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Abstract We describe the soil microfungal communities
in 30-year-old birch (Betula pendula Roth) stands plant-
ed either on former spruce forest soil (BS) or on former
arable soil (BF) and compare these with the soil micro-
fungal communities in spruce forests (S), arable fields
(F) and old deciduous forests (D). Fungi were isolated
from 0- to 3-cm and 3- to 6-cm samples collected in Sep-
tember 1997 and May 1998. Principal components anal-
ysis differentiated fungal communities in the S and BS
sites from those in the other site types. The Morisita-
Horn index of similarity indicated that fungal communi-
ties in the F and BF sites were less similar to those in the
other site types. Fungal communities of the BS and S
sites were more similar in the 3- to 6-cm layer than in
the 0- to 3-cm layer, suggesting that it takes >30 years to
replace the spruce litter and associated fungal communi-
ty. Similarity between fungal communities in the F and
BF sites was low, indicating significant changes in the
fungal community composition following afforestation
of field soil by birch. Fungal communities in the BS and
BF sites were more similar to each other than those of
their original site types. Fungal communities of the BS,
BF and S sites were more similar to those of the D sites
than those of the F sites were to the D sites. Differences
between the fungal communities of the different site
types were attributed primarily to litter quality, earth-
worm community, and secondarily to organic matter, pH,
KCl-extractable NH4+, and PO43–.
Keywords Fungal community · Afforestation ·
Deciduous forest · Microfungi
Introduction
The area of broadleaved forest stands (particularly birch)
is increasing and expected to continue to increase in the
Nordic countries, mainly due to three factors: (1) refor-
estation of agricultural land, largely with silver birch be-
cause of its economic importance and good growth on
arable soil, (2) recent trends in forestry practice, tending
to retain or increase biodiversity of the forest ecosystem
e.g. by leaving a mixture of deciduous trees in conifer-
ous stands, and (3) the expected increase in CO2and av-
erage global temperatures, resulting in enhanced compet-
itive ability of broadleaved tree species.
This type of land use change affects soil organisms
and processes through changes in the vegetation and
therefore the quantity and quality of organic matter
(OM) inputs both above and below ground. Replacement
of one vegetation type with another has been shown to
significantly affect humus and soil development (Muys
et al. 1992), and C and N pools and fluxes (e.g. Glaser et
al. 2000; Solomon et al. 2000; Yeates et al. 2000; Zeller
et al. 2000; Zou and Bashkin 1998).
Changes in land use may affect the microbial commu-
nity through altered OM or nutrient characteristics or di-
rectly through the vegetation. It is well documented that
different leaf and wood litters have distinguishable mi-
crobial assemblages due to differences in litter chemical
components (e.g. C, N, phenolics, lignin) (see Christensen
1969; Frankland 1966; Kendrick 1963; Lumley et al.
2001). However, direct evidence of land use affecting the
microbial community is scarce. Zeller et al. (2000) ob-
served increased fungal biomass in pastures abandoned
for 10 years. Also it appears that changes in plant com-
position within a vegetation type may affect the microbi-
al community. In an experiment involving selective re-
moval of plant functional groups from grassland, Wardle
et al. (1999) observed that differences in the phospholip-
id fatty acid composition of the soil microbial communi-
ty were related to treatments, suggesting that 3–4 years
of changed plant community structure were enough to
cause changes in the microbial community.
M.A. McLean (✉) · V. Huhta
Department of Biological and Environmental Science, PO Box 35,
University of Jyväskylä, 40351 Jyväskylä, Finland
Present address:
M.A. McLean, Department of Life Sciences,
Indiana State University, Terre Haute, IN 47809, USA,
e-mail: lsmclean@isugw.indstate.edu,
Tel.: +1-812-2372425, Fax: +1-812-2374480
Biol Fertil Soils (2002) 35:1–12
DOI 10.1007/s00374-001-0431-7
ORIGINAL PAPER
M. A. McLean · V. Huhta
Microfungal community structure in anthropogenic birch stands
in central Finland
Received: 21 September 2001 / Published online: 17 November 2001
© Springer-Verlag 2001
Soil chemical changes following changes in land use
can last many years. Using variations in the natural
abundance of 15N, Koerner et al. (1999) showed that pre-
vious land use (i.e. arable field or garden) could be de-
tected even 100 years after afforestation. In forests in the
northeastern U.S., Compton and Boone (2000) observed
that C, N and P contents and their ratios were consistent-
ly different between sites which had been cultivated
>90 years ago and those which had been forested. If
chemical properties of previous land uses can persist in
the soil for many decades, one might expect that the mi-
crobial communities associated with previous litter types
might be equally persistent in the soil. As evidence of
this possibility, dominant fungal species characteristic of
both forests and grasslands were observed by Christensen
(1981) in a grassland which had once been forested.
Here we were interested in the persistence or alteration
in the fungal community following a change in land use
over the relatively short term (30 years). Did the fungal
communities in an spruce forest soil or arable soil replanted
with birch come to resemble that of a natural deciduous
stand, or did they retain the character of their original site
types? The main objective of this study was to describe the
structure of the saprotrophic fungal community in anthropo-
genic silver birch stands that originally were: (1) spruce for-
ests, or (2) cultivated fields and compare these with (3)
original spruce forests, (4) original cultivated fields and (5)
natural deciduous forests of the same latitude.
Materials and methods
Site descriptions
Six main planted birch (Betula pendula Roth) stands were chosen
in central Finland. Three of these were grown on spruce forest soil
after clear cutting (BS) and three had been planted on arable soil
2
Table 1 Site descriptions, including location, soil, stand age, stand density, and other vegetation
Site Soil, pH Stand Stand Height Shrubs and dwarf shrubs
age density (m)
(years) (no./ha) (% Cover ≥1%) (Total and dominant spp.)
