Nutrient addition drives declines in grassland species richness primarily via enhanced species loss

Authors: MUEHLEISEN, ANDREW - University Of Oregon; WATKINS, CARMEN - University Of Oregon; ALTMIRE, GABRIELLA - University Of Oregon; SHAW, E - University Of Oregon; CASE, MADELON - University Of Oregon; AOYAMA, LINA - University Of Oregon; BRAMBILA, ALEJANDRO - University Of Oregon; REED, PAUL - University Of Oregon; LAFORGIA, MARINA - University Of California, Davis; BORER, ELIZABETH - University Of Minnesota; SEABLOOM, ERIC - University Of Minnesota; BAKKER, JONATHAN - University Of Washington; ARNILLAS, CARLOS - University Of Toronto; BIEDERMAN, LORI - Iowa State University; CHEN, QINGPIN - Peking University; CLELAND, ELSA - University Of California; ESKELINEN, ANU - German Centre For Integrative Biodiversity Research (IDIV); FAY, PHILIP - Retired ARS Employee; HAGENAH, NICOLE - University Of Pretoria; HARPOLE, STAN - Martin Luther University; HAUTIER, YANN - Utrecht University; HENNING, JEREMIAH - University Of South Alabama; KNOPS, JOHANNES - Liverpool University; KOMATSU, KIMBERLY - Smithsonian Environmental Research Center; LADOUCEUR, EMMA - University Of Leipzig; LAUNGANI, RAMESH - Brooklyn College; MACDOUGALL, ANDREW - University Of Guelph; MCCULLEY, REBECCA - University Of Kentucky; MOORE, JOSLIN - Arthur Rylah Institute; OHLERT, TIM - University Of New Mexico; POWER, SALLY - Western Sydney University; RAYNAUD, XAVIER - The Sorbonne University; STEVENS, CARLY - Lancaster University; VIRTANEN, RISTO - University Of Oulu; WILFAHRT, PETER - University Of Minnesota; HALLETT, LAUREN - University Of Oregon

Submitted to: Journal of Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/23/2022
Publication Date: 4/4/2023
Citation: Muehleisen, A.J., Watkins, C.R., Altmire, G.R., Shaw, E.A., Case, M.F., Aoyama, L., Brambila, A., Reed, P.B., LaForgia, M., Borer, E.T., Seabloom, E.W., Bakker, J.D., Arnillas, C.A., Biederman, L., Chen, Q., Cleland, E.E., Eskelinen, A., Fay, P.A., Hagenah, N., Harpole, S., Hautier, Y., Henning, J.A., Knops, J.M., Komatsu, K.J., Ladouceur, E., Laungani, R., MacDougall, A., McCulley, R.L., Moore, J.L., Ohlert, T., Power, S.A., Raynaud, X., Stevens, C.J., Virtanen, R., Wilfahrt, P., Hallett, L.M. 2023. Nutrient addition drives declines in grassland species richness primarily via enhanced species loss. Journal of Ecology. 111(3):552-563. https://doi.org/10.1111/1365-2745.14038.
DOI: https://doi.org/10.1111/1365-2745.14038

Interpretive Summary: The ability of grasslands to provide important ecosystem services depends on their productivity and on the diversity of plant species. Plant diversity is threatened by excessive nutrients in the environment. Understanding the mechanisms by which nutrients reduce plant diversity is crucial to predict the consequences for ecosystem services and to designing effective mitigation strategies. In this study, a fertilization experiment was conducted where nitrogen, phosphorus, and potassium combined with micronutrients were applied to 30 grasslands for up to 10 years. New species appearing and existing species disappearing were recorded over this period. Fertilization with nitrogen, especially in combination with phosphorus or potassium increased rates at which species were lost from these grasslands while also reducing the appearance of new species. These trends continued over the entire duration of the experiment. The results highlight how fertilizing diverse grasslands drives down their diversity by causing loss of previously established species.

Technical Abstract: Declines in grassland diversity in response to nutrient addition are a general consequence of global change. This decline in species richness may be driven by multiple underlying processes operating at different time-scales. Nutrient addition can reduce diversity by enhancing the rate of local extinction via competitive exclusion, or by reducing the rate of colonization by constraining the pool of species able to colonize under new conditions. Partitioning net change into extinction and colonization rates will better delineate the long-term effect of global change in grasslands. We synthesized changes in richness in response to experimental fertilization with nitrogen, phosphorus and potassium with micronutrients across 30 grasslands. We quantified changes in local richness, colonization, and extinction over 8–10 years of nutrient addition, and compared these rates against control conditions to isolate the effect of nutrient addition from background dynamics. Total richness at steady state in the control plots was the sum of equal, relatively high rates of local colonization and extinction. On aggregate, 30%–35% of initial species were lost and the same proportion of new species were gained at least once over a decade. Absolute turnover increased with site-level richness but was proportionately greater at lower-richness sites relative to starting richness. Loss of total richness with nutrient addition, especially N in combination with P or K, was driven by enhanced rates of extinction with a smaller contribution from reduced colonization. Enhanced extinction and reduced colonization were disproportionately among native species, perennials, and forbs. Reduced colonization plateaued after the first few (<5) years after nutrient addition, while enhanced extinction continued throughout the first decade. Synthesis. Our results indicate a high rate of colonizations and extinctions underlying the richness of ambient communities and that nutrient enhancement drives overall declines in diversity primarily by exclusion of previously established species. Moreover, enhanced extinction continues over long time-scales, suggesting continuous, long-term community responses and a need for long-term study to fully realize the extinction impact of increased nutrients on grassland composition.