Priority effects during fungal community establishment in beech wood

The ISME Journal (2015) 9, 2246–2260 © 2015 International Society for Microbial Ecology All rights reserved 1751-7362/15 OPEN www.nature.com/ismej ORIGINAL ARTICLE Priority effects during fungal community establishment in beech wood Jennifer Hiscox1, Melanie Savoury1, Carsten T Müller1, Björn D Lindahl2, Hilary J Rogers1 and Lynne Boddy1 1 School of Biosciences, Cardiff University, Sir Martin Evans Building, Cardiff CF10 3AX, UK and 2Department of Soil and Environment, Swedish University of Agricultural Sciences, Uppsala, Sweden Assembly history of fungal communities has a crucial role in the decomposition of woody resources, and hence nutrient cycling and ecosystem function. However, it has not been clearly determined whether the fungal species that arrive first may, potentially, dictate the subsequent pathway of community development, that is, whether there is a priority effect at the species level. We used traditional culture-based techniques coupled with sequencing of amplified genetic markers to profile the fungal communities in beech (Fagus sylvatica) disks that had been pre-colonised separately with nine species from various stages of fungal succession. Clear differences in community composition were evident following pre-colonisation by different species with three distinct successor communities identified, indicating that individual species may have pivotal effects in driving assembly history. Priority effects may be linked to biochemical alteration of the resource and combative ability of the predecessor. The ISME Journal (2015) 9, 2246–2260; doi:10.1038/ismej.2015.38; published online 20 March 2015 Introduction Community structure is a key driver of ecosystem dynamics (Deacon et al., 2006; Hansen et al., 2008). However, variation in ecophysiological properties of decomposer communities often confound models predicting carbon cycling and other ecosystem functions (Bardgett et al., 2008; Chapin et al., 2009), because changes in decomposer identities are often idiosyncratic and difficult to predict, as well as being highly sensitive to environmental variation (Wardle, 2002; Heichmann and Reichstein, 2008). In ecosystem models, the microbial community is often considered a 'black box' (Andren and Balandreau, 1999), and community structure is omitted despite the fact that understanding decomposer community dynamics is critical for elucidating the processes underlying carbon dynamics (McGuire and Treseder, 2010). Wooddecay fungi are key determinants of decomposition of recalcitrant lignocellulose and, therefore, of nutrient cycling and carbon sequestration rates in forest ecosystems (Baldrian and Lindahl, 2011). Neglect of fungal community composition and dynamics may lead to major discrepancies between observed and predicted decay rates in models of Correspondence: J Hiscox, School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff CF10 3AX, UK. E-mail: Received 31 October 2014; revised 28 January 2015; accepted 6 February 2015; published online 20 March 2015 wood decomposition (Radtke et al., 2009; Zell et al., 2009; Palviainen et al., 2010; Woodall, 2010; Van der Wal et al., 2014). Assembly history (the timing and sequence in which species join a community) has a large influence on community structure and function in decomposer communities (Fukami et al., 2010; Dickie et al., 2012; Ottosson et al., 2014). Simply put, the identity and abundance of species that first colonise an environment may affect the colonisation success of species that arrive later, and thus determine the structure of the community. Such 'priority effects' likely have a major role in explaining the variation in the structure of communities found in different habitats with similar environmental conditions (Chase, 2010; Weslien et al., 2011). Wood-decay fungi are ideal for studies of assembly history and priority effects; it is well established that some species colonise wood earlier than others, but there is large stochastic variation in the timing of species immigration and the interactions between species within woody resources (Boddy, 2001; Boddy and HeilmannClausen 2008; Fukami et al., 2010). Early colonisers of wood are often ruderal opportunists arriving as spores, or endophytes latently present in functional sapwood, which develop overtly forming communities fairly characteristic for different angiosperm tree species (Boddy et al., 1989; Hendry et al., 2002; Parfitt et al., 2010). Later colonisers arrive as spores or via the soil as mycelium, often aggregated to form cords or rhizomorphs (Fricker et al., 2008; Boddy et al., 2009). Priority effects in fungal communities J Hiscox et al 2247 Fungal community change most commonly results from antagonistic interactions, but also from changes in the microclimatic environment (Boddy and Heilmann-Clausen, 2008). Mycelial antagonism results either in deadlock (where there is no change in territory occupied by either combatant) or replacement (partial or complete) of one combatant by another, leading to community change (Boddy, 2000). The intial community will gradually alter as species are displaced by more aggressive 'secondary' colonisers, which may in turn be replaced by even more combative species and by stress-tolerant species (Holmer and Stenlid, 1997; Boddy, 2001; Boddy and Heilmann-Clausen, 2008). Different species vary in the rate and ways in which they decompose wood, for example, in the relative proportion and location of substrates used, alteration of physical properties or the production of secondary metabolites (Worrall et al., 1997; Boddy, 2000; Boddy and Heilmann-Clausen, 2008; Woodward and Boddy, 2008). Decaying wood can, thus, be thought of as a three-dimensional mosaic of interspecific interactions and abiotic conditions manipulated by the fungi within. Alteration of the resource will affect both current and subsequent inhabitants. Different predecessor species may, therefore, effectively select for successor species that are adapted to certain conditions. For example, circumstantial evidence for priority effects are provided by co-occurring pairs of predecessors/ successors, identified in fruit body surveys (Ottosson et al., 2014). To assess priority effects in wood-decay communities accurately, the abundance and diversity of species following on from different individual preceding species must be determined experimentally. To date, studies of priority effects have either used few initial species (for example, Lindner et al., 2011), or examined the effects of several pre-colonisers on a fixed set of successor species (for example, Fukami et al., 2010; Dickie et al., 2012). Here we test the hypothesis that priority effects determine fungal community composition in wood, by pre-colonising beech disks with one of nine species from different successional stages and placing them on the floor of a deciduous woodland for up to 24 months, followed by characterisation of the resulting (...truncated)