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.

2009 The Authors. Journal compilation 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 the same mycorrhizal fungus. (Wang & Qiu 2006; Brundrett 2009). Hence, the question of

2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1139–1150 Socialism in soil? The importance of mycorrhizal fungal networks 1141 whether all plant species benefit from mycorrhizal fungi can be Twenty-one seedling species (48% of cases investigated) answered simply with a ‘no’. Finally, the effect of mycorrhizal benefited from mycorrhizal networks while 12 species (25% of fungi on plant growth is context dependent (Johnson, Graham cases) responded negatively. The biomass of 15 seedling species & Smith 1997; Jonsson et al. 2001). At high soil fertility, there (27% of the cases) was not significantly influenced by the pres- is often no benefit and plant growth can be slightly reduced in ence or absence of mycorrhizal fungal networks (Fig. 2; the presence of mycorrhizal fungi due to their carbon demand Appendix S1). The distribution of cases differed significantly (Smith, Grace & Smith 2009). Further, a mycorrhizal fungus among the three categories (P = 0.05). The average growth may be mutualistic with one host plant species, and parasitic response of all seedlings ⁄ cases was +14% or +20% when on another host species as Plattner & Hall (1995) report for non-mycorrhizal (NM) plants not hosting mycorrhizal fungi Tuber melanosporum. were removed from analysis. We also performed the analysis separately for plants associ- ating with AM fungi or with EM fungi. Mycorrhizal networks Is benefit dependent on the size of a plant? formed by EM fungi promoted seedling growth in seven cases Mycorrhizal fungi usually colonize all plant individuals from (75% of the cases), while in three cases (25%) seedling growth mycotrophic hosts, irrespective of their size or development. did not vary between treatments with or without mycorrhizal An intriguing question is whether all plant individuals (e.g. fungi. For AM fungi, 16 out of 37 species (and 42% of the small seedlings and larger plants) receive the same amount of cases) responded significantly positively, 15 species (33% of benefit from mycorrhizal fungi. To test for general patterns, the cases) responded negatively, while growth responses of 12 we performed a literature analysis with studies where seedlings seedling species (29% of the cases) did not vary significantly in were grown together with larger ⁄ adult plants in the presence treatments with or without mycorrhizal fungal networks. and absence of mycorrhizal fungi. We made a distinction Growth responses of several species (e.g. Plantago lanceolata – between studies where seedlings were grown with adult ⁄ larger see Appendix S1) were tested repeatedly in different studies. plants from the same species and studies in which seedlings Hence, the distribution of cases as discussed above and pre- grew together with different plant species. In addition to this, a sented in Fig. 2 does not match precisely to the number of distinction was made between plants hosting arbuscular investigated seedling species. Based on this analysis, it can be mycorrhizal (AM) fungi and ectomycorrhizal (EM) fungi. EM concluded that seedling establishment of plants forming asso- fungi belong to the Basidiomycetes and Ascomycetes and asso- ciations with EM fungi is more heavily dependent on mycor- ciate with a range of trees, especially those from temperate and rhizal fungi compared with plants associating with AM fungi. tropical forests. AM fungi belong to the Glomeromycota Note, however, that a much broader range of plant species (Schu¨ ßler, Schwarzott & Walker 2001) and associate with an (including several non-mycorrhizal hosts) were included in the estimated 65% of all land plants, including many grasses, analysis with AM fungi, also reflecting the fact that habitats herbs and tropical trees (Wang & Qiu 2006; Brundrett 2009). where AM fungi are abundant probably contain a higher pro- The results of the analysis are shown in the next section. This portion of non-mycorrhizal plants. Moreover, the analysis for analysis focuses on experiments where several plants co-occur EM fungi is based on only a few cases and the observed effect in pots, microcosms or in the field. These experiments are eco- logically more realistic than those where plants are grown alone in pots with or without mycorrhizal fungi. In pots with 35 multiple plants (e.g. seedlings and adult plants), interactions between plants occur (e.g. competition or facilitation) and the 30 effects of common mycorrhizal networks on plant growth can 25 be tested, thus better simulating conditions usually observed in natural communities. 20

15 Mycorrhizal networks and seedling establishment near larger plants Number of cases 10

We performed a literature survey and found 20 studies where 5 seedlings were grown near larger plants in the presence and 0 absence of mycorrhizal fungal networks (see Appendix S1 in PositiveNegative No effect Supporting Information). In most studies, several seedling spe- Seedling mycorrhizal dependency cies were tested and results of 60 cases were included in the analysis. Thirteen studies were performed with AM fungi, and Fig. 2. Output from literature analysis showing effects of mycorrhizal seven with EM fungi (Appendix S1). Three categories were fungal networks on seedling growth and establishment. Positive and distinguished: cases where seedlings had significantly higher negative response indicates the number of cases where seedlings bio- mass was significantly enhanced or reduced in the presence of mycor- biomass in the presence of mycorrhizal fungal networks, cases rhizal fungal networks. ‘No response’ indicates cases where seedling where seedling biomass was significantly reduced and cases biomass was not significantly affected by the presence or absence of without significant differences. mycorrhizal networks. For further information see Appendix S1.

