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Biogeochemical cycling of nickel and nutrients in a natural high-density stand of the hyperaccumulator Phyllanthus rufuschaneyi in Sabah, Malaysia

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Abstract

The extend of biogeochemical cycling of nickel (Ni) by tropical hyperaccumulator plants in their native habitat is largely unknown, although these unusual plants are suspected to play a major role in the recycling of this element in ultramafic ecosystems. In this study, we have assessed the biogeochemical cycling of Ni (and other elements, including mineral nutrients) by a tropical Ni hyperaccumulator plant, i.e., Phyllanthus rufuschaneyi, which is one of the most promising species for tropical Ni agromining. The study site was a young secondary forest in Sabah (Malaysia) where Phyllanthus rufuschaneyi occurs as the dominant species on an ultramafic Cambisol. For 2 years, we monitored a 100-m2 plot and collected information on weather, biomass increase, soil fertility, water fluxes to the soil and litter fluxes for a wide range of elements, including Ni. The Ni cycle is mainly driven by internal fluxes, notably the degradation and recycling of Ni-rich litter. Over the period of investigation, the Ni litter flux corresponded to the total Ni stock of the litter (5.2 g m−2 year−1). The results further show that Ni turnover varies significantly with the accumulation properties of the plant cover. This points to the major influence of Ni hyperaccumulator plants in building up Ni available stocks in the topsoils, as has also been shown in temperate ultramafic systems. Litterfall and throughfall contribute substantially to the cycling of phosphorus, sulphur and potassium in this ecosystem, with throughfall contributing 2-, 220- and 20-fold higher to the respective nutrient fluxes relative to litterfall. The magnesium:calcium ratio far exceeded 1 in the soil, but was < 1 in the leaves of Phyllanthus rufuschaneyi. The insights from this study should be taken into account when designing tropical agromining operations; as Ni stocks could be more labile than initially thought. The removal of Ni- and nutrients-rich biomass will likely affect available Ni (and major nutrients) for the next cropping seasons, and requires sustainable fertilisation, to be utilized to replenish depleted major nutrients. These findings also have major ecological implications.

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Acknowledgements

We would like to express our gratitude to Sabah Parks for their support and thank the Sabah Biodiversity Centre for granting permission for conducting research in Sabah (license JKM/MBS.1000-2/2 JLD.8). Serge Didier from UR BEF (INRAE) has provided substantial expertise to set up the instrumentation at the experimental site. The French National Research Agency through the national “Investissements d’avenir” program (ANR-10-LABX-21, LABEX RESSOURCES21 and Lorraine Université d’Excellence-LUE-Grant for traveling to Malaysia in 2019–2020) is acknowledged for funding support to R. Tisserand.

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Authors and Affiliations

  1. Laboratoire Sols et Environnement, INRAE, Université de Lorraine, 54000, Nancy, France

    Romane Tisserand, Antony van der Ent & Guillaume Echevarria

  2. Centre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, Brisbane, QLD, Australia

    Philip Nti Nkrumah, Antony van der Ent & Guillaume Echevarria

  3. Sabah Parks, Kota Kinabalu, Sabah, Malaysia

    Sukaibin Sumail

  4. INRAE, Centre de Nancy, Ecosystémes Forestiers, 54280, Champenoux, France

    Bernhard Zeller

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  1. Romane Tisserand
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  2. Philip Nti Nkrumah
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  3. Antony van der Ent
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  4. Sukaibin Sumail
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  5. Bernhard Zeller
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  6. Guillaume Echevarria
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Correspondence to Guillaume Echevarria.

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Communicated by Marko Rohlfs.

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Tisserand, R., Nkrumah, P.N., van der Ent, A. et al. Biogeochemical cycling of nickel and nutrients in a natural high-density stand of the hyperaccumulator Phyllanthus rufuschaneyi in Sabah, Malaysia. Chemoecology 32, 15–29 (2022). https://doi.org/10.1007/s00049-021-00363-3

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