CHAPTER SEVENTEEN The extinction and decline of Hawaiian avi- fauna due to introduced mosquito-borne Managing Disease disease has become a classic example of the impact of introduced diseases on naive DENNIS A. LAPOINTE, wildlife populations (Warner 1968; this CARTER T. ATKINSON, volume, Chc'lPter9). Along with rinderpest AND SUSAN 1. JARVI virus and rabies virus, avian malaria (Plas- modiumrelictum)and avian pox virus (Avipox- virus sp.) stood for decades as rare cases of invasive pathogens in wildlife species (Guliand 1995). Today,however, with ever- increasing globalization, emergent and in- vasive human and wildlife diseases are on the rise (Daszak et al. 2000, Gubler 2001, Friend et al. 2004). Once an academic curiosity to conservation biologists out- side of Hawaii, avian malaria and pox and their impact on Hawaii's native forest birds now have continental relevance with West Nile virus's sweep across North Amer- ica and its potential threat to endangered species populations (Marra et al. 2004, Kilpatrick et al. 2007). The Hawaiian Islands, like other iso- lated oceanic islands, experienced limited natural colonization by terrestrial biota. These founders brought few, if any, para- sites and pathogens with them (Torchin et al. 2003; this volume, Chapter 1). For parasites with complex life cycles, alter- nate hosts were absent, as were the insect vectors of pathogens, such as mosquitoes, black flies, biting midges, and others. This all changed with the arrival of Westerners to the Hawaiian Islands in 1778 and the subsequent introduction of mosquitoes and mosquito-borne avian disease. Intro- duced mosquito-borne avian disease is con- sidered a major factor limiting Hawaiian forest bird populations and an obstacle to the restoration of the islands' avifauna (U.S. Fish and Wildlife Service 2006). Future ef- forts to protect remaining Hawaiian forest bird species and to restore their populations 405 406 APPLYING RESEARCH TO MANAGEMENT will rely on the development of disease native forest bird habitats, and only C.quin- management strategies that can be applied quefasciatusis presently common above 900 at the landscape level. The long history doc- m in elevation (Goff and van Riper 1980, umenting the control of vector-borne hu- LaPointe 2000). Culex quinquefasciatusis a man disease (Harrison 1978) suggests that known vector of avian malaria in Hawai'i there will be no simple solutions and that (LaPointe et al. 2005) and is the most likely an integrative and diligent approach will vector of avian pox virus (van Riper et al. be necessary (Rose 200 1) . 2002). Only a few individuals of Aalbopic- In this chapter we (1) provide a brief tus and W mitchellii were found to support overview of the mosquitoes in Ha«rai'i sporogany of Plasmodiumrelictum in the lab- and the pathogens they vector to birds (see oratory (LaPointe et al. 2005). Preliminary Chapter 9 for a more detailed account of trials with the newly established A japonicus disease biology); (2) outline possible man- suggest that this species does not support agement practices and evaluate them in the sporogony in the laboratory (LaPointe, context of endemic Hawaiian bird conser- unpubl. data). Avian pox virus does not vation, from single-species captive popu- require a specific vector and may be trans- lations to intact communities across broad mitted by any mosquito or biting arthro- landscapes; and (3), in synthesis, suggest pod. Although these three mosquito species management strategies to minimize the im- may be more or less opportunistic in host pact of vector-borne disease in Hawaiian selection (Tempelis et al. 1970, Edman forest birds. and Haeger 1977, Tanaka et al. 1979) and abundant in some lowland Hawaiian for- ests, their marginal susceptibility to avian KNOW THINE ENEMY malaria and limited altitudinal distribu- tion make them unlikely to be important Mosquito Vectors of Avian vectors of either avian malaria or pox. Their Pathogens in Hawai'i possible role as minor, incidental vectors Six biting species of mosquito have become of avian malaria or pox is still unknown. established in the Hawaiian Islands since Thus, due to its high level of vector com- the nineteenth century: Culex quinquefasciatus petence and altitudinal distribution, C.quin- (established by ca.18 2 6), Aedes aegypti (ca. quefasciatuscan alone account for the cur- 1892), Aedes albopictus(ca. 1902), Aedes vex- rent distribution and prevalence of avian ans nocturnus (ca. 196 2), Wyeomyia mitchellii malaria and pox in forest bird communities. (ca. 1981), and Aedes japonicus (ca. 2003) (Hardy 1960, Joyce and Nakagawa 1963, Hawaiian Landscapes, Feral Pigs, Shroyer 1981, Larish and Savage 2005) (Fig. and Mosquito Abundance 17. 