2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1139–1150 1142 M. G. A. van der Heijden & T. R. Horton might change considerably if more studies are included. The Appendix S1): in two cases Plantago seedlings benefited outcome of this analysis is roughly the same if the number of greatly from the presence of mycorrhizal networks (Grime studies and not the number of seedling species or cases is used et al. 1987 & Francis & Read 1995) while in two cases seedling for the analysis (Appendix S1). growth was clearly suppressed (Nakano-Hylander & Olsson An interesting question is whether the benefit seedlings 2007). The study by Grime et al. (1987) was performed under derive from mycorrhizal fungal networks is higher, lower or nutrient-poor conditions (as shown by poor overall plant pro- equal compared with coexisting older and larger plants of the ductivity), whereas plant nutrient availability in the study by same species. This could be tested for nine studies (Table 1). Nakano-Hylander & Olsson (2007) was much higher as evi- Three of these studies indicated that the relative benefit to seed- denced by a higher plant biomass obtained in a shorter growth lings was similar to that of largerplants(comparethemycor- period. The effect of mycorrhizal fungi on plant growth is rhizal dependencies in Table 1: see Ocampo 1986; Kytoviita, strongest at low soil fertility (e.g. Smith & Read 2008), perhaps Vestberg & Tuom 2003; Pietikainen & Kytoviita 2007), two explaining why the results of the studies by Grime et al. (1987) studies found that seedlings benefited more (van der Heijden and Nakano-Hylander & Olsson (2007) contrasted so much. 2004; Eissenstat & Newman 1990; although not significantly We determined the average seedling response to mycorrhizal so in the latter case) and in two studies adult plants benefited fungi in studies where several treatments with mycorrhi- from mycorrhizal fungi while seedling growth was significantly zal fungi were compared (e.g. treatments with different reduced (Moora & Zobel 1998; Nakano-Hylander & Olsson mycorrhizal fungal species or communities). In some of these 2007). These findings are in line with Moora & Zobel (2009) cases, the seedling response varied greatly depending on who observed that mycorrhizal networks are less beneficial for mycorrhizal treatment. For instance, Nara (2006a) inoculated seedlings of the same species (intraspecific combinations) com- Salix reinii plants with 11 different EM fungi plus a nonmycor- pared with seedlings of different plant species (interspecific rhizal control under glasshouse conditions. After 11 months of combinations). Interestingly, in green orchids cost–benefit growth, these plants were then planted in the field to establish relationships appear to change over a plant’s life cycle. Net individual mycorrhizal networks, and the effect of these fungus to plant carbon transfer supports seedling establish- mycorrhizal networks on the growth of nearby seedlings was ment of the tiny non-photosynthetic orchid protocorms in the tested. A previous study had shown that this field lacked early growth phases while adult orchids ‘repay’ the carbon to mycorrhizal inoculum for Salix (Nara & Hogetsu 2004). There their mycorrhizal associates when they are older and larger was considerable variation in the effects of adult plants on (Cameron et al. 2008). nearby seedlings establishment. Mycorrhizal networks of most We have used a wide range of species and a wide range of of the fungal species improved the growth and nutrient status study systems for this analysis. Hence, the experimental condi- of the seedlings over the control except Laccaria amythestina, tions (e.g. nutrient availability, soil type, light conditions, wherenoneofthevariablesweresignificantlydifferentfrom mycorrhizal fungal identity) were highly variable among the the control. This study clearly shows that established plants different studies and probably explain the variable results of can facilitate seedling establishment. However, it is unclear the analysis. For instance, the seedling response of Plantago whether this is due to direct facilitative effects through mycor- lanceolata was tested four times in three different studies (see rhizal networks, or simply because established plants provide

Table 1. Biomass (mg) of seedlings grown together with larger plants from the same plant species in the absence (NM) or presence (M) of hyphal networks formed by arbuscular mycorrhizal fungi. The Mycorrhizal dependency shows the percentage growth increase or decrease of mycorrhizal plants relative to non-mycorrhizal plants (calculated after van der Heijden (2002). The summary shows whether seedlings (first position) and adults (second position) had significantly higher (+), lower ()) or statistically equal biomass (0) in the presence of mycorrhizal networks

Seedlings Larger plants

Mycorrhizal Mycorrhizal Plant species NM M dependency NM M dependency Reference Summary

Sorghum vulgare 632a 736b 14.9 1600 2364 32.3 Ocampo 1986 (+;+) Festuca ovina 24.1 22.0 )8.8 922 609 )51.4 Grime et al. 1987 (); )) Plantago lanceolata 18.1 28.3 36.0 1980 1430 )38.5 Eissenstat & Newman 1990 (0; 0) Hypericum perforatum* 1070 800 )25.2 1470 2720 85.0 Moora & Zobel 1998 ();+) Sibbaldia procumbens* 7 8 12.5 1700 1800 5.5 Kytoviita, Vestberg & Tuom 2003 (0; 0) Gnaphalium norvegicum 1.5 2.0 26.1 978 1369 28.6 Pietikainen & Kytoviita 2007 (0;+) Bromus erectus† 8.3 14 40.7 105.6 92.1 )14.7 van der Heijden 2004 (+; 0) Plantago lanceolata 22 7 )68.2 810 2230 63.7 Nakano-Hylander & Olsson 2007 ();+) Trifolium subterraneum 60 40 )33.3 260 1810 85.6 Nakano-Hylander & Olsson 2007 ();+)

*The biomass of seedlings grown with or without mycorrhizal fungal networks was estimated from graphs. †Seedlings were grown in treatments inoculated with different mycorrhizal fungi. The average seedling response of all mycorrhizal fungal treatments was taken.

