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Recent Meetings

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A simple individual-based model for the transmission of avian malaria in Hawai'i

Date: August 3-9, 2003
Location: 88th Annual Ecological Society of America, Savannah, Georgia

Authors: Jorge A. Ahumada, Michael Samuel, Andy Dobson, Dennis LaPointe and Carter Atkinson

Abstract: We present an individual based model that simulates the transmission of avian malaria (Plasmodium relictum) by mosquitoes (Culex quinquefasciatus) on honeycreeepers in the big island of Hawai'i. We explore the properties and predictions of this model as we vary the intensity and statistical distribution of biting rates on hosts, the numerical ratio of vector and hosts, the differential attraction of vectors to infected hosts and the population dynamics of vectors along an elevational gradient. We also suggest ways to estimate some of the transmission parameters (particularly bitting rates on hosts) using field measurements of parasite prevalence on hosts and vectors and their population abundance.

Presentation Slides are available.

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Avian malaria dynamics along an elevational gradient in Hawaii: a model simulation

Date: August 2004
Location: Ecological Society of America, Portland, Oregon

Authors: Ahumada, J.A., M.D. Samuel, C.T. Atkinson, B. Woodworth, D.A. LaPointe, and A.P. Dobson

Abstract: We present a model of avian malaria dynamics in endemic Hawaiian forest birds along an altitudinal gradient on the eastern slope of Mauna Loa, Island of Hawaii. The model integrates several submodels for vectors, transmission, host and habitat features in a spatially-explicit framework (grid-based landscape) from sea level up to the tree line. A submodel simulates the dynamics of the primary vector of avian malaria (Culex quinquefasciatus) as a function of rainfall, temperature and cavity availability. We include the effects of temperature on parasite development by adjusting the time the vectors are latent and infectious at different elevations. This submodel is coupled with a multispecies bird submodel that simulates the biting and transmission process under several scenarios. The model predicts higher vector abundance and less seasonal variation at lower elevations than at middle and higher elevations. These patterns affect the intensity and temporal dynamics of transmission between elevations; birds at lower elevations are exposed to a larger number of vectors through a longer period of time than birds at middle and higher elevations. However, increased cavity availability for mosquitoes at middle and higher elevations (due to human and pig disturbance) may increase transmission compared to otherwise unaltered habitat.

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Avian malaria dynamics along an elevational gradient in Hawaii: A model simulation

Date: May 2004
Location: Meeting on Infectious Diseases, Emory University

Authors: Ahumada, J.A., M.D. Samuel, C.T. Atkinson, B. Woodworth, D.A. LaPointe, and A.P. Dobson

Abstract: We present a model of avian malaria dynamics in endemic Hawaiian forest birds along an altitudinal gradient on the eastern slope of Mauna Loa, Island of Hawaii. The model integrates several submodels for vectors, transmission, host and habitat features in a spatially-explicit framework (grid-based landscape) from sea level up to the tree line. A submodel simulates the dynamics of the primary vector of avian malaria (Culex quinquefasciatus) as a function of rainfall, temperature and cavity availability. We include the effects of temperature on parasite development by adjusting the time the vectors are latent and infectious at different elevations. This submodel is coupled with a multispecies bird submodel that simulates the biting and transmission process under several scenarios. The model predicts higher vector abundance and less seasonal variation at lower elevations than at middle and higher elevations. These patterns affect the intensity and temporal dynamics of transmission between elevations; birds at lower elevations are exposed to a larger number of vectors through a longer period of time than birds at middle and higher elevations. However, increased cavity availability for mosquitoes at middle and higher elevations (due to human and pig disturbance) may increase transmission compared to otherwise unaltered habitat.

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Avian malaria in native Hawaiian forest birds

Date: July 2005
Location: Seminar sponsored by the Adelaide Zoological Society, Adelaide, Australia

Authors: Samuel, M.D.

Abstract:

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Biocomplexity in the Environment Awardees Meeting

Date: 14-17 September 2003
Location: Arlington, VA

Authors: D. Duffy

Abstract: David C. Duffy, University of Hawaii Manoa. Biocomplexity of Introduced Avian Diseases in Hawaii: Threats to Biodiversity of Native Forest Ecosystems. DEB00-83944.

With the necessity that each vector mosquito must successfully bite an appropriate host twice, malaria would appear a disease with an easily broken transmission cycle; however, the malarias, both human and animal, have resisted medical control, even though they were among the first diseases to be understood epidemiologically. Simple parasite-host studies appear unable to capture the behavior of malaria in the wild. This project uses an avian malaria in the Hawaiian Islands to study the malaria system at levels ranging from the genetics of the disease, its vector and its hosts, to the response of hosts to infection, the effect of seasonality on host and vector populations, through to the effect of landscape patterns and anthropogenic change on disease cycles.

