Directory UMM :Data Elmu:jurnal:A:Applied Soil Ecology:Vol16.Issue1.Jan2001:

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Succession of soil nematodes in pine forests on coal-mining

sands near Cottbus, Germany

Ladislav Hánˇel

∗

Institute of Soil Biology, Academy of Sciences of the Czech Republic, Na sádkách 7, CZ-370 05 ˇCeské Budˇejovice, Czech Republic Received 19 July 1999; received in revised form 29 May 2000; accepted 31 May 2000

Abstract

The succession of soil nematodes from initial planting with Pinus sylvestris seedling to about 30-year-old pine plantations on coal mining sands in the Lusatian lignite-mining district near Cottbus (Germany) was studied and compared with the nematode fauna of a 40-year-old semi-natural pine forest on naturally formed sandy soil. The initial stage was primarily characterised by a very low abundance (20×103individuals/m2), which increased over a period of two years to values common in older pine plantations (500–600×103_{individuals/m}2_{). In the semi-natural forest the mean abundance of nematodes was about} 1300×103individuals/m2. Populations of Tardigrada, Rotifera and Enchytraeidae also increased with stand age. Nematode biomass increased from 49 to 543 mg m−2_{in pine plantations and slightly decreased in the semi-natural forest to 301 mg m}−2 over the period of investigation. The early colonisation of the initial stage was by bacterivorous (Acrobeloides) and fungal feeding (Aphelenchoides) nematodes, but the communities diversified as succession progressed with bacterivorous nematodes of the genera Plectus, Wilsonema and Metateratocephalus, root-fungal feeding Filenchus, omnivorous Aporcelaimellus and

Eudorylaimus, and predacious Prionchulus becoming abundant. The abundance of plant-parasitic nematodes was very low.

Keywords: Nematoda; Community structure; Tardigrada; Rotifera; Enchytraeidae

1. Introduction

Soil nematodes are a widespread group of animals, which can be found in every terrestrial ecosystem. Due to their small body and adaptations to survive adverse environmental conditions they can be easily transported over long distances by wind, water, on or in plant and animals or by other means. In collections made from wind and water various species from var-ious ecological groups can be found and these can reach new areas irrespective of the passive mode of

∗_Tel.:₊_{420-38-777-5759; fax:}₊_{420-38-41001.}

E-mail address: [email protected] (L. H´anˇel).

their spreading. However, their further development depends on their ability to find food resources and suit-able habitats in the new location. Their activity con-tributes to modification of their environment and the new qualities facilitate survival and reproduction of new species. This successive colonisation and extinc-tion of nematode species from ecosystems gives not only information on their biology but also information about relationships with other organisms and changes in soil properties; for these reasons, it receives the at-tention of nematode ecologists.

Wasilewska (1970, 1971) and Brzeski (1995) in Poland studied the succession of nematodes in pine forest on European inland sands. De Goede et al. 0929-1393/01/$ – see front matter © 2001 Elsevier Science B.V. All rights reserved.

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(1993a,b) evaluated nematode communities in vari-ous successional stages of pine on shore drift sands in The Netherlands. Slepetiene (1986) gave data on nematodes in different pine growths on coastal sand accumulations in Lithuania. These papers investigated nematodes in sandy substrates that had been exposed to recent (quaternary) inland climates for a long time (Poland) or modified by continental+maritime factors (The Netherlands, Lithuania). The sandy substrates comprising spoils from coal-mining sites, which have been buried for millions of years but recently opened up by mining and suddenly exposed to recent cli-mates, are a different situation. They are free of re-cent organic matter but rich in fossil carbon, contain pyritic substrates and acidify during the weathering of iron-disulfides. They were close to or in contact with ground water, with relatively stable temperatures, and then subjected to rapid desiccation and consider-able fluctuation of air temperature. The questions are: How do populations of current soil nematode species colonise such areas? Does the succession of soil nema-todes follow the common patterns described in papers mentioned above or those attributed to succession in general? Do soil nematode assemblages in pine woods on coal-mining sands have any specific characteris-tics?

