The Impact of Climate Change on Woodland Saprotrophic and

Mycorrhizal Fungi

A.C. Gange, PhD
School of Biological Sciences, Royal Holloway, University of London Egham, Surrey TW20 0EX
&
E.G. Gange
Belvedere, Southampton Road, Salisbury, Wilts SP5 3DZ

Summary
Fungi are important agents of decomposition and nutrient cycling in woodlands and many species
with different life histories occur together in this habitat. Using a data set consisting of over
60,000 individual records of fruit body appearance, an analysis is presented of changes in fruiting
patterns over the last 60 y. Fruiting of 271 species has changed dramatically over this time, with
the length of the autumnal fruiting season having doubled. Saprotrophic and mycorrhizal fungi
have responded differently; the former show extensions in their fruiting season, while the latter
do not. This is because saprotrophs are more affected by changes in temperature and rainfall,
while mycorrhizal species are tied to their hosts phenology. Individualistic responses are
common, leading to the suggestion that climate change has caused significant changes in fungal
activity, community structure and ecosystem processes in woodlands.

Introduction
Changes in climate, particularly higher temperatures, have been linked to changes in the
phenology, distribution and abundance of species from many taxonomic groups and geographical
locations (Parmesan & Yohe, 2003). Despite the plethora of studies on single species and
taxonomic groups, the consequences of climate change for the structure and function of
ecosystems remains virtually unknown (Martin, 2007). Disruption of species assemblages is
predicted, due to variation in the responses of different species to temperature and rainfall
(Walther et al., 2002; Voigt et al., 2003), hence there is an urgent need to study how changing
climate will affect the structure of natural communities. The vast majority of phenological
studies have documented changes in spring events, such as flowering or egg laying and involved
higher organisms, such as plants, insects or birds (Parmesan & Yohe, 2003). However, all of
these studies have reported the responses of a taxon across many habitats, and there has yet to be
a large scale analysis of a taxon within one habitat type. This has precluded a proper
consideration of climatic effects on community structure. Fungi present a unique opportunity to
conduct such an analysis, as in woodlands many species with differing life histories co-occur.

Recently, three studies have documented changes in macrofungal fruiting patterns over the last
60 y (Gange et al., 2007; Mattock et al., 2007; Kauserud et al., 2008). Mattock et al. reported
dramatic changes in vernal fungi, mainly associated with grasslands, while the other two papers
examined autumnal fruiting patterns. The approach taken and the conclusions reached differ in
the two studies. Gange et al. (2007) used real field sampling data over a 56 y period (1950
2006) and examined changes in first (hereafter referred to as FFD) and last fruiting dates.
Using averaged data of 315 species from nearly 1,400 localities (a total of 52,382 records), they
found that the length of the autumnal fruiting season has increased, with significant changes
becoming apparent since the mid 1970s. The change in fruiting is coincidental with a marked
200
240
280
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360
1950 1960 1970 1980 1990 2000 2010
D
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change in the British climate since 1975 (Fitter & Fitter, 2002).

However, Kauserud et al. (2008) used herbarium data collected from 1940 2006 in the
Norwegian Mycological Societys database, representing 83 species and a total of 34,500 records.
Their main conclusion was that early fruiting species have shown delays, while late fruiting
species have shown advancements in appearance, leading to a constriction of the fruiting season.

These two data sets provide an excellent template with which to examine the responses of fungal
communities to climate change. Fungal fruiting is intimately linked with temperature and rainfall
(Straatsma et al., 2001; Salerni et al., 2002) and the phenology of fruiting is the only feasible
indicator of mycelial activity and community structure that can be obtained at the field scale. In
this paper, I examine the responses of different functional groups of fungi to climate change,
namely saprotrophic and mycorrhizal species co-occurring in the same habitat. By taking this
approach, my aims are to identify changes in fungal community structure and to reconcile
differences in the UK and Norwegian studies.

