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Biol. Rev. (2010), 85, pp. 643667.

643
doi: 10.1111/j.1469-185X.2010.00121.x

A conceptual framework for the colonisation


of urban areas: the blackbird Turdus merula
as a case study
Karl L. Evans , Ben J. Hatchwell, Mark Parnell and Kevin J. Gaston
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK

(Received 12 December 2009; revised 15 December 2009; accepted 3 January 2010)

ABSTRACT

Despite increasing interest in urban ecology the factors limiting the colonisation of towns and cities by species from rural
areas are poorly understood. This is largely due to the lack of a detailed conceptual framework for this urbanisation
process, and of sufficient case studies. Here, we develop such a framework. This draws upon a wide range of ecological
and evolutionary theory and the increasing number of studies of how the markedly divergent conditions in urban
and rural areas influence the traits of urban populations and the structure of urban assemblages. We illustrate the
importance of this framework by compiling a detailed case study of spatial and temporal variation in the urbanisation
of the blackbird Turdus merula. Our framework identifies three separate stages in the urbanisation process: (i) arrival, (ii)
adjustment, and (iii) spread. The rate of progress through each stage is influenced by environmental factors, especially
human attitudes and socio-economic factors that determine the history of urban development and the quality of urban
habitats, and by species ecological and life-history traits. Some traits can positively influence progression through one
stage, but delay progression through another. Rigorous assessment of the factors influencing urbanisation should thus
ideally pay attention to the different stages. Urbanisation has some similarities to invasion of exotic species, but the two
clearly differ. Invasion concerns geographic range expansion that is external to the species original geographic range,
whilst urbanisation typically relates to filling gaps within a species original range. This process is exemplified by the
blackbird which is now one of the commonest urban bird species throughout its Western Palearctic range. This is in
stark contrast to the situation 150 years ago when the species was principally confined to forest. Blackbird urbanisation
was first recorded in Germany in 1820, yet some European cities still lack urban blackbirds. This is especially so in
the east, where urbanisation has spread more slowly than in the west. The timing of blackbird urbanisation exhibits a
marked spatial pattern, with latitude and longitude explaining 76% of the variation. This strong spatial pattern contrasts
with the weaker spatial pattern in timing of urbanisation exhibited by the woodpigeon Columba palumbus (with location
explaining 39% of the variation), and with the very weak spatial pattern in timing of black-billed magpie Pica pica
urbanisation (in which location explains 12% of the variation). Strong spatial patterns in timing of urbanisation are more
compatible with the leap-frog urbanisation model, in which urban adapted or imprinted birds colonise other towns and
cities, than with the independent urbanisation model, in which urban colonisation events occur independently of each
other. Spatial patterns in isolation do not, however, confirm one particular model. Factors relating to the arrival and
adjustment stages appear particularly likely to have influenced the timing of blackbird urbanisation. Spatial variation
in the occurrence of urban populations and the timing of their establishment creates opportunities to assess the factors
regulating urbanisation rates, and how the composition of urban assemblages develops as a result. These are major
issues for urban ecology.

Key words: adaptation, blackbird, Columba palumbus, corvids, magpie, Pica pica, Turdus merula, range expansion, species
traits, urbanisation, woodpigeon

* Address for correspondence: (Tel: 0114 2220125; Fax: 0114 2220002; E-mail: karl.evans@sheffield.ac.uk)

Biological Reviews 85 (2010) 643667 2010 The Authors. Journal compilation 2010 Cambridge Philosophical Society
644 K. L. Evans and others

CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 644
II. The three stages of the urbanisation process . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 645
(1) Arrival . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 645
(2) Adjustment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 646
(a) Environmental factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 646
(b) Mechanisms of adjustment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 647
(c) Species traits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 648
(3) Spread . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 648
(4) Positive and negative feedbacks between stages . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 648
III. The blackbird Turdus merula as a case study . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 650
(1) Data compilation and assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 651
(2) Spatial and temporal patterns . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 651
(3) Independent or leap-frog urbanisation? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 654
IV. Applying the conceptual framework to the blackbird . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 654
(1) Stage 1 - arrival . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 654
(2) Stage 2 - adjustment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 655
(3) Stage 3 - spread . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 657
V. Variation in urbanisation - the blackbird in a broader context . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 657
(1) What proportion of Turdus species are urbanised? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 657
(2) Spatial and temporal patterns in urbanisation in other species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 658
(a) Turdus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 658
(b) Corvus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 659
(c) Columba . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 660
(d) Other genera . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 661
VI. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 661
VII. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 662
VIII. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 662
IX. Supporting Information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 667

I. INTRODUCTION and thus differ from those exhibited by rural conspecifics (e.g.
Marzluff, 2001; Yeh, Hauber & Price, 2007; Chamberlain
The world is becoming increasingly dominated by concrete et al., 2009; Evans et al., 2009b,c; reviewed by Evans, in press).
and other hard surfaces, with about 4% of the terrestrial These research agendas have clear connections to a num-
area currently urbanised (UNDP, 2000; UN, 2008). This ber of well-established fields including conservation biology,
percentage is much higher in some areas, such as western macroecology, island biogeography and invasion biology.
Europe, in which urban land comprises approximately 10% Whilst invasion biology and urban ecology both concern
of Britain (Haines-Young et al., 2000; Fuller et al., 2002) and changes in species distributions and adaptation to novel envi-
12% of the Netherlands (CBS, 2003). At a global scale, ronments there is a notable contrast between the two. Broadly
urbanisation is the fastest growing land use, and half of speaking, invasion biology concerns processes external to
the worlds human population now resides in urban areas a species original geographic range, whilst colonisation of
(UN, 2008). urban areas generally relates to processes internal to a species
Interest in the ecological effects of urbanisation was rather range, i.e. filling gaps within range boundaries. There is a lack
limited until recently, but is now growing rapidly. Topics cur-
of a clear conceptual framework for this internal range expan-
rently under investigation include (i) how urbanisation influ-
sion process, which is not helped by the paucity of case studies.
ences habitat quality and other environmental conditions
Here we first develop such a framework, and then provide a
(e.g. Grimm et al., 2008; Evans, Newson & Gaston, 2009d), (ii)
describing variation in biodiversity along gradients in human detailed case study focusing on spatial and temporal variation
population density or other measures of urbanisation (e.g. in the colonisation of urban areas by the blackbird Turdus
Blair, 1996; Marzluff, 2001; Evans et al., 2006; Evans, Green- merula (hereafter referred to as the blackbird), which across
wood & Gaston, 2007; Tratalos et al., 2007), (iii) how species much of its geographic range is one of the commonest avian
ecological and life history traits influence their ability to species in urban areas. This is in stark contrast to the situa-
colonise and survive in urban areas (e.g. Lim & Sodhi, 2004; tion 150 years ago, when it was regarded as a forest specialist
Croci, Butet & Clergeau, 2008; Kark et al., 2007; Thompson (Luniak, Mulsow & Walasz, 1990). In so doing we compare
& McCarthy, 2008), and (iv) how these traits respond to the the spatial patterns in the occurrence and timing of urbani-
different environmental conditions occurring in urban areas sation exhibited by the blackbird with that of other species.

Biological Reviews 85 (2010) 643667 2010 The Authors. Journal compilation 2010 Cambridge Philosophical Society
A conceptual framework for the colonisation of urban areas 645

II. THE THREE STAGES OF THE URBANISATION stage, with the outcome depending on numerous factors that
PROCESS are stage specific. These factors are environmental ones and
species ecological and life-history traits. The environmental
How species become urbanised (i.e. colonise urban areas) is factors primarily relate to the spatial configuration and
poorly understood and has received rather little attention in development history of urban areas and the quality of urban
the ecological literature. There has been some exploration habitats; they are thus dependent on human attitudes and
of the traits that characterise synanthropic species and socio-economics. Notably, some species traits may have
urban adapters, primarily focusing on birds (Lim & Sodhi, opposing effects on the rate of progression through different
2004; Chace & Walsh, 2006; McKinney, 2006; Bonier, stages.
Martin & Wingfield 2007; Kark et al., 2007; for plants see
Thompson & McCarthy, 2008). However, few studies have (1) Arrival
attempted to describe how such species initially become
established in urban areas and subsequently expand their This stage concerns the initial dispersal to an urban area.
urban populations (but see Vuorisalo et al., 2003; Yeh & The importance of dispersal in determining species richness is
Price, 2004; Rutz, 2008). firmly recognised by island biogeography theory (MacArthur
An understanding of the urbanisation process has been & Wilson, 1967), and its importance in determining
hindered by the lack of discrimination between each of its urban biodiversity has received some initial discussion
three distinctive stages. These are rarely explicitly recognised (Marzluff, 2005).
in the urbanisation literature (but see Marzluff, 2005) despite The probability of a species initially arriving in an urban
much focus being given to their equivalents in invasion area will increase with both the proportion of its geographic
biology (e.g. Williamson, 1996; Kolar & Lodge, 2001; Puth range that is urbanised, and the time available for this process,
& Post, 2005). The three stages of the urban colonisation i.e. the history of urban development (Fig. 1). Concerning
process are (1) arrival in urban areas, (2) adjustment to the species traits, a high population density in surrounding rural
urban environment, and (3) spread within urban areas and habitats will increase the numerical probability of dispersal
to neighbouring towns and cities (Fig. 1). Whilst urbanisation to urban areas. Indeed, annual intraspecific variation in
is essentially a continuous process it can usefully be divided the frequency of avian species occurring in gardens in the
into these three stages because it can succeed or fail at each United Kingdom, most of which are urban, is positively

Fig. 1. Schematic representation of the three stages of the urbanisation process, and the environmental and species characteristics
that increase the probability of each stage being successful. Socio-economics and human attitudes play a major role in shaping the
environmental characteristics, but have been excluded for simplicity. Some factors influence more than one stage, but can have
opposing effects on different stages. See Section II for more details.

