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Applied Soil Ecology 12 (1999) 113±128

Effects of climate change on soil factors and metazoan microfauna
(nematodes, tardigrades and rotifers) in a Swedish tundra soil ±
a soil transplantation experiment
BjoÈrn Sohleniusa,*, Sven BostroÈmb
a

Department of Invertebrate Zoology, Swedish Museum of Natural History, Box 50007, SE-104 05, Stockholm, Sweden
b
Zoo-tax, Swedish Museum of Natural History, Box 50007, SE-104 05, Stockholm, Sweden
Received 10 September 1998; received in revised form 11 December 1998; accepted 15 December 1998

Abstract
In order to study the effects of climate changes on soil organisms and processes, a transplantation experiment was undertaken.
Eighteen soil blocks from an ombrotrophic mire (Stordalenmyren) at Abisko in northern Sweden were transplanted to nine
sites in Sweden, from UmeaÊ in the north to Alnarp in the south. The study was part of the EC-project DEGREE (Diversity
effects in grassland ecosystems of Europe). The development of populations of nematodes, tardigrades and rotifers was
followed in a monthly sampling programme. Microbial biomass and inorganic nitrogen were determined by other partners in
the project. Some effects could be related to climatic conditions at the transplantation sites and the most clear in¯uence was
found at open sites with great ¯uctuations in temperature and moisture. The parameters most clearly in¯uenced were amount of

mineralized nitrogen, numbers of bacterial feeding nematodes belonging to the Rhabditida, and numbers of tardigrades. These
components had a fairly large coef®cient of variation (CV ˆ 0.9±1.2). Microbial biomass as indicated by the CFE and Ergosterol
methods varied less (CV ˆ 0.3). The Shannon index, Evenness and Maturity index varied very little (CV ˆ 0.1). In most changing
parameters the effect was most clearly seen during the autumn. The ¯uctuations of microorganisms, nematodes, tardigrades and
inorganic nitrogen could indicate a food web interaction. # 1999 Elsevier Science B.V. All rights reserved.
Keywords: Climate change; Soil factors; Metazoan microfauna; Nematodes; Tundra soil; Transplantation experiment

1. Introduction
Expected changes in climate due to increased
amounts of greenhouse-gases are likely to in¯uence
animal and plant communities especially strongly in
polar areas. Although changes in the soil system will
primarily be caused by changes in vegetation and
primary production, there are also direct climatic

*Corresponding author. Tel.: +46-08-519 54230; fax: +46-08519 54125; e-mail: bjorn.sohlenius@nrm.se

effects on soil organisms (Whitford, 1992). In tundra
soils, signi®cant quantities of nutrients are bound in
the peat because of low temperatures and permafrost.

An increase in temperature is therefore expected to
have dramatic in¯uences on soil organisms and mineralization processes (Billings and Peterson, 1992).
To study the effects of climate change on metazoan
microfauna (nematodes, rotifers and tardigrades),
microorganisms and mineralization, a soil transplantation experiment was undertaken. Soil blocks were
taken from a tundra soil at Abisko, northern Sweden
and transferred to nine warmer places in the country.

0929-1393/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved.
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114

B. Sohlenius, S. BostroÈm / Applied Soil Ecology 12 (1999) 113±128

The changes in soil life induced by such transplantation may be of different kinds. Responses of soil
animals to transplantation of soil cores to warmer
places have been described by Briones et al. (1997).
Changes of substrate properties, vegetation and liberation of bound nutrients may, apart from the direct
in¯uences of moisture and temperature, in¯uence

performance of various species of soil organisms
differently. This can be expected to in¯uence food
webs, competitive ability etc., resulting in changes in
microfaunal structure, microbial biomass, and amount
of mineralized carbon and nitrogen (Clarholm et al.,
1981; Ingham et al., 1985; Coleman and Crossley,
1996).
It is well known from various laboratory experiments that microbial feeding nematodes can in¯uence
microbial biomass and rate of mineralization (Ingham
et al., 1985). When blocks of tundra soil are transferred to warmer places, this should result in an
increased rate of mineralization re¯ected by the
increased numbers of certain groups of nematodes
and accumulation of inorganic nutrients. The bacterial
feeding nematodes have been shown to re¯ect C and N
mineralization rates (Mikola and SetaÈlaÈ, 1998). Little
is known about the rates of these changes and how the
temperature and moisture will in¯uence them.
In this paper the overall effects of climate change on
microfauna, microbial biomass and nitrogen mineralization will be analysed. Increased rates of mineralization were anticipated, especially at warmer sites.
It was expected that such changes should stimulate

nematodes such as Rhabditida which require a rapid
microbial production.
The study is included in the EC-project Diversity
effects in grassland ecosystems of Europe (DEGREE).
Analysis of data from all participants is found in
Ekschmitt et al. (in press).

