Download Coupled Relationships between Humans and other Organisms in

OUP UNCORRECTED PROOF – FIRST PROOF, 09/29/10, SPi
CHAP TER 3.1
Coupled Relationships between
Humans and other Organisms
in Urban Areas
Barbara Clucas and John M. Marzluff
3.1.1 Introduction
Today’s urban landscapes, from cities and suburbs
to sparse rural and exurban settlements, are the
stages for an incredible evolutionary play. Humans
are the lead actors, affecting the genetic and cultural
inheritance of other species. But non-human organisms are also important players, influencing our
culture and genetic legacy. Humans, other species,
and abiotic elements and processes are tightly coupled in urban ecosystems, perhaps more today than
ever before. This coupling of human and natural
systems (Liu et al. 2007a, b) has recently gained
attention, with researchers expressing a need to
investigate the mechanistic underpinnings and
complexities of these interactions (Grimm et al.
2000; Alberti et al. 2003; Liu et al. 2007a, b). This need
stems from both a purely theoretical point of view
and an applied perspective. As the world becomes
more urbanized, our increased well-being has come
at a cost to nature, which in turn is now becoming
costly to humans (Tarsitano 2006; Lui et al. 2007a).
Although we might appreciate the potential
extent of human and natural system coupling as
our urban footprint (Marzluff et al. 2008; Fig. 3.1.1),
it is more difficult to imagine our ongoing evolution. It appears that we have distanced ourselves
from the natural world, creating ‘artificial’ environments by altering nature in physical ways, with the
removal of vegetation and building of man-made
structures, and changing the way we obtain food
(e.g. no longer hunting or gathering). However, as
urban areas increase worldwide we are increasing
both the number of our interactions with the natural world and the intensity of these interactions (Liu
et al. 2007a, b), and these increases affect people and
nature (Marzluff & Angell 2005a).
The influence of humans on other organisms,
from wild to domesticated, is profound (see also
Adams and Lindsay, Chapter 2.4). Humans affect
species survival, population structure, reproduction, behaviour, and evolution in urban areas (e.g.
Marzluff 2001, 2005; Chace & Walsh 2006; Ditchkoff
et al. 2006; Brunzel et al. 2009). Changing landcover
has had a major influence on wildlife populations
and communities across the globe, and fragmentation, degradation, and pollution are also known to
have negative and positive consequences for the
survival of animal and plant populations (Donnelly
& Marzluff 2006). However, less is known about the
extent to which human behaviour towards other
organisms (intentional or unintentional) can affect
urban plants and wildlife and subsequently affect
their population viability and evolution.
In this chapter we provide a brief background on
the relationship between humans and natural systems and how complex feedback loops can emerge
and form coupled systems. We will then focus on
interactions between humans and other organisms,
the selective forces they impose, and the potential
outcomes of such relationships. We document interactions that began with early sedentary lifestyles up
to present urban settings and discuss the potential
for coevolution. We then describe in detail how a
135
0001215609.INDD 135
9/29/2010 6:43:24 PM
OUP UNCORRECTED PROOF – FIRST PROOF, 09/29/10, SPi
136
URBAN ECOLOGY
Global Inputs
(e.g., oil, gas, manufactured goods)
Biosphere:
plants
and animals
Pedosphere
Atmosphere
Lithosphere
Anthropospher:
politics, economics,
administration,
civic participation,
planning,
demographics
Hydrosphere
The Urban Ecosystem
Global Outputs
(e.g., CO2, manufactured goods,
pollutants)
Figure 3.1.1 Components of the urban ecosystem (white area) and
the relationships between humans (anthroposphere) and nature
(other elements of the ecosystem) within the ecosystem. Coupling of
human and natural systems is indicated by the dual-headed arrows
linking components (arrow width indicates relative magnitude of
linkage). The global footprint of the coupled human and natural
system that is the urban ecosystem is indicated by the gray area.
Reprinted from Marzluff et al. (2008)
focal group (birds) and humans interact in urban
areas. To conclude, we will discuss how studying
coupled relationships of humans and other organisms is a new direction of research for urban ecologists and some other potential areas to be explored.
3.1.2 Humans and natural systems
Humans have been important components of
almost every ecosystem for thousands of years, but
their influence on natural processes has increased
dramatically in the recent past (Grimm et al. 2000;
Liu et al. 2007a). Ecosystem dynamics are driven by
patterns and processes associated with biotic and
physical factors, as well as climate and element
cycles. Humans contribute to these processes by
using land and resources, producing waste, and
changing communities of fauna and flora (Grimm
et al. 2000). Although humans play a large role in
these systems, the outcomes are not always favour-
0001215609.INDD 136
able to humans themselves (e.g. pollution). Research
on the complex ways humans and natural systems
interact has been stressed as a means of understanding how we can work to decrease negative consequences of our actions (Liu et al. 2007a, b).
Interactions between humans and natural systems can form positive and negative feedback loops
(Liu et al. 2007a). An example of a positive (unregulated) feedback loop is the over-exploitation of natural resources. Short-term economic gains for
corporations can fuel the unsustainable degradation of natural systems at a large cost to the general
populace. For instance, intensive farming of shrimp
or salmon pollutes and depletes the aquatic environment for short-term profit but long-term loss of
ecosystem services (Balmford et al. 2002). As natural
production of salmon and shrimp collapse, aquaculture may increase because wild alternatives are
extinct, further degrading the natural ecosystem
and robbing society of ecological services. We suspect unregulated feedback loops to be rare, because
of their great cost to society (Liu et al. 2007a). Perhaps
more likely are negative, or self-regulating, feedback loops. For example, loss of iconic ecosystem
elements in urban ecosystems, like salmon or redwood trees, may trigger policies to stem extinction
(listing of salmon in Seattle, Washington, under the
US Endangered Species Act, or reservation of redwood forests as US National Parks, for example) or
the recognized economic benefits of ecosystem
services may prompt watershed conservation over
degradation and development of water treatment
facilities. Self-regulation is often delayed until costs
to society and nature are extreme.
