Abstract
Forested landscapes containing eastern hemlock (Tsuga canadensis) are under threat by the invasive hemlock woolly adelgid (Adelges tsugae) in eastern North America. Although several studies have shown the negative effects of adelgid invasion in local bird communities, its regional impacts have not yet been quantified. Using broad-scale spatial (eastern US hemlock range) and temporal (> 40 years of bird data) databases, we built spatial auto-regressive generalized mixed linear models to estimate the effects of adelgid infestation on fourteen bird species’ demographic trends. We also evaluated how winter temperature mediates the relationship between infestation and bird trends. We selected the best models using WAIC and validated model performance and power using Monte Carlo simulation, permutation tests, and sensitivity analysis. The best model for all but one species included the effects of adelgid infestation on abundance trends. We observed a > 30% decline for two hemlock-associate species after infestation: the Blackburnian warbler, and the Hermit thrush. In contrast, no control species showed similar declines. When evaluated at a broad spatiotemporal scale, hemlock associates also decline in abundance following infestation. At the same time, declines are not as universal compared to local studies, suggesting that spatial heterogeneity might buffer them. Declines were greater in the warmest part of species ranges. Rising temperatures due to climate change will likely affect bird persistence even further by lowering adelgid overwinter mortality. Despite the difficulties of understanding and connecting landscape-scale processes with those at finer scales, it is critical to evaluate biodiversity distribution from a regional perspective.
Resumen
Los paisajes forestales que contienen la cicuta oriental (Tsuga canadensis) en el este de América del Norte están amenazados por la invasión del adelgido lanudo de cicuta (Adelges tsugae). Aunque varios estudios han mostrado los efectos negativos de la invasión del adelgido en las comunidades locales de aves, sus impactos regionales aún no han sido cuantificados. Utilizando bases de datos espaciales a gran escala (área de distribución del adelgido en el este de los Estados Unidos) y temporales (> 40 años de datos de aves), construimos modelos lineales mixtos generalizados autorregresivos espaciales para estimar los efectos de la infestación del adelgido lanudo de cicuta en las tendencias demográficas de catorce especies de aves. También evaluamos cómo la temperatura invernal media la relación entre la infestación y las tendencias de las poblaciones de aves. Seleccionamos los mejores modelos utilizando WAIC y validamos el rendimiento y la potencia del modelo utilizando simulación de Monte Carlo, pruebas de permutación y análisis de sensibilidad. El mejor modelo para todas las especies, excepto una, incluyó los efectos de la infestación del adelgido en las tendencias de abundancia. Observamos una disminución de más del 30% en dos especies asociadas al abeto después de la infestación: la reinita gorjinaranja y el zorzalito colirrufo. En contraste, ninguna de las especies control mostró disminuciones similares. Cuando evaluadas a una escala espaciotemporal amplia, las especies asociadas al adelgido también disminuyeron en abundancia después de la infestación. Al mismo tiempo, las disminuciones no son tan universales en comparación con los estudios locales, lo que sugiere que la heterogeneidad espacial podría amortiguarlas. Las disminuciones fueron mayores en la parte más cálida de las áreas de distribución de las especies. El aumento de las temperaturas debido al cambio climático probablemente afectará aún más la persistencia de las aves al reducir la mortalidad invernal del adelgido. A pesar de las dificultades para comprender y conectar los procesos a escala de paisaje con los de escala más fina, es fundamental evaluar la distribución de la biodiversidad desde una perspectiva regional.
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Data Accessibility
All the bird and hemlock woolly adelgid invasion data are publicly available. BBS data were downloaded as a.csv file (https://www.pwrc.usgs.gov/bbs/rawdata/), adelgid infestation shape files were requested to the USDA Forest Service, and temperature data from WorldClim were downloaded using the R package ‘raster’ (version 3.4–13). The R codes used for the analyses are openly available on GitHub (https://github.com/br-amaral/BirdHWA).
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Acknowledgements
We thank M. Marshall and F. Buderman for their comments on drafts of the manuscript, and M. Tingley for the challenging questions about the system and modeling approach. We also thank Ann Steketee from the USFS for the assistance in getting the hemlock wooly adelgid infestation data.
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All authors contributed to the study's conception and design. All authors conceived and designed the analysis, and data preparation and analysis were performed by B. R. Amaral. The first draft of the manuscript was written by B. R. Amaral, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Amaral, B.R., Wilson, A.M., Blum, J. et al. Quantifying regional-scale impacts of hemlock woolly adelgid invasion on North American forest bird communities. Biol Invasions 25, 4009–4025 (2023). https://doi.org/10.1007/s10530-023-03156-7
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DOI: https://doi.org/10.1007/s10530-023-03156-7
Keywords
- Bird population decline
- Climate change
- Hemlock woolly adelgid
- Invasive species
- Adelges tsugae
- Tsuga canadensis