2. Materials and methods
2.1. Transplantation experiment
On the 3±4 June 1996, 18 blocks of peat were taken
from the Stordalen mire in the north and transplanted
on 5±12 June to nine sites along temperature and
moisture gradients in Sweden (Fig. 1). The blocks,
measuring 55 cm  35 cm  22 cm, were placed in

Fig. 1. Map of the transplantation sites in Sweden. Abbreviations:
AB ± Abisko, AL ± Alnarp, JC ± JaÈdraaÊs clearing, JF ± JaÈdraaÊs
forest, LA ± Lanna, SC ± Skogaby clearing, SF ± Skogaby forest,
TO ± Torslunda, UL ± Ultuna, UM ± UmeaÊ.

plastic boxes. In the bottom of each box 24 holes
(diameter 8 mm) were drilled for drainage and a net
(mesh size 1 mm) covered the bottom to prevent larger
animals and roots from entering the box from below.
The boxes were dug into the soil so that the rim of the
box and the surface of the peat was level with the
surrounding soil. The sensor of an electronic min/
max-thermometer was placed at a depth of 5 cm in
order to register soil temperature. On each sampling
occasion maximum and minimum temperatures were
recorded.
2.2. The Abisko site
The Stordalen mire at Abisko (AB ± Site 15) is
described in Sonesson (1980). It was the ®eld site of
the Swedish contribution to the tundra investigations

B. Sohlenius, S. BostroÈm / Applied Soil Ecology 12 (1999) 113±128

in the International Biological Program (IBP). Now it
is a nature reserve used for ecological studies.

The site is situated at Stordalen in the eastern part of
the TornetraÈsk area, 10 km east of Abisko and 70 km
from the sea. Some details of the site are given in
Table 1. It is about 1 km from and 10 m above Lake
TornetraÈsk, which has an area of 322 km2. The original research area is a 25 ha treeless, mainly oligotrophic mire. The mire is typical of the peatlands in the
eastern continental parts of northern Fennoscandia
with respect to the occurrence of permafrost and
the composition of the plant cover. The annual mean
temperature is about ÿ1.08C, the warmest month
being July, the coldest February, with monthly mean
temperatures of 11.58C and ÿ11.78C, respectively.
The main surface soil of the mire is peat to a depth
of 3 m overlaying silt and/or sand. Granite boulders or
bedrock are also present locally. The peat is acid, pH
(H2O) about 4.0, and very poor in available nutrients.
More detailed descriptions of the site can be found in
Rosswall et al. (1975) and Sohlenius et al. (1997).

115

Ultuna (UL ± Site 2) is an open grassland area close
to the Meteorological Station of SLU at Ultuna,
Uppsala.
Lanna (LAA/LAB - Sites 8 and 9) is an open
agricultural area at the Agricultural Field Station of
SLU, Lanna-Saleby.
Torslunda (TOA/TOB - Sites 3 and 4) is situated on
È land in the Baltic Sea. The site is an open
the island O
grassland area at the Agricultural Experimental Station Torslunda, SLU.
Skogaby, is an area in south Sweden with stands of
Norway spruce (Picea abies (L.) Karst) of various
ages used for i.a. studies on the effects of climate and
air pollution on spruce forest growth and vitality. The
site is thoroughly described by Bergholm et al. (1995).
Skogaby forest (SFA/SFB ± Sites 13 and 14) is a
mature Norway spruce forest in block II of the Skogaby site. Skogaby clearing (SC ± Site 10) is a
deforested open area in block IV of the Skogaby site.
Alnarp (AL ± Site 7) is an open grassland area at the
Agricultural Experimental Station LoÈnnstorp of SLU

at Alnarp.

2.3. Transplantation sites
2.4. Sampling, extraction and counting
The blocks were transplanted from Abisko to the
sites shown in Fig. 1. Two blocks were placed at each
site. The position and climatic conditions at the sites
are indicated in Table 1. The sites were numbered 1±
14 to be coordinated with ®eld experiments carried out
by the other partners in the EC-project. The numbering does not correspond to the north±south distribution
of the sites followed in this paper. In the general layout
of the EC project parallel values from the two blocks
of some treatments were for statistical reasons handled
as separate sets of data and these were marked A and B.
UmeaÊ (UMA/UMB ± Sites 11 and 12) is an open
grassland area in North Sweden at the Swedish University of Agricultural Sciences (SLU), RoÈbaÈcksdalen.
JaÈdraaÊs, IvantjaÈrnsheden, is an area in Central Sweden with stands of Scots pine (Pinus sylvestris L.) of
various ages. The site was used by the Swedish
Coniferous Forest Project (SWECON) and is thoroughly described by Axelsson and BraÊkenhielm
(1980). JaÈdraaÊs forest (JFA/JFB - Sites 5 and 6) is a

35±40 year old stand of Scots pine (IhII according to
SWECON). JaÈdraaÊs clearing (JC - Site 1) is a clearcut
rather open area with regrowth of pine trees about 2±
3 m high (Ih0 in the terminology of SWECON).

The transplanted blocks were sampled between
Days 2 and 11 of each month from July to December
1996. A ®nal sampling was carried out in June 1997.
On each sampling 6 (3 ‡ 3) cores (diameter 2.3 cm)
were taken from the blocks at the sites JC (1), UL (2),
SC (10) and AL (7). At the replicated sites UM (11/
12), JF (5/6), LA (8/9), TO (3/4) and SF (13/14) four
cores were taken from each block at each sampling.
The cores were put into plastic tubes, sealed and kept
cold (8±108C) for transport to the laboratory. UM was
not possible to sample in December since the soil was
frozen hard.
The cores were prepared for extraction on the
second day after sampling. From each core a subsample of peat (3±8 gfw) was extracted for microfauna by a wet funnel method (Sohlenius, 1979) and
the % soil moisture content of the peat was determined.

