Abstract
A key question in evolutionary behavioural ecology is how species cope with changes in their environments. In the last centuries, humans have caused dramatic changes in our planet that have affected the way many animals behave. In order to live in cities, most animals are forced to adjust their behaviour and life histories to the new urban habitat. While growing evidence reports behavioural differences between rural and urban conspecifics as common and cross-taxonomical, the mechanisms underlying such differences in behaviour remain largely unknown. Recent research using animals with limited experience of their natural urban or rural environments points to the existence of intrinsic differences in behaviour between rural and urban conspecifics. This suggests that phenotypic plasticity might not be the only mechanism explaining behavioural differences between rural and urban individuals and that differences in individually consistent behavioural traits could also be the result of microevolution in the urban environment.
Knowing that urbanization is and will continue to be a major environmental challenge to most living organisms, it is urgent to understand the mechanisms allowing animals to cope with our urbanizing world. In this chapter, I focus on the existence of different behavioural phenotypes between rural and urban animals and on the possible mechanisms leading to such behavioural differences.
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Keywords
- Animal personalities
- Anthropogenic environmental change
- Behavioural syndromes
- Colonization
- Microevolution
- Phenotypic plasticity
- Urbanization
1 Introduction
According to the United Nations (2014), two and a half billion people inhabited our planet in 1950. Remarkably, in 2011, little more than 60 years later, that number had almost tripled to seven billion people, and an impressive increase to over nine billion inhabitants is expected by 2050. Along with the world’s extreme human population growth, the last few decades have witnessed an unprecedented increase in the number and size of cities. While in the 1950s 30 % of the human population lived in urban areas, that number suffered a drastic growth to 54 % in 2014 and is estimated to further increase to 66 % by 2050 (United Nations 2014).
In the last decades, the significant development of urban ecology as a scientific discipline reflects the now widely accepted fact that the phenomenon of urbanization has a profound impact on ecological systems, being a major threat to many species (Shochat et al. 2006; Gaston 2010).
In their natural habitats, animals are continuously facing environmental challenges, as coping with disturbances, adjusting to shifts in food availability and distribution and interacting and competing with other animals. The manner in which an individual animal responds to such challenges can greatly affect its future chances of survival and reproduction. Over the last centuries, urbanization arose as a new major environmental challenge that may favour individuals consistently behaving in different ways. The colonization of an urban habitat often requires organisms to adapt, among other factors, to increased disturbance levels, shifts in food resources, new species composition, a different microclimate and increased chemical, light and noise pollution (Klausnitzer 1989; Partecke et al. 2006; Brearley et al. 2012; Lowry et al. 2013; Dominoni 2016; Kekkonen 2016). Typically, the changes caused by urbanization occur in a quick and dramatic manner, being thus expectable that many organisms should be unable to cope with these changes, causing their potential exclusion from urban environments (Hendry et al. 2008; Sih et al. 2011). Accordingly, it is well documented that urbanization leads to a drastic loss in species diversity (Shochat et al. 2010; Daniels and Kirkpatrick 2016). On the other hand, it has been argued that urban environments may offer important benefits for certain species, such as warmer temperatures (Arnfield 2003), nocturnally illuminated foraging areas (Lourenço et al. 2008; Santos et al. 2010) and anthropogenic food (Bateman and Fleming 2012; Gleditsch 2016). Supporting this idea, numerous species seem to prosper in urban environments (Case 1996), being therefore crucial to understand how animals cope with urbanization and which are the consequences of living in the new urban habitats. Evidence suggests that, in many species, urban populations differ in several aspects, including timing of reproduction (see Chamberlain et al. 2009 for a literature review), daily activity patterns (Dominoni et al. 2013), stress physiology (Partecke et al. 2006; Fokidis et al. 2009) and even rates of cellular ageing.
Remarkably, urban animals also frequently change the way they behave, and this is the focus of this chapter. In the next sections, I will begin by reviewing the studies documenting shifts in behaviour between rural and urban conspecifics. Next, I will focus on the possible ultimate causes that might lead to such behavioural differences between rural and urban animals, namely, phenotypic plasticity or microevolution in the urban environment. I include some considerations about physiology as a possible proximate cause of shifts in behaviour in urban species. Finally, I will discuss some possible impacts of the observed shifts in behaviour in urban species.
