuss to what extent our results can be extrapolated to other wild bird species and speculate about the adaptive value of the typical upward shift in frequency found in many city birds.

Condition‐Dependent Choosiness For Highly Attractive Songs In Female Canaries

AbstractPartner choice in animals has evolved under the effects of intra‐ and inter‐sexual selection. Even if a consensus between females is often observed towards some males, certain females can drastically change their mating decision. Different conditions such as early learning, mate‐choice copying, prior experience or subtle intrinsic factors can interfere with the decision. One of them is body condition of the females at the time of choosing. In this experiment, the flight feathers of female canaries Serinus canaria were cut, thus decreasing their flight ability. After a short period in a flight room, two types of artificial songs containing different tempi of the test ‘A’ phrase (16 vs. 8 syllables per second) were played to these females. It is known that only A phrases with a high tempo provoke a high level of sexual response in females. Female preference was evaluated by counting the number of Copulation Solicitation Displays (CSDs). The results show that, in both (normal and physically reduced) conditions, females prefer songs containing an A16 phrase. However, the strength of this preference is lower in females with compromised body condition than in females from the control group, suggesting a decreased choosiness in the poor body condition females.

When Less Is Best: Female Brown-Headed Cowbirds Prefer Less Intense Male Displays

Sexual selection theory predicts that females should prefer males with the most intense courtship displays. However, wing-spread song displays that male brown-headed cowbirds (Molothrus ater) direct at females are generally less intense than versions of this display that are directed at other males. Because male-directed displays are used in aggressive signaling, we hypothesized that females should prefer lower intensity performances of this display. To test this hypothesis, we played audiovisual recordings showing the same males performing both high intensity male-directed and low intensity female-directed displays to females (N = 8) and recorded the females' copulation solicitation display (CSD) responses. All eight females responded strongly to both categories of playbacks but were more sexually stimulated by the low intensity female-directed displays. Because each pair of high and low intensity playback videos had the exact same audio track, the divergent responses of females must have been based on differences in the visual content of the displays shown in the videos. Preferences female cowbirds show in acoustic CSD studies are correlated with mate choice in field and captivity studies and this is also likely to be true for preferences elucidated by playback of audiovisual displays. Female preferences for low intensity female-directed displays may explain why male cowbirds rarely use high intensity displays when signaling to females. Repetitive high intensity displays may demonstrate a male's current condition and explain why these displays are used in male-male interactions which can escalate into physical fights in which males in poorer condition could be injured or killed. This is the first study in songbirds to use audiovisual playbacks to assess how female sexual behavior varies in response to variation in a male visual display.

Amplitude modulation of sexy phrases is salient for song attractiveness in female canaries (Serinus canaria)

Song discrimination and recognition in songbird species have usually been studied by measuring responses to song playbacks. In female canaries, Serinus canaria, copulation solicitation displays (CSDs) are used as an index of female preferences, which are related to song recognition. Despite the fact that many studies underline the role of song syntax in this species, we observed that short segments of songs (a few seconds long) are enough for females to discriminate between conspecific and heterospecific songs, whereas such a short duration is not sufficient to identify the syntax rules. This suggests that other cues are salient for song recognition. In this experiment, we investigated the influence of amplitude modulation (AM) on the responses (CSDs) of female canaries to song playbacks. We used two groups of females: (1) raised in acoustic isolation and (2) raised in normal conditions. When adult, we tested their preferences for sexy phrases with different AMs. We broadcast three types of stimuli: (1) songs with natural canary AM, (2) songs with AM removed, or (3) song with wren Troglodytes troglodytes AM. Results indicate that female canaries prefer and have predispositions for a song type with the natural canary AM. Thus, this acoustic parameter is a salient cue for song attractiveness.

Operant conditioning and copulation solicitation display assays reveal a stable preference for local song by female swamp sparrows Melospiza georgiana

Operant conditioning assays are increasingly being used to test mating signal preferences in female birds. Operant behavior may be seen as farther removed from mate choice behavior as compared to other methods for measuring mating signal preferences, which could limit the evolutionary interpretation of operant results. I compared the song preferences of female swamp sparrows (Melospiza georgiana) as measured both by a copulation solicitation display assay and by an operant preference test. Both methods revealed a strong preference for songs from the females' Conneaut Marsh breeding population over songs from a Millbrook population over 500 km distant, which remained stable after extensive exposure to Millbrook songs. Further, there was a striking congruence in results on an individual level from the two assays. These findings support the conclusion that operant methods reveal evolutionarily significant mate choice preferences, providing the opportunity to study such preferences under circumstances when the copulation solicitation assay is less practical.

