Which of the following statements best describes the symbiotic relationship of mycorrhizae?

Abstract

Mycorrhizal fungi account for about 10% of identified fungal species, including essentially all of the Glomeromycota and substantial fractions of the Ascomycota and Basidiomycota. Several distinct types of mycorrhizal associations exist, including arbuscular, ericoid, orchid and ectomycorrhiza. Although arbuscular mycorrhiza evolved first, ectomycorrhizal and orchid mycorrhizal fungi are the most speciose types, and each of these types arose from multiple independent evolutionary events, followed by convergent evolution. Coevolution between mycorrhizal fungi and plants has played a key role in fungal diversification, but fungal diversification generally has not paralleled plant diversification, and relatively few fungi show strict host specificity.

4.3 MYCORRHIZAS AS NUTRITIONAL MUTUALISMS

Except for orchid and monotropoid associations, mycorrhizas involve plant exchange of photosynthates in return for fungal exchange of mineral nutrients. The convergence of so many unrelated forms of mycorrhizas is a testament for the mutual benefits of these trading partnerships. To understand the dynamics of resource exchange in mycorrhizas, we must examine the mechanisms by which resources are acquired by both partners. Mycorrhizal fungi improve nutrient uptake for plants, in part, by exploring the soil more efficiently than plant roots. Mycorrhizal fungal hyphae occupy large volumes of soil, extending far beyond the nutrient depletion zone that develops around roots. Simard et al. (2002) estimated that, on average, the external hyphae of EM fungi produce a 60-fold increase in surface area. The small diameter of fungal hyphae allows them to extract nutrients from soil pore spaces too small for plant roots to exploit (van Breemen et al. 2000). Recent studies on phosphate and ammonium uptake also reveal that mycorrhizal fungi improve uptake kinetics through reductions in Km and increases in Vmax (van Tichelen and Colpaert 2000).

Most mycorrhizal fungi depend heavily on plant photosynthate to meet their energy requirements; AM fungi are obligate biotrophs while EM and ericoid fungi are biotrophs with some saprotrophic abilities. The carbon cost of mycorrhizas is difficult to accurately estimate, but field and laboratory studies suggest that plants allocate 10–20 percent of net primary production to their fungal associates (Smith and Read 1997). Root colonization by mycorrhizal fungi often increases rates of host plant photosynthesis. This effect has been attributed to mycorrhizal enhancement of plant nutritional status in some systems (Black et al. 2000) and a greater assimilate sink in other systems (Dosskey et al. 1990).

Mycorrhizal fungi are a significant carbon sink for their host plants, and if nutrient uptake benefits do not outweigh these carbon costs, then both plant and fungal growth can be depressed (Peng et al. 1993; Colpaert et al. 1996). Mycorrhizal biomass has been shown to both increase and decrease with increasing availability of soil nitrogen (Wallenda and Kottke 1998; Johnson et al. 2003a). Treseder and Allen (2002) proposed a conceptual model to account for this apparent contradiction (Figure 4.2a). The model is based on three premises:

Both plants and mycorrhizal fungi have minimum N and P requirements and plants have a higher total requirement for these nutrients than fungi.

Biomass of mycorrhizal fungi is limited by the availability of plant carbon allocated belowground.

Plants allocate less photosynthate belowground when they are not limited by nitrogen and phosphorus; thus, mycorrhizal growth decreases when availability of these nutrients is high.

At very low soil nitrogen and phosphorus availability, both plants and mycorrhizal fungi are nutrient limited, so enrichment of these resources will increase mycorrhizal growth. At very high nitrogen and phosphorus availability, neither plants nor fungi are limited by these elements; consequently mycorrhizal biomass is reduced as plants allocate relatively less photosynthate belowground and more aboveground to shoots (shaded area in Figure 4.2a). This model is useful because it provides a simple heuristic framework for understanding how the relative availability of below- (minerals) and aboveground (photosynthate) resources control mycorrhizal biomass. Considering the interplay between nitrogen and phosphorus availability may further enhance the predictive value of this model. Because mycorrhizal fungi generally acquire phosphorus more readily than their host plants, we predict that the mutualistic value of mycorrhizal associations to plants will be highest at high soil N:P ratios and diminish as N:P ratios decrease.