2. Materials and methods

Investigations were carried out in the Lusa-tian lignite-mining district near Cottbus (Germany; 14◦₂₀′_{E, 51}◦₄₆′_{N). The coal-mining dumps from} open-cast mining activities in the Cottbus area are formed by tertiary sand from lignite rich deposits

Table 1

Characteristics of the various sites investigateda

Characteristics WB BB SD MR DDM DDO NP

Age of stand (years) 1 14 17 18 32 32 40

pH (H2O) 2.70 4.41 4.95 5.02 3.70 4.65 3.85

pH (KCl) 2.58 3.55 4.05 4.24 2.98 4.06 3.15

P (total) (mg kg−1₎ ₄₃₇ ₂₇₃ ₁₅₅ ₁₆₉ ₅₉₈ ₃₅₈ ₁₉₃

P (available) (mg kg−1₎ ₂₇ ₁₂ ₁₂ ₈ ₆ ₈ ₈

P (water-soluble) (mg kg−1₎ ₂ ₃ ₅ ₄ ₄ ₅ _4.5

Cox(%) 1.46 3.61 1.92 5.86 19.16 12.12 2.85

a_WB₌_{Weissagker Berg; BB}₌_Bärenbru˝_{cker Höhe 1; SD}=Schlabendorf-Nord; MR=Meuro; DDM=Domsdorf 1; DDO=Domsdorf 2; NP=Bärenbr˝u_{cker Höhe 2.}

and are characterised by low pH values of 2–3. Mean annual air temperature of the area averages 8–9◦_C and precipitation averages 500–550 mm per annum. In 1997 and 1998, mean annual temperatures were 9.6 and 7.9◦_{C, and total precipitation was 528 and} 485 mm, respectively. Communities of soil nema-todes, abundance of Enchytraeidae, Rotifera and Tardigrada were studied in six pine forest localities es-tablished on mining dumps and one semi-natural pine forest. Carbon (Cox organic carbon=recent+fossil) and phosphorus were determined according to Frouz and Kalˇc´ık (1997). The site characteristics are given below and in Table 1.

• WB — Weissagker Berg: an initial succession site with Pinus sylvestris L. seedlings planted in 1997 (1-year-old in 1997) and with a dense Secale mul-ticaule growth.

• BB — Bärenbr˝u_{cker Höhe 1, a 14-year-old (in} 1997) plantation of Pinus nigra Arnold with Cala-magrostis epigeios (L.) Roth, Avenella flexuosa (L.) Drejer, Carex hirta L.

• SD — Schlabendorf-Nord, a 17-year-old plantation of P. sylvestris with scarce grass of C. epigeios, C. hirta, and A. flexuosa in the understorey.

• MR — Meuro, an 18-year-old plantation of P. sylvestris with pine litter in the understorey and sparse vegetation patches of C. epigeios and Rubus sp. and patches of pine litter.

• DDM — Domsdorf 1, a 32-year-old plantation of P. sylvestris with understorey vegetation patches of C. epigeios, A. flexuosa and Fragaria vesca L. com-bined with patches of pine litter.

• DDO — Domsdorf 2, a 32-year-old plantation of P. sylvestris with scarce grass but prevailing bare pine litter in understorey.

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• NP — Bärenbr˝u_{cker Höhe 2, a semi-natural P.} sylvestris forest approximately 40-year-old on nat-urally formed sandy soil not affected by mining (a control plot to compare with pine plantations on coal-mining sandy dumps), patches of bare pine litter, grass (mainly A. flexuosa) and moss in understorey.

The sand dumps had been ameliorated with power plant fly ash at the rate of about 1000 t ha−1_{and NPK} fertilisers to adjust the pH of the substrate, with the exception of SD where the fly ash was replaced by lime.

Soil samples for investigation of soil microfauna and mesofauna were taken using a cylindrical soil corer of cross-sectional area 10 cm2 down to a depth of 10 cm. Five replicate samples were taken on 30 May–1 June 1997 (1), 29 September–1 October 1997 (2), 27–30 April 1998 (3), and 29–30 October 1998 (4). In the laboratory, the soil was thoroughly mixed and nematodes, enchytraeids, rotifers and tardigrades were isolated from four 10 g sub-samples by means of the modified Baermann funnel method, fixed in 3% formaldehyde and studied in glycerine slides (for details, see Hánˇel, 1995). The Shannon index (H′_{) with natural logarithms was calculated from the}

