skip to main content


The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 11:00 PM ET on Thursday, June 13 until 2:00 AM ET on Friday, June 14 due to maintenance. We apologize for the inconvenience.

Title: Variation in Hematological Indices, Oxidative Stress, and Immune Function Among Male Song Sparrows From Rural and Low-Density Urban Habitats
A central theme in the field of ecology is understanding how environmental variables influence a species’ distribution. In the last 20 years, there has been particular attention given to understanding adaptive physiological traits that allow some species to persist in urban environments. However, there is no clear consensus on how urbanization influences physiology, and it is unclear whether physiological differences in urban birds are directly linked to adverse outcomes or are representative of urban birds adaptively responding to novel environmental variables. Moreover, though low-density suburban development is the fastest advancing form of urbanization, most studies have focused on animals inhabiting high intensity urban habitats. In this study, we measured a suite of physiological variables that reflect condition and immune function in male song sparrows ( Melospiza melodia ) from rural and suburban habitats. Specifically, we measured hematological indices [packed cell volume (PCV), hemoglobin concentration, mean corpuscular hemoglobin concentration (MCHC)], circulating glutathione (total, reduced, and oxidized), oxidative damage (d-ROM concentration), antioxidant capacity, and components of the innate immune system [bacteria killing ability (BKA), white blood cell counts]. We also measured whole-animal indices of health, including body condition (scaled mass index length) and furcular fat. Song sparrows inhabiting suburban environments exhibited lower hemoglobin and MCHC, but higher body condition and furcular fat scores. Additionally, suburban birds had higher heterophil counts and lower lymphocyte counts, but there were no differences in heterophil:lymphocyte ratio or BKA between suburban and rural birds. PCV, glutathione concentrations, and oxidative damage did not differ between suburban and rural sparrows. Overall, suburban birds did not exhibit physiological responses suggestive of adverse outcomes. Rather, there is some evidence that sparrows from rural and suburban habitats exhibit phenotypic differences in energy storage and metabolic demand, which may be related to behavioral differences previously observed in sparrows from these populations. Furthermore, this study highlights the need for measuring multiple markers of physiology across different types of urban development to accurately assess the effects of urbanization on wildlife.  more » « less
Award ID(s):
Author(s) / Creator(s):
; ; ; ; ;
Date Published:
Journal Name:
Frontiers in Ecology and Evolution
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Human activity around the globe is a growing source of selection pressure on animal behavior and communication systems. Some animals can modify their vocalizations to avoid masking from anthropogenic noise. However, such modifications can also affect the salience of these vocalizations in functional contexts such as competition and mate choice. Such is the case in the well-studied Nuttall's white-crowned sparrow ( Zonotrichia leucophrys nuttalli ), which lives year-round in both urban San Francisco and nearby rural Point Reyes. A performance feature of this species' song is salient in territorial defense, such that higher performance songs elicit stronger responses in simulated territorial intrusions; but songs with lower performance values transmit better in anthropogenic noise. A key question then is whether vocal performance signals male quality and ability to obtain high quality territories in urban populations. We predicted white-crowned sparrows with higher vocal performance will be in better condition and will tend to hold territories with lower noise levels and more species-preferred landscape features. Because white-crowned sparrows are adapted to coastal scrub habitats, we expect high quality territories to contain lower and less dense canopies, less drought, more greenness, and more flat open ground for foraging. To test our predictions, we recorded songs and measured vocal performance and body condition (scaled mass index and fat score) for a set of urban and rural birds ( N = 93), as well as ambient noise levels on their territories. Remote sensing metrics measured landscape features of territories, such as drought stress (NDWI), greenness (NDVI), mean canopy height, maximum height, leaf area density (understory and canopy), slope, and percent bare ground for a 50 m radius on each male territory. We did not find a correlation between body condition and performance but did find a relationship between noise levels and performance. Further, high performers held territories with lower canopies and less dense vegetation, which are species-preferred landscape features. These findings link together fundamental aspects of sexual selection in that habitat quality and the quality of sexually selected signals appear to be associated: males that have the highest performing songs are defending territories of the highest quality. 
    more » « less
  2. Abstract