Biological Reviews 85 (2010) 643667 2010 The Authors. Journal compilation 2010 Cambridge Philosophical Society
646 K. L. Evans and others

correlated with the nature of their population trends in and food, which can be an important influence on urban
the wider countryside (Cannon et al., 2005). In addition, assemblages (Fuller et al., 2008; Davies et al., 2009; Evans
if rural densities are high relative to the environmental et al., 2009d), (ii) levels of predation by humans (Vuorisalo
carrying capacity, selection pressures that favour dispersal to et al., 2003) and their commensals, such as domestic cats
unoccupied areas, such as urban ones, may increase (Herzig, (Baker et al., 2008; Sims et al., 2008), and (iii) the location
1995; Loxdale & Lushai, 1999; Lambin, Aars & Piertney, of urban areas, which is likely to be non-random with
2001). These selection pressures take numerous forms, but regard to their ecological situations (e.g. towns and cities
may be related to deteriorating quality of rural environments; are more likely to be located in areas of relatively high
for example, a succession of severe winters and increased primary productivity, close to permanent water supplies, or
persecution are associated with the arrival of goshawks at sites whose topography promotes defence), and which
Accipiter gentilis in Hamburg (Rutz, 2008). Similarly, a rapid could increase the divergence between urban and rural
increase in the urban population of Australian white ibis habitats.
Threskiornis molucca in Sydney in recent decades is associated The second major difference between rural and urban
with a reduction in the extent of their inland wetland habitat areas is that the latter are characterised by elevated
due to drought, dam construction and agricultural water temperatures and modified rainfall patterns (Lowry, 1998;
extraction (J. Martin, unpublished data). Arnfield, 2003; Zhou et al., 2004; Collier, 2006), and thus
The successful introduction of species to urban areas tend to have longer growing seasons and altered patterns of
within their natural range indicates that a lack of dispersal, vegetation phenology (White et al., 2002; Zhang et al., 2004;
rather than insufficient habitat, can limit a species Neil & Wu, 2006). Third, towns and cities are frequently
occurrence in urban areas (Cade & Bird, 1990; Martell, more polluted than rural areas, with regard to chemicals,
Englund & Tordoff, 2002). Indeed, long-term studies night-time lights and noise (Sharp, 2002; Small, Pozzi &
document a gradual increase in avian species richness in Elvidge, 2005; Grimm et al., 2008).
urban areas as the time available for species to colonise Fourth, native species richness is typically very low in
increases. In some cases this is largely in response to city centres, although at local scales the richness of some
successional changes in vegetation structure (Vale & Vale, taxa, such as birds, may peak in suburban areas (Clergeau,
1976), but in others it is a consequence of colonisation events Jokimaki & Savard, 2001; Marzluff, 2001; Tratalos et al.,
that are independent of changes in habitat quality (Abs & 2007; Grimm et al., 2008). Fifth, urban areas often contain
Bergen, 2008). It thus seems likely that the arrival stage can increased numbers of exotic species, especially of plants
frequently limit the structure of urban assemblages. (Blair, 2001; McKinney, 2006; Smart et al., 2006; de Victor
et al., 2007; Grimm et al., 2008). Sixth, species population
(2) Adjustment densities typically differ markedly between urban and rural
areas; whilst most species occur at lower densities in urban
Following arrival in an urban area an individual must cope
areas a significant, but small, proportion of species reach
with a markedly different environment than its former
much higher densities in towns and cities (Tratalos et al.,
rural one. The adjustment stage concerns the processes
2007; Evans et al., 2009d). Seventh, these alterations in
through which this adjustment occurs. In this section we
first summarise the characteristics of urban areas, and assemblage composition may change the nature of species
thus describe the novel environment to which urbanising interactions and have a major influence on the quality of
species must adjust. We then outline the processes that urban habitat types, e.g. pollination rates may be reduced due
can generate the required adjustments, and conclude by to a relative lack of insect pollinators (Cheptou & Avendano,
reviewing examples of the adjustments exhibited by urban 2006). Similarly, urbanisation can dramatically influence
populations. exposure to natural enemies, i.e. predators, pathogens
and parasites, and competitors. There is support for the
contrasting hypotheses that for birds urban areas provide
(a) Environmental factors safe nesting environments (Gering & Blair, 1999; Kosinski,
Broadly speaking urban and rural environments differ in 2001; Newhouse, Marra & Johnson, 2008), and that predator
seven ways. First, habitat modification is marked in urban densities and thus predation rates are higher in urban areas
areas, with the magnitude of change often exceeding that (Thorington & Bowman, 2003; Jokimaki et al., 2005; Beck
resulting from rural land-uses, such as logging and farming. & Heinshon, 2006; Marzluff et al., 2007; Sims et al., 2008),
Urban centres are characterised by highly fragmented and meta-analysis shows that no general trends have yet
habitat patches with a simple habitat structure and very emerged with regard to the impact of urbanisation on rates
low habitat diversity, although at small spatial scales of predation on birds nests (Chamberlain et al., 2009). The
habitat diversity may be markedly higher in suburban areas nature of general patterns in the prevalence and intensity of
(Marzluff & Ewing, 2001; Grimm et al., 2008; Evans et al., parasites and pathogens is equally uncertain, and probably
2009d). The magnitude of this divergence between urban differs markedly with the identity of the parasite/pathogen,
and rural habitats is clearly regulated by human attitudes its vector and host (Bradley & Altizer, 2007; Gosselink et al.,
and socio-economic factors that determine: (i) the level of 2007; Bradley, Gibbs & Altizer, 2008; Fokidis, Greiner &
supplementary resource provision, such as avian nest sites Deviche, 2008; Evans et al., 2009c; reviewed by Evans, in

Biological Reviews 85 (2010) 643667 2010 The Authors. Journal compilation 2010 Cambridge Philosophical Society
A conceptual framework for the colonisation of urban areas 647

press). Competitors can also be viewed as natural enemies. urban and rural environments, but their usefulness in
Interspecific competition can structure urban asssemblages assessing the relative roles of plasticity and genetic change
[plants - Ogawa & Mototani (1985); reptiles - Petren & in generating trait divergence is limited as most studies
Case (1996); Ptilinopus fruit doves in New Guinea - Bell have focused on describing patterns rather than assessing
(1986); corvids - Lehmann (2002); sparrows - Bannerman & their causal mechanisms, few determine the adaptive value
Bannerman (1965)], and higher densities of some generalists of trait divergence in urban areas, and almost none has
in urban areas may increase the intensity of both intra- distinguished between genetic adaptation and epigenetic
and inter-specific competition (Tratalos et al., 2007; Grimm effects. Addressing these limitations will be a major challenge
et al., 2008). for urban ecology in the future.
In combination, the above seven factors will determine There is, however, some evidence that trait divergence
the magnitude of contrast between urban and rural between urban and rural populations is attributable to
environments, and thus the requirement for adjustment. phenotypic plasticity. The frequently documented tendency
For some species urban features may be sufficiently similar for urban birds to have louder and/or higher pitched
to those of ancestral rural areas to limit the requirement songs than rural conspecifics (which may be an adaptive
for adjustment. For example, ruderal plant species that are response to noise pollution in cities, and the low frequency
adapted to early successional vegetation stages tend to do of anthropogenic noise, but see Nemeth & Brumm, 2009)
particularly well in urban environments due to frequent appears to have arisen primarily through phenotypic
anthropogenic disturbance of soils (Gilbert, 1989). More plasticity (Brumm, 2004; Slabbekoorn & Ripmeester, 2008;
specifically, plants adapted to growing on rocky surfaces, e.g. Bermudez-Cuamatzin et al., 2009; Mockford & Marshall,
Sedum species, frequently grow on similar surfaces in cities, 2009). Vegetation phenology and the timing of avian
such as roof tiles and concrete. Similarly, the breeding sites reproduction typically occur earlier in urban areas than
of urban peregrines Falco peregrinus, tower blocks and other rural ones (Zhang et al., 2004; Chamberlain et al., 2009), and
tall buildings, have been considered analogous to the cliff this seems likely to be a plastic response as phenological
ledges used by rural peregrines (Cade & Bird, 1990). advancement in response to climate change is typically
driven by phenotypic plasticity (Brommer et al., 2005;
(b) Mechanisms of adjustment Brommer, Rattiste & Wilson, 2008; Charmantier et al.,
Given these marked differences between urban and rural 2008). Furthermore, experiments indicate that the early
areas it is highly likely that almost all species which colonise reproduction of urban blackbirds, relative to rural ones, is
towns and cities from rural sites will require some adjustment a plastic response (Partecke, vant Hof & Gwinner, 2004).
to the novel urban environment. Phenotypic plasticity and Urban birds typically have shorter flight initiation distances
genetic adaptation are both likely to contribute to this following human disturbance than their rural counterparts
adjustment. In some cases phenotypic plasticity may be (Cooke, 1980; Campbell, 2006; Mller, 2008). Individual
all that is required for the establishment of an urban Eurasian woodpigeons Columba palumbus (hereafter termed
population, in which case progress through the adjustment woodpigeon) change their reactions to disturbance when
stage will be rapid. It is more likely, however, that optimal foraging in urban and rural areas, indicating that at least
urban phenotypes will require genetic adaptation. The in this species changes are a consequence of a flexible
requirement for genetic adaptation may arise for three strategy (Tomiaojc, 1976). Plasticity thus appears to be
reasons (Price, Qvarnstrom & Irwin, 2003; West-Eberhard, a major mechanism through which adjustments to urban
2005; Ghalambor et al., 2007). First, even if plasticity results environments arise, but it is plausible that the ability to
in an adaptive phenotype it may do so in a more costly exhibit plastic responses is under genetic control (Price et al.,
manner than that possible with genetic adaptation, resulting 2003; West-Eberhard, 2005; Ghalambor et al., 2007).
in selection pressures that ultimately generate genetic change. Turning to genetic adaptation, experiments in which
Second, plastic responses to the new environment may urban and rural individuals were raised in identical
approach, but fall short of, the optimum urban phenotype, conditions are increasingly suggesting that adjustment to
resulting in directional selection for extreme phenotypes urban areas can have a genetic basis. This is the case for the
which generates genetic adaptation (i.e. genetic assimilation; smaller body size of urban house sparrows Passer domesticus
Waddington, 1961). Third, the plastic responses induced by (Liker et al., 2008) and increased sedentariness and reduced
arrival in novel environments, such as urban areas, may stress response of urban blackbird populations (Partecke,
generate additional selection pressures that drive genetic Schwabl & Gwinner, 2006; Partecke & Gwinner, 2007),
adaptation of other traits. although epigenetic effects cannot be ruled out in either of
Marked intraspecific trait divergence between rural and these studies. The clearest example of genetic adaptation to
urban conspecific populations is increasingly documented urban environments concerns the annual plant Chamaecrista
for a wide range of morphological, physiological and fasciculate. This species engages in mutualistic interactions
behavioural traits (e.g. Slabbekoorn & den Boer-Visser, with ants; the plant provides ants with food from extra-
2006; Angilletta et al., 2007; Evans et al., 2009b,c; reviewed floral nectaries, and the ants feed on herbivorous insects
by Evans, in press). These studies provide evidence regarding that attack the plants. Urban plants have significantly fewer
the magnitude to which selection pressures differ between extra-floral nectaries than rural ones as there are fewer

