Alternative forms of song matching in song sparrows

Song matching, replying to a song with a similar song, occurs in many songbird species. Almost all investigations of song matching have been of type matching, where one bird's reply is unambiguously similar to the other's song (i.e. the same song type). In many populations, however, neighbours do not share song types, and therefore cannot type-match. We hypothesized that a bird lacking a true type match could still song-match a stimulus song with a song from his repertoire that was similar in some way the birds recognized. We tested this hypothesis in song sparrows, Melospiza melodia, in two playback experiments. We played the subject a stranger song that was similar to one or more of his songs, but a type match to none of them. In the first experiment, we used playback songs that began with two buzzes (‘double-buzz’ songs). In the second experiment, we used songs that began with a slow trill that increased in tempo ('speed-up' songs). Birds replied at rates significantly above chance with their own double-buzz, or speed-up song match to the respective types of playback. The results suggest that birds who do not share true song types, can still song-match each other. This broad-sense form of song matching may also occur in populations with low song type sharing. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Geographic song discrimination in relation to dispersal distances in song sparrows

Whether geographic variation in signals actually affects communication between individuals depends on whether discriminable differences in signals occur over distances that individuals move in their lifetimes. We measure the ability of song sparrows (Melospiza melodia) to discriminate foreign from local songs using foreign songs recorded at a series of increasing distances and compare the results with previous measurements of dispersal distances. We test discrimination in males using playback of songs on territories and measuring approach and in females using playback to estradiol-treated captives and measuring courtship display. Females fail to discriminate against foreign songs recorded at 18 km but do discriminate against foreign songs recorded at 34, 68, 135, and 540 km. Males fail to discriminate against foreign songs recorded at 18, 34, 68, 135, and 270 km but do discriminate against foreign songs from 540 km. Females are more discriminating, but even they do not discriminate at a distance three times the root-mean-square dispersal distance, as estimated from mtDNA variation. We suggest that female preference for local songs benefits females not because it allows them to reject foreign males but because accurate production of local song serves as a test of song-learning ability.     

Female Lincoln's sparrows modulate their behavior in response to variation in male song quality

Sexually reproducing organisms should mate with the highest quality individuals that they can. When female songbirds choose a mate, they are thought to use several aspects of male song that reflect his quality. Under resource-limited environmental conditions, male Lincoln's sparrows (Melospiza lincolnii) vary among one another in several aspects of song quality, including song length, song complexity, and trill performance. In a 2-pronged approach, we tested whether variation in song quality of male Lincoln's sparrows influences the behavior of females that are in a reproductive-like state. Over two trials, we exposed females to songs from the high and low ends of the distribution of naturally occurring song quality variation and found a higher level of behavioral activity in females exposed to high-quality songs, especially when they had first been exposed to low-quality songs. We also examined female phonotaxis toward antiphonally played songs with experimentally elevated and reduced trill performance and found that females moved preferentially toward the songs with elevated trill performance. Contrary to most studies investigating the behavioral responses of wild, female songbirds to variation in male song, we obtained our results without administering exogenous estradiol, which can artificially perturb the female's physiology. Our results demonstrate that the behavior of female Lincoln's sparrows is modulated by the quality of male songs to which they are exposed and that trill performance plays a significant role in this behavioral modulation. Furthermore, as the order of song quality presentation matters, it appears that recent song experience also influences female behavior.     

Species song discrimination in adult female song and swamp sparrows

Six female song sparrows (Melospiza melodia) and six female swamp sparrows (Melospiza georgiana) were treated with oestradiol, and their response to song measured by frequency and intensity of copulation-solicitation display. Test stimuli were synthetic songs composed of either song sparrow or swamp sparrow syllables assembled in either song-sparrow-like or swamp-sparrow-like temporal patterns. Female song sparrows responded preferentially to songs containing their own species' syllables and to songs containing their own species' temporal patterns. Swamp sparrows were also sensitive to both syllable type and temporal, pattern, in contrast to male swamp sparrows, which show no preference for swamp sparrow temporal patterns.     

Stress,song and survival in sparrows

The stress response—increases in circulating glucocorticoids following a stressor—is typically considered adaptive, but few studies address the fitness consequences of individual variation in stress response. Generally, due to negative consequences of prolonged elevation of glucocorticoids, animals should have a transient stress response just sufficient to cope with the stressor. In rodents, stress responsiveness is affected by early developmental experience, and hyper-responsiveness to stress is linked to morbidity and mortality. We assessed individual variation in stress responses in free-living song sparrows, Melospiza melodia, in relation to fitness-related measures including song and overwinter survival. Birds with greater increases in corticosterone 30 min following restraint stress were less likely to return to breed the following year. Stress responsiveness was also correlated with song complexity: males with fewer syllables in their song repertoires had greater stress reactivity. Our findings support the hypothesis that developmental stressors both impair song development and affect the adult stress response. Thus, individual variation in the stress response may relate to variation in fitness.     

