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Local Prevalence and Transmission of Avian Malaria in the Alakai Plateau of Kauai, Hawaii, U.S.A

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Local Prevalence and Transmission of Avian Malaria in the Alakai Plateau of Kauai, Hawaii, U.S.A Vol. 40, no. 2 Journal of Vector Ecology 221 Local prevalence and transmission of avian malaria in the Alakai Plateau of Kauai, Hawaii, U.S.A. Anouk Glad1* and Lisa H. Crampton2 1University of Hawai`i at Manoa, Department of Botany, Kaua`i Forest Bird Recovery Project, Hanapepe, HI 96716, U.S.A., [email protected] 2State of Hawai`i, Department of Land and Natural Resources, Kaua`i Forest Bird Recovery Project, Hanapepe, HI 96716, U.S.A. Received 27 October 2014; Accepted 11 March 2015 ABSTRACT: Avian malaria is among the most important threats to native Hawaiian forest birds. It is caused by the parasite Plasmodium relictum and is transmitted by the introduced mosquito vector Culex quinquefasciatus. Temperature increases and precipitation declines due to climate change over the last decade may be responsible for the observed recent expansion in the range and prevalence of avian malaria on the Alakai Plateau, Kauai Island. To examine the hypothesis that conditions are now favorable for transmission of malaria on the Plateau, mosquitoes were sampled with CO2 and Reiter oviposition traps at three sites (Kawaikoi, Halepa’akai, and Koke’e) on several occasions between October, 2013 and April, 2014. P. relictum infection was assessed by PCR or dissection under a microscope. We also surveyed mosquito larvae along Halepa’akai and Kawaikoi streams. We observed that Cx. quinquefasciatus is well established on the Alakai Plateau, as mosquitoes were caught on all field trips, except in April at Halepa’akai, and larvae were found throughout the year. We observed differences in adult abundance among sites and microhabitats (stream vs ridge lines). Journal of Vector Ecology 40 (2): 221-229. 2015. Keyword Index: Climate change, mosquito-borne disease, stream flow, honeycreeper. INTRODUCTION larval development and reduce adult survival (Farajollahi et al. 2011). Indeed, cold temperatures reduced female survival Introduced diseases, such as avian malaria, are among to two to six weeks at a constant temperature of 5° C (Almirón the major threats to bird populations in the United States, and Brewer 1996). The incubation period is between three to after habitat fragmentation and introduction of predators five days, and larval development between 10 to 12 days with a (Gurevitch and Padilla 2004). Hawaiian native birds suffer developmental threshold of 9.5°-10.4° C, but low temperature greatly from these threats (Wilcove et al. 1998) and are one increased both incubation and development to up to 28 of most endangered wildlife groups in the United States days at 17° C (Almirón and Brewer 1996, Rueda et al. 1990). (Leonard and David 2008). The isolation of the Hawaiian This species is known to exist in various habitats: canals, Islands led to a unique evolution and speciation of the marshes, ornamental ponds, swimming pools, temporary avifauna, which flourished in a predator and disease-free pools, puddles, or ditches (Muturi et al. 2008, Manimegalai environment until human colonization of the islands 1,800 and Sukanya 2014). On Hawaii Island, it is principally found years ago (Atkinson et al. 2013). During their evolution, in anthropogenic larval habitats when available. On Hawaii many native Hawaiian forest birds lost or failed to develop Island, Maui, and Kauai, larvae were observed in rock pools resistance to mosquito-borne diseases and now are highly in the bed of stream drainages and stream margins. However, sensitive to the recently introduced avian malaria. This is larvae were also found in fern tree cavities and ground pools manifested by a very high mortality for some native species, (created by feral game) on Hawaii Island (Reiter and LaPointe 90% for the I’iwi (Vestiaria coccinea) or 75% for the Maui 2009, Aruch et al. 2007, Atkinson et al. 2014). ‘alauahio (Paroreomyza montana) after exposure to a single Across the archipelago, many native bird populations infected mosquito (Atkinson 2005). The species causing avian have declined dramatically and have almost disappeared from malaria on the Hawaiian archipelago is Plasmodium relictum, lower and mid-elevations as a result of malaria (Atkinson transmitted mostly by the mosquito Culex quinquefasciatus. 