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Invasive consumers provoke ecosystem-wide disruption of salt marsh functions by dismantling a keystone mutualism

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Abstract

Mutualisms enhance ecosystem biodiversity, functioning, and service provisioning through direct and indirect positive interactions. However, invasive species can interrupt mutualisms and disrupt ecosystem functions when they affect foundation species and their keystone mutualist partners. In the southeastern US, mussels aggregate around cordgrass stems, a keystone mutualist-foundation species interaction that controls marsh structure, function, and resilience. Invasive hogs trample cordgrass and consume mussels, yet the multi-scale effects of this mutualism disruption remain uncertain. Here, we quantified the effects of hog-mediated mutualism disruption on four critical ecosystem functions: cordgrass biomass, macroinvertebrate biomass, denitrification, and sediment deposition. We compared a hog-disturbed marsh (27% area disturbed) and a hog-free marsh (0.05% disturbed) and experimentally demonstrated that hog predation causes the observed 93% reduction in mussels on the hog marsh. Plot-scale measurements revealed that hog trampling of cordgrass doubles net denitrification rates but decreases cordgrass biomass, crab biomass, and sediment deposition by 74%, 80% and 55%, respectively, relative to areas without hogs. Mussels stimulate cordgrass biomass, crab biomass, denitrification, and sediment deposition by 19%, 39%, 134% and 140%, effects that are only evident in the mussel-dense hog-free marsh. Using hog damage and mussel cover surveys to extrapolate plot-scale measurements to the 20 m2 scale, we estimate that hogs stimulate cordgrass biomass and denitrification by 27% and 5% but, by driving mussel loss, depress crab biomass and sediment deposition by 48% and 38%. Disruption of the cordgrass-mussel mutualism by invasive hogs alters ecosystem functioning, modifications which will likely affect marsh ecosystem service provisioning and resilience region-wide.

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Data availability

Datasets generated during this study are included as Online Resource 3. At the conclusion of the project, data will be publicly archived with the NOAA Centralized Data Management Office.

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Acknowledgements

Field work assistance from Sydney Williams, Julie Grissett, Kristie Perez, Emory Wellman, Donovan Mitchell, Chloe Schwab, and Jonathan Crabill. Lab assistance from Katie Heiden, Gabriela Reyes, and Heather Donnelly. We thank Andrew Altieri for his comments on the manuscript and an anonymous reviewer for their detailed comments.

Funding

Funded by Florida Sea Grant (PD-21-03) and NSF Career Award (#1652628) to C. Angelini, UF/IFAS Early Career Seed Grant, USDA National Institute of Food and Agriculture (Hatch project FLA-TRC-005764), and NOAA NERR Science Collaborative to A. Smyth, and a Ruth D. Turner Fellowship to H. Fischman.

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All authors contributed to the study conception and design. Data collection was performed by HF and AS. Data analysis was performed by HF. The first draft of the manuscript was written by HF and CA, AS provided edits on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Hallie S. Fischman.

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Fischman, H.S., Smyth, A.R. & Angelini, C. Invasive consumers provoke ecosystem-wide disruption of salt marsh functions by dismantling a keystone mutualism. Biol Invasions 26, 169–185 (2024). https://doi.org/10.1007/s10530-023-03167-4

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  • DOI: https://doi.org/10.1007/s10530-023-03167-4

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