Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems

Authors

  • Marcel G. A. Van Der Heijden,

    Corresponding author
    1. Ecological Farming Systems, Agroscope Reckenholz-Tänikon, Research Station ART, Zurich, Switzerland
      *Correspondence author. E-mail: marcel.vanderheijden@art.admin.ch
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  • Thomas R. Horton

    1. Department of Environmental and Forest Biology, SUNY-Environmental Science and Forestry, Syracuse, NY, USA
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*Correspondence author. E-mail: marcel.vanderheijden@art.admin.ch

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 assimilates.

2. Many mycorrhizal fungi are not host specific and one fungal individual can colonize and interconnect 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 networks, (ii) is benefit dependent on the size or age of a plant, (iii) is fungal support related to the relative 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 interactions 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. Seedlings 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 communities by facilitating and influencing seedling establishment, by altering plant–plant interactions and by supplying and recycling nutrients.

Introduction

Plants interact in many ways, both negative and positive. Negative interactions such as plant competition received much attention in the 1980s and 90s (Sapp 2004). However, there is increasing recognition that positive interactions such as facilitation also play a key role in plant communities (Callaway et al. 2002; Brooker et al. 2008). Facilitation is defined here as positive non-trophic interactions that occur between physiologically independent plants and that are mediated through changes in the abiotic environment or through other organisms (Brooker et al. 2008). Examples of facilitation are the positive effects of nitrogen fixing plants on neighbours and pollination of multiple plant species by the same insects.

In this paper, we focus on the 400 million-year-old symbiosis between the majority of land plants and mycorrhizal fungi (Smith & Read 2008). Such interactions have facilitative effects when mycorrhizal associations formed or maintained by one plant are beneficial for other plants. The mycorrhizal symbiosis is based on reciprocal exchange of resources: the fungi provide limiting nutrients to plants in return for plant assimilates (Smith & Read 2008). In natural ecosystems, plants obtain up to 80% of their requirement for nitrogen and up to 90% of phosphorus from mycorrhizal fungi (van der Heijden, Bardgett & van Straalen 2008). These nutrients are acquired by complex hyphal networks (Leake et al. 2004; Selosse et al. 2006) which are specialised to forage for soil nutrients (Olsson, Jakobsen & Wallander 2002). Moreover, mycorrhizal fungi can also provide resistance to stress, drought and in some cases to soil pathogens (Auge 2001; Sikes, Cottenie & Klironomos 2009).

Most mycorrhizal fungi are not host specific and one fungal individual can simultaneously colonize a large number of plants from the same but also from different plant species (Fig. 1). Moreover, both small seedlings and large plants can be colonized by one mycorrhizal fungal individual (Newman 1988; Horton & van der Heijden 2008). Thus, plants can be interconnected by mycorrhizal fungal networks in the so-called ‘wood-wide-webs’ (Simard et al. 1997). The existence of these networks implies that fungi have the ability to distribute resources among plants irrespective of their size, status (i.e. their relative dominance in the plant community) or identity. For clarity, a mycorrhizal fungal network is defined here as an established fungal mycelium that simultaneously colonizes and interconnects roots of the same or different plant species. The fungi able to form mycorrhizal fungal networks are those that form the typical mycorrhizal structures inside plant roots or on the surface of plant roots after a complex molecular dialogue between plant and fungus.

Figure 1.

 Resource sharing in mycorrhizal networks. One mycorrhizal fungal individual colonizes different plant individuals from the same, but also from different plant species. Carbon and nutrients (N) can move through this common hyphal network. Different numbers represent different plant species. For instance, plant species 1, 2 and 3 are colonized by the same mycorrhizal fungi (dashed line). Nutrients can be acquired by this fungus from a nutrient patch near plant 1 (N1) and move to plant 1 or 2. Nutrients of patch N2 could flow to plant 2 or 3. In addition, plant species 1, 2 and 3 are also colonized by another mycorrhizal fungus (solid line). Some plant species are not colonized by mycorrhizal fungi (plant 4). Plant size also varies (see plant species 3) showing that plants in different growth stages can be colonized by the same mycorrhizal fungus.

In this paper, we explore the significance of mycorrhizal fungal networks as facilitators in plant communities. In particular we investigate: (i) whether all plants benefit from mycorrhizal fungi, (ii) whether support is dependent on the size of a plant, (iii) whether there are host-dependent barriers and physiological constraints for support, (iv) whether there is interplant carbon and nutrient transfer via mycorrhizal networks and (v) whether mycorrhizal networks influence plant–plant interactions and plant community dynamics. Moreover, using an analysis of published studies, we test whether mycorrhizal networks facilitate growth of small seedlings that establish between or near larger plants. We end with conclusions and identify future research priorities.

Do all plant species benefit?

Many plant communities are dominated by mycorrhizal plants, including most grasslands, savanna, boreal-, temperate- & tropical forests (Read 1991). In these communities, abundant mycorrhizal fungal networks are formed (Leake et al. 2004) and the majority of plants are usually extensively colonized by these mycorrhizal networks. Pot experiments performed 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 75% of the investigated plant species benefited from mycorrhizal fungal networks with enhanced growth (Grime et al. 1987; van der Heijden 2004). Experiments with a number of tree species indicate that many of them benefit from mycorrhizal colonization, especially at low soil fertility (Simard, Durall & Jones 2002; Karst et al. 2008). However, the impact of mycorrhizal fungal networks on tree growth in natural systems is difficult to study because mycorrhizal fungi are often already present (but see Nara 2006a; Dickie, Koide & Steiner 2002; see also below).