From each site and replicate, peat samples were
sealed in plastic bags and shipped in cooling containers to the Department of Animal Ecology, Justus
Liebig University, Giessen, Germany for determination of microbial biomass (mg C gdwÿ1; chloroform,

116

Geographic position and climatic conditions of Stordalen and the transplantation sites in Sweden
Site

Position
Latitude

Annual values
Longitude Altitude
(m.a.s.l)

Values for the study period June-Dec 1996

Long term 30 years
Precipitation Air

(mm)

temperature

1996/1997

Soil temperature

Precipitation

Air

Soil

Period

Period

(mm)

temperature

temperature

08C

(8C)

(8C)

(days)

(days)

(8C)

Mean 8C

Max 8C

Precipitation
before
sampling

Water contents
Mean %

Min %

(mm/day)

Abisko (Stordalen) AB

688220 N

198030 E

351

300

ÿ0.7

±

±

±

±

±

±

±

±

UmeaÊ (UM)

638480 N

208130 E

10

650

2.7

609

3.4

±

142

223

8.5

23.2

1.61

83.4

81.3

JaÈdraaÊs forest (JF)

608490 N

168300 E

185

570

3.8

673

3.6

4.8

147

218

8.2

18

2.51

84.0

82.1

JaÈdraaÊs clearing (JC)

608490 N

168300 E

185

570

±

673

±

±

±

±

8.6

20

2.51

84.7

82.4

Ultuna (UL)

598490 N

178390 E

12

530

5.5

456

6

6.4

98

267

11.2

22.7

1.61

77.5

70.2

Lanna (LA)

588210 N

138080 E

72

560

6.1

532

5.2

7.4

102

263

11.4

26.4

1.66

80.9

76.7

Torslunda (TO)

568380 N

168300 E

41

475

7.4

540

6.3

9.3

82

283

12.3

22.5

2.02

80.8

77.8

Skogaby forest (SF)

568330 N

138130 E

115

1100

±

±

8.9

17.1

2.23

82.6

80.1

Skogaby clearing (SC)

568330 N

138130 E

115

Alnarp (AL)

558390 N

138070 E

10

±

±

1242

1100

7.5

1242

7.1

655

7.9

535

6.7

±

±

±

±

50

315

10.9

23.6

2.23

79.7

74.3

67

298

12.0

22.5

1.90

81.6

77.8

B. Sohlenius, S. BostroÈm / Applied Soil Ecology 12 (1999) 113±128

Table 1

B. Sohlenius, S. BostroÈm / Applied Soil Ecology 12 (1999) 113±128

fumigation and extraction procedure, CFE-method;
Vance et al., 1987) and fungal biomass (mg gdwÿ1;
Ergosterol method; Djajakirana et al., 1996), and to
the Department of Ecology, Aristotle University,
Thessaloniki, Greece for determination of inorganic
nitrogen (mg N gdwÿ1; Allen, 1974). Plant biomass
(gdw mÿ2) was estimated at the December 1996 sampling. Samples from each site and replicate were
shipped to Germany in June 1997 for estimates of
respiration (mg C gdwÿ1 hÿ1; alkali trap and titration
method; Isermeyer, 1952).
All the animals from each subsample were ®xed in
TAF (triethanolamine and formalin) and counted in
dishes under low magni®cation (40). After counting,
the suspensions from three or four (replicated sites)
extractions were combined for subsequent analysis of
faunal structure. The pooled suspensions were analyzed under higher magni®cation (125±200) and in
each suspension about 150±250 randomly selected
nematodes were identi®ed. The number of examined
animals was about 10±50% of the extracted number.
In Table 2 and Figs. 2±4, the values for A and B are
given separately. In all other cases the parallel series
are treated as one unit. The microbiological and
chemical parameters were analysed only in the samples taken during July±December 1996.
2.5. Classification of fauna into S/F-groups
The nematode fauna was classi®ed into semitaxonomic feeding groups (S/F-groups) according to Sohlenius (1996) with the food sources for particular taxa
taken from Yeates et al. (1993). The S/F-groups are
indicated in Table 5. They include Tylenchida feeding
on root-hairs (RH), Tylenchida (including Aphelenchida) feeding on fungal hyphae (HY); bacterial feeders
(BF) belonging to Secernentea (Rhabditida) or Adenophorea (Teratocephalida, Araeolaimida and Monhysterida); omnivorous Dorylaimida feeding on algae
etc. (OM); Dorylaimida feeding on fungal hyphae
(HY).
2.6. Analysis of faunal structure and relationships
between parameters
Diversity of the nematode community within each
treatment was calculated with the Shannon±Wiener
information function (H0 ) (Shannon and Weaver,

117

1949) and using the evenness factor (J0 ) (Pielou,
1966). The maturity index (MI), which considers
life-history patterns and growth rate (Bongers,
1990), was calculated as a means to indicate the
degree of disturbance. To compare the variability of
different parameters the coef®cient of variation CV
(standard deviation/mean value) of all the samplings
from all the stations was calculated. Relationships
between different parameters studied in the
DEGREE-project have been analysed by multiple
linear regression and reported by Ekschmitt et al.
(in press). Some details of possible causal relations
and covariations in the present material were tested
with linear regression analysis.

3. Results
3.1. Temperature and moisture at the different
transplantation sites
Mean and maximum values of soil temperature
measurements, and mean and minimum water contents from the blocks are indicated in Table 1 together
with measurements of soil temperatures and daily
mean precipitation for the period before sampling
obtained from the weather stations.
The variation of soil temperature and soil water
contents between different sites was large during the
summer. These factors did not vary with the latitude but
rather with local climate at the sites (Fig. 2). Thus, at
forest localities (JF and SF) the mean soil temperatures
were lower and the soil water contents often higher than
those at more open localities. It was not until November and December that the temperatures clearly varied
with latitude. Water content was higher during autumn
with little relation to latitude or type of locality.
The temperature ¯uctuations were much larger at
open than at closed sites. This is indicated by the
maximum soil temperatures with the highest registered temperature of 26.48C at LA at the September
sampling (Table 1). The largest variations in water
contents between the sites were found during August
and September 1996 and in June 1997 (Fig. 2). The
driest conditions occurred at UL, LA and SC. In
August 1996 and June 1997 the warmer sites (UL,
LA, SC, TO and AL) were clearly drier than the colder
ones (UM, JC, JF and SF).

