Australia: The Land Where Time Began

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The function of ECM communities in the perspective of climate change

Factors that drive climate changes

An increase in atmospheric greenhouse gases that results from deforestation, the combustion of fossil fuel and other anthropogenic activities have begun to modify the global system, following the previous 1,000 – 2.000 years of fairly stable climate (WMO, 2006). Over the past decades there had been an increase in extreme events such as tornadoes or late frosts. It is likely that these changes will affect forest ecosystems, especially ECM communities that have a key position at the plant – soil interface (Cuelemans et al., 1999). There are 3 factors that can alter the ECM symbiosis by:

1.    Directly influence the host plant (such as an increase of atmospheric CO₂,

2.    Directly influence the fungal symbiont by altering allocation of C from the host (such as the rate of photosynthesis), and

3.    Directly influence the fungal symbiont (such as warming, water availability).

These factors act in combination in most cases which makes it difficult to attribute the response of the ecosystem to a single factor.

Climate change factors that induce ECM responses on the global scale

Temperature increase

A trend toward warming is one of the characteristics of global climate change. It is predicted that surfaces temperatures will increase by between 1.8 and 3.6^oC by the year 2100 (IPCC, 2007). In cool and temperate zones forests are adapted to the seasonal cycle, with a period of dormancy in winter that is triggered by variations in temperature and photoperiod (Menzel & Fabian, 1999). Therefore, it is expected that global warming will alter tree phenology and to increase the length of the growing season (Walther et al., 2002; Parmesan & Yohe, 2003; Cleland et al., 2007; Morin et al., 2007). The average growing season in Europe has lengthened by 10.8 days since the early 1960s. Bud break is the critical phenological event which determines plant growth and development during the growing season (Hӓnninen, 1995).

The rate of photosynthesis is also increased by warming, and the additional carbohydrate flux favours the production of fine roots (Kellomӓki & Wang, 1996; Norby et al., 2004; Norby & Luo, 2004). The recent changes in autumnal mushroom phenology coincide with the extension of the growing season of trees that has resulted from global climate change and high temperatures during autumn and winter months delay the production of fruiting bodies of ECM fungi in the same year and in the following year (Kauserud et al., 2008). A surprising find (Malcolm et al., 2008) that the respiration of the ECM fungi C. geophilum, Suillus sp. and Lactarius sp. was reduced by 20-65%, though it would have been expected that it would increase with temperature. Therefore, the ability to withstand elevated temperature is a complex trait that will determine the populations of ECMs to adapt to and acclimatise to global warming and which is well worth an extensive study.

Elevated atmospheric CO₂ concentration

Elevated levels of CO₂ at the tree level increases the rates of photosynthesis by 40 – 80% provided there is an adequate supply of nutrients (Körner et al., 2005), increases the allocation of C to the roots (Janssens et al., 2005; Palmroth et al., 2005) and accelerates the ontogeny and growth of roots (Janssens et al., 2005; Norby et al., 2005). Rising levels of [CO₂] at the fungus level shifts the composition and structure of the ECM fungal communities (though not their richness) and the abundance of a few common species (Godbold et al., 1997; Rygiewicz et al., 2000; Fransson et al., 2001). Moreover, the number of species that form extensive extraradical mycelia and rhizomorphs increases (Godbold et al., 1997; Rouhier and Read, 1998; Parrent et al., 2006). There are a few studies that have examined the response of fungal biomass to atmospheres that are enhanced in CO₂ and they have, however, yielded conflicting results (Klironomos et al., 1997; Klamer et al., 2002; Alberton et al., 2005; Staddon, 2005; Parrent & Vilgalys, 2007). ECM respiration is also increased by elevated concentrations of CO₂          (Alberton et al., 2005; Fransson et al., 2007) and metabolic activity (Chung et al., 2006).

Availability of water: a climate change factor that induced ECM responses at the local scale

In 2003 the extreme drought that occurred at that time is considered to be the type of event that might occur with increasing frequency in the near future (Schӓr et al., 2004; Hyvönen et al., 2007). The need to understand the key process that allows trees and ECM fungi to overcome such severe water shortages is highlighted by it. The performance of the conducting system that is formed by the soil-mycelium-mantle-root-xylem-stomata continuum is an important physical factor that controls the transfer of water to the tree (Muhsin & Zwiazeck, 2002). According to Courty et al. it is clear that ECM fungi are diverse in the way that they influence the water status of trees. It is, for instance, that the ability of C geophilum to establish the symbiosis is stimulated by low water potential, and its ECM to survive better than others (i.s., Lactarius subdulcis) under extreme water stress conditions, which confers the ability on the tree to immediately benefit from any returning moisture following a period of drought (Jany et al., 2003; di Pietro et al., 2007). This aspect of the function of the ECM has been neglected to a large extent and it would be worth more studies to be undertaken that compared ECMs of different types especially in the context of climate change.

The response of forest trees to water stress is to close their stomata and reduce their assimilation of CO₂, which means a reduction in the amount of carbon that is allocated to ECM fungal communities. This may induce premature mortality of roots and ECMs, and alter dramatically the structure of ECM communities.

