Ecology Letters, (2013) 16: 140–153
doi: 10.1111/ele.12085
REVIEW AND
SYNTHESIS
Nancy C. Johnson,1* Caroline
Angelard,2 Ian R. Sanders2 and
E. Toby Kiers3
Predicting community and ecosystem outcomes of mycorrhizal
responses to global change
Abstract
Mycorrhizal symbioses link the biosphere with the lithosphere by mediating nutrient cycles and energy flow
though terrestrial ecosystems. A more mechanistic understanding of these plant–fungal associations may
help ameliorate anthropogenic changes to C and N cycles and biotic communities. We explore three interacting principles: (1) optimal allocation, (2) biotic context and (3) fungal adaptability that may help predict
mycorrhizal responses to carbon dioxide enrichment, nitrogen eutrophication, invasive species and land-use
changes. Plant–microbial feedbacks and thresholds are discussed in light of these principles with the goal
of generating testable hypotheses. Ideas to develop large-scale collaborative research efforts are presented.
It is our hope that mycorrhizal symbioses can be effectively integrated into global change models and eventually their ecology will be understood well enough so that they can be managed to help offset some of
the detrimental effects of anthropogenic environmental change.
Keywords
CO2 enrichment, enzyme activity, mutualism, mycorrhizal adaptability, optimal allocation, plant–microbe
feedbacks, R*, resource competition terrestrial N eutrophication.
Ecology Letters (2013) 16: 140–153
Mycorrhizal partnerships between plants and fungi play an integral
role in structuring and changing terrestrial ecosystems throughout
the world. These symbioses are hypothesised to have facilitated the
evolutionary radiation of terrestrial plants (Pirozynski & Malloch
1975; Brundrett 2002) and contributed to massive changes in the
earth’s atmosphere: the rise of vascular plants 410–340 Ma corresponds with a 90% reduction in atmospheric carbon dioxide (CO2)
levels (Taylor et al. 2009; Field et al. 2012). The arrival of deep roots
and their associated mycorrhizas are hypothesised to have enhanced
the release of calcium and magnesium from silicate rock and the
reaction of these cations with CO2 generated carbonate sediments
in the oceans, effectively moving CO2 from the atmosphere to the
lithosphere (Taylor et al. 2009).
In today’s ecosystems, mycorrhizas continue to play a crucial role
in elemental cycles because they are major vectors and reservoirs of C
belowground, as well as potential decomposers of soil organic matter
(Talbot et al. 2008; Meyer et al. 2010; Cheng et al. 2012). Most of the
Earth’s terrestrial C stock is stored in soils (Swift 2001). Studies estimate that ectomycorrhizas account for approximately one-third of
the living biomass in forest soils (H€
ogberg & H€
ogberg 2002) and arbuscular mycorrhizal fungi could make up as much as one half of the
microbial biomass in agricultural systems (Olsson et al. 1999). Even
small changes in the processes controlling C flux into and out of
mycorrhizas may have large impacts on the global C balance (Orwin
et al. 2011). Furthermore, for most plant species, mycorrhizas are
critical for nutrient uptake. Maximising mycorrhizal benefits in
agriculture, horticulture and forestry has been identified as a potential
strategy to reduce the growing footprint of global food and fibre
production (Verbruggen & Kiers 2010).
An expanding human population has rapidly become a dominant
driver of change to Earth systems. Indeed, the term ‘global change’
has come to mean anthropogenic environmental changes. An
important question of our time is how interactions of global importance, such as mycorrhizal symbioses, will fare in a rapidly changing
world. Human actions are enriching the earth with CO2 and nutrients, and altering the composition of biotic communities. Changes
to the structure and functioning of microbial processes are predicted to strongly mediate community and ecosystem responses to
anthropogenic environmental change (Singh et al. 2010). Understanding the ecological and evolutionary mechanisms by which
mycorrhizal symbioses respond to environmental changes will help
us predict, and possibly ameliorate, some of the undesirable outcomes of rapid anthropogenic changes that we currently face.
Three distinct types of mycorrhizas are likely to be important for
ecosystem responses to global change. (1) Arbuscular mycorrhizas
are symbioses formed between Glomeromycota and Endogone-like
fungi and approximately three-fourths of all plant species, ranging
from primitive liverworts and mosses to the most advanced herbaceous and woody angiosperms (Brundrett 2009; Bidartondo et al.
2011). This ancient symbiosis is also found in most agricultural
crops. (2) Ectomycorrhizas are symbioses between thousands of different taxa of fungi including Basidomycetes, Ascomycetes, and
Zygomycetes and primarily woody plant species (Tedersoo et al.
2010). The dominant trees in temperate and boreal forests are over-
1
3
INTRODUCTION
School of Earth Sciences and Environmental Sustainability, Department of
Institute of Ecological Science, Vrije Universiteit, Amsterdam,
Biological Sciences, Northern Arizona University, Flagstaff, AZ, 86011, USA
The Netherlands
2
*Correspondence: E-mail: [email protected]
Department of Ecology & Evolution, University of Lausanne, Lausanne, 1015,
Switzerland
© 2013 John Wiley & Sons Ltd/CNRS
Review and Synthesis
whelmingly ectomycorrhizal. (3) Ericoid mycorrhizas are symbioses
between Ascomycetes and ericaceous plants that predominate in
heathland and boreal habitats.
There are many excellent reviews of mycorrhizal responses to
global change (e.g. Rillig et al. 2002; Drigo et al. 2008; Singh et al.
2010). The objective of this article is to build upon insights gained
from these reviews and introduce three principles that describe mechanisms by which mycorrhizas respond to a changing environment.
We examine the usefulness of these principles for understanding
mycorrhizal responses to interrelated drivers of global change: enrichment of atmospheric CO2, nitrogen (N) eutrophication and changes
in biota through invasive species and land-use change (Fig. 1).
Throughout this analysis, we discuss the consequences of mycorrhizal
feedbacks to community and ecosystem patterns and processes. The
ultimate goal of our article is to contribute to the development of testable hypotheses that predict mycorrhizal responses to global changes,
and community and ecosystem outcomes of these responses.
