Research
Species level patterns in 13C and 15N abundance of
ectomycorrhizal and saprotrophic fungal sporocarps
Blackwell Publishing Ltd.
Andy F. S. Taylor1, Petra M. Fransson1, Peter Högberg2, Mona N. Högberg2 and Agneta H. Plamboeck3
1
Department of Forest Mycology and Pathology, Swedish University of Agricultural Sciences, PO Box 7026, SE-750 07 Uppsala, Sweden; 2Section of Soil
Science, Department of Forest Ecology, Swedish University of Agricultural Sciences, S-901 83 Umeå, Sweden. 3Center for Stable Isotope Biogeochemistry,
Department of Integrative Biology, University of California, Berkeley, CA 94720, USA.
Abstract
Author for correspondence:
Andy Taylor
Tel: +46 18 672797.
Fax: +46 18 673599
Email: [email protected]
Received: 24 February 2003
Accepted: 15 May 2003
doi: 10.1046/j.1469-8137.2003.00838.x
• The natural abundance of 13C (δ13C) and 15N (δ15N) of saprotrophic and ectomycorrhizal (ECM) fungi has been investigated on a number of occasions, but the
significance of observed differences within and between the two trophic groups
remains unclear.
• Here, we examine the influence of taxonomy, site, host and time upon isotopic
data from 135 fungal species collected at two forest sites in Sweden.
• Mean δ13C and δ15N values differed significantly between ECM and saprotrophic
fungi, with only a small degree of overlap even at the species level. Among
ECM fungi, intraspecific variation in δ15N was low compared with interspecific and
intergeneric variation. Significant variation due to site, year and host association
was found.
• At broad scales a number of factors clearly influence δ13C and δ15N values making
interpretation problematic. We suggest that values are essentially site-specific within
the two trophic groups, but that species-level patterns exist potentially reflecting
ecophysiological attributes of species. The species is therefore highlighted as the
taxonomic level at which most information may be obtained from fungal δ13C and
δ15N data.
Key words: fungal diversity, functional groups, nutrient cycling, ectomycorrhizal
(ECM) fungi, saprotrophic fungi, stable isotopes.
© New Phytologist (2003) 159: 757–774
Introduction
Ectomycorrhizal (ECM) fungi, obligate root symbionts of
most boreal forest trees, and saprotrophic macromycetes
contribute most to the observed fungal diversity within boreal
forest ecosystems (Bills et al., 1986; Såstad & Jenssen, 1993;
Renvall, 1995; Väre et al., 1996). Traditionally, these fungi
have been regarded as two distinct functional groups within
ecosystems (Dighton, 1995; Leake & Read, 1997) with
saprotrophic fungi obtaining carbon (C) and nutrients from
the degradation of organic compounds (Swift et al., 1979)
and ECM fungi facilitating the uptake of nutrients by their
autotrophic host plants in return for fixed C as photosynthate
(Smith & Read, 1997). However, over the past two decades
the distinction between the two groups has become less well
defined. There is now considerable evidence that some ECM
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fungi have the potential to assimilate many of the major
nitrogen (N)- and phosphorus (P)-containing organic
molecules in plant, microbial and animal detritus (Leake
& Read, 1997). This may occur either directly via the
production of catabolic extracellular enzymes or indirectly
via combative interactions with saprotrophic fungi (Lindahl
et al., 1999). In addition, some fungi formally regarded as
saprotrophs are now known to be ECM fungi (see Agerer &
Beenken, 1998; Erland & Taylor, 1999; Kõljalg et al., 2000).
Direct in situ observation of fungi is difficult because of the
small size of the vegetative structures and the opaque nature
of the growing medium. Consequently, most knowledge concerning the involvement of these fungi in ecosystem processes
is derived from laboratory investigations. One method that
has, in recent years, been investigated as a potential indirect
method for assessing the functional roles of the fungi in
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ecosystems is the analysis of the stable isotopes 13C and 15N
in fungal material.
Cycling of C and N through different components of
ecosystems create small but measurable differences in the
isotope ratios of 13C : 12C and 15N : 14N (Dawson et al., 2002).
These differences have been used extensively to investigate
plant ecology and the pathways of C and N cycling through
ecosystems (Farquhar et al., 1989; Fung et al., 1997; Högberg,
1997) and this approach has also been used as a tool to
investigate ECM and saprotrophic fungal ecology (Hobbie
et al., 1999a, 2001; Högberg et al., 1999b; Henn & Chapela,
2001). Direct analysis of soil mycelia is rarely practical and
nearly all of these studies have involved determining the
natural abundance of 15N and 13C in the sporocarps of
macromycetes. One exception to this is the study by Högberg
et al. (1996), where the 15N abundance in the mantles of
beech (Fagus sylvatica) mycorrhizas was determined. Some
general patterns are becoming apparent from these studies.
Ectomycorrhizal fungi are generally more depleted in 13C and
more enriched in 15N than saprotrophic fungi (Hobbie et al.,
1999b; Högberg et al., 1999b; Kohzu et al., 1999; Henn &
Chapela, 2001). Among the saprotrophs, litter fungi are more
enriched in 15N than wood decomposers, with both groups
enriched relative to their substrates (Gebauer & Taylor, 1999;
Kohzu et al., 1999).
Another general pattern is emerging in which ECM fungi
are considerably enriched in 15N relative to their host plants
(Gebauer & Dietrich, 1993; Högberg et al., 1996, 1999a;
Taylor et al., 1997; Michelsen et al., 1998; Hobbie et al.,
1999b). Given that > 95% of the host root tips are usually
colonized by ECM fungi (Dahlberg et al., 1997; Fransson
et al., 2000; Taylor et al., 2000), most of the N taken up by the
tree would have to pass through the fungi. It could therefore
be expected that the 15N signatures of the fungi and the host
plant would be similar. Fractionation during transfer of N
from the soil through the fungal tissue to the host plant has
been suggested as the main reason for the observed differences
between the host and fungal 15N abundances (Hobbie et al.,
1999b; Högberg et al., 1999a).
In many of the field investigations cited above, fungi are
often split into large ecological groups (ECM, litter or wood
decomposers), within which species are considered to carry
out similar functions within the ecosystem. It therefore
follows that within a functional group, species are expected
to have similar isotope signatures and conclusions concerning
the significance of observed values are therefore often made at
these very broad functional levels, regardless of the taxonomic
diversity of the organisms involved. There is, however, considerable evidence, both physiological and ecological, which
strongly suggests that this assumption of ecological equivalency within fungal functional groups is invalid (Smith &
Read, 1997).
Among ECM fungi, much variation exists among species,
even within the same genus, with regard to enzymatic
capabilities, carbon demand and habitat preferences (Tyler,
1985; Leake & Read, 1997; Cairney, 1999). All of these
factors could be expected to affect the δ15N and δ13C values
of the sporocarps produced by individual ECM species. It is
also well established that there are distinct successions of
saprotrophic fungi colonizing plant debris (Renvall, 1995), with
each fungal species or group of species capable of utilizing
different chemical components of the plant material (Tanasaki
et al., 1993). As these components may vary with respect to
15N (Högberg, 1997) and 13C abundance (Gleixner et al.,
1993), it seems inevitable that the 15N and 13C signatures of
sporocarps will reflect a differential substrate usage (Gebauer
& Taylor, 1999).
If differences in the 15N and 13C abundance of sporocarps
are a reflection of the physiological diversity among fungal
species, then the data may be most informative at the taxonomic
level of the species. Support for this idea comes from the study
by Högberg et al. (1999b), which demonstrated that by
analysing 13C abundance data from mycorrhizal fungi at the
species level, host specificity between trees and their associated
ECM fungi could be examined in situ for the first time.
The present study examines the 15N and 13C natural
abundance in sporocarps of ECM and saprotrophic fungi to
determine (1) how site, host and time influence 15N and 13C
natural abundance and (2) if species-specific patterns exist. In
addition, inter-yearly variation was also examined. The data is
derived from extensive collections of ECM and saprotrophic
fungi at sites in central and northern Sweden. The results
show that potentially important ecological information
may be lost when 15N and 13C natural abundance data are
interpreted above the level of the species and that using the
data to distinguish between saprotrophic and ECM fungi
must be done with caution.
Materials and Methods
Sites
The study was conducted at Stadsskogen in Uppsala, central
Sweden (59°52′N, 17°13′E, 35 m above sea level) and at
Åheden in the Svartberget Research Forest, 60 km north-west
of Umeå, northern Sweden (64°14′N, 19°46′E, 175 m above
sea level). Both forests have 150-yr-old Scots pine (Pinus
sylvestris L.) as an overstorey with Norway spruce (Picea abies
(L.) Karst.) approaching the role of a codominant. At
Stadsskogen, understorey deciduous tree species included
aspen (Populus tremula L.), birch (Betula pendula Roth),
willow (Salix caprea L.), and alder (Alnus incana (L.) Moench).
At Åheden, birch was the only understorey tree species.
Sampling
Sampling was conducted in an area of c. 1 ha at Åheden in
August 1997 and at five plots, each with an area of 0.25 ha at
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Stadsskogen between August and October 1997. Between
one and eight mature sporocarps from each fungal species
were sampled at each site (see Appendix 1). Nomenclature
primarily follows that of Hansen & Knudsen (1992, 1997).
At Åheden, sampling in 1993, 1995 and 1997 allowed
examination of interannual variability (see later). In addition,
at each site, leaves and current needles of tree species were
sampled (> 10 g dry wt per sample) from branches on the
south side, close to the top of the tree, from up to 10
specimens per tree species.
