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Despite the purported role of avian pox (Avipoxvirus spp.) in the decline of endemic Hawaiian birds, few studies have been conducted on the dynamics of this disease, its impact on freeliving avian populations, or its interactions with avian malaria (Plasmodium relictum). We conducted four longitudinal studies of 3–7 yr in length and used generalized linear models to evaluate cross-sectional prevalence of active pox infection and individuals with healed deformities that had recovered from pox. Our goal was to understand how species, season, elevation, malaria infection, and other biological characteristics influenced pox infection in ʻApapane, Hawaiʻi ʻAmakihi, ʻIʻiwi, and Japanese White-eye across low-, mid-, and high-elevation forests on the island of Hawaiʻi. We also used multistate capture-recapture (longitudinal) models to estimate pox infection rates, recovery rates, and potential pox-related mortality. Pox infection rates were typically highest in low-elevation forests, followed by mid-elevation forests, and lowest in high-elevation forests. We also found seasonal changes in pox prevalence throughout the annual cycle; typically increasing from spring through summer, peaking in fall, and declining in winter. These seasonal changes occurred in low- and mid-elevation forests, but not in high elevations where pox infection was low. Seasonal and elevation patterns of pox infection are like those for avian malaria, strongly implicating mosquito vectors, rather than other biting arthropods or contact transmission, as the primary source of transmitting both diseases. Most native Hawaiian birds recovered from pox infection within 6 months; frequently without permanent lesions. Contrary to our expectations, we found no direct evidence that pox is a substantial mortality factor in any of the three native bird species we studied. Birds with chronic malaria infection were more likely to have both active pox infection and healed pox lesions suggesting a synergistic interaction that may influence the evolution of pox virulence. Because pox infection can be assessed visually, and birds have a high recovery rate, this disease may be a sensitive indicator of the seasonal and annual risk of transmission of malaria in Hawaiʻi.

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.

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 rates that varied among elevations, likely in response to ecological factors that drive mosquito abundance. Malaria infection was highest at low elevations, moderate at mid elevations, and limited in high-elevation forests. Infection rates were highest for Iiwi and Apapane, likely contributing to the absence of these species in low-elevation forests. Adult malaria fatality rates were highest for Iiwi, intermediate for Amakihi at mid and high elevations, and lower for Apapane; low-elevation Amakihi had the lowest malaria fatality, providing strong evidence of malaria tolerance in this low-elevation population. Our study indicates that hatch-year birds may have greater malaria infection and/or fatality rates than adults. Our study also found that mosquitoes prefer feeding on Amakihi rather than Apapane, but Apapane are likely a more important reservoir for malaria transmission to mosquitoes. Our approach, based on host abundance and infection rates, may be an effective alternative to mosquito blood meal analysis for determining vector-host contacts when mosquito densities are low and collection of blood-fed mosquitoes is impractical. Our study supports the hypothesis that avian malaria has been a primary factor influencing the elevational distribution and abundance of these three species, and likely limits other native Hawaiian species that are susceptible to malaria.

The role of introduced avian malaria Plasmodium relictum in the decline and extinction of native Hawaiian forest birds has become a classic example of the potential effect of invasive diseases on biological diversity of naïve populations. However, empirical evidence describing the impact of avian malaria on fitness of Hawai[reverse prime]i's endemic forest birds is limited, making it difficult to determine the importance of disease among the suite of potential limiting factors affecting the distribution and abundance of this threatened avifauna. We combined epidemiological force-of-infection with multistate capture--recapture models to evaluate a 7-year longitudinal study of avian malaria in [reverse prime]apapane, a relatively common native honeycreeper within mid-elevation Hawaiian forests. We found that malaria transmission was seasonal in this mid-elevation forest; transmission peaked during fall and during some years produced epizootic mortality events. Estimated annual mortality of hatch-year birds typically exceeded 50% and mortality of adults exceeded 25% during epizootics. The substantial impact of avian malaria on this relatively common native species demonstrates the key role this disease has played in the decline and extinction of Hawaiian forest birds.

