The Developing Relationship Between the Study of Fungal Communities and Community Ecology Theory

Fungal Ecology xxx (xxxx) xxx

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Fungal Ecology

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Commentary The developing relationship between the study of fungal communities and community ecology theory

Thomas D. Bruns

Dept. Plant and Microbial Biology, University of California, Berkeley, United States article info abstract

Article history: Plant and animal systems had a head start of several decades in community ecology and have largely Received 30 October 2018 created the theoretical framework for the field. I argue that the lag in fungal community ecology was Received in revised form largely due to the microscopic nature of fungi that makes observing species and counting their numbers 28 November 2018 difficult. Thus the basic patterns of fungal occurrence were, until recently, largely invisible. With the Accepted 10 December 2018 development of molecular methods, especially high-throughput sequencing, fungal communities can Available online xxx now be “seen”, and the field has grown dramatically in response. The results of these studies have given Corresponding Editor: Lynne Boddy us unprecedented views of fungal communities in novel habitats and at broader scales. From these advances we now have the ability to see pattern, compare it to existing theory, and derive new hy- Index descriptors: potheses about the way communities are assembled, structured, and behave. But can fungal systems Competition contribute to the development of theory in the broader realm of community ecology? The answer to this Mutualisms question is yes! In fact fungal systems already have contributed, because in addition to many important Diversity-function natural fungal communities, fungi also offer exceptional experimental communities that allow one to Community assembly manipulate, control, isolate and test key mechanisms. I discuss five well-developed systems and some of Experimental communities the contributions they have made to community ecology, and I briefly mention one additional system History that is amenable to development. © 2018 Elsevier Ltd and British Mycological Society. All rights reserved.

Community ecology is focused on interactions among organ- 1. What predicts the composition of a community in time isms, and its broadest goals are to understand the processes that and space? determine the occurrence of assemblages of species in time and space as well as the functional consequences of these communities. This is a classic question in community ecology, and it was In the hierarchy of ecological studies, community ecology fits be- essentially the first question addressed. Plant systems provided the tween the autecological or population ecology levels that focus on earliest answers with the classic work of Fredric Clements (1916). the properties of individual species, and the ecosystems level that He envisioned communities passing through definable serial stages focuses on the biogeochemical processes that emerge from in- until they reached a stable climax community, and he described teractions between communities and their environments. These this successional process using the metaphor of organismal different levels of ecology are human constructs, but in nature they development. The climax community varied with the location and exist as a continuum such that properties of individual species ul- climate, but given these parameters plant communities should be timately determine which species form a community, and the definable and predictable - the hallmarks of a useful, deterministic structure of the community ultimately determines its ecosystem model. This was a huge leap forward and his model captured functions. Studies in fungal ecology occur at all these levels, but for enough of the observable pattern that it ruled the field until this paper I focus on a subset of studies at the community ecology experimental work started to cast doubt on the validity of the level, and I place them in the context of some of the classic ques- underlying pattern and mechanisms in the 1950s, but it continued tions that community ecology tries to answer. to permeate textbooks well into the 1970s. Henry Gleason, who was a contemporary of Clements, saw things quite differently. He took exception to the quasi organism metaphor, thought that Clements glossed over the variation among communities, and stated that community composition was deter- E-mail address: [email protected]. mined by the individual traits of the plants included in them https://doi.org/10.1016/j.funeco.2018.12.009 1754-5048/© 2018 Elsevier Ltd and British Mycological Society. All rights reserved.