Biological Reviews 85 (2010) 643667 2010 The Authors. Journal compilation 2010 Cambridge Philosophical Society
648 K. L. Evans and others

herbivorous insects in urban areas. Experiments indicate that rural areas have reduced fitness relative to urban individuals
this trait divergence between urban and rural populations that remain in an urban area (Evans et al., 2009a).
arises entirely from genetic adaptation, and not plasticity or The third factor that may regulate the rate of genetic
epigenetic effects (Rios, Marquis & Flunker, 2008). adaptation to urban areas is gene flow, which can prevent
Species will adapt rapidly to urban environments in genetic adaptation to local conditions by swamping evolving
those, probably relatively few, cases where phenotypic locally adaptive genotypes (Postma & Van Noordwijk, 2005;
plasticity is sufficient for complete adaptation. Plasticity will Rasanen & Hendry, 2008). To assess the potential for this
probably also facilitate most other urbanisation events by in the specific context of urban populations we compiled
increasing the ability to persist in urban environments, whilst data on gene flow between urban and rural populations.
further beneficial adaptation occurs through genetic change. Table 1 shows that such populations are rarely panmictic,
However, much additional work is required to assess the but gene flow is frequently marked, suggesting that there
extent to which such genetic adaptation facilitates adjustment is often the potential for genetic adaptation to urban
to urban environments. environments to be hindered by gene flow from rural
populations. However, divergent selection pressures can
(c) Species traits enable local genetic adaptations to arise despite strong gene
flow (e.g. Garant et al., 2005; Senar et al., 2006), and barriers
Ecologically flexible species are more likely than specialists to to gene flow can evolve rapidly in sympatric populations (i.e.
exhibit sufficient plasticity to cope with the novel urban envi- within dozens of generations; Hendry, Nosil & Rieseberg,
ronment. Indeed, generalists appear to contribute dispro- 2007). The extent to which gene flow from rural populations
portionately to urban assemblages (Bonier et al., 2007; Kark prevents local adaptation to urban environments is thus
et al., 2007; K.L. Evans, D.E. Chamberlain, B.J. Hatchwell, uncertain, and assessing the magnitude of this effect is another
R.D. Gregory & K.J. Gaston, unpublished data). Behavioural major challenge for urban ecology.
flexibility may also play a role in adjustment to urban areas.
This trait is linked to relative brain size in birds and mam-
mals, which can predict a species ability to invade areas (3) Spread
outside their natural range, and their response to rapid envi- The third and final stage of urbanisation concerns the spread
ronmental change (Shultz et al., 2005; Sol et al., 2005). So far, of populations that have adjusted to urban environments;
however, studies have failed to find an association between broadly speaking, this spread may arise through two
relative brain size and avian species responses to urban mechanisms. First, through independent urbanisation events,
areas (Kark et al., 2007; K.L. Evans, D.E. Chamberlain, B.J. thus limiting this final stage to spread within an urban area.
Hatchwell, R.D. Gregory & K.J. Gaston, unpublished data). Alternatively, urbanisation may follow a leap-frog model
When adjustment requires genetic adaptation three factors in which urban environments are colonised by individuals
will determine the rate at which this genetic change occurs. from other urban populations that disperse over or through
The first concerns life-history traits that are associated with rural environments. This could occur because individuals
rapid rates of evolution, the most prominent ones are sexual are adapted to urban habitats, and/or because they are
reproduction and fast reproductive rates; notably, both of imprinted on them (Davis, 2008); such a leap-frog model is
these traits facilitate adaptation in invasive exotic species more likely to generate a strong spatial pattern in timing of
(Nikolaev et al., 2007; Barrett, Colautti & Eckert, 2008). urbanisation than independent urbanisation events.
Other life-history traits may promote faster evolution, for In the leap-frog model the spread of urbanised populations
example intense sexual selection may do so by increasing will partly be determined by the spatial configuration of
mutation rates, but the evidence for this effect is more urban areas, with faster rates of spread expected where
equivocal (Ellegren, 2007; Petrie & Roberts, 2007). those areas are close together. Species traits influencing
Second, the magnitude of genetic diversity limits the rates of dispersal are likely to play a greater role in
capacity of populations to adapt to novel conditions (Pujol & determining the rate of spread of urbanised populations
Pannell, 2008). Initial reduction in genetic diversity is likely in leap-frog urbanisation events than independent ones.
to occur as a consequence of founder effects associated with Leap-frog urbanisation is also more likely to occur in species
colonisation of urban areas by a small number of individuals. that require genetic change to adjust to urban areas; this is
To assess the scale of this effect, we compiled data on the rel- because the genetic adaptations will already be present in
ative genetic diversity of urban and rural populations. These the colonising individuals from urban populations, but not
data certainly indicate that genetic diversity is more limited in those that originate from rural populations.
in many, but not all, urban populations compared to nearby
rural ones (Table 1). Mutation and immigration from rural
(4) Positive and negative feedbacks between stages
populations may subsequently enable urban populations to
recover genetic diversity, at least partially. This has been Factors influencing the three urbanisation stages may be
documented for the red fox Vulpes vulpes (Wandeler et al., correlated with each other. This is perhaps most obviously
2003). By contrast, urban blackbird populations appear to the case for environmental factors. Regions with a high
become increasingly isolated from nearby rural birds over proportion of urbanised land are likely to have longer his-
time; this pattern may arise if urban birds that disperse to tories of urban development, and shorter distances between

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A conceptual framework for the colonisation of urban areas 649

Table 1. Changes in genetic diversity of urban populations relative to nearby rural ones. A, number of alleles; AR , allelic richness;
Ha, number of haplotypes; H, Shannons diversity index; HaD , haplotype diversity; Ho , observed heterozygozity; GD, Neis gene
diversity; GI, mean number of genotypes per individual; H, Shannons diversity index; PB, percentage of polymorphic bands; PL,
percentage of polymorphic loci. Genetic divergence is measured by FST , and its related metric PT , Neis genetic distance DS (Nei
1978), and the Nei and Li distance coefficient DNL (Nei & Li 1979). Ns, not significant

Change in urban
Group Species Region genetic diversity Genetic divergence Source
Plants the moss Leptodon smithii Italy Ha -36%, PL -20% FST 0.37 Spagnuolo et al. (2007)
McGillivray Grevillea Australia A +95%, Ho +27% n/a Roberts et al. (2007)
macleayana
common dandelion USA GI -41% n/a Keane et al. (2005)
Taraxacum officinale
broad-leaved Scotland A -10%, Ho -29% n/a Hollingsworth & Dickson
helleborine Epipactis (1997)
helleborine
rue-leaved saxifrage Germany ns (GD, H, PB) PT 0.30 Reisch (2007)
Saxifraga tridactlites
downy yellow violet USA ns (H, PL) DNL 0.45 Culley et al. (2007)
Viola pubescens
Invertebrates small white butterfly Japan ns (PL) n/a Takami et al. (2004)
Pieris rapae
the butterfly P. melete Japan ns (PL) n/a
the ground beetle UK ns (AR , Ho ) n/a Desender et al. (2005)
Pterostichus madidus
Belgium ns (AR , Ho ) n/a
the ground beetle Abax UK AR -15%, Ho -88% n/a
ater
Belgium ns (AR , Ho ) n/a
Amphibians the frog Leptodactylus GD -46%, PB -32% DS 0.21 Aruda & Morielle-Versuta
ocellatus (2008)
the frog L. fuscus GD -10%, PB -8% DS 0.04
the frog L. podicipinus GD +50%, PB +37% DS 0.04
the frog L. labyrinthicus GD +11%, PB +6% DS 0.06
common toad Bufo bufo UK A -22%, Ho -15% n/a Hitchings & Beebee (1998)
common frog Rana UK A -10%, Ho -25% n/a Hitchings & Beebee (1997)
temporaria
red-backed salamander Canada A -29%, AR -39%, FST 0.19 Noel et al. (2007)
Plethodon cinerus Ho -34%
Reptiles caissaca viper Bothrops Brazil PL -28% FST 0.19 Dutra et al. (2008)
moojeni
Blandings turtle USA PB -18% n/a Rubin et al. (2001)
Emydoidea blandingii
Birds dark-eyed junco Junco USA AR -41%, Ho -21% n/a Rasner et al. (2004)
hyemalis
blackbird Turdus merula Western AR -3% to -20%, FST 0.00 to 0.04, DS Evans et al. (2009a)
Palearctic Ho +8% to -11%, 0.00 to 0.07,
depending on city depending on city
Eurasian kestrel Falco Poland AR -10%, Ho -8% FST 0.05 Rutkowski et al. (2006)
tinnunculus
Mammals large Japenese field Japan Ha -77%, HaD - 71% FST 0.49 Hirota et al. (2004)
mouse Apodemus
speciosus
red fox Vulpes vulpes Switzerland A -14%, Ho -17% FST 0.04 Wandeler et al. (2003)

urban areas, than less developed regions; all these factors have large geographic ranges (Gaston, Blackburn & Lawton,
will positively influence both the arrival and spread stages 1997; Blackburn, Cassey & Gaston, 2006), which will further
of urbanisation (Fig. 1). Positive correlations may also exist increase the probability of arrival in urban areas as larger
between species traits, for example, species with high pop- ranges increase the probability of a species range encompass-
ulation densities are more likely to arrive in urban areas ing towns and cities, and these species tend to have greater
(Fig. 1) because such species will have a larger number of dispersal ability (Gaston, 2003). Species with high population
dispersive offspring. These abundant species also tend to densities also tend to use resources that are abundant in the

