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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

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ETH Library Soil Biology and Biochemistry 148 (2020) 107876

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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 with soil structure. et al., 2012), suggesting its importance for fitness. Our main hypothesis is that restrictions imposed on soil organisms’ The soil is not only a dark place, it is also a complex labyrinth that ability to sense and access food resources/prey by soil physical structure hinders the transport of volatiles and the movement of consumers to­ essentially shape trophic interactions in soil. Here, we mainly describe ward food resources/prey. A number of studies have focused on the role the soil physical structure in terms of pore space, as pores set the habitat of volatiles in vitro (Bengtsson et al., 1988; Wood et al., 2001; Ali et al., and pathways where most soil organisms (except ecosystem engineers) 2011; Staaden et al., 2011; Brückner et al., 2018), but ignored the role of can move, sense and access resources/prey, as well as hide from pred­ soil structure in modulating the distribution and efficacy of these com­ ators (Elliott and Coleman, 1988). Pores are the air or water-filled vol­ pounds under fieldconditions. We review here studies that investigated ume left by solid soil material (mineral and organic; Hillel, 2004; Rabot attraction by volatiles under more realistic settings, and highlight the et al., 2018) generally assembled in form of soil aggregates (Tisdall and main mechanisms underlying the effect of soil structure on Oades, 1982; Yudina and Kuzyakov, 2019). We mainly focus on soil volatile-mediated food sensing. First, the soil physical structure overall organisms unable to create pores themselves, such as protists, nema­ reduces the distance over which food sensing via volatile detection oc­ todes and microarthropods, and thereby essentially depend on existing curs in soil (Fig. 2). Under real soil conditions, nematodes are able to pore space forming their microhabitat (Elliott and Coleman, 1988). This detect a food source over a distance up to 50 cm, with a travel speed contrasts geophageous organisms, such as earthworms, which create ranging from 0.03 to 0.15 cm per hour (Dusenbery, 1983; Rasmann pores by deforming the soil by borrowing or by ingesting soil and thus et al., 2005; Ackermann et al., 2016). For comparison, when tests were engineer their own microhabitat (Capowiez et al., 2012; Bottinelli et al., conducted on agar plates without restrictions on volatile transport and 2015; Ruiz and Or, 2018), and are thus excluded from the scope of this movement of nematodes, average travel speed was much higher, up to review. We further hypothesize that feeding preferences of soil micro­ 1.5 cm per hour (Andrew and Nicholas, 1976). biota and mesofauna are likely to have evolved in face of restrictions of Volatiles often comprise low molecular weight compounds with high food sensing and accessibility. These soil organisms hence may consume vapor pressure and low boiling point, thus enabling rapid diffusion over what is available locally in the soil pore volume accessible to them. This large distances (Baldwin et al., 2006) and conferring their importance soil pore volume thereby definestheir physical niche and limits foraging for long-range chemotaxis. Volatiles are transported in soils by diffusion for more favorable resources. and advection (Minnich and Schumacher, 1993) in both the gas and The primary objective of this review is to delineate how soil physical aqueous phase. Volatiles are thus travelling through air-filled and structure influencestrophic interactions (Fig. 1). We firsthighlight how water-filled pores (Aochi and Farmer, 2005; Asensio et al., 2008). In soil structure influencesthe ability of soil microbiota and mesofauna to general, the well-known effects of soil physical structure on gas and sense volatiles/chemical signals and access their food resources/prey. water transport are thus expected to impact the transport of volatiles as Then, we detail the specific role of the dynamic aqueous phase (soil well and modulate the effective distances over which consumer­ water) in restricting the living and feeding space accessible to aquatic s/predators can sense food sources/prey emitting these volatiles. In organisms, notably protists and nematodes. We further discuss how particular, the role of pore size, connectivity, tortuosity and soil hy­ constraints imposed on trophic relations by the soil structure can shed dration state (soil water content or matric potential) influenceboth gas light on the “enigma of soil animal species diversity” (Anderson, 1975), and water transport in soil (Moldrup et al., 2000, 2001; Young et al., stressing the high density and diversity of organisms despite feeding on 2001; Ebrahimi and Or, 2015; Fig. 2). In addition, water retention and similar resources co-occurring in small volumes of soil. To conclude, we transport in soil is affected by hydrophilic and hydrophobic properties of highlight effects of soil physical structure on trophic interactions and soil surfaces (Ellerbrock et al., 2005), which also affect volatile potential feedback effects. Finally, we outline challenges for interdisci­ transport. plinary research merging soil physics and soil food web ecology. In The soil physical structure and hydration state jointly affect volatile- particular, we discuss novel technologies to achieve this goal, inspired mediated sensing in soils because of the slow diffusion of volatiles in the from the growing interdisciplinary community working on in­ aqueous phase, which is about 10,000 times slower than in the gas phase terrelationships between soil physics and soil microbial ecology (Nunan (Moldrup et al., 2000; Minnich and Schumacher, 1993). This affects et al., 2003; Ruamps et al., 2011; Vos et al., 2013; Tecon and Or, 2017; signal travel distance and magnitude, and thereby likely impacts the Baveye et al., 2018). sensing ability of aquatic soil organisms such as protists and nematodes (Fig. 2, lower panel). In the meantime, water-filled pores are essential 2. Soil structure as determinant of how soil organisms sense and for soil aquatic organisms, as they define their habitat and delineate access food resources/prey where they can move. From drier to wetter conditions, we further detail how such dual and opposite effects of the soil hydratation status on 2.1. Sensing food resources/prey in the opaque soil labyrinth volatile transport vs. aquatic microbiota mobility impact volatile-mediated sensing. As soil water potential decreases, large pores Soil is a dark labyrinth and visual detection of prey is unlikely to play drain first, and aquatic organisms become restricted to small and a dominant role below the soil surface. The loss of visual detection or­ disconnected pores. Pore dead-ends and discontinuities in the aqueous gans in collembolans living in soil while canopy collembolans have eyes phase act as barriers and increase the tortuosity of the travel distance is an illustration of this phenomenon (Salmon et al., 2014). Chemical (Tecon and Or, 2017). Moreover, the movement in thin water films communication seems much more developed in soil with volatiles could be significantlyhindered (Otobe et al., 2004; Tecon and Or, 2016). serving as the primary compounds used by consumers/predators to Consequently, the reduced mobility and tortuous path hinder movement locate their food resources/prey. For example, nematodes (McCallum toward volatile emitting food resources under low matric potential and and Dusenbery, 1992; Young et al., 1998; Rasmann et al., 2012), col­ thereby reduce foraging ranges of nematodes (Griffiths et al., 1995; lembolans (Bengtsson et al., 1988, 1991; Wood et al., 2001) and mites Young et al., 1998). On the other hand, under drier conditions, gas (Brückner et al., 2018) showed preferential or avoidance movement diffusion through connected air-filled pores increases and facilitates toward certain food resources/microbial prey driven by volatiles. The faster and longer range transport of volatiles (Minnich and Schumacher, olfactive ability of nematodes is related to their sensing organs, papilla 1993; Tyc et al., 2015). As a consequence, in drier soils nematodes can and setae, connected to chemosensory neurons (Bargmann and Horvitz, better sense their food resources/prey due to rapid diffusion of volatiles, 1993), which can be considered as adaptation to sense food resource­ but may not be able to efficiently migrate toward these sources due to s/prey in the soil darkness. Phylogenetic analyses of nematodes revealed restrictions on their movement (Fig. 2, lower panel). Conversely, at high that the ability to use olfactive cues, notably CO2, to locate food soil matric potential, nematode movement increases through the

