The Mutualistic Niche: Mycorrhizal Symbiosis and Community Dynamics
The niche is generally viewed in terms of species' intrinsic physiological potential and limitations due to competition. Although DNA sequencing has revealed the ubiquity of beneficial microbial symbioses, the role of mutualisms in shaping species niches is not broadly recognized. In this review, I use a widespread terrestrial mutualism, the ectomycorrhizal symbiosis, to help develop the mutualistic niche concept. Using contemporary niche theory, I show how mycorrhizal symbioses expand environmental ranges (requirement niche) and influence resource use (impact niche) for both plants and fungi. Simple niche models for competition between resource specialists and generalists also predict a range of ecological phenomena, from unexpected monodominance by some tropical trees to the functional biogeography of mycorrhizal symbiosis. A niche based view of mutualism may also help explain stability of mutualisms even in the absence of clear benefits. The niche is a central concept in ecology, and better integration of mutualism will more accurately reflect the positive interactions experienced by nearly all species. 143 Click here to view this article's online features: Download figures as PPT slides Navigate linked references Download citations Explore related articles Search keywords ANNUAL REVIEWS Further A nn u. R ev E co l. E vo l. Sy st 2 01 6. 47 :1 43 1 64 D ow nl oa de d fr om w w w .a nn ua lr ev ie w s. or g A cc es s pr ov id ed b y St an fo rd U ni ve rs ity M ai n C am pu s R ob er t C ro w n L aw L ib ra ry o n 11 /0 4/ 16 F or p er so na l u se o nl y. ES47CH07 Peay ARI 14 September 2016 19:36 Mutualism: a cooperative relationship between species based on mutually beneficial interactions, such as the reciprocal exchange of resources or services Symbiosis: the living together of different species in intimate associations that range from mutualism to parasitism Arbuscular mycorrhiza: mycorrhiza formed by fungi in the Glomeromycota and characterized by formation of branched structures (arbuscules) within root cells. It is the ancestral and most common form of mycorrhizal symbiosis Ectomycorrhiza: mycorrhiza distinguished by a sheath of fungal tissue totally encompassing plant terminal roots. It evolved at least 150 Mya and involves a diverse range of Basidiomycota and Ascomycota fungi with saprotrophic ancestors Ericoid mycorrhiza: mycorrhiza formed by plants in the family Ericaceae and fungi predominately from the orders Helotiales and Sebacinales. It evolved at least 80 Mya and is characterized by the formation of fungal coils within root cells 1. MUTUALISM IN ECOLOGY: A CHANGED PARADIGM Although the potential for mutually beneficial cooperation between species (hereafter mutualism) (West et al. 2007) was recognized early in the history of biology (De Bary 1879) ecologists for many years considered the phenomenon to be uncommon (Rich Boucher 1976) As a result, research on ecological interactions historically focused on antagonisms such as natural enemies and competition, leaving the consequences of mutualisms relatively unexplored (Boucher et al. 1982) Since Boucher, physiological studies have repeatedly demonstrated the beneficial nature of widespread interactions, such as mycorrhizal symbiosis (Smith Read 2008) and key conceptual papers have framed the potential impacts of mutualisms and other positive interactions on ecological communities (Bertness Callaway 1994, Bruno et al. 2003) In addition, technical advances in DNA sequencing, in conjunction with other tools, have greatly facilitated investigation of communities of cryptic organisms, such as bacteria and fungi (Horton Bruns 2001) and have rapidly expanded the known incidence and variety of mutualistic interactions (Marquez et al. 2007, Partida Martinez Hertweck 2005) Thus, despite an early focus on negative interactions, mutualisms are now widely recognized as common and important. Accumulating evidence for the importance of mutualism has driven several attempts to understand how mutualism impacts ecological systems. These studies have looked through the lenses of functional traits (Friesen et al. 2011) market theory (Schwartz Hoeksema 1998) and food webs (Holland et al. 2013) Although the niche concept has been a cornerstone of ecological theory for many years (Chase Leibold 2003, Chesson 2000, Grinnell 1917, Hutchinson 1957, MacArthur 1958) thereby helping to identify the factors controlling species distributions and predict the outcome of interactions with other species (Holt 2009, Pulliam 2000) integration of mutualism lags behind other areas of niche theory (Chase Leibold 2003) Some theory has applied niche concepts to mutualistic systems (Bever et al. 2010, Bruno et al. 2003, de Mazancourt Schwartz 2010) and a small but growing number of empirical studies examine the impact of mutualism on species niches (Afkhami et al. 2014, Elias et al. 2008, Kazenel et al. 