2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1139–1150 Socialism in soil? The importance of mycorrhizal fungal networks 1143 an inoculum source (mycorrhizal networks) for nearby seed- beside mycorrhizal fungi, pathogenic fungi were also part lings. In this respect, it is important to mention that in some of this fungal network. Hence, the negative effects of the cases seedlings and adult plants are colonized by different fungal network on the growth of the dominant plant could mycorrhizal fungal communities (Aldrich Wolfe 2007), mak- also be due to pathogens. Overall, the studies mentioned ing it unclear to what extent resource sharing among seedlings above indicate that the ‘status’ and relative dominance of and larger plants occurs. Overall, the studies discussed above a plant in the community does not determine how much show that the growth response of seedlings to mycorrhizal fun- benefit it receives. The results appear to depend on the gal networks is variable, depending on factors such as mycor- identity of the dominant plant and its relationship with rhizal identity, plant species identity, plant species mycorrhizal fungi. The observations by Grime et al. (1987) combinations and nutrient availability (see above). and van der Heijden et al. (1998) also imply that there are Seedling establishment is also strongly determined by the many factors that determine the dominance of plants in dominant mycorrhizal network in a community. For instance, plant communities: in some cases mycorrhizal fungi are Horton, Bruns & Parker (1999) showed that the diverse com- important, while in other cases other factors such as munity of mycorrhizal fungi associated with Arctostaphylos growth form, relative growth rate, competitive ability, supported Pseudotsuga menziesii seedling establishment, while resistance to stress or disturbance determine plant abun- mycorrhizal communities found near Adenostoma did not. dance. Pseudotsuga menziesii, associates with EM fungi and the differ- ence is probably explained by Arctostaphylos shrubs support- Free access for everyone? Host specificity & ing well-developed EM networks whereas Adenostoma shrubs physiology of mycorrhizal networks primarily associate with AM fungi. Similarly, Dickie, Koide & Steiner (2002) reported a positive seedling response when Pot experiments with AM fungi isolated from field soil have Quercus seedlings were planted near Quercus trees, but a nega- shown that most AM fungal species can colonize most plant tive response when planted near the arbuscular mycorrhizal species used as bait plants. This lack of specificity is also Acer even though some EM colonization was observed on reflected by the fact that some AM fungal species have a world- seedlings near Acer. Moreover, a recent study by Collier & Bi- wide distribution, associating with a wide range of plant spe- dartondo (2009) showed that the invasion of EM pines into cies in very different ecosystems (Opik et al. 2006). Despite this heathland (with ericoid mycorrhizal fungi) is limited due to the lack of specificity, a considerable number of studies showed absence of EM fungi. The absence of suitable EM inoculum that AM fungi have host preferences and that different plant has also been shown to inhibit Pinaceae invasion into native species are colonized by different AM fungal communities (e.g. Nothofagus communities in Isla Victoria (Nun˜ez, Horton & Vandenkoornhuyse et al. 2003; Opik et al. 2006). Still, in any Simberloff 2009). given plant community that has been studied to date, it appears that some of the fungi form extensive networks con- necting multiple plant species. Is fungal support related to the relative The specificity of EM fungi has received more attention than dominance of a plant in the community AM fungi because of the relative ease in finding sporocarps in Many ecosystems are dominated by plants forming mycor- the field and of culturing mycorrhizal seedlings in the labora- rhizal associations (Read 1991). It is still unclear whether tory. It was believed that EM fungi were more host specific plants that dominate a specific plant community also than AM fungi. Many of the examples of EM fungi with nar- obtain most benefit from mycorrhizal fungi. Studies per- row host ranges fall into the genera Suillus, Leccinum, Gomphi- formed so far gave conflicting results. Hartnett & Wilson dius, Chroogomphus, Brauniellula, and Gomphogaster (Molina, (1999), studying tall grass prairie in North America, Massicotte & Trappe 1992), all in the Boletales. This suggests observed that the dominant C4 grasses obtained most ben- that the narrow host range of these genera is phylogenetically efit from mycorrhizal fungi. They suggested that mycorrhi- determined. There is always a risk of assigning specificity based zal fungi reduced plant diversity in these communities by on sporocarp appearance or pure culture synthesis experi- supporting the dominant plant. Similarly, it is proposed ments. Evidence from field-collected root tips from mixed EM that in some tropical rainforests EM associations encour- plant communities suggests that most of the root tips recov- age dominance of certain tree species (Connell & Lowman ered are colonized by fungi associating with multiple host spe- 1989). Studies performed with European calcareous grass- cies (Horton & Bruns 1998; Horton, Bruns & Parker 1999; land provide opposite results. Both Grime et al. (1987) and Cullings et al. 2000; Kennedey, Izzo & Bruns 2003; Horton, van der Heijden et al. (1998) show that subordinate plant Molina & Hood 2005; Dulmer 2006; Ishida, Nara & Hogetsu species benefited most when mycorrhizal fungi were pres- 2006; Lian et al. 2006; Nara 2006b). While there are some EM ent, while biomass of the dominant grass was not fungi that are relatively host specific, most appear to have enhanced, or even reduced in presence of mycorrhizal intermediate to broad host rangesandcanformnetworkswith fungi. As a consequence, mycorrhizal fungi enhanced plant multiple plant species in a mixed stand (Molina, Massicotte & diversity in these grassland communities. Note that, in the Trappe 1992). study by Grime et al. (1987), field roots were used as inoc- From the above, it follows that a considerable number of ulum to establish a fungal network. It is possible that, plant species from a specific community can be colonized by