Methods
The data set from Gange et al. (2007) was used, with the addition of data from 2006 and 2007.
This comprised 60,406 records, obtained from VC8, collated by E.G.G. and obtained by at least
weekly sampling over the period 1950 2007. Details of data collection are given in the
Supplementary Online Material to that paper. For the purposes of the current analysis, only
saprotrophic or ectomycorrhizal species were considered; a total of 271 species. The date of each
fruit body collection was expressed as Julian day, enabling determination of first fruiting date
(FFD), and the range in fruiting (last fruiting date minus FFD). To examine changes over time,
linear regression was used to relate FFD or range in fruiting date of each species to year.

To estimate the displacement in fruiting time for each species, I calculated the average fruiting
date in the 2000 decade and subtracted from this the average for the 1950s decade. Analysis of
variance was used to examine differences in displacement of first fruiting date and range in
fruiting season, using fungal functional group (deciduous or coniferous mycorrhizal, litter or
wood saprotroph) as a factor.

Weather records (daily temperature and rainfall) were obtained from Southampton Weather
Centre, supplemented by personal data when the station closed in 2002. To examine species
responses to climate, monthly mean temperature and total rainfall were used in regressions with
FFD for each species.

Results and Discussion
Both first (FFD) and last (LFD) fruiting date of woodland species has changed dramatically over
the 58 y (Fig. 1).






Leaf litter saprotrophs
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200 250 300 350
Mean fruiting date
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Deciduous mycorrhizas
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200 250 300 350
Mean fruiting date
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Wood decayers
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200 250 300 350
Mean fruiting date
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Coniferous mycorrhizas
-1.2
-1
-0.8
-0.6
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0
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200 250 300 350
Mean fruiting date
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Fig. 1. Mean first (lower line) and last fruiting date of 271 woodland saprotrophic and mycorrhizal fungi over 58 y.

The net result of these changes is that the range in fungal fruiting (i.e. the length of the autumnal
season) has increased from an average of 33.2 1.9 d in the 1950s to 67.9 7.1 d in the current
decade. The change in fruiting has become apparent since the late 1970s, and mirrors the distinct
change in the British climate of higher summer and autumnal temperatures that have occurred
since that time (Fitter & Fitter, 2002).

Species were divided into four functional groups; litter saprotrophs, those mycorrhizal with
deciduous or coniferous trees and those that decay wood. For all species, the average date of
appearance (mean of all records over all years) was calculated and plotted against the regression
coefficient obtained by relating FFD to year. A positive value of this coefficient indicates that a
species shows a trend to delayed FFD and vice versa. All functional groups displayed a similar
pattern, in that those species which appear early in the season are tending to show delays in FFD,
while later season species are showing an advancement (Fig. 2). It is interesting that these are
identical patterns to that found by Kauserud et al. (2008), leading those authors to the conclusion
that the overall fruiting season has become constricted.
























-24
-16
-8
0
8
16
24
Leaf litter
saprotrophs
Deciduous
mycorrhizas
Coniferous
mycorrhizas
Wood
decayers
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,

d
Fig. 2. Relations between mean fruiting date and regression coefficients of FFD v. year. Significant relations
indicated by trend lines.

Thus in the UK data set, there is an apparent paradox; the trends in Fig. 2 suggest a shortening of
the fruiting season, but Fig. 1 shows that it has expanded.

In order to resolve this paradox, we must consider the magnitude of change when FFD is
advanced or delayed and the contribution to the overall relationship of each functional group.
These analyses were conducted using the displacement in fruiting time, defined above.

There is a significant (F
1, 269
= 9.45, P < 0.01) difference in the displacement (in d) of species
with earlier first fruiting dates compared with those having delayed FFDs. There are 134 species
that show an advanced FFD, averaging 30.8 1.9 d, and 137 species that show a delayed FFD,
averaging 23.2 1.3 d. Thus, the magnitude of the change in species that show advancement in
fruiting is greater than the delay in those fruiting later. A similar situation occurs with LFD: 102
species show an earlier LFD, averaging 19.2 1.8 d, while 169 species show a delayed LFD,
averaging 24.8 1.3 d (F
1,269
= 6.11, P < 0.05). Taken together, these differences result in an
extended fruiting season, not a constricted one, and show that an analysis based purely on
regression coefficients can give a misleading interpretation.

