ReviewHormones in the city: Endocrine ecology of urban birds
Highlights
► Urban habitat presents novel challenges to organisms all across the globe. ► This review describes findings of studies of the endocrine ecology of urban birds. ► Numerous endocrine effects associated with urban habitat have been described. ► However, clear, consistent patterns have not yet been revealed. ► With more rigorous approaches, future work will provide important advances.
Introduction
Somewhat paradoxically, when we look at coarse geographic scales across the globe, human population density and species richness are positively associated with each other (Balmford et al., 2001, Evans and Gaston, 2005, Hunter and Yonzon, 1993, Pautasso, 2007, Vazquez and Gaston, 2006). This positive correlation is unlikely to be driven by a positive influence of urbanization on biodiversity, but by a tendency for human populations to occur at high densities in areas with high primary productivity that are also biodiverse (Evans and Gaston, 2005, Pautasso, 2007). Instead, urbanization almost uniformly reduces vertebrate species richness (Cam et al., 2000, McKinney, 2002, McKinney, 2008). And so, with expanding urbanization in biodiverse regions of the globe, an increasing number of species will confront the challenge of urbanization, and many will not persist in the face of this challenge.
The modern form of the field of urban ecology originated in the 1970s (Sukopp et al., 2008). The work of urban ecologists has been aimed at understanding how climate, biogeochemical cycles, ecosystems, and organisms respond to urbanization (Arnfield, 2003, Beissinger and Osborne, 1982, Kalnay and Cai, 2003, Kaye et al., 2006, Marzluff and Neatherlin, 2006, McKinney, 2006). We have learned much from this previous work, but we still have very little understanding of the mechanisms that underlie species and ecosystem responses to urbanization (Marzluff, 2001, Rodewald and Shustack, 2008, Shochat et al., 2006).
As an area is converted from natural to urban habitat, a number of environmental characteristics change. Habitat structure and resource availability are altered: food might become more available for species that are able to exploit anthropogenic food sources, and for predatory species with more abundant prey in cities (e.g., peregrine falcons, Falco peregrinus, that hunt rock pigeons, Columba livia) (Chace and Walsh, 2006, Fedriani et al., 2001, Marzluff and Neatherlin, 2006). In contrast, for many other species, such as insectivores and many other foraging specialists, food might become less abundant (Chace and Walsh, 2006, McKinney, 2002). For species reliant on native vegetation, suitable habitat might be limited or nonexistent in cities, whereas for species that can use human-made structures and exotic flora, suitable habitat becomes more abundant (Chace and Walsh, 2006, McKinney, 2002). Water availability changes—in some cases, such as cities in a desert habitat matrix, water becomes more available (Faeth et al., 2005), whereas, in other settings, water can become more scarce in cities dominated by impervious surfaces that promote runoff (Arnfield, 2003, Arnold and Gibbons, 1996). Temperatures can increase and stabilize because of heat-island effects of cities (Arnfield, 2003), but also, because of increased availability of shade and shelter, high temperatures and inclement weather might be more readily avoided. Species interactions likely change because of increased densities of domestic, feral, and invasive species as well as changing densities and diversity of native species (Marzluff and Neatherlin, 2006, McKinney, 2006). These changes could lead to increased or decreased predation and competition (Byers, 2002, Gering and Blair, 1999, McKinney, 2006, Ryder et al., 2010).
Despite the complexities of the impacts of urbanization, clear patterns of response do emerge. Vertebrate species richness declines and biotas become more homogeneous (McKinney, 2006, McKinney, 2008). Avian studies comprise the majority of the urban ecology literature, revealing several apparently generalized responses to urbanization. Across the globe, birds found commonly breeding in cities have broader environmental tolerance than closely-related species that do not breed in cities (Bonier et al., 2007b). Generalist species tend to fare better than specialists (Evans et al., 2011). Across 12 European cities (Maklakov et al., 2011) and in one South American city (Carrete and Tella, 2011), birds that successfully colonize urban habitat have larger relative brain sizes than birds that appear to avoid urban areas (but see Evans et al., 2011, Kark et al., 2007). Native birds that persist in cities often do so at lower densities than that at which they are found at in natural habitat (Marzluff, 2001, Mills et al., 1989). In contrast, several avian species, such as American crows (Corvus brachyrhynchos), house sparrows (Passer domesticus), European starlings (Sturnus vulgaris), and rock pigeons, generally increase their densities in response to urbanization all across the globe (Chace and Walsh, 2006, Marzluff, 2001, Marzluff and Neatherlin, 2006, McKinney, 2002, Mills et al., 1989). Such contrasting responses to urbanization prompted urban ecologists to adopt the terms urban avoider, urban adapter, and urban exploiter to categorize species that respectively are absent from, persist in, and thrive in cities (Blair, 1996, McKinney, 2002).