PREDICTING MYCORRHIZAL RESPONSES TO GLOBAL CHANGE:
THREE PRINCIPLES
Mycorrhizas respond to changes in the quantity and quality of essential resources and to changes in their biotic environment. These
responses can be characterised by three principles (Fig. 1). First, the
principle of optimal allocation suggests that environmental fluctuations which change the availability of soil-based resources (e.g. N, P,
Zn and water) will drive host and fungal symbionts to optimise
resource use through changes in allocation to biomass and associated enzyme systems. Second, the principle of biotic context argues
that plant and fungal fitness are influenced by the biotic interactions
within their environment. Natural selection is expected to favour
phenotypes of plants and mycorrhizal fungi that are most efficient at
acquiring limiting resources and avoiding losses due to competition,
disease, herbivory and fungivory. These biotic interactions will determine which phenotypes have the highest fitness. Finally, the principle of adaptability postulates that the range of genetic variability
maintained within populations of plants and fungi will ultimately
determine their potential responses to environmental change. Here,
we explain these three principles and explore how they can help predict mycorrhizal responses to environmental change (Fig. 1).
Mycorrhizas and global change 141
Principle 1 Optimal allocation: Plants and mycorrhizal fungi preferentially allocate biomass and energy towards acquiring the resources
that are most limited in supply. For example, the chemical quality of
limiting resources determines which enzyme systems are most advantageous for plants and associated fungi.
This principle originates from the ‘Law of the Minimum’ and is
embodied in the functional equilibrium and optimal allocation models (for review see Johnson 2010). These optimisation models are
potentially useful in helping predict mycorrhizal responses to global
changes because human activities are enriching essential resources
to the point that formerly limiting resources are becoming nonlimiting. When this occurs, plants and fungi are predicted to shift
allocation to structures in a manner that maximises the acquisition
of the next most limiting resource. When an anthropogenic change
makes belowground resources relatively more limiting than aboveground resources (e.g. CO2 enrichment), plants generally increase
root biomass, specific root length and the degree to which they support fungal symbionts (Fig. 2a). Similarly, mycorrhizal fungi often
adjust to nutrient limitations through increased allocation to networks of absorptive hyphae (Antoninka et al. 2011; Cavagnaro et al.
2011). In contrast, anthropogenic changes that decrease limitation
of belowground resources relative to aboveground resources (e.g. N
eutrophication) have the opposite effects on plants and mycorrhizal
fungi (Fig. 2b). The principle of optimal allocation (functional equilibrium) has been shown to be useful for predicting patterns of
plant and fungal responses to fertilisation at the scale of individual
plant species as well as entire communities (Liu et al. 2012).
Organisms utilise various ‘optimisation’ strategies to acquire limiting resources. Sometimes this involves adjusting to changes in the
‘quality’ of limiting resources rather than to resource quantity.
Plants, mycorrhizal fungi and bacteria inhabiting the ‘mycorrhizosphere’ produce a diversity of extracellular and cell wall bound
enzymes that facilitate the acquisition of recalcitrant minerals from
the soil (Pritsch & Garbaye 2011). In many natural ecosystems, the
depolymerisation of proteins and other organic compounds in litter
is the rate-limiting step in the generation of bioavailable N (Schimel
& Bennett 2004). Mycorrhizal fungi are increasingly recognised for
their direct role in decomposition and uptake of organic forms of
N and P (Talbot et al. 2008). Also, mycorrhizas may help plants
Figure 1 Anthropogenic changes to the environment influence plants, associated fungi and mycorrhizal symbioses both directly and indirectly. These effects can impact
community and ecosystem structure and function. The principles of optimal allocation, biotic context and mycorrhizal adaptability can help explain and predict these
community and ecosystem outcomes.
© 2013 John Wiley & Sons Ltd/CNRS
142 N. C. Johnson et al.
Review and Synthesis
(a)
(b)
A
A
S
S
IH
EH
EH
IH
V
V
C
Figure 2 Optimal allocation (functional equilibrium) predicts that plants and their associated mycorrhizal fungi will preferentially allocate biomass to structures that forage
for the most limiting resource. (a) Relatively more biomass will be allocated to roots and mycorrhizal fungi in systems in which belowground resources are relatively more
limited than light and CO2. (b) Relatively less biomass will be allocated to roots and mycorrhizas in systems with fertile soil and ample water. This Figure illustrates an
arbuscular mycorrhiza: S are spores, EH are extra-radical hyphae, IH are intraradical hyphae, V are vesicles, and C are coils. Drawing of mycorrhizal roots courtesy of
Diane Rowland. This Figure is modified from Johnson et al. 2003a.
out-compete saprotrophic soil bacteria for nutrients (Schimel &
Bennett 2004). Availability of C and essential nutrients in space and
time appear to structure mycorrhizal allocation to different catabolic
enzyme systems (Read & Perez-Moreno 2003; Bu"ee et al. 2007).
Heathlands are characterised by acidic, organic rich soils that
tightly sequester N and P in organic polymers. It is no coincidence
that the ericoid mycorrhizal fungi that dominate these systems are
powerful saprotrophs with extracellular enzymes that decouple N
and P from complex polymers in low pH, organic soils. Mineral
forms of N and P become more available and soil pH increases as
the warmer conditions of temperate forest and grassland biomes
accelerate decomposition and mineralisation processes (Read &
Perez-Moreno 2003; Fig. 3). These changes are accompanied by
changes in the dominant forms of mycorrhizas, generating a continuum of saprotrophy in forest ectomycorrhizas (Koide et al. 2008),
to grassland arbuscular mycorrhizas, with little or no saprotrophic
abilities. Although AM fungi may not function as traditional saprotrophs, there is increasing evidence that they may act as ‘decomposers in disguise’ because they have been shown to assimilate amino
acids and accumulate N from decomposing organic matter (Talbot
et al. 2008; Hodge & Fitter 2010). A better understanding of the
© 2013 John Wiley & Sons Ltd/CNRS
enzymatic capabilities of local mycorrhizas to decompose soil
organic matter will help predict whether the system has the potential to be a belowground C-source or C-sink.
Principle 2 Biotic context: Mycorrhizal function depends on both
abiotic and biotic context. This context dependency determines plant and
fungal fitness and the outcome of mycorrhizal feedbacks for communities.
Bottom-up (resources) and top-down (exploitation) factors simultaneously shape communities and determine the traits that are most
important for plant and fungal fitness and mycorrhizal function. Species and genotypes of plants and fungi differ in their growth rates,
dispersal strategies, stress tolerance and competitive abilities (Grime
1979). The presence or absence of herbivores, pathogens and competitors will determine the optimal plant strategies and whether
mycorrhizal symbioses improve plant fitness. Similarly, carbon allocation patterns of hosts, presence or absence of fungivores and competing microorganisms will determine optimal fungal strategies.