3 A. Erktan et al. Soil Biology and Biochemistry 148 (2020) 107876

Fig. 2. Influence of soil physical structure on volatile-mediated prey sensing. Main panel: Volatile transport through the soil matrix from a fungal resource to consumers (collembolans, mites, earth­ worms). The upper panel shows mechanisms limiting the transport of volatiles through the soil matrix, namely adsorption to mineral surfaces, accumulation in dead-end pores, reduced transport through small pore neck and in water filled pores. The lower panel specifies the balance between sensing ability and resource accessibility for aquatic organisms, namely a nematode consumer and its bacterial prey. Under wetter conditions, water-filled pores dominate, resulting in slow diffusion of volatiles (weakening prey sensing), but consumers are less restricted to move towards the prey. Under drier conditions, moisture is concentrated in small pores, resulting in rapid diffusion of volatiles in air-filled pores (facili­ tating prey sensing) while consumers are strongly restricted in their movement towards prey.

connected water-filled pore space, but volatile diffusion is more 1993; Aochi and Farmer, 2005; Insam and Seewald, 2010). Higher restricted (Fig. 2, lower panel). Both extreme cases favor localised sorption rates are expected to reduce the diffusion of volatiles and thus foraging, either because of restricted mobility of aquatic organisms or the ability of consumers/predators to sense their food resources/prey in because of low sensing ability. Intermediate optimal hydration condi­ the soil matrix. In some cases, volatiles sorbed to minerals may be tions simultaneously allow movement of aquatic soil organisms through subject to abiotic degradation, catalyzed by the mineral surface (Min­ connected water-filled pores and the diffusion of volatiles through nich and Schumacher, 1993), further limiting their diffusion and the connected air-filledpores and seem to coincide with optimal conditions sensing by consumers. for aerobic microbial activity in soil (Or et al., 2007; Tecon and Or, While focusing here primarily on volatiles due to their important role 2017). in sensing of prey by consumers in soils, volatiles as well can play a role Another mechanism underlying the influence of soil physical struc­ in consumer - consumer communication. For example, bacteria feeding ture on volatile-mediated sensing of food resources by consumers is the on root exudates were shown to produce volatile compounds informing sorption of volatile compounds to soil particles, limiting their dispersion starving bacteria in their neighborhood about the presence of food re­ (Fig. 2, upper panel). As described in Effmert et al. (2012), sorption of sources and thereby modulate their activity (Schmidt et al., 2015; volatiles in soil depends on the polarity of the compounds as well as on Schulz-Bohm et al., 2015; Tyc et al., 2017). This example highlights that texture, architecture and humidity of the soil. Importantly, effects of volatile-mediated communication between bacteria in soil also affects humidity on sorption processes depend on scale, with high humidity trophic interactions by affecting adaptation of small mobile consumers reducing sorption of volatiles to minerals at microscale, but increasing to the scarcity and temporal variation in the availability of food re­ sorption to organic matter at macroscale (Minnich and Schumacher, sources in soil. Moreover, concerning short-range communication, other

4 A. Erktan et al. Soil Biology and Biochemistry 148 (2020) 107876 compounds, such as water-soluble molecules, can also act as attractants appears to greatly affect the feeding regime of microarthropods, pre­ or repellants of consumers to certain food resources in soil (Venturi and sumably these effects are linked to the accessibility of food resource­ þ Keel, 2016). Notably, this is the case of Na and pyrine, acting as s/prey. We review here experimental evidence on how soil structure attractant for nematodes (Grewal and Wright, 1992), while some bac­ drives the way consumers access food resources/prey, applying to a terial toxins and antibiotics act as repellent (Dusenbery, 1983). As they wide range of soil organisms not only microarthropods. only diffuse in the aqueous phase, they are expected to be affected by similar mechanisms that determine water retention and transport 2.2.1. Small pores protect resources/prey from consumers/predators through the soil. Soil organisms that are unable to directly create their own pores e.g., bacteria, fungi, protists, nematodes and microarthropods, depend on 2.2. Access to food resources/prey in the soil labyrinth access via pore space and aquatic organisms rely on the continuity of the aqueous phase. Despite their small size, micron-size bacteria are no A simple but informative example on the role of soil microstructure exception. It has been estimated that 15–50% of soil pore spaces are for food accessibility in soil comes from the observation that minute inaccessible to bacteria due to pore necks narrower than 0.2 μm (Has­ changes in microstructure may significantlymodify food relationships of sink et al., 1993; Chenu and Stotzky, 2002; Fig. 3). Removal of such collembolans (Anderson, 1978), whereas large-scale changes in land restrictions at the microscale are thought to contribute to explain the cover, e.g. from beech to spruce forest, had little impact on what col­ flush of CO2 when tilling soil and crushing soil aggregates exposing lembolans consume (Ferlian et al., 2015). Soil microstructure thus carbon occluded in aggregates and making it accessible to

Fig. 3. Size segregation and refuge of small organisms. Small pores serve as refuge for food resources/prey protecting them from larger-bodied consumers. Dimensions of typical pore size openings providing refuge space are given. Source of pictures: - Bacteria - Dani Or; - Protist, nematode and mite - Margaret McCully.

