Effects of climate change on soil factors and metazoan microfauna
(nematodes, tardigrades and rotifers) in a Swedish tundra soil ±
a soil transplantation experiment
BjoÈrn Sohlenius
a,*, Sven BostroÈm
baDepartment of Invertebrate Zoology, Swedish Museum of Natural History, Box 50007, SE-104 05, Stockholm, Sweden bZoo-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 (CV0.9±1.2). Microbial biomass as indicated by the CFE and Ergosterol
methods varied less (CV0.3). The Shannon index, Evenness and Maturity index varied very little (CV0.1). 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
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 miner-alization processes (Billings and Peterson, 1992).
To study the effects of climate change on metazoan microfauna (nematodes, rotifers and tardigrades), microorganisms and mineralization, a soil transplan-tation experiment was undertaken. Soil blocks were taken from a tundra soil at Abisko, northern Sweden and transferred to nine warmer places in the country. *Corresponding author. Tel.: 519 54230; fax:
+46-08-519 54125; e-mail: bjorn.sohlenius@nrm.se
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 experi-ments that microbial feeding nematodes can in¯uence microbial biomass and rate of mineralization (Ingham et al., 1985). When blocks of tundra soil are trans-ferred 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 alization will be analysed. Increased rates of miner-alization 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 cm35 cm22 cm, were placed in
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
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 origi-nal research area is a 25 ha treeless, mainly oligo-trophic 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 andÿ11.78C, 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).
2.3. Transplantation sites
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 number-ing 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 Uni-versity of Agricultural Sciences (SLU), RoÈbaÈcksdalen. JaÈdraaÊs, IvantjaÈrnsheden, is an area in Central Swe-den with stands of Scots pine (Pinus sylvestrisL.) of various ages. The site was used by the Swedish Coniferous Forest Project (SWECON) and is thor-oughly 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).
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 the island OÈ land in the Baltic Sea. The site is an open grassland area at the Agricultural Experimental Sta-tion 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 Sko-gaby site. SkoSko-gaby 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.
2.4. Sampling, extraction and counting
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 (33) 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 sub-sample of peat (3±8 gfw) was extracted for micro-fauna by a wet funnel method (Sohlenius, 1979) and the % soil moisture content of the peat was deter-mined.
From each site and replicate, peat samples were sealed in plastic bags and shipped in cooling contain-ers to the Department of Animal Ecology, Justus Liebig University, Giessen, Germany for determina-tion of microbial biomass (mg C gdwÿ1
Table 1
Geographic position and climatic conditions of Stordalen and the transplantation sites in Sweden
Site Position Annual values Values for the study period June-Dec 1996
Long term 30 years 1996/1997 Latitude Longitude Altitude
(m.a.s.l)
Precipitation (mm)
Air temperature (8C)
Precipitation (mm)
Air temperature (8C)
Soil temperature (8C)
Period <08C (days)
Period >08C (days)
Soil temperature Precipitation before sampling (mm/day)
Water contents
Mean8C Max8C Mean % Min %
Abisko (Stordalen) AB 688220N 19
8030E 351 300 ÿ0.7 ± ± ± ± ± ± ± ± ± ±
UmeaÊ (UM) 638480N 20
8130E 10 650 2.7 609 3.4 ± 142 223 8.5 23.2 1.61 83.4 81.3
JaÈdraaÊs forest (JF) 608490N 16
8300E 185 570 3.8 673 3.6 4.8 147 218 8.2 18 2.51 84.0 82.1
JaÈdraaÊs clearing (JC) 608490N 168300E 185 570 ± 673 ± ± ± ± 8.6 20 2.51 84.7 82.4
Ultuna (UL) 598490N 178390E 12 530 5.5 456 6 6.4 98 267 11.2 22.7 1.61 77.5 70.2
Lanna (LA) 588210N 138080E 72 560 6.1 532 5.2 7.4 102 263 11.4 26.4 1.66 80.9 76.7
Torslunda (TO) 568380N 168300E 41 475 7.4 540 6.3 9.3 82 283 12.3 22.5 2.02 80.8 77.8
Skogaby forest (SF) 568330N 138130E 115 1100 ± 1242 ± ± ± ± 8.9 17.1 2.23 82.6 80.1
Skogaby clearing (SC) 568330N 138130E 115 1100 7.5 1242 7.1 50 315 10.9 23.6 2.23 79.7 74.3
Alnarp (AL) 558390N 13
8070E 10 655 7.9 535 6.7 ± 67 298 12.0 22.5 1.90 81.6 77.8
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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 sam-pling. 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 ana-lyzed 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 sam-ples taken during July±December 1996.