Perhaps of more interest is the fact that different functional groups of fungi show variations in
their phenological responses (Fig. 3). Species ectomycorrhizal (ECM) with coniferous trees, and
in particular those that decay wood, now fruit considerably earlier than in the 1950s. Species that
form ECM with deciduous trees begin to appear later, while litter saprotrophs still appear at the
same time in autumn (mean displacement of FFD not different from zero).













Fig. 3. Average change ( s.e.) in FFD of species in each functional group, between 1950s and 2000s.

However, the advantage that the UK data set has over the Norwegian one is that it can pinpoint
first and last dates of appearance with a much higher degree of accuracy. This enables us to
obtain estimates of the length of the fruiting period for each species. Fig. 4 shows that the
extension of the fruiting season has been greatest in saprotrophs of leaf litter or wood.
a
b b
a
0
5
10
15
20
25
Leaf litter
saprotrophs
Deciduous
mycorrhizas
Coniferous
mycorrhizas
Wood
decayers
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,

d












Fig. 4. Average change ( s.e.) in fruiting season between 1950s and 2000s. Bars with different letters are
significantly different at P = 0.05.

It is interesting that within the two groups of saprotrophs or mycorrhizas, the net effect is the
same, yet the mechanism by which this occurs is different. The changes in FFD, LFD and range
are summarised in Table 1 for each functional group.


First fruiting date Last fruiting date Fruiting season
Litter saprotrophs Unchanged Later Large extension
Deciduous mycorrhizas Later Later Small extension
Coniferous mycorrhizas Earlier Earlier Unchanged
Wood decayers Earlier Unchanged Large extension
Table 1. Summary of the overall changes in each functional group of fungi 1950 2007.


It is likely that fruiting of saprotrophic fungi is affected more by weather conditions (temperature,
and in particular, rainfall) than that of mycorrhizal species. The latter are closely tied to the
phenology of the host and sporophore production is often triggered by the movement of nutrients
to the roots, coincidental with leaf fall (Last et al., 1979). There is some evidence that leaf fall
occurs later than it did 50 y ago (Peuelas et al., 2002), giving a plausible explanation for the
effects on deciduous mycorrhizas in Table 1. However, those species that associate with
coniferous trees may be less responsive to the host, where there is no substantial leaf fall. Gange
et al. (2007) reported that fungi which can associate with both deciduous and coniferous trees
showed later average fruiting date in the former woodland type, but not in the latter.

Clearly, functional groups of fungi have changed their fruiting patterns in different ways,
reflecting their ecological habits. This fact provides a further explanation for the difference in the
results of Gange et al. (2007) and Kauserud et al. (2008). If the two data sets are divided into
broad categories of saprotrophic or mycorrhizal, we find that the UK data are dominated by the
former (66%), while mycorrhizal species predominate (70%) in Norway. As can be seen from
Table 1, saprotrophic species have shown much greater extensions in their fruiting than have
mycorrhizas

Leaf litter saprotrophs
0
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70
Earlier Later
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temperature rain both
Deciduous mycorrhizas
0
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70
Earlier Later
P
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temperature rain both
Wood decayers
0
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60
70
Earlier Later
P
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n
t
temperature rain both
A feature of the phenological literature is that species often show individualistic responses to
climate change, leading to the potential for community change (Voigt et al., 2003). Fungi are no
exception and within each of the four functional groups represented here there is a wide range in
the responses of FFD and length of the fruiting season. Thus, the suite of species likely to be
found fruiting at any one point in time is now radically different to what it was 60 y ago. If we
make the reasonable assumption that fruiting is indicative of mycelial activity (albeit with some
form of time lag) (Moore et al., 2007) then competitive interactions and community structure are
likely to have changed too. The extension of the fruiting season may also suggest increased fruit
body production, indicating enhanced decomposition rates and greater nutrient cycling. If such
processes feed back into tree growth, then the entire forest ecosystem may be affected, via
multitrophic effects of subterranean food webs on above-ground processes (Wardle et al., 2004).



























