Changing climate and the altitudinal range of avian malaria in the Hawaiian Islands – an ongoing conservation crisis on the island of Kaua'i

Abstract

Transmission of avian malaria in the Hawaiian Islands varies across altitudinal gradients and is greatest at elevations below 1500 m where both temperature and moisture are favorable for the sole mosquito vector, Culex quinquefasciatus, and extrinsic sporogonic development of the parasite, Plasmodium relictum. Potential consequences of global warming on this system have been recognized for over a decade with concerns that increases in mean temperatures could lead to expansion of malaria into habitats where cool temperatures currently limit transmission to highly susceptible endemic forest birds. Recent declines in two endangered species on the island of Kaua'i, the 'Akikiki (Oreomystis bairdi) and 'Akeke'e (Loxops caeruleirostris), and retreat of more common native honeycreepers to the last remaining high elevation habitat on the Alaka'i Plateau suggest that predicted changes in disease transmission may be occurring. We compared prevalence of malarial infections in forest birds that were sampled at three locations on the Plateau during 1994-1997 and again during 2007-2013, and also evaluated changes in the occurrence of mosquito larvae in available aquatic habitats during the same time periods. Prevalence of infection increased significantly at the lower (1100 m, 10.3% to 28.2%), middle (1250 m, 8.4% to 12.2%), and upper ends of the Plateau (1350 m, 2.0% to 19.3%). A concurrent increase in detections of Culex larvae in aquatic habitats associated with stream margins indicates that populations of the vector are also increasing. These increases are at least in part due to local transmission because overall prevalence in Kaua'i 'Elepaio (Chasiempis sclateri), a sedentary native species, has increased from 17.2% to 27.0%. Increasing mean air temperatures, declining precipitation, and changes in streamflow that have taken place over the past 20 years are creating environmental conditions throughout major portions of the Alaka'i Plateau that support increased transmission of avian malaria.

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

“…We note that our malaria fatality and non-malaria survival estimates were influenced by prior experimental data or constrained to correspond with previous results, respectively. However, we found lower malaria fatality for low-elevation Amakihi (3% vs. 17%; Atkinson et al 2014), but similar fatality for Iiwi (93% vs. 95%) compared to previous laboratory experiments (Atkinson et al 1995). A surprising pattern in our results was the apparent higher level of malaria infection and/or malaria fatality we found in young birds.…”

“…Increasing temperatures may eliminate high-elevation refugia that currently protect many Hawaiian bird populations, and increase malaria transmission and epizootics in midelevation forests . There is recent evidence this may already be taking place on Kaua'i (Atkinson et al 2014). This combination of factors will likely produce further reductions and extinctions of native Hawaiian birds, particularly for threatened species with small, fragmented populations in high-elevation forests and for species with high susceptibility to malaria such as the Iiwi.…”

“…In Hawaii, the spatial gradient in selection pressure has apparently produced two opposing outcomes-local adaptation of low-elevation Amakihi for malaria-tolerance (Woodworth et al 2005, Foster et al 2007, Atkinson et al 2013 or local extinction of highly susceptible species like Iiwi from low and mid-elevation forests (van Riper et al 1986). As climate warms and malaria infection risk increases in Hawai'i (Benning et al 2002, Atkinson and LaPointe 2009b, Atkinson et al 2014 it is uncertain whether other endemic v www.esajournals.org honeycreepers will be able to evolve tolerance to malaria. Further research is needed to determine the suite of biotic and abiotic factors that facilitate the coexistence of pathogens and hosts (via either resistance or tolerance) and how these factors interact with host demography and movement across a landscape of heterogeneous selection pressures.…”

Collapsing avian community on a Hawaiian island

“…The Hawaiian archipelago is already experiencing a warming trend ( 8 ), especially at higher elevations, which were historically disease-free ( 9 ). A recent study of avian malaria prevalence in upper-elevation forests on the Alaka‘i Plateau of Kaua‘i documented a sharp increase in disease prevalence over a 15-year period, with surveys in 2007–2013 indicating a more than doubling of disease prevalence from the 1994–1997 levels ( 10 ). Prevalence of malarial infections was highest in the lower elevations of the plateau and decreased upslope.…”

Assessing the potential of translocating vulnerable forest birds by searching for novel and enduring climatic ranges

“…Parallel to these climatic trends, recent research has documented substantial range contractions of all native forest birds on Kaua'i over the last four decades, with species losing 25%–70% of their range (Paxton et al., 2016). Given that both temperature and precipitation delineate the distribution of the mosquito vector of avian malaria and consequently the disease‐susceptible native forest birds (Ahumada, LaPointe, & Samuel, 2004; Benning et al., 2002; Liao et al., 2015), future changes in these environmental variables will likely further impact Hawaiian forest birds (Atkinson et al., 2014). In fact, extensive modeling efforts using downscaled end‐of‐century climate projections estimate a range loss of 50%–100% for most Hawaiian forest birds in the absence of effective vector control or increased disease resistance (Fortini et al., 2015).…”