Honeycreepers Research Articles

The Role of Geography, Diet, and Host Phylogeny on the Gut Microbiome in the Hawaiian Honeycreeper Radiation.

The animal gut microbiome can have a strong influence on the health, fitness, and behavior of its hosts. The composition of the gut microbial community can be influenced by factors such as diet, environment, and evolutionary history (phylosymbiosis). However, the relative influence of these factors is unknown in most bird species. Furthermore, phylosymbiosis studies have largely focused on clades that diverged tens of millions of years ago, and little is known about the degree of gut microbiome divergence in more recent species radiations. This study explores the drivers of microbiome variation across the unique and recent Hawaiian honeycreeper radiation (Fringillidae: Drepanidinae). Fecal samples were collected from 14 extant species spanning the main islands of the Hawaiian archipelago and were sequenced using three metabarcoding markers to characterize the gut microbiome, invertebrate diet, and plant diet of Hawaiian honeycreepers. We then used these metabarcoding data and the honeycreeper host phylogeny to evaluate their relative roles in shaping the gut microbiome. Microbiome variation across birds was highly individualized; however, source island had a small but significant effect on microbiome structure. The microbiomes did not recapitulate the host phylogenetic tree, indicating that evolutionary history does not strongly influence microbiome structure in the honeycreeper clade. These results expand our understanding of the roles of diet, geography, and phylogeny on avian microbiome structure, while also providing important ecological information about the diet and gut microbiota of wild Hawaiian honeycreepers.

Environmental and geographical factors influence the occurrence and abundance of the southern house mosquito, Culex quinquefasciatus, in Hawai‘i

Hawaiian honeycreepers, a group of endemic Hawaiian forest birds, are being threatened by avian malaria, a non-native disease that is driving honeycreepers populations to extinction. Avian malaria is caused by the parasite Plasmodium relictum, which is transmitted by the invasive mosquito Culex quinquefasciatus. Environmental and geographical factors play an important role in shaping mosquito-borne disease transmission dynamics through their influence on the distribution and abundance of mosquitoes. We assessed the effects of environmental (temperature, precipitation), geographic (site, elevation, distance to anthropogenic features), and trap type (CDC light trap, CDC gravid trap) factors on mosquito occurrence and abundance. Occurrence was analyzed using classification and regression tree models (CART) and generalized linear models (GLM); abundance (count data) was analyzed using generalized linear mixed models (GLMMs). Models predicted highest mosquito occurrence at mid-elevation sites and between July and November. Occurrence increased with temperature and precipitation up to 580 mm. For abundance, the best model was a zero-inflated negative-binomial model that indicated higher abundance of mosquitoes at mid-elevation sites and peak abundance between August and October. Estimation of occurrence and abundance as well as understanding the factors that influence them are key for mosquito control, which may reduce the risk of forest bird extinction.

Beak morphometry and morphogenesis across avian radiations.

Adaptive avian radiations associated with the diversification of bird beaks into a multitude of forms enabling different functions are exemplified by Darwin's finches and Hawaiian honeycreepers. To elucidate the nature of these radiations, we quantified beak shape and skull shape using a variety of geometric measures that allowed us to collapse the variability of beak shape into a minimal set of geometric parameters. Furthermore, we find that just two measures of beak shape-the ratio of the width to length and the normalized sharpening rate (increase in the transverse beak curvature near the tip relative to that at the base of the beak)-are strongly correlated with diet. Finally, by considering how transverse sections to the beak centreline evolve with distance from the tip, we show that a simple geometry-driven growth law termed 'modified mean curvature flow' captures the beak shapes of Darwin's finches and Hawaiian honeycreepers. A surprising consequence of the simple growth law is that beak shapes that are not allowed based on the developmental programme of the beak are also not observed in nature, suggesting a link between evolutionary morphology and development in terms of growth-driven developmental constraints.

High resolution lidar data shed light on inter-island translocation of endangered bird species in the Hawaiian Islands.

