Abstract
This paper provides a review of the urbanization gradient and its effects on the density
and diversity of avian species. The literature in this review reveals that increasing
urbanization is negatively correlated with avian diversity and positively correlated with
avian density. Urbanization occurs on a gradient and represents the transition from
wild land to city. The changes in density and diversity are precipitated by the
structural changes in habitat, i.e. vegetation, as a direct result of the urbanizing
process. Further research needs include creating a standardized definition of
urbanization and quantifying the effects of the intensity of development of avifauna. A
conceptual framework based on predicting avian response to urbanization can lead to
smart urban design and effective conservation plans.
Keywords:
urbanization gradient; urbanization; gradient; avian composition; habitat
change, avian density and diversity; patchiness; land use; land management; urban
design; avian conservation; rural; suburban; wild land
Urbanization defined
It is obvious that the urban landscape will dominate in many parts of the world. It is
one of the major forces in the process of land use change. The world’s population
exceeded 6 billion people in 1999 and continues to grow by 1.8% every year (Matson
1990). The growing global population is largely concentrated in cities, and the
associated development and resource use are the primary reasons that avian habitats
are at risk.
As the landscape is modified, natural resources and habitat are replaced by
artificial resources and exotic species, and built structures (Boren et al. 1997). The
avian species within and without the modified landscape are exposed to novel
ecosystem characteristics. These characteristics, which are largely associated with the
changes in habitat, preferentially select for certain species (generalists) over others
(specialists).
For the purposes of this paper, I have defined the urbanization gradient as the
different habitat structures promulgated by the urbanizing process, i.e. the range of
structures observed as one moves from a wild area to a city, where the city is the
ultimate form of urbanization. A suburb is part of the gradient but it is not part of the
natural progression from wild land to city. Rather, suburban development usually
occurs as a residential extension of a city. For the majority of the studies in this review,
the authors operated under this definition. However, one case (Jokimaki and Suhonen
1993) subdivided the city landscape into its own gradient based on the degree of
development within the city’s boundaries.
Data from Batten’s (1972) work on diversity in relation to increasing
urbanization in a north London town shows the substantial drop in species diversity
with percent increases of urbanization (see Figure 1). The variables affected in the
urbanizing process are not well understood. The compositional changes –
density/diversity and habitat – are discussed here. But these are only two of the
myriad aspects of avian ecology. We need more research to help elucidate the
appropriate responses to urbanization, in terms of land use, planning and conservation.
Ecological consequences of urbanization
Habitat structure
In his seminal work on the description and comparison of avian habitats, Emlen (1956)
describes habitat as a “physical entity possessing a number of measurable features, or
‘dimensions’.” The “dimensions” of habitat are the arrangements of the multiple
vegetation types within a patch. Habitat in the urban and suburban environment is
fragmented and isolated. In contrast to forested wild lands, the urban environment has
the most vegetation coverage at the ground level with low levels of middle and upper
vegetation (Beissinger and Osborne 1982). In shrublands and grasslands, the
arrangements of vegetation tend to be concentrated at the ground or middle levels. The
urban areas that border these ecosystems also have vegetative arrangements at the
ground and middle levels.
The more urban environments contain less of the full complement and
arrangement of vegetation types. Native plant species are increasingly removed and
replaced by exotics as you move towards the cityscape of the gradient. In cities, which
are characterized by extreme development, most, if not all vegetation, is replaced by
built elements. The diversity of covering regulates the avian communities that settle in
an area (Valvo et al. 1985). The variations in abundance (density of individuals) and
richness (diversity of species) closely track the changes in habitat. Investigations have
been made that relate the locations of species across the urbanization gradient to the
array of habitat.
Compositional changes in avian populations
There are four types of species associated with corresponding levels of
urbanization. The native species that achieve the greatest numbers only in the most
natural landscapes, i.e. wild lands, are known as “urban avoiders” (Blair 1996).
