A leap forward in geographic scale for forest ectomycorrhizal fungi

Abstract

Conclusion The functionally critical role of mycorrhizal fungi in forest ecosystems, and the imminent threat of climate change that may
act to alter mycorrhizal functional biodiversity, means there is an urgent need for a regional to continental-scale assessment
of mycorrhizal distributions. Until recently, it had not been possible to cost-effectively assess mycorrhizas precisely and
accurately. A large-scale survey of ICP Forests plots would be only the first stage in answering many of the questions outlined
above, but it is essential if future studies are going to address these questions with hypothesis-driven research in a cohesive
manner, rather than remain independent for lack of a unified approach. The chance to utilise the vast network of biomonitoring
plots at this time is a remarkable opportunity because it minimises the logistics and costs associated with achieving such
an enormous effort and provides a rare stable — past and future — ground for forest ecosystem scientific investigation. In
the face of rapid global change, we finally have an opportunity to accurately integrate mycorrhizal distribution data with
long-term environmental monitoring, providing a basic understanding of functionally crucial organisms, and at the same time
creating an invaluable resource for future research.

Full text

Ann. For. Sci. 67 (2010) 200 Available online at:
c
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DOI: 10.1051/forest/2009107 Letter to the editor
A leap forward in geographic scale for forest ectomycorrhizal fungi
Filipa Cox1,2,3*,NadiaB
arsoum3, Martin I. Bidartondo1,2, Isabella Børja4,ErikLilleskov5,
Lars O. Nilsson6,PasiRauti o7,KathTubby3,LarsVesterdal6
1Royal Botanic Gardens, Kew TW9 3DS, UK
2Imperial College London, London SW7 2AZ, UK
3Forest Research, Alice Holt Lodge, Farnham, Surrey GU10 4LH, UK
4Norwegian Forest and Landscape Institute, P.O Box 115, 1431, Ås, Norway
5USDA Forest Service, Northern Research Station, 410 MacInnes Dr., Houghton, MI, 49901, USA
6Forest and Landscape Denmark, University of Copenhagen, Hørsholm Kongevej 11, 2970 Hørsholm, Denmark
7Finnish Forest Research Institute, Rovaniemi Research Unit, Etelaranta 55, 96300, Rovaniemi, Finland
(Received 30 August 2009; accepted 18 November 2009)
Keywords: biogeography /ICP Forests /function /mycorrhizas /symbiosis
In this letter we propose a first large-scale assessment of
mycorrhizas with a European-wide network of intensively
monitored forest plots as a research platform. This effort
would create a qualitative and quantitative shift in mycorrhizal
research by delivering the first continental-scale map of myc-
orrhizal fungi. Readers may note that several excellent detailed
accounts of ectomycorrhizal biology, including its method-
ological and conceptual strengths and weaknesses, are avail-
able elsewhere (e.g., Peay et al., 2008; Smith and Read, 2008;
Taylor, 2002). Although we focus on a specific group of fungi
in this letter, many of the methods and ideas discussed could
be extended to include communities of other groups of forest
fungi, such as saprobes and pathogens.
Ectomycorrhizal (ECM) fungi form intimate symbioses
with most temperate and boreal tree species, playing a piv-
otal functional role in the uptake of nutrients, as well as pro-
viding protection against pathogens and drought (Baxter and
Dighton, 2005). In exchange, the tree host supplies ca. 15% of
its current photoassimilate to the fungi (Hobbie and Hobbie,
2006; Smith and Read, 2008). The diversity of ECM fungi is
high, with estimates of over 7 000 species worldwide, asso-
ciating with approximately 8 000 plant species (Rinaldi et al.,
2008; Wang and Qiu, 2006), leading to research efforts into the
degree of functional diversity within ECM fungi. It is known,
for example, that different species of ECM fungi can access
alternative nitrogen sources (Lilleskov et al., 2002b), and that
certain ECM species may play a role in the decomposition of
organic carbon (Chapela et al., 2001); some fungi confer more
benefit to their host than others under certain environmental
conditions (Gorissen and Kuyper, 2000; Johnson et al., 1997),
and different species of fungi can have different carbon re-
quirements from the host (Bidartondo et al., 2001; Fransson
* Corresponding author: f.cox06@imperial.ac.uk
et al., 2007). Therefore, the biodiversity of ECM fungi in any
given forest is likely to have direct implications for host tree
health, carbon and nitrogen cycling, and the resiliency of forest
functional biodiversity. Because forests are major players in
the sequestration of atmospheric carbon, it is critical to under-
stand the processes acting to maintain forest ecosystem func-
tion. To gain an understanding of factors that influence the
mycorrhizal communities of forests, studies have used both
natural gradients and manipulative experiments, demonstrat-
ing that pH, soil type, moisture, host tree species and ni-
trogen availability, amongst others, are determinants of my-
corrhizal communities at local scales (e.g. Børja and Nilsen,
2009; Gehring et al., 1998;Kauserudetal.,2008; Lilleskov
et al., 2002a).
