Aligning spatial ecological theory with the study of clonal organisms : the case of fungal coexistence

This is a self-archived version of an original article. This version may differ from the original in pagination and typographic details. Author(s): Title: Year: Version: Copyright: Rights: Rights url: Please cite the original version: CC BY-NC 4.0 https://creativecommons.org/licenses/by-nc/4.0/ Aligning spatial ecological theory with the study of clonal organisms : the case of fungal coexistence © 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society Published version Bielčik, Miloš; Schlägel, Ulrike E.; Schäfer, Merlin; Aguilar‐Trigueros, Carlos A.; Lakovic, Milica; Sosa‐Hernández, Moisés A.; Hammer, Edith C.; Jeltsch, Florian; Rillig, Matthias C. Bielčik, M., Schlägel, U. E., Schäfer, M., Aguilar‐Trigueros, C. A., Lakovic, M., Sosa‐Hernández, M. A., Hammer, E. C., Jeltsch, F., & Rillig, M. C. (2024). Aligning spatial ecological theory with the study of clonal organisms : the case of fungal coexistence. Biological Reviews, Early View. https://doi.org/10.1111/brv.13119 2024 Aligning spatial ecological theory with the study of clonal organisms: the case of fungal coexistence MilošBielˇ cik 1,2,3, *,Ulrike E. Schlägel 4 ,Merlin Schäfer 4,5 , Carlos A. Aguilar-Trigueros 1,2,6,7 ,Milica Lakovic 1,2 ,Moisés A. Sosa-Hernandez 1,2 , Edith C. Hammer 8 ,Florian Jeltsch 2,4 and Matthias C. Rillig 1,2 1 Institute of Biology, Freie Universität Berlin, Altensteinstr. 6, Berlin 14195, Germany 2 Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Altensteinstr.34, Berlin 14195, Germany 3 Microbial Biogeochemistry, Research Area Landscape Functioning, Leibniz Center for Agricultural Landscape Research (ZALF), Eberswalder Str.84, Müncheberg 15374, Germany 4 Institute of Biochemistry and Biology, University of Potsdam, Am Mühlenberg 3, House 60, Potsdam-Golm 14476, Germany 5 Federal Agency for Nature Conservation, Alte Messe 6, Leipzig 04103, Germany 6 Hawkesbury Institute for the Environment, Western Sydney University, Hawkesbury Campus, Building R2, Locked Bag 1797, Penrith, New South Wales 2751, Australia 7 Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35, Seminaarinkatu 15, Jyväskylä 40014, Finland 8 Department of Biology, Microbial Ecology, Lund University, Ekologihuset, Sölvegatan 37, Lund 22362, Sweden ABSTRACT Established ecological theory has focused on unitary organisms, and thus its concepts have matured into a form that often hinders rather than facilitates the ecological study of modular organisms. Here, we use the example of filamentous fungi to develop concepts that enable integration of non-unitary (modular) organisms into the established community ecology theory, with particular focus on its spatial aspects. In doing so, we provide a link between fungal community ecology and modern coexistence theory (MCT). We first show how community processes and predictions made by MCT can be used to define meaningful scales in fungal ecology. This leads to the novel concept of the unit of community interactions (UCI), a promising conceptual tool for applying MCT to communities of modular organisms with indeterminate clonal growth and hierarchical individuality. We outline plausible coexistence mechanisms structuring fungal communities, and show at what spatial scales and in what habitats they are most likely to act. We end by describing challenges and opportunities for empirical and theoretical research in fungal competitive coexistence. Key words: modular organisms, clonal growth, fungal competition, fungal community ecology, modern coexistence theory, metacommunity, intransitive coexistence, competition–colonisation trade-off, growth–density covariance, spatial storage effect. CONTENTS I. Introduction .........................................................................2 II. Spatial and biological scales .............................................................4 (1) General overview ................................................................. 4 (2) Meaningful spatial scale ............................................................ 4 (3) Meaningful biological scale: concept of unit of community interactions ....................... 5 III. Coexistence in spatially homogeneous environments ..........................................8 *Author for correspondence (Tel.: +49 33432 82 352; E-mail: [email protected]). Biological Reviews (2024) 000–000 © 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. Biol. Rev. (2024), pp. 000–000. 1 doi: 10.1111/brv.13119 (1) General overview ................................................................. 8 (2) Life-history trade-offs in systems with patch dynamics ..................................... 9 (a) Competition–colonisation trade-off ............................................... 9 (b) Competition–growth rate trade-off ................................................ 9 (c) Where to look for it: UCIS and spatial scales ........................................ 9 (3) Intransitive coexistence in local neighbourhoods ........................................ 10 (a) Intransitive coexistence and fungal biology ........................................ 10 (b) Where to look for it: UCIS and spatial scales ....................................... 10 IV. Coexistence in spatially heterogeneous environments .........................................10 (1) General overview ................................................................ 10 (2) Conditions for heterogeneity-dependent coexistence and evidence in fungi ................... 11 (3) Where to look for it: coexistence in heterogeneous habitats ................................ 12 (a) Where to look for it: habitat properties ........................................... 12 (b) Where to look for it: UCIS ..................................................... 12 V. Future perspectives ...................................................................13 (1) General overview ................................................................ 13 (2) Importance of basic knowledge on natural history ....................................... 13 (3) Size of the saprobic fungus ........................................................ 14 (4) Competition other than interference ................................................. 14 (5) Microcosms to study species coexistence .............................................. 15 (6) The role of the UCI concept in model parameterisation and tests of coexistence ............... 15 (7) Future theoretical perspectives ..................................................... 16 VI. Conclusions .........................................................................18 VII. Acknowledgements ...................................................................19 VIII. References ..........................................................................19 I. INTRODUCTION From the perspective of ecological dynamics in space, it is useful to divide organisms into two groups: unitary and modular. The former is represented by motile animals, singlecelled microbes, and non-clonal plants. Although all plants are modular from a morphological standpoint, we focus here on ecological interactions in space. Thus, the ecologically modular organisms include a range of life forms such as coral polyps, colonial bryozoans, slime molds, clonal plants, colonial Prokaryota (e.g. Actinobacteria; Wink, Mohmmadipanah & Hamedi, 2017) and most notably, filamentous fungi (Booth, 2014;Pringle&Taylor,2002). We argue that mainstream ecological theory has focused on unitary organisms and that its concepts often hinder the inclusion of ecologically modular life forms. The most obvious example is the clear dichotomy between individual and population, which is central to population and community ecology and yet difficult to apply to ecologically modular organisms. However, there are further, less-obvious examples of conceptual obstacles, including the common understanding of reproduction or the definition of growth, movement and dispersal (Bielˇ cik et al., 2019; Chaudhary et al., 2022; Pringle & Taylor, 2002). Here, we develop a conceptual framework which allows translation of features of modular biology and ecology into existing ecological theory. The central theoretical topic is spatial competitive coexistence (Amarasekare, 2003;Chesson,2000a), but the concept is applicable to other areas of spatial ecology. As a model life form, we chose to focus on one of the most abundant and intensively studied forms of ecologically modular organisms: filamentous fungi. Due to their roles in organic matter decomposition, soil carbon storage and plant symbiosis, filamentous fungi are of great importance in all terrestrial ecosystems. The