118

Table 2
Values of some important components in the transplantation experiment

UMA
UMB
JFA
JFB
JC
UL
LAA
LAB
TOA
TOB
SFA
SFB
SC
AL

Block
number

11
12
5
6
1
2
8
9
3
4
13
14
10
7

Microbial biomass
CFE
(mgC)

Ergosterol
(mg)

64.2
45.3
43.8
29.9
27.0
33.0
44.0
64.5
34.2
37.9
33.4
30.9
30.9
48.6

80
74
88
116
111
110
87
171
111
83
117
89
165
90

Inorganic
nitrogen
(mg)

Nematoda
total
(No)

Bacterial
feeders
(No.)

Rhabditida
(No.)

Tylenchida
(No.)

Tardigrada
(No.)

Plant biomass
Dec 96
(gdw mÿ2)

Respiration
June 97
(mg CO2 hÿ1)

0.52
1.02
0.34
0.60
0.58
0.26
1.22
0.51
0.29
0.36
0.29
0.61
0.15
0.61

185
198
664
579
516
756
588
896
735
598
747
812
548
912

145
185
591
458
440
585
530
822
597
567
690
709
473
752

0.5
11.2
17.5
26.3
8.2
98.3
106
105
22.2
7.3
60.1
9.7
26.2
33.7

7.0
10.5
47.8
97.0
39.6
274
43.2
217
177
47.2
72.9
66.6
102
128

26.6
19.4
166
170
127
99.4
176
44.4
104
44.4
170
86.2
43.2
51.8

n.d.
n.d.
674
515
804
440
465
575
452
291
313
517
549
414

5.8
6.1
10.5
10.5
5.0
n.d.
8.1
5.4
10.0
n.d.
7.4
9.5
4.2
6.6

Except for the last two columns the figures show mean values for the period October±December 1996. All the figures except plant biomass are given as gdwÿ1 of soil material.
Bold figures show the largest values for each component.
For abbreviations of sites see Fig. 1.

B. Sohlenius, S. BostroÈm / Applied Soil Ecology 12 (1999) 113±128

Site

B. Sohlenius, S. BostroÈm / Applied Soil Ecology 12 (1999) 113±128

119

Fig. 2. Mean soil temperatures (curves: 8C) during the period prior to each sampling and soil water contents (bars: %) at the time of sampling
for the transplantation sites. The sites are arranged in order from north (UM) to south (AL). Double dots in the temperature curves indicate the
sites where values from each block (A and B) are given. The December value for water contents from UM is taken to be the same as the
November value. The sites repeated each month are from left to right: UMA, UMB, JFA, JFB, JC, UL, LAA, LAB, TOA, TOB, SFA, SFB, SC
and AL. For abbreviations and geographic position see Fig. 1.

3.2. Plant biomass, soil respiration, microbial
biomass and inorganic nitrogen
Plant biomass and soil respiration were measured
only once, i.e., plant biomass in December 1996 and
respiration in June 1997 (Table 2). There were no
clear differences in these values between the sites that
could be related to treatment. The fungal and bacterial
biomasses were measured on most sampling occasions
during 1996. The variation in the CFE-estimates of
microbial biomass was generally not large (Tables 2
and 4, Fig. 3), except in October when the variations
in CFE were larger with higher values in UM (64.9 mg
C gdwÿ1), LA (92.1 mg C gdwÿ1) and AL (74.5 mg
C gdwÿ1).
Fungal biomass (Ergosterol) varied less
(CV ˆ 0.26) than total microbial biomass (CFE)
(CV ˆ 0.33). There were tendencies for peak
values in September±December at the different sites

with the highest value in November at LA
(179 mg gdwÿ1).
The amounts of inorganic nitrogen varied greatly
(CV ˆ 0.89) with time and block (Tables 2 and 4,
Fig. 3). The highest amount of inorganic nitrogen
occurred in most blocks towards the end of 1996
and generally with peaks in November. The most
pronounced increase occurred at LA, with the peak
amount in November (1.5 mg N gdwÿ1). There was a
signi®cant negative correlation between temperature
and inorganic nitrogen (r ˆ ÿ0.41, p < 0.01) and a
positive correlation between nitrogen and moisture
(r ˆ 0.36, p < 0.01), when data from June 1996 to
December 1996 were analysed.
3.3. Nematodes, tardigrades and rotifers
The variation in numbers of nematodes from all
samplings was moderate (CV ˆ 0.55) (Tables 2 and 4;

120

B. Sohlenius, S. BostroÈm / Applied Soil Ecology 12 (1999) 113±128

Fig. 3. Microbial biomass CFE (bars: mg C gdwÿ1) and amount of inorganic nitrogen (curves: mg N gdwÿ1) of the soil at the transplantation
sites. The sites are arranged as in Fig. 2. Note that there are no values from UM in December as the soil was frozen.