2.5. Classification of fauna into S/F-groups
The nematode fauna was classi®ed into semitaxo-nomic feeding groups (S/F-groups) according to Soh-lenius (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 Aphelench-ida) feeding on fungal hyphae (HY); bacterial feeders (BF) belonging to Secernentea (Rhabditida) or Ade-nophorea (Teratocephalida, Araeolaimida and Mon-hysterida); 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,
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 con-tents 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 Novem-ber and DecemNovem-ber that the temperatures clearly varied with latitude. Water content was higher during autumn with little relation to latitude or type of locality.
Table 2
Values of some important components in the transplantation experiment
Site Block number
Microbial biomass 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 CO2h
ÿ1)
CFE (mgC)
Ergosterol (mg)
UMA 11 64.2 80 0.52 185 145 0.5 7.0 26.6 n.d. 5.8
UMB 12 45.3 74 1.02 198 185 11.2 10.5 19.4 n.d. 6.1
JFA 5 43.8 88 0.34 664 591 17.5 47.8 166 674 10.5
JFB 6 29.9 116 0.60 579 458 26.3 97.0 170 515 10.5
JC 1 27.0 111 0.58 516 440 8.2 39.6 127 804 5.0
UL 2 33.0 110 0.26 756 585 98.3 274 99.4 440 n.d.
LAA 8 44.0 87 1.22 588 530 106 43.2 176 465 8.1
LAB 9 64.5 171 0.51 896 822 105 217 44.4 575 5.4
TOA 3 34.2 111 0.29 735 597 22.2 177 104 452 10.0
TOB 4 37.9 83 0.36 598 567 7.3 47.2 44.4 291 n.d.
SFA 13 33.4 117 0.29 747 690 60.1 72.9 170 313 7.4
SFB 14 30.9 89 0.61 812 709 9.7 66.6 86.2 517 9.5
SC 10 30.9 165 0.15 548 473 26.2 102 43.2 549 4.2
AL 7 48.6 90 0.61 912 752 33.7 128 51.8 414 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 gdwÿ1of soil material.
Bold figures show the largest values for each component. For abbreviations of sites see Fig. 1.
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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 (CV0.26) than total microbial biomass (CFE) (CV0.33). There were tendencies for peak values in September±December at the different sites
with the highest value in November at LA (179mg gdwÿ1).
The amounts of inorganic nitrogen varied greatly (CV0.89) 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 ÿ0.41, p< 0.01) and a positive correlation between nitrogen and moisture (r0.36, p< 0.01), when data from June 1996 to December 1996 were analysed.
3.3. Nematodes, tardigrades and rotifers
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 num-bers 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 ÿ0.39,p< 0.01). This was mainly due to lower nematode numbers during the summer. The number of nematodes gen-erally increased during the autumn, noticeably more rapidly at warm than at cold sites. In November there
was a signi®cant positive relationship between tem-perature and numbers of nematodes (r0.83,
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 moist-ure and numbers of nematodes. At the sites that had been drier during August and September, the nema-tode 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 ampli-tude 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 (CV0.94) (Table 2, Fig. 5(b)). Similar to nema-todes, there was a tendency for numbers to increase Fig. 3. Microbial biomass CFE (bars: mg C gdwÿ1) and amount of inorganic nitrogen (curves:
mg N gdwÿ1) of the soil at the transplantation
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 (r0.55,p< 0.01).