2005, Reynolds et al. 2003). Above 1,500 m, ambient Other common mosquitoes, including Aedes albopictus and temperature historically has been sufficiently cool at any time Wyeomyia mitchelli, are refractory to infection (LaPointe et of year to prevent mosquito and P. relictum development, al. 2005, Atkinson et al. 2008). which are both temperature-dependent (Benning et al. 2002). Culex quinquefasciatus is a nocturnal, widely distributed Thus, malaria is less prevalent and some native forest birds mosquito that has been established in the Hawaiian species that disappeared from low and mid-elevation are archipelago since 1826 (LaPointe et al. 2009). Females occur still present in high elevation forests (Atkinson and LaPointe in warm and temperate areas, feed mostly on birds, and do 2009). However, recent findings suggest that temperature not hibernate. Thus,Cx. quinquefasciatus continue to feed and increases at high elevations throughout Hawaii may promote reproduce in winter, even if the low temperatures slow down increased prevalence of avian malaria and more drastic forest 222 Journal of Vector Ecology December 2015 bird declines (Benning et al. 2002, Atkinson and LaPointe temperature and lower rainfall frequency) occurred from 2009). July to September. Temperature increases and precipitation On Kauai, the Alakai Plateau historically has been a declines due to climate change over the last decade may have refuge for forest birds due to the low prevalence of malaria, extended the favorable period for P. relictum transmission by even though the Plateau lies only between 1,100 and 1,569 allowing mosquitoes to better hatch and survive throughout m. The particular climate occurring on the Alakai Plateau the year, and P. relictum to complete its life cycle, in high may prevent a high transmission rate of P. relictum (LaPointe altitude areas on Kauai (Atkinson et al. 2014). This possibility et al. 2010). The Alakai Plateau constitutes the entire is one focus of this study. In addition, climate change may remaining range of three endangered endemics species: have allowed mosquitoes from lower altitudes to migrate to Akikiki (Oreomystis bairdi), Akeke’e (Loxops caeruleirostris) upper elevations throughout the year and to survive longer and Puaiohi (Myadestes palmeri) (Reed et al. 2012). The on the Plateau, increasing the transmission of P. relictum to three other endemic species on Kauai island (Kauai Amakihi forest birds. (Hemignathus kauaiensis), Kauai Elepaio (Chasiempis We hypothesized that current conditions on the Alakai sclateri), and Anianiau (Magumma parva)), and two widely Plateau may allow mosquitoes to complete their life cycles distributed species across the Hawaiian archipelago (Apapane on the Plateau even in the cooler winter and spring months (Himatione sanguine) and I’iwi (Vestiaria coccinea)), are also because climate change favors both mosquito and larval found only on the Alakai Plateau. At least five of these species survival and development. The varied topography of the Alakai were formerly widespread on Kauai Island (Kauai Amakihi, Plateau offers diverse microhabitats (lower elevation streams, Kauai Elepaio, Anianiau, Puaiohi, and Apapane) (Burney et higher elevation ridgelines) and altitude and precipitation al. 2001). Since 1973, some species, such as I’iwi, Akeke’e, decrease from east to west (Giambelluca et al. 2013). Thus, we and Akikiki, have exhibited alarming range contractions and hypothesized that mosquito and malaria prevalence is more population declines on Kauai, which are thought to be related likely to occur at Koke’e and Kawaikoi than Halepa’akai, since to increased prevalence of malaria, among other threats the latter site is located at a higher altitude and experiences a (Atkinson et al. 2014, Foster et al. 2004). This hypothesis is higher rainfall average and fewer anthropogenic disturbances. supported by the increase in malaria prevalence in Kauai forest We also hypothesized that mosquito abundance and P. birds, observed between two sampling period (1994-1997 relictum transmission will be greater near streams than on and 2007-2013) and by the detection of Cx. quinquefasciatus ridge lines, as Cx. quinquefasciatus larvae had never been larvae by Atkinson et al. (2014). found anywhere other than in stream margins and rock pools The occurrence of malaria is dependent on along stream drainages on Kauai (Atkinson et al. 2014). To environmental conditions, such as temperature (Rueda address these hypotheses, samples of both larval and adult et al. 1990), precipitation (Shaman and Day 2007), wind Cx. quinquefasciatus were collected to assess their relative (influencing vector dispersion), availability of larval habitat abundance and distribution and to determine the prevalence influenced by habitat degradation, forest fragmentation (feral of P. relictum in different areas of the Alakai Plateau. ungulates, human activities) (Reiter and LaPointe 2007, 2009, LaPointe et al. 2012), and potential host abundance (Samuel MATERIALS AND METHODS et al. 2011), which impact both parasite and vector life cycles (Atkinson and LaPointe 2009). On Hawaii Island, elevation Study sites gradient, temperature, and precipitation were the three Samples were collected at sites representing different major factors influencing Cx. quinquefasciatus population altitudes, meteorological
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