Not all interactions with mycorrhizal fungal are positive: some plant species perceive mycorrhizal fungi as antagonists. These include some non-mycotrophic plant species (plants that are unable to form symbiotic associations with mycorrhizal fungi) and some plant species characteristic of ruderal environments (Francis & Read 1995; Klironomos 2003). It must be remembered that approximately 10–15% of all vascular plant species, including the model plant Arabidopsis thaliana), are non-mycorrhizal and do not benefit from mycorrhizal fungi (Wang & Qiu 2006; Brundrett 2009). Hence, the question of whether all plant species benefit from mycorrhizal fungi can be answered simply with a ‘no’. Finally, the effect of mycorrhizal fungi on plant growth is context dependent (Johnson, Graham & Smith 1997; Jonsson et al. 2001). At high soil fertility, there is often no benefit and plant growth can be slightly reduced in the presence of mycorrhizal fungi due to their carbon demand (Smith, Grace & Smith 2009). Further, a mycorrhizal fungus may be mutualistic with one host plant species, and parasitic on another host species as Plattner & Hall (1995) report for Tuber melanosporum.

Is benefit dependent on the size of a plant?

Mycorrhizal fungi usually colonize all plant individuals from mycotrophic hosts, irrespective of their size or development. An intriguing question is whether all plant individuals (e.g. small seedlings and larger plants) receive the same amount of benefit from mycorrhizal fungi. To test for general patterns, we performed a literature analysis with studies where seedlings were grown together with larger/adult plants in the presence and absence of mycorrhizal fungi. We made a distinction between studies where seedlings were grown with adult/larger plants from the same species and studies in which seedlings grew together with different plant species. In addition to this, a distinction was made between plants hosting arbuscular mycorrhizal (AM) fungi and ectomycorrhizal (EM) fungi. EM fungi belong to the Basidiomycetes and Ascomycetes and associate with a range of trees, especially those from temperate and tropical forests. AM fungi belong to the Glomeromycota (Schüßler, Schwarzott & Walker 2001) and associate with an estimated 65% of all land plants, including many grasses, herbs and tropical trees (Wang & Qiu 2006; Brundrett 2009). The results of the analysis are shown in the next section. This analysis focuses on experiments where several plants co-occur in pots, microcosms or in the field. These experiments are ecologically more realistic than those where plants are grown alone in pots with or without mycorrhizal fungi. In pots with multiple plants (e.g. seedlings and adult plants), interactions between plants occur (e.g. competition or facilitation) and the effects of common mycorrhizal networks on plant growth can be tested, thus better simulating conditions usually observed in natural communities.

Mycorrhizal networks and seedling establishment near larger plants

We performed a literature survey and found 20 studies where seedlings were grown near larger plants in the presence and absence of mycorrhizal fungal networks (see Appendix S1 in Supporting Information). In most studies, several seedling species were tested and results of 60 cases were included in the analysis. Thirteen studies were performed with AM fungi, and seven with EM fungi (Appendix S1). Three categories were distinguished: cases where seedlings had significantly higher biomass in the presence of mycorrhizal fungal networks, cases where seedling biomass was significantly reduced and cases without significant differences.

Twenty-one seedling species (48% of cases investigated) benefited from mycorrhizal networks while 12 species (25% of cases) responded negatively. The biomass of 15 seedling species (27% of the cases) was not significantly influenced by the presence or absence of mycorrhizal fungal networks (Fig. 2; Appendix S1). The distribution of cases differed significantly among the three categories (= 0.05). The average growth response of all seedlings/cases was +14% or +20% when non-mycorrhizal (NM) plants not hosting mycorrhizal fungi were removed from analysis.

Figure 2.

 Output from literature analysis showing effects of mycorrhizal fungal networks on seedling growth and establishment. Positive and negative response indicates the number of cases where seedlings biomass was significantly enhanced or reduced in the presence of mycorrhizal fungal networks. ‘No response’ indicates cases where seedling biomass was not significantly affected by the presence or absence of mycorrhizal networks. For further information see Appendix S1.

We also performed the analysis separately for plants associating with AM fungi or with EM fungi. Mycorrhizal networks formed by EM fungi promoted seedling growth in seven cases (75% of the cases), while in three cases (25%) seedling growth did not vary between treatments with or without mycorrhizal fungi. For AM fungi, 16 out of 37 species (and 42% of the cases) responded significantly positively, 15 species (33% of the cases) responded negatively, while growth responses of 12 seedling species (29% of the cases) did not vary significantly in treatments with or without mycorrhizal fungal networks. Growth responses of several species (e.g. Plantago lanceolata– see Appendix S1) were tested repeatedly in different studies. Hence, the distribution of cases as discussed above and presented in Fig. 2 does not match precisely to the number of investigated seedling species. Based on this analysis, it can be concluded that seedling establishment of plants forming associations with EM fungi is more heavily dependent on mycorrhizal fungi compared with plants associating with AM fungi. Note, however, that a much broader range of plant species (including several non-mycorrhizal hosts) were included in the analysis with AM fungi, also reflecting the fact that habitats where AM fungi are abundant probably contain a higher proportion of non-mycorrhizal plants. Moreover, the analysis for EM fungi is based on only a few cases and the observed effect might change considerably if more studies are included. The outcome of this analysis is roughly the same if the number of studies and not the number of seedling species or cases is used for the analysis (Appendix S1).

