- Dr Giles Johnson
Despite urban expansion causing an overall decrease in the number and variety of animals that inhabit a given area, some vertebrate species have made a success of urban living. Using the red fox, the Norway rat, the rock dove, and the peregrine falcon as case studies, this review analyses the resources and features that allow these animals to thrive in human settlements; and in turn how living in such environments affects them. The literature provides evidence of the ample food that urban centres provide for vertebrates, primarily in the form of waste. In the case of the peregrine falcon, the arrival of the pigeon has provided a source of prey. The living requirements of each species differed due to differences in size, reproductive behaviour and the ability to fly. Living in urban environments has dramatic effects on these species; changes in social behaviour and reproduction contribute to more efficient exploitation of the resources available. We argue that a flexible strategy in terms of behaviour and diet is fundamental to urban success in vertebrates. Knowledge in this area may provide the means to better control populations, curbing the spread of pest species and encouraging desirable species into urban centres.
Despite the homogenising effect of urban expansion on species richness some vertebrates have successfully colonised the urban niche. Using Vulpes vulpes, Rattus norgevicus, Columba livia, and Falco peregrinus as case studies, this review analyses the resources available to these species and in the strategies employed to better exploit them. Urban centres provide ample food for vertebrates primarily in the form of human waste. In the case of F.peregrinus the establishment of colonies of C.livia provides a constant prey source encouraging expansion into urban centres; providing an example of secondary succession. Differences in size and behaviour as well as terrestrial and aerial lifestyles result in different living requirements and thus preference in urban density. Living in urban environments also exerts pressures on these species. Spatio-temporal changes in resources specifically result in changes in social behaviour as well as reproductive behaviour and physiology as an adaptive response. We argue that plasticity in response to diet, behaviour and physiology are fundamental to urban vertebrate success. We suggest further research into whether such responses are genotypic or phenotypic. Better understanding of such phenomena may provide humans with better means to manage urban ecology.
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A 2014 report on urbanisation by the UN found 54% of the global population lived in urban centres at the time, meaning for the first time in human history more people live in urban than rural environments. This figure compares to 30% in 1950 with a projection to reach 66% by 2050. These trends are encouraged by both migration and an expected rise in the population from 7.2 billion to 9.6 billion by 2050 (UN, 2014). Despite urbanisation being attributed to threatening 8% of terrestrial species (Mcdonald et al., 2008) and having a ‘homogenising’ effect on biodiversity (Clergeau et al., 2006), Angold et al. (2006) state that wildlife can indeed prosper in the urban environment. Although, Mckinney et al. (2006) correctly point out that some ‘urban adaptable’ species tend to dominate the urban niche and spread globally resulting in biotic homogenisation. This review is concerned with vertebrate species that dominate the urban environment; assessing both the causes of such success and observing the effects that urban life has upon these species. The introduction will define ‘urbanisation’ and address both the potential negative and positive effects on overall biodiversity and on individual species. The body of this review will use two mammal and two bird species as case studies focusing on food, shelter, group behaviour, and reproduction as indicators of how species exploit the urban niche, and how in turn urban life can cause changes in these species.
Jones and Leather (2012) define an urban area as a human settlement with a population greater than 10,000, characterised by a mosaic of land uses including residential, commercial, industrial and infrastructural with occasional green spaces. Moller et al. (2009) define urbanisation as the ‘conversion of natural habitats into areas partly covered by buildings, heavily fragmented and with a high level of edge effects’. Bateman and Fleming (2012) argue that urbanisation is difficult to define and will not only vary from region to region, but also exists on a scale with cities offering the most extreme of disturbed anthropogenic altered environments, through to towns and villages as well as infrastructure and parkland.
It is often difficult to quantify the direct impact of urbanisation on an ecosystem due to urban centres usually predating modern ecological analysis, but, although caution should be taken with estimation, studies that compare urban systems to undisturbed natural ecosystems can provide some insight. One such study by Brook et al. (2003) assessed the impact that potential habitat loss in Singapore had on local biodiversity since the British colonised the region in 1819. The analysis combined historic documentation on land clearance and development with evidence of recent extinctions in the area. They calculated that 95% of the rainforest habitat had been cleared, estimating that the figure for overall biodiversity loss could be at minimum 28% with a vertebrate extinction rate between 34-43%. They further highlight the ‘bleak’ outlook for wildlife in the region with 77% of local wildlife currently ‘threatened’. A recent study by Newbold et al. (2015) analysed the impact of land use on local biodiversity. The findings suggest that local richness, rarefied richness and abundance decrease as the intensity of human interference and population density increases, attributes all associated with urbanisation. These analyses draw attention to the impact that habitat loss caused through urban development can have on animal biodiversity.