Clearly, urbanization dramatically changes the landscape, and, in order to respond to those changes, whether they represent challenges or opportunities, an animal must react to them physiologically and behaviorally. The endocrine system is a primary candidate for playing a role in mediating an organism's physiological and behavioral responses to novel environments (Table 1), a fact recognized by several biologists who have sought to characterize differences in endocrine function between urban and nonurban populations (e.g., Bonier et al., 2007a, Fokidis et al., 2009, French et al., 2008, Partecke et al., 2006, Schoech et al., 2007).
Only in the past decade have biologists turned to field endocrine methods to elucidate physiological responses to urban habitat, and the majority of these urban endocrine ecology studies have focused on birds. Birds are ideal subjects for such studies, because of the strong foundation of both field endocrine and urban ecological studies in birds that provide validated methods and reference data for explorations of avian endocrinology in cities (Marzluff et al., 2001, Wingfield and Farner, 1976).
The vast majority of the urban endocrine literature has focused on effects on two central endocrine axes, the hypothalamic–pituitary–adrenal (HPA) axis and the hypothalamic–pituitary–gonadal (HPG) axis. These axes are responsible, respectively, for maintaining energetic balance in the face of shifting metabolic demands and for regulating reproduction (Adkins-Regan, 2005, Sapolsky et al., 2000). Specifically, most work has focused on measuring circulating concentrations of glucocorticoid hormones, one of the final products of activation of the HPA axis, or concentrations of the reproductive steroids secreted following activation of the HPG axis, most often estradiol and testosterone. This focus follows from an interest in understanding 1) how animals respond to and cope with the novel challenges associated with urbanization (e.g., Bonier et al., 2007a, Partecke et al., 2006), a process likely mediated in part by the HPA axis, and 2) how regulation of reproduction differs in urban populations that are often characterized by earlier onset and extended periods of breeding (e.g., Partecke et al., 2004, Schoech et al., 2004).
This previous work allows us to assess patterns of variation in endocrine traits associated with urban habitat in birds. Here, I review what the past decade of studies of the endocrine ecology of urban birds has revealed. Based on this review, I make recommendations for future work, describing unanswered questions and proposing strong approaches to address these questions.
Section snippets
Is allostatic load different in urban birds?
The urban endocrine ecology literature is dominated by studies involving measurement of glucocorticoid hormones (Table 2). Many of these studies propose to measure glucocorticoid (hereafter, cort) levels in an effort to test a process hypothesis related to the functional role of the hypothalamic–pituitary–adrenal (HPA) axis in mediating responses to urbanization (e.g., Partecke et al., 2006), but, to date, very few studies have experimentally manipulated either hormone levels or environmental
Recommendations for future directions in urban endocrine ecology
Given that the nascent field of urban endocrine ecology has not yet revealed any strong, consistent patterns, we must reconsider our approach and the sorts of questions that we might be able to address with field endocrine methods. Below, I suggest approaches to future field endocrine ecology studies of urban birds that might be productive.
Conclusions
The current urban endocrine ecology literature does not reveal any consistent patterns, but has demonstrated that populations of birds in urban habitat often exhibit differences in endocrine traits, particularly hormone concentrations, when compared to conspecifics in nonurban habitat. With rigorous approaches involving careful selection of study sites and subjects, quantification of ecological characteristics, control for life history, and replication across cities and species in future
Acknowledgments
I would like to thank P. R. Martin for discussions and advice, E. Dobson for assistance with literature searching, Z. M. Benowitz-Fredericks, R. Montgomerie, W. Goymann, and two anonymous referees for comments on earlier versions of the manuscript, and J. Atwell, E. Ketterson, and H. B. Fokidis for access to manuscripts in review and in press. A Banting Postdoctoral Fellowship from the National Sciences and Engineering Research Council of Canada provided financial support.
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