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The Importance of Mycorrhizal Fungal Networks for Facilitation in Natural Ecosystems

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The Importance of Mycorrhizal Fungal Networks for Facilitation in Natural Ecosystems Journal of Ecology 2009, 97, 1139–1150 doi: 10.1111/j.1365-2745.2009.01570.x SPECIAL FEATURE FACILITATION IN PLANT COMMUNITIES Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems Marcel G. A. van der Heijden1* and Thomas R. Horton2 1Ecological Farming Systems, Agroscope Reckenholz-Ta¨nikon, Research Station ART, Zurich, Switzerland; and 2Department of Environmental and Forest Biology, SUNY-Environmental Science and Forestry, Syracuse, NY, USA Summary 1. Almost all plants are engaged in symbiotic relationships with mycorrhizal fungi. These soil fungi can promote plant growth by supplying limiting nutrients to plant roots in return for plant assimi- lates. 2. Many mycorrhizal fungi are not host specific and one fungal individual can colonize and inter- connect a considerable number of plants. The existence of these so-called mycorrhizal networks implies that fungi have the potential to facilitate growth of other plants and distribute resources among plants irrespective of their size, status or identity. In this paper, we explore the significance of mycorrhizal fungal networks for individual plants and for plant communities. 3. We address the following questions: (i) are all plant species benefitting from mycorrhizal net- works, (ii) is benefit dependent on the size or age of a plant, (iii) is fungal support related to the rela- tive dominance of plants in a community, (iv) are there host dependent barriers and physiological constraints for support and (v) what is the impact of mycorrhizal networks on plant–plant interac- tions and plant community dynamics? Moreover, using a review of published studies, we test whether mycorrhizal networks facilitate growth of small seedlings that establish between or near larger plants. 4. We found 60 cases where seedling species were grown together with larger plants with or without mycorrhizal fungal networks. Mycorrhizal networks promoted seedling growth in 48% of the cases (for 21 seedling species), while negative effects (25%) and no effects (27%) were also common. Seed- lings associating with ectomycorrhizal fungi benefitted in the majority of the cases while effects on seedlings associating with arbuscular mycorrhizal fungi were more variable. Thus, the facilitative effects of mycorrhizal fungal networks depend on seedling species identity, mycorrhizal identity, plant species combinations and study system. We present a number of hypothetical scenarios that can explain the results based on cost–benefit relationship of individual members in a network. 5. Synthesis. Overall, this review shows that mycorrhizal networks play a key role in plant commu- nities by facilitating and influencing seedling establishment, by altering plant–plant interactions and by supplying and recycling nutrients. Key-words: arbuscular mycorrhizal fungi, common mycorrhizal networks, ectomycorrhizal fungi, facilitation, hyphal links, mutualism, plant competition, positive interactions tation also play a key role in plant communities (Callaway Introduction et al. 2002; Brooker et al. 2008). Facilitation is defined here as Plants interact in many ways, both negative and positive. Neg- positive non-trophic interactions that occur between physio- ative interactions such as plant competition received much logically independent plants and that are mediated through attention in the 1980s and 90s (Sapp 2004). However, there is changes in the abiotic environment or through other organ- increasing recognition that positive interactions such as facili- isms (Brooker et al. 2008). Examples of facilitation are the positive effects of nitrogen fixing plants on neighbours and *Correspondence author. E-mail: [email protected] pollination of multiple plant species by the same insects. Ó 2009 The Authors. Journal compilation Ó 2009 British Ecological Society 1140 M. G. A. van der Heijden & T. R. Horton In this paper, we focus on the 400 million-year-old symbiosis established fungal mycelium that simultaneously colonizes and between the majority of land plants and mycorrhizal fungi interconnects roots of the same or different plant species. The (Smith & Read 2008). Such interactions have facilitative effects fungi able to form mycorrhizal fungal networks are those that when mycorrhizal associations formed or maintained by one form the typical mycorrhizal structures inside plant roots or on plant are beneficial for other plants. The mycorrhizal symbio- the surface of plant roots after a complex molecular dialogue sis is based on reciprocal exchange of resources: the fungi pro- between plant and fungus. vide limiting nutrients to plants in return for plant assimilates In this paper, we explore