Research Collection Review Article The physical structure of soil: Determinant and consequence of trophic interactions Author(s): Erktan, Amandine; Or, Dani; Scheu, Stefan Publication Date: 2020-09 Permanent Link: https://doi.org/10.3929/ethz-b-000424423 Originally published in: Soil Biology and Biochemistry 148, http://doi.org/10.1016/j.soilbio.2020.107876 Rights / License: Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library Soil Biology and Biochemistry 148 (2020) 107876 Contents lists available at ScienceDirect Soil Biology and Biochemistry journal homepage: http://www.elsevier.com/locate/soilbio Review Paper The physical structure of soil: Determinant and consequence of trophic interactions Amandine Erktan a,*, Dani Or b, Stefan Scheu a,c a J.F. Blumenbach Institute of Zoology and Anthropology, University of Gottingen,€ Untere Karspüle 2, 37073, Gottingen,€ Germany b ETHZ, Universitatstra€ ße 16, 8092, Zürich, Switzerland c Centre of Biodiversity and Sustainable Land Use, University of Gottingen,€ Büsgenweg 1, 37077, Gottingen,€ Germany ARTICLE INFO ABSTRACT Keywords: Trophic interactions play a vital role in soil functioning and are increasingly considered as important drivers of Soil pores the soil microbiome and biogeochemical cycles. In the last decade, novel tools to decipher the structure of soil Soil microhabitat food webs have provided unprecedent advance in describing complex trophic interactions. Yet, the major Microbiota challenge remains to understand the drivers of the trophic interactions. Evidence suggests that small scale soil Mesofauna physical structure may offer a unifying framework for understanding the nature and patterns of trophic in­ Soil food web ’ Matric potential teractions in soils. Here, we review the current knowledge of how restrictions on soil organisms ability to sense and access food resources/prey inherent to soil physical structure essentially shape trophic interactions. We focus primarily on organisms unable to deform the soil and create pores themselves, such as bacteria, fungi, protists, nematodes and microarthropods, and consider pore geometry, connectivity and hydration status as main de­ scriptors of the soil physical structure. We point that the soil physical structure appears to mostly limit the sensing and accessibility to food resources/prey, with negative effects on bottom up controls. The main mech­ anisms are (i) the reduced transport of sensing molecules, notably volatiles, through the soil matrix and (ii) the wide presence of refuges leading to pore size segregation of consumer/predators and food sources/prey in pores of contrasting size. In addition, variations in the connectivity of the soil pores and the water filmis suggested as a central aspect driving encounter probability between consumers/predator and food source/prey and hence locally decrease or increase top-down controls. Constraints imposed by the soil physical structure on trophic interactions are thought to be major drivers of the soil diversity and local community assemblage, notably by favoring a variety of adaptations to feed in this dark labyrinth (food specialists/flexible/generalists) and by limiting competitive exclusion through limited encounter probability of consumers. We conclude with possible future ways for an interdisciplinary and more quantitative research merging soil physics and soil food web ecology. 1. Introduction communities on biogeochemical cycles. This novel emphasis on biotic top-down regulations (Ott et al., 2014; Lang et al., 2014; Lucas et al., Soils host an unparalleled diversity of organisms (Dindal, 1990) that 2020; Coulibaly et al., 2019) challenge the previous common vision that are interconnected via numerous trophic links and span complex food soil microbial communities were mainly driven by bottom-up regula­ webs (Brose and Scheu, 2014). Trophic interactions play a major role in tions (plant inputs, Leff et al., 2018). Over the last decade, the devel­ soil functioning, notably in litter decomposition (Santos and Whitford, opment of biochemical tracers to identify trophic links provided novel 1981; Hattenschwiler€ et al., 2005; Srivastava et al., 2009) and C and N opportunities to describe complex soil food webs with increasing pre­ cycling (Ingham et al., 1985; de Vries et al., 2013, Morrien€ et al., 2017). cision (Traugott et al., 2013; Potapov et al., 2018; Ruess et al., 2007; More precisely, higher trophic levels were recently suggested to act as Ruess and Müller-Navarra, 2019) and contributed to highlight the important determinant of the soil microbiome (Thakur and Geisen, importance of trophic regulation in