Positive, mutually reinforcing, reciprocal feedback loops are also possible between humans and
animals. For example, the Wolong Nature Reserve
in China provides needed habitat for threatened
giant pandas (Ailuropoda melanoleuca), but humans
are also living in the reserve and they degrade the
habitat by collecting firewood and setting up agriculture (An et al. 2006). These actions negatively
affect both the panda population and the local economy because if pandas are not doing well, ecotourism suffers. An et al. (2006) hypothesize that if
the quality of electricity is increased in the area (e.g.
voltage increases), humans would collect less wood
for fires and this would then support panda viability and increase profit from ecotourism.
9/29/2010 6:43:24 PM
OUP UNCORRECTED PROOF – FIRST PROOF, 09/29/10, SPi
COUPLED RELATIONSHIPS BETWEEN HUMANS AND OTHER ORGANISMS IN URBAN AREAS
These examples of reciprocal feedback loops
between humans and nature demonstrate that to
understand these interactions, one must to integrate
information about human socio-economic factors,
animal and plant biology, as well as human behaviour (e.g. legislation).
3.1.3 Interactions between humans
and other organisms
Humans have had an unavoidable link to animals
in their environment. During human evolution we
have in part transitioned from being prey to predators and then caretakers of other animals as our diet
and lifestyles changed over time (e.g. nomadic to
sedentary; O’Connor 1997, Heffner 1999). However,
human–animal relationships go beyond those of
food: we are tightly connected to numerous animal
species, from microbial organisms in our intestines
that aid digestion, to rodents living uninvited in our
homes (Somerville 1999), to captive elephants that
provide a work force.
To help distinguish what type of relationships
humans have with certain species, it is useful to
determine the effects each interaction has on each
participant (positive, negative, or neutral). Most animals living with humans in urban areas are commensal: they benefit from living in proximity to
humans without overtly harming them. In some
cases, these relationships are very old and their origins coincide with human sedentism (O’Connor
1997). Indeed, the presence of rat (Rattus spp.) and
mouse (Mus domesticus) remains can be used as a
proxy of human settlement at archeological sites
(Somerville 1999). These species were most likely
attracted to the increase in foraging opportunities
provided by human rubbish and warmth provided
by human dwellings. The historical relationship
of rats (R. rattus and R. norvegicus) and mice (M.
domesticus) with humans is marked by changes in
human behaviour. There is archaeological evidence
for increased efficiency of food storage devices that
is attributed to preventing pilferage by rodents
(Somerville 1999). In addition, the negative effects
(or at times negative perception) of rodents have led
humans to tolerate the presence of rodent predators
such as mustelids and felines (Somerville 1999).
Humans in urban areas often have negative perceptions of many other organisms sharing their
0001215609.INDD 137
137
environment (e.g. cockroaches, pigeons, raccoons,
opossums, bats, dandelions and other weedy or
poisonous plants). These organisms thrive on living
in proximity with humans by foraging on human
refuse or finding suitable habitat in gardens, housing, or attics. Urban pests have adapted to living
with humans by adjusting their activity patterns
(e.g. nocturnality) or habituating to humans.
Sometimes, these organisms can have serious negative impacts on humans, such as the spread of rabies
or other diseases, however in most instances they
are simply nuisances.
Some urban pests are non-native species as urban
areas seem to select for or attract exotic, invasive
species. Native species, which are adapted to local
habitats, are often replaced by these invasive species that tend to be generalists capable of quickly
adjusting to an urban lifestyle (e.g. Marzluff 2001).
Transition from native to exotic communities of
organisms can be attributed to structural changes in
habitat, temperature changes (urban areas tend to
be warmer than outside areas), and, for certain species, availability of human refuse (as mentioned
above) for foraging. However, humans can also
directly contribute to these species changes. For
instance, vegetation in cities consists of more exotics than native species due to humans planting
exotics and the increased dispersal of seeds by
human foot and automobile traffic (Sukopp 1973;
Kowarik 1995; Brunzel et al. 2009).
Humans also share positive interactions with other
organisms, whereby both parties benefit from forming a mutualistic relationship. Perhaps the best-known
historical mutualism is that of humans and dogs, the
‘domesticated’ relative of wild canids. The exact origins and history of this relationship is a bit contentious
(see Schleidt & Shalter 2003), but today dogs provide
benefits to humans as companions, guards, and workers (hunting partners, seeing-eye, sheep herders, drug
and people finders). In turn, dogs benefit from humans
because they are provided with food, shelter, protection, and from the species level, have increased their
population sizes and spread throughout the world
(Heffner 1999). Although indirect, humans and urban
animals share a positive interaction with trees and
plants. Urban parks provide habitat and increase viability for many animal species while also providing a
view of nature for humans which has positive health
benefits (Maller et al. 2005).