Table 2

Mean abundance of soil nematodes, enchytraeids, rotifers, and tardigrades (×103_{individuals/m}2_{) in pine forests, biomass and diversity of}

nematodes, with codes used for ordination of genera (Figs. 2 and 3)a

Genus/locality Code WB BB SD MR DDM DDO NP

Bacterial feeders 370 274 411 310 227 248 568

Acrobeloides 9 355 113 164 165 58 16 106

Plectus 4 8 110 170 109 124 175 213

Panagrolaimus 14 4 33 53 13 10 15 13

Wilsonema 6 1 1 3 3 7 100

Rhabditis 16 1 3 3 3 16 3 23

Metateratocephalus 7 1 6 19 23

Cervidellus 12 2 46

Prismatolaimus 29 1 15 7 2

Drilocephalobus 13 1 1 1 22

Eumonhystera 1 2 2 5 3 3

Bursilla 15 7 1 4 2 2

Heterocephalobus 10 3 1 2 1 3

Teratocephalus 8 1 3 3

Alaimus 31 1 4

Cephalobus 47 3 1

Ceratoplectus 5 2 2

Prodesmodora 3 3

Geomonhystera 2 1 1

Eucephalobus 11 1 1

abundance of nematode genera (gen) (H’gen). The maturity index (MI) and the plant parasite index were calculated according to Bongers (1990) and the sum maturity index P

MI was calculated according to Yeates (1994). Dendrograms of structural similarity were produced from log(x+1) abundance data for genera by the CLUSTAN program (Wishart, 1981) with Euclidean distance and Ward’s clustering algo-rithm. Principal component analysis was performed by CANOCO (Ter Braak, 1987) on logarithmically transformed abundance values.

3. Results

A total of 47 nematode genera was found in the area studied. The majority of nematode individuals belonged to the genera Acrobeloides (21%), Plectus (20%), Aphelenchoides (16%), Filenchus (13%), Eu-dorylaimus (6%), and Ditylenchus (5%). The distribu-tion of these and less abundant genera in individual pine forests is given in Table 2. In general, abundance and dominance of the genus Acrobeloides decreased with the age of pine plantation whereas that of the genus Plectus increased. The genus Aphelenchoides

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Table 2. (Continued )

Genus/locality Code WB BB SD MR DDM DDO NP

Fungal feeders 200 136 162 128 116 58 227

Aphelenchoides 18 183 86 106 80 101 38 148

Ditylenchus 27 15 41 48 26 12 10 70

Tylencholaimus 39 7 20 7 1

Paraphelenchus 45 1 7

Deladenus 28 1 2 4 1

Tylolaimophorus 40 6

Aphelenchus 41 2 1 2

Root hair-fungal feeders 1 57 3 65 165 326

Filenchus 19 57 1 65 165 286

Malenchus 22 21

Tylenchus 20 1 19

Cephalenchus 23 2

Coslenchus 21 1 1

Plant parasites 1 4 1 3 1

Helicotylenchus 24 1 2 2 1

Rotylenchus 25 2

Pratylenchus 26 1

Tylenchorhynchus 42 1

Omnivores 2 23 38 43 61 76 160

Eudorylaimus 37 2 7 11 6 55 23 150

Aporcelaimellus 38 14 16 16 3 48 8

Thonus 46 2 17 2 4 1

Mesodorylaimus 36 1 9 4 1 1

Prodorylaimus 35 1

Aporcelaimus 44 1

Predators 1 3 2 3 27 45 2

Prionchulus 32 1 1 3 27 45 2

Anatonchus 34 1

Clarkus 33 1 1

Tripyla 30 1

Mylonchulus 43 1

Insect parasites

Steinernema larvae 17 2 15 16 20

Sum of abundance 574 499 629 502 498 594 1303

Number of genera 13 24 22 23 22 27 32

H’gen 0.94 2.15 1.99 2.09 2.18 2.14 2.44

MI 2.00 2.05 2.10 2.24 2.32 2.52 2.24

MI 2.00 2.05 2.10 2.25 2.37 2.74 2.35

PPI 2.07 2.04 2.01 2.00 2.03 2.00 2.00

Total biomass (mg m−2₎ ₄₉ ₁₆₆ ₂₈₄ ₁₈₈ ₂₇₂ ₅₄₃ ₃₀₁

Mean individual biomass (mg) 0.15 0.33 0.41 0.41 0.60 0.98 0.23

B/F 1.85 2.02 2.54 2.43 1.96 4.24 2.51

B/(F+RF) 1.84 1.42 2.54 2.37 1.26 1.11 1.03

Enchytraeidae 3 6 7 18 21 21

Rotifera 22 31 22 27 23 36 114

Tardigrada 6 12 32 39 44 37 99

a_B/F₌_{bacterial feeders/fungal feeders, B/(F}₊_RF)₌_{bacterial feeders/(fungal feeders}₊_{root hair-fungal feeders). For abbreviations of sites}

