Emerging Infectious Disease: Host and Parasite Perspectives

Avian malaria and related haematozoa are nearly ubiquitous parasites that can impose fitness costs of variable severity and may, in some cases, cause substantial mortality in their host populations. One example of the latter, the emergence of avian malaria in the endemic avifauna of Hawaii, has become a model for understanding the consequences of human-mediated disease introduction. The drastic declines of native Hawaiian birds due to avian malaria provided the impetus for examining more closely several aspects of host-parasite interactions in this system. Host-specificity is an important character determining the extent to which a parasite may emerge. Traditional parasite classification, however, has used host information as a character in taxonomical identification, potentially obscuring the true host range of many parasites. To improve upon previous methods, I first developed molecular tools to identify parasites infecting a particular host. I then used these molecular techniques to characterize host-specificity of parasites in the genera Plasmodium and Haemoproteus. I show that parasites in the genus Plasmodium exhibit low specificity and are therefore most likely to emerge in new hosts in the future. Subsequently, I characterized the global distribution of the single lineage of P. relictum that has emerged in Hawaii. I demonstrate that this parasite has a broad host distribution worldwide, that it is likely of Old World origin and that it has been introduced to numerous islands around the world, where it may have been overlooked as a cause of decline in native birds. I also demonstrate that morphological classification of P. relictum does not capture differences among groups of parasites that appear to be reproductively isolated based on molecular evidence. Finally, I examined whether reduced immunological capacity, which has been proposed to explain the susceptibility of Hawaiian endemics, is a general feature of an "island syndrome" in isolated avifauna of the remote Pacific. I show that, over multiple time scales, changes in immune response are not uniform and that observed changes probably reflect differences in genetic diversity, parasite exposure and life history that are unique to each species.

Bat-plant pollination interactions in southern Thailand

The overwhelming majority of flowering plant species depend on animals for pollination, and such pollinators are important for the reproductive success of many economically and environmentally important plant species. Yet pollinators in the Old World tropics are relatively understudied, particularly paleotropical nectarivorous bats (Pteropodidae), and much is unknown about their interactions with night-blooming plant species. To better understand these bat-plant pollination interactions, I conducted fieldwork in southern Thailand for a total of 20 months, spread across three years. I examined the foraging times of pteropodid bat species (Chapter 1), and found that strictly nectarivorous species foraged earlier, and for a shorter duration, than primarily frugivorous species. I also studied year-long foraging patterns of pteropodid bats to determine how different species track floral resources across seasons (Chapter 2). Larger species capable of flying long distances switched diets seasonally to forage on the most abundant floral species, while smaller species foraged throughout the year on nearby plant species that were low-rewarding but highly reliable. To determine which pteropodid species are potentially important pollinators, I quantified the frequency and effectiveness of their visits to six common bat-pollinated plant taxa for an entire year (Chapter 3). The three strictly nectarivorous species were responsible for almost all pollination, but pollinator importance of each bat species varied across plant species. I further examined the long-term reliability of these pollinators (Chapter 4), and found that pollinator importance values were consistent across the three study years. Lastly, I explored mechanisms that reduce interspecific pollen transfer among bat-pollinated plants, despite having shared pollinators. Using a flight cage experiment, I demonstrated that these plant species deposit pollen on different areas of the bat’s body (mechanical partitioning), resulting in greater pollen transfer between conspecific flowers than heterospecific flowers (Chapter 5). Additionally, while I observed ecological and phenological overlap among flowering plant species, pollinators exhibited high floral constancy within a night, resulting in strong ethological separation (Chapter 6). Collectively, these findings illustrate the importance of understudied Old World bat pollinators within a mixed agricultural-forest system, and their strong, interdependent interactions with bat-pollinated plant species within a night, across seasons, and across years.