Sprucea
S1, Konginkangas, Silt, 4.0 59 800 18 Sorbus aucuparia 2 Herbs 7
Iitsalo, Dwarf shrubs 30 Grasses 15
62 48′N 25 58′EVaccinium myrtillus 28 Deschampsia flexuosa 15
Mosses 41
Litter 49
S2, Konginkangas, Fine sand, 65 700 19 Dwarf shrubs 12 Herbs 8
Liimattala, Moraine, 4.3 V. myrtillus 11 Grasses 10
62°40′N 25°50 E D. flexuosa 10
Mosses 45
Litter 53
S3, Viitasaari, Fine sand, 63 900 19 – Herbs 1
Ilmolahti, Moraine, 4.2 Ferns 8
62°58′N 25°50′EMosses 43
Litter 59
Birch after spruceb
BS1, Konginkangas, Fine sand, 33 1,300 16 – Herbs 55
Liimattala, Moraine, 5.1 Melampyrum sylvaticum 20
62°40′N 25°50′EMaianthemum bifolium 12
Grasses 68
D. flexuosa 58
Mosses 0.3
Litter 50
BS2, Konginkangas, Fine sand, 28 1,100 13 – Herbs 51
Liimattala, Moraine, 4.9 Rubus saxatilis 17
62°40′N 25°50 E Solidago virgaurea 9
Grasses 65
Agrostis capillaris 42
Calamagrostis
arundinaceus 22
Mosses 0.3
Litter 50
BS3, Konginkangas, Silt, 5.3 33 1,000 13 – Herbs 38
Iitsalo, M. bifolium 9
62°48′N 25°58′EGrasses 29
C. arundinaceus 24
Mosses 1.1
Litter 82
3
Deciduousc
D1, Leivonmäki, Moder, thick organic 65 Birch 700 17 Shrubs 7 Herbs 47
Rutalahti, layer, little mixing, Picea abies 50 Rubus idaeus 7M. bifolium 13
61°58′N 25°59′E no burrowing Populus tremula 110 Viola palustris 13
earthworms, 4.6 Alnus incana 90 Ferns 21
Athyrium filix-femina 10
Litter 31
D2, Korpilahti, Mull, 90 Birch 700 24 Dwarf shrubs 13 Herbs 22
Oittila, Lumbricus terrestris P. tremula 18 V. myrtillus 13 Grasses 8
61°56′N 25°45′E present, 5.1 Alnus incana 11 Ferns 29
Matteuchia struthiopteris 27
Mosses 9
Litter 67
D3, Jyväskylä, Mull, well mixed, 75 Birch 500 25 Shrubs Herbs 50
Kuokkala, high populations of Pinus sylvestris 150 R. idaeus Oxalis acetosella 26
62°13′N 25°45′EL. terrestris, Grasses 17
Aporrectodea D. caespitosa 11
caliginosa, 5.5 Ferns 16
Equisetum sylvaticum 13
Mosses 37
Litter 53
D4, Muurame, Moder, organic layer, Populus tremula 600 18 –
Härkäpohja, no burrowing Alnus incana 500
62°04′N 25°42′E earthworms Birch 300
Picea abies 90
Birch after fieldd
BF1, Uurainen, Fine sand, 6.2 26 1,800 10 – Herbs 53
Oikari, Silene dioica 14
62°24′N 25°30′EGrasses 30
A. capillaris 28
Mosses 23
Litter 53
BF2, Viitasaari, Sandy moraine, 5.4 43 700 19 Acer platanoides 4 Herbs 50
Ilmolahti, Veronica chamaedrys 10
63°00′N 25°50′EGrasses 13
Deschampsia caespitosa 13
Mosses 1.6
Litter 40
BF3, Viitasaari, Fine sand, 33 1,000 15 Rubus idaeus 2 Herbs 55
Ilmolahti, moraine, 5.6 Filipendula ulmaria 8
62°58′N 25°50′ECirsium helenoides 7
Grasses 27
A. capillaris 11
Mosses 1.4
Litter 54
Fielde
F1, Uurainen, Fine sand, 5.9 – – – – –
Oikari,
62°24′N 25°30′E
F1, Konginkangas, Fine sand, 7.0 – – – – –
Liimattala,
62°40′N 25°50′E
F3, Viitasaari, Fine sand, 6.0 – – – – –
Ilmolahti,
62°58′N 25°50′E
a Spruce (Myrtillus type) stands were iron podsols with raw humus
b Spruce stands (Myrtillus type) were originally iron podsols with raw humus, clear-cut and mechanically mixed before reforestation
c Mixed deciduous forests including Betula pendula
d Fields were originally iron podsols, normally cultivated before reforestation
e Fields were in continuous cultivation (last crop cereals), originally iron podsols with raw humus
Table 1 Continued
Site Soil, pH Stand Stand Height Shrubs and dwarf shrubs
age density (m)
(years) (no./ha) (% Cover ≥1%) (Total and dominant spp.)
(BF). All the planted birch forests were about 30 years old. Six
secondary sites were chosen in the immediate vicinity of these
main sites. Three of these were spruce forests (S) and three were
arable fields (F). As well, three natural deciduous forest stands (D)
were also chosen in the area. In each case, the three sites were rep-
licates and were chosen to be fairly similar to each other, with the
exception of deciduous sites 3 and 4. Deciduous site 4 was sam-
pled in September 1997 and due to the extreme stoniness of this
soil, another site (3) was sampled in May 1998. Descriptions of
the sites are provided in Table 1.
The sites were sampled on 19 and 22 September 1997, and 21
and 22 May 1998.
Sampling
To ensure representative sampling of each stand, at each sampling
time, six cores (5.5 cm diameter×6 cm) were randomly taken from
a 20×20-m area in each stand using a cylindrical corer. Each core
was divided into 0–3 cm and 3–6 cm depths. The six cores at each
depth were pooled and sieved through 2 mm mesh. From this
pooled material, 2 g was used for fungal isolations and the rest was
used to determine pH, OM content, soil moisture and nutrients.
Fungal community
A washing technique (Parkinson 1994) was used to remove spores
and permit the isolation of fungi active as hyphae at the time of
sampling. Each 2 g sample was washed in 20 changes of water
(determined by preliminary experiment to be the optimum number
of washes to remove all spores) and sieved to obtain the 49- to
74-µm fraction. From each depth of each stand, 150 particles were
plated, one per plate, 100 of these on 2% malt extract agar
(MEA)+antibiotics (0.1% streptomycin+0.05% aureomycin) and
50 were plated on MEA+antibiotics (0.1% streptomycin+0.05%
aureomycin)+benomyl (5 ppm).