2 Urbanization-Driven Shifts in Behavioural Traits: The Nature of Urban Behaviour
An individual’s behavioural phenotype is a set of elements that is crucial for coping with environmental challenges such as urbanization and that might be related with major life history decisions, as whether to colonize new habitats or not and their consequences. Urbanization is a relatively new and strong selection pressure challenging organismal adaptation capabilities. The environmental challenges driven by urbanization can result in various phenotypic shifts, including shifts in behaviour (Sol et al. 2013; Partecke 2013). Indeed, an increasing body of evidence shows that rural and urban conspecifics commonly differ in many behavioural traits (but see literature review in Table 7.1). In specific, a study has assessed how common are shifts in animal behaviour related to the urbanization phenomenon, by reviewing empirical studies comparing rural and urban conspecifics in different behaviours towards stimuli (Miranda et al. 2013). Here, over 2 years later, using the methodology in the aforementioned study (Miranda et al. 2013), I conducted an identical literature search with the objective of finding studies comparing rural and urban populations in the following behaviours: aggression (attacks or other aggressive interactions or displays), alarm (alarm calls in response to disturbing stimuli), escape (retreat behaviours when facing disturbing or threatening stimuli), exploration (exploration of new environments), innovation (ability to solve problems, usually associated with a food reward), neophilia (attraction to novelty), neophobia (novelty avoidance) and risk-taking (exposure to risk). The literature search was performed in ISI Web of Knowledge (http://www.isiknowledge.com) in April 2015, with the following exact search terms: Topic = (Aggression OR Alarm OR Anti-predator OR Behavioural-syndrome OR Bold OR Defense OR Escape OR Exploration OR Fear OR Flight-initiation-distance OR Flush OR Innovation OR Neophilia OR Neophobia OR Novel OR Personality OR Risk-taking OR Shy OR Temperament) AND Topic = (Urbani* OR (Urban NEAR/1 Rural) a OR “Exposure to Humans”) AND Topic = (Behaviour) AND Topic = (Animal OR Species). From the retrieved results, I selected all relevant articles in English from appropriate research areas, as well as articles resulting from backward or forward searches of the original search. Statistically significant differences (P < 0.05) were classified into ‘rural > urban’ or ‘rural < urban’ depending on the direction of the trend. In articles focusing on multiple species or related behaviours, I considered significant differences when these were shown in at least one species and behaviour in the same category. For clarity, only studies that focused both on rural and urban populations of the same species, excluding studies focusing on gradients of urbanization, or disturbance in only rural or urban environments. Nonetheless, the concept of rural and urban certainly differs in many of the retrieved studies regarding characteristics of the habitat and degree of anthropogenic disturbance.
The literature review reinforces the idea that only individuals able to behaviourally cope with the new urban selection pressures can be successful in urban habitats. However, with the few number of studies available for each species, we can only speculate about the specific behavioural traits that could benefit a specific city dweller. Most likely, there are various ways for an animal to be successful in an urban habitat, and the optimal behavioural strategies might also vary according to different stages of colonization (for a review on the theme, see Sol et al. 2013) or to the characteristics of each urban habitat. It should be noted that not all urban species are urban colonizers in the true sense of the word; instead, for many populations, their natural habitats are ‘colonized’ by urban settings. Birds seem to be an ideal taxa to study the urbanization-related shifts in behavioural traits, with two thirds of the studies from our literature review focusing on this group (Fig. 7.1).
The literature review retrieved 36 empirical studies comparing rural and urban conspecifics in aggressive, alarm, escape, neophilic, neophobic, innovative and risk-taking behaviours towards different types of stimuli (Table 7.1). Most of the studies were made in the wild, with only nine studies made under controlled laboratory conditions and only two of these studies using individuals with limited experience of their natural rural or urban environment (Atwell et al. (2012) made a common garden experiment using birds caught as juveniles; Miranda et al. (2013) made a common garden experiment using birds caught as nestlings). Of the 36 studies, 33 showed significant differences between rural and urban populations for at least one of the behaviours and species analysed. Urban populations seemed to be more aggressive (5 of 6 studies in the wild) and showed reduced escape behaviour (24 of 26 studies), having mixed results regarding risk-taking behaviour (6 of 11 studies found that urban populations incurred in higher risk-taking behaviours). For the other considered behaviours, 9 of 12 studies showed differences between rural and urban conspecific populations. Repeatability was only assessed in five studies, in which four found the behaviours under study to be repeatable. Eleven studies assessed correlations between different behaviours, finding that most of the behaviours were correlated.