Two lines of evidence suggest that mycorrhizal plants have evolved mechanisms to actively balance photosynthate costs with mineral nutrient benefits. First, environmental factors that reduce photosynthetic rates, such as low light intensity, lead to reductions in mycorrhizal development (e.g., Gehring 2003). Secondly, plant allocation to root structures is sensitive to mycorrhizal benefits. This is observed at both a gross taxonomic level and within ecotypes of the same plant species. Plant taxa with coarse root systems (low surface area) are generally more dependent upon mycorrhizas than those with fibrous root systems (high surface area). This suggests that for highly mycotrophic plant taxa, it is more adaptive to provide a fungal partner with photosynthates than to maintain fibrous root systems (Newsham et al. 1995). Also, it appears that mycotrophic plants have evolved a certain degree of plasticity in their allocation to roots in response to their mycorrhizal status. Mycorrhizal plants often have reduced root:shoot ratios compared to non-mycorrhizal plants of the same species grown under identical conditions (Mosse 1973; Colpaert et al. 1996; Figure 4.1).

There is evidence that local ecotypes of plants and mycorrhizal fungi co-adapt to each other and to their local soil environment (Figure 4.3a). A comparison of Andropogon gerardii ecotypes from phosphorus-rich and phosphorus-poor prairies show that each ecotype grew best in the soil of its origin. Furthermore, the A. gerardii ecotype from the phosphorus-poor soil was three times more responsive to mycorrhizal colonization and had a significantly coarser root system than the ecotype from the phosphorus-rich soil (Schultz et al. 2001). These results suggest that the genetic composition of plant populations evolve so that mycorrhizal costs are minimized and benefits are maximized within the local soil fertility conditions.

Mycorrhizae

Mycorrhizal fungi are strong carbohydrate sinks, using large amounts of carbohydrates for metabolism and growth of the fungal biomass. The strong sink strength of mycorrhizal fungi is related largely to high respiration rates associated with their large amounts of cytoplasm and mitochondria as well as very active enzyme systems (Barnard and Jorgensen, 1977; Smith and Gianinazzi-Pearson, 1988).

The strong sink strength of mycorrhizae is shown by rapid basipetal translocation of 14C-photosynthate to the cortex, Hartig net, and mantle of mycorrhizal hyphae surrounding the roots (Cox et al., 1975; Bauer et al., 1991). Whereas shoots of nonmycorrhizal red pine plants exported only 5% of their photosynthate to the roots, those of mycorrhizal plants exported 54% (Nelson, 1964). It has been estimated that 6 to 10% more photosynthate is used by mycorrhizal roots than by nonmycorrhizal roots (Snellgrove et al., 1982; Koch and Johnson, 1984).

Mycorrhizae

Mycorrhizal fungi play a very important role in increasing mineral uptake from the soil (see Harley and Smith, 1983, for review). Kramer and Wilbur (1949) showed that larger amounts of radioactive P were accumulated by mycorrhizal pine roots than by nonmycorrhizal roots. Melin and co-workers demonstrated that mycorrhizal fungi transferred P, N, Ca, and Na from the substrate to tree roots (Melin and Nilsson, 1950a,b; Melin et al., 1958).

The rate of absorption of mineral nutrients is determined by nutrient transfer in the soil, the extent of the root system, and the absorbing capacity of roots. Contact between root surfaces and soil nutrients is necessary for absorption. The contact can be the result of root growth to where the nutrients are located or transport of nutrients to the root surface. The absorption of nutrients by roots varies with plant species and genotype as well as with environmental conditions.

Both inoculation of red pine seedlings with Hebeloma arenosa and amendment of soil with P influenced seedling growth. In P-unamended soil, the inoculated plants formed abundant mycorrhizae and, after 19 weeks, had 12 times the root dry weight and 8 times the shoot dry weight of nonmycorrhizal seedlings (MacFall et al., 1991). In another study, mycorrhizal red pine seedlings grown in P-unamended soil had higher root and shoot P concentrations than did nonmycorrhizal seedlings growing in similarly unfertilized soil, but the concentrations were lower than for either mycorrhizal or nonmycorrhizal seedlings grown in P-amended soil (Fig. 10.12). Hence, even though the mycorrhizae increased both the P concentration of seedlings and seedling dry weights when grown in P-unamended soil, the amount of available P in the soil was too low for the seedlings to achieve their full growth potential (MacFall et al., 1992).