Fungi were identified to species where possible (i.e. sporula-
tion) and percent frequency of occurrence of each taxon in each
sample was calculated for both media. For MEA, frequency of oc-
currence of each taxon was calculated as number of times taxon A
was isolated from a sample/100 particles plated per sample×100.
4
Table 2 Mean % frequency of occurrence of most common fungal
taxa, total number of identified taxa and number of unidentified
taxa in different habitats in September 1997 and May 1998. Each
value is the mean of three sites and two layers (0–3 cm and
3–6 cm depths) (n=6). BS Birch after spruce, BF birch after field,
Dnatural deciduous, Sspruce, Ffield
Taxa S BS D BF F
1997 1998 1997 1998 1997 1998 1997 1998 1997 1998
Chrysosporium merdarium 1.3 0.0 2.2 0.5 1.8 0.8 0.8 0.5 0.0 0.0
(Link ex Grev.) Carm.
Chrysosporium pannorum 0.0 0.2 0.0 0.8 0.0 1.5 0.2 4.3 0.2 0.3
(Link) Hughes
Gymnoascus reessii Baran. 0.0 0.2 0.3 0.8 0.8 2.2 0.0 0.2 0.0 0.3
Mortierella humilis Linnem. 2.5 0.3 3.5 0.8 1.3 0.5 1.3 0.0 0.3 0.3
Mortierella isabellina Oudem. 3.7 18.5 3.0 13.5 2.8 2.7 0.0 4.7 0.2 0.7
Mortierella microspora var. 3.2 0.0 2.5 1.0 0.7 0.8 0.0 0.0 0.0 0.0
macrocystis (Gams) Linnem.
Mortierella nana Linnem. 7.2 0.7 13.0 1.7 4.0 0.0 0.3 0.3 0.3 0.2
Mortierella nr humilis 0.5 0.0 0.5 0.0 1.7 0.2 1.0 0.0 0.0 0.0
Mortierella parvispora Linnem. 3.2 1.2 9.3 4.0 6.2 7.3 4.3 2.0 0.8 2.2
Mortierella ramanniana (Möller) 1.2 8.3 4.3 4.2 0.0 0.5 0.0 2.0 0.0 0.0
Linnem.
Mortierella vinacea Dixon-Stewart 0.8 2.7 0.5 8.8 2.8 7.0 2.0 6.5 0.0 0.3
Mucor circinelloides van Tiegh. 1.7 0.0 0.5 0.0 0.8 0.0 0.3 0.0 0.2 0.0
f. circinelloides
Mucor hiemalis f. corticola 0.0 0.5 0.0 0.3 0.0 1.5 0.3 0.8 0.0 0.7
(Hagem) Schipper
Oidiodendron scytaloides 1.5 0.2 1.0 1.5 0.7 1.3 0.8 0.0 0.0 0.2
Gams and Söderström
Paecilomyces carneus 2.5 0.0 1.7 0.2 4.0 1.8 4.5 1.3 2.3 1.8
(Duché and Heim)
A.H.S. Brown and G. Sm.
Penicillium cf. variable Sopp 0.2 0.0 0.8 0.0 1.7 0.0 1.0 0.0 0.2 0.0
Penicillium montanense 0.7 0.2 2.0 0.2 1.2 0.2 1.3 0.0 0.2 0.0
Christensen and Backus
Penicillium olivicolor Pitt 0.2 0.0 1.0 0.0 0.8 0.0 1.3 0.0 0.0 0.0
Penicillium spinulosum Thom 1.5 2.8 5.3 0.5 3.8 0.3 2.7 1.2 0.2 0.2
Penicillium 159 0.3 0.0 1.8 0.3 2.0 0.0 0.3 0.2 0.0 0.0
Penicillium 423 0.0 0.7 0.0 1.2 0.0 1.0 0.0 1.3 0.0 0.0
Tolypocladium geodes W. Gams 0.0 0.5 0.0 1.3 0.0 0.7 0.0 1.2 0.0 0.0
Tolypocladium niveum 0.0 2.7 0.2 0.5 0.3 0.3 0.0 0.5 0.0 0.0
(Rostrup) Bissett
Trichoderma polysporum 1.8 3.2 0.3 1.0 1.0 1.2 0.5 2.2 0.0 0.3
(Link ex Pers.) Rifai
Trichosporiella 200 Kamyschko ex 0.0 0.2 0.0 1.8 0.0 2.0 0.0 1.2 0.0 2.5
W. Gams and Domsch
Basidiomycete 233 3.2 0.0 4.0 0.0 3.2 0.0 2.2 0.0 3.2 0.0
Total number of identified species 56 37 57 56 55 61 57 60 47 47
Total number of unknown taxa 28 3 21 6 13 8 22 5 21 13
For MEA+benomyl, frequency of occurrence of each taxon was
calculated as number of times taxon A was isolated from a sam-
ple/50 particles plated per sample×100. If a particular taxon was
isolated from both media, the higher frequency of occurrence was
used as being more representative of the frequency in the sample.
Fungal biomass
Fungal biomass was assessed only on the samples from May 1998
using the ergosterol method of Nylund and Wallander (1992).
Soil analyses
Moisture content, pH, OM content, and nutrient analyses [2 M
KCl-extractable NH4+, NO2–+NO3–(May 1998 only) and 2 M
KCl-extractable PO43+ (September 1997 only)] were performed on
each of the pooled samples using standard methods (standard SFS
3032 for N ions and Standard INSTA-VH 22 for PO43–).
Statistical analysis
Only those taxa which could be identified either to species or genus
were included in the fungal analysis (Table 2). Percent frequency
of occurrence data was used to calculate the Morisita-Horn quanti-
tative similarity index, species richness (S), the Berger-Parker in-
dex of dominance (d) and the inverse Simpson index of diversity
(1/D). Since there were large differences between the numbers of
isolates in each sample, rarefaction was employed to determine the
number of species in a sample size of ten (S10). The fungal commu-
nity parameters (S10, S, dand 1/D) were analysed using a three fac-
tor ANOVA followed by Tukey's test for paired comparisons.