Destruction of habitat can also cause habitat fragmentation; the process of a habitat breaking apart and becoming increasingly isolated (Fahrig, 2003). Haddad et al. (2015) analysed data collected from over 35 years from several biomes globally and various fragment sizes. They found that fragmentation reduced biodiversity by between 13-70% with the effect greatest on the smallest and oldest fragments. The size and scale of this study provides strong evidence for such effects. Fragmentation can also exert genetic effects on a population by creating barriers through which genetic information cannot easily flow (Templeton et al., 1990). The smaller and more genetically isolated these populations are the greater likelihood the population will go extinct (Slatkin, 1977). Behavioural and morphological effects have also been observed in fragmented populations. The work of Hill et al. (1999) on the butterfly Hesperia comma in the South Downs found that individuals residing in more isolated fragments tended to invest in larger flight muscles; a trait associated with increased dispersal distances, whereas individuals in less fragmented habitats tended to invest less in flight muscles and more in larger reproductive organs.
Despite the negative impact on biodiversity there are opportunities in the urban ecosystem for animals that can take advantage. Anthropogenic food sources in the form of refuse (Gardner-Santana et al., 2009), spillage (Murton, 1972), and cultural feeding practices (Doncaster and Macdonald, 1990) all provide ample food supply for urban populations. Although buildings and infrastructure can cause fragmentation and mortality risk (Bateman and Fleming, 2012), the patchwork mosaic of commercial, residential and green spaces provides a variety of potential homes for animals (Angold et al., 2006). Once initial colonisation has taken place, the dramatic reduction in competition and abundance of resources allows a ‘niche shift’, contributing to a rapid establishment (Diamond, 1970). Despite the potential benefits, urban environments are still one of the most challenging for animals to live in due to the high level and wide range of anthropogenic disturbances; mostly in the form of development and traffic (Bateman and Fleming, 2012). This review will make the case that in this shifting environment a high level of behavioural, physiological and morphological plasticity contributes greatly to a species’ success.
The four case studies were selected with three criteria in mind. First a sufficient body of literature to allow for detailed comparison. Second to provide insight into the effects urbanisation has on urban vertebrates. Third species were selected that offer specific challenges to society such as pest or endangeredÂ species. The four vertebrate case studies analysed in this paper are the red fox, Vulpes vulpes; the Norway rat, Rattus norgevicus; the urban pigeon or rock dove, Columba livia; and the peregrine falcon, Falco peregrinus. V.vulpes was selected due to the the well documented comparison between both its urban and rural ecology and behaviour. C.livia is another well studied urban species with a long urban history; originally being kept as a source of protein throughout the middle ages (Murton et al., 1972). The ecology R.norgevicus is less well studied. This is surprising as it isone of the most ecologically destructive vertebrates (Higgins et al., 2015), regarded among the most numerous and pervasive of urban pests (Feng et al., 2012), and known to harbour many zoonotic pathogens (Himsowrth et al., 2013) making it an important topic for study. C.livia also presents similar problems, befouling public spaces through defecation, the fine particles of which are loaded with zoonotic pathogens creating a risk to public health (Hetmanski et al., 2010). F.peregrinus Is a particularly interesting case of an urban success story as they also represent one of the great conservation management success stories of the last century. In the Midwest it now exclusively resides in urban centres where it was extirpated following the population crash during the 50s and 60s (Caballero, 2016).
Understanding what makes these species successful could potentially help with population control of dangerous pest species such as the Norway rat and the pigeon. Understanding the factors that contribute to these species success may also allow us to build environments that encourage desirable animals, such as the peregrine and the fox, as well as creating opportunities for less successful species.This review will analyse the traits that allow successful vertebrates to exploit the anthropogenic resources available, primarily in the form of food and shelter. It will also cover the behavioural and reproductive effects that the urban environment exerts upon these groups.
