Effects of urbanization on animal behaviour : patterns, underlying mechanisms and ultimate causes

Human-altered environmental conditions affect many species at the global scale. An extreme form of anthropogenic alteration is the existence and rapid increase of urban areas. A key question is how animals cope with urbanization. In order to live in cities, animals have to adjust their behaviour and life histories to the urban novel environment.The main objectives of this thesis were to investigate (i) the existence of behavioural changes related to the urbanization process, (ii) the ultimate mechanisms leading to urbanization-related changes in behaviour, (iii) the physiological mechanisms underlying differences in behaviour between rural and urban conspecifics and (iv), the heritability and correlated evolution of behavioural traits in rural and urban individuals.Chapter 2 focused on the effects of urbanization on song behaviour. In urban areas, noise pollution interferes with animals’ vocal interactions by limiting the detection of acoustic signals. Recent studies show that urban birds sing at higher-frequencies than their rural conspecifics. Although this has been considered a strategy to avoid masking by traffic noise, this idea is debated, as singing louder (with higher amplitudes) should be more efficient than singing at higher frequencies. We tested this hypothesis in the European blackbird (Turdus merula), a successful urban colonizer, for which it was suggested that urban birds sing with higher-frequency elements. Our results confirmed that urban individuals preferentially sang higher-frequency elements. We found out that these elements could only be produced at higher amplitudes, which are less masked in traffic noise. Our results suggest that singing with high-frequency elements, traditionally pointed as an adaptive strategy to avoid masking by urban noise, might in fact be a consequence of singing louder. This chapter allowed new insights into the questions of why birds sing at higher frequencies in cities.In Chapter 3, I investigated the existence of differences in behavioural reactions to novelty between rural and urban conspecifics, and whether such differences are the result of phenotypic plasticity or of intrinsic differences. In a literature review, I showed that behavioural differences between rural and urban conspecifics are common and taxonomically widespread among animals, suggesting a significant ecological impact of urbanization on animal behaviour. In order to gain insight into the mechanisms leading to behavioural differences in urban individuals, we hand-raised and kept blackbird nestlings from a rural and a nearby urban area under common-garden conditions. Using these birds, we investigated individual variation in two behavioural responses to the presence of novel objects: approach to an object in a familiar area (here defined as neophilia), and avoidance of an object in a familiar foraging context (defined as neophobia). Neophilic and neophobic behaviours were mildly correlated and repeatable even across a time period of one year, indicating stable individual behavioural strategies. Blackbirds from the urban population were more neophobic and seasonally less neophilic than blackbirds from the nearby rural area. These intrinsic differences in personality traits are, thus, likely the result of microevolutionary changes, although we cannot fully exclude early developmental influences.In the initial chapters of this thesis we showed that urban and rural conspecifics commonly differ in behavioural traits. But the physiological mechanisms behind such differences in behaviour are largely unknown. In Chapter 4, I investigated whether testosterone is a factor underlying changes in agonistic behaviour of urban animals. Using the previously described common-garden setup with hand-raised rural and urban blackbirds, we investigated aggression behaviour and associated hormonal traits in three trials of a simulated territorial intrusion (STI) experiment. In this experiment, for each individual, we introduced a blackbird decoy of the same sex in the individual home cage. Rural individuals were more aggressive than their urban counterparts towards the decoy. Aggression to the decoy showed long-term individual consistency and differences in means between the rural and the urban population. For both sexes, aggression was seasonally related to baseline plasma testosterone, but androgen levels did not differ between rural and urban individuals. Testosterone did not increase following the STI, but the results of a challenge with gonadotropin-releasing hormone (GnRH) suggest that most individuals would have had the physiological capacity to increase testosterone. Our results suggest that, although endogenous testosterone seems to be seasonally related to aggressive behaviour in both sexes, there should be other factors explaining differences in agonistic behaviour between rural and urban conspecifics.In Chapter 5, I investigated the quantitative genetics of personality traits in rural and urban European blackbirds. The data from previous chapters suggest that individually consistent differences in behaviour between rural and urban conspecifics might be due to microevolution rather than phenotypic plasticity. If indeed pre- or post-colonization selective pressures favour different behaviours in urban colonizers than those present in the wild original environments, it should be expected that the behaviour is not only repeatable, but also heritable. Another key aspect is whether behavioural elements evolve alone or as part of a suite of behaviours, and whether these behavioural suites might differ between rural and urban populations. Using our hand-raised European blackbirds from a rural and an urban population, we investigated repeatability and broad-sense heritability of behavioural elements and the existence of a behavioural syndrome integrating the studied behaviours. Although we cannot exclude maternal or early environmental effects, our results with the hand-raised blackbirds suggest that neophobia, neophilia, aggression, and latency to enter a novel environment are highly repeatable, and possibly heritable. Finally, we did not find evidence of correlated evolution regarding the studied behaviours. In this chapter we provide quantitative Information on the genetic architecture of specific behavioural traits that will facilitate future research on the evolutionary consequences of urbanization