Developmental stress, social rank and song complexity in the European starling (Sturnus vulgaris)

Bird song is a sexually selected trait and females have been shown to prefer males that sing more complex songs. However, for repertoire size to be an honest signal of male quality it must be associated with some form of cost. This experiment investigates the effects of food restriction and social status during development on song complexity in the European starling (Sturnus vulgaris). Birds that experienced an unpredictable food supply early in life produced a significantly smaller repertoire of song phrases than those with a constant food supply. Social status during development was also significantly correlated with repertoire size, with dominant birds producing more phrase types. This study therefore provides novel evidence that social as well as nutritional history may be important in shaping the song signal in this species.     

Experimentally Elevated Plasma Testosterone Levels Do Not Influence Singing Behaviour of Male Blue Tits (Parus caeruleus) During the Early Breeding Season

Sexual selection theory suggests that females might prefer males on the basis of testosterone (T)‐dependent secondary sexual traits such as song. Correlational studies have linked high plasma T‐levels to high diurnal song output. This has been confirmed in experiments where T‐levels were kept high at times when natural T‐levels have decreased. However, surprisingly little is known about the relation between T‐levels during the early breeding season and song. In many passerine birds males sing at a high rate at dawn early in the breeding season, referred to as the dawn chorus. In blue tits (Parus caeruleus), the dawn chorus coincides with the fertile period of the female, whereas diurnal song occurs throughout the breeding season. Previous studies on blue tits showed that characteristics of the dawn chorus correlate with male reproductive success. We experimentally elevated plasma T‐levels in male blue tits during the pre‐fertile and fertile period. Our aim was to test whether increased plasma T‐levels affect dawn song characteristics and increase the amount of diurnal song. Although T‐implants successfully raised circulating T‐levels, we did not find any difference between T‐ and control males in temporal performance measures of dawn song or in diurnal song output. Our results suggest that either there is no direct causal link between song output or quality and individual T‐levels, or experimental manipulations of T‐levels using implants do not permit detection of such effects during the early breeding season. Although we cannot exclude that individual T‐levels are causally linked to other (e.g. structural) song parameters, our results cast doubt on T‐dependence as the mechanisms that enforces honesty on song as a sexually selected trait.     

Song diversification and complexity in canaries and seedeaters (Serinus spp.)

Bird song is a composite trait that shows great variation in syntax and phonology between taxa, which hampers the precise quantification of complexity. This should be more feasible for closely-related species that share aspects of song organization. We conducted a comparative study of song and syllable characteristics in the largest fringillid genus, Serinus (canaries and seedeaters), with two objectives: (1) to describe and quantify song complexity in the genus and (2) to assess evolutionary dynamics of song, in particular whether interspecific song diversification evolved along intraspecific lines of covariation between syllable characteristics. We document a pattern of intense, very labile evolution of song in the genus. Well-known vocal constraints such as the relationship between frequency and body size did not appear to limit this evolution, and intraspecific trade-offs between different aspects of syllable complexity did not constrain interspecific diversification. Factor analysis returned an axis of variation that comprehensively expresses song complexity in the genus, and is defined by song speed, repertoire size, and also various aspects of syllable phonology. The species body size is not related to this axis of complexity, but to a minor axis that may indicate better respiratory capacity of larger birds. We discuss the pattern of song evolution in Serinus spp. in the context of the evolutionary dynamics of sexually selected traits.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 183–194.     

Elevating perceived predation risk modifies the relationship between parental effort and song complexity in the song sparrow Melospiza melodia