Contesse et al. (2004) found that 85% of households in Zurich had anthropogenic food accessible to foxes. There is a vast array of literature that supports the claim that V.vulpes exploits such sources. Doncaster and Macdonald (1990) analysed the diet of the fox population in Oxford finding that a majority of 37% of the average annual food intake was scavenged, a result reflected by Contesse et al. (2004) in the city of Zurich where it reached 50%. Interestingly, in both studies this figure fluctuates in response to seasonal variation. Doncaster and Macdonald (1990) found scavenging was highest during the winter when other food sources were lower, and lowest during the late summer/autumn when seasonal fruits were abundant. This flexibility in diet is reflected in studies of V.vulpes in rural environments. One study in southern England found two thirds of the diet comprised of game, withÂ mostly rodents and fruit making up the remainder (Reynolds and Tapper, 1995). Whilst another found that for foxes inhabiting mountainous regions in the Czech Republic rodents made up the majority, supported by varying quantities of beetles, ungulates, plant matter and fruit depending on the season (Hartova-Nentichova et al., 2010). In the urban context Contesse et al. (2004) note that the more extreme urban environments, such as the city centre, were associated with increased levels of dietary scavenge. Baker and Harris (2007) suggest opportunistic feeding a factor in the successful colonisation of the urban niche and these studies support such a claim. Pickett et al. (2001) propose that the increased quantity and continuous source of food in the form of human food waste as well as the cultural practice of feeding urban wildlife has a positive impact on the fox population. Further to this, Contesse et al. (2004) calculated that the surplus of refuse removed food as a limiting factor for the fox population in Zurich which has resulted in a large and increasing population.
Unlike the Zurich fox population food is usually determines carrying capacity for urban rat populations (Higgins et al., 2015). This is possibly due to the varying lengths of time these populations have been established. V.vulpes colonised the UK in the 1930s (Doncaster and Macdonald, 1990) and Zurich in the 1980s (Contesse et al., 2004) whilst the commensal rat population has potentially lived alongside humans for thousands of years (Feng et al, 2014). An opportunistic generalist, R.norgevicus occupies urban centres and feeds primarily on refuse (Gardner-Santana et al, 2009). Schein and Orgain (1953) calculated that one third of anthropogenic refuse is a suitable food source for rats providing a constantly replenishing food source in urban areas. The Norway rat is so well adapted to urban life that it is rarely found in the wild, suggesting they require humans to survive (Feng and Himsworth, 2014). Although dietary flexibility has contributed to the colonisation of the urban niche the suggestion that this species are now completely dependent upon it for survival might imply a lack of flexibility once established.
A comparative study by Murton and Westwood (1966) found the rural population of C.livia nesting on the cliffs at Farnborough head fed on a variety of grains, legumes weed seeds and some small invertebrates; the ratios of which fluctuated in response to the agricultural season. The diet of the population in Leeds consisted primarily of bread but also fruit cake and commercial seed mix provided by the public. However, much of the produce found in the rural population was also present in the urban population. Murton and Westwood (1966) attributed this to the public but a study by Rose et al. (2006) provides further insight. The study analysed the spatio-temporal use of the urban habitat of C.livia in the city of Basel. They found that there were three different foraging strategies employed: 1) in the streets, squares and parks near the home site 2) In agricultural areas surrounding the city 3) on docks and railway lines in the harbour. Most individuals stayed within 0.3km of their nesting site in the city with only 7.5% of the population flying to the agricultural and dock sites which were over 2km away. It was found that these foraging strategies were only employed in conjunction with foraging near the home site suggesting they were secondary strategies when access to local sources was restricted. Evidence that urban pigeons employ a flexible foraging strategy.
Ali et al. (2013) suggests that the worldwide urban pigeon population has boomed due to the continuous supply of anthropogenic food compared to seasonal fluctuations in rural environments. Interestingly, this population boom has potentially aided the colonisation of the urban niche and the recovery of the peregrine falcon. A study by Drewitt and Dixon (2008) analysed the diet of peregrines in three British cities: Bristol, Bath and Exeter. They found that pigeons and other doves comprised 47% of the peregrine diet making up the majority of the peregrine diet; reflecting figures from a study in Warsaw 32% (Rejt, 2001). Both studies observed seasonal fluctuations in the proportion of pigeon taken. Drewitt and Dixon (2008) noted that during the starling breeding season juveniles can make up 19% of the peregrine diet, whilst Rejt (2001) recorded a drop to 10-19% of pigeon in the diet during the migration season and exceeding 50% over the harsher winter months. It is thought that the ‘countershading’ present on migrating birds which is beneficial in natural light is maladaptive in the artificial glare of the city lights allowing the peregrines to take advantage (Ruxton et al., 2004). TheseÂ studies provide evidence for a flexible, opportunistic feeding strategy. Interestingly from an ecological perspective, the urban pigeon forming the base prey for urban peregrines (Cade and Bird, 1990) suggests secondary succession occurring in the urban environment; with the pioneer species C.livia allowing the establishment of F.peregrinus.
These four case studies not only highlight the variety of food sources available to urban species but also provide insight in the type of feeding strategy enables species to exploit this niche. Although diet and preference might vary, a generalist opportunistic approach strategy is favoured, suited to the often constant but highly varied anthropogenic food types available.
