Urban and rural male song sparrows (Melospiza melodia) differ in territorial aggression and activation of vasotocin neurons in response to song challenge.

When living in urban habitats, 'urban adapter' species often show greater aggression toward conspecifics, yet we do not understand the mechanisms underlying this behavioral shift. The neuroendocrine system regulates socio-sexual behaviors including aggression and thus could mediate behavioral responses to urbanization. Indeed, urban male song sparrows (Melospiza melodia), which are more territorially aggressive, also have greater abundance of the neuropeptide arginine vasotocin (AVT) in nodes of the brain social behavior network. Higher abundance of AVT could reflect long-term synthesis that underlies baseline territoriality or short-term changes that regulate aggression in response to social challenge. To begin to resolve the timeframe over which the AVT system contributes to habitat differences in aggression we used immediate early gene co-expression as a measure of the activation of AVT neurons. We compared Fos induction in AVT-immunoreactive neurons of the bed nucleus of the stria terminalis (BSTm) and paraventricular nucleus of the hypothalamus (PVN) between urban and rural male song sparrows in response to a short (< 5 min.) or long (> 30 min.) song playback to simulate territorial intrusion by another male. We found that urban males had a higher proportion of Fos-positive AVT neurons in both brain regions compared to rural males, regardless of the duration of song playback. Our results suggest that AVT neurons remain activated in urban males, independently of the duration of social challenge. These findings that Fos induction in AVT neurons differs between rural and urban male song sparrows further implicate this system in regulating behavioral responses to urbanization.

Hypothalamic-pituitary-adrenal axis regulation and organization in urban and rural song sparrows.

Urban habitats present animals with persistent disturbances and acute stressors not present in rural habitats or present at significantly lower levels. Differences in the glucocorticoid stress response could underlie colonization of these novel habitats. Despite urban habitats characterization as more stressful, previous comparisons of urban and rural birds have failed to find consistent differences in baseline and stress induced glucocorticoid levels. Another aspect of glucocorticoid regulation that could underlie an animal's ability to inhabit novel habitats, but has yet to be well examined, is more efficient termination of the glucocorticoid stress response which would allow birds in urban habitats to recover more quickly after a disturbance. The glucocorticoid stress response is terminated by negative feedback achieved primarily through their binding of receptors in the hippocampus and hypothalamus and subsequent decreased synthesis and release from the adrenals. We investigated if male song sparrows (Melospiza melodia) in urban habitats show more efficient termination of the glucocorticoid stress response than their rural counterparts using two approaches. First, we measured glucocorticoid receptor, mineralocorticoid receptor and 11ß-HSD2 (an enzyme that inactivates corticosterone) mRNA expression in negative feedback targets of the brain (the hippocampus and hypothalamus) as a proxy measure of sensitivity to negative feedback. Second, we measured plasma corticosterone levels after standardized restraint and again following a challenge with the synthetic glucocorticoid, dexamethasone, as a means of assessing how quickly birds decreased glucocorticoid synthesis and release. Though there were no differences in the hypothalamus of urban and rural song sparrows, urban birds had lower glucocorticoid receptor and 11ß-HSD2 mRNA expression in the hippocampus. Further, urban and rural birds had similar reductions in corticosterone following the dexamethasone challenge, suggesting that they do not differ in how quickly they decrease glucocorticoid synthesis and release. Thus, urban and rural song sparrows display similar termination of the glucocorticoid stress response even though urban birds have decreased hippocampal glucocorticoid receptor and 11ß-HSD2 abundance.

Male zebra finches exposed to lead (Pb) during development have reduced volume of song nuclei, altered sexual traits, and received less attention from females as adults.