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Fig. 1. Dendrograms of cluster analysis of nematode genera in individual sites (A) and of nematode genera in individual sites and sampling dates (B); 1=samples taken spring 1997; 2=samples taken autumn 1997; 3=samples taken spring 1998; 4=samples taken autumn 1998. For explanation of site abbreviations see Table 1.

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Fig. 2. Ordination (PCA) of sites and nematode genera; Euclidean distance biplot, eigenvalues for axes 1, 2, 3, 4 are 0.54, 0.22, 0.13, and 0.05, respectively; for codes of genera and site abbreviations see Tables 1 and 2. The genera given by name are those with overall dominance greater than 1.1% except for Panagrolaimus which appeared in the group of genera around the intersection of the ordination axes. Less dominant genera are indicated by number codes.

reached its greatest abundance and dominance in the initial stages of succession. The abundance and dom-inance of the genus Filenchus increased with succes-sion towards the semi-natural P. sylvestris forest and also increased in the P. nigra plantation (especially in Autumn, 1998). The abundance of the genus

Eudory-laimus showed an increase with the age of pine forests but the abundance of the genus Ditylenchus fluctuated between the different stages of succession.

Fig. 1A shows the dendrogram of structural similar-ity of nematode communities in individual sites. There were two main clusters: the first comprised nematode

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communities in younger pine forests, whilst the sec-ond included nematode communities in older succes-sional stages. In the first cluster, the youngest stage of P. sylvestris was clearly different from the others and there was also a difference between the P. nigra plan-tation (BB) and planplan-tations of P. sylvestris of similar age (SD, MR). Fig. 1B shows the similarities in num-bers of nematodes between individual sites and at dif-ferent sampling times. There were two main clusters again, the first including younger successional stages and the second with older successional stages of ne-matode communities. Departures from this main pat-tern were MR3 in the group with samples from initial successional stages and BB4 in the cluster comprising the older successional stages.

Fig. 2 shows Euclidean distance biplots from prin-cipal component analysis (PCA) of nematode com-munities in individual sites and of nematode genera. The diagrams show that the nematode assemblages with Acrobeloides and Aphelenchoides as the domi-nant genera in early successional stages changed into those with Plectus and Filenchus as dominants in older successional stages. Acrobeloides and Filenchus were on opposite sides of the gradient along the first ordination axis extracted and the two genera marked the main trend in the development of nematode as-semblages from the initial successional stage (pine seedling planting) to the developed successional stage (semi-natural pine forest). The nematode assemblages in older pine plantations (DDM, DDO) were diver-sified with Prionchulus and Aporcelaimellus being characteristic. Wilsonema and Eudorylaimus (and also Filenchus) characterised the nematode community in the semi-natural pine forest (NP). Table 3 gives the correlation coefficients of environmental variables with the ordination axes for genera. The first ordi-nation axis was correlated with the age of pine trees and separated nematode communities in the youngest successional stages from those in older successional stages. The second ordination axis was correlated with Cox and total P. The third ordination axis re-flected acidity, available P and water-soluble P in soil. Fig. 3 shows the ordination of nematode assemblages in individual sites and sampling dates. In the main, the results were very similar to those shown in Fig. 2. Moreover, rapid development of nematode assem-blages was obvious in the initial successional stage (WB), which corresponded with marked changes in

Table 3

Correlation coefficients of environmental variables with ordination axes for genera in Fig. 2

Characteristics Axis 1 Axis 2 Axis 3 Axis 4 Age of pine forest 0.921 0.127 −0.204 −0.213 pH (H2O) 0.323 0.302 −0.858 0.063

pH (KCl) 0.325 0.336 −0.855 0.021 P (total) 0.458 0.609 0.058 0.018 P (available) 0.218 0.126 −0.832 0.478 P (water-soluble) 0.525 0.240 −0.700 −0.278

Cox 0.316 0.686 0.216 −0.281

total nematode abundance (Table 4). On the other hand, development in semi-natural P. sylvestris (NP) suggested long-term cyclic changes in the structure of nematode assemblages. The position of BB4, close to the group of older successional stages, in-dicated faster nematode community development in this site than in comparatively old P. sylvestris stands (MR, SD). This was in accordance with results in Figs. 1 and 2 and Table 2, which reflected devel-opment of populations of the genus Filenchus in P. nigra soil.