An interesting question is whether the benefit seedlings derive from mycorrhizal fungal networks is higher, lower or equal compared with coexisting older and larger plants of the same species. This could be tested for nine studies (Table 1). Three of these studies indicated that the relative benefit to seedlings was similar to that of larger plants (compare the mycorrhizal dependencies in Table 1: see Ocampo 1986; Kytoviita, Vestberg & Tuom 2003; Pietikainen & Kytoviita 2007), two studies found that seedlings benefited more (van der Heijden 2004; Eissenstat & Newman 1990; although not significantly so in the latter case) and in two studies adult plants benefited from mycorrhizal fungi while seedling growth was significantly reduced (Moora & Zobel 1998; Nakano-Hylander & Olsson 2007). These findings are in line with Moora & Zobel (2009) who observed that mycorrhizal networks are less beneficial for seedlings of the same species (intraspecific combinations) compared with seedlings of different plant species (interspecific combinations). Interestingly, in green orchids cost–benefit relationships appear to change over a plant’s life cycle. Net fungus to plant carbon transfer supports seedling establishment of the tiny non-photosynthetic orchid protocorms in the early growth phases while adult orchids ‘repay’ the carbon to their mycorrhizal associates when they are older and larger (Cameron et al. 2008).

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
Plant speciesSeedlingsLarger plantsReferenceSummary
NMMMycorrhizal dependencyNMMMycorrhizal dependency
  1. *The biomass of seedlings grown with or without mycorrhizal fungal networks was estimated from graphs.

  2. Seedlings were grown in treatments inoculated with different mycorrhizal fungi. The average seedling response of all mycorrhizal fungal treatments was taken.

Sorghum vulgare632a736b14.91600236432.3Ocampo 1986(+; +)
Festuca ovina24.122.0−8.8922609−51.4Grime et al. 1987(−; −)
Plantago lanceolata18.128.336.019801430−38.5Eissenstat & Newman 1990(0; 0)
Hypericum perforatum*1070800−25.21470272085.0Moora & Zobel 1998(−; +)
Sibbaldia procumbens*7812.5170018005.5Kytoviita, Vestberg & Tuom 2003(0; 0)
Gnaphalium norvegicum1.52.026.1978136928.6Pietikainen & Kytoviita 2007(0; +)
Bromus erectus8.31440.7105.692.1−14.7van der Heijden 2004(+; 0)
Plantago lanceolata227−68.2810223063.7Nakano-Hylander & Olsson 2007(−; +)
Trifolium subterraneum6040−33.3260181085.6Nakano-Hylander & Olsson 2007(−; +)

We have used a wide range of species and a wide range of study systems for this analysis. Hence, the experimental conditions (e.g. nutrient availability, soil type, light conditions, mycorrhizal fungal identity) were highly variable among the different studies and probably explain the variable results of the analysis. For instance, the seedling response of Plantago lanceolata was tested four times in three different studies (see Appendix S1): in two cases Plantago seedlings benefited greatly from the presence of mycorrhizal networks (Grime et al. 1987 & Francis & Read 1995) while in two cases seedling growth was clearly suppressed (Nakano-Hylander & Olsson 2007). The study by Grime et al. (1987) was performed under nutrient-poor conditions (as shown by poor overall plant productivity), whereas plant nutrient availability in the study by Nakano-Hylander & Olsson (2007) was much higher as evidenced by a higher plant biomass obtained in a shorter growth period. The effect of mycorrhizal fungi on plant growth is strongest at low soil fertility (e.g. Smith & Read 2008), perhaps explaining why the results of the studies by Grime et al. (1987) and Nakano-Hylander & Olsson (2007) contrasted so much.

We determined the average seedling response to mycorrhizal fungi in studies where several treatments with mycorrhizal fungi were compared (e.g. treatments with different mycorrhizal fungal species or communities). In some of these cases, the seedling response varied greatly depending on mycorrhizal treatment. For instance, Nara (2006a) inoculated Salix reinii plants with 11 different EM fungi plus a nonmycorrhizal control under glasshouse conditions. After 11 months of growth, these plants were then planted in the field to establish individual mycorrhizal networks, and the effect of these mycorrhizal networks on the growth of nearby seedlings was tested. A previous study had shown that this field lacked mycorrhizal inoculum for Salix (Nara & Hogetsu 2004). There was considerable variation in the effects of adult plants on nearby seedlings establishment. Mycorrhizal networks of most of the fungal species improved the growth and nutrient status of the seedlings over the control except Laccaria amythestina, where none of the variables were significantly different from the control. This study clearly shows that established plants can facilitate seedling establishment. However, it is unclear whether this is due to direct facilitative effects through mycorrhizal networks, or simply because established plants provide an inoculum source (mycorrhizal networks) for nearby seedlings. In this respect, it is important to mention that in some cases seedlings and adult plants are colonized by different mycorrhizal fungal communities (Aldrich Wolfe 2007), making it unclear to what extent resource sharing among seedlings and larger plants occurs. Overall, the studies discussed above show that the growth response of seedlings to mycorrhizal fungal networks is variable, depending on factors such as mycorrhizal identity, plant species identity, plant species combinations and nutrient availability (see above).

