The study of urban birds has increased exponentially in the last century. A prior review of the scientific literature up to the year 2000 found 100 research articles on urban birds, but in the past decade alone, over 1000 have been published. Here I review the studies from 2006–2015 to characterize their approach, location, general findings and recent obsessions, with an eye toward suggesting important future directions. Urban ornithology remains centred in the northern hemisphere, although there is a rapid increase in studies from southern, tropical and biodiverse settings. Studies in the north have changed from documentation of the composition of urban avifaunas to include many studies of the demographic response to aspects of urban environments. Studies of pattern remain most common in Latin America, Asia, Africa, New Zealand and the Middle East. Across the world, ornithologists are revealing the rapid evolution of behavioural and morphological adaptations by birds to the urban environment, much of which is due to phenotypic plasticity. The relationship of humans to nature generally and birds specifically has been increasingly studied as a driver of avifaunal change as well as a factor affecting human ethics. Urban ornithology remains rarely experimental, but it has matured to the point of supporting synthetic reviews and meta-analyses that quantify the loss of avian diversity from city centres, characterize successful urban birds, discuss the role of amount and arrangement of vegetation on bird life, and explore the complex relationships between the subsidies and hazards of urban life and the survival and reproduction of birds. Yet much remains to be learned, including how some species thrive in cities with abundant predators; how city form and location affect the peak in avian richness that occurs typically at intermediate levels of urbanization; the significance of functional biotic homogenization; and the ways in which engaging citizens in urban bird life informs their broader environmental land ethic.
Human enterprise – specifically our industry, resource use and settlement – is a strong selective pressure on our species and the ecology and evolution of other species with which we coexist. To better understand these pressures and responses, geographers, anthropologists, economists, political scientists, planners, architects, other practitioners and ecologists increasingly collaborate on transdisciplinary investigations of urban ecosystems (Grimm et al. 2000, Pickett et al. 2001, Alberti et al. 2003, Endlicher et al. 2011). Through these and other small-scale investigations we understand that human domination of Earth's ecosystems drives many species to extinction (Vitousek et al. 1997). But our actions also provide the impetus for other species to adapt or exploit us (Marzluff 2012). This varied response to human action is exemplified by avian reactions to urbanization (Aldrich & Coffin 1980, Cramp 1980, Jones 1981, Recher & Serventy 1991, Blair 1996, Marzluff 2014). For example, as native forests are changed to savannah-like subdivisions, species reliant on a luxurious understorey, such as Pacific Wren Troglodytes pacificus, are rapidly replaced by those more tolerant of clearings and able to exploit gardens, such as Bewick's Wren Thryomanes bewickii (Farwell & Marzluff 2013).
Perhaps in part because of their aesthetic appeal and accessibility, urban avifaunas have been the subjects of study for over a century (Cramp 1980). However, as cities have grown and humans have predominantly taken on an urban lifestyle, the study of urban ornithology has flourished. Past reviews of this research revealed the myriad effects of built landscapes on vegetation, predators, competitors, foods, climate and human persecution/disturbance that are essential to avian reproduction, survivorship and community composition (Marzluff 2001, Chace & Walsh 2006, Ortega-Alvarez & MacGregor-Fors 2011). Research, especially that conducted before 2000, typically comprised 2- to 4-year studies that correlated urban form and density with the abundance and diversity of birds (Marzluff et al. 2001). The vast majority of the roughly 100 studies published from 1900 to 2000 were conducted in northern Europe, the USA, Canada, Scandinavia or Australia (Marzluff et al. 2001). Here, I survey the recent literature (2006–2015) to characterize modern studies of urban birds, their general findings and recent obsessions with a view to suggesting important future directions.
I conducted a search of the recent literature concerning urban avian ecology and evolution. I used the Web of Science search engine (http://apps.webofknowledge.com/) to discover articles archived with the key words ‘Birds’ AND ‘Urban’ published during 2006–2015, inclusive. Marzluff et al. (2001) and Chace and Walsh (2006) previously reviewed publications up to 2006. My search produced 1021 articles, of which I retained the 989 that reported empirical research or novel meta-analyses.