9/29/2010 6:43:24 PM
OUP UNCORRECTED PROOF – FIRST PROOF, 09/29/10, SPi
138
URBAN ECOLOGY
Domestication is the extreme in symbiotic relationships between humans and animals. Domestication
can loosely be defined as ‘the capture and taming by
man of animals of a species with particular behavioural characteristics, their removal from their natural living area and breeding community, and their
maintenance under controlled breeding conditions
for mutual benefits’ (O’Connor 1997). Interestingly,
as O’Connor (1997) points out, this definition ends
by claiming animals benefit from being domesticated
by humans. Indeed, domestication of animals by
humans not only increased our fitness but also those
of the animals, as they quickly became more numerous and widespread than their wild ancestors
(Heffner 1999). Furthermore, this ‘selection by man’
created animals that became dependent on humans
for survival and reproduction and in turn, humans
developed a dependence on these animals for food,
horsepower, and in some cases, companionship and
protection (Heffner 1999). O’Connor (1997) continues by suggesting, ‘domestication is unlikely to be
one-sided’ and that domestication can be seen as a
form of coevolution between humans and animals
(see also Schleidt & Shalter 2003).
3.1.4 Coevolution of humans
and animals
Coevolution occurs in nature when two species are
interlocked in evolutionary interactions that drive
reciprocal selection between the species. When
humans select for certain phenotypic traits in other
species that, in turn, affect human phenotypes, we
can call this coevolution. Two excellent examples of
coevolution through positive interactions between
humans and an animal species involve cooperation to
gain a common food source. The first is between the
Boran people of East Africa and a bird species, the
Greater Honeyguide (Indicator indicator) (see Marzluff
& Angell 2005a). Honeyguides eat wax and larvae of
honeybees but cannot raid hives themselves due to
the thickness of the hives. They can forage on honeycombs, however, after they lead humans to, and
humans break open, the hive. Thus, working together,
humans and honeyguides can efficiently locate and
access a food source that is rarely obtained by either
species working alone. The second example is
between fishers in Laguna, Brazil, and bottlenose dol-
0001215609.INDD 138
phins (Tursiops truncates) (Marzluff & Angell 2005b).
Here again both parties have altered their behaviour
to work with another species for a mutual benefit—
dolphins chase fish into the fisher’s nets. However, in
this example the interaction between organisms is
culturally coevolved (Marzluff & Angell 2005b).
Dolphins learn this ‘hunting behaviour’ and likewise
people must learn how to work with the dolphins.
Humans are known to have large evolutionary
influences on other species in urban environments
(Palumbi 2001) but we know less about how urban
animals influence humans. Interactions between
humans and animals in urban areas have the
potential for forming feedback loops and leading to
coevolution of behavioural (including cultural),
physiological, or morphological traits. Our ancient
and ongoing relationships with birds of the corvid
family (crows, ravens, magpies, nutcrackers, and
jays; hereafter ‘crows’) provide many examples,
including arms races between crows and humans
that are intent on scaring or hunting them, and
mutually supportive interactions between crows
and individual people or societies who worship
them (Marzluff & Angell 2005a, b). Consider our
propensity to import fruits, pave ground, and drive
cars. These human cultures spawn unique corvid
foraging activities, which include socially learned
customs or cultures, which in turn feed back to
reshape human culture. Carrion Crows (Corvus corone) in Sendai, Japan, harvest walnuts each autumn
and carefully place them in front of cars stopped at
traffic signals. When the cars move, the nuts are
crushed, and the birds fly down to eat the nutritious
nutmeat (Nihei & Higuchi 2001). This behaviour is
spreading slowly from the place it was first observed
20 years ago, which is consistent with social learning. In accordance with cultural evolution, other
populations of Carrion Crows do not use cars to
crack nuts, but they do drop nuts to crack them.
Drivers in Sendai are changing their habits, in part
because of the interest the world has shown in their
innovative crows: they now routinely and purposefully run over nuts (H. Higuchi, pers. comm.).
3.1.5 Humans and birds in urban areas
Ask an urban dweller what type of animal is seen
on a daily basis and the response will likely be
9/29/2010 6:43:24 PM
OUP UNCORRECTED PROOF – FIRST PROOF, 09/29/10, SPi
COUPLED RELATIONSHIPS BETWEEN HUMANS AND OTHER ORGANISMS IN URBAN AREAS
birds. The connection between birds and human
settlements is not a novel one. The House
Sparrow’s (Passer domesticus) commensal relationship with humans is estimated to have begun
between 400,000 and 10,000 years ago in the
Middle East (Anderson 2006). This species is
hypothesized to have become an obligate commensal species with humans because of yearround access to stored grain, and has also changed
from a migratory to a sedentary lifestyle (Anderson
2006). Similar to human commensal rodent species, abundant remains of House Sparrows at
archeological sites serves as a proxy of human settlement (Somerville 1999).
3.1.5.1 Effects humans have on birds
Due in part to their popularity as a study species
and presence in cities, there are many studies on
bird species in urban areas, addressing aspects from
species compositions and abundances to life history
and behaviour (see Chace & Walsh 2006, Robb et al.
2008, Chamberlain et al. 2009, Evans et al. 2009). The
effects humans have on birds in urban areas are
both positive and negative (Table 3.1.1a) and vary
across species (see below; Marzluff 2001). Key factors negatively affecting bird species are habitat
alteration (loss, fragmentation, small patch sizes,
vegetation changes) and introduced/exotic species
(predators and competitors; Chace & Walsh 2006;
see also Table 3.1.1a). These factors, however, are
mostly indirect. Direct negative effects of human
behaviour in urban areas, such as disturbance, have
received less attention (Evans et al. 2009, but see
Fernandez-Juricic et al. 2003; Möller 2008; Schlesinger
et al. 2008).