The total average abundance of nematodes was very similar in all pine plantations on coal-mining sands (502–629×103individuals/m2) and was about one-half of the total abundance of nema-todes in the soil of the semi-natural pine forest (1303×103individuals/m2). In this forest, there were less marked seasonal fluctuations in nematode abun-dance in comparison to the abrupt increase found in the initial successional stage (Table 4). The total biomass of nematodes increased with the age of pine plantations and was somewhat lower in semi-natural pine forest. The mean biomass of an individual ne-matode followed similar trends (Table 2).

The lowest number of nematode genera occurred in the initial successional stage. After this, the number of genera increased and was more or less similar in the other pine plantations on coal-mining sands (with the exception of DDO, which had somewhat more gen-era). The greatest number of nematode genera was in semi-natural pine forest (Table 2). The changes of H’gen values were very similar to those of number of genera. MI andP

MI increased as succession pro-gressed and were somewhat lower in semi-natural pine forest. Changes in the values of PPI were negligible. The B/F ratio had the highest value in DDO. The

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high-Fig. 3. Ordination (PCA) of nematode genera in individual sites and sampling dates; Euclidean distance biplot, eigenvalues for axes 1, 2, 3, 4 are 0.35, 0.20, 0.11, 0.07, respectively; for codes of genera and site abbreviations see Tables 1 and 2 and for times of sampling see Fig. 1. The genera given by names are those with dominance greater than 1.1% overall. Less dominant genera are indicated by number codes.

est value of B(F+RF) was in SD and decreased in older pine forests.

Bacterial feeders were the most prominent trophic group of nematodes with about 52% of individuals followed by fungivores (22%), root-fungal feeders (13%), and omnivores (9%). The proportion of plant parasites was negligible (Table 2).

The abundance of Enchytraeidae, Rotifera and Tardigrada increased as succession progressed. Their seasonal changes are given in Table 4. Fast initial colonisation of coal-mining sands (WB) was espe-cially visible in Rotifera from undetectable pop-ulations in spring 1997 to 50×103individuals/m2 in autumn 1998. The greatest populations of

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Ro-Table 4

Seasonal changes of abundance of soil nematodes, enchytraeids, rotifers, and tardigrades (×103_{individuals/m}2_{) in pine forests}

Date/locality WB BB SD MR DDM DDO NP Nematoda

Spring 1997 19 548 452 707 666 1089 1591 Autumn 1997 128 518 927 442 503 317 1343 Spring 1998 1239 372 454 200 526 597 1160 Autumn 1998 908 558 681 661 299 372 1117 Enchytraeidae

Spring 1997 3 16 3 7 28 22

Autumn 1997 5 5 2 39 13 28

Spring 1998 3 2 14 20 30 30

Autumn 1998 4 3 9 5 15 6

Rotifera

Spring 1997 62 16 27 19 38 146

Autumn 1997 4 27 27 11 31 34 182 Spring 1998 11 18 17 21 32 37 90 Autumn 1998 50 18 29 51 10 35 37 Tardigrada

Spring 1997 11 100 21 47 70 114

Autumn 1997 9 9 9 19 16 17 154

Spring 1998 4 24 14 88 92 37 80

Autumn 1998 5 4 6 27 20 23 48

tifera and Tardigrada occurred in semi-natural pine forest.