question of fungal coexistence is thus not only interesting in itself, as a precursor to our understanding of community dynamics in ecologically modular organisms but is also relevant to challenges of the Anthropocene. Understanding the mechanisms that maintain fungal biodiversity is essential to make predictions about the impacts of global change factors acting at different spatial and temporal scales, and to improve our mitigation and conservation capabilities (Catford, Bode & Tilman, 2018; Godoy, 2019; Valladares et al., 2015). The importance of spatial properties of the environment has been documented in fungi for diverse scales (Boddy, 1999; Held et al., 2009;O’Leary et al., 2020). Yet it remains unknown exactly which spatial processes drive persistence or decline of fungal biodiversity. As a way forward, in line with Peay (2014), we argue for theory-driven, mechanism-focused research on fungal communities, which we believe has potential to bridge the gap between reductionist and holistic approaches in microbial ecology (as described in Tecon et al., 2019). Our focus on spatial aspects of modern coexistence theory (MCT) enables us to tackle two interrelated problems of fungal ecology. First, it enables us to delineate the meaningful spatial scales on which research should focus (Dini-Andreote et al., 2021; Nemergut et al., 2013). Second, it enables us to address the challenges posed by implementing theory developed largely for unitary Biological Reviews (2024) 000–000 © 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 2MilošBielˇ cik and others 1469185x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/brv.13119 by University Of Jyväskylä Library, Wiley Online Library on [07/08/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License organisms into the realm of modular organisms (Booth, 2014;Maet al., 2016; Pringle & Taylor, 2002). The network-like bodies of filamentous fungi and spatial complexities of their habitats cause each mycelium to interact with others on multiple spatial scales simultaneously, from microscopic hyphal tips to macroscopic mycelia (see Table 1for glossary) (Bielˇ cik et al., 2019; Boddy, 2000; Hanson et al., 2006). Moreover, many empirical approaches in MCT require measurements of population dynamics over multiple generations (Godwin, Chang & Cardinale, 2020; Siepielski & McPeek, 2010). In filamentous fungi, the distinction between an individual and its population is not clear, nor is the definition of the temporal scale of a generation (Booth, 2014). Therefore, we begin by showing how MCT can be employed in identifying the relevant spatial scale and the level of biological organisation practical for a given study (Pringle & Taylor, 2002). In doing so, we introduce the concept of unit of community interaction (UCI) as a practical surrogate for the concept of individuality. Following this, we introduce pertinent spatial coexistence mechanisms, show under what circumstances they can drive fungal coexistence, and what spatial scales and UCIs are practical to follow for each mechanism. In accordance with established theory, we organise spatial coexistence Table 1. Glossary. Clonal subsidizing Ability of a physiologically integrated genet to support ramets that grow under less-favourable conditions (e.g. lower nutrient availability, higher competitive pressure). Competitive coexistence In the context of modern coexistence theory, the term ‘coexistence’has a narrower meaning than in the current ecological literature. In the broader ecological literature, the term can be used to describe the coexistence of, for example, prey and predators, hosts and parasites, or humans and wildlife. In modern coexistence theory, the term refers to competitive coexistence: the coexistence of ecologically similar species that compete for resources without competitively displacing each other. Competitive rankings and intransitive competition This refers to competitive hierarchies between ecologically similar species. Competitive ranking is often expressed by arrows, e.g., pointing from species A that outcompetes species B (A !B). It is important to note that competitive rankings are context dependent. They can be reversed if, for example, the environment changes (from A !B, to A B). In communities with three or more species, competitive rankings can be transitive (i.e. hierarchical), where species A is competitively dominant over both B and C (A !B!C A), or intransitive (non-hierarchical), where species A outcompetes species B but is outcompeted by species C (A !B!C!A). Competitively homogeneous and competitively heterogeneous environment This describes the relationship between competitive rankings of species and space. The environment is competitively homogeneous if competitive rankings remain the same throughout the area. That is, species 1 is a superior competitor of species 2 throughout the area, even if abiotic and biotic heterogeneities are present (but not in a quality or quantity that alters the competitive ranking). If environmental heterogeneities change the competitive ranking within the area, the area is competitively heterogeneous. Hierarchical individuality This describes life forms where the distinction between individual and population is not clear. Instead, multiple levels of organisation of the organism can be described as an individual (e.g. ramets and genets). Hypha, hyphal tip The hypha is the basic cellular unit of the morphology of filamentous fungi. It grows (elongates) at its end, called the hyphal tip. It has the shape of a long, branched thread. Indeterminate clonal growth A property of ecologically modular organisms, this refers to the ability to spread into adjacent favourable habitat in the form of a physiologically integrated genet, spatially constrained only by habitat availability. Mutual invasibility In the context of modern coexistence theory, the term (mutual) invasibility has a different meaning than in invasion biology. It refers to the key condition of species coexistence: as the population size of a species decreases, that species will experience reduced competition from conspecifics. If competition from heterospecifics is lower due to lower niche overlap, overall competition decreases and the species experiences population growth. Thus, when a small number of individuals are added to the equilibrium state of a population or community of competing species, the new species can invade it, i.e. reproduce and coexist. This scenario must apply in a mutual manner to all species in the community if they are to coexist. Mycelial cord, mycelium A mycelium is the collection of interconnected hyphae that form a single organism, i.e. a body of a filamentous fungus. Mycelia may have the character of a simple network of microscopic hyphae. In some species, intertwined aggregations of hyphae may form pseudo-organs. An example of this is mycelial cords, which are elongated, often macroscopic structures formed by a parallel alignment of multiple hyphae. Through their growth, mycelial cords can seek out and colonize new resource units. Mycelial interference Interference competition is manifested as a direct, aggressive behaviour between competing individuals. In fungi, it occurs at the level of entire mycelia. Mycelia can interfere with each other by producing chemical agents or morphological structures designed to harm or protect against the competitor. Mycophagous bacteria Species of bacteria able to feed on living fungal mycelia. Propagule A life stage dedicated to dispersal to new habitats. A typical example is a plant seed or hyphal spore. In organisms with clonal growth, elongated growing structures (e.g. mycelial cords) can also play the role of a propagule. Source-sink dispersal In competitively heterogeneous habitats, species can maintain continuous dispersal from a favourable area (i.e. the source population) to an unfavourable area. Without this continuous dispersal from the source, the local population in the unfavourable area (i.e. the sink population) would go extinct. Biological Reviews (2024) 000–000 © 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Coexistence theory and filamentous fungi 3 1469185x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/brv.13119 by University Of Jyväskylä Library, Wiley Online Library on [07/08/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License mechanisms into two major blocks (Amarasekare, 2003): those which can function in a competitively homogeneous environment, and those which require environmental heterogeneity. The former are colonisation-related trade-offs and intransitive coexistence (Amarasekare, 2003; Barabas, D’Andrea & Stump, 2018; Kerr et al., 2002). The latter are spatial storage effect and