Humans may unintentionally negatively affect
birds in urban areas simply by passing by a nest or
walking in a foraging area (Fernandez-Juricic et al.
2003; Möller 2008). Human visitation to parks and
other natural areas can disturb birds’ foraging,
breeding, and nesting behaviour (Chace & Walsh
2006). Although we have a considerable understanding about risk assessment in animals, most
studies attempting to test effects of human disturbance on bird species were conducted in seminatural areas (parks, forest remnants or fragments,
0001215609.INDD 139
139
or by lakes) within cities. Perhaps the assumption
that birds in less natural areas in cities are more
habituated to humans (see Evans et al. 2009) or that
it is easier to conduct such research in semi-natural
areas accounts for paucity of studies in less natural
areas.
A major direct action by humans towards birds
occurs with supplementary food. In fact, up to 43
per cent of households in the United States and 75
per cent in the United Kingdom feed birds (Robb
et al. 2008), and 48 per cent of urban households in
the UK provide food for birds (Evans et al. 2009).
The effect of supplementary feeding on birds in
urban areas has the potential to be substantial (Table
3.1.1a; Lepczyk et al. 2004, Chace & Walsh 2006,
Fuller et al. 2008, Robb et al. 2008, Chamberlain et al.
2009). Most experimental studies on the influences
of feeding birds, however, have been conducted in
rural areas (see Evans et al. 2009). Nevertheless,
feeding birds is likely to have an overall positive
effect on birds in urban areas and is often cited as a
large contributing factor to the increased density of
certain species in cities.
3.1.5.2 Effects birds have on humans
Due to their abundance in urban areas, birds are
often the most visible wildlife in human-dominated
areas. The influences birds have on humans are outlined in Table 3.1.1b. Just the presence of birds can
positively effect human health and well-being, as
studies have shown that viewing nature can
decrease recovery time after surgeries; improve
blood pressure, cholesterol levels, and outlook on
life; reduce stress and mental fatigue; and improve
concentration (Bjerke & Ostdahl 2004; Maller et al.
2005). Birds can also perform certain ecological
services for humans, such as decreasing pest arthropod numbers (Kepczyk et al. 2004).
The negative impacts of birds on humans are
mostly indirect—damage to property (including
homes, vegetable gardens, and fruit trees) and nesting and defecating in undesirable places; however,
birds can transmit disease and some species will even
attack humans (e.g. corvids and gulls; Marzluff et al.
1994). In fact, this propensity to attack people may be
a cultural and genetic response of birds to the lack of
hunting in cities (Knight 1984, Knight et al. 1987).
9/29/2010 6:43:24 PM
OUP UNCORRECTED PROOF – FIRST PROOF, 09/29/10, SPi
140
URBAN ECOLOGY
Table 3.1.1a Positive and negative effects of human actions on birds
Human action
Direct
Feeding
Harassing
Unintentional disturbance
Intentional killing
Driving vehicles
Indirect
Habitat destruction/alteration
Vegetation changes
Habitat fragmentation
Pesticides
Light pollution
Noise pollution
Exotic species introduction
Road-kill
Waste
Effect on birds
Positive: increased winter survival1, population sizes1, and prey base for raptors1
Negative: decreased diet quality2; inadequate diet for nestlings2; increase disease transmission1,
predation risk1, and exotics (negative for native species)2
Negative: time wasted fleeing; disturbed from foraging, mating, nesting, and other activities
Negative: decrease in reproductive success (nest desertion; decrease in hatchling success, ability to feed
young and parental attendance; increase in predation)1; disturbed from foraging, mating, nesting, and
other activities decrease in species richness3
Positive: decrease of exotics (positive for native species)
Negative: decreased population sizes
Positive: provision of food for scavengers
Negative: death or injury from collision1
Negative: loss of nesting and foraging sites; increased exposure to predators4; collisions with buildings1;
decrease in species richness
Positive: population increases due to exotic vegetation (especially for exotic bird species)1;
Negative: loss of nesting and foraging sites; increased exposure to predators; decrease in species richness
Positive: increased proximity of diverse land covers and resources used by generalist species
Negative: limiting dispersal
Negative: toxic and/or lethal5; decrease of arthropod pests5
Positive: advanced breeding2
Negative: inappropriate behaviour (e.g. singing at night)
Negative: decrease in communication efficiency1
Negative: increased competition for food and nesting sites; increased predation
Negative: negative when a bird is killed
Positive: positive for scavengers
Positive: increased winter survival and population sizes
Negative: decreased diet quality1; inadequate diet for nestlings; increased exotics (negative for native species)1
1
Chace & Walsh 2006
Chamberlain et al. 2009
3
Schlesinger et al. 2008
4
Evans et al. 2009
5
Lepczyk et al. 2004
2
3.1.5.3 Factors contributing to variation
in human–animal interactions
The interactions between humans and birds in urban
areas are influenced by various factors. First, characteristics of the urban environment, such as city age
(Marzluff in press), size, geographic location, and
habitat type can influence relationships. For example,
in comparison to European cities, North American
cities are relatively young and species compositions
of birds may include species that are currently
adapting to urban life or being driven to extinction,
0001215609.INDD 140
whereas older European cities may include more
adapted species (Marzluff in press).
