Bethany L. Woodworth

Genetic structure and evolved malaria resistance in Hawaiian honeycreepers

Infectious diseases now threaten wildlife populations worldwide but population recovery following local extinction has rarely been observed. In such a case, do resistant individuals recolonize from a central remnant population, or do they spread from small, perhaps overlooked, populations of resistant individuals? Introduced avian malaria (Plasmodium relictum) has devastated low‐elevation populations of native birds in Hawaii, but at least one species (Hawaii amakihi, Hemignathus virens) that was greatly reduced at elevations below about 1000 m tolerates malaria and has initiated a remarkable and rapid recovery. We assessed mitochondrial and nuclear DNA markers from amakihi and two other Hawaiian honeycreepers, apapane (Himatione sanguinea) and iiwi (Vestiaria coccinea), at nine primary study sites from 2001 to 2003 to determine the source of re‐establishing birds. In addition, we obtained sequences from tissue from amakihi museum study skins (1898 and 1948–49) to assess temporal changes in allele distributions. We found that amakihi in lowland areas are, and have historically been, differentiated from birds at high elevations and had unique alleles retained through time; that is, their genetic signature was not a subset of the genetic variation at higher elevations. We suggest that high disease pressure rapidly selected for resistance to malaria at low elevation, leaving small pockets of resistant birds, and this resistance spread outward from the scattered remnant populations. Low‐elevation amakihi are currently isolated from higher elevations (> 1000 m) where disease emergence and transmission rates appear to vary seasonally and annually. In contrast to results from amakihi, no genetic differentiation between elevations was found in apapane and iiwi, indicating that slight variation in genetic or life‐history attributes can determine disease resistance and population recovery. Determining the conditions that allow for the development of resistance to disease is essential to understanding how species evolve resistance across a landscape of varying disease pressures.

Survival, dispersal, and home-range establishment of reintroduced captive-bred puaiohi, Myadestes palmeri

Abstract We monitored the survival, dispersal, and home-range establishment of captive-bred, reintroduced puaiohi Myadestes palmeri , a critically endangered thrush endemic to the island of Kauai. Fourteen captive-bred, juvenile birds were released from hacktowers in January–February 1999 and monitored for 8–10 weeks using radiotelemetry. All 14 birds (100%) survived to 56 days post-release. Two birds (14.3%) dispersed greater than 3 km from release site within 1 day of release. The remaining birds settled within 1 week and established either temporary home-ranges (mean area=7.9±12.0 ha, range 0.4–31.9) or breeding home-ranges (mean area 1.2±0.34 ha, range 0.8–1.6). Temporary home ranges were abandonded by the beginning of the breeding season, and ultimately 6 of the 14 birds (43%) established breeding home ranges in the release area. The high survival rate bodes well for establishing additional populations through captive breeding and release; however, the 57% dispersal rate out of the target area means that several releases of birds may be necessary in order to repopulate a given drainage. Furthermore, observed dispersal and gene flow between the reintroduced and wild populations have important implications for management of the captive flock.

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

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.

Brood parasitism, nest predation, and season-long reproductive success of a tropical island endemic

The Puerto Rican Vireo (Vireo latimeri) is a single-island endemic resident on Puerto Rico. The Shiny Cowbird (Molothrus bonariensis), a generalist brood parasite native to South America, arrived on the island in 1955 and has established itself as a breeding resident. To determine the impact of the exotic cowbird on vireo reproductive success, I studied the demography of marked Puerto Rican Vireos in Guanica Forest, Puerto Rico, in 1990-1993. Vireo breeding season length varied among years (69-106 days), apparently influenced by rainfall. The primary causes of reproductive failure were nest parasitism and nest predation. Cowbirds parasitized 73-83% of vireo nests. Parasitism reduced the number of vireos fledged per successful nest by 82%, primarily through decreased hatching success and fledging success. Vireos did not abandon nests in response to cowbird egglaying, but frequently deserted if cowbirds removed host eggs. Native avian predators and exotic mammalian predators together caused the demise of about 70% of all nest attempts. As a result, daily nest survival rate was low (0.93 ± 0.01), and only 13-19% of nests fledged vireo or cowbird young. Pairs renested after failure and attempted to raise second broods. Females in this population attempted two to six nests per season and fledged an average of 1.33 vireos in 1991 and 0.24 vireos in 1993. The combination of restricted breeding season, high predation and parasitism rates, large impact of parasitism on reproductive output, and low seasonal fecundity of females suggests that, despite high survival rates, the Puerto Rican Vireo is in danger of extirpation from portions of its range.

Development of Restoration Techniques for Hawaiian Thrushes: Collection of Wild Eggs, Artificial Incubation, Hand-rearing, Captive-breeding, and Re-introduction to the Wild

From 1995 to 1999, two species of endemic Hawaiian thrushes, `Oma`o (Myadestes obscurus) and Puaiohi (M. palmeri), were captive-reared and re-introduced into their historic range in Hawai`i by The Peregrine Fund, in collaboration with the U.S. Geological Survey–Biological Resources Division (BRD) and the Hawai`i State Department of Land and Natural Resources. This paper describes the management techniques that were developed (collection of wild eggs, artificial incubation, hand-rearing, captive propagation, and release) with the non-endangered surrogate species, the `Oma`o; techniques that are now being used for recovery of the endangered Puaiohi. In 1995 and 1996, 29 viable `Oma`o eggs were collected from the wild. Of 27 chicks hatched, 25 were hand-reared and released into Pu`u Wa`awa`a Wildlife Reserve. Using the techniques developed for the `Oma`o, a captive propagation and release program was initiated in 1996 to aid the recovery of the endangered Puaiohi. Fifteen viable Puaiohi eggs were collected from the wild (1996–1997) to establish a captive breeding flock to produce birds for re-introduction. These Puaiohi reproduced for the first time in captivity in 1998 (total Puaiohi chicks reared in captivity 1996–1998 = 41). In 1999, 14 captive-bred Puaiohi were re-introduced into the Alaka`i Swamp, Kaua`i. These captive-bred birds reproduced and fledged seven chicks in the wild after release. This is the first endangered passerine recovery program using this broad spectrum of management techniques (collection of wild eggs, artificial incubation, hand-rearing, captive-breeding, and release) in which re-introduced birds survived and bred in the wild. Long-term population monitoring will be published separately [BRD, in preparation]. Zoo Biol 19:263–277, 2000.