The numbers of rotifers (CV0.69) 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 presen-tation of the mean abundances of different taxa based on all the samplings compared with the initial values from Abisko in June 1996.PlectusandTeratocephalus
were the most abundant genera in the fauna. The most abundant genera among the Tylenchida were
Mal-enchusand Aphelenchoides. Among the Rhabditida,
Rhabditiss.l. and Acrobeloides sometimes increased
markedly in numbers.Eudorylaimuswas the dominat-ing 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 BFAdenophorea BF) were the largest feeding group in all treatments (Table 4). Tylenchida HY, Fig. 4. Abundance of nematodes (bars: No gdwÿ1) and mean soil temperatures (curves:
feeding on fungal hyphae, contributed only 1.5±10% of the fauna, and all Tylenchida contributed 9±29% of the fauna. Rhabditida BF (CV1.20) and Tylenchida HY responded to the different treatments and increased especially at open and warm sites such as UL and LA. Adenophorea BF (CV0.56) also increased most pronouncedly at warm sites, but there were no large differences between the various sites. Tylenchida (CV0.86) 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 (r0.57,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-Fig. 5. Fluctuations in abundance (No gdwÿ1) of (a) nematodes, (b) tardigrades and (c) rotifers at the transplantation sites. The three most
todes obviously did not re¯ect the fungal/bacterial biomass ratio. There was a weak positive correlation between inorganic nitrogen and rhabditid nematodes (r0.28,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 nitro-gen) and microbial production as measured by num-bers 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 (CV0.06±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 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 UM JF JC UL LA TO SF SC AL
Tylenchida RH (root-hair feeders)
Filenchus spp. 11 2.0 8.2 3.9 21 13 8.4 7.6 7.7 4.6
Malenchus sp. 6.8 4.1 26 17 109 23 30 35 42 53
Lelenchus sp. 0 0.1 0.2 0 1.1 2.0 0.3 0.3 0.2 0.2
Tylenchus sp. 1.9 4.6 4.3 0.2 1.1 1.1 1.5 1.5 0 1.8
Tylenchinae sp. 0 0.4 1.6 1.3 3.9 2.1 1.3 2.2 4.1 2.9
Tylenchidae sp. 0 0.7 0.6 0.7 1.2 0.6 1.5 0.3 0.1 0.6
Tylenchida HY (hyphal feeders)
Ditylenchus sp. 0.6 0 0.3 0.1 0 0.2 0 0.1 0.1 0
Aphelenchoides sp. 4.7 2.5 8.3 9.1 63 57 36 25 35 24
Rhabditida BF (bacterial feeders)
Acrobeloides sp. 1.7 0.7 0.3 1.5 50 26 3.7 4.1 12 12
Panagrolaimus spp. 1.3 2.1 1.2 1.5 7.4 1.7 5.3 7.7 0.6 4.1
Rhabditis s.l. sp. 0 1.1 9.1 2.7 1.5 34 7.8 12 2.3 6.7
Diplogaster sp. 0 0 0 0 0 0 0.7 0 0 0.8
Bunonema spp. 0.9 0.5 1.4 0.4 1.1 0.7 2.7 2.0 0.3 1.2
Adenophorea BF (bacterial feeders)
Teratocephalus costatus 0 1.6 5.0 3.1 8.8 2.2 7.5 6.9 1.3 14.5
Teratocephalus spp. 69 36 126 119 181 105 81 185 123 143
Metateratocephalus sp. 1.8 2.9 7.4 3.6 4.3 2.0 5.2 2.7 4.2 8.1
Plectus tenuis 1.6 0.1 0.8 0.1 0 0.1 0.3 0.2 0.4 0
P. longicaudatus 10.8 36 78 60 70 103 170 104 92 181
Plectus spp. 7.1 24 63 41 72 113 84 95 63 126
Chronogaster sp. 0.3 0 0.3 0.3 0 0.3 0.2 0.5 0 0
Rhabdolaimus sp. 0 0.1 0 0.2 0.4 0.4 0.4 0 0 0
Wilsonema sp. 0.3 0.1 0 0 0 1.9 0.1 0 1.8 0.3
Eumonhystera sp. 2.7 7.3 14 6.0 17 6.9 26 20 8.2 17
Prismatolaimus dolichurus 12 23 41 43 29 29 30 44 21 38
Dorylaimida OM (omnivores)
Eudorylaimus spp. 17 13 39 41 42 34 41 53 37 82
Dorylaimida HY (hyphal feeders)
Tylencholaimus mirabilis 0.5 0 0 0 0 0 0 0 0 0
Nematoda total numbers 152 162 435 357 684 558 546 609 457 721
Figures show number of nematodes gdwÿ1soil material.
