Urbanization and its implications
for avian aggression: A case study of urban black kites (Milvus migrans) along Sagami Bay in Japan
Dana Galbreath, Tomohiro Ichinose, Tomoyuki
Furutani, Wanglin Yan, and Hiroyoshi Higuchi
Abstract: Urbanization has caused
countless changes in the lives, behaviors, and community structures of wild
animals. Habitat loss in urban areas has led to the proliferation of certain
species over others; in the case of birds, insectivores, frugivores, and
certain predators can be found in abundance in cities. These birds, however,
occasionally show novel behaviors that can cause stress within human-wildlife
interactions. The black kite, Milvus
migrans, for example, has displayed a tendency to attack humans for their
food in certain urban areas in Japan. In order to determine how habitat
availability and land-use types affected these aggressive tendencies, field
observations were combined with GIS analysis of five locations along Sagami Bay
in Japan. These locations; Enoshima, Fujisawa; Kamakura Beach, Kamakura; Zushi
Beach, Zushi; Oiso Beach, Oiso; and Iwa Beach, Manazuru; were assessed
according to the amount of each land-use type present and the aggressive
tendencies of each location’s black kite population. The aggression of each
population, designated by the log of the Aggression Index (AI), was found to be
significantly affected by the amount of forest area per black kite
(β=-2.704, p<0.001), the amount of non-rice-paddy agricultural area per
black kite (β=-9.284, p<0.001), and the season (spring β=0.384,
p<0.001). Thus, aggression was higher amongst populations with less forested
or agricultural area within their foraging zones, and aggression increased
during spring, which is the breeding season.
Keywords: black kite; urbanization; green
space; behavior; aggression; land-use types
Introduction
Urbanization, which can be
defined as a concentration of humans, their residences and industry, and their
associated anthropogenic influences (Chase and Walsh, 2006), has had dramatic
effects upon urban and natural ecosystems. Recent research projects often
center upon the potential mitigation of harm done to animals via human
developmental projects; due to these studies, urbanization has been widely
recognized as one of the primary causes of species endangerment (Blair, 1996;
Leider and Haddad, 2011; Walpole and Bowman, 2011), disturbance, and behavioral
changes (Anderies et al., 2007;
Walpole and Bowman, 2011; Blair, 1996; Chase and Walsh, 2006; Bonier et al., 2007; Tavernia and Reed, 2010). Although
many urban animal species have been monitored in order to determine these
reactions to human influences, birds are a particularly useful study animal
when testing the effects of anthropogenic influences upon resident wildlife due
to their sensitivity to habitat changes (Imai and Nakashizuka, 2010).
Studies have shown that changing
habitats and land-use types cause bird community structures to change
accordingly. As urban development progresses, species richness decreases while
abundance increases (Ortega-Alvarez and Macgregor-Fors, 2009; Chase and Walsh,
2006; Imai and Nakashizuka, 2010; Blair, 1996). The species-specific life
history traits, such as diet and nesting habits, of urban birds lead to certain
species thriving in the cities while other species retreat to more rural areas.
Consequently, biodiversity in cities is typically very low, leaving only a
handful of urban exploiter species such as pigeons, sparrows, crows, and black
kites to compete over abundant resources. Unfortunately, easy access to food
has led to higher numbers of like-minded animals competing for the same
resources, and abundance levels are often above the carrying capacity of the
city, which in turn leads to increased intraspecific competition (Anderies et al., 2007). Predation pressures also
change from natural to urban environments (Gering and Blair, 1999), leading to
novel interspecific and intraspecific interactions; for example, some
small-range raptors may inhabit cities with poor nesting sites simply because
in those areas, they are now free from predation (Chase and Walsh, 2006).
Human
disturbance upon ecosystems is also a major concern in urban wildlife
conservation. Urban environments provide a range of anthropogenic stimuli that can
be considered disturbing to birds; noise, physical presence of humans, and
motor vehicles, for example, can cause stress in species that are less capable
than others of tolerating such activity (Pease et al., 2005; Gonzales et
al., 2005; Burton, 2007; Møller,
2008; Baudains and Lloyd, 2007). Since
urban bird abundance is high, those birds have a greater tolerance for most
human activities than their rural counterparts, although their reactions to
human disturbance vary on both the individual level and the species level
(Blumstein et al., 2005; Blumstein, 2006). However, tolerance has its
limits, and human activities within cities can still negatively impact the
birds that live there (Chase and Walsh, 2006; Bonier et al., 2007). Bird
populations’ reactions to human disturbance and their tolerance of intensive
human presence are closely related to the overall behavioral changes found in
urban exploiters. According to various research projects, urban environments
tend to select for bold and aggressive birds, most likely as a correlation to
the extremely high amounts of anthropogenic stimuli (Scales et al., 2011; Møller, 2008; Evans et al., 2010; Evans, Boudreau, and
Hyman, 2010; Searcy et al., 2006). Boldness
in birds seems to be a heritable trait, which means that urban habitats may be
selecting for increasingly bolder generations that lack fear of humans.