Distribution and abundance of forest birds in low-altitude habitat on Hawai'i Island: evidence for range expansion of native species

Summary The Hawaiian honeycreepers are thought to be limited primarily to middle- and high-altitude wet forests due to anthropogenic factors at lower altitudes, especially introduced mosquitotransmitted avian malaria. However, recent research has demonstrated that at least one native species, the Hawai‘i ‘Amakihi (Hemignathus virens virens), is common in areas of active malaria transmission. We examined the current distribution and abundance of native and exotic forest birds within approximately 640 km 2 of low-altitude (0–326 m) habitat on south-eastern Hawai‘i Island, using roadside variable circular plot (VCP) at 174 stations along eight survey transects. We also re-surveyed 90 stations near sea level that were last surveyed in 1994–1995. Overall, introduced species were more abundant than natives; 11 exotic species made up 87% of the total individuals detected. The most common exotic passerines were Japanese White-eye (Zosterops japonicus), House Finch (Carpodacus mexicanus) and Northern Cardinal (Cardinalis cardinalis). Two native species, Hawai‘i ‘Amakihi and ‘Apapane (Himatione sanguina), comprised 13% of the bird community at low altitudes. Hawai‘i ‘Amakihi were the most common and widespread native species, being found at 47% of stations at a density of 4.98 birds/ha (95% CI 3.52–7.03). ‘Amakihi were significantly associated with ‘ohi’a (Metrosideros polymorpha)-dominated forest. ‘Apapane were more locally distributed, being found at only 10% of stations. Re-surveys of 1994–1995 transects demonstrated a significant increase in ‘Amakihi abundance over the past decade. This work demonstrates a widespread recovery of Hawai‘i ‘Amakihi at low altitude in southeastern Hawai‘i. The changing composition of the forest bird community at low-altitudes in Hawai‘i has important implications for the dynamics of avian malaria in low-altitude Hawai‘i, and for conservation of Hawai‘i’s lowland forests.

Temporal Variation in Bird and Resource Abundance Across an Elevational Gradient in Hawaii

ABSTRACT. We documented patterns of nectar availability and nectarivorous bird abundance over ∼3 years at nine study sites across an 1,800-m elevational gradient on Hawaii Island to investigate the relationship between resource variation and bird abundance. Flower density (flowers ha-1) and nectar energy content were measured across the gradient for the monodominant ‘Ōhi’a (Metrosideros polymorpha). Four nectarivorous bird species were captured monthly in mist nets and surveyed quarterly with point-transect distance sampling at each site to examine patterns of density and relative abundance. Flowering peaks were associated with season but not rainfall or elevation. Bird densities peaked in the winter and spring of each year at high elevations, but patterns were less clear at middle and low elevations. Variability in bird abundance was generally best modeled as a function of elevation, season, and flower density, but the strength of the latter effect varied with species. The low elevations had the greatest density of flowers but contained far fewer individuals of the two most strongly nectarivorous species. There is little evidence of large-scale altitudinal movement of birds in response to ‘Ōhi’a flowering peaks. The loose relationship between nectar and bird abundance may be explained by a number of potential mechanisms, including (1) demographic constraints to movement; (2) nonlimiting nectar resources; and (3) the presence of an “ecological trap,” whereby birds are attracted by the high resource abundance of, but suffer increased mortality at, middle and low elevations as a result of disease.

Genetic structure along an elevational gradient in Hawaiian honeycreepers reveals contrasting evolutionary responses to avian malaria

BackgroundThe Hawaiian honeycreepers (Drepanidinae) are one of the best-known examples of an adaptive radiation, but their persistence today is threatened by the introduction of exotic pathogens and their vector, the mosquito Culex quinquefasciatus. Historically, species such as the amakihi (Hemignathus virens), the apapane (Himatione sanguinea), and the iiwi (Vestiaria coccinea) were found from the coastal lowlands to the high elevation forests, but by the late 1800s they had become extremely rare in habitats below 900 m. Recently, however, populations of amakihi and apapane have been observed in low elevation habitats. We used twelve polymorphic microsatellite loci to investigate patterns of genetic structure, and to infer responses of these species to introduced avian malaria along an elevational gradient on the eastern flanks of Mauna Loa and Kilauea volcanoes on the island of Hawaii.ResultsOur results indicate that amakihi have genetically distinct, spatially structured populations that correspond with altitude. We detected very few apapane and no iiwi in low-elevation habitats, and genetic results reveal only minimal differentiation between populations at different altitudes in either of these species.ConclusionOur results suggest that amakihi populations in low elevation habitats have not been recolonized by individuals from mid or high elevation refuges. After generations of strong selection for pathogen resistance, these populations have rebounded and amakihi have become common in regions in which they were previously rare or absent.

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...