growth–density covariance (Barabas et al., 2018; Chesson, 2000a). Even though intransitive coexistence currently stands outside the MCT framework, we argue that no account on fungal coexistence can be complete without it. Each section on a particular coexistence mechanism ends with a subsection on where to look for it. This contains the likely spatial scales at which a given mechanism operates and the UCIs involved. We consider our selection of coexistence mechanisms sufficient to demonstrate conceptual principles, and to serve as a bridge between MCT and fungal community ecology. We do not discuss the coexistence mechanisms of heteromyopia and spatial relative non-linearity in order to prevent overly speculative discussion, given the insufficient state of knowledge relating to these mechanisms in fungi (Amarasekare, 2003; Chesson, 2000a; Murrell & Law, 2002). In the last section, we outline knowledge gaps and perspectives for both empirical and theoretical research, focusing on natural history and experimental approaches in fungal competition and coexistence (Peay, 2014). We hope to achieve two interrelated goals in our review. In addition to conceptual developments around the UCI concept, we also hope to provide fungal ecologists with an accessible bridge to the MCT framework. In explaining modern coexistence theory, there is a trade-off between intuitive language and language that is faithful to the mathematical foundations of MCT. Given our second goal to introduce coexistence theory to (fungal) ecologists and to motivate cross-talk between MCT and the ecology of modular organisms, we tend to use intuitive language. For explanations of coexistence mechanisms more directly linked to themathematicalmodelsofcoexistence,werecommend Amarasekare (2003) and Barabas et al.(2018). For application of MCT in empirical studies, we recommend Ellner et al.( 2019), Grainger, Levine & Gilbert (2019b), and Godwin et al.( 2020). Finally, Grainger et al.(2021) provide help navigating the theory for empirical ecologists. Unlike previous work that concentrated on fungal symbionts of plants (Kennedy, 2010), we focus on the saprobic guild of filamentous fungi since more is known about the nature of their competition, growth, dispersal, and interactions with environmental heterogeneities (Peay, Kennedy & Bruns, 2008). In addition, the problem of coexistence in symbionts is likely more complex due to sophisticated interactions with the host, and different community interactions within and outside of the host (Bogar et al., 2019; Kummel & Salant, 2006; Valyi et al., 2016). Yet, some aspects of our review are relevant to symbiotic species, and we use empirical knowledge on these whenever relevant. Finally, it is important to note that the list of potential coexistence mechanisms in filamentous fungi and other ecologically modular organisms presented here is not exhaustive. For example, we have not considered mechanisms related to resource partitioning or temporal niche partitioning (e.g. the temporal storage effect) (Chesson, 2000b). While these mechanisms likely play an important role in the coexistence of ecological communities, we focus on the spatial aspects of coexistence. It is alongside the spatial niche dimension where the modular organisation and multi-scale interactions of fungi pose the most challenges (Chaudhary et al., 2022; Valyi et al., 2016). And it is in the spatial niche dimension where we see the most potential to advance the discussion of fungal fitness and individuality, and to align this discussion with the requirements of community ecology research (Booth, 2014; Lakovic & Rillig, 2022; Pringle & Taylor, 2002). II. SPATIAL AND BIOLOGICAL SCALES (1) General overview A frequent problem of microbial ecology is a tendency for arbitrary approaches to space and spatial scales (Dini-Andreote et al., 2021). There is a growing recognition of the need for, and the difficulty of defining a meaningful spatial scale (Dini-Andreote et al., 2021; Ladau & Eloe-Fadrosh, 2019;Monyet al., 2020). Specifically for fungi, complex life histories, network-like bodies and hierarchical individuality can make application of even elementary spatial concepts difficult (Booth, 2014;Pringle& Taylor, 2002;Valyiet al., 2016). Thus, the possibility of using MCT to delineate the relevant spatial scale and level of biological organisation in fungal mycelium (hereafter biological scale) is of great interest. For dispersal, we always use its broad definition, as movement that drives spatial population dynamics within the current or into new habitat patches (Schlägel et al., 2020). In fungi, dispersal can include mycelial outgrowth (Bielˇ cik et al., 2019;Boddyet al., 2009; Chaudhary et al., 2022). (2) Meaningful spatial scale Here, we show that meaningful spatial scale can be the one at which a given community process is expected to take place. For instance, for intransitive coexistence (see Section III.3) driven by mycelial interference (see Table 1) (Hiscox et al., 2017; Maynard et al., 2017), the focal spatial scale covers local neighbourhoods of interfering mycelia. In Euclidian space, the extent of this scale will differ based on the size of mycelia and range of interactions (which may differ from the mycelium size if the competition is at a distance) (Evans et al., 2008). Similarly, for coexistence mechanisms in metacommunities, the meaningful scales will be local and regional (Amarasekare, 2003; Shoemaker & Melbourne, 2016). Here, not only the Euclidian extent of scales varies, but also the definition of local and regional will depend on a particular coexistence mechanism (or metacommunity model to which the Biological Reviews (2024) 000–000 © 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 4MilošBielˇ cik and others 1469185x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/brv.13119 by University Of Jyväskylä Library, Wiley Online Library on [07/08/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License mechanism refers). In coexistence mechanisms related to the metacommunity model of patch dynamics (e.g. competition– colonisation trade-off), a particular habitat patch equals locality, and the assemblage of separated patches represents the region (see Section III). For coexistence mechanisms related to the metacommunity model of species sorting (e.g. spatial storage effect), locality can be either an isolated patch, or not isolated area (see Section IV)(Fournieret al., 2017; Melbourne et al., 2007; Shoemaker & Melbourne, 2016). Whether the locality is isolated or not, it must extend over the space in which the environmental conditions remain favourable for the focal species i.e. competitive rankings are unchanged (Amarasekare, 2003; see Table 1), and that is large enough for the dispersal not to prevent aggregation of individuals in their favoured locality (Amarasekare, 2003;Chesson,2000a; Snyder, 2008). Hence, local and regional are defined by the processes of interest and species traits (e.g. size, dispersal range) (see Section IV). Based on this, we briefly outline for soil habitats (see also Ritz & Young, 2004) the role of spatial coexistence processes on the Euclidian microscale, a topic gaining considerable attention in fungal ecology. First, microstructure properties can contribute to habitat connectivity (see Section III) influencing dispersal between two patches (Falconer et al., 2012; Kravchenko et al., 2011). Second, we speculate that they can act as environmental variables in heterogeneous environments: if species are adapted to different microstructures and the belowground areas differ in microstructural properties, each species can have a competitive advantage in a different locality. Our speculation is based on current research on micro-environments (Aleklett et al., 2021; Fukuda et al., 2021; Hanson et al., 2006; Held, Edwards & Nicolau, 2008; Held et al., 2009; Hopke et al., 2021), which additionally identified species-specific responses (traits) in navigating microstructures (Aleklett et al., 2021; Fukuda et al., 2021; Held et al., 2009; Hopke et al., 2021). (3) Meaningful biological scale: concept of unit of community interactions The concepts used by MCT (e.g. individual, propagule, population growth) fitbettertounitaryorganismsthantonetworked mycelia with hierarchical individuality, indeterminate growth and convoluted life histories (Booth, 2014;Pringle& Taylor, 2002). For instance, operational definitions of fitness and population growth in MCT are often based on quantifying the number of discrete propagules produced per individual and established new individuals that share common anatomical and physiological characteristics (e.g. seeds, established seedlings) (Adler, Ellner & Levine, 2010;Angertet