Cascading effects of earthworm invasion increase graminoid density and rodent grazing intensities.
Lumbricidae
earthworms
grazing
non-native
plant community
soil moisture
tundra
Journal
Ecology
ISSN: 1939-9170
Titre abrégé: Ecology
Pays: United States
ID NLM: 0043541
Informations de publication
Date de publication:
23 Nov 2023
23 Nov 2023
Historique:
revised:
30
08
2023
received:
05
04
2023
accepted:
19
10
2023
pubmed:
24
11
2023
medline:
24
11
2023
entrez:
24
11
2023
Statut:
aheadofprint
Résumé
Human-mediated dispersal of non-native earthworms can cause substantial changes to the functioning and composition of ecosystems previously earthworm-free. Some of these earthworm species have the potential to "geoengineer" soils and increase plant nitrogen (N) uptake. Yet the possible consequences of increased plant N concentrations on rodent grazing remains poorly understood. In this study, we present findings from a common garden experiment with two tundra communities, meadow (forb dominated) and heath (shrub dominated), half of them subjected to 4 years of earthworm presence (Lumbricus spp. and Aporrectodea spp.). Within four summers, our earthworm treatment changed plant community composition by increasing graminoid density by, on average, 94% in the heath vegetation and by 49% in the meadow. Rodent winter grazing was more intense on plants growing in soils with earthworms, an effect that coincided with higher N concentrations in plants, indicating a higher palatability. Even though earthworms reduced soil moisture, plant community productivity, as indicated by vegetation greenness (normalized difference vegetation index), was not negatively impacted. We conclude that earthworm-induced changes in plant composition and trophic interactions may fundamentally alter the functioning of tundra ecosystems.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e4212Subventions
Organisme : Stiftelsen Oscar och Lili Lamms Minne
ID : DO2018-0030
Organisme : Svenska Forskningsrådet Formas
ID : 2018-01312
Informations de copyright
© 2023 The Authors. Ecology published by Wiley Periodicals LLC on behalf of The Ecological Society of America.
Références
Bergeron, J. M., and L. Jodoin. 1987. “Defining “High Quality” Food Resources of Herbivores: The Case for Meadow Voles (Microtus Pennsylvanicus).” Oecologia 71(4): 510-517.
Blouin, M., P. Lavelle, and D. Laffray. 2007. “Drought Stress in Rice (Oryza sativa L.) Is Enhanced in the Presence of the Compacting Earthworm Millsonia Anomala.” Environmental and Experimental Botany 60(3): 352-359. https://doi.org/10.1016/j.envexpbot.2006.12.017.
Blume-Werry, G., E. J. Krab, J. Olofsson, M. K. Sundqvist, M. Väisänen, and J. Klaminder. 2020. “Invasive Earthworms Unlock Arctic Plant Nitrogen Limitation.” Nature Communications 11(1): 1766. https://doi.org/10.1038/s41467-020-15568-3.
Cameron, E. K., J. F. Cahill, Jr., and E. M. Bayne. 2014. “Root Foraging Influences Plant Growth Responses to Earthworm Foraging.” PLoS One 9(9): e108873. https://doi.org/10.1371/journal.pone.0108873.
Craven, D., M. P. Thakur, E. K. Cameron, L. E. Frelich, R. Beauséjour, R. B. Blair, B. Blossey, et al. 2017. “The Unseen Invaders: Introduced Earthworms as Drivers of Change in Plant Communities in North American Forests (A Meta-Analysis).” Global Change Biology 23(3): 1065-1074. https://doi.org/10.1111/gcb.13446.
Dobson, A., and B. Blossey. 2015. “Earthworm Invasion, White-Tailed Deer and Seedling Establishment in Deciduous Forests of North-Eastern North America.” Journal of Ecology 103(1): 153-164. https://doi.org/10.1111/1365-2745.12350.
Dobson, A. M., B. Blossey, and J. B. Richardson. 2017. “Invasive Earthworms Change Nutrient Availability and Uptake by Forest Understory Plants.” Plant and Soil 421(1): 175-190. https://doi.org/10.1007/s11104-017-3412-9.
Drouin, M., R. Bradley, and L. Lapointe. 2016. “Linkage between Exotic Earthworms, Understory Vegetation and Soil Properties in Sugar Maple Forests.” Forest Ecology and Management 364: 113-121. https://doi.org/10.1016/j.foreco.2016.01.010.
Eisenhauer, N., O. Butenschoen, S. Radsick, and S. Scheu. 2010. “Earthworms as Seedling Predators: Importance of Seeds and Seedlings for Earthworm Nutrition.” Soil Biology and Biochemistry 42(8): 1245-1252. https://doi.org/10.1016/j.soilbio.2010.04.012.