The native forest birds of Hawaii had apparently no resistance to malaria when it was introduced into the islands sometime in the last century. In response, these species disappeared from the lowlands and became confined to the higher elevations of mountains, above the reach of malaria-bearing mosquitoes. While our work is still ongoing, it suggests that at least some of the species have acquired some form of resistance to malaria and they are now present in the lowlands where they are able to survive and breed, even under intense exposure to malaria. Preliminary work suggests that native bird species with the least degree of genetic dispersal have the greatest degree of resistance, perhaps because they are exposed to strong local selection, while less philopatric birds may dilute selection, delaying the development of resistance.

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Climate Change, Vector-borne Avian Diseases and Hawaiian Forest Birds - What Will the Future Bring?

Date: June, 2007
Location: Presidential Symposium, First North American Parasitology Congress

Authors: Atkinson, C.T., B.L. Woodworth, D.A. LaPointe, and M.D. Samuel

Abstract: Hawaiian honeycreepers are spectacular examples of adaptive radiation, but face one of the highest rates of extinction in the world. Of more than 50 species and subspecies documented since discovery of the islands by the Western world, only 13 are believed to be extant and more than half of these are critically endangered. Both population declines and dramatic changes in the altitudinal distribution of native birds have been tied closely to the introduction of mosquito vectors, avian malaria (Plasmodium relictum) and avian pox virus (Avipoxvirus spp.). In this presentation, we will discuss how climate interacts with biotic components of this disease system, affecting transmission across steep altitudinal gradients of temperature and rainfall. Keys to sustaining the remaining diversity of this endemic avifauna likely lie at the extremes of these altitudinal gradients, both in the lowlands where natural selection is fostering evolution of disease resistance and in remaining high elevation refugia where restoration efforts are seeking to improve and expand habitat.

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Distribution and abundance of native forest birds in low-elevation habitats on Hawaii

Date: July 2003
Location: Hawaii Conservation Conference, Honolulu, HI

Authors: Caleb S. Spiegel, Patrick Hart, Erik Tweed, Carlene Henneman, Jaymi LeBrun, and Bethany L. Woodworth

Abstract: Recent studies have reported breeding populations of native bird species at low-elevation (<350m) sites on Hawai'i. These findings contrast with previous studies which showed that low-elevation areas were nearly devoid of native birds. Here we document the distribution and abundance of native forest birds over a wide area of low-elevation habitat on Hawai'i. We conducted systematic Variable Circular Plot (VCP) counts along aproximately 116 kilometers of primary and secondary roads on the east slope of Kilauea volcano (Lower Puna District) from Febuary-June 2003. A total of 166 survey stations ranged in elevation from sea level to 320 meters covering much of the land between Hawai'i Paradise Park subdivision and Kalapana town. Native Hawai'i 'Amakihi (Hemignathus virens) were distributed widely throughout the study area and were common and patchily abundant at sea level, while native Apapane (Himatione sanguinea) were found less frequently, in smaller numbers, and locally below 30m. Relative abundance and frequency of Hawai'i 'Amakihi along a 35-km section of our lowest elevation route (0-55m) appear to have increased over the past decade: surveys in February 2003 documented 'Amakihi at 11/50 stations (19%, mean 'Amakihi per station =0.56, SE=0.17), compared with no 'Amakihi at 12 stations surveyed in December 1993 - February 1994. Our data expand the known range of native bird species on Hawai'i, and demonstrate the need for greater conservation efforts to preserve remaining low-elevation Hawaiian forests as potential habitat for both existant and recolonizing populations of native bird species.

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Diversity and pathogenicity of Avipox viruses from Hawaiian Forest Birds

Date: July 26, 2006
Location: Honolulu, Hawaii

Authors: Alexis Giannoulis1, Susan I. Jarvi1, Carter T. Atkinson3 Dennis Triglia2, Kiara Bianchi1 Margaret EM Farias1 and Leayne Patch-Highfill 1,2

1 Department of Biology, University of Hawaii, Hilo
2 USGS Hawaii Cooperative Studies Unit, Pacific Aquaculture and Coastal Resources Center, University of Hawaii, Hilo
3U.S. Geological Survey - Biological Resources Discipline, Pacific Island Ecosystems Research Center