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 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
4.1. Fluctuations in various components
Multiple linear regression analysis yielded no cor-relations among nematodes, microbial parameters and
Tylenchida RH% 12.9 7.3 9.4 6.5 20.1 7.4 7.9 7.8 11.8 8.7
Tylenchida HY% 3.5 1.5 2.0 2.6 9.2 10.3 6.6 4.2 7.7 3.3
Dorylaimida HY% 0.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Rhabditida BF% 2.6 2.7 2.7 1.7 8.8 11.1 3.7 4.2 3.4 3.4
Adenophorea BF% 69.3 80.3 77.0 77.6 55.8 65.1 74.2 75.2 68.9 73.2
Dorylaimida OM% 11.4 8.1 8.9 11.6 6.1 6.1 7.6 8.6 8.2 11.3
Fungal biomass (Ergosterol)mg ± 96.4 114 96.9 114 118 102 110 126 89.6
Microbial biomass (CFE) mg C ± 43.6 38.9 34.3 31.6 44.3 39.5 38.7 31.9 40.7
Inorganic nitrogen mg N ± 0.41 0.36 0.36 0.20 0.64 0.30 0.30 0.10 0.37
Maturity index (MI) 2.50 2.51 2.56 2.64 2.41 2.33 2.39 2.54 2.50 2.50
Evenness 0.67 0.80 0.71 0.67 0.73 0.73 0.66 0.77 0.79 0.65
Shannon index 1.98 1.72 1.69 1.69 1.88 1.72 1.62 1.67 1.80 1.67
Fungal f/Bact f (F/B) 1/21 1/54 1/41 1/31 1/7.1 1/7.4 1/12 1/19 1/9.4 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.
Fig. 6. Fluctuations of total microbial biomass (CFE), inorganic nitrogen (NH4NO3), rhabditid nematodes, and tardigrades at (a)
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 com-ponents 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 stron-gest at the open sites UL and LA, which was unex-pected 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 pre-cipitation. 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 ¯uctua-tions 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,
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 trans-ferred 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 micro-bial biomass to occur in October, the micromicro-bial bio-mass 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 con-sumption 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 nema-todes had little in¯uence on microbial biomass and mineralization processes in this case.
consid-tion between nematodes and tardigrades.
4.3. Connections between climate and fluctuations of components
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 rhab-ditids (Acrobeloides and Rhabditiss.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 miner-alization 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 consum-ing 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 observa-tions 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 micro-bial 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
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 nema-todes in an incubation experiment using humus mate-rial 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 interpreta-tion 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 interpre-tation of the typical reaction of the system.
Acknowledgements
The study was supported by a grant from the European Commission to the project Diversity Effects in Grassland Ecosystems of Europe (ENV4-CT95-0029). 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 inor-ganic 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 people: Nils-AÊ ke Andersson, Abisko naturvetenska-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 Lanna-Saleby; Ulf Johansson, ToÈnnersjoÈhedens foÈrsoÈkspark; Lennart Henriksson, SLU Alnarp; and Torsten Kel-lander, Torslunda foÈrsoÈksstation. Anders Bignert is thanked for making the map.
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