Seasonal changes in song nuclei and song behavior in Gambel's white-crowned sparrows

In males of several songbird species, the morphology of forebrain nuclei that control song changes seasonally. The only seasonally breeding songbird in which seasonal changes in the structure of song control nuclei have been reported not to occur is the nonmigratory Nuttall's subspecies of white-crowned sparrow. In the present study, we manipulated photoperiod and plasma testosterone concentrations in captive male white-crowned sparrows of the migratory Gambel's subspeices. Males exposed to photoperiods and plasma testosterone concentrations typical of those experienced by wild breeding males had larger song control nuclei than males held on a winter photoperiod. We also found seasonal change in stereotypy of spectral and temporal parameters of song in wild Gambel's white-crowned sparrows. We hypothesize that seasonal changes in song control nuclei may correlate with seasonal changes in song stereotypy. © 1995 John Wiley & Sons, Inc.     

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.     

Estimating the time to extinction in an island population of song sparrows

We estimated and modelled how uncertainties in stochastic population dynamics and biases in parameter estimates affect the accuracy of the projections of a small island population of song sparrows which was enumerated every spring for 24 years. The estimate of the density regulation in a theta-logistic model (theta = 1.09 suggests that the dynamics are nearly logistic, with specific growth rate r1 = 0.99 and carrying capacity K = 41.54. The song sparrow population was strongly influenced by demographic (ŝigma2(d) = 0.66) and environmental (ŝigma2(d) = 0.41) stochasticity. Bootstrap replicates of the different parameters revealed that the uncertainties in the estimates of the specific growth rate r1 and the density regulation theta were larger than the uncertainties in the environmental variance sigma2(e) and the carrying capacity K. We introduce the concept of the population prediction interval (PPI), which is a stochastic interval which includes the unknown population size with probability (1 - alpha). The width of the PPI increased rapidly with time because of uncertainties in the estimates of density regulation as well as demographic and environmental variance in the stochastic population dynamics. Accepting a 10% probability of extinction within 100 years, neglecting uncertainties in the parameters will lead to a 33% overestimation of the time it takes for the extinction barrier (population size X = 1) to be included into the PPI. This study shows that ignoring uncertainties in population dynamics produces a substantial underestimation of the extinction risk.     

Species song discrimination in choice experiments with territorial male swamp and song sparrows

Playbacks of synthetic and normal songs were used to determine what song parameters are important to species song recognition by territorial male swamp sparrows (Melospiza georgiana) and song sparrows (Melospiza melodia). Syllable morphology influences the discrimination of conspecific song from song sparrow song in adult swamp sparrows, but temporal pattern does not; this result duplicates that found in studies of song learning of the young in this species. Species song recognition is influenced by both syllable morphology and temporal pattern in adult song sparrows, in contrast to the situation in young sparrows, which seem not to distinguish their own species' song from that of swamp sparrows on either cue.     

Immediate and long-term effects of testosterone on song plasticity and learning in juvenile song sparrows

Steroid sex hormones play critical roles in the development of brain regions used for vocal learning. It has been suggested that puberty-induced increases in circulating testosterone (T) levels crystallize a bird's repertoire and inhibit future song learning. Previous studies show that early administration of T crystallizes song repertoires but have not addressed whether new songs can be learned after this premature crystallization. We brought 8 juvenile song sparrows (Melospiza melodia) into the laboratory in the late summer and implanted half of them with subcutaneous T pellets for a two week period in October. Birds treated with T tripled their singing rates and crystallized normal songs in 2 weeks. After T removal, subjects were tutored by 4 new adults. Birds previously treated with T tended toward learning fewer new songs post T, consistent with the hypothesis that T helps to close the song learning phase. However, one T-treated bird proceeded to learn several new songs in the spring, despite singing perfectly crystallized songs in the fall. His small crystallized fall repertoire and initial lag behind other subjects in song development suggest that this individual may have had limited early song learning experience. We conclude that an exposure to testosterone sufficient for crystallization of a normal song repertoire does not necessarily prevent future song learning and suggest that early social experiences might override the effects of hormones in closing song learning.     