al., 2009;Godoy, Kraft & Levine, 2014). However, this definition of fitness is problematic in fungi, as they can reproduce and disperse via anatomically and physiologically diverse structures such as spores, mycelial fragments, growing mycelium or even as symbiotic life stages (e.g. pre-colonised wood) (Bielˇ cik et al., 2019; Chaudhary et al., 2022; Ortiz-Urquiza, 2021; Pringle & Taylor, 2002; Song et al., 2017). Thus, even though the MCT has potential to increase mechanistic understanding of community assembly and biodiversity persistence, the task of applying MCT to fungi can become troublesome to unfeasible because it is being framed using definitions restrictive to unitary organisms. In order to simplify this task, we propose a broader and universally applicable concept termed ‘unit of community interactions’(UCI), analogous to Booth’s unit of selection (Booth, 2014), or to unit of reproduction (Ma et al., 2016). This concept allows for the operational definition of community assembly agents (units). UCIs are defined based primarily on their role in community processes, rather than on physiological, structural, or developmental details of an ecologically modular organism and its segments, (pseudo)organs and tissues. That is, rather than focusing on how the fungus is organised biologically (e.g. hyphal segment versus spore, symbiotic phase versus free-living), the UCI concept highlights what role particular segments or biological scales play in a particular community process or coexistence mechanism, and thus enables a comparison of fitness between fungal competitors with different life-history strategies. For instance, in defining UCIs it is of primary interest whether the dispersal is local or regional. It is secondary or irrelevant if the dispersal is by spore, mycelial outgrowth, or another life-history stage (Boddy et al., 2009; Chaudhary et al., 2022). Similarly, a mycelium can be defined as a single UCI, or as a population of lower-level UCIs. Crucially, the choice depends less on the degree of physiological integration within the mycelium than on the coexistence mechanism on which the researcher aims to focus (but see the example below). In a research design, UCIs are meant to serve as a tractable, simplifying substitute for the individuals and propagules of MCT. We first provide a glimpse of the concept’s usefulness by using an example, then provide the definition, followed by our reasoning behind the definition. Let us say a researcher aims to model the coexistence of wood-decomposing species, driven by a competition– colonisation trade-off among wood logs across a given area (i.e. among patches) (Amarasekare, 2003; Boddy et al., 2009; Levins & Culver, 1971). Some mycelia may extend between multiple wood blocks (Bebber et al., 2007; Boddy et al., 2009; Boddy, 1999). Using the concept of the individual and quantifying its fitness is challenging as mycelia can remain physiologically integrated (i.e. contiguous mycelia) across all wood blocks (Booth, 2014; Simonin et al., 2012) (Fig. 1A). In other words, an ‘individual’can be present in two different patches (and local communities) at the same time, a situation that hinders the applicability of MCT, as there is no concept or framework within MCT that could accommodate this situation. The problem can be easily solved if we shift the focus from biological individuals to UCIs. Applying the concept of UCI in the context of a competition–colonisation trade-off, the mycelium in each patch is perceived as a separate UCI regardless of the physiological integration (Fig. 1B,D), and mycelial cords (see Table 1) spreading from a parental patch are regarded as a form of highly competitive propagule-type UCI (Kennedy et al., 2011) (Fig. 1C). Thus, the degree of Biological Reviews (2024) 000–000 © 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Coexistence theory and filamentous fungi 5 1469185x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/brv.13119 by University Of Jyväskylä Library, Wiley Online Library on [07/08/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License physiological integration matters in a manner analogous to the degree of investment by a parental plant into a single seed (Levine & Rees, 2002). By introducing the UCI concept, instead of attempting to fit the complexities of fungal organisation into the concepts and mechanisms developed largely by studying unitary organisms, we show that the mechanisms of coexistence can be utilised to define operationally the organisational units of interest. In other words, the meaningful biological scale becomes the one at which important community processes or coexistence mechanisms are hypothesised to act. We define UCI as: (i) a physiologically integrated entity (propagule, segment or a whole organism), (ii) whose growth influences (and can be influenced by) its external competitive environment, and (iii) and has the capacity to either produce, or to act as agent(s) of dispersal. This capacity is defined as having both the pluripotency, and available biomass/ resources. Necessary biomass (energy) can be either contained within the structure of dispersal (e.g. spore, sclerotium), or provided by the hyphal network (e.g. mycelial cords subsidised by parental mycelium). Dispersal is defined as any movement, by a spore or mycelial outgrowth, capable of reaching new habitat both in the immediate vicinity or at a larger spatial scale, and thus contributing to (meta)population dynamics (Chaudhary et al., 2022; Schlägel et al., 2020). Our definition of UCI covers all biological and spatial scales at which fungi interact in a fashion predicted by MCT, i.e. engage in (meta)community competitive dynamics driven by an interplay between niche differences, competitive differences, habitat variability and dispersal (Barabas et al., 2018; Chesson, 2000a; Shoemaker & Melbourne, 2016). Following this definition, individual contiguous mycelia, their local segments (i.e. ramets), and specialised propagules can act as UCIs. The first condition (i) of physiological integration prevents two or more disconnected mycelia from being considered as a single UCI, even if they have the same genetic identity (i.e. single genet). If they re-establish connection through hyphal fusion (i.e. anastomosis), they once again meet the condition of physiological integration (Wu et al., 2012). The condition of physiological integration must be fulfilled to ensure that UCIs can be perceived as individual-surro- gates that are internally organised and potentially compete with each other (within a population of multiple UCIs). Thus, while each UCI must be physiologically integrated, the converse is not true. Each physiologically integrated mycelium does not need to be a single UCI, but instead can be regarded as a population of lower-level UCIs (e.g. see the above example of UCIs in competition–colonisation trade-off). The operational choice depends, again, on the community process of interest (Fig. 2). For instance, if the aim is to study interference competition, the contiguous mycelia are the best candidatefortheUCI.Duringinterference,theresponse can be organised at the level of entire mycelium (Boddy, 2000; Kolesidis et al., 2019). Partitioning it into lower-level UCIs would likely obscure, rather than elucidate important processes. By contrast, in coexistence via growth–density covariance (see below), of primary importance is the ability to concentrate (population) growth in a favourable area (Barabas et al., 2018; Chesson, 2000a; Melbourne et al., 2007; Shoemaker & Melbourne, 2016). It is of secondary importance whether this growth remains physiologically integrated or not. What is crucial is that the MCT can justify simplification and address all growth at the population level. The UCI concept offers the flexibility to meet theoretical expectations, and thus all spores or mycelial segments are assorted regardless of their biological character into populations of locally dispersing UCIs, or Fig. 1. Concept of unit of community interaction (UCI) in modular organisms, illustrated for the example of a patch dynamics model in fungi. Patches are depicted as rectangles, mycelia and mycelial cords as pale blue circles and blue lines, respectively. From a biological perspective (A), the entire physiologically integrated modular organism is a single unit (an individual). This remains the case also if it spreads between multiple resource patches. Within the framework of coexistence in competitive metacommunities, it is useful to distinguish (regardless of the physiological integration) between adult-like UCIs (B and D) and propagule-like UCIs (C), i.e. mycelia in local patches and mycelial cords dispersing between patches, respectively. Biological