Complementary/alternative medicine: engulfed by postmodernism, anti-science and regressive thinking

<h3>Abstract</h3> It is the female response to male signals that determines courtship success. In most songbirds, females control reproduction via the copulation solicitation display (CSD), an innate, stereotyped posture produced in direct response to male displays. Because CSD can be elicited in the absence of males by the presentation of recorded song, CSD production enables investigations into the effects of underlying signal features and behavioral state on female mating preferences. Using computer vision to quantify CSD trajectory in female brown-headed cowbirds (<i>Molothrus ater</i>), we show that both song quality and a female’s internal state predict CSD production, as well as the onset latency and duration of the display. We also show that CSD can be produced in a graded fashion based on both signal strength and internal state. These results emphasize the importance of underlying receiver state in determining behavioral responses and suggest that female responsiveness acts in conjunction with male signal strength to determine the efficacy of male courtship.

Immediate early gene (ZENK, Arc) expression in the auditory forebrain of female canaries varies in response to male song quality

In male songbirds, the song control pathway in the forebrain is responsible for song production and learning, and in females it is associated with the perception and discrimination of male song. However, experiments using the expression of immediate early genes (IEGs) reveal the activation of brain regions outside the song control system, in particular the caudomedial nidopallium (NCM) and the caudomedial mesopallium (CMM). In this study on female canaries, we investigate the role of these two regions in relation to playback of male songs of different quality. Male canaries produce elaborate songs and some contain syllables with a more complex structure (sexy syllables) that induce females to perform copulation solicitation displays (CSD) as an invitation to mate. Females were first exposed to playback of a range of songs of different quality, before they were finally tested with playback of songs containing either sexy or nonsexy syllables. We then sectioned the brains and used in situ hybridization to reveal brain regions that express the IEGs ZENK or Arc. In CMM, expression of ZENK mRNA was significantly higher in females that last heard sexy syllables compared to those that last heard nonsexy syllables, but this was not the case for NCM. Expression of Arc mRNA revealed no differences in either CMM or NCM in both experimental groups. These results provide evidence that in female canaries CMM is involved in female perception and discrimination of male song quality through a mechanism of memory reconsolidation. The results also have further implications for the evolution of complex songs by sexual selection and female choice.

Sexual preferences for songs in female domestic canaries ( Serinus canaria ): can late song exposure, without social reinforcement, influence the effects of early tutoring?

We studied the relative effects of early and late song exposure without social reinforcement on female sexual preferences in the domestic canary (Serinus canaria). Young female canaries were tape-tutored during their first 4 months of life with songs of either domestic or wild male canaries (DT and WT conditions). When they reached sexual maturity, these females were placed in breeding conditions and some of them were re-exposed to songs. During this “late exposure” the females, according to their experimental group, were either presented with new domestic or wild songs (DL and WL conditions) over 40 days, or were kept without song stimulation (− condition). Afterwards, we assessed the sexual preferences of all the females for domestic or wild songs using the copulation solicitation display assay. The results showed that both DT/– and DT/DL females showed a clear preference for domestic songs. However, whereas WT/WL females preferred wild songs; WT/– females did not show any preference. Finally, DT/WL and WT/DL females failed to show any preference. It appeared that a second song experience at the beginning of their first breeding season, without any social reinforcement, allowed the emergence or stabilisation of early preferences, or interfered with these early preferences depending on whether the song category used during the late exposure phase matched or not the song category used during the early tutoring phase, and also depending on which category was used during the first tutoring phase. This behavioural plasticity could help young adult females to adjust the ‘standard’ they built during infancy to new environmental conditions.

Preferences and Predispositions For Intra-syllabic Diversity in Female Canaries (Serinus Canaria)

The aim of this study is to examine the preferences of female canaries for a particular cue in male song: the intra-syllabic diversity (number and form of notes constituting a syllable) and to test both the role of predispositions and of song experience in the development of these preferences. Two groups of females were used. The first consisted of adult females raised in acoustic isolation without song males experiences (ISO group); the second, of song experienced adult females raised with singing male in an aviary (AVI group). Female preferences for intra-syllabic diversity were evaluated using the behavioral index of copulation solicitation displays (CSD). Five different types of songs were tested: three were made up of poor intra-syllabic diversity and two were made up of great intra-syllabic diversity. The results demonstrate that, in each group (AVI and ISO), intra-syllabic diversity is preferred to intrasyllabic simplicity. In addition, the inter-group comparison showed no significant differences between the two groups. In the aviary group, song learning by sexual and sound experience did not seem to modify or influence the intra-syllabic diversity preferences. Thus, female preferences for such a diversity would result from early predispositions that are maintained in adulthood.

