Dennis A. LaPointe

Interactions of climate change with biological invasions and land use in the Hawaiian Islands: Modeling the fate of endemic birds using a geographic information system

The Hawaiian honeycreepers (Drepanidae) represent a superb illustration of evolutionary radiation, with a single colonization event giving rise to 19 extant and at least 10 extinct species [Curnutt, J. & Pimm, S. (2001) Stud. Avian Biol. 22, 15–30]. They also represent a dramatic example of anthropogenic extinction. Crop and pasture land has replaced their forest habitat, and human introductions of predators and diseases, particularly of mosquitoes and avian malaria, has eliminated them from the remaining low- and mid-elevation forests. Landscape analyses of three high-elevation forest refuges show that anthropogenic climate change is likely to combine with past land-use changes and biological invasions to drive several of the remaining species to extinction, especially on the islands of Kauai and Hawaii.

Ecology and conservation biology of avian malaria

Avian malaria is a worldwide mosquito‐borne disease caused by Plasmodium parasites. These parasites occur in many avian species but primarily affect passerine birds that have not evolved with the parasite. Host pathogenicity, fitness, and population impacts are poorly understood. In contrast to continental species, introduced avian malaria poses a substantial threat to naive birds on Hawaii, the Galapagos, and other archipelagoes. In Hawaii, transmission is maintained by susceptible native birds, competence and abundance of mosquitoes, and a disease reservoir of chronically infected native birds. Although vector habitat and avian communities determine the geographic distribution of disease, climate drives transmission patterns ranging from continuous high infection in warm lowland forests, seasonal infection in midelevation forests, and disease‐free refugia in cool high‐elevation forests. Global warming is expected to increase the occurrence, distribution, and intensity of avian malaria across this elevational gradient and threaten high‐elevation refugia, which is the key to survival of many susceptible Hawaiian birds. Increased temperatures may have already increased global avian malaria prevalence and contributed to an emergence of disease in New Zealand.

Bottlenecks and multiple introductions: population genetics of the vector of avian malaria in Hawaii

Avian malaria has had a profound impact on the demographics and behaviour of Hawaiian forest birds since its vector, Culex quinquefasciatus the southern house mosquito, was first introduced to Hawaii around 1830. In order to understand the dynamics of the disease in Hawaii and gain insights into the evolution of vector‐mediated parasite–host interactions in general we studied the population genetics of Cx. quinquefasciatus in the Hawaiian Islands. We used both microsatellite and mitochondrial loci. Not surprisingly we found that mosquitoes in Midway, a small island in the Western group, are quite distinct from the populations in the main Hawaiian Islands. However, we also found that in general mosquito populations are relatively isolated even among the main islands, in particular between Hawaii (the Big Island) and the remaining Hawaiian Islands. We found evidence of bottlenecks among populations within the Big Island and an excess of alleles in Maui, the site of the original introduction. The mitochondrial diversity was typically low but higher than expected. The current distribution of mitochondrial haplotypes combined with the microsatellite information lead us to conclude that there have been several introductions and to speculate on some processes that may be responsible for the current population genetics of vectors of avian malaria in Hawaii.

EFFECTS OF CHRONIC AVIAN MALARIA (PLASMODIUM RELICTUM) INFECTION ON REPRODUCTIVE SUCCESS OF HAWAII AMAKIHI (HEMIGNATHUS VIRENS)

Abstract We studied the effects of chronic avian malaria (Plasmodium relictum) infections on the reproductive success of a native Hawaiian honeycreeper, Hawaii Amakihi (Hemignathus virens). Chronic malaria infections in male and female parents did not significantly reduce reproductive success as measured by clutch size, hatching success, fledging mass, number of nestlings fledged, nesting success (daily survival rate), and minimum fledgling survival. In fact, nesting success of pairs with chronically infected males was significantly higher than those with uninfected males (76% vs. 38%), and offspring that had at least one parent that had survived the acute phase of malaria infection had a significantly greater chance of being resighted the following year (25% vs. 10%). The reproduction and survival of infected birds were sufficient for a per-capita population growth rate >1, which suggests that chronically infected Hawaii Amakihi could support a growing population. Efectos de las Infecciones Crónicas de Malaria Aviaria (Plasmodium relictum) en el Éxito Reproductivo de Hemignathus virens