Human interactions with and attitudes towards
animals can be influenced by human demographic,
socio-economic, and cultural factors. For instance,
age, gender, and education can affect whether landowners feed birds, and occupation and relative
house size can influence if they use pesticides or
herbicides, which can harm birds (Lepczyk et al.
2004). In addition, people in deprived areas are less
likely to feed birds (e.g. Fuller et al. 2008). Human
interest and concern for animals have been shown
9/29/2010 6:43:24 PM
OUP UNCORRECTED PROOF – FIRST PROOF, 09/29/10, SPi
COUPLED RELATIONSHIPS BETWEEN HUMANS AND OTHER ORGANISMS IN URBAN AREAS
141
Table 3.1.1b Positive and negative effects of bird actions on humans
Bird action
Effect on humans
Visiting feeder
Positive: reward for feeding1, health aspects of viewing nature3, growth of bird feeding
industry
Negative: loss of crops or fruit
Positive: decrease of insect pests
Positive: decrease of rodent pests1
Negative: damage to property, possible disease transmission
Positive: healthy aspects of view nature
Negative: damage, increased noise, fecal droppings
Negative: time and cost of repair
Positive: health aspects of viewing nature2; education value3; increasing conservation
awareness3
Negative: negative perception of urban animals (e.g. pigeons)3
Foraging on crops and/or fruit trees
Foraging on insects
Raptors foraging
Defecating
Nesting or roosting on property
Damage to property
Visual presence
Increased exotics
1
Chace & Walsh 2006
Maller et al. 2005
3
Dunn et al. 2006
2
to vary with age, gender, and education level (see
review in Bjerke & Ostdahl 2004). An increase in
education corresponds to an increase in positive
attitudes towards animals, and there are subtle species preference differences between children and
adults and between females and males (Bjerke &
Ostdahl 2004). Cultural differences also exist among
countries where human attitudes and actions
towards animals were surveyed (e.g. USA, Germany,
and Japan; Bjerke & Ostdahl 2004).
Birds’ relationship with humans can vary according
to life history and morphological, physiological and
behavioural traits. Habitat use, degree of specialization (e.g. diet), local history (native or exotic), activity
patterns (e.g. nocturnal vs. diurnal), migratory and
reproductive behaviour, intelligence (e.g. degree of
innovative behaviour), physiological tolerance, and
personality (e.g. risk adverse or explorative) have all
been shown to effect whether bird species are urban
adaptors or avoiders (Jerzak 2001; Chance & Walsh
2006; Croci et al. 2008; Möller 2008; Marzluff in press).
3.1.5.4 Evolutionary changes
Most of the direct and indirect human actions towards
birds and the subsequent effects on bird species,
populations, and individuals described above and in
Table 3.1.1a are proximate in nature. However, our
0001215609.INDD 141
introductions of species and industrial lifestyles often
place urban birds into environments that cause rapid
genetic responses (Marzluff in press). Europeans seeking to acclimate to new lands, for example, enriched
native avifaunas with birds from their homeland.
Since introduction, their morphology, colouration,
and basic migratory habits evolved in response to
novel climatic conditions. In another example, soot
from urban factories in eighteenth- and nineteenthcentury Europe darkened the substrates animals lived
among and allowed predators to drive the evolution
of colouration in many insects and at least one bird,
the Feral Pigeon (Columba livia). Initially, heavy soot
provided an advantage to dark (melanic) forms of
pigeons whose better match to the dark background
reduced predation and provided a selective advantage over lighter morphs (Bishop & Cook 1980). This
classic demonstration of natural selection leading to
‘industrial melanism’ is continuing to respond to
urban policies. With increased pollution control in
urban areas in the latter half of the twentieth century,
the lighter-coloured trees, rocks, and buildings provided safe resting sites for paler morphs and natural
selection has adjusted downward the relative frequency of melanic forms (Cook et al. 1986).
Birds in urban environments have learned to eat
a wide variety of exotic and prepared foods (Marzluff
& Angell 2005a). Some of these innovations have
spread through local populations as culturally
9/29/2010 6:43:24 PM
OUP UNCORRECTED PROOF – FIRST PROOF, 09/29/10, SPi
142
URBAN ECOLOGY
evolved traditions. The cultural evolution of novel
feeding behaviour has been experimentally demonstrated within urban Feral Pigeons (Lefebvre 1986). It
has been implicated in the removal of milk bottle lids
by tits and corvids in Britain (Lefebvre 1995) and in
the use of cars as nutcrackers by Carrion Crows in
Japan as discussed above (Nihei & Higuchi 2001).
Traffic, industry, and built surfaces that characterize urban areas have profoundly altered the acoustic environments that many birds rely on. Low
frequency noise, disruption of sound waves by
large, flat surfaces, and altered sound channels have
selected for shorter, higher frequency, louder, faster,
and novel songs (e.g. Slabbekoorn & den BoerVisser 2006). Such adjustments benefit singing birds
because they enable potential mates and territorial
intruders to hear vocal advertisements in noisy
environments (Slabbekoorn & Smith 2002). In oscine
songbirds, social learning is allowing such changes
to proceed rapidly by cultural evolution, which
may initially constrain, but later promote, speciation (Slabbekoorn & Smith 2002).