The increased mineral uptake by roots of plants with mycorrhizae is traceable largely to their extensive absorbing surface. The fungal hyphae often extend into the portion of the soil that is not penetrated by roots or root hairs. Often the hyphae enter spaces between soil particles that are too small to be invaded by roots. Bowen and Theodorou (1967) estimated that the volume of soil exploited by a mycorrhizal root may be as much as 10 times greater than that exploited by a nonmycorrhizal root. Increased efficiency of mineral uptake by mycorrhizal roots also may be associated with reduction in air gaps between soil particles and plant roots because of decreased shrinkage of mycorrhizal roots, a low-resistance pathway of the fungus for movement of ions throughout the root cortex, and increased root growth. The greater rooting intensity associated with mycorrhizal infection increases absorption of immobile nutrients such as P much more than that of highly mobile nutrients (Bowen, 1984). Mycorrhizal fungi also may increase nutrient availability by hydrolyzing certain nutrients in the soil. For example, surface acid phosphatases in mycorrhizae may hydrolyze organic and inorganic forms of phosphate (Reid, 1984).

In addition to affecting establishment and growth of individual trees, mycorrhizae often influence the structure of entire ecosystems by at least three mechanisms (Perry et al., 1987): (1) enabling trees to compete with grasses and herbs for resources, (2) decreasing competition among plants and increasing productivity of species mixtures, especially those on infertile sites, and (3) increasing interplant transfers of compounds essential for growth of higher plants. The hyphae of the external mycelium can initiate mycorrhizal infections within and between species. In this way a persistent network of hyphal interconnections is established among plants within an ecosystem. The mycelial strands comprise a network of direct pathways through which some minerals, water, and carbohydrates can move in channels that are functionally analogous to xylem and phloem (see also Chapter 12) (Taber and Taber, 1984; Francis and Read, 1984; Read et al., 1985). Griffiths et al. (1991) reported that the ectomycorrhizal fungi Gautieria monticola and Hysterangium setchellii formed dense hyphal mats in Douglas fir stands. All seedlings under the canopy of a 60- to 75-year-old stand were associated with mats formed by ectomycorrhizal fungi. The mats apparently acted as nurseries for seedlings by providing them with carbohydrates and suppressing infection by pathogens. Because Douglas fir is a relatively shade-intolerant species, it appeared unlikely that a seedling could support the mass of hyphae with which it was associated. Hence the mycorrhizal fungi probably were a conduit for carbohydrate transport from the overstory trees to the shaded seedlings. According to Newman (1988), mycorrhizal links between plants alter growth primarily by modifying competition for nutrients and nutrient cycling rather than by replacing them.

Mycorrhizas in Arbutus and Arctostaphylos

The fungi mycorrhizal with Arbutus and other plants in the Arbutoideae were long believed to be basidiomycetes because of the structural similarities between ECM and arbutoid mycorrhizas. This has been confirmed both by synthesis experiments and by the descriptions of dolipore septa in fungi associated with mycorrhizas of Arctostaphylos (Duddridge, 1980; Scannerini and Bonfante-Fasolo, 1983; Read, 1983). The work of Zak (1973, 1974, 1976a, 1976b) who both traced mycelium and performed synthesis experiments, showed that mycorrhizas in Arbutus menziesii and Arctostaphylos uva-ursi are formed by fungi which also form ectomycorrhizas. The fungi involved included Hebeloma crustuliniforme, Laccaria laccata, Lactarius sangufluus, Poria terrestris var. subluteus, Rhizopogon vinicolor, Pisolithus tinctorius, Poria terrestris, Thelephora terrestris, Piloderma bicolor and Cenococcum geophilum. Similarly, Molina and Trappe (1982a) tested the ability of 28 ECM fungi to form mycorrhizas with Arbutus menziesii and Arctostaphylos uva-ursi in pure culture. All but three produced arbutoid mycorrhizas with both species. The conclusion here must be that the plant plays an important part in regulating the development of mycorrhizas, with the consequence that different structures are produced in different taxa of plant.

There is no evidence which will allow comparison of function in arbutoid and ectomycorrhizas, but the assumption is that they operate similarly. The plants are all woody and photosynthetic and, since mycorrhizas are the common form of absorbing organ of members of the Arbutoideae, an important and ecologically significant group of species, the symbiosis must be assumed to be of selective advantage. This is even more likely because the sheath on the roots, as in ectomycorrhizas, may not only have a storage function, but also separates the plant from the soil. Hence, the fungus calls the tune in absorption by the short roots, and everything absorbed by them must pass through it. It seems extremely likely that the mycelium and rhizomorphs in soil are important in nutrient scavenging.