Preparation and sample analysis
The sporocarps and foliar samples were dried (700C, 24 h)
and then ground in a ball mill. Samples were analysed for
15N and 13C abundance using an on-line continuous flow
CN analyser coupled to an isotope ratio mass spectrometer
(Ohlsson & Wallmark, 1999). Results are expressed in the
standard notation (δ13C and δ15N) in parts per thousand
(‰) relative to the international standards V-PDB and
atmospheric N2, where δ13C or δ15N = ((Rsample/Rstandard) −
1] × 1000, and R is the molar ratio 13C : 12C or 15N : 14N.
The standard deviation based on the analysis of replicated
samples was 0.15‰ and 0.20‰ for 13C and 15N, respectively.
Statistical analysis
Many species were represented by more than one collection
(a sporocarp) and this is a potential source of bias when
calculating mean values for different groups or categories of
fungi. It was therefore necessary to calculate weighted means
that took this into account. Weighted means of δ15N, %N,
δ13C, %C and C : N-values were calculated separately for
saprotrophic and mycorrhizal fungi. A mean value for each
group was obtained by calculating the sum of the mean values
for the different fungal species in the group and then by
dividing this by the number of species in the group. The
estimated variance of the group mean was the sum of the
variances of the species means, divided by the square root of
number of species in the group. Group means were then
compared using Tukey’s test at the 5%, 1%, and 0.1% levels.
Most analyses were restricted to Stadsskogen, from which
we obtained the more complete data set. For the ECM fungi,
the (δ15N, %N, (δ13C, %C and C : N data were compared at
the family and generic taxonomic levels. The weighted means
of the nine ECM families represented by more than three
species and intergeneric differences were compared using one
way analysis of variance () and Tukey’s family error
(5%) test. Possible differences related to host specificity on the
major tree species (Pinus, Picea and Betula) were compared in
the same way. The δ13C data has been presented in detail
previously (Högberg et al., 1999b).
Temporal effects due to sampling date and differences
between the five plots sampled in Stadsskogen were also tested
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using  and Tukey’s family error (5%) test. Temporal
effects were examined by calculating mean values for each of
the six sampling periods based on all sporocarps collected at
that time. Twelve ECM species occurred with two or more
sporocarps on both sites, Stadsskogen and Åheden. These
species were used to make intersite comparisons of δ15N, %N
δ13C, %C-values and C : N ratios, using paired t-tests.
Inter-yearly differences in (δ15N were examined by comparing data from sporocarps collected at Åheden in 1993 and
1995 (data from Taylor et al., 1997) with the mean value for
1997. This was possible for six species that were collected on
three or more occasions in 1997. The 95% confidence interval
was calculated for the mean value for each of these six species
and any value from 1993 or 1995 which lay outside this
interval was therefore considered significantly different from
the mean at P = 0.05.
Results
Comparison of functional groups (ECM and
saprotrophic fungi)
A total of 135 fungal species (118 ECM and 17 saprotrophic)
representing 25 ECM and 15 saprotrophic genera were
analysed in the study (Appendix 1). In general, the mean
values for (δ15N, %N δ13C, and %C values and C : N ratios
differed significantly between saprotrophic and ECM fungi,
irrespective of site (Table 1). The general pattern was for
ECM fungi to be more enriched in 15N, but more depleted in
13C, and have a higher percentage of carbon than saprotrophic
fungi. At Stadsskogen, the %N of ECM sporocarps was
significantly lower than in saprotrophs, but at Åheden, the
reverse pattern was observed. The %N varied considerably
more than %C, resulting in sporocarp C : N ratios being
largely determined by the percentage of N they contained
(Table 1). The significant difference observed in the C : N
ratio between the two life forms reflects the changing N status
of the two groups (Table 1).
Plotting δ15N against the δ13C values for the individual
species separated most saprotrophic from ECM fungi (Fig. 1).
However, at Stadsskogen there was some overlap between the
two groups. Adding a third axis representing %N, %C or the
C : N ratio of the sporocarps did not significantly increase
the distinction between the groups (data not shown).
Comparison of ECM fungi at different taxonomic levels
The data for ECM fungi analysed at different taxonomic levels
is presented in the following increasing order of resolution:
family, genus and species. Fourteen ECM families were
represented in the collections from Stadsskogen with nine of
these represented by three or more species. There were highly
significant differences among these nine families with respect
to %N, δ15N, %C δ13C values and C : N ratios (Table 2).
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Table 1 Mean values for percentage nitrogen (%N), δ15N, percentage carbon (%C), δ13C and C : N ratios in sporocarps of ectomycorrhizal
(ECM) and saprotrophic fungi collected from two forests in Sweden (Åheden, northern Sweden; Stadsskogen, central Sweden)
δ15N (‰)
δ13C (‰)
%N
%C
C/N ratio
Åheden ECM
fungi (n = 28)
Saprotrophic
(n = 5)
P1
Stadsskogen ECM
fungi (n = 109)
Saprotrophic
(n = 14)
P1
7.8a2
−25.8
3.9
43.0
11.9
−0.8
−23.4
3.1a
42.2
15.1
< 0.001
< 0.001
0.05 > P > 0.01
ns
0.01 > P > 0.001
5.8b
−25.8
3.9
43.5
11.5
0.8
−23.2
5.8b
41.7
9.2
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
1
Significance of within site differences between fungal life strategies, analysed using students t-test; ns, not significant. 2Between-site
comparisons of mean values for each life form; means with different letters are significantly different at P = 0.05.
Table 2 Mean values ± SE for percentage nitrogen (%N), δ15N, percentage carbon (%C), δ13C and C : N ratios in sporocarps of ectomycorrhizal
fungi from nine families, collected in a mixed boreal forest at Stadsskogen, Uppsala, central Sweden
Family
%N1
δ15N (‰)
%C
δ13C (‰)
C:N
Amanitaceae
Boletaceae
Gomphidiaceae
Hygrophoraceae
Tricholomataceae
Cortinariaceae
Russulaceae
Thelephoraceae
Cantharellaceae
F (d.f. 8,95).
P
4.3 ± 0.2 a,c,d
4.9 ± 0.3 c,d
3.4 ± 0.2 a
3.9 ± 0.4 a,c
3.8 ± 0.3 a,b
4.1 ± 0.1 a,e
3.8 ± 0.1 a
5.1 ± 0.4 b,c,e
3.1 ± 0.1 a
5.30
< 0.001
4.1 ± 1.1 a,b
8.7 ± 1.3 b
7.7 ± 1.5 a,b
2.6 ± 2.3 a,b
9.0 ± 1.5 b
5.6 ± 0.4 a,b
4.3 ± 0.5 a
9.7 ± 0.8 a,b
3.4 ± 1.1 a,b
5.38
< 0.001
44.1 ± 0.6 a,b,c
42.4 ± 0.3 d
43.5 ± 0.4 a,d,e
42.5 ± 0.3 c,d
42.8 ± 0.4 c,d
42.7 ± 0.1 d
44.3 ± 0.2 a,e
46.3 ± 0.3 b,f
43.9 ± 0.3 a,d,f
12.38
< 0.001
−25.5 ± 0.3 a,b
−25.8 ± 0.5 b
−25.1 ± 0.2 a,b
−26.2 ± 1.0 b
−25.6 ± 0.4 b
−26.1 ± 0.2 b
−25.8 ± 0.2 b
−22.8 ± 0.2 a
−25.5 ± 0.4 a,b
3.04
< 0.0042
10.3 ± 0.4 a,b
9.1 ± 0.6 a
13.0 ± 0.9 b
11.1 ± 1.2 a
11.6 ± 0.9 a,b
10.8 ± 0.3 a,b
11.9 ± 0.3 b
9.4 ± 0.9 a,b
14.2 ± 0.5 b
4.96
< 0.001
1
Within columns mean values sharing the same letter are not significantly different. 2Excluding the data from Thelephoraceae gives a
nonsignificant result (F = 0.78, P = 0.603).
A total of 24 genera were collected at Stadsskogen, of which
eight were represented by three or more species. The mean
values for %N, δ15N, %C δ13C and C : N ratios varied
considerably among these eight genera (Fig. 2). The δ13C
values clearly separated those genera that were either nearly or
entirely represented by species forming specific associations
with Pinus (Suillus) or Betula (Leccinum). The 13C values of
other genera that were represented by a range of specific and
nonspecific species did not differ. The δ15N-values also varied
considerably among the genera, even between the closely
related genera Russula and Lactarius (Fig. 2). As mentioned
above, the C : N ratio of the sporocarps was largely determined by the percentage of N they contained and this
relationship was also evident at the generic level (R 2 = 0.962;
P < 0.001). With this exception, no other two parameters
were significantly correlated at the generic level.
Fig. 1 Natural 15N and 13C abundance in sporocarps of
ectomycorrhizal (ECM) (open circles) and saprotrophic (triangles)
fungal species collected from mixed boreal forests at (a) Åheden,
northern Sweden, and (b) Stadsskogen, central Sweden. Data points
represent mean values (n = 1–8). (*, Chalciporus piperatus,
traditionally considered ectomycorrhizal but the δ13C value clearly
separates it from the other ECM fungal species).
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Fig. 2 Inter-generic variation (mean ± SE) in the natural abundance
of 15N and 13C in sporocarps of ectomycorrhizal fungi collected in a
mixed boreal forest at Stadsskogen, central Sweden. Numbers in
brackets represent the number of species analysed within each genus.