Boldness also correlates to aggression, particularly conspecific or territorial
aggression (Scales et al., 2011;
Bell, 2005). As urban areas grow and new populations take root, these new
populations tend towards high initial aggression that eventually lowers over
time. Although high aggression is detrimental overall, aggressive birds enjoy
higher fitness levels in new populations. Thus, newly developed areas and other
urban areas have been subjected to increasing numbers of aggressive, bold
birds. However, the influence of habitat availability upon aggression is
largely unknown, and the influence of intensive human presence upon aggression
is also unclear.
This research project focuses
upon these issues in order to determine the effects of urbanization upon
aggressiveness in black kites (Milvus
migrans). Although black kites are found in numerous countries around the
world and are in decline in Europe (Sergio et
al., 2011), they have become a nuisance animal in Japan. Black kites found
along Sagami Bay in the Kanto region of Japan have been known to attack humans
bearing foodstuffs; these occurrences are so common in seaside cities such as
Kamakura and Fujisawa that the presiding prefectural and/or city environmental
municipal offices have posted signs warning visitors of the danger of black
kites. When contacted, tourism centers and health clinics along Sagami Bay
cited frequent injuries amongst beachgoers. Due to the aforementioned tendency
of wild birds to consider human presence disturbing, this novel behavior of
urban black kites is disconcerting. If urbanization has influenced black kite
behavior to this degree, future city planning must take these effects into
account in order to facilitate mitigation. Unfortunately, urban habitat
fragmentation and destruction is a major problem in Japan (Matsushita, 2002),
and urban habitat fragments must be carefully managed in order to preserve
wildlife (Hedblom and Soderstrom, 2010; Fernandez-Juricic and Jokimaki, 2001;
MacGregor-Fors, 2010; Khera et al.,
2009).
Black kites were monitored in
coastal areas in Japan in order to determine how habitat availability and human
visitation affected a population’s overall aggressiveness. The two hypotheses
that formed the basis of this study were: (H1) the amount of viable habitat in
each population’s foraging zone is negatively correlated to the aggressiveness
of black kites, and (H2) the number of human visitors (which is related to
urbanization factors such as transportation, convenience, etc.) to a foraging
zone is positively correlated to the aggressive tendencies of Black Kites.
Methods
Focal Species
The black kite, Milvus migrans, is a medium-sized
(630-940g), migratory raptor (Forero et
al., 1999; Sergio et al., 2011). The
natural prey of the black kite tends to be aquatic (e.g., fish), which supports
the tendency of black kites to roost and forage near large bodies of water
(Forero et al., 2002); however, they
are also known to be opportunistic predators that will take advantage of
spatiotemporal fluctuations in prey availability (Koga and Shiraishi, 1994).
These birds are well known for their behavioral flexibility with regards to
resource availability (Sergio et al.,
2011).
Research Locations
Five locations were chosen along
Sagami Bay in order to provide a green space gradient: in order from lowest to
highest percentages of foraging zone green space, these locations were
Enoshima, Fujisawa; Kamakura Beach, Kamakura; Zushi Beach, Zushi; Oiso Beach,
Oiso; and Iwa Beach, Manazuru (Fig. 1). For the sake of maximizing homogeneity
amongst the different locations, each observation point was located upon a
beach in each city or town regardless of whether or not black kites could be
found elsewhere.
Fig. 1: Satellite imagery of the
research locations: a.) Enoshima, Fujisawa, where research was conducted from
the western shore; b.) Kamakura Beach, Kamakura; c.) Zushi Beach, Zushi; d.)
Oiso Beach, Oiso, where research was conducted from the eastern shore; and e.)
Iwa Beach, Manazuru. (Images ©Google Earth 2012)
Field
Observations
Field observations were carried
out at specified observation points at each research location, using Nikon
Eagleview Zoom binoculars for black kite monitoring and identification. Observations
were conducted for a period of six hours on each trial day from 10:00 am to
4:00 pm; this period was chosen due to the fact that the majority of aggressive
behaviors and human visitors appeared during this time frame (determined during
preliminary observations at each location). During each trial, the amount of
intra- and interspecific attacks, the times at which they occurred, the number
of humans present, the total number of black kites present, the weather
conditions, and the number of aggressive birds (which engaged in aggressive
activity at any point during the observation period) were recorded as per
typical bird observation study methods (Koga and Shiraishi, 1994; Sergio et al., 2003; Pease et al., 2005; Forero et al.,
1999; Baudains and Lloyd, 2007). Food was prohibited during observation hours
in order to avoid drawing attention to the researcher.
Observations were recorded during
three seasons: early fall (September to mid-October), spring (March through
May), and summer (June through August). Winter was not included due to the
migration tendencies of the black kites; the birds present during the winter
were not the same populations as those present during the spring and the
summer.