Figs. 4 and 5(a)). In Table 2 and Fig. 4 the A and B
blocks are kept separate at the sites UM, JF, LA, TO,
and SF, whereas the data in Fig. 5(a) are mean values
from each transplantation site. The highest value was
found at TO in June 1997 (1070 nematodes gdwÿ1)
and
the
second
highest
number
(1040
nematodes gdwÿ1) at AL in November 1996. The
patterns of variation at the different sites were rather
similar with the exception of UM, where the numbers
remained rather constant. After low nematode numbers in July and August in most blocks, the densities
increased with the highest numbers in November or
December 1996, or at the warmer sites in June 1997
(Figs. 4 and 5(a)).
A comparison of all data (July 1996±June 1997) for
total nematode numbers and temperature showed a
signi®cant negative correlation (r ˆ ÿ0.39, p < 0.01).
This was mainly due to lower nematode numbers
during the summer. The number of nematodes generally increased during the autumn, noticeably more
rapidly at warm than at cold sites. In November there

was a signi®cant positive relationship between temperature and numbers of nematodes (r ˆ 0.83,
p < 0.01). After the winter there was a clear difference
in abundance of nematodes between warm and cold
sites with much higher abundances at warm sites in
June 1997 (Fig. 5(a)).
There were no simple relationships between moisture and numbers of nematodes. At the sites that had
been drier during August and September, the nematode numbers tended to be higher later in the autumn
than those from sites that were wetter during the
summer.
There was no correlation between total nematode
numbers and inorganic nitrogen, although the amplitude of variation in both parameters increased with
time and peak values of nematodes and inorganic
nitrogen were obtained during late autumn, especially
in November (Figs. 3 and 4).
Numbers of tardigrades varied considerably
(CV ˆ 0.94) (Table 2, Fig. 5(b)). Similar to nematodes, there was a tendency for numbers to increase

B. Sohlenius, S. BostroÈm / Applied Soil Ecology 12 (1999) 113±128

121

Fig. 4. Abundance of nematodes (bars: No gdwÿ1) and mean soil temperatures (curves: 8C) at the transplantation sites. Double dots and
arrangement of sites as in Fig. 2. The nematode abundance for UM in December is estimated as the mean abundance of November 1996 and
June 1997.

towards the end of 1996. However, it was not until
June 1997 that a dramatic increase in tardigrade
abundance occurred (Fig. 5(b)), with a maximum
abundance of 63 specimens gdwÿ1 being obtained
at TO on that date. There was a signi®cant positive
correlation between tardigrade and nematode numbers
(r ˆ 0.55, p < 0.01).
The numbers of rotifers (CV ˆ 0.69) varied quite
differently to those of tardigrades and nematodes and
there were no correlations between abundance of
rotifers and the other two animal groups (Fig. 5(c)).
There was a tendency for decreasing abundance of
rotifers with time with the highest abundances at most
samplings being found at cold and wet sites. The
densities of rotifers were rather similar to those of
tardigrades, i.e., a mean value of 24 specimens gdwÿ1
and a maximum value of 92 specimens gdwÿ1 at JC in
December.

3.4. Composition of the nematode fauna
Thirty-®ve nematode taxa were identi®ed in the
study. Table 3c shows a somewhat condensed presentation of the mean abundances of different taxa based
on all the samplings compared with the initial values
from Abisko in June 1996. Plectus and Teratocephalus
were the most abundant genera in the fauna. The most
abundant genera among the Tylenchida were Malenchus and Aphelenchoides. Among the Rhabditida,
Rhabditis s.l. and Acrobeloides sometimes increased
markedly in numbers. Eudorylaimus was the dominating genus in the Dorylaimida.
The most abundant group at all samplings was
Adenophorea BF (56±80% of nematode numbers)
(Table 4). Thus, bacterial feeders (Rhabditida
BF ‡ Adenophorea BF) were the largest feeding
group in all treatments (Table 4). Tylenchida HY,

122

B. Sohlenius, S. BostroÈm / Applied Soil Ecology 12 (1999) 113±128

Fig. 5. Fluctuations in abundance (No gdwÿ1) of (a) nematodes, (b) tardigrades and (c) rotifers at the transplantation sites. The three most
northern sites are indicated by open symbols. For abbreviations of sites see Fig. 1.

feeding on fungal hyphae, contributed only 1.5±10%
of the fauna, and all Tylenchida contributed 9±29% of
the fauna. Rhabditida BF (CV ˆ 1.20) and Tylenchida
HY responded to the different treatments and
increased especially at open and warm sites such as
UL and LA. Adenophorea BF (CV ˆ 0.56) also
increased most pronouncedly at warm sites, but there
were no large differences between the various sites.
Tylenchida (CV ˆ 0.86) did not increase much at the
three coldest sites but further south, from UL to AL,
they increased considerably. There was a positive
correlation between Tylenchida and Rhabditida
(r ˆ 0.57, p < 0.01).

There were no clear correlations between numbers
of hyphal feeders and fungal biomass (Ergosterol), or
between total nematode numbers or numbers of any
speci®c feeding group of nematodes and microbial
biomass (CFE).
The bacterial feeders increased proportionally more
than the fungal feeders, which almost retained their
initial abundance, at the colder sites. This led to a very
low proportion of fungal feeders at these sites. The
highest proportion of fungal feeders were found at UL
and LA, but there were still about seven times more
bacterial than fungal feeding nematodes (Table 4).
The ratio of fungal feeding to bacterial feeding nema-

123

B. Sohlenius, S. BostroÈm / Applied Soil Ecology 12 (1999) 113±128
Table 3
Mean abundance of nematode taxa from all samplings (July 1996±June 1997) in the transplanted blocks and June 1996 at AB
Taxa

Site
AB

Tylenchida RH (root-hair feeders)
Filenchus spp.
Malenchus sp.
Lelenchus sp.
Tylenchus sp.
Tylenchinae sp.
Tylenchidae sp.