Reviews (2024) 000–000 © 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 6MilošBielˇ cik and others 1469185x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/brv.13119 by University Of Jyväskylä Library, Wiley Online Library on [07/08/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License regionally dispersing UCIs. To summarise, a physiologically integrated mycelium can be treated as a single UCI or as a population of lower-level UCIs, depending on the natureoftherespectivecoexistencemechanisms. The second condition (ii)ofgrowthinfluencing (and can be influenced by) the external competitive environment excludes (for instance) individual nuclei (the units of selection of Booth, 2014) from having the status of a UCI. In accordance with MCT, the growth of any UCI is affected by and affects the competitive environment (e.g. resources, predators, competitors) (Chesson, 2000a,b). From the perspective of a nucleus, the environment is the cytoplasm, and does not directly influence the competitors or external resources (Lakovic & Rillig, 2022). The last condition (iii) of the UCI (i.e. the capacity to either produce or to act as agent(s) of dispersal) points to the ability of UCIs to contribute to the (meta)population dynamics described by MCT (e.g. patch colonisation, source–sink dispersal; see Table 1) (Amarasekare et al., 2004; Shoemaker & Melbourne, 2016), and simultaneously sets the lower limit for a mycelial segment (or fragment) that can still have the status of a UCI. In theory, any segment/fragment can start a new mycelium following an outgrowth into a new resource patch, or fragmentation by external forces (Boddy et al., 2009; Pringle & Taylor, 2002; Rayner, 1991). While in laboratory conditions, a mycelium can re-establish from a single hyphal tip, in natural communities the threshold for available biomass/resources to act as a unit of dispersal might be higher (Nix-Stohr, Moshe & Dighton, 2008; Qandah & Del Rio Mendoza, 2012). Similarly, mycelia of wood decomposers can persist in wood patches after depletion of the resource base necessary to build a fruiting body (i.e. available biomass/resources to produce unit(s) of dispersal) (Kubartovaet al., 2012). From the perspective of population dynamics, unless the species routinely disperses vegetatively, these mycelia are destined for local extinction, unable to contribute to population dynamics as described by MCT (Kubartovaet al., 2012). Note that the definition of UCI is intentionally ambiguous to account for the hierarchical individuality and indeterminate growth of filamentous fungi. Thus, for proper use of the concept, it is critical to explain clearly what is defined as the UCI in a given study and why, i.e. based on what mechanism and context. Finally, we illustrate how the concept of UCI and the resulting rigorous approach to biological and spatial scales can benefit study of the fungal coexistence program, with examples from previous studies. Pringle & Bever (2002)proposed that temporal niche partitioning supports coexistence in mycorrhizal fungi. They quantified fungal activity using spore production as a proxy, based on the assumption that an increase in spore counts is driven by an increase in physiological activity in the recent past. While this assumption is reasonable for certain species, the ability to disperse both by spore and mycelial growth prevents a similar approach to defining fitness for a wider range of competitors (Valyi et al., 2016). To conduct similar studies on a wider range of species, propagule-like UCIs can be used as a surrogate for spores in fitness definitions (Chaudhary et al., 2022;Valyiet al., 2016). Besides the definition of fitness (Pringle & Taylor, 2002), fungal ecology also faces the challenge of establishing robust links between patterns of co-occurrence and putative mechanisms of coexistence. There is a tendency to oversimplify the task of coexistence testing by focusing only on one potentially relevant UCI, namely the fully grown mycelia in the resource patch. The observation of a pattern of mycelia unable to displace each other within the local neighbourhood (i.e. interference deadlock) can be interpreted as coexistence driven by the directly observed UCIs (Cui, Yue & Cao, 2023; Fukasawa & Matsukura, 2021). The absence of competitive differences at the mycelial level can actually lead Fig. 2. Flexibility in defining units of community interaction (UCIs; green dashed circles) in ecologically modular organisms. The figure shows growth of the same mycelium (blue dots and lines and blue arrows), which can be viewed as the movement (green arrows) of a single individual (left) or the dispersal of a population (right). The choice is operational, and it depends on the ecological context and the research question. Biological Reviews (2024) 000–000 © 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Coexistence theory and filamentous fungi 7 1469185x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/brv.13119 by University Of Jyväskylä Library, Wiley Online Library on [07/08/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License to competitive exclusion when all relevant UCIs of the life cycle and their corresponding scales are considered. For instance, if two species are competitively similar at the level of mycelia (local UCIs), but one of the two species is superior in dispersal through any form of propagule-like UCIs, competitive exclusion may eventually take place because the conditions for a trade-off between competition and colonisation are not met (Amarasekare, 2003; Levins & Culver, 1971; Tilman, 1994). These topics are discussed in more detail in the following sections. III. COEXISTENCE IN SPATIALLY HOMOGENEOUS ENVIRONMENTS (1) General overview To begin, we clarify the relevant terminology of spatial ecology. MCT makes a clear distinction between habitat heterogeneity (i.e. qualitative differences between patches) and habitat structure where all patches can have the same properties [also referred to as patchiness or physiognomy (Amarasekare et al., 2004; Dunning, Danielson & Pulliam, 1992)]. If competitive rankings among species remain the same in all patches, the environment is structured, but competitively homogeneous (Amarasekare, 2003) (Fig. 3A, Table 1). Whenever we discuss heterogeneity or homogeneity, we mean (unless specified otherwise) the spatial, rather than temporal properties of habitat (Chesson, 2000a). Habitat connectivity refers to the interplay between movement capacity of the organism (in fungi both by spores and/or mycelial outgrowth; Bielˇ cik et al., 2019), and habitat features that influence the movement and survival rates between patches (Henein & Merriam, 1990; Taylor et al., 1993). In fungi, these can include diverse environmental variables such as soil porosity and micro-geometry (Aleklett et al., 2021; Arellano-Caicedo et al., 2021; Falconer et al., 2012; Kravchenko et al., 2011), distances between patches, wind characteristics (Norros et al., 2012), presence of animal mobile linkers (da Silva et al., 2016; Danks et al., 2020), A B C D Fig. 3. Coexistence in homogeneous and heterogeneous habitats. Habitat patch(es) are depicted as rectangles. Green shading represents habitat heterogeneity. Coexistence to which spatial processes are relevant can take place in habitats which are homogeneous-structured (A), homogeneous-unstructured (B), heterogeneous-structured (C), and heterogeneous-unstructured (D). (A) Coexistence via colonisation–competition trade-off is depicted as successive events (i–iv) within the same array of four habitat patches. A superior coloniser arrives first (i) and its mycelial structures and spores are depicted in blue. A superior competitor is depicted in orange. (B) Intransitive coexistence is possible in homogeneous and unstructured habitats, provided the competition maintains a certain spatial property, i.e. is limited to local neighbourhoods. Intransitive competitive dominance is depicted as the circle of arrows. (C, D) Coexistence in heterogeneous habitats is possible regardless of the habitat structure, provided dispersal towards the unfavourable patches is limited. The competitive rankings must shift with environmental gradient, so the blue species is competitively dominant in one area (x), while the yellow species is dominant in another (y). Biological Reviews (2024) 000–000 © 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 8MilošBielˇ cik and others 1469185x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/brv.13119 by University Of Jyväskylä Library, Wiley Online Library on [07/08/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License Phenotypic plasticity has been shown to promote coexistence in