Anthropogenic factors that influence resource availability and/or
the composition of biotic communities will likely influence the costs
and benefits of mycorrhizal symbioses, and this may alter feedbacks
Mycorrhizas and global change 143
Review and Synthesis
Positive feedback
Heathland
Boreal forest
Ericoid (EM)
EM (ericoid)
Temporate forest
EM (AM)
Grassland
AM
Humus and organic compunds
Nitrification and mineralization rates
Negative feedback
Plant hosts
A
B
A
B
Symbiotic fungi
X
Y
X
Y
Figure 4 The fitness relationships between plant species A and B and their
associated fungal communities X and Y can generate positive or negative
feedbacks. Arrows depict beneficial effects and the thickness of the arrow is the
relative strength of the interaction. Positive feedback between plants and their
symbiotic fungi will tend to reduce the diversity of plant communities, whereas
negative feedback will increase it. Figure modified from Bever et al. 2010.
Soil P availability
Soil pH
Saprotrophic capability
Figure 3 Latitudinal patterns (northern hemisphere) of predominant mycorrhizal
types, soil properties and importance of saprotrophy for mycorrhizal acquisition
of minerals. Ericod mycorrhizas with strong saprotrophic capabilities dominate
in heathlands, ectomycorrhizas with a gradient of saprotrophic fungi dominate
boreal and temperate forests, arbuscular mycorrhizas with little or no
saprotrophic capacity dominate grasslands. Figure modified from Read & PerezMoreno 2003.
between communities of plants and mycorrhizal fungi. Theory
suggests that positive mycorrhizal feedbacks are likely to reduce plant
diversity, while negative feedbacks increase plant diversity (Fig. 4;
Bever et al. 2010). Mycorrhizal fungi that increase the competitive
ability (fitness) of their plant host will potentially be allocated more
carbohydrates, resulting in higher fitness compared to inferior competing fungal symbionts. The mutual benefits of these increasingly
beneficial symbioses will generate a positive feedback such that the
plant species hosting strongly beneficial mutualisms may competitively exclude species with less efficient symbioses, and in this way,
plant diversity is reduced. In contrast, negative feedbacks between
plants and fungi will increase plant diversity because the symbiosis is
more beneficial to plants other than their hosts (Fig. 4). Thus, environmental changes that influence the symbiotic benefits of locally
adapted mycorrhizas may either increase or decrease plant diversity.
Mycorrhizas may contribute directly to the competitive abilities of
plants through their affects on the uptake of soil resources. Competition theory defines the equilibrium resource level (R*) as the lowest
concentration that particular resources can be diminished by particular species and phenotypes (Tilman 1988). In isocline models, R* is
the resource concentration at which the net rate of population change
is zero: in other words, reducing resource availability below this
threshold will reduce population growth rate. Mycorrhizal fungi may
substantially reduce plants’ R* for immobile elements like P and Zn,
and this may influence the outcome of competitive interactions within
plant communities (van der Heijden 2002; Fig. 5). Living organisms
require many different resources, and a critical R* can be defined for
Figure 5 Resource dependent zero net growth isoclines for plant species A (blue
dashed line) and B (red solid line) growing across a gradient of two resources.
The hypothetical scenario on the left illustrates a system without mycorrhizas in
which species A can competitively exclude species B because it has a lower R*
for both resource 1 and 2. The scenario on the right shows how mycorrhizas
reduce the R* for resource 1 in species B and this allows for stable coexistence
when resources 1 and 2 are at intermediate levels of availability. The arrows on
the right panel represent consumption vectors for species A and B. Figure based
on van der Heijden 2002 and Tilman 1988.
each resource. Coexistence of two or more species is predicted when
each is a superior competitor for a different resource (Tilman 1988).
Mycorrhizal associations may be a very effective way for plants to
partition belowground resources in space and time, and essentially
avoid competitive interactions (Bever et al. 2010). We can use this
principle to help predict how mycorrhizas will mediate community
responses to anthropogenic changes, such as enrichment of essential
resources, invasive species threats and landscape modifications.
Principle 3: Mycorrhizal adaptability: Ecological and evolutionary agility in response to a changing environment depends on the amount
of genetic variation that exists and/or can be generated in local populations of symbiotic fungi.
The mode and tempo of mycorrhizal responses to environmental
change varies with the life history and reproductive strategies of the
© 2013 John Wiley & Sons Ltd/CNRS
144 N. C. Johnson et al.
Review and Synthesis
(a)
Nuclei separated in
compartments by septa
Fruitbody
Monokaryon
Germinating
haploid spores
Dikaryon
Karyogamy
and Meiosis
(able to produce mycorrhizas
and fruiting body)
Monokaryon
(b)
New spores are genetically
different from parental spores
due to meiosis and could
have different adaptability
New haploid
spores
Heterokaryon
New spores
Hyphae without septa
Germinating
spore
New spores can have a different
proportion of nucleotypes due to segregation
of nuclei at spore formation and could have
different adaptability
(c)
Spatial change
of biotic factors
Plant A
Change in nucleotype
composition to adapt to plant A
Plant B
Change in nucleotype
composition to adapt to plant B
Plant C
Change in nucleotype
composition to adapt to plant C
(d)
Spatial change
of abiotic factors
Low Posphate
Low Nitrogen
Change in nucleotype
composition to adapt to Low P low N
High Posphate
High Nitrogen
Change in nucleotype
composition to adapt to High P High N
Low Posphate
High Nitrogen
Change in nucleotype
composition to adapt to Low P High N
Figure 6 (a) Ecto and ericoid mycorrhizal fungi (Ascomycota and Basidomycota) often have a complex mating system involving the fusion of two monokaryons to form
a dikaryon. Only dikaryons produce mycorrhizal symbioses and fruiting bodies (e.g. mushrooms). Meiosis occurs in the fruiting body to create new haploid spores that
are genetically different from the parents. (b) AM fungi (Glomeromycota) contain genetically different nucleotypes that can differentially segregate into new spores
resulting in a change of proportion of nucleotypes, some nucleotypes can even be lost. Thus, even though clonal, AM fungi can produce genetically different offspring.
(c) AM fungi often connect different plant hosts with a common mycorrhizal network, potentially leading to local variation of nucleotype frequencies and simultaneous
adaptation to multiple plant species. (d) Extensive hyphal networks can span large areas with heterogeneous soil conditions, and they are hypothesised to generate finescale local adaptation to changing environments through this mechanism.