Translocation, often a management solution reserved for at-risk species, is a highly time-sensitive intervention in the face of a rapidly changing climate. The definition of abiotic and biotic habitat requirements is essential to the selection of appropriate release sites in novel environments. However, field-based approaches to gathering this information are often too time intensive, especially in areas of complex topography where common, coarse-scale climate models lack essential details. We apply a fine-scale remote sensing-based approach to study the 'akikiki (Oreomystis bairdi) and 'akeke'e (Loxops caeruleirostris), Hawaiian honeycreepers endemic to Kaua'i that are experiencing large-scale population declines due to warming-induced spread of invasive disease. We use habitat suitability modeling based on fine-scale light detection and ranging (lidar)-derived habitat structure metrics to refine coarse climate ranges for these species in candidate translocation areas on Maui. We found that canopy density was consistently the most important variable in defining habitat suitability for the two Kaua'i species. Our models also corroborated known habitat preferences and behavioral information for these species that are essential for informing translocation. We estimated a nesting habitat that will persist under future climate conditions on east Maui of 23.43 km2 for 'akikiki, compared to the current Kaua'i range of 13.09 km2 . In contrast, the novel nesting range for 'akeke'e in east Maui was smaller than its current range on Kaua'i (26.29 vs. 38.48 km2 , respectively). We were also able to assess detailed novel competitive interactions at a fine scale using models of three endemic Maui species of conservation concern: 'ākohekohe (Palmeria dolei), Maui 'alauahio (Paroreomyza montana), and kiwikiu (Pseudonestor xanthophrys). Weighted overlap areas between the species from both islands were moderate (<12 km2 ), and correlations between Maui and Kaua'i bird habitat were generally low, indicating limited potential for competition. Results indicate that translocation to east Maui could be a viable option for 'akikiki but would be more uncertain for 'akeke'e. Our novel multifaceted approach allows for the timely analysis of both climate and vegetation structure at informative scales for the effective selection of appropriate translocation sites for at-risk species.

Designing a mate choice program: Tactics trialed and lessons learned with the critically endangered honeycreeper, 'akikiki (Oreomystis bairdi)

AbstractPractitioners have increasingly turned to conservation breeding to address species extinction. Breeding programs aim to maximize genetic diversity, but often genetic pairings are behaviorally incompatible, which can compromise offspring production. Allowing animals to choose their own mate can improve compatibility and increase the number and quality of offspring produced. However, designing mate choice protocols can be challenging when dealing with endangered species where little is known about their reproductive biology and behavior. We present the first experimental attempt to develop a mate‐choice program for the endangered Hawaiian honeycreeper, the 'akikiki (Oreomystis bairdi). We aimed to determine (1) which behaviors predict preference, (2) how best to observe preference, and (3) whether preference predicts successful socialization, nest building and egg production. We gave each female a choice between two males and assessed preference over multiple observations. Each female was then paired with a preferred or a nonpreferred male and their breeding outcomes were tracked. 'Akikiki paired with a preferred mate were more likely to lay eggs and had more eggs per clutch. We identify the optimal length, number, and complexity of observations for determining preference, thereby balancing the time investment of staff, while maximizing the potential reproductive output of the program.

Gene expression reveals immune response strategies of naïve Hawaiian honeycreepers experimentally infected with introduced avian malaria.

The unprecedented rise in the number of new and emerging infectious diseases in the last quarter century poses direct threats to human and wildlife health. The introduction to the Hawaiian archipelago of Plasmodium relictum and the mosquito vector that transmits the parasite has led to dramatic losses in endemic Hawaiian forest bird species. Understanding how mechanisms of disease immunity to avian malaria may evolve is critical as climate change facilitates increased disease transmission to high elevation habitats where malaria transmission has historically been low and the majority of the remaining extant Hawaiian forest bird species now reside. Here, we compare the transcriptomic profiles of highly susceptible Hawai'i 'amakihi (Chlorodrepanis virens) experimentally infected with P. relictum to those of uninfected control birds from a naïve high elevation population. We examined changes in gene expression profiles at different stages of infection to provide an in-depth characterization of the molecular pathways contributing to survival or mortality in these birds. We show that the timing and magnitude of the innate and adaptive immune response differed substantially between individuals that survived and those that succumbed to infection, and likely contributed to the observed variation in survival. These results lay the foundation for developing gene-based conservation strategies for Hawaiian honeycreepers by identifying candidate genes and cellular pathways involved in the pathogen response that correlate with a bird's ability to recover from malaria infection.