Abstract: Reports by early naturalists suggest that Avipox viruses have been impacting native Hawaiian forest birds for over 100 years. Clinical signs of the cutaneous form of avipox in Hawaii include the appearance of nodular lesions on unfeathered areas of the body, especially the feet. Avipox viruses are exceptional in that they possess genes that can modify innate host immunity, and may therefore play a significant role, with malaria, in the decline of native forest bird populations. To begin to evaluate the diversity and pathogenicity of Avipoxvirus in Hawaiian birds, we produced isolates in Muscovy duck embryonic fibroblasts from lesions collected from seven species of birds originating from four Hawaiian islands. To begin to characterize genetic variation we sequenced a fragment of the 4b core protein gene. To evaluate within-individual variation, multiple clones were sequenced from several individuals. Dates of collection of samples from which isolates were prepared ranged from 1993-2004. Ancient DNA techniques were used to obtain and confirm 4b sequence from an infected museum elepaio collected in 1900. Phylogenetic analysis of these 4b sequences indicate two variants of pox exist in Hawaii. The two clusters are approximately 6% divergent. Within-individual variation appears minimal suggesting individuals are infected by a single pox variant. The pox variants we recovered in chickens appear to be fowl pox variants and are distinct from the canarypox-like variants detected in Hawaiian passerines. Reciprocal experimental infections suggest that neither long-term immunity nor reciprocal immunity was induced and thus the two variants are antigenically distinct or may induce only short-term immunity.

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Diversity, abundance, seasonality and infection rates of mosquitoes on windward Mauna Loa

Date: July 10 -11, 2003
Location: Hawaii Conservation Conference, Honolulu, Hawaii

Authors: Thomas C. Smith, Aaron Gregor, A. Dan Lease, Rachel DeMots and Dennis A. LaPointe

Abstract: As part of the Biocomplexity of Avian Disease project, we have spent the last year investigating mosquito populations and avian malaria, Plasmodium relictum in mosquitoes. Using CO2 traps and Reiter Oviposition traps we trapped approximately 7000 trap nights over 12 months, on nine one-square-kilometer study grids at low- (<500ft), mid- (4000ft) and high- (600ft) elevations. We trapped three non-native species of mosquito, Culex quinquefasciatus, Aedes albopictus, and Wyeomeia mitchelli, in a variety of forest types between 0 and 2000m elevation on the southeast slopes of Mauna Loa.. Culex quinquefasciatus mosquitoes (most competent P. relictum vector) were dissected and infection status determined by microscopy. All three species of mosquito were present at low-elevation, with highly variable relative abundances among sites. Only Culex mosquitoes were found at mid and high elevation, with great variability between field sites, and virtually no mosquitoes found at high-elevation. Wyeomyia populations increased from May- June; Aedes and Culex populations at low elevation and Culex at mid elevation increased from June through November. At mid and low elevation sites, Culex populations experienced large spikes throughout the year. Plasmodium relictum was found at all sites below 6000ft. Prevalence of P. relictum in Culex mosquitoes varied greatly among low elevation sites and among mid-elevation sites. Infection rates appear to rise in late summer and fall, decreasing again in winter.

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Ecology of avian malaria in native Hawaiian forest birds

Date: July 2005
Location: International Wildlife Disease Congress, Cairns, Australia

Authors: Samuel, M.D., C.T. Atkinson, J.A. Ahumada, D.A. LaPointe, B.W. Woodworth, and D.C. Duffy

Abstract: The introduction of mosquitoes and avian malaria to Hawaii and subsequent decline of endemic honeycreepers provides a premier example of the effect of introduced disease on susceptible island populations. Malaria is believed one of the primary factors responsible for native bird disappearance at lower elevations and the restriction of highly susceptible species to upper elevation forests. Outbreaks of malaria in native Hawaiian bird populations depend on environmental conditions which drive mosquito abundance and disease transmission, and the relative abundance of susceptible birds in the population. Based on field investigations, laboratory studies, computer modeling, analysis of malaria prevalence, and climate patterns we evaluated the dynamics of avian malaria infection in apapane in mid-elevation forests on the island of Hawaii. Field investigations suggest that evolution in disease resistance has occurred in low-elevation amakihi populations. Our research provides a linkage between annual climate variation (especially rainfall), mosquito abundance, epizootic disease events, and host impacts. These linkages help explain annual cycles and elevational gradients in the dynamics of avian malaria. Restoration of Hawaiian forest bird communities will depend on management strategies based on the dynamics of malaria at the landscape and evolutionary scales.

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Experimental Evidence of Evolving Disease Resistance in Low Elevation Hawaii Amakihi

Date: June 29, 2004
Location: Hawaii Conservation Conference, Honolulu, Hawaii

Authors: K. Schletz, D. Triglia and C.T. Atkinson

Abstract: One of the primary hypotheses explaining the relatively recent emergence of low elevation native bird populations on both Oahu and Hawaii is natural selection for resistance to introduced avian pox and malaria. While this hypothesis is appealing, supporting data have been circumstantial and other alternative explanations have not been ruled out. We measured morbidity and mortality to acute malaria (Plasmodium relictum) in a group of uninfected low elevation Hawaii Amakihi (Hemignathus virens) from Puna, and a group of uninfected high elevation Hawaii Amakihi from Upper Waiakea Forest Reserve by exposing birds to single infective mosquito bites. Control groups included superinfected low and high elevation Amakihi and uninfected high elevation Amakihi. Low elevation Amakihi had lower peripheral parasitemias, lost significantly less body weight, and had lower mortality during acute phases of the infection than high elevation birds. These findings provide the first definitive evidence that natural selection may be driving evolution of more disease resistant native birds in areas with intense disease transmission. The high rates of disease transmission that occur in some low elevation habitats may be critical for speeding selection of disease resistance, highlighting the importance of protecting and managing low and mid elevation native forests.

