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Monitoring ectomycorrhizal fungi at large scales for science, forest management, fungal conservation and environmental policy

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The ICP Forests network can be a platform for large-scale mycorrhizal studies. Mapping and monitoring of mycorrhizas have untapped potential to inform science, management, conservation and policy regarding distributions, diversity hotspots, dominance and rarity, and indicators of forest changes. A dearth of information about fungi at large scales has severely constrained scientific, forest management, fungal conservation and environmental policy efforts worldwide. Nonetheless, fungi fulfil critical functional roles in our changing environments and represent a considerable proportion of terrestrial biodiversity. Mycorrhizal fungi are increasingly viewed as a major functional guild across forest.
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ORIGINAL PAPER
Monitoring ectomycorrhizal fungi at large scales for science,
forest management, fungal conservation and environmental
policy
Laura M. Suz &Nadia Barsoum &Sue Benham &Chris Cheffings &Filipa Cox &
Louise Hackett &Alan G. Jones &Gregory M. Mueller &David Orme &Walt er S eidli ng &
Sietse Van Der Linde &Martin I. Bidartondo
Received: 30 June 2014 /Accepted: 12 December 2014
#INRA and Springer-Verlag France 2015. This article is published with open access at Springerlink.com
Abstract
&Key message The ICP Forests network can be a platform
for large-scale mycorrhizal studies. Mapping and moni-
toring of mycorrhizas have untapped potential to inform
science, management, conservation and policy regarding
distributions, diversity hotspots, dominance and rarity,
and indicators of forest changes.
&Context A dearth of information about fungi at large scales
has severely constrained scientific, forest management, fun-
gal conservation and environmental policy efforts world-
wide. Nonetheless, fungi fulfil critical functional roles in
our changing environments and represent a considerable
proportion of terrestrial biodiversity. Mycorrhizal fungi are
increasingly viewed as a major functional guild across forest
Handling Editor: Ana RINCON
Contribution of the co-authors All co-authors attended the workshop
in which this article is based and contributed to the generation of ideas
and their discussion. MI Bidartondo and LM Suz led the writing, helped
by essential comments and contributions of all co-authors.
L. M. Suz (*)
Royal Botanic Gardens, Kew, Richmond Surrey, England TW9 3DS,
UK
e-mail: l.martinez-suz@kew.org
N. Barsoum :S. Benham
Forest Research, Farnham, Surrey GU10 4LH, UK
N. Barsoum
e-mail: Nadia.Barsoum@forestry.gsi.gov.uk
S. Benham
e-mail: sue.benham@forestry.gsi.gov.uk
C. Cheffings
Joint Nature Conservation Committee, Monkstone House, City
Road, Peterborough PE1 1JY, UK
e-mail: Chris.Cheffings@jncc.gov.uk
F. Cox
School of Earth, Atmospheric and Environmental Sciences,
University of Manchester, Manchester M13 9PL, UK
e-mail: filipa.cox@manchester.ac.uk
L. Hackett
Woodland Trust, Kempton Way, Grantham NG31 6LL, UK
e-mail: LouiseHackett@woodlandtrust.org.uk
A. G. Jones
Earthwatch, University of Oxford, Mayfield House, 256 Banbury
Road, Oxford OX2 7DE, UK
e-mail: ajones@earthwatch.org.uk
G. M. Mueller
Chicago Botanic Garden, 1000 Lake Cook Road, Glencoe, IL 60022,
USA
e-mail: gmueller@chicagobotanic.org
D. Orme
Division of Biology, Imperial College London, Silwood Park, Ascot,
Berkshire SL5 7PY, UK
e-mail: d.orme@imperial.ac.uk
W. Seidling
Thünen Institute of Forest Ecosystems, Alfred-Möller-Str. 1,
16225 Eberswalde, Germany
e-mail: walter.seidling@ti.bund.de
S. Van Der Linde :M. I. Bidartondo
Imperial College London & Royal Botanic Gardens, Kew,
England TW9 3DS, UK
S. Van Der Linde
e-mail: s.van-der-linde@imperial.ac.uk
M. I. Bidartondo
e-mail: m.bidartondo@imperial.ac.uk
Annals of Forest Science
DOI 10.1007/s13595-014-0447-4
ecosystems, and our ability to study them is expanding
rapidly.
&Aims This study aimed to discuss the potential for starting a
mycorrhizal monitoring programme built upon the existing
forest monitoring network, raise questions, propose hypothe-
ses and stimulate further discussion.
&Results An overview of the state-of-the-art regarding forest
ectomycorrhizal ecology raises questions and recommenda-
tions for scaling up mycorrhizal assessments aimed at
informing a variety of stakeholders, with a new focus on
conservation and policy.
&Conclusion Fungal research and conservation are areas that
canbeinformedbyICPForestsandmayleadtousefulspin-
offs; research linked to long-term forest monitoring plots will
enhance the relevance of science and conservation.
Keywords Mycorrhizas .ICP Forests .Monitoring .Air
pollution .Indicator .Red list
1 Introduction
Nearly all tree roots in boreal and temperate forests form
ectomycorrhizas. These intimate fungusplant mutualisms
play crucial ecological roles by determining the nutrient ac-
quisition and drought tolerance of trees (Smith and Read
2008). There is concern that we lack baseline data on mycor-
rhizal species distributions and abundances against which to
assess the effects of global change (Courty et al. 2010;Kjøller
et al. 2012; Lilleskov and Parrent 2007;Peayetal.2010).
Research on mycorrhizas has been focused at local scales (i.e.
stand level), leaving a widely recognised gap in our under-
standing of patterns of diversity and their drivers at landscape,
regional, continental and global scales (Bruns 1995; Peay
et al. 2010). We still know very little about diversity and its
drivers for any key soil organisms above local scales, even
though various ecological processes are only apparent at much
larger spatial scales (Levin 2000). For ectomycorrhizal (ECM)
fungi, mapping, monitoring and evaluation need to reach
beyond national boundaries to reflect large-scale fungal dis-
tributions and their drivers of change.
The vast European forest monitoring network (www.icp-
forests.org) is an ideal study platform because its intensively
monitored long-term forest plots have tremendous potential
for developing and scaling up forest mycorrhizal research and
biomonitoring (Cox 2010; Cox et al. 2010a,b; Suz et al.
