Scott A. MacDougall-Shackleton

Auditory scene analysis by songbirds: stream segregation of birdsong by European starlings (Sturnus vulgaris).

Three experiments examined the capacity of European starlings to segregate perceptually 2 superimposed, intermixed auditory stimuli. The stimuli were 10-s song samples from 2 of 4 songbird species: European starling, brown thrasher, mockingbird, and nightingale. The birds first learned a discrimination between the intermixed song pairs. Then, they maintained the discrimination with novel song exemplars in the mixtures and when song stimuli for each species were presented alone. Performance fell, but remained above chance, when song pairs were mixed with the dawn chorus of bird song. The results show that starlings were identifying the songs of individual species within the baseline superimposed song pairs, a process of auditory stream segregation and scene analysis (A. S. Bregman, 1990).

Auditory scene analysis by European starlings (Sturnus vulgaris): Perceptual segregation of tone sequences

Like humans, animals that use acoustic stimuli to perceive their world ought to be able to parse the auditory scene into functionally significant sounds. The ability to do so ought to have significant adaptive value when, for example, an animal can identify the sounds of a predator among other natural noises. In earlier work it was shown that a species of songbird, the European starling, can identify excerpts of both its own song and songs from other avian species when the songs are mixed concurrently with other natural signals. In this experiment it is demonstrated that starlings can segregate two synthetic pure-tone sequences when the sequences differ in frequency. Taken together, the experiments show that at least one nonhuman species is capable of auditory scene analysis both for natural and for non-natural acoustic stimuli. This suggests in turn that auditory scene analysis may be a general perceptual process that occurs in many species that make use of acoustic information.

Do stable isotopes reflect nutritional stress? Results from a laboratory experiment on song sparrows

Stable isotope analysis is an increasingly valuable tool in ecological studies and shows promise as a measure of nutritional stress in wild animals. Thus far, however, the only studies on endotherms that have conclusively shown changes in δ15N and δ13C values in response to nutritional stress were conducted on fasting animals and animals growing under extreme levels of food restriction. We conducted a laboratory experiment to test whether δ15N and δ13C values provide a general index of nutritional stress. We compared the isotopic composition of whole blood, liver, muscle and feathers between two groups of juvenile song sparrows (Melospiza melodia) hand-reared in captivity under identical conditions except for feeding regime. To verify that our experimental treatment induced a biologically meaningful level of nutritional stress, we simultaneously measured the effects on physiology, growth and development at multiple scales. While food-restricted birds were physiologically stressed, physically smaller, and showed poorer growth and brain development compared to ad libitum-fed birds, there was no effect of feeding regime on either δ15N or δ13C values in any tissue. Instead of a continuum where the level of change in 15N or 13C contents corresponds to the level of nutritional stress, we suggest there may be a threshold level of nutritional stress below which such isotopic changes are likely to be negligible.

Early nutritional stress impairs development of a song-control brain region in both male and female juvenile song sparrows (Melospiza melodia) at the onset of song learning

Birdsong is a sexually selected trait and is often viewed as an indicator of male quality. The developmental stress hypothesis proposes a model by which song could be an indicator; the time during early development, when birds learn complex songs and/or local variants of song, is of rapid development and nutritional stress. Birds that cope best with this stress may better learn to produce the most effective songs. The developmental stress hypothesis predicts that early food restriction should impair development of song-control brain regions at the onset of song learning. We examined the effect of food restriction on song-control brain regions in fledgling (both sexes, 23–26 days old) song sparrows (Melospiza melodia). Food restriction selectively reduced HVC volume in both sexes. In addition, sex differences were evident in all three song-control regions. This study lends further support to a growing body of literature documenting a variety of behavioural, physiological and neural detriments in several songbird species resulting from early developmental stress.

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.

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.

Sexual Selection and the Evolution of Song Repertoires

Bird song is an acoustic ornament. That is, bird song is a conspicuous, elaborate trait with no apparent survival value. Thus, along with long tails and showy plumage, bird song has been extensively studied as a model of avian sexual selection. There has now accumulated much experimental evidence, from both field and laboratory studies, that song functions to attract mates and to repel competitors from territories (Kroodsma and Byers, 1991; Searcy and Andersson, 1986). One of the most conspicuous and elaborate aspects of bird song is its extreme complexity and variety. Individuals of many species of birds sing multiple variants of their species-typical songs; that is, they possess song repertoires. Large song repertoires are the acoustic analogue of a peacock’s tail. Because songs are so showy and seem so redundant, much research has been devoted to describing song repertoires and patterns of singing behavior. Similarly, many researchers have hypothesized ways in which sexual selection may favor birds that have larger song repertoires. The purposes of this paper are to (1) review the distribution of song repertoires in passerine birds and (2) review the numerous hypotheses that have been proposed to account for the evolution of song repertoires.