Given the observed responsiveness of mycorrhizal fungi
to shifts in environmental variables and global environmental
change, it is of immediate concern to know how mycorrhizal
communities will respond to environmental shifts at the re-
gional and continental scale, and what effects such shifts will
have on forest health and function. This task requires knowl-
edge about current mycorrhizal distributions, both to provide
a baseline against which to measure changes in communities,
and to understand the effect of broad-scale environmental con-
ditions (e.g., annual temperature, latitude, rainfall) on mycor-
rhizal biogeography. Whilst it would be convenient to extract
these data from the numerous investigations of local ECM
fungal communities carried out so far, the diversity of sam-
pling methodologies employed makes this an impossible task.
A primary disparity is that much research has relied upon mor-
phology of reproductive structures (fruitbodies) and/or myc-
orrhizal roots to establish fungal identity, whilst more recent
studies tend to apply various DNA techniques to mycorrhizas
to identify fungi, posing problems when comparing datasets
Article published by EDP Sciences

Ann. For. Sci. 67 (2010) 200 Filipa Cox et al.
basedonthetwodifferent methodologies (Gardes and Bruns,
1996; Horton and Bruns, 2001). In addition, most studies do
not collect environmental data in a consistent fashion, mak-
ing incorporation of data from multiple studies into a single
predictive model extremely challenging.
Methodological inconsistencies aside, the responses of my-
corrhizal communities to changes in environmental conditions
appear to be complex, and it is difficult to confidently iden-
tify trends across studies. This is probably due to the localized
nature and constrained time-scale at which most studies have
been carried out, making results highly context-dependent.
Particular site characteristics, pre-existing ECM fungi, and the
scale of environmental change being studied, may all play
a part in generating the complex picture of ECM fungal re-
sponses to specific environmental changes we see when com-
paring studies. It was in this context that Lilleskov and Parrent
(2007) recently called for the development of a large-scale,
unified approach to ectomycorrhizal research, which would al-
low the distributions of individual species of ECM fungi to
be mapped. Here we identify a specific research platform and
strategy aimed at meeting this challenge, through the utilisa-
tion of one of the largest biomonitoring networks on Earth.
ICP FORESTS – AN INVALUABLE PLATFORM
FOR LARGE-SCALE RESEARCH
The International Co-operative Programme on Assessment
and Monitoring of Air Pollution Effects on Forests (ICP
Forests, http://www.icp-forests.org) was launched in 1985.
The programme is operated under the United Nations Eco-
nomic Commission for Europe Convention on Long-Range
Transboundary Air Pollution that is ratified by 51 parties. The
over-arching aim of ICP Forests is to understand the links be-
tween forest health, air pollution, climate change and biodiver-
sity, through the establishment and monitoring of two comple-
mentary networks of forest plots. The first of these networks
(called Level I) includes over 6 000 forest plots, set-up on
a16×16 km grid across Europe, each monitored for tree
crown condition (defoliation, discoloration and visible dam-
age). Many Level I plots have been extended to undergo more
extensive monitoring as part of the BioSoil program, which
aims to develop a common baseline of European forest soils,
as well as assessing forest biodiversity. A further subset of
800 strategically located plots (Level II) forms an intensive
continual monitoring system. Here, additional measurements
include tree growth and phenology, ground vegetation, atmo-
spheric deposition, soil chemistry, soil solution chemistry, fo-
liar nutrient levels, and water balances. Expert panels are in
place to ensure the harmonisation of methods used in the field,
and quality assurance and control in laboratories. These net-
works cover the major tree species in Europe, and involve the
participation of 41 countries.