The rapid rise in the frequency of publications on avian urban ecology and evolution from 1960 to 2000 (Marzluff et al. 2001) has continued (Fig. 1). The annual number of publications in 2011, 2013, 2014 and 2015 was greater than the total of 103 known from 1900–2000. Annually, most publications were derived from studies in Europe, the USA and Canada. However, the decadal growth in publications from Latin America (Mexico, Central and South America, and the Caribbean) and Asia has outpaced the growth from Europe, USA and Canada (Fig. 1; a 325% increase from eight publications vs. a 104% increase from 47). Publications from New Zealand, the Middle East and Africa, while still rare in 2006–2015, increased steadily and were substantially more frequent than in the prior century, during which only two African publications were found (Marzluff et al. 2001).
Studies in Europe, USA, Canada and Australia increasingly focus on the processes by which birds respond to urbanization, rather than to the pattern of response (Fig. 2a). A similar though less dramatic shift in research emphasis occurred in studies elsewhere (Fig. 2b). The rise in studies addressing demographic processes, from eight publications in 2006 to 28 in 2015, was especially pronounced in Europe, USA, Canada and Australia (e.g. Chamberlain et al. 2009, Evans et al. 2015). Across the rest of the world, demographic studies remained rare (n = 28 publications from 2006–2015), whereas studies of behavioural and physiological correlates of response increased steadily over the decade.
Adaptation to the challenges of urban life, including especially city noise (e.g. Patricelli & Blickley 2006, Slabbekoorn & den Boer-Visser 2006, Warren et al. 2006) was rarely studied before 2000, but has commanded considerable attention during the past decade (Fig. 3). The benefits of supplemental food to some species, especially during winter (Fuller et al. 2008, Robb et al. 2008), sometimes at the expense of other species (Bonnington et al. 2014, Galbraith et al. 2015), and its potential detriments during chick-rearing (Harrison et al. 2010, Plummer et al. 2013), were the topics of 32 studies. In addition to audible noise, studies recognized other increasingly important challenges that urban birds face, such as predation and disturbance by domestic cats Felis domesticus (Bonnington et al. 2013, Loss et al. 2013), ultrasound (Jenni-Eiermann et al. 2014), electromagnetic fields (Balmori 2014, Engels et al. 2014), flame retardants (Chen et al. 2008, Gentes et al. 2012, Morrissey et al. 2014), windows (Klem et al. 2009, Hager & Craig 2014, Cusa et al. 2015), lights (Kempenaers et al. 2010, Dominoni et al. 2013, Da Silva et al. 2015) and climate change (Solonen & Hilden 2014). An inability to tolerate one or more aspect of the urban environment excludes many species from the city. However, successful urban birds were found to be adjusting to city life by changing song (Proppe et al. 2011, Lowry et al. 2012, although see Nemeth & Brumm 2010 and Moiron et al. 2015), plumage and morphology (Badyaev et al. 2008, Evans et al. 2009a), diet and foraging behaviour (Stracey et al. 2014, Lill & Muscat 2015, Russ et al. 2015), migration and dispersal (Partecke & Gwinner 2007, Møller et al. 2015a, Plummer et al. 2015), breeding behaviour and location (Yeh et al. 2007, Møller 2010), phenology (Solonen & Hilden 2014, Møller et al. 2015b), stress physiology (Fokidis & Deviche 2011, Atwell et al. 2012, Costantini et al. 2014), and the normally fearful response wild animals have towards humans (Clucas & Marzluff 2012, Lin et al. 2012, Miranda et al. 2013). These adjustments are mostly consistent with phenotypically plastic responses (the expression of distinct phenotypes in different environments; Hendry et al. 2008). Together, these studies indicate that the stressors of urban settings are many, both subtle and obvious, and that they influence birds’ demography, behaviour, morphology and physiology. If the past is indicative of the future, then further research will uncover even more challenges. Despite the ability of birds to adapt to many aspects of urban life, a nearly universal inability to tolerate free-ranging house cats and to avoid deadly collisions with glass windows remain the greatest challenges for birds in urban areas (Calvert et al. 2013, Loss et al. 2013, 2014).
