Functional divergence in nitrogen uptake rates explains diversity–productivity relationship in microalgal communities

Mandal, Shovon; Shurin, Jonathan B.; Efroymson, Rebecca A.; Mathews, Teresa J.

doi:10.1002/ecs2.2228

Title: Functional divergence in nitrogen uptake rates explains diversity–productivity relationship in microalgal communities

Journal Article · Wed May 23 00:00:00 EDT 2018 · Ecosphere

DOI:https://doi.org/10.1002/ecs2.2228· OSTI ID:1439901

Mandal, Shovon ^[1]; Shurin, Jonathan B. ^[2]; Efroymson, Rebecca A. ^[1]; Mathews, Teresa J. ^[1]

Environmental Sciences Division Oak Ridge National Laboratory Oak Ridge Tennessee 37831 USA
University of California at San Diego La Jolla California 92093 USA

The relationship between biodiversity and productivity has emerged as a central theme in ecology. Mechanistic explanations for this relationship suggest that the role organisms play in the ecosystem (i.e., niches or functional traits) is a better predictor of ecosystem stability and productivity than taxonomic richness. Here, we tested the capacity of functional diversity in nitrogen uptake in experimental microalgal communities to predict the complementarity effect (CE) and selection effect (SE) of biodiversity on productivity. We grew five algal species as monocultures and as polycultures in pairwise combinations in homogeneous (ammonium, nitrate, or urea alone) and heterogeneous nitrogen (mixed nitrogen) environments to determine whether complementarity between species may be enhanced in heterogeneous environments. We show that the positive diversity effects on productivity in heterogeneous environments resulted from complementarity effects with no positive contribution by species–specific SEs. Positive biodiversity effects in homogeneous environments, when present (nitrate and urea treatments but not ammonium), were driven both by CE and SE. Our results suggest that functional diversity increases species complementarity and productivity mainly in heterogeneous resource environments. Furthermore, these results provide evidence that the positive effect of functional diversity on community productivity depends on the diversity of resources present in the environment.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE)

Grant/Contract Number:: DE‐AC05‐00OR22725; AC05-00OR22725

OSTI ID:: 1439901

Alternate ID(s):: OSTI ID: 1439153; OSTI ID: 1454894

Journal Information:: Ecosphere, Journal Name: Ecosphere Vol. 9 Journal Issue: 5; ISSN 2150-8925

Publisher:: Wiley Blackwell (John Wiley & Sons)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 18 works

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References (54)