The Morisita-Horn index of similarity has the advantages that
it is independent of sample size and number of species, and when
log-transformed is unaffected by the abundance of the most abun-
dant species (Wolda 1981). Therefore the percent frequency of oc-
currence data were transformed [ln(x+1)] prior to calculation of
the index. This index is 1.00 when the communities are identical
and 0.00 when the communities are completely different. Howev-
er, this theoretical maximum is not the value to which community
similarities ought to be compared, but rather the expected maxi-
mum under the null hypothesis that two samples are random sam-
ples from the same fungal flora (Wolda 1981), i.e. in this case, to
the within site type fungal similarities.
The fungal species data were analysed using principal compo-
nents analysis (PCA) followed by correlation of the extracted axes
with environmental variables [site types, top or bottom layers;
analysis of May and September data only), pH, OM, extractable
NH4+, extractable NO2–+NO3–(May 1998 only) and extractable
PO43+ (September 1997 only)]. Since the environmental constraints
were different in the two layers and the two dates sampled, the
PCA analysis was conducted on each layer and at each date sepa-
rately. In all cases the old deciduous sites (D sites) were considered
to be the “control” or the standard to which the other sites were
compared, and were used as the dummy variable in the ordinations.
The fungal biomass data were analysed using two-way AN-
OVA followed by Tukey's test for paired comparisons.
Results
Fungal community
With the exception of the F sites, fungal community sim-
ilarity was generally greater within site types than be-
tween site types (Tables 3, 4). The fungal community in
BS sites was more similar to the S sites than that in the
BF sites was to the F sites. The fungal community in the
BS sites was more similar to that in the D sites than was
that in the BF sites.
The lowest similarities were observed between the
fungal communities in the S and F sites. The highest
similarities observed were between the fungal communi-
ties in the S, BS and D sites. At both sampling times the
fungal communities in the F sites were more different
than the fungal communities in any of the other sites.
5
Table 3 Mean Morisita-Horn quantitative index of similarity
[ln(x+1)] between fungal communities in 0–3 cm and 3–6 cm
depths in different habitats in September 1997 (n=3aor n=10). For
abbreviations, see Table 2
SBSD BFF
September 1997, 0–3 cm depth
0.596 0.609 0.556 0.391 0.279 S
0.757 0.645 0.467 0.254 BS
0.653 0.528 0.331 D
0.492 0.369 BF
0.376 F
September 1997, 3–6 cm depth
0.605 0.641 0.645 0.388 0.284 S
0.642 0.599 0.348 0.286 BS
0.586 0.455 0.349 D
0.417 0.290 BF
0.337 F
a For data given in italics
Table 4 Mean Morisita-Horn quantitative index of similarity
[ln(x+1)] between fungal communities in 0–3 cm and 3–6 cm
depths in different habitats in May 1998 (n=3aor n=10). For ab-
breviations, see Table 2
SBSD BFF
May 1998, 0–3 cm depth
0.691 0.468 0.383 0.392 0.163 S
0.605 0.599 0.524 0.254 BS
0.646 0.569 0.261 D
0.509 0.209 BF
0.209 F
May 1998, 3–6 cm depth
0.590 0.572 0.419 0.467 0.147 S
0.624 0.486 0.500 0.215 BS
0.550 0.436 0.331 D
0.427 0.230 BF
0.283 F
a For data given in italics
Table 5 Mean Morisita-Horn quantitative index of similarity
[ln(x+1)] between fungal communities in the 0–3 cm and 3–6 cm
depths of each habitat in September 1997 and May 1998 (n=3).
For abbreviations, see Table 2
SBSDBFF
September 1997 0.500 0.682 0.697 0.537 0.413
May 1998 0.639 0.636 0.609 0.608 0.310
The fungal communities in the two layers were fairly
similar to each other in the S, BS, D and BF sites and
less similar in the F sites (Table 5).
The total number of species isolated from these sites
was 177. The total number of species in each site type
was: S, 80 species; BS, 92 species; D, 97 species; BF,
97 species; F, 81 species. Raw fungal species richness,
rarefied species richness, dominance and number of iso-
lates differed significantly between sites (Table 6). Mean
raw species richness in the F sites was significantly low-
er than that in the BS, BF, or D sites and was significant-
ly lower in the S sites than in the BS sites. Mean rarefied
species richness in the S sites was significantly lower
than that in the BF, D and F sites. Mean fungal domi-
nance in the S sites was higher than that in the BF and D
sites. On average, fewer fungi were isolated in the F sites
than in any of the other sites, and fewer fungi were iso-
lated in the BF sites than in the BS sites.
Fungal species
The most frequently isolated fungal taxa are listed in Ta-
ble 2. Mortierella spp. tended to be the dominant species
at both sampling times in the forested sites.
In the top layer, the first three PCA axes accounted
for 72% of the variation in the fungal species data. OM
(P<0.05) and the BS site (P<0.02) correlated with the
first PCA axis; the BS site (P<0.05) correlated positively
and NH4+content (P<0.001) correlated negatively with
the second PCA axis; and OM content (P<0.01) and the
BS (P<0.01) correlated positively and the S sites
(P<0.01) correlated negatively with the third PCA axis,
accounting for 41%, 19% and 13% of the variation in the
fungal species data, respectively (Fig. 1). Mortierella ra-
manniana, Mortierella isabellina, Mucor near pyrifor-
mis, Oidiodendron griseum, Oidiodendron periconioides,
Tolypocladium niveum, Gliocladium 448, Pythium 452,
Hyalodendron 124, Penicillium lividum and Penicillium
species 416 and 428, correlated positively and Paecilo-
myces carneus correlated negatively with OM content.