Adult‐directed predation risk elevates costs of parental care, and may modify relationships between sexually selected ornaments and parental effort by accentuating the tradeoff between survival and parental investment. We assessed multiple hypotheses regarding the relationship between maternal effort, paternal effort, and the sexually selected trait of male song complexity in the song sparrow Melospiza melodia. Further, we explored whether experimentally elevating perceived adult‐directed predation risk near nests affected these relationships. We quantified two dimensions of song complexity: song repertoire size and residual syllable number (the relative number of syllables for a given song repertoire size). Under elevated perceived predation risk, but not in the absence of the predator stimuli, females mated to males with higher residual syllable number displayed higher nestling provisioning rates and performed a greater proportion of nestling provisioning trips. In other words, elevating perceived predation risk induced a pattern of maternal investment consistent with differential allocation. In contrast, under elevated perceived predation risk, only, females performed a lesser proportion of provisioning trips when mated to males with large song repertoire sizes. Further, consistent with the good parent hypothesis, males with large song repertoire sizes displayed lower latencies to return to the nest, independent of the predator stimuli. Results suggest that residual syllable number may reflect some aspect of male genetic quality, such that females are more willing to maintain maternal effort while facing heightened predation risk. On the other hand, females may gain paternal benefits when mated to males with large song repertoires. Our study supports the hypothesis that increased costs of parental care associated with predation risk may induce relationships between sexually selected traits and parental behavior, which may increase the strength of sexual selection. Additionally, results suggest that different aspects of song complexity may fulfill non‐equivalent signaling roles.     

Song as an indicator of male parental effort in the sedge warbler

Repertoire size has been found to be a sexually selected trait in a number of bird species, although the advantages of mating with a male who possesses a complex song remain unclear. We studied the potential role of song as an indicator of male parental effort in the sedge warbler Acrocephalus schoenobaenus. The male provisioning rate was used as a measure of male parental effort and was found to increase with nestling age and brood size. When controlling for chick age, brood size and other variables, we found a highly significant positive correlation between a measure of song complexity (repertoire size) and male parental effort. Both male parental effort and repertoire size were found to be positively correlated with chick weight when controlling for chick age. We found no correlation between a measure of song output (amount of song flighting) or territory size and parental effort. Repertoire size is known to be the most important cue in female choice amongst sedge warblers and we discuss the possible reasons for this. We suggest that, in choosing a male with a large repertoire, a female obtains not only indirect benefits but also direct benefits in the form of increased parental effort.     

Song Amplitude of Rival Males Modulates the Territorial Behaviour of Great Tits During the Fertile Period of Their Mates

Bird song is a widely used model in the study of sexual selection. Variation in the expression of sexually selected traits is thought to reflect variation in male genetic and/or phenotypic quality. Vocal amplitude is a song parameter that has received little attention in the context of sexual selection, but there is some evidence that the intensity of bird song affects female preferences. Here, we tested whether the amplitude of broadcast song plays a role in male–male competition. We used song playback with varying song amplitude (within the natural amplitude range of the species) and a dummy bird taxidermy to simulate territorial intrusions in the great tit, Parus major, during the fertile period of the female and measured the response of the local male. The results show that playback amplitude significantly affected the subjects’ behaviour: after approaching to within 25 m around the loudspeaker, territorial males stayed longer within that perimeter after the playback of high‐amplitude songs compared with low‐amplitude songs. Our findings add to the small but growing body of evidence suggesting that vocal amplitude may be a sexually selected song trait.     

Singing Activity Reveals Personality Traits in Great Tits

In animal communication, sexually selected signals have been shown to often signal individual attributes such as motivation or quality. Birdsong is among the best studied signalling systems, and song traits vary substantially among individuals. The question remains if variation in signalling also reflects more general and consistent individual characteristics. Such consistent individual differences in behaviour that are relatively stable over time and contexts are referred to as personality or behavioural syndromes. Here, we studied the relation between singing and explorative behaviour, a well‐studied personality trait, using great tits (Parus major) under standardized aviary conditions. The results show that singing activity measured as the number of songs sung in spring prior to breeding correlated with male but not with female explorative behaviour. In contrast, song repertoire was not related to explorative behaviour but varied over the day. The link between explorative and singing behaviour suggests that sexually selected signals are more than signals of quality but can also reflect other intrinsic behavioural characteristics such as personality traits.     