(Gleason, 1926, 1927, 1939). His papers, however, were largely plant ecology. Much of this theory fit fungi very well, because like ignored at the time, and were only revived and appreciated in the plants, fungi are largely sessile, compete for resources by occupying late 1940s and early 1950s (McIntosh, 1975). Reading his papers territories, and disperse to new territories by propagules or growth. now, I wonder if their lack of impact was due in part to Gleason's These shared features determine much about the ways that plant rather acidic writing style and his relatively data-free arguments, and fungi assemble into communities. but whatever the reason, Clements' climax view prevailed for decades. 2. What changed to make fungal community ecology a If we now fast-forward to current times Clement's climax theory vibrant field? is viewed as a quaint historical model, and the current community assembly theory (Kraft et al., 2015) has become very “Gleasonian”. Today community ecology is certainly alive and well in The basic idea is that organisms pass through a number of filters to mycology, and this can been seen from the trends in the literature establish a community, and these filters: dispersal, physical envi- over the past 20 y (Fig. 1). This explosion in the field has been very ronment, and competition with other organisms, interact with the method-driven, especially by application of molecular methods individualist characteristics of the species to determine the set of (Peay et al., 2008; Nilsson et al., 2018). The general nature of these community residents (Kraft et al., 2015). This model is strikingly tools has also opened the study of fungal communities to micro- similar to Gleason's last defense of his ideas (Gleason, 1939), and it biologist and plant ecologists and has lead to greater integration of has now been widely applied to plant, animal, fungal, and microbial fungi into these disciplines. Meetings and workshops supported by systems. the Ecological Society of America, the NordForsk research network, Where, might you ask, were fungal ecologists in the develop- and the series of Ecology of Soil Microorganisms meetings provide ment of such theories? The answer during the time of Clements and good examples of this trend. Gleason was: “doing other things”. One of the true giants in This broadening of the field has been facilitated by coordinated mycology, A.H. Reginald Buller, published his first volume of Re- work of many mycologists. Databases that make these DNA searches on Fungi in 1909, and the second in 1922 (Buller, 1909, 1922). Thus he was a contemporary of Clements and Gleason, and at this time fungi were plants and the botany literature was where the fungal literature was to be found. In fact when Gleason argued about the differences between a reproducing organism and a regenerating community he used the fungus Rhizopus as the example of an organism (Gleason, 1926), while Clements mentioned Pyronema con- fluens in fire succession and discussed Pythium as an agent for seedling mortality (Clements, 1916). Clements also authored three books on fungi that Buller had in his library along with a copy of Weaver and Clements' 1929 book on plant ecology (Oliver, 1965). Thus it is highly likely that Buller was fully aware of the de- velopments in plant community ecology. Buller certainly conducted ecological work, but primarily at the autecological level. For example Researchers on the Fungi volume 2 had studies of squirrel and slug mycophagy (Buller, 1922). So ecology was within Buller's broad set of interests, but community ecology apparently was not. Moreover, this is not just Buller's lack of interest, but also that of the entire field of mycology for several decades. Why? I think the primary answer to this question is that fungal communities are not as easily seen as plant or animal communities. Fungal species and individuals could not be tallied, and that is the basis for describing communities. Without the ability to see patterns it was hard to apply theories, let alone develop them. My- cologists did eventually become interested in communities, as is well documented by the early series of Fungal Community books (Wicklow and Carroll, 1981; Carroll and Wicklow, 1992), but the first necessary steps were to catalogue the species in communities, and this was a difficult and time-consuming process in the days before molecular methods. In her presidential address to the British Mycological Society Juliet Frankland (1998) noted this lag in mycological contributions to theory and after similarly summari- zing Clements’ views she stated: “Mycologists, however, lagged behind in developing a quanti- tative and predictive science. For many years they continued to Fig. 1. Growth in Fungal Community Ecology Publications. be absorbed in describing and listing species. As late as 1992 it (A) Results from a Web of Science search for papers that include “fung* and commu- could still be said by [Alan] Rayner that `fungi are commonly nit*” in the title, abstract or key words are shown over a 20 y period. Trend line show e omitted from the ecological and evolutionary debates of the exponential growth with nearly an 11-fold increase from 208 papers in 1998 2240 papers in 2017. (B) Subset of the papers in A that include “mycorrhiz* ” (solid circles) or ” day'. “endophyt*” (X) show exponential increase during the same period. Subsets of papers in A that include the terms “Yeast*”, “marine or ocean”,or“wood AND decay” (not shown) exhibit similar dramatic increases though at a lesser scale, while papers Thus as fungal community ecology started to take off it devel- include the terms “’next generation sequence’ OR ‘high throughput sequence’“in- oped into a pre-existing body of theory developed primarily in crease exponentially after 2007 (not shown).

