Growing in a city: Consequences on body size and plumage quality in an urban dweller, the house sparrow (Passer domesticus)

Highlights

• Juvenile and adult sparrows were captured at 30 sites that differ in urbanization rates.

• Body size and plumage quality were negatively correlated with urbanization.

• The impact of urbanization on feather quality was only observed in juveniles.

• Urban environments energetically constrain sparrows during their development only.

Abstract

In urban environments, wild vertebrates have to adjust to new environmental challenges (e.g., modified resource availability, increased chemical, noise and light pollutions). However, while the pace of urbanization is constantly increasing, little is known about the ultimate consequences of urban life on the condition of free-living organisms during different life-history stages. In this study, we investigated the influence of urbanization on the condition and non-ornamental feather quality in a common wild bird species, the House sparrow (Passer domesticus). Using a national network of trained ringers, almost 600 juvenile (early post-fledging) and adult sparrows were captured at 30 sites that differ in urbanization rates. To specifically test whether urbanization differentially affect individuals during different parts of the life cycle, we used several proxies for the energetic and nutritional conditions experienced during (1) the developmental period (body size, juvenile feather quality), (2) at the time of capture (body condition), or (3) during the molting period (adult feather quality). Using this methodology, we showed for the first time that urbanization is associated with both reduced body size and feather quality in this urban-dweller species across a large geographical scale. Importantly, only tarsus length and juvenile plumage quality, both determined during development in the nest, were affected by the degree of urbanization. Conversely, body condition and plumage quality did not differ along the urbanization gradient in adults. Our results thus suggest that urban house sparrows could suffer from nutritional deficit during their development while such constraints disappear once the chicks have completed their growth.

Introduction

Increasing urbanization is currently among the most important human-induced environmental changes, and poses an important threat to biodiversity (Grimm et al., 2008; Seto, Güneralp, & Hutyra, 2012). Indeed, compared to natural environments, urban areas are often characterized by highly altered environmental conditions that can have detrimental effects on wildlife (e.g., habitat fragmentation and degradation; increased chemical, noise and light pollutions; modified resource availability and micro-climate; Chace and Walsh, 2006, Grimm et al., 2008, McKinney, 2008, Pickett et al., 2011). As a result, species richness and diversity are often reduced in urban environments (Clergeau, Croci, Jokimäki, Kaisanlahti-Jokimäki, & Dinetti, 2006; McIntyre, 2000, McKinney, 2008). Yet, for species that persist in cities, the consequences of urban life are poorly understood (Bonier, 2012, Partecke, 2014; Shochat, Warren, Faeth, McIntyre, & Hope, 2006; Sol, Lapiedra, & González-Lagos, 2013). Although several studies have shown that survival and reproductive performances are often impaired in cities (Chamberlain et al., 2009; Ryder, Reitsma, Evans, & Marra, 2010), a few species seem to be able to benefit from the urban environment. These successful city dwellers are regularly found in higher densities in urban compared to rural environments (Chace and Walsh, 2006, Møller et al., 2012, Shochat et al., 2006). However, to date, the proximate and ultimate causes of these inter-specific differences remain subject to debate, and better assessing them is considered as a research priority in urban ecology (Evans, Chamberlain, Hatchwell, Gregory, & Gaston, 2011; Lowry, Lill, & Wong, 2013; Shochat et al., 2006).