The Great Tit (Parus major) is a model species illustrating adaptive, contemporary, cultural evolution of
song in urban environments. Loud, low frequency
noise in major European cities favours short, fast,
and high frequency song (Slabbekoorn & den BoerVisser 2006). Phenotypic plasticity in singing enables
tits to vary song characters. Learning may rapidly fit
songs to the acoustic environment because songs
that can be heard can also be copied and those that
do not elicit responses can be dropped (Slabbekoorn
& den Boer-Visser 2006). Because tits learn in part
through interactions with neighbours on their breeding territory, urban tit songs are consistent and different from rural tit songs (Slabbekoorn & den
Boer-Visser 2006). Assortative mating for habitatdependent song characteristics and their genetic
basis may lead to reproductive isolation and possible
speciation of urban tits (Slabbekoorn & Smith 2002).
But currently, phenotypic plasticity and cultural evolution are simply allowing tits of various genotypes
to persist in urban environments, thereby softening
the force of natural selection on genetic variation.
Some evolution in urban populations is neither
directional nor clearly an adaptive response to natural selection. The culturally derived unique songs
of eastern House Finches (Pytte 1997), for example,
may reflect the random action of genetic drift or the
0001215609.INDD 142
chance occurrence of unique individuals in small
founding populations.
The detailed work needed to understand the relative contributions of phenotypic plasticity, genetic
drift, and adaptive responses to natural selection is
exemplified in Yeh’s (2004) studies of plumage evolution in urban Dark-eyed Juncos (Junco hyemalis). By
raising juncos from urban and wildland nests in a
common environment, determining the effective
population size, and quantifying the rate of evolution, Yeh concluded that the observed reduction in
the proportion of white in the tails of urban (San
Diego, California, USA) juncos was an adaptive
response to natural selection. A variety of aspects of
the San Diego environment may have favoured less
conspicuous tails, including a lengthened breeding
season that favours greater parental investment over
aggressive defense of a territory, increased risk of
predation, and novel climate, food, and vegetation.
Similar experimentation is also documenting the
interplay between phenotypic plasticity and genetic
differentiation in urban Blackbirds (Turdus merula).
In European cities, lack of persecution by people,
artificial light, and supplemental food have enabled
Blackbirds to attain unprecedented densities. Urban
Blackbirds are tamer, less migratory, breed and moult
earlier, and suppress stress responses relative to rural
Blackbirds (Partecke et al. 2006). Changes in stress
response, migratory behaviour, and timing of reproduction are mainly a result of phenotypic plasticity
with some genetic change in adaptive characters
(Partecke et al. 2006). Despite adaptive genetic microevolution, divergence in neutral alleles has not been
detected (Partecke et al. 2006). Experiments on
Blackbirds and Dark-eyed Juncos show how phenotypic plasticity, behavioural innovation, and the
effects of small founding populations may set the initial range of responses that birds exhibit in novel
urban environments, and how heritable traits quickly
evolve in adaptive responses to natural selection.
3.1.5.5 Coupled relationships
As described above, humans can form reciprocal
relationships with natural systems, including animals (An et al. 2006). Due to the high densities
and close contact of humans and animals in urban
areas, these are ideal places to look for such coupled
9/29/2010 6:43:24 PM
OUP UNCORRECTED PROOF – FIRST PROOF, 09/29/10, SPi
COUPLED RELATIONSHIPS BETWEEN HUMANS AND OTHER ORGANISMS IN URBAN AREAS
relationships. A good example is that of humans
and House Sparrows (Anderson 2006).
The relationship between humans and House
Sparrows is ancient (Anderson 2006). House
Sparrows are considered a commensal human species that thrives in urban areas. Recently, however,
declines of native populations in Europe have called
attention to the understanding of the mechanisms
by which House Sparrows have evolved such an
obligate relationship (De Laet & Summers-Smith
2007). House Sparrow populations had decreased
in the past (early 1900s) due to changes in human
lifestyles: the exchange of horse transport for automobiles removed a major food source for the sparrows, as they would feed on oats that spilled out of
the horses’ nosebags (De Laet & Summers-Smith
2007). Therefore, it might be likely that current
declines in urban centres are due to additional
changes in human actions. Indeed, a recent review
suggests a link between the decline and human
socio-economic status (Shaw et al. 2008).
143
Habitat structure in urban areas can differ
depending on the socio-economic status of humans.
For example, in the UK deprived areas are characterized by older houses with gardens that contain
native shrub species, whereas affluent areas are
characterized by newer houses with gardens that
contain more pavement and exotic shrubbery (Shaw
et al. 2008). House Sparrows are likely to be affected
by the increase of affluent areas for several reasons
(Shaw et al. 2008; see Fig. 3.1.2). First, House
Sparrows nest in roof cavities of older houses;
newer houses removed these nesting possibilities.
Second, replacement of native shrubs with exotic
plants and pavement can decrease the abundance
of arthropods that House Sparrows need to feed
their young. Finally, decreasing vegetation can
increase predation risk of visual predators, such as
raptors and domestic or feral cats. These compounding factors can affect adult and nestling survival,
reproduction, and foraging behaviour, all of which
can lead to population declines.