Please cite this article as: Bruns, T.D., The developing relationship between the study of fungal communities and community ecology theory, Fungal Ecology, https://doi.org/10.1016/j.funeco.2018.12.009 T.D. Bruns / Fungal Ecology xxx (xxxx) xxx 3 sequences retrievable and useful have been instrumental in pro- study on Antarctic lakes, where the most abundant fungal se- pelling the field forward, and the UNITE database, with its curated quences belong to unknown basal groups in or near the Chy- set of sequences organizing into “species hypotheses”, has been triodiomycota and Rosellomycota (Cryptomycota) (Rojas-Jimenez particularly important in this regard (Koljalg et al., 2005; et al., 2017). Abarenkov et al., 2010). Statistical and bioinformatical advances The amount we have recently learned about the basic patterns have also kept pace with the data and have allowed researchers to of occurrence of fungi is truly phenomenal. Studies include soil and find pattern in the otherwise overwhelming volume of data derived arbuscular mycorrhizal fungi on a worldwide scale, ectomycor- from noisy environmental backgrounds (Nilsson et al., 2018). FESIN rhizal fungi on continental scales, indoor dust-associated fungi at (fungal environmental sampling and informatics network), a Na- multiple scales, marine fungi, biocrusts, arctic and antarctic fungi, tional Science foundation research coordination network, helped to and many more (Amend et al. 2010, 2012; Adams et al., 2013; Talbot disseminate these methods widely to the mycological and ecolog- et al., 2013; Amend, 2014; Tedersoo et al., 2014; Davison et al., 2015; ical communities through a series of six workshops. The first and Grantham et al., 2015; Tisthammer et al., 2016; Rojas-Jimenez et al., fifth of these meetings were held in conjunction with UNITE (Bruns 2017; van der Linde et al., 2018). These studies represent our first et al., 2008; Bruns and Kennedy, 2009), and this facilitated an views of fungi at these scales or in these habitats, and although the internationally coordinated effort. The recent electronic compila- larger scale studies provide a low-resolution view interpolated tion of herbarium records in North America (Thiers and Halling, from a relatively small number of sites, it is a huge leap forward. 2018) and Europe (Andrew et al., 2017), the collaboration with One of the most surprising distributional results to emerge is that the European environmental monitoring network (Cox et al., 2010; some fungal groups have non-canonical global distributions with Suz et al., 2014; van der Linde et al., 2018), the electronic classifi- species richness increasing away from the equator. Tedersoo et al. cation of fungi into ecological guilds (Nguyen et al., 2016), and (2014) showed this pattern for ectomycorrhizal fungi, and Amend public observational databases such as Mushroom Observer et al. (2010) found it in indoor dust. (Wilson and Hollinger, 2006) and iNaturalist (Agrin et al., 2008) Many strong correlations between fungal community compo- continue to expand this trend of providing us with unprecedented sition and physical or biological components have been found in views of pattern and occurrence of fungi at global scales. recent studies. These correlations include plant host, soil pH, other cation concentrations, soil nitrogen, and deposition of nitrogen and 3. Five advances in our knowledge of fungal communities are potassium (Gao et al., 2013; Talbot et al., 2013; Tedersoo et al., 2014; especially significant Glassman et al., 2017; Bahram et al., 2018; van der Linde et al., 2018; Zhang et al., 2018a). When viewed in the context of community We have learned a tremendous amount from this explosion of assembly theory such correlations are consistent with the idea of fungal community ecology literature in the last two decades, and I “environmental filtering”, but as shown from plant ecology there is cannot present a comprehensive review of it in this short paper. a high bar to demonstrate causality because many parameters of However, I want to highlight five findings from this literature that I the physical environment are co-correlated, and context dependent think are particularly significant for advancement of the field: (1) competitive interactions are often difficult to disentangle from true the discovery of many unknown groups of fungi that often are environmental filters (Kraft et al., 2015). In any case these studies important components in communities, (2) the global and conti- have provided the necessary groundwork for additional experi- nental patterns in fungal diversity, (3) the correlation of community mental work. composition with environmental parameters, (4) the widespread Dispersal limitation is a fundamental process in community pattern of dispersal limitation in fungi, and (5) the common assembly theory (Kraft et al., 2015). If everything is everywhere, occurrence and unique manifestations of priority effects in fungal then communities should be defined only by environmental and competition. competitive processes. However, for fungal communities the The main reason that discovery of unknown fungal groups is “strong” environmental correlations that I refer to above typically important to community ecology is that many of these previously explain a rather modest amount of the variance in species unknown groups are major components of communities of interest composition, and “distance decay”, the turnover of species (Rosling et al., 2011), and it is still the norm to report a significant composition with distance, usually remains a statistically signifi- number of unknown, unclassified, putatively fungal sequences in cant pattern at multiple scales of distance (Amend et al., 2010; high-throughput sequence studies. More exotic or previously Adams et al., 2013; Talbot et al., 2013; Tedersoo et al., 2014; unsampled habitats may have more unknowns, but even well- Tisthammer et al., 2016; Rosenthal et al., 2017; van der Linde et al., sampled habitats still produce them (Talbot et al., 2013; Tedersoo 2018). Such unexplained variance and turnover of species with et al., 2014; Rojas-Jimenez et al., 2017; van der Linde et al., 2018). distance is certainly not limited to fungi, and is probably common The most important reason is that these taxa are not connected to in all hyper-diverse communities. Plant assemblages in tropical rain any specimens or cultures that have been sequenced. Brock et al. forests are good examples and these served as part of the motiva- (2009) showed that even within herbaria, the number of unse- tion for Hubble's neutral theory (Hubbell, 2001; Rosindell et al., quenced, undescribed species is shockingly high. However, a sec- 2011). Distance decay can be caused by dispersal limitation, but it ond reason that environmental sequences are not easily classified is can also be caused by the turnover of environmental or biological that the ITS region, the locus used in most of these studies, does not parameters with distance. For this reason I will refer to several provide useful information on deeper branches of the fungal tree. more direct examples where dispersal was measured or where Tedersoo et al. (2017) solved the ITS part of the problem for a dispersal limitation can be inferred at the individual species level. common subset of unknown sequences by going back to DNA First, there is strong evidence that most fungal species are not samples and retrieving larger DNA sequences that contain more of globally dispersed. The work of Sato et al. (2012) does a nice job of the structural rRNA genes. This allowed the unknown sequences to demonstrating this point for a large number of ectomycorrhizal be placed within novel lineages of the fungi. These novel groups (EM) and saprobic species by using the patterns of ITS sequences were distributed throughout the fungal kingdom, but the basal present in the public nucleotide sequence databases. Perhaps the lineages of fungi were particularly rich in these environmentally strongest evidence that the lack of global distributions are caused, defined sequence groups (Tedersoo et al., 2017). To make the point at least in part, by dispersal limitation comes from the large number about how important some of these groups are, I point to a recent of fungal pathogens that have been moved across continents in

