Undirected Song in Wild Zebra Finch Flocks: Contexts and Effects of Mate Removal

Wild zebra finches, Taeniopygia guttata, sing frequently throughout the year but the function of undirected song, the most prevalent type, is unknown. Paired males commonly sang undirected song in feeding flocks where it occurred more frequently in the non-breeding season than in the breeding season. Song rate varied greatly among males. The context of the singer and the absence of any overt responses from flock members excludes direct aggressive and mate-attracting functions. Performance of undirected song may have energetic costs and predatory risks. The finding that singers are active individuals with ‘spare time’, that are neither hungry, nor tired, nor sexually motivated, suggests that singers are advertising their ‘quality’ as potential mates and/or participants for extra-pair copulations. When the female partner in non-breeding pairs was experimentally removed, the rate of undirected song of the ‘widower’ increased significantly. Males quickly re-paired. This experiment supports the hypothesis that singing in the flock has a mate-attracting role.     

Nocturnal and diurnal singing activity in the nightingale: correlations with mating status and breeding cycle

This study on the nightingale, Luscinia megarhynchos, is the first to examine both nocturnal and diurnal singing activity of mated and unmated males throughout a species' entire breeding cycle. Nocturnal song was sung mostly by unmated males. After pair formation, males ceased nocturnal singing and resumed it if their mate deserted. These results strongly suggest that nocturnal song of unmated males functions to attract a mate. Diurnal singing activity before females settled was low and did not predict future mating status. However, unmated males showed a continuous increase in diurnal singing activity until the end of the breeding cycle, but diurnal singing activity of mated males decreased after the egg-laying period. Mated males resumed nocturnal song for, on average, 3 nights during egg laying by their mates. This second period of nocturnal song coincided with the peak of diurnal singing activity. Such a high male singing effort during egg laying might allow the female to adjust her reproductive effort to male quality, deter rival males (e.g. through honest announcement of the female's fertility) or attract females for extrapair copulations. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris)

In male starlings (Sturnus vulgaris) courtship song plays a critical role in mate attraction. During the breeding season courtship song occurs prior to copulation and appears to reflect male sexual arousal. Outside the breeding season starlings sing, but song appears unrelated to reproduction. The aromatization of testosterone (T), likely within the medial preoptic nucleus (POM), is critical for the expression of male sexual arousal. The present study was performed to determine whether seasonal changes in the POM might relate to seasonal changes in courtship singing behavior in male starlings. T concentrations, the volume of the POM, and aromatase within the POM were examined both during and outside of the breeding season in male starlings. Song was also recorded at these times both with and without a female present. The POM was largest and contained dense aromatase immunostaining only during the spring breeding season, when T concentrations were highest and males responded to a female with an increase in courtship song. Outside the breeding season the volume of the POM was small, T concentrations were low, and males displayed no changes in song expression in response to female conspecifics. Song bout length was positively related to POM volume, and males sang longer songs in spring. Only males with nestboxes in spring responded to a female, and the POM tended to be larger in these males, suggesting that nestbox possession might influence neuroplasticity within the POM. Overall, the findings suggest that T-dependent plasticity and aromatase activity within the POM might regulate courtship singing in a wild songbird.     

Seasonal Changes in Courtship Song and the Medial Preoptic Area in Male European Starlings (Sturnus vulgaris)