Factors that add complexity to the response community to climate change

Inputs of nitrogen have increased significantly over the last 30 years, in Europe in particular (Galloway et al., 2004; Phoenix et al., 2006). The response of forest trees has been by an increased rate of photosynthesis and the production of new leaves, wood and coarse roots (Livonen et al., 2006; Hyvönen et al., 2007), though there is a lessening of the species richness of ECM fungal communities and differ in structure and composition where there is an elevation of N deposition (Carfrae et al., 2006; Parrent et al., 2006; Avis et al., 2008). A decrease in the activity of fungal lignin-enzymes has also been observed with increased deposition of atmospheric N (Lucas & Casper, 2008), which might slow the degradation of dead wood and leaf litter.

One of the major air pollutants that is present during the growing season in the temperate zone is tropospheric ozone O₃, which reduces productivity at leaf, tree and stand scales (Dizengremel, 2001). Conflicting results have been yielded by studies that examined the response of ECM fungi to an atmosphere enriched in O₃ and the production of extraradical mycelium (Grebenc & Kraigher, 2007; Haberer et al., 2007; Millard et al., 2007; Rathnayake et al.,2007; Pritsch et al., 2008). Courty et al. suggest that more research is needed in this field, while keeping in mind that effects studied are mostly indirect and mediated through tree hosts.

ECM communities as a C sink in the context of global change

A special attention to forests has been aroused by the current concerns with the levels of atmospheric CO₂ concentrations as a cause of global warming, an in particular to forest soils and humus, as compartments of the biosphere where C can be sequestered. How ECM communities will adapt to the changing climate will affect the efficiency of forest ecosystems as C sinks, as ECMs are pivotal in controlling the tree-soil fluxes.

CO₂ concentrations can modify the quality of the litter and its content of C, which hampers heterotrophic activity and affects its mineralisation by fungi (Knorr et al., 2005). SOM can be used by some ECM fungi as an alternative C source when:

1                   Supplies of photosynthate from the host plant are low (i.e., severe drought),

2                   Carbon contest of the litter increases and,

3                   Allocation of plant photosynthates ECM roots is high, such that the plant C primes the saprotrophic activity of the ECM fungi (Talbot et al., 2008).

Unfortunately, their combination result in equilibria that are extremely unstable, even if these mechanisms have been ascertained in specific conditions, which leaves a high uncertainty regarding how elevated concentrations of CO₂ will modulate the role of the fungal partner in the ECM symbiosis.

Trees can support more species of ECM that produce more extraradical mycelium under the same conditions of CO₂ concentrations and of increased net primary photosynthesis (Godbold et al., 1997). This leads to increased allocation of C to structural polymers such as chitin, or to intracellular fungal storage compounds such as mannitol and trehalose (Staddon, 2005). These ECM fungi that have a high C demand could then provide the trees with more nutrients and improve productivity of the forest (Alberton et al., 2005). A plausible hypothesis is that enrichment with CO₂ will favour species that are producing the greatest amounts of extraradical mycelium, considering the high exportation of ECM with abundant extraradical mycelium, combined with increased plant nutrient demand in conditions of CO₂ that are elevated (Rygiewicz et al., 2000). Present knowledge is not sufficient, however, to predict how these changes will affect the rate of decomposition/accumulation of litter      and humus, which is the key to C storage in the forest floor in the boreal and temperate zones.

Host-symbiont joint strategies for survival in response to climate change

According to Courty et al. Adaptation capabilities of trees and fungal species may be exceeded by shifts in climate zones. Therefore, it is difficult to predict how rapidly they can jointly respond to changes even if palaeo-records can provide clues to help understanding of the resilience, adaptation or migration of the 2 partners in the symbiosis, as has been done retrospectively for the black truffle T. melanosporum that is associated by oak (Murat et al., 2004).

The rates of climate change of the present may require much faster rates of migration than those that have been observed during postglacial times, and therefore, biodiversity may be reduced by selection of species that are highly mobile and opportunistic. There are 3 categories of factors that are expected to influence co-migration of trees with their fungal partners:

1                   Barriers to dispersal,

2                   Ecological amplitude, (i.e., range of environmental conditions that are favourable to a species: Malcolm et al., 2002), and

3                   Efficiency in cycling and storage of nutrients (the condition to benefit from limited resources: Dixon, 2000).

There are many tree and fungal species that could benefit under changes of climate because longer growing seasons and temperatures minima are likely to dominate the future forest stands (Svenning & Skov, 2004; Wiens & Donoghue, 2004). The ability to survive, to migrate, or to invade new ecosystems is also influenced greatly by the degree of host specificity of ECM fungi.

Finally, co-migration of trees and of ECM fungi may result in migrations by some fungal symbionts, as is shown in the recent review of fungal invasions by Desprez-Loustau et al. (2007). These authors stress, however, the difficulty of distinguishing genuine invasions that are due to environmental stages from intrinsic dynamic of species that are due to anthropogenic introductions. Generally, such introductions tend to be accidental though they can be deliberate as in the case of ECM inoculation in plantation forests.

Courty, P.-E., et al. (2010). "The role of ectomycorrhizal communities in forest ecosystem processes: New perspectives and emerging concepts." Soil Biology and Biochemistry 42(5): 679-698.