4. The structure of Competition

Competition is a fundamental process that shapes the structure of communities, and fungal systems are starting to have a large impact on our understanding of competition and its roles in structuring communities. Competition was certainly one of the processes that Gleason had in mind with his individualistic view (Gleason, 1927, 1939), it is well integrated into the current com- Fig. 2. Ways that competition can be structured. Competitive outcomes for species A, B munity assembly theory (Kraft et al., 2015), and understanding the and C are depicted.(i) Transitive competition occurs when competitive abilities can be ordered as a hierarchy, and higher ranked species predictably replace lower ranked structure and effects of competition has become its own discipline ones. According to Keddy (2001) competition in most species across all kingdoms is within the field (Keddy, 2001). Competition also has a long history structured this way. (ii) Intransitive competition is not hierarchical, and complex in fungal systems, particularly in the plant pathology literature networks may not result in predicable species replacements. According to Kerr et al. (e.g., Garrett, 1956) but, as Kennedy (2010) pointed out, that early (2002) this is likely to be a common mode in microbial communities that use chem- work was largely missed in the ecological literature. ical toxins to compete with each other. (iii) Priority effects, a subset of the intransitive mode, depends on order of arrival such that if A arrives first, it can prevent B from One of the central ecological questions about competition is colonizing, while reversing the arrival order reverses the outcome. In wood, and other what prevents it from reducing species diversity in communities, or spatially structured communities, this can result in deadlock if different parts of the to put it another way: why do the best competitors not eliminate resource are colonized by A and B, as neither is able to outcompete the other once the less competitive species? Early work by Gause (1934) developed territorial priority is established. In the terminology of Cooke and Rayner (1984), the first arriving species competes by primary resource capture, and later arriving species the idea that species competing for the same resource cannot must employ combative competition to displace them. This concept links dispersal coexist, and his ideas were based on experimental microcosms and competition, because species that invest most heavily in dispersal are the most with Paramecium species. Niche theory embraced this concept and likely winners of primary resource capture.