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Fine scale genetic differentiation and isolation by distance in the Hawaii vector of avian malaria,

Date: 3 - 7 December 2003
Location: 52nd Annual Meeting of the American Society of Tropical Medicine and Hygiene, Philadelphia, PA

Authors: Nusha Keyghobadi, Dennis Lapointe, Dina M. Fonseca, Genetics Program, National Museum of Natural History, Smithsonian Institution, Washington DC; Wildlife Disease Laboratory, USGS-BRD-PIERC, Hawaii National Park HI; Genetics Program, National Museum of Natural History, Smithsonian Institution, Washington DC.

Abstract: Geographic factors affecting the movement and distribution of disease vectors are critical determinants of the spatial dynamics of disease systems. Avian malaria in Hawaii represents a model tropical disease system that appears strongly affected by elevation gradients. We examined the effects of distance and elevation on population structure of the mosquito vector of avian malaria (Cx. quinquefasciatus) by conducting a survey of genetic variation within and among populations along an elevation gradient on the island of Hawaii. We analyzed samples of mosquitoes from nine field sites (3 low-, 5 mid-, and 1 high-elevation) using twelve microsatellites. Genetic differentiation among all of the sites was significant and an analysis of molecular variance with populations grouped by elevation class (low, mid, or high), showed significant differentiation among elevation classes and among populations within elevation class. The most dramatic differences were between the one high elevation site and all other sites. An assignment test with sub-sampling to control for differences in sample size showed that the high elevation samples had the most unique genetic signature. Among low and mid elevation sites we observed significant isolation by distance over only 40 km, Our results indicate that despite their recent introduction to Hawaii (mid-1820s), significant genetic differentiation among populations of Cx. quinquefasciatus at a fine geographic scale can be detected using highly variable microsatellite markers. Among the mid- and low elevation sites, the significant pattern of isolation by distance indicates limited dispersal and gene flow among populations. Furthermore, the large degree of differentiation of the high elevation suggests that the small numbers of mosquitoes occasionally seen at high elevation site are not temporary vagrants from the lower sites, but may represent a population adapted to high elevations that persists locally at low densities and that is rarely detected.

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Impacts of avian malaria on endemic Hawaiian forest birds

Date: September 2005
Location: The Wildlife Society, 12th Annual Conference, Madison, Wisconsin

Authors: Samuel, M.D., C.T. Atkinson, J.A. Ahumada, and D.A. LaPointe

Abstract: The introduction of mosquitoes and avian malaria to Hawaii and the subsequent decline of endemic honeycreepers provides a premier example of the effect of introduced disease on susceptible populations. Despite the role of this disease on reducing the biodiversity of native Hawaiian forest birds, we have little understanding of its epidemiology and transmission dynamics. Based on field investigations, computer modeling, analysis of malaria prevalence, and climate patterns we determined transmission of avian malaria infection to native Hawaiian apapane in mid-elevation forests on the island of Hawaii. Transmission of avian malaria to birds occurred primarily during fall and corresponded with a predicted peak in mosquito abundance. Survival was lower in susceptible birds than in birds which survived infection, indicating a significant impact of malaria on native bird populations. Predicted mosquito abundance and disease transmission was much higher during a wet year, when 90% of the apapane population became infected, than during a dry year, when only 50% became infected. Mortality of native Hawaiian bird populations from avian malaria may depend on environmental conditions which drive mosquito abundance and disease transmission, and the relative abundance of susceptible birds in the population. Our results provide a linkage between annual climate variation (especially rainfall), mosquito abundance, epizootic disease events, and host impacts. These linkages help explain annual cycles and elevational gradients in the dynamics of avian malaria.

