Avian malaria in Hawaiian forest birds: infection and population impacts across species and elevations

Abstract

Abstract. Wildlife diseases can present significant threats to ecological systems and biological diversity, as well as domestic animal and human health. However, determining the dynamics of wildlife diseases and understanding the impact on host populations is a significant challenge. In Hawai'i, there is ample circumstantial evidence that introduced avian malaria (Plasmodium relictum) has played an important role in the decline and extinction of many native forest birds. However, few studies have attempted to estimate disease transmission and mortality, survival, and individual species impacts in this distinctive ecosystem. We combined multi-state capture-recapture (longitudinal) models with cumulative age-prevalence (crosssectional) models to evaluate these patterns in Apapane, Hawai'i Amakihi, and Iiwi in low-, mid-, and high-elevation forests on the island of Hawai'i based on four longitudinal studies of 3-7 years in length. We found species-specific patterns of malaria prevalence, transmission, and mortality rates that varied among elevations, likely in response to ecological factors that drive mosquito abundance. Malaria infection was highest at low elevations, moderate at mid elevations, and limited in high-elevation forests. Infection rates were highest for Iiwi and Apapane, likely contributing to the absence of these species in low-elevation forests. Adult malaria fatality rates were highest for Iiwi, intermediate for Amakihi at mid and high elevations, and lower for Apapane; low-elevation Amakihi had the lowest malaria fatality, providing strong evidence of malaria tolerance in this low-elevation population. Our study indicates that hatch-year birds may have greater malaria infection and/or fatality rates than adults. Our study also found that mosquitoes prefer feeding on Amakihi rather than Apapane, but Apapane are likely a more important reservoir for malaria transmission to mosquitoes. Our approach, based on host abundance and infection rates, may be an effective alternative to mosquito blood meal analysis for determining vector-host contacts when mosquito densities are low and collection of blood-fed mosquitoes is impractical. Our study supports the hypothesis that avian malaria has been a primary factor influencing the elevational distribution and abundance of these three species, and likely limits other native Hawaiian species that are susceptible to malaria.

Mitigating Future Avian Malaria Threats to Hawaiian Forest Birds from Climate Change

“…Malaria-tolerant Amakihi are the primary native honeycreeper able to thrive in lowland forests with high transmission of avian malaria [26,28–29]. Although Apapane are also found in lowland forests their abundance is limited.…”

“…In our simulations these subpopulations were allowed to grow and/or decline independently based on elevation-specific malaria transmission rates (selection pressure) and their simulated degree of malaria-tolerance. Malaria fatality rates for susceptible Amakihi (68%), Apapane (47%), and Iiwi (93%) were estimated from capture-recapture data for wild birds across high and mid elevations [26]. For malaria-tolerant Amakihi, we used a malaria fatality rate of 2.5% based on estimates for low-elevation Amakihi [26].…”

“…Malaria fatality rates for susceptible Amakihi (68%), Apapane (47%), and Iiwi (93%) were estimated from capture-recapture data for wild birds across high and mid elevations [26]. For malaria-tolerant Amakihi, we used a malaria fatality rate of 2.5% based on estimates for low-elevation Amakihi [26]. Without evidence for malaria tolerance in Apapane or Iiwi, we simulated three different levels of reduction (25%, 50%, and 75%) in malaria mortality.…”

“…In mid-elevation forests, seasonal transmission becomes longer and more intense for all three climatic projections, and may lead to mid-elevation extinction for disease susceptible Iiwi populations, which have already been decimated by malaria. In contrast to mid and high elevations, lowland forests have high malaria transmission because this is a highly favorable environment for mosquitoes and malaria transmission [14,26–27]. Therefore, predicted future climate changes will have only limited additional impacts on malaria transmission at low elevation.…”

“…Therefore, predicted future climate changes will have only limited additional impacts on malaria transmission at low elevation. Recent studies have demonstrated that only the Hawai’i Amakihi ( Chlorodrepanis virens ) has been able to evolve malaria tolerance and re-populate low-elevation forests in the face of high malaria transmission [21,26,28–30]; providing limited optimism that evolution of malaria tolerance may also allow other native Hawaiian birds to avoid extinction.…”