Fungi made a significant contribution to these ideas, by pointing out competitors meet in the substrate and neither is able to advance that it is the form of competition, not competition itself that varies and replace the other. This interaction has large consequences on among species, and they stated that competition occurs in two the effect of competition on species diversity as was shown by ways: primary resource capture and combative competition (sec- Maynard et al. (2017). ondary resource capture). Thus they viewed dispersal as a form of If we turn to the book on competition (i.e., Keddy, 2001) there is competition, because species that invest heavily in it are more not a single mention of deadlock (or stalemate) in the 553 pages, likely to succeed in primary resource capture, while those that do although these types of interactions are briefly mentioned as subset not must be better at combative take over of resources. This may of “symmetric” competitions in Keddy's terminology. In any case, seem like a subtle point, but it is critically important for three what we learn in the book is that “asymmetric” competitions are reasons. First, it makes Tilman's trade-off between dispersal and the rule. These are situations where one species reliably beats competition more natural, as it becomes a single gradient of another, and the interactions are usually “transitive” meaning that competitive strategy rather than two apparently different traits they can be arranged in hierarchies (Fig. 2). Competitive hierarchies that may or may not be linked. Second, it brings up the point that are found across almost all life forms and communities including dispersal has a strong deterministic component to it; species that wood decay communities (see chapter 5 in Keddy). In contrast, invest more in it are likely to win at primary resource capture and intransitive interactions can result in competitive networks (Fig. 2) be founders of new communities as a result. Finally, it emphasizes in which competition does do not result in an overall winner, the necessary link between territory and resources; this is critically except in pairwise interactions. The idea of such networks dates important because fungi in most communities must capture and back to work on coral reefs (Buss and Jackson, 1979), but was given hold territory to access the resources in it. With this background little weight in Keddy's book. However, Kerr et al. (2002), showed let's now turn to fungal experimental communities. that one could construct such a network with E. coli stains by plating three strains that either produced an antibiotic, were 5. Nectar yeasts e a sweet experimental community resistant to it, or were susceptible to it, and they suggested that these types of interactions would be common among organisms The nectar yeasts and associated bacteria have been developed that compete chemically with toxins in a spatial defined environ- into a highly versatile experimental system for studying basic ments (i.e, not liquid). With this background we are now ready to features of community ecology (Chappell and Fukami, 2018), but it appreciate the results of the Maynard et al. (2017) study. is specifically the work on priority effects that I want to mention Maynard et al. (2017) paired cultures of 37 wood decay fungi in here. The experimental system involves a small number of yeast Petri dishes with synthetic media, scored the competitive out- species that normally arrive in flowers of Mimulus aurantiacus, via comes, and modeled the results of the higher order interactions. humming bird pollinators and compete for the resources in the They found that there were large differences in competitive ability, nectar (Belisle et al., 2012). These yeasts were added experimen- but there was also a high level of intransitive interactions, where tally in all possible pairs either simultaneous or with one yeast lesser competitors could beat higher-ranked opponents. However, added a day before the second (Peay et al., 2012a). Strong priority the most common overall outcome was deadlock, where neither effects were found in some pairs, but not others; what determines species was able to win. Interestingly competitive replacement was this difference? Peay et al. (2012a) found that closely related yeasts most common in pairing of more distantly related or more exerted stronger priority effects than distantly related yeasts, and ecologically dissimilar species. Note that this seems to be just this phylogenetic correlation was co-correlated with the specific opposite of the result found in the nectar yeasts where only close amino acids that limited their growth. This looks a lot like Tilman's relatives and ecologically similar species were able to exert a pri- R*; yeasts limited by different amino acids are able to coexist, while ority effect (Peay et al., 2012a). However, this difference is again those limited by the same amino acids exclude each other. How- based on the distinction between competing in a liquid versus a ever, the real advantage of this system is that the role of resource spatially structured environment. In the liquid the entire resource partitioning in maintaining species diversity could be compared to is one territory, and closely related species that are limited by the other mechanisms that are also operating in nature, such as fluc- same resource can block each other from colonizing based on tuating environment (Tucker and Fukami, 2014; Letten et al., 2018), arrival order; we call this a priority effect. In spatially structured dispersal and metacommunity structure (Vannette and Fukami, environments, like wood, when two species encounter each other 2017), and even competition with bacteria (Vannette et al., 2013; at borders of their territories, the inability of one species to replace Vannette and Fukami, 2018), so that a more complete and realistic another is scored as a deadlock, but it too is essentially a priority view of these interacting processes could be obtained (Fukami, effect, but one limited to the parts of the resource that are colo- 2015). nized. Thus the result is the same in both systems: closely related species are unable to encroach on each other's territories. 6. Wood decay communities - uniquely fungal, and yet The most interesting result from the Maynard et al. (2017) study changing the field of community ecology at large comes from their patch occupancy model that was parameterized from the pair-wise interactions. What their model predicted is that Keeping competition in mind, I want to turn to wood decay species loss from competition drops as the number of species communities to showcase the power of another fungal system that interacting is increased, hence the title of their paper: “diversity is generating new ideas in community ecology. Wood decay com- begets diversity …”. Note that this is a very different answer than munities are quintessential fungal-dominated systems that have a Tilman or Grime proposed to the question of “what prevents long history of study, particularly with respect to the structure and competition from reducing diversity?”; competition does not need roles of competition in a spatially structured environment (Boddy, to be partitioned in some way to prevent species loss. Interestingly 2000). I cannot begin to summarize all the work that has been done Maynard et al.'s result was strongest when the percentage of in these systems, but I will point to Rayner and Boddy (1988) book intransitive interactions (including deadlock) increased in the pool on fungal decay of wood that synthesizes the older literature and of species (Maynard et al., 2017). Thus, it is the non-transitive type lays out many of the ideas that have been followed up more of competition that drives this result, and that type is likely to be recently. One of their ideas is that of “deadlock” as a competitive common in a whole range of spatially structured microbial outcome. This is an observable situation in wood where two fungal communities.