Landscape factors influencing the spatial distribution and abundance of mosquito vector Culex quinquefasciatus (Diptera: Culicidae) in a mixed residential-agricultural community in Hawai'i

Abstract Mosquito-borne avian diseases, principally avian malaria (Plasmodium relictum Grassi and Feletti) and avian pox (Avipoxvirus sp.) have been implicated as the key limiting factor associated with recent declines of endemic avifauna in the Hawaiian Island archipelago. We present data on the relative abundance, infection status, and spatial distribution of the primary mosquito vector Culex quinquefasciatus Say (Diptera: Culicidae) across a mixed, residential–agricultural community adjacent to Hawai‘i Volcanoes National Park on Hawai‘i Island. We modeled the effect of agriculture and forest fragmentation in determining relative abundance of adult Cx. quinquefasciatus in Volcano Village, and we implement our statistical model in a geographic information system to generate a probability of mosquito capture prediction surface for the study area. Our model was based on biweekly captures of adult mosquitoes from 20 locations within Volcano Village from October 2001 to April 2003. We used mixed effects logistic regression to model the probability of capturing a mosquito, and we developed a set of 17 competing models a priori to specifically evaluate the effect of agriculture and fragmentation (i.e., residential landscapes) at two spatial scales. In total, 2,126 mosquitoes were captured in CO2-baited traps with an average probability of 0.27 (SE = 0.10) of capturing one or more mosquitoes per trap night. Twelve percent of mosquitoes captured were infected with P. relictum. Our data indicate that agricultural lands and forest fragmentation significantly increase the probability of mosquito capture. The prediction surface identified areas along the Hawai‘i Volcanoes National Park boundary that may have high relative abundance of the vector. Our data document the potential of avian malaria transmission in residential–agricultural landscapes and support the need for vector management that extends beyond reserve boundaries and considers a reserve’s spatial position in a highly heterogeneous landscape.

The dynamics, transmission, and population impacts of avian malaria in native Hawaiian birds: a modeling approach

We developed an epidemiological model of avian malaria (Plasmodium relictum) across an altitudinal gradient on the island of Hawaii that includes the dynamics of the host, vector, and parasite. This introduced mosquito-borne disease is hypothesized to have contributed to extinctions and major shifts in the altitudinal distribution of highly susceptible native forest birds. Our goal was to better understand how biotic and abiotic factors influence the intensity of malaria transmission and impact on susceptible populations of native Hawaiian forest birds. Our model illustrates key patterns in the malaria-forest bird system: high malaria transmission in low-elevation forests with minor seasonal or annual variation in infection; episodic transmission in mid-elevation forests with site-to-site, seasonal, and annual variation depending on mosquito dynamics; and disease refugia in high-elevation forests with only slight risk of infection during summer. These infection patterns are driven by temperature and rainfall effects on parasite incubation period and mosquito dynamics across an elevational gradient and the availability of larval habitat, especially in mid-elevation forests. The results from our model suggest that disease is likely a key factor in causing population decline or restricting the distribution of many susceptible Hawaiian species and preventing the recovery of other vulnerable species. The model also provides a framework for the evaluation of factors influencing disease transmission and alternative disease control programs, and to evaluate the impact of climate change on disease cycles and bird populations.