Investigations of pattern typically documented changes in the diversity and/or abundance of an entire avian community across a gradient of urbanization (n = 386 publications). More rarely the response of a guild, often waterbirds (e.g. McKinney et al. 2011, Murray et al. 2013, Musilova et al. 2015, Yam et al. 2015), cavity nesters (Davis et al. 2013, Hong et al. 2013, Kane et al. 2015), grassland birds (Veech 2006, Dresseno & Overbeck 2013, Hauptfleisch & Dalton 2015) or raptors (Palomino & Carrascal 2007, Rullman & Marzluff 2014, Hogg & Nilon 2015), was the topic of study (n = 106 publications). Nearly half of all studies focused on one or two species (n = 459 publications) in order to investigate adaptations (e.g. Common Blackbird Turdus merula, Evans et al. 2009a), invasive/aggressive species (e.g. myna, parrots; Old et al. 2015), predators/parasites (e.g. Cooper's Hawk Accipiter cooperi, Stout et al. 2007) or demography (e.g. Evans et al. 2009b, Rosenfield et al. 2009, Whittaker & Marzluff 2009, Bell et al. 2010, Gordon et al. 2010, Vargas et al. 2011, Rodewald et al. 2013). The most studied urban birds were the House Sparrow Passer domesticus (n = 38 publications), Common Blackbird (n = 37), Rock Dove Columba livia (n = 35) and Great Tit Parus major (n = 25). The variety of urban birds that have been closely monitored remains small and mostly limited to those species tolerant of the city. However, a general consensus emerges across ecological guilds that birds with general as opposed to specialized living requirements can thrive in the city. Urban avifaunas therefore include some ground, shrub and canopy nesters, migrants and residents, terrestrial and aquatic species, and granivores, frugivores, piscivores, carnivores and nectarivores. Birds from a wide variety of taxonomic groups also live in the city, especially ducks, raptors, vultures, pigeons, parrots, swifts, woodpeckers, flycatchers, corvids, swallows, wrens, thrushes, sparrows and icterids. Because birds do not uniformly suffer or benefit from urbanization, the differential success of generalist over specialist species leads to turnover in community composition through time or space as lands transition from natural or rural to urban cover.
The relationship of humans to nature generally and birds specifically has been increasingly studied in urban ecosystems (Fig. 3). Birds and humans were described as being in mutually reinforcing relationships, especially at bird feeders (e.g. Davies et al. 2009, Shaw et al. 2013, Clucas & Marzluff 2015) and in gardens (Cammack et al. 2011, Shaw et al. 2013). The appreciation of nature by young people has been enhanced in areas with diverse bird song (Hedblom et al. 2014). Some birds have been studied as a health (Shwartz et al. 2014) or economic (Caula et al. 2009, Farmer et al. 2013, Luck et al. 2013, Clucas et al. 2015) benefit to people, whereas others (especially Rock Pigeons) have been documented as a health risk (Holevinski et al. 2006, Charles & Linklater 2013, Belaire et al. 2015) or nuisance (Mdegela et al. 2006, Duarte et al. 2011, Sacristan et al. 2014, Caballero et al. 2015). Research into effective and humane strategies to reduce the numbers of less-appreciated urban birds suggests that limiting food subsidies is an important first step (Stock & Haag-Wackernagel 2016).
Most studies of urban birds were of short duration, typically 2 years. However, exceptions to this pattern are increasing in frequency. Changes in avian community composition have been documented over the course of a century of city growth in London, Cambridge, MA, and Berkeley, CA (Shultz et al. 2012, Woodward & Arnold 2012, Strohbach et al. 2014). Studies spanning a decade that investigate the individual actions and histories of marked birds in three USA locations (Seattle, WA, Columbus, OH, and Washington, DC) are beginning to bear fruit (Ryder et al. 2010, Rodewald et al. 2013, Evans et al. 2015, Marzluff et al. 2015).