5 A. Erktan et al. Soil Biology and Biochemistry 148 (2020) 107876 microorganisms (Balesdent et al., 2000; Chevallier et al., 2011). Fungi linkages are rare (Ackermann et al., 2016). We argue that soil texture, are also limited in resource accessibility by soil physical structure. and more widely soil structure, should be re-considered as a central Although fungal hyphae are capable of growing across air-filled pores aspect in soil micro-food web studies allowing to explain inconsistencies larger than 10 μm (Effmert et al., 2012), they were shown to preferen­ in experimental and field observations conducted in the past decades tially grow in larger (>100 μm) air-filled pores (Otten et al., 2001; based on soils of contrasting texture. Soufan et al., 2018; Fig. 3). Manipulating pore size by varying soil bulk We further consider tri-partite interactions (bacteria, protist, and density and aggregate size, Otten et al. (2001) showed that when large nematode) to illustrate more complex relations between soil structure pores > 100 μm were replaced by smaller pores < 30 μm fungal colo­ and trophic interactions in the micro-food web. Using microcosms Rønn nisation was slower and the volume of soil accessible for fungi to acquire et al. (1995) showed that reducing soil pore size by increasing the clay nutrients was significantlyreduced. Using a micromodel soil mimicking content benefitssmall protists (amoebae), whereas nematodes benefited the heterogeneous soil matrix, Soufan et al. (2018) provided more from coarse-textured soils. The authors suggested two main reasons to detailed insight into the growth of fungi in realistic pores (>100 μm) and explain these results. The more obvious explanation is that protist showed that fungal hyphae tended to follow pore walls and kept elon­ abundance was directly related to their accessibility to nematodes, with gating until hitting the pore wall, presumably facilitating resource lower predation pressure in fine-texturedsoils because of the presence of capture. Overall, these examples highlight that accessibility to food re­ pores <30 μm offering protection to protists. In this case, increased sources of both bacteria and fungi is restricted by the presence of small top-down regulation has been assumed to be the main driver of the pores or narrow pore necks preventing them to access resources (Fig. 3). decrease in protist abundance in coarse-texture soils. Alternatively, the In addition, associations of organic compounds to mineral phases lower abundance of protists in coarse-textured soils may have resulted further limit the accessibility of food resources to microbes. Organic from the higher abundance of large air-filledpores, beneficialfor fungal compounds serving as food resource for microbes, can adsorb onto the growth and hence favoring fungal-feeding nematodes. The lower surface of minerals (notably clay; Kleber et al., 2007), co-precipitate abundance of protists in coarse-textured soils thus may have resulted with Fe or Al cations to form secondary mineral phases (Fe and Al from reduced bacterial populations serving as food for protists. In this oxyhydroxides; Rasmussen et al., 2018; Tamrat et al., 2019), or associate case, bottom-up control has been suggested to explain the variations in þ with di- or trivalent ions, notably Ca2 (Rasmussen et al., 2018; Rowley the abundances of protists and nematodes. This example nicely shows et al., 2018). When such organo-mineral associations form, the organic that the interplay between soil physical structure and trophic in­ compounds are considered to be “protected”, with positive effects on C teractions including more than two actors may result in non-trivial storage, because the accessibility of the organic compounds for micro­ outcomes, with either top-down or bottom-up control being the major bial consumption is reduced (for details see Basile-Doelsch et al., 2020). driver of trophic interactions. In some cases, some microbes can access to organic compounds in Nematodes themselves are consumed by larger organisms and also organo-mineral associations, but it requires the secretion of specific benefitfrom refuge related to the soil physical structure. In a microcosm enzymes or organic ligands. For example, organic compounds adsorbed experiment, Hohberg and Traunspurger (2005) showed that predation onto mineral surfaces can be consumed by microbes if they excrete en­ by tardigrades (Macrobiotus richtersi) on nematodes was significantly zymes with their affinityto the organic compounds being higher than its reduced in a sand - soil matrix compared to agar substrate. Similar ob­ adsorption affinity (Basile-Doelsch et al., 2020). Overall, servations were made by Beier et al. (2004) studying predation on organo-mineral associations are common in soil, in which the solid nematodes by plathelminths (Dugesia gonocephala). They showed that phase comprises 90–99% mineral elements (Calvet et al., 2011), and predation effectiveness increased with larger and less protective pores. further reduce the accessibility of organic compounds to microbes. Overall, trophic interactions in the micro-food web generally occur in The main microbial predators in the soil micro-food web are protists pores <150 μm and there is experimental evidence that food resource­ (>5 μm) and nematodes (diameter ca. 10 μm, length ca. 1000 μm). Their s/prey of any size are protected from consumers/predators when located large bodies (relative to their prey) restrict their access to small pores in pores too small to allow the latter to enter. where bacteria and fungi may findrefuge. In particular, protists, notably Larger non-aquatic organisms such as microarthropods are thought amoebae (Acanthamoeba sp.; Vargas and Hattori, 1986), ciliates (Col­ to colonize air-filled pores >50 μm (Joschko, 1990; Heisler and Kaiser, poda sp.; Rutherford and Juma, 1992) and small flagellates (Kuikman 1995), but given the wide range of body size of microarthropods, from et al., 1991), may access water-filled pores with openings down to 2–3 60 to 5000 μm body length for mites and 120–17,000 μm for collem­ μm (Fig. 2 A). Pores with smaller opening thus function as refuge for bolans (Orgiazzi et al., 2016), a wide range of pores > 50 μm serves as bacteria and most bacteria - protist interactions are thought to occur in habitat. It is known that microarthropod densities in temperate soils the water filmof pores ranging in diameter from 2 to 10 μm (Rutherford relate to differences in pore size, as evidenced by comparing and Juma, 1992). Such microscale sheltering affects predator - prey coarse-textured and fine-textured soils (Van de Bund, 1970; Vree­ dynamics of protists feeding on bacteria. In fact, preyed upon by protists ken-Buijs et al., 1998) or compacted vs. uncompacted soils (Heisler and the survival of bacteria was increased when soil was mixed with clay, Kaiser, 1995). Microarthropod density was shown to be higher in resulting in reduced pore space and size (Heijnen et al., 1988, 1993). By coarse-textured soils (Vreeken-Buijs et al., 1998) and positively related controlling the colonisation of pores of different size by bacteria, Wright to relatively large pores, typically of a few hundred microns for et al. (1995) confirmed that predation by ciliate protists was more temperate European species (Vreeken-Buijs et al., 1998; Ducarme et al., pronounced in larger (6–30 μm) compared to smaller pores (<6 μm). 2004; Nielsen et al., 2008). These pores presumably are large enough to Overall, protist populations are favored in coarse textured soils (Ruth­ be colonised by microarthropods, contain food resources accessible to erford and Juma, 1992), associated with higher predation rates of bac­ them and provide protection from predators (Fig. 3). We expect that teria (Gupta and Germida, 1989), compared to fine-texturedsoils, where such an optimal pore size range, offering a tradeoff between access to increased presence of small pores (<2–3 μm) serve as refuge for bacteria. food resources and sheltering from predators, is widespread, but the Nematodes are larger than protists and are thought to access bacteria in specificpore size range depends on species and needs to be investigated. pores down to about 30 μm (Jones and Thomasson, 1976; Fig. 3). Under More detailed information on the minimal dimension of pore openings fieldconditions, nematode populations were favored in coarse-textured allowing microarthropods access to food resources/microbial prey soils (Ingham et al., 1982; Hassink et al., 1993), presumably because of needs as well to be studied. It is clear that a large part of bacterial rich higher accessibility of bacterial prey. Altogether, these experimental habitats, located in pores <1.2 μm (Hassink et al., 1993), are not evidences demonstrate that textural pores are essential for sheltering accessible to microarthropods simply because of evident size restriction effects of microbiota. Remarkably, these studies are all rather old and (Vreeken-Buijs et al., 1998), even for the smallest individuals (Fig. 3). more recent studies focusing on soil structure - soil micro-food web However, many microarthropods ingest bacteria (Pollierer et al., 2012),