the significance of mycorrhizal fun- (Smith & Read 2008). In natural ecosystems, plants obtain up gal networks as facilitators in plant communities. In particular to80%oftheirrequirementfornitrogenandupto90%of we investigate: (i) whether all plants benefit from mycorrhizal phosphorus from mycorrhizal fungi (van der Heijden, Bardgett fungi, (ii) whether support is dependent on the size of a plant, & van Straalen 2008). These nutrients are acquired by complex (iii) whether there are host-dependent barriers and physiologi- hyphal networks (Leake et al. 2004; Selosse et al. 2006) which cal constraints for support, (iv) whether there is interplant are specialised to forage for soil nutrients (Olsson, Jakobsen carbon and nutrient transfer via mycorrhizal networks and & Wallander 2002). Moreover, mycorrhizal fungi can also (v) whether mycorrhizal networks influence plant–plant inter- provide resistance to stress, drought and in some cases to actions and plant community dynamics. Moreover, using an soil pathogens (Auge 2001; Sikes, Cottenie & Klironomos analysis of published studies, we test whether mycorrhizal net- 2009). works facilitate growth of small seedlings that establish Most mycorrhizal fungi are not host specific and one fungal between or near larger plants. We end with conclusions and individual can simultaneously colonize a large number of identify future research priorities. plants from the same but also from different plant species (Fig. 1). Moreover, both small seedlings and large plants can Do all plant species benefit? be colonized by one mycorrhizal fungal individual (Newman 1988; Horton & van der Heijden 2008). Thus, plants can be Many plant communities are dominated by mycorrhizal interconnected by mycorrhizal fungal networks in the so-called plants, including most grasslands, savanna, boreal-, temperate- ‘wood-wide-webs’ (Simard et al. 1997). The existence of these & tropical forests (Read 1991). In these communities, abun- networks implies that fungi have the ability to distribute dant mycorrhizal fungal networks are formed (Leake et al. resources among plants irrespective of their size, status (i.e. 2004) and the majority of plants are usually extensively colo- their relative dominance in the plant community) or identity. nized by these mycorrhizal networks. Pot experiments per- Forclarity,amycorrhizalfungalnetworkisdefinedhereasan formed with plants grown under the nutrient-poor conditions typical for most natural plant communities show that many plants benefit from the presence of mycorrhizal fungi (Smith & Read 2008). However, most experiments have been performed with single plants grown in the absence of competition and only a few studies have tested the importance of mycorrhizal networks. Studies that mimicked the field situation using microcosms simulating nutrient-poor European calcareous grassland with established mycorrhizal networks showed that 3 4 4 75% of the investigated plant species benefited from mycorrhi- 1 3 zal fungal networks with enhanced growth (Grime et al. 1987; van der Heijden 2004). Experiments with a number of tree spe- 2 cies indicate that many of them benefit from mycorrhizal colo- nization, especially at low soil fertility (Simard, Durall & Jones N1 2002; Karst et al. 2008). However, the impact of mycorrhizal fungal networks on tree growth in natural systems is difficult N2 to study because mycorrhizal fungi are often already present (but see Nara 2006a; Dickie, Koide & Steiner 2002; see also Fig. 1. Resource sharing in mycorrhizal networks. One mycorrhizal below). fungal individual colonizes different plant individuals from the same, Not all interactions with mycorrhizal fungal are positive: but also from different plant species. Carbon and nutrients (N) can some plant species perceive mycorrhizal fungi as antagonists. move through this common hyphal network. Different numbers rep- resent different plant species. For instance, plant species 1, 2 and 3 are These include some non-mycotrophic plant species (plants that colonized by the same mycorrhizal fungi (dashed line). Nutrients can are unable to form symbiotic associations with mycorrhizal be acquired by this fungus from a nutrient patch near plant 1 (N1) fungi) and some plant species characteristic of ruderal environ- and move to plant 1 or 2. Nutrients of patch N2 could flow to plant 2 ments (Francis & Read 1995; Klironomos 2003). It must be or 3. In addition, plant species 1, 2 and 3 are also colonized by another remembered that approximately 10–15% of all vascular plant mycorrhizal fungus (solid line). Some plant species are not colonized by mycorrhizal fungi (plant 4). Plant size also varies (see plant species species, including the model plant Arabidopsis thaliana),are 3) showing that plants in different growth stages can be colonized by non-mycorrhizal and do not benefit from mycorrhizal fungi
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