The Paradox of the Plankton Hutchinson, G. E. The American Naturalist, Vol. 95, Issue 882 https://doi.org/10.1086/282171	journal	May 1961
Environmental and trait variability constrain community structure and the biodiversity-productivity relationship Hodapp, Dorothee; Hillebrand, Helmut; Blasius, Bernd Ecology, Vol. 97, Issue 6 https://doi.org/10.1890/15-0730.1	journal	June 2016
Biodiversity improves water quality through niche partitioning Cardinale, Bradley J. Nature, Vol. 472, Issue 7341 https://doi.org/10.1038/nature09904	journal	April 2011
Ammonium uptake and growth limitation in marine phytoplankton Sunda, William G.; D., Ransom Hardison Limnology and Oceanography, Vol. 52, Issue 6 https://doi.org/10.4319/lo.2007.52.6.2496	journal	November 2007
Variation in nitrogen-15 natural abundance and nitrogen uptake traits among co-occurring alpine species: do species partition by nitrogen form? Miller, Amy E.; Bowman, William D. Oecologia, Vol. 130, Issue 4 https://doi.org/10.1007/s00442-001-0838-8	journal	February 2002
Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity Huston, Michael A. Oecologia, Vol. 110, Issue 4 https://doi.org/10.1007/s004420050180	journal	May 1997
The functional role of producer diversity in ecosystems Cardinale, Bradley J.; Matulich, Kristin L.; Hooper, David U. American Journal of Botany, Vol. 98, Issue 3 https://doi.org/10.3732/ajb.1000364	journal	March 2011
Genotypic richness and dissimilarity opposingly affect ecosystem functioning: Genotypic diversity and ecosystem functioning Jousset, A.; Schmid, B.; Scheu, S. Ecology Letters, Vol. 14, Issue 6 https://doi.org/10.1111/j.1461-0248.2011.01613.x	journal	March 2011
Functional identity is the main driver of diversity effects in young tree communities Tobner, Cornelia M.; Paquette, Alain; Gravel, Dominique Ecology Letters, Vol. 19, Issue 6 https://doi.org/10.1111/ele.12600	journal	April 2016
Biodiversity effects in the wild are common and as strong as key drivers of productivity Duffy, J. Emmett; Godwin, Casey M.; Cardinale, Bradley J. Nature, Vol. 549, Issue 7671 https://doi.org/10.1038/nature23886	journal	September 2017
Think ratio! A stoichiometric view on biodiversity–ecosystem functioning research Hillebrand, Helmut; Cowles, Jane M.; Lewandowska, Aleksandra Basic and Applied Ecology, Vol. 15, Issue 6 https://doi.org/10.1016/j.baae.2014.06.003	journal	September 2014
Resource availability and biodiversity effects on the productivity, temporal variability and resistance of experimental algal communities Zhang, Quan-Guo; Zhang, Da-Yong Oikos, Vol. 114, Issue 3 https://doi.org/10.1111/j.2006.0030-1299.14723.x	journal	September 2006
Diatoms and biomonitoring: should cell size be accounted for? Lavoie, Isabelle; Campeau, Stéphane; Fallu, Marie-Andrée Hydrobiologia, Vol. 573, Issue 1 https://doi.org/10.1007/s10750-006-0223-z	journal	July 2006
Partitioning selection and complementarity in biodiversity experiments Loreau, Michel; Hector, Andy Nature, Vol. 412, Issue 6842 https://doi.org/10.1038/35083573	journal	July 2001
Heterogeneity in Nitrogen Sources Enhances Productivity and Nutrient Use Efficiency in Algal Polycultures Mandal, Shovon; Shurin, Jonathan B.; Efroymson, Rebecca A. Environmental Science & Technology, Vol. 52, Issue 6 https://doi.org/10.1021/acs.est.7b05318	journal	February 2018
Phytoplankton-Specific Response to Enrichment of Phosphorus-Rich Surface Waters with Ammonium, Nitrate, and Urea Donald, Derek B.; Bogard, Matthew J.; Finlay, Kerri PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0053277	journal	January 2013
Human-caused environmental change: Impacts on plant diversity and evolution Tilman, D.; Lehman, C. Proceedings of the National Academy of Sciences, Vol. 98, Issue 10 https://doi.org/10.1073/pnas.091093198	journal	May 2001
Apparent plasticity in functional traits determining competitive ability and spatial distribution: a case from desert Xie, Jiang-Bo; Xu, Gui-Qing; Jenerette, G. Darrel Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep12174	journal	July 2015