Microbiomes associated with avian malaria survival differ between susceptible Hawaiian honeycreepers and sympatric malaria-resistant introduced birds.

Of the estimated 55 Hawaiian honeycreepers (subfamily Carduelinae) only 17 species remain, nine of which the International Union for Conservation of Nature considers endangered. Among the most pressing threats to honeycreeper survival is avian malaria, caused by the introduced blood parasite Plasmodium relictum, which is increasing in distribution in Hawai'i as a result of climate change. Preventing further honeycreeper decline will require innovative conservation strategies that confront malaria from multiple angles. Research on mammals has revealed strong connections between gut microbiome composition and malaria susceptibility, illuminating a potential novel approach to malaria control through the manipulation of gut microbiota. One honeycreeper species, Hawai'i 'amakihi (Chlorodrepanis virens), persists in areas of high malaria prevalence, indicating they have acquired some level of immunity. To investigate if avian host-specific microbes may be associated with malaria survival, we characterized cloacal microbiomes and malaria infection for 174 'amakihi and 172 malaria-resistant warbling white-eyes (Zosterops japonicus) from Hawai'i Island using 16S rRNA gene metabarcoding and quantitative polymerase chain reaction. Neither microbial alpha nor beta diversity covaried with infection, but 149 microbes showed positive associations with malaria survivors. Among these were Escherichia and Lactobacillus spp., which appear to mitigate malaria severity in mammalian hosts, revealing promising candidates for future probiotic research for augmenting malaria immunity in sensitive endangered species.

Transcriptional response of individual Hawaiian Culex quinquefasciatus mosquitoes to the avian malaria parasite Plasmodium relictum

BackgroundPlasmodium parasites that cause bird malaria occur in all continents except Antarctica and are primarily transmitted by mosquitoes in the genus Culex. Culex quinquefasciatus, the mosquito vector of avian malaria in Hawaiʻi, became established in the islands in the 1820s. While the deadly effects of malaria on endemic bird species have been documented for many decades, vector-parasite interactions in avian malaria systems are relatively understudied.MethodsTo evaluate the gene expression response of mosquitoes exposed to a Plasmodium infection intensity known to occur naturally in Hawaiʻi, offspring of wild-collected Hawaiian Cx. quinquefasciatus were fed on a domestic canary infected with a fresh isolate of Plasmodium relictum GRW4 from a wild-caught Hawaiian honeycreeper. Control mosquitoes were fed on an uninfected canary. Transcriptomes of five infected and three uninfected individual mosquitoes were sequenced at each of three stages of the parasite life cycle: 24 h post feeding (hpf) during ookinete invasion; 5 days post feeding (dpf) when oocysts are developing; 10 dpf when sporozoites are released and invade the salivary glands.ResultsDifferential gene expression analyses showed that during ookinete invasion (24 hpf), genes related to oxidoreductase activity and galactose catabolism had lower expression levels in infected mosquitoes compared to controls. Oocyst development (5 dpf) was associated with reduced expression of a gene with a predicted innate immune function. At 10 dpf, infected mosquitoes had reduced expression levels of a serine protease inhibitor, and further studies should assess its role as a Plasmodium agonist in C. quinquefasciatus. Overall, the differential gene expression response of Hawaiian Culex exposed to a Plasmodium infection intensity known to occur naturally in Hawaiʻi was low, but more pronounced during ookinete invasion.ConclusionsThis is the first analysis of the transcriptional responses of vectors to malaria parasites in non-mammalian systems. Interestingly, few similarities were found between the response of Culex infected with a bird Plasmodium and those reported in Anopheles infected with human Plasmodium. The relatively small transcriptional changes observed in mosquito genes related to immune response and nutrient metabolism support conclusions of low fitness costs often documented in experimental challenges of Culex with avian Plasmodium.

Wild gut microbiomes reveal individuals, species, and location as drivers of variation in two critically endangered Hawaiian honeycreepers.

