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Microscale patchiness leads to large and important intraspecific internal nutrient heterogeneity in phytoplankton

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Abstract

Phytoplankton stoichiometry or nutrient content has been shown to vary in a number of dimensions (species, condition, time, space), but the heterogeneity within a species at a given time and location, and the underlying mechanisms and importance have not been explored. There are a number of mechanisms that can create intraspecific heterogeneity, and theory suggests it can affect the population growth rate. We studied heterogeneity in P content of the freshwater diatom Cyclotella meneghiniana in the Charles River in Boston. Single-cell observations using synchrotron-based X-ray fluorescence show that the nutrient status varies from P-starved to P-replete. We simulate individual cells using an agent-based model that accounts for a number of mechanisms that can create heterogeneity, including surface area–based uptake, mortality differentiation, stochastic biological variability in states and behavior, macroscale mixing, and microscale nutrient patch encounter. By performing a number of simulations with various mechanisms turned on/off and comparing to data, we conclude that the heterogeneity is mostly due to microscale patchiness (85%). We explore the importance of accounting for heterogeneity in models by performing a simulation with the growth rate based on the population-average internal nutrient, as is done in conventional population-level models. This shows that ignoring heterogeneity increases the population growth rate by a factor of 1.47. To account for different heterogeneity in the laboratory and field, population-level ecosystem models should reduce maximum growth rates. The magnitude of this correction depends on local conditions, and in our case, it is a factor of 0.72.

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Acknowledgments

Thanks to Kelly Crawford, Alida Durrant, Dave Burke, and Jen Forbes for help with the field sampling and laboratory analysis. Jim Sweet (Aquatic Analysts) performed the species analyses. Camp Dresser & McKee Inc. provided the landside model results. Two anonymous reviewers provided constructive criticism. Use of the Advanced Photon Source, an Office of Science User Facility operated for the U.S. Department of Energy (DOE) Office of Science by Argonne National Laboratory, was supported by the U.S. DOE under Contract No. DE-AC02-06CH11357. This research was sponsored by grants from the National Science Foundation to BST (CBET 0730061 and 0913071) and FLH (CBET 0730239).

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  1. Vanni Bucci

    Present address: Department of Computational Biology, Memorial Sloan-Kettering Cancer Center, New York, NY, USA

  2. Daliangelis Nunez-Milland

    Present address: Coastal Carolina University, Conway, SC, USA

  3. Benjamin S. Twining

    Present address: Bigelow Laboratory for Ocean Sciences, West Boothbay Harbor, ME, 04575, USA

Authors and Affiliations

  1. Civil and Environmental Engineering Department, Northeastern University, Boston, MA, 02115, USA

    Vanni Bucci & Ferdi L. Hellweger

  2. Center for Urban Environmental Studies, Northeastern University, Boston, MA, 02115, USA

    Vanni Bucci & Ferdi L. Hellweger

  3. Department of Chemistry and Biochemistry, University of South Carolina, Columbia, SC, 29208, USA

    Daliangelis Nunez-Milland & Benjamin S. Twining

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  1. Vanni Bucci
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Correspondence to Ferdi L. Hellweger.

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Bucci, V., Nunez-Milland, D., Twining, B.S. et al. Microscale patchiness leads to large and important intraspecific internal nutrient heterogeneity in phytoplankton. Aquat Ecol 46, 101–118 (2012). https://doi.org/10.1007/s10452-011-9384-6

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