Resources: Places to Live
Throughout the year V.vulpes rest in lays, structures that provide the fox with shelter, situationally (Doncaster and Macdonald, 1990). However, during the breeding season red foxes require open ground to construct breeding dens, due to this they prefer less dense residential areas where open ground provides suitable sites (Doncaster and Macdonald, 1990). In comparison the requirements of R.norgevicus are minimal, being smaller in size and less particular in regards to breeding sites. All that is needed is adequate harborage and a nearby food source, typically refuse (Gardner et al., 1948). Rats will burrow in soil, use abandoned structures, and even climb buildings and make nests from anthropogenic materials (Gardner et al., 1948). As a result rats thrive in run down neighbourhoods where there are more abandoned and neglected properties that provide harbourage (Himsworth et al., 2013). Although these two species require both refuge and food, differences in size and breeding behaviour results in different requirements. As a consequence the fox faces greater restriction.
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Although birds face similar problems the spatial differences in habitat mean birds are less affected by fragmentation (Fahrig, 2003). A study by Ali et al., (2013) on the ecology of C.livia in Islamabad found pigeons to be present on bridges, tall buildings, as well as in semi urban spaces such as parks and gardens. Interestingly, population density increased around urban centres and decreased around semi-urban spaces showing a clear bias to extreme urban environments. The human environment also provides suitable nesting sites for F.peregrinus, with urban peregrines roosting on the tallest buildings in an urban space (Cade and Bird, 1990). It could be suggested that tall man-made structures such as skyscrapers mimic the cliff side habitat of these species allowing successful colonisation to occur.
Effects: Range and Group Behaviour
The urban environment is characterised by high level of disturbance. Construction, demolition and changes in human population all contribute to fluctuations in the spatial distribution of resources (Doncaster and Macdonald, 1990). In response to this we see high levels of plasticity in fox social behaviour (Doncaster and Macdonald, 1991; Baker et al., 1998). The home range of urban foxes is dramatically reduced usually extending for less than 100ha (Doncaster and Macdonald, 1991), whilst in rural individuals it can exceed 2000ha (Contesse et al., 2004). This is associated with increased resources over a smaller area which also results in increased population density (Doncaster and Macdonald, 1991). Interestingly, this has implications for the social behaviour of urban foxes. Red foxes are usually solitary animals that form pairs during the breeding season, but in urban settings live in groups of three to five (Doncaster and Macdonald, 1991). This is best explained by the spatio-temporal variation in the availability of resources in the anthropogenic environment which impacts both individual benefit and defence costs potentially leading to group formation (Doncaster and Macdonald, (1991); Baker et al., (1998). The spatial distribution of resources in towns and cities is such that with only two members the perimeter cannot be fully defended whilst the amount of resources within a territory are often abundant enough to promote group formation (Donacaster and Macdonald, 1991). These changes in social structure show high levels of behavioural plasticity which has potentially aided the expansion of the red fox into the urban niche.
There are interesting parallels to draw between urban rat and fox populations, particularly in relation to range and social behaviour. The home range of urban rats is typically small; consisting of narrow strips between the animals harbourage and its food supply (Davis, 1953). Gardner-Santana et al. (2009) proposed that the range of urban rats is much smaller in urban environments, ranging from 25-150m (Davis, 1953), compared to those of rats in rural environments, which range from 260-2000m (Taylor and Quy, 1978). Feng et al. (2014) suggest that range is dependent on the availability of suitable harborage and food sources as well as pressure from conspecifics. This is comparable to the reduction in fox range which was attributed to a high density of anthropogenic resources in the urban environment. Like the red fox, urban rats also exist in larger colonies than their rural counterparts although, unlike foxes, they lack co-operative behaviour (Feng et al., 2014). In fact, the increased population density and fierce competition often results in increased levels of aggression (Feng et al., 2014).
There is also evidence that spatio-temporal distribution of resources affects group size and behaviour in C.livia. Murton et al. (1972) noted that the flock size of C.livia was directly related to the quantity of daily food spillage, unlike in the closely related wood pigeon, C.palambus, where seasonal food supply dictates flock size. Murton also observed that pigeonsociety exists in hierarchical structure with some birds occupying the centre of the flock and having preferential access to the best feeding spots. Despite differences in social structure, the changes in range and group living in the fox, rat and pigeon offer insight into the effects that urban living can exert upon the behaviour of species. It could be suggested that the plastic nature of these behaviours has contributed to the success of these animals in the urban niche. Questioning whether such effects stem from the environment working on established plasticity within the genotype or whether such changes are the result of natural selection would provide an interesting topic for further study.