Biological Reviews 85 (2010) 643667 2010 The Authors. Journal compilation 2010 Cambridge Philosophical Society
650 K. L. Evans and others

environment (Gregory & Gaston, 2000), increasing the prob- also important. Such studies are difficult to conduct because
ability that they will occur in urban areas, thus reducing the the arrival of many species in urban areas is unlikely to have
difference between urban and rural areas and the amount of been consistently recorded throughout a region. For native
adjustment to the former that is required (Fig. 1). species this is no doubt partly because the process is internal
Species traits that influence the urbanisation process to the geographic range. Thus an urbanising species will
may, however, have opposing effects on the three stages be familiar to observers from rural areas, perhaps reducing
of urbanisation. For example, high dispersal rates promote the likelihood of its initial occurrence in urban areas being
arrival in urban areas (Fig. 1), but may hinder adjustment documented. The speed at which urbanisation occurs may
for two reasons. First, selection pressure in urban areas also have an influence on the probability of the process being
can favour reduced dispersal (Cheptou et al., 2008). Second, recorded, with gradual urbanisation events being less likely
species with strong dispersal abilities will experience marked to be noted.
gene flow between urban and rural populations that may The blackbird is a widespread Palearctic thrush (Fig. 2).
hinder the evolution of locally adaptive genotypes (see It originally inhabited forests, but is now common in urban
Section II. 2c). The rate of progression though each stage areas throughout much, but not all, of its geographic range
of the urbanisation process may thus correlate negatively. (Luniak et al., 1990). Due to the species conspicuousness
The presence of such complex interactions between traits and ease of identification there is a wealth of literature
that influence different stages of the urbanisation process documenting its arrival in urban areas; it thus provides a
emphasise the importance, when sufficient data are available, notable exception to the dearth of detailed data on the timing
of considering each stage independently when assessing of urbanisation events. Whilst there have been attempts to
which ecological or life-history traits promote urbanisation. review this literature (Heyder, 1955; Luniak et al., 1990),
much of it remains obscure and highly dispersed, and no
formal analyses of spatial and temporal patterns have been
conducted. Here we synthesise the available information to
III. THE BLACKBIRD TURDUS MERULA provide a formal case study documenting the spatial and
AS A CASE STUDY temporal spread of urban populations across much of a
species range. We use these data to analyze spatial patterns
A failure to recognise the three separate stages of the in the timing of urbanisation, to record the rate at which
urbanisation process has undoubtedly hindered studies of the habit of occupying urban areas has spread through the
urban colonisation, but the lack of detailed case studies is species range, and apply our conceptual framework of the

Fig. 2. The distribution of subspecies in each of the four species in the Eurasian blackbird species complex: (i) Eurasian blackbird:
E At Turdus merula aterrimus, E Az T. m. azorensis, E Ca T. m. cabrerae, E In T. m. intermedius, E Ma T. m. mauritanicus, E Me T. m.
merula, E Sy T. m. syriacus; (ii) Tibetan blackbird: T Ma Turdus maximus maximus; (iii) Chinese blackbird: C Ma Turdus mandarinus
mandarinus, C So T. m. sowerbyi; and (iv) Indian Blackbird I Bo Turdus simillimus bourdilloni, I Ki T. s. kinisii, I Ni T. s. nigropileus and
I Si T. s. simillimus. The position of Australasia, in the inset, has been moved for presentation purposes.

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A conceptual framework for the colonisation of urban areas 651

urbanisation process to these data to discuss the underlying 2006). We thus conduct analyses using both the entire dataset
factors driving the urbanisation process in relation to its three (N = 81 locations), and data restricted to the nominate
different stages. subspecies (N = 68 locations). Data were insufficient to
conduct separate analyses for other blackbird sub-species.
(1) Data compilation and assessment Sample sizes are smaller than those used to produce country
summaries (Appendix A) due to the repetition of data from
Data on blackbird urbanisation dates were obtained different sources, and exclusion of data with insufficiently
using five methods. First, we consulted material in the precise urbanisation dates.
Alexander Library at the Edward Grey Institute of Field A strong spatial pattern in the timing of urbanisation is
Ornithology, Oxford University; this is arguably the best less likely to arise if urbanisation occurs independently than
ornithological library in the world relating to the focal if it occurred in a leap-frog manner (Section II. 3). We thus
region. For each country within the range of the blackbird assessed the strength of any spatial pattern by regressing
we searched country-specific reprint collections, regional urbanisation date against latitude and longitude using linear,
handbooks and local ornithological journals. Second, we quadratic and cubic terms for each predictor. Within our
consulted all papers in our research groups collection data latitude and longitude were weak predictors of each
on urban ecology and urbanisation. Third, we referred other (all data r 2 = 8%; nominate subspecies r 2 = 10%), thus
to the citations in papers obtained using the above analyses are not influenced strongly by colinearity. We used
methods. Fourth, we corresponded with local ornithologists. an information theoretic approach to model building, and
Finally, using Web of Knowledge (WoK) we conducted followed standard protocols (Burnham & Anderson, 2002;
searches using the terms Turdus* AND urban* and Johnson & Omland, 2004). We constructed all possible
Turdus* AND town*; equivalent searches were conducted models given our set of predictor variables, and using
on the Ornithological Worldwide Literature (OWL) database Akaike Information Criteria (AIC) values we calculated each
(http://egizoosrv.zoo.ox.ac.uk/OWL/default.htm), which models weight, i.e. the probability that it provides the most
focuses on the grey literature. parsimonious fit to the data. The smallest number of models
Following del Hoyo, Elliott & Christie (2005) we recognize whose cumulative weights summed to 0.95 was included in
seven sub-species of Turdus merula (Fig. 2), although it is the 95% confidence set of models, and model averaging was
not always possible to delimit precisely the geographic conducted to assess the influence of predictor variables on
range boundaries of the continental subspecies due to urbanisation date. All analyses were conducted using SAS
clinal variation (Cramp, 1988). Three taxa have recently (v. 9.1).
been recognized as distinct species but were previously We compared the rate of spread of urban blackbird
considered to be conspecific with T. merula, these are Tibetan populations, i.e. internal range expansion, to the rate
blackbird T. maximus and Indian blackbird T. simillimus (split of documented avian range expansions that have been
from T. merula by both Clement et al., 2000 and del Hoyo external to a species original geographic range. To facilitate
et al., 2005) and Chinese blackbird T. mandarinus (which is discussion of the environmental factors determining the rate
regarded as a separate species by Clement et al., 2000). of spread of blackbird urbanisation we also assessed regional
Of these only T. mandarinus is urbanised (del Hoyo et al., variation in its magnitude. A formal analysis of rate of spread
2005; A. Clements, personal communication; J. Hornskov, assumes that urban birds moved throughout the species
personal communication), but we do not consider these taxa range from a single locality. This assumption is most likely to
in the rest of this paper. be valid for blackbirds if data are restricted to a single sub-
In total we collated over 120 references to blackbird species. The first records of urbanisation by the nominate
urbanisation. We use the names of geopolitical units and race are from Bamberg and Erlangen (Germany) in 1820,
towns/cities as listed in the Times Comprehensive Atlas of the which are located 34 km apart. We calculated the annual rate
World (2000). Latitude and longitude for each location were of spread from the mid-point between these two localities to
obtained from the Google Earth mapping service. When every urban population of T. merula merula for which we could
urbanisation dates referred to a specific region, rather than estimate the timing of urbanisation. We then calculated the
a town or city, we used the latitude and longitude of the overall mean rate of spread, and assessed if this differed for
town closest to the geographic centre of the focal region. The localities to the east and west of the initial urbanisation event.
pattern of urbanisation in each geopolitical unit is described
in Appendix A.
(2) Spatial and temporal patterns
The literature tended to state a range of possible
urbanisation dates. In statistical analyses we used the mid- There is a strong spatial pattern in the timing of blackbird
point of any such ranges, but discarded data when the date urbanisation (Fig. 3). When data from all sub-species were
range exceeded 50 years; although in the vast majority of pooled together three models were retained in the 95%
cases the date range was much smaller than this. The extent of confidence set (Table 2). Model averaging revealed that
genetic differentiation and gene flow between each subspecies total explanatory power was high (r 2 = 76%). Urbanisation
of the blackbird is uncertain; indeed, many avian subspecies date was not strongly related to latitude (model averaged
described from the Western Palearctic do not represent partial r 2 = 7%; Fig. 4A), but was strongly related to
independent genetic units (Zink, 2004; Phillimore & Owens, longitude in a positive decelerating manner (model averaged

Biological Reviews 85 (2010) 643667 2010 The Authors. Journal compilation 2010 Cambridge Philosophical Society
652 K. L. Evans and others

Fig. 3. Timing of urbanisation in the Eurasian blackbird Turdus merula. Each panel represents a different time period (A) 18201849,
(B) 18501879, (C) 18801909, (D) 19101939, and (E) 1940 onwards. Circles represent urban locations for which data are
available. Black circles indicate the presence of urban blackbirds, and grey ones their absence. In E a grey circle represents the
absence of urban blackbirds by 2000. The position of Iceland, in the inset, has been adjusted for presentation purposes.

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A conceptual framework for the colonisation of urban areas 653

Table 2. Results of multiple regression analyses of spatial patterns in the urbanisation dates of blackbird Turdus merula, magpie Pica
pica, and woodpigeon Columba palumbus. The linear, quadratic and cubic terms of latitude (lat) and longitude (long) were used as
predictors. Model selection followed an information theoretic approach, and for each response variable we present all models in the
95% confidence set

lat lat2 lat3 long long2 long3 model weight model r 2 (%) partial r 2 lat (%) partial r 2 long (%)
T. merula all populations + + 0.88 76.15 7.34 41.50
+ + + 0.04 76.65 7.84 41.08
+ + 0.03 72.81 4.00 72.73
T. m. merula only + + + 0.37 73.28 5.58 24.99
+ + 0.22 71.03 10.36 22.74
+ + 0.17 71.39 3.69 33.95
+ + 0.10 73.27 5.76 24.98
+ + 0.04 71.36 3.85 33.92
+ + 0.02 67.45 6.78 30.01
+ + 0.02 74.07 6.23 25.78
Pica pica + 0.65 13.45 0.00 13.45
+ 0.20 13.49 0.04 13.45
0.12 0.02 0.02 0.00
Columba palumbus + + + 0.40 39.85 7.35 35.20
+ + 0.18 36.15 3.65 35.38
+ + + + 0.16 39.86 7.36 35.21
+ + + 0.07 36.17 3.66 35.40
+ 0.06 34.93 2.43 34.17
+ + + + 0.06 45.13 7.56 40.48
+ 0.02 34.96 2.46 34.20

(A) (B)

(C) (D)

Fig. 4. Relationships between known dates of Eurasian blackbird Turdus merula urbanisation across the species range and (A) latitude
and (B) longitude, and for only the nominate sub-species with (C) latitude and (D) longitude. Note the variation in the scale of the x
axes.