UM

JF

JC

UL

LA

TO

SF

SC

AL

11
6.8
0
1.9
0
0

2.0
4.1
0.1
4.6
0.4
0.7

8.2
26
0.2
4.3
1.6
0.6

3.9
17
0
0.2
1.3
0.7

21
109
1.1
1.1
3.9
1.2

13
23
2.0
1.1
2.1
0.6

8.4
30
0.3
1.5
1.3
1.5

7.6
35
0.3
1.5
2.2
0.3

7.7
42
0.2
0
4.1
0.1

4.6
53
0.2
1.8
2.9
0.6

Tylenchida HY (hyphal feeders)
Ditylenchus sp.
Aphelenchoides sp.

0.6
4.7

0
2.5

0.3
8.3

0.1
9.1

0
63

0.2
57

0
36

0.1
25

0.1
35

0
24

Rhabditida BF (bacterial feeders)
Acrobeloides sp.
Panagrolaimus spp.
Rhabditis s.l. sp.
Diplogaster sp.
Bunonema spp.

1.7
1.3
0
0
0.9

0.7
2.1
1.1
0
0.5

0.3
1.2
9.1
0
1.4

1.5
1.5
2.7
0
0.4

50
7.4
1.5
0
1.1

26
1.7
34
0
0.7

3.7
5.3
7.8
0.7
2.7

4.1
7.7
12
0
2.0

12
0.6
2.3
0
0.3

12
4.1
6.7
0.8
1.2

Adenophorea BF (bacterial feeders)
Teratocephalus costatus
Teratocephalus spp.
Metateratocephalus sp.
Plectus tenuis
P. longicaudatus
Plectus spp.
Chronogaster sp.
Rhabdolaimus sp.
Wilsonema sp.
Eumonhystera sp.
Prismatolaimus dolichurus

0
69
1.8
1.6
10.8
7.1
0.3
0
0.3
2.7
12

1.6
36
2.9
0.1
36
24
0
0.1
0.1
7.3
23

5.0
126
7.4
0.8
78
63
0.3
0
0
14
41

3.1
119
3.6
0.1
60
41
0.3
0.2
0
6.0
43

8.8
181
4.3
0
70
72
0
0.4
0
17
29

2.2
105
2.0
0.1
103
113
0.3
0.4
1.9
6.9
29

7.5
81
5.2
0.3
170
84
0.2
0.4
0.1
26
30

6.9
185
2.7
0.2
104
95
0.5
0
0
20
44

1.3
123
4.2
0.4
92
63
0
0
1.8
8.2
21

14.5
143
8.1
0
181
126
0
0
0.3
17
38

Dorylaimida OM (omnivores)
Eudorylaimus spp.

17

13

39

41

42

34

41

53

37

82

Dorylaimida HY (hyphal feeders)
Tylencholaimus mirabilis
Nematoda total numbers

0.5
152

0

0

0

0

0

0

0

0

0

162

435

357

684

558

546

609

457

721

Figures show number of nematodes gdwÿ1 soil material.
For abbreviation of sites see Fig. 1.

todes obviously did not re¯ect the fungal/bacterial
biomass ratio. There was a weak positive correlation
between inorganic nitrogen and rhabditid nematodes
(r ˆ 0.28, p < 0.05).
3.5. Diversity, evenness and maturity index
In order to see if there were any connections
between processes and diversity the changes in Shan-

non index, Evenness and MI were compared with
nitrogen mineralization (amount of inorganic nitrogen) and microbial production as measured by numbers of microbial feeding nematodes. Mean values of
the indices are given in Table 4. There were only small
changes in the three indices throughout the experiment
(CV ˆ 0.06±0.1). Evenness had a tendency for lower
values towards the end of the experiment and MI
tended to be lower at UL, LA and TO, i.e. places

124

B. Sohlenius, S. BostroÈm / Applied Soil Ecology 12 (1999) 113±128

Table 4
Total nematode numbers (gdwÿ1), relative contribution (%) to total numbers by semitaxonomic feeding groups of nematodes (for
abbreviations see Table 3), fungal biomass (Ergosterol method), total microbial biomass (CFE-method), and some indices of the nematode
fauna
AB

UM

JF

JC

UL

LA

TO

SF

SC

AL

Total nematode numbers
Tylenchida RH%
Tylenchida HY%
Dorylaimida HY%
Rhabditida BF%
Adenophorea BF%
Dorylaimida OM%

152
12.9
3.5
0.3
2.6
69.3
11.4

162
7.3
1.5
0.0
2.7
80.3
8.1

435
9.4
2.0
0.0
2.7
77.0
8.9

357
6.5
2.6
0.0
1.7
77.6
11.6

684
20.1
9.2
0.0
8.8
55.8
6.1

558
7.4
10.3
0.0
11.1
65.1
6.1

546
7.9
6.6
0.0
3.7
74.2
7.6

609
7.8
4.2
0.0
4.2
75.2
8.6

457
11.8
7.7
0.0
3.4
68.9
8.2

721
8.7
3.3
0.0
3.4
73.2
11.3

Fungal biomass (Ergosterol) mg
Microbial biomass (CFE) mg C
Inorganic nitrogen mg N
Maturity index (MI)
Evenness
Shannon index
Fungal f/Bact f (F/B)