Elmendorf, S. C., G. H. R. Henry, R. D. Hollister, R. G. Björk, A. D. Bjorkman, T. V. Callaghan, L. S. Collier, et al. 2012. “Global Assessment of Experimental Climate Warming on Tundra Vegetation: Heterogeneity over Space and Time.” Ecology Letters 15(2): 164-175. https://doi.org/10.1111/j.1461-0248.2011.01716.x.
Ferlian, O., M. P. Thakur, A. Castañeda González, L. M. San Emeterio, S. Marr, B. da Silva Rocha, and N. Eisenhauer. 2020. “Soil Chemistry Turned Upside Down: A Meta-Analysis of Invasive Earthworm Effects on Soil Chemical Properties.” Ecology 101(3). https://doi.org/10.1002/ecy.2936.
Frelich, L. E., B. Blossey, E. K. Cameron, A. Dávalos, N. Eisenhauer, T. Fahey, O. Ferlian, et al. 2019. “Side-Swiped: Ecological Cascades Emanating from Earthworm Invasions.” Frontiers in Ecology and the Environment 17: 502-510. https://doi.org/10.1002/fee.2099.
Goodall, D. W. 1952. “Some Considerations in the Use of Point Quadrats for the Analysis of Vegetation.” Australian Journal of Biological Sciences 5(1): 1-41.
Hartley, S. E., K. Nelson, and M. Gorman. 1995. “The Effect of Fertiliser and Shading on Plant Chemical Composition and Palatability to Orkney Voles Microtus Arvalis Orcadensis.” Oikos 72(1): 79. https://doi.org/10.2307/3546041.
Hendrix, P. F., M. A. Callaham, J. M. Drake, C. Y. Huang, S. W. James, B. A. Snyder, and W. X. Zhang. 2008. “Pandora's Box Contained Bait: The Global Problem of Introduced Earthworms.” Annual Review of Ecology, Evolution, and Systematics 39: 593-613. https://doi.org/10.1146/annurev.ecolsys.39.110707.173426.
Iqbal, A., Q. Dong, X. Wang, H. Gui, H. Zhang, X. Zhang, and M. Song. 2020. “High Nitrogen Enhance Drought Tolerance in Cotton through Antioxidant Enzymatic Activities, Nitrogen Metabolism and Osmotic Adjustment.” Plants 9(2): 178. https://doi.org/10.3390/plants9020178.
Jefferies, R. L., D. R. Klein, and G. R. Shaver. 1994. “Vertebrate Herbivores and Northern Plant Communities: Reciprocal Influences and Responses.” Oikos: 193-206.
Johnson, S. N., J. T. Staley, F. A. L. McLeod, and S. E. Hartley. 2011. “Plant-Mediated Effects of Soil Invertebrates and Summer Drought on above-Ground Multitrophic Interactions.” Journal of Ecology 99(1): 57-65. https://doi.org/10.1111/j.1365-2745.2010.01748.x.
Jonsson, H., J. Olofsson, G. Blume-Werry, and J. Klaminder. 2023. “Cascading Effects of Earthworm Invasion in Tundra Increase Graminoid Density and Rodent Grazing Intensities.” Dryad, Dataset. https://doi.org/10.5061/dryad.zpc866tbm.
Klaminder, J., E. J. Krab, M. Larsbo, H. Jonsson, J. Fransson, and J. Koestel. 2022. “Holes in the Tundra: Invasive Earthworms Alter Soil Structure and Moisture in Tundra Soils.” Science of the Total Environment 859: 160125. https://doi.org/10.1016/j.scitotenv.2022.160125.
Lindén, E., L. Gough, and J. Olofsson. 2021. “Large and Small Herbivores Have Strong Effects on Tundra Vegetation in Scandinavia and Alaska.” Ecology and Evolution 11(17): 12141-12152. https://doi.org/10.1002/ece3.7977.
Mattson, W. J. 1980. “Herbivory in Relation to Plant Nitrogen Content.” Annual Review of Ecology and Systematics 11(1): 119-161.
Newington, J. E., H. Setälä, T. M. Bezemer, and T. H. Jones. 2004. “Potential Effects of Earthworms on Leaf-Chewer Performance.” Functional Ecology 18(5): 746-751. https://doi.org/10.1111/j.0269-8463.2004.00888.x.
Nuzzo, V., J. C. Maerz, and B. Blossey. 2009. “Earthworm Invasion as the Driving Force behind Plant Invasion and Community Change in Northeastern North American Forests.” Conservation Biology 23(4): 966-974. https://doi.org/10.1111/j.1523-1739.2009.01168.x.