Fig. 4 Intrageneric variation (mean ± SE) in the natural abundance of
15
N and 13C in sporocarps of the ectomycorrhizal genera (a) Amanita,
(b) Cantharellus, (c) Suillus and (d) Russula collected in a mixed
boreal forest at Stadsskogen, central Sweden. Numbers in brackets
represent the number of collections analysed within each species.
Fig. 3 Intra-generic variation (mean± SE) in the natural abundance
of 15N and 13C in sporocarps of the ectomycorrhizal fungal genus
Lactarius collected in a mixed boreal forest at Stadsskogen,
central Sweden. Host preference in brackets (Gen., generalist).
1, L. badiosanguineus (Picea); 2. L. camphoratus (Gen.): 3,
L. deliciosus (Pinus); 4, L. deterrimus (Picea); 5, L. fuliginosus
(Gen.); 6, L. glyciosmus (Betula); 7, L. helvus (Gen.); 8, L. mitissimus
(Gen.); 9, L. musteus (Pinus); 10, L. necator (Gen.); 11, L. obscuratus
(Alnus); 12, L. repraesentaneus (Gen.); 13, L. rufus (Gen.);
14, L. scrobiculatus (Picea); 15, L. theiogalus (Gen.);
16, L. torminosus (Betula); 17, L. trivialis (Gen.); 18,
L. uvidus (Betula); and 19, L. vietus (Betula).
Intrageneric variation was high: in most cases where genera
were represented by two or more species, there were significant
differences in both δ15N and δ13C values between species. For
example, within the genus Lactarius mean δ15N values for
individual species ranged from 1.7 to 8.5‰ (Fig. 3), with the
19 species represented spread more or less evenly across this
range. The δ13C values also showed considerable variation
among species, ranging from −27.1 to −23.5‰. However,
there was greater overlap in δ13C values among species than
with the δ15N values. Other genera also showed marked
variation among species with regard to δ15N values (Fig. 4).
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In particular, within the genus Suillus there was a striking
difference between S. variegatus and the two other species
examined (Fig. 4c).
Spatial and temporal effects
At Stadsskogen, there was a significant difference in the mean
(δ15N value of ECM fungi (F = 3.14, P = 0.011) among
plots. The sporocarps from one area (δ15N = 7.1) were
enriched by as much as 2.1‰ relative to that in three other
areas (δ15N = 5.0–5.1). There were no significant differences
in the %N, δ13C and %C values or C : N ratio among plots.
There was some evidence that sporocarp %N (F = 2.06,
P = 0.070) and δ13C (F = 1.87, P = 0.099) were both affected
by sampling date. The %N value did not show any particular
pattern over the sampling period, but δ13C showed a clear
trend to decrease as the fruiting season progressed (Fig. 5).
The δ15N values of the ECM fungi at Åheden were significantly higher than those at Stadsskogen (Table 1). An
analysis of 12 ECM species that were represented by two
or more collections at both sites revealed that with the
exception of Amanita muscaria, sporocarps were generally
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enriched in 15N at Åheden (Fig. 6). The %N of saprotrophic fungi was, however, higher at Stadsskogen than at
Åheden. No clear pattern was found with respect to %C or
δ13C values.
It was possible to construct confidence intervals for the
mean δ15N values of six species collected at Åheden in
1997. A comparison between these and data from collections made at Åheden in 1993 and 1995 (data from Taylor
et al., 1997) demonstrated that values from five out of the
six species were significantly different from the 1997 mean
Fig. 5 Mean natural 13C abundance in sporocarps of ectomycorrhizal
fungi collected in a mixed boreal forest at Stadsskogen, central
Sweden. Sporocarps were collected at six sampling periods, approx.
2 wk apart from August to October 1999.
value on at least one of the two previous collecting periods
(Table 3).
The 15N and 13C natural abundance of tree hosts and
host-specific fungi
At Åheden, the two codominant tree species, pine and spruce,
had similar 13C values (Table 4), with both values significantly
higher than those of birch. At Stadsskogen, δ13C increased in
the following order: birch < spruce < pine. The other understorey tree species at Stadsskogen had values very similar to
those of the birch (data not shown). The δ13C values of the
fungi and their relationship to host values have been presented
previously (Högberg et al., 1999b). The 15N values of pine,
spruce and birch differed little within site and only birch
differed between sites (Table 4, Fig. 7). There was a clear difference between sites with respect to host-specific fungi (Fig. 7),
with δ15N-values significantly higher at Åheden (paired t-test
T = 4.63, P = 0.04). The difference between fungal and plant
δ15N was also greater at Åheden (difference in δ15N = 3.2 ±
0.1‰, paired t-test T = 37.04, P = 0.0007). On average, the
differences in δ15N between host and host-specific fungi were
8.4‰ and 11.7‰ at Stadsskogen and Åheden, respectively.
Fig. 6 Natural 15N abundance in the
sporocarps of 12 species of ECM fungi
collected from two mixed boreal forests at
Stadsskogen, central Sweden (filled columns)
and Åheden, northern Sweden (tinted
columns). A. mu., Amanita muscaria; Ch. r.
– Chroogomphus rutilus; Co. a., Cortinarius
armillatus; Co. l., Cortinarius laniger; Co. m.,
Cortinarius malachius; D. se., Dermocybe
semisanguineus; La. r., Lactarius rufus; Le. s.,
Leccinum scabrum; Le. vs., Leccinum
versipelle; R. c., Rozites caperata; S. va.,
Suillus variegatus; T. fl., Tricholoma
flavovirens.
Table 3 Inter-annual variation in the δ15N values in sporocarps of ectomycorrhizal fungi collected in a mixed boreal forest at Åheden, northern
Sweden
Species
n
Mean value
for 1997
95% CI1
for 1997
1993 Value2,3
1995 Value2,3
Chroogomphus rutilus
Cortinarius laniger
Dermocybe semisanguinea
Lactarius rufus
Suillus variegatus
Tricholoma flavovirens
4
6
3
6
6
5
3.8
10.1
7.4
4.0
6.0
9.9
1.4–6.2
8.7–11.5
4.3–10.5
3.0–4.9
4.9–7.2
8.2–11.7
0.9
12.7
5.9
1.8
4.8
10.6
6.2
9.7
7.5
3.2
4.6
7.6
1
95% Confidence interval for the mean 15N abundance in sporocarps collected in 1997. 2Values in bold type are significantly different from the
1997 mean values. 3Data from Taylor et al. (1997).
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Table 4 Mean values for percentage nitrogen (%N), δ15N, percentage carbon (%C), δ13C and C : N ratios in current tree foliage collected from
two forests in Sweden (Åheden, northern Sweden; Stadsskogen, central Sweden)
Site
Tree species
n
%N
δ15N (‰)
%C
δ13C (‰)
C:N
Åheden
Pinus sylvestris
Picea abies
Betula pendula
Pinus sylvestris
Picea abies
Betula pendula
9
9
9
10
10
10
1.5 ± 0.1 a1
1.4 ± 0.1 a
2.3 ± 0.1 b
1.6 ± 0.1 a
1.4 ± 0.1 a
2.2 ± 0.1 b
−2.9 ± 0.2
−3.8 ± 0.2
−4.1 ± 0.82
−2.8 ± 0.3
−3.5 ± 0.3
−2.2 ± 0.52
50.6 ± 0.1
52.1 ± 0.2
49.5 ± 0.2
50.9 ± 0.2
50.2 ± 0.1
50.3 ± 0.4
−27.0 ± 0.3 a
−27.4 ± 0.3 a
−29.6 ± 0.8 b
−26.8 ± 0.2 a
−27.9 ± 0.3 b
−29.7 ± 0.2 c
32.8
37.2
21.9
32.4
36.1
22.7
Stadsskogen
1
Within site, means not sharing the same letter are significantly different at P = 0.05. 2The δ15N values for birch differed significantly between
sites (T = −2.36, P = 0.033).
Fig. 7 Natural 15N abundance in host
plants and in the sporocarps of host-specific
ectomycorrhizal fungi at Stadsskogen, central
Sweden (filled columns) and Åheden,
northern Sweden (tinted columns).
Discussion
Differences between trophic groups
A number of recent studies have suggested that ECM and
saprotrophic fungi may be separated on the basis of δ15N,
and δ13C values (Hobbie et al., 1999b; 2001; Högberg et al.,
1999b; Kohzu et al., 1999; Henn & Chapela, 2001). A
comparison between the mean values for the two groups
within the present study strongly supports this idea. However,
when viewed at the species level, only at Åheden were species
from each group clearly separated from each other (Fig. 1). An
analysis of data from all collections from Stadsskogen (327
ECM and 21 saprotrophic sporocarps) showed some overlap
between ECM and saprotrophic fungi. In particular, the δ15N
values from two species of terricolous (growing on forest floor)
saprotrophs (Clitocybe clavipes and Agaricus haemorrhoideus)
were high, placing them well within the ECM group.
However, their δ13C values clearly associated them with
© New Phytologist (2003) 159: 757–774 www.newphytologist.com
the saprotrophic fungi. New data (unpublished) obtained
from three other Agaricus species (A. aestivalis, A. arvensis
and A. bitorquis) also show consistently high δ15N values
(7–13.2‰). The high δ15N values may reflect the high %N
contents of these species.