The ICP Forests network provides mycorrhizal researchers
with a huge and largely un-tapped resource on which to con-
duct a large-scale assessment of distributions, measure re-
sponses to environmentalgradients, and link communitycom-
position directly to forest ecosystem function. The intensively
monitored Level II plots of the ICP Forests programme confer
a number of advantages: (i) pre-established and maintained
plots enable and facilitate project design, (ii) access to an exist-
ing, large, and harmonized forest monitoring dataset, (iii) ac-
cess to information on site history, management practices and
disturbances, allowing individual studies to control for, or
take into account, specific inter-site variables, and (iv) a long-
term perspective to detect, and validate predictions for, future
change.
METHODOLOGICAL CONSIDERATIONS
Selection of sites across the ICP network can be random-
ized, or based on a statistically rigorous algorithm that strati-
fies sampling across the variables hypothesizedto control fun-
gal distribution at multiple scales. Ensuring adequate sampling
across these variables can lay the foundation for rigorous mod-
elling of species- and community-environment relationships to
serve as the basis for predictions of current and future mycor-
rhizal communities across Europe.
Reliable across-site comparisons are difficult when sam-
pling is not of sufficient intensity to capture species diver-
sity (Peay et al., 2008;Taylor,2002). Before launching into
a large-scale study of ECM communities in forests plots, it
would be ideal to first develop a standardised sampling design
which maximises the chance of fully capturing ECM species
diversity within plots, and this will likely require iterative fine-
tuning as the project develops. Preliminary data on the number
of samples required, and the scale at which samples should be
taken to ensure independence, are currently available for pine,
beech, oak, and spruce plots (F. Cox, unpublished data).
Identification of fungi colonising roots, versus fungi present
in the soil as hyphae, can give contrasting views of the ECM
fungal community (Koide et al., 2005), and the collection of
both can provide a better overall picture of mycorrhizal diver-
sity than one method in isolation of the other. High-throughput
molecular ecology techniques would be essential for generat-
ing data with the speed and efficacy required for such a large
study, and novel techniques such as pyrosequencing (e.g.,
Buee et al., 2009) may complement this approach, particu-
larly if and when sample throughput increases so that bulk-
ing of roots and/or soil can be avoided. These technologies
are in their infancy, and sampling methodologies still need
to be validated to ensure accurate characterisation of fungal
communities. For example, a recent study has shown that cur-
rent methods of pooling samples can lead to inaccurate fun-
gal community descriptions (Avis et al., 2009). Level II sites
in which the ECM fungal community have previously been
well characterised using Sanger sequencing of individual root
tips, may offer a useful baseline upon which to validate new
methodologies associated with these techniques.
Species delimitation of ECM fungi can be standardized
initially by relying on nuclear ribosomal internal transcribed
spacer DNA sequence similarity cut-offs to provide repro-
ducible estimates of species boundaries (Nilsson et al., 2008),
whilst multi-locus analyses, taxonomic collections and exper-
tise will be useful when linking species names to DNA se-
quences (Brock et al., 2009;Hedhetal.,2008). The gradual
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A continental survey of forest mycorrhizas Ann. For. Sci. 67 (2010) 200
development of a publicly accessible online data-base of ECM
fungal distributional data, and DNA sequence alignments of
closely related taxa, would be an exceptionally useful outcome
of this research for the scientific community.
IMMEDIATE RESEARCH OUTCOMES
FROM A CONTINENTAL ASSESSMENT
A continental-scale survey of ECM fungi would produce
immediate research outputs, as well as providing data key
to the development of local and regional scale research that
is ecologically relevant and hypothesis-driven. Carrying out
a large-scale assessment of ECM fungi in plots throughout
Europe would dramatically improve our understanding of the
factors that drive function and biodiversity of mycorrhizal
trees and fungi in a number of ways (Fig. 1, Phase 1).