2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1139–1150 1144 M. G. A. van der Heijden & T. R. Horton the same mycorrhizal fungus and are, thus, connected to the investment costs and benefits are interlinked. When discussing same network. Important questions that follow are: which this, it is important to remember that mycorrhizal fungi are plants maintain this network, which plants receive benefit and independent from plants, aiming to enhance their own fitness. how is this physiologically organised? There are several scenar- Hence, the fungi may resist plants when these try to sanction ios (Fig. 3). One option is that carbon investment and plant them under unfavourable conditions. benefit are tightly interlinked: the more a plant invests in the It is also possible that the relationship between carbon invest- network, the more benefit it receives in return (Fig. 3a). Physi- ment and plant benefit is positive, but with a different angle for ological studies which show that nutrient supply to the plant different plant species or different plant individuals (Fig. 3a). increases with enhanced carbohydrate availability for the fun- This could explain why, in some cases, seedlings benefit more gus (Bucking & Shachar-Hill 2005) provide evidence for this from a connection to the mycorrhizal network compared with scenario. Studies which show that co-occurring seedlings and adult plants (see above). It also explains why the outcome of adult plants obtain, per unit of biomass, the same relative ben- competition between two mycorrhizal plant species is often not efit from mycorrhizal fungi (e.g. Kytoviita, Vestberg & Tuom balanced (e.g. Finlay 1989; Perry et al. 1989; Marler et al., 2003; Pietikainen & Kytoviita 2007) also indicate that costs 2004; Scheublin, Van Logtestijn & Van der Heijden 2007). (carbon investment) and benefit (stimulation of plant growth) The second option is that there is no relationship between are interlinked (Fig. 3a). Be aware that under this scenario lar- carbon investment and plant benefit (Fig. 3b). Every plant ger plants obtain more resources in total, because they also individual has a different relationship, thus resulting in a large invest more, but the relative benefit is the same. Several studies scatter of points (Fig. 3b). This has similarities to the so-called also show that plants which obtain large amounts of nutrients idiosyncratic relationship between biodiversity and ecosystem from mycorrhizal fungi also have larger hyphal networks. functioning (Johnson et al. 1996) stating that the relationship Hence, there is evidence that cost–benefit relationships of is highly variable, depending on factors such as soil type, nutri- plants with mycorrhizal fungi are interlinked for a considerable ent availability and plant species identity. This scenario would number of plant species. mean that some plant individuals obtain much more benefit Many plants can, at least partly, control colonization by from a mycorrhizal network per unit carbon they invest, com- mycorrhizal fungi under less beneficial conditions. At high pared with other plants that receive relatively less benefit per phosphorus availability, root colonization levels and spore unit invested carbon. The relationship could also differ with production by arbuscular mycorrhizal fungi are usually different mycorrhizal fungal species or for different growth reduced (Oehl et al. 2003; but see Graham, Duncan & Eissen- stages of one plant species (e.g. the relative benefit of seedlings stat 1997). Ectomycorrhizal fungi are also less abundant and is much higher compared with adult plants, as shown for a few EM fungal communities are less diverse when nitrogen avail- plant species in our analysis). ability increases (Wallenda & Kottke 1998; Lilleskov et al. Plant–mycorrhizal network interactions are very hard to 2002), probably because plants suppress colonization (Nehls explore in the field because most plants are colonized by multiple et al. 2007). Moreover, plants can repress mycorrhizal phos- fungal species (networks), each with its own cost–benefit phorus uptake and down-regulate fungal phosphorus trans- interaction. In addition, some plant species might, on aver- porter genes at high phosphorus availability (e.g. Nagy et al. age, benefit more from mycorrhizal networks compared 2009) when the fungus is not required for nutrient uptake. On with other plant species. For instance, several studies the other hand, plants exude signals to attract mycorrhizal showed that mycorrhizal fungi reduce biomass of Festuca fungi under nutrient deficiency (Yoneyama et al. 2007). This ovina when this grass is coexisting or competing with other suggests that plants have mechanisms to regulate their invest- plant species (Grime et al. 1987; van der Heijden et al. ment in mycorrhizal fungi, providing additional evidence that 1998; Scheublin, Van Logtestijn & Van der Heijden 2007).

(a) (b) (c)

1 3 3 Costs 2 4 4

Benefit

Fig. 3. Three hypothetical relationships between costs (carbon investment) and benefits (assessed as biomass gain) of the mycorrhizal symbiosis. Cost and benefits are positively correlated (a), are variable, depending on fungus ⁄ plant pair, or environmental conditions (b) or are negatively correlated (c). Cost and benefit relationships can be positively correlated, but with a different angle for different groups of plant species or for seedlings compared with adult plants (solid and interrupted line in a). Plant species can invest large amounts of carbon in mycorrhizal fungi and receive much benefit in return (plant 1), or plants invest small amounts of energy in mycorrhizal networks and receive little in return (plant 2). Some plant individuals invest much but get not much in return (plant 3) while other plants receive much benefit, without large investments (plant 4).