soils. Yet, the major challenge re­ 2019), and thus indirectly drive the central role of microbial mains to understand the drivers of the trophic interactions. * Corresponding author. E-mail address: [email protected] (A. Erktan). https://doi.org/10.1016/j.soilbio.2020.107876 Received 18 June 2019; Received in revised form 26 May 2020; Accepted 29 May 2020 Available online 7 June 2020 0038-0717/© 2020 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). A. Erktan et al. Soil Biology and Biochemistry 148 (2020) 107876 Findings accumulated in the last decade on soil food web structure pools, and their incorporation in food webs further confirms the hy­ and soil C dynamics suggest that the physical structure of soil functions pothesized importance of physical accessibility. In the study of Pausch as important driver of trophic interactions in belowground commu­ et al. (2016), bacteria constituted the dominant C pool, but fungal C was nities. First, the turnover of organic compounds has been identifiedto be more intensively channeled to higher trophic levels. This matches well mainly driven by their physical protection in organo-mineral associa­ with the fact that fungi preferably grow in large air-filled pores (>100 tions or small pores (Dungait et al., 2012; Basile-Doelsch et al., 2020), μm, Otten et al., 2001), whereas a large part of bacteria are thought to invalidating the long-lasting vision that C turnover is mainly driven by live in micropores (<1.2 μm; Hassink et al., 1993), and thus be less chemical properties of organic matter, notably recalcitrance (Gleixner, accessible to soil microbial consumers. Finally, soil food webs are 2013). Whether organic C enters the soil food web thus is increasingly characterised by the dominance of omnivorous species with a wide food thought to be driven by its accessibility to microbiota and soil animals spectrum (Maraun et al., 1998; Scheu and Setal€ a,€ 2002; Thompson et al., (Dungait et al., 2012; Briones, 2018). Another important finding that 2007; Digel et al., 2014; Briones, 2018; Maraun and Scheu, 2000). changed our vision on the structure and functioning of soil food webs is Notably, switches in diet have been observed in response to changes in the importance of root-derived C in fueling soil food webs (Pollierer microhabitats for collembolans and mites that became more generalist et al., 2007; Ferlian et al., 2015; Li et al., 2020). Contrary to litter on the feeders as fungi availability decreased (Anderson, 1978; Teuben and surface of the soil, roots are embedded in the soil matrix, and the Smidt, 1992). Altogether, recent findingspoint to the important role of acquisition of root-derived resources thus obligatory poses the question soil physical structure for trophic interactions. However, soil structure of their physical accessibility in the opaque and labyrinthine soil matrix. has not been integrated into mainstream research of soil food web The lack of relation between the C pool size, namely bacterial vs. fungal ecology. At least in part this might be due to the opacity of soil and the Fig. 1. General overview of the effects of soil physical structure on trophic interactions and consequences for soil biodiversity. Upper panel: Soil physical structure drives sensing and access to re­ sources via providing refuge and limiting the mobility of the soil organisms in the soil matrix. Retroactively, trophic interactions contribute to the formation of soil physical structure via relocating and mixing mineral and organic compounds. Restrictions of interactions between consumers and food resources/prey in soil contribute to the co-existence of a high diversity of soil organisms in small volumes of soil. Lower panel: At the microbial level, low mobile organisms are speci­ alised in consuming certain food resources and the ability to form dormant stages under unfavorable conditions, allowing coexistence of a wide diversity of food specialists. At the mesofauna level, most organ­ isms are unable to form dormant stages and are food generalists, allowing them to consume what is present and accessible. Low mobility and physical habitat constraints enable weak and strong competitors to co- exist. Overall, restriction of sensing and accessibility of resources/prey imposed by the soil physical struc­ ture on trophic interactions enable the co-existence of wide diversity of microbiota, meso- and macrofauna. 2 A. Erktan et al. Soil Biology and Biochemistry 148 (2020) 107876 exceedingly complex pore spaces that limit direct in situ observation of resources/prey is highly conserved across nematode groups (Rasmann trophic interactions and their variations