A small number of ECM species produced sporocarps with
either low δ15N values or high δ13C, values placing them in
the saprotrophic group. Some presumed ECM species, most
notably Chalciporus piperatus, Hydnellum ferrugineum, Hydnellum peckii and Phellodon niger, overlapped strongly with
saprotrophic δ13C values. As pointed out previously (Högberg
et al., 1999b), the mycorrhizal status of C. piperatus is unconfirmed, but according to its isotopic signature it seems
likely that this taxon is a saprotroph. The three other species
are known to form mycorrhizas (Agerer, 1986–98). However,
they differ from other ECM species included in this study
because their sporocarps survive for a much longer period
(> 1 month) than other species and the mycorrhizas associated
with the sporocarps appear to be degraded. Ectomycorrhizas
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formed by these species that are not associated with sporocarps
are, however, morphologically typical of other ECM species
(A. Taylor, pers. obs.). The high δ13C values and the state of
the sporocarp-associated mycorrhizal tips suggest that, during
sporocarp formation, the mutualistic balance favours the fungus.
The reduced distinction between ECM and saprotrophic
trophic groups at Stadsskogen may, at least in part, be due to
the much greater number of species sampled compared with
Åheden. It is possible that further collections, particularly of
terricolous saprotrophs, from the sites may further increase
the degree of overlap.
Saprotrophic and ECM fungi may be distinguished on the
basis of how they obtain their C. Ectomycorrhizal fungi
depend primarily on current photosynthate from host plants
(Söderström & Read, 1987; Högberg et al., 2001) and saprotrophic fungi degrade organic matter (Swift et al., 1979).
These C sources are likely to differ in 13C content (Benner
et al., 1987; Nadelhoffer & Fry, 1988; Gleixner et al., 1993),
providing a basis for the observed differences in 13C signatures in fungi (Henn & Chapela, 2001). The differentiation
between the two functional groups (termed the EM/SAP
divide, Henn & Chapela, 2001) has been used to infer ECM
or saprotrophic lifestyles for fungal taxa of unknown trophic
status.
Henn & Chapela (2001) performed a field study in
California and a meta-analysis of three earlier studies and
found strong evidence for a distinction between ECM and
saprotrophic fungi in isotopic signatures. However, they
emphasized that the accuracy of distinguishing between the
groups deteriorated when data from geographically different
areas were compared. In addition, doubt was raised over
studies where trophic status was assigned to fungal taxa on the
basis of single sporocarps.
Kohzu et al. (1999) reported δ15N and δ13C values from a
large number of ECM, wood-decomposing and litterdecomposing fungi from a range of forest types in Japan and
Malaysia. In the Japanese material they found considerable
overlap in the δ15N-values from all three groups of fungi.
However, some of this overlap may be explained by the
inclusion of several fungi of dubious mycorrhizal status within
the ECM category (e.g. Entoloma spp., Catathelasma sp. and
Lyophyllum sp.). All three of these taxa have high δ13C values
compared with the great majority of the rest of the ECM
species. The δ15N mean value for the ECM fungi included in
the study by Kohzu et al. (1999) was 5.5‰, which is very
similar to that recorded in the present study. The range of
δ15N values, −6 to +22‰, in ECM species recorded by Kohzu
et al. (1999) was even greater than that found in the present
study (−3.6 to +19.4‰). Two Hebeloma species accounted for
the very high values in their study; both of these are known to
be associated with the buried remains of mammals or faeces
(Soponsathien, 1998; Yamanaka, 1999). Decomposition of
protein rich substrates is often accompanied by ammonia
volatilization that can leave the remaining N highly enriched
in 15N (Högberg, 1997). It seems likely that the high values
for Hebeloma reported by Kohzu et al. (1999) are a result of
this process.
As mentioned above, C sources differ between saprotrophic
and ECM fungi. By contrast to this the mycelia of both
groups are, with few exceptions, likely to forage in the same
substrates for N. In the absence of fractionation during N
metabolism this sharing of resources should mean considerable
overlap in δ15N-values between the two groups. However, it
is clear from the present study and previous works that mean
δ15N-values for the two groups may differ significantly
(Hobbie et al., 1999b). Fractionation against the heavier 15N
isotope during the transfer of N from ECM fungi to the host
plant has been proposed to explain this difference (Högberg
et al., 1996, 1999a; Taylor et al., 1997; Hobbie et al., 1999b).
In addition, this fractionation step is thought to explain the
observed difference between host and ECM δ15N-values.
Fractionation against the heavier isotope during the transfer of
N to the host plant has recently been confirmed in laboratory
studies (Högberg et al., 1999a; Kohzu et al., 2000; Emmerton
et al., 2001). Thus, the δ15N of saprotrophic fungi, which do
not transfer N taken up any further, should reflect the isotopic
signature of the source, while the δ15N of ECM fungi is
dependent on both source signature and the efficiency of
transfer of N to their host plant (Högberg et al., 1999a;
Hobbie et al., 2000). However, unlike the ECM fungi, the N
concentration and δ15N of saprotrophs growing on litter at
Stadsskogen is strongly correlated (r = 0.966, P < 0.001, n =
9). This correlation was also seen in the saprotrophs examined
by Hobbie et al. (2001). This relationship between N concentration and δ15N would probably not be found if the signature
of the N source used was the single determinant of δ15N of
saprotrophic fungi.
Taxonomic level patterns
One striking feature of the present study is that irrespective of
the taxonomic level at which the ECM data was analysed
(family, genus or species) there were significant differences
within taxonomic levels. This contrasts with Kohzu et al. (1999)
who found few significant differences at any taxonomic level.
They, however, included material from a wide range of
habitats and sites, making comparisons difficult owing to
site effects. At Stadsskogen, mean δ13C values at family and
generic levels were highly influenced by the proportion of
host-specific species found at that level. We have reported
previously that the stratification of the trees at this site results
in a clear separation between the δ13C values of the foliage of
the mycorrhizal host plants pine, spruce and birch (Table 4)
(Högberg et al., 1999b). Where fungal genera or families
contain a high proportion of pine- or birch-specific fungi, this
separates them from those groups where the majority of the
fungal species are nonspecific. Although nonspecific fungi
are likely to receive C from a number of hosts, they appear to
www.newphytologist.com © New Phytologist (2003) 159: 757–774
Research
receive most of the C from the dominant overstorey pine trees
(Högberg et al., 1999b).
By contrast to the significant differences found at higher
taxonomic levels, the variation at species level was low and
consistent within and between sites. In addition, the speciesspecific patterns in δ15N values found in species common to
both study sites suggests that there is an ecophysiological
explanation for the values observed. This assertion is supported
by the work of Lilleskov et al. (2002) who demonstrated that
species producing sporocarps with high δ15N-values had
greater capacity to utilize organic N sources than those with
lower values. We have already demonstrated that the 13C
abundance of host-specific fungi is influenced by the host
signature (Högberg et al., 1999b). The situation with N is
more complex. In addition to a wider range of source signatures
than C, there are a number of steps where fractionation for
or against 15N may occur. As already stated the difference
between host and ECM fungal signatures is thought to be
primarily due to fractionation against 15N during the transfer
of N from the fungus to the host. If this theory is correct, then
species differences in δ15N will, to some extent, reflect the
efficiency of N transfer to the host. Efficiency is used here in
a phytocentric perspective to indicate the fraction of N taken
up by the fungus that is transferred to the host. The greater the
proportion of N that is taken up and transferred, the higher
the δ15N value of the fungus will be and hence the greater the
difference between the host and the fungus. Some support
comes for this idea from the work of Gorissen & Kuyper
(2000) who showed that Suillus spp. supplied more N to the
host plant than Laccaria. These genera have high and low 15N
values, respectively.
Spatial and temporal patterns
We detected both spatial and temporal patterns in the data
set in which spatial variation ranged from local to a regional
scale and temporal variation ranged from a seasonal to a yearly
scale. The differences in 15N values between collection areas in
Stadsskogen and between the sites may reflect differences in
N availability, N source and taxonomic composition of the
fungal community sampled. At Åheden (the northern site)
low decomposition rates have resulted in an extensive
accumulation of organic matter at the soil surface. Available
mineral N levels are low, NO3-N is not detectable in most of
the soil layers while NH4-N occurs at low concentrations
(Persson et al., 2000). At more southern sites, such as
Stadsskogen, the mineral N-availability is higher (Persson &
Wirén, 1993). The higher δ15N of sporocarps observed at the
northern site may, at least in part, reflect a greater use of
organic N-sources because soil mineral N is close to zero.
Lilleskov et al. (2002) found that there was a strong relationship
between ECM species producing sporocarps with high δ15Nvalues and their ability to use organic N sources. Organic Nsources are enriched in 15N compared with mineral-N sources
© New Phytologist (2003) 159: 757–774 www.newphytologist.com
according to the few data that are available (Nadelhoffer &
Fry, 1994; Koba et al., 1998; Hobbie et al., 1999a). The higher
δ15N-values of the fungi at Åheden can also explain the
significantly greater difference between host plants and
specific ECM fungi at Åheden compared with Stadsskogen.