The primary benefit of distribution data would be the ability
to identify patterns in ECM community composition in forests
across geographic regions, and link this to broad environmen-
tal variables recorded at each sampling location. With these
data, it should be possible to predict mycorrhizal communities
in un-sampled European forests as a result of site character-
istics via GIS layers, enabling the mapping of current fungal
distributions across the continent. Whilst predicting the dis-
tributions of infrequent species that constitute the major part
of fungal diversity will prove challenging, realistic predictions
for dominant taxa should be achievable, and they would rep-
resent a test of the power of predictive mapping. A baseline
map, combined with information about dynamic responses to
changing environmental conditions, can also allow the predic-
tion of future distributions of dominant species as a result of
changes in climate, atmospheric pollution and land use (Ellis
et al., 2007).
Currently, mycorrhizal species ranges based on fruitbody
collections have been described for some ECM fungal species
at national scales (e.g., Courtecuisse et al., 2008). However,
these data are lacking for the majority of species, do not take
into account below-ground presence, and are poorly “harmo-
nizable” over the continental scale due to differing morphos-
pecies concepts. Through DNA sequence based distribution
maps, we could infer the extent to which geographic disper-
sal constraints act on mycorrhizal fungal species distributions,
and how these differ among species, higher taxonomic levels,
and functional guilds.
Continental scale distribution data would also allow us to
identify the most abundant and widespread mycorrhizal fungi
across Europe, providing a prioritized list of fungal species
to target as models for future research (e.g., genetics, ecol-
ogy, physiology, genomics), increasing its applicability and
relevance.
Linking environmental and mycorrhizal community data
will allow the effects of variables such as temperature, rain-
fall, and soil type on the community assemblage of ECM fungi
to be tested. These data would identify broad niches for indi-
vidual species (host type, soil type, climatic constraints). In
particular, we would be able to extend and test existing knowl-
edge on mycorrhizal specialists and generalists (e.g., Molina
et al. 1992) and edaphic endemics. In addition, we would test
and identify fungi sensitive to particular agents of pollution,
such as atmospheric N deposition and oxidants. It may also be
possible for mycorrhizal community data to be linked directly
to data on the composition of ground flora and environmen-
tal characteristics. Although such inferences would be limited
by the power of regression and correlation analyses, they can
still point the way forward for experiments designed to pro-
vide a mechanistic understanding of fungus-environment in-
teractions.
Analysis of mycorrhizal diversity across ICP Forests plots
would allow us to identify geographic areas with the great-
est diversity, as well as areas of endemism. These mycorrhizal
“hotspots” can then be the target for habitat conservation ac-
tion to maintain soil biodiversity. In combination with envi-
ronmental and geographic data, we should be able to model
the factors that are likely contributors to hotspot generation,
leading to predictions of hotspots elsewhere.
Although mycorrhizal fungi are less understood compared
to other large perennial organisms, there is nevertheless evi-
dence of a sharp decline in the reproductive output of some
mycorrhizal fungi in polluted regions of Europe (Arnolds,
1991). Currently, declining, “Red list” and locally extinct my-
corrhizal fungi are assessed and monitored only through their
sporadic and ephemeral reproductive structure production.
This information does, however, constitute a warning signal
to uncover their distribution and source/sink dynamics below-
ground at the continental scale. Reliable large-scale distribu-
tion data would allow the conservation status of individual
species to be assessed – species not previously considered rare
may be identified as targets for conservation activities, and
vice-versa. By sampling a large geographic area belowground,
we will also have the opportunity to improve our imprecise
estimates of the total number of ECM fungal species (Rinaldi
et al. 2008), and discover what proportion have not been taxo-
nomically described to date.
Lessons learnt from studies like these would undoubtedly
inform work on communities of other groups of forest fungi
which also play pivotal roles in forest vitality, and could pro-
vide basic knowledge to help design and carry out studies on
general fungal biogeography.
SMALLER-SCALE RESEARCH FACILITATED
BY DISTRIBUTIONAL DATA
A European survey of forest mycorrhizas is imperative
to the development of further research and model systems
that are focused, hypothesis-driven, and ecologically relevant.
There are a number of key areas of ecosystem and mycorrhizal
research that would be directly informed by a European survey
in ICP Forests plots (Fig. 1, Phase 2).
The identification of dominant mycorrhizal species by indi-
cator species analyses would be a first step for many potential
future studies. The development of species-specific primers
would permit the quantification of ECM in both rootsand soils
of plots known to contain the mycorrhizal species of interest.