In male starlings (Sturnus vulgaris) courtship song plays a critical role in mate attraction. During the breeding season courtship song occurs prior to copulation and appears to reflect male sexual arousal. Outside the breeding season starlings sing, but song appears unrelated to reproduction. The aromatization of testosterone (T), likely within the medial preoptic nucleus (POM), is critical for the expression of male sexual arousal. The present study was performed to determine whether seasonal changes in the POM might relate to seasonal changes in courtship singing behavior in male starlings. T concentrations, the volume of the POM, and aromatase within the POM were examined both during and outside of the breeding season in male starlings. Song was also recorded at these times both with and without a female present. The POM was largest and contained dense aromatase immunostaining only during the spring breeding season, when T concentrations were highest and males responded to a female with an increase in courtship song. Outside the breeding season the volume of the POM was small, T concentrations were low, and males displayed no changes in song expression in response to female conspecifics. Song bout length was positively related to POM volume, and males sang longer songs in spring. Only males with nestboxes in spring responded to a female, and the POM tended to be larger in these males, suggesting that nestbox possession might influence neuroplasticity within the POM. Overall, the findings suggest that T-dependent plasticity and aromatase activity within the POM might regulate courtship singing in a wild songbird.     

Testosterone Affects Song Modulation during Simulated Territorial Intrusions in Male Black Redstarts (Phoenicurus ochruros)

Although it has been suggested that testosterone plays an important role in resource allocation for competitive behavior, details of the interplay between testosterone, territorial aggression and signal plasticity are largely unknown. Therefore, we investigated if testosterone acts specifically on signals that communicate the motivation or ability of individuals to engage in competitive situations in a natural context. We studied the black redstart, a territorial songbird species, during two different life-cycle stages, the early breeding phase in spring and the non-breeding phase in fall. Male territory holders were implanted with the androgen receptor blocker flutamide (Flut) and the aromatase inhibitor letrozole (Let) to inhibit the action of testosterone and its estrogenic metabolites. Controls received a placebo treatment. Three days after implantation birds were challenged with a simulated territorial intrusion (STI). Song was recorded before, during and after the challenge. In spring, both treatment groups increased the number of elements sung in parts of their song in response to the STI. However, Flut/Let-implanted males reacted to the STI with a decreased maximum acoustic frequency of one song part, while placebo-implanted males did not. Instead, placebo-implanted males sang the atonal part of their song with a broader frequency range. Furthermore, placebo-, but not Flut/Let-implanted males, sang shorter songs with shorter pauses between parts in the STIs. During simulated intrusions in fall, when testosterone levels are naturally low in this species, males of both treatment groups sang similar to Flut/Let-implanted males during breeding. The results suggest that song sung during a territorial encounter is of higher competitive value than song sung in an undisturbed situation and may, therefore, convey information about the motivation or quality of the territory holder. We conclude that testosterone facilitates context-dependent changes in song structures that may be honest signals of male quality in black redstarts.     

Singing strategies among male Black-browed Reed Warblers Acrocephalus bistrigiceps during the post-fertile period of their mates

Bird song is critical to mate attraction. Because singing involves fitness costs, males that sing vigorous and complex songs are thought to be of high quality. Males of the Black-browed Reed Warbler Acrocephalus bistrigiceps sang actively when they were solitary, but stopped singing as soon as they had attracted a female. Males exhibited two distinct patterns of singing behaviour after the fertile period of their mates: some resumed singing, whereas others did not. Males that resumed singing acquired secondary females more frequently than those that did not sing, suggesting that resuming males seek polygynous mating. The occurrence of extra-pair fertilization was rare (6.4%) in the study population, and extra-pair young were sired by both resuming and non-resuming males. There is no strong evidence that non-resuming males compensate for their disadvantage in social mate acquisition by extra-pair paternity. Resuming males arrived at the breeding ground earlier, suggesting that they were high-quality males.     

Spatial and Temporal Distribution of Song in the Yellowhammer Emberiza citrinella

The temporal and spatial distribution of song was studied in a population of yellowhammers Emberiza citrinella. Song was most frequent during the breeding season, and within the breeding season during the fertile period of both first, second, and replacement clutches. Song activity peaked at sunrise and sunset. During the fertile period most singing took place in the central parts of the territory. Song post heights peaked during the fertile period, and more song posts lacked foliage at that time. Intrusions by male conspecifics peaked in the fertile period and in territories where males sang relatively little. Song activity and mate guarding were strongly positively correlated. Song volume was loud and song was thus apparently used in long-distance communication. These observations are in accordance with a male deterrence hypothesis, suggesting that males sing to deter neighbouring males from trespassing during the fertile period of their mate. A female attraction hypothesis, suggesting that males sing to attract neighbouring females and thereby obtain extra-pair copulations, and a female reproduction hypothesis, suggesting that males sing to start the female reproductive cycle, were partly supported by observations.     