Seedling establishment is also strongly determined by the dominant mycorrhizal network in a community. For instance, Horton, Bruns & Parker (1999) showed that the diverse community of mycorrhizal fungi associated with Arctostaphylos supported Pseudotsuga menziesii seedling establishment, while mycorrhizal communities found near Adenostoma did not. Pseudotsuga menziesii, associates with EM fungi and the difference is probably explained by Arctostaphylos shrubs supporting well-developed EM networks whereas Adenostoma shrubs primarily associate with AM fungi. Similarly, Dickie, Koide & Steiner (2002) reported a positive seedling response when Quercus seedlings were planted near Quercus trees, but a negative response when planted near the arbuscular mycorrhizal Acer even though some EM colonization was observed on seedlings near Acer. Moreover, a recent study by Collier & Bidartondo (2009) showed that the invasion of EM pines into heathland (with ericoid mycorrhizal fungi) is limited due to the absence of EM fungi. The absence of suitable EM inoculum has also been shown to inhibit Pinaceae invasion into native Nothofagus communities in Isla Victoria (Nuñez, Horton & Simberloff 2009).

Is fungal support related to the relative dominance of a plant in the community

Many ecosystems are dominated by plants forming mycorrhizal associations (Read 1991). It is still unclear whether plants that dominate a specific plant community also obtain most benefit from mycorrhizal fungi. Studies performed so far gave conflicting results. Hartnett & Wilson (1999), studying tall grass prairie in North America, observed that the dominant C4 grasses obtained most benefit from mycorrhizal fungi. They suggested that mycorrhizal fungi reduced plant diversity in these communities by supporting the dominant plant. Similarly, it is proposed that in some tropical rainforests EM associations encourage dominance of certain tree species (Connell & Lowman 1989). Studies performed with European calcareous grassland provide opposite results. Both Grime et al. (1987) and van der Heijden et al. (1998) show that subordinate plant species benefited most when mycorrhizal fungi were present, while biomass of the dominant grass was not enhanced, or even reduced in presence of mycorrhizal fungi. As a consequence, mycorrhizal fungi enhanced plant diversity in these grassland communities. Note that, in the study by Grime et al. (1987), field roots were used as inoculum to establish a fungal network. It is possible that, beside mycorrhizal fungi, pathogenic fungi were also part of this fungal network. Hence, the negative effects of the fungal network on the growth of the dominant plant could also be due to pathogens. Overall, the studies mentioned above indicate that the ‘status’ and relative dominance of a plant in the community does not determine how much benefit it receives. The results appear to depend on the identity of the dominant plant and its relationship with mycorrhizal fungi. The observations by Grime et al. (1987) and van der Heijden et al. (1998) also imply that there are many factors that determine the dominance of plants in plant communities: in some cases mycorrhizal fungi are important, while in other cases other factors such as growth form, relative growth rate, competitive ability, resistance to stress or disturbance determine plant abundance.

Free access for everyone? Host specificity & physiology of mycorrhizal networks

Pot experiments with AM fungi isolated from field soil have shown that most AM fungal species can colonize most plant species used as bait plants. This lack of specificity is also reflected by the fact that some AM fungal species have a worldwide distribution, associating with a wide range of plant species in very different ecosystems (Opik et al. 2006). Despite this lack of specificity, a considerable number of studies showed that AM fungi have host preferences and that different plant species are colonized by different AM fungal communities (e.g. Vandenkoornhuyse et al. 2003; Opik et al. 2006). Still, in any given plant community that has been studied to date, it appears that some of the fungi form extensive networks connecting multiple plant species.

The specificity of EM fungi has received more attention than AM fungi because of the relative ease in finding sporocarps in the field and of culturing mycorrhizal seedlings in the laboratory. It was believed that EM fungi were more host specific than AM fungi. Many of the examples of EM fungi with narrow host ranges fall into the genera Suillus, Leccinum, Gomphidius, Chroogomphus, Brauniellula, and Gomphogaster (Molina, Massicotte & Trappe 1992), all in the Boletales. This suggests that the narrow host range of these genera is phylogenetically determined. There is always a risk of assigning specificity based on sporocarp appearance or pure culture synthesis experiments. Evidence from field-collected root tips from mixed EM plant communities suggests that most of the root tips recovered are colonized by fungi associating with multiple host species (Horton & Bruns 1998; Horton, Bruns & Parker 1999; Cullings et al. 2000; Kennedey, Izzo & Bruns 2003; Horton, Molina & Hood 2005; Dulmer 2006; Ishida, Nara & Hogetsu 2006; Lian et al. 2006; Nara 2006b). While there are some EM fungi that are relatively host specific, most appear to have intermediate to broad host ranges and can form networks with multiple plant species in a mixed stand (Molina, Massicotte & Trappe 1992).