Massicotte et al. (1993) carried out a detailed analysis of the structure and histochemistry of arbutoid mycorrhizas, synthesized in growth pouches between Arbutus menziesii and the basidiomycetes Pisolithus tinctorius and Piloderma bicolor. The morphology of the mycorrhizas was strongly influenced by the identity of the fungal symbiont. In the case of plants colonized by P. tinctorius, repeated pinnate branching of first and second-order lateral roots produced a complex structure (Figure 7.5), similar to that originally described by Rivett (1924) in Arbutus unedo. This pattern of branching, which has been observed in associations between Arbutus spp. and a range of other fungi (Molina and Trappe, 1982a, 1982b; Giovannetti and Lioi, 1990), appears to arise from precocious initiation of individual lateral roots, rather than by dichotomy of the apical meristem of the root, as is typically seen in ectomycorrhizas of Pinus (Piché et al., 1982; see Chapter 6). Each of the rootlets colonized by P. tinctorius is ensheathed in a well-developed mantle, from the outer layer of which an extensive system of rhizomorphs develops. This is a feature previously recorded in associations between Arbutus and several other species ECM fungi (Zak, 1976b; Molina and Trappe, 1982b).

Mycorrhizas formed by P. bicolor, in contrast, were largely unbranched and had a thin or non-existent mantle, sparse surface hyphae being embedded in mucilage in a manner similar to that seen in ectendomycorrhizas formed in Pinus by Wilcoxina spp. (Piché et al., 1986; Scales and Peterson, 1991a).

A longitudinal section of the pinnately branched type of mycorrhiza formed by P. tinctorius (Figure 7.6) reveals a thick mantle, intercellular development of mycelium to produce a Hartig net and penetration of some epidermal cells by fungal hyphae which proliferate to form dense hyphal complexes (Massicotte et al., 1993). The combined presence of mantle, Hartig net and intracellular proliferation are diagnostic features of arbutoid mycorrhizas which can only be revealed by anatomical investigation. There are reports (e.g. Largent et al., 1980) that Arbutus spp. are ECM, but these are based only on superficial recognition of the presence of a mantle. Clearly, in the absence of more detailed structural analyses such reports must be regarded with suspicion.

It was observed by Rivett (1924) and subsequently confirmed (Fusconi and Bonfante-Fasolo, 1984; Münzenberger, 1991; Massicotte et al., 1993) that the Hartig net in Arbutus is of the para-epidermal kind typically found in ectomycorrhizas in the majority of angiosperms (Brundrett et al., 1990; Chapter 6). Massicotte et al. (1993) propose that deeper penetration may be prevented by deposition of suberin lamellae and a Casparian strip in radial walls of the outer tier of cortical cells, so forming an exodermis. The epidermal cell walls contain phenolic substances but no suberin and clearly do not inhibit fungal penetration. The physiological activity and potential storage role of the fungal tissue is indicated by the presence of glycogen rosettes and of polyphospate (polyP) (Ling Lee et al., 1975).

Common Mycorrhizal Networks

Mycelium of mycorrhizal fungi that can extend into the soil beyond the host root may colonise adjacent host plants. Separate individual plants may thus become linked into an underground mycorrhizal network – the so-called wood-wide web. Nutrient exchange can occur between plants of different species linked by a mycelial network where plant and fungal partners are compatible. Fungi that form mycelial cords have been found to redistribute significant amounts of nutrients between plants. In nature, some plant species regularly occur together in some habitats, prompting speculation that they might be mutually supportive in this way. In the north of Scotland, pine (Pinus) trees commonly grow with an understorey of cowberry, Vaccinium vitis-idaea. Molecular analysis identified a fungal ECM of pine roots as Meliniomyces, in the ascomycete Hymenoscyphus ericae clade, which also formed ERM with cowberry roots. The fungus formed mycelial connections between plants in microcosms, and was found to mediate reciprocal carbon and nitrogen nutrient exchange between pine and cowberry, indicating that Meliniomyces mycelium may also channel a mutualistic exchange of resources in the field. The ERM association presumably helps the partners acquire nitrogen form the peaty, N-poor soil, while the ECM-pine connection supplies the shaded cowberry with photosynthate from the sunlit pine canopy.