GIS
Analysis of Green Space
In accordance with the goals
stated above, the amount of green space, defined as any land-use type that
could be considered potential habitat for the black kite or its prey, and the
area of each land-use type within each black kite population’s foraging zone
were required for analysis. The foraging zone of each population was determined
using data from the study conducted by Sergio et al. (2003), in which black kites were found to forage up to one
kilometer from their nests. As the nesting locations were not easily accessible
in all research locations, the potential foraging zone of each observed
population was centered upon the observation point and delineated by a buffer
with a two-kilometer radius. Because each bird tends to forage up to one
kilometer away from its nest, and because the observation points were within
each population’s foraging zone, the nests in question could be up to one
kilometer away from the observation point. Thus, the area with the maximum
likelihood of foraging black kites included a maximum distance of two
kilometers in all directions from the observation point.
Once the foraging zone of each
test population had been determined, the green space percentage of each zone
was determined using ArcMap 10 for Desktop (Windows version). The observation
points were plotted on a vector map of Japan, and then buffers with
two-kilometer radii were placed around each point. Land-use data from the ESRI
standard pack for Japan was then used to determine the amount of green space
within each foraging zone. Any land-use type that could potentially be
considered habitat for the black kite or its prey was considered “green space”;
thus, wetlands, beaches, grasslands, forests, and agricultural areas were
included in the analysis. All land-use types were tabulated within the buffer
zones, and the area of each type in square kilometers was determined.
Once the field trials and the GIS
analysis had been completed, the data was compared in order to determine if any
significant correlations could be distinguished.
Definitions
Due to the nature of this
research, several definitions were required. The definitions used are as
follows:
— Attack:
Any intentional contact with or attempt to contact a human/their food or
another bird.
Due to their tendency towards aerial
acrobatics, an attack between black kites or between black kites and other
birds was recorded if and only if the talons came into use. Attacks upon humans
were recorded if the black kite had its talons out to grab food from the
human’s hands or from the victim’s immediate physical proximity (within arm’s
reach of the person being attacked). Once the food was knocked out of arm’s
reach, no further attempts to retrieve it by black kites were considered attacks
due to the lowered probability that they would come into physical contact with
humans.
— Aggressive:
Engaging in attacks at any point during the observation period.
In order to avoid bias based
solely on the number of attacks committed during the observation period, the
number of individuals present who engaged in any aggressive activity were
recorded and compared to the total number of individuals observed.
— Aggression
Index: ,
where n=number of behavior types,
j=type of behavior, Bj=score for attack type, Nj=number of that attack type,
Pa=number of aggressive birds, and T=total birds. Bj scores are: Attacks (Other
Birds)=1, Attacks (Black Kites)=2, and Attacks (Humans)=3.
By weighting different aggressive
behaviors according to the inherent level of aggression or risk-taking involved,
populations that engaged in riskier behavior would have higher aggression index
results than populations that engaged only in low-risk or low-aggression
behaviors (Errard and Hefetz, 1997; Tanner et
al., 2011). Each population as a whole was tested for its overall AI on
each trial day.
Analysis
GIS
Analysis
The ESRI standard pack land-use
data was entered into ArcMap 10, buffers were created around the observation
points in order to simulate each black kite population’s foraging zone, and the
land-use types were tabulated within each buffer in order to determine the
percentage of green space within each foraging zone. Figure 2 shows the
resulting map.
Fig. 2: A map showing the land-use types
for Japan with the vector map for Kanagawa Prefecture. Foraging zone buffers
are delineated by orange circles.
According
to the analysis, the green space percentages of each foraging zone were, in
order of smallest to largest: Enoshima=12.83%, Kamakura Beach=29.0%, Zushi
Beach=36.15%, Oiso Beach=50.43%, and Iwa Beach=70.17%. The area of each
land-use type at each location is shown in Table 1. Although the foraging zones
for Kamakura Beach and Zushi Beach overlapped, the foraging zones did not
overlap at the observation points (and so any birds viewed and recorded at one
observation point would be unlikely to be found at or near the other
observation point), and birds viewed in that overlapping region were not
included in the observational data; consequently, duplicated aggression values
are not present.
Table 1: The amount of each land-use type within each population’s foraging zone.
Multiple
Regression Analysis and Univariate ANOVA
Many ecological aggression
studies use ANOVA tests in order to determine how the tested variables affect
the test species’ behavior (Castro and Santiago, 1998; Trubl et al., 2011; Gillies et al., 2006; Fokidis et al., 2011). For the purposes of this
study, stepwise multiple regression analysis was first used to determine the
shared and unique variability of the different land-use types and the number of
humans present upon the aggression index data obtained. The analysis was
performed using IBM SPSS Statistics 20. As each independent variable was found
to be redundant, it was automatically removed in order to find the best-fit
model with the fewest predictors for the response variable, AI (log).
Because the data obtained for the
aggression index (AI) were shown to be non-normal and showed outliers, those
values were log10 transformed. Due to the presence of zero values,
the AI values were transformed using the following equation: AI (log)=log10(AI+AImin/2).
