URBANIZATION AND VECTOR-BORNE DISEASE IN MIGRATORY AND NOMADIC WILDLIFE

Abstract

Vector-borne diseases (VBDs) represented 30% of all emerging infectious diseases at the start of the century (Jones et al. 2008) and pose a devastating global health burden, causing an estimated one million deaths every year. Arthropod vectors and the pathogens they carry are highly sensitive to changes in their environment, and VBD infection dynamics are therefore expected to respond strongly to ongoing anthropogenic impacts on climate and the landscape. Anthropogenic land-use change, such as urbanization, is the most frequently cited influence on the emergence of zoonotic VBDs. Intensifying anthropogenic land-use can increase VBD prevalence by altering the composition of host and vector communities and by exposing hosts to features of urban landscapes that can interact with immunity, such as immunotoxic pollutants and sources of anthropogenic provisioning. Because infection dynamics of VBDs are intricately linked to vector distributions and environmental conditions, they are uniquely difficult to predict in wildlife taxa that undergo periodic long-distance movements to track seasonal fluctuations in resources. For example, migratory wildlife may be exposed to variable levels of vector activity and urban land-use throughout the distinct breeding, overwintering, and stop-over sites used throughout their annual cycle. In addition, the physiological demands of migration are a source of intrinsic stressors that could interact with extrinsic anthropogenic stressors to shape seasonal infection outcomes. Studying the intersection between animal migration, anthropogenic land-use, and infectious disease is impactful both for the conservation of vulnerable migratory populations and to predict how pathogens might be dispersed to human and wildlife communities across their large geographic range. For example, migratory birds can facilitate the long-distance dispersal of ticks vectoring Lyme borreliosis, and mediate the spread and enzootic maintenance of West Nile virus after its introduction to the Western Hemisphere. In this dissertation, I take three distinct but complementary approaches to evaluating how anthropogenic land-use interacts with seasonal wildlife movement to produce vector-borne infection outcomes across ecological and evolutionary scales. Chapter 1 centers on Australian black flying foxes (Pteropus alecto), a nomadic nectarivore with winter foraging movements that bring it into increasing contact with anthropogenically modified landscapes and human populations when natural food sources are scarce. Our molecular and phylogenetic work identifies overwintering black flying foxes as hosts of a newly described bacterial VBD closely related to zoonotic Borrelia lineages (e.g., the causative agents of Lyme disease in humans), suggesting this species and its ectoparasites warrant further study as potential sources of zoonotic VBDs at the human–wildlife interface in Australia. In Chapter 2, I focus on temperate migratory songbirds to study how land-use intensity and proximity to spring migration could jointly affect VBDs (haemosporidian parasites and West Nile virus) in New World sparrows wintering in central Oklahoma. I did not find evidence of enzootic West Nile virus activity in overwintering sparrows across 4 sampling years, but both land-use and seasonality predicted birds’ infection with haemosporidian parasites. Wintering in urban or suburban habitats overall reduced the probability birds would be infected with any haemosporidian parasite relative to wintering in more natural habitats. I also report evidence that the stationary non-breeding season is a period of active transmission for at least one group of haemosporidian parasites, challenging the paradigm that acute haemosporidian infections do not impact temperate migratory bird populations outside the breeding season. In Chapter 3, I evaluate the possibility of migration and urban tolerance as host traits that impact patterns of diversification by host-switching in avian haemosporidia by exposing birds to more heterogeneous habitats and their parasite communities over evolutionary time. I found that while urban tolerance did not affect co-evolutionary relationships between hosts and parasites, bird species undergoing long-distance migration had haemosporidian associations that contributed less to global cophylogenetic congruence, suggesting migration drives host-switching events in a common VBD.