From the above, it follows that a considerable number of plant species from a specific community can be colonized by the same mycorrhizal fungus and are, thus, connected to the same network. Important questions that follow are: which plants maintain this network, which plants receive benefit and how is this physiologically organised? There are several scenarios (Fig. 3). One option is that carbon investment and plant benefit are tightly interlinked: the more a plant invests in the network, the more benefit it receives in return (Fig. 3a). Physiological studies which show that nutrient supply to the plant increases with enhanced carbohydrate availability for the fungus (Bucking & Shachar-Hill 2005) provide evidence for this scenario. Studies which show that co-occurring seedlings and adult plants obtain, per unit of biomass, the same relative benefit from mycorrhizal fungi (e.g. Kytoviita, Vestberg & Tuom 2003; Pietikainen & Kytoviita 2007) also indicate that costs (carbon investment) and benefit (stimulation of plant growth) are interlinked (Fig. 3a). Be aware that under this scenario larger plants obtain more resources in total, because they also invest more, but the relative benefit is the same. Several studies also show that plants which obtain large amounts of nutrients from mycorrhizal fungi also have larger hyphal networks. Hence, there is evidence that cost–benefit relationships of plants with mycorrhizal fungi are interlinked for a considerable number of plant species.

Figure 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).

Many plants can, at least partly, control colonization by mycorrhizal fungi under less beneficial conditions. At high phosphorus availability, root colonization levels and spore production by arbuscular mycorrhizal fungi are usually reduced (Oehl et al. 2003; but see Graham, Duncan & Eissenstat 1997). Ectomycorrhizal fungi are also less abundant and EM fungal communities are less diverse when nitrogen availability increases (Wallenda & Kottke 1998; Lilleskov et al. 2002), probably because plants suppress colonization (Nehls et al. 2007). Moreover, plants can repress mycorrhizal phosphorus uptake and down-regulate fungal phosphorus transporter genes at high phosphorus availability (e.g. Nagy et al. 2009) when the fungus is not required for nutrient uptake. On the other hand, plants exude signals to attract mycorrhizal fungi under nutrient deficiency (Yoneyama et al. 2007). This suggests that plants have mechanisms to regulate their investment in mycorrhizal fungi, providing additional evidence that investment costs and benefits are interlinked. When discussing this, it is important to remember that mycorrhizal fungi are independent from plants, aiming to enhance their own fitness. Hence, the fungi may resist plants when these try to sanction them under unfavourable conditions.

It is also possible that the relationship between carbon investment and plant benefit is positive, but with a different angle for different plant species or different plant individuals (Fig. 3a). This could explain why, in some cases, seedlings benefit more from a connection to the mycorrhizal network compared with adult plants (see above). It also explains why the outcome of competition between two mycorrhizal plant species is often not balanced (e.g. Finlay 1989; Perry et al. 1989; Marler et al., 2004;Scheublin, Van Logtestijn & Van der Heijden 2007).

The second option is that there is no relationship between carbon investment and plant benefit (Fig. 3b). Every plant individual has a different relationship, thus resulting in a large scatter of points (Fig. 3b). This has similarities to the so-called idiosyncratic relationship between biodiversity and ecosystem functioning (Johnson et al. 1996) stating that the relationship is highly variable, depending on factors such as soil type, nutrient availability and plant species identity. This scenario would mean that some plant individuals obtain much more benefit from a mycorrhizal network per unit carbon they invest, compared with other plants that receive relatively less benefit per unit invested carbon. The relationship could also differ with different mycorrhizal fungal species or for different growth stages of one plant species (e.g. the relative benefit of seedlings is much higher compared with adult plants, as shown for a few plant species in our analysis).

Plant–mycorrhizal network interactions are very hard to explore in the field because most plants are colonized by multiple fungal species (networks), each with its own cost–benefit interaction. In addition, some plant species might, on average, benefit more from mycorrhizal networks compared with other plant species. For instance, several studies showed that mycorrhizal fungi reduce biomass of Festuca ovina when this grass is coexisting or competing with other plant species (Grime et al. 1987; van der Heijden et al. 1998; Scheublin, Van Logtestijn & Van der Heijden 2007). The study by Grime et al. (1987) indicated that there is carbon transfer from Festuca ovina to other plant species through common mycorrhizal fungal networks. The significance of this carbon transfer is still under debate. However, the fact that carbon from Festuca was found in the roots of other mycorrhizal plant species, and not in non-mycorrhizal plants, suggests that Festuca was at least supplying carbon to the hyphal network in this study and that other plants benefited from the hyphal network. The outcome of our analysis, which shows that effects of mycorrhizal networks on seedling establishment can be positive, neutral and negative, fits to the scenario shown in Fig. 3b.

It has been proposed that the symbiosis between plants and mycorrhizal fungi is based on the exchange of luxury goods (Kiers & van der Heijden 2006). At low soil fertility, plant growth is limited more by nutrients than by carbon supply, and carbohydrates accumulate in plant organs (e.g. Poorter & de Jong 1999; Korner 2003). Under these conditions, it is advantageous for the plant to allocate assimilates to the fungi because, by doing so, plants acquire more of the resources they need, without additional costs. The investment of a luxury good (carbon) in mycorrhizal fungi by some plants, and the co-use of mycorrhizal networks by other plants could explain the variable responses. However, this scenario would only work if the plant investing a luxury good is not negatively affected (e.g. by enhanced competitive ability of other plants) and obtains at least a benefit at some point in its life cycle (e.g. during seedling establishment).

