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Parasitism within mutualist guilds explains the maintenance of diversity in multi-species mutualisms

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Abstract

We consider here mutualisms where there are multiple species sharing a resource supplied by the same partner. If, as commonly assumed, there is competition between the species, then only the superior competitor should persist. Nevertheless, coexistence of multiple species sharing the same mutualistic partner is a widespread phenomenon. Regulation of nutrient exchange, where each species receives resources from the partner in proportion to the strength of the mutualism between the two, has been proposed as the main mechanism for coexistence in multi-species mutualisms involving the transfer of nutrients. Significant arguments, however, challenge the importance of partner selection processes. We present a mathematical model, applied to the arbuscular mycorrhizal symbiosis, to propose an alternative explanation for this coexistence. We show that asymmetric resource exchange between the plant and its fungal guild can lead to indirect parasitic interactions between guild members. In our model, the amount of carbon supplied by the plant to the fungi depends on both plant and fungal biomass, while the amount of phosphorus supplied by the fungi to the plant depends on both plant and fungal biomass when the plant is small, and effectively on fungal biomass only when the plant is large. As a consequence of these functional responses, more beneficial mutualists increase resource availability, and are indirectly exploited by less beneficial species that consume the resource and grow larger than they would in the absence of the better mutualists. As guild mutualists are not competing, competitive exclusion does not occur. Hence, the interaction structure can explain the maintenance of diversity within guilds in the absence of spatial structure and niche-related processes.

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Funding

MMH received NSERC Discovery Grant RGPIN-2018-237774. JG received NONLOCAL project (ANR-14-CE25-0013), GLOBNETS project (ANR-16- CE02-0009), and the European Research Council (ERC) under the European Unions Horizon 2020 research and innovation program (grant agreement No 639638, MesoProbio). RCT received NSERC Discovery Grant RGPIN-2016-05277 and the “Make our planet great again (MOPGA)” grant.

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  1. Department of Mathematics, University of British Columbia, Kelowna, Canada

    Maria M. Martignoni & Rebecca C. Tyson

  2. Department of Biology, University of British Columbia, Kelowna, Canada

    Miranda M. Hart

  3. Laboratoire de Mathématiques (LAMA), CNRS and Université de Savoie-Mont Blanc, Chambery, France

    Jimmy Garnier

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  1. Maria M. Martignoni
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Correspondence to Maria M. Martignoni.

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Martignoni, M.M., Hart, M.M., Garnier, J. et al. Parasitism within mutualist guilds explains the maintenance of diversity in multi-species mutualisms. Theor Ecol 13, 615–627 (2020). https://doi.org/10.1007/s12080-020-00472-9

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