Although it is now unquestionable that the conquest of urban habitats by animals is linked to intraspecific behavioural shifts, the underlying mechanisms of this changes remain unclear. Are behavioural changes in urban animals due to phenotypic plasticity or to microevolution? Although behavioural plasticity is likely to play an important role in helping animals to cope with the urban environment, recent studies suggest that behavioural differences between rural and urban individuals might be intrinsic, potentially resulting from divergent selection pressures on rural and urban populations (Atwell et al. 2012; Carrete and Tella 2013; Miranda et al. 2013). Next, I will focus on the two possible responsible mechanisms for behavioural shifts in urban animals, behavioural plasticity and microevolution of behavioural traits.
It should be noted that, while throughout this chapter I portray behavioural plasticity and microevolution of behavioural traits separately for the sake of simplicity, I believe that in most cases both mechanisms contribute in some extent to the behaviour observed in urban animals.
3 Behavioural Plasticity in Urban Environments
Phenotypic plasticity is a common phenomenon in nature that can be defined as the capacity of an individual with a particular genotype to alter its phenotype under certain environmental conditions (Thibert-Plante and Hendry 2011). Phenotypic plasticity is the primary mechanism enabling individual organisms to adjust their morphology OR physiology OR behavior OR phenology to better suit changes in their environmental conditions, thereby potentially increasing fitness (Thibert-Plante and Hendry 2011; Van Buskirk 2012).
Behaviour, which consists of a motoric response to a sensorial input, is an essential function for animals to interact with their surrounding environment. Being able to adjust behaviour in response to environmental changes can have important life history consequences for an organism. It is generally assumed that behavioural plasticity plays a critical role for the success of city dwellers, as it enables organisms to more efficiently and rapidly deal with the different challenges of the novel urban environment, as finding new resources and effectively using them and coping with unfamiliar and potentially dangerous animals, objects or situations (Sol et al. 2013; Lowry et al. 2013). Under rapid environmental changes as urbanization, behavioural plasticity can be advantageous over evolutionary changes because it can emerge immediately in response to a new environment. It has been suggested that organisms lacking phenotypic plasticity might be naturally excluded from altered environments (Badyaev 2005).
Although having flexibility in behaviour might be advantageous in specific circumstances, it involves an investment of time and energy, implying important costs that might ultimately have a negative effect on reproduction and survival (Sol et al. 2013). Another potentially negative side effect is that behavioural plasticity, by uncoupling the genotype from the phenotype, might decrease the efficacy of evolutionary responses to selection (Van Buskirk 2012). It is important to note, however, that behavioural plasticity is not independent of the mechanisms involving evolution and adaptation: plasticity can evolve in response to changes in the environment if selection acts on reaction norms or if the trait means are correlated with plasticity (Van Buskirk 2012).
4 Microevolution of Behaviour in Urban Environments
In many species, certain individuals exhibit behavioural traits that might make them inherently well suited to occupy urban environments. Behaviours that are consistent across time and contexts for one individual (personality traits) might indeed provide important advantages for invading new environments. Animal personalities are taxonomically widespread, being documented in over 100 species (Wolf et al. 2008). In the last years, a number of studies revealed the variation in (van Oers et al. 2004; Schielzeth et al. 2011).
Despite the generalized evidence showing behavioural differences between urban and rural conspecifics, the vast majority of studies so far were not able to disentangle microevolution from behavioural plasticity (Table 7.1). Nevertheless, two recent common garden experiments conducted with urban and rural conspecific bird populations indicate that consistent behavioural traits differ intrinsically between rural and urban individuals (Atwell et al. 2012; Miranda et al. 2013). These differences are likely the result of microevolutionary changes, although the experimental setups could not fully exclude early developmental influences.