2014). In April 2014, a multidisciplinary workshop focused
on how the network can be used to investigate mycorrhizal
diversity and ecology at large scales (www3.imperial.ac.uk/
ecosystemsandenvironment/events/workshops/
nercimpactworkshops/macroecologyofmicrobes).
Presentations and discussions assessed the state-of-the-art,
findings from ECM communities in a pine study across
England and Germany (Cox et al. 2010b), a study of oak
plots across Europe (Suz et al. 2014) and from an ongoing
Europe-wide analysis of ECM fungi in spruce, pine and beech
plots carried out in plots belonging to this network and using
its rich in situ environmental data (listed below). The comple-
mentary needs and resources of the monitoring, nature con-
servation, scientific and forest management communities were
discussed. A new focus was generating data on ECM com-
munities to inform fungal conservation in the context of the
recent International Union for the Conservation of Nature
Initiative on Global Fungal Red Listing (Dahlberg and
Mueller 2011, iucn.ekoo.se). Participants included govern-
ment and NGO forest managers, government and academic
conservation experts and ecologists. The outcomes of discus-
sions and the questions raised are summarised here. The
overarching goals of this article are to stimulate debate, to
encourage expanding the spatial and temporal scales across
which studies are carried out and to explain the rationale
behind the ongoing assessments of mycorrhizas across
Europes forest monitoring network.
Overall, five main questions covering current knowledge
gaps were formulated: (1) What are the spatial patterns of
mycorrhizal diversity and community structure? (2) What are
the environmental and ecological factors that control mycor-
rhizal distributions at landscape and larger scales? (3) What
are the likely responses of dominant mycorrhizal fungi to
global change and how will they affect the long-term spatial
cohesion of communities? (4) Will communities change (e.g.
shifts in dominant species and/or extinction of certain fungi)
under changing environmental conditions, and if so, will these
changes affect forest growth and resilience to global change?
(5) How can forests be managed more sensitively to protect
and enhance the diversity and functions of fungi?
Progress in answering some of these questions is being
made by combining molecular ecology with geographic infor-
mation systems (e.g. Tse-Laurence and Bidartondo 2011)to
generate new data on ECM communities through sampling
forest plots belonging to the ICP Forests network. These ap-
proaches reduce previous analytical limitations in large-scale
mycorrhizal studies. Engaging stakeholders, such as forest
managers, conservationists and policy makers, is essential to
raise awareness, enhance collaborations and join fundraising
efforts to include mycorrhizal surveys in forest monitoring.
2 How to assess fungal distributions
The distinctive life cycles and growth forms of fungi (see Peay
et al. 2008 for an excellent review) pose unique challenges and
opportunities for mapping fungal species distributions at large
spatial and temporal scales. At present, the limited, typically
national, data available on fungal species distributions and
L.M. Suz et al.
how they change originate from studying the reproductive
structures visible to the naked eye that are formed by some
macroscopic fungi (e.g. mushrooms, truffles, crusts) (Arnolds
1991; Kauserud et al. 2012). Most of the more apparent
mushrooms (and to a lesser extent the more cryptic truffles
and crusts) are ephemeral (days to weeks) and sporadically
produced but have been recorded for over a century and are
well researched. Some fruiting bodies can be assessed in the
field via multi-year surveys. Reproductive structures are par-
tially represented in collections at museums for the purposes
of taxonomic research, some of which have been databased
and can be accessed via the public Global Biodiversity
Information Facility (www.gbif.org).
In addition to visible fruiting bodies, there are fungal
structures such as filaments (mycelium), dispersal propagules
(spores and sclerotia) and structures formed together with
plant host rootscalled mycorrhizasthat are all found in
the soil. These structures may not be visible to the naked eye
but can be much larger and/or longer-lived than reproductive
structurese.g. the average size of individuals of the ECM
fungus Suillus variegatus has been reported to range from 10
to 20 m (Dahlberg 1997) and sclerotia of the ubiquitous ECM
fungus Cenococcum geophilum might rest in soil for over 1,
000 years (Watanabe et al. 2007). Less well recorded and
researched than fruiting bodies are the soil filaments that are
also ephemeral (days to weeks) and the spores that are poten-
tially viable for years (Nguyen et al. 2012). Soil filaments can
be assessed through in-growth mesh bags or cores, and resis-
tant spores and sclerotia can be assessed via soil bioassays.
Spores and sclerotia of some ECM fungi can be abundant in
soil, forming spore banks analogous to the seed banks of
plants. This variety of forms merits thorough consideration
when designing field sampling and interpreting data.
Despite the relatively short life (weeks) of the individual
ECM roots, the diversity of ECM fungi can remain stable at
scales >10 cm (Cox 2010; Douhan et al. 2011;Izzoetal.2005;
Koide et al. 2007;Lianetal.2006). Crucially, ectomycorrhizas
are always present as nearly all roots are colonised by mycor-
rhizal fungieven under high nutrient availabilityas shown
by a meta-analysis (Cudlin et al. 2007). Sampling roots is thus
a convenient and efficient way to monitor active ECM popu-
lations likely to give a more complete characterisation of the
mycorrhizal communities present compared to spore, myceli-
um and fruiting body surveys. Functional traits of particular
interest in ectomycorrhizas are conferred by their soil explora-
tion types which are characterised by short, medium or long
filaments linking mycorrhizal roots to soil (Agerer 2001,2006)
and their ability to uptake organic nitrogen (N) (driven by the
production and release into soil of a battery of fungal enzymes,
some of which may degrade recalcitrant organic matter as a
side effect, Bödeker et al. 2014). Moreover, these functional
traits that define each exploration type can confer different
capabilities with regard to storing carbon and taking up and
translocating nutrients (Courty et al. 2010; Hobbie and Agerer
2010). We have seen that mycorrhizal communities in temper-
ate oak forests respond differently to environmental variables
depending on their soil exploration type (Suz et al. 2014).
Because the effects of changes in the presence and proportions
of different ECM functional groups across Europe may affect
the resilience of forests to environmental change, they need
more investigation. However, trait databases for mycorrhizas
are in their infancy (e.g. www.deemy.de) with only about 320
mycorrhizal types characterized, although information on soil
exploration strategies of 143 ECM genera has been recently
compiled (Tedersoo and Smith 2013).