One could argue that the Petri-dish setting and the fairly This is a very reasonable interpretation given that the discs that haphazard collection of species tested make the Maynard et al. retained a diversity of fungi did so because of the many deadlocked (2017) experiment an unrealistic setting. Crowther et al. (2018) outcomes. Note that this result unites community ecology and responded to this concern when they stated: ecosystem function in a novel way e through the predominant type of competition in its members, and again, this is a type of compe- “Importantly, these systems are not intended to mimic the in tition that seems to be widespread in microbial systems. This is situ dynamics of a specific microbial community, particularly unlikely to be the final word on the relationship between species since competitive outcomes are highly context-dependent and richness and wood decay efficiency because there seem to be in- are only one of the many ecological processes determining termediate levels of diversity that result in increased degradation, species coexistence. Rather, the model system used here is especially under conditions of fluctuating environments (Toljander intended to explore how complex patterns arise from simple et al., 2006). Nevertheless, it shows that generalities derived from pairwise interactions.” plant communities do not always fit well in microbial settings, and the relatively simple experimental systems of the wood decay In other words their system did what all other experimental community are a great place to further develop our understanding community systems do - they simplify nature and allow one to of these relationships. focus on a few questions, mechanisms, or parameters of interest. If understanding specific communities is the goal, then wood 7. Mutualisms - a part of the field that fungi should own decay communities lend themselves to more realistic experimental settings. For example, experiments on wood discs or chips are a Mutualisms fit in the realm of community ecology because they common experimental medium that captures the features of the involve emergent properties of species interactions. As a sub- natural habitat in a two-dimensional, easily replicated format discipline within the field theory development has taken an inde- (Holmer and Stenlid, 1997; Song et al., 2017; Toljander et al., 2006). pendent track from community ecology at large, and experimental Taking this system to the next level, O'Leary et al. (2018) expanded systems have been crucial to this process (Bronstein, 2015). Fungi to three dimensions by inoculating wooden blocks and stacking are involved in so many classic, widespread, and important mutu- them in various configurations to explore the effects of wood alisms such as lichens, mycorrhizas, clavicipitalian endophytes, structure and arrangement on fungal communities. Interestingly epiparasitism of mutualistic fungi, ant cultivation, and bark and they too found that intransitive interactions were key for main- ambrosia beetles, that one might assume they have contributed taining species diversity, but also showed that these interactions heavily to the development of theory, but that is not really the case. preserved diversity most effectively when fungal individuals were Instead plant-insect pollination mutualisms such as fig wasps and less spatially fragmented (O'Leary et al., 2018). yucca moth have been the premier experimental systems until Wood decay communities have also weighed in on the classic more recently when the Bradyrhizobium-legume system has made question: “what are the functional consequences of species di- significant contributions (Bronstein, 2001; Yu, 2001; Kiers et al., versity?” This is a pivotal ecological question that has the potential 2003; Pellmyr, 2003; Sachs et al., 2010). One of the classic ques- to unite community ecology and ecosystem ecology. Like all such tions in mutualisms is: how are they stabilized? Or to put it another important questions, the plant ecologists have been interested in it way what prevents or limits cheating? This question has had a lot of for a longtime, and the answer that they found is that species di- attention in intimate, specific mutualisms in which one partner versity increases productivity. There is debate about the shape of lives within the other (Bronstein, 2001; Yu, 2001; Kiers et al., 2003; the curve and the drivers of the relationship, but I think it is uni- Pellmyr, 2003; Sachs et al., 2010), but in diffuse mutualisms such a versally recognized that the relation is positive at least up to some mycorrhizas, where each organism is connected to multiple part- threshold (Duffy et al., 2017). The Tilman et al. (2001) Science paper ners, it is a much more difficult problem to test. is perhaps the most well-cited study in this literature, but there are Arbuscular mycorrhizal (AM) systems are an excellent example many papers before and after it that establish this same relation- of a diffuse mutualism, and they are critical in most terrestrial ship (Duffy et al., 2017). The Tilman paper, like many others, was a ecosystems. The fact that the AM fungi cannot be grown or main- replicated, experimental manipulation that involved planted, tained without a plant host adds a barrier to making it into a weeded plots, essentially the Petri-dish or wood disc equivalent of tractable experimental system. However, many AM fungi can be plant communities, and this setting was highly effective in allowing maintained in pot cultures (e.g. Morton et al., 1993), and a subset the factor of species numbers to be isolated from multiple con- can be grown in Petri dishes in co-culture with transformed carrot founding variables (Tilman et al., 2001). Van der Heijden et al. roots (Becard and Fortin, 1988). The pot-culture approach has been (1998) addressed the same question for arbuscular mycorrhizal used extensively to generate inoculum for experiments in com- (AM) by manipulating species diversity of AM fungi in plant mes- munity ecology. The Van der Heijden et al. (1998) study, which I ocosms, and showed that plant diversity, shoot biomass, root mentioned above in the section on ecosystem function, is one good biomass, hyphal length, phosphorus extraction from the soil, and example of manipulated AM communities, and there are many plant phosphorus content all increased with increasing AM species others. However, to dissect the structure of the AM mutualism, richness. So the question is answered in a more general way: Kiers et al. (2011) combined the techniques of isotope labeling, with increased diversity results in increased ecosystem function. pot cultures and root-organ cultures of three different AM fungi. However, if we turn to Fukami et al. (2010) we get an entirely They showed that the plant rewarded the most cooperative fungus different answer to this question in wood decay communities. They by giving it the most carbon when all three fungi were simulta- inoculated 10 wood decay fungi, selected from 96 that they had neously attached to a single plant in a pot culture, and they used isolated from the local forest, onto discs of southern beech wood. transformed root cultures in divided Petri dishes to show that When they compare the resulting species richness to the percent of plants send more carbon to fungi that have access to more phos- wood decayed they found a strong, negative, linear correlation phorus, while fungi deliver more phosphorus to plants that have (R2¼0.70, P < 0.001). Thus ecosystem function was lowered by di- more sugar to trade (Kiers et al., 2011). This study and others versity in this system! What is the reason for this completely (Fellbaum et al., 2014; Bever, 2015) that have shown reciprocal different finding? They speculate it is due to the high frequency of rewards in AM systems have become the basis for applying “bio- antagonistic interactions among the species (Fukami et al., 2010). logical market” theory to explain the stability of the mutualism