BackgroundThe gut microbiome of animals is an important component that has strong influence on the health, fitness, and behavior of its host. Most research in the microbiome field has focused on human populations and commercially important species. However, researchers are now considering the link between endangered species conservation and the microbiome. In Hawaiʻi, several threats (e.g., avian malaria and habitat loss) have caused widespread population declines of Hawaiian honeycreepers (subfamily: Carduelinae). These threats can have a significant effect on the avian gut microbiome and may even lead to disruption of microbial function. However, the gut microbiome of honeycreeper in the wild has yet to be explored.MethodsWe collected 13 and 42 fecal samples, respectively, from two critically endangered honeycreeper species, the ʻakikiki (Oreomystis bairdi) and the ʻakekeʻe (Loxops caeruleirostris). The 16S rRNA gene was sequenced and processed though a MOTHUR-based bioinformatics pipeline. Bacterial ASVs were identified using the DADA2 program and bacterial community analyses, including alpha and beta diversity measures, were conducted using R packages Phyloseq and vegan.ResultsA total of 8,958 bacterial ASVs were identified from the fecal samples. Intraspecific differences in the gut microbiome among individual birds explained most of the variation present in the dataset, however differences between species did exist. Both species had distinct microbiomes with minimal overlap in beta diversity. ‘Akikiki had a more diverse microbiome compared to ‘akekeʻe. Additionally, small but stastically significant differences in beta diversity also exist between sampling location and sexes in ʻakikiki.ConclusionʻAkikiki and ʻakekeʻe are currently the focus of captive breeding efforts and plans to translocate the two species to other islands are underway. This baseline knowledge will help inform management decisions for these honeycreeper species in their native habitats, on other islands, and in captivity.

Variation in immunity and health in response to introduced avian malaria in an endemic Hawaiian songbird

AbstractEmerging infectious diseases are spreading at unprecedented rates and affecting wildlife worldwide, with particularly strong effects on islands. Since the introduction of avian malaria to Hawaii a century ago, the disease has contributed to the decline and extinction of several endemic Hawaiian honeycreeper species. At low elevation, where avian malaria is prevalent, Hawaii Amakihi Chlorodrepanis virens honeycreeper populations have experienced strong selection by the disease and have evolved increased malaria resilience, the ability to recover from infection. The goals of this study were to describe malaria infection rates across Hawaii Island, to examine the role of innate immunity in malaria resilience, and to determine the effects of resilience and chronic infection on Amakihi health. We measured malaria infection and metrics of innate immunity and health in low elevation Amakihi populations, which are more resilient to malaria, and high elevation populations, which have experienced weak malaria selection and are less resilient to malaria. Avian malaria infection was higher at low than high elevation. Measures of innate immunity were higher in low than high elevation Amakihi, but also depended on whether the birds were from the leeward side of the island (low rainfall) or windward side of the island (high rainfall) and whether they were free‐living or captive. Regarding measures of health, body condition was better in malaria‐infected than uninfected Amakihi, while hematocrit did not vary by malaria infection but was higher in high than low elevation birds. These are among the first results to describe variation in immunity and health according to avian malaria selection and infection in Hawaiian honeycreepers. Understanding the impacts of introduced diseases on island species, which are particularly susceptible to novel pathogens, will provide critical insight into how introduced disease may affect endangered species.

Individual and seasonal variation in the movement behavior of two tropical nectarivorous birds

