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In systems where nutrients are limiting, such as boreal and temperate forests, mycorrhizae play a particularly important role in mediating the nutrient cycling of the ecosystem. They are allowed this control because they are brokers of certain limiting resources, which they are adept at scavenging from the soil (Read, Leake, & Perez-moreno, 2004). All tree species form mutualistic associations with mycorrhizal fungi (Simard, 2009), and for a given tree species there are many fungal species with which it can form associations.
Mycorrhizae act as an extension of the root system into the bulk soil, increasing the absorbing length of roots (Chapin, Matson, & Mooney, 2002) and allowing a greater volume of soil to be exploited. The fungal hyphae can also bridge the zone of nutrient depletion that tends to form around roots, and enter soil pores that are too small for plant roots to access (Godbold, 2004). In exchange for the provision of nutrients, plants invest upwards of 30% of their carbon (C) in supporting mycorrhizal symbionts.
Underground networks of mycorrhizae can connect different plant individuals and even species within a forest (Simard, 2009; Simard et al., 2012). Carbon, nutrients, and water can be transferred among the individuals connected by a common mycorrhizal network according to source-sink gradients. These networks have been shown to facilitate plant species coexistence, regeneration after disturbances, and the persistence of seedlings growing in shaded areas. The presence of mycorrhizal networks not only impacts plant productivity and species composition, but also has great influence on the amount of carbon that is able to be stored in the soil. This review will discuss ways in which mycorrhizae influence the functioning of temperate and boreal ecosystems and how mycorrhizal presence serves to tighten the cycling of nutrients within nitrogen-limited ecosystems. It will conclude with a discussion of recent methodological advances used to study mycorrhizae and a few possible directions for future research.
Nutrient cycling in forest ecosystems is highly localized within the root zone of plants, and is driven by the release of nitrogen (N) and phosphorous (P) from organic sources such as amino acids, proteins, and leaf litter by enzymes secreted by microorganisms, including mycorrhizae (Schimel & Bennett, 2004). It was previously thought that the mineralization of nutrients from the organic polymer form was only done by free-living decomposers in the soil, but ectomycorrhizae have shown a widespread ability to carry out this function as well (Read & Perez-moreno, 2003). Indeed, ectomycorrhizae are critical for N recycling and acquisition in boreal and temperate forests (Schlesinger & Bernhardt, 2013), directly mobilizing nutrients from organic sources by excreting extracellular phosphatase and cellulase enzymes (Lambers, Chapin, & Pons, 2008). These nutrients are absorbed by the fungal hyphae and may then be transferred to the symbiotic plant hosts (Perez-moreno & Read, 2000).
The ability of ectomycorrhizal fungi to mineralize organic nutrients was most clearly demonstrated in a study of birch (Betula pendula) seedlings inoculated with the ectomycorrhizal fungus Paxillus involutus. Seedlings were planted in transparent observation chambers in factorial treatments of mycorrhizae inoculation and litter addition (Perez-moreno & Read, 2000). The presence of the mycorrhizae reduced litter nutrient concentrations, particularly P, indicating that the fungus was able to mineralize organic nutrient supplies. Concurrently, the birch seedlings with mycorrhizal inoculation treatments had significantly increased biomass production and tissue nutrient concentrations with litter present compared to treatments without litter, implying that the organic compounds were passed from the mycorrhizae to the tree seedlings.
The ability of mycorrhizal fungi to mobilize recalcitrant nutrient sources allows plants to survive in systems where rates of N mineralization would not otherwise be fast enough to meet plant requirements. In the pygmy forests of California, the soil is extremely infertile, acidic, and N-limited. The Pinus contorta trees in this environment have formed a tight nutrient cycle with their fungal symbionts, Amanita muscaria. The plants immobilize N in their tissues by producing high amounts of tannins (Northrup, Yu, Dahlgren, & Vogt, 1995). Tannins are very recalcitrant complexes, which lock up N in a form that is then only available to plants via mineralization by ectomycorrhizal fungi. When the tannin-rich litter is deposited in the soil the tannins adsorb to soil surfaces and are then able to be taken up by the plants’ own mycorrhizal symbionts. In this way the trees have adapted to maximize their chances of recovering the N lost in their own litter.