intransitive communities, with the underlying mechanism analogous to bet-hedging: the more phenotypes a species has, the more likely it is to persist (Maynard et al., 2019b; Milles et al., 2023). It would be intriguing to explore how coexistence can be affected in fungi, where phenotypic plasticity can be accompanied by dramatic changes in competing UCIs. For example, a mycelium can be outcompeted as a single, large UCI under laboratory conditions in homogeneous environments, but in more natural and structured environments it can be split into a population of small UCIs with each of these smaller UCIs consequently adopting a different phenotype in response to its local competitive environment (Evans et al., 2008; Hiscox et al., 2010). (5) Microcosms to study species coexistence Once relevant life-history traits are identified, it is possible to design coexistence experiments and define the UCIs in a way that is relevant to the dynamics of biodiversity in real environments (Gomez-Llano et al., 2023; Siepielski & McPeek, 2010). Here we outline what features the microcosms should have. Ideally, microcosms should enable establishment of community equilibria and measurement of population-level competition (Barabas et al., 2018; Siepielski & McPeek, 2010). For this, microcosms should contain model species with smaller UCIs (either as multiple small mycelia, or as loosely spread mycelia with defined ramet-level UCIs). To mimic long-lived natural systems (e.g. soil), microcosms should have an option for resupplying the system with nutrients, and include representatives of other trophic levels that are likely to modulate population-level competitive interactions between fungi and enable the establishment of realistic equilibrium states (e.g. bacterial communities, selected protists and invertebrate species) (Crowther et al., 2013; Hart, Freckleton & Levine, 2018). While time series data are ideal to measure population dynamics (as a response to competition and signal of coexistence) (Hart et al., 2018; Siepielski & McPeek, 2010), acquiring time series in systems that can not be visually accessed (e.g. soil communities) is a troublesome task. Fortunately, not all coexistence studies require time series (Grainger et al., 2019b). Notably in annual plant systems, seed production is a fitness measure obtained from a single destructive harvest. Similar approaches could be applied in fungal species with analogous life histories. For fungi with a semelparous life history, i.e. sporulating once in the life cycle, destructive-harvest experiments analogous to seed counting in annual plants can be a feasible option (Pringle & Taylor, 2002). In addition, an argument can be made that in these species, allocation of resources between mycelial growth and sporulation is of lesser concern (Damialis et al., 2015; Pringle & Taylor, 2002). The requirement for ecological relevance, continuous supply of resources and the presence of consumers for the establishment of an equilibrium state make soil microcosms particularly attractive candidates for experiments on fungal coexistence. Yet, their construction and maintenance will require significant effort. They also have the disadvantage that processes in soil microcosms cannot be observed nondestructively. Alternative experimental systems with properties essential for coexistence experiments (e.g. establishment of community equilibrium, natural context of interactions) include ‘cheesy and shitty’systems, i.e. microcosms of cheese rind and dung communities, respectively (Bruns, 2019). Ultimately, the development of easily observable laboratory systems (e.g. agar plate or microfluid-based systems) that meet the above requirements would be a great contribution to the study of fungal communities (Aleklett et al., 2021; Mafla-Endara et al., 2021). Such systems, which allow direct, continuous observation of competing UCIs, would expand the scope of available coexistence models and empirical approaches. We introduce these topics in the following section. (6) The role of the UCI concept in model parameterisation and tests of coexistence Empirical tests of species coexistence often struggle to account correctly for the necessary scale, life stages, and system complexity that must be incorporated into experimental design (Gomez-Llano et al., 2023; Hawlena et al., 2022). This can be challenging even for unitary organisms where there is no difficulty in defining the individual. In the case of fungi, the challenge is exacerbated by their indeterminate individuality and complex life history. The concept of UCI can help address the challenges of empirical studies in at least four ways. First, the UCI concept can bring clarity to thinking about which levels of biological organisation are important for which coexistence mechanisms. As exemplified above, some mechanisms focus on physiologically integrated mycelia in local neighbourhoods, while others focus on lower-level UCIs and their role within and between environmental patches. Second, the UCI concept helps to design studies in which the relevant spatial scales for specific coexistence mechanisms and fungal species are correctly identified. For ecologically modular organisms, there is no reason to assume that physiologically integrated individuals are always local (Smith, Bruhn & Anderson, 1992). That is, a physiologically integrated mycelium may extend over a heterogeneous region. In this case, lower-level UCIs are needed to design the study properly. Third, there is no reason to believe that the above works the same way for all competing species. Different competitors may use different morphological structures as UCIs with the same competitive function. For instance, different competitors may use different morphological types for dispersal within a region, and competitors may span different spatial scales, with some mycelia acting as local UCIs while in other species mycelia are better represented as populations of UCIs (Boddy, 1999; Hiscox et al., 2018). Thus, the UCI concept provides a robust, theory-based comparison between Biological Reviews (2024) 000–000 © 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Coexistence theory and filamentous fungi 15 1469185x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/brv.13119 by University Of Jyväskylä Library, Wiley Online Library on [07/08/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License competing species with different life histories, helping to avoid pitfalls of inappropriate comparisons. Finally, the UCI concept facilitates the definition of relevant vital rates and variables used for quantitative tests of species coexistence (Barabas et al., 2018). So far, we have explained the utility of the UCI concept to define clearly the competing entities in organisms with indeterminate individuality. This is important to provide clarity in defining research questions, scales, selecting models, and designing experiments. Once the competing units are delineated, the next step in empirical coexistence studies is to determine which UCIs (and aspects thereof) should be used as a fitness proxy to measure the effects of environment and competition (Barabas et al., 2018; Chesson, 2000b; Pringle & Taylor, 2002). That is, we need to define which UCIs and their characteristics are appropriate to quantify the key parameter of growth rate for residents and invaders (Barabas et al., 2018;Grainger et al., 2019b). For organisms such as unitary microbes, this is straightforward, and the same unit, the single cell, which is expected to interact in the community, is used to quantify the competitive and environmental responses of the population (Narwani et al., 2013). Once the organism has a modular morphology and/or multiple life stages, the competing and quantified UCIs may differ, and in general, the quantified UCIs may be more variable. To illustrate, in plants, researchers quantified the number of seeds per individual (Angert et al., 2009;Godoy et al., 2014), the number of newly established seedlings (Adler et al., 2010;Angertet al., 2009;Chu&Adler,2015), the proportion of surviving seeds (Godoy et al., 2014), the number of inflorescences in annual plants (Sears & Chesson, 2007), or the area covered by an adult plant (Adler et al., 2010;Chu& Adler, 2015). In these plant studies, the decision about quantified UCIs was made based on species life history, and the particular coexistence model applied to this life history. Similarly, fungal ecologists must consider the variability of life histories and the characteristics of coexistence mechanisms to quantify coexistence. For example, if the environment can be idealised as two-dimensional and the coexistence mechanism does not involve regional dispersal, then the