© 2013 John Wiley & Sons Ltd/CNRS
Review and Synthesis
plant and fungal symbionts. To a certain extent, mycorrhizal fungi
and plants can acclimate to changes in their environment through
plasticity. However, over longer periods of time, the process of
adaptation to a changed environment involves the production of a
variety of genetically novel offspring on which selection can act. In
this regard, AM fungi differ substantially from ecto and ericoid
symbionts. Many Ascomycota and Basidomycota that form ecto and
ericoid mycorrhizas reproduce sexually. Genetic variation arising
from sexual reproduction will allow a range of adaptability in the
offspring to environmental variation (Fig. 6a). In contrast, Glomeromycota are thought to be entirely asexual and this clonal trait is
generally assumed to limit adaptability to new environments. Evidence suggests that AM fungi contain genetically different nuclei, or
nucleotypes, within a single individual (Fig. 6b). This heterokaryotic
state (i.e. when different nuclei share one common cytoplasm) in
AM fungi has been challenged by Pawlowska & Taylor (2004). Subsequently, Ehinger et al. (2012) have provided an explanation for
how the data presented by Pawlowska and Taylor are also consistent with the hypothesised heterokaryotic state. Recent work has
demonstrated that nucleotype frequencies in AM fungi differ among
offspring (Angelard et al. 2010; Ehinger et al. 2012). This gives AM
fungi the ability to rapidly produce offspring that are genetically and
phenotypically different, despite being ‘clonal’ (Angelard et al. 2010;
Angelard & Sanders 2011; Ehinger et al. 2012). A remarkable
amount of genetically different progeny, with a wide array of different phenotypes, has been shown to arise from a single AM fungal
parent (Ehinger et al. 2012), thus giving rise to progeny that potentially may be better adapted to a new environment than the old
environment. This is possible because heterokaryosis allows the fungus to partition different proportions of nucleotypes into their
spores; a process that creates phenotypically variable offspring over
time (Fig. 6b).
Understanding the mechanisms by which organisms respond to
change and acclimate or adapt to their environment is key to predicting their dynamics in a changing world. Genetic variation is
required in populations for adaptation to occur in changing environments. Little is known about the genetic diversity of most naturally occurring populations of fungi; however, there is evidence
that co-adaptation may maximise benefits and minimise costs of
the symbiosis. A recent comparative study showed that geographical ecotypes of the AM fungus Gigaspora gigantea were most beneficial to their plant hosts when grown in their native soil (Ji et al.
2013). The high degree of genetic variation discovered in AM
fungal populations (B€
orstler et al. 2008; Croll et al. 2008) suggests
that there is a considerable amount of genetic variability within
an AM fungal species on which selection could act during a
change in the environment. In addition to this variation among
AM fungal individuals, separation of genetic material among nuclei
that are potentially mobile within the fungal mycelium could create spatial agility in adaptation. Local selection for particular
nucleotypes within the hyphal network could allow different parts
of individual AM fungal clones to generate rapid, fine-scale adaptation to heterogeneity of the biotic (Fig. 6c) and abiotic (Fig. 6d)
environment, although this has yet to be experimentally demonstrated. A key research area is to understand the role this unique
genetic system plays in adaptation to changed environments, especially in the field and also to assess how much genetic variability
within and among AM fungal species contributes to the mycorrhizal response to changing environments. The role of genetic
Mycorrhizas and global change 145
diversity for mycorrhizal adaptation is an important area for
future investigation.
APPLICATION OF PRINCIPLES TO MYCORRHIZAL RESPONSES TO
GLOBAL CHANGE
Global changes can impact both plants and fungi directly, or indirectly via modifications to the symbiosis (Rillig et al. 2002; Singh
et al. 2010). For example, it is generally assumed that atmospheric
CO2 enrichment directly influences plants and indirectly influences
fungi though increased photosynthate (Drigo et al. 2008; Fig. 1). In
contrast, changes to biota and N eutrophication directly impact
both plants and fungi. Understanding both individual and interactive
effects of environmental changes on plants and fungi are necessary
to predict the net effects of global changes on mycorrhizal
symbioses.
Microbial feedbacks have been insinuated in community and ecosystem responses to global change drivers, but we currently lack
sufficient knowledge to predict the relative importance, or even the
direction, of these feedbacks (Singh et al. 2010). The principles of
optimal allocation, biotic context and adaptability may provide a
useful platform to begin to construct and test hypotheses about the
mechanisms of mycorrhizal responses to global change factors and
the outcomes of these responses for communities and ecosystems.
Enrichment of atmospheric CO2 and N
In the past century, human activities have increased the concentration of CO2 in the atmosphere from ~250 ppm to 385 ppm.
Although there are exceptions, particularly in N-limited systems
(e.g. Parrent & Vilgalys 2007), CO2 enrichment generally increases
the biomass of roots and mycorrhizal fungi (Rillig et al. 2002; Drigo
et al. 2008). This finding is in accord with Principle 1: if enriched
atmospheric CO2 increases the production of photosynthate such
that plant demand for soil nutrients increases, then allocation
belowground to mycorrhizas is expected to increase.
Concurrently with CO2 enrichment, humans have more than doubled the rate of N input into the biosphere (Vitousek et al. 1997).
This has been linked to changes in the species composition of communities and accelerated loss of plant diversity (Clark & Tilman
2008), and mycorrhizal fungal diversity (Lilleskov et al. 2002; Liu
et al. 2012). Mycorrhizas exhibit variable responses to N enrichment,
and fungal biomass has been reported to decrease, increase or
remain unchanged (reviewed in Rillig et al. 2002). Nevertheless,
these variable responses to N enrichment generally conform to the
predictions of optimal allocation in Principle 1. A comparison of
five long-term field experiments demonstrated that N enrichment
caused AM colonization of roots, spore biovolume and density of
extraradial hyphae (outside the root) to decrease at sites with ample
soil P, and increase at a site with limited levels of soil P (Johnson
et al. 2003a). We expect this pattern if plants allocate energy to
structures needed to acquire the most limiting resource: adding N
to P-rich soil will diminish the relative value of roots and mycorrhizas, while N enrichment of a P-limited soil will exacerbate P limitation and enhance the value of the symbioses.
There is increasing recognition of the importance of synergistic
effects when multiple anthropogenic changes occur. A free air CO2
enrichment (FACE) experiment in Switzerland showed that after
10 years of treatment, the CO2 9 N interaction had a significant
© 2013 John Wiley & Sons Ltd/CNRS
146 N. C. Johnson et al.
© 2013 John Wiley & Sons Ltd/CNRS
40
(a)
*
(b)
*
2
1.6
35
30
1.2
25
20
0.8
15
10
Foliar N from soil (%)
45
Foliar N concentration (µg mg–1)
effect on AM fungi, even though there was not a significant main
effect of CO2 (Staddon et al. 2004). Interestingly, Staddon and colleagues found that when N was in limited supply (but not
enriched), the formation of AM colonisation inside plant roots
decreased in response to enrichment of CO2, while the density of
extraradical hyphae increased. This conforms with the expectation
of optimal allocation because when N is more limited than C, there
should be increased growth of extraradical hyphae to forage for N.