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Impacts of avian malaria on endemic Hawaiian forest birds

Date: August 2004
Location: Ecological Society of America, Portland, Oregon

Authors: Samuel, M.D., C.T. Atkinson, J.A. Ahumada, and D.A. LaPointe

Abstract: The introduction of mosquitoes and avian malaria to Hawaii and the subsequent decline of endemic honeycreepers provides a premier example of the effect of introduced disease on susceptible populations. Despite the role of this disease on reducing the biodiversity of native Hawaiian forest birds, we have little understanding of its epidemiology and transmission dynamics. Based on field investigations, computer modeling, analysis of malaria prevalence, and climate patterns we determined transmission of avian malaria infection to native Hawaiian apapane in mid-elevation forests on the island of Hawaii. Transmission of avian malaria to birds occurred primarily during fall and corresponded with a predicted peak in mosquito abundance. Predicted mosquito abundance and disease transmission was much higher during a wet year, when 90% of the apapane population became infected, than during a dry year, when only 50% became infected. Mortality of native Hawaiian bird populations from avian malaria may depend on environmental conditions which drive mosquito abundance and disease transmission, and the relative abundance of susceptible birds in the population. Our results provide a linkage between annual climate variation (especially rainfall), mosquito abundance, epizootic disease events, and host impacts. These linkages help explain annual cycles and elevational gradients in the dynamics of avian malaria.

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In the Eyes of the Mosquito, All Birds are Not Created Equal

Date: June 29, 2004
Location: Hawaii Conservation Conference, Honolulu, Hawaii

Authors: D. Monie and D. LaPointe

Abstract: It has been demonstrated that non-native birds in Hawaii are an unlikely reservoir of avian malaria, therefore making them potential sinks for transmission. This assumes that all birds are equal in their desirability and complacency to serve as blood hosts to mosquitoes. As part of an attempt to model the transmission of avian malaria across a broad landscape, we looked at the mosquito defensive behavior of some native and non-native passerines in Hawaii. We used Iiwi, Apapane, and Hawaii Amakihi and the introduced Japanese White Eye, Red-Billed Leiothrix, and House Sparrow. Unrestrained individual birds were exposed to 20 mosquitoes (Culex quinquefasciatus) for a three hour period. Birds were removed and mosquitoes were collected and examined for feeding success. Mosquito blood feeding success rates on Iiwi ranged from 57% to 85%, on Apapane ranged from 72% to 92%, and on Amakihi ranged from 35% to 92%. With the Japanese White Eye, mosquitoes had blood feeding success rates ranging from 5% to 23% and for the Red-Billed Leiothrix the rates ranged from 1.6% to 10%, while with the House Sparrows the range was from 55% to 68%. These preliminary results suggest that while individuals may vary in their tolerance to mosquito blood-feeding, non-native birds show more defensive behavior in general than native birds. Since mosquitoes host seek until they are fully engorged, encounters with non-native birds would not necessarily translate into diminished transmission to native birds.

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Introduced mosquito-borne avian disease and endemic avifauna of Hawaii: an overview of past, present

Date: February, 5-6, 2003
Location: West Nile Virus Wildlife Health Workshop, Smithsonian Environmental Research Center, Edgewater, MD

Authors: Dennis A LaPointe, Bethany L. Woodworth and Carter T. Atkinson

Abstract: Endemic Hawaiian bird species and populations have been in decline since the arrival of Polynesians. The subsequent colonization by Europeans has accelerated species extinction and population decline. While many factors have contributed to the loss of native birds, introduced mosquito-borne disease is believed to be the main limiting factor affecting populations. Biting flies were not present in the Hawaiian Islands until 1826 when Culex quinquefasciatus was first reported in the port town of Lahaina, Maui. By the turn of the century naturalists were reporting pox-like lesions on the feet of native birds collected in low elevation forests. Research conducted during the 50?s and 70?s identified the presence of avian malaria and avian pox and documented the impact of these pathogens on native Hawaiian forest birds. Since 1991 the USGS has been conducting research on avian disease in Hawaii and has recently initiated a collaborative study with scientists from the Smithsonian Institute, University of Hawaii, and Princeton University to model the biocomplexity of these diseases over the broad landscape of Mauna Loa. While avian malaria still has a clear negative impact on some populations there is evidence to suggest that other populations have persisted or recovered in the presence of disease. The possible arrival of West Nile Virus (WNV) in the Hawaiian Islands is likely to have a profound effect on the present disease system and bird communities. Three currently listed species may be particularly vulnerable: the Hawaiian Goose, Hawaiian Crow and Hawaiian Hawk.