As with other organisms, the main public information re-
pository for fungi as DNA sequence data is the International
Nucleotide Sequence Database (www.insdc.org), though some
specialised public sub-databases are also availablee.g.
UNITE for the fungal DNA barcode for identification (unite.
ut.ee) and MarjaAM for arbuscular mycorrhizal fungi
(maarjam.botany.ut.ee). These DNA databases effectively
integrate data from all fungal structures and life history stages.
Globally, it is estimated that most fungal species, particularly
those outside the developed world, await taxonomic descrip-
tion and are not yet represented in collections or databases
(Blackwell 2011). Of the fungi that have a taxonomic descrip-
tion, relatively few have been sequenced (Brock et al. 2009).
Some of these unknownfungiundescribed and/or
unsequencedcan be dominant belowground even in relative-
ly well-studied European forests (e.g. Cox et al. 2010b).
3 Monitoring mycorrhizas for improved forest
management
Since mycorrhizal communities are integral to most forest
ecosystems and play essential rolesaccessing different in-
organic and organic nutrient pools, conferring drought toler-
ance or plant resistance to pathogensthere is a need to better
understand how they vary among forest types, across environ-
mental gradients and management regimes in order to practice
more sensitive management (e.g. thinning, clearing, fire con-
trol, harvest regulation of edible mushrooms). There is evi-
dence, for example, that tree species composition influences
mycorrhizal communities (Ishida et al. 2007) and that there
are generalist and host-specific fungi (e.g. Molina et al. 1992).
Where non-nativemycorrhizas are imported on planted
trees, especially on non-native tree species (Pennington et al.
2011), what are the implications on existing mycorrhizal
communities, particularly in any neighbouring native tree
species stands? There are examples of invasive ECM
fungisee Vellinga et al. (2009)forareviewonECM
introductionssuch as the deadly European Amanita
phalloides in North America (Wolfe et al. 2010). Moreover,
what are the consequences of a much altered mycorrhizal
Monitoring mycorrhizas in ICP Forests
community? What is the link between major changes in forest
condition (e.g. dieback) and the structure of mycorrhizal com-
munities? It is intriguing that strong correlations have recently
been reported between eucalyptus forest decline, soil chemis-
try and ECM community structure (Horton et al. 2013).
There is also a gap in understanding how much the success
of forest restoration and afforestation is linked to restoring and
building mycorrhizal communities. For instance, is it neces-
sary to restore the mycorrhizal community of a native broad-
leaf woodland when converting from conifer to broadleaf or
vice versa? Baskin (1997) describes a number of cases where
highly disturbed forest soils no longer support the mycorrhizal
communities required for the successful establishment of sap-
lings, resulting in many failed reforestation attempts. The
protection, restoration and creation of woodland both near
and far from existing woodlands as well as conifer-broadleaf
transitions are of interest to many land managershow do
mycorrhizas drive or constrain these different practices? How
redundant are roles played by different ECM fungi in a forest?
Under which conditions those roles might become unique and
susceptible to disappearing? Many woodlands are heavily
fragmented, e.g. 74 % of English woodland is ca. 100 m from
a woodland edge (Riutta et al. 2014). Edge effects on light,
water and pollution are relatively well understood, but wood-
land edges typically represent strong mycorrhizal transitions
as well and these have only received limited attention (e.g.
Branco et al. 2013).
4 The present and future of global fungal conservation
The very limited existing fungal diversity and distribution data
(e.g. Fig. 1) are a critical gap in nature conservation; many
fungi are now known to have discrete distributions, similar to
those of animals and plants, but distribution and population
trend data for fungi lag far behind equivalent datasets available
for plants and animals. For detailed reviews of different aspects
of the importance of fungal conservation, see Pringle et al.
(2011) and others in the same issue of Fungal Ecology.
Historically, there has been some resistance to red listing from
within the fungal research community, largely due to a lack of
basic ecological information about species. Consequently, fun-
gi have long been overlooked by and left out of the influential
International Union for the Conservation of Nature (IUCN)
process of listing rare and endangered species to enhance their
protection (i.e. currently only one macrofungus and two
lichenised fungi are among the over 21,000 red-listed organ-
isms). This is particularly striking when we consider the im-
portant functional role of many fungi in ecosystems and also
the vast scale at which wild ECM forest fungi are commercially
harvested and exported (Sitta and Davoli 2012).
Undoubtedly, more diversity data are neededespecially
at large spatial and temporal scalesbut it is already possible
to identify targets and risk factors and to quantify uncertainty,
at least locally, nationally or regionally (Dahlberg and Mueller
2011; Lilleskov et al. 2011;Molinaetal.2011). A consistent
Fig. 1 A first geographic distribution map for the false truffle
Elaphomyces granulatusa dominant mycorrhizal fungus of pine
forests overlooked in fruiting body surveys due to its underground
fruiting that is currently a candidate for global red listinggenerated
using inverse distance-weighted interpolation on DNA sequences from
Level II pine sites and georeferenced GenBank accessions showing that
large-scale mapping of dominant ectomycorrhizal fungi is feasible
L.M. Suz et al.
problem for red listing of any particular species ishow to scale
up or extrapolate ecology and distribution information that
justifies the need for conservation of fungi at risk beyond
local, national or regional datasets, e.g. from relatively well-
studied Nordic, Dutch or Swiss fungi, to nearby countries,
pan-European scales and beyond. Generation time and
persistence are key considerations when assessing changes
in population size over time. Assessments following IUCN
guidelines are based on three generations. A key question for
fungal conservation remains developing biologically
meaningful, defensible estimations of generation times for
species of ECM fungi. The suggested generation times
presented in Dahlberg and Mueller (2011) need additional
validation from a diversity of species across disturbance gra-
dients, soil differences and host associations. Belowground
sampling coupled with population genetic studies of targeted
taxa/habitats can provide these needed data. How long do
fungi persist belowground under particular environmental
pressures (e.g. pollution)? What is the host range of obligate
symbiotic fungi? Thanks to research developmentslargely
driven by the molecular ecology revolution since the 1990s
many of these questions have been answered at local scales
and that has now finally been sufficient to attract interest and
support from IUCN, but extrapolation is risk-laden. The cur-
rent first IUCN Red Listing Initiative for Fungi can ultimately
lead to identifying endangered fungi, indicators of restoration
success (e.g. UK waxcap grasslands) and fungal diversity
hotspots or key fungal biodiversity areas. Better integration
between the research and conservation communities is urgent-
ly needed. The biomonitoring community can act as a natural
integrator with its platform for generating rigorous data on
mycorrhizal diversity, distribution, turnover (spatially and
temporally), host specificity, and responses to anthropogenic
stressors and land management issues that are key needs of the
fungal conservation community. These data are starting to be
captured through the first mycorrhizal sampling of diverse
ICP Forests plots. Ongoing communication between the con-
servation, research and biomonitoring communities and ten-
tative statistical modelling approaches will help ensure shar-
ing of data and ideas and also enable action on the ground in
terms of potential funding and site availability for research.
