Review Research review Mycorrhizal fungi affect orchid distribution and population dynamics Author for correspondence: Melissa K. McCormick Melissa K. McCormick 1,2 Canchani-Viruet 1 2 Tel: +1443 4822433 Email: [email protected] Received: 10 April 2018 Smithsonian Environmental Research Center, 647 Contees Wharf Rd, Edgewater, MD 21037, USA; Universidad Accepted: 17 April 2018 Metropolitana, Escuela de Ciencias y Tecnologıa, 1399 Avenida Ana G. Mendez, San Juan 00926, Puerto Rico 1 1 , Dennis F. Whigham and Armando Summary New Phytologist (2018) doi: Symbioses are ubiquitous in nature and influence individual plants and populations. Orchids have 10.1111/nph.15223 life history stages that depend fully or partially on fungi for carbon and other essential resources. As a result, orchid populations depend on the distribution of orchid mycorrhizal fungi (OMFs). We Key words: fungal distribution, fungus focused on evidence that local-scale distribution and population dynamics of orchids can be abundance, mycorrhizae, orchid distribution, limited by the patchy distribution and abundance of OMFs, after an update of an earlier review orchid mycorrhizal fungi, orchid performance, confirmed that orchids are rarely limited by OMF distribution at geographic scales. Recent Orchidaceae. evidence points to a relationship between OMF abundance and orchid density and dormancy, which results in apparent density differences. Orchids were more abundant, less likely to enter dormancy, and more likely to re-emerge when OMF were abundant. We highlight the need for additional studies on OMF quantity, more emphasis on tropical species, and development and application of next-generation sequencing techniques to quantify OMF abundanceinsubstratesanddeterminetheirfunctioninassociationwithorchids.Researchisalso needed to distinguish between OMFs and endophytic fungi and to determine the function of nonmycorrhizalendophytesin orchidroots.These studieswillbeespecially importantifwe areto link orchids and OMFs in efforts to inform conservation. Introduction Roger et al., 2013; Minton et al., 2016), the distribution of nonnative (Menzel et al., 2017) and native species, and Plant population ecological and evolutionary dynamics are allowing growth on nutrient-poor substrates (e.g. Denison & determined by many factors, including distances between Kiers, 2011). Most studies of symbiotic interactions have been individuals and local variation in population density, that primarily concerned with whether plants had a mycorrhizal together determine propagule production and dispersal and the association or not, rather than whether the distribution, identity, behavior of pollinators, and thus gene flow (Kunin & Iwasa, or abundance of mycorrhizal partners affected characteristics of 1996; Colas et al., 1997; Matsumura & Wahitani, 2000; plants and plant populations, such as frequency of emergence Goverde et al., 2002; Grindeland et al., 2005; Pierce et al., or density of plants. There is evidence, however, that the patchy 2006). Plant population dynamics are also influenced by distribution of mycorrhizal fungi affects local plant distribution, symbioses. Symbioses are ubiquitous in nature and are key by altering pollen flow and subsequent seed production and interactions in structuring ecological communities (Bronstein, dispersal (Carvalho et al., 2003). 1994; Stachowicz, 2001). This is especially true for Ecologically, fungi can limit the size of plant populations mycorrhizal associations (Brundrett, 2009), which are known to because patchy distribution of mycorrhizal fungi can affect key affect plant and population characteristics as diverse as processes such as seed germination and plant growth and flowering time (Wagner et al., 2014; Panke-Buisse et al., 2015), survival. For example, Jacquemyn et al. (2012) found that local resistance to pathogens and herbivores (e.g. Vicari et al., 2002; spatial segregation of orchids was determined by the No claim to original US Government works New Phytologist (2018) New Phytologist 2018 New Phytologist Trust 1 www.newphytologist.com 2 Review New Research review Phytologist distribution of the distinct mycorrhizal fungi needed by the carbon from orchids under some conditions, the fungi grow well species. The patchy distribution of plants and fungi can also without orchids and are likely distributed independently. contribute to diversification, because limited gene flow among As already indicated, the distribution of OMFs is potentially populations and small population sizes create ideal conditions a critical factor in determining the distribution and fate of for speciation, which is particularly relevant for the species-rich orchids. From a conservation perspective, orchids that are orchid family (Tremblay et al., 