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Introduced Mosquito-Borne Avian Disease: Past Impacts and Future Hopes

Date: June, 2007
Location: Cooper Ornithological Society, Moscow, Idaho

Authors: LaPointe, D.A. and C.T. Atkinson

Abstract: Through observations and experiments conducted over a half century ago, Richard Warner formally proposed a causal relation between introduced mosquito-borne disease and the extinction and decline of Hawaiian avifauna. The continued research by Charles van Riper and others confirmed the susceptibility of Hawaiian forest birds to avian pox and avian malaria. Since the introduction of the vector Culex quinquefasciatus around 1826 there have been waves of avian extinction and population declines as first avian pox and then avian malaria moved across the islands. Today endangered species are restricted to high elevation refugia where vectors are scarce and cool temperatures retard parasite development while epizootics of varying severity annually occur at mid elevations. The avian disease system remains dynamic, however, and while one species, the amakihi, appears to have evolved a tolerance to the disease and is returning to its former range, global climate change, new vector species and new pathogens threaten remaining species and populations. The intractable nature of disease presents a formidable obstacle to the recovery and restoration of Hawaiian forest birds throughout much of their former range. Although there are no easy solutions to avian disease, the close association between feral pigs and mosquitoes provides some hope toward the reduction of mosquito-borne disease.

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Introduced Pathogens and Persistent Bird Populations in Hawaii: Biocomplexity of an Evolving Diseas

Date: July 2002
Location: Hawaii Conservation Conference, Honolulu, HI

Authors: Patrick Hart, Bethany L. Woodworth, Carter Atkinson, Dennis LaPointe, Paul Banko, Sue Jarvi, Robert Fleischer, Michael Samuel, Dina Fonseca, David Duffy, Andrew Dobson, Erik Tweed, Kelly Kozar, Carlene Hennemen, Tami Dennette, Caleb Speigel, Dan Lease, Aaron Gregor, Kiara Banks, and Peggy Farias.

Abstract: Avian malaria and pox are known to have severe detrimental impacts on native bird populations in Hawaii, leading to the near-absence of native birds from most low-elevation habitats, where mosquito vectors are abundant. The "Biocomplexity of Introduced Avian Disease" project is investigating host species, vectors, and parasitic infections in 9 ohia-dominated forests from sea level to 5400 m on eastern Mauna Loa. We have detected year-round presence of the southern house mosquito (Culex quinquefasciatus), the vector of avian malaria, in 3 low-elevation forests. Mosquitos infected with malaria have been found at all 3 sites, demonstrating that local disease tramission is occuring. Nonetheless, the forests continue to harbor high densities of the native Hawaii Amakihi (Hemignathus virens). Amakihi are resident and breeding at low elevations in densities approximately 2-3 times those found at high elevations (16.2 birds captured/100 net-hrs and 5.7 birds/count period at low elevations, compared with 5.7 birds/100 net-hrs and 2.1 birds/count period at high elevations). Amakihi persist despite extremely high prevalence rates of malaria (60-90% of birds infected). Laboratory challenge experiments lend support to the idea that the primary reservoir of avian malaria at low elevations on Hawaii is the Hawaii Amakihi. The genetic, epidemiological, immunological, and demographic basis for persistence of these populations is the subject of ongoing research. In the face of expanding mosquito populations and continued threat of disease, understanding how these populations persist may hold the key to preservation of other native bird species in Hawaii.

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Introduced pathogens and persistent bird populations in Hawaii: Biocomplexity of an evolving disease

Date: September 2002
Location: North American Ornithological Congress, New Orleans, Louisiana

Authors: BETHANY L. WOODWORTH, CARTER T. ATKINSON, DENNIS LAPOINTE, PAUL BANKO, USGS/BRD, PATRICK HART, ERIK TWEED, KELLY KOZAR, CARLENE HENNEMEN, TAMI DENETTE, CALEB SPEIGEL, DAN LEASE, AARON GREGOR, Hawaii National Park, Hawaii; SUE JARVI, KIARA BANKS, PEGGY FARIAS, Univ. of Hawaii, Hilo, Hawaii; ROBERT FLEISCHER, DINA FONSECA, LORI EGGERT, EBEN GERING, Smithsonian Institution, Washington, DC; MICHAEL SAMUEL, JORGE AHUMADA, USGS-National Wildlife Health Center, Madison, WI; ANDREW DOBSON, Princeton University, Princeton, NJ; and DAVID DUFFY, University of Hawaii, Honolulu, HI.

Abstract: The introduction of mosquito-borne avian malaria (Plasmodium relictum) and pox (Poxvirus avium) to Hawaii are known to have had severe detrimental impacts on the native avifauna, leading to restriction of most native birds to high elevation refugia where mosquitos are rare. Recent emergent phenomena, such as persistence of some native bird populations in low-elevation habitats, indicate that this system is still evolving. Our studies show that native Hawaii Amakihi (Hemignathus virens) are resident and breeding in low-elevation forests in densities approximately 2-3 times those found at high elevations. Amakihi persist despite malaria prevalence rates of 60-90%, with a single host infected with up to 9 variants of P. relictum. Malaria-infected Culex quinquefasciatus occur at all three low-elevation sites, demonstrating local disease tramission. Laboratory challenge experiments lend support to the idea that the primary reservoir of avian malaria at low elevations on Hawaii is the Hawaii Amakihi. The genetic, epidemiological, immunological, and demographic basis for persistence of these populations is the subject of ongoing research. Understanding the mechanisms by which low-elevation native bird populations persist may hold the key to long-term preservation of the Hawaiian avifauna.

