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.

Bioenergetic and ecological consequences of diet variability in Atlantic croaker Micropogonias undulatus

Atlantic croaker Micropogonias undulatus is a commercially and ecologically important bottom-associated fish that occurs in marine and estuarine systems from Cape Cod, MA to Mexico. I documented the temporal and spatial variability in the diet of Atlantic croaker in Chesapeake Bay and found that in the summer fish, particularly bay anchovies Anchoa mitchilli, make up at least 20% of the diet of croaker by weight. The use of a pelagic food source seems unusual for a bottom-associated fish such as croaker, but appears to be a crepuscular feeding habit that has not been previously detected. Thus, I investigated the bioenergetic consequences of secondary piscivory to the distribution of croaker, to the condition of individuals within the population and to the ecosystem. Generalized additive models revealed that the biomass of anchovy explained some of the variability in croaker occurrence and abundance in Chesapeake Bay. However, physical factors, specifically temperature, salinity, and seasonal dynamics were stronger determinants of croaker distribution than potential prey availability. To better understand the bioenergetic consequences of diet variability at the individual level, I tested the hypothesis that croaker feeding on anchovies would be in better condition than those feeding on polychaetes using a variety of condition measures that operate on multiple time scales, including RNA:DNA, Fulton's condition factor (K), relative weight (Wr), energy density, hepatosomatic index (HSI), and gonadosomatic index (GSI). Of these condition measures, several morphometric measures were significantly positively correlated with each other and with the percentage (by weight) of anchovy in croaker diets, suggesting that the type of prey eaten is important in improving the overall condition of individual croaker. To estimate the bioenergetic consequences of diet variability on growth and consumption in croaker, I developed and validated a bioenergetic model for Atlantic croaker in the laboratory. The application of this model suggested that croaker could be an important competitor with weakfish and striped bass for food resources during the spring and summer when population abundances of these three fishes are high in Chesapeake Bay. Even though anchovies made up a relatively small portion of croaker diet and only at certain times of the year, croaker consumed more anchovy at the population level than striped bass in all simulated years and nearly as much anchovy as weakfish. This indicates that weak trophic interactions between species are important in understanding ecosystem processes and should be considered in ecosystem-based management.