2005). grown in laboratory cultures and transplanted to nature need to Orchid mycorrhizae be already inoculated with an appropriate OMF or the OMFs need to be present at the transplantation site to increase the Association with mycorrhizal fungi is a crucial symbiosis that probability that mediatesgrowth, competitive interactions,and pathogen theorchidwillsurvive.McCormick&Jacquemyn(2014)reviewed protection for the vast majority of terrestrial plants, but the the literature on whether the distribution of OMFs limited ability of fungi to drive plant dynamics is perhaps most likely orchid distribution. They concluded that orchid distribution was to be seen in orchid mycorrhizal associations (Swarts & Dixon, not limited by OMFs at geographic scales, but it could be 2017). Orchid mycorrhizaehavebeenstudiedfor morethan a locally limited. Some of the apparent lack of limitation and wide century(Rasmussen,2002) geographic distribution of OMFs, as well as many arbuscular and,unlikemanyothertypesofmycorrhizae,theorchidmycorrhiza and ectomycorrhizal fungi, may be a result of lumping fungi l association is only obligate for the orchids, with the fungi into ‘species’ based on inappropriate DNA sequence similarity maintaining independent distributions. Orchids form (Bruns & Taylor, 2016). The goal of this review is to expand mycorrhizal associations with phylogenetically and beyond the conclusions of McCormick and Jacquemyn by ecologically diverse fungi. The mostcommonlyorchid- examining more associatedfungalgeneraare Tulasnella, Ceratobasidium, and recentresearchresultsandtheevidenceforthewaysinwhichOMFs Serendipita, which include saprotrophs, ectomycorrhizal fungi, can be limiting at local scales, including evidence for the effects root endophytes, and some parasites and plant pathogens of OMFs abundance and identity. We also present results of (Dearnaley et al., 2012). Some orchids associate with other recent research that demonstrate a relationship between the basidiomycete ectomycorrhizal fungi, ascomycetes quantity of OMF and orchid density, further demonstrating the (Bidartondo et al., 2004; Selosse et al., 2004; Dearnaley, 2007), potential importance of OMFs on population dynamics. wood decomposers (Kinoshita et al., 2016), and other saprotrophic basidiomycetes (Ogura-Tsujita & Yukawa, 2008; Martos et al., 2009; Kottke et al., 2010; Leeet al., Effects of mycorrhizae on orchid distribution 2015).Mycorrhizalinteractions are especially critical in plants McCormick & Jacquemyn (2014) found that orchids were that are partially (Roy et al., 2013) or fully mycoheterotrophic rarely limited by the availability of appropriate OMFs at a (Leake, 1994; Smith & Read, 2008; geographic scale, but there were some orchids that were limited Hynson&Bruns,2009;Hynsonet al.,2016).Allorchidsareatleast by availability of OMFs at a local scale. We examined the initially mycoheterotrophic (Leake, 1994; Rasmussen, 2002) studies used in McCormick & Jacquemyn (2014) and those and are fully dependent on orchid mycorrhizal fungi (OMFs) at published since that time (details in Supporting Information the Tables S1, S2) to determine whether any further distinctions protocormstage,butalsointeractwithfungitovaryingdegreesatthe have emerged about OMF limitations of orchid distribution and seedling stage (Whigham et al., 2008) and beyond (Girlanda et also whether there was evidence for an effect of OMF al., 2011; Selosse & Martos, 2014; St€ockel et al., 2014). Fully abundance on orchid ecology. mycoheterotrophic orchids are dependent on OMFs throughout As concluded by McCormick & Jacquemyn (2014), the their lives (Rasmussen, 2002; McCormick et al., 2012). Some majority of studies found that OMFs did not limit orchid partially and most fully mycoheterotrophicorchids have distribution (Table 1). With additional studies, however, a beenfound to associate with Agaricomycetes (e.g. Taylor et al., pattern is now emerging about when OMFs do limit orchid 2002; Bidartondo et al., 2004; McCormick et al., 2009; Roy et distribution. al., 2009) and some ascomycetes (Selosse et al., 2004) that also AllbutoneofthestudiesthatfoundaroleforOMFsindetermining form ectomycorrhizae with other plants. orchid distribution involved specialist orchids (13/151 orchids Fungi associated with orchids have diverse nutritional needs in 9/22 studies), and all limitations involved local distributions. (Nurfadilah et al., 2013), but it is not currently thought that they OMFs were patchy in distribution and/or abundance in the soil, needtoassociatewithorarenecessarilyco-distributedwithorchids. andorchiddistributionreflectedthatpatchiness.Anadditionalline A few studies have demonstrated or intimated that orchids may of evidence has been provided by OMF inoculation studies. contribute carbon