This equation was recommended by Carsten Dormann, PhD (Faculty of Forest and
Environmental Science, University of Freiburg, Germany). The resulting AI (log)
values were found to be normally distributed and could be analyzed using SPSS
multiple regression methods (Tabachnick and Fidell, 2007).
Once the stepwise multiple
regression analysis was performed upon the data and the most important continuous
predictor variables were determined, an ANOVA was conducted in order to create
a model equation for the response of AI (log) to the predictors. The model equation
took the form of:
Y' = βo + β1X1
+ β2X2 + … + βkXk ,
where Y' is the predicted value
of the response variable, βo is the value of Y' when all X’s
are zero, and β1 through βk refer to the coefficient
of each predictor variable, X1 through Xk. Seasonal
effects were categorical and thus required a mixed-effects ANOVA in order to
determine how the seasons, as well as the other predictor variables, affected
AI (log).
The AI (log) values and the various independent
variables were tested for correlations amongst each other and for collinearity.
AI (log) and the various land-use types, with the exception of other
agriculture, were almost all significantly correlated to each other; however,
the collinearity diagnostics showed that no multicollinearity was evident once
the factors had been reduced to the best models.
Results
Amongst
the various land-use types, only two were found to have the highest
contribution to predicting the response variable, AI (log). These two values
were forest area per black kite and other agricultural (i.e. non-rice paddy)
area per black kite. In both the multiple regression and the ANOVA tests, the
number of humans per black kite had no statistically significant effect upon
the AI (log) values; consequently, H2 was rejected. According to the stepwise
multiple regression output (Table 2), forest area per black kite and other
agricultural area per black kite were both negatively correlated to AI (log)
(p<0.001). Thus, the more forest or other agricultural area (consisting of any
agricultural area excluding rice paddies, such as orchards, vegetables, etc.)
that was present within the population’s foraging zone, the less aggressive the
black kites from that population tended to be, as was implied by the
now-supported H1. Each of the two variables had approximately equal effects on
AI (log): unique variability for forest area per black kite was 0.346, while
the unique variability of other agricultural area per black kite was 0.329, totaling
an R2 of 0.675 (adjusted R2=0.660). According to this
information, approximately two-thirds of the variability within the recorded AI
(log) values can be accounted for by these two independent variables (R2
95% confidence limits from 0.531 to 0.819).
Table
2: Results of
the stepwise multiple regression analysis depicting correlations between the
significant variables, their unique variability, and their coefficients.
Seasonality, as a random effect, was added to the
ANOVA along with the values for forest area per black kite and other
agricultural area per black kite. Of the three seasons (fall, spring, and
summer) during which observations were recorded, only spring was found to have
a significant effect upon AI (log). Fall had no statistically significant
effect, and summer was found to be redundant. Spring had a smaller overall
effect upon AI (log) (partial η2=0.163) than forest area per
black kite (partial η2=0.582) or other agricultural area per
black kite (partial η2=0.530). While the two significant green
land-use types both inhibited aggressive tendencies, aggressiveness rose in the
spring. The best model to predict AI (log) was based upon the aforementioned
equation and is displayed as follows:
AI(log) = βo + β1(
The coefficients determined by the ANOVA resulted in
the following final model:
AI(log) = 1.466 – 2.208(
Fig. 3: Mean AI (log) and forest area
per black kite values by location. The circles represent the AI (log) values,
and the triangles represent the forest area per black kite values.
Fig. 4: Mean AI (log) and other
agricultural area per black kite values by location. The circles represent the
AI (log) values, and the triangles represent the other agricultural area per
black kite values.
Discussion
According
to the above data and analysis, H1, which posited that habitat availability has
an inverse relationship with black kite aggression, was supported while H2,
which suggested that the number of human visitors in a foraging zone promote
aggressive tendencies in black kites, was rejected. Black kites in the more
rural locations showed a distinct lack of interest in human visitors, and
occasional feeding from humans did not appear to induce those populations to
consider them a viable food source. These results suggest that variable human
presence does not have as much of a sustained effect on bird behavior as
large-scale human impacts upon urbanized environments. These results may also
have been affected by the circumstances of this study, in which the birds were
required to encroach upon human space rather than vice versa, as was the case
in most other research regarding physical human-bird interactions. The concept
that habitat availability affects black kite behavior, however, was supported
by the fact that two major green land-use types, forests and agriculture,
significantly lowered the aggressive tendencies of resident black kite
populations.
Several
implications can be derived from the knowledge of how these land-use types
affect black kite aggression. Black kites build nests in trees and have a
preference for cliffs, heavily wooded areas with low human traffic, and
proximity to large water bodies when doing so (Sergio et al., 2003); consequently, a lack of forested area in a foraging
zone, which includes their nesting locations, results in a lack of nesting
resources. Black kites that choose to nest in areas with little forested area
and high human traffic, such as Enoshima and Kamakura, are forced into more
intraspecific competition for these nesting habitats than other populations.