Habitat
Predators
–Affluent areas: new houses, tidy and paveed gardens
–Affluent habitat
lacks nesting areas
and lacks native
shrubs that provide
protection from
predators
+Deprived areas: old houses, native shrubs
Socio-economic status +Affluent humans more likely to feed birds
Education level +Higher-educated humans more interested in birds
Humans
+Providing provisions (food, nestboxes)
House sparrows
+Provide a view of nature
–Nesting and defecating in undesirable places
Positive +
Negative –
Indirect effects
Figure 3.1.2 Interactive relationship between humans and house sparrows in urban areas. House sparrows are urban/human commensal species
that profit from supplementary food provided by humans. In return, House Sparrows provide humans with a view of nature which can provide
health benefits (e.g. reduce stress). Recent declines in House Sparrows in urban areas are in part due to habitat change from old houses
(preferential nest sites) and native shrubs (protection from predators) to new houses with more paved and tidy gardens. However, humans in
affluent areas are more likely to feed birds, and higher educated humans are more likely to be interested and concerned with birds. Therefore,
combined interactions and effects of socio-economic status and education in humans and habitat selection and foraging behaviour in House
Sparrows may be quite complex (see Shaw et al. 2008)
0001215609.INDD 143
9/29/2010 6:43:24 PM
OUP UNCORRECTED PROOF – FIRST PROOF, 09/29/10, SPi
144
URBAN ECOLOGY
Due to their habituation to humans and foraging
behaviour, House Sparrows provide humans with an
up-close view of nature in urban areas. Any restaurant
or café with outdoor seating and leftovers attract sparrows and allow for intimate interactions. Such viewing of, and interaction with, wildlife are known to
positively influence human health and well-being. As
shown in Fig. 3.1.2, the combined interactions and
effects of socio-economic status and education in
humans and habitat selection and foraging behaviour
in House Sparrows may be quite complex, and it is
only through an understanding of these couple interactions that we will be able to modify our actions to
aid in the conservation of this species and others that
share tight connections with humans in urban areas.
3.1.5.6 Potential for coevolution
A unique aspect of contemporary evolution (evolution that occurs in less than a few hundred generations) in urban ecosystems is the potential
coevolutionary relationship between people and
other organisms. We summarize here what we have
explored elsewhere (Marzluff & Angell 2005a;
Marzluff in press) of this intriguing relationship by
extending the theory of niche construction (OdlingSmee et al. 2003) to explicitly consider how people
influence and in turn can be influenced by aspects
of their environment. We suggest that when humans
interact with other social species, who themselves
have the ability to evolve culture, then simple feedbacks from a culturally evolving ‘environment’ can
stimulate rapid cultural evolution in humans.
Exploring this ‘cultural coevolution’ (Marzluff &
Angell 2005a, b) may expand our understanding of
evolution in social urban birds and increase our
awareness of the important cultural services people
obtain from nature.
Humans and other social animals have a dual
inheritance system whereby gene frequencies change
through time in response to mutation, natural and
cultural selection, and drift (genetic inheritance); and
meme frequencies change through time in response
to innovation, natural and cultural selection, learning, and drift (cultural inheritance; Fig. 3.1.3. At any
point in time, human culture is composed of memes
that reflect genetic, individually learned, and socially
0001215609.INDD 144
transmitted information (Boxes in Fig. 3.1.4; Laland
et al. 2000). We follow the more mechanistic definition of culture—variation acquired and maintained
by indirect and direct social learning (Boyd &
Richerson 1985).
Humans are potent agents of natural selection
affecting the microevolution of organisms and
modifying the configuration and functioning of the
physical environment (Fig. 3.1.4). Environmental
responses to these effects can force cultural and
natural selection on humans, affecting an individual’s inclusive fitness and the cultural fitness of their
memes, as originally postulated by gene-culture
and niche construction theory. Niche construction
theory recognizes that the environment changes in
response to human natural and cultural selection so
that humans ‘inherit’ a change in ecology as well as
a change in gene and meme frequency (Laland et al.
2000). This ‘ecological inheritance’ is not only the
physical and ecological change wrought by people,
but also the cultural change in response to human
activity by animals capable of social learning. Many
animals, especially social, long-lived, and intelligent ones, acquire information through social learning and develop traditions that meet the
social-learning based definition of culture (Avital &
Jablonka 2000). Where human activity results in differential cultural fitness of another animal’s memes
(Fig. 1.3.3; cultural selection from humans to the
environment) and the resulting cultural evolution
in the animal affects the cultural fitness of human
memes (cultural selection from the environment to
humans), then human and animal memes may
become coevolved. This cultural coevolution is
analogous to traditional genetic coevolution where
reciprocal natural selection between organisms
drives mutual change in genes.
Corvids, a common component of urban bird
communities throughout the world, provide many
examples of cultural coevolution with people
(Marzluff & Angell 2005a). Interacting with people
favours cultural adjustment by corvids because
human attitudes and important resources regularly
and rapidly change. Three aspects of human culture
appear especially important to corvid culture: persecution, provision of new food, and creation of
new opportunities. The power of persecution is evident in the nest defense culture of crows and ravens
9/29/2010 6:43:24 PM
OUP UNCORRECTED PROOF – FIRST PROOF, 09/29/10, SPi
COUPLED RELATIONSHIPS BETWEEN HUMANS AND OTHER ORGANISMS IN URBAN AREAS
Humans
145
Environment
Natural selection
Cultural selection
Genes
Genes
Culture
Culture
Development
& learning
Development
& learning
Time
Cultural selection
Cultural
inheritance
Genetic
inheritance
Genes
Culture
Development
& learning
Genetic
coevolution
Genetic
inheritance
Natural selection
Genes
Cultural
inheritance
Ecological
inheritance
Culture
Development
& learning
Cultural
coevolution
Figure 3.1.3 Integration and expansion of gene-culture coevolution and niche construction models to illustrate genetic and cultural coevolution
between two interacting species (here humans and another social animal in their environment, after Laland et al. 2000). The collection of
phenotypes within a population (boxes) emerge as a joint product of genetic, individually-acquired, and socially learned (culture) information.