The physical extent of fungal webs in soil must, at least in part, depend on specificity between plant and fungus, and on genetic compatibility between fungi. Where all the plants are compatible with predominant mycorrhizal fungi, and the fungi themselves are compatible and capable of fusing with adjacent mycelia, a mycelial web encompassing many plants is theoretically possible. A community composed of different plant species may be connected via a single genetic type of mycelium provided that the fungus is sufficiently generalist in its plant specificity. There may, however, be greater specificity at sub-specific taxonomic levels than has been recognised. Interactions between mycorrhizal fungi and plants in communities have been investigated using network analysis to discern pattern in multiple interactions. Instead of conventional pair-wise analysis, network theory deals with patterns of multiple interactions, such as those between the whole fungal population of a habitat and the community of plants which potentially interact with them. The topology of interaction networks can predict previously undetected host specificity. ‘Nested’ network structures, where specialists interact with symbionts that also interact with generalists, are common in mutualistic associations. For example, when Glomeromycota sequences from 450 plants in 100 square metres of woodland were analysed, the pattern of interaction predicted the existence of both generalist and specialist AMF fungi. This had been expected from previous findings, for example, the fact that natural plant communities host a more diverse AMF population than agricultural monoculture. However, network analysis has the additional power of potentially identifying the interacting species via their sequences, providing a basis for in situ investigation of the taxa of interest.

Habitat factors can be as influential as phylogeny in the composition of mycorrhizal assemblages. An intriguing result was obtained in a network analysis of 430 orchid plants and their mycorrhizal fungi on the island of Reunion in the Indian Ocean. The orchids are either epiphytic, living in the branches of trees, or terrestrial, with roots in the soil. The fungi all belong to the basidiomycete anamorphic group Rhizoctonia. However, there was little phylogenetic overlap between fungal populations in terrestrial and epiphytic orchids. The two different fungal populations had apparently assembled from varied phylogenetic origins through shared ecology. The analysis suggested a difference in fungal niche adaptation. Both terrestrial and epiphytic plants utilise fungi to supplement the tiny reserves carried in their powder-like seeds, but the terrestrial orchids continue to employ fungi to acquire carbon resources from soil, and so it might be predicted that these would be selected for an additional set of attributes such as cellulolytic ability.

Common mycorrhizal networks pre-existing in a habitat can help newly-arrived plants to become established by nurturing their seedlings, providing photosynthate from established mature plants. For example, mycorrhizal networks play a key role in the gradual establishment of vegetation on the volcanic desert slopes of Mount Fuji. Here, the first vegetation consists of scattered clumps of willow, whose ectomycorrhiza, acquired from airborne fungal spores, then fosters the growth of other plants which are compatible with the mycorrhizal fungus. This ‘nurse’ function of common mycorrhizal networks is exploited in forestry to regenerate forest ecosystems by planting pre-colonised saplings which host suitable ECM fungi. For example, nursery plants of Arbutus menziesii, which hosts a wide range of mycorrhizal taxa that develop extramatrical networks into surrounding soil, is planted to help re-establish mixed evergreen forests in Oregon.

In mature woodland, the pattern of tree colonisation by ectomycorrhizal fungal individuals was mapped in relation to host trees of various sizes. Different fungal species, Rhizopogon vinicolor, and Rhizopogon vesiculosus, each formed 13–14 genets (see Chapter 4, p.100) within a 30 m × 30 m plot of Douglas fir (Picea abies) forest, each genet colonising up to 19 trees. Rhizopogon vesiculosus genets were larger and connected more trees than Rhizopogon vinicolor. Large trees provided dominant nodes in spatial networks, forming centres of mycelial systems which extended over an area of several metres, containing other trees of various ages which were also colonised.

Fungal connections in common mycorrhizal networks are dynamic and variable. The spatial extent and duration of connectivity can be expected to vary as hyphal connections are continually made and broken under the influence of physical changes and biotic interactions. Mapping the area of underground distribution of ECM fungi of several common species in woodland showed that the relative size of the area occupied by each species changes. Some, but not all, ECM fungal species are patchily distributed, and the size of patches differs between species and seasons.