They must also deal with more anthropogenic stimuli such as cars and continual
physical human presence than the other populations—a situation which lends
itself to a tendency towards bold behaviors (Pease et al., 2005; Scales et al.,
2011; Bell, 2005). These combined factors may be the cause of the high amounts
of intraspecific attacks found in each of these populations; even Manazuru,
which had a large amount of total green space but little forested area per
black kite, showed this tendency towards intraspecific aggression amongst some
of its population’s members. Manazuru, however, had a high amount of other
agricultural area, which diminished the effects of nesting habitat reduction
upon its population’s aggression.
The
amount of other agricultural area also heavily impacted the aggressive
tendencies of each black kite population. These areas, which include orchards,
farms, non-rice grain fields, vegetable fields, etc., are a major source of
food for scavenging black kites (Shiraishi et
al., 1990; Koga and Shiraishi, 1994; Blanco, 1994). A lack of the preferred
foraging ground for black kites can also cause increased territoriality and
aggression amongst conspecifics for the remaining food resources (Anderies et al., 2007; Shochat et al., 2004). As a result, the
combination of a lack of the preferred foraging areas and nesting resources
appears, as per the above analysis, to lead to an associated rise in the
aggressive tendencies of black kite populations. Competition over foraging and
nesting resources seems to lead to higher numbers of attacks upon humans, other
black kites, and other bird species. The effect of seasonality upon aggression
in birds, particularly during breeding season, has been well-documented in
previous research (Hamao, 2011; Valeria et
al., 2011).
Agricultural
areas are important not only to black kites, but to other species of birds as
well. In recent research, agricultural areas have been tested for their
viability as habitats; for example, High Nature Value agricultural areas, which
tend to have a large amount of native flora nearby and environmentally friendly
farming practices, have been shown to positively affect bird communities (Doxa et al., 2012; Danhardt et al., 2010; Catry et al., 2012). Unfortunately, agriculture is declining in Japan due
to its aging rural population and agricultural land abandonment or conversion
to other land-use types (Matsushita, 2002; Matsuki, 2002). While remaining
Japanese farmers, with the support of several governmental agencies, are attempting
to promote environmentally friendly practices, the lack of young citizens who
are interested in farming and the urbanization of rural areas are causing the
continued decline and degradation of Japanese agriculture (Matsuki, 2002).
Projects such as the Satoyama Initiative, however, are tackling this problem in
the hopes of promoting and preserving ecologically friendly agriculture in
Japan (Satoyama Initiative, 2012).
Despite
the apparent importance of forests to the mitigation of black kite aggression,
Japanese forestry laws have difficulty preserving urban forest patches. The
various agencies that hold administrative powers over forest development lack
coordination and often fail to communicate despite amendments to the National
Forest Law that require such efforts during any transitional planning
(Matsushita, 2002). As a result, a forest patch that is slated for development
under one agency’s plan may continue being considered a forest by another
agency throughout the planning period. If the forested area under consideration
is smaller than 1 ha, or if the development involves any of the numerous
exceptions listed in the Forest Law (including roads, railroads, broadcasting
facilities, schools, etc.), permission is not required to develop that land
(Matsushita, 2002). These issues create problems when attempting to preserve
urban forestland and when trying to promote quality forests nationally. Preserving
the amount of total forested area in Japan, as has been the primary goal of many
forest conservation agencies (Matsushita, 2002), is inadequate in terms of
providing sufficient ecological habitats for urban animals and for the
mitigation of problem behaviors that arise with a loss of habitat.
In the
face of the loss and degradation of Japanese forests, several mitigating
factors have arisen. Several companies, local governments, and citizen-led
groups have created programs dedicated to reforestation, forest management, and
public education (Iwai, 2002). Animal conservation groups, such as the Japan
Wildlife Conservation Society, not only conduct projects dedicated towards
preserving biodiversity in Japan, but also teach citizens about the importance
of wildlife (Japan Wildlife Conservation Society, 2012). Similarly, efforts
based upon educating the public as to the potential of creating nuisance
animals and inadvertently encouraging bothersome or dangerous behaviors amongst
urban animals should be conducted. Although signs requesting that visitors
refrain from feeding black kites are regularly posted in Kamakura and Enoshima,
over the course of this study, several instances of visitors feeding black
kites and subsequently being attacked by them were witnessed. Public forums
addressing the issue of urban habitat degradation and loss and the adverse
effects upon wildlife-human interactions should be conducted, especially in
areas where these aggressive, dangerous behaviors are common.