4. Discussion

The development of nematode communities in pine stands on coal-mining sands corresponded with the succession of nematodes in pine forests on sand dunes of Kampinos Forest in Poland studied by Wasilewska (1970, 1971) in many respects. Abundance was very low in the initial stage, then increased and the com-munities of nematodes diversified as succession pro-gressed. However, the increase in abundance was less in the stands studied than in Kampinos Forest. The abundance and dominance of omnivores increased in the succession studied whereas their dominance de-creased in the localities studied by Wasilewska (1971). Sites studied by De Goede et al. (1993a,b) on drift sands in The Netherlands also showed gradual changes in nematode faunal structure as succession proceeded but were characterised by greater total abundance of nematodes than the localities that I studied. There was also a great abundance of omnivores in early

succes-sional stages in these sites, with 32% of the nema-todes being omnivores in a six-year-old pine forest in Poland.

The high populations of omnivores in dune and drift sands in Poland and The Netherlands could reflect the presence of small amounts of organic matter and asso-ciated microrganisms. Coal-mining sands are primar-ily without humus organic matter (although they are contaminated with fossil carbon), which subsequently appears as a result of accumulation of plant debris on the surface of sandy dumps or can be added dur-ing amelioration measures. Accumulation of plant lit-ter can support zymogenous (fast-growing) microflora, which was indicated by the development of abun-dant populations of Acrobeloides and Aphelenchoides. By contrast, the genus Rhabditis had a comparatively low abundance and it is known that this genus re-quires higher population densities of bacteria for de-velopment than Acrobeloides (Bongers and Bongers, 1998).

The composition of nematode assemblages in the initial successional stage on coal-mining sands could also reflect extremely low values of pH. It is known that both Acrobeloides and Aphelenchoides are toler-ant to acidification (Ruess and Funke, 1992; Ruess et al., 1993) but Dorylaimida are not (Dmowska, 1993). Low population densities of nematodes were also found in pine forests on sand accumulations at Kurschskaya Kosa, Lithuania (Slepetiene, 1986). The soils were characterised by low pH and low humus contents and supported relatively few nema-todes (from 0.63 to 1.35×106individuals/m2), with fewest species being found in soil with the lowest pH but with the highest humus content. This indi-cates that, in pine forests on sands, pH and humus contents are important factors limiting nematode pop-ulations and influencing the composition of nematode assemblages. However, the ageing of forest is the most important complex factor determining the direc-tion of development of nematode communities. This complex factor includes development of herbaceous undergrowth, litter accumulation and increase in hu-mus contents, together with differentiation of the soil profile (Wasilewska, 1971; De Goede et al., 1993a). Vegetation and decomposition processes modify pH values and the availability of nutrients. Ordination by PCA supported this general hypothesis. The first ordination axis was best correlated with the age of

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pine trees, the second axis with humus contents and total P, and the third axis with pH and available P.

An important phenomenon was the increase in pop-ulation densities of Filenchus species in the succession studied. It is well known that the genus Filenchus (or Tylenchus s.l.) is dominant in pine soil and that pop-ulation densities increase with the age and maturity of pine forest ecosystems (Wasilewska, 1970; Arpin and Ponge, 1986; Slepetiene, 1986; De Goede et al., 1993b). Magnusson (1983b) observed feeding of Ty-lenchus on hyphae of ecto-mycorrhizal Suillus granu-latus (L. ex Fr.) O. Kuntze. Sohlenius and Wasilewska (1984) found the numbers of fungal-feeding nema-todes correlated with metabolically-active fungal biomass. In spruce forests, Filenchus populations con-centrate in mycorrhizae (Hánˇel, 1998). It is also known from laboratory studies that Filenchus species can feed and reproduce on fungal cultures, including my-corrhizal species (Ruess and Dighton, 1996; Brzeski, 1998). Therefore, increase in abundance of the genus Filenchus in the succession studied could indicate an increase in populations of mycorrhizal fungi and es-tablishment of ectomycorrhiza. Increasing population densities of Filenchus in BB could also indicate faster development of mycorrhizal mycoflora in the planta-tion of P. nigra than in plantaplanta-tions of P. sylvestris of similar age on the coal-mining sands investigated. The genus Ditylenchus inhabited all successional stages and it is known that most species of Ditylenchus can feed on various fungi (Yeates et al., 1993).

