Chapter 8 Biogeography of Orchid Mycorrhizas Hans Jacquemyn, Karl J. Duffy, and Marc-Andre´ Selosse 8.1 Introduction The mycorrhizal interaction between plants and fungi is probably one of the most important symbiotic associations of terrestrial ecosystems (van der Heijden et al. 2015) and is one that has the longest evolutionary history for terrestrial plants (Selosse et al. 2015). In this mutualism, the soil fungus contributes mineral nutrition and water to the plant that, in turn, contributes photosynthetically fixed carbon back to the fungus, by way of a dual organ made of roots colonized by fungal hyphae, the mycorrhiza (Smith and Read 2008). While many studies have shown that plant species are mycorrhizal generalists, in that they can interact with many taxonom- ically disparate mycorrhizal taxa, there are also cases of plants that are mycorrhizal specialists (van der Heijden et al. 2015). Hence, it is widely assumed that coevo- lutionary patterns between plants and fungi are weak or nonexisting. Some plant groups have reversed the mycorrhizal nutrient exchange and obtain carbon from their fungal partner for at least a portion of their life cycle, a nutritional strategy called “mycoheterotrophy.” Orchids are all mycoheterotrophic on germi- nation. Their minute seeds are devoid of nutritional resources (endosperm), and the undifferentiated embryo relies on a fungus for its nutrition, including water, mineral salts, and carbon supply (Rasmussen 1995; Merckx 2013). During further devel- opment, seedlings often become autotrophic and subsequently revert to usual H. Jacquemyn (*) • K.J. Duffy Plant Conservation and Population Biology, KU Leuven, 2435, Kasteelpark Arenberg 31, Leuven 3001, Belgium e-mail: [email protected] M.-A. Selosse Muse´um National d’Histoire Naturelle, Institut de Syste´matique, E´ volution, Biodiversite´, Sorbonne Universite´s, 57 Rue Cuvier—CP39, 75005 Paris, France Department of Plant Taxonomy and Nature Conservation, University of Gdansk, Wita Stwosza 59, 80-308 Gdansk, Poland © Springer International Publishing AG 2017 159 L. Tedersoo (ed.), Biogeography of Mycorrhizal Symbiosis, Ecological Studies 230, DOI 10.1007/978-3-319-56363-3_8 160 H. Jacquemyn et al. mycorrhizal functioning (Cameron et al. 2008). Yet, some species from forest environments remain mycoheterotrophic at adulthood. Some orchids develop par- tial photosynthetic capacity but still rely on fungi for carbon resources, a nutritional strategy called “mixotrophy” or “partial mycoheterotrophy” (Gebauer and Meyer 2003; Julou et al. 2005; Selosse and Roy 2009). Others never develop photosyn- thetic capacity and therefore rely completely on their fungus for nutrition. This nutritional mode, which has evolved >30 times independently in orchids (Merckx 2013), is termed “obligate mycoheterotrophy.” Given the reliance of orchids on OMF, it is increasingly important to understand how OMF affect orchid distribution to accurately predict whether orchids can colonize new habitats or become threatened in others under conditions of rapid environmental change. While it has traditionally been assumed that broad-scale geographical ranges of taxa are determined mainly by abiotic variables (e.g., annual rainfall, mean spring temperature; Grinnell 1917), it is becoming clear that inter- actions between organisms (e.g., competition for nutritional resources or symbiont availability) also play a role in shaping the distribution of taxa. Yet, because biotic interactions are often only measured on local (population) scales, they are often seen as not playing as an important role in determining the larger-scale geograph- ical distributions of taxa. Indeed, the realized niche of a particular species is often referred to in the context of habitat suitability, determined by resources available and the environmental conditions it can tolerate (Sobero´n 2007). It is therefore important to recognize the current extent of orchids’ geographical distributions to understand whether mutualists, such as OMF, can affect their distributions and whether this will be affected by environmental change. Fortunately, there has been a recent rapid increase in the availability of biodiversity databases, niche modeling software, and geographical information system (GIS) techniques, and it is becom- ing increasingly accessible to understand the determinants of the ranges of taxa under various environmental scenarios (e.g., Lurgi et al. 2015). Despite this, basic observational data about the distribution of mutualists are needed and informative experimental manipulations in field settings to test the reliance of organisms on mutualists are still required. Afkhami et al. (2014) dem- onstrated the importance of soil mutualists in determining species distribution. They