2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1139–1150 Socialism in soil? The importance of mycorrhizal fungal networks 1145

The study by Grime et al. (1987) indicated that there is car- where wealth and power are distributed more evenly. On the bon transfer from Festuca ovina to other plant species contrary, a capitalist mycorrhizal network would be privately through common mycorrhizal fungal networks. The signifi- controlled for profit by the plant or plants establishing the net- cance of this carbon transfer is still under debate. However, work. Our analysis provides both examples of ‘socialist’ and the fact that carbon from Festuca was found in the roots of ‘capitalist’ tendencies of mycorrhizal networks. In several cases other mycorrhizal plant species, and not in non-mycorrhi- small seedlings obtained more benefit (in terms of biomass gain) zal plants, suggests that Festuca was at least supplying car- compared with the larger plants that established the mycorrhizal bon to the hyphal network in this study and that other networks (e.g. Eissenstat & Newman 1990; van der Heijden plants benefited from the hyphal network. The outcome of 2004), pointing to socialist tendencies. However, in all studies our analysis, which shows that effects of mycorrhizal net- performed so far, the actual investments (in terms of car- works on seedling establishment can be positive, neutral bon ⁄energy input into the network) by small and large plants and negative, fits to the scenario shown in Fig. 3b. were not determined and there is no empirical evidence that It has been proposed that the symbiosis between plants and resources are preferentially allocated to small seedlings. It is not mycorrhizal fungi is based on the exchange of luxury goods unlikely that in many cases the larger plants facilitated establish- (Kiers & van der Heijden 2006). At low soil fertility, plant ment of the small seedlings by (i) providing improved mycorrhi- growth is limited more by nutrients than by carbon supply, zal inoculum potential and (ii) reducing the carbon cost of and carbohydrates accumulate in plant organs (e.g. Poorter & establishing a functioning mycorrhizal network around the seed- de Jong 1999; Korner 2003). Under these conditions, it is lings’ roots. However, there are also several examples which advantageous for the plant to allocate assimilates to the fungi show that small seedlings receive proportionally the same or even because, by doing so, plants acquire more of the resources they less benefit from networks as larger plants (Table 1). In terms of need, without additional costs. The investment of a luxury total biomass gains then, the larger plants thus benefit more from good (carbon) in mycorrhizal fungi by some plants, and the mycorrhizal networks, pointing to capitalist tendencies. co-use of mycorrhizal networks by other plants could explain Mycorrhizal networks can alsobeviewedaspartof‘super- the variable responses. However, this scenario would only organisms’ (sensu Clements 1936), with the fungal species in work if the plant investing a luxury good is not negatively the network being redundant physical extensions of the roots affected (e.g. by enhanced competitive ability of other plants) that translocate nutrients freely between plants. However, each and obtains at least a benefit at some point in its life cycle (e.g. fungal species has its own niche and mycorrhizal fungi differ in during seedling establishment). many ways including growth rate (Olsson, Jakobsen & Wal- A third option is that there is a negative relationship lander 2002), soil type preference, resistance to stress and dis- between investment and benefit (Fig. 3c). This implies that turbance (Oehl et al. 2003), ability to acquire nutrients some plant species invest in mycorrhizal networks while others (Jakobsen, Smith & Smith 2002), ability to solubilise nutrients obtain benefit from them. Generally, this relationship is unli- from organic matter and plant host range (Molina, Massicotte kely, because plants would select against mycorrhizal coloniza- & Trappe 1992). Moreover, mycorrhizal fungi have evolved tion if other plants always benefited more and if this resulted in mechanisms for recognizing and preventing fusion of non self a reduced competitive ability (but see negative feedback model tissue. For instance, in AM fungi, hyphal fusions have only in Bever, Westover & Antonovics (1997). This relationship been observed between individuals of the same genotype while does fit mycoheterotrophic plants, which lack chlorophyll and fusion between individuals of different genotypes, species or indirectly parasitize other plants by obtaining carbon and families do not occur (Giovannetti, Azzonlini & Citernesi nutrients from mycorrhizal networks. These plants (also called 1999; but see Croll et al. 2009). Soils are, thus, colonized by epiparasites) obtain benefit from mycorrhizal networks of a several independent networks simultaneously competing for single fungal species, while the surrounding vegetation main- nutrients and roots. Moreover, in many cases mycorrhizal tains the mycorrhizal network. There are about 400 species in plants acquire nutrients not directly from the soil in competi- the world with this strategy, distributed in eleven families tion with other plants, but from their fungal networks. A fun- including the Orchidacea and Ericaceae, and all of them lack gus may compete with other fungi for soil nutrients, and then chlorophyll (Leake 1994; Taylor et al. 2002). Recent studies deliver those nutrients to the various plants it colonizes. The indicate that some other plants of these families have a mixed distribution of the nutrients to plants in a network are then a strategy and acquire carbon both through photosynthesis and function of variations in compatibility between a fungal indi- via hyphal links (Julou et al. 2005; Girlanda et al. 2006; Tedersoo vidual and its colonized plant hosts, and variation in carbon et al. 2007; but see Hynson et al. 2009). It is still unclear whether flow to the fungus among the plants. these plants also invest in mycorrhizal networks (but see Bidart- ondo et al. 2000). Experimental studies are required to test this in Mycorrhizal networks and plant–plant more detail. interactions The role of mycorrhizal networks in regulating plant–plant Socialism or capitalism in soil? interactions and plant community dynamics is still poorly It is tempting to compare mycorrhizal networks with socialist understood. From our analysis it follows that seedlings of systems, where all individuals have equal opportunities and several plant species benefit from the presence of mycorrhizal