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.     

Behavioral phenotypes persist after gonadal steroid manipulation in white-throated sparrows

White-throated sparrows (Zonotrichia albicollis) exhibit a behavioral polymorphism that segregates with a plumage marker. Individuals with a white stripe (WS) on the crown engage in an aggressive strategy that involves more singing, whereas individuals with a tan stripe (TS) sing less and engage in more parental care. Previous work has shown that plasma levels of gonadal steroids differ between the morphs in both sexes, suggesting a hormonal mechanism for the polymorphic behavior in this species. Here, we eliminated morph differences in plasma levels of testosterone (T) in males and estradiol (E2) in females in order to test whether morph differences in behavior would be similarly eliminated. Males and females in non-breeding condition were treated with T or E2, respectively, so that plasma levels in the treated groups were high and equal between the WS and TS morphs. We found that despite hormone treatment, WS and TS birds differed with respect to singing behavior. WS males sang more in response to song playback than did TS males, and WS females exhibited more spontaneous song than TS females. We also found that WS males gave more chip calls, which are often used in contexts of territorial aggression. Overall, these results suggest that WS birds engage in more territorial vocalization, particularly song, than do TS birds, even when T or E2 levels are experimentally equalized. This behavioral difference may therefore be driven by other factors, such as steroid metabolism, receptor expression or function, or steroid-independent neurotransmitter systems.     

The song structure and seasonal patterns of vocal behavior of male and female bellbirds (Anthornis melanura)

The bellbird (Anthornis melanura) is a honeyeater endemic to New Zealand, which uses song to defend breeding territories and/or food resources year round. Both sexes sing and the song structure and singing behavior have not yet been quantified. The number of song types, spectral structure, repertoire size, and singing behavior of male and female bellbirds was investigated for a large island population. Song types differed between the sexes with males singing a number of structurally distinct song types and females producing song types that overlapped in structure. Singing behavior also differed between the sexes; males often sung long series of songs while females sung each song at relatively long and variable intervals. Singing by both sexes occurred year round but the frequency of male and female singing bouts showed contrasting seasonal patterns. The frequency of female singing bouts increased as the breeding season progressed, whereas male singing bouts decreased. In contrast to almost all studied passerines, female bellbirds exhibited significant singing behavior and sung songs of complex structure and variety that parallel male song. These results provide a quantitative foundation for further research of song in bellbirds and in particular the function of female vocal behavior.     

Context-dependent effects of castration and testosterone treatment on song in male European starlings

Most seasonally breeding songbirds display dramatic seasonal fluctuations in plasma testosterone (T) levels and mate attraction behaviors, including song. However, males of some songbird species, such as the European starling (Sturnus vulgaris), continue to sing at high levels after the breeding season, when T levels are basal. In male starlings song during the breeding season functions mainly to attract mates, whereas song during the nonbreeding season appears unrelated to reproduction. This suggests that song produced in a context unrelated to female courtship, unlike song directed toward females, is not regulated by plasma T. In captive males housed in large outdoor aviaries we explored the relationship between plasma T and song produced during the breeding season within and outside a courtship context. This was achieved by determining the effects of castration and subsequent T treatment on song and mate attraction behaviors in both the presence and the absence of a female. Compared to intact males, castrated males did not show reduced song activity in the absence of a female for at least 6 months after the operation, strongly suggesting that the expression of noncourtship song is not regulated by plasma T. Likewise, we found that experimentally elevating T levels in castrated males did not affect noncourtship song rates. However, control castrated males receiving empty implants tended to show reduced noncourtship song rates after implantation. This may have been due to a suppressive effect caused by the presence of the T-implanted castrated males in the same aviary. In contrast, courtship singing was clearly controlled by plasma T: it was abolished by castration and restored by subsequent T replacement when males were housed both individually and in a group situation. High plasma levels of T also appeared necessary for the activation of three other behavioral traits critical for mate attraction, namely, nesthole occupancy, spending time (singing) in a nesthole, and carrying green nesting material into a nesthole.     