Group Copulation Solicitation Display among Female Greater Rheas

Abstract In this paper we report the copulation behavior of the Greater Rhea (Rhea americana), a species in which males defend a harem of females. We describe the females' behavior during 14 copulation events observed from 1995–1997 at Buenos Aires province, Argentina. During copulations, females performed a more active role than previously suggested. Moreover, on three occasions we observed that harem females performed a complex copulation solicitation display, forming a closed circle to attract the male. We hypothesize that this display could be a reliable signal to the male of the tendency of females to be inseminated and lay eggs communally.

Effects of unilateral lesions of HVC on song patterns of male domesticated canaries.

Bird song is a model for studying neural control and lateralization of a learned behavior. Adult male canary develops large and varied song repertoires. Particular features of the male are well known to stimulate the reproductive activities of the female. We report here on the effect of lesions of either the left or right HVC, a key nucleus of the descending vocal control network of songbirds, on different song parameters of common domesticated male canaries of an European outbred strain. These canaries are useful to evaluate the question of central versus peripheral lateralization because they do not show syringeal dominance for syllable production compared to the previously studied canary strains. Right-sided lesions reduced the highest frequency and the widest frequency band. Left-sided lesion increased the lowest frequency. The size of the left-sided lesions correlated with the reduction of the repertoire of simple syllables, of the total repertoire and of the highest repetition rate, and with the increase of the lowest frequency. These results suggest a lateralized specialization of both left and right vocal pathways for particular features of the song, especially those that are known to elicit a great number of copulation solicitation displays (CSD). Lesions of both left and right pathways affected, however, sound amplitude of all syllables. Because this effect was more sever following left-sided lesions, and because the syrinx morphology of canaries has a left-right asymmetry, we suggest a peripheral mechanism for the observed lateralized specializations.

Female preference for the songs of older males and the maintenance of dialects in brown-headed cowbirds (Molothrus ater)

Female preferences for local song types have been implicated in the maintenance of local song dialects in songbirds. Such preferences can be assessed by copulation solicitation displays (CSDs) of females in response to playback of male songs. We used CSDs to determine if female brown-headed cowbirds (Molothrus ater) in the Sierra Nevada of California discriminate between yearling and adult male vocalizations based on two vocal characteristics that often distinguish songs of these age classes, incomplete renditions of the local dialect flight whistle and 'unique', unshared perched song types. We predicted stronger responses to adult songs because yearlings are rarely involved in copulations observed in these dialects although they are sexually mature. Eleven estradiol-treated females trapped in the Convict flight whistle dialect were more sexually stimulated by complete Convict flight whistles recorded from either adults or yearlings than by incomplete flight whistles typical of yearlings. Females also found the shared perched song types of local adults more stimulating than the 'unique' types of yearlings. These sexual preferences for complete and appropriate local songs are consistent with the hypothesis that females use vocal differences between the age classes as cues in their choice of adults as mates. Furthermore these preferences would create selection pressure on young males to conform to the local song culture. Mainly because of a learning constraint in their hatching year, yearlings do not complete their development of local repertoires until the start of their second season when they are two years old. The vocal deficits of yearling males serve as uncheatable indicators of age, and age in turn is a likely correlate of male genetic quality, which may explain female preference for songs that reliably identify older males. This system shows that signal honesty can be maintained by developmental constraints rather than by high signal cost alone.

Directional female preference for an exaggerated male trait in canary (Serinus canaria) song.

Motor constraints on vocal production impose a trade-off between trill rate and frequency bandwidth within birdsong. We tested whether domesticated canary (Serinus canaria) females, reared either in acoustic isolation or in aviary conditions, had a preference for broad bandwidth songs with artificially increased syllable rates. The copulation solicitation display (CSD) was used as an index of female preference. As predicted, both naive and experienced females were especially responsive to syllables with a broad bandwidth emitted at an artificially increased rate. Female preference for supernormal stimuli provide support for the honest-signalling hypothesis and our results are consistent with recent findings indicating that production of song phrases maximizing both bandwidth and syllable rate may be a reliable indicator of male physical or behavioural qualities. We suggest that female preference for vocal emissions, which simultaneously maximize these two parameters, could be a widespread pattern within songbirds.