5 Ectomycorrhizas and conservation policy
Ongoing barcoding of sporocarps initiatives, population ge-
netic studies and regional collections database projects are
providing the comparative data needed to integrate roots and
other environmental samples to enable us to understand mul-
tiple aspects of biodiversity (taxonomic, ecological and genet-
ic) across various scales in ways never before possible. Issues
of scale and evidence quality are of paramount importance for
informing policy makers on conservation issues, particularly
if costly interventions, such as industry regulation, are re-
quired in order to achieve conservation objectives. For in-
stance, consideration of N deposition impacts needs to be
based on both small-scale experimental manipulations and
large-scale correlations between biodiversity change and de-
position gradients (see Stevens et al. 2011;Emmettetal.2011;
ROTAP 2012). Once small-scale manipulations are combined
with greater certainty that large-scale biodiversity change is
being driven by N deposition, then it becomes possible to
modify the critical value used in mapping and to start to infer
pressures and threats on protected sites (Whitfield et al. 2012).
Agencies such as the UK Joint Nature Conservation
Committee support national fungal red listing (i.e.
Boletaceae, Geastraceae), but they are also increasingly fo-
cused on acquiring information about fungal communities in
the context of a range of ecosystem processes (for instance
how N deposition will affect ecosystem function via impacts
on fungal communities), rather than only on rare and/or de-
clining species. Clear demonstrations of changes in mycorrhi-
zal communities with increasing N deposition analogous to
the changes that have been reported for other organisms
(Stevens et al. 2011; Emmett et al. 2011) are emerging from
analyses of ICP Forests mycorrhizal data (Cox et al. 2010b;
Suz et al. 2014). There are also some hints as to which traits
are likely to respond, e.g. soil exploration strategy. This leads
to the question of how fungi recover through spore banks and/
or via dispersal? And, when mycorrhizal community recovery
is relatively slow, how does it limit vascular plant recovery?
6 Why monitor mycorrhizas in the ICP Forest Network
Level II plots?
The ICP Forest Level II plots have been used successfully for
national (e.g. Helmisaari et al. 2009) and increasingly for
trans-national (e.g. Clarke et al. 2011; Cox et al. 2010b;
Kristensen et al. 2004) research. European forests are uniquely
suitable and tractable for the study of mycorrhizas because (1)
there is relatively low forest biodiversity compared to North
America and Asia, (2) an extensive and intensive forest mon-
itoring network is available, (3) over 95 % of forest area is
covered by ECM trees, (4) fungi are relatively well-
characterised compared with other areas of the world and (5)
there are strong natural and anthropogenic environmental
gradients (e.g. pollution, Taylor et al. 2000). Thus, it is an
excellent place to generate understanding and predictions on
the behaviour of the natural environment and its resources by
developing and testing bioindicators, contributing to assess-
ments of carbon sequestration, macronutrient cycling, and
identifying biotic and abiotic causeeffect relationships re-
sponsible for biome condition. There are about 800 intensive-
ly monitored (Level II) plots, 0.25 ha each, covering Europes
major forest types. Monitoring in Level II plots includes (1)
Monitoring mycorrhizas in ICP Forests
continuous measurement of atmospheric deposition, soil so-
lution chemistry and meteorology; (2) biannual measurement
of foliar chemistry (i.e. C, Ca, Cd, Cu, Fe, K, Mg, Mn, N, P,
Pb, S, Zn); (3) annual measurement of crown condition; (4)
recording of tree growth and understory vegetation every
5 years; and (5) decadal measurements of solid phase param-
eters (most recently 20062007). Soil solution chemistry pa-
rameters include organic C, total N, carbonates, exchangeable
acidity, exchangeable cations, Al, Ca, Cd, Cr, Cu, Fe, Hg, K,
Mg, Mn, Na, P, Pb, S, Zn and total elements. Physical soil
structure is characterised using organic layer weight, percent-
age of coarse fragments, bulk density, particle size distribu-
tions, clay, silt and sand content. At selected plots, additional
information is gathered continuously on stand structure (in-
cluding the amount of dead wood), lichen diversity, ambient
air quality, phenology and/or litterfall. Growing season tem-
perature and meteorological measurements are available from
many plots. Land history is available from the national or
regional agencies that are responsible for managing the plots.
Monitoring in ICP Forests is discussed in detail by Ferretti and
Fischer (2013).
Mycorrhizas are increasingly recognised as a major miss-
ingbiotic factor regulating development, biodiversity and
productivity in terrestrial ecosystems (Peay et al. 2010). The
ICP Forests network represents an unrivalled platform for
research to fill this knowledge gap (Cox et al. 2010a). A first
essential research step is to produce a large dataset for robust
tests of key macroecological hypotheses and to provide the
baseline high-quality mycorrhizal data to enable future moni-
toring of changes in community composition and diversity.
Among them: (1) increased N availability impacts Europes
mycorrhizal diversity; (2) soil pH, altitude, stand age and
climatic conditions affect mycorrhizas; (3) there are dominant
mycorrhizal fungi associated with Europes major trees; (4)
there are geographic hotspotsof mycorrhizal biodiversity that
correspond with those of vascular plants; (5) mycorrhizal rich-
ness follows latitudinal trends; and (6) there are mycorrhizal
fungi that can act as indicators of environmental conditions.