    The concept of a pace‐of‐life syndrome describes inter‐ and intraspecific variation in several life‐history traits along a slow‐to‐fast pace‐of‐life continuum, with long lifespans, low reproductive and metabolic rates, and elevated somatic defences at the slow end of the continuum and the opposite traits at the fast end. Pace‐of‐life can vary in relation to local environmental conditions (e.g. latitude, altitude), and here we propose that this variation may also occur along an anthropogenically modified environmental gradient. Based on a body of literature supporting the idea that city birds have longer lifespans, we predict that urban birds have a slower pace‐of‐life compared to rural birds and thus invest more in self maintenance and less in annual reproduction. Our statistical meta‐analysis of two key traits related to pace‐of‐life, survival and breeding investment (clutch size), indicated that urban birds generally have higher survival, but smaller clutch sizes. The latter finding (smaller clutches in urban habitats) seemed to be mainly a characteristic of smaller passerines. We also reviewed urbanization studies on other traits that can be associated with pace‐of‐life and are related to either reproductive investment or self‐maintenance. Though sample sizes were generally too small to conduct formal meta‐analyses, published literature suggests that urban birds tend to produce lower‐quality sexual signals and invest more in offspring care. The latter finding is in agreement with the adult survival hypothesis, proposing that higher adult survival prospects favour investment in fewer offspring per year. According to our hypothesis, differences in age structure should arise between urban and rural populations, providing a novel alternative explanation for physiological differences and earlier breeding. We encourage more research investigating how telomere dynamics, immune defences, antioxidants and oxidative damage in different tissues vary along the urbanization gradient, and suggest that applying pace‐of‐life framework to studies of variation in physiological traits along the urbanization gradient might be the next direction to improve our understanding of urbanization as an evolutionary process.

    more » « less
  3. Abstract

    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 toward 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.

    more » « less
  4. Abstract

    In many taxa, melanin-based coloration is a signal of dominance or fighting ability and is associated with concentrations of hormones that may mediate aggressive behavior. Previous studies found that experimental manipulation of melanin-based signals can result in manipulated individuals receiving more social challenges in some but not all species. These differences could arise from mismatches between the signal, behavior, and hormone concentrations. In the present study, we experimentally manipulated the chest spotting of urban and rural male song sparrows (Melospiza melodia) following an assessment of their territorial aggression and initial concentrations of corticosterone and testosterone and then assessed their behavior and hormone concentrations 2 weeks later. We found that males generally displayed less territorial aggression in the second trial, consistent with our previous findings. Males in the enlarged treatment decreased aggression to a greater degree than those in the reduced treatment. The effect of the plumage manipulation was similar across the rural and urban habitats. Despite the changes in behavior we detected, we found no effects of the manipulation on concentrations of testosterone or corticosterone. Our results show that melanin-based spotting in male song sparrows is a signal of territorial aggression but the physiological mechanisms that mediate the relationships between chest spotting and behavior remain to be identified.

    Significance statement

    Many bird species use their plumage to signal their dominance status, fighting ability, or motivation during interactions with other individuals to resolve conflicts without a fight. Here, we asked whether chest spotting is a signal in territorial interactions among male song sparrows. We experimentally increased or reduced the extent of spotting in males and measured the change in their aggression. We found that reduced-spotting males showed a more moderate seasonal decrease of aggression compared to males with enlarged spotting reduced aggression, possibly because the former experienced more intrusions later on in the breeding season while the latter experienced fewer intrusions. These results are consistent with chest spotting size in song sparrows functioning as a signal of territory holding potential of the bearer.

    more » « less
  5. Abstract Urbanization is one of the most extreme forms of land transformation and results in changes to ecosystems and species compositions. As a result, there are strong directional selection pressures compared to nearby rural areas. Despite a surge in research on the different selection pressures on acoustic communication in urban and rural areas, there has been comparatively little investigation into traits involved with visual communication. We measured the plumage of museum specimens of white-crowned sparrows (Zonotrichia leucophrys) from urban and adjacent rural habitats in San Francisco, CA, to assess the effects of divergent habitats on plumage. We found significant differences in dorsal plumage, but not crown plumage, between urban and rural populations that have been diverging over the past 100 years. Urban birds have increasingly darker and duller dorsal plumage, whereas rural birds in adjacent areas have plumage with richer hues and more color complexity. Our findings suggest a newly observed adaptation to urban environments by native species and suggest that many traits, in addition to acoustic signals, may be changing in response to urban selection pressures. Additional collections in urban areas are needed to explore likely divergences in plumage coloration between urban and rural environments. 
    more » « less