1). The first three species are known vectors of human pathogens and have been Larval mosquitoes are aquatic and can be widely distributed throughout the tropic found in a wide range of temporary and and subtropic regions by Western com- permanent waters. C. quinquefasciatuslarvae merce (LaPointe 2007). By contrast, A v. occur in natural and artificial containers, nocturnus and A japonicusare competent lab- ditches, puddles, irrigation channels, cess- oratory hosts of encephalitis viruses but pools, and the margins of ponds and are not documented vectors of human or flowing streams. This species is adapted wildlife pathogens (Turell et al. 2001, to eutrophic waters heavily enriched Sardelis et al. 2003). W mitchellii is not with organic matter. Although generally known to transmit any vertebrate patho- not found in forest ground pools or open gens (Shroyer 198 1) . bogs in Hawai'i (Fig. 17.2), C. quinquefas- Only C.quinquefasciatus,A. albopictus,A[cpon- ciatus larvae have been recovered from icus, and W mitchellii have been found in ground pools and wallows where fecal MANAGING DISEASE 407 Figure17.1. Common mosquito species found in forest ests above 1,500 m in elevation on Hawai'i bird habitats on Hawai'i Island. Left side, top to bottom: Island (Goff and van Riper 1980, LaPointe Egg rafts, larvae, and adult female Culex quinquefasciatus,the 2000). Intermittent and ephemeral streams, main vector of avian disease in the Hawaiian Islands. Right side, top to bottom: Aedes albopictus,Aedes japonicus, however, may be important larval mosquito and Wyeomyia mitchellii.Source:Photos by Dennis LaPointe, habitats in some Hawaiian landscapes. U.S. Geological Survey. Surveys in Kipahulu Valley on Maui doc- umented C. quinquefnsciutus larvae in rock matter from livestock or feral ungulates pools of intermittent streambeds (Aruch may have enhanced the microhabitat (D. et al. 2007). LaPointe, pers. 0bs.) . In stark contrast, the younger volcanic Mosquitoes do not typically occur in landscapes of the east flank of Mauna many natural areas in the Hawaiian Islands Loa, Hawai'i Island, are all but devoid of because of temperature constraints on their permanent surface water. C. quinquefasciatus, development or the absence of suitable however, are abundant in these wet forests, larval habitat. Adult and larval mosquitoes where their larvae rely primarily on rain- were rarely encountered in windward for- water-filled cavities in the native tree fern, 408 APPLYING RESEARCH TO MANAGEMENT large tracts of forest undermines this nat- 60 ural protection (LaPointe 2000) (see Fig. Q) t1l 50 17.2). 2: ...Jt1l 40 Feral pigs, however, are not the only cul- £; prits. The numbers of C. quinquefasciatus are .3: 30 much greater in suburban and agricultural c 20 70 Q) areas than in natural areas. Conservation ~ 10 Q) 0.. areas in Hawai'i often abut residential and 0 Hapu'u Cavities Ground Pools agricultural communities that can produce high densities of mosquitoes through the Figure17.2. Larval Culex quinquefasciatusoccupancy of avail- creation of larval habitat and the presence able aquatic habitats in windward Mauna Loa forests, of abundant hosts for blood meals (Mian Hawai"i Island. The numbers over the columns rep- et al. 1990, Reisen et al. 199 0, Reisen et al. resent the total number of individual habitats of the habitat type sampled for mosquito larvae that were en- 1992). The rural community of Volcano countered in 4.5 ha of forest. Although prevalent in Village, located just outside the bound- these forests, ground pools do not appear to support aries of Hawai'I Volcanoes National Park, mosquito larvae (LaPointe 2000). serves as an excellent example. Mosquito capture rates in the village are nearly three times greater than capture rates within the hapu 'u (Cibotium spp.) (Fig. 17.3). These nearby forest (Reiter and LaPointe 2007). cavities are formed by the feral descen- Household water storage in residential dants of domestic pigs (Sus scrofa), which areas contributes to local mosquito abun- feed on the starchy core of the tree fern. dance, but the impact of artificial containers After-extracting the starch, a cup- or bowl- and impoundments may be several times shaped cavity remains that will collect rainwater and leaflitter, thereby providing Figure 17.3. Water-filled cavity in a hapu'u tree fern (Ci- a favorable habitat for larval mosquitoes. botiumglaucum) trunk created by feral pig feeding. Such Although the geological and hydrological cavities are the main breeding sites for mosquitoes in some native forests.Removal of feral pigs would reduce nature of the Mauna Loa landscape pre- the number of breeding sites, which in turn would cludes the production of mosquitoes, the potentially reduce disease transmission among birds. occurrence of hapu'u cavities throughout Source:Photo by Daniel Lease, U.S.Geological Survey. MANAGING DISEASE 409 greater on agricultural lands. Cattle opera- trol of infectious disease in humans and tions, in particular, create favorable habi- domestic animals are well documented. tats for C.quinquefascietus in the form of stock However, these approaches have not been ponds, troughs, cisterns, settlement ponds, as successful in wild animal populations. and the old tires and tarps commonly used Chemotherapy of wildlife populations is to cover feed (Reiter and LaPointe 2007).