The Dawn Song of the Blue Tit Parus caeruleus and its Role in Sexual Selection

Sexual selection arises when variance in male reproductive success is non-randomly related to phenotypic characters of males. Song can be considered as such a phenotypic character and several studies have shown that song complexity and/or song output are important in competition among males or in partner choice. In the blue tit Parus caeruleus a peak in male singing activity occurs at dawn during the female fertile period, i.e. after pair formation. The function of this dawn chorus is not well understood. In this study 20 male blue tits were recorded at dawn and song complexity and output were expressed as versatility, mean strophe length, mean percentage performance time and bouts with or without drift, i.e. with or without a systematic decline in percentage performance time. Females mated to males with a higher mean percentage performance time (output) and a higher versatility (complexity) started to lay eggs earlier, but the latter was not significant. Females mated to males that showed no drift in their song bouts laid significantly larger clutches. Our results thus suggest that in the blue tit, song output at dawn, rather than song complexity, might be a trait under sexual selection.     

Testosterone increases repertoire size in an open-ended learner: An experimental study using adult male European starlings (Sturnus vulgaris)

Song in songbirds is a learned secondary sexual behavior, first acquired during a sensitive phase of juvenile development, which is affected by hormones such as testosterone (T). While the latter has received much attention, the potential involvement of T in the adult repertoire changes observed in a number of species is much less understood. Yet, this may prove essential to understand the role of song as a sexually selected trait. We therefore performed a T-implantation experiment during the non-breeding season (when T is basal), using adult male European starlings (Sturnus vulgaris), a songbird species in which song repertoire size (and composition) changes seasonally and increases with age. Repertoire size increased rapidly in T-males, but not in control males, indicating a role for T in repertoire size changes. This increase resulted from a lower proportion of dropped song types in T-males than in control males, while the proportion of added song types did not differ between both groups. Interestingly, the observed repertoire turnover (adding and removing song types from the repertoire) in both groups, suggests that elevated plasma T levels were not essential for changes in repertoire composition (contrary to repertoire size). Finally, T-males (but not control males) significantly increased their song rate, while neither group showed a significant change in their song bout length and phrase repetition rate. Taken together, our results suggest a role for T in adult song learning and provide new insights into the information content of repertoire size and song bout length as sexually selected traits.     

Testosterone increases repertoire size in an open-ended learner: An experimental study using adult male European starlings (Sturnus vulgaris)

Song in songbirds is a learned secondary sexual behavior, first acquired during a sensitive phase of juvenile development, which is affected by hormones such as testosterone (T). While the latter has received much attention, the potential involvement of T in the adult repertoire changes observed in a number of species is much less understood. Yet, this may prove essential to understand the role of song as a sexually selected trait. We therefore performed a T-implantation experiment during the non-breeding season (when T is basal), using adult male European starlings (Sturnus vulgaris), a songbird species in which song repertoire size (and composition) changes seasonally and increases with age. Repertoire size increased rapidly in T-males, but not in control males, indicating a role for T in repertoire size changes. This increase resulted from a lower proportion of dropped song types in T-males than in control males, while the proportion of added song types did not differ between both groups. Interestingly, the observed repertoire turnover (adding and removing song types from the repertoire) in both groups, suggests that elevated plasma T levels were not essential for changes in repertoire composition (contrary to repertoire size). Finally, T-males (but not control males) significantly increased their song rate, while neither group showed a significant change in their song bout length and phrase repetition rate. Taken together, our results suggest a role for T in adult song learning and provide new insights into the information content of repertoire size and song bout length as sexually selected traits.     

Zebra finch song reflects current food availability

Food availability is a major evolutionary force that has direct effects on an individual’s body condition. Since sexually selected traits are often condition-dependent, they are likely to reflect food availability or other ecological constraints. Here we test whether bird song, which is thought to be under intense female choice, is sensitive to food availability and might be used by females to assess male body condition and/or territory quality. We manipulated food availability of male zebra finches (Taeniopygia guttata) and assessed the within-individual effects of the treatment on song parameters that are thought to be important in mate choice. We found no effect of food availability on syllable repertoire, proportion of sound versus silence within a song, and mean song frequency. In contrast, treatment birds showed a reduced song rate, an increased latency to sing, and a lowered song amplitude and fundamental frequency. Our study demonstrates that zebra finch song reflects food availability and that songs of well-fed males contain traits that have previously been reported to be more attractive to females. This adds strong support to the general assumption that female song preferences evolved because song reflects male quality and/or territory quality. Moreover, our study provides corroborative evidence for the notion that variation in environmental factors plays an important role in the evolution of mating signals.     