The publication of several focused reviews and meta-analyses point to the maturation of urban avian ecological science. The question of why some species thrive in cities and others do not has been a topic of great interest. Birds that are generalists or behaviourally flexible are often noted as being successful at colonizing and persisting in cities (McKinney 2006, Bonier et al. 2007, Møller 2009, Evans et al. 2011, Lowry et al. 2013, Sol et al. 2013). Important flexibility in behaviour, which is consistent with phenotypic plasticity, includes changes in phenology, diet, vigilance and communication, all of which affect reproduction, survival and dispersal (Lowry et al. 2013). At the heart of these distinct phenotypes may be population differences in the personalities of birds, which may be understood best by evaluating their role in three distinct stages: arrival, establishment and population increase (Sol et al. 2013). Personality traits that are often associated with successful city birds include bold, social, exploratory, neophilic and less reactive temperaments (Lowry et al. 2013, Møller et al. 2015a). During the arrival stage, innovative, bold, explorative and less reactive phenotypes increase the chances of birds dispersing to and selecting novel urban habitats (Sol et al. 2013). Phenotypes that tolerate disturbance quickly learn to recognize and avoid new predators and those that adjust their communication to the city's acoustics (Cardoso 2014) may best survive small population bottlenecks (establishment stage; Sol et al. 2013). The efficient use of novel resources, such as safe nest and roost sites or superabundant foods (Evans et al. 2011), and a tolerance of high conspecific density may finally allow some species to dominate the urban avifauna (increase stage; Sol et al. 2013).
There is some disagreement in the literature about the importance of specific behavioural adjustments, and the personality traits that underlie them, to urban success. For example, whereas some studies show differences in brain size and problem-solving ability between urban and non-urban birds (Liker & Bókony 2009, Maklakov et al. 2011), others do not (Kark et al. 2007, Møller 2009, Evans et al. 2011, Sol et al. 2014). Some inconsistent findings may reflect regional vagaries (Sol et al. 2014) or simply differences in how one quantifies urban abundance (presence only, relative abundance or difference in abundance between urban and rural locations; Evans et al. 2011).
Synthetic reviews also suggest that the avian community found in cities is a direct function of the amount and arrangement of vegetation therein. Local features of the urban habitat, notably the size of habitat patches, and to a lesser extent their connectivity, are especially influential (Evans et al. 2009c, Beninde et al. 2015). Species diversity increases with vegetative complexity (Evans et al. 2009c), as was proposed half a century ago (MacArthur & MacArthur 1961). Because of this relationship, diversity often peaks at intermediate levels of urbanization, characteristic of suburbs and exurbs, where the juxtaposition of various land covers enhances local diversity (Blair 1996, Marzluff 2005).
Finally, reviews demonstrate that species living in urban areas vary greatly in reproductive success and annual survival. Both demographic parameters may decline from rural to urban settings in sensitive species, but increase or remain unchanged in species that exploit or adapt to urban conditions (Chamberlain et al. 2009, Ryder et al. 2010, Evans et al. 2015, Marzluff et al. 2015). Species nesting on or close to the ground often (Evans et al. 2011, Cardoso 2014), although not always (Marzluff et al. 2015), reproduce poorly. Species that hedge their bets by spreading reproductive investment across many broods fare particularly well in urban settings (Sol et al. 2014). Supplemental food, and the ability to exploit it, is likely to explain much of the variation in how species’ demographics are affected by urbanization. In response to increased resources and the urban heat island effect, the timing of reproduction is usually advanced in urban areas, whereas clutch size, nestling quality and the subsequent survival of fledglings that require an arthropod-rich diet (Robb et al. 2008, Chamberlain et al. 2009) may be reduced. The supplemental resources available in cities can enhance annual survival (Evans et al. 2015, Marzluff et al. 2015), but it may also be reduced in some species that are susceptible to communal diseases and increased predation around feeders (Robb et al. 2008).