Mortierella parvispora, Mortierella nana, Mortierella
humilis, Mucor nr pyriformis, Penicillium 159, Penicilli-
um thomii, Penicillium spinulosum, Penicillium olivicol-
or, Penicillium montanense, Penicillium nr variabile,
Pseudoerotium zonatum, Paecilomyces 244, Chloridium
clavaeforme, Oidiodendron truncatum, Gilmaniella?,
and basidiomycete 233 were positively and Mortierella
vinacea, Pythium 452 and Penicillium species 425 and
428 were negatively correlated with NH4+content. Mor-
tierella ramanniana, Mortierella isabellina, Mucor nr
pyriformis, O. griseum, O. periconioides, Tolypocladium
niveum, Gliocladium 448, Pythium 452, Hyalodendron
124, Penicillium lividum and Penicillium species 416
and 428, correlated positively and Paecilomyces carneus
correlated negatively with the spruce sites. Penicillium
spinulosum, Penicillium thomii, Mortierella nana, Mu-
cor globosus, Chloridium clavaeforme, Trichoderma
longibrachiatum, O. truncatum, Gilmaniella? and Peni-
cillium 159 were associated with the BS site.
In the bottom layer, the BS site (P<0.05) correlated
positively and pH (P<0.05) correlated negatively with
the second PCA axis; and S sites (P<0.02) correlated
with the third PCA axis, accounting for 22% and 13% of
the variation in the fungal species data, respectively
(Fig. 2). Trichoderma 264 correlated positively and Pen-
icillium spinulosum, Penicillium melinii, Mortierella ra-
manniana, O. griseum and Humicola? 354 correlated
negatively with pH. Penicillium spinulosum, Penicillium
melinii, Mortierella ramanniana, O. griseum and Humi-
cola? 354 correlated positively and Trichoderma 264
correlated negatively with the BS sites. Penicillium spin-
6
Table 6 Mean (±SE) raw species richness (S), species richness af-
ter rarefaction (S10), inverse Simpson index of diversity (1/D) and
Berger-Parker index of dominance (d) of fungal communities in
0–3 cm and 3–6 cm depths in different habitats in September 1997
and May 1998 (n=3). For other abbreviations, see Table 2
Site Year SS
10 1/Dd
0–3 cm 3–6 cm 0–3 cm 3–6 cm 0–3 cm 3–6 cm 0–3 cm 3–6 cm
S 1997 24 (7) 17 (3) 8.1 (0.9) 7.0 (0.6) 24.4 (14.5) 9.9 (3.8) 0.14 (0.05) 0.28 (0.10)
1998 12 (3) 13 (4) 4.1 (0.5) 5.8 (1.3) 3.8 (0.9) 7.8 (5.4) 0.46 (0.06) 0.33 (0.16)
BS 1997 30 (1) 23 (5) 7.8 (0.7) 7.4 (0.9) 16.6 (6.6) 13.9 (6.5) 0.19 (0.08) 0.23 (0.07)
1998 26 (8) 16 (6) 7.2 (1.2) 6.4 (0.8) 12.9 (8.6) 7.2 (1.9) 0.26 (0.14) 0.35 (0.06)
D 1997 25 (4) 18 (3) 8.2 (0.8) 7.9 (0.9) 21.4 (3.5) 20.1 (9.5) 0.13 (0.02) 0.18 (0.06)
1998 23 (10) 18 (6) 7.6 (0.6) 7.3 (0.7) 16.7 (3.9) 12.7 (7.6) 0.19 (0.06) 0.25 (0.12)
BF 1997 19 (7) 17 (9) 8.2 (0.3) 7.2 (1.4) 22.9 (4.9) 18.2 (14.6) 0.14 (0.02) 0.19 (0.11)
1998 23 (1) 18 (6) 7.6 (0.7) 7.4 (1.1) 15.6 (7.8) 16.4 (11.0) 0.20 (0.07) 0.19 (0.06)
F 1997 11 (3) 13 (4) 8.0 (0.9) 7.7 (0.9) 22.7 (7.8) 17.0 (10.1) 0.18 (0.00) 0.25 (0.13)
1998 14 (2) 10 (5) 8.0 (0.1) 6.3 (1.1) 19.0 (1.7) 10.9 (3.8) 0.18 (0.03) 0.26 (0.04)
ANOVA factors
Site *** ** **
Layer ** * * *
Date *** ** ***
*P<0.05, **P<0.01, ***P<0.001
7
Fig. 1 Principal components
analysis (PCA) of fungal species
in the top (0–3 cm) soil layer in
September 1997 and May 1998.
BS Birch following spruce forest,
OM organic matter and spruce
forest, NH4 NH4+, b233 basidio-
mycete 233, chl Chloridium cla-
vaeforme, gc Gliocladium 448,
gi Gilmaniella?, h124 Hyaloden-
dron 124, mh Mortierella humilis,
mi Mortierella isabellina,
mn Mortierella nana, mp Mortier-
ella parvispora, mr Mortierella
ramanniana, mug Mucor globo-
sus, mup Mucor nr pyriformis,
mv Mortierella vinacea, og Oidio-
dendron griseum, op Oidioden-
dron periconioides, or Oidioden-
dron truncatum, p159 Penicillium
159, p416 Penicillium 416, p417
Penicillium 417, p418 Penicillium
418, p423 Penicillium 423, p428
Penicillium 428, pa244 Paecilo-
myces 244, pac Paecilomyces
carneus, pl Penicillium lividum,
pmo Penicillium montanense, po
Penicillium olivicolor, ps Penicil-
lium spinulosum, pt Penicillium
thomii, py452 Pythium 452, pz
Pseudeurotium zonatum, tl Tri-
choderma longibrachiatum, ton
Tolypocladium niveum, tp Tricho-
derma polysporum
Fig. 2 PCA of fungal species in
the lower (3–6 cm) soil layer in
September 1997 and May 1998.
PH pH, cm Chrysosporium mer-
darium, cv Chloridium virescens
var. chlamydosporum, c401
Chrysosporium 401, g266 Geo-
trichum 266; hu Humicola?,
mh Mortierella humilis and Mor-
tierella parvispora, mm Mortier-
ella microspora var. macrocys-
tis, mnh Mortierella nr humilis,
mp Mortierella parvispora and
Mortierella humilis, mr Mortier-
ella ramanniana, my Myc-
eliophthora 442, p425 Penicilli-
um 425, p344 Penicillium 344,
pme Penicillium melinii, py189
Pycnostysanus 189 and Mortier-
ella vinacea, t264 Trichoderma
264, tf Trichoderma fascicu-
latum,ton Tolypocladium ni-
veum and Penicillium 423; for
other abbreviations, see Fig. 1
ulosum, Penicillium 418, Mortierella ramanniana, Mor-
tierella isabellina, O. griseum and Myceliophthora 442
correlated positively and Trichoderma 264 correlated
negatively with the S sites.