Experimental Tests of the Function and Flexibility of Song Consistency in a Wild Bird

Measures of bird song that capture aspects of motor performance, such as consistency, have become a major focus in understanding sexual selection on song. Despite accumulating evidence that consistency is related to reproductive success in many species, the relative importance of male–male interactions and female–male interactions is still unclear. We studied the function and flexibility of song consistency and song rate in common yellowthroat warblers (Geothlypis trichas). A previous study of this population found that song consistency—measured as the amount of variability within a bout of songs—was positively correlated with the likelihood of siring extrapair young. In this study, we conducted two experiments aimed at testing (1) the role of song consistency and rate in mediating male–male and male–female interactions and (2) whether song effort is flexibly adjusted to changes in social context. In the first experiment, we simulated a male territorial intrusion with song playbacks that varied in consistency and rate; focal males responded aggressively to playbacks, but their response did not differ with playback consistency or rate. In the second experiment, we presented focal males with a taxidermic female mount and female vocalizations; focal males approached the speaker, but continued to sing and did not perform the aggressive rattle vocalization observed during male encounters. Immediately after the simulated female encounter, focal males increased in song consistency. Taken together, our results are most consistent with the hypothesis that song consistency in common yellowthroats is primarily a female‐directed signal that is actively adjusted in response to rapidly changing social conditions.     

Song repertoire size varies with HVC volume and is indicative of male quality in song sparrows (Melospiza melodia)

Complex birdsong is a classic example of a sexually selected ornamental trait. In many species, females prefer males with large song repertoires, possibly because repertoire size is limited by the size of song control nuclei which reflect developmental success. We investigated whether song repertoire size was indicative of brain area and male quality in song sparrows (Melospiza melodia) by determining if repertoire size was related to the volume of song control nucleus HVC, as well as several morphological, immunological and genetic indices of quality. We found that males with large repertoires had larger HVCs and were in better body condition. They also had lower heterophil to lymphocyte ratios, indicating less physiological stress and a robust immune system as measured by the number of lymphocytes per red blood cell. Song repertoire size also tended to increase with neutral-locus genetic diversity, as assessed by mean d2, but was not related to internal relatedness. Our results suggest several mechanisms that might explain the finding of a recent study that song sparrows with large song repertoires have higher lifetime fitness.     

Short records of marsh warbler ( Acrocephalus palustris) song provide indices that correlate with nesting success

The migrant Marsh Warbler (Acrocephalus palustris) has a complex song repertoire, but such complexity makes quantitative comparison of songs between individual males both time consuming and challenging. We investigate a streamlined method of song analysis that uses 2-min records of song to provide simpler relative indices of repertoire size, including the use of capture-recapture and species-richness models. For each male, three attributes of song were determined: the song complexity, the total repertoire elements and the estimated repertoire size based on the Burnham and Overton jackknife method. Males with higher song indices tend to have greater nesting success, suggesting that even short records of song can indicate male quality to prospective female mates. Why should male Marsh Warblers have long and sustained songs when only 2-min records correlate with nesting success? Assuming that song advertises the quality of the male, and that the quality of such advertisement is sustained throughout the males song period, we argue that the female may need to have only brief exposure initially to that song to assess its quality and hence the quality of the male. More continuous periods of song may reinforce that initial choice by the female, and allow males to remain conspicuous to transient females moving around the territories of potential male mates.     

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.     

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.     

Quality of song learning affects female response to male bird song

Bird song is unusual as a sexually selected trait because its expression depends on learning as well as genetic and other environmental factors. Prior work has demonstrated that males who are deprived of the opportunity to learn produce songs that function little if at all in male-female interactions. We asked whether more subtle variation in male song-learning abilities influences female response to song. Using a copulation solicitation assay, we measured the response of female song sparrows (Melospiza melodia) to songs of laboratory-reared males that differed in the amount of learned versus invented material that they included and in the degree to which learned material accurately matched the model from which it was copied. Females responded significantly more to songs that had been learned better, by either measure. Females did not discriminate between the best-learned songs of laboratory-reared males and songs of wild males used as models during learning. These results provide, to our knowledge, a first experimental demonstration that variation in learning abilities among males plays a functionally important part in the expression of a sexually selected trait, and further provide support for the hypothesis that song functions as an indicator of male quality because it reflects variation in response to early developmental stress.     

