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Consumer Aggregations Drive Nutrient Dynamics and Ecosystem Metabolism in Nutrient-Limited Systems

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Abstract

Differences in animal distributions and metabolic demands can influence energy and nutrient flow in an ecosystem. Through taxa-specific nutrient consumption, storage, and remineralization, animals may influence energy and nutrient pathways in an ecosystem. Here we show these taxa-specific traits can drive biogeochemical cycles of nutrients and alter ecosystem primary production and metabolism, using riverine systems that support heterogeneous freshwater mussel aggregations. Freshwater unionid mussels occur as distinct, spatially heterogeneous, dense aggregations in rivers. They may influence rates of production and respiration because their activities are spatially concentrated within given stream reaches. Previous work indicates that mussels influence nutrient limitation patterns, algal species composition, and producer and primary consumer biomass. Here, we integrate measures of organismal rates, stoichiometry, community-scaled rates, and ecosystem rates, to determine the relative source–sink nutrient dynamics of mussel aggregations and their influence on net ecosystem processes. We studied areas with and without mussel aggregations in three nitrogen-limited rivers in southeastern Oklahoma, USA. We measured respiration and excretion rates of mussels and collected a subset of samples for tissue chemistry and for thin sectioning of the shell to determine growth rates at each site. This allowed us to assess nutrient remineralization and nutrient sequestration by mussels. These rates were scaled to the community. We also measured stream metabolism at three sites with and without mussels. We demonstrated that mussel species have distinct stoichiometric traits, vary in their respiration rates, and that mussel aggregations influence nutrient cycling and productivity. Across all mussel aggregations, we found that mussels excreted more nitrogen than they sequestered into tissue and excreted more phosphorus than they sequestered except at one site. Furthermore, gross primary productivity was significantly greater at reaches with mussels. Collectively, our results indicate that mussels have ecosystem-level impacts on nutrient availability and production in nutrient-limited rivers. Within these streams, mussels are affecting the movement of nutrients and altering nutrient spiralling.

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Acknowledgements

We thank Lynda Callaway, Kristie Hargrove, Ashley McElmurry, and Lisa Costantino at the Robert S. Kerr Laboratory in Ada, Oklahoma, for laboratory assistance and equipment use. Walter Dodds provided the solver spreadsheet for stream ecosystem metabolism calculations. Alan Covich, Stephen Golladay, and two anonymous reviewers provided helpful comments on a previous version of this manuscript. We appreciate the cooperation of several landowners in granting us access to their properties for this research. Notice: The US Environmental Protection Agency through its Office of Research and Development collaborated in the research described herein. It has been subject to an administrative review but does not necessarily reflect the views of the Agency. No official endorsement should be inferred. Mention of trade names, products, or services does not convey and should not be interpreted as conveying, official EPA approval, endorsement, or recommendation.

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  1. Department of Biological Sciences, University of Alabama, 300 Hackberry Lane, Tuscaloosa, Alabama, 35487, USA

    Carla L. Atkinson

  2. Civil, Structural, and Environmental Engineering, University at Buffalo, 207 Jarvis Hall, Buffalo, New York, 14260, USA

    Brandon J. Sansom

  3. Oklahoma Biological Survey, Department of Biology and Ecology and Evolutionary Biology Graduate Program, University of Oklahoma, 111 E. Chesapeake St., Norman, Oklahoma, 73019, USA

    Caryn C. Vaughn

  4. Robert S. Kerr Environmental Research Center, Office of Research and Development, United States Environmental Protection Agency, Ada, Oklahoma, 74820, USA

    Kenneth J. Forshay

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  1. Carla L. Atkinson
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Correspondence to Carla L. Atkinson.

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C. Atkinson designed the study, conducted the research, analyzed the data, and wrote the initial draft of the paper. B. Sansom assisted with data analysis. C. Vaughn assisted with study design. K. Forshay assisted with data analysis. All authors contributed to writing the manuscript and subsequent revisions.

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Atkinson, C.L., Sansom, B.J., Vaughn, C.C. et al. Consumer Aggregations Drive Nutrient Dynamics and Ecosystem Metabolism in Nutrient-Limited Systems. Ecosystems 21, 521–535 (2018). https://doi.org/10.1007/s10021-017-0166-4

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