±
±
±
2.50
0.67
1.98
1/21

96.4
43.6
0.41
2.51
0.80
1.72
1/54

114
38.9
0.36
2.56
0.71
1.69
1/41

96.9
34.3
0.36
2.64
0.67
1.69
1/31

114
31.6
0.20
2.41
0.73
1.88
1/7.1

118
44.3
0.64
2.33
0.73
1.72
1/7.4

102
39.5
0.30
2.39
0.66
1.62
1/12

110
38.7
0.30
2.54
0.77
1.67
1/19

126
31.9
0.10
2.50
0.79
1.80
1/9.4

89.6
40.7
0.37
2.50
0.65
1.67
1/23

Figures are based on all samplings (July 1996±June 1997) for nematodes; June±December 1996 for microorganisms and nitrogen.
For abbreviations of sites see Fig. 1.

where a great increase of Rhabditida BF occurred.
There were signi®cant negative correlations between
MI and total numbers of nematodes and between
Evenness and total number of nematodes (r ˆ ÿ0.3,
p < 0.01 for both).
3.6. Trends in development of microorganisms,
nematodes, tardigrades and inorganic nitrogen
over time
The microbial biomass, numbers of nematodes and
tardigrades, and amounts of inorganic nitrogen
showed some relationships in their patterns of changes
over time (Fig. 6(a, b)). Thus, microbial biomass on
average, reached a peak in October. Nematode and
inorganic nitrogen peaks generally occurred 1 month
later (in November) whereas tardigrades increased
still later. This pattern of variation was particularly
marked in LA (Fig. 6(a)).

4. Discussion
Fig. 6. Fluctuations of total microbial biomass (CFE), inorganic
nitrogen (NH4 ‡ NO3), rhabditid nematodes, and tardigrades at (a)
Lanna and (b) mean values of all the transplantation sites. The
graphi curves show percentages of mean values from all samplings.

4.1. Fluctuations in various components
Multiple linear regression analysis yielded no correlations among nematodes, microbial parameters and

B. Sohlenius, S. BostroÈm / Applied Soil Ecology 12 (1999) 113±128

nitrogen pools (Ekschmitt et al., in press). The failure
of this analysis to reveal causal relationships that may
have existed is almost certainly due to the great spatial
and temporal variation in the parameters sometimes
coupled with pronounced time lags. Thus, for instance
conditions that promoted nematode growth or nitrogen
mineralization were probably not re¯ected in the data
until some months later.
Some of the components investigated such as
amounts of inorganic nitrogen and abundance of
rhabditid nematodes ¯uctuated strongly, while components such as microbial biomass did not vary much.
Especially at cold sites and warm and exposed sites an
effect of climatic conditions appears to be clear.
The ¯uctuations of system components were strongest at the open sites UL and LA, which was unexpected since they were not the warmest places. Both
TO and AL have higher annual mean temperatures. It
is probable that this strong reaction at UL and LA is
due to the fact that they are exposed and inland
localities with the largest ¯uctuations in temperature
and water contents.
The highest soil temperature (26.48C) was found at
LA and the lowest relative water content (70%) was
found at UL; LA and UL also had the lowest precipitation. The warmest sites, TO and AL, were
situated at places with a more maritime climate and
thus not exposed to large climatic ¯uctuations. TO and
AL had higher precipitation during the investigated
year than UL and LA.
Large quantities of nutrients were immobilized in
the peat due to the wet and cold conditions prevailing
at the mire. Periods of drying and temperature ¯uctuations may have been of great importance for liberation
of these nutrients in the transplanted soil blocks. It has
been demonstrated that periods of drought followed by
heavy rains will greatly promote bacterial production,
bacterial feeding protozoans and nematodes, and rate
of mineralization (Clarholm et al., 1981; SchnuÈrer
et al., 1986).
4.2. Food web relations
One aim of the present investigation was to look for
connections between abundance and composition of
the nematode fauna and soil processes. The results
from some of the sites indicated such connections. At
LA especially the variation in microbial biomass,

125

nematode numbers and amount of inorganic nitrogen
indicated that nematodes were part of the processes
and that their changes in abundance were of indicative
importance (Fig. 6(a)).
The variation of some major components in the
system may indicate a food web interaction with
certain time lags. When the soil blocks were transferred to warmer sites this probably liberated carbon
sources leading to a period of immobilization followed
by a period of net mineralization seen as increased
numbers of nematodes prior to an increased amount of
inorganic nitrogen.
Although there were tendencies for peaks of microbial biomass to occur in October, the microbial biomass did not increase with temperature, moisture,
nematode numbers or amount of mineralized nitrogen.
The largest effect on inorganic nitrogen, microbial
biomass and nematodes was seen at LA and it is
interesting to observe a time lag with a peak of
microbial biomass in October followed by a peak of
inorganic nitrogen in November (Fig. 6(a)). This may
indicate that part of this nitrogen was liberated from
microbial cells perhaps partly due to nematode consumption of bacteria. Similar kinds of successional
changes explainable as food web interactions were
observed in an earlier study with laboratory incubated
humus material (Clarholm et al., 1981) and are also in
line with results from other investigations (Wardle
et al., 1995; Coleman and Crossley, 1996).
Sohlenius (1990) suggested that the nematodes
increased their rate of bacterial consumption in
response to bacterial production in such a way that
they kept the microbial biomass rather constant. The
effect of the increased bacterial production was then
seen as increased numbers of nematodes and increased
amounts of mineralized nitrogen. In the present study,
the peaks of inorganic nitrogen coincided with or
followed the peaks of nematode abundance (Fig. 6(a,
b)). Similar kinds of patterns were observed in the
study by Clarholm et al. (1981). However, the fact that
in UM the increase in nematodes was small while the
microbial biomass was constant and the inorganic
nitrogen increased runs counter to the suggestion of
a nematode effect. It could also indicate that nematodes had little in¯uence on microbial biomass and
mineralization processes in this case.
The food web hypothesis could be elaborated still
further when tardigrades, many of which are consid-