In September 1997, the BS site (P<0.001) correlated
with the first PCA axis and PO43– content (P<0.02) and
the S site (P<0.02) correlated with the third PCA axis, ac-
counting for 50% and 7%, of the variation in the fungal
species data, respectively (Fig. 3). Basidiomycete 233,
Penicillium griseum, Penicillium thomii, Penicillium 159,
Mortierella isabellina, Mortierella ramanniana, Mucor
globosus, Oidiodendron tenuissimum, Trichoderma fasc-
iculatum and Trichoderma longibrachiatum were positive-
ly correlated with PO43– content. Verticillium fungicola
var. fungicola, O. griseum, Mortierella ramanniana, Mor-
tierella isabellina, Mortierella nana, Mortierella micro-
spora var. macrocystis, Mortierella humilis, Mortierella
parvispora, Mucor globosus, Penicillium spinulosum,
Penicillium 159, Paecilomyces carneus, Chloridium cla-
vaeforme and Chrysosporium merdarium were positively
and Acremonium 268 and Cladosporium cladosporioides
were negatively correlated with the BS site. Mortierella
microspora var. macrocystis, Penicillium janczewskii and
Phoma 283 were positively correlated with the spruce site.
In May 1998, OM content (P<0.01) and the BS site
(P<0.01) correlated with the first PCA axis and NH4+con-
tent (P<0.01) and the BS site (P<0.05) correlated with the
second PCA axis, accounting for 52% and 14% of the vari-
ation in the fungal species data, respectively (very similar
to the top layer; data not shown). Mortierella ramanniana,
Mortierella isabellina, Mucor nr pyriformis, Gliocladium
448, Tolypocladium niveum, O. griseum, Oidiodendron nr
maius and Penicillium spinulosum were positively and
Paecilomyces carneus, Acremonium butyri and Trichos-
poriella 200 were negatively correlated with the OM con-
tent. Phialophora nr lagerbergii, Penicillium 29, Tricho-
derma minutisporum, Chrysosporium merdarium, Mortier-
ella microspora var. macrocystis, Mortierella parvispora,
Mortierella nr humilis, Penicillium 420, Penicillium 423,
Oidiodendron scytaloides, Chloridium 454, Tolypocladium
geodes, Hyalodendron 124, Phialophora lagerbergii and
Idriella? 360 were positively and Mucor nr pyriformis was
negatively correlated with NH4+content. Penicillium mon-
tanense, Penicillium spp 417, 423 and 428, Pythium 452,
Hyalodendron 124, Phialophora lagerbergii, Chloridium
454, Mortierella vinacea, O. scytaloides and To-
lypocladium geodes were positively and Phialophora 238,
Dactylaria 453, Coniella 438, Cylindrocarpon magnusi-
anum were negatively correlated with the BS sites.
Fungal biomass
Fungal biomass as measured by ergosterol was signifi-
cantly (P<0.001) higher in the S sites than in all the oth-
er sites (Table 7).
8
Fig. 3 PCA of fungal species
in the 0- to 3-cm and 3- to
6-cm soil layers in September
1997. PO4 PO43–, a268 Acre-
monium 268, b301 basidiomy-
cete 301, cc Cladosporium cla-
dosporioides, chl Chloridium
clavaeforme and Mortierella
microspora var. macrocystis,
cv Chloridium virescens var.
chlamydosporum and Phoma
283, mh Mortierella humilis,
ot Oidiodendron tenuissimum,
pj Penicillium janczewskii, pro
Penicillium roseopurpureum;
for other abbreviations, see
Figs. 1 and 2
Discussion
Vegetational differences can affect the fungal community
in the litter and soil in several ways; directly through the
quality of the litter as a resource for the fungi, directly
through the quality of root exudates as fungal resources,
indirectly through the changes in soil chemical and phys-
ical properties; and indirectly through soil fauna such as
earthworms. Since the plant litter, roots, fungi and fauna
interact, it is difficult to separate these effects. However,
it is evident that there are associations between fungal
taxa and vegetation types (e.g. Christensen 1969), that
root exudates in the form of amino acids and sugars dif-
fer in amount and type between different plant species
(Dix and Webster 1995), that rhizosphere bacterial C
substrate use differs between plants (Grayston et al.
1998), that fungal species have different requirements
for and tolerances to OM, moisture and nutrient contents
and pH (e.g. Bååth and Arnebrandt 1993; Bissett and
Parkinson 1979; Christensen 1969; Shameemullah et
al.1971; Widden 1986a, 1986b), and that there are nega-
tive interactions between earthworms and fungi (McLean
and Parkinson 2000).
Vegetation exerts a strong control over soil develop-
ment (i.e. on structure, profile development and aggregate
stability) even over relatively short periods of time (with-
in 20 to 80 years) (Graham et al. 1995; Muys et al. 1992;
Wardenaar and Sevink 1992). Litter quality and quantity,
which depends on tree species, were the main factors de-
termining the type of humus formation in forest stands
grown on former meadow soil (Muys et al. 1992). High
C/N ratio litters produced moder humus formation while
low C/N ratio litters produced active mull humus in the
presence of anecic earthworms (Muys et al. 1992).
As well, the effects of previous vegetation and land
use on soil chemical properties can last many years. Ra-
diocarbon data and the ratios of phenolic acids probably
derived from lignin residues in a pasture soil in New
Zealand suggested that the former forest vegetation was
still traceable in the pasture subsoil after more than
100 years (Stout et al. 1976). Using variations in the nat-
ural abundance of 15N, Koerner et al. (1999) showed that
previous land use (i.e. arable field or garden) could be
detected even 100 years after afforestation. As well,
Compton and Boone (2000) found that forest floor C/N,
C/P and N/P ratios, forest floor C and mineral soil light
fraction C were consistently lower, and N and P contents
were higher in sites that had been cultivated >90 years
ago than in sites which had been forested >90 years ago.