change in area covered by mycelia over the period of competition may be a useful vital rate to measure, similar to some plant studies (Adler et al., 2010; Chu & Adler, 2015). If the coexistence mechanism involves persistent stages, the survival rate of persistent UCI (which can have many morphological forms, such as spores or mycelial structures) can be quantified (Hopkins & Bennett, 2023; Willetts & Bullock, 1992). If the coexistence mechanism is based on patch dynamics and involves both local competition and dispersal between patches, then depending on the model, researchers can quantify the results of local competition, dispersal kernels or the number of newly colonised patches (Shoemaker & Melbourne, 2016; Tilman, 1994). Before providing examples, it is useful to clarify the relationship between two levels of abstraction in MCT: canonical coexistence mechanisms and coexistence models adapted for specific systems. Coexistence research operates at several levels of abstraction. At the core are the most general concepts of MCT, i.e. the mechanisms of species coexistence (Amarasekare, 2003; Barabas et al., 2018; Chesson, 2000b). They can be viewed as ecological principles that provide insight into the general conditions under which species can or cannot coexist. As such, their parameters are general and broadly defined. To adapt them to a specific system, it is often necessary to introduce more detailed parameters and relationships (Fig. 5; Adler et al., 2010; Warner & Chesson, 1985). These more detailed models should inform in a straightforward manner what UCIs we quantify and what aspects should be measured. In Fig. 5and in the text below, we present two simple example models and show how the choice of a particular model affects the definition of a UCI and its properties that need to be quantified. Warner & Chesson (1985) developed a model of coexistence based on the storage effect and recruitment fluctuations in species with overlapping generations. Similar models could be adapted to iteroparous fungi. The key step in this adaptation is to use the UCI concept to distinguish between generations (i.e. parent mycelia and new recruits) (Fig. 5). Adler et al.( 2010) developed an agent-based model for perennial plants that captures multiple stabilising mechanisms arising from both competitive interactions in local neighbourhoods and temporal environmental fluctuations. The structure of the model takes into account competition for space and competition at a distance, processes that are important in fungal communities (Adler et al., 2010;Kolesidiset al., 2019). In fungi, competing agents in similar agent-based models could be defined as UCIs at different levels of organisation (Fig. 5). To conclude, testing species coexistence through model parameterisation offers several advantages. This approach can provide insights into which coexistence mechanism, vital rates (e.g. recruitment, growth, mortality), or which UCI (submycelial regions, entire mycelia, propagule-like UCIs) contribute to coexistence and to what extent (Adler et al., 2010; Chu & Adler, 2015; Hawlena et al., 2022). The use of models provides a mechanistic, quantifiable insight into species coexistence. However, if this approach is not feasible, ecologists can still test coexistence at a more phenomenological level by applying the mutual invasibility test (Adler et al., 2010; Narwani et al., 2013; Siepielski & McPeek, 2010). (7) Future theoretical perspectives In order to introduce fungi into MCT, we offered the theory mostly in its established form (Amarasekare et al., 2004; Chesson, 2000a,b), and contributed the novel concept of the UCI. However, we do not want to give the impression that the final, conclusive state of theory has been reached. The field is undergoing theoretical developments, and we highlight those that are most relevant to fungi and ecologically modular organisms, together with our further suggestions for theoretical developments beyond the UCI concept Biological Reviews (2024) 000–000 © 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 16 MilošBielˇ cik and others 1469185x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/brv.13119 by University Of Jyväskylä Library, Wiley Online Library on [07/08/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License that are desirable specifically for ecologically modular organisms. We also provide examples of how the UCI concept can be used in the design and communication of fungal studies related to priority effects, agent-based modelling or neutral coexistence. First, original work by Chesson (2000a,b) assumes a fully deterministic mutual invasibility, i.e. there is no lower bound for the invader’s population size. In fact, theory suggests that the lower the invader’s initial density, the faster will be its initial growth. However, species with positive within-species interactions (e.g. Allee effect) may only invade from a certain initial threshold density (Grainger et al., 2019b; Schreiber, Yamamichi & Strauss, 2019). When interference is a substantial component of competition, and interference ability is positively dependent on density (UCI size, or UCI counts) (Kolesidis et al., 2019), even potentially coexisting species may be incapable of mutual invasion from low numbers (or spore count, or mycelium size) (Nix-Stohr et al., 2008). Hence, fungal ecologists should observe and contribute to the ongoing theoretical debate on the mutual invasibility criterion (Ellner et al., 2022). Second, further theoretical research is needed to clarify the role of priority effects in fungal coexistence. Priority effects in the narrow sense of the term (i.e. as niche Fig. 5. (I) The equation Njt+1ðÞ=1−dj  NjtðÞ+RjtðÞNjtðÞ, adapted from Warner & Chesson (1985), represents a simple model for the population dynamics of a species jover time. In this equation, the population size at time t+1,N j (t+1), is influenced by the population size N j at the previous time step, the fluctuating recruitment rate R j (green), and the constant mortality rate d j (red). This model is applicable in situations where the environmental and competitive factors affect new recruits and older individuals (units of community interaction, UCIs) differently. Originally developed for plants (I.A), the model does not explicitly consider seeds, i.e. pre-recruitment UCIs, in its basic form (grey, 1). The model does consider and distinguishes between three types of UCIs: UCIs newly recruited in the current time step (green, 2), the sum of living older UCIs and new recruits (blue, 3 and green, 2), and UCIs that perished in the current time step (red, 4). I.B illustrates the flexibility of the UCI concept in modifying the plant model for modular organisms. A specific property of UCIs (e.g. threshold size, degree of physiological autonomy, or variations in environmental responses) is predetermined to categorise some UCIs as individual-surrogates (5, 6 and 7), while the remaining ramets and spores, i.e. pre-recruitment UCIs, are not quantified (8, 9 and 10). (II) Adapted from Appendix S1 in Adler et al.( 2010), the equation wjk =πNkXk αkAprovides another example from a plant model with potential applications in fungi. This equation is employed in the model to define the crowding effect in local plant neighbourhoods (II.A). wjk can be interpreted as the impact of neighbourhood competition imposed by species kon species jin sessile systems where spatial competition can be coupled with other forms of more distant interactions, such as chemically driven interference competition. These effects are accounted for by the terms Xk(red arrows), representing the average size of an individual of species k, and αk(pink arrows and dashed areas), denoting the spatial scale of the effect of species kon all other species in its vicinity. N k represents the number of individuals (UCIs), and Asignifies the unit of modelled area (orange). We use this equation to demonstrate the utility of UCIs in the rigorous definition of processes and variables in local neighbourhoods of modular organisms at different spatial and biological scales (II.B, C). The model can be applied to fungi at different levels of organisation: either mycelia (II.B), or ramets within the mycelium (II.C). While doing so, the UCI concept helps maintain conceptual clarity and aids in answering questions about the characteristics of UCIs that are essential for correct application of the model. For instance, it helps in assigning the average size of the ramet or genet, the unit of area (A), or it helps in navigating the model’s assumptions. For example, the assumption of randomness in UCI distribution is acceptable in (II.B), but not in (II.C): here, we should expect the mycelium to tend