Aside
from introducing public forums, promoting environmental education, and
increasing cooperation between forest management agencies, other methods can
also be taken in order to increase the viability of urban habitats. A study by
Johan Colding in 2007, for example, described how ecological land-use
complementation (ELC) can promote biodiversity within cities. Because urban
green spaces are highly fragmented, local habitat quality (and, consequently,
its management) is of utmost importance to biodiversity protection. Although it
is difficult to create more green space in large cities, Colding hypothesized
that habitat enlargement can be completed through the use of different types of
green patches; for example, domestic gardens, native tree stands, and ponds can
all attract wildlife and act as habitats. Even wooded streets can help group
together these green patches, effectively creating a larger habitat for
wildlife (Colding, 2007; Fernandez-Juricic and Jokimaki, 2001). If at all
possible, clustering of these green areas could promote habitat viability and a
great amount of biodiversity, and the principles of High Nature Value
evaluations imply that agriculture would benefit from the placement of native
tree stands near urban farmlands.
Another
recent innovation that increases biodiversity and urban green space is the
“green roof.” Urban buildings create a green space by laying down a growing
medium such as dirt over a waterproof membrane upon the roof and growing plants
within them (Orbendorfer et al.,
2007; Fernandez-Canero and Gonzales-Redondo, 2010). These green roofs not only
act as an insulator, thereby saving energy, and as aesthetic space, but they
also provide shelter, protection, and food to birds, insects, and small
mammals. Green roofs with thick substrates can even host trees, thus increasing
the potential for creating urban forested areas. By using green roofs, small
parks, domestic gardens, and wooded streets, urban planners can effectively
increase the available habitat in cities without sacrificing human comfort. Although
not all roofs in cities are capable of supporting green roofs, and the initial
cost of installing green roofs can be high (Orbendorfer et al., 2007; Fernandez-Canero and Gonzales-Redondo, 2010), the
potential benefits towards urban ecosystems should be thoroughly investigated,
particularly in light of the inherent difficulties of creating viable habitat
space in cities (Henry and Frascaria-Lacoste, 2012; Francis and Lorimer, 2011;
Francis, 2010).
By
combining these green roof and ELC tactics with the aforementioned changes in
administration and education, the negative effects of urbanization upon bird
aggressiveness can potentially be mitigated. Previous research has shown that careful
city planning, architectural and habitat design, and wildlife management,
nuisance behaviors that have developed in urban species over decades of acclimatization
can be alleviated (Belant, 1997), resulting in wildlife that is less harmful to
itself and to humans. Although black kites were chosen as the focus animal of
this study, various other urban birds, such as crows, have become nuisances in
countless cities worldwide, and the effects of green space reduction seen here
could have implications for other urban animals as well.
When
birds become pests or begin displaying troublesome behavior, as the black kite
has in Japan, management should take these behavioral changes into account and
investigate the potential underlying causes. The injuries suffered by victims
of black kite aggression along Sagami Bay serve as an example of potential
damages caused by behavioral shifts in wildlife due to urbanization; mitigation
or prevention of these behaviors should be a major concern to developers. Through
this study, urban green space reduction has been shown to have a significant
impact upon black kite aggression. Forests and agricultural areas are
particularly important for mitigating aggressive tendencies, and steps should
be taken to properly conserve and manage these land-use types. Although the
amount of habitat space alone cannot account for all of the behavioral
differences witnessed, nesting habitat and preferred foraging habitats are clearly
of some importance to black kites, as evidenced from each population’s
differences in behavior. Thus, in order to prevent further novel, harmful
behaviors from developing amongst urban animals, cities should attempt to
determine which types of green space are of vital importance to resident
wildlife and consider them accordingly when planning future urban landscapes.
References
Anderies,
J. M., M. Katti, and E. Shochat. 2007. Living in the city: Resource
availability, predation, and bird population dynamics in urban areas. Journal
of Theoretical Biology 247: 36–49.
Baudains,
T. P. and P. Lloyd. 2007. Habituation and habitat changes can moderate the
impacts of human disturbance on shorebird breeding performance. Animal
Conservation 10: 400–407.
Bell,
A. M. 2005. Behavioural differences between individuals and two populations of
stickleback (Gasterosteus aculeatus).
J. Evol. Biol. 18: 464–473.
Belant,
J. L. 1997. Gulls in urban environments: landscape-level management to reduce
conflict. Landscape and Urban Planning 38: 245-258.
Blair,
R. 1996. Land use and avian species diversity along an urban gradient.
Ecological Applications 6(2): 506-519.
Blanco, G. 1994. Seasonal abundance of black kites
associated with the rubbish dump of Madrid, Spain. J. Raptor Res. 28 (4):
242-245.
Blumstein,
D. T. 2006. Developing an evolutionary ecology of fear: how life history and
natural history traits affect disturbance tolerance in birds. Animal Behavior
71: 389–399.
Blumstein,
D. T., E. Fernandez-Juricic, P. A. Zollner, and S. C. Garity. 2005.
Inter-specific variation in avian responses to human disturbance. Journal of
Applied Ecology 42: 943–953.
Bonier,
F., P. R. Martin, and J. C. Wingfield. 2007. Urban birds have broader
environmental tolerance. Biol. Lett. 3: 670-673.