BackgroundMovement of animals directly affects individual fitness, yet fine spatial and temporal resolution movement behavior has been studied in relatively few small species, particularly in the tropics. Nectarivorous Hawaiian honeycreepers are believed to be highly mobile throughout the year, but their fine-scale movement patterns remain unknown. The movement behavior of these crucial pollinators has important implications for forest ecology, and for mortality from avian malaria (Plasmodium relictum), an introduced disease that does not occur in high-elevation forests where Hawaiian honeycreepers primarily breed.MethodsWe used an automated radio telemetry network to track the movement of two Hawaiian honeycreeper species, the ʻapapane (Himatione sanguinea) and ʻiʻiwi (Drepanis coccinea). We collected high temporal and spatial resolution data across the annual cycle. We identified movement strategies using a multivariate analysis of movement metrics and assessed seasonal changes in movement behavior.ResultsBoth species exhibited multiple movement strategies including sedentary, central place foraging, commuting, and nomadism , and these movement strategies occurred simultaneously across the population. We observed a high degree of intraspecific variability at the individual and population level. The timing of the movement strategies corresponded well with regional bloom patterns of ‘ōhi‘a (Metrosideros polymorpha) the primary nectar source for the focal species. Birds made long-distance flights, including multi-day forays outside the tracking array, but exhibited a high degree of fidelity to a core use area, even in the non-breeding period. Both species visited elevations where avian malaria can occur but exhibited little seasonal change in elevation (< 150 m) and regularly returned to high-elevation roosts at night.ConclusionsThis study demonstrates the power of automated telemetry to study complex and fine-scale movement behaviors in rugged tropical environments. Our work reveals a system in which birds can track shifting resources using a diverse set of movement behaviors and can facultatively respond to environmental change. Importantly, fidelity to high-elevation roosting sites minimizes nocturnal exposure to avian malaria for far-ranging individuals and is thus a beneficial behavior that may be under high selection pressure.

Population estimates and trends of three Maui Island‐endemic Hawaiian Honeycreepers

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Divergent movement patterns of adult and juvenile ‘Akohekohe, an endangered Hawaiian Honeycreeper

The movement patterns of birds across a landscape are often highly variable and influenced by complex interactions between individuals and environments. Because periods of movement can be marked by high mortality, especially among juvenile birds, understanding these patterns may be vital for the conservation of many bird species. However, these patterns can be challenging to quantify. We used radio-telemetry to document the movement patterns of ‘Akohekohe (Palmeria dolei), an endangered Hawaiian Honeycreeper endemic to Maui Island, Hawai'i. This species is believed to be highly susceptible to mosquito-transmitted avian malaria (Plasmodium relictum) and only breeds in high-elevation wet forests on the windward side of east Maui (> 1715 m) that serve as mosquito-free refugia. Over a 2-yr period (2013–2014), we used radio-telemetry and resightings of color-banded birds to track the movements of juveniles (N = 11) and adults (N = 24) and quantified home ranges with minimum convex polygons (MCP) and 95% fixed kernels (KHR). Movement patterns and home range sizes of adult and juvenile ‘Akohekohe were significantly different, with adults having relatively small home ranges (0.57 ha, MCP; 1.09 ha, KHR) and juveniles moving greater distances and having larger home ranges (25.02 ha, MCP; 90.56 ha, KHR). Only juveniles moved into lower-elevation forests that can support mosquito populations, at least seasonally. The absence of adults in this transitional malaria zone suggests that adult ‘Akohekohe cannot maintain long-term home ranges in areas with an increased risk of malaria infection. In addition, the long-distance movements of juveniles during the post-fledging, pre-breeding period likely increases their risk of contracting avian malaria and could be a key factor limiting the population of this species. Patrones de movimiento divergentes de adultos y juveniles Akohekohe, un mielero hawaiano en peligro de extinción Los patrones de movimiento de las aves en un paisaje a menudo son muy variables y están influenciados por interacciones complejas entre individuos y entornos. Debido a que los períodos de movimiento pueden estar marcados por una alta mortalidad, especialmente entre las aves juveniles, comprender estos patrones puede ser vital para la conservación de muchas especies de aves. Sin embargo, estos patrones pueden ser difíciles de cuantificar. Usamos radiotelemetría para documentar los patrones de movimiento del Akohekohe (Palmeria dolei), un mielero endémica hawaiano en peligro de extinción de la isla de Maui, Hawaii. Se cree que esta especie es muy susceptible a la malaria aviar transmitida por mosquitos (Plasmodium relictum) y solo se reproduce en bosques húmedos de gran altura en el lado de barlovento del este de Maui (> 1715 m) que sirven como refugio libre de mosquitos. Durante un período de dos años (2013–2014), utilizamos radiotelemetría y avistamientos de aves con bandas de colores para rastrear los movimientos de juveniles (N = 11) y adultos (N = 24) y cuantificamos los rangos de hogar con polígonos convexos mínimos (MCP) y 95% de granos fijos (KHR). Los patrones de movimiento y los tamaños del área de distribución de adultos y juveniles Akohekohe fueron significativamente diferentes, con adultos que tenían áreas de distribución relativamente pequeñas (0.57 ha, MCP; 1.09 ha, KHR) y juveniles moviéndose distancias mayores y teniendo rangos de hogar más grandes (25.02 ha, MCP; 90.56 ha, KHR). Solo los juveniles se trasladaron a bosques de menor elevación que pueden sustentar las poblaciones de mosquitos, al menos estacionalmente. La ausencia de adultos en esta zona de transición de la malaria sugiere que los adultos de Akohekohe no pueden mantener áreas de distribución a largo plazo en áreas con un mayor riesgo de infección por malaria. Además, los movimientos a larga distancia de los juveniles, durante el período posterior al emplumado y antes de la reproducción, probablemente aumentan el riesgo de contraer malaria aviar y podrían ser un factor clave que limita la población de esta especie. Appendix S1. Ohia flowering phenology. Table S1. Banding and resighting information for 35 `Akohekohe tracked in Waikamoi Preserve, Maui, in 2013 and 2014. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.