Corticosterone and dehydroepiandrosterone have opposing effects on adult neuroplasticity in the avian song control system

Chronic elevations in glucocorticoids can decrease the production and survival of new cells in the adult brain. In rat hippocampus, supraphysiological doses of dehydroepiandrosterone (DHEA; a sex steroid precursor synthesized in the gonads, adrenals, and brain) have antiglucocorticoid properties. With male song sparrows (Melospiza melodia), we examined the effects of physiological doses of corticosterone, the primary circulating glucocorticoid in birds, and DHEA on adult neuroplasticity. We treated four groups of nonbreeding sparrows for 28 days with empty (control), corticosterone, DHEA, or corticosterone + DHEA implants. Subjects were injected with BrdU on days 3 and 4. In HVC, a critical song control nucleus, corticosterone and DHEA had independent, additive effects. Corticosterone decreased, whereas DHEA increased, HVC volume, NeuN+ cell number, and BrdU+ cell number. Coadministration of DHEA completely reversed the neurodegenerative effects of chronic corticosterone treatment. In an efferent target of HVC, the robust nucleus of the arcopallium (RA), DHEA increased RA volume, but this effect was blocked by coadministration of corticosterone. There were similar antagonistic interactions between corticosterone and DHEA on BrdU+ cell number in the hippocampus and ventricular zone. This is the first report on the effects of corticosterone treatment on the adult song control circuit, and HVC was the most corticosterone‐sensitive song nucleus examined. In HVC, DHEA is neuroprotective and counteracts several pronounced effects of corticosterone. Within brain regions that are particularly vulnerable to corticosterone, such as the songbird HVC and rat hippocampus, DHEA appears to be a potent native antiglucocorticoid. J. Comp. Neurol. 518:3662–3678, 2010.

Immediate early gene expression following exposure to acoustic and visual components of courtship in zebra finches.

Sensory driven immediate early gene expression (IEG) has been a key tool to explore auditory perceptual areas in the avian brain. Most work on IEG expression in songbirds such as zebra finches has focused on playback of acoustic stimuli and its effect on auditory processing areas such as caudal medial mesopallium (CMM) caudal medial nidopallium (NCM). However, in a natural setting, the courtship displays of songbirds (including zebra finches) include visual as well as acoustic components. To determine whether the visual stimulus of a courting male modifies song-induced expression of the IEG ZENK in the auditory forebrain we exposed male and female zebra finches to acoustic (song) and visual (dancing) components of courtship. Birds were played digital movies with either combined audio and video, audio only, video only, or neither audio nor video (control). We found significantly increased levels of Zenk response in the auditory region CMM in the two treatment groups exposed to acoustic stimuli compared to the control group. The video only group had an intermediate response, suggesting potential effect of visual input on activity in these auditory brain regions. Finally, we unexpectedly found a lateralization of Zenk response that was independent of sex, brain region, or treatment condition, such that Zenk immunoreactivity was consistently higher in the left hemisphere than in the right and the majority of individual birds were left-hemisphere dominant.

Developmental stress has sex-specific effects on nestling growth and adult metabolic rates but no effect on adult body size or body composition in song sparrows

SUMMARY Variation in the prenatal and postnatal environments can have long-term effects on adult phenotype. In humans and other animals, exposure to stressors can lead to long-term changes in physiology. These changes may predispose individuals to disease, especially disorders involving energy metabolism. In addition, by permanently altering metabolic rates and energy requirements, such effects could have important fitness consequences. We determined the effects of early-life food restriction and corticosterone (CORT) treatment on growth and adult body size, body composition (assessed via quantitative magnetic resonance) and metabolic rates in the song sparrow, Melospiza melodia. Nestlings were hand-raised in captivity from 3 days of age. Treatments (ad libitum food, food restriction or CORT treatment) lasted from day 7 to day 60. Both experimental treatments had sex-specific effects on growth. In the nestling period, CORT-treated males weighed more than controls, whereas CORT-treated females weighed less than controls. Food-restricted males weighed the same as controls, whereas food-restricted females weighed less than controls. Both experimental treatments also had sex-specific effects on standard metabolic rate (SMR). Females exposed to food restriction or CORT treatment during development had higher SMRs in adulthood than control females, but neither stressor affected SMR in males. There were no effects of either treatment on adult body size, body composition (lean or fat mass) or peak metabolic rate. Therefore, early-life stress may have sex-specific programming effects on metabolic rates and energy expenditure in song sparrows. In addition, both treatments affected nestling growth in a manner that exaggerated the typical sex difference in nestling mass, which could provide male nestlings with a competitive advantage over their sisters when developing in a poor-quality environment.