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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