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Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development

Nature Plants volume 1, Article number: 15050 (2015) Cite this article

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Abstract

Plant species diversity increases as soil phosphorus availability declines during long-term ecosystem development1,2. The increase in plant species diversity is associated with a decline in above-ground functional diversity, because leaf traits converge on a high phosphorus-use efficiency strategy on old and infertile soils3,4. In contrast, the response of below-ground traits that directly influence nutrient acquisition remains poorly understood3,5; yet it might be key to understanding how soil fertility drives patterns of plant species diversity1. Here we show a marked increase in the richness and diversity of plant nutrient-acquisition strategies with declining soil phosphorus availability during long-term ecosystem development in a global biodiversity hotspot. Almost all nutrient-acquisition strategies currently known were found in plants from the most infertile soils, despite these being some of the most phosphorus-impoverished soils on Earth. Mycorrhizal plants declined in relative abundance by >30%, although the decline was compensated by an increase in non-mycorrhizal, carboxylate-exuding species that ‘mine’ phosphorus from the soil using different strategies. Plant species richness within individual nutrient-acquisition strategies also increased dramatically, with the species richness of many strategies more than doubling between the youngest and oldest soils. These results reveal increasing functional diversity of below-ground traits related to nutrient acquisition during ecosystem development, suggesting that no single combination of traits, including those related to nutrient-acquisition strategies, is superior to all others at extremely low soil fertility. Furthermore, the increasing diversity of nutrient-acquisition strategies with declining soil fertility, despite functional convergence of above-ground traits4,6, suggests that fundamentally different plant community assembly processes operate above- and below-ground.

The biotic composition of many ecosystems is being altered at an alarming rate7, so there is an urgent need to better understand the fundamental processes that shape the assembly of ecological communities and maintain their biodiversity. Soil fertility strongly influences plant community composition through plant traits related to nutrient acquisition and use8,9. Functional convergence of above-ground plant traits during plant community assembly is associated with the dominance of species with ‘slow’ leaf economic traits (for example long-lived leaves with low nutrient concentrations) in soils of low fertility, whereas species with ‘fast’ leaf traits (for example short-lived leaves with high nutrient concentrations) are favoured in fertile soils3,8. Much less is known, however, about the below-ground traits that directly influence nutrient acquisition.

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Acknowledgements

G.Z. was supported by a scholarship from the Paul Hasluck Bequest administered by the Kwongan Foundation. We acknowledge the assistance of many people in conducting the flora surveys. Funding was provided by research awards from UWA and a DECRA (DE120100352) from the Australian Research Council (ARC) to E.L. H.L. was supported by the Australian Research Council (ARC DP0985685). We thank D. Agudo and A. Bielnicka for laboratory support. We acknowledge the Department of Parks and Wildlife (Western Australia) and the Shires of Dandaragan, and Coorow for permission to conduct research on land under their administration. We acknowledge the facilities, and the scientific and technical assistance of the Australian Microscopy & Microanalysis Research Facility at the Centre for Microscopy, Characterisation & Analysis, The University of Western Australia, a facility funded by the University, State and Commonwealth Governments.

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Authors and Affiliations

  1. School of Plant Biology, The University of Western Australia, Crawley (Perth), 6009, Western Australia, Australia

    Graham Zemunik, Benjamin L. Turner, Hans Lambers & Etienne Laliberté

  2. Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancon, Republic of Panama

    Benjamin L. Turner

  3. Institut de Recherche en Biologie Végétale, Université de Montréal, 4101 Sherbrooke Est, Montréal, H1X 2B2, Quebec, Canada

    Etienne Laliberté

Authors
  1. Graham Zemunik
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  2. Benjamin L. Turner
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  3. Hans Lambers
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  4. Etienne Laliberté
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Contributions

G.Z. designed the study with assistance from E.L. and H.L. G.Z. collected the vegetation and mycorrhizal data, and performed the statistical analyses. E.L. and B.T. collected the soil data and B.T. analysed the soil samples. G.Z wrote the manuscript and all authors contributed to revisions.

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Correspondence to Graham Zemunik.

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Zemunik, G., Turner, B., Lambers, H. et al. Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nature Plants 1, 15050 (2015). https://doi.org/10.1038/nplants.2015.50

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