A third option is that there is a negative relationship between investment and benefit (Fig. 3c). This implies that some plant species invest in mycorrhizal networks while others obtain benefit from them. Generally, this relationship is unlikely, because plants would select against mycorrhizal colonization if other plants always benefited more and if this resulted in a reduced competitive ability (but see negative feedback model in Bever, Westover & Antonovics (1997). This relationship does fit mycoheterotrophic plants, which lack chlorophyll and indirectly parasitize other plants by obtaining carbon and nutrients from mycorrhizal networks. These plants (also called epiparasites) obtain benefit from mycorrhizal networks of a single fungal species, while the surrounding vegetation maintains the mycorrhizal network. There are about 400 species in the world with this strategy, distributed in eleven families including the Orchidacea and Ericaceae, and all of them lack chlorophyll (Leake 1994; Taylor et al. 2002). Recent studies indicate that some other plants of these families have a mixed strategy and acquire carbon both through photosynthesis and via hyphal links (Julou et al. 2005; Girlanda et al. 2006; Tedersoo et al. 2007; but see Hynson et al. 2009). It is still unclear whether these plants also invest in mycorrhizal networks (but see Bidartondo et al. 2000). Experimental studies are required to test this in more detail.

Socialism or capitalism in soil?

It is tempting to compare mycorrhizal networks with socialist systems, where all individuals have equal opportunities and where wealth and power are distributed more evenly. On the contrary, a capitalist mycorrhizal network would be privately controlled for profit by the plant or plants establishing the network. Our analysis provides both examples of ‘socialist’ and ‘capitalist’ tendencies of mycorrhizal networks. In several cases small seedlings obtained more benefit (in terms of biomass gain) compared with the larger plants that established the mycorrhizal networks (e.g. Eissenstat & Newman 1990; van der Heijden 2004), pointing to socialist tendencies. However, in all studies performed so far, the actual investments (in terms of carbon/energy input into the network) by small and large plants were not determined and there is no empirical evidence that resources are preferentially allocated to small seedlings. It is not unlikely that in many cases the larger plants facilitated establishment of the small seedlings by (i) providing improved mycorrhizal inoculum potential and (ii) reducing the carbon cost of establishing a functioning mycorrhizal network around the seedlings’ roots. However, there are also several examples which show that small seedlings receive proportionally the same or even less benefit from networks as larger plants (Table 1). In terms of total biomass gains then, the larger plants thus benefit more from mycorrhizal networks, pointing to capitalist tendencies.

Mycorrhizal networks can also be viewed as part of ‘superorganisms’ (sensuClements 1936), with the fungal species in the network being redundant physical extensions of the roots that translocate nutrients freely between plants. However, each fungal species has its own niche and mycorrhizal fungi differ in many ways including growth rate (Olsson, Jakobsen & Wallander 2002), soil type preference, resistance to stress and disturbance (Oehl et al. 2003), ability to acquire nutrients (Jakobsen, Smith & Smith 2002), ability to solubilise nutrients from organic matter and plant host range (Molina, Massicotte & Trappe 1992). Moreover, mycorrhizal fungi have evolved mechanisms for recognizing and preventing fusion of non self tissue. For instance, in AM fungi, hyphal fusions have only been observed between individuals of the same genotype while fusion between individuals of different genotypes, species or families do not occur (Giovannetti, Azzonlini & Citernesi 1999; but see Croll et al. 2009). Soils are, thus, colonized by several independent networks simultaneously competing for nutrients and roots. Moreover, in many cases mycorrhizal plants acquire nutrients not directly from the soil in competition with other plants, but from their fungal networks. A fungus may compete with other fungi for soil nutrients, and then deliver those nutrients to the various plants it colonizes. The distribution of the nutrients to plants in a network are then a function of variations in compatibility between a fungal individual and its colonized plant hosts, and variation in carbon flow to the fungus among the plants.

Mycorrhizal networks and plant–plant interactions

The role of mycorrhizal networks in regulating plant–plant interactions and plant community dynamics is still poorly understood. From our analysis it follows that seedlings of several plant species benefit from the presence of mycorrhizal networks. The effect of mycorrhizal networks on interactions between already established plants is still poorly understood. In particular it is unclear if there are plant species that maintain mycorrhizal networks through carbon supply while there are other species that benefit by acquiring nutrients present in the network (other than the obvious examples of mycoheterotrophic plants). Physiological studies such as those by Voets et al. (2008), performed under sterile in vitro conditions are necessary to investigate this in detail. Plant competition experiments show that not all plant species receive equal benefit from mycorrhizal networks (e.g. Finlay 1989; Perry et al. 1989; Scheublin, Van Logtestijn & Van der Heijden 2007). For instance, several studies showed that Festuca ovina can benefit from mycorrhizal fungi when grown alone but, in competition, its competitive ability is reduced compared with other plants (van der Heijden et al. 1998; Scheublin, Van Logtestijn & Van der Heijden 2007). This indicates that the cost–benefit ratio of plants connected to a mycorrhizal network is not the same for each plant species. Microcosm studies have also shown that AM fungi alter plant diversity and plant community structure (Grime et al. 1987; van der Heijden et al. 1998; Hartnett & Wilson 1999) because different plant species receive different amounts of benefit from mycorrhizal network. Moreover, the composition and number of mycorrhizal fungi present in plant communities is also important in determining plant productivity and plant diversity (van der Heijden et al. 1998; Klironomos et al. 2000; Vogelsang, Reynolds & Bever 2006). Studies with microcosms are of particular interest because the plants are coexisting and plants can be colonized by the same fungi.