Effects of competition on phylogenetic signal and phenotypic plasticity in plant functional traits Burns, Jean H.; Strauss, Sharon Y. Ecology, Vol. 93, Issue sp8 https://doi.org/10.1890/11-0401.1	journal	August 2012
Plant Preference for Ammonium versus Nitrate: A Neglected Determinant of Ecosystem Functioning? Boudsocq, S.; Niboyet, A.; Lata, J. C. The American Naturalist, Vol. 180, Issue 1 https://doi.org/10.1086/665997	journal	July 2012
A guide for using functional diversity indices to reveal changes in assembly processes along ecological gradients Mason, Norman W. H.; de Bello, Francesco; Mouillot, David Journal of Vegetation Science, Vol. 24, Issue 5 https://doi.org/10.1111/jvs.12013	journal	November 2012
Onset of the aerobic nitrogen cycle during the Great Oxidation Event Zerkle, Aubrey L.; Poulton, Simon W.; Newton, Robert J. Nature, Vol. 542, Issue 7642 https://doi.org/10.1038/nature20826	journal	February 2017
THE ECOLOGICAL CONSEQUENCES OF CHANGES IN BIODIVERSITY: A SEARCH FOR GENERAL PRINCIPLES ¹⁰¹ Tilman, David Ecology, Vol. 80, Issue 5 https://doi.org/10.1890/0012-9658(1999)080[1455:TECOCI]2.0.CO;2	journal	July 1999
Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems Elser, James J.; Bracken, Matthew E. S.; Cleland, Elsa E. Ecology Letters, Vol. 10, Issue 12 https://doi.org/10.1111/j.1461-0248.2007.01113.x	journal	December 2007
Functional diversity: back to basics and looking forward Petchey, Owen L.; Gaston, Kevin J. Ecology Letters, Vol. 9, Issue 6 https://doi.org/10.1111/j.1461-0248.2006.00924.x	journal	June 2006
Trait diversity enhances yield in algal biofuel assemblages Shurin, Jonathan B.; Mandal, Shovon; Abbott, Rachel L. Journal of Applied Ecology, Vol. 51, Issue 3 https://doi.org/10.1111/1365-2664.12242	journal	March 2014
Industrial-strength ecology: trade-offs and opportunities in algal biofuel production Shurin, Jonathan B.; Abbott, Rachel L.; Deal, Michael S. Ecology Letters, Vol. 16, Issue 11 https://doi.org/10.1111/ele.12176	journal	September 2013
The Influence of Functional Diversity and Composition on Ecosystem Processes Tilman, D. Science, Vol. 277, Issue 5330 https://doi.org/10.1126/science.277.5330.1300	journal	August 1997
Economic construction and operation of hectare-scale wastewater treatment enhanced pond systems Craggs, Rupert; Park, Jason; Sutherland, Donna Journal of Applied Phycology, Vol. 27, Issue 5 https://doi.org/10.1007/s10811-015-0658-6	journal	July 2015
Microalga Scenedesmus obliquus as a potential source for biodiesel production Mandal, Shovon; Mallick, Nirupama Applied Microbiology and Biotechnology, Vol. 84, Issue 2 https://doi.org/10.1007/s00253-009-1935-6	journal	March 2009
Impacts of plant diversity on biomass production increase through time because of species complementarity Cardinale, B. J.; Wright, J. P.; Cadotte, M. W. Proceedings of the National Academy of Sciences, Vol. 104, Issue 46 https://doi.org/10.1073/pnas.0709069104	journal	November 2007
The Statistical Inevitability of Stability‐Diversity Relationships in Community Ecology Doak, D. F.; Bigger, D.; Harding, E. K. The American Naturalist, Vol. 151, Issue 3 https://doi.org/10.1086/286117	journal	March 1998
Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra McKane, Robert B.; Johnson, Loretta C.; Shaver, Gaius R. Nature, Vol. 415, Issue 6867 https://doi.org/10.1038/415068a	journal	January 2002
Environment-enhancing algal biofuel production using wastewaters Zhou, Wenguang; Chen, Paul; Min, Min Renewable and Sustainable Energy Reviews, Vol. 36 https://doi.org/10.1016/j.rser.2014.04.073	journal	August 2014
Does functional redundancy exist? Loreau, Michel Oikos, Vol. 104, Issue 3 https://doi.org/10.1111/j.0030-1299.2004.12685.x	journal	March 2004
Evidence for a three-way trade-off between nitrogen and phosphorus competitive abilities and cell size in phytoplankton Edwards, Kyle F.; Klausmeier, Christopher A.; Litchman, Elena Ecology, Vol. 92, Issue 11 https://doi.org/10.1890/11-0395.1	journal	November 2011
