Avian malaria is a worldwide mosquito-borne disease caused by Plasmodium parasites. These parasites occur in many avian species but primarily affect passerine birds that have not evolved with the parasite. Host pathogenicity, fitness, and population impacts are poorly understood. In contrast to continental species, introduced avian malaria poses a substantial threat to naive birds on Hawaii, the Galapagos, and other archipelagoes. In Hawaii, transmission is maintained by susceptible native birds, competence and abundance of mosquitoes, and a disease reservoir of chronically infected native birds. Although vector habitat and avian communities determine the geographic distribution of disease, climate drives transmission patterns ranging from continuous high infection in warm lowland forests, seasonal infection in midelevation forests, and disease-free refugia in cool high-elevation forests. Global warming is expected to increase the occurrence, distribution, and intensity of avian malaria across this elevational gradient and threaten high-elevation refugia, which is the key to survival of many susceptible Hawaiian birds. Increased temperatures may have already increased global avian malaria prevalence and contributed to an emergence of disease in New Zealand.
More than half of the Hawaiian honeycreepers (Drepanidinae) known from historical records are now extinct. Introduced mosquito-borne disease, in particular the avian malaria Plasmodium relictum , has been incriminated as a leading cause of extinction during the 20th century and a major limiting factor in the recovery of remaining species populations. Today, most native Hawaiian bird species reach their highest densities and diversity in high elevation (>1,800 m above sea level) forests. We determined the thermal requirements for sporogonic development of P. relictum in the natural vector, Culex quinquefasciatus , and assessed the current distribution of native bird species in light of this information. Sporogonic development was completed at constant laboratory and mean field temperatures between 30 and 17 C, but development, prevalence, and intensity decreased significantly below 21 C. Using a degree-day (DD) model, we estimated a minimum threshold temperature of 12.97 C and a thermal requirement of 86.2 DD as necessary to complete development. Predicted (adiabatic lapse-rate) and observed summer threshold isotherm (13 C) correspond to the elevation of high forest refuges on the islands of Maui and Hawai'i. Our data support the hypothesis that avian malaria currently restricts the altitudinal distribution of Hawaiian honeycreeper populations and provide an ecological explanation for the absence of disease at high elevation.
The past quarter century has seen an unprecedented increase in the number of new and emerging infectious diseases throughout the world, with serious implications for human and wildlife populations. We examined host persistence in the face of introduced vector-borne diseases in Hawaii, where introduced avian malaria and introduced vectors have had a negative impact on most populations of Hawaiian forest birds for nearly a century. We studied birds, parasites, and vectors in nine study areas from 0 to 1,800 m on Mauna Loa Volcano, Hawaii from January to October, 2002. Contrary to predictions of prior work, we found that Hawaii amakihi (Hemignathus virens), a native species susceptible to malaria, comprised from 24.5% to 51.9% of the avian community at three low-elevation forests (55-270 m). Amakihi were more abundant at low elevations than at disease-free high elevations, and were resident and breeding there. Infection rates were 24 -40% by microscopy and 55-83% by serology, with most infected individuals experiencing low-intensity, chronic infections. Mosquito trapping and diagnostics provided strong evidence for yearround local transmission. Moreover, we present evidence that Hawaii amakihi have increased in low elevation habitats on southeastern Hawaii Island over the past decade. The recent emergent phenomenon of recovering amakihi populations at low elevations, despite extremely high prevalence of avian malaria, suggests that ecological or evolutionary processes acting on hosts or parasites have allowed this species to recolonize low-elevation habitats. A better understanding of the mechanisms allowing coexistence of hosts and parasites may ultimately lead to tools for mitigating disease impacts on wildlife and human populations.Hemignathus virens ͉ host-parasite coevolution ͉ Plasmodium relictum ͉ Culex quinquefasciatus T he past quarter century has seen an unprecedented increase in the number of new and emerging infectious diseases throughout the world, with serious implications for human and wildlife populations (1). This rise in the emergence of new infectious diseases is attributed to many factors, among them human alteration of habitats, transportation of vectors and pathogens, and climate and weather patterns, including anthropogenic climate change (2, 3). Vector-borne diseases in particular may undergo geographic range shifts and large changes in abundance with climate change because rising temperatures will affect vector distribution, parasite development, and transmission rates (4).Identifying the factors that allow for coexistence of hosts and parasites has been a topic of intensive study in the ecological literature for decades (5, 6). Modeling and empirical studies have identified host and vector abundance, vector competence and behavior, host community, spatial and metapopulation dynamics, host demography, seasonality, parasite virulence, and host resistance, among others, as being of importance (7,8). A better understanding of the mechanisms of host-parasite coexistence may ultimately lead to t...
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