(Wyatt et al., 2014; Werner and Kiers, 2015) and, although the motile bacteria using the water film on hyphal networks for model is not without controversy (Walder and van der Heijden, dispersal. This is an important finding because it is a great example 2015; Kiers et al., 2016), it has definitely shaped the way we now of facilitation, and this mechanism is likely to occur in many other think about a broad class of microbial mutualisms and explained systems where fungi and bacteria occur together (e.g., soil, some of the community-level patterns in AM systems (Werner compost, dung, even wood). et al., 2014; Werner and Kiers, 2015). Herbivore dung is the last system I will mention. It is a poten- Cross-feeding yeasts offer another fungal system that is useful tially rich experimental system that has not received much modern for developing and testing mutualistic theory (Muller et al., 2014; attention. Although dung lacks the charisma of other systems I have Hoek et al., 2016). As currently implemented the system consists of discussed, dung decomposition certainly has an underappreciated pairs of Saccharomyces cerevisiae strains that are engineered to be importance in ecosystems. In fact, herbivore dung is so abundant complementary auxotrophs for two amino acids. To grow on min- and fruiting of fungi on it so predictable that spores of Sporormiella, imal media the strains must grow together because each lacks the a common dung fungus, are used in the fossil record to document ability to produce an amino acid that the other produces in abun- the abundance of grazing megafuna (Johnson et al., 2015)! dance. The strength of this dependence can be adjusted by sup- The potential to use dung communities as an experimental plying one or both amino acids in the media, and this can be tested system is high because it contains a tractable number of common, across a range of concentrations. The strains are tagged with rapidly growing fungi that fruit in defined time sequences florescent proteins; thus the outcome of experiments can be (Webster, 1970). Most or all of these grow well in culture, although determined rapidly with digital imagery on Petri dishes (Muller some require slightly exotic (e.g. dung agar) media to do so. The et al., 2014)orflow cytometry in liquid media (Hoek et al., 2016). habitat is also rich in mycoparasitic, invertebrate, and bacterial- The simple conditions, rapid growth, and automated analysis allow fungal interactions so a full set of community interactions occur high replication of multiple conditions within just a few days. In in this habitat. The primary mode of fungal dispersal is via herbi- many ways these cross-feeding yeasts are the polar opposite of AM vore feeding on plant material that is inoculated with dung fungi; fungal systems that are technically demanding and relatively slow this route ensures a diverse inoculum on freshly deposited dung. to setup and analyze. Of course, the yeast mutualism is totally Later arrival of fungi via dung beetles, flies and phoretic mites in- contrived; nonetheless it provides detailed insights into the success creases diversity, especially of mycoparsites, and presumably aerial of the two “mutualists” as their interactions transition between dispersal is also involved but is likely to be much less predicable. obligate mutualism, facultative mutualism, parasitism, and Dung samples can be sterilized and inoculated with selected fungi competitive exclusion (Hoek et al., 2016), and shows how the or incubated under varying conditions to affect the outcome of strength of the mutualism interacts with independent dispersal of fungal colonization or fruiting, and like wood-decay communities the two participants (Muller et al., 2014). Future elaborations of this competitive interactions can also be simplified to Petri-dish arenas. system are likely to produce many key insights into mutualistic Dung is a rich medium with an abundance of dead and dying interactions. fecal microbes combined with partially digested plant material. In combination these materials provide both highly labile and recal- 8. Cheesy and shitty fungal systems with great potential citrant carbon pools coupled with abundant organic nitrogen and phosphorus. Thus, dung provides a variety of different limiting What predicts the composition of a community in time and resources that could facilitate niche partitioning based on chemical space? Let us return to this original question in community ecology substrates. The earliest ideas about succession in dung fungi were to showcase two more fungal systems of note: cheese and dung. based on the “nutritional hypothesis”, where the labile compounds First, I will turn to cheese rind communities that have both fungal are consumed first by fast-growing fungi with limited enzymatic and bacterial components, and that under controlled conditions resources (e.g. Mucorales), and these are followed by fungi that yield highly predicable, reproducible outcomes. Clements would be target the more recalcitrant compounds like cellulose and lignin. It jealous of the deterministic character of cheese rind communities! is a beautiful, uniquely fungal theory. Unfortunately many obser- However, these very predictable, stable communities are derived vations and experimental results are inconsistent with it (Webster, from a carefully choreographed inoculation of a nearly sterile 1970), and although the theory retains historical significance, the habitat that is then incubated under controlled conditions; this explanatory value of it has largely been discarded in much the same industrial process thus uses the “Gleasonian” individualism of the way as Clements’ climax theory. component organisms, shaped by a highly controlled environment, The experimental work on dung communities is quite limited, to yield a predictable outcome. The “natural” communities within and predates molecular methods. Early work by Harper and cheese have now been sampled fairly well, so the species involved Webster (1964) investigated the apparent succession of fungi on are well documented and are also easily cultured (Wolfe et al., rabbit dung and concluded that time to fruiting alone account for 2014; Irlinger et al., 2015). The best part, however, is that these the sequence, and no “succession” was necessary to account for the cheese communities can be assembled in microtiter plates, so pattern. A later study by Wicklow and Hirschfield (1979) found replication can be very high, and experiments can be run in a few evidence for direct interference competition by fungi in cattle dung. days (Wolfe et al., 2014). It is hard to think of a better experimental Some of the competition, especially involving Coprinus and Copri- community system. nellus species seems to involve direct chemical antagonism and Recent work on the cheese community by Zhang et al. (2018b) hyphal interference (Webster, 1970). In total it is ripe for develop- has shown that the founding fungal species has an enormous ef- ment into an experimental community, now that we have modern fect on which bacteria dominate. These fungi could be viewed as tools for assessing species composition. “keystone” species. Although the abundant biomass of the fungi in these systems probably stretches the original definition, there is 9. Final thoughts precedent for application of this concept to species that ultimately have large biomass (Paine, 1995). In any case, Zhang et al. (2018a,b), Fungi offer experimental communities of every scale and show that the bacterial community is strongly affected by having a description to enable us to test and develop theory. Their contri- fungus present, and it is also specifically affected by which fungus is bution to the broader field of community ecology is potentially present. They go on to show that the general fungal effect is due to enormous because they offer systems where complexity can be

