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Inducible phenotypic plasticity in plants regulates aquatic ecosystem functioning

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Abstract

Differences among individuals within species affect community and ecosystem processes in many systems, and may rival the importance of differences between species. Intraspecific variation consists of both plastic and genetic components that are regulated by different processes and operate on different time scales. Therefore, probing which mechanisms can affect traits sufficiently strongly to affect ecosystem processes is fundamental to understanding the consequences of individual variation. We find that a dominant deciduous tree of Pacific Northwest riparian ecosystems, red alder, exhibits strong and synergistic responses to nutrient resources and herbivory stress. These induced responses, which include shifting nutrient and plant secondary metabolite composition, have cascading effects on aquatic ecosystem function. Defense responses suppress leaf litter decomposition in small streams, thus altering the rate of energy capture for one of the most abundant terrestrial carbon sources entering aquatic systems. We find that alder responses to herbivory stress largely depend on availability of soil nutrients, with modification of the highly cytotoxic diarylheptanoid group of secondary metabolites being favored in nutrient-poor environments and modification of the typically dose-dependent ellagitannins being favored in nutrient-rich environments. Importantly, these findings identify traits for herbivore resistance in alder trees and demonstrate that plastic responses occurring within a species and over short time scales substantially alter a key function of an adjacent ecosystem. Furthermore, demonstrating plasticity among alder secondary metabolites lends insight into this system, in which decomposer communities are known to adjust to the secondary chemistry of local alder trees to facilitate rapid decomposition of locally derived leaf litter.

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Acknowledgements

We thank J.T. Wootton, C. Pfister, T. Price, J. Bergelson and G. Dwyer for constructive comments and discussion on this work and L. Harris for assistance in the field. We thank Merrill & Ring Inc. and J. Murray for facilitating research on their lands, A. Colman, A. Mine, G. Olack, and the Colman Isotope Lab at University of Chicago for assistance with nitrogen, carbon and phosphorus analyses, and D. Hurd and M. Hurd for providing work facilities.

Funding

This work was supported by the NSF GRFP, the DOE GAANN, NSF DDIG DEB-1311293, ARCS® (Achievement Rewards for College Scientists) Foundation, Inc.’s Scholar Illinois Chapter (2014 and 2015), National Geographic Young Explorer’s Grant, and University of Chicago Hinds Fund grants to SLJ; an Olympic Natural Resources Grant and NSF grant DEB 09-19420 to J.T. Wootton; and an NSF grant OCE-0928232 to C.A. Pfister.

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Author notes

  1. Sara L. Jackrel

    Present address: Department of Ecology and Evolutionary Biology, University of Michigan, 830 N. University Avenue, Ann Arbor, MI, 48109, USA

Authors and Affiliations

  1. Department of Ecology and Evolution, The University of Chicago, 1101 E 57th Street, Chicago, IL, 60637, USA

    Sara L. Jackrel & Timothy C. Morton

Authors
  1. Sara L. Jackrel
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  2. Timothy C. Morton
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Contributions

SLJ conceived and designed the study, conducted field experiments, generated the nutrient and mass spectra data, performed statistical analyses and wrote the manuscript. TCM design secondary metabolite analyses, generated the mass spectra data, characterized secondary metabolites and assisted with writing the manuscript.

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Correspondence to Sara L. Jackrel.

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We have no competing interests.

Data availability

All leaf decomposition and nutrient data can be found here: http://dx.doi.org/10.5061/dryad.ph812. A subset of mass spectra chromatograms and details about identifying secondary metabolites are available in our supplementary materials. Contact authors for remaining mass spectra.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by Amy Austin.

We document that plasticity in secondary metabolites occurring within plants over short times scales affects the rate of leaf decomposition in adjacent river ecosystems. This work changes our understanding of the temporal stability and regulation of this ecosystem function.

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Jackrel, S.L., Morton, T.C. Inducible phenotypic plasticity in plants regulates aquatic ecosystem functioning. Oecologia 186, 895–906 (2018). https://doi.org/10.1007/s00442-018-4094-6

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