Biological Reviews 85 (2010) 643667 2010 The Authors. Journal compilation 2010 Cambridge Philosophical Society
654 K. L. Evans and others

partial r 2 = 43%; Fig. 4B). When restricting data to the In some regions, urbanisation was probably independent
nominate subspecies seven models were retained in the from that in Europe. The most likely candidates
95% confidence set (Table 2). Model averaging revealed for populations exhibiting independent urbanisation are
that total explanatory power was high (r 2 = 72%). Latitude T. merula azorensis and T. merula cabrerae, subspecies that
(partial r 2 = 6%; Fig. 4C) explained less of the variation in are confined to Atlantic islands (the Azores, Canaries and
urbanisation date than longitude (partial r 2 = 27%; Fig. 4D), Madeira) that are outside the normal wintering range of other
which was related to urbanisation date in a more linear blackbird populations. Another strong case for independent
manner than when data from all subspecies were used. urbanisation is the north-west African subspecies, T. merula
Blackbirds were thus urbanised earlier in the west of their mauritanicus. Urban blackbirds were common in this region
range than in the east, and to a lesser extent were urbanised within 70 years of the first urbanisation events being
earlier in the south than in the north. In nine countries documented in Europe, at localities approximately 1,700 km
occupied by the nominate subspecies the timing of blackbird away. The mean adult and natal dispersal distances of
urbanisation is closely associated with an increase in the blackbirds are 3.2 km and 3.3 km respectively (Paradis et al.,
species geographic range or population size in the wider 1998). Whilst dispersal over much longer distances occurs,
landscape (Appendix A). When these data are excluded it is a rare event. Paradis et al. (1998) recorded a maximum
from analyses the timing of urbanisation remains strongly dispersal distance of 300 km between breeding sites for adults
associated with longitude (model averaged partial r 2 = 49%), (N = 1,800), and 350 km for first-year birds (N = 2,200).
and poorly associated with latitude (model averaged partial Given the very small number of urban blackbirds in Europe
r 2 = 0.4%). at the start of the urbanisation process it is highly unlikely
The overall mean rate of spread of blackbird urbanisation that sufficient individuals could have colonised north-west
within the range of the nominate subspecies was 7.7 Africa and started the urbanisation process there. Indeed,
0.7 km per year (mean S.E.M). Spread was faster to the mean rate of spread to the west, i.e. in the direction of
the west (10.1 1.7 km per year, N = 23) than to the east Tunisia, from the first urbanisation event is just 10 km per
(6.5 0.6 km, N = 42); the 84% confidence intervals of these year. A much faster rate of spread (approximately 25 km
estimates do not overlap and the difference is thus statistically per year) would be required if urbanised blackbirds from the
significant at = 0.05 (Payton, Greenstone & Schenker, site of the first documented urbanisation events in Germany
2003). This pattern remains when data from countries in were to have reached Tunisia at the time of blackbird
which the blackbird has experienced more general range urbanisation in that country. Therefore, in combination,
expansions are excluded from analyses (westerly spread the data strongly suggest that within the range of T. merula
10.0 2.0 km per year, N = 20; easterly spread 5.3 urbanisation happened independently in north-west Africa
0.7 km per year, N = 32; again 84% confidence intervals do and Europe. Urbanisation events in other subspecies (i.e.
not overlap). T. merula aterrimus, intermedius and syriacus) would also be
independent if these taxa are genetically distinct from the
(3) Independent or leap-frog urbanisation? nominate subspecies. There is no evidence for this, however,
and many avian subspecies that have been described from
The strong spatial pattern in the timing of blackbird
Europe are not genetically distinct (Zink, 2004; Phillimore &
urbanisation is predicted by the leap-frog urbanisation model
Owens, 2006).
in which individuals from an established urban population
Therefore, despite the strong spatial signal in the
colonise other built-up areas either because they are adapted
urbanisation of blackbirds across their Western Palearctic
to such areas, or because they are imprinted on them.
range, independent colonisation of urban areas has almost
However, spatial patterns in the timing of urbanisation
certainly occurred in parts of that range. Furthermore,
cannot, in isolation, confirm a particular urbanisation
model, and it is important to consider other evidence. The analysis of the genetic structure of paired urban and rural
introduction of rural blackbirds to previously uncolonised blackbird populations does confirm that urbanisation has
urban areas failed in Bialystok and Olsztyn (north-east often occurred through multiple independent colonisations
Poland), whilst the introduction of urban blackbirds to other of towns and cities from nearby rural populations (Evans
uncolonised cities, Lublin in south-east Poland and Kiev in et al., 2009a).
Ukraine, succeeded (Grachyk et al., 1975; Graczyk, 1982).
This suggests that urban blackbirds, relative to rural ones,
are more likely to colonise built-up areas. Indeed, urban IV. APPLYING THE CONCEPTUAL
blackbirds exhibit some adjustments to towns and cities that FRAMEWORK TO THE BLACKBIRD
probably arise, at least in part, from genetic adaptation
(Partecke et al., 2006; Partecke & Gwinner, 2007). The
(1) Stage 1 - arrival
genetic basis of such urban adaptations may explain why
introductions of rural blackbirds to urban environments Throughout Europe, cities existed long before blackbirds
failed; however, an effect of climate cannot be ruled out, and other avian species became urbanised. For example,
as the failed introductions were also to colder environments London occupied 2 km2 in 1300, over 4 km2 by 1673, and
than the successful ones. 12.5 km2 by 1819 (Shepherd, 1300; Blome, 1673; Howgego,

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A conceptual framework for the colonisation of urban areas 655

1978; Fitter, 1990), yet blackbirds did not become common in annual productivity between urban and rural blackbird
English city centre gardens until the 1920s and 1930s (Simms, populations (Chamberlain et al., 2009), suggests that urban
1978; de Laet, 2000). Below we discuss the mechanisms habitats are currently no less preferable than rural ones. This
that may have contributed to the long time lag between was probably also true in the past as there are historical
the development of urban areas and their colonisation by reports of high blackbird densities in urban areas (Heyder,
blackbirds. 1955; Luniak et al., 1990).
The first stage of urbanisation is arrival in urban areas Blackbirds frequently first arrived in urban areas in the
(Fig. 1). In much of Europe blackbirds appear to have been winter (e.g. Glaser, 1871; Fallon, 1875; le Rabe, 1886;
reasonably abundant in rural areas for hundreds of years Collett, 1921; Heyder, 1955; Graczyk, 1959; Rabose et al.,
before urbanisation (Appendix A), and it is unlikely that a 1995). A similar situation still applies; for example, blackbirds
lack of dispersal into built-up areas limited the potential for occur in the centre of Montpellier (France) in winter, but
urbanisation to commence. However, this is not the case in do not yet breed there. Other avian studies also document
northern and eastern Europe where a marked increase in the that breeding in towns is preceded by winter occurrences,
size of blackbird populations and their range has occurred in examples include the hill pigeon Columba rupestris (del Hoyo,
nine countries (Belarus, Denmark, Estonia, Finland, Iceland, Elliott & Sargatal, 1997), dark-eyed junco Junco hyemalis
Latvia, Lithuania, Norway and Sweden). This process started (Yeh, 2004), and mallard Anas platyrhynchos (Pulliainen, 1963).
in Denmark and Norway approximately 150 years ago, and Counter examples are available, such as the woodpigeon
spread eastwards and northwards; blackbirds are currently (Tomiaojc, 1976), but at least in temperate regions the typical
much commoner throughout Scandinavia, the Baltic states first step in avian urbanisation may be wintering in urban
and Iceland than previously. This range expansion is linked areas. Temperate urban areas are likely to be particularly
to climatic amelioration and habitat conversion (Jarvinen advantageous in winter, compared to rural ones, due to
& Vaisanen, 1979; Burton, 1995; Newton, 2003). Also, higher temperatures, and human activities that increase food
in Denmark the Game Act of 1849 prohibited catching availability. The latter may occur directly through provision
blackbirds and the species population increase commenced at bird feeders, or indirectly by activities such as planting of
shortly after the acts introduction (Lppenthin, 1967). In trees that produce berries or fruit, and clearing areas of snow
eight of the nine countries (Belarus is the exception) in which that facilitates foraging by ground-feeding birds.
blackbirds have markedly increased their range, urbanisation Many blackbirds in northern and eastern Europe are
has occurred within two decades of the range expansion. This migratory, and this proportion was even higher in the past
suggests that a delayed arrival in urban areas, due to a small than is the case today (Rivalan et al., 2007; van Vliet, Musters
number of potential colonisers in the wider landscape, may & ter Keurs, 2009). The small number of resident blackbirds
have slowed the urbanisation process in north-east Europe. in north-east Europe, prior to urbanisation, may thus have
It is notable, however, that the strong spatial pattern in the further limited the number of individuals that could have
timing of urbanisation remains even when data from these undertaken the initial urbanisation step by wintering in
nine countries are excluded from analyses. local towns. It is also possible that urbanisation began
in central Europe due to the combination of a sufficient
Other Turdus species also exhibit a close similarity in the
number of resident blackbirds that could start the process,
timing of range expansion and urbanisation, including the
and sufficiently cold winters to provide a greater selective
fieldfare T. pilaris (Section V. 2a) and kurrichane thrush
advantage in doing so compared to warmer regions elsewhere
T. libonyana (Vernon, 1997). More generally, urbanisation
within the species range.
of the woodpigeon, magpie, sparrowhawk Accipiter nisus and
peregrine in the UK is associated with population increases,
often following recovery from persecution and accidental (2) Stage 2 - adjustment
poisoning (Newton, 1986; Marchant et al., 1990; Ratcliffe, The lag between the development of urban areas and
1993; Wilson, 1993). Similarly, the number of goshawk blackbird urbanisation may also have arisen if time is
observations in Hamburg and surrounding rural areas required for blackbirds to adjust to urban areas. In areas of
increased simultaneously (Rutz, 2008), and urbanisation Europe where its arrival is unlikely to have been limiting this
of the black woodpecker Dryocopus martius in Hungary is time-lag may have occurred because of factors that influence
associated with range expansion (Gorman, 1998). It is thus the rate of adjustment to urban environments (Fig. 1). First,
plausible that in many cases the initial arrival stage of the urban environments are dynamic and their characteristics
urbanisation process may be a response to high population may have changed over time in a manner that favoured
densities in rural habitats increasing the number of potential blackbirds, and thus increased the extent to which they were
colonisers, and possibly the selection pressure to colonise pre-adapted to urban areas (Fig. 1). Second, urbanisation
other areas (Fig. 1). This process has some similarities to the may have required genetically determined adaptations that
buffer effect (Brown, 1969), in which a species colonises new took time to evolve (Fig. 1). These mechanisms are not
habitats when the preferred ones are saturated. However, mutually exclusive and we consider each in turn.
the higher densities of blackbirds, and some other species, The dynamic nature of towns and cities means that habitat
in urban areas than rural ones (Tratalos et al., 2007; Evans availability and quality may have improved over time. In
et al., 2009d), and the lack of a significant difference in 1895 blackbirds were rarely present in Neisse (Germany)