6 A. Erktan et al. Soil Biology and Biochemistry 148 (2020) 107876 even though they often are not their preferred food source (Ruess et al., pores, presumably to prevent damage of their wax coat (Choudhuri, 2007). We suggest that bacteria are essentially ingested as by-catch 1961). Overall, we argue that the simple idea that body size driven re­ when microarthropods feed on microbial hotspots, such as detritu­ strictions to enter pores of corresponding dimension is not the main sphere or rhizosphere, present in pores large enough to allow them to determinant of the accessibility of food resources to microarthropods in enter. Moreover, it may not simply be that smaller bodied micro­ soil. arthropods preferably feed in smaller pores, while larger-bodied ones Even though not directly related to the soil physical structure, the feed in larger pores. Indeed, microarthropods of different body size, presence of moss (Vucic-Pestic et al., 2010) or beech cupules (Melgui­ including predatory mites, non-cryptostigmatid mites and omnivorous zo-Ruiz et al., 2016) has been shown to provide refuge for springtails collembolans, were all associated with pores >90 μm in the case study of against hunting spiders and other predators. Together, these results Vreeken-Buijs et al. (1998), although non-cryptostigmatid mites had provide evidence that differences in pore size affects predator – prey much smaller bodies and could enter smaller pores. Presumably, this interactions by providing refuge for prey at virtually all scales of body preference for relatively large pores stems from the preferential growth size of predators and prey. Similar relationships presumably apply to of fungi in large (>100 μm) air-filled pores (see above). Bottom-up dead organic matter/litter resources and their accessibility to consumers control associated with the location of food resources in large pores in soil. thus may be more important in driving the distribution of micro­ arthropods in soil, regardless of their size, than effects related to niche 2.2.2. Soil pore space restricts the movement of soil organisms and shapes partitioning due to size segregation. Whether this is a general mecha­ interactions between consumers/predators and food resources/prey nism remains to be experimentally tested. Other reasons may be Unless for ecosystem engineers, mobility and dispersal of most or­ responsible for the lack of relation between pore size and micro­ ganisms in soil is limited and this is true for bacteria (1.6–9.4 mm per arthropod size. For example collembolans tend to avoid entering narrow day; Bashan and Levanony, 1987; Ebrahimi and Or, 2014; Juyal et al.,

Fig. 4. Restriction of mobility and co-existence of food resources/prey and consumers in close vi­ cinity. Low mobility of soil organisms (here collem­ bolans, fungi, nematodes and bacteria) reduces opportunities for consumers to encounter food re­ sources/prey. Blue arrows indicate movement of in­ dividuals. Length of blue arrows represents distances typically bridged per day. The lower panel highlights that the presence of small pore necks reduces the accessibility (green striped area) of prey (fungal hy­ phae) to consumers (collembolans) although large air- filled pores colonized by fungi are present. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

