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

Background The 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. Methods We 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. Results A 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. Conclusion ʻAkikiki 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.

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

Background Movement 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. Methods We 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. Results Both 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. Conclusions This 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.

Wild gut microbiomes reveal individuals, species, and location as drivers of variation in two critically endangered tropical birds

The gut microbiome of an animal has a strong influence on the health, fitness, and behavior of its host, and is thus a critical component of the animal itself. 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 have caused widespread population declines of Hawaiian honeycreepers (subfamily Carduelinae). These threats, and the environmental changes that result, can have a significant effect on the avian gut microbiome and may even lead to disruption of microbial function. However, no previous study has explored the natural patterns of the gut microbiome of a honeycreeper species in the wild. This project used amplicon-based sequencing of the 16S rRNA gene to characterize the gut microbiome of two critically endangered species of Hawaiian honeycreepers. The two species differed significantly in both alpha and beta diversity. Intraspecific variation of the gut microbiome among individual birds was a major factor. However, small but significant differences also exist between sampling location and sexes. This baseline knowledge will help inform management decisions for these honeycreeper species both in their native habitats and in captivity.

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.