These
species are remarkably sensitive to human initiated disturbance. The urban avoiders
are not specifically addressed in this review. Some species described as “urban
exploiters” exhibit a plastic response to urbanization and development and perform well
in the urban environment (Blair 1996). Blair (1996) termed the third group of species
“suburban adaptable”. These species successfully utilize the seeming middle ground
between complete urbanization and wild land. Colonizers of the rural landscape, here
classified as “rural associates,” take advantage of the fact that agricultural land use is
not far removed from natural processes, in terms of proximity and vegetation
composition.
The urban exploiter
The integrity of the original wild land is greatly compromised during the
urbanization process. As such, the bird species typical of urban areas are exotic and
invasive. Emlen (1974) argued that the species that reach high densities in urban areas
are invaders that are tied to the urban and suburban development in their areas of
origin. Similarly, Blair (1996) noted that urban-adaptable species are exotics based on
the traditional definition (humans have introduced them).
While urban exploiters reach maximal densities in the urban landscape
compared to densities in wild lands, the species diversity is low. There is dominance by
a few species that quickly settle and reproduce in the urban environment. Beissinger
and Osborne (1982) documented that the urban area in Oxford, OH supported nine
fewer species than the original forested lands. The authors highlight the loss in
richness as one moves from forest to city. They compare their data to Emlen (1974) to
show that this effect is significant across ecosystem types. In Oxford, there was a 28%
decline in diversity between the forest and the city, while there was a 33% decrease in
species richness between Emlen’s desert and city.
It is clear that diversity and density of avian species do not move in the same
direction in a city. These factors are closely linked to the diversity of habitat available
in the city. The relationship between habitat and avifauna suggests that because cities
have high habitat diversity, species should respond positively and show a high richness.
Emlen (1974) shows that this correlation does not hold (also see Figure 2). He
calculated high habitat diversity for Tucson’s urban area based on ornamental trees,
shrubs, and non-vegetative structures. However, the richness calculation for avifauna
in the city was low. Similarly, Lancaster and Rees (1979) found that high urban habitat
diversity does not correspond with high species richness. They argued that the features
provided by the urban environment, built structures and mostly exotic and artificial
vegetation, do not “contribute to structural diversity in any ecologically significant way.”
Basically, these new habitat features do not provide new niche spaces for many species.
The species that do utilize these features tend to be versatile exotics. Although it has
been shown that natives will use the urban space (Mills et al. 1989), this only holds if
there is sufficient native vegetation and/or food and water resources set out by
humans.
Patterns of avian species assemblages track the vegetative makeup of habitat,
i.e. urban assemblages typically consist of species that can optimize the urban
vegetative environment (Gavareski 1976, Mills et al. 1989). Mason (1985) provides a
general description of the avian guilds that form in urban areas (also see Figure 3A, B).
In cities with grassy areas and vacant blocks, ground feeders are the first colonizers.
Species that require protection when feeding but feed in lower-level vegetation colonize
areas with native plantings, such as gardens and parks. Granivores, omnivores, and
some insectivores do well in urban environments due to the feeding stations and higher
temperatures in this area during the winter months (Bezzel 1985).
Granivores and omnivores that eat fruits from exotics, ornamentals and seeds,
grain, bread, and scraps provided by people take advantage of the city’s vast food
resources (Lancaster and Rees 1979, Tweit and Tweit 1986). Seedeaters are also
dominant in cities due to feeders, but are also found in urban and/or suburban areas
with a high percent of grass (lawn) cover (Mason 1985). Exotic insectivores are
dominant in the urban habitat due to the presence of insects that feed on the foliage
and bark of exotics and ornamentals (Beissinger and Osborne 1982). Water-dependent
species will shift to the city if water is provided. For example, Emlen (1974) noted that
water-dependent species flocked to Tucson’s urban area due to pools, fountains, etc.
Their numbers decreased in the desert.
Omnivores that nest in cavities and on the ground and ledges find suitable sites
in urban areas (Lancaster and Rees 1979). Sewell and Catterall (1998) argued that the
styles of buildings in urban areas have a huge impact on the numbers and types of
these species that inhabit the area. Similarly Geis (1974) found that the number of
“unwanted” species, in this case sparrows and starlings, increased with buildings that
had small openings that provide nesting space.