2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1139–1150 1146 M. G. A. van der Heijden & T. R. Horton networks. The effect of mycorrhizal networks on interactions plants give it away for ‘free’. Moreover, nitrogen fixation by between already established plants is still poorly understood. nitrogen fixing plants is energetically expensive, implying that In particular it is unclear if there are plant species that maintain direct transfer from a nitrogen fixer to a non-nitrogen fixer is mycorrhizal networks through carbon supply while there are probably low. The significance of interplant carbon transfer other species that benefit by acquiring nutrients present in the has been unequivocally shown in mycoheterotrophic plants network (other than the obvious examples of mycohetero- which parasitize on mycorrhizal networks from which they trophic plants). Physiological studies such as those by Voets obtain carbon and nutrients (see above). In addition, evidence et al. (2008), performed under sterile in vitro conditions are for carbon movement between green plants comes from Sim- necessary to investigate this in detail. Plant competition experi- ard et al. (1997) and Lerat et al. (2002). There is debate about ments show that not all plant species receive equal benefit from the ecological significance of C transfer between plants via mycorrhizal networks (e.g. Finlay 1989; Perry et al. 1989; mycorrhizal networks (Robinson & Fitter 1999). Graves et al. Scheublin, Van Logtestijn & Van der Heijden 2007). For (1997) and Wu, Nara & Hogetsu (2001) have shown that C instance, several studies showed that Festuca ovina can benefit fixed by one plant and transferred to another remains in the from mycorrhizal fungi when grown alone but, in competition, root system, and presumably the hyphae, of the second plant. its competitive ability is reduced compared with other plants However, C must move out of the root system in mycohetero- (van der Heijden et al. 1998; Scheublin, Van Logtestijn & Van trophs and the studies by Simard and Lerat suggest this can der Heijden 2007). This indicates that the cost–benefit ratio of happen in green plants as well. What is not clear in these stud- plants connected to a mycorrhizal network is not the same for ies is the source of the carbon translocated from the fungi. It is each plant species. Microcosm studies have also shown that likely that some of the C atoms are part of amino acids such as AM fungi alter plant diversity and plant community structure glutamine or glutamate that are transferred as N sources to the (Grime et al. 1987; van der Heijden et al. 1998; Hartnett & plants from the fungi. How these amino acids influence the Wilson 1999) because different plant species receive different energy budget of these plants, especially those that cannot fix amounts of benefit from mycorrhizal network. Moreover, the their own carbon, remains to be determined. composition and number of mycorrhizal fungi present in plant communities is also important in determining plant productiv- Ecological function of mycorrhizal fungal ity and plant diversity (van der Heijden et al. 1998; Klirono- networks mos et al. 2000; Vogelsang, Reynolds & Bever 2006). Studies with microcosms are of particular interest because the plants Mycorrhizal fungal networks provide a wide range of services arecoexistingandplantscanbecolonizedbythesamefungi. to plants and ecosystems (Table 2). The most important one is In communities with several mycorrhizal fungi (most EM probably nutrient uptake, followed by seedling support (see communities have tens of species), different plant species can analysis). Other functions, such as the prevention of nutrient be colonized by different mycorrhizal fungi and it is even possi- leaching, internal cycling of nutrients (e.g. transfer of nutrient ble that guilds of plants exist interconnected by the same from dying roots and leaf litter) and their ability to facilitate mycorrhizal networks (although no proof for this has been bacterial dispersion, have been largely overlooked (Table 2). obtained). Molecular techniques that detect specific mycorrhi- Moreover, the fact that seedlings in perennial plant communi- zal fungi, could test whether this is actually happening. More- ties become quickly colonized by mycorrhizal fungi (e.g. within over, different mycorrhizal networks are likely to coexist in 3–6 days after seedling emergence (Read, Koucheki & Hodg- mixed forests where trees associate both with AM and EM son 1976; Birch 1986) is probably very important because small fungi, or in EM forests with an understorey of AM herbs seedlings then have immediate access to a cheap ‘nutrient (Newman & Redell 1988). Some mycorrhizal fungi can also adsorption machine’ provided and maintained by the sur- form functional associations with plants with different mycor- rounding vegetation (Newman 1988). Plant growth in many rhizal types as was recently shown for the fungus Piceirhiza communities (e.g. grassland or savanna) is limited by nutrient bicolorata (Grelet et al. 2009). availability and not by light availability. Hence, a connection to mycorrhizal networks (as a source of inoculum) is extremely important for plant survival, even if seedlings have to supply Carbon and mineral nutrient transfer through carbon to maintain their own small part of the fungal network. mycorrhizal networks However, the function of hyphal networks is less clear in eco- One important consequence of mycorrhizal networks is that systems where light availability is the main limiting factor for nutrients, carbon and water can be transferred from one plant seedling establishment. For instance, enhanced mycorrhizal to another. The significance of interplant carbon & nutrient colonization did not improve seedling survival in a tropical forest transfer has been widely debated (see reviews by Simard, Dur- (Gehring & Connell 2006). Work by Simard et al. (1997) all & Jones 2002 & Selosse et al. 2006). Selosse et al. (2006) showed that tree seedlings in forest obtain carbon from estimatedthatupto40%ofplantnitrogeninreceiverplants mycorrhizal networks. This may enhance seedling survival, can be derived from donor plants (e.g. nitrogen fixing plants) although experimental evidence for this is still unclear. and be transferred through mycorrhizal networks. In most sit- The importance of mycorrhizal networks for seedling estab- uations this proportion is probably much lower, as nitrogen is lishment has been known for some time and this is now also usually limiting plant productivity, making it unlikely that being applied in forestry and agriculture. Moreover, a manage-

2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1139–1150 Socialism in soil? The importance of mycorrhizal fungal networks 1147

Table 2. Ecological functions and significance of mycorrhizal fungal networks and of the presence of mycorrhizal fungi