7 A. Erktan et al. Soil Biology and Biochemistry 148 (2020) 107876

2018), fungi (1–7 mm per day; Otten et al., 2001), nematodes (8 mm per accessibility of food resources to decomposers, and thus soil C turnover day; Ackermann et al., 2016) and microarthropods (typically < 1 cm per (Schmidt et al., 2011; Dungait et al., 2012). Further, linking this concept day; Ojala and Huhta, 2001; Lehmitz et al., 2012). This low dispersal in to land management practices, such as tillage or land abandonment, the soil matrix restricts the ability of consumers/predators to reach food known to influencethe pore connectivity (Lucas et al., 2020), may allow resources/prey, contrasting aquatic and aboveground habitats where understanding why C inputs and soil C storage often are not closely movement is far less restricted (Fig. 4). Importantly, it is not the size of related (Basile-Doelsch et al., 2020). pores which is crucial here, as detailed above for the “refuge” function, but their connectivity. The latter is influencedby pore geometry, and the distribution of water at microscale, notably the connectivity of the water 2.3. Water in soil drives trophic interactions film (see section 2.3). For example, even though large air-filled pores (>50 μm) representing the habitat of microarthropods are present, if Aquatic and semi-aquatic microorganisms, such as protists and their connectivity is low, microarthropod movement will be restricted, nematodes, are restricted by the size and connectivity of the aqueous potentially resulting in heavy colonisation of these pores by fungi habitats they live in. As large pores drain first, small pores, water-films (Fig. 4, lower panel). Such restrictions are expected to affect all soil and pendular water in grain contact become the primary habitat for organisms, especially those unable to create their own pore space, but these organisms under drying conditions (Fig. 2 lower panels and Fig. 3). experimental evidence is scarce. In a recent experiment, bacterial spread Subsequently, prey may become isolated from predators because they and colonisation (in absence of water movement) were shown to depend occupy disconnected water filled pores, resulting in reduced top-down on characteristics of soil pores, notably pore connectivity (Juyal et al., control. Alternatively, predators and prey may be confined to the 2020). In this study, the density of bacteria (Pseudomonas fluorescens) same shrinking aqueous microhabitats resulting in enhanced predation decreased by about half when soil bulk density increased from 1.3 g opportunities, enhancing top-down regulation. Such effects have been À 3 À 3 cm to 1.5 g cm , and the solid-pore interfacial area and pore con­ demonstrated by varying soil matric potential but mostly in laboratory nectivity decreased. Changes in pore geometry were supposed to be the studies. For example, studies where the matric potential (expressed as main driver of restricted bacterial spread, and ultimately limit the access water tension) determined the ability of protists (ciliates) to move into of bacteria to food sources. A more basic study focusing on pla­ pore spaces and thus reach bacterial prey (Darbyshire, 1976; Vargas and thelminths (Dugesia gonocephala) preying on nematodes in sand vs. agar Hattori, 1986; Fig. 5). The mobility and the portion of water-filledpores suggested that increased search and handling time of plathelminths by constituting the habitat of protists was reduced as soil matric potential reduced visual, mechanical and/or chemical detection of prey in sand decreased. At relatively high matric potential (<10 kPa), water film contribute to lower predation efficiency in sand vs. agar (Beier et al., connectivity allowed protists to move into the inter-aggregate pore 2004). However, there is no experimental evidence on the role of pore space, exploiting the full range of pores and thereby exerting maximum connectivity on trophic interactions involving larger soil organisms, top-down control on bacterial prey (Vargas and Hattori, 1986). By neither for most of the soil microbiota and mesofauna. contrast, extensive refuge space was formed in drier soil at lower matric Technical difficulties are a major reason which prevented re­ potential (>120 kPa), where protists were confined to small internal searchers so far to investigate the role of pore connectivity for trophic pore space within aggregates as only those pores remained moist interactions involving microbiota and mesofauna in situ and in experi­ (Fig. 5). Water distribution within the soil matrix as well may result in mental studies. Tools to study overall soil pore connectivity (using X-ray promoting predation by containing prey and predators in small microtomography), considering pores ranging from a few microns to water-filledpores. This has been exemplifiedfor nematodes, which rely several hundreds of microns are only yet starting to be developed (Lucas on water-filled pores as habitat (Fig. 5). In particular, bacterivore et al., 2020) and may allow to link pore connectivity to trophic in­ nematodes concentrated in intra-aggregate pores after the teractions in situ. In experimental studies, soil of different texture has inter-aggregate pore space dried up (Neher, 2010), and this facilitated been used widely to investigate the role of textural pore size for predation and resulted in higher nutrient turnover and carbon miner­ (simplified) trophic interactions (Heijnen et al., 1988; Rutherford and alisation (Savin et al., 2001). Similar observations have been made with Juma, 1992; Rønn et al., 1995). These textural pores can vary in terms of protists and their microbial prey, highlighting the role of habitat space connectivity (Lucas et al., 2020), but their size mostly remains below a in determining predator – prey interactions (Finlay and Fenchel, 2001). few hundred microns, which does not allow investigating larger soil As a consequence, top-down regulation is increased because consumers organisms such as microarthropods and their associated predators. are confined with their prey in small pore volumes. Overall, water dis­ Contrary to textural pores, structural pores are much more difficult to tribution at the microscale determines the co-location of consumers and recreate in a reproducible manner. Wet and dry cycles create cracks and prey, resulting either in enhanced or reduced top-down regulation by increase pore connectivity (Koestel, 2020) and could be further used to driving encounter probabilities. set up microcosm experiments with increasing connectivity of relatively In case of larger non-aquatic organisms, similar confiningeffects may large structural pores (more than few hundred microns). Further, con­ occur when the activity and movement of these organisms are driven by trol of the connectivity of the aqueous phase could be achieved by soil moisture. For example, at drier conditions collembolans (as prey) controlling matric potential under laboratory conditions. and centipedes (as predators) concentrate in moist microhabitats which Despite technical difficultiesand overall low experimental evidence, likely facilitates predator – prey interactions (Verdeny-Vilalta and we argue that the role of pore connectivity on trophic interactions is of Moya-Larano,~ 2014). When incubating prey and predator together on major importance. Overall, the increase in pore connectivity is likely to 2D surfaces differing in moisture, predators caused the prey to shift to increase the strength of interactions between consumers and resources, dryer places. This shift in prey behavior suggests that in a more realistic thereby enhancing both bottom-up control of predators by prey and top- 3D soil matrix prey species may move to microsites avoided by or down control of prey by predators as well as competition between inaccessible to predators. Soil structure thus provides a labyrinth habitat consumers. Whether changes in bottom-up and top-down regulation space, where prey may seek for microsites fulfilling their physiological ultimately result in enhanced or decreased prey vs. predator population requirements in terms of moisture and being unfavorable for or inac­ density is likely to depend on their traits (Thakur and Geisen, 2019). cessible to predators. A large part of soil meso- and macrofauna need Future experimental work including a variety of soil organism groups moisture as shown by sharp decrease in soil animal diversity and and trophic levels is needed to test and refine these predictions. We abundance under severe drought (Lindberg et al., 2002; Eisenhauer argue that integrating the concept of “biological accessibility” into soil et al., 2012; Peguero et al., 2019). Thus, we expect that moist soil spots ecological studies may help in mechanistically understanding trophic act as attractants of meso- and macrofauna prey and predators, and thus interactions in soil and how soil physical structure determines the represent areas of high encounter probability and trophic interactions.

8 A. Erktan et al. Soil Biology and Biochemistry 148 (2020) 107876

Fig. 5. The role of water in prey accessibility. The presence of water in pores defines the habitat of aquatic organisms in soil. Under wet conditions (left side), consumers (protists and nematodes) can move in large water filled pores and benefit from extended access to bacterial colonies. Under drier conditions (right side), bacterial prey benefits from refuge from consumers due to disconnection of water filled pores. On the other hand, predation may be increased due to confinement of e.g., bacterial prey and nematode predator concentrated in small water filled pores while the larger pores dried up.

3. Adaptations to feed in the soil labyrinth and consequences for pores inaccessible to nematodes and then were fed by nematodes when soil biodiversity moving into larger pores (>30 μm). Even though not specialised in feeding on protists, we consider the ability of nematodes to ingest and 3.1. Adaptations of consumers and prey to feeding constraints inherent to digest protists as an evolutionary advantage indirectly enhancing access the opaque and labyrinthine nature of soil of nematodes to bacterial prey (Fig. 6C). Finally, the dominance of omnivory and food flexibility among microarthropods (Ponge, 1991; Feeding in soil is constrained because sensing and accessibility of Maraun et al., 1998; Briones et al., 2010; Brose and Scheu, 2014; resources is restricted by soil structure. Specificitiesin the feeding mode Briones, 2018) may as well be viewed as an adaptation to the scarcity of certain soil organisms indicate evolutionary adaptations to these and discontinuous accessibility of food resources in space and time in constraints. Without aiming to be exhaustive, we detail here some the soil matrix. Being food generalist is advantageous as it allows relevant examples taken from various taxa. Our firstexample deals with feeding on a variety of resources when movement is restricted and the protists. Microscopic analyses of soil thin sections allowed to visualise animals are confined to certain pore space limiting access to microbial that amoebae can extend their pseudopods into pores down to 1 μm prey (Fig. 6D). width and extend pseudopods in these pores to a depth of 20 μm to catch Adaptations also concern prey species by increasing protection from bacteria in pores typically considered to be inaccessible to predators predators. For example, soil structure can induce changes in prey (Foster and Dormaar, 1991; Fig. 6A). We argue that the soft body of mobility resulting in enhanced avoidance of predators. By comparing amoebae allowing them to adopt virtually any shape is an adaptation nematode mobility on agar and in sand substrate, Hohberg and Traun­ enhancing prey accessibility in the soil (or sediment) matrix and thereby spurger (2005) showed that nematode movement in sand was increased the fitness of these organisms (Giometto et al., 2013). For nematodes, and related to water content and the presence of soil particles. Maximum that are larger than protists, tri-partite interactions between bacteria, movement in saturated conditions is predicted when the size of soil protists and nematodes may be considered as adaptation allowing them particles is about one third of the length of nematodes (Nicholas, 1975), to benefit from the access to hidden bacterial prey by protists. Indeed, i.e. in finesand substrate with particles of a diameter of about 100 μm. the growth of nematodes (Mesodiplogaster and Caenorhabditis elegans) Low predation rates of nematodes in sand substrate presumably are due was enhanced in presence of protists (amoebae and flagellates; Elliott to nematodes avoiding large pores where their movement is restricted et al., 1980; Bjørnlund et al., 2009). Interestingly, this was more pro­ (Otobe et al., 2004) and where they may be attacked by predators. The nounced in fine-textured soil, where fine pores (<30 μm) are more suggested preference of nematodes for small pores (ca. 40 μm) and their abundant. Presumably, protists exploited bacterial prey in these fine enhanced mobility in these pores thus may be considered as adaptation