Sex role similarity and sexual selection predict male and female song elaboration and dimorphism in fairy‐wrens

Historically, bird song complexity was thought to evolve primarily through sexual selection on males; yet, in many species, both sexes sing and selection pressure on both sexes may be broader. Previous research suggests competition for mates and resources during short, synchronous breeding seasons leads to more elaborate male songs at high, temperate latitudes. Furthermore, we expect male–female song structure and elaboration to be more similar at lower, tropical latitudes, where longer breeding seasons and year‐round territoriality yield similar social selection pressures in both sexes. However, studies seldom take both types of selective pressures and sexes into account. We examined song in both sexes in 15 populations of nine‐fairy‐wren species (Maluridae), a Southern Hemisphere clade with female song. We compared song elaboration (in both sexes) and sexual song dimorphism to latitude and life‐history variables tied to sexual and social selection pressures and sex roles. Our results suggest that song elaboration evolved in part due to sexual competition in males: male songs were longer than female songs in populations with low male survival and less male provisioning. Also, female songs evolved independently of male songs: female songs were slower paced than male songs, although only in less synchronously breeding populations. We also found male and female songs were more similar when parental care was more equal and when male survival was high, which provides strong evidence that sex role similarity correlates with male–female song similarity. Contrary to Northern Hemisphere latitudinal patterns, male and female songs were more similar at higher, temperate latitudes. These results suggest that selection on song can be sex specific, with male song elaboration favored in contexts with stronger sexual selection. At the same time, selection pressures associated with sex role similarity appear to favor sex role similarity in song structure.     

Variation in Song Rate during the Breeding Cycle of the Chaffinch,Fringilla coelebs

The variation in song rate during the breeding season was studied in two individually marked chaffinch Fringilla coelebs populations. We gathered data to investigate especially the recently presented mate-guarding hypothesis. The active singing has been supposed to function as a form of mate guarding during the female's fertile period by announcing the high status of the male and preventing extra-pair copulations by neighbouring males. There was no clear dawn chorus in the chaffinch, i.e. a peak in the song rate before sunrise. Male chaffinches continued to sing after mating, but the song rate dropped significantly. In contrast to the mate-guarding hypothesis the song rate was lower during the fertile period of the female than during pre-mating and incubation. Thus, the males do not announce the fertility status of their mates or their own quality and status by active singing. The song does not function as a form of mate guarding in the chaffinch. One function of the song of the chaffinch is mate attraction: singing activity was highest before pair formation in early spring and decreased after mating but increased again if the male lost his mate later in the breeding season.     

Regulation of the HPA axis is related to song complexity and measures of phenotypic quality in song sparrows

Regulation of the hypothalamic-pituitary-adrenal (HPA) axis is a key component of the vertebrate stress response. Prior studies have found that variation in HPA responses were correlated to measures of fitness and physiological condition. In addition, sexually-selected traits have also been found to correlate to measures of condition. The proximate mechanisms responsible for such covariation between sexually selected traits and measures of quality are unclear, but could involve variation in HPA regulation. We investigated whether HPA activity is related to song complexity, body size/condition and leukocyte profiles in wild male song sparrows (Melospiza melodia). We characterized three aspects of HPA activity: 1) response to restraint stress; 2) negative feedback, assessed by the ability of exogenous dexamethasone to suppress corticosterone levels; and 3) adrenal sensitivity to exogenous adrenocorticotropic hormone (ACTH). Birds with lower responses to restraint stress had more complex song and more heterophils and higher heterophil to lymphocyte (H:L) ratios. Birds with more effective negative feedback were larger and had fewer heterophils and lower H:L ratios, suggesting lower levels of physiological stress or infection. We observed no relationship between adrenal sensitivity to exogenous ACTH and any of the factors. These findings illustrate important relationships between HPA activity, song complexity, and morphological and physiological traits. Song complexity may thus provide receivers with information about the ability of the singer to cope with stressors.