Effects of nitrogen sources on cell growth and lipid accumulation of green alga Neochloris oleoabundans Li, Yanqun; Horsman, Mark; Wang, Bei Applied Microbiology and Biotechnology, Vol. 81, Issue 4 https://doi.org/10.1007/s00253-008-1681-1	journal	September 2008
Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms Ashton, Isabel W.; Miller, Amy E.; Bowman, William D. Ecology, Vol. 91, Issue 11 https://doi.org/10.1890/09-1849.1	journal	November 2010
Seaweed Diversity Enhances Nitrogen Uptake via Complementary use of Nitrate and Ammonium Bracken, Matthew E. S.; Stachowicz, John J. Ecology, Vol. 87, Issue 9 https://doi.org/10.1890/0012-9658(2006)87[2397:SDENUV]2.0.CO;2	journal	September 2006
Limiting Resources and the Regulation of Diversity in Phytoplankton Communities Interlandi, Sebastian J.; Kilham, Susan S. Ecology, Vol. 82, Issue 5 https://doi.org/10.1890/0012-9658(2001)082[1270:LRATRO]2.0.CO;2	journal	May 2001
Effects of Algal Diversity on the Production of Biomass in Homogeneous and Heterogeneous Nutrient Environments: A Microcosm Experiment Weis, Jerome J.; Madrigal, Daniel S.; Cardinale, Bradley J. PLoS ONE, Vol. 3, Issue 7 https://doi.org/10.1371/journal.pone.0002825	journal	July 2008
Influence of nitrogen sources on biomass productivity of microalgae Scenedesmus bijugatus Arumugam, Muthu; Agarwal, Ankur; Arya, Mahesh Chandra Bioresource Technology, Vol. 131 https://doi.org/10.1016/j.biortech.2012.12.159	journal	March 2013
Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition, with emphasis on nitrogen-enriched conditions: Pluses and minuses of NH4+ Glibert, Patricia M.; Wilkerson, Frances P.; Dugdale, Richard C. Limnology and Oceanography, Vol. 61, Issue 1 https://doi.org/10.1002/lno.10203	journal	October 2015
Human Alteration of the Global Nitrogen Cycle: Sources and Consequences Vitousek, Peter M.; Aber, John D.; Howarth, Robert W. Ecological Applications, Vol. 7, Issue 3 https://doi.org/10.1890/1051-0761(1997)007[0737:HAOTGN]2.0.CO;2	journal	August 1997
System and method for research-scale outdoor production of microalgae and cyanobacteria Schoepp, Nathan G.; Stewart, Ryan L.; Sun, Vincent Bioresource Technology, Vol. 166 https://doi.org/10.1016/j.biortech.2014.05.046	journal	August 2014
Biodiversity and ecosystem stability across scales in metacommunities Wang, Shaopeng; Loreau, Michel Ecology Letters, Vol. 19, Issue 5 https://doi.org/10.1111/ele.12582	journal	February 2016
FDiversity: an Integrated Tool to Estimate and Analyze Functional Diversity Casanoves, Fernando; Pla, Laura E.; Di Rienzo, Julio A. Bulletin of the Ecological Society of America, Vol. 92, Issue 2 https://doi.org/10.1890/0012-9623-92.2.147	journal	April 2011
Plant diversity and ecosystem productivity: Theoretical considerations Tilman, D.; Lehman, C. L.; Thomson, K. T. Proceedings of the National Academy of Sciences, Vol. 94, Issue 5 https://doi.org/10.1073/pnas.94.5.1857	journal	March 1997
Biovolume Calculation for Pelagic and Benthic Microalgae Hillebrand, Helmut; Dürselen, Claus-Dieter; Kirschtel, David Journal of Phycology, Vol. 35, Issue 2 https://doi.org/10.1046/j.1529-8817.1999.3520403.x	journal	April 1999
A distance-based framework for measuring functional diversity from multiple traits Laliberté, Etienne; Legendre, Pierre Ecology, Vol. 91, Issue 1 https://doi.org/10.1890/08-2244.1	journal	January 2010
A user's guide to functional diversity indices Schleuter, D.; Daufresne, M.; Massol, F. Ecological Monographs, Vol. 80, Issue 3 https://doi.org/10.1890/08-2225.1	journal	August 2010
Functional traits explain ecosystem function through opposing mechanisms Cadotte, Marc W. Ecology Letters, Vol. 20, Issue 8 https://doi.org/10.1111/ele.12796	journal	June 2017
YELLOW-GREEN ALGAE WITH CHLOROPHYLLIDE C ^1, ² Guillard, Robert R. L.; Lorenzen, Carl J. Journal of Phycology, Vol. 8, Issue 1 https://doi.org/10.1111/j.1529-8817.1972.tb03995.x	journal	March 1972
High Productivity in Grassland Ecosystems: Effected by Species Diversity or Productive Species? Aarssen, Lonnie W. Oikos, Vol. 80, Issue 1 https://doi.org/10.2307/3546531	journal	October 1997

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