Female canaries that respond and discriminate more between male songs of different quality have a larger song control nucleus (HVC) in the brain.

In male songbirds the song control pathway in the forebrain is responsible for song production and learning. In most species, females do not sing and have smaller nuclei in the song control pathway. Although the function of the pathway in females is assumed to be associated with the perception of male song, there is little direct evidence to support this view. In this study on female canaries, we investigate the role of two key nuclei in the song control pathway (HVC and lMAN) in relation to playback of male song. Male canaries produce elaborate songs that function to attract and stimulate females. The songs are constructed from smaller units called syllables, and special syllables with a more complex structure (sexy syllables) are known to induce females to perform copulation solicitation displays (CSD) as an invitation to mate. By using computer-edited experimental songs, we first show that females discriminate between songs by producing significantly more CSD to those containing sexy syllables. We then sectioned the brains and used in situ hybridization to reveal song nuclei containing androgen receptors. We report positive correlations between the size of HVC and both total CSD response and the amount of discrimination between sexy and nonsexy songs. We found no such relationships between these measures and the size of lMAN. These results provide some evidence to support the view that, in female canaries HVC is involved in female perception and discrimination of male song. The results also have implications for the evolution of complex male songs by sexual selection and female choice.

Progesterone Inhibits Female Courtship Behavior in Domestic Canaries (Serinus canaria)

We studied copulation solicitation display (CSD) responses to playback in photostimulated female canaries given systemic injections of progesterone. Eight females received injections of 0.1 mg of progesterone dissolved in olive oil during their first breeding cycle and were untreated during their second breeding cycle; eight females received only the oil vehicle during their first breeding cycle and received no treatment during their second breeding cycle. The injections were performed every second day during 15 days, after the onset of nest building. Progesterone treatment resulted in a significant increase of plasma progesterone which in turn provoked an inhibition of females' CSDs and decreased the size of the clutch. During the first breeding cycle, progesterone-treated females had lower CSDs and egg-laying scores than did control females. During the second breeding cycle, when females received no treatment, no differences emerged between the two groups. The suppressive effect of progesterone on female sexual responses was observed as soon as 48 h after the beginning of the treatment. We propose that progesterone plays a key role in mediating the transition from active female courtship behavior to sexual refractoriness in this species. Suppressive effects of progesterone on female sexual behavior have been previously described in lizards as well as in rodents. Our data are consistent with the hypothesis of Godwin et al. (J. Godwin, V. Hartman, M. Grammer, and D. Crews, Horm. Behav. 30, 138–144, 1996) which proposed that the decrease in sexual behavior following plasma progesterone increase represents an evolutionarily conserved mechanism in the regulation of female sexual behavior.

Early tutoring and adult reproductive behaviour in female domestic canary ( Serinus canaria )

We studied the effect of early tutoring on the subsequent sexual preferences and reproductive activity of female domestic canaries (Serinus canaria). Young female canaries were exposed during the first 4 months of life to songs of either domestic or wild canaries. When adult, these females were again exposed to domestic or wild songs. In the first experiment, the sexual responses of the females to unfamiliar domestic and wild songs were quantified with the copulation solicitation display (CSD) assay. In the second experiment, the same females were tested again with modified tutoring songs. In the third experiment, song stimulation of nest-building and egg-laying was studied. Domestic-strain-tutored females gave more CSDs to domestic than to wild songs. In contrast, wild-strain-tutored females showed no sexual preference. We propose that the sexual preference of adult domestic-strain-tutored female canaries for domestic songs is the consequence of learning and categorisation processes. The discrepancy between the results of the domestic-strain-tutored females and those of the wild-strain-tutored females suggests that female canaries have a predisposition to learn songs of their own strain rather than songs of an alien strain. In the third experiment nest-building and egg-laying activities appeared to be unaffected by early tutoring conditions: there was no significant differential effect of the different tutoring and exposure conditions on nest-building and egg-laying scores. Mate attraction and stimulation of females’ reproductive activity appear to be two separate functions of male song, which may have been shaped by different evolutionary constraints.