to space lower-level UCIs in an orderly fashion. Biological Reviews (2024) 000–000 © 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Coexistence theory and filamentous fungi 17 1469185x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/brv.13119 by University Of Jyväskylä Library, Wiley Online Library on [07/08/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License pre-emption; Fukami, 2015) have been proposed as one of the drivers of coexistence in symbiotic fungi (Kennedy, 2010). However, in the coexistence literature, priority effects are now perceived as preventing rather than driving the coexistence (Fukami, Mordecai & Ostling, 2016;Grainger et al., 2019a). Still, priority effects are characterised by small fitness differences between species. Small fitness differences could potentially promote coexistence, if coupled with niche differentiation that occurs at a different scale from that at which preemption is observed (Kennedy, 2010). Since the priority effects of modular organisms depend on scale and UCI type, it should always be made clear which UCIs prevent invasion (e.g. compact or loosely grown mycelia) and in what form of propagule-like UCIs the competitor arrives. For example, if we show that colonisation by spores results in priority effects, this may not be true if dispersal is by propagule-like UCIs in theformofmycelialoutgrowth.Wesuggesttheresultsshould be communicated with similar resolution. Another theoretical challenge is the role of within-species variability in coexistence (Hart, Schreiber & Levine, 2016). Mathematical models of MCT imply no within-species variability. Yet in fungi, competitive ability depends not only on species identity but also on an individual’s mycelium size (Kolesidis et al., 2019). Therefore, it is likely that approaches such as individual-based modelling will become a valuable tool in fungal coexistence research, as they can readily address the influence of within-species variability (Grimm, Aylion & Railsback, 2017; Jeltsch et al., 2019; Milles, Dammhahn & Grimm, 2020). For agent-based models, the use of UCI concepts is straightforward, as agent and UCI can often be treated as synonyms. UCI can then help to define and communicate the state variables, properties of agents and their interactions (Grimm et al., 2020). An important conceptual feature of MCT is the dualism between within-species (i.e. intra-specific) and among-species (i.e. interspecific) competition. Yet in fungi and some other groups of ecologically modular organisms, this dualism may be imprecise, since within-species interactions differ dramatically based on the ability of interacting mycelia to fuse (Paoletti, 2016; Shahi et al., 2016; Stahl & Christensen, 1992). Mycelia of a single species that do not fuse (i.e. anastomose) will compete for space and resources without establishing any degree of cooperation (Stahl & Christensen, 1992). By contrast, if mycelia fuse, their constituent, lower-level UCIs can interact in both a competitive and cooperative manner (Richard, Glass & Pringle, 2012). Therefore, for fungi and similar organisms capable of somatic fusion, we propose adaptation of MCT terminology to distinguish between three types of competitive interactions: intra-clonal, intra-specific and inter-specific. Furthermore, it is important to note that the theoretical assumptions on which MCT is based have not been fully resolved. For example, debate continues about the importance of higher order interactions, coexistence in communities of multiple species or in systems with alternative stable states (Barabas et al., 2018; Singh & Baruah, 2021; Spaak & Schreiber, 2023). Similarly, discussion is ongoing on the importance of equilibria and fully deterministic, stable coexistence (Revilla & Weissing, 2008). It is debated to what degree biodiversity can be maintained by unstable coexistence, with overlapping concepts of effective coexistence, unprotected coexistence, and coviability (Amarasekare, 2003; Jeltsch et al., 2019). The latter framework highlighted the importance of stochastic processes within local neighbourhoods, which could be of great significance for fungal coexistence (Jeltsch et al., 2019). Fungal ecologists can contribute to this debate by using UCIs to define the scales at which local neighbourhoods drive important processes, and by using UCIs to define agents in agent-based models of species co-viability (Jeltsch et al., 2019). Finally, in addition to deterministic biodiversity concepts based on niche theory, such as MCT, a neutral theory of species coexistence has been proposed (Hubbell, 2005). Recent developments in MCT state that neutral coexistence is a rather special, unlikely case that is only possible when both niche and fitness differences between competitors are zero (Grainger et al., 2019a). While this scenario seems unlikely, the really interesting scientific question might not be whether coexistence is neutral or not, but to what extent it is neutral (Adler, HilleRisLambers & Levine, 2007;Graingeret al., 2019a). And while the scenario of perfect neutrality seems unlikely indeed, the abundance of interactions in species-rich communities can act as an equalising factor. This has been hypothesised for intransitive networks: while competitivedifferencebetweentwospecies may be high, a third species can lower this by giving an advantage to the weaker competitor (Allesina & Levine, 2011;Levine et al., 2017). Thus, neutral processes of emigration, immigration, and drift have received attention in explaining biodiversity persistence in species-rich systems such as tropical rainforests (Bongalov et al., 2019; Vandermeer, 1996). Fungal communities exhibit similarly high species richness, and although studies have shown a relationship between fungal community composition and environmental gradients (as would be expected from the determinism of niche theory; Brown et al., 2013), it is also important to note that each locality (definedhereasanareawhere environmental variables are homogeneous) can host multiple species simultaneously (Baldrian et al., 2012;Krahet al., 2018; Kubartovaet al., 2012). Fungal ecology is just beginning to explain the processes that produce these patterns, but neutral processes may also play a role. Research on symbiotic fungi suggests that both niche-based and neutral processes structure fungal communities in space (Caruso et al., 2012; Dumbrell et al., 2010). Unravelling the contribution of possible nichebased and neutral processes will require mechanistic insights based on a clear definition of spatial scales, local and propagule-like UCIs, and their role in the respective processes (Brown et al., 2013). VI. CONCLUSIONS (1) Existing theory in spatial ecology has been developed focusing on unitary organisms. In effect, the concepts and Biological Reviews (2024) 000–000 © 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 18 MilošBielˇ cik and others 1469185x, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/brv.13119 by University Of Jyväskylä Library, Wiley Online Library on [07/08/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License frameworks of spatial ecology, represented here by modern coexistence theory, do not facilitate research on modular life forms. We argue that conceptual development is an essential step in designing feasible coexistence research for complex modular life forms, as represented here by filamentous fungi. (2) In addition, a closer integration of fungal community ecology and modern coexistence theory is missing. This integration could facilitate both fundamental and applied research on mechanisms that govern fungal biodiversity, and could benefit both disciplines. (3) Answering these requirements for theoretical development, we used modern coexistence theory to define a practical concept of unit of community interaction. This is a conceptual development that facilitates feasible coexistence research for complex clonal life forms. This concept enables a focus on biological features that are primarily relevant to the process a researcher intends to study, and distinguishes them from complexities of clonal life forms that are of secondary interest. (4) We showed that modern coexistence theory can be a very practical framework for navigating empirical research in the community ecology of fungi and other clonal organisms. It provides insight into which spatial scales and levels of biological organisation are meaningful to study. It places competitive interactions into a wider, holistic framework and elucidates natural history gaps. (5) Our novel concept of UCI is defined as process-centric, always based on how the coexistence mechanism/model is defined. 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