Lead (Pb) is a pervasive global contaminant that interferes with sensitive windows for neurological development and causes oxidative damage to tissues. The effects of moderate and high exposure to Pb have been well-studied in birds, but whether low-level early-life exposure to Pb influences adult phenotype remains unclear. Female songbirds use a male's song and coloration to discriminate between high- and low-quality males. Therefore, if early-life exposure to Pb disrupts song learning ability or shifts the allocation of antioxidant pigments away from colorful secondary sexual traits, male birds exposed to Pb may be less attractive to females. We exposed developing zebra finches (Taeniopygia guttata) to Pb-contaminated drinking water (100 or 1000 parts per billion [ppb]) after hatching (days 0-100). Once male finches reached adulthood (120-150 days post hatch), we measured song learning ability, coloration of bill and cheek patches, and volume of song nuclei in the brain. We also measured female preference for Pb-exposed males relative to control males. Finally, we measured motoric and spatial cognitive performance in male and female finches to assess whether cognitive traits differed in their sensitivity to Pb exposure. Male zebra finches exposed to 1000 ppb Pb had impaired song learning ability, reduced volume of song nuclei, bills with less redness and received less attention from females. Additionally, Pb exposure impaired motoric performance in both male and female finches but did not affect performance in a spatial cognitive task. Adult finches exposed to Pb-contaminated water had higher blood-Pb levels, though in all cases blood-Pb levels were below 7.0 µg dL-1. This study suggests that low-level exposure to Pb contributes to cognitive deficits that persist into adulthood and may indirectly influence fitness by altering secondary sexual traits and reducing male attractiveness.

What About Females? Urban Female Song Sparrows Elevate Aggressive Signaling Compared to Rural.

The costs and benefits of breeding behaviors are influenced by environmental conditions, and habitat variation can shift the degree to which behaviors are expressed. Novel urban habitats have been shown to differ significantly in disturbances such as noise, light at night, and human presence, as well as resource availability, compared to rural habitats. Perhaps because of these environmental differences, urban males of several species are consistently more aggressive than rural males, raising the hypothesis that greater territorial aggression is beneficial in urban habitats. Though often ignored, female songbirds of many species also perform aggressive territorial behaviors towards conspecifics during the breeding season. For socially monogamous songbirds, this aggression functions to ensure partner fidelity and secure resources for reproduction. Studies of the effects of urbanization on songbird behavior have yet to determine if urban females also express greater territorial aggression. Importantly, energetically demanding behaviors such as territoriality and parental care should constrain one another, leading to behavioral trade-offs during the breeding season. Though territorial aggression and parental care are inversely related in males of several species of songbird, this relationship is understudied in female songbirds, particularly those facing environmental change such as urbanization. In this study, we compared aggressive signaling and a measure of parental care (maternal nest visitation rates) between female song sparrows (Melospiza melodia), living in urban and rural habitats. We hypothesized that female aggressive signaling would be higher in urban environments compared to rural, and negatively correlated with maternal visitation rates. We found that urban females, like males, expressed increased aggressive signaling compared to rural. However, female aggressive signaling was not related to our measure of maternal care, suggesting females aren't facing a trade-off between these two behaviors. Collectively, our results are consistent with the hypothesis that urban habitats promote territorial aggression in female song sparrows. As urbanization continues to spread, understanding the behavioral changes animals employ in urban environments requires studying individuals of different sexes and age classes, and will help us understand how some species are able to cope with human induced rapid environmental change.

Effects of low-density urbanization on genetic structure in the Song Sparrow.

Urbanization fragments landscapes and can impede the movement of organisms through their environment, which can decrease population connectivity. Reduction in connectivity influences gene flow and allele frequencies, and can lead to a reduction in genetic diversity and the fixation of certain alleles, with potential negative effects for populations. Previous studies have detected effects of urbanization on genetic diversity and structure in terrestrial animals living in landscapes that vary in their degree of urbanization, even over very short distances. We investigated the effects of low-intensity urbanization on genetic diversity and genetic structure in Song Sparrows (Melospiza melodia). We captured 208 Song Sparrows at seven sites along a gradient of urbanization in and around Blacksburg, VA, USA, then genotyped them using a panel of fifteen polymorphic microsatellite loci. We found that genetic diversity was comparable among the seven study sites, and there was no evidence of genetic structuring among sites. These findings suggest that over a gradient of urbanization characterized by low density urban development, Song Sparrows likely exist in a single panmictic population.