9 A. Erktan et al. Soil Biology and Biochemistry 148 (2020) 107876

Fig. 6. Adaptations to feed in the dark soil laby­ rinth. Panels (A), (C) and (D) illustrate adaptations of consumers to access food resources. (A): Protists (amoebae) can extend pseudopods into pores of 1 μm diameter up to 20 μm in length, allowing them to catch bacterial prey inaccessible to other predators. (C): Tri-partite interactions provide access to bacterial prey for nematodes through smaller sized protists functioning as intermediate predators. (D): Domi­ nance of generalist feeders among microarthropods as adaptation to the discontinuous availability of specific resources in soil. Panel (B) illustrate adaptation of prey to avoid predators. Example of enhanced pred­ ator (tardigrade) avoidance due to increased mobility of nematodes preferring small pores and being more mobile in these small pores.

increasing predator avoidance in the soil matrix (Fig. 6B). 2012). In particular by influencing oxygen accessibility, soil structure promotes the co-existence of aerobic and anaerobic bacterial commu­ nities depending on their location in the soil matrix (Tecon and Or, 3.2. Consequences of the soil physical structure/trophic relationships links 2017; Borer et al., 2018). Thus, by affecting moisture, oxygen and food for soil biodiversity resource accessibility, soil physical structure selects for certain micro­ bial species and communities (Vos et al., 2013; Gupta and Germida, The high abundance and diversity of organisms occurring in small 1989; Tecon and Or, 2017). Remarkably, gradients of resources defined pieces of soil has long been noticed and numerous attempts to explain it by soil physical structure at the microscale promote microbial diversity have been put forward (Anderson, 1975; Ettema and Wardle, 2002; by favoring specialisation to certain combinations of food resources, Bardgett, 2002). Remarkably, soil bulk characteristics, such as pH, soil moisture and oxygen partial pressure conditions (Ruamps et al., 2011; organic carbon content or soil density often failed to explain patterns of Borer et al., 2018; Nunan et al., 2020). Importantly, in case of unfa­ soil diversity, notably microbial diversity (Terrat et al., 2012) and vorable conditions, bacteria can survive for long in dormant stages, and microarthropod trophic niches (Maraun and Scheu, 2000; Ferlian et al., be re-activated when the soil physical structure is modified in a way to 2015). This lack of explanatory power suggests that parameters at other provide more favorable conditions (Sorensen and Shade, 2020). scales are at stake. Given the small size of soil organisms, we argue that By contrast, food specialisation is generally rare in larger and more the physical structure of soil at the micro-scale is an important driver of mobile organisms, such as meso- and macrofauna, which typically are soil diversity, notably because of its role in driving trophic interactions. generalist/food flexible feeders (Ponge, 1991; Maraun et al., 1998; At the micro-scale, soil structure constrains food accessibility, local Scheu and Setal€ a,€ 2002; Digel et al., 2014; Briones, 2018). Contrary to oxygen and moisture conditions, representing major drivers of microbial microbes, these organisms usually are unable to survive for long in diversity and community composition, and thereby of microbial com­ dormant state (Villani et al., 1999) and being food generalists therefore munity structure at the micrometer scale (Kerr et al., 2002; Eilers et al.,