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656 K. L. Evans and others

but numbers increased soon after the establishment of parks, (Pulliainen, 1963). One British study has demonstrated that in
and by 1906 the species was a common breeder (Kollibay, urban areas the total breeding density of all bird species that
1906). Blackbirds reach higher densities in urban areas with take supplementary food, including the blackbird, increases
more green space and a greater proportion of trees and with the density of feeding stations (Fuller et al., 2008).
shrubs, although the strength of such relationships appears However, it is uncertain if such patterns are causal as they
to be scale dependent (Karlsson & Kallander, 1977; Mason, may arise because people provide more food where there
2003). Increased availability of bushy vegetation also appears are more birds. Unfortunately, it is not possible to correlate
to promote recruitment into the breeding population, and the timing of blackbird urbanisation with when feeding of
such areas are preferred as breeding territories (Fernandez- garden birds started because insufficient data are generally
Juricic & Telleria, 1999; Wysocki et al., 2004). It is thus highly available [although it commenced in Finland at the end of the
likely that changes in the nature of some urban areas would 19th Century (Vuorisalo, Lahtinen & Laaksonen, 2001), i.e.
have increased their suitability for blackbirds. For example, in a few decades prior to blackbird urbanisation]. Moreover,
Britain many parks were created in urban areas between the the provision of supplementary food is unlikely to have
1830s and early 1900s (Jordan, 1994; Taylor, 1995), which been a consistently important factor in promoting blackbird
broadly coincides with when the species became urbanised urbanisation as this activity is still rare in many regions of
(Appendix A). eastern Europe that contain urbanised populations.
The extent to which such changes were essential for Concerning less positive human attitudes, the lack of
blackbird urbanisation is, however, debatable. Historical urban blackbirds in south-east France has previously been
descriptions of urban areas suggest that suitable habitat for attributed to the high levels of persecution of Turdus species
breeding blackbirds was present many decades before they in this region (Ingram, 1926). Other authors have also linked
colonised cities. For example, Aeneas Sylvius Piccolomini urbanisation to a change in levels of human persecution,
described the presence of rich flower gardens and orchards albeit in combination with habitat alteration. For example,
in the German towns of Erfurt, Frankfurt, Nuremberg and Holloway (2002) states that at the end of the 19th Century
Augsburg in 1485 (Landau & Schneider, 1928). Similarly, a switch from using suburban gardens for growing food
large parks in central London, such as St. Jamess Park and to planting of ornamental shrubs and plants that provided
Hyde Park, were broadly similar in the early 1700s to their better nesting sites was associated with reduced persecution,
appearance today (Fitter, 1990). The successful introduction and probably allowed blackbirds to become tamer, and thus
of blackbirds to urban environments which previously lacked to start adapting to urban environments. Similarly, in the
them, such as Poznan and Kiev (Grachik et al., 1975; 1930s in Belgium, the blackbird was much commoner in
Graczyk, 1982), is clear evidence that urbanisation does urban gardens with shrubs than in village gardens where
not always occur as soon as conditions are suitable. In vegetables were grown, perhaps due to improved habitat
addition, the blackbird and song thrush Turdus philomelos structure and reduced persecution (Morbach, 1939). Rural
have similar habitat requirements (their densities in urban persecution is certainly associated with the occurrence of
areas of the United Kingdom are positively correlated; Evans urbanised populations of other species (Section II. 1), but
et al., 2009d), but song thrushes are urbanised in Moscow there is insufficient evidence to suggest that the timing of
and blackbirds are not. This strongly suggests that a lack blackbird urbanisation is a consequence of changes in human
of suitable habitat has not prevented the urbanisation of attitudes.
blackbirds in some regions. A greening of urban areas The second suite of factors influencing the rate of progress
also appears unlikely to explain the timing of urbanisation through the adjustment stage of urbanisation concerns the
in some woodpigeon populations. Both the blackbird and extent to which genetic adaptation is required, and the rate
woodpigeon are originally woodland species, and their at which such adaptations can arise. Avian body size has a
densities in urban areas of Britain are strongly correlated strong genetic basis (Glazier, 2002), and some populations of
(Evans et al., 2009d), suggesting that they have similar habitat urban blackbirds are morphologically divergent from their
preferences in cities. However, the blackbird colonised rural counterparts (Gregoire, 2003). However, blackbirds do
Munich 90 years before woodpigeons did, suggesting that not appear to require any specific morphological adaptations
suitable habitat was present for the latter species many to become established in urban areas (Evans et al., 2009b).
years prior to their arrival. Similarly, woodpigeons arrived By contrast, urban blackbirds have a reduced corticosterone
in Prague and Vienna respectively 55 and 60 years after stress response than rural ones, and rearing urban and
blackbirds. Therefore, although it is probable that improved rural individuals in a shared environment suggests that these
habitat conditions may have partly facilitated urbanisation differences have a genetic basis (Partecke et al., 2006). Also,
in some cases, this seems unlikely to have been a general a number of anecdotal reports state that urban blackbirds
factor. are more sedentary than rural ones (Bruch et al., 1978;
Another factor contributing to the dynamic nature of Luniak, 2004). Experimental studies have also found reduced
urban areas concerns changes in human activities related migratory restlessness in urban blackbirds relative to forest
to wildlife. It is possible that anthropogenic supplementary ones (Graczyk, 1961), and stable isotope analysis of migratory
feeding facilitated urbanisation in some regions, as is thought behaviour of paired urban and rural blackbird populations
to be the case for mallard wintering in urban areas in Finland indicates that the former are less migratory (K.L. Evans,

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A conceptual framework for the colonisation of urban areas 657

J. Newton, K.J. Gaston, S. Sharp, A. McGowan & B.J. urbanised species exhibit spatial variation in the occurrence
Hatchwell unpublished data). There is good evidence from and timing of their establishment.
many passerines that such changes in migratory strategy
require genetic change (Berthold et al., 1992), and rearing (1) What proportion of Turdus species are
experiments suggest that increased sedentariness in urban urbanised?
blackbirds partly has a genetic basis (Partecke & Gwinner,
2007). Therefore, at least some of the changes documented It is a common perception that avian genera differ in the
in urban blackbird populations probably require genetic extent to which they are urbanised, but there has been
adaptation, but early maternal effects cannot be excluded little formal assessment of variation in the proportion of
(Partecke et al., 2006; Partecke & Gwinner, 2007). Whether urbanised species in different genera, and of whether this
such changes were requirements for urbanisation to succeed, is consistent across faunal regions. Here, we conduct a
or if they arose following urbanisation is unknown. It is preliminary assessment of these issues. We compare the
thus not possible to conclude that the need for genetic Turdus genus to Corvus, which is often considered to be
adaptation has contributed to the time required for blackbirds one of the most highly urbanised avian genera (Marzluff,
to adjust to urban areas, but such effects are certainly 2001), and Columba which contains one of the most highly
possible. urbanised bird species in the world, the feral pigeon
C. livia.
Data on habitat use by each species of Turdus, Corvus and
(3) Stage 3 - spread Columba in their native ranges were obtained by consulting
We provide the first estimate of the rate of avian range recently published guides to each genus (Turdus: Clement
expansion that is internal to a species geographic range, i.e. et al., 2000; del Hoyo et al., 2005; Corvus: Madge & Burn,
colonisation of unoccupied areas within a species original 1994; Columba: del Hoyo et al., 1997; Gibbs, Barnes &
range. Assuming a leap-frog model we find that the mean rate Cox, 2001). We also searched Web of Knowledge (WoK)
of spread of urban blackbirds, 8 km per annum, is very similar and the Ornithological Worldwide Literature (OWL) database
to the median value documented for avian range expansions using the terms Turdus* AND urban* and Turdus* AND
that are external to species geographical ranges (6 km per town* and their equivalents for Corvus and Columba. We
annum, Table 3). This similarity may arise because both classified species as being fully urbanised if their habitat
internal and external range expansion involve dispersal and descriptions included towns, cities, urban or suburban
adaptation to novel areas with different ecological conditions areas, and being partly urbanised if they occurred in large
and may thus be limited by similar processes. As in studies gardens, villages, or on the edge of towns, cities or urban
of external range expansion we find geographical variation areas.
in the rate of spread. Urbanisation of T. m. merula has been Globally, there was marked variation in the proportion
more rapid in the west of its range than in the east. Part of of each genus that was urbanized. Urbanisation was most
this variation may be due to delayed arrival in eastern urban prevalent in Corvus and least common in Columba (Table 4).
areas. This is unlikely to be a consequence of the species Whilst this lends some support to the assertion that Corvus is
former rarity in parts of this region, because the rate of amongst the most highly urbanised of avian genera (Marzluff,
spread is still slower in the east when such areas are removed 2001), the genus does not contain significantly more fully
from the analysis. Spatial variation in migratory strategies urbanised species than the other taxa ( 2 = 1.50, P =
(Section IV. 1) may also contribute to variation in the rate 0.47), and the trend for Corvus to be more urbanised still
of spread, and the less urbanised nature of this region may only tended towards significance when partially and fully
have further slowed the urbanisation process by reducing the urbanised species were combined ( 2 = 4.91, P = 0.09).
number of focal points at which urbanisation could occur It is thus perhaps more appropriate to consider Corvus as
(Fig. 1). just one example of a highly urbanised genus. Corvids
are particularly intelligent, as evidenced by their relatively
large brain size, and the high rate at which they acquire
novel feeding adaptations (Emery, 2006). This behavioural
V. VARIATION IN URBANISATION - THE flexibility may be one factor contributing to their success in
BLACKBIRD IN A BROADER CONTEXT urban areas (Fig. 1).
The three genera differed with respect to which geographic
We place our analysis of blackbird urbanisation in a wider region contained the greatest proportion of urbanised species
context in two ways. First, we assess the extent to which (Table 4). The clearest example of this is that the Indo-Malay
other Turdus species are urbanised, and compare this to the region supports the greatest proportion of fully urbanised
proportion of urbanised species in other avian genera at Corvus species (50%), but that none of its ten Turdus species or
a global scale. We use these data to facilitate a discussion its six Columba species are fully urbanised. The mechanisms
of the environmental and biological traits that influence driving this variation are uncertain, but variation among
the probability of urbanisation. Second, in order to assess genera in the spatial congruence between species geographic
whether the patterns we describe for the blackbird can be ranges and urban areas may contribute to the pattern.
considered general, we assess the extent to which other Indeed, most Turdus species in the Indo-Malay region occur