Burton,
N. H. K. 2007. Landscape approaches to studying the effects of disturbance on
waterbirds. Ibis 149 (Suppl. 1): 95–101.
Castro,
J. J. and J. A. Santiago. 1998. The
influence of food distribution on the aggressive behaviour of juvenile
white-seabream (Diplodus sargus cadenati de
la Paz, Bauchot and Daget, 1974). Aggressive Behavior 24: 379-384.
Catry,
I., T. Amano, A. M. A. Franco, and W. J. Sutherland. 2012. Influence of spatial
and temporal dynamics of agricultural practices on the lesser kestrel. Journal
of Applied Ecology 49: 99-108.
Chase,
J. F. and J. J. Walsh. 2006. Urban Effects on Native Avifauna: A Review.
Landscape and Urban Planning 74: 46–69.
Colding,
J. 2007. ‘Ecological land-use complementation’ for building resilience in urban
ecosystems. Landscape and Urban Planning 81: 46–55.
Danhardt,
J., M. Green, A. Lindstrom, M. Rundlof, and H. G. Smith. 2010. Farmland as
stopover habitat for migrating birds—effects of organic farming and landscape
structure. Oikos 119 (7): 1114-1125.
Doxa,
A., M. L. Paracchini, P. Pointereau, V. Devictor, and F. Jiguet. 2012.
Preventing biotic homogenization of farmland bird communities: the role of High
Nature Value farmland. Agriculture, Ecosystems & Environment 148: 83-88.
Errard,
C. and A. Hefetz. 1997. Label
familiarity and discriminatory ability of ants reared in mixed groups. Insectes
soc. 44: 189-198.
Evans,
J., K. Boudreau, and J. Hyman. 2010. Behavioural Syndromes in Urban and Rural
Populations of Song Sparrows. Ethology 116: 588–595.
Evans,
K. L., B. J. Hatchwell, M. Parnell, and K. J. Gaston. 2010. A conceptual
framework for the colonization of urban areas: the blackbird Turdus merula as a case study. Biol.
Rev. 85: 643–667.
Fernandez-Carero,
R. and P. Gonzales-Redondo. 2010. Green Roofs as a Habitat for Birds: A Review.
J. Anim. Vet. Adv. 9 (15): 2041-2052.
Fernandez-Juricic,
E. and J. Jokimaki. 2001. A habitat island approach to conserving birds in
urban landscapes: case studies from southern and northern Europe. Biodiversity
and Conservation 10: 2023–2043.
Fokidis,
H. B., M. Orchinik, and P. Deviche. 2011. Context-specific territorial behavior
in urban birds: No evidence for involvement of testosterone or corticosterone.
Hormones and Behavior 59: 133-143.
Forero,
M. G., J. A. Donazar, J. Blas, and F. Hiraldo. 1999. Causes and consequences of
territory change and breeding dispersal distance in the Black Kite. Ecology,
80(4): 1298–1310.
Forero,
M. G., J. A. Donazar, and F. Hiraldo. 2002. Causes and fitness consequences of
natal dispersal in a population of black kites. Ecology 83 (3): 858-872.
Francis,
R. A. 2011. Wall ecology: A frontier
for urban biodiversity and ecological engineering. Progress in Physical
Geography 35: 43-63.
Francis, R. A. and J. Lorimer. 2011. Urban
reconciliation ecology: the potential of living roofs and walls. Journal of
Environmental Management 92: 1429-1437.
Gering,
J. C. and R. B. Blair. 1999. Predation on artificial bird nests along an urban
gradient: predatory risk or relaxation in urban environments? Ecography 22:
532-541.
Gillies,
C. S., M. Hebblewhite, S. E. Nielsen, M. A. Crawchuk, C. L. Aldridge, J. L.
Frair, D. J. Saher, C. E. Stevens, and C. L. Jerde. 2006. Application of random effects to the study of
resource selection by animals. Journal of Animal Ecology 75: 887-898.
Gonzalez,
L. M., B. E. Arroyo, A. Margalida, R. Sanchez, and J. Oria. 2005. Effect of
human activities on the behaviour of breeding Spanish imperial eagles (Aquila adalberti): management
implications for the conservation of a threatened species. Animal Conservation
9: 85–93.
Hamao, S. 2011. Seasonal increase
in intensity of nest defense against little cuckoos by Japanese bush warblers.
Animal Behavior 82 (4): 869-874.
Hedblom,
M. and B. Soderstrom. 2010. Landscape effects on birds in urban woodlands: an
analysis of 34 Swedish cities. J. Biogeogr. 37: 1302–1316.
Henry,
A. and N. Frascaria-Lacoste. 2012. The green roof dilemma—A discussion of
Francis and Lorimer (2011). Journal of Environmental Management 104: 91-92.
Imai,
H. and T. Nakashizuka. 2010. Environmental factors affecting the composition
and diversity of avian community in mid- to late breeding season in urban parks
and green spaces. Landscape and Urban Planning 96: 183–194.