The decrease in δ13C values of sporocarps over the vegetation season that was found may be explained by changes in
weather related to season. The 13C signal of the carbon that is
fixed by the leaves of a plant is influenced by a number of
factors, including soil moisture, air humidity, temperature
and radiation (Farquhar et al., 1989, Dawson et al., 2002). As
autumn progresses temperature and radiation decrease and
precipitation often increases. The isotopic discrimination
against 13CO2 during plant photosynthesis is strong but
variable and can be explained by differing internal CO2
partial pressures in the leaf under different conditions. The
discrimination is stronger at low rates of photosynthesis, which
typically occur at low temperatures and low light intensity,
and weaker when plants close their stomata during drought
stress (Farquhar et al., 1989). It has also been shown that δ13C
in needles and wood differs among years due to interannual
differences in weather (Garten & Taylor, 1992; Leavitt,
1993). Furthermore, Pate & Arthur (1998) found that the
13C abundance of carbon in phloem sap also had seasonal
fluctuations, which were reflected about a month later in the
insoluble carbon of recently formed xylem in the trunk. Thus,
we expect that the lower δ13C in sporocarps at the end of the
fruiting season reflect low temperatures, moist soil and air and
low irradiance.
Conclusions
The use of stable isotopes to investigate the cryptic nature of
fungal ecology is a potentially powerful tool. However, the
data and analyses outlined in this paper demonstrate that the
collection and subsequent interpretation of field data should
be made with caution. Site-related effects may alter both the
position and the width of the divide between saprotrophic
and ECM fungi. For example, N deposition can significantly
influence the δ15N signatures of forest organisms (Gebauer
et al., 1994; Bauer et al., 2000). Despite this need for caution,
an analysis of δ13C and δ15N data from a site, based on a range
of fungal species, can give a good indication of the trophic
status of a species.
The results highlight the importance of the taxonomic
composition of the ECM community in determining the
overall δ13C and δ15N-values recorded for a site. It is clear that
significant differences in δ15N-values can be found at both the
family and the generic level. However, the large variation in
the data at these higher levels of resolution, at least with
respect to δ15N values, imply that much of the potentially
useful information may be lost when data are considered above
the species level. The observed species-level patterns suggest
that if there is an ecological functional basis to the measured
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values then it is at the level of the species that the data should
be interpreted and the level at which most information may
be obtained. Lilleskov et al. (2002) have already demonstrated
that some ECM species with high δ15N values were able to use
organic sources of N to a greater degree than species with
lower values. More studies of this type are needed to verify this
observation.
Acknowledgements
We thank Sven-Gunnar Ryman (Uppsala Museum) for help
with identification of sporocarp material. This research was
supported by grants from the Swedish Natural Sciences
Research Council and the Swedish Council for Forestry and
Agricultural Research to P. H.
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3.8
2.8–3.5
3.9–3.9
1
4
4
4
4
6
4
1
2
5
5
5
1
4
1
1
1
6
2
Betula
Betula
Betula
Betula
Pinus
Pinus
Gen.
Gen.
Gen.
Gen.
Conifers
Betula
Conifers
Conifers
Conifers
Picea
Betula
Picea
Conifers
3.4–4.3
4.0–4.1
3.6
3.1–4.6
5.8
1
N%
Range
?
n
3.3
3.9
–
–
3.7
–
4.3
–
3.2
3.9
4.0
–
3.6
3.1
2.5
4.6
4.4
–
4.6
–
Mean
0.1
–
–
–
0.2
–
0.2
–
0.1
0.2
0.1
–
0.4
0.2
0.3
0.1
0.3
–
0.3
–
SE
8.7–12.0
3.1
7.7
7.0–10.3
12.3
6.3–11.3
3.1
5.7–8.4
4.9–6.2
0.5–2.0
11.0
8.8–11.4
4.6–7.7
2.0–5.1
4.7–9.8
11.4–13.0
9.0
6.8–11.7
8.3
δ15N
Range
10.1
–
–
8.3
–
9.2
–
7.2
5.5
1.3
–
10.0
6.0
3.8
7.7
12.3
–
9.2
–
Mean
0.5
–
–
0.7
–
0.9
–
0.5
0.2
0.8
–
0.6
0.4
0.8
1.1
0.3
–
1.2
–
SE
41.5 – 43.6
9.9–11.1
41.7
41.6
40.7– 41.8
42.9
42.5 – 43.2
42.1
41.0 – 41.6
42.9 – 46.4
42.8 – 44.0
43.0
41.8 – 44.3
42.1– 43.5
45.3– 46.1
42.5 – 44.0
43.5 – 45.8
43.2
43.3– 45.9
C%
Range
Most probable host species; ?, mycorrhizal status doubtful, na, not applicable, Gen., generalist. 2Occasionally on Salix. 3Occasionally on Picea.
1
Åheden
Mycorrhizal species
Boletales
Boletaceae
Chalciporus piperatus
(Bull. ex Fr.) Bat.
Leccinum molle (Bon) Bon
Leccinum scabrum
(Bull. Ex Fr.) S.F. Gray
Leccinum variicolor Watl.
Leccinum versipelle
(Fr.) Snell
Gomphidiaceae
Chroogomphus rutilus
(Schff. ex Fr.) O.K. Miller
Suillus variegatus (Swartz ex Fr.)
O. Kuntze
Agaricales
Tricholomataceae
Tricholoma flavovirens
(Pers. ex Fr.)
Tricholoma virgatum
(Fr. : Fr.) Kumm.
Laccaria bicolor (Maire) Orton
Amanitaceae
Amanita muscaria (L.) Hook
Cortinariaceae
Cortinarius armeniacus
(Schaeff. : Fr.) Fr.
Cortinarius armillatus (Fr.) Fr.
Cortinarius bataillei
(Moser) Høiland
Cortinarius biformis Fr.
Cortinarius camphoratus
(Fr. : Fr.) Fr.
Cortinarius evernuis
(Fr. : Fr.) Fr.
Cortinarius hemitrichus
(Pers. : Fr.) Fr.
Cortinarius laniger Fr.
Cortinarius malachius Fr.
Host1
42.1
10.5
–
–
41.3
–
42.9
–
41.3
44.7
43.4
–
42.7
42.9
45.7
43.5
44.9
–
44.9
–
Mean
0.3
0.3
–
–
0.2
–
0.1
–
0.1
0.6
0.6
–
0.6
0.2
0.2
0.4
0.5
–
0.6
–
SE
–
–
−27.5
−27.6
−27.5
−26.0
−25.0
−25.4
–
−25.3
−26.6
−24.5
−26.9
–
−25.2
–
–
–
−26.4
−24.8
−27.6
−27.8 –26.9
−28.6 –26.7
−27.9–26.7
−26.7–25.5
−25.6 –24.5
−26.5 –24.7
−25.2
−25.8–24.9
−27.6 –25.0
−25.5–24.0
−27.8–24.6
−25.3
−25.8–24.6
−25.6
−24.8
−27.8
−28.7–24.7
−24.9 –24.7
Mean
−22.3
δ13C
Range
0.7
0.1
–
–
0.3
–
0.6
–
0.3
0.4
0.5
–
0.4
0.2
0.3
0.4
0.3
–
0.2
–
SE
Appendix 1 Values for %N, δ15N, %C, δ13C and C : N ratios in sporocarps of ectomycorrhizal (ECM) and saprotrophic fungi collected from two forests in Sweden. (Åheden - northern Sweden;
Stadsskogen, central Sweden).
768 Research
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© New Phytologist (2003) 159: 757–774 www.newphytologist.com
5.0
2.7
1
2
4
6
1
1
2
1
1
Conifers
(Pinus)
Gen.
Gen.
Conifers
Gen.
na
na
4.4–8.0
6.9
4.4–4.8
3.4
2.9–5.6
4.7
3.7–4.6
5
1
3
1
6
1
2
Gen.
Pinus
Populus
Betula
Betula
Betula
Betula
5.0–6.4
2
?
2.0
1
na
na
2.7–2.9
5.1
3.2–4.0
3.6
4.6
3.1–3.3
3.0–4.8
3.7
3.3–5.0
1
3
Gen.
Conifers
3.5–4.9
6
Betula
n
N%
Range
–
4.1
–
4.0
6.5
–
4.5
5.7
–
–
–
2.8
–
3.6
–
–
3.3
3.9
–
4.2
4.0
Mean
–
0.4
–
0.4
0.6
–
0.1
0.7
–
–
–
0.1
–
0.2
–
–
0.1
0.4
–
0.5
0.2
SE
5.3
9.2–14.2
2.2
2.6–9.5
6.1–10.3
17.5
7.5–11.4
9.2–9.4
–
11.7
–
7.3
8.5
–
9.0
9.3
–
–
−1.7
0.2
–
−2.0
−1.9–2.2
1.4
–
4.0
–
–
11.9
8.1
–
7.4
5.7
Mean
14.1
2.7–5.0
6.3
8.6
9.7 −14.2
5.9 −10.2
5.4
6.0–8.2
4.2–6.7
δ15N
Range
–
2.5
–
1.1
0.9
–
1.2
0.1
–
–
–
0.14
–
0.4
–
–
2.2
0.9
–
0.7
0.4
SE
42.3
40.8 – 44.0
42.9
42.1– 45.9
39.7– 43.1
40.5
42.2– 42.9
42.4 – 42.8
42.5
44.7
42.3
40.1– 41.2
44.7
43.3– 45.2
42.5
42.9
42.4 – 42.6
40.6 – 42.8
43.7
42.1– 44.0
42.2– 43.5
C%
Range
Most probable host species; ?, mycorrhizal status doubtful, na, not applicable, Gen., generalist. 2Occasionally on Salix. 3Occasionally on Picea.
1
Cortinarius pholideus
(Fr. : Fr.) Fr.
Cortinarius scaurus (Fr. : Fr.) Fr
Cortinarius semisanguineus
(Fr.) Gill.
Cortinarius strobilaceus Mos.
Cortinarius traganus Fr.
Rozites caperata (Pers. ex Fr.)
Karst.