Biological Reviews 85 (2010) 643667 2010 The Authors. Journal compilation 2010 Cambridge Philosophical Society
658 K. L. Evans and others

Table 3. Mean rates of spread for avian range expansions external to species original ranges. Data include natural range expansions
and those following introduction to non-native locations. When a range of rates is given this represents geographical variation,
for bronzed cowbird and great-tailed grackle it also includes temporal variation. In some species estimates vary between studies.
Additional papers describe or map range changes for other species, but no attempt has been made to calculate rates of change from
such data

Species Exotic Location Rate km year1 Source


Bewicks wren Thryomanes bewickii no North America 0.4 Hitch & Leberg (2007)
red kite Milvus milvus no Wales 0.5 Lensink (1997)
osprey Pandion haliaetus no Scotland 0.9 Lensink (1997)
tree sparrow Passer montanus yes North America 1 Williamson (1996)
summer tanager Piranga rubra no North America 1.6 Hitch & Leberg (2007)
marsh harrier Circus aeruginosus no England 2 Lensink (1997)
carolina chickadee Poecile carolinensis no North America 2.1 Hitch & Leberg (2007)
yellow-billed sapsucker Sphyrapicus varius no North America 2.2 Hitch & Leberg (2007)
buzzard Buteo buteo no UK & Holland 0.32.3 Lensink (1997)
Egyptian goose Alopochen aegyptiacus yes Holland 3 Lensink (1998)
sparrowhawk Accipiter nisus no UK & Holland 2.43.1 Lensink (1997)
blue-winged warbler Vermivora pinus no North America 3.3 Hitch & Leberg (2007)
bobolink Dolichonyx oryzivorous no North America 3.4 Hitch & Leberg (2007)
yellow-rumped warbler Dendroica coronata no North America 3.5 Hitch & Leberg (2007)
hooded warbler Wilsonia citrina no North America 4.4 Hitch & Leberg (2007)
peregrine Falco peregrinus no UK 1.14.5 Lensink (1997)
goshawk Accipiter gentiles no UK & Holland 1.54.5 Lensink (1997)
tree sparrow Passer montanus yes Australia 5 Blakers et al. (1984)
fish crow Corvus ossifragus no North America 5.1 Hitch & Leberg (2007)
willow flycatcher Empidonax trailii no North America 5.2 Hitch & Leberg (2007)
Swainsons thrush Catharus ustulatus no North America 5.4 Hitch & Leberg (2007)
Kentucky warbler Opornis formosus no North America 5.7 Hitch & Leberg (2007)
white-winged crossbill Loxia leucoptera no North America 6.1 Hitch & Leberg (2007)
Bachmans sparrow Aimophila aestivalis no North America 6.8 Hitch & Leberg (2007)
pine siskin Carduelis pinus no North America 7.1 Hitch & Leberg (2007)
alder flycatcher Empidonax alnorum no North America 7.4 Hitch & Leberg (2007)
golden-winged warbler Vermivora chrysoptera no North America 8.4 Hitch & Leberg (2007)
Inca dove Columbina inca no North America 9.8 Hitch & Leberg (2007)
black-billed cuckoo Coccyzus erythropthalmus no North America 10.6 Hitch & Leberg (2007)
blue-grey gnatcatcher Polioptila caerulea no North America 12.1 Hitch & Leberg (2007)
bronzed cowbird Molothrus aenus no America 6.213.8 Kostecke et al. (2004)
serin Serinus serinus no Europe 16.5 Margalef (1974)
yellow-breasted bunting Emberiza aureola no Europe 16.5 Timofeeff-Ressovsky (1940)
house sparrow P. domesticus yes North America 16.8 van den Bosch et al. (1992)
Brewers blackbird Euphagus cyanocephalus no America 17.5 Stepney & Power (1973)
house finch Carpodacus mexicanus yes North America 18.9 Mundinger & Hope (1983)
house finch Carpodacus mexicanus yes North America 20.8 Veit & Lewis (1996)
great-tailed grackle Quiscalus mexicanus no North America 12.722.6 Wehtje (2003)
house sparrow Passer domesticus no Europe 27.9 van den Bosch et al. (1992)
shiny cowbird Molothrus bonariensis no Caribbean 8.330.6 Post & Wiley (1977)
serin Serinus serinus no Europe 40 Olsson (1971)
collared dove Streptopelia decaoto no Europe 43.7 van den Bosch et al. (1992)
starling Sturnus vulgaris yes North America 91.6 van den Bosch et al. (1992)
cattle egret Bubuculus ibis no Americas 93.3 Kuyt (1971), Rodriguez- Mata (1973)
house sparrow Passer domesticus yes Australia 6100 Blakers et al. (1984)
cattle egret Bubuculus ibis no Americas 106.2 van den Bosch et al. (1992)
starling Sturnus vulgaris yes North America 200 Grosholz (1996)

in the extreme north where urban areas are rare, thus limiting (2) Spatial and temporal patterns in urbanisation in
the potential for species to become urbanised, whilst most other species
Corvus species in this region have large geographic ranges (a) Turdus
that overlap with many cities. This variation emphasises the
potential importance of the history of urban development in In many Turdus species urban populations do not occur
determining the potential for a species to become urbanised throughout a species geographic range. For example,
(Fig. 1). the mistle thrush T. viscivorus is absent as an urban

Biological Reviews 85 (2010) 643667 2010 The Authors. Journal compilation 2010 Cambridge Philosophical Society
A conceptual framework for the colonisation of urban areas 659

Table 4. Regional variation in the proportion of partly and fully urbanised Turdus, Corvus and Columba species in their native ranges.
The summed number of species in each region is greater than the global total as some species occur in more than one region. Data
are primarily from Madge & Burn (1994) for Corvus; from Clement et al. (2000) and del Hoyo et al. (2005) for Turdus; and from del
Hoyo et al. (1997) and Gibbs et al. (2001) for Columba. Biogeographic realms were defined following Olson et al. (2001)

Turdus Corvus Columba


% fully or % fully or % fully or
%fully partly % fully partly % fully partly
# species urbanised urbanised # species urbanised urbanised # species urbanised urbanised
Global 70 29 41 46 33 57 50 20 28
Afrotropics 9 33 44 6 17 33 13 15 39
Australasia 1 0 100 16 25 38 3 33 67
Indo-Malay 10 0 20 4 50 75 6 0 17
Nearctic 1 100 100 7 43 57 1 100 100
Neotropics 33 30 48 4 25 75 17 18 18
Oceania 0 n/a n/a 2 0 0 0
Palearctic 19 26 32 11 36 82 12 25 25

breeding species in many towns in eastern Europe, including The rufous-bellied thrush T. rufiventris is only urbanised in
St. Petersburg (Russia; Khrabryi, 2005) and Lublin (Poland; the south of its range, occurring in the centre of cities such
Biaduo, 2005), and is rare in many other towns in this as Rio de Janerio (Brazil) and Buenos Aires (Argentina).
region (e.g. Warsaw, Poland; Luniak, 2005). By contrast, it The pale-breasted thrush T. leucomelas frequents parklands
frequently occurs in urban areas in western Europe, including and gardens in some areas, including suburbs of Caracas,
Belgium (Weiserbs & Jacob, 2005) and the United Kingdom Venezuela, and has recently colonised urban areas in Rio
(Mason, 2000; Evans et al. 2009d). Similarly, the song thrush Grande do Sul (southern Brazil; Bencke & Grillo, 1995).
T. philomelos is absent from Warsaw (Luniak, 2005), yet is The creamy-bellied thrush T. amaurochalinus occurs in parks
an urban breeder in towns to the east (e.g. St. Petersburg, and large gardens, including around large cities, just in the
Khrabryi, 2005; Moscow, Konstantinov & Zakharov, 2005; southern parts of its South American range. Similarly, the
Lublin, Biaduo, 2005), and the west (e.g. in Hamburg: great thrush T. fuscater has become common in gardens in
Mulsow, 2005; in Brussels: Weiserbs & Jacob, 2005; and large cities, such as Quito (Ecuador) and la Paz (Bolivia),
throughout the United Kingdom: Mason, 2000; Evans et al., in the last few decades but is not urbanised elsewhere. In
2009d). Species also vary in their timing of urbanisation, Mexico, the rufous-backed thrush T. rufopalliatus colonised
for example the song thrush colonised German cities in the Mexico City and Oaxaca City during the 1980s and 1990s,
1930s, several decades later than in the United Kingdom and was first noted in San Miguel de Allende in the late
(Fitter, 1990). 1990s. It is uncertain if this species has become urbanised
More detailed data on the timing of urbanisation are through natural range expansion or establishment of escaped
available for the fieldfare, which has only recently become cage birds, but the data clearly demonstrate the potential for
urbanised in parts of its range. It colonised Krakow it to thrive in urban areas in some but not all parts of its
(south-east Poland) in the 1960s (Harmata, 1979), and Lublin range (Howell & Webb, 1995; Brooks, 1999).
(south-east Poland) in the late 1970s, when it started to breed In the Afrotropics the olive thrush T. olivaceus is urbanised
in parks and cemeteries before moving to more residential in South Africa, but not in the more northern parts of
areas of the city in the early 1990s where it is now established its range (Urban, Fry & Keith, 1997). The taxonomy of
(Biaduo, 2005). Fieldfares began breeding in inner Warsaw this species is, however, complex and the sub-species in
(central Poland) in 1975 when there were less than 10 pairs, the non-urbanised section of the range may be specifically
but it has since become more numerous with 80100 pairs distinct from the taxa in the urbanised section of the range
in 1985 and 250350 pairs in 1990 (Luniak et al.,1990). (Bowie et al., 2005). Similarly, the Palearctic Tickells thrush
Fieldfares became urbanised in the Vosges region (north- T. unicolor is a rural bird in most of its range, but is partially
east France) in the late 1970s and early 1980s (Sueur & urbanised in some sections, such as the Kashmir region of
Sueur-Bellart, 1983). These examples of recent urbanisation the Indian sub-continent (Clement et al., 2000).
by the fieldfare are against a background of a marked south-
westwards expansion in its breeding range between the 1800s
(b) Corvus
and 1960s (Lubcke & Furrer, 1985).
Away from Europe there are numerous other examples Corvus species also exhibit temporal variation in their
of Turdus species being urbanised in only part of their occurrence in urban areas. In Australia, the Torresian crow
geographic range. Such variation is exhibited by at least C. orru was rarely seen in urban areas prior to the 1950s, but
seven of the 33 Turdus species occurring in the Neotropics is now ubiquitous (Low, 2002; Everding & Jones, 2006). The
(unless stated otherwise data are from Clement et al., 2000). jungle crow C. macrorhynchos became much more urbanised