In communities with several mycorrhizal fungi (most EM communities have tens of species), different plant species can be colonized by different mycorrhizal fungi and it is even possible that guilds of plants exist interconnected by the same mycorrhizal networks (although no proof for this has been obtained). Molecular techniques that detect specific mycorrhizal fungi, could test whether this is actually happening. Moreover, different mycorrhizal networks are likely to coexist in mixed forests where trees associate both with AM and EM fungi, or in EM forests with an understorey of AM herbs (Newman & Redell 1988). Some mycorrhizal fungi can also form functional associations with plants with different mycorrhizal types as was recently shown for the fungus Piceirhiza bicolorata (Grelet et al. 2009).

Carbon and mineral nutrient transfer through mycorrhizal networks

One important consequence of mycorrhizal networks is that nutrients, carbon and water can be transferred from one plant to another. The significance of interplant carbon & nutrient transfer has been widely debated (see reviews by Simard, Durall & Jones 2002 & Selosse et al. 2006). Selosse et al. (2006) estimated that up to 40% of plant nitrogen in receiver plants can be derived from donor plants (e.g. nitrogen fixing plants) and be transferred through mycorrhizal networks. In most situations this proportion is probably much lower, as nitrogen is usually limiting plant productivity, making it unlikely that plants give it away for ‘free’. Moreover, nitrogen fixation by nitrogen fixing plants is energetically expensive, implying that direct transfer from a nitrogen fixer to a non-nitrogen fixer is probably low. The significance of interplant carbon transfer has been unequivocally shown in mycoheterotrophic plants which parasitize on mycorrhizal networks from which they obtain carbon and nutrients (see above). In addition, evidence for carbon movement between green plants comes from Simard et al. (1997) and Lerat et al. (2002). There is debate about the ecological significance of C transfer between plants via mycorrhizal networks (Robinson & Fitter 1999). Graves et al. (1997) and Wu, Nara & Hogetsu (2001) have shown that C fixed by one plant and transferred to another remains in the root system, and presumably the hyphae, of the second plant. However, C must move out of the root system in mycoheterotrophs and the studies by Simard and Lerat suggest this can happen in green plants as well. What is not clear in these studies is the source of the carbon translocated from the fungi. It is likely that some of the C atoms are part of amino acids such as glutamine or glutamate that are transferred as N sources to the plants from the fungi. How these amino acids influence the energy budget of these plants, especially those that cannot fix their own carbon, remains to be determined.

Ecological function of mycorrhizal fungal networks

Mycorrhizal fungal networks provide a wide range of services to plants and ecosystems (Table 2). The most important one is probably nutrient uptake, followed by seedling support (see analysis). Other functions, such as the prevention of nutrient leaching, internal cycling of nutrients (e.g. transfer of nutrient from dying roots and leaf litter) and their ability to facilitate bacterial dispersion, have been largely overlooked (Table 2). Moreover, the fact that seedlings in perennial plant communities become quickly colonized by mycorrhizal fungi (e.g. within 3–6 days after seedling emergence (Read, Koucheki & Hodgson 1976; Birch 1986) is probably very important because small seedlings then have immediate access to a cheap ‘nutrient adsorption machine’ provided and maintained by the surrounding vegetation (Newman 1988). Plant growth in many communities (e.g. grassland or savanna) is limited by nutrient 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 to maintain their own small part of the fungal network. However, the function of hyphal networks is less clear in ecosystems where light availability is the main limiting factor for seedling establishment. For instance, enhanced mycorrhizal colonization did not improve seedling survival in a tropical forest (Gehring & Connell 2006). Work by Simard et al. (1997) showed that tree seedlings in forest obtain carbon from mycorrhizal networks. This may enhance seedling survival, although experimental evidence for this is still unclear.

Table 2.   Ecological functions and significance of mycorrhizal fungal networks and of the presence of mycorrhizal fungi
FunctionEcological significanceReferences
  1. *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 phosphorus year−1 hectare−1 are lost in this way (Herzog et al. 2008; Sims, Simard & Joern 1998). The prevention of nutrient leaching is especially 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).

  2. †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).

  3. ‡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 indicate that mycorrhizal fungal hyphae are not very palatable and do not belong to the diet of collembola, abundant soil arthropods (Gange 2000).