Russulales
Russulaceae
Lactarius rufus (Scop.) Fr.
Russula paludosa Britz
Thelephorales
Bankeraceae
Phellodon tomentosa (L. : Fr.)
Baker
Saprotrophic species
Agaricales
Tricholomataceae
Armillaria borealis
Marx. & K. Korh.
Strophariaceae
Stropharia hornemanii
(Fr. : Fr.) Lund.
Cortinariaceae
Gymnopilus penetrans
(Fr.). Murr
Coriolales
Coriolaceae
Trametes hirsuta
(Wulfen : Fr.) Pil.
Stadsskogen
Mycorrhizal species
Boletales
Boletaceae
Chalciporus piperatus
(Bull. ex Fr.) Bat.
Boletus edulis Bull. ex Fr.
Boletus pinophilus Pil. & Dermek
Leccinum aurantiacum
(Bull. ex St. Am.) S.F. Gray
Leccinum holopus (Rostk.) Watl
Leccinum scabrum
(Bull. ex Fr.) S.F. Gray
Leccinum variicolor Watl.
Leccinum versipelle (Fr.) Snell
Host
1
–
42.4
–
44.0
41.7
–
42.5
42.6
–
–
–
40.7
–
44.2
–
–
42.5
41.5
–
43.1
42.7
Mean
–
1.6
–
0.6
0.7
–
0.2
0.2
–
–
–
0.5
–
0.3
–
–
0.1
0.5
–
0.6
0.2
SE
–
−24.1
–
−22.0
−24.6
–
−27.3
–
−26.4
–
−27.1
−22.6–21.4
−25.4–24.0
−24.7
−28.2–26.4
−29.2
−28.0 –25.4
−26.1
−27.9–26.3
–
−24.0
−22.4
–
−24.9
–
−25.4 –23.6
−25.0
−23.1
–
−25.2
−25.8
−27.0
−25.5−24.8
−26.3–25.3
−23.8
–
−24.9
−25.2
−25.6 –24.2
−23.9–23.7
−27.6
Mean
−28.8–26.5
δ13C
Range
–
0.8
.–
0.8
0.2
–
0.5
0.6
–
–
–
0.09
–
0.3
.–
–
0.4
0.2
.–
0.4
0.4
SE
Research
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2.3– 4.1
3.6 – 4.0
3.5
3.3–3.4
3.2– 4.7
5
3
2
1
2
5
Picea
Gen.
Gen.
Pinus
Conifers
Betula
4.5–6.0
3.2–5.4
5
Conifers
1.9– 4.3
2
Pinus
3.9
4.3– 4.6
3
Gen.
1
2.5 – 4.2
7
Pinus
Picea
3.4 –5.2
3.0 – 4.5
3.0 – 4.0
5
6
6
Pinus
Pinus
Pinus
3.3– 4.7
2.4 – 4.0
3
Picea
5
2.3–2.9
6
Pinus
Gen.
4.5
1
Gen.
2.6–5.9
4.5–6.0
N%
Range
5
4
n
Pinus
Gen.
Host1
3.9
3.3
–
3.8
5.1
3.2
4.6
–
4.0
3.1
4.1
3.4
4.0
3.7
3.4
3.3
2.6
–
4.4
5.2
Mean
0.3
0.1
–
0.2
0.5
0.3
0.4
–
0.3
1.2
0.4
0.2
0.3
0.2
0.2
0.5
0.1
–
0.6
0.4
SE
10.5–13.8
7.8–8.6
13.1
7.2–8.2
12.5
8.2
–
2.7
1.6
−1.7
−3.6–0.1
2.4–3.5
3.1
–
3.0
9.5
9.1
4.8
6.7
12.5
11.8
0.6–5.5
6.4
1.8–3.3
7.7–11.2
3.9–19.4
2.4–6.9
4.4–9.8
10.3–15.0
8.6–13.7
6.0
4.2
−0.45– 6.6
4.2–7.0
–
12.8
5.6
Mean
6.7
10.4–18.9
2.9–8.5
δ15N
Range
0.7
0.4
–
0.5
2.0
0.6
1.0
–
0.5
1.8
5.1
0.7
0.9
0.7
0.8
0.9
1.6
–
1.5
1.2
SE
42.5– 43.5
42.1– 42.5
41.1
44.0– 44.4
42.3– 43.0
40.9– 42.8
41.4– 42.5
43.0
41.8– 46.0
42.7– 45.5
42.2– 42.6
42.7– 44.1
41.8– 43.5
43.6– 44.6
42.7– 43.6
42.7– 43.8
43.2– 47.2
42.8
40.0–44.0
43.0–43.5
C%
Range
Most probable host species; ?, mycorrhizal status doubtful, na, not applicable, Gen., generalist. 2Occasionally on Salix. 3Occasionally on Picea.
1
Leccinum vulpinum Watl.
Xerocomus badius
(Fr. : Fr.) Gilb.
Xerocomus subtomentosus
(L : Fr) Quél.
Gomphidiaceae
Chroogomphus rutilus
(Schff. ex Fr.) O.K. Miller
Gomphidius glutinosus
(Schff.) Fr
G. roseus L. : Fr.
Suillus bovinus (L.) Kuntze
Suillus luteus
(L. ex Fr.) S.F. Gray
Suillus variegatus
(Swartz ex Fr.) O. Kuntze
Paxillaceae
Paxillus involutus (Batsch) Fr.
Rhizopogonaceae
Rhizopogon obtextus
(Spreng) S. Rauschert
Strobilomycetaceae
Tylopilus felleus
(Bull. : Fr.) Karst.
Agaricales
Hygrophoraceae
Hygrophorus agathosmus
(Fr.) Fr.
Hygrophorus camarophyllus
(Alb. & Schw. : Fr.) Dumée et al.
Hygrophorus olivaceoalbus
(Fr. ex Fr.) Fr.
Tricholomataceae
Laccaria laccata (Scop. ex Fr.)
Bk. & Br.
Tricholoma flavovirens
(Pers. ex Fr.)
Tricholoma fracticum
(Britz.) Kreisel
Tricholoma fucatum
Kummer (Fr.)
Tricholoma fulvum
(DC : Fr.) Sacc
Appendix 1 continued
43.0
42.3
–
44.2
42.6
42.2
41.9
–
43.7
44.5
42.4
43.1
42.6
44.0
43.1
43.3
45.3
–
42.0
43.2
Mean
0.2
0.3
–
0.2
0.2
0.4
0.2
–
0.7
1.4
0.1
0.2
0.3
0.1
0.1
0.3
0.6
–
0.7
0.1
SE
−26.0
−25.3
−26.1
–
−25.8
−26.6
−26.7–24.1
−26.3–24.4
−26.7–25.6
−24.3
−26.3–25.4
−27.3–26.0
−24.6
−26.4 –23.5
−25.0
−25.2–24.8
–
−26.6
−26.9–26.2
−28.1
−24.3
−25.8–23.2
−25.0
−24.9
−25.2
−24.6
−25.5–23.8
−25.8–24.5
−24.9–23.9
−25.7–24.3
−26.4
−27.1–25.9
–
−25.9
−25.3
−25.0
−25.3
−25.8–23.8
−26.2–24.4
−26.1–24.4
Mean
δ13C
Range
0.3
0.4
–
0.5
0.6
0.5
0.6
–
0.2
0.2
0.2
0.3
0.3
0.2
0.2
0.4
0.3
–
0.3
0.4
SE
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© New Phytologist (2003) 159: 757–774 www.newphytologist.com
3.9–5.8
3.7
3.7
4.0–6.2
4.2–5.2
3.9–4.3
2.7–3.9
3.3–4.1
4.7
2
6
4
8
5
7
1
1
3
3
2
1
1
4
2
2
3
3
7
1
7
1
3
3
2
3
7
4
Gen.
(Betula)
Gen.
Conifers
Gen.
Gen.
Betula
Conifers
Betula
(Betula)
(Conifers)
Conifers
Gen.
(Picea)
(Picea)
Conifers
Conifers
Picea
Conifers
Betula
Conifers
Conifers
Conifers
Conifers
(Pinus)
Salix
Conifers
Gen.
2.8–3.5
3.3–3.5
3.1–4.1
3.3–3.9
3.4–5.9
3.5–5.5
4.6
3.4–4.7
2.9–3.9
3.6–3.8
2.7–5.0
2.7
3.3–3.8
4.0
3.3–5.1
3.6–4.8
4.1–4.8
3.1–5.2
3.7–5.0
1
2.7
N%
Range
Picea
n
3.2
3.4
3.4
3.6
5.0
4.4
–
3.9
–
4.1
3.5
3.7
3.6
3.7
3.8
–
3.5
–
5.2
4.6
–
–
4.9
4.2
4.1
4.4
4.0
4.4
–
Mean
0.2
0.1
0.3
0.3
0.9
0.3
–
0.2
–
0.1
0.4
0.1
0.2
0.1
1.1
–
0.2
–
0.6
0.3
–
–
0.3
0.3
0.2
0.2
0.3
0.7
–
SE
1.6–2.8
5.6–8.8
4.0–4.3
8.3–9.7
1.7–6.2
3.5–8.1
6.0
3.4–8.8
5.4
5.8–7.1
2.0–7.2
2.0–4.9
4.1–6.1
5.2–11.5
4.4–8.8
4.3
4.9–6.6
7.6
8.4–10.5
8.6–10.1
5.4
10.7
2.2–5.5
3.5–5.2
0.2–3.2
7.1–8.8
1.2–2.8
9.8–11.6
9.4
δ15N
Range
2.1
6.4
4.2
9.0
3.2
6.2
–
6.4
–
6.3
5.0
3.5
5.3
8.3
6.6
–
5.8
–
9.1
8.8
–
–
4.1
4.3
2.1
7.9
2.1
10.7
–
Mean
0.2
1.0
0.1
0.7
1.5
0.6
–
0.7
–
0.4
1.6
0.7
0.4
3.2
2.2
–
0.9
–
0.7
0.7
–
–
0.6
0.3
0.4
0.4
0.2
0.9
–
SE
42.0–43.0
41.7–42.6
40.3–42.0
42.8–43.0
42.4–42.7
41.9–42.7
45.1
41.6–43.3
42.4
40.6–42.1
42.5–44.1
41.6–42.2
42.4–43.2
41.7–41.9
42.7–43.8
43.5
41.9–43.2
43.0
42.0–42.9
42.5–43.0
42.4
41.6
41.6–45.7
40.4–44.3
41.2–46.1
43.2–47.9
44.4–47.0
42.9–43.4
43.1
C%
Range
Most probable host species; ?, mycorrhizal status doubtful, na, not applicable, Gen., generalist. 2Occasionally on Salix. 3Occasionally on Picea.
