Antagonistic interactions between above- and belowground biota reduce their negative effects on a tree species

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Antagonistic interactions between above- and belowground biota reduce their negative effects on a tree species Qiang Yang & Arjen Biere & Jeffrey A. Harvey & Jianqing Ding & Evan Siemann

Received: 31 July 2019 / Accepted: 17 July 2020 # Springer Nature Switzerland AG 2020

Abstract Aims Plants in nature are confronted by a variety of beneficial and antagonistic above- and belowground organisms, including leaf herbivores, soil fungi, and soil nematodes. While their individual effects are usually well studied, their joint effects on plant performance are less well known. Synergistic or antagonistic interactions between these organisms would mean that their joint effects on plant performance are more or less detrimental or beneficial than expected from their individual effects. Methods We conducted a factorial greenhouse experiment in which we manipulated the presence of aboveground herbivores (weevils), soil nematodes, and soil

fungi using addition (weevil) or removal (fungicide, nematicide) treatments to test how these groups of organisms alone and in combination affect Triadica sebifera biomass production, when grown individually or under intraspecific competition. Results Soil fungi and aboveground weevils alone each strongly decreased plant root and total biomass. Interestingly, soil nematodes alone slightly reduced plant biomass but they mitigated the negative impacts of aboveground weevils, indicating antagonism in their effects on plant biomass. However, in the presence of soil fungi this antagonism was less pronounced, illustrating the complexity of interactive effects of aboveground and belowground biota on plant biomass.

Responsible Editor: Hans Lambers. Electronic supplementary material The online version of this article (https://doi.org/10.1007/s11104-020-04642-w) contains supplementary material, which is available to authorized users. Q. Yang State Key Laboratory of Grassland Agro-ecosystems, School of Life Sciences, Lanzhou University, Lanzhou 730000 Gansu, China Q. Yang Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074 Hubei, China A. Biere : J. A. Harvey Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PBWageningen, The Netherlands

J. A. Harvey Department of Ecological Science, Section Animal Ecology, VU University Amsterdam, Amsterdam, The Netherlands J. Ding (*) State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng 475004 Henan, China e-mail: [email protected] E. Siemann Department of Biosciences, Rice University, Houston, TX 77005, USA

Plant Soil

Aboveground herbivory increased nematode infections, but only in the absence of soil fungi. Intraspecific competition strongly enhanced nematode infection loads and slightly decreased T. sebifera root biomass but did not modulate the direction or the strength of interactions among these aboveground and belowground biota. Conclusions Our f