If these birds are nesting it stands to reason that they are successfully
reproducing. Several researchers have questioned this premise. Blair (1996) wrote that
high densities are not indicative of a sustainable population, since these populations
may receive an influx of individuals from other sites. Bezzel (1985) who argued that
while these urban species reproduce, the rates could not sustain a stable population
supports this point. Some species are extremely sensitive to urban development. In
work done in Tucson, Tweit and Tweit (1986) hypothesized that the northern flicker
(Colaptes auratus) would stop breeding as urbanization intensified. Therefore, these
urban populations are reliant on outside populations; i.e. dispersal and migration are
important factors in supporting urban avifauna.
It has been suggested that urban habitat may be refuges for native species that
have lost habitat (Mills et al. 1989). This argument comes on the heels of the
differential response to urbanization by resident versus temperate migrants in the
tropics. Petit et al. (1999) found that resident birds in the tropics are more sensitive
than winter migrants to the habitat change wrought by urbanization. They proposed
that native tropical habitat provides greater niche specialization and an abundance of
microhabitats. Additionally, because these migrants are coming from vastly differing
land types, these species have a particular hardiness that makes them less susceptible
to changes in habitat. On the other hand, the study done by Rosenberg et al. (1987) in
Tucson showed that desert residents responded positively to the exotic features of the
urban environment, whereas the migratory breeders performed poorly. Their
explanation rests on the dependence of the southwestern river valley migrants on native
plant species, which tend to be largely absent in urban areas.
The suburban adaptable
The second class of urbanization avifauna termed “suburban adaptable” by Blair
(1996) successfully thrives in areas of moderate development. In areas of intermediate
urbanization, i.e. suburbia, species reach peak density and diversity. The resources
associated with this degree of development provide the optimal habitat for suburban
adaptable species. Going beyond this, Blair (1996) based on work done by McDonnell
et al. (1993), concludes that biotic limitations are high at the rural end and physical
limitations are high at the urban end. Therefore, since suburbia supposedly represents
equal levels of physical and biotic resources, some species will have high densities and
the species diversity will be greater compared to the urban and wild ends of the
spectrum. Following Connell’s (1978) and McDonnell et al.’s (1993) argument,
Jokimaki and Suhonen (1993) presented data that shows an eventual decline in species
richness if development continues beyond an optimal window where suburbia equals
high density and diversity. As urbanization intensifies and the diversity of vegetation
declines to an ecologically insignificant level, species diversity will drop off (Aldrich and
Coffin 1980).
The types of species that inhabit the suburbs are a combination of the invasive
exotics and natives. Native species can be subdivided into two categories – species with
wide ranges and tolerances, and those limited species that are dependent on native
habitat (Blair 1996). This second class of native would not survive beyond the wild
land. The urban and suburban species compositions described are unique; such
assemblages that would be absent in an area that had only native vegetation (Sewell
and Catterall 1998). Similarly, once native habitat is removed, some native species will
not reappear in a disturbed site (Blair 1996, Sewell and Catterall 1998).
The associated habitat diversity of suburbia includes exotic trees, shrubs
(typically berry-producing), lawns, remnants of original forest, housing structures,
utility wires, seed feeders, and water sources (Aldrich and Coffin 1980, Tweit and Tweit
1986), which provide food, nest sites and perches. Suburban habitat often provides a
base for exotics to invade surrounding native areas. For example, the European
starling (Sturnus vulgaris) uses holes and crevices in a suburban area from which to
colonize nearby desert (Tweit and Tweit 1986). In Tucson, a wide-ranging native
species, such as the house finch (Carpodacus mexicanus) can use native and exotic
resources (feeders, sugar water) to expand its population density (Tweit and Tweit
1986).
Blair (1996) cautions that the increased diversity of species with associated
moderate development applies only to overall species diversity. That in fact, native
diversity decreases even though overall richness increases. Furthermore, if we are
interested in preserving diversity, it is important to examine of definition of diversity.