They attributed this to the use of manures in nineteenth
century agriculture (Compton and Boone 2000).
Given the long-term changes in soil chemical proper-
ties due to vegetation or land use, it is not too surprising
that Christensen (1981) observed that a once forested
grassland contained dominant fungal species characteris-
tic of both forests and grassland.
In the present study, litter quality, the presence of
earthworms and soil properties (OM, NH4+, pH and
PO43–) appeared to be the main factors affecting differ-
ences in fungal community composition among various
site types. With the present data set it was not possible to
assess the importance of exudates from roots of differing
plant species.
Spruce vs. birch planted on spruce soil
Spruce forests in Finland are likely to contain at least the
epigeic species Dendrobaena octaedra, although Lum-
bricus rubellus and Dendrodrilus rubidus may also be
present (Terhivuo 1988). The addition of a higher quality
litter (birch: C/N ratio of 33, Howard and Howard 1974)
to soil containing the residues of spruce needle litter
(spruce: C/N ratio of 83; Taylor et al. 1989), might be
expected to increase resource quality for the soil biota.
This improvement in resource quality was probably one
of the main reasons that the BS sites contained anecic
and endogeic earthworms such as Lumbricus terrestris
and Aporrectodea caliginosa as well as epigeics such as
L. rubellus and D. rubidus and large numbers of D. octa-
edra (M. Raty and V. Huhta, in preparation). Consump-
tion of litter by endogeic and anecic earthworms, which
are capable of incorporating large amounts of OM each
year (e.g. Bohlen et al. 1999), is reflected in the lower
OM and moisture content and higher NH4+-N and pH in
the BS sites.
The changes in earthworm fauna and soil chemical
properties were accompanied by decreased fungal bio-
mass (as ergosterol) and increased raw fungal species
richness. Otherwise, the fungal communities in the BS
and S sites were quite similar to each other relative to the
other sites in the study (0.539 and 0.607 in the 0- to 3-
cm and 3- to 6-cm layers, respectively) and decomposi-
tion potential (M. A. McLean and V. Huhta, in prepara-
tion) did not differ between these two site types. These
results indicate that the BS sites have retained much of
the fungal community and microbial activity of the S
sites. That the fungal communities in the lower layer in
the BS and S sites were more similar to each other than
those in the top layer suggests that it takes longer than
30 years for the birch litter fungal community to replace
9
Table 7 Mean (SE) ergosterol content (µg g–1 dry weight) of soil
samples at 0–3 cm and 3–6 cm depths in different habitats in May
1998 (n=3). For abbreviations, see Table 2
Site 0–3 cm 3–6 cm
S 74.49 (21.03) 11.64 (11.66)
BS 12.69 (6.07) 1.73 (1.28)
D 24.40 (27.47) 1.74 (1.08)
BF 6.86 (4.39) 0.93 (0.81)
F 0.30 (0.43) 0.56 (0.42)
ANOVA factors
Site ***
Layer ***
*P<0.05, **P<0.01, ***P<0.001
the spruce litter fungal community in the profile. In
boreal Picea glauca forests in Canada mean residence
time for OM in the organic layers varied from 16 to
35 years (Prescott et al. 1989). Since OM in the mineral
soil is much more recalcitrant, the effect of spruce in
these BS soils at lower depths could last decades longer.
Higher extractable NH4+levels in the BS sites than in
the S sites were important for fungal species abundances,
especially in the top layer and in May 1998. Penicillium
spinulosum, several other species of Penicillium, several
species of Mortierella and Oidiodendron and 15 other
species were correlated either positively or negatively
with NH4+-N in the present study. Arnebrandt et al.
(1990) observed that Penicillium spinulosum and Oidio-
dendron echinulatum were isolated more frequently and
Penicillium brevi-compactum, Mortierella sp, Oidioden-
dron griseum were isolated less frequently in NH4NO3-
amended pine forest plots relative to control plots. There
is an abundance of other studies indicating that the oc-
currence of fungal species can be related to the presence
or amount of NH4+or NO3–(e.g. Park 1976; Widden
1986a). As well, some species of Mucorales and basidio-
mycetes are unable to use NO3–(Dix and Webster 1995).
Since the presence of NH4+represses nitrate reductase,
NH4+will be used preferentially when NH4NO3is pro-
vided (Griffen 1994).
Five fungal species (Penicillium thomii, Penicillium
159, Mortierella nana, Mucor globosus, Chloridium cla-
vaeforme) were correlated with extractable PO43– and the
BS sites in September, and were correlated with NH4+-N
and the BS sites in May, suggesting that P was limiting
in September and N was limiting in May. That pH was
an important factor affecting the fungal community in
the bottom layer probably reflects the persistence of low-
er-pH spruce residues and their associated fungal com-
munity in the lower layer. And indeed, several species of
Penicillium, Mortierella and Oidiodendron which corre-
lated negatively with pH in the present study were char-
acterized by Christensen (1981) as typical of forests and
heaths.
Field vs. birch planted on field soil
In comparison with the fungal communities in the F
sites, those in the BF sites were characterized by higher
numbers of fungal isolates and raw species richness and
reduced decompositional abilities. As well, similarity be-
tween the fungal communities in these two site types
was low (0.289 and 0.260 in the 0- to 3-and 3- to 6-cm
layers, respectively). However, the ordination did not
distinguish between the fungal communities of the BF
and F sites, nor did it distinguish between the fungal
communities of the BF and F sites and those of the D
sites.
The use of the Morisita-Horn similarity index and
PCA showed two perspectives on the fungal communi-
ties of the F and BF sites. The Morisita-Horn index is a
quantitative index which includes the abundance of all
species in the community. PCA tends to emphasize the
importance of total abundance rather than relative spe-
cies abundance (ter Braak 1987–1992). This suggests
that the fungal communities in the F sites comprised dif-
ferent species than those in the other site types and that
the overall abundance of the fungi in the F sites was sim-
ilar to that of the BF and D sites.
What accounts for these differences? Two factors
which may account for these differences between the BF
and F sites are differences in earthworm community and
changes in litter quality.
The earthworm fauna of the BF sites included large
numbers (331±85 m–2) of A. caliginosa and a few L. ter-
restris (31±32 m–2) and epigeic species (28±31 m–2) (M.