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660 K. L. Evans and others

in Japan between the 1970s and 1990s, probably in response 12%; Table 2), with latitude having a negligible influence on
to changes in waste disposal practices that increased food urbanisation date (model averaged partial r 2 < 1%; Table 2,
availability (Ueta et al., 2003). Similarly, the hooded crow Fig. 5A), and a slight trend for more recent urbanisation
Corvus cornix is becoming more urbanised in many European in eastern Europe (longitude: model averaged partial r2 =
regions. The species first bred in Finnish cities in the earlier 12%; Fig. 5B). The very weak spatial signal in these data
half of the 20th Century, but remained at low population suggests that this species has become urbanised in a largely
densities until the 1960s (Vuorisalo et al., 2003), and also independent manner, preventing an analysis of rates of
became urbanised in other European cities at a similar time spread of urban populations.
(e.g. Berlin; Lehmann, 2002). This contrasts with a much
older association with towns and cities further east in its (c) Columba
range (Madge & Burn, 1994). Even the archetypal urban bird, the rock pigeon C. livia, is
We are not aware of sufficiently large compilations of data not fully urbanised throughout its range. This species started
on timing of urbanisation in any Corvus species for assessing to colonise cities in Turkmenistan and Uzbekistan only in
spatial patterns in urbanisation, but such a compilation is the early 1980s (Obukhova, 2001). Similarly, in the 1980s
available for another corvid, the magpie (Jerzak, 2001). the population of C. livia breeding in Dushanbe (Tajikistan)
We analysed the spatial pattern of urbanisation using the fed almost entirely on crops located 1015 km outside the
methods described above for the blackbird (Section III. 1), city, rather than on food sources within the city (Obukhova,
but longitude was rescaled to facilitate the use of polynomial 2001). The hill pigeon Columba rupestris started to invade
terms (thus the most westerly location, Dublin, had a towns in the early 1900s, initially to feed during the winter,
longitude of zero rather than -6, i.e. 6 W). There is little with regular breeding in urban areas occurring in the second
association between latitude and longitude in these data (r 2 = half of the century; in some regions over 90% of this species
0.5%), thus colinearity is not a concern. Magpie urbanisation population now occurs in urban areas (del Hoyo et al., 1997).
date exhibits a limited spatial pattern (model average r 2 = A number of other Columba species are urbanised just in

(A) (B)

(C) (D)

Fig. 5. Relationships between known dates of magpie Pica pica urbanisation and (A) latitude, and (B) longitude (data from Jerzak
2001), and of woodpigeon Columba palumbus urbanisation with (C) latitude, and (D) longitude (data from Tomiaojc 1976) in Europe.
The open symbols represent the raw data, and the grey line the model averaged predicted values from the models described in
Table 2. To facilitate the use of polynomial terms in the magpie data longitude was rescaled so that the western-most location,
Dublin, had a longitude of zero rather than 6 W.

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A conceptual framework for the colonisation of urban areas 661

portions of their ranges, examples include the band-tailed studies that seek to explain interspecific variation in
pigeon C. fasciata (urbanised in parts of the USA, but not species responses to urban areas. Rather than viewing the
South America), picazuro pigeon C. picazuro (urbanised in composition of urban assemblages as fixed, it is perhaps
south-east Brazil and Argentina, but not further north), and more appropriate to consider them as a dynamic suite of
spot-winged pigeon C. maculosa (urbanised in Bolivia and species that is subject to continuing colonisation events, as
Peru, but not further south; all data from Gibbs et al., 2001). well as local extinction. The detailed case study of spatial and
The woodpigeon also exhibits much spatial and temporal temporal patterns we present for the blackbird enables us
variation in the development of urban populations. Whilst to assess how underlying factors related to each of the three
Tomiaojc (1976) documents this urbanisation process there stages of the urbanisation process drives the development of
has been no formal assessment of spatial patterns in the urban populations. Additional case studies are required from
timing of these urbanisation events. Using the methods we a diverse range of taxonomic groups and regions to assess
applied to the blackbird (Section III.1), we found a moderate fully which aspects of our conceptual framework have the
spatial pattern in the timing of woodpigeon urbanisation greatest influence on the development of urban assemblages.
in Europe (model average r 2 = 39%; Table 2; again there
is little colinearity in longitude and latitude in these data,
r 2 = 1.4%). Urbanisation exhibited a complex but weak
relationship with latitude (model averaged partial r 2 = 6%; VI. CONCLUSIONS
Fig 5C), but was more recent in the east (model averaged
partial r 2 = 35%, Fig. 5D). The strength of the spatial signal (1) Studies of range expansions have focused on those that
in these data is sufficiently weak to prevent an analysis of rates are external to a species original range, rather than
of spread, and suggests that leap-frog urbanisation events are internal processes in which gaps within the current
unlikely to be frequent in this species, although they cannot range are filled. The urbanisation of a species is
be entirely excluded. a prime example of such internal range expansion.
However, despite a recent explosion of interest in the
(d) Other genera ecological effects of urbanisation, a detailed theoretical
Spatial variation in the occurrence of urban populations has framework for studies of biotic colonisation of urban
been recorded in many other avian genera. Towns and cities areas has previously not been available. We provide
have been colonised by the merlin Falco columbarius in the such a framework.
Nearctic (Sodhi et al., 1992), wallcreeper Tichodroma muraria (2) There are two main potential mechanisms through
in Tibet (Gantlett & Millington, 1992), black woodpecker which a species may colonise urban areas. First,
in Hungary (Gorman, 1998), dunnock Prunella modularis in colonisation may arise independently in a number
the United Kingdom (Vogel & Tuomenpuro, 1997), lesser of locations. Alternatively, leap-frog urbanisation may
whitethroat Sylvia curruca in eastern Europe (Bijlsma & Saris, occur in which individuals first adapt to an urban
1997), northern wheatear Oenanthe oenanthe in parts of north- environment in a single location and then disperse to
east Europe (Walasz & Mielczarek, 1992), and common other towns and cities.
redstart Phoenicurus phoenicurus and thrush nightingale Luscinia (3) Each of these types of urbanisation progresses through
luscinia in parts of eastern Europe (Lykov, Avilova & Beme, three stages: (i) arrival, (ii) adjustment, and (iii) spread.
2009); in other parts of their geographic ranges these species The rate of progress through these stages will vary
are absent from urban areas. with environmental factors relating to the spatial
A number of other bird species also show temporal configuration and development of urban areas (and
variation in their occurrence in urban areas. The following which are influenced by human attitudes and socio-
are just some of the examples from the European avifauna: economic factors), species ecological and life-history
long-tailed tit Aegithalos caudatus has recently colonised such traits and whether urbanisation occurs independently
habitats in Europe (Nilsson, 1997); goshawks Accipiter gentilis or in a leap-frog manner. These factors may be
moved into urban parks in some European countries, interrelated in ways that can synergistically promote
including Latvia, Germany and The Netherlands, at the progress through different stages or facilitate progress
end of the 20th Century, but are absent from many through one stage yet delay progress through another.
European cities (Wurlefs, 1994; Bijlsma & Sulkava, 1997); the (4) We use the framework that we have developed
greenfinch Carduelis chloris has become increasingly common to inform discussion of avian urbanisation events,
in many European towns and villages since the 1950s (Gil- focusing primarily on the blackbird Turdus merula. This
Delgado & Newton, 1997); the Eurasian jay Garrulus glandarius is currently one of the most widely urbanised avian
colonised urban areas in western and central Europe from species within its Western Palearctic range, but there
the 1930s, Latvia in the 1960s, Ukraine in the 1970s and is marked spatial variation in the occurrence of urban
more recently in Russia (Bejcek & Gorban, 1997). populations and the timing of their establishment,
Spatial and temporal variation in urbanisation patterns which varies by over 150 years. The occurrence of
are thus probably more general phenomena than is typically such variation is likely to be a general pattern in other
recognised. Indeed, this variation may hinder large-scale taxa and regions.

Biological Reviews 85 (2010) 643667 2010 The Authors. Journal compilation 2010 Cambridge Philosophical Society
662 K. L. Evans and others

(5) The blackbird appears to be unusual in that the timing was funded by the Natural Environment Research Coun-
of urbanisation exhibits a strong spatial signature, cil. K.J.G. holds a Royal Society-Wolfson Research Merit
such a signature is much less marked in the magpie Award.
and woodpigeon. Whilst the blackbirds strong spatial
pattern is suggestive of leap-frog urbanisation other
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