Child maltreatment and the developing HPA axis

The developing HPA axis is under strong social regulation in infancy and early childhood and is vulnerable to perturbation in the absence of sensitive, responsive caregiving. Child maltreatment has complex, long-term influences both on basal cortisol levels and on HPA responsivity to pharmacological and psychological stressors, depending on current psychiatric status, current life adversity, age, and most likely, genetic factors. Among the more consistent findings, maltreated children with internalizing problems have elevated basal cortisol most often detected in early AM concentrations, whereas adults maltreated as children often exhibit low basal cortisol levels and elevated ACTH response to psychological stressors. To disentangle these complicated interactions, future research must take the above qualifiers into account, study the transition to puberty, explore the moderating role of candidate genes, and utilize animal models and pharmacological challenges, when ethical, to localize changes in the HPA axis. Post-institutionalized children may provide a model to separate early adverse care histories from current adversity.     

Testosterone induction of song in photosensitive and photorefractory male sparrows

Song in male songbirds is activated by the sex steroid testosterone (T). Using male song sparrows (Melospiza melodia), we compared effects of T in the normal spring state of photosensitivity (i.e., when the pituitary-gonadal axis is sensitive to stimulation by increasing daylength) and in the late summer-early fall state of photorefractoriness (i.e., when they are insensitive to increasing daylength). Photosensitive males experienced short days for 8 weeks and then long days for another 22 weeks to induce photorefractoriness. T implants were given to the birds twice, first when on short days and photosensitive, and second when on long days and photorefractory. Song rates were compared among 5 conditions: (1) photosensitive, short days, low T titers; (2) photosensitive, short days, high T titers; (3) photosensitive, long days, high T titers; (4) photorefractory, long days, low T titers; and (5) photorefractory, long days, high T titers. Plasma levels of T were monitored throughout the experiment by radioimmunoassay. T was equally effective in inducing song in both the photosensitive and photorefractory conditions. Thus, no seasonal change was found in the sensitivity to hormone action of the neural target sites mediating this behavior in song sparrows. Photosensitive birds sang at a higher rate when on long days than when on short days, however, even though there was no concomitant increase in plasma levels of T. This finding suggests that environmental factors can alter the expression of song activated by similar levels of T.     

Seasonal changes in intrinsic electrophysiological activity of song control neurons in wild song sparrows

Song behavior and its underlying neural substrate can change seasonally in adult songbirds. To test whether environmental cues induce seasonal changes in electrophysiological characteristics of song control neurons, we measured in vitro intrinsic neuronal activity in the song control nucleus RA of adult male song sparrows (Melospiza melodia) in both the fall non-breeding and spring breeding seasons. We found that RA neurons in spring-captured birds show a more than threefold increase in spontaneous firing rate compared to those from fall-captured birds. We conclude that environmental cues are sufficient to induce seasonal changes in electrophysiological properties of song control neurons, and that changes in these properties may underlie seasonal changes in song behavior.     

Spatial movements and social networks in juvenile male song sparrows

The time between fledging and breeding is a critical period in songbird ontogeny, but the behavior of young songbirds in the wild is relatively unstudied. The types of social relationships juveniles form with other individuals can provide insight into the process through which they learn complex behaviors crucial for survival, territory establishment, and mate attraction. We used radio telemetry to observe social associations of young male song sparrows (Melospiza melodia) from May to November. Juvenile song sparrows were frequently observed in social flocks and generally associated with more birds in the summer than in the autumn months. Most juvenile subjects formed stable social relationships with other birds and were seen with the same individual on up to 60% of the days observed. The strongest associations occurred with other juvenile males, and these individuals were often seen <1 m from the subject, even when the subject moved large distances between tracking observations. Associations also had long-term behavioral consequences as subjects were more likely to establish territories near their associates and learn shared song types. Our results indicate that male song sparrows spend a large percentage of the juvenile life stage forming social relationships and suggest that these associations may be important for the ecology of young birds and the ontogeny of their behaviors.     

Fitness correlates of song repertoire size in free-living song sparrows (Melospiza melodia)

Models of sexual selection propose that exaggerated secondary sexual ornaments indicate a male's own fitness and the fitness of his offspring. These hypotheses have rarely been thoroughly tested in free-living individuals because overall fitness, as opposed to fitness components, is difficult to measure. We used 20 years of data from song sparrows (Melospiza melodia) inhabiting Mandarte Island, British Columbia, Canada, to test whether a male's song repertoire size, a secondary sexual trait, predicted overall measures of male or offspring fitness. Males with larger song repertoires contributed more independent and recruited offspring, and independent and recruited grandoffspring, to Mandarte's population. This was because these males lived longer and reared a greater proportion of hatched chicks to independence from parental care, not because females mated to males with larger repertoires laid or hatched more eggs. Furthermore, independent offspring of males with larger repertoires were more likely to recruit and then to leave more grandoffspring than were offspring of males with small repertoires. Although we cannot distinguish whether observed fitness variation reflected genetic or environmental effects on males or their offspring, these data suggest that female song sparrows would gain immediate and intergenerational fitness benefits by pairing with males with large song repertoires.