A second step should involve multiple scale manipulative
experiments across a range of sites in order to maximise
predictive power. However, this second future step cannot be
designed without the information arising from a baseline
assessment of diversity and a macroecological understanding
of that diversity across geographic gradients. Furthermore, the
effects of experiments may differ from those resulting from
long-term geographic gradients, so that both approaches are
valuable and complementary.
7 Large-scale monitoring of mycorrhizas
So far, mycorrhizal assessments as part of the network (Fig. 2)
have been carried out in 12 Scots pine (Pinus sylvestris)ICP
Forest Level II plots in Britain and Germany (Cox et al.
2010b) and 22 oak level II plots (Quercus robur and/or
Quercus petraea) across nine countries (Suz et al. 2014).
Over 3,000 soil cores have been examined and over 10,000
mycorrhizas analysed using DNA-based techniques that iden-
tified 112 mycorrhizal fungi in pine and ca. 400 in oak forests
(see Fig. 3a for species accumulation curves). A further study
of over 100 spruce, pine and beech plots is due for completion
in 2016. The genetic screening approach used allows for the
study of long-term associations, provides a least biased sam-
ple of the dominant active ECM fungi and preserves mycor-
rhizal root specimens for further study. Direct observation of
fruiting bodies, inoculum potential bioassays to assess spore
banks and detection of soil filaments may provide useful
complementary information.
Overall, N pollution and soil pH are emerging as major
factors driving ECM communities through impacts on tree
roots, fungi and soil conditions (Fig. 3b). Both mycorrhizal
richness and evenness decrease when soil pH decreases, lead-
ing to dominance by acidophilic fungi.Similarly, N deposition
decreases the richness and evenness of mycorrhizal commu-
nities, and it shifts dominance towards nitrophilic fungi
resulting in a decrease or even loss of N-sensitive fungi.
There are species that show a consistently negative response
to increasing N inputs and are not detected in plots receiving
high N loads. There is a need to detect the critical N loads for
mycorrhizal communities in European forests above which
communities suffer changes that can affect forest ecosystem
processes, as previously reported for forests in North America
(Pardo et al. 2011) and oak forests in Europe (Bobbink and
Hettelingh 2011; Suz et al. 2014). These thresholds may be
similar to other taxa such as vascular plants that also demon-
strate a sensitive response to N loading and changes in soil pH
(Ikauniece et al. 2013). Simultaneously, we need to identify
species and sets of species that can indicate and predict eco-
system condition and vice versa (e.g. Suz et al. 2014).
So far, we have found that (1) nitrogen is a primary deter-
minant of mycorrhizal distribution in Europe (Cox et al.
2010b; Suz et al. 2014;Fig.3b); (2) rarely studied, poorly
culturable and/or inconspicuously fruiting mycorrhizal fungi
can dominate belowground both within and across plots (e.g.
the truffles Elaphomyces and Hydnotrya and the crusts
Piloderma and Tomentella), some of which (e.g.
Elaphomyces muricatus and Hydnotrya tulasnei) are being
considered for red listing by IUCN based on fruiting body
records; (c) in common with other large perennial organisms,
ECM communities can be spatially stable between seasons
and years, even following seedling transplant between envi-
ronmentally divergent plots (Cox 2010); (d) there can be
abundant dormant propagules (i.e. sclerotia) in soil from fungi
found rarely as mycorrhizas, questioning the assumption that
bulk soil environmental DNA is from active fungi (e.g.
Anderson et al. 2014; Talbot et al. 2014); and (e) dominant
L.M. Suz et al.
but taxonomically unknown ECM fungi can be linked to
previously informally described mycorrhizas (e.g. a
Leotiomycete to Piceirhiza sulfo-incrustatasensu Palfner
et al. 2005).
8 Conclusion
The availability of long-term datasets is the strongest
limiting factor in global change research (Willis and
MacDonald 2011). Soil biology data will be of value
to forest monitoring efforts that can impact on policy by
UNECE and the EU (e.g. Biodiversity Strategy).
European trees and ground floor vegetation are being
monitored and are leading to significant findings (e.g.
Dirnboeck et al. 2014;Seidlingetal.2008; Van Dobben
and de Vries 2010; Veresoglou et al. 2014), but fungi
are not yet included in the current monitoring scheme.
Science and conservation are areas that can be built into
ICP Forests and/or may lead to useful spin-offs; re-
search linked to these long-term plots has the potential
to enhance the relevance of science and conservation.
Fig. 2 a Thirty-four Level II plots belonging to the ICP Forests network
have been used so far for mycorrhizal assessments. Dark grey circles are
Scots pine plots sampled by Cox et al. (2010b), and light grey circles are
oak plots sampled by Suz et al. (2014). bA schematic map of a typical
Level II plot shows the presence of numbered trees that facilitates
randomisation of tree to tree transects for mycorrhizal root sampling
within plots, as well as allowing the spatial location of samples to be
recorded should within-site spatial analyses or re-sampling be required
Fig. 3 A Species accumulation curves (Mao Tau) showing that the
sampling design used recovered on average 70 % of the estimated
richness across plots (x-axis: number of soil cores sampled for
mycorrhizas; y-axis: number of fungal taxa detected). bNon-metric
multidimensional scaling (NMDS) analysis of mycorrhizal communities
at oak Level II plots shows that among other variables, nitrogen
availability, soil pH and root density are main drivers of mycorrhizal
diversity and community composition (Suz et al. 2014)
Monitoring mycorrhizas in ICP Forests
Acknowledgments The ideas presented in this article were discussed
and developed at a workshop supported by the UK Natural Environment
Research Council, Imperial College Londons Grand Challenges in Eco-
systems and the Environment initiative and the Royal Botanic Gardens,
Kew. Research projects were supported by a Marie Curie postdoctoral
fellowship to LMS (FP7-PEOPLE-2009-IEF-253036), to two Bentham-
Moxon Trust grants to MIB and LMS a NERC case studentship to FC
(NER/S/A/2006/14012) and a NERC grant to MIB and DO (NE/
K006339). We are grateful to the constructive comments of two anony-
mous reviewers.
Open Access This article is distributed under the terms of the Creative
Commons Attribution License which permits any use, distribution, and
reproduction in any medium, provided the original author(s) and the
source are credited.