Stable isotope analysis of multiple tissues from Hawaiian honeycreepers indicates elevational movement.

We have limited knowledge of the patterns, causes, and prevalence of elevational migration despite observations of seasonal movements of animals along elevational gradients in montane systems worldwide. While a third of extant Hawaiian landbird species are estimated to be elevational migrants this assumption is based primarily on early naturalist's observations with limited empirical evidence. In this study, we compared stable hydrogen isotopes (δ2H) of metabolically inert (feathers) and active (blood plasma, red blood cells) tissues collected from the same individual to determine if present day populations of Hawaiian honeycreepers undergo elevational movements to track areas of seasonally high flower bloom that constitute significant food resources. We also measured stable carbon isotopes (δ13C) and stable nitrogen isotopes (δ15N) to examine potential changes in diet between time periods. We found that the majority of 'apapane (Himatione sanguinea) and Hawai'i 'amakihi (Chlorodrepanis virens) captured at high elevation, high bloom flowering sites in the fall were not year-round residents at the capture locations, but had molted their feathers at lower elevations presumably in the summer after breeding. δ2H values of feathers for all individuals sampled were higher than blood plasma isotope values after accounting for differences in tissue-specific discrimination. We did not find a difference in the propensity of elevational movement between 'apapane and Hawai'i 'amakihi, even though the 'amakihi is considered more sedentary. However, consistent with a more generalist diet, δ15N values indicated that Hawai'i 'amakihi had a more diverse diet across trophic levels than 'apapane, and a greater reliance on nectar in the fall. We demonstrate that collecting multiple tissue samples, which grow at different rates or time periods, from a single individual can provide insights into elevational movements of Hawaiian honeycreepers over an extended time period.

Fostering real-time climate adaptation: Analyzing past, current, and forecast temperature to understand the dynamic risk to Hawaiian honeycreepers from avian malaria