Raty and V. Huhta, in preparation). There is abundant ev-
idence that cultivation of arable soils decreases popula-
tions and changes the composition of earthworm commu-
nities (e.g. Edwards and Bohlen 1996), so it is likely that
earthworm numbers were higher in the BF sites than the
F sites. Aside from the indirect effects of earthworms
on the fungal community through their effects on soil
physical and chemical properties (e.g. McLean and
Parkinson 2000), earthworms may also have direct effects
on the fungal community through differential viability of
fungal spores during earthworm gut passage (e.g. Moody
et al. 1996). Changes in the earthworm community due to
improved litter quality in the BF sites relative to the F
sites may account for some portion of the differences ob-
served in the fungal communities of these two site types.
Birch leaf litter has a much lower C/N ratio (33;
Howard and Howard 1974) than cereal straw (approxi-
mately 120; Lynch 1985) and this alone may account for
the differences observed between the fungal communi-
ties in BF and F sites. Cereal straw contains 75–80% cel-
lulose and hemicellulose and 14% lignin (Harper and
Lynch 1981). Leaves and grass contain much lower pro-
portions of lignocellulose and higher proportions of wa-
ter-soluble components (Lynch 1985). Given the varying
abilities of fungi to utilize lignin, cellulose and other
plant constituents (Domsch et al. 1993; Dix and Webster
1995), one might expect different communities of fungi
on birch leaf litter and cereal straw.
Birch planted on spruce soil vs. birch planted
on field soil
The BS and BF sites retained two soil characteristics and
one fungal community characteristic of their original site
types; pH and total numbers of earthworms were lower
and number of fungal isolates was higher in the BS than
the BF sites. However, other measures indicated how
significantly afforestation with birch had altered the soil
and the fungal communities of the original site types.
The mean similarity between the fungal communities in
the S and F sites was 0.221 and 0.216, and that in field
sites afforested with birch was 0.496 and 0.424 in the 0-
to 3-cm and 3- to 6-cm layers, respectively. Also, while
the S sites had significantly lower rarefied species rich-
10
ness and decomposition potential than the F sites, there
were no differences in species richness or decomposition
potential (M. A. McLean and V. Huhta, in preparation)
between the BF and BS sites.
Although the microbial communities in the sites
afforested with birch were more similar than the micro-
bial communities in the original site types, they were
still 50–60% dissimilar and that they were separated by
PCA suggests that not only was the fungal species com-
position different, but overall fungal abundance was dif-
ferent. Several interacting factors probably contributed
to these continuing differences between the microbial
communities in the BS and BF sites: the quality of OM
residues in the soil, pH and differences in earthworm
community composition.
Spruce litter decomposes more slowly than grasses or
deciduous leaf litter (Taylor et al. 1991) and persists in
the organic layers for many years (Prescott et al. 1989).
Polyphenols, commonly found in coniferous leaf litter
may reduce plant litter quality for some members of the
fungal community through the formation of resistant
complexes with proteins or by direct inhibition of fungal
activity (Swift et al. 1979). The ability of fungi to over-
come these compounds varies widely and may partially
account for the existence of a typical “forest/heath” fun-
gal flora as in Christensen's (1981) study.
Lower pH and quality of litter residues may account
for the differences in the earthworm communities in
these two sites which in turn affected the fungal commu-
nity. In the BS sites where there were 4 times as many
epigeic earthworms, one would expect more comminu-
tion and less incorporation and mixing of OM into the
mineral soil as opposed to in the BF sites where there
were 50 times more endogeic earthworms [BS,
110±75 m–2 and 6±7 m–2; BF, 28±31 m–2 and
331±85 m–2 for epigeics and endogeics, respectively (M.
Raty and V. Huhta, in preparation)]. Since even commi-
nution of OM due to epigeic earthworm activity can sig-
nificantly alter the fungal community, favouring fast-
growing species and reducing fungal diversity, species
richness and the abundance of Zygomycete species
(McLean and Parkinson 2000), it is likely that the more
thorough incorporation of OM into mineral soil accom-
plished by endogeic earthworm species would also sig-
nificantly affect the fungal community.
Birch planted on spruce soil and birch planted
on field soil vs. old deciduous soil
Although the fungal communities in the D, BS and BF
sites were fairly similar, relative to other comparisons in
this study, they were still 35–60% dissimilar. This may
reflect the time necessary for deciduous litter to decay
and move down the profile or the presence of ferns
(15–30% cover) only in the D sites. The fungal commu-
nities in the upper layers of both the BS and BF sites
were more similar to those of the D sites than the lower
layers, reflecting the persistence of OM residues (and
fungal communities) in the lower layers from the previ-
ous land use even after 30 years. The presence of ferns in
the D sites may account for some portion of the differ-
ences observed in the fungal communities in these site
types. Fern leaf litter decomposed faster in the D sites
than in either the BS or BF sites (M. A. McLean and V.
Huhta, in preparation), indicating the presence of a fun-
gal (microbial) community capable of degrading this
rather recalcitrant litter in the D sites. Fern decay differs
from that of angiosperm litter and resembles that of
wood in that lignin decomposers invade early in the suc-
cession, soft rots are present and decay is slow (Dix and
Webster 1995; Frankland 1966, 1969).
In conclusion, the fungal communities of former
spruce and arable soil afforested with birch about
30 years ago were more similar to those of old deciduous
forests and to each other than the fungal communities of
the original site types. The similarities were more pro-
nounced in the 0- to 3-cm layer than in the 3- to 6-cm
layer. These changes were attributed primarily to in-
creased litter quality and increased earthworm abun-
dance, and secondarily to changes in OM, pH, NH4+and
PO43–.
Acknowledgement The study was supported by the Finnish
Academy of Sciences. We wish to thank the Soil Ecology group of
the Department of Biological and Environmental Sciences, Uni-
versity of Jyväskylä, especially Mika Raty for sharing his prelimi-
nary physical, chemical and earthworm data and for doing the
ANOVAs, Piippa Wali-Blomquist for help with the earthworms,
and Mustapha Boucelham and Leena Kontiola for valuable techni-
cal assistance.
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