Forests of the Hawaiian archipelago are a global hotspot for conserving avian diversity and contain among the world's most imperiled species. Demographic studies are necessary to determine primary causes of Hawaiian forest bird population declines. We conducted research on the nesting success of multiple bird families on the island of Kauaʿi, allowing us to investigate the importance of factors related to breeding biology on forest bird declines at a community scale. Our study included two Hawaiian honeycreepers, ʿanianiau Magumma parva and ʿapapane Himatione sanguinea, a native monarch flycatcher, Kauaʿi ʿelepaio Chasiempis sclateri, and one introduced species, Japanese white-eye Zosterops japonicus. Data from 123 nests showed that nesting success ± SE, estimated using program MARK, was low for ʿapapane (0.23 ± 0.10), but did not vary substantially among our other study species (ʿanianiau = 0.56 ± 0.09, Kauaʿi ʿelepaio = 0.63 ± 0.08, Japanese white-eye = 0.52 ± 0.11). Causes of nest loss for 51 nest failures included nest predation (43%), unknown (25%), empty after termination with no signs of nest predation (e.g. eggshell or chick remains in nest, disheveled nest) (24%), and abandoned clutch or brood (4% each). Kauaʿi ʿelepaio suffered more than twice as many nest losses to predation compared to our other study species, but also had the highest nesting success; and, ʿapapane suffered least to nest predation, but had the lowest nesting success. Further, rates of nesting success derived in our study were relatively high compared to multi-species studies in mainland tropics. Therefore, although nest predation accounted for the greatest proportion of nest failures, it may not be a cause of forest bird population declines in our system. We suggest that future demographic studies focus on post-fledgling, juvenile, and adult survival, in addition to the importance of double-brooding and renesting attempts on annual reproductive success.

Next-generation 454 sequencing techniques were used to re-examine diversity of mitochondrial cytochrome b lineages of avian malaria (Plasmodium relictum) in Hawaii. We document a minimum of 23 variant lineages of the parasite based on single nucleotide transitional changes, in addition to the previously reported single lineage (GRW4). A new, publicly available portal (Integroomer) was developed for initial parsing of 454 datasets. Mean variant prevalence and frequency was higher in low elevation Hawaii Amakihi (Hemignathus virens) with Avipoxvirus-like lesions (P = 0·001), suggesting that the variants may be biologically distinct. By contrast, variant prevalence and frequency did not differ significantly among mid-elevation Apapane (Himatione sanguinea) with or without lesions (P = 0·691). The low frequency and the lack of detection of variants independent of GRW4 suggest that multiple independent introductions of P. relictum to Hawaii are unlikely. Multiple variants may have been introduced in heteroplasmy with GRW4 or exist within the tandem repeat structure of the mitochondrial genome. The discovery of multiple mitochondrial lineages of P. relictum in Hawaii provides a measure of genetic diversity within a geographically isolated population of this parasite and suggests the origins and evolution of parasite diversity may be more complicated than previously recognized.

The adaptive radiation of the Hawaiian honeycreepers is the largest ever recorded for birds on an oceanic archipelago. Despite including >50 species in 21 genera, no hybridizations across honeycreeper species have ever been confirmed. Here, we report genetic and morphological analyses that verify the first hybrid between two Hawaiian honeycreeper species: the 'I'iwi (Vestiaria coccinea) and 'Apapane (Himatione sanguinea). This hybridization is notable given that the parental species diverged ∼1.6 mya and show distinct morphological differences. Further, this discovery is important in light of recent evidence that hybridization plays an important role in speciation and genetic diversity in both plants and animals.

We used behavioral, physiological, and parasitological measures to document effects of acute malarial infections on activity budgets of experimentally infected juvenile Apapane (Himatione sanguinea). Five of eight birds died within 20 to 32 days after exposure to a single infective mosquito bite. Infected Apapane devoted less time to locomotory activities involving flight, walking or hopping, and stationary activities such as singing, preening, feeding, and probing. The amount of time spent sitting was positively correlated with parasitemia and increased dramatically after infection and between treatment and control groups. Birds that succumbed to infection experienced a significant loss of body mass and subcutaneous fat, whereas surviving Apapane were better able to maintain body condition and fat levels. When rechallenged with the parasite five months after initial infection, surviving birds experienced no increase in parasitemia, indicating that they had become immune to reinfection. Regardless of the outcome, infected birds experienced acute illness that would have left them unable to forage or to escape from predators in the wild.

Modeling the spatial distribution of animals can be complicated by spatial and temporal effects (i.e. spatial autocorrelation and trends in abundance over time) and other factors such as imperfect detection probabilities and observation-related nuisance variables. Recent advances in modeling have demonstrated various approaches that handle most of these factors but which require a degree of sampling effort (e.g. replication) not available to many field studies. We present a two-step approach that addresses these challenges to spatially model species abundance. Habitat, spatial and temporal variables were handled with a Bayesian approach which facilitated modeling hierarchically structured data. Predicted abundance was subsequently adjusted to account for imperfect detection and the area effectively sampled for each species. We provide examples of our modeling approach for two endemic Hawaiian nectarivorous honeycreepers: 'i'iwi Vestiaria coccinea and 'apapane Himatione sanguinea.

The application of molecular techniques to conservation genetics issues can provide important guidance criteria for management of endangered species. The results from this study establish that PCR-based approaches for sex determination developed in other bird species (Griffiths and Tiwari 1995; Griffiths et al. 1996, 1998; Ellegren 1996) can be applied with a high degree of confidence to at least four species of Hawaiian honeycreepers. This provides a rapid, reliable method with which population managers can optimize sex ratios within populations of endangered species that are subject to artificial manipulation through captive breeding programmes or geographic translocation.