Various vector control options are increasingly being considered to safeguard forest birds in their natural habitats from avian malaria transmission. However, vector control options require localized deployment that is not logistically, ethically, ecologically, nor economically viable everywhere and all the time. Based on thermal tolerances of the sporogonic stages of avian malaria (Plasmodium relictum) parasite and its vector, the southern house mosquito (Culex quinquefasciatus), we examined the long-term weather trends for three high value, forest bird refuges (Alakai Wilderness Preserve on Kaua’i, Hanawi Natural Area Reserve on Maui, and Hakalau Forest National Wildlife Refuge on Hawai’i Island) to understand the temporal and site-specific differences of temperature-driven suitability for localized avian malaria transmission.On average, Alakai had mean ambient temperatures suitable for both the vector’s immature stage development and parasite sporogonic development most of the time (85.3%), indicating that observed variability in vector abundance or disease transmission may be driven by other factors. At higher elevation sites like Hakalau and Hanawi, current mean ambient temperatures suitable only for vector development prevail (91.7% and 96.6%, respectively), while mean ambient temperatures for both vector and parasite sporogonic development seldom occur (4.4% and 0% respectively). Our results not only show differences in the temperature suitability for transmission across elevation, but also different levels of vulnerability to avian malaria transmission with any additional projected increase in temperature. For instance, under a conservative warming scenario of 1.0 °C, the joint temperature suitability of parasite and vector development increases at higher elevation sites such as Hakalau (+35.8%) and Hanawi (+15.4%). While mean ambient temperatures suitable for both vector and parasite development already occur most of the time at Alakai, the occurrence also increases (+8.4%) as well under this conservative warming scenario.By linking current site-specific weather data to real-time weather forecasts, we developed a real-time avian malaria warning system to assist managers in identifying conditions when vector control is most needed at these three selected study sites. This online tool determines when conditions are likely to be suitable for local development of P. relictum and C. quinquefasciatus at Alakai, Hanawi, and Hakalau. This tool illustrates how managers can incorporate climate and current weather patterns into decision making without having to consider the uncertainties of long-term climatic and ecological projections.

The consequences of craniofacial integration for the adaptive radiations of Darwin's finches and Hawaiian honeycreepers.

The diversifications of Darwin's finches and Hawaiian honeycreepers are two text-book examples of adaptive radiation in birds. Why these two bird groups radiated while the remaining endemic birds in these two archipelagos exhibit relatively low diversity and disparity remains unexplained. Ecological factors have failed to provide a convincing answer to this phenomenon, and some intrinsic causes connected to craniofacial evolution have been hypothesized. The tight coevolution of the beak and the remainder of the skull in diurnal raptors and parrots suggests that integration may be the prevalent condition in landbirds (Inopinaves). This is in contrast with the archetypal relationship between beak shape and ecology in Darwin's finches and Hawaiian honeycreepers, which suggests that the beak can adapt as a distinct module in these birds. Modularity has therefore been proposed to underpin the adaptive radiation of these groups, allowing the beak to evolve more rapidly and freely in response to ecological opportunity. Here, using geometric morphometrics and phylogenetic comparative methods in a broad sample of landbird skulls, we show that craniofacial evolution in Darwin's finches and Hawaiian honeycreepers seems to be characterized by a tighter coevolution of the beak and the rest of the skull (cranial integration) than in most landbird lineages, with rapid and extreme morphological evolution of both skull regions along constrained directions of phenotypic space. These patterns are unique among landbirds, including other sympatric island radiations, and therefore counter previous hypotheses by showing that tighter cranial integration, not only modularity, can facilitate evolution along adaptive directions.

Facilitated adaptation for conservation – Can gene editing save Hawaii's endangered birds from climate driven avian malaria?

Avian malaria has played a significant role in causing extinctions, population declines, and limiting the elevational distribution of Hawaiian honeycreepers. Most threatened and endangered honeycreepers only exist in high-elevation forests where the risk of malaria infection is limited. Because Culex mosquito vectors and avian malaria dynamics are strongly influenced by temperature and rainfall, future climate change is predicted to expand malaria infection to high-elevation forests and intensify malaria infection at lower elevations, likely resulting in future extinctions and loss of avian biodiversity in Hawaii. Novel, landscape-level mosquito control strategies are promising, but are logistically challenging and require costly long-term efforts. As an alternative or supplemental strategy, we evaluated the potential of releasing a gene-edited malaria-resistant honeycreeper (Iiwi, Drepanis coccinea) in Hawaiian rainforests; a strategy known as facilitated adaptation. While this approach also has significant technical challenges and costs, it may offer a more permanent solution to increasing malaria threats. If malaria-resistant honeycreepers can be developed, facilitated adaptation may provide a practical strategy for the reestablishment of abundant avian populations in Hawaiian forests. A successful strategy could be the release of malaria-resistant Iiwi in mid-elevation forests where development of a resistant population has the best chance of success. Establishment of a resistant Iiwi population could provide a source for dispersal and development of resistant populations in high-elevation forests and a permanent source of resistant individuals for translocation to other vulnerable areas.