Fig. 5. The proportion of significant changes (earlier or later) in FFD of each functional group that can be explained
by changes in temperature, rainfall or both. Coniferous mycorrhizas are missing, because the sample size was too
small.

Individualistic responses are caused by variations in each organisms requirements for
environmental parameters such as temperature and rainfall (Voigt et al., 2003). One might
expect that fungi would show less variation in these responses (Straatsma et al., 2001), but as can
be seen from Fig. 5, this is not so and in this respect, fungi are as variable as other organisms

-10
-5
0
5
10
15
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30
35
40
Amanita Inocybe Lactarius Russula Clitocybe Collybia Mycena
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These graphs show that the majority of fungal responses can be explained by meteorological
parameters. As both temperature and precipitation have changed markedly in the UK over the
last 60 y (Jones & Conway, 1995), one may attribute the changes in fungal fruiting patterns to
changes in the prevailing climate. However, the response of each group differs; with litter
saprotrophs, every species that has shown an advancement in fruiting is affected significantly by
temperature, rain or both. For those mycorrhizal species with deciduous trees, only 50% of the
species showing earlier fruiting are affected by the weather, and all of these respond to
temperature. For the vast majority of species, higher temperatures in July and August contribute
to earlier fruiting, while a delay in LFD is determined by rainfall in October. In the UK, July and
August temperatures and October rainfall all show positive trends over the 60 y, i.e. to hotter
summers and wetter autumns, thereby contributing to the extended fruiting season

Variation in community structure can be further examined by inspecting the responses of species
that fruit at similar times. These analyses have been conducted at the genus level, as in all
phylogenetic analyses, one would expect species that are taxonomically closely related to respond
in a similar manner (Harvey & Pagel, 1991).












Fig. 6. Average displacement in length of the fruiting season for deciduous mycorrhizal and saprotrophic genera.

It can be seen in Fig. 6 that litter saprotrophs (Clitocybe, Collybia and Mycena) all show
considerable extensions in their fruiting seasons, while the mycorrhizal genera do not. This is
further evidence for saprotrophs being more dependent on external meteorological parameters for
the control of fruiting, while mycorrhizas are more closely tied to their host phenology.
Although there is some evidence of climate-induced delayed leaf fall of trees in southern Europe
(Peuelas et al., 2002), a European-wide analysis failed to detect significant patterns
(Chmielewski & Rtzer, 2001). The mycorrhizal data in the current study are consistent with the
latter study. The above genera were chosen for this comparison because they often co-occur in
woodlands and have ecologically similar habits. These data suggest that the mycelial activity of
these species within the communities has changed, so that saprotrophic fungi may now be active
for longer, while mycorrhizal species have remained unchanged
Russula
-20
-10
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10
20
30
40
D
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Clitocybe
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Variation within a genus is also evident in these data. Fig. 7 shows the responses of two large
genera, the mycorrhizal Russula and the saprotrophic Clitocybe.



















Fig. 7. The change in length of the fruiting season for 17 species of Russula and 9 species of Clitocybe over the last
60 y.

The saprotrophic Clitocybe shows a more consistent response, with 78% of species showing an
extension of the fruiting season. However, in the mycorrhizal Russula, only 58% show an
extension and there is a greater variation in the response. The species showing the greatest
contraction of the fruiting season is Russula nigricans, and that with the greatest extension is R.
ochroleuca. There are no obvious habitat differences between these and both species occur under
a wide range of deciduous trees (Kibby, 2007). Variations in response therefore seem to be due
entirely to natural variation in the biology of the species.

Conclusion

To conclude, it is evident that fungi are extremely responsive to changes in climate and there
have been large changes in the autumnal fruiting season over the last 60 y. Many species
responses can be related to changed temperature and rainfall. The potential exists for significant
alteration of fungal community structure in woodlands, with significant effects on decomposition
rates, nutrient cycling and the structure of woodland ecosystems.

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