In contrast, the BioCON FACE experiment in Minnesota USA
showed that CO2 enrichment significantly increased the density of
extraradical hyphae, but there was no interaction with N supply
(Antoninka et al. 2011). There are many possible reasons for the
different findings at the two FACE experiments, including differences in the soil properties, climate and the composition of the
plant and fungal communities. So while the optimal allocation principle can help predict the general direction of future shifts, differences among communities and ecosystems introduce serious
variation.
The potential for mitigating rising CO2 levels though increased
allocation and storage in mycorrhizas and other belowground C
pools is currently debated (Kowalchuk 2012; Phillips et al. 2012;
Verbruggen et al. 2013). Recent studies suggest that when atmospheric CO2 levels are elevated, mycorrhizas may actually speed up
the decomposition of soil organic matter, and thus generate net Csources rather than C-sinks (Cheng et al. 2012; Phillips et al. 2012).
Even though Glomeromycota are not saprotrophic themselves,
under elevated CO2, AM fungi appear to have a priming effect on
bacteria and other organisms in the mycorrhizosphere such that
decomposition of organic matter is accelerated. Priming appears to
stimulate saprotrophic bacteria to release N which is rapidly assimilated by both fungi and plants in AM symbioses (Cheng et al. 2012).
Notably, the degree to which AM fungi enhanced decomposition
can vary among taxa. When grown under elevated CO2, Gigaspora
margarita and Glomus clarum enhanced decomposition much more
strongly than Acaulospora morrowiae (Cheng et al. 2012). This pattern
is intriguing because a different research team showed that CO2
enrichment generated a very rapid shift in symbiotic partners inside
plant roots from Acaulospora to Glomus (Drigo et al. 2010). This
study highlights the need for future research to identify functional
groups of AM fungi that may be distinguished according to their
enzymatic capabilities and competitive dominance under different
resource environments.
There is some evidence that altering the abiotic environment (i.e.
nutrient availability) can also lead to genetic changes in AM fungi
(Ehinger et al. 2009), and these changes may be linked to differences in symbiotic functioning. Adaptation of AM fungi in response
to abiotic selection pressures, Principle 3, has been demonstrated
previously, with researchers finding that a gradual shift in CO2 levels over 21 generations provided time for adaptation to occur and
generated a much different mycorrhizal response compared to a
sudden CO2 increase during a single generation (Klironomos et al.
2005). Similarly, a study at the Swiss FACE site that compared the
nutritional response of white clover to colonisation by Glomus isolates derived from elevated or ambient CO2 showed that within just
8 years of CO2 treatment, the functioning of Glomus isolates
diverged such that isolates from plots treated with elevated CO2
improved the N nutrition of their host plants significantly more
than those in plots treated with ambient CO2 (Gamper et al. 2005;
Fig. 7a). Furthermore, a larger proportion of N was derived from
Review and Synthesis
0.4
5
0
0
Fungal pCO2 history
Figure 7 Rapid selection for efficient nutrient uptake and transfer by AM fungi
can influence host plant performance in changing environments. (a)
Concentration of foliar N and (b) proportion of total foliar N acquired from the
soil in Trifolium repens grown with AM fungi isolated from field plots treated for
8 years with either ambient (open bars) or elevated (black bars) CO2. Data
courtesy of Gamper et al. (2005), (n = 7), mean ! SE * significant difference at
P " 0.05.
soil pools rather than through N-fixation (Fig. 7b). These results
are in accord with the recent discoveries that CO2 enrichment generates a strong selection pressure for enhanced N uptake capacity
(Cheng et al. 2012); and, that geographical isolates of AM fungi differ in their abilities to acquire N from the soil (Johnson et al. 2010;
Ji et al. 2013). Does the heterokaryotic characteristic of AM fungal
clones allow for rapid genetic and functional changes when fungi
are exposed to changing environmental conditions (Fig. 6c, d)?
More research is needed to understand these types of rapid functional changes in AM fungi.
Research suggests that ectomycorrhizal and AM communities
respond similarly to CO2 enrichment. In both type of mycorrhizas,
CO2 enrichment has been shown to accelerate decomposition of
soil organic matter through priming (Carney et al. 2007; Phillips
et al. 2012). In ectomycorrhizal systems, the fungi, in addition to
associated saprotrophic bacteria, have the enzymatic capability to
break down complex organic compounds (Bu"ee et al. 2007; Drake
et al. 2011). Fourteen years of CO2 enrichment of loblolly pine at
the Duke FACE site in North Carolina USA enhanced decomposition rates because of more rapid turnover of roots and EM structures in addition to a priming effect on old soil organic matter
(Phillips et al. 2012). Likewise, 6 years of CO2 enrichment of a
scrub-oak ecosystem in Florida USA increased production of phenol oxidase (Carney et al. 2007; Fig. 8a), a key enzyme in the
decomposition of lignin and other recalcitrant organic materials; and
it also increased the abundance of fungi relative to bacteria
(Fig. 8b).
The principles of optimal allocation, biotic context and adaptability can help explain the apparent lack of an enhanced mycorrhizal
C-sink under elevated CO2. Principle 1, optimal allocation, accounts
for the higher N demand in response to increased availability of
labile C belowground (Hu et al. 2001). Principle 2, biotic context,
predicts that fungi may become competitively dominant in CO2
enriched systems because they can better translocate nutrients and
have a lower C : N ratio than bacteria. Consequently, N limitation
Mycorrhizas and global change 147
Review and Synthesis
(a)
(b)
Figure 8 Enzymatic activity and composition of soil microbes is influenced by 6 years of CO2 enrichment of a scrub-oak ecosystem. (a) Phenol oxidase and (b) fungus:
bacteria ratios were significantly higher under elevated CO2 compared to ambient. Means ± SE (n = 8 for ambient, and n = 6 for elevated CO2). Data courtesy of Carney
et al. 2007.
induced by CO2 enrichment generally favours fungi over bacteria
(Hu et al. 2001), with fungi utilising lignolytic enzymes to acquire
recalcitrant forms of organic N under elevated CO2. Finally, Principle 3, adaptability, accounts for the rapid change in the ability of
AM fungi to supply additional N to their host plants. These principles allow us to make predictions that can be tested in future experiments. For example, the optimal allocation principle predicts that
CO2 enrichment of N-rich soil will not stimulate production of
lignolytic enzymes because there is already ample N in the system.