The second most important genus of bacterio-phagous nematodes was Plectus. The abundance of the genus Plectus was very low in the initial stage of succession but then increased considerably and reached its maximum in semi-natural pine forest. Representatives of the genus Plectus are common in pine stands because of their ability to withstand extreme climatological conditions (De Goede et al., 1993b; Sohlenius, 1996). Coal-mining sands are sus-ceptible to desiccation (and pine litter can dry out very quickly, too) that can limit other bacterivorous nema-todes and contribute to the final low total abundance of nematode populations. The region studied also has very low precipitation (about 500 mm per year) together with relatively high mean annual tempera-tures (8–9◦_{C) compared with, for example, localities} in Sweden with about 600 mm and 4–5◦_C (Magnus-son, 1983a; Sohlenius, 1996). In addition, the surface

mining of lignite is accompanied by a lowering of the ground-water table. Therefore, the relatively low abundance of nematodes in the set of localities studied was not surprising and may have been due to water shortage. On the other hand, abundance of nematodes of the genus Wilsonema increased as succession pro-ceeded with a peak in the semi-natural pine forest. This suggests that the genus Wilsonema could be a good indicator of undisturbed forest soil; in spruce forests heavily damaged by industrial emissions the genus Wilsonema disappeared completely or occurred with a low abundance (Hánˇel, 1993).

Some other genera also had greater abundance in older successional stages: Metateratocephalus, Cervidellus, Drilocephalobus, Eumonhystera, Tera-tocephalus, Alaimus, Geomonhystera, Eucephalobus, Tylolaimophorus, Deladenus, Thonus, and Aporce-laimellus. Their C-P values, according to Bongers (1990), ranged from 1 to 5 and the weighted means of their C-P values (MI andP

MI) increased as succes-sion progressed but with a decrease in the semi-natural pine forest. The utility of C-P values and the ability of maturity indices to detect disturbing influences on nematode assemblages has been discussed frequently (Freckman and Ettema, 1993; Yeates, 1994; Ruess and Funke, 1995; Armendáriz et al., 1996; Sohle-nius, 1997; Wasilewska, 1997; and others). Based on the results of the present study, several nematode genera could be given higher C-P values than orig-inally specified by Bongers (1990): Geomonhystera 3, Wilsonema 3, Plectus 2–3, Cervidellus 3, Drilo-cephalobus 3, Tylolaimophorus 4–5, Filenchus 3. On the other hand, Aporcelaimellus can colonise rela-tively young successional stages more easily than Eudorylaimus as shown in the primary succession studied here or in the secondary succession investi-gated by Hánˇel (1995). In the succession studied by Wasilewska (1970) Aporcelaimellus obtusicaudatus (Bastian, 1865) increased in population density in older pine forests. De Goede et al. (1993b) reported Eudorylaimus to be highly dominant in young as well as older successional stages, whereas the dominance of Aporcelaimellus decreased in older stages. This indicates that different species of the genus Eudory-laimus and different populations of A. obtusicaudatus can adopt variable strategies when inhabiting similar ecosystems in different areas with particular pedolog-ical and climatologpedolog-ical conditions.

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The increase of omnivorous and predatory species during succession is in accordance with many find-ings that these groups of nematodes prefer undisturbed habitats and indicate interconnections between trophic food webs (see Wasilewska, 1997). The low abun-dance of plant-parasitic nematodes in pine forests is in accordance with the results of Brzeski (1995). De Goede et al. (1993b) also found low population den-sities of plant-parasitic nematodes in pine forests of different age and only Tylenchorhynchus was common in all stands.

Begon et al. (1990) defined succession as the non-seasonal, directional and continuous pattern of colonisation and extinction on a site by species pop-ulations. Such changes were evident in the youngest successional stages studied (Figs. 1B and 3) and partially in the P. nigra plantation. In older stands, there was a trend towards increasing prominence of seasonal aspects, exemplified by the cyclic changes in the semi-natural P. sylvestris forest. Some species colonised the early successional stages and then be-came extinct (e.g. Paraphelenchus pseudoparietinus Micoletzky, 1922), others occurred in the middle stages and disappeared later (e.g. Cephalobus perseg-nis Bastian, 1865) or recurred in older stages (e.g. Prismatolaimus intermedius Bütschli, 1873). How-ever, the major trend was the diversification of ne-matode communities as succession progressed, at least in the range of pine tree age classes studied. The increase in food-web complexity and symbiotic relationships in more mature successional stages is also mirrored by changes in nematode communities (increase in abundance of omnivores+predators, in-crease in abundance of Filenchus, greater number of species and genera). On the other hand, nematodes classified as r-strategists (or colonisers) also had im-portant positions in the nematode communities found in older successional stages (values of MI andP

MI were relatively low).