Urbanization is widely recognized as a major force affecting the planet's biological diversity. At moderate levels, local diversity may be increased by suburban and exurban development (Marzluff 2014), but when most land is converted from natural open space to a dense urban area, diversity plummets as a few species that are able to tolerate and adapt to human action come to dominate the community (Blair 1996, Marzluff 2005, McKinney 2006, Sol et al. 2014). In response to the threat of urbanization to birds, ornithological research in urban areas is increasing at an exponential rate. This increase is sustained by continued interest from European, North American and Australian researchers and especially by rising interest from Latin American, Asian and African ornithologists. As a basic understanding of urban biodiversity is gained, the focus of research has also changed. Studies before 2000 in North America and Europe focused on the response of the avian community to the urban environment, especially the pattern of built vs. vegetated area (Fig. 4a; Marzluff et al. 2001). This type of study now dominates urban ornithology in Latin America, Asia, Africa, the Middle East and New Zealand. In the past decade, Europeans, North Americans and Australians have increasingly focused on the ways reproduction, survival and, to a lesser extent, dispersal enable some birds to colonize and adapt to urban areas, whereas others become extinct locally (Fig. 4b). These studies are producing a mechanistic understanding of community change (Shochat et al. 2006, Chamberlain et al. 2009, Rodewald et al. 2013, Buxton & Benson 2015, Evans et al. 2015, Marzluff et al. 2015) and providing insights into the evolutionary processes operating in urban areas (Marzluff 2012, Alberti et al. in press). Although far from conclusive, current studies suggest that birds unable to survive in urban areas may fail for very different reasons, including poor reproduction (Rodewald et al. 2013), low annual survival of breeders (Evans et al. 2015, Marzluff et al. 2015) and the production of poor-quality offspring (Chamberlain et al. 2009). The ability of species to survive (Varner et al. 2014, Evans et al. 2015, Marzluff et al. 2015) and reproduce (Ryder et al. 2010, Rodewald et al. 2013, Buxton & Benson 2015) in cities is enhanced by their behavioural flexibility (Lowry et al. 2013, Sol et al. 2013). This variability is likely to be the result of phenotypic plasticity, which enables populations to adapt rapidly to the novel challenges of city life (Hendry et al. 2008). Adaptations to urbanization may be sustained by phenotypic plasticity (Hendry et al. 2008), but also may evolve from sexual and natural selection (Berthold et al. 1992, Yeh 2004, Yeh & Price 2004, Badyaev et al. 2008), as well as from social learning, which diversifies culture (Cornell et al. 2012).
The study of urban birds, although growing, continues to raise unanswered questions. How, for example, do some species thrive in cities rife with small predators, such as domestic cats? This ‘predation paradox’ may occur because abundant foods and expanded breeding periods in cities enable generalists reproductively to swamp their predators (Fischer et al. 2012). However, it may be that nesting behaviours have also coevolved with predator activities, or that stress physiology enables a muted response to predator disturbance. An understanding of the physiological mechanisms that underpin behavioural adaptation in general requires further study (Bonier 2012).
Natural vegetation and its abundance, floristic diversity, structural complexity and ability to harbour native invertebrates clearly enhance bird life in the urban environment (Evans et al. 2009c, Huang et al. 2015), but basic aspects of this relationship require further research. The common peak in avian diversity at intermediate levels of urbanization (typically in suburbs or exurbs; Marzluff 2005), for example, may vary with the degree to which green and built spaces are interspersed (Morimoto et al. 2006) or the relative richness of native and built habitats (Fig. 5; Marzluff 2005). Little is also known about the value of various types of anthropogenic vegetation, such as green walls and roofs (Fernandez-Canero & Gonzalez-Redondo 2010), for example whether their size and connectivity is beneficial to birds, as is the case with more traditional urban green spaces (Evans et al. 2009c). Targeted research could inform planners about integrating vegetation on roofs, walls, planters and street verges into a larger green space plan.