Interactions with soil fauna and above- and below-ground herbivores

Interactions of mycorrhizal fungi with the vast diversity of animals that inhabit the soil has received rather limited attention, probably because of the enormous difficulties of studying the highly complex interactions, effects of which can only be detected by combining sensitive experimental design with careful data analysis. Pot experiments involving additions of the organisms under investigation risk being too simplistic, whereas field experiments utilizing biocides are difficult to interpret because of the lack of specificity of the chemicals applied to suppress different groups. Recent reviews have addressed some of these complexities in relation to herbivores (Gehring and Whitham, 2002) and soil invertebrates (Gange and Brown, 2002).

It is well established that soil animals, such as collembolans, mites and nematodes play very significant roles in nutrient turnover, due to their effects in fragmenting litter and grazing on decomposer organisms such as fungi and bacteria. The grazing may also stimulate growth and reproduction of the fungi (Lussenhop, 1992). Analysis of effects of below-ground grazing on ectomycorrhizas has concentrated on fungivory, because most of the youngest root tissue is enveloped in mycelium. Ek et al. (1994a) examined the effects of different densities of the collembolan Onychiurus armatus on ecotymycorrhizas of Pinus contorta formed by Paxillus involutus. Impacts of fungivory on nutrient uptake by the extramatrical mycelium were examined by placing cups, containing 15NH4 or phytin, to which the fungus alone had access, in the soil. Low densities of the collembolan induced greater development of ECM mycelium and increased uptake of and transfer of 15N to the plants. Mycelial growth was reduced only at high densities of O. armatus. Collembolan populations did not increase in ECM treatments compared with non-mycorrhizal ones, possibly suggesting that alternative, preferred, food sources were present. In another investigation, ECM birch and pine plants were exposed to either a naturally complex microfaunal assemblage or a highly simplified one. The complex animal assemblage reduced colonization after 57 weeks, but actually increased shoot growth and N and P uptake compared to the plants that had received the simple assemblage (Setala, 1995).

In the case of AM fungi, considerable emphasis has been placed on the possibility that the grazing fauna may damage the fungal networks and hence reduce their capacity to deliver nutrients to associated plants (Fitter and Garbaye, 1994). It was thought that such effects might partially explain the apparent lack of AM responses under field situations. McGonigle and Fitter (1988a) applied the broad-spectrum insecticide chlorfenvinphos to a semi-natural, species-rich grassland in northern Britain and monitored the response of a constituent grass of the plant assemblage, Holcus lanatus. In the presence of the insecticide, which reduced density of collembolans to one third of the original population, there was a large increase in P uptake by the grass and a significantly greater shoot biomass. Clearly, the lack of specificity of the insecticide makes interpretation of these responses difficult, but increases of P uptake per unit root length or area is hard to explain by any mechanism other than one involving increased AM function when insects were suppressed.

Pot experiments with collembolans have sometimes suggested that the insects damage AM mycelial networks and consequently reduce the potential for enhanced P delivery to the plants (Warnock et al., 1982). This finding was essentially confirmed by Finlay (1985) whose results did, however, indicate that the density of collembolans was important (as shown also for ectomycorrhizas). At low densities, AM responses were actually increased, possibly because increased nutrient mobilization was more important than mycelial damage. Increase in collembolan numbers did result in increased damage to AM hyphal networks of Glomus intraradices in an agar culture experiment (Klironomos and Ursic, 1998), but these authors also showed that AM fungal hyphae were not the preferred food source of Folsomia candida. This collembolan selectively grazed on Alternaria alternata or Trichoderma harzianum, in preference to G. intraradices and was more fecund when feeding on the conidial fungi, regardless of density. Using compartmented pots to separate roots from AM hyphae and collembolans, Larsen and Jakobsen (1996) again showed that F. candida probably did not graze on hyphae of G. caledonium or G. intraradices. Furthermore, at densities of the collembolan similar to those found in the field, there were no significant effects on the delivery of 32P to plants of Trifolium subterraneum via the mycorrhizal pathway. Later investigations have confirmed that experimental outcomes can be highly variable, emphasizing the complexities of the interactions and their underlying mechanisms (Harris and Boerner, 1990; Kaiser and Lussenhop, 1991; Gange, 2000; Lussenhop and BassiriRad, 2005). Lussenhop and BassiriRad (2005) again confirmed that hyphae of G. intraradices were a minor food source for F. candida, as only about 5% of gut contents were fungal hyphae and there were no effects of the collembolan on length density of the external mycelium. This work also showed that the greatest N uptake by seedlings of Fraxinus pennsylvanica was in AM plants with moderate collembolan numbers. The effects of collembolans in damaging AM fungal mycelium and hence reducing nutrient uptake may well have been given undue emphasis, but the interactions and their outcomes in realistic field situations deserve more consideration. Recently, Johnson et al. (2005) demonstrated in a natural grassland that the collembolan Protaphorura armata at natural densities decreased C flux through soil measured after pulse labelling the sward with 13CO2. Other data presented were strongly indicative of disruption of AM mycelium in soil by the collembolans.