AUDITORY EXPERIENCE DOES NOT SHAPE SEXUAL PREFERENCES FOR SONGS IN FEMALE NORTHERN CARDINALS

AbstractBird song is typically used by males to attract females. As a consequence of the vocal learning process, the acoustic morphology of male songs shows marked geographic variation. Whether females use variation in male songs to choose mates has been controversial (reviewed by Catchpole &amp; Slater, 1995). In some species, the song types that females produce when treated hormonally have been considered to be the song types they prefer in the context of mate choice. To examine this notion, I investigated the song type preferences of female northern cardinals (Cardinalis cardinalis) using a more direct measure, copulation solicitation display. Unlike females of many other species of songbirds in the Temperate zone, female cardinals naturally develop songs by imitating adults just as males do, allowing direct identification of when and what song types are memorized by females for vocal production. I sought to determine if the memory trace formed for vocal performance is identical with the memory trace that guides song type preference in a sexual context, and whether females truly form any song type preference based on auditory experience during the first year of their lives. To address these questions, audio-video playback experiments were carried out on captive-raised adult cardinals whose complete auditory history was known. The results showed that female cardinals did not come to prefer any song type based on experience; they responded equally to all conspecific song types. Thus, memory formed for vocal production in females is not equal to song type preferred in sexual context. The results suggest that variation in song types is not important for mate choice in cardinals.

Effects of fadrozole on sexual displays and reproductive activity in the female canary

LEBOUCHER, G., N. BÉGUIN, R. MAUGET AND M. KREUTZER. Effects of fadrozole on sexual displays and reproductive activity in the female canary. PHYSIOL BEHAV 65(2) 233–240, 1998.–We used fadrozole, a potent inhibitor of the aromatization of androgens to estrogens, to investigate the influence of estradiol on copulation solicitation displays (CSD) and reproductive activity in female canaries ( Serinus canaria). Systemic injections of fadrozole during 10 consecutive days were effective in reducing plasma estradiol concentrations in adult female canaries submitted to photostimulation. Fadrozole provides a powerful tool for limiting an individual’s exposure to estradiol, and the results of this study emphasize the influence of estradiol secretion in the regulation of behavioral transitions along the reproductive cycle of the female canary. When females were injected at the beginning of photostimulation, the emergence of copulation solicitation displays in response to conspecific songs was delayed. When females were injected later, after they were sexually active, the fadrozole treatment did not affect sexual displays. These results are consistent with the hypothesis that a threshold level of estradiol is critical to activate the neural circuitry mediating the copulation solicitation displays response in the female canary. They also suggest that the magnitude of sexual response is not related in a dose-dependent manner to estrogen concentrations observed during the period of sexual responsiveness. When females were injected at the beginning of photostimulation, egg-laying was delayed; when females were injected later, after they were sexually active, the fadrozole treatment dramatically reduced egg-laying and prevented incubation.

Sexual Preferences for Mate Song in Female Canaries (Serinus Canaria)

Abstract Recent studies have shown that female passerine birds give more sexual displays for songs of their mates than for songs of other males. The present study aimed to determine to what extent familiarisation with a song may account for females' song preferences. Ten female canaries were paired with a male during 3 days before egg laying; females were subsequently left alone to incubate and rear their young. Females were subjected to the familiarisation procedure when nestlings were 9 days old, until they were 17 days old. During the familiarisation period, twice a day, each female was successively exposed to the playback of three successive song records: (a) The mate song (M), a song frequently emitted by their previous sexual partner; when this song was played back, females were concurrently exposed to the sight of their previous mate. (b) The song of a non-mate accompanied by the sight of the mate (NMAS), a song emitted by a non-mate male; when this song was played back, females were also exposed to the sight of their previous mate. (c) The song of a non-mate not accompanied by the sight of the mate (NMNAS). At the end of this familiarisation period, the sexual preferences of the females for these songs were studied. Sexual responses were elicited by the emission of the M, NMAS and NMNAS songs, without male presentation. We analysed the total number of copulation solicitation displays (CSDs) elicited by each song. Females displayed more for M song than for NMAS or NMNAS songs. Eight of the 10 females gave at least half of their displays to M song. In a separate experiment, females without reproductive experience with the males failed to present a preference for any of these songs. Taken together, these results strongly suggest that mate recognition is not a mere effect of familiarisation with songs but is closely associated with previous reproductive experience. Song preferences that develop as a result of association with a particular male may be important in the maintenance of pair bonds and could influence future copulation acceptance with this mate.