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Monitoring mycorrhizas in ICP Forests
... Lactarius have been found to produce polyphenol oxidases (Giltrap 1982) and in a few cases both Russula and Lactarius have retained copies of MnPs (Looney et al. 2022). Some species of Russula are affected by nitrogen deposition, but the intolerance varies across the genus (Suz et al., 2015). ...
... Fungal conservation was 'initiated' with the onset and recognition of global change factors, such as acid rain and pathogen attacks in central Europe (Arnolds 1991). As time went on, fertilization (Bååth et al. 1981;Arnebrant & Söderstrom 1992), nitrogen deposition (Lilleskov et al. 2002;Suz et al. 2015) and intensified land-use change, such as clear-cutting, (Dahlberg et al. 2010), have all been recognized as important drivers in the decline of fungal species of conservation concern. The effects of cutting trees on common ectomycorrhizal species, such as Lactarius deterrimus, had been realized even 100 years ago (Romell 1930). ...
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... Recent studies suggest that forest stand structure (including plant species, age and density, landscape, canopy cover and the relationship between tree and sporocarp production) and forest management practices (e.g., understory thinning and clearing, regulation of edible sporocarp harvest and mycorrhizal plant regeneration and use) also play an essential role (Suz et al., 2015;Tomao, Bonet, et al., 2017) (see Table S1). For example, Collado et al. (2019) found that sporocarp yield was correlated with tree growth (seasonal wood production) and mediated by summer and autumn precipitation, indicating that tree growth and sporocarp biomass are sensitive to precipitation events under water-limited conditions. ...
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... One major knowledge gap concerns the distribution and population structure of tropical ECM fungi, and such data are necessary to assess threats (e.g., Douhan et al. 2011). Given the lack of information, preserving tropical ectotrophic forests in their primary condition may be the best near-term solution to protect their symbiotic fungi (Suz et al. 2015). ...
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The tropics were long considered to have few ectomycorrhizal fungi, presumably due to a paucity of ectomycorrhizal host plants relative to higher-latitude ecosystems. However, an increase in research in tropical regions over the past 30 years has greatly expanded knowledge about the occurrence of tropical ectomycorrhizal fungi. To assess their broad biogeographic and diversity patterns, we conducted a comprehensive review and quantitative data analysis of 49 studies with 80 individual data sets along with additional data from GlobalFungi to elucidate tropical diversity patterns and biogeography of ectomycorrhizal fungi across the four main tropical regions: the Afrotropics, the Neotropics, Southeast Asia, and Oceania. Generalized linear models were used to explore biotic and abiotic influences on the relative abundance of the 10 most frequently occurring lineages. We also reviewed the available literature and synthesized current knowledge about responses of fungi to anthropogenic disturbances, and their conservation status and threats. We found that /russula-lactarius and /tomentella-thelephora were the most abundant lineages in the Afrotropics, the Neotropics, and Southeast Asia, whereas /cortinarius was the most abundant lineage in Oceania, and that /russula-lactarius, /inocybe, and /tomentella-thelephora were the most species-rich lineages across all of the tropical regions. Based on these analyses, we highlight knowledge gaps for each tropical region. Increased sampling of tropical regions, collaborative efforts, and use of molecular methodologies are needed for a more comprehensive view of the ecology and diversity of tropical ectomycorrhizal fungi. ARTICLE HISTORY
... Mycorrhizas provide an interface between trees and soil, are responsible for driving carbon sequestration globally and regulate many vital forest ecosystem processes, including plant survival, productivity and diversity, and soil formation (Averill et al., 2014;van der Heijden et al., 2015;Terrer et al., 2016;Tedersoo and Bahram, 2019). Understanding changes in the soil 'black box' is crucial to informing forest conservation and management, shaping environmental policy and expanding our knowledge (Suz et al., 2015). The robust belowground baseline generated has allowed us to identify a nitrogen critical load and tipping point for EM communities and forests. ...
... Au vu des résultats du Chapitre 2 et des données fournies par la littérature sur le sujet (références dans le texte), le rôle des champignons ECM dans la dynamique forestière naturelle semble évident. Pour ne pas exclure la biodiversité des sols de l'aménagement forestier durable, des états de référence de la forêt naturelle devraient être mis en place et les champignons pris en compte dans les politiques d'aménagement (Suz et al., 2015). 4.3.2 ...
Thesis
Au Québec, le 49° de latitude nord représente la frontière entre d'une part la forêt mixte dominée par le sapin baumier et le bouleau et d'autre par la forêt boréale dominée par l'épinette noire. Cette frontière tend à migrer vers le nord avec la migration du sapin. Dans les plaines argileuses de l'Abitibi-Témiscamingue qui se trouvent à cette latitude, le sapin possède localement une meilleure capacité d'établissement sous les couverts dominés par le peuplier faux-tremble en comparaison à ceux dominés par l'épinette noire. Les conditions climatiques et édaphiques sont similaires dans les deux types de peuplement, mais les conditions biotiques diffèrent. Le sous-bois sous épinette est dominé par les mousses et des arbustes de la famille des éricacées, tandis que le sous-bois associé aux peuplements de peupliers présente une richesse spécifique plus élevée, plus particulièrement en espèces arbustives et herbacées. Les communautés végétales des strates arborées et de sous-bois sont connues pour affecter les communautés fongiques du sol et notamment les communautés mycorhiziennes. Or, ces dernières pourraient expliquer les différences d'établissement du sapin observées entre les deux types de peuplement. En effet, les mycorhizes sont des symbioses à bénéfices réciproques entre des champignons et les racines des arbres et elles sont particulièrement importantes pour la nutrition des plantes en forêt boréale. Cependant, il y a très peu d'informations sur les mycorhizes dans le système boréal québécois relativement à la Scandinavie ou l'Alaska. Dans ce projet, nous avons testé 1) si les communautés de champignons du sol sont différentes entre les peuplements de peuplier et d'épinette, 2) si les sapins s'associent avec un plus grand nombre d'espèces de champignons, mais aussi à des espèces différentes sous les peupliers et 3) si les symbioses mises en place sous les peupliers sont plus efficaces que celles sous les épinettes pour la nutrition du sapin. Le séquençage haut débit de l'ADN des champignons du sol a permis de détecter une forte diversité fongique et de mettre en évidence des différences dans la composition des communautés fongiques du peuplier et de l'épinette, aussi bien pour les champignons décomposeurs que pour les champignons mycorhiziens. Pendant deux années, soixante jeunes plants de sapins ont été suivis sur le terrain afin de relier la croissance et le taux de nutriments dans les aiguilles (deux estimateurs de la vigueur) au taux de mycorhization et à la diversité fongique. L'analyse a révélé que le taux de nutriments dans les aiguilles du sapin était supérieur sous les peupliers par rapport au sapin poussant sous les épinettes à proximité de plantes éricacées. De plus, la présence des plantes éricacées était corrélée à des changements de la communauté fongique mycorhizienne associée aux racines du sapin, ainsi qu'à une diminution du contenu en azote dans les aiguilles. Des expériences ont également été menées en chambre de croissance afin de déterminer si la mycorhization avait un impact sur la germination, la survie, la nutrition et la croissance des jeunes plantules. Pour ce faire, des sapins ont été semés dans des sols organiques et minéraux provenant des différents types de peuplement et la moitié a été stérilisée afin d'éliminer les microorganismes. Les résultats obtenus après trois saisons de croissance ont permis de détecter un effet de l'identité des microorganismes du sol plutôt qu'un effet du taux de mycorhization sur la nutrition et la croissance du sapin. De plus, les sapins poussant dans les sols récoltés sous épinette mais à distance des éricacées ont eu une meilleure nutrition azotée que dans les sols prélevés sous peuplier.