Interactions between AM plants and the fungal-feeding nematode Aphelenchus avenae provide an interesting comparison with the work with collembolans (Bakhtiar et al., 2001). This organism is also fungivorous and AM fungi do appear to support its growth. Populations declined when A. avenae was inoculated onto non-mycorrhizal plants of T. subterraneum, but increased markedly when the plants were colonized by either G. coronatum or Gi. margarita, with final populations much higher with G. coronatum. Presence of the nematode decreased root colonization by both fungi to the same extent and decreased the percentage of spores with contents, markedly so for G. coronatum. It therefore appeared that G. coronatum was either more palatable or more accessible to the nematode. Despite this damage, mycorrhizal growth responses were increased at moderate nematode densities (Figure 16.13), again suggesting that increased hyphal turnover as a result of nematode grazing had beneficial effects that offset damage to the hyphae if nematode populations were not exceptionally high. Effects on the two fungi were again different, highlighting the diversity of interactions to be expected in complex soil environments.

Interactions between mycorrhizal fungi and above-ground herbivores are at least as complex as those with soil animals, but our knowledge is even more fragmentary. By surveying published literature, Gehring and Whitham (1994, 2002), have shown that both ECM and AM colonization is reduced by herbivory in about two-thirds of the investigations and either unaffected or very infrequently increased in the remainder. The predominance of negative effects has been attributed to a reduced capacity of the plants to support their fungal symbionts with organic C. The authors highlighted the facts that again most work has been carried out on AM plants and that investigations focused mainly on the extent of colonization and rarely explored outcomes in terms of functioning of the symbioses or consequences for community interactions.

Effects of mycorrhizal colonization on the herbivores has also been investigated, again with a predominance of AM investigations. In these, the generalist herbivores were more often negatively affected by AM colonization than the specialists, an effect attributed to the greater sensitivity of generalists to defensive compounds produced by their hosts and by the possibility that production of these compounds is likely to be enhanced in mycorrhizal plants.

E Additional Factors

Symbioses between mycorrhizal fungi and C4 species are nearly ubiquitous (Ingham and Molina, 1991; Rabatin and Stinner, 1991), and symbiosis between the roots of C4 plants and diazotrophic N2-fixing bacteria is very common, particularly in tropical and subtropical ecosystems (Marschner, 1995). These two mutualistic associations are important for plant acquisition of nutrients, especially P and N, and mycorrhizae may also improve plant water uptake (Ingham and Molina, 1991; Rabatin and Stinner, 1991; Marschner, 1995). Mycorrhizae and N2-fixing bacteria may, therefore, affect plant-herbivore relations by influencing plant nutrient and water status, which are known to play an important role in plant–herbivore interactions (Jones and Coleman, 1991; McNaughton, 1991b). The effects of these symbionts on plant-herbivore relations may be either positive or negative. For example, improved plant nutrient and water status resulting from these symbioses will most likely increase herbivory tolerance. However, these symbioses are known to be carbon-costly to the host plant and can decrease plant competitive ability when carbon resources are limiting (e.g., in low-light growth conditions, during drought, and following folivory) (Ingham and Molina, 1991). The high photosynthetic rates and WUE of C4 species may allow them to more readily pay the carbon costs of these and other mutualistic symbioses (e.g., endophytic fungi) in high-light, warm, and water-limited environments. However, recovery from folivory may be slowed if such symbioses are a severe carbon drain and if C4 species support a greater mass of symbiotic microbes than C3 species in a given habitat (e.g., mycorrhizae infection in C4 grasses of tallgrass prairie is greater than in C3 grasses; Hetrick et al., 1988).