1
Tricholoma vaccinum
(Pers. : Fr) Kumm.
Tricholoma virgatum
(Fr. : Fr.) Kumm.
Amanitaceae
Amanita fulva (Sch : Fr) Fr.
Amanita muscaria (L.) Hook
Amanita porphyria
(Alb & Schw : Fr) Mlady
Amanita rubescens
(Pers : Fr.) SF Gray
Amanita virosa
(Kamarck) Bertillon
Cortinariaceae
Cortinarius albo-violaceus
(Pers : Fr.) Fr.
Cortinarius armeniacus.
(Schaeff. : Fr.) Fr
Cortinarius armillatus (Fr.) Fr
Cortinarius bolaris
(Pers : Fr.) Fr.
Cortinarius brunneus Fr.
Cortinarius camphoratus
(Fr. : Fr.) Fr.
Cortinarius crocea
(Schff.) Big. & Guill.
Cortinarius gentilis (Fr.) Fr.
Cortinarius laniger Fr.
Cortinarius limonius
(Fr. ex Fr.) Fr.
Cortinarius malachius Fr.
Cortinarius muscigenus Peck
Cortinarius paleaceus
(Weinm.) Fr.
Cortinarius pholideus
(Fr. : Fr.)Fr.
Cortinarius semisanguineus
(Fr.) Gill.
Cortinarius speciosissimus
Kühner & Rom.
Cortinarius stillatitius Fr.
Cortinarius strobilaceus Mos.
Cortinarius traganus Fr.
Cortinarius uliginosus Berk.
Cortinarius vibratilis
(Fr. : Fr.) Fr.
Hebeloma crustuliniforme
(Bull : Fr.) Quél.
Host1
42.7
42.4
41.3
42.9
42.6
42.2
–
42.8
–
41.4
43.2
41.9
42.8
41.8
43.3
–
42.6
–
42.4
42.8
–
–
43.4
42.1
44.1
45.6
45.6
43.2
–
Mean
0.2
0.4
0.5
0.1
0.1
0.1
–
0.2
–
0.4
0.5
0.1
0.2
0.1
0.6
–
0.7
–
0.3
0.1
–
–
0.5
0.6
0.8
1.0
0.3
0.3
–
SE
−24.3
−26.3
−26.3
−24.8
−25.3
−25.1
–
–
−27.5
−27.0
−26.1
–
–
−25.6
−25.9
−25.9
−25.5
−26.1
−25.7
–
−25.2
–
−24.2
−25.5
−25.6
−28.0
−25.1
−27.1
−24.5–24.2
−28.3–25.0
−27.3–25.7
−26.2–23.9
−25.6–24.4
−26.2–23.7
−28.4
−25.1
−28.4–26.7
−27.9–26.4
−26.3–26.0
−23.7
−29.2
−26.0–24.8
−27.0–24.9
−27.7–24.1
−26.9–24.1
−26.8–25.3
−27.4–23.6
−26.3
−25.6–24.8
−25.8
−25.3–23.1
−26 1–24.6
−26.6–24.6
−29.5–27.1
−27.3–23.9
−30.2–25.9
Mean
–
–26.9
δ13C
Range
SE
1.0
0.6
0.5
1
0.8
0.4
–
0.1
–
0.8
0.5
0.5
0.3
1.1
1.8
–
0.2
–
0.5
0.5
–
–
0.3
0.2
0.5
0.3
0.3
0.1
–
Research
771
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4.8
3.9–4.6
4.0–4.4
4.0–5.1
3.6–4.2
3.4–4.9
3.5–3.6
3.2–5.0
3.2–5.1
3.8
3.1
3.2–3.9
4.3–5.6
3.5–4.0
1
1
1
3
1
1
5
2
5
6
8
2
4
4
1
1
5
3
1
3
2
3
3
1
2
5
5
1
Gen.
Gen.
Conifers
Gen.
Gen.
Conifers
Gen.
Picea
Gen.
pinus
Picea
Betula
Betula
Gen.
Gen.
Pinus
Gen.
Alnus
Gen.
Gen.
Picea
Gen.
Betula
Gen.
Betula2
Betula2
Conifers
Betula
3.9
3.2–5.0
2.2–4.9
3.0–3.9
3.3
3.4–4.4
3.2–3.4
3.2
5.6–5.9
5.3
4.8
4.8
3.8
4.6–5.1
2.7–3.5
2
Gen.
N%
Range
n
Host1
–
4.1
3.9
3.5
–
3.8
4.8
3.9
3.3
–
5.7
3.9
4.2
3.6
3.8
4.3
–
–
3.5
4.5
4.2
–
4.3
–
–
–
–
5.0
3.1
Mean
–
0.9
0.5
0.2
–
0.2
0.4
0.3
0.1
–
0.1
0.1
0.2
0.1
0.4
0.4
–
–
0.1
0.2
0.2
–
0.1
–
–
–
–
0.2
0.4
SE
6.6
2.6–4.5
−0.2–3.0
−0.3–4.5
−0.7
4.3–6.3
2.0–3.0
1.7–2.1
7.1–8.1
6.4
5.0–6.8
3.8–9.5
6.4–8.9
6.2–6.6
2.5–5.8
5.9–8.2
5.4
1.6
0.5–4.2
1.9–5.4
7.6–9.4
1.3
5.1–8.4
1.5
2.9
3.5
4.1
4.2–4.3
8.4–8.5
δ15N
Range
–
3.5
1.7
1.4
–
5.5
2.5
2.0
7.6
–
6.0
6.5
7.5
6.4
4.3
6.9
–
–
2.5
3.8
8.5
–
6.6
–
–
–
–
4.2
8.4
Mean
–
0.9
0.6
0.8
–
0.6
0.3
0.1
0.5
–
0.6
0.9
0.3
0.2
0.7
0.6
–
–
0.7
0.6
0.9
–
0.6
–
–
–
–
0.03
0.1
SE
45.4
43.8–46.5
43.9–45.1
44.1–45.2
45.4
43.6–44.8
43.0–45.2
42.8–44.7
45.0–45.2
44.1
42.5–43.2
44.4–46.8
43.9–46.8
44.8–44.9
43.9–45.6
42.5–45.4
44.1
43.6
43.6–45.8
43.9–45.3
44.2–44.6
43.4
41.3–42.9
43.2
43.9
43.0
42.9
42.4–43.6
41.7–41.8
C%
Range
Most probable host species; ?, mycorrhizal status doubtful, na, not applicable, Gen., generalist. 2Occasionally on Salix. 3Occasionally on Picea.
1
Hebeloma mesophaeum
(Pers) Quél.
Inocybe acuta Boud.
Inocybe cincinnata (Fr.) Quél.
Inocybe friesii Heim.
Inocybe geophylla
(Sow. ex Fr.) Kummer
Inocybe pseudodestricta
Stangl. & Veselsky
Inocybe tigrina Heim
Rozites caperata
(Pers. ex Fr.) Karst.
Russulales
Russulaceae
Lactarius badiosanguinea
Kuehn. & Rom.
Lactarius camphoratus
(Bull.) ex Fr.
Lactarius deliciosus Fr.
Lactarius deterrimus Groeger
Lactarius fuliginosus Fr.
Lactarius glyciosmus Fr.
Lactarius helvus Fr.
Lactarius mitissimus Fr.
Lactarius musteus Fr.
Lactarius necator
(Bull. em Pers. ex Fr.) Karst.
Lactarius obscuratus
(Lasch) Fr.
Lactarius repraesentaneus
Britz
Lactarius rufus (Scop.) Fr.
Lactarius scrobiculatus
(Scop. ex Fr.) Fr.
Lactarius theiogalus
(Bull : Fr.) SF Gray
torminosus (Schff. ex Fr.)
S.F. Gray
Lactarius trivialis Fr.
Lactarius uvidus Fr.
Lactarius vietus Fr.
Russula atrorubens Quél.