In this situation, the increased production of mycorrhizas under elevated CO2 may indeed increase the accrual of C in soil organic matter. Studies of mycorrhizas across more habitat types are clearly
necessary before the symbiosis can be effectively managed for its
role in C and N cycling.
Another challenge in managing the symbiosis for N and C cycling
is that complex interactions among anthropogenic enrichment of
resources and mycorrhizal feedbacks may generate large-scale state
changes in communities and ecosystems. The critical threshold levels at which state changes occur are difficult to predict because of
the complexity of the interactions among factors. One of the most
famous examples of a state-shift related to mycorrhizas is the relationship between anthropogenic N deposition and the loss of European heathlands. These ecosystems are characterised by acidic,
organic rich soils and thick stands of heather (Calluna vulgaris) with
ericoid mycorrhizas that have enzyme systems capable of releasing
tightly bound N from polyphenolic compounds (Fig. 3). Airborne
N inputs diminish N limitation and increase biomass production,
which makes P more limited. At some point during this eutrophication process a threshold is reached, and the ericoid heather loses its
competitive advantage and becomes replaced by Molinia caerulea an
AM grass with a lower R* for P and a higher R* for N (Aerts
2002). This example illustrates how eutrophication of a limiting
resource can restructure above- and belowground feedbacks and
facilitate the conversion of heathland to grassland.
The structure of grasslands may also be influenced by mycorrhizal
responses to N and CO2 enrichment. In community-scale mesocosm experiments, grasses with C3 photosynthesis generally benefit
less from mycorrhizas and more from CO2 enrichment compared
to C4 grasses (Johnson et al. 2003b; Antoninka et al. 2009). These
findings support the idea that mycorrhizas can mediate competitive
interactions among different functional groups of plants and that
resource availability will affect the outcome of these interactions on
community diversity. Principle 2, biotic context, is relevant here
because most of the problematic exotic grasses invading native
North America grasslands are C3 species that are not strongly
dependent on mycorrhizas (Wilson & Hartnett 1998). Invasive species and land-use change, discussed below, are among the two most
important anthropogentic drivers altering mycorrhizal relationships.
Changes to biota: invasive species
Studies suggest that mycorrhizal fungi can play an important role in
determining patterns of abundance and invasiveness of introduced
species (Bever et al. 2010). Introduced host plants have been shown
to alter closely interlinked ecological relationships, many of which
have co-evolved within native systems (Inderjit & van der Putten
2010). Although subtle, and rarely studied, these re-organisation
processes are likely very common responses to global change that
can decrease the efficacy of symbiotic partnerships and potentially
lead to long-term, system-wide changes.
When invasive plants are introduced, at least three microbially
mediated outcomes have been identified (Bever et al. 2010; Inderjit
& van der Putten 2010; Fig. 9). All three outcomes can be linked to
biotic context (Principle 2), and adaptability (Principle 3). One possibility is an ‘enhanced mutualism response’ in which native mutualisms facilitate the success of invading plant species (Reinhart &
Callaway 2006). Mycorrhizas have been shown to facilitate the
spread of non-native plants from low to super high abundance if
the invading plant species benefits more from the symbioses than
the indigenous plants. For example, spotted knapweed, Centaurea
maculosa (Fig. 9a), is a noxious perennial plant that appears to generate an enhanced mutualism with native AM fungi. Many invading
plant species exhibit higher growth rates than endemic species (e.g.
van Kleunen et al. 2010a), and associating with native AM symbionts may facilitate this process by allowing them to gain access to
more nutrients to support this growth. This highly efficient mycorrhizal partnership has likely facilitated the spread of knapweed
throughout much of the native prairie in the northwestern USA
(Harner et al. 2010). More generally, mutualistic facilitation of plant
invasion arises when AM fungi alter nutrient uptake, competitive
© 2013 John Wiley & Sons Ltd/CNRS
148 N. C. Johnson et al.
(a)
(b)
(c)
Figure 9 Examples of three microbially mediated outcomes of plant species
invasion. (a) Enhanced mutualistic response – Knapweed (Centaurea maculosa)
relies on AM fungi to aid its invasion of the Bitterroot Valley grasslands in
Western mountain ranges of the USA (photo: Dan Mummey). (b) Degraded
mutualism response – Garlic mustard (Alliaria petiolata), an invasive species in
North America, has been shown to facilitate its spread by disrupting mycorrhizal
associations (photo: Ben Wolfe). (c) Mutualistic barrier – Invasive pines (i.e.
Pinus contorta) only became a problem when appropriate fungal symbionts were
introduced to the environment (photo: Jon Sullivan).
© 2013 John Wiley & Sons Ltd/CNRS
Review and Synthesis
dynamics, successional changes and/or plant–herbivore interactions
to the advantage of the exotic species and detriment of the native
species (Shah et al. 2009). In furthering Principle 2, ecologists are
designing new tools for assessing the determinants of invasiveness
(van Kleunen et al. 2010b), which will eventually facilitate a more
systematic approach to predicting mycorrhizal response to invasive
species.
It has been predicted that enhanced mutualistic responses are also
most likely to emerge when the invasive hosts associate with widespread, generalist AM fungal taxa, rather than specialised taxa
(Moora et al. 2011). This is in accord with Principle 3, mycorrhizal
fungal adaptability. One idea is that the wide host range observed
in AM fungi may be maintained by co-existence of genetically different nuclei and that the fungus can maximise its fitness in a given
host by an alteration in the relative frequency of genetically different
nuclei. There is some evidence for this in the study by Ehinger et al.
2009; in which small genetic changes were observed in clonal AM
fungal lines when grown on different host plants. If true, then this
would mean that AM fungi could have the capacity to rapidly adapt
to new invasive plant species. In these cases, the native plant species may disappear, but the native, generalist fungi, which are now
better adapted to the invasive host, remains in symbiosis with the
invasive species. A similar response may occur in host plants as
well: one recent case documented a generally non-mycorrhizal invasive plant species hybridising with a generally mycorrhizal native
species to produce invasive offspring that benefited from the
mycorrhizal association (Eberl 2011).
A second microbially mediated outcome occurs when a nonnative plant species reduces the densities of native fungal symbionts
and causes the subsequent loss of native host plants (Wilson et al.