Although several traits are certainly involved in the ability of species to adapt to urbanized habitats (Evans et al., 2011, Gil and Brumm, 2014, Lowry et al., 2013, Møller, 2009, Sol et al., 2013), the capacity to switch from natural to anthropogenic food, in particular, may be a pre-requisite of an urban way of life (Lowry et al., 2013, Møller, 2009, Sol et al., 2013). Indeed, urban environments greatly differ from natural habitats in terms of food types and abundance (Chamberlain et al., 2009, Shochat et al., 2006). For instance, while natural food availability is often reduced as a result of reduced vegetation cover in cities, urban vertebrates can have access to large amounts of new types of food (i.e., anthropogenic food, birdseed, refuse; Chace and Walsh, 2006, Chamberlain et al., 2005, Chamberlain et al., 2009, Davies et al., 2009). The consequences of the ability of species to adjust to this new trophic situation is however complex because urban food may benefit to individuals during specific phases of their life cycle only, while imposing important constraints during others (Heiss, Clark, & McGowan, 2009; Peach, Mallord, Ockendon, Orsman, & Haines, 2015; Plummer, Bearhop, Leech, Chamberlain, & Blount, 2013; Seress et al., 2012). Thus, anthropogenic food may be sufficient to sustain nutritional needs during most of the life cycle, but not during specific life-history stages (e.g., reproduction, development, molt). Moreover, in addition to this new trophic situation, urban vertebrates are exposed to other environmental constraints, such as increased noise, light and chemical pollutions or modified biotic interactions (e.g., competition, predation regimes), that are also likely to differentially affect individuals during different parts of the life cycle (Bonier, 2012, Chace and Walsh, 2006, Gil and Brumm, 2014). Because of these potential stage-dependent impacts of urbanization and associated environmental constraints, it is often difficult to evaluate the overall impact of urban life on individual constitution and life history traits.

Indeed, the impacts of urbanization on condition or physiology seem inconsistent. For instance, urban individuals are in poorer condition than their rural conspecifics in some studies (e.g., Chávez-Zichinelli et al., 2013; Fokidis, Greiner, & Deviche, 2008; French, Fokidis, & Moore, 2008; Partecke, Van’t Hof, & Gwinner, 2005) but not in others (e.g., Foltz et al., 2015; Giraudeau, Mousel, Earl, & McGraw, 2014; Grunst, Rotenberry, & Grunst, 2014). Importantly, such discrepancies can also be found within the same species (e.g., Bókony, Kulcsár, & Liker, 2010; Bókony, Seress, Nagy, Lendvai, & Liker, 2012; Fokidis et al., 2008; Liker, Papp, Bókony, & Lendvai, 2008; Meillère, Brischoux, Parenteau, & Angelier, 2015), with differences depending on the sex, age, or life-history stage of individuals or the geographic area of the study sites (e.g., due to region- or city-specific environmental characteristics). This supports the idea that the influence of urbanization on condition is not only species-specific but also that urbanization may be primarily detrimental during specific life-history stages. To our knowledge, most studies have focused on adults during the pre-breeding or the breeding season while neglecting other phases of the life cycle (but see Fokidis et al., 2008). For example, only a few studies have investigated the impact of urbanization on the developmental (growth) or the molting period (e.g., Grunst et al., 2014; Hope, Stabile, & Butler, 2016; Seress et al., 2012) despite these two phases of the life cycle being the most energy and nutrient demanding (beside reproduction; Dawson, Hinsley, Ferns, Bonser, & Eccleston, 2000; Monaghan, 2008). The developmental phase is crucial for vertebrates because poor developmental conditions can alter the growth of the organism with potential long-lasting detrimental effects on morphology, behavior, physiology, and consequently, individual performances during adulthood (reviewed in Monaghan, 2008). Similarly, the molting period is crucial because this is an energetic demanding period and plumage quality is known to further affect individual performances during the following seasons (Dawson et al., 2000). Finally, the influence of urbanization on condition has mainly been investigated by comparing very few urban and rural sites only (but see Bókony et al., 2012; Evans, Gaston, Sharp, McGowan, & Hatchwell, 2009), and as a consequence, it remains difficult to make general inferences of the influence of urbanization on wild vertebrates.