Do we want to preserve native species diversity or overall diversity, which is largely
based on wide-ranging and exotic species rather than natives? In the former case, the
increased resource (physical and biotic) of the suburban area may not be the most
beneficial compromise.
Going beyond this, Bezzel (1985) documented that many species have high site
fidelity. The seeming adaptation to urbanization may really be a relic of previous
behavior patterns. Some breeding individuals will persistently try to nest and breed at
a site even though it has changed from a mixed forest to a hiking trail. The offspring of
these individuals will not survive because of lack of appropriate resources but the
breeding pair will faithfully return every year. He supports his hypothesis with work
done by several researchers including Matter (1982). Matter’s study showed that
although the lapwing (Vanellus vanellus) did not attain the reproductive rate required to
achieve a stable population, the coastal populations were sustaining the inland
populations.
The rural associate
Finally, I will address the avian assemblages associated with the variety of
agricultural land uses in rural areas. The effect of agriculture on avian assemblages
has been the subject of work done by Petit et al. (1999). The authors showed that bird
species are differentially affected by each category of agriculture. Research conducted
in Panama on lands allocated to forest (remnants and unfragmented), shade coffee
plantations, and Pinus caribbea and sugar cane plantations. The forests supported the
greatest total species richness. However, when the forests were broken into gallery,
premontane and lowland forests, the species diversity among these types varied greatly.
Petit et al. (1999) uses this result to support the argument that tropical forest residents
have narrow niche requirements. Of the agricultural land uses, shade coffee supported
comparable species in terms of numbers and diversity to both lowland and premontane
forests. Shade coffee plantations provide habitat niches to mostly Nearctic migrants,
but some residents used the plantations. The species richness and composition of the
vegetation, as well as the distance to forest habitat are several factors that make shade
coffee plantations suitable habitat.
Similarly, Bezzel’s (1985) study in Central Europe shows that rural areas with
low to moderate human use/disturbance support high bird species numbers and
diversity. Like Petit et al. (1999), Bezzel suggests that rural habitat suitability is
influenced by isolation from forest habitat as well as the structural diversity of the
vegetation.
The consensus in the results
Many native species absolutely require native habitat. Suburban landscapes contain a
high diversity and density of species consisting of natives that can tolerate some
disturbance and exotic species. However, the high diversity in the suburban areas is
not indicative of increased diversity with increased land development. In the urban
landscape, where species diversity is low and while density is high, the assemblages are
mostly dominated by a few species.
The presence of native vegetation in areas along the urbanization gradient will
significantly enhance the diversity of the landscape and increase the likelihood of the
survival of native avifauna. However, several additional factors including vegetative
species composition, spatial scale, and the land use activities surrounding areas of
native vegetation, influence the types of species that are likely to persist in areas of
native vegetation.
Future directions: land planning and conservation
In the course of this review, the following research needs were identified.
•
Which types of natural features support the requirements of avifauna?
Research should focus on determining the relationship between urbanization
and these natural features, specifically vegetation. Also, the site carrying
capacity or environment thresholds for avian species should be quantified.
•
How do we characterize urbanization?
This is a multidimensional task. In
characterizing urbanization, we can determine the how the intensity of
urbanization affects bird density and diversity. From this analysis, we can
describe the types of urban development that are most compatible with
native birds. The results can be used to establish a database from which to
develop and practice smart, responsible and sustainable management.
•
How do the categories of urban, suburban, rural and wild land relate to each
other and affect avian diversity and density?
Data needs to be collected on
the interaction between the different parts of a landscape. We clearly need
to assess how the modulating potential of factors such as matrix, habitat
orientation, and geometry affects avian species habitat.
Given the rate of urbanization, it is imperative to consolidate a sound conceptual
background. Only well-designed, long-term studies will be able to reliably reveal
universal patterns and the factors that influence the role urbanization plays in avian
species composition in each specific case. To the extent that we are able to accurately
predict the impacts of all levels of urbanization, we will be able to appropriately design
cities and conservation plans that mitigate the deleterious effects of urbanization.
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Illustrations