Table 1 Summary of fungal experimental communities discussed. Features that make an experimental community useful include: ease of manipulation, simplicity in species and conditions, ability to run high numbers of replicates, ability to realistically capture processes of a natural community, importance of that process, and use by several independent research groups. þ characteristic present, - absent, þ/ present or absent depending on implementation, (þ) present marginally or with difﬁculty; ? unclear.

Ease of manipulation Simplicity High replication Realism Natural importance # groups using it

Nectar Yeasts þþþþ?(þ) Wood Decay þþþþ/þ þ In vitro AM fungi e þ (þ) þ/þ (þ) Cheese þþþþ(þ)(þ) X-feeding yeasts þþþee (þ) Dung þþþþ(þ) e reduced, factors can be isolated, and conditions can be highly Acknowledgements replicated to obtain a mechanistic understanding of processes of community assembly and function. The experimental communities I thank my students and postdoctoral associates, who deserve discussed above have the attributes necessary to become great credit for my continued training me as an ecologist, and Peter ecological study systems (Table 1), and with the exception of the Kennedy, Kabir Peay, Bjørn Lindahl, Lynne Boddy, and an anony- dung system, all have already produced results that have made an mous reviewer for their suggestions on earlier versions of this impact on the field of community ecology. manuscript. I am grateful to various ecology programs of US Na- It is particularly encouraging that the experimental systems that tional Science foundation, and the USDA for past funding and the I have discussed are largely spearheaded by researchers who would Department of Energy DE-SC0016365 for current funding in this likely identify themselves primarily as ecologists, rather than my- area. cologists. My evidence for this is that they were largely absent from the recent IMC meeting in Puerto Rico, and the papers themselves References are focused on the ecological principles involved, rather than the uniquely fungal features. This pattern brings up one additional Abarenkov, K., Nilsson, R.H., Larsson, K.H., Alexander, I.J., Eberhardt, U., Erland, S., characteristic that experimental systems need to reach their full Hoiland, K., Kjoller, R., Larsson, E., Pennanen, T., Sen, R., Taylor, A.F.S., potential: multiple groups of users. This is important because there Tedersoo, L., Ursing, B.M., Vralstad, T., Liimatainen, K., Peintner, U., Koljalg, U., 2010. The UNITE database for molecular identification of fungi - recent updates are synergistic effects from many people working on the same and future perspectives. New Phytol. 186, 281e285. system. Cultures and protocols can be developed more quickly and Adams, R.I., Miletto, M., Taylor, J.W., Bruns, T.D., 2013. Dispersal in microbes: fungi shared, and complementary studies can help to fill in different in indoor air are dominated by outdoor air and show dispersal limitation at short distances. ISME J. 7, 1262e1273. aspects of the problem that a single group is unlikely to see. To that Agrin, N., Kline, J., Ueda, K.-I., 2008. iNaturalist. website. https://www.inaturalist. end I hope that more ecologists interested in an experimental org/. approach and mycologists who know these organisms will embrace Amend, A., 2014. From Dandruff to Deep-Sea Vents: malassezia-like Fungi Are Ecologically Hyper-diverse. PLoS Pathog. 10 (8) e1004277. these powerful fungal systems. Amend, A., Samson, R., Seifert, K.A., Bruns, T.D., 2010. Deep sequencing reveals On the sampling side we have made great progress due to the diverse and geographically structured assemblages of fungi in indoor dust. Proc. widespread application of current and emerging technologies, but Natl. Acad. Sci. U. S. A 107, 13748e13753. Amend, A.S., Barshis, D.J., Oliver, T.A., 2012. Coral-associated marine fungi form this work has only scratched the surface of the goal of producing a novel lineages and heterogeneous assemblages. ISME J. 6, 1291e1301. comprehensive view of the diverse fungal communities across the Andrew, C., Heegaard, E., Kirk, P.M., Bassler, C., Heilmann-Clausen, J., Krisai- planet. 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