Social factors affect the singing rates of female northern cardinals Cardinalis cardinalis

Social factors, such as the duration of territorial occupancy or of time paired with a mate can affect the rate at which individual birds sing. This study examined the influence of duration of pair-bond and territory occupancy as well as date on the rate of singing by male and female northern cardinals Cardinalis cardinalis . When differences in breeding status were controlled, female cardinals sang at higher rates earlier in the season. Females in newly formed pairs sang at significantly higher rates than those in pairs that had previously bred together. In contrast, male cardinals did not show significant variation in the rate of singing throughout the season. The song rates of males in newly formed and established pairs did not differ significantly. Song rates for males and females in mated pairs were not significantly correlated. This study suggests that social factors have a strong effect on the rate at which female cardinals sing. It is possible that increased intra-sexual aggression by females when they are establishing a new territory with a new mate leads to this higher level of song output. Once females have established a territory and acquired a mate, dear-enemy effects might diminish the need for acoustic territorial defence. Differences in the constraints of nesting or the attraction of extra-pair mates might explain the sexual differences in male and female singing behaviour.     

Social context affects testosterone-induced singing and the volume of song control nuclei in male canaries (Serinus canaria)

The contribution of social factors to seasonal plasticity in singing behavior and forebrain nuclei controlling song, and their interplay with gonadal steroid hormones are still poorly understood. In many songbird species, testosterone (T) enhances singing behavior but elevated plasma T concentrations are not absolutely required for singing to occur. Singing is generally produced either to defend a territory or to attract a mate and it is therefore not surprising that singing rate can be influenced by the sex and behavior of the social partner. We investigated, based on two independent experiments, the effect of the presence of a male or female partner on the rate of song produced by male canaries. In the first experiment, song rate was measured in dyads composed of one male and one female (M-F) or two males (M-M). Birds were implanted with T-filled Silastic capsules or with empty capsules as control. The number of complete song bouts produced by all males was recorded during 240 min on week 1, 2, 4, and 8 after implantation. On the day following each recording session, brains from approximately one-fourth of the birds were collected and the volumes of the song control nuclei HVC and RA were measured. T increased the singing rate and volume of HVC and RA but these effects were affected by the social context. Singing rates were higher in the M-M than in the M-F dyads. Also, in the M-M dyads a dominance-subordination relationship soon became established and dominant males sang at higher rates than subordinates in T-treated but not in control pairs. The differences in song production were not reflected in the size of the song control nuclei: HVC was larger in M-F than in M-M males and within the M-M dyads, no difference in HVC or RA size could be detected between dominant and subordinate males. At the individual level, the song rate with was positively correlated with RA and to a lower degree HVC volume, but this relationship was observed only in M-M dyads, specifically in dominant males. A second experiment, carried out with castrated males that were all treated with T and exposed either to another T-treated castrate or to an estradiol-implanted female, confirmed that song rate was higher in the M-M than in the M-F condition and that HVC volume was larger in heterosexual than in same-sex dyads. The effects of T on singing rate and on the volume of the song control nuclei are thus modulated by the social environment, including the presence/absence of a potential mate and dominance status among males.     