Ecological Function significance References

Direct effects of mycorrhizal networks Facilitation of seedling establishment Low to See literature analysis in this paper very high Rapid colonization of seedlings Very high Read, Koucheki & Hodgson 1976 Increased mycorrhizal inoculum potential High Newman 1988; Dickie et al. 2005; Dickie & Reich of soil around established plants 2005; Nara 2006b; Nun˜ez, Horton & Simberloff Reduced seedling costs of establishing High Newman 1988 mycorrhizal associations Prevention of nutrient leaching High* van der Heijden 2009 Transfer of nutrients from dying roots High Ritz & Newman 1985; Mikkelsen, Rosendahl & Jakobsen 2008 Transport of substances between plants transfer of carbon Probably low Simard et al. 1997; Robinson & Fitter 1999; Lerat et al. 2002 transfer of phosphorus Probably low Simard, Durall & Jones 2002; Selosse et al. 2006 transfer of nitrogen Still unclear He et al. 2005; Selosse et al. 2006; transfer of water Unknown transfer of plant signals Unknown Changes in fungal community composition and High Bever, Westover & Antonovics 1997; Collier & abundance (including plant–soil feedback) Bidartondo 2009; Hubert & Gehring 2008 Ecological functions of the presence of mycorrhizal fungi Nutrient uptake Very high Summarized in van der Heijden, Bardgett & van Straalen 2008 Decomposition of litter High Lindahl et al. 2007 Improvement of soil structure by enmeshing soil High Rillig & Mummey 2006 aggregates in stable structures Carbon transfer to soils High† Water uptake and hypdraulic lift Variable Auge 2001; Egerton-Warburton, Querejeta & Allen 2007 Hyphal highways for bacterial dispersion Very low Perotto & Bonfante 1997; Kohlmeier et al. 2005 for plants Food for other organisms Low for plants‡ Gange 2000

*Considerable amounts of nutrients are lost due to leaching and surface run off: in some areas up to 160 kg N and up to 30 kg of phos- phorus year)1 hectare)1 are lost in this way (Herzog et al. 2008; Sims, Simard & Joern 1998). The prevention of nutrient leaching is espe- cially important for non-renewable nutrients (e.g. P or K) and in sandy soils or soils where these nutrients cannot be fixed to soil particles (Sims, Simard & Joern 1998). †Plant carbon allocation to mycorrhizal fungi in soil is highly variable, between 0 and 20% of plant carbon is allocated to mycorrhizal fungi (Hobbie 2006; Jakobsen, Smith & Smith 2002). ‡In forests, mycorrhizal fungi often dominate the microbial biomass, with up to 50% of soil dry weight in areas with particular dense proliferation of mycelia (Ingham et al. 1991). These hyphae can be consumed by a wide range of organisms. However, some studies indi- cate that mycorrhizal fungal hyphae are not very palatable and do not belong to the diet of collembola, abundant soil arthropods (Gange 2000). ment practice in agriculture that is receiving increased atten- acquiring limiting nutrients. Many plants benefit from fungal tion is conservation tillage (Holland 2004). Conservation till- support, but there are also a considerable number of cases age minimises the disruption of the soil structure, promotes where there is no, or even a negative effect of mycorrhizal soil biodiversity and reduces soil erosion and drought stress. fungi. The results presented in our analysis clearly reflect this Several studies reported that mycorrhizal networks increase in as we observed significant growth stimulation of small seed- abundance under conservation tillage (e.g. Jansa et al. 2003). lings by mycorrhizal fungal networks in only 48% of cases, It is likely, although not proven, that the positive effects of con- while negative effects occurred in 25% of the cases. Mycorrhi- servation tillage are, at least in part, mediated by mycorrhizal zal fungal networks have the ability to support co-occurring networks. plants of different sizes, but effects are highly variable. Thus, mycorrhizal networks do have some similarities to socialist systems in that small plants can benefit from networks that are Conclusions and outlook supported by bigger plants in the community. However, In this review, we have shown that mycorrhizal fungal net- whether this is actually occurring is highly context dependent, works play a key role in natural ecosystems. Mycorrhizal fungi and varies with study system (e.g. plant species identity, fun- can facilitate seedling establishment and plant growth by gal identity, nutrient availability). Beside effects on plant