2012). Entitled the ‘degraded mutualism hypothesis’ this outcome is
possible when native plants are more dependent on mycorrhizal
symbioses than invasive species (Shah et al. 2009) and/or invasive
species directly degrade microbial targets (Cipollini et al. 2012). Invasion by non-native plants with low mycorrhizal dependencies can
reduce mycorrhizal fungal densities in the soil, further facilitating
invasion by non-mycorrhizal plants (Vogelsang & Bever 2009). This
has been shown repeatedly across different mycorrhizal types (Shah
et al. 2009; Castellano & Gorchov 2012), and can lead to long-term
legacy effects, even after the invasive species has been removed
(Meinhardt & Gehring 2012).
In some extreme cases, an introduced plant species can be lethal
for the native symbiosis (Cipollini et al. 2012). A well-known example involves Alliaria petiolata (Fig. 9b), a European invader of North
American forests, which suppresses native plant growth by actively
disrupting mutualistic associations between native canopy tree seedlings and both AM (Stinson et al. 2006) and ectomycorrhizal (Wolfe
et al. 2008) fungi. Suppression of North American mycorrhizal fungi
by A. petiolata corresponds to decreased growth of North American
plant species that rely heavily on fungal symbionts (Callaway et al.
2008) and changes in AM fungal community composition (Barto
et al. 2011).
A third outcome is that an introduced plant species is unable to
establish because the new habitat is void of the appropriate symbiont. In accordance with Principle 2, host fitness will depend
strongly on the biotic context: in these cases, the lack of specific
mycorrhizal propagules can be a critical factor in slowing invasion
of fragile habitats. For example, initial plantings of pine (Pinus sp.;
Review and Synthesis
Fig. 9c) in the southern hemisphere often failed because of the
absence of the necessary ectomycorrhizal fungi (reviewed in Pringle
et al. 2009). Ironically, after the appropriate fungal symbionts are
introduced to the environment, pine has become a problematic
invasive species in many areas of the world (Nu~
nez et al. 2009).
Exotic pine species have been shown to host exotic ectomycorrhizal
fungi, and their spread into new habitats is essentially a co-invasion
of exotic fungi and its host (Dickie et al. 2010). Although some
attention has been paid to the potential dangers of the application
of commercial products to purposely introduce mycorrhizal fungal
inoculum into novel habitats (e.g. Schwartz et al. 2006), this area
requires more research, especially in situations where fungi introduced as inoculum can become invasive (Jairus et al. 2011), or can
facilitate invasion of exotic plant species.
Changes to biota: land-use changes
Humans have fragmented or removed over half of the global and
temperate broadleaf and mixed forests, and roughly one quarter of
the tropical rainforests (Wade et al. 2003). This is worrying because
forests store ~45% of terrestrial C and contribute ~50% of terrestrial net primary production (Bonan 2008). Similar to invasions by
introduced species, land-use change can dramatically alter native
mycorrhizal symbioses, forcing changes in the aboveground community, and revealing feedbacks in the belowground community. At
a global scale, the loss of forests and heathlands and the gain of
deserts and croplands will reduce the abundance of ecto and ericoid
mycorrhizas and increase the abundance of arbuscular mycorrhizas
(Fig. 3). These changes may have major impacts on soil properties,
heterotrophic respiration and the potential for belowground C
sequestration.
A review of the literature suggests that if clear-cut forests are
replanted with tree seedlings, mycorrhizal colonisation of the seedlings is generally not reduced; however, there are often dramatic
shifts in the species composition of ectomycorrhizal fungi (Jones
et al. 2003; Curlevski et al. 2010). These changes in fungal communities are likely driven by physical, chemical and biological changes in
the reforested environment. It has been suggested that post-disturbance communities of ectomycorrhizal fungi may better aid their
hosts under the altered environmental conditions (Jones et al. 2003).
This seems likely because the deforestation and reforestation process is likely to have a dramatic impact on the organic horizon of
the forest floor and species of ectomycorrhizal fungi differ in their
enzymatic capabilities to acquire nutrients from detritus (Bu"ee et al.
2007; Pritsch & Garbaye 2011). Future studies are needed to determine whether symbiotic function and fungal fitness are optimised in
the mycorrhizas that reassemble following disturbance.
Conversion of diverse natural forests to plantations of exotic tree
species may reduce species richness as well as change the composition of the native community of mycorrhizal fungi. Introduced Pinus
contorta in New Zealand was found to host only 14 fungal species
(93% were exotic), while co-occurring endemic Nothofagus solandri
hosted 98 species of native ectomycorrhizal fungi (Dickie et al.
2010). A comprehensive study suggested that even if species richness of ectomycorrhizal fungal communities is maintained, the species composition is generally altered when native forests are
converted to plantations (O’Hanlon & Harrington 2012). This result
was confirmed in a study investigating the effects of conversion of
native forest to avocado plantations; differences in mycorrhizal
Mycorrhizas and global change 149
composition, but not richness, were found (Gonzalez-Cortes et al.
2012). In accordance with Principle 2, changes in species composition can have strong functional consequences for biotic interactions,
raising the risk that future conversion back to native forest will be
problematic. For example, changes in the community composition
of mycorrhizal fungi have been shown to constrain the re-establishment of desired flora (William et al. 2011).
Tropical forest fragmentation and conversion to agricultural systems has been shown to negatively affect AM fungal interactions,
with root colonisation, spore diversity and spore abundance positively correlated to fragment size, which is also negatively correlated
with soil N and P availability (Grilli et al. 2012). In accordance with
Principle 1, optimal allocation, we would expect higher soil fertility
in fragmented plots to be correlated with a reduction in mycorrhizal
fungi, as was found (Fig. 10).
With a growing interest in the functioning of mycorrhizal communities in agricultural systems, significant progress has been made
in studying how land management regimes affects AM fungal communities. For instance, differences in the composition of fungal
communities are often noted in high vs. low tillage regimes (Alguacil et al. 2008) and when grasslands, organic and conventional agricultural systems are compared (Verbruggen et al. 2010). These
studies indicate that disturbances such as tillage – which disrupts
AM hyphal networks – can negatively affect crop-mycorrhizal interactions compared to when hyphal networks are left intact (Verbruggen & Kiers 2010). Principle 3 suggests that intact networks of AM
fungi have the ability to adapt rapidly to environmental changes by
alterations in nucleotype frequencies within hyphal networks. This
could explain the surprising resilience of AM fungal communities
when, for example, fires drove the conversion of a Costa Rican dry
tropical forest to a monoculture of African grass (Johnson & Wedin
1997). Whether all mycorrhizal communities can recover when land
is restored after disturbance is far from clear: long-term effects of
disturbance appear to be very site specific (e.g. Tedersoo et al.