10 A. Erktan et al. Soil Biology and Biochemistry 148 (2020) 107876 is considered of major importance to allow them to consume locally 4. Feedbacks of trophic interactions on soil physical structure available food resources as the soil matrix restricts searching for alter­ native food resources of higher quality. Soil physical structure therefore Soil structure is dynamic and strongly influencedby the activities of is likely to set evolutionary constraints for the diversification of soil soil organisms. However, most studies considered organisms in isolation meso- and macrofauna by hampering the evolution of food specialists and the role of trophic relationships and interactions on soil structure and thereby the diversification of soil animal taxa. However, this does has rarely been in focus of scientific studies (Thakur et al., 2014; Leh­ not mean that the physical structure of soils promotes homogeneity of mann et al., 2017). Even though often not considered as such, the effect soil meso- and macrofauna communities. By limiting interactions be­ of earthworms (Blouin et al., 2013), and more widely geophageous or­ tween potential competitors feeding on similar food resources, soil ganisms in general (Barois et al., 1998; Fujimaki et al., 2010), feeding on physical structure is an important driver of the co-existence of soil an­ microbes by ingesting soil is a trophic interaction with major conse­ imal species and thereby for the high diversity of soil animals. This has quences for the physical structure of soils. For example, the feeding been exemplified in a microcosm experiment showing that micro­ activity of earthworms result in compaction or decompaction (Ruiz arthropod diversity was higher when four litter resources were sepa­ et al., 2017), remodeling of soil pores (Blanchart et al., 1999; Deca€ens rated into four distinct patches in soil compared to when they were and Jim�enez, 2002), changes in water infiltration (Le Bayon et al., mixed in a single patch (Sulkava and Huhta, 1998). This experiment 2002), litter incorporation into the soil matrix (Knollenberg et al., 1985; nicely shows that spatial segregation of resources, combined with Edward and Bohlen, 1995) and dispersal of microbes (Vos et al., 2013). limited movement of microarthropods, facilitates resource exploitation Ecosystem engineers, particularly earthworms, have been extensively by weak competitors, thereby promoting diversity. Similar beneficial studied for their effect on soil physical structure (Blouin et al., 2013; effects of resource patchiness have been demonstrated for Cammeraat and Risch, 2008; Bottinelli et al., 2015; Jouquet et al., bacterial-feeding nematodes reaching lower biomass when litter and 2016). Ultimately, the major effect of ecosystem engineers such as humus were mixed compared to arranged in patches (Mikola and Sul­ earthworms on soil physical structure fundamentally affects virtually all kava, 2001). Moreover, microarthropods can shift their trophic position species in soil and their trophic interactions and this has been well and hence reduce competitive pressure trough niche partitioning appreciated (Eisenhauer, 2010; Ferlian et al., 2018; Frelich et al., 2019). (Anderson, 1975; Gao et al., 2014; Magilton et al., 2019), further By contrast, here we focus on soil micro- and mesofauna not able to limiting competitive exclusion. Altogether, reduced competition due to physically alter soil structure themselves as ecosystem engineers. limited mobility of soil animals in the soil matrix, combined with food Soil micro- and mesofauna species typically cannot drill into the soil generalism, are essential drivers of soil animal diversity and and form pores for their own habitat. Nevertheless, however, they may co-existence. substantially affect the physical structure of soils, notably because many Overall, soil physical structure functions as major driver of soil di­ of them feed on microbes that are key players in forming soil physical versity and act through two distinct mechanisms on microbial and structure (Chenu and Cosentino, 2011). Bacteria and fungi are well mesofauna communities. In microorganisms soil physical structure fa­ known for their role in soil particle cohesion (Chenu, 1989, 1993; Liu vors a wide diversity of microbial food specialists (though with different et al., 2013) and their effect on soil aggregation (Lehmann et al., 2017). degrees of specialisation, notably for bacteria; Nunan et al., 2020) able They usually increase soil particle cohesion through a variety of mech­ to survive for long in dormancy and only becoming active when favor­ anisms, in particular the release of extracellular (polymeric) substances able soil conditions resume, i.e. at “hot moments” (Kuzyakov and Bla­ (Chenu, 1993; Daynes et al., 2012; Zheng et al., 2016). Importantly, godatskaya, 2015). In mesofauna species soil physical structure quality and quantity of extracellular substances vary among microbial promotes food generalists and their co-existence is favored by their strains, leading to differential effects on soil particle cohesion (Cae­ limited mobility, resulting in the survival of weak competitors. Notice­ sar-TonThat et al., 2014; Costa et al., 2018). Microbial-driven soil par­ ably, the importance of the probability of encountering prey/food re­ ticle cohesion can trigger the formation of cracks and structural pores sources for soil mesofauna diversity match well with the proposition that following wet and dry cycles (Czarnes et al., 2000). Microbial consumers mesofauna community assembly is based predominantly on stochas­ therefore, are likely to modify these microbial-driven effects on soil pore ticity rather than e.g., the composition of food resources (Caruso et al., formation as they impact microbial community composition and activity 2012; Zinger et al., 2019). via top-down control (Thakur and Geisen, 2019). In fact, trophic regu­ The availability of physical refuge for prey species and the limitation lation of the microbial identity and activity has been shown to affect of resource exploitation by consumers in the soil matrix, however, need aggregate properties (Siddiky et al., 2012; Erktan et al., 2020), but not necessarily result in food webs being only regulated by basal consequences for soil pore formation has been little studied. In addition resource or prey availability, i.e. by bottom-up forces. Negative and to direct consumptive effects, consumers of soil microorganisms may positive top-down regulation has been observed in soil food webs further impact the microbial community by transporting them from one (Griffiths and Bardgett, 1997; Mamilov et al., 2001; Rønn et al., 2001; place to another in the soil matrix, leading to community coalescence Lang et al., 2014; Coulibaly et al., 2019), documenting that microbial (Rillig et al., 2015), with expected consequences on organo-mineral consumers and predators also effectively regulate lower trophic levels associations. Several mechanisms trigger such displacement, in partic­ (Crowther et al., 2011; Schneider et al., 2012; Thakur and Geisen, 2019). ular the transport of microbes on the body surface (Renker et al., 2005; Here, we stressed that the importance of top-down regulation may be Gormsen et al., 2004; Weigmann, 2006; Erktan et al., 2020), the driven by soil physical structure. Notably, we documented that varia­ comminution and transport of litter debris (Lussenhop, 1992), and the tions in habitat connectivity driven by pore geometry and water distri­ deposition of faeces (Foster and Dormaar, 1991; Coleman et al., 2002). bution at the microscale modulate predator - prey encounter In fact, the upper layers of many soils contain high quantities of probabilities (sections 2. 2 and 2.3), resulting in enhanced (Neher, 2010) microarthropod faeces (Rusek, 1985; Bernier et al., 1993; Bardgett, or decreased (Vargas and Hattori, 1986) top-down regulation. Overall, 2005), which can directly increase soil porosity because of the micro­ the wide presence of refuge in the soil likely contributes to the domi­ porosity of fecal pellets and their assemblage porosity (Foster and Dor­ nance of bottom-up regulation in soil food webs, however, it also favors maar, 1991). Altogether, microbial consumers, such as protists, local exploitation of prey by predators (top-down regulations), thereby nematodes and microarthropods, are thought to impact soil physical promoting the co-existence of a wide variety of species of different structure mainly by modifying microbial communities, either directly trophic level at local scale and thus contributing to the high species via trophic interactions or through associated non-trophic interactions, diversity in soil. such as the transport of microbial propagules on their body surface. While their effect is undoubtedly less strong than that of ecosystem engineers (and roots), we argue that they may be substantial and are