Effects: Reproduction and Population
Due to their high fecundity, even in urban environments with an abundant resources, food usually determines the carrying capacity of the urban rat population. A sexually mature female can produce five litters per year with 4-8 pups per litter (Margulis, 1977). The work of Ziporyn and McClintock (1991) noted that females living in groups often establish oestrus in synchrony, observing that when this occurred 80% of pups would survive compared to asynchronous breeders. These co-ordinated events result in population booms (ibid) which maintains the numerous population. Glass and Herbert (1988) also noted that urban rats grow faster and reach sexual maturity sooner than their rural counterparts, suggesting the abundance of anthropogenic resources as a cause. Understanding when these ‘booms’ occur could help humans better control urban rat populations.
The effect of increased resources on rats draws parallels with the population dynamics of C.livia. Hetmanski et al. (2010) found that the size of a pigeon population in an urban environment was linked not only to the size of the urban environment but also with the density of the human population, suggesting a correlation with increased anthropogenic resources. Murton et al. (1972) noted that due to the copious food supply there is little migration resulting in nest sites remaining occupied all year and rarely becoming available. This change in behaviour meant that two thirds of the pigeon population failed to breed potentially decreasing the effective population size. Further to this, there is evidence that males carry an allele that lengthens the breeding season and increases fertility (Murton et al., 1973) suggesting there is a selective advantage for remaining sexually active for longer.
Changes in reproductive strategy in urban F.peregrinus have been attributed to the speed of its recovery since the population crash in the 50s/60s. A study by Kauffman et al. (2003) compared the survival rate of rural and urban peregrines in California. During the first year it was found that urban young had a 65% chance of survival compared to 28% in rural individuals. Caballero et al. (2016) also found that the urban clutch size tends to be larger, with an average clutch size reaching 4-5 in urban environments compared to 3 in rural. This effect has resulted in a population boom with populations in the UK and Germany already exceeding pre-crash levels (Rejt, 2001) Although the mechanisms differ, there is a clear pattern for increased fecundity in urban populations of these species contributing to their success.
The case studies discussed provide evidence of the opportunities available to vertebrates with the means to take advantage of them. Despite different needs, the human habitat offers ample shelter for vertebrates, with rats and foxes occupying spaces determined by their size and behaviour whilst man-made structures mimicking the natural habitat of peregrines and pigeons offer nesting sites. Anthropogenic waste and cultural practice supplies foxes, rats and pigeons with an abundant food supply that, although fluctuates spatio-temporally in relation to human rhythms, does not suffer the same seasonal fluctuations which characterise the rural environment. This combines with the opportunistic generalist nature that characterises these species allowing them to take advantage of such resources.
Consequentially, there are marked changes in behaviour with determined by the change in urban resource distribution. This has resulted in increased group size and co-operation in V.vulpes; alteration in flock size relating to daily opposed to seasonal resource fluctuations in C.livia; and larger more aggressive colonies of R.norgevicus. Peregrines also benefit from a constant food supply in the form of the anthopogenically supported pigeon population; an example of secondary succession of the urban environment. They exhibit opportunistic behaviour in both the species they hunt and their potential use of skyscrapers as hunting aids. The argument for a degree of behavioural plasticity allowing these species to take better advantage of such resources is well supported but questions are still to be answered on whether such changes are a result of natural selection or are phenotypic responses to changes in environment.
Similar questions also arise when considering the effects the urban environment has on reproduction. Although the mechanisms differ, we see a pattern of increased fecundity across the case studies. Increase in fledgeling success in F.peregrinus is easily explained by ecological factors, but the change in peregrine clutch size and the increased growth and approach to sexual maturity in R.norgevicus are less easily determined. The identification of an allele in C.livia that extends the breeding season suggests a genetic cause in this instance. However, each case should be considered independently and these situations open up a multitude of questions in relation to whether cases of behavioural and physiological plasticity is related to the genotype or phenotype of an organism.
There are surprising gaps in the literature and areas that appear to be poorly replicated. Reviews on urban rats comment on the lack of ecological understanding of R.norgevicus. From a utilitarian perspective this is counterintuitive considering the risk it poses ecologically, economically, and to public health. Conversely, the literature on urban foxes is both extensive and varied, perhaps denoting the popularity of this animal in the public mind. From a practical perspective this information is perhaps less useful although the cultural impact of urban wildlife should not be dismissed or undervalued. The projected increase of urbanisation highlights the importance of understanding both the traits of successful species and qualities of the environment that encourage vertebrate success. Such information can provide us with the means to better manage urban populations. In regards to pest species this could aid efforts to control and minimise their success, whilst better planning could attract not only current successful species but also edge species into the urban environment.
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