2011). Understanding the patterns of recovery after major and
minor land-use changes is critical for predicting community level
responses. This knowledge hinges on first understanding the composition of mycorrhizal fungal communities in natural undisturbed
ecosystems. Very few studies have assessed mycorrhizal fungi in
natural habitats and there is an urgent need to recognise the importance of protecting natural areas for the preservation of these
unseen, but important organisms so that future studies can use
these as reference sites to guide ecosystem restoration efforts
(Turrini & Giovannetti 2012).
Although loss of biodiversity is a major concern, loss of global carbon stores may be an even more pressing issue under current global
change trajectories. The density of mycorrhizal hyphae in grasslands
is often strongly correlated with soil organic C content (Wilson et al.
2009). Over the past century, natural grasslands have been increasingly converted to cropland, accelerating soil erosion, land degradation and releasing soil organic C stores (Qiu et al. 2012). Although
careful management of ectomycorrhizas may help increase soil C
sequestration within forest ecosystems (Hoeksema & Classen 2012),
conversion of natural grasslands into tree plantations for C mitigation
projects may be misguided. This is particularly true if ectomycorrhizal
fungi that are introduced with the exotic trees may access C pools not
available to the native AM fungi and actually increase C lost through
respiration (Chapela et al. 2001). Does the short-term gain of an
aboveground C-sink (wood) outweigh the long-term loss of a below© 2013 John Wiley & Sons Ltd/CNRS
150 N. C. Johnson et al.
Review and Synthesis
Total AMF spores abundance 100 g soil
Total mycorrhizal colonization (%)
105
95
85
75
65
55
45
35
135
115
95
75
55
35
15
50
45
105
40
85
35
NH4+ (ppm)
P (ppm)
125
155
65
45
25
25
20
15
10
5
–15
–0.5
30
5
0.5
1.5
2.5
Log area (ha)
3.5
0
–0.5
0.5
1.5
2.5
3.5
Log area (ha)
Figure 10 Relationship between fragment size of Chaco forest in Co′rdoba, Argentina and the abundance of mycorrhizas, and the availability soil P, and N. Top left,
total mycorrhizal colonisation of roots from Euphorbia acerensis (filled diamond) and E. dentate (open square). Top right, abundance of AM fungal spore abundance per
100 g of soil. Bottom left, concentration of soil P (ppm). Bottom right, concentration of soil NH4+ (ppm). Means ! SE (n = 8). Data courtesy Grilli et al. 2012.
ground C storage in recalcitrant organic compounds (Drake et al.
2011)? Given the current trajectory of land conversion as demands
for food and agricultural commodities rise, more research is needed
to provide reliable estimates of long-term C storage in above and
belowground reservoirs across different types of ecosystems (Reich
2011). Mycorrhizas are an important component of belowground
C-budgets and projections of future C-dynamics (Drake et al. 2011).
FUTURE RESEARCH DIRECTIONS
Development of strategies to conserve and manage mycorrhizas for
their benefits in food and fibre production, soil stabilisation, belowground C sequestration and natural area and biodiversity protection
will require a coordinated effort. Recent advances in technological
platforms, computation science and electronic communication will
provide the opportunity to integrate knowledge across disciplines
and interest groups to generate an increasingly comprehensive
understanding of the role of mycorrhizal symbioses in ecosystems.
This will be driven by collaborative research among a diversity of
workers. We envision that contributions by five different groups
will be particularly useful:
1 Partnerships with foresters, agronomists and ecosystem scientists
to sample mycorrhizas in plants and soils across a global-scale gradient of biomes including all major arable systems and soil types. This
effort should be coordinated with ongoing long-term research networks and utilise existing data sets to the fullest possible extent.
2 Collaborations with molecular biologists to apply high throughput technologies to look for hypothesised functional patterns in the
samples collected from around the world. This effort should use a
‘community genetics’ approach and analyse whole assemblages of
© 2013 John Wiley & Sons Ltd/CNRS
genotypes with the ultimate aim of linking the genes to ecosystem
processes (e.g. He et al. 2010; Johnson et al. 2012). This analysis
should also focus on the level of individual organisms to assess the
genetic variability within populations of mycorrhizal fungi and their
hosts. This information is necessary to test hypotheses about the
tempo and mode of mycorrhizal responses to a changing environment.
3 Collaborations with biochemists to identify the enzyme systems
expected for catabolism of the dominant organic and inorganic
forms of essential soil nutrients under different chemical and physical environments. This knowledge will inform hypotheses about the
potential role for mycorrhizas in C, N and P dynamics in changing
environments.
4 Work together with systems modellers to incorporate mycorrhizas into currently existing (e.g. Meyer et al. 2010; Orwin et al. 2011)
and new models to test hypotheses about the role of soil feedbacks
for C-dynamics (including sequestration), erosion, nutrient retention,
ecosystem productivity and climate.
5 Perhaps most importantly, research findings should be used to
inform resource management. This requires direct participation of
the people (farmers, foresters and land managers, etc.) who are conducting the management actions on a day-to-day basis. They are
essential in providing the solid grounding and a practical perspective
on the systems that we are trying to understand.
The potential to mitigate undesirable effects of anthropogenic
changes to the environment is a ‘tantalising prospect for the future’,
that will require a coordinated effort of reductionist and multifactorial approaches (Singh et al. 2010). Granting agencies are increasingly providing support for crosscutting research efforts. There is
Review and Synthesis
no better time for mycorrhizal researchers to develop ‘mutualistic
associations’ with co-workers in other fields.
ACKNOWLEDGEMENTS
We thank M. Rillig for logistical support and Matthew Bowker for
helpful comments on an earlier version of this manuscript. Nancy
C. Johnson is funded by the National Science Foundation of the
USA (DEB-0842327); E.T. Kiers is funded by the Dutch Science
Foundation (NWO) ‘vidi’ and ‘meervoud’ grants; I.R. Sanders is
funded by the Swiss National Science Foundation (31003A-127371);
and C. Angelard is funded by a Marie Curie Outgoing International
Fellowship within the 7th European Community Framework Program (PIOF_GA_2009-251712). We apologise to the many authors
of relevant papers that could not be cited due to space constraints.
AUTHORSHIP
NCJ developed the conceptual framework and wrote many sections
of the manuscript. Throughout all stages, ETK provided ideas and
editorial suggestions. Also, ETK wrote the sections on invasive species and land-use change. IRS and CA wrote the sections on genetic
mechanisms, and ‘principle 3’, in particular. CA created almost all
of the Figures.
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Editor, John Klironomos
Manuscript received 1 October 2012
First decision made 4 November 2012
Manuscript accepted 26 December 2012
© 2013 John Wiley & Sons Ltd/CNRS