2015, Warren et al. 2010) however, the prevalence of mutualism and the centrality of niches in ecological theory calls for greater integration of the two topics. From this perspective, mycorrhizal symbiosis which involves reciprocal complementary resource exchange between plant roots and soil dwelling fungi provides an excellent opportunity to synthesize progress in niche theory with the rapidly accumulating empirical data on communities of cryptic organisms, such as fungi and bacteria. Mycorrhizal symbiosis evolved nearly 500 Mya and represents the ancestral condition for most plants, as it occurs in ~80% of all extant species (Brundrett 2009, Field et al. 2015, Redecker et al. 2000) Along with lichens and pollinators, mycorrhizal symbiosis represents one of the great terrestrial mutualisms. Multiple forms of mycorrhizal symbiosis have evolved over the past 500 Mya, such as arbuscular mycorrhizas, ectomycorrhizas, and ericoid mycorrhizas, generally involving distinct anatomies and plant and fungal partners (Smith Read 2008, van der Heijden et al. 2015) Although I discuss all three forms, I center discussion on ectomycorrhizas as they represent the first major departure from the ancestral arbuscular mycorrhizal state, they occur in many dominant temperate and tropical tree families, and the evolution of ectomycorrhizal fungi from multiple wood decomposing lineages has a unique impact on their mycorrhizal niche. In addition to synthesizing current literature on the mycorrhizal niche, I also apply the theoretical framework of contemporary niche theory (CNT) (Chase Leibold 2003) to develop explicit models of how mycorrhizal mutualism affects plant and fungal niches and show how these models can be used to explain a variety of ecological patterns. This approach should be generalizable to many mutualistic systems, such as corals, pollinators, legume rhizobia, and fungal endophytes, and my goal is to stimulate further interest in mutualistic niche models. 144 Peay A nn u. R ev E co l. E vo l. Sy st 2 01 6. 47 :1 43 1 64 D ow nl oa de d fr om w w w .a nn ua lr ev ie w s. or g A cc es s pr ov id ed b y St an fo rd U ni ve rs ity M ai n C am pu s R ob er t C ro w n L aw L ib ra ry o n 11 /0 4/ 16 F or p er so na l u se o nl y. ES47CH07 Peay ARI 14 September 2016 19:36 Individualistic niche: the potential niche space in which a species could maintain a population in the absence of biotic interactions, including mutualist partners Mutualistic niche: the potential niche space in which a species could maintain a population in the presence of mutualist partners 2. THE MUTUALISTIC NICHE The niche concept has been variously defined during its long history in ecology: the specific habitats a species occupies (Grinnell 1917) an abstract N dimensional hypervolume circumscribing the environmental conditions necessary for a species to practice its way of life (Hutchinson 1957) or the ecological role a species plays within a community or ecosystem (Elton 1927) Although a species' niche should predict where it can be found in nature, Hutchinson recognized that species occupy only a subset of their potential (or fundamental) niche space and termed this phenomenon the realized niche (Hutchinson 1957, Pulliam 2000) (Figure 1a) Most commonly, the fundamental niche is defined in terms of abiotic properties of the environment (Pulliam 2000, Warren et al. 2014) and the realized niche is defined as the outcome of negative biotic interactions (e.g. competition, predation) with other species, although dispersal limitation may also lead to unoccupied niche space (Hargreaves et al. 2014, Pulliam 2000) Mutualisms complicate the traditional niche concept because much of what is generally considered part of a species' fundamental niche may have been made by mutualistic interactions (Figure 1a) Empirical examples from mycorrhizal symbiosis include numerous situations in which the absence of fungi prevents their plant hosts from colonizing what would otherwise be considered suitable habitat, and vice versa (Nunez et al. 2009, Weber et al. 2005) Using the conventional terminology, either the fundamental niche implicitly includes mutualism and other positive interactions, or the realized niche is often larger than the fundamental niche (Bruno et al. 2003) To facilitate discussion of these different components of the niche, I use the individualistic niche to distinguish the N dimensional set of environmental conditions in which a species can maintain a population in the absence of all biotic interactions, including mutualist partners and competitors, and the mutualistic niche as the full set of environmental conditions in which a population can be maintained in the presence of mutualist partners but in the absence of antagonistic biotic interactions (Figure 1a) Because occupation of suitable parts of mutualistic niche space may still be limited by antagonistic interaction with other species, the realized niche is the net result of both positive and n