Russula betularum Hora
Appendix 1 continued
–
45.2
44.5
44.7
–
44.2
44.4
44.0
45.1
–
43.0
45.8
45.2
44.9
44.5
43.7
–
–
44.5
44.8
44.4
–
42.1
–
–
–
–
43.0
41.7
Mean
–
1.3
0.2
0.2
–
0.3
0.7
0.6
0.1
–
0.3
0.4
0.3
0.1
0.4
0.7
–
–
0.4
0.3
0.2
–
0.3
–
–
–
–
0.4
0.1
SE
Mean
−26.8
–
–
–
−25.0
–
–
−24.7
−26.2
−26.8
−24.9
−26.6
−24.9
−27.0
−23.8
–
–
−26.0
−27.1
–
−25.3
−27.3
−27.1
−25.8
–
−26.0
−26.2
−25.5
–
δ13C
Range
−27.2–26.5
−26.2
−26.5
−27.0
−25.4–24.5
−26.5
−26.9
−25.7–24 0
−26.2
−27.7–25.7
−25.6–24.0
−27.9–25.3
−25.2–24.7
−27.6–26.3
−24.2–23.5
−25.1
−24.9
−27.0–24.5
−26.4–27.5
−26.5
−25.8–24.9
−27.7–26.9
−28.1–26.6
−24.2–26.7
−23.5
−26.2–25.8
−26.8–25.3
−26.3–24.3
−25.1
–
0.2
0.3
0.3
–
0.8
0.5
0.3
0.4
–
0.4
0.2
0.3
0.3
0.3
0.2
–
–
0.5
0.4
0.1
–
0.3
–
–
–
–
0.3
0.3
SE
772 Research
© New Phytologist (2003) 159: 757–774 www.newphytologist.com
2.9–3.8
3.2–4.1
3.2
2
2
1
2
3
6
3
2
4
2
1
1
2
1
Pinus
Conifers
Pinus3
Conifers
Gen.
Gen.
Gen.
Picea
and Betula
(Picea)
Conifers
Conifers
Gen.
na
na
2.8
4.4–4.7
4.2
5.8
4.6–5.6
2.7–3.7
2.9–3.2
2.8–3.0
2.4–3.1
2.6–4.1
2.6–3.9
3.7
3.3–3.8
4.2
3.4
4.0
3.6–4.0
1
2
1
1
1
3
(Picea)
Conifers
Gen.
Picea
Picea
Pinus3
3.0–3.6
3.2–4.0
3.6–4.1
4.1
2.4
3.7
2
5
2
1
1
1
n
Pinus
Conifers
Pinus2
Gen.
Betula
Conifers
Host
N%
Range
–
4.6
–
–
5.1
3.4
3.0
2.9
2.7
3.2
3.2
3.3
3.7
–
–
3.5
–
–
–
3.8
3.3
3.7
3.8
–
–
–
Mean
–
0.1
–
–
0.5
0.2
0.1
0.1
0.2
0.2
0.7
0.4
0.4
–
–
0.3
–
–
–
0.1
0.3
0.2
0.2
–
–
–
SE
–
−3.0
−3.2–2.8
0.2
–
–
10.7
1.5
5.3
2.6
8.6
8.9
6.1
4.4
−0.03
–
–
3.8
–
–
–
9.0
5.1
0.8
3.4
–
–
–
Mean
8.1
10.4
9.8–11.5
0.3–3.0
5.1–5.5
2.3–2.8
7.0–9.6
7.9–9.8
5.1–7.1
4.1–4.7
−0.2–0.2
−0.4
4.4
2.6–5.0
1.8
7.9
0.5
7.1–10.5
5.0–5.1
−0.3–2.1
1.5–5.4
8.4
8.4
2.6
δ15N
Range
SE
–
0.2
–
–
0.9
0.7
0.1
0.3
0.8
0.3
1.0
0.3
0.2
–
–
1.2
–
–
–
1.0
0.1
0.4
2.0
–
–
–
44.6
41.0–42.2
46.1
45.9
46.5–47.1
43.2–45.2
44.0–44.2
42.9–44.0
43.1–43.9
43.4–46.0
43.8–45.1
45.4–47.4
42.4–43.3
43.3
42.6
43.2–43.4
42.3
46.3
45.7
43.9–44.8
41.9–42.7
43.0–43.8
43.6
45.3
45.6
43.3
C%
Range
Most probable host species; ?, mycorrhizal status doubtful, na, not applicable, Gen., generalist. 2Occasionally on Salix. 3Occasionally on Picea.
1
Cantharellus tubaeformis Fr.
Thelephorales
Thelephoraceae
Hydnellum ferrugineum
(Fr. : Fr.) Karst.
Hydnellum peckii
Banker apud Peck
Phellodon niger
(Fr. : Fr.) Karst.
Stadsskogen
Saprotrophic species
Boletales
Paxillaceae
Hygrophoropsis aurantiaca
(Wulf. : Fr.) Mre.
Paxillus atromentarius
(Batsch : Fr.) Fr.
Agaricales
Tricholomataceae
Russula coerulea Fr.
Russula decolorans Fr.
Russula emetica Fr.
Russula foetens Fr.
Russula gracillima Schaeff.
Russula griseascens
(Bon & Gaugué) L. Marti
Russula integra L. ex Fr.
Russula paludosa Britz.
Russula puellaris Fr.
Russula queletii Fr.
Russula rhodopoda Zv.
Russula sanguinea
(Bull. ex St. am.) Fr.
Russula sardonia Fr. ex Rom.
Russula vinosa Lindbl.
Russula xerampelina
(Schff. ex Secr.) Fr.
Cantharellales
Albatrellaceae
Albatrellus ovinus (Fr.)
Kotl. & Pouz.
Hydnaceae
Hydnum repandum L. : Fr.
Hydnum rufescens Fr.
Cantharellaceae
Cantharellus cibarius Fr.
Cantharellus lutescens Fr.
1
–
41.6
–
–
46.8
44.3
44.1
43.5
43.5
44.6
44.5
46.4
42.9
–
–
43.3
–
–
–
44.4
42.3
43.3
43.6
–
–
–
Mean
–
0.6
–
–
0.3
0.5
0.1
0.6
0.2
0.4
0.6
1.0
0.4
–
–
0.1
–
–
–
0.3
0.4
0.1
0.1
–
–
–
SE
−25.4
−25.4
−26.3
−25.0
−25.2
−22.5
–
–
−26.5–25.4
−25.8–24.9
−27.2–23–2
−26.6–26.0
−24.9–25.0
−25.9–24.4
−22.9–22.2
−23.3
−22.7
–
−25.9
−27.5–25.0
−25.6–25.1
−26.3
−23.0
−26.3
−25.3
–
−25.4
−25.4–24.9
−25.5
−27.5
−26.0
−24.9–24.1
−21.6
–
−25.2
–
–
–
−24.5
−24.4–23.9
−25.7–24.9
−24.9
−24.8
−27.7
−26.4
−22.3–20.8
Mean
−24.1
−25.4
−24.9
–
–
–
δ13C
Range
–
0.8
–
–
0.4
0.3
0.2
0.1
0.3
0.6
0.6
1.2
0.3
–
–
0.3
–
–
–
0.2
0.2
0.1
0.1
–
–
–
SE
Research
773
n
3
1
1
2
3
1
2
1
2
2
1
Host1
na
na
na
na
na
na
na
na
na
na
na
9.0
1.5–1.9
3.8–4.5
8.1–8.5
5.5
7.3–8.9
6.0
8.2–9.1
5.1
6.6
4.3–5.2
N%
Range
–
1.7
4.1
8.3
–
8.0
–
8.6
–
–
4.7
Mean
–
0.2
0.3
0.2
–
0.5
–
0.5
–
–
0.3
SE
4.3
−3.0
–
−4.6–1.4
−2.0
5.9
–
2.2
–
2.5–6.0
4.9–6.8
1.0
1.5–2.7
2.0
6.7
–
−3.0
5.4–7.9
–
−2.1
−1.1–2.9
0.8
Mean
δ15N
Range
–
1.6
1.7
0.9
–
0.4
–
1.2
–
–
0.5
SE
44.1
42.2–43.2
42.8–43.7
39.2–40.8
42.2
35.9–40.4
40.6
39.5–40.2
44.1
43.7
41.6–43.0
C%
Range
Most probable host species; ?, mycorrhizal status doubtful, na, not applicable, Gen., generalist. 2Occasionally on Salix. 3Occasionally on Picea.
1
Clitocybe clavipes
(Pers. ex Fr.) Kummer
Mycena pura (Pers. ex Fr.)
Kummer
Mycena rosella (Fr.) Kummer
Entolomataceae
Clitopilus prunulus
(Scop. ex Fr.) Kummer
Entoloma nitidum Quél.0.2
Rhodocybe nitellina (Fr.) Sing.
Agaricaceae
Agaricus silvaticus Schaeff.
Cystoderma carcharias
(Pers. ex Secr.) Fay.
Cortinariaceae
Gymnopilus junonius (Fr. : Fr.)
Orton
Hericiales
Auriscalpiaceae
Auriscalpium vulgare S.F.Gray
Lycoperdales
Lycoperdaceae
Lycoperdon foetidum Bonord.
Appendix 1 continued
–
42.7
43.3
40.0
–
38.8
–
39.8
–
–
42.3
Mean
–
–
–
–
–
0.5
0.5
0.8
1.5
0.4
SE
−23.5
–
−22.0
–
−24.0
−23.9–23.1
−20.8
−23.3–22.7
−23.8
−26.1–21.8
−24.5
–
−22.2
−22.9
−23.0–22.9
−22.8–21.7
–
–
−22.9
−23.3
−25.6
Mean
−24.4–26.4
δ13C
Range
–
0.5
2.2
0.3
–
0.2
–
0.1
–
–
0.6
SE
774 Research
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