Impact of landscape anthropization on pathogen transmission dynamics and wild birds health

The intensification of agriculture, animal husbandry and the expansion of cities, has led to changes in environmental conditions, reduced biodiversity and altered interactions between organisms affecting many ecological processes, involving pathogen transmission. In addition, detrimental effects of habitat anthropization on the life history of many species of birds have been reported, including in some species apparently thriving in urban areas. Urbanization affects not only the life history, abundance, and composition of vertebrate communities, but also those of hematophagous insects living in these areas and, consequently, the vector-borne pathogens they transmit. Urbanization can alter the incidence and distribution of vector-borne parasites, as well as the susceptibility of vertebrates to infectious diseases through its effects on host immunocompetence. In this thesis, I used a multidisciplinary approach to determine how the dynamics of vector-borne parasites are affected by habitat anthropization, and how the joint effects of anthropization and parasite infections impact the health of wild birds. For this purpose, I focussed on the widespread vector-borne parasites of the genus Plasmodium, commonly known as avian malaria parasites, and the related genera Haemoproteus and Leucocytozoon, which were molecularly identified. In addition, I used the house sparrow (Passer domesticus), one of the best examples of urban exploiter historically associated with human settlements, as the avian study model species. Since the 1970s, this bird species has been suffering a dramatic decline across Europe, especially in cities, with human activities and infectious diseases being identified as the main factors. Using an extensive dataset of birds sampled at localities in southern Spain, I first determined how vector-borne parasites dynamics are affected by habitat anthropization (Section 1). To do that, I compared the variation in the prevalence and richness of the three genera of blood parasites over two years in 15 wild house sparrow populations that included urban, rural, and natural habitats (Ch. 1). The prevalence of both Haemoproteus and Leucocytozoon parasites differed and were correlated between years, while no significant differences were found for Plasmodium parasites. Variation in the environmental requirements between vector groups, habitat characteristics and climatic variability strongly determined the stability and activity of vector populations, potentially affecting bird exposure and thus prevalence in the population. Both Haemoproteus and Leucocytozoon richness also varied with habitat and time. Variation in the composition of vector and/or bird communities may affect the number and identity of parasite lineages circulating and infecting house sparrows, but host-related factors and susceptibility may also explain the infection patterns found. Secondly, I determined the impact of both anthropization and parasite infections on the health of wild house sparrows (Section 2). In the three chapters included in this section, I measured three major variables reflecting the health of birds, namely body condition (Ch. 2), the composition of plasma fatty acids (Ch. 3)and the oxidative status (Ch. 4) in relation to Plasmodium, Haemoproteus andLeucocytozoon infection status and including house sparrow populations from urban, rural and natural habitats. Results show that urbanization increased the levels of fatty acids and oxidative damage to lipids and negatively affected bird body condition which, in turn, influenced the activity of antioxidant enzymes. Among other possibilities, this could be due to the low availability of good quality food in urban habitats that prevent birds to fulfil physiological requirements during development resulting in lower body condition, immunocompetence and antioxidant capacity. Moreover, Plasmodium infected juvenile house sparrows had lower proportion of ω-6 and higher proportion of ω-3 PUFAs, as well as lower activity of antioxidant enzymes (GPx, SOD and GR). These results may reflect that, due to the low antioxidant activity of infected birds, only birds with moderate levels of pro-inflammatory fatty acids against parasite infection were likely to survive. Additionally, results from this thesis show that birds exposed to two different sources of stress, namely urbanization and parasite infection, may suffer greater deleterious effects. Birds from natural habitats infected by Plasmodium
showed lower ω-6/ω-3 ratio and tended to have a higher proportion of ω-3. It is likely that, due to differential availability of ω-3 PUFA between habitats, only infected house sparrows from natural habitats can promote a greater anti-inflammatory immune response to Plasmodium infections because the consumption of food rich in ω-3 PUFA. Moreover, higher body condition of juvenile house sparrows was associated with infections by Plasmodium and Haemoproteus, especially in urban habitats. This result may be explained by a higher mortality rate of infected birds with worst body condition unable to respond to infection, consequently, infected individuals surviving to infection were in a higher body condition than uninfected ones. To sum up, in this thesis I provide novel information on the dynamics of vector-borne parasites in anthropized ecosystems and the joint negative effects of urbanization and parasite infections on wild birds. I highlight the importance of also including habitats with different landscape uses, such as rural habitats, in the studies of urbanization impact, where the effect of human activities and domestic animals on wildlife may differ from cities. Moreover, pollutants levels, availability of green spaces or the stability of resources may widely differ among cities, which may determine the final effects on wildlife health and the interpretation that researchers can make of the impact of urbanization. This work contributes to the growing area of Urban Ecology and may help to better understand the effects that both urbanization and pathogens have on the ecology and evolution of wildlife under the current scenario of global change