In environments with slow rates of mineralization, fungal associations are particularly important for plants to acquire adequate nutrient supplies (Godbold, 2004). Mycorrhizae are more abundant and have greater N mineralizing activity in areas with fewer N inputs and less nitrification, such as the more northerly boreal forests compared with temperate forests (Read & Perez-moreno, 2003). Further north, the soil is often more acidic, with fewer nutrient resources and therefore less mineralization in the absence of the fungi. This has been demonstrated using N isotopes to illuminate pathways of N transfer (Hobbie, Macko, & Williams, 2000; Hogberg et al., 1996). Natural abundances of 15N are altered when they pass through different transformations. When transferred from mycorrhizae to plants, the lighter 14N isotopes are preferentially passed to plants, causing depletion in foliar δ15N signatures (Hogberg et al., 1996). When this material is returned to the soil as plant litter, it results in deeper soil layers having greater 15N enrichment and surface layers being more depleted in 15N. An experiment in coniferous and broadleaved forests in central and northern Europe showed this effect to be most pronounced in N-limited forests (Hogberg et al., 1996). Hobbie et al (2000) got a similar result from a study conducted in Alaskan boreal forests. They found that trees in older sites with low N concentrations had lower foliar δ15N.
Both studies indicate that a greater proportion of plant nutrition was obtained by way of fungal symbionts when N was scarcer. This trend was also correlated with a decline in total foliar N concentrations, likely due to increased allocation to belowground C (Hobbie, Macko, & Shugart, 1999). This evidence suggests that as N availability increases, foliar N concentrations also increase, while mycorrhizal fungi decline. Therefore, boreal forests tend to have greater dependence on mycorrhizae for the mineralization of organic nutrient sources, and their associated fungi often have increased abilities for polymerase function.
Mycorrhizal networks can serve to transfer carbon, nutrients, and water to younger trees to help with growth and establishment (Simard, 2009). For example, seedling survival and growth rate in Douglas fir (Pseudotsuga menziesii) is improved when connected to mycorrhizal networks containing large trees (Simard et al., 2012), though the mature trees themselves have competitive effects on seedlings. This creates an area of maximum seedling performance in a circle around mature trees, but out of the way of competitive effects (Buscardo et al., 2012). These networks can prevent nutrient leaching from the system by taking up nutrients and distributing them where most needed based on source-sink gradients.
Recent technological advances have greatly improved our ability to study the role of mycorrhizae in nutrient cycling. For example, culture-independent DNA analysis has been key in identifying fungal symbionts to genus or species, which was previously impossible (Simard et al., 2012). Advanced microscopy techniques have also been helpful in elucidating mycorrhizal physiology. Still, of the 5000 species that can form mycorrhizal associations, only a small number of these have been studied because of the difficulty of culturing them. In situ studies will be important for studying fungi that are not culturable (Read & Perez-moreno, 2003).
In light of projected changes in climate, it will be necessary to estimate the importance of mycorrhizal-mediated nutrient cycles for soil C storage. Since mycorrhizae increase the proportion of C in the soil relative to N and P concentrations, they contribute to soil carbon retention (Read & Perez-moreno, 2003). Warmer temperatures may disrupt the tight cycling of boreal forest nutrient cycling by diminishing the performance of extracellular enzymes, which function optimally at low temperatures. This could cause systems to lose more N and decrease their ability to store C. Increased rates of N deposition will also affect the function and abundance of mycorrhizal networks. Since mycorrhizal associations are favored by low-nutrient systems, increased N loads could decrease dependence on mycorrhizae.
Symbiotic mycorrhizae control nutritional processes, productivity, and species composition in boreal and temperate forests. These fungi provide a shortcut in nutrient cycling by accelerating the mineralization of organically-bound nutrients and providing them to plants faster than would be possible via diffusion in the soil (Lambers et al., 2008). Though mycorrhizal associations are critical for plant survival in systems that are limited by nutrients, their importance declines as N availability increases. Complex, belowground mycorrhizal networks influence the sink-source balance of carbon in the system by mediating storage and transfer of carbon and nutrients, thereby determining to a large extent the quality of the plant tissues that are returned to the soil in the form of litter (Read et al., 2004). Understanding how mycorrhizal networks are regulated will greatly improve our understanding of forest ecosystem processes.
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