As mentioned before, C4 species occur primarily in warm, high-light, and often osmotically stressful habitats of tropical-to-warm temperate latitudes. This necessarily means that the herbivores that can potentially feed on C4 plants are a subset of the herbivores that potentially inhabit the environments in which C4 plants are found. Clearly, this defines and limits the potential range of plant-herbivore relationships in these ecosystems. For example, these habitats may not be well-suited for small invertebrate herbivores with high surface/volume ratios, and hence high rates of water loss. Thus, the habitats in which C4 species occur might have less diverse invertebrate communities with larger-sized aboveground herbivores (e.g., grasshoppers), or a predominance of belowground grazers due to inhospitable aboveground climates. Also, vertebrate folivores may predominate in these C4 habitats.

In many temperate ecosystems, the growth of C4 species is largely restricted to the warmest part of the growing season. In contrast, competing C3 species are often dormant during this time, and are instead active during the cool seasons (Teeri and Stowe, 1976; Stowe and Teeri, 1978; Osmond et al., 1981; Monson, 1989; Ehleringer and Monson, 1993). The success of C4 relative to C3 species during the warm season is related not only to the higher temperature optima of photosynthesis common in C4 plants, but also to higher temperature optima for other nonphotosynthetic traits as well (e.g., belowground processes), which likely reflects the tropical and subtropical origins of C4 plants (Jones, 1985; Marschner, 1995). In temperate habitats containing a mix of C3 and C4 species, certain herbivores (e.g., large mammalian grazers) may have to rely on C4 foliage during the warm season, but have C3 foliage available to them during the remaining period of the year. If herbivores cannot use C4 leaves, then they have to either migrate to habitats wherein C3 species are active, restrict their foraging to those C3 species that are active during the warm season, or become dormant during the warm season.

Lastly, as pointed out earlier in this chapter and in other chapters of this volume, most C4 species are grasses and this fact alone has important implications for plant–herbivore interactions. Most grasses have both intercalary meristems and apical and axillary meristems that are not exposed to aboveground grazers; thus, C4 species are usually relatively tolerant of folivory because shoot meristems are not lost to grazing (Hyder, 1972).

Introduction

The widespread occurrence of mycorrhizal fungi of all types on crops and trees in natural ecosystems, together with effects on their mineral nutrition and growth, led to the early recognition that the different mycorrhizal symbioses might be manipulated to increase crop yields in different types of primary production systems. Most plants used in agriculture and horticulture, as well as some forest species, form arbuscular mycorrhizas (AM), but other mycorrhizal types are important in particular situations: ectomycorrhizas (ECM) for forest production and in reafforestation programmes, ericoid mycorrhizas (ERM) for fruit crops such as blueberries and orchid mycorrhizas for enhanced propagation particularly for conservation. As components of the soil biota, all mycorrhizal types are potentially important in restoration of sites degraded by mining or by forestry operations. In consequence, the effects of such disturbance on communities of mycorrhizal fungi and outcomes for productivity are receiving increasing attention. Furthermore, the multifaceted roles of mycorrhizas in soil aggregation and stabilization, in disease tolerance and in mobilizing forms of nutrients that are not directly available to roots (see Chapters 5, 9, 10 and 15) have attracted attention in the areas of biological farming and sustainable management of production systems. Techniques to enhance the yields of edible fruit bodies of ectomycorrhizal fungi, many of which command very high prices, are being actively pursued. This chapter will review selected examples of the application of arbuscular and ectomycorrhizas in managed environments and discuss possible avenues for future work.

36.2.5.2 Mutualists

These are mostly, mycorrhizal fungi, which are the best known, to grow in rhizosphere region and also inside plant roots. Arbusclar mycorrhizae are the most common, especially in agricultural plant associations. These fungi have arbuscles, growths formed inside the plant root that have many small projections into root cells, as well as their hyphae outside the root. This growth pattern increases the plant’s contact with the soil, improving access to water and nutrients, while their mass of hyphae protects roots from pests and pathogens. Mutualistic mycorrhizal fungi form a beneficial relationship with plants. Ingham et al. (2000) reported that “mycorrhizae” grow within the root cells and are commonly associated with grasses, row crops, vegetables, and shrubs. Some plant species like the Cruciferae family (e.g., cabbage, broccoli, mustard, and canola) and the Chenopodiaceae family (e.g., lambsquarters, spinach, beets, and oilseed radish) do not form mycorrhizae associations.