showed that fungal endophytes ameliorated drought stress and broadened the range of their host grass Bromus laevipes by thousands of kilometers. This highlights that the current observed distribution of a species can be affected by many factors. Further work is needed to test whether biotic interactions, such as mutualists, in tandem with abiotic factors, are important in determining range limits of species. This is particularly important in a plant group such as the Orchidaceae as they not only rely on pollinators to set seed but also on mycorrhizal fungi to germinate and establish seedlings (Smith and Read 2008; Rasmussen and Rasmussen 2009). With an estimated 27,000 species (Dressler 2005), the Orchidaceae represents one of the most species-rich plant families. Orchids occur across the entire globe, except Antarctica, and occupy a wide range of habitats including tropical and temperate rainforest, dry tropical forest, savannas, temperate forest, temperate grasslands, Mediterranean shrubland, and even arctic tundra (Givnish et al. 2016). 8 Biogeography of Orchid Mycorrhizas 161 In the Southern Hemisphere, the most southern populations occur on the subant- arctic Macquarie Island (Brown et al. 1978; Clements and Jones 2007). The widespread occurrence of orchids across the globe suggests that the OMF that are necessary for orchid germination and establishment are widespread and not espe- cially limited by biogeographical regions. However, we know little of the bioge- ography of OMF. Without such information, it is difficult to assess how the distributions of both OMF and orchids will respond to a rapidly changing environment. In this chapter, we investigate biogeographic patterns in orchid mycorrhizal fungi from the global scale to the population level. We first give an overview of the most important mycorrhizal fungi associating with orchids, and then investi- gate whether biogeographic patterns in the distribution of OMF exist. Finally, we discuss the population-scale interactions that can determine orchid co-occurrence. 8.2 Main Orchid Mycorrhizal Fungal Symbionts 8.2.1 Rhizoctonias Stemming from the pioneering work of Noe¨l Bernard (see Selosse et al. 2011), OMF were traditionally classified as “rhizoctonias.” However, rhizoctonias belong to three distinct basidiomycete families, namely, Tulasnellaceae and Ceratobasidiaceae (both from the order Cantharellales) and Serendipitaceae (Sebacinales). Although they have a reputation of being saprotrophic fungi (Rasmussen 1995; Smith and Read 2008), they may also be endophytic in non-orchid roots (e.g., Selosse and Martos 2014), meaning that they grow dif- fusely within living plant tissues, without apparent infection symptoms or forming symbiotic organs termed mycorrhizas. Members of Tulasnellaceae are enigmatic basidiomycetes (Cruz et al. 2016; Chap. 12), whose genome displays wide saprotrophic enzymatic abilities (Kohler et al. 2015), but some also have endophytic abilities (Girlanda et al. 2011). Members of Ceratobasidiaceae encom- pass endophytic, plant-parasitic, and free-living (perhaps saprotrophic) species. Indeed, phylogenetic analysis of Ceratobasidiaceae has shown that species that are OMF tend to be closely related (Veldre et al. 2013). Serendipitaceae (formerly called Sebacinales clade B) tend to have saprotrophic capacities (Kohler et al. 2015) but are well known as endophytes of non-orchid plants (Weiss et al. 2016). The well-studied root endophyte model Serendipita (¼ Piriformospora) indica is indeed orchid mycorrhizal (Oliveira et al. 2014). Members of this group are often described as “Sebacina” spp. incl. “Sebacina vermifera,” but recently the species complex has been transferred into the genus Serendipita (Weiss et al. 2016). Despite the recent increase in our knowledge of the taxonomy of these mycor- rhizas, the exact distribution of rhizoctonias as saprotrophs or endophytes, beyond 162 H. Jacquemyn et al. their association with the relatively few investigated orchid taxa, remains to be determined. 8.2.2 Other Mycorrhizal Fungi While orchids have a long, likely plesiomorphic evolutionary history of association with rhizoctonias (Yukawa et al. 2009; Dearnaley et al. 2013), many more mycor- rhizal fungi have been found recently, each associated with a limited number of orchids. The study of OMF in obligate mycoheterotrophic and partially mycoheterotrophic orchid species has revealed a large diversity of ectomycorrhizal fungi (Merckx 2013), including some ascomycete taxa (Selosse et al. 2004) and saprotrophic fungi from the Psathyrellaceae and Mycenaceae (Selosse et al. 2010; Dearnaley et al. 2013). This suggests that the same fungi could form both ectomycorrhizal and orchid mycorrhizal associations depending on their host. Autotrophic orchids may