Modeling the population impacts of avian malaria on Hawaiian honeycreepers: Bifurcation analysis and implications for conservation

Avian malaria is a mosquito-borne parasitic disease of birds caused by protists of the genera Plasmodium, most notably Plasmodium relictum. This disease has been identified as a primary cause of the drastic decline and extinctions of birds, in particular Hawaiian honeycreepers (Drepanidinae), where rates of mortality may exceed 90%. We formulate an epizootiological model of the transmission dynamics of avian malaria between populations of bird hosts and mosquito vectors using a system of compartmental ordinary differential equations. We derive the basic reproduction number as well as criteria for the existence and local stability of disease-free and enzootic equilibria. These results provide useful information for evaluating management strategies. A local sensitivity analysis of certain model invariants to uncertain parameter values is performed to ascertain which biological factors have the largest impact on ecological outcomes and, in particular, long-term bird population densities. We discuss and compare the effectiveness of two disease control and conservation strategies: captive propagation of honeycreepers and larval mosquito habitat reduction. We provide examples of combinations of these strategies that either are predicted to eliminate enzootic avian malaria or to increase predicted bird density above a given ecologically meaningful threshold.

Loss of cultural song diversity and the convergence of songs in a declining Hawaiian forest bird community.

The effects of population decline on culturally transmitted behaviours in animals have rarely been described, but may have major implications to population viability. Learned vocal signals in birds are of critical importance to behaviours associated with reproduction, intrasexual interactions and group cohesion, and the complexity of vocal signals such as song can serve as an honest signal of an individual's quality as well as the viability of a population. In this study, we examined how rapid population declines recently experienced by Hawaiian honeycreepers on the island of Kaua‘i (USA) may have influenced the diversity, complexity and similarity of learned honeycreeper songs. We analysed the acoustic characteristics of songs recorded during three time periods over a 40-year time frame for three species of declining Kaua‘i honeycreepers. We detected a loss of song complexity and diversity over the 40-year time period that paralleled dramatic population declines. Concurrent with the loss of complexity, we also found that the acoustic characteristics of the three honeycreepers' songs became more similar to one another. To our knowledge, this is the first documentation of convergence of acoustic characteristics among rapidly declining species. The reduction in song complexity and diversity and convergence of songs not only signals a loss of culturally transmitted behaviours in these endemic Hawaiian honeycreepers, but also potential challenges to the recovery of these rapidly declining species. Moreover, the present study highlights that there is a ‘hidden’ cost to declining populations beyond just the loss of individuals that is not often considered, the loss of culturally transmitted social behaviours.

Large-scale tree mortality from Rapid Ohia Death negatively influences avifauna in lower Puna, Hawaii Island, USA

Abstract ‘Ōhi’a lehua (Metrosideros polymorpha) is the principle tree species in forests across the Hawaiian Islands and provides critical foraging and nesting habitat for native passerines. Rapid Ohia Death (ROD), caused by the vascular wilt fungus Ceratocystis lukuohia and the canker pathogen C. huliohia, was first detected in the Puna District of Hawaii Island in 2010. It affects all life stages of ‘ōhi’a and as of July 2018 had spread to an estimated 40,469 ha across Hawaii Island. To determine the impact of ROD on the forest bird community we conducted point counts in lowland ‘ōhi’a forest in 2016 and compared them to counts from 2003 to 2004, before the appearance of ROD. We found an increase in species diversity and a significant decrease in the densities of a native Hawaiian honeycreeper, the Hawaii Amakihi (Chlorodrepanus virens), and the nonnative Japanese White-eye (Zosterops japonicus). Yellow-fronted Canary (Crithagra mozambica) and Saffron Finch (Sicalis flaveola), 2 nonnative passerines associated with the shrub layer and more open habitats, were only detected in 2016. Proportion of survey points occupied were comparable between survey periods, but relative abundances were generally lower. Hawaii Amakihi densities declined by 79% and Japanese White-eye densities declined by 33%. Our findings suggest that the loss of ‘ōhi’a canopy due primarily to ROD has adversely affected populations of native Hawaii Amakihi and nonnative Japanese White-eye, 2 of the most abundant species of lowland Hawaiian forests.