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Taxaarea Relationship and Neutral Dynamics Influence the Diversity Of bs_bs_banner Environmental Microbiology (2012) 14(6), 1488–1499 doi:10.1111/j.1462-2920.2012.02737.x Taxa–area relationship and neutral dynamics influence the diversity of fungal communities on senesced tree leavesemi_2737 1488..1499 Larry M. Feinstein* and Christopher B. Blackwood to environmental changes may be enhanced with Department of Biological Sciences, Kent State increased understanding of the processes that regulate University, Kent, Ohio, USA fungal distributions. Variation in composition of ecological communities is commonly divided into two components: alpha diversity (number and evenness of taxa within a Summary sampling unit) and beta diversity (taxa turnover among This study utilized individual senesced sugar maple areas) (Gaston and Blackburn, 2000). and beech leaves as natural sampling units within For macroorganisms, it has been frequently observed which to quantify saprotrophic fungal diversity. Quan- that there is a correlation between the size of habitat tifying communities in individual leaves allowed us to patches or survey areas and the most fundamental determine if fungi display a classic taxa–area relation- measure of alpha diversity, number of taxa detected ship (species richness increasing with area). We (Rosenzweig, 1995; Connor and McCoy, 2001; Lomolino, found a significant taxa–area relationship for sugar 2001; Drakare et al., 2006). The ‘taxa–area relationship’ maple leaves, but not beech leaves, consistent with (TAR) refers to the shape of the increase in number of Wright’s species-energy theory. This suggests that taxa with increasing area, and has been most often mod- energy availability as affected plant biochemistry is a elled as a power law (S = cAz) where S is number of key factor regulating the scaling relationships of species, A is area, c is the intercept in log-log space, and fungal diversity. We also compared taxa rank abun- z is a constant related to the rate of species turnover dance distributions to models associated with niche across space (Arrhenius, 1921; Gleason, 1922). Taxa– or neutral theories of community assembly, and area relationships have been used to extrapolate species tested the influence of leaf type as an environmental richness (Colwell and Coddington, 1994; He and Leg- niche factor controlling fungal community composi- endre, 1996; Plotkin et al., 2000), estimate regional tion. Among rank abundance distribution models, the diversity inventories (Chong and Stohlgren, 2007), and zero-sum model derived from neutral theory showed compare species abundance distributions (May, 1975; the best fit to our data. Leaf type explained only 5% Harte et al., 1999; Pueyo, 2006). TARs are also used as of the variability in community composition. Habitat an important tool in conservation efforts to protect species (vernal pool, upland or riparian forest floor) and site from habitat fragmentation and destruction (Faith et al., of collection explained > 40%, but could be attributed 2008). Quantifying fungal TARs may help us understand to either niche or neutral processes. Hence, although processes regulating fungal community assembly and niche dynamics may regulate fungal communities at determine how sampling design affects our ability to the habitat scale, our evidence points towards neutral detect fungal diversity. assembly of saprotrophic fungi on individual leaves, Communities in discrete habitat patches (e.g. islands) with energy availability constraining the taxa–area have proven useful in studying TAR patterns because relationship. such communities have well-defined boundaries (Mac- Arthur and Wilson, 1967; Schoener, 1976; Bell et al., 2005). Although a few studies have utilized leaves as Introduction discrete habitats for microbial communities (Kinkel et al., Fungal community composition has been shown to be an 1987; Jacques et al., 1995; Newell and Fell, 1997), most important factor regulating decomposition (Balser and Fir- previous molecular studies examining forest floor fungal estone, 2005; Waldrop and Firestone, 2006). Therefore, communities have utilized homogenized mixed ‘grab’ our ability to predict decomposition rates and responses samples of leaves (O’Brien et al., 2005; Neubert et al., 2006; Blackwood et al., 2007a; Keeler et al., 2009; Received 29 July, 2011; revised 5 March, 2012; accepted 7 March, 2012. *For correspondence. E-mail [email protected]; Tel. (+1) Redford et al., 2010). However, early after leaf fall, 330 672 3895; Fax (+1) 330 672 3713. individual leaf boundaries must limit the size of fungal © 2012 Society for Applied Microbiology and Blackwell Publishing Ltd Taxa–area relationship in fungi on leaves 1489 communities because the leaves are each colonized indi- distribution models including the pre-emption (geometric) vidually in the canopy, during leaf fall, and on top of the and broken stick models (Motomura, 1932; MacArthur, existing forest floor. At later successional stages it is 1957). The lognormal and Zipf-Mandlebrot are more flex- unclear to what extent the scale of communities coincides ible models that have also been related to niche theory with individual leaves because some fungi will colonize (McGill et al., 2007). The second method is to explain leaves from existing mycelia in the forest floor. However, variation in composition among communities (i.e. beta even if individual fungi extend beyond the boundaries of a diversity). If variation in community composition is due to single leaf, individual leaves are still a natural sampling environmental filtering, we would expect community com- unit because they represent unit resources with differing position to be related to environmental or resource gradi- characteristics depending on plant species of origin, and ents (Jongman et al., 1995; Chase et al., 2004), whereas in which a highly diverse assemblage of fungal taxa can this would not be the case under neutral dynamics be found (Cooke and Rayner, 1984). In other words, fungi (Hubbell, 2001). interact with leaves as discrete units, unlike, for example, Our goals in this study were to (i) characterize fungal soil cores or vegetation quadrats, which are arbitrary sub- TARs utilizing the discrete nature of leaf habitat, (ii) test samples of a larger area. Hence, taking advantage of the the importance of leaf type and habitat in determining individual nature of forest floor leaves may provide impor- fungal alpha and beta diversity, and (iii) determine tant insight into fungal community organization. whether taxa rank abundances correspond with niche- Fungal alpha and beta diversity may be influenced by a based and/or neutral models of community assembly. To variety of environmental and biological mechanisms that determine the effects of leaf biochemistry and habitat soil act on the organism niche. The biochemical makeup of moisture, we collected two leaf types of differing recalci- leaves (e.g. proportion of soluble compounds, hemicellu- trance from the forest floor of three habitats providing loses, cellulose and lignin) represents the carbon and variable levels of moisture, vegetation type and soil con- energy resources available to saprotrophic fungi. Some ditions: upland forest, riparian forest and vernal pools. compounds (e.g. solubles) are easily metabolized and While upland forest floor remains dry other than during support a wide range of organisms; in contrast, lignin rainfall or snowmelt, vernal pools are saturated with water requires oxidative enzymes predominantly produced by in late winter, spring and periodically over the rest of the white-rot Basidiomycetes. Because biochemical composi- year, and riparian is occasionally flooded. Fungal diversity tion varies among tree species (Hobbie et al., 2006), leaf and community composition were determined by PCR species type may act as an ‘environmental filter’, favour- amplification and sequencing of the fungal internal tran- ing microbial taxa that are able to exploit the resources scribed spacer (ITS) region, a common fungal taxonomic present (Weand et al., 2010; Wu et al., 2011). In addition, marker (Martin and Rygiewicz, 2005). competitive interactions may influence diversity of fungi that share similar niches. Fungal diversity may also be affected by environmental variability in abiotic conditions Results such as soil moisture. In general, saprotrophic fungal Sequence analysis species richness is lower in aquatic habitats than terres- trial habitats (Nikolcheva et al., 2005; Fischer et al., 2009; Leaves were collected from two forest floor sites per Gessner et al., 2010). This could be mediated by lower habitat. At each site, sequences were obtained separately spatial and temporal variation in aquatic habitats, as well from the largest and smallest beech and maple leaves. A as enhanced water-dependent dispersal among micro- total of 2701 sequences met our selection criteria (con- sites, leading to greater dominance by competitively taining both primers or longer than the longest sequence superior taxa. Under these conditions, we might also containing both primers), and these were clustered into expect a shallower TAR (i.e. a lower z-value) because of 416 distinct operational taxonomic units (OTUs) at 97% lower beta diversity among habitat patches. sequence similarity. The majority of OTUs (278) were Alternatively, neutral theory seeks to explain community singletons, and these comprised 11.1% of total OTU rela- composition strictly by immigration dynamics, ignoring tive abundance. We classified 41 OTUs as ‘dominant’ species niches (Hubbell, 2001; Maurer and McGill, 2004). (Ն 5% relative
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