The idea of a genetic basis for behavioural shifts in urban individuals is further supported by a recent comparative study that assessed candidate genes for behavioural traits on several rural and urban blackbird populations across Europe (Mueller et al. 2013). In the above-mentioned study, a candidate gene for harm avoidance behaviour (the SERT gene) exhibited a significant association with habitat type.
Two different evolutionary processes could be responsible for heritable differences in personality traits between rural and urban conspecifics (Miranda et al. 2013): (1) microevolution in personality traits as an adaptation to new urban selective pressures that shift the behavioural optima (post-colonization adaptation) or (2) microevolution of personality traits via non-random gene flow, through a personality-dependent colonization of the urban habitat (pre-colonization adaptation, Edelaar and Bolnick 2012). The two processes might occur concurrently and potentially under distinct selection pressures indifferent stages of colonization (Martin and Fitzgerald 2005).
5 Differences in Physiology as Potential Precursors of Differences in Urban Behaviour
The endocrine system is an essential causal mechanism behind animal behaviour. To understand how hormones might shape behaviours under different selection pressures, it is essential to investigate the covariation between hormonal and phenotypic traits and how those could relate to fitness. It has been suggested that differences in suites of behaviours might be influenced by modifications of the two main endocrine axes, the hypothalamic-pituitary-adrenal axis (HPA axis, related with the production of corticosteroid hormones) and the hypothalamic-pituitary-gonadal axis (HPG axis, related with the production of estrogens or androgens) (van Oers et al. 2011). Understanding if and how the endocrine system relates to differences in behaviours between rural and urban conspecifics should be a crucial focus of research in behavioural urban ecology.
In recent years, several studies have focused on differences between rural and urban conspecifics on hormones associated with the hypothalamic-pituitary-adrenal axis (HPA), such as corticosterone, which might improve the chances of survival under adverse environmental conditions. Studies with captive bird populations suggest the existence of an intrinsically reduced acute corticosterone stress response in urban animals (Partecke et al. 2006; Atwell et al. 2012). However, field studies on the subject provided less clear results (Schoech et al. 2004; French et al. 2008; Fokidis et al. 2009). One recent common garden experiment with rural and urban dark-eyed juncos (Junco hyemalis) simultaneously assessed differences in behavioural traits and in HPA responsiveness in rural and urban conspecific, concluding that intrinsic differences in exploratory behaviour might be correlated to differences in the corticosterone stress response (Atwell et al. 2012).
The lack of knowledge is even greater when considering hormones associated with the hypothalamic-pituitary-gonadal axis (HPG), such as estrogens or androgens (Buchanan and Partecke 2012). An existing study suggests that, in the wild, male rural blackbirds have higher levels of plasma testosterone and luteinizing hormone than urban males (Partecke et al. 2005). However, virtually no study assesses simultaneously differences in behavioural traits and in HPG responsiveness in rural and urban conspecifics.
Although the existence of correlations between baseline or maximum hormone levels and individual consistent behavioural traits have been suggested, they have rarely been found (Johnsen 1998; McGlothlin et al. 2007; but see Atwell et al. 2012). It is possible that correlations between behavioural and hormonal traits are not stable during the annual cycle but rather transient (reviewed in Adkins-Regan 2005). Moreover, while some studies found differences in hormone concentration between rural and urban animals, there is a lack of comparisons of other factors involved in the HPA and HPG axis. In fact, many of the reported differences in behaviour between rural and urban conspecifics could be related to aspects of the HPA and HPG axis, not only hormone concentration but also to differences in transport proteins, differences in the number or sensitivity of hormone receptors or cofactors or hard-wired (neural) differences that are not under hormonal control. All these aspects should be addressed in future studies.
6 Synthesis and Directions for Future Research
In this chapter, I revised the literature showing that urban animals across many taxa exhibit differences in behaviour when compared to their rural counterparts. I further focused on how behavioural shifts in urban animals can arise from plasticity or from microevolutionary changes and on the possible relations between differences in physiology and in behaviour in urban animals.