Seasonal patterns of singing in the willow warbler: evidence against the fertility announcement hypothesis

Males of many bird species use a variety of behaviour patterns that reduce their chances of being cuckolded. The 'fertility announcement' hypothesis (M?ller 1991, American Naturalist, 138, 994-1014) proposes that song might be one such paternity guard. According to this hypothesis, paired males would announce their female's fertile status by singing. This has been interpreted as an honest signalling, evolutionarily stable strategy. Contrary to the predictions of this hypothesis, male willow warblers, Phylloscopus trochilus, sang very little when females were fertile. Intrusions by other males in the fertile period were not less common when males sang at higher rates. Mate guarding and singing are best interpreted as two conflicting behaviours during this period, the former being directed to the fertile female and the latter to attracting a second female, or an extrapair female. A survey of recent studies suggests that, in most passerine species studied, males do not sing during the fertile period of their females. The different conclusions of M?ller (1991) are probably due to his use of population-wide estimates of the timing of singing behaviour and egg laying. Breeding asynchronies within populations would be responsible for the apparent matching between the peaks of singing activity and fertility. Copyright 1999 The Association for the Study of Animal Behaviour.     

Social factors affect the singing rates of female northern cardinals Cardinalis cardinalis

Social factors, such as the duration of territorial occupancy or of time paired with a mate can affect the rate at which individual birds sing. This study examined the influence of duration of pair‐bond and territory occupancy as well as date on the rate of singing by male and female northern cardinals Cardinalis cardinalis. When differences in breeding status were controlled, female cardinals sang at higher rates earlier in the season. Females in newly formed pairs sang at significantly higher rates than those in pairs that had previously bred together. In contrast, male cardinals did not show significant variation in the rate of singing throughout the season. The song rates of males in newly formed and established pairs did not differ significantly. Song rates for males and females in mated pairs were not significantly correlated. This study suggests that social factors have a strong effect on the rate at which female cardinals sing. It is possible that increased intra‐sexual aggression by females when they are establishing a new territory with a new mate leads to this higher level of song output. Once females have established a territory and acquired a mate, dear‐enemy effects might diminish the need for acoustic territorial defence. Differences in the constraints of nesting or the attraction of extra‐pair mates might explain the sexual differences in male and female singing behaviour.     

Conveying information with one song type: changes in dawn song performance correspond to different female breeding stages

Many bird species participate in dawn singing, a behaviour categorized by intensive singing at dawn; however, many of these species deliver only one song type at dawn. While there are many proximate and ultimate hypotheses for why birds sing at dawn, little is known about whether males are able to vary one simple song to convey different information. We used autonomous acoustic recorders to record dawn songs of field sparrows and quantified three parameters of singing performance: 1) bout length, 2) song rate, and 3) song complexity. We found that males sang the longest dawn bouts during their mate's fertile period, the highest song rates during the post-fertile period, and the most complex songs during the pre-fertile period. The change in dawn singing behaviour with their mate's breeding stage suggest the purpose of dawn song may be context dependent. Our results demonstrate that male field sparrows, while only having a single song type sung at dawn, may convey information for both intra- and intersexual purposes. While it is generally assumed that dawn song has a specific function, the variability in the duration, rate, and complexity of dawn song in field sparrows suggests that they are conveying different information and that dawn song likely has multiple functions.     

Honest advertisement and song output during the dawn chorus of black-capped chickadees

Costly signals can evolve under sexual selection, as only thosesignals that are difficult to produce and reflect the relativequality of individuals should be important in mate choice. Onesuch signal may be dawn singing behavior in birds. We assessedwhether the song output at dawn of breeding male black-cappedchickadees Parus atricapilhis honestly reflects quality, whererelative quality is assessed by relative dominance rank in winterflocks. Dawn choruses were recorded from 20 male chickadeesfrom 10 flocks during the fertile period of their mates in 1992,1994, and 1995. Dominance ranks of males were assessed by tabulatinginteractions at winter feeders from 1993 to 1995. A comparisonof the dawn singing behavior of the high-ranking and the low-rankingmales from each of the 10 flocks showed that high-ranking malesbegan singing earlier, sang longer, and sang at higher averageand maximum rates than low-ranking flockmates. Age of the maleshad less effect on song output at dawn than rank; older malestended to sing longer dawn choruses, but there was no differencein onset of singing, average song rate, or maximum song rateat dawn between hatch year and after-hatch year males. Our findingssuggest the dawn chorus can provide an accurate signal to femalesof the relative quality of their mate compared to neighboringmales     