... Belowground transitions should impact forest capacity to access inorganic, and especially organic, N and P (Lilleskov et al., 2019) with direct consequences for tree nutrition. Understanding the interplay of ectomycorrhizas and forest conditions and functions and the mechanisms of forest ecosystem tipping points has untapped potential to inform fundamental understanding of terrestrial ecosystems, forest management, environmental policy, restoration and conservation practices (Suz et al., 2015). ...
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The resilience of forests is compromised by human‐induced environmental influences pushing them towards tipping points resulting in major shifts in ecosystem state that might be difficult to reverse, are difficult to predict and manage, and can have vast ecological, economic and social consequences. The literature on tipping points has grown rapidly, but almost exclusively based on aquatic and aboveground systems. So far little effort has been made to make links to soil systems, where change is not as drastically apparent, timescales may differ, and recovery may be slower. Predicting belowground ecosystem state transitions and recovery, and their impacts on aboveground systems, remains a major scientific, practical and policy challenge. Recently observed major changes in aboveground tree condition across European forests are likely causally‐linked with ectomycorrhizal (EM) fungal changes belowground. Based on recent breakthroughs in data collection and analysis, we 1) apply tipping point theory to forests, including their belowground component, focusing on EM fungi, 2) link environmental thresholds for EM fungi with nutrient imbalances in forest trees, 3) explore the role of phenotypic plasticity in EM fungal adaptation to, and recovery from, environmental change, and 4) propose major positive feedback mechanisms to understand, address and predict forest ecosystem tipping points.
... Contact Laura at:l.martinez-suz@kew.org Understanding belowground changes in our forests can inform science, forest management, environmental policy and conservation efforts(Suz et al. 2015). We have recently linked belowground ectomycorrhizal diversity of dominant trees in forests across Europe with environmental conditions, and we identified clear thresholds for community composition change of ectomycorrhizas (Table 2). ...
... Sampling substrata (soil, wood, leaves, and roots) has great potential for documenting the presence of fungi even in the absence of visible spore bodies (e.g., mushrooms). Mycologists use eDNA to assess the potential conservation value of sites (Griffith, Cavalli, & Detheridge, 2019) and monitor, document, and model the distribution of taxa (Hao, Guillera-Arroita, May, Lahoz-Monfort, & Elith, 2020;Keepers et al., 2019;Suz et al., 2015). ...
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Plant and fungal biodiversity support all life on earth and merit careful stewardship in an increasingly uncertain environment. However, gaps and biases in documented extinction risks to plant and fungal species impede effective management. Formal extinction risk assessments help avoid extinctions, through engagement, financial or legal mechanisms, but most plant and fungal species lack assessments. Available global assessments cover c. 30% of plant species (ThreatSearch). Red List coverage over-represents woody perennials and useful plants but underrepresents single-country endemics. Fungal assessments overrepresent well-known species and are too few to infer global status or trends. Proportions of assessed vascular plant species considered threatened vary between global assessment datasets: 34% (ThreatSearch), 44% (International Union for Conservation of Nature Red List f Threatened Species). Our predictions, correcting for several quantifiable biases, suggest that 39% of all vascular plant species are threatened with extinction. However, other biases remain unquantified, and may affect our estimate. Preliminary trend data show plants moving toward extinction. Quantitative estimates based on plant extinction risk assessments may understate likely biodiversity loss: they do not fully capture the impacts of climate change, slow-acting threats, or clustering of extinction risk which could amplify loss of evolutionary potential. The importance of extinction risk estimation to support existing and emerging conservation initiatives is likely to grow as threats to biodiversity intensify. This necessitates urgent and strategic expansion of efforts toward comprehensive and ongoing assessment of plant and fungal extinction risk.
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Root-associated fungal communities play a key role in plant productivity and soil processes in forest ecosystems. However, how diversity and composition of root-associated fungi change with forest development and their linkage with soil enzyme activities remain largely unknown. We characterized the root-associated fungal communities, plant and soil properties, and extracellular enzyme activities along a chronosequence spanning young (15 years old) to over-mature (63 years old) Pinus massoniana forest development stages. Our results showed that P. massoniana roots harbored diverse root-associated fungal communities and they varied with forest development. Near-mature (36 years old) forest stands had the lowest alpha-diversity but higher relative abundances of ericoid mycorrhizal and activities of enzymes involved in C, N and P acquisition. The relative abundances of ectomycorrhizal fungi and endophyte were higher in middle-age (24 years old) and mature stands (45 years old), whereas the relative abundance of ericoid mycorrhizal fungi was highest in the near-mature stand. Soil pH, soil C:P and N:P ratios were important factors shaping the diversity and composition of root-associated fungal communities. Structural equation modeling indicated that changes in the community composition, but not richness of root-associated fungi, had significant correlations with soil enzymatic C:N and N:P stoichiometry. In conclusion, this study suggests that different stand development stages exhibit distinct diversity and composition of root-associated fungal communities, which affecting soil functions in terms of enzymatic activity.