Iwai,
Y. 2002. “New relationship between forests and city dwellers in Japan.” Forestry and the Forest Industry in Japan.
Ed. Yoshiya Iwai. UBC Press: 278-291.
Japan
Wildlife Conservation Society. Accessed 25 June 2012.
<
http://www.jwcs.org/activity/college.html>
Khera,
N., V. Mehta, and B. C. Sabata. 2009. Interrelationship of birds and habitat
features in urban greenspaces in Delhi, India. Urban Forestry & Urban Greening
8: 187–196.
Koga,
K. and S. Shiraishi. 1994. Copulation behaviour of the Black Kite Milvus
migrans in Nagasaki Peninsula. Bird Study 41: 1, 29—36.
Leidner,
A. K. and N.M. Haddad. 2011. Combining
measures of dispersal to identify conservation strategies in fragmented
landscapes. Conservation Biology 25: 1022-1031.
MacGregor-Fors,
I. 2010. How to measure the urban-wildland ecotone: redefining ‘peri-urban’
areas. Ecol. Res. 25: 883–887.
Matsuki,
Y. 2002. Agri-food supply chain
development by various chain leaders: case studies in Japan and new concept of
High Nature Value. Proceedings of the International Farm Management Association.
Accessed 25 June 2012.
<
http://ageconsearch.umn.edu/bitstream/6971/2/cp02ma05.pdf>
Matsushita,
K. 2002. “Forest planning.” Forestry and
the Forest Industry in Japan. Ed. Yoshiya Iwai. UBC Press: 118-144.
Møller,
A. P. 2008. Flight distance of urban birds, predation, and selection for urban
life. Behav. Ecol. Sociobiol. 63: 63-75.
Orbendorfer,
E., J. Lundholm, B. Bass, R. R. Coffman, H. Doshi, N. Dunnet, S. Gaffin, M.
Kohler, K. K. Y. Liu, and B. Rowe. 2007. Green Roofs as Urban Ecosystems:
Ecological Structures, Functions, and Services. Bioscience 57 (10): 825-833.
Ortega-Alvarez,
R. and I. MacGregor-Fors. 2009. Living in the big city: Effects of urban
land-use on bird community structure, diversity, and composition. Landscape and
Urban Planning 90: 189–195.
Pease,
M. L., R. K. Rose, and M. J. Butler. 2005. Effects of human disturbances on the
behavior of wintering ducks. Wildlife Society Bulletin 33: 103-112.
The
Satoyama Initiative. Accessed 25 June 2012. <
http://satoyama-initiative.org/en/>
Scales,
J., J. Hyman, and M. Hughes. 2011. Behavioral syndromes break down in urban
song sparrow populations. Ethology 117: 887-895.
Searcy,
W. A., R. C. Anderson, and S. Nowicki. 2006. Bird song as a signal of
aggressive intent. Behav. Ecol. Sociobiol. 60: 234–241.
Sergio,
F., P. Pedrini, and L. Marchesi. 2003. Adaptive selection of foraging and
nesting habitat by black kites (Milvus
migrans) and its implications for conservation: a multi-scale approach.
Biological Conservation 112: 351–362.
Sergio,
F., J. Blas, L. López, A. Tanferna, R. Díaz-Delgado, J. A. Donázar, and F.
Hiraldo. 2011. Coping with uncertainty:
breeding adjustments to an unpredictable environment in an opportunistic
raptor. Oecologia 166: 79-90.
Shiraishi, S., K. Koga, and N. Kawaji. 1990. Food
habits of the black-eared kite, Milvus migrans lineatus, in Nagasaki airport
and its adjacent areas. J. Fac. Agric Kyushu Univ. 34:247-254.
Tabachnick, B. G., and L. S. Fidell. 2007. Using Multivariate Statistics. Ed. Susan
Hartman. Pearson Education, Inc.
Tanner, C. J., G. D. Salat, and A. L. Jackson. 2011.
Feeding and non-feeding aggression can be induced in invasive shore crabs by
altering food distribution. Behav. Ecol. Sociobiol. 65: 249-256.
Tavernia, B. G. and J. M. Reed. 2010. Spatial,
temporal, and life history assumptions influence consistency of landscape
effects on species distributions. Landscape Ecol. 25: 1085-1097.
Trubl, P., V. Blackmore, and J. C. Johnson. 2011.
Wasteful Killing in Urban Black Widows: Gluttony in Response to Food Abundance.
Ethology 117: 236-245.
Valeria,
M., L. Fuscani, F. Dessì-Fulgheri, and V. Canoine. 2011. Non-migratory stonechats show seasonal
changes in the hormonal regulation of non-seasonal territorial aggression.
Hormones and Behavior 60 (4): 414-419.
Walpole, A. A. and J. Bowman. 2011. Patch occupancy
by squirrels in fragmented deciduous forest: effects of behavior. Acta.
Theriol. 56: 63-72.