On one hand, species in which individuals show high plasticity in behaviour have an inherent capacity to quickly adjust to altered conditions and, in consequence, might be particularly predisposed to occupy urban environments. On the other hand, microevolution of individually consistent behavioural traits (personality traits) as an adaptation to the urban environment could also explain the observed shifts in behavioural traits in urban animals. By allowing populations to flexibly adjust their behaviours to environmental changes, behavioural plasticity can potentially decrease the need for selection to act on behavioural traits (Price et al. 2003). Conversely, it is also possible that the selection of individuals presenting only specific behavioural traits that are beneficial under urban environmental conditions might be associated with a reduction in behavioural plasticity (Martin and Fitzgerald 2005).
Variation in behaviour, either plastic or intrinsic, is an essential aspect that allows species to respond to environmental challenges as urbanization. Individuals from species with a large variation in their behavioural phenotypes are thought to better cope with urbanization when compared to species with narrower ranges of behavioural phenotypes (Sih et al. 2010). To understand the role of evolution versus plasticity in shaping behavioural traits, we would ideally need to separate the genetic and environmental components of the behaviour and to assess its fitness value in urban and rural habitats. Although these data might be difficult to obtain, studies with repeated measures of behavioural elements in which family effects can be estimated could be the foundation for revealing the basis of variation in behaviour. In the future, behavioural ecologists working with urbanization should more thoroughly address behavioural variation within individuals (plasticity), between individuals (personality), within populations and between populations (Araya-Ajoy and Dingemanse 2013; Dingemanse and Dochtermann 2013). By gaining knowledge about the variation in behaviour and the environmental correlates, we will be able to better understand which are the species that will be excluded from urban habitats and which will be the ones successfully colonizing them, maybe even being able to foresee the shifts in behaviour in our ever changing world.
If microevolution acts in the urban environment through selection pressures favouring specific personality traits, the decrease in between-individual variation (or lower heritability) could lead to the reduction in genetic diversity that is commonly observed in anthropogenically impacted animal populations and usually attributed to genetic drift (Carere and Maestripieri 2013). To date, few publications have focused on assessing the effects of urbanization on shaping the strength and direction of behavioural syndromes, but it has been suggested that urbanization might act on behavioural syndromes by changing the correlations between behaviours via correlational selection (Bell and Sih 2007) or directly by disrupting certain behavioural traits (Scales et al. 2011; Bókony et al. 2012; Royauté et al. 2013). Variation in syndrome structures between different populations may reflect adaptation to local environmental conditions (Bell 2005; Dingemanse et al. 2007). However, selection can also act on independent behavioural traits. In either case, proving that these traits are adaptive would require the evaluation of selection gradients, such as estimating the survival of each behavioural type in natural conditions (Bell and Sih 2007; Sweeney et al. 2013).
It is also particularly important to assess the individual consistency of the behavioural phenotypes. In theory, selection should only act on traits where the intra-individual variation is larger than the between-individual variation (Boake 1989). Repeatability of a behavioural trait is the proportion of the variance of the trait that is explained by differences among individuals, and in most cases the repeatability of a behavioural trait sets the upper limit for heritability (Falconer and Mackay 1996). Thus, in general, genetically determined traits on which selection is able to act are repeatable.
The majority of studies in urbanization has been done on temperate northern regions, where the process of urbanization is older and more widespread (Sol et al. 2013). But research is also needed on regions where the urbanization process is still at an early stage.
Currently, we only have rudimentary knowledge about the mechanisms that allow some species to cope with anthropogenic environmental change. Developing a realistic interpretation of the mechanisms behind differences in behaviour in urban animals requires an integrative approach, of behaviour, physiology, ecology, genetics and evolution of urban populations. The answers are likely to be complex, but we will hopefully be able to contribute to unravelling the evolutionary ecological consequences of urbanization.
Although understanding organismic behavioural adaptations to urbanization is a topic of major importance, the most crucial achievement should be changing human behaviour itself. The consequences of human environmental change are so devastating that none of our research efforts will be relevant if humans keep destroying natural habitats and depleting natural resources at the current pace.
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I thank the editors, Enrique Murgui and Marcus Hedblom, for the kind invitation to contribute to this book.
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Miranda, A.C. (2017). Mechanisms of Behavioural Change in Urban Animals: The Role of Microevolution and Phenotypic Plasticity. In: Murgui, E., Hedblom, M. (eds) Ecology and Conservation of Birds in Urban Environments. Springer, Cham. https://doi.org/10.1007/978-3-319-43314-1_7
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