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Introduced Pathogens and recovering bird populations in Hawaii

Date: July 2003
Location: 17th Annual Meeting of the Society for Conservation Biology, Duluth, Minnesota

Authors: WOODWORTH, BETHANY L., Carter T. Atkinson, Dennis A. LaPointe, Patrick J. Hart, Erik J. Tweed, Carlene Henneman, Caleb Spiegel, Tami Denette, Jaymi LeBrun, Kelly L. Kozar, Dennis Triglia, Dan Lease, Aaron Gregor, Tom Smith, Michael Samuel, David Duffy.

Abstract: The introduction of mosquito-borne avian malaria (Plasmodium relictum) and pox (Poxvirus avium) to Hawaii are known to have had severe detrimental impacts on the native avifauna, leading to restriction of most native birds to high elevation refugia where mosquitos are rare. Recent emergent phenomena, such as recolonization of low-elevation habitats by some native bird populations, indicate that this system is still evolving. Our studies show that native Hawaii Amakihi (Hemignathus virens) are resident and breeding in low-elevation forests in densities approximately 2-3 times those found at high (disease-free) elevations. Amakihi persist despite malaria prevalence rates of 60-90%, with a single host infected with up to 9 variants of P. relictum. Malaria-infected mosquitoes, Culex quinquefasciatus, occur at all three low-elevation sites, demonstrating local disease tramission. The genetic, epidemiological, immunological, and demographic basis for persistence of these populations is the subject of ongoing research. Understanding the mechanisms by which low-elevation native bird populations persist may hold the key to long-term preservation of the Hawaiian avifauna.

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Non-Native Forest Birds: are they important reservoir hosts for avian malaria?

Date: July 18-19, 2002
Location: Hawaii Conservation Conference

Authors: Kelly Kozar, Carter T. Atkinson, Eben Gering, Peggy Farias and Susan I. Jarvi

Abstract: Avian malaria (Plasmodium relictum) continues to be a major factor limiting the recovery of native Hawaiian forest birds. Most disease transmission occurs at elevations below 5,000 ft. because of thermal constraints on both the mosquito vector and parasite. Transmission can occur at higher elevations in warmer months, however. The role non-native birds play as reservoir hosts for initiating these outbreaks has been controversial, with some suggesting that their removal from native forest bird habitats might be an effective strategy for preventing epidemics. We tested susceptibility of Japanese White-Eyes (Zosterops japonicus), Red-Billed Leiothrix (Leiothrix lutea), and House Sparrows (Passer domesticus) to malaria and measured their infectiousness to mosquitoes over time. House sparrows were the most susceptible of these species and capable of infecting mosquitoes up to 200 days post infection (PI). Japanese White-Eyes and Red-Billed Leiothrix were difficult to infect by mosquito bite and were infectious to mosquitoes for only a brief time. Removal of these two species from recovery habitats will probably have little impact on disease transmission. House Sparrows, however, could serve as focal sources for infection. Their association with human infrastructure and water sources at higher elevations should be a concern for resource managers.

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Serological Evaluation of poxvirus and malarial infection of native birds on the island of Hawai'i

Date: July 10-11, 2003
Location: Hawaii Conservation Conference, Honolulu, Hawaii

Authors: Dennis Triglia, Bethany L. Woodworth, Patrick Hart and Carter T. Atkinson

Abstract: Avian pox (Poxvirus avium) infections may severely impact native bird populations in Hawai?i. The disease is characterized by proliferative lesions on the unfeathered skin of the toes, legs or head, and in severe cases on the mucous membranes of the mouth, eyelids and upper respiratory tract. We have developed an assay (ELISA) to measure avian IgG plasma antibodies directed against a poxvirus strain isolated from a cutaneous lesion removed from an ?I?iwi (Vestiaria coccinea) and propagated in vitro in Muscovy duck (Cairina moschata) embryonic fibroblast culture. Antibodies to poxvirus were detected in heparinized plasma from 11/110 Hawai?i ?Amakihi (Hemignathus virens), 25/103 ?Apapane (Himatione sanguinea) and 4/48 ?I?iwi captured between April 2001 and March 2003 at 9 study locations from 200 m to 1800 m elevation on eastern Mauna Loa and Kilauea volcanoes. The same birds were tested for exposure to avian malaria (Plasmodium relictum) using another ELISA. The birds fell into 3 categories: (1) malaria-negative/pox-negative, (2) malaria-positive/pox-positive and (3) malaria-positive/pox-negative. We found no serological evidence of pox-positive/malaria-negative birds in the sample we evaluated. Strong association of pox antibody with mosquito-transmitted malarial infections (40 of 132 malaria-positive birds were also pox-positive) indicates poxvirus transmission in forest birds is predominantly mosquito-mediated, rather than between infected and susceptible birds or by contact with contaminated objects. Control of the vector mosquito Culex quinquefasciatus is critical to minimizing the spread of poxvirus and malaria in native forest birds.

