Host population persistence in the face of introduced vector-borne diseases: Hawaii amakihi and avian malaria

Abstract

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...

Prevalence and Distribution of Pox-Like Lesions, Avian Malaria, and Mosquito Vectors in Kīpahulu Valley, Haleakalā National Park, Hawai‘i, Usa

“…In this case, such habitat is associated with rock holes along stream margins. In support of this hypothesis and in contrast to other areas in Hawai'i where malarial prevalence is higher (Atkinson et al, 2005), we found no significant interaction between elevation and host status (native or nonnative species) and no significant association between elevation and malarial infection. Our sampling was conducted during an abnormally dry fall, and during this 5-mo study, we experienced only one episode of torrential rain with flash flooding that would have scoured stream margins.…”

“…We found a low prevalence of both poxlike lesions and malarial infections in Kīpahulu Valley relative to other locations in Hawai'i where comparable methodologies have been used (Atkinson et al, 2005). This suggests that these two introduced diseases are not well established in this area.…”

“…In Hawai'i, vector populations and transmission rates become more seasonal as altitude increases; declining temperatures limit larval development and place thermal constraints on development of malarial parasites within adult mosquitoes (LaPointe, 2000;Benning et al, 2002). These conditions generally lead to declines in prevalence and transmission of these diseases as elevation increases (van Riper et al, 1986(van Riper et al, , 2002Atkinson et al, 2005). Culex quinquefasciatus populations typically peak in late summer and early fall in the Hawaiian Islands, and we timed our fieldwork so that it encompassed the presumed peak time for disease transmission on Haleakalā Volcano (van Riper et al, 1986;LaPointe, 2000).…”

“…One hundred 5003 fields were examined on each slide, which was equivalent to a search effort of approximately 30,000 erythrocytes per smear. Plasma samples were screened by immunoblotting (Atkinson et al, 2001a(Atkinson et al, , 2005 to detect antibodies to P. relictum. We used both microscopy and results from immunoblotting to establish infection status for each individual.…”

“…Active pox-like lesions were identified by presence of swellings or crusty scabs. Inactive pox-like lesions were identified by presence of missing toes that were otherwise healed (van Riper et al, 2002;Atkinson et al, 2005).…”