The question of biotic homogenization has received considerable attention, but current research raises more questions than it answers. Clearly, the avian communities of cities are more similar to one another than are the communities of other, less human-dominated lands (Clergeau et al. 2006, McKinney 2006, Olden et al. 2006). However, this is to be expected because cities are inherently similar in structure, being dominated by buildings and travel corridors with an interspersion of natural to semi-natural green spaces and water features. Despite this similarity in form and composition, there are very few cosmopolitan species (Aronson et al. 2014, Marzluff 2014), with the result that the homogenization that is occurring is more functional than taxonomic (Devictor et al. 2007). However, with increasing introduction of non-native species to cities, taxonomic homogenization may also increase in the future (Case 1996). In addition, homogenization may be perceived, whereas the actual processes at work are habitat-specific species turnover or simple decline of sensitive species (Catterall et al. 2010). Understanding the mechanisms behind these processes is now more important than further documentation of the pattern. Natural areas are expected to show less homogenization across space because of differences in their disturbance history, floristic composition and landscape setting. In the future, rigorous comparisons of homogeneity between natural and anthropogenic lands should control for these and other factors.
Perhaps the most significant gap in urban bird research is the lack of experimental studies. This is surprising because the rapid pace of urbanization provides abundant ready-made experiments. In Seattle, WA, USA, for example, it has been possible to compare the abundance and demography of birds before, during and after development by monitoring avian communities and populations as new subdivisions were carved out of native forest (Marzluff et al. 2015). Comparing the changes in these developing areas to avifaunal dynamics in nearby control forests and subdivisions provided a quasi-experimental, causal understanding of which birds thrived and which perished during development. Moreover, by marking and observing individual birds belonging to species that varied in their response to urbanization, it is possible to gain insights into how population dynamics responded to changes in reproduction, survival and dispersal. Expanding this relatively long-term (decadal) approach to other rapidly urbanizing areas would greatly advance our understanding of the avian urban ecology.
Connecting to conservation
The realization that a rich diversity of birds inhabits urban ecosystems (Aronson et al. 2014) and rapidly evolves therein is a means by which urban ornithologists can enhance avian conservation (Shwartz et al. 2014). Citizens become more deeply connected to nearby nature as they learn more about it (Evans et al. 2005), and this engagement may strengthen their practice of measures that sustain biological diversity both at home and on behalf of distant ecosystems (Fig. 4c; Turner et al. 2004, Miller 2005, 2006, DeSteffano 2010, Beatley 2011, Wells & Lekies 2012, Soga & Gaston 2016). Understanding how best to inform a sustainable land ethic with experiences in the citizenry's backyard, the ‘pigeon paradox’ (Dunn et al. 2006), remains a challenge. Recent studies link a diversity of activities including participation in bird banding and observation (Evans et al. 2005), bird feeding (Robb et al. 2008, Davies et al. 2009, Clucas & Marzluff 2015) and gardening (Shaw et al. 2013) to increased biophilia. Moreover, the appreciation of nature, including birds, by urban residents is responsive to the aesthetic (Hedblom et al. 2014, Belaire et al. 2015), health (Bonta 2008, Luck et al. 2011) and economic (Farmer et al. 2013) benefits of greenspace and biodiversity. However, people may not fully notice the diversity of birds around them without active engagement and conspicuous interpretation (Shwartz et al. 2014). This suggests that involving urban residents in ornithological study and making them aware of findings will be crucial to their ecological literacy. The potential benefits of an ecologically informed land ethic that begins in one's backyard and extends to wild and remote reaches of Earth are great, and include citizen-driven changes in policies and practices that affect climate, productivity and habitat, which in turn affect the ecology and evolution of bird populations and communities (Fig. 4c).
As we learn more about birds in our environment, we will also discover unique ways to engage people in their conservation. People are inspired by fascinating discoveries: for example, the plasticity and rapid evolution of new migratory routes in Blackcaps Sylvia atricapilla (Berthold et al. 1992, Plummer et al. 2015) or the ability of urban birds to recognize and remember individual people (Levey et al. 2009, Marzluff et al. 2010, Lee et al. 2011, Stephan et al. 2012). Adding to the discoveries that inspire the public and learning how best to transform inspiration into compassionate conservation should motivate urban ornithologists to make sure the next decade of research surpasses the extremely productive previous one.
I thank the BOU for inviting me to review the urban ornithological literature for the 2016 annual meeting. The University of Washington James W. Ridgeway endowed professorship funded my research. Jeremy Wilson, Jose A. Sanchez-Zapata and an anonymous reviewer called my attention to additional references and insights, for which I am grateful.