126

B. Sohlenius, S. BostroÈm / Applied Soil Ecology 12 (1999) 113±128

ered as nematode predators (Hallas and Yeates, 1972;
HyvoÈnen and Persson, 1996), are included in the
analyses. The present observation of increases in
tardigrades, often after the nematode peaks, can be
interpreted as a food web interaction. In this context it
is worth considering that there was a positive correlation between nematodes and tardigrades.

biomass. The proportion of fungal to bacterial feeding
nematodes was extremely low especially at UM, JF
and JC. This is in line with observations on dominance
of bacterial feeding nematodes in polar areas (Kuzmin, 1992).

4.3. Connections between climate and fluctuations of
components

Some of the data differed greatly between the two
soil blocks from the same site. This was almost
certainly an effect of the heterogeneity of the blocks.
Thus, small variations in the beginning may have
largely in¯uenced the outcome of the changes. This
was demonstrated by Sohlenius (1993) with nematodes in an incubation experiment using humus material which showed that the changes in composition of
the nematode fauna were of rather low predictability.
In transplantation experiments, especially with small
soil blocks or cores, the transplantation as such may
induce a disturbance in¯uencing the results. The
changes observed in this experiment were rather slow
and the structure of the blocks were little altered since
the material was interwoven with roots and humus
material. Therefore, it seems as if the transplantation
itself induced little disturbance on organisms and
processes. Also the vegetation remained almost
unchanged throughout the experiment. Obviously a
much longer time is needed before any substantial
changes may occur.
The irregularities in the data make their interpretation dif®cult. The patterns of change are not very clear
and there occur irregularities which may be both due
to the random variation and variations due to sampling
problems. In spite of this there seem to be some
patterns in the results justifying the outlined interpretation of the typical reaction of the system.
Another problem concerned the actual interpretation of the results. Were the observed changes a
climate effect on soil organisms or an indirect effect
via changes of substrate and primary producers? The
main weakness of this study was that its duration was
too short. Previous studies on effects of clear cutting
show that it takes several years until the soil system
stabilizes itself into another faunal structure (Sohlenius, 1996, 1997). Interpretations of the results were
made more dif®cult as changes in abundance and
composition of the nematode fauna were slower than
expected.

Sites with an open structure at the warmer locations
had a tendency for more rapid changes in composition
of the nematode fauna and more rapid increases in
total nematode numbers. Population increases in rhabditids (Acrobeloides and Rhabditis s.l.) and tylenchids
especially were found at these sites. Increases in
Rhabditis s.l. numbers seem to be connected with
high bacterial production and increased rates of mineralization often including accumulation of inorganic
nitrogen. The present ®nding of a positive correlation
between rhabditid nematodes and inorganic nitrogen
adds support to the observations by Sohlenius (1973)
and BaÊaÊth et al. (1978). It has been suggested that
these nematodes promote mineralization by consuming bacteria (Ingham et al., 1985), but it has also been
observed that nitrogen application promotes rhabditid
nematodes (BaÊaÊth et al., 1978).
The ¯uctuation patterns of nematodes with
increases during the autumn are in line with observations in coniferous forest soils (Sohlenius, 1979).
Temperature effects are re¯ected in the tendency for
more rapid increases at warmer sites as indicated by
the positive correlation between nematode abundance
and temperature in November. It was interesting to
notice that some of the colder sites (JC and JF) had
pronounced decreases in nematode numbers after the
winter whereas the sites UL and southward retained
levels similar to those before the winter. The results
also indicate that members of the Rhabditida and the
Tylenchida were sensitive to cold conditions and did
not increase at the colder sites in spite of high microbial biomass and high rates of nitrogen mineralization.
The proportions of fungal to bacterial feeding
nematodes have been suggested to mirror fungal
and bacterial production. This investigation, however,
indicates that fungal feeders were hampered by cold
conditions at the northern sites despite the high fungal

4.4. Reliability of results

B. Sohlenius, S. BostroÈm / Applied Soil Ecology 12 (1999) 113±128

Acknowledgements
The study was supported by a grant from the
European Commission to the project Diversity Effects
in Grassland Ecosystems of Europe (ENV4-CT950029). The partners in the project are thanked for
fruitful cooperation and we are especially grateful to
the German and Greek colleagues, who carried out the
analyses of microbial and fungal biomass, and inorganic nitrogen. Many people have assisted us in
various ways whilst we performed the transplantation
experiment and they are all gratefully acknowledged.
We would especially like to thank the following
Ê ke Andersson, Abisko naturvetenskapeople: Nils-A
pliga station; Sven Hellqvist, SLU RoÈbaÈcksdalen;
Bertil Andersson and Elisabeth Henningsson, JaÈdraaÊs
foÈrsoÈkspark; Arne Gustavsson, Stig Karlsson and Per
Nyman, SLU Ultuna; Johan Roland, SLU LannaSaleby; Ulf Johansson, ToÈnnersjoÈhedens foÈrsoÈkspark;
Lennart Henriksson, SLU Alnarp; and Torsten Kellander, Torslunda foÈrsoÈksstation. Anders Bignert is
thanked for making the map.
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