Direct effects of mycorrhizal networks
 Facilitation of seedling establishmentLow to very highSee literature analysis in this paper
 Rapid colonization of seedlingsVery highRead, Koucheki & Hodgson 1976
 Increased mycorrhizal inoculum potential of soil around established plantsHighNewman 1988; Dickie et al. 2005; Dickie & Reich 2005; Nara 2006b; Nuñez, Horton & Simberloff
 Reduced seedling costs of establishing mycorrhizal associationsHighNewman 1988
 Prevention of nutrient leachingHigh*van der Heijden 2009
 Transfer of nutrients from dying rootsHighRitz & Newman 1985;Mikkelsen, Rosendahl & Jakobsen 2008
 Transport of substances between plants
  transfer of carbonProbably lowSimard et al. 1997; Robinson & Fitter 1999; Lerat et al. 2002
  transfer of phosphorusProbably lowSimard, Durall & Jones 2002; Selosse et al. 2006
  transfer of nitrogenStill unclearHe et al. 2005; Selosse et al. 2006;
  transfer of waterUnknown 
  transfer of plant signalsUnknown 
 Changes in fungal community composition and abundance (including plant–soil feedback)HighBever, Westover & Antonovics 1997; Collier & Bidartondo 2009; Hubert & Gehring 2008
Ecological functions of the presence of mycorrhizal fungi
 Nutrient uptakeVery highSummarized in van der Heijden, Bardgett & van Straalen 2008
 Decomposition of litterHighLindahl et al. 2007
 Improvement of soil structure by enmeshing soil aggregates in stable structuresHighRillig & Mummey 2006
 Carbon transfer to soilsHigh† 
 Water uptake and hypdraulic liftVariableAuge 2001; Egerton-Warburton, Querejeta & Allen 2007
 Hyphal highways for bacterial dispersionVery low for plantsPerotto & Bonfante 1997; Kohlmeier et al. 2005
 Food for other organismsLow for plants‡Gange 2000

The importance of mycorrhizal networks for seedling establishment has been known for some time and this is now also being applied in forestry and agriculture. Moreover, a management practice in agriculture that is receiving increased attention is conservation tillage (Holland 2004). Conservation tillage minimises the disruption of the soil structure, promotes soil biodiversity and reduces soil erosion and drought stress. Several studies reported that mycorrhizal networks increase in abundance under conservation tillage (e.g. Jansa et al. 2003). It is likely, although not proven, that the positive effects of conservation tillage are, at least in part, mediated by mycorrhizal networks.

Conclusions and outlook

In this review, we have shown that mycorrhizal fungal networks play a key role in natural ecosystems. Mycorrhizal fungi can facilitate seedling establishment and plant growth by acquiring limiting nutrients. Many plants benefit from fungal support, but there are also a considerable number of cases where there is no, or even a negative effect of mycorrhizal fungi. The results presented in our analysis clearly reflect this as we observed significant growth stimulation of small seedlings by mycorrhizal fungal networks in only 48% of cases, while negative effects occurred in 25% of the cases. Mycorrhizal fungal networks have the ability to support co-occurring 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 supported by bigger plants in the community. However, whether this is actually occurring is highly context dependent, and varies with study system (e.g. plant species identity, fungal identity, nutrient availability). Beside effects on plant growth, we identified a number of other important ecological functions of mycorrhizal networks in soil. These include recycling of nutrients, prevention of nutrient losses, contribution to soil structure, food for other organisms, and mycorrhizal fungal networks acting as hyphal highways for bacterial dispersion.

For a better understanding of the impact of mycorrhizal fungal networks on seedling growth and ecosystem functioning, several key questions need to be answered. First, cost–benefit relationships of individual plants connected to mycorrhizal networks are still poorly understood. It is unclear which plants invest, and how this is related to the amount of benefit received. The fact that most (if not all) physiological studies are performed with single plants, grown in highly simplified study systems, without hyphal interconnections to other plants, does not contribute to a better understanding of process occurring in mycorrhizal networks. The use of dual labelling (with 13C; 14C, 15N 33P) as performed by some investigators is important. Second, we have shown here that mycorrhizal networks are important for seedling establishment in several cases. However, in order to draw more precise conclusions, additional studies are required (e.g. studies with EM fungal networks showed positive effects in 75% of the cases. However, this conclusion is based on seven independent studies). Furthermore, as far as we know, there are no studies which tested whether hyphal networks formed by plants with ericoid or orchid mycorrhizas promote seedling establishment of nearby plants. Third, the contribution of mycorrhizal networks to nutrient uptake by plants and nutrient cycling in natural ecosystems is still poorly understood and mainly based on experiments performed in the laboratory (but see Hobbie & Hobbie 2006). Fourth, there are many other factors that facilitate seedling establishment and plant growth as discussed in this issue of the Journal of Ecology. The relevance of mycorrhizal networks compared with these other factors is often poorly understood. Fifth, most studies have been performed with mycorrhizal fungi that can be easily cultured. However, molecular techniques have shown that in the case of AM fungi, 60% of environmental sequences do not match with AM fungi that have been brought into culture (van der Heijden, Bardgett & van Straalen 2008). Hence, it will be extremely important to cultivate these fungi and assess their ecological relevance. Sixth, the spatial distribution and movement of nutrients in mycorrhizal networks is still poorly understood. Finally, our climate is changing and periods of drought or heavy rainfall are expected to increase in many countries. It is important to understand how these changes influence the stability of mycorrhizal networks and their ability in facilitating plant growth.

Acknowledgements

We would like to thank Erik Lilleskov and Mari Moora for discussion and providing data. Toby Kiers and David Read commented on a very early version of this paper. We thank the editor and the two referees for helpful and constructive comments. Financial support was provided to M.G.A.V.D.H by the Swiss Federal Government and the Swiss National Science Foundation award 31003A_125428 and to T.R.H by the National Science Foundation award DEB-0614381, the Mianus River Gorge Preserve, and the USDA Forest Service.

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