Dispersal of Culex quinquefasciatus (Diptera: Culicidae) in a Hawaiian Rain Forest

Abstract Introduced mosquito-borne pathogens avian malaria (Plasmodium relictum Grassi and Feletti) and avian pox virus (Avipoxvirus) have been implicated in the past extinctions and declines of Hawaiian avifauna and remain significant obstacles to the recovery and restoration of endemic Hawaiian birds. Effective management of avian disease will require extensive mosquito control efforts that are guided by the local ecology of the vector Culex quinquefasciatus Say (Diptera: Culicidae). During October and November 1997 and September through November 1998 five mark–release–recapture experiments with laboratory-reared Cx. quinquefasciatus were conducted in a native rain forest on Hawaii Island. Of the overall 66,047 fluorescent dye-marked and released females, 1,192 (1.8%) were recaptured in 43–52 CO2-baited traps operated for 10–12-d trapping periods. Recaptured mosquitoes were trapped in all directions and at distances up to 3 km from the release site. The cumulative mean distance traveled (MDTs) over the trapping period ranged from a high of 1.89 km after 11 d (September 1998) to a low of 0.81 km after 11 d (November 1998). Released mosquitoes moved predominately in a downwind direction and they seemed to use forestry roads as dispersal corridors. Applying an estimated MDT of 1.6 km to a geographical information system-generated map of the Hakalau Forest National Wildlife Refuge clearly demonstrated that the effective refuge area could be reduced 60% by mosquitoes infiltrating into managed refuge lands. These findings should have significant implications for the design of future refuges and development of effective mosquito-borne avian disease control strategies.

Fine‐scale population genetic structure of a wildlife disease vector: the southern house mosquito on the island of Hawaii

The southern house mosquito, Culex quinquefasciatus, is a widespread tropical and subtropical disease vector. In the Hawaiian Islands, where it was introduced accidentally almost two centuries ago, it is considered the primary vector of avian malaria and pox. Avian malaria in particular has contributed to the extinction and endangerment of Hawaiis native avifauna, and has altered the altitudinal distribution of native bird populations. We examined the population genetic structure of Cx. quinquefasciatus on the island of Hawaii at a smaller spatial scale than has previously been attempted, with particular emphasis on the effects of elevation on population genetic structure. We found significant genetic differentiation among populations and patterns of isolation by distance within the island. Elevation per se did not have a limiting effect on gene flow; however, there was significantly lower genetic diversity among populations at mid elevations compared to those at low elevations. A recent sample taken from just above the predicted upper altitudinal distribution of Cx. quinquefasciatus on the island of Hawaii was confirmed as being a temporary summer population and appeared to consist of individuals from more than one source population. Our results indicate effects of elevation gradients on genetic structure that are consistent with known effects of elevation on population dynamics of this disease vector.

Prevalence and distribution of pox-like lesions, avian malaria, and mosquito vectors in Kipahulu Valley, Haleakala National Park, Hawai'i, USA.

We determined prevalence and altitudinal distribution of introduced avian malarial infections (Plasmodium relictum) and pox-like lesions (Avipoxvirus) in forest birds from Kīpahulu Valley, Haleakalā National Park, on the island of Maui, and we identified primary larval habitat for the mosquito vector of this disease. This intensively managed wilderness area and scientific reserve is one of the most pristine areas of native forest remaining in the state of Hawai‘i, and it will become increasingly important as a site for restoration and recovery of endangered forest birds. Overall prevalence of malarial infections in the valley was 8% (11/133) in native species and 4% (4/101) in nonnative passerines; prevalence was lower than reported for comparable elevations and habitats elsewhere in the state. Infections occurred primarily in ‘Apapane (Himatione sanguinea) and Hawai‘i ‘Amakihi (Hemignathus virens) at elevations below 1,400 m. Pox-like lesions were detected in only two Hawai‘i ‘Amakihi (2%; 2/94) at elevations below 950 m. We did not detect malaria or pox in birds caught at 1,400 m in upper reaches of the valley. Adult mosquitoes (Culex quinquefasciatus) were captured at four sites at elevations of 640, 760, 915, and 975 m, respectively. Culex quinquefasciatus larvae were found only in rock holes along intermittent tributaries of the two largest streams in the valley, but not in standing surface water, pig wallows, ground pools, tree cavities, and tree fern cavities. Mosquito populations in the valley are low, and they are probably influenced by periods of high rainfall that flush stream systems.

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

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 (cross-sectional) 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 r...