Long-term influence of simulated territorial intrusions on dawn and dusk singing in the Winter Wren: spring versus autumn

Males of many songbird species have peaks of singing activity at dawn and dusk. Singing during those twilight periods can function in territory proclamation, and males are suggested to adjust song output to the level of intruder pressure. We used song playback during the breeding season to simulate intrusions into territories of male Winter Wrens (Troglodytes troglodytes) shortly after dawn. We then compared male singing behaviour during the dawn and dusk chorus before and 1 day after the simulated intrusion. One day after the playback, male Wrens increased their song output before sunrise, which confirms our results from a previous study on dawn singing in autumn territories. At dusk, on the evening following the playback, males slightly increased song output after sunset, but singing activity at dusk was generally very low. We found no significant changes of song output after sunrise, before sunset, and between 2 days of control without playback. These results are consistent with the hypothesis that dawn and dusk singing is important for territory defence in spring. Unlike in autumn, however, increased singing in spring at dawn and dusk could also serve to defend other resources such as fertile mates or to strengthen the pair bond after a territorial challenge. In comparison with the results on autumnal singing, male Wrens started singing earlier at dawn during the breeding season, and they generally sang more songs at dawn and immediately after playback. The increase in absolute numbers of songs sung in the morning after playback seemed greater in spring than in autumn; however, the proportional increase relative to overall song output was similar in both seasons.     

Behavioral and neural lateralization of vision in courtship singing of the zebra finch

Along with human speech and language processing, birdsong has been one of the best-characterized model systems for understanding the relationship of lateralization of brain function to behavior. Lateralization of song production has been extensively characterized, and lateralization of song perception has begun to be studied. Here we have begun to examine whether behavior and brain function are lateralized in relation to communicative aspects of singing, as well. In order to monitor central brain function, we assayed the levels of several activity dependent immediate early genes after directed courtship singing. Consistent with a lateralization of visual processing during communication, there were higher levels of expression of both egr-1 and c-fos in the left optic tectum after directed singing. Because input from the eyes to the brain is almost completely contralateral in birds, these results suggest that visual input from the right eye should be favored during normal singing to females. Consistent with this, we further found that males sang more when they could use only their right eye compared to when they could use only their left eye. Normal levels of singing, though, required free use of both eyes to view the female. These results suggest that there is a preference for visual processing by the right eye and left brain hemisphere during courtship singing. This may reflect a proposed specialization of the avian left hemisphere in sustaining attention on stimuli toward which a motor response is planned.     

Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris)

Bird song is a sexually selected male trait where females select males on the basis of song quality. It has recently been suggested that the quality of the adult male song may be determined by nutritional stress during early development. Here, we test the 'nutritional-stress hypothesis' using the complex song of the European starling. Fledgling starlings were kept under experimental treatment (unpredictable short-term food deprivations) or control conditions (ad libitum food supply), for three months immediately after independence. We measured their physiological and immune responses during the treatment and recorded song production during the following spring. Birds in the experimental group showed increased mass during the treatment and also a significantly suppressed humoral response compared with birds in the control group. There was no difference between the groups in the cell-mediated response. Next spring, males in the experimental group spent less time singing, sang fewer song bouts, took longer to start singing and also sang significantly shorter song bouts. These data support the hypothesis that both the quality and quantity of song produced by individual birds reflect past developmental stress. The results also suggest the 'nutritional-stress hypothesis' is best considered as a more general 'developmental-stress hypothesis'.