Dominant fungal taxa could also be targeted for the next se-
quencing programs of fungal genomes, which would provide
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Ann. For. Sci. 67 (2010) 200 Filipa Cox et al.
Figure 1. The potential research outputs of a European-wide survey of mycorrhizal fungi in biomonitoring plots. Rectangles represent a research
effort, ovals indicate a research output and diamonds indicate an instance when data gathered from ICP Forest plots would enhance research
efforts. Phase 1: Whilst the primary research achievement would be European-wide distributional data for mycorrhizal fungi, a number of
immediate secondary research outputs would also be generated. Combining the mycorrhizal fungal survey data with environmental data would
be critical to the development of Phase 2, which focuses on ecologically-relevant and hypothesis-driven research at smaller scales. Combining
these data with tree health and environmental data can pinpoint key links between shifts in mycorrhizal fungal community composition and
forest ecosystem health. ICP: The International Co-operative Programme on Assessment and Monitoring of Air Pollution Effects on Forests.
genetics markers to gain some of the first insights into the pop-
ulation structure, recombination levels, genet size and overlap,
as well as the extent and direction of gene-flow and dispersal
between geographically separated populations (e.g., Kretzer
et al., 2004).
The importance of mycorrhizalfungi as carbon sinks in for-
est ecosystems (Högberg et al., 2001; Smith and Read, 2008),
and the potential for carbon demand to change due to elevated
CO2and elevated nitrogen availability (Alberton and Kuyper,
2009; Bidartondo et al., 2001), makes it necessary to under-
stand the role of mycorrhizal fungi in global carbon and ni-
trogen dynamics. A critical area for research will be whether
evenness shifts, replacement of dominants, and allocation to
root colonisation vs. soil colonisation as a result of environ-
mental change will alter the carbon sink potential of forest
ecosystems.
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A continental survey of forest mycorrhizas Ann. For. Sci. 67 (2010) 200
Pre-characterised mycorrhizal communities in ICP Forests
plots would provide an unrivalled platform for experimental
manipulations, such as nitrogen fertilisation. By selecting sites
with similar initial mycorrhizal species composition, treating a
subset of these sites, and then comparing the degree and direc-
tion of any changes in the mycorrhizal communities between
treatment and control groups, the effects of elevated N avail-
ability could be ascertained at a larger scale, and in a more
informed, replicated and controlled way, than has ever been
possible.
Finally, assessing micro-scale habitats for a range of factors
(e.g., soil pH, moisture, organic matter, coarse woody debris,
nutrient availability), should allow correlations between the
presence and/or abundance of mycorrhizal species and specific
environmental conditions. When conducted at several sites, ro-
bust inferences about niches of individual fungi can be made,
with implications for forest management practices (e.g., re-
moval of brash and other deadwood) that alter the availability
of micro-niche sites.
CONCLUSION
The functionally critical role of mycorrhizal fungi in forest
ecosystems, and the imminent threat of climate change that
may act to alter mycorrhizal functional biodiversity, means
there is an urgent need for a regional to continental-scale as-
sessment of mycorrhizal distributions. Until recently, it had
not been possible to cost-effectively assess mycorrhizas pre-
cisely and accurately.A large-scale survey of ICP Forests plots
would be only the first stage in answering many of the ques-
tions outlined above, but it is essential if future studies are go-
ing to address these questionswith hypothesis-drivenresearch
in a cohesive manner, rather than remain independent for lack
of a unified approach. The chance to utilise the vast network
of biomonitoring plots at this time is a remarkable opportunity
because it minimises the logistics and costs associated with
achieving such an enormous effort and provides a rare stable –
past and future – ground for forest ecosystem scientific inves-
tigation. In the face of rapid global change, we finally have
an opportunity to accurately integrate mycorrhizal distribution
data with long-term environmental monitoring, providing a ba-
sic understanding of functionally crucial organisms, and at the
same time creating an invaluable resource for future research.
Acknowledgements: We would like to thank the NERC Centre
for Population Biology and the Alice Holt Research Centre (For-
est Research) for hosting the symposium from which this work
stems; and the two anonymous reviewers for their helpful com-
ments. This work was supported by a NERC Case Studentship
(NER/S/A/2006/14012), and Forest Research’s Chief Executive
Fund.
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