2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1139–1150 1148 M. G. A. van der Heijden & T. R. Horton growth, we identified a number of other important ecological References functions of mycorrhizal networks in soil. These include Aldrich Wolfe, L. (2007) Distinct mycorrhizal communities on new and estab- recycling of nutrients, prevention of nutrient losses, contribu- lished hosts in a transitional tropical plant community. Ecology, 88,559– tion to soil structure, food for other organisms, and mycorrhi- 566. zal fungal networks acting as hyphal highways for bacterial Auge, R.M. (2001) Water relations, drought and vesicular-arbuscular mycor- rhizal symbiosis. Mycorrhiza, 11, 3–42. dispersion. Bever, J.D., Westover, K.M. & Antonovics, J. (1997) Incorporating the soil For a better understanding of the impact of mycorrhizal fun- community into plant population dynamics: the utility of the feedback gal networks on seedling growth and ecosystem functioning, approach. Journal of Ecology, 85, 561–573. Bidartondo, M.I., Kretzer, A.M., Pine, E.M. & Bruns, T.D. (2000) High root several key questions need to be answered. First, cost–benefit concentration and uneven ectomycorrhizal diversity near Sarcodes sangui- relationships of individual plants connected to mycorrhizal nea (Ericaceae): a cheater that stimulates its victims? American Journal of networks are still poorly understood. It is unclear which plants Botany, 87, 1783–1788. Birch, C.P.D. (1986) Development of VA mycorrhizal infection in seedlings in invest, and how this is related to the amount of benefit received. semi-natural grassland turf. Physiological and Genetic Aspects of Mycorrhi- The fact that most (if not all) physiological studies are zae (eds V. Gianinazzi-Pearson & S. Gianinazzi), pp. 233–237. INRA, Paris, performed with single plants, grown in highly simplified study France. Brooker, R.W., Maestre, F.T., Callaway, R.M., Lortie, C.L., Cavieres, L.A., systems, without hyphal interconnections to other plants, does Kunstler, G. et al. (2008) Facilitation in plant communities: the past, the not contribute to a better understanding of process occurring present, and the future. Journal of Ecology, 96, 18–34. in mycorrhizal networks. The use of dual labelling (with 13C; Brundrett, M.C. (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by 14C, 15N 33P) as performed by some investigators is impor- resolving conflicting information and developing reliable means of diagnosis. tant. Second, we have shown here that mycorrhizal net- Plant and Soil, 320, 37–77. works are important for seedling establishment in several Bucking, H. & Shachar-Hill, Y. (2005) Phosphate uptake, transport and transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimu- cases. However, in order to draw more precise conclusions, lated by increased carbohydrate availability. New Phytologist, 165, 899–912. additional studies are required (e.g. studies with EM fungal Callaway, R.M., Brooker, R.W., Choler, P., Kikvidze, Z., Lortie, C.J., Micha- networks showed positive effects in 75% of the cases. However, let, R. et al. (2002) Positive interactions among alpine plants increase with stress. Nature, 417, 844–848. this conclusion is based on seven independent studies). Fur- Cameron, D.D., Johnson, I., Read, D.J. & Leake, J.R. (2008) Giving and thermore, as far as we know, there are no studies which tested receiving: measuring the carbon cost of mycorrhizas in the green orchid, whether hyphal networks formed by plants with ericoid or Goodyera repens. New Phytologist, 180, 176–184. Clements, F.E. (1936) Nature and structure of the climax. Journal of Ecology, orchid mycorrhizas promote seedling establishment of nearby 24, 252–284. plants. Third, the contribution of mycorrhizal networks to Collier, F.A. & Bidartondo, M.I. (2009) Waiting for fungi: the ectomycorrhizal nutrient uptake by plants and nutrient cycling in natural eco- invasion of lowland heathlands. Journal of Ecology, 97, 950–963. Connell,J.H.& Lowman,M.D.(1989)Low-diversitytropicalrainforests–some systems is still poorly understood and mainly based on experi- possiblemechanismsfortheirexistence.AmericanNaturalist,134,88–119. ments performed in the laboratory (but see Hobbie & Hobbie Croll, D., Giovannetti, M., Koch, A.M., Sbrana, C., Ehinger, M., Lammers, 2006). Fourth, there are many other factors that facilitate seed- P.J. & Sanders, I.R. (2009) Nonself vegetative fusion and genetic exchange in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytologist, ling establishment and plant growth as discussed in this issue of 181, 924–937. the Journal of Ecology. The relevance of mycorrhizal networks Cullings, K.W., Parker, V.T., Finley, S.K. & Vogler, D.R. (2000) Ectomycor- compared with these other factors is often poorly understood. rhizal specificity patterns in a mixed Pinus contorta and Picea engelmannii forest in Yellowstone National Park. Applied and Environmental Microbiol- Fifth, most studies have been performed with mycorrhizal ogy, 66, 4988–4991. fungi that can be easily cultured. However, molecular tech- Dickie, I.A., Koide, R.T. & Steiner, K.C. (2002) Influences of established trees niques have shown that in the case of AM fungi, 60% of envi- on mycorrhizas, nutrition, and growth of Quercus rubra seedlings. Ecologi- cal Monographs, 72, 505–521. ronmental sequences do not match with AM fungi that have Dickie, I.A. & Reich, P.B. (2005) Ectomycorrhizal fungal communities at forest been brought into culture (van der Heijden, Bardgett & van edges. Journal of Ecology, 93, 244–255. Straalen 2008). Hence, it will be extremely important to culti- Dickie, I.A., Schnitzer, S.A., Reich, P.B. & Hobbie, S.E. (2005) Spatially dis- junct effects of co-occurring competition and facilitation. Ecology Letters, 8, vate these fungi and assess their ecological relevance. Sixth, the 1191–1200. spatial distribution and movement of nutrients in mycorrhizal Dulmer, K. (2006). Mycorrhizal associations of American chestnut seedlings: a networks is still poorly understood. Finally, our climate is lab and field bioassay. Environmental and Forest Biology.p.106.SUNY- ESF Syracuse, New York, U.S.A. changing and periods of drought or heavy rainfall are expected Egerton-Warburton, L.M., Querejeta, J.I. & Allen, M.F. (2007) Common to increase in many countries. It is important to understand mycorrhizal networks provide a potential pathway for the transfer of how these changes influence the stability of mycorrhizal net- hydraulically lifted water between plants. Journal of Experimental Botany, 58, 1473–1483. works and their ability in facilitating plant growth. Eissenstat, D.M. & Newman, E.I. (1990) Seedling establishment near large plants – effects of vesicular –arbuscular mycorrhizas on the intensity of plant competition. Functional Ecology, 4,95–99. Acknowledgements Finlay, R.D. (1989) Functional aspects of phosphorus uptake and carbon translocation in incompatible ectomycorrhizal associations between Pinus We would like to thank Erik Lilleskov and Mari Moora for discussion and pro- sylvestris and Suillus grevillei and Boletinus cavipes. New Phytologist, 112, viding data. Toby Kiers and David Read commented on a very early version of 185–192. this paper. 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