Olofsson, J., H. Tømmervik, and T. V. Callaghan. 2012. “Vole and Lemming Activity Observed from Space.” Nature Climate Change 2(12): 880-883. https://doi.org/10.1038/nclimate1537.
Olofsson, J., and E. Post. 2018. “Effects of Large Herbivores on Tundra Vegetation in a Changing Climate, and Implications for Rewilding.” Philosophical Transactions of the Royal Society B: Biological Sciences 373(1761): 20170437.
Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar, and R Core Team. 2022. “Nlme: Linear and Nonlinear Mixed Effects Models.” https://svn.r-project.org/R-packages/trunk/nlme/.
R Core Team. 2022. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/.
RStudio Team. 2020. RStudio: Integrated Development for R. Boston: RStudio, Inc. http://www.rstudio.com/.
Scharn, R., C. G. Brachmann, A. Patchett, H. Reese, A. D. Bjorkman, J. M. Alatalo, R. G. Björk, A. K. Jägerbrand, U. Molau, and M. P. Björkman. 2021. “Vegetation Responses to 26 Years of Warming at Latnjajaure Field Station, Northern Sweden.” Arctic Science 8(3): 858-877. https://doi.org/10.1139/as-2020-0042.
Siewert, M. B., and J. Olofsson. 2021. “UAV Reveals Substantial but Heterogeneous Effects of Herbivores on Arctic Vegetation.” Scientific Reports 11(1): 19468. https://doi.org/10.1038/s41598-021-98497-5.
SMHI. 2021. “SMHI, Sveriges Meteorologiska Och Hydrologiska Institut-Open Data.” https://www.smhi.se/data/utforskaren-oppna-data.
Strengbom, J., J. Olofsson, J. Witzell, and J. Dahlgren. 2003. “Effects of Repeated Damage and Fertilization on Palatability of Vaccinium Myrtillus to Grey Sided Voles, Clethrionomys Rufocanus.” Oikos 103(1): 133-141.
Sundqvist, M. K., R. Giesler, B. J. Graae, H. Wallander, E. Fogelberg, and D. A. Wardle. 2011. “Interactive Effects of Vegetation Type and Elevation on Aboveground and Belowground Properties in a Subarctic Tundra.” Oikos 120(1): 128-142. https://doi.org/10.1111/j.1600-0706.2010.18811.x.
Thakur, M. P., T. Künne, S. B. Unsicker, A. Biere, O. Ferlian, U. Pruschitzki, L. Thouvenot, M. Türke, and N. Eisenhauer. 2021. “Invasive Earthworms Reduce Chemical Defense and Increase Herbivory and Pathogen Infection in Native Trees.” Journal of Ecology 109(2): 763-775. https://doi.org/10.1111/1365-2745.13504.
Veen, G. F., M. K. Sundqvist, D. Metcalfe, and S. D. Wilson. 2015. “Above-Ground and Below-Ground Plant Responses to Fertilization in Two Subarctic Ecosystems.” Arctic, Antarctic, and Alpine Research 47(4): 693-702. https://doi.org/10.1657/AAAR0014-085.
Venables, W. N., and B. D. Ripley. 2002. Modern Applied Statistics with S, Fourth ed. New York: Springer.
Vitousek, P. M. 1990. “Biological Invasions and Ecosystem Processes: Towards an Integration of Population Biology and Ecosystem Studies.” Oikos 57(1): 7-13. https://doi.org/10.2307/3565731.
Wackett, A. A., K. Yoo, J. Olofsson, and J. Klaminder. 2018. “Human-Mediated Introduction of Geoengineering Earthworms in the Fennoscandian Arctic.” Biological Invasions 20(6): 1377-1386. https://doi.org/10.1007/s10530-017-1642-7.
Wang, P., L. Mommer, J. van Ruijven, F. Berendse, T. C. Maximov, and M. M. P. D. Heijmans. 2016. “Seasonal Changes and Vertical Distribution of Root Standing Biomass of Graminoids and Shrubs at a Siberian Tundra Site.” Plant and Soil 407(1): 55-65. https://doi.org/10.1007/s11104-016-2858-5.
Wickham, H. 2016. Ggplot2: Elegant Graphics for Data Analysis 260. New York: Springer-Verlag.
Wood, S. N. 2017. An Introduction with R, Second ed. New York: Chapman and Hall/CRC. https://doi.org/10.1201/9781315370279.
Zhong, C., X. Cao, J. Hu, L. Zhu, J. Zhang, J. Huang, and Q. Jin. 2017. “Nitrogen Metabolism in Adaptation of Photosynthesis to Water Stress in Rice Grown under Different Nitrogen Levels.” Frontiers in Plant Science 8: 1079. https://doi.org/10.3389/fpls.2017.01079.