Citizen science and the use of networks of volunteers could help urban ecologists to circumvent these problems because this methodology allows scientists to gather relevant data over large geographic and time scales. Accordingly, citizen science has been used to study ecological processes at national scale and/or during long-term periods (Dickinson, Zuckerberg, & Bonter, 2010; Morrison, Robinson, Leech, Dadam, & Toms, 2014; Silvertown, 2009). Obviously, one of the drawbacks of this method is the inability of volunteers to collect complex data (e.g., blood samples), but several basic measurements can be accurately and easily assessed by trained people (Couvet, Jiguet, Julliard, Levrel, & Teyssèdre, 2008; Dickinson et al., 2010, Schmeller et al., 2009). For instance, morphological data are relevant to assess the impact of environmental conditions on individuals in birds (Tellería, Hera, & Perez-Tris, 2013). Thus, body size is often a reliable proxy for developmental conditions, with small individuals having been energetically constrained during their growth (although adaptive reduction of body size is also possible, see Gardner, Peters, Kearney, Joseph, & Heinsohn, 2011). Body condition (i.e., energetic or nutritional state of an individual – e.g., estimated using size-adjusted body mass) is also relevant because it can provide cues on the ability of individuals to sustain their energetic needs (Peig and Green, 2009, Peig and Green, 2010). Similarly, feather collection (easily performed by volunteers) can provide ecologists with crucial data on the molting period as feathers integrate the conditions encountered by the individual during molt (Harms et al., 2015, Saino et al., 2013). Thus, feather length, mass and density are often used as proxies for feather quality and a nutritional deficit during the molt is often associated with shorter and lighter feathers (Murphy, King, & Lu, 1988; Pap, Vágási, Czirják, & Barta, 2008). In addition, fault bars (i.e., narrow, translucent bands found in the plumage of many bird species) are linked with malnutrition and the occurrence of stressors during the molt (Bortolotti, Dawson, & Murza, 2002; Machmer, Esselink, Steeger, & Ydenberg, 1992; Vágási et al., 2012). Finally, the fluctuating asymmetry of feathers has been suggested as a proxy for nutritional and energetic stress during the molting period (Møller, 1992, Swaddle and Witter, 1994). Therefore, the number of fault bars and the fluctuating asymmetry of feathers can be relevant complementary indices to assess the nutritional constraints that occur during the molt.

In this study, we investigated the influence of urban life on the condition and non-ornamental plumage quality in a common wild bird species, commensal of human settlements, the House sparrow (Passer domesticus). To do so, we used a national network of trained bird ringers to obtain reliable measurements of body size and condition and to collect tail feathers from both juvenile and adult sparrows over a large geographical scale across France. Our objective was to test whether urbanization had detrimental effects only during specific parts of the life cycle. The house sparrow is especially relevant to test our hypothesis for several reasons. First, this species is quite common in France and, contrary to most species, can be found along the whole urbanization gradient (from rural to highly urbanized areas; Anderson, 2006, Bichet et al., 2013). Second, although the house sparrow is certainly one of the most successful birds in the urban environment, it has undergone important population declines in urbanized areas during the past decades (De Coster, De Laet, Vangestel, Adriaensen, & Lens, 2015; Robinson, Siriwardena, & Crick, 2005; Shaw, Chamberlain, & Evans, 2008), suggesting that this species has recently suffered from urban environmental conditions. Finally, previous studies have suggested that the urban nutritional environment could be sufficient to sustain adults’ nutritional needs, but may be inadequate to satisfy the nutritional requirements of developing chicks (Bókony et al., 2012, Meillère, Brischoux, Parenteau et al., 2015, Peach et al., 2015, Seress et al., 2012). Here, to specifically test whether urbanization differentially affect sparrows during different parts of the life cycle, we used several proxies for the energetic and nutritional conditions experienced during the developmental period (body size, juvenile feather quality), at the time of capture (body condition), or during the molting period (adult feather quality). Based on the previous findings described above, we predicted that urbanization is associated with altered phenotypes in sparrows (reduced body size and condition, poor plumage quality). Moreover, we also predicted that the detrimental influence of urbanization may be exacerbated during energetically demanding life-history stages when rich-protein diet is required to fulfil nutritional needs (i.e., development and molt).