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The biocomplexity of introduced avian disease in Hawaii: An overview and summary of preliminary find

Date: February 19-20, 2003
Location: Pacific Entomological Conference, Honolulu, Hawaii

Authors: Dennis A. LaPointe, Bethany L. Woodworth, Carter T. Atkinson, and Dina Fonseca

Abstract:

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The Japanese White Eye (Zosterops japonicus): Reservoir for Avian Malaria or Dead-End Host

Date: July 26, 2006
Location: Hawaii Conservation Conference

Authors: Kimberly Wiegand1, Carter T. Atkinson2, Susan I. Jarvi1

1Department of Biology, University of Hawaii, Hilo
2U.S. Geological Survey, Pacific Island Ecosystems Research Center

Abstract: The introduced Japanese White Eye (Zosterops japonicus) is now the most common forest bird in the Hawaiian Islands. The distribution of this species extends from sea level to tree line on all of the major islands and it is a major component of the forest bird community in the most remote areas. While this species is susceptible to avian malaria (Plasmodium relictum), pathogenicity of the parasite is low and prevalence of malaria in wild populations is usually less than 5% by both microscopy and serology. We evaluated the reservoir potential of Japanese White Eyes through a series of experimental infections that evaluated duration and intensity of parasitemia and infectiousness to mosquito vectors. Nested Real Time PCR was more sensitive than both nested PCR and microscopy for detecting extremely low intensity infections. Approximately 50% of Japanese White Eyes that were smear positive were infectious to mosquitoes, but mean numbers of oocysts per mosquito were extremely low. Fewer than 30% of birds that were positive by Nested Real Time PCR were capable of infecting mosquitoes, most likely because of extremely low numbers of parasites in the peripheral circulation. This species is a poor reservoir host for avian malaria, but could play an indirect role in the epidemiology of the disease if individual birds absorb infective mosquito bites that would otherwise go to highly susceptible native birds.

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Transmission models and population effects of vector-borne diseases: avian malaria in hawaiian fores

Date: Agust 9-14, 2003
Location: Wildlife Disease Association Meetting, Saskatoon, Saskatchewan, Canada

Authors: Michael Samuel, Carter Atkinson, Jorge Ahumada and Bethany Woodworth

Abstract: Determining the rates of disease transmission is of primary importance in understanding the epidemiology and dynamics of most disease systems. In conjunction with studies on vector-borne malaria in Hawaiian forest birds we are currently developing generalized disease transmission models that can incorporate data from both concurrent infection (e.g., parasitemia, viremia) and cumulative infection (e.g., seroconversion). These models can be applied to known age animals, to marked animals studied over time, and to cross-sectional data collected from populations. Transmission rates can be corrected to account for bias that occurs when acute infection causes mortality that reduces the probability of detecting recently infected individuals. These models are illustrated by estimating seasonal transmission of avian malaria in Hawaiian forest birds. By combining information on disease transmission rates and case fatality rates, with the number of susceptible and immune animals, we can estimate the effects of disease of wild populations.

Presentation Slides are available.

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Transmission Models for vector-borne diseases: avian malaria in Hawaiian forest birds

Date: February 2003
Location: Smithsonian Institution

Authors: Samuel, M.D., C.T. Atkinson, and J.A. Ahumada

Abstract: Determining the rates of disease transmission is of primary importance in understanding the epidemiology and dynamics of most disease systems. In conjunction with studies on vector-borne malaria in Hawaiian forest birds we are currently developing generalized disease transmission models that can incorporate data from both concurrent infection (e.g., parasitemia, viremia) and cumulative infection (e.g., seroconversion). These models can be applied to known age animals, to marked animals studied over time, and to cross-sectional data collected from populations. Transmission rates can be corrected to account for bias that occurs when acute infection causes mortality that reduces the probability of detecting recently infected individuals. These models are illustrated by estimating seasonal transmission of avian malaria in Hawaiian honeycreepers.

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This material is based upon work supported by the National Science Foundation under Grant No. 0083944 and by the U.S. Geological Survey, Invasive species and wildlife programs. Any opinions, findings and conclusions expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation or the U.S. Geological Survey.

The Biocomplexity Project thanks the following organizations for their support:
United States Geological Survey, University of Hawaii at Manoa, University of Hawaii at Hilo, Smithsonian Institution, Princeton University, and many other collaborators
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