Populations evolve as genetic and learned information is transferred through time by genetic and cultural inheritance. As people interact with their
environment they cause changes in other organisms’ inclusive fitness (natural selection) or the cultural fitness of their memes (cultural selection).
Reciprocal changes in humans caused by organisms in their environment can lead to coevolved genes (—) or cultures (…). Redrawn from Marzluff
and Angell (2005b)
alluded to earlier. American Crows (Corvus brachyrhynchos) and Common Ravens (Corvus corax) in the
western USA aggressively defend their nests in cities and towns where shooting is outlawed and in
general where persecution is frowned upon, but
quietly retreat out of gun range in rural areas where
an aggressive bird would be wounded or killed
(Knight 1984, Knight et al. 1987). We do not know if
these cultural changes in crows and ravens affect
human culture, but annoyance with aggressive city
crows is common and responded to with control
efforts in some cities (e.g. Lancaster, Pennsylvania,
USA) which may diminish future aggressive tendencies of city crows. In other settings, people bond
0001215609.INDD 145
with crows almost as closely as they bond with their
pets, feeding them daily. This favours tameness and
solicitation by crows that recognize the individuals
who provide for them (Marzluff et al. in review).
The response of crows to people, be it aggressive or
solicitous, has stimulated a radiation of popular
culture from the naming of sports teams and rock
bands to the myriad trappings and tales traditional
in American Halloween celebrations.
The cultural responses of people to nature often
depend on the frequency and effect of the interaction. This may be an important factor in the likelihood of coevolution. When birds like corvids are
rare, people often ignore or revere them, but once
9/29/2010 6:43:25 PM
OUP UNCORRECTED PROOF – FIRST PROOF, 09/29/10, SPi
146
URBAN ECOLOGY
Urban environment
Exotic and subsidized predators and competitors, human persecution, novel plant communities,
anthropogenic subsidies, noise, altered disturbance pegimes, changed of biogeochemical cycles,
movement barriers, new land cover and land use dynamics, altered climate, pollutants, toxins
Mutation
Selection
Genetic
variation
Population
size
Population
isolation
Gene-culture
coevolution
Genetic
assimilation
Behavioral
innovation
Gene
flow
Drift
Phenotypic
plasticity
Heritability
Stochasticity
Learning
Social learning
Genetic and
cultural change
nt
me
on
vir
En
Extinction
Ne
l
Microevolution
Micro-to
macroevolution
Genetic
variation
consistent with
designation of
urban races,
subspecies,
species, and
higher taxa
Local
adaptation
Figure 3.1.4 Key processes and interactions of contemporary evolution in urban ecosystems. Many novel and challenging aspects of urban
environments affect phenotypic and genotypic variability (coloured circle) of an urban animal population, but they do so in two fundamental ways:
as agents of natural selection and as mutagenic toxins and pollutants. Genotypes (lighter portion of circle) and phenotypes (darker portion of
circle) interact in complex ways within and between generations to determine phenotypic variation that is exposed to selection. Responses of a
population to selection may be mediated by small population size (drift) and gene flow but genetic traits are inherited and cultural traits are
passed on by social learning to change the genetic and cultural composition of future generations. This change, or evolutionary adjustment to the
environment, interacts with environmental and demographic stochasticity (triangle) in such a way that small populations are at risk of extinction as
they are adapting to the novel urban environment. Larger or rapidly growing populations are at less risk of stochastic extinction and evolve local
adaptations that may be deemed sufficient to warrant taxonomic designations of urban populations as races, subspecies, or full species. Redrawn
from Marzluff (in press)
they become competitors they are viewed as pests
and despised, harassed, and perhaps controlled.
Our interaction with urban nature thus has a built
in negative feedback mechanism that favours
novel cultures in people and birds as the frequency
and type of their interaction changes. When fewer
in numbers and less a rival for resources, ravens,
for example, were birds of the gods, even gods
themselves, and useful guardians, navigators for
0001215609.INDD 146
mortals, and efficient sanitation engineers. When
their abundance was thought to reduce valuable
game or their consumption of human flesh evoked
horror, guns and control policies were used to
reduce their numbers and change their culture.
Persecuted ravens became rare and shy around
people. This contemporary rareness brought mystery, wonder, and concern from enough people
that a culture of restoration developed (Glandt
9/29/2010 6:43:25 PM
OUP UNCORRECTED PROOF – FIRST PROOF, 09/29/10, SPi
COUPLED RELATIONSHIPS BETWEEN HUMANS AND OTHER ORGANISMS IN URBAN AREAS
2003). Understanding our role in such cyclical
cultural phenomena may be important to conservation and restoration efforts in urban settings.
3.1.6 Conclusions
Most efforts in urban ecology are independent
investigations of either how humans degrade nature
or, to a lesser extent, how nature affects humans. As
when studying any ecosystem, a fuller understanding of urban ecology can be gained by explicitly
studying the degree to which humans and nature
are linked in reciprocal feedback loops, what we
0001215609.INDD 147
147
refer to as coupled systems. In the case of understanding the roles of animals in urban ecosystems,
we not only need to interest ourselves in the biology
of non-human animals, but the effects of human
behaviour on these other species and the consequences of such interactions on people. Therefore,
we might find that incorporating sociological data
provides insight into the adaptability of wildlife to
urban areas. Indeed, as urbanization increases
worldwide, future wildlife conservation efforts will
increasingly broaden from focusing on natural areas
to working to conserve ecological processes and
species in cities (e.g. Dunn et al. 2006).
9/29/2010 6:43:25 PM