11 A. Erktan et al. Soil Biology and Biochemistry 148 (2020) 107876 currently largely neglected. Experimental studies will be indispensable for improving the mechanistic understanding of the role of soil physical structure for tro­ 5. Outlook: integrating soil food web ecology and soil physics phic interactions. Options to recreate soil structure of contrasting physical characteristics in a reproducible manner are currently being To better integrate the role of soil physical structure into trophic developed and offer promising possibilities for experimental work. A interactions will require (i) improved knowledge on small-scale habitats relatively simple option is to use repacked soil aggregates, which has the of soil organisms, especially for those unable to modify or create their advantage to build model soils with real soil materials, and thus realistic own pore space, and (ii) laboratory studies to experimentally explore physical and chemical properties. Repacking soils with contrasting bulk how soil physical structure drives trophic interactions within and among soil densities enabled to artificiallyestablish soil pore space of different micro-, meso- and macrofauna. For achieving these goals, new tools characteristics (Otten et al., 2001). Using such strategy allowed to have to be developed, or adapted from soil physics and soil food web explore the influence of soil pore characteristics, measured by μCT research fields. scanning, on the spread of selected fungal and bacterial strains (Otten First, soil food web ecologists need to include descriptors of the et al., 2001; Juyal et al., 2019, 2020). A similar design may be developed characteristics of soil physical structure as standard parameters in the to investigate how the pore architecture of soils influence trophic in­ analysis of soil food webs. Partnering with soil physicists and ecohy­ teractions involving micro-, meso- and macrofauna. To establish soil drologists is needed to incorporate in a systematic way characteristics of animal populations in a given small volume of soil, compartments may the soil pore space and aqueous phase into soil food web ecology. Using be used as in Ackermann et al. (2016). Placement of specific microbial μCT-scanning may be particularly helpful in providing more detailed strains in the inner or outer areas of soil aggregates has recently been information on pore dimensions, connectivity and tortuosity (soil ar­ achieved (Harvey et al., 2020) and could be a way to further control the chitecture sensu Baveye et al., 2018; see also Young and Crawford, 2004; initial location of microorganisms within the reconstructed soil structure Vogel et al., 2018 and Lucas et al., 2020) as descriptors of the soil or­ made of repacked aggregates. More artificial options have been devel­ ganisms’ habitat (Young and Ritz, 2000). However, such measurements oped and allow a better control of some specific aspects of the soil require expensive infrastructure, such as X-ray scanners, and know-how physical structure, but this usually comes with reduced realism of for reconstructing soil structure in three dimensions. Indirect methods to overall soil physical and chemical properties. For example, artificial assess soil pore dimensions and water-related properties, such as mer­ porous media might be used for improving the mechanistic under­ cury porosimetry, water retention curves and gas adsorption (Rabot standing of trophic interactions in soil, e.g. by using glass beads in mi­ et al., 2018) represent a possible way to allow soil food web ecologists to crocosms resting on ceramic plates allowing to control the matric better account for soil structure, with lower requirements in terms of potential and to disentangle the physical and physiological constraints costs, skills and equipment. of these interactions (Kleyer et al., 2019). Porous rough surfaces may Relationships between food web structure and pore characteristics further allow to systematically vary the hydration state (matric poten­ including the role of the aqueous phase are likely to shed new light on tial) and to explore the movement of microorganisms directly (Tecon the role of the architecture of habitat space on trophic interactions and Or, 2016). Such artificialporous media have the advantage to offer allowing a mechanistic understanding of fundamental ecological pro­ detailed control of the aqueous phase and thereby may allow to quan­ cesses such as dispersion, foraging and predation. Knowledge on con­ titatively test for the role of increased discontinuity of the aqueous phase straints of these processes is needed to understand and quantify the upon drying (or reconnection upon wetting) on trophic interactions. limitations of microbial grazers in accessing food resources/prey. To do More high-tech possibilities to reconstruct model soils with determined so, identifying food resources and trophic niches of non-geophageous pore geometry include soil chips (Aleklett et al., 2017), 3D polymer soil organisms such as microarthropods in context of the structure of nanostructured fabric (De Cesare et al., 2020) and soil 3D printing the soil matrix is needed. Studies investigating the gut microbiome of (Otten et al., 2012). Soil chips are artificialtransparent thin model soils microarthropds (mites, collembolans) using molecular gut content produced by microfluid technology and opened unprecedented possi­ analysis and in parallel investigating the microbiome of soil hotspots is a bilities to directly observe how microbiota grow, move and interact in promising way forward. To identify the composition of microbial hot­ model pore space with defined pore geometry, connectivity and tortu­ spots, a number strategies may be pursued. A rather simple approach is osity (Aleklett et al., 2017; Borer et al., 2018). Due to size and water based on aggregate dissection (Vos et al., 2013), coupled with meta­ constraints, microfluids are a promising tool to study the behavior of genomic analyses of microbial communities in the dissected hotspots. microbiota (Aleklett et al., 2017), but currently do not offer experi­ Increased precision may be obtained by promising developments of mentation with larger aerobic organisms. Soil like models developed micromanipulators (Frohlich€ and Konig,€ 2000; Ishøy et al., 2006), laser using 3D polymer nanostructured fabric are obtained by electrospining printing techniques (Ringeisen et al., 2015) and optical tweezers and contain a mixture of nano-to microfibresand microbeads mimicking (Whitley et al., 2017), allowing to extract co-existing microorganisms the fibrous materials and particles comprising the main components of from reduced area/volume of soil hotspots, with the ultimate goal to soil (organic matter and mineral particles), and their spatial architecture extract single-cells (see Baveye et al., 2018 for a detailed review on these at the micro- and nanoscale (De Cesare et al., 2020). Even though precise techniques). Classical metagenomic approaches or single-cell genomics pore geometry cannot be achieved, these soil-like models offer the (Blainey, 2013) may then allow insight into microbial identity of the possibility to reproduce realistic micropores, which are the main habitat extracted microbes and possibly erect finescale maps of the composition of soil bacteria and are not achieved by the microfluid technology. of soil microbial hotspots. In parallel, the microbial gut content of Nanostructured soil models are best suitable for bacteria and may be microarthropods obtained by heat extraction of the same soil sample can used for investigating bacteria - protist interactions, but not larger or­ be measured, for example as done by Gong et al. (2018). Such meth­ ganisms. Finally, recent advances in imaging and translation of these odologies might be extended by including experimental manipulations images into printed pore networks have been promising to reconstruct to explore in more detail what portion of soil is exploited by soil animals, model soil of relatively large dimensions (several centimeters) with notably microarthropods, and where they access food resources/prey. definedpore geometry (Otten et al., 2012; Matsumura et al., 2017). One The addition of 13C labelled food resources (dissolved or particulate main current issue is that 3D printing of soil structure only has been organic matter) may further allow to trace microbial C use in soil hot­ done using plastic polymers and for fully connected pores larger than spots and identify their accessibility to higher trophic levels by few hundreds micrometers (Otten et al., 2012). Recent developments in measuring bulk or compound-specific 13C in soil microorganisms and additive manufacturing allows to use clay (de Witte and Fehlhaber, animal consumers (Ruess and Chamberlain, 2010; Hünninghaus et al., 2019) as well as organic material for printing (Sun et al., 2015). Such 2019). technological advances open the perspective that 3D printing of soil

12 A. Erktan et al. Soil Biology and Biochemistry 148 (2020) 107876 with a mixture of mineral and organic material might be achieved in interests or personal relationships that could have appeared to influence near future allowing to vary in a systematic way pore characteristics of the work reported in this paper. model soil (with printed pores down to few hundred microns and mi­ cropores present in the printed material). Such model systems then may Acknowledgements be inoculated with a range of organisms, including micro-, meso- and macrofauna, allowing to explore the relative importance of pore size, This work was funded from the European Union’s Horizon 2020 tortuosity and connectivity for predator - prey interactions. The tech­ research and innovation program under the Marie Skłodowska-Curie nology of 3D soil printing provides the perspective for designing realistic grant agreement No [750249]. 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