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Forest ecosystems have been widely frag-mented by human land use, inducing significant microclimatic and biological changes at the forest edge. If we are to rigorously assess the ecological impacts of habitat fragmentation, there is a need to effectively quantify the amount of edge habitat within a landscape, and to allow this to be modelled for individual species and processes. Edge effect may extend only a few metres or as far as several kilometres, depending on the species or process in question. Therefore, rather than attempting to quantify the amount of edge habitat by using a fixed, case-specific distance to distinguish between edge and core, the area of habitat within continuously-varying distances from the forest edge is of greater utility. We quantified the degree of fragmentation of forests in England, where forests cover 10 % of the land area. We calculated the distance from within the forest patches to the nearest edge (forest vs. non-forest) and other landscape indices, such as mean patch size, edge density and distance to the nearest neighbour. Of the total forest area, 37 % was within 30 m and 74 % within 100 m of the nearest edge. This highlights that, in fragmented landscapes, the habitats close to the edge form a considerable proportion of the total habitat area. We then show how these edge estimates can be combined with ecological response functions, to allow us to generate biologically meaningful estimates of the impacts of fragmentation at a landscape scale. Electronic supplementary material The online version of this article (doi:10.1007/s10980-014-0025-z) contains supple-mentary material, which is available to authorized users.
Book
The roots of most plants are colonized by symbiotic fungi to form mycorrhiza, which play a critical role in the capture of nutrients from the soil and therefore in plant nutrition. Mycorrhizal Symbiosis is recognized as the definitive work in this area. Since the last edition was published there have been major advances in the field, particularly in the area of molecular biology, and the new edition has been fully revised and updated to incorporate these exciting new developments. . Over 50% new material . Includes expanded color plate section . Covers all aspects of mycorrhiza . Presents new taxonomy . Discusses the impact of proteomics and genomics on research in this area.
Chapter
Spruce (Picea abies [L.] Karst.) and beech (Fagus sylvatica L.) which are among the most important tree species, respectively, of boreal and temperate forest ecosystems in Europe are characteristically ectomycorrhizal (Meyer 1973). While the forests dominated by these plants have a low diversity of tree species, the trees themselves typically support a very diverse community of fungal symbionts (Trappe 1962; Väre et al. 1996). In recent years, however, concern has been expressed over an apparent reduction in the number of fungal species represented in the form of carpophores in European forests (Arnolds 1991). While this is an important concern in itself, from the standpoint of tree nutrition and forest health the key issue is the structure of the fungal community on the roots rather than that observed above ground as carpophores.
Chapter
The utilization, preservation, and trade of fungal fruiting bodies for food purposes trace far back in the history of mankind. Hundreds of edible ectomycorrhizal mushroom (EEMM) species are known to be eaten in the world, and records are sparse for many regions, particularly in Africa and South America. A few species have well-established worldwide markets in excess of US$2 billion, while many other species are important at a local scale. In this chapter, the international trade of fresh and preserved EEMMs for most important species with higher prices and/or a significant market share is analyzed in detail. Common techniques for mushroom preservation, e.g., drying, freezing, brining (i.e., preservation in brine), are also reviewed. Problems with the correct mycological determination of traded fungal species are examined, including issues of contrasting evaluation of edibility, both in mushroom field guides (some recommend eating species that others reject as poisonous), and in regulations of different countries. Finally, regulations in international EEMMs trade are discussed in relation to food safety and quality control of fresh and preserved EEMMs (radioactivity, heavy metals, nicotine and pesticide residues, presence of dipteran larvae and other “parasites”).
Chapter
Over the past decades, the demand for and interest in harmonized data on the status of forests has changed in nature, increasing and becoming cross-sectoral. Although its history is much more recent than forest inventories, forest monitoring today has a great potential to provide useful data and information. The chapter outlines the development of monitoring needs over the past 40 years, the value of monitoring and its importance for other forms of scientific inquiry, introduces the basic methodological issues, and presents an overview of the major forest monitoring programs. Emphasis is placed on the importance that monitoring be driven by explicit objectives and grounded on solid scientific background. This chapter presents the aims and structure of the book.
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We used DNA sequences of 20 ectomycorrhizal fungal species obtained from roots in Britain and Germany to find location data within Europe for these fungi in the public DNA databases. These data were used to plot species presence on maps, environmental layers were laid over these maps, and information from those sites was extrapolated using geographic information systems. Through randomization tests the significant factors for each species from available data were tested. Similar methodology was used for fungal samples identified using morphology from the Global Biodiversity Information Facility to compare data quality and quantity. This analysis exposed the need for uniform methodology and greater distribution of sampling in order to create viable species distribution models for ectomycorrhizas.
Article
Ectomycorrhizal fungi are major ecological players in temperate forests but they are rarely used in measures of forest condition because large-scale, high-resolution, standardized and replicated belowground data is scarce. We carried out an analysis of ectomycorrhizas at 22 intensively-monitored long-term oak plots, across nine European countries, covering complex natural and anthropogenic environmental gradients. We found that at large scales mycorrhizal richness and evenness declined with decreasing soil pH and root density, and with increasing atmospheric nitrogen deposition. Shifts in mycorrhizas with different functional traits were detected; mycorrhizas with structures specialized for long-distance transport related differently to most environmental variables than those without. The dominant oak-specialist Lactarius quietus, with limited soil exploration, responds positively to increasing N inputs and decreasing pH. In contrast, Tricholoma, Cortinarius and Piloderma species, with medium-distance soil exploration, show a consistently negative response. We also determined N critical loads for moderate (9.5 – 13.5 kg N ha−1 yr−1) and drastic (17 kg N ha−1 yr−1) changes in belowground mycorrhizal root communities in temperate oak forests. Overall, we generated the first baseline data for ectomycorrhizal fungi in the oak forests sampled, identified nitrogen pollution as one of their major drivers at large scales, and revealed fungi that individually and/or in combination with others can be used as belowground indicators of environmental characteristics.This article is protected by copyright. All rights reserved.