An increase in body size of organisms in older suc-cessional stages is frequently assumed to occur. De Goede et al. (1993b) discussed Odum (1969) hypoth-esis that relatively small animals predominate in the initial stages of succession and that body sizes increase as succession proceeds. They found, in accordance with the results of Wasilewska (1971), that body size of soil nematodes decreased with pine succession and attributed this phenomenon to the increase in soil

or-ganic matter. In the pine sites studied here, the mean individual biomass of nematodes increased with Cox (r=0.713, P<0.10, n=7). This increase in individual biomass was associated with increase in population densities of Plectus, Eudorylaimus, Aporcelaimellus, and Prionchulus (bacterivores, omnivores, predators). In the semi-natural pine forest, high population den-sities of Aphelenchoides and Filenchus (fungal and root-fungal feeders) resulted in a decreased mean body size of an individual nematode in the community. It can be hypothesised that in successive pine forests of the area studied the body size of nematodes in the community increases from initial to relatively young forests and then decreases, reflecting changes in the nematode diet that occur during succession.

5. Conclusion

It was shown that the succession of soil nematodes in pine forests on sandy substrates can vary region-ally with regard to the composition of nematode as-semblages and their subsequent colonisation by dif-ferent groups of nematode species. Peculiarities of nematode development in the coal-mining area stud-ied (relatively low abundance, increase in individual body size followed by a decrease, predominance of acid-tolerant species in initial stages) could be related to the arid climate, low pH of tertiary sandy substrates, absence of recent but presence of fossil carbon, mining and amelioration practices. In accordance with a gen-eral definition of succession the populations of nema-todes (as well as those of Enchytraeidae, Rotifera and Tardigrada) and their diversity increased and there was also extinction of some groups of species in older suc-cessional stages. On the other hand, nematodes adopt-ing an r-strategy (colonisers) occurred in older suc-cessional stages side by side with K-strategists (per-sisters). The expected trend of increasing body size proved to be only partially valid for soil nematodes in the succession sere studied and was found to be re-versed in other regions.

Acknowledgements

The research was supported by Deutsche Forschungs-gemeinschaft, Internationales Büro des BMBF and

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the KONTAKT program (Grant no. ME 076). I also thank my colleagues in the Institute of Soil Biology AS CR (especially Jan Frouz, Václav Pižl, and Jan Materna) who kindly took soil samples for me. I wish to thank two anonymous referees for comments on the manuscript.

References

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communities in younger pine forests, whilst the sec-ond included nematode communities in older succes-sional stages. In the first cluster, the youngest stage of

P. sylvestris was clearly different from the others and

there was also a difference between the P. nigra plan-tation (BB) and planplan-tations of P. sylvestris of similar age (SD, MR). Fig. 1B shows the similarities in num-bers of nematodes between individual sites and at dif-ferent sampling times. There were two main clusters again, the first including younger successional stages and the second with older successional stages of ne-matode communities. Departures from this main pat-tern were MR3 in the group with samples from initial successional stages and BB4 in the cluster comprising the older successional stages.

Filenchus) characterised the nematode community in

the semi-natural pine forest (NP). Table 3 gives the correlation coefficients of environmental variables with the ordination axes for genera. The first ordi-nation axis was correlated with the age of pine trees and separated nematode communities in the youngest successional stages from those in older successional stages. The second ordination axis was correlated with Cox and total P. The third ordination axis

re-flected acidity, available P and water-soluble P in soil. Fig. 3 shows the ordination of nematode assemblages in individual sites and sampling dates. In the main, the results were very similar to those shown in Fig. 2. Moreover, rapid development of nematode assem-blages was obvious in the initial successional stage (WB), which corresponded with marked changes in

Table 3

Correlation coefficients of environmental variables with ordination axes for genera in Fig. 2

Characteristics Axis 1 Axis 2 Axis 3 Axis 4 Age of pine forest 0.921 0.127 −0.204 −0.213

pH (H2O) 0.323 0.302 −0.858 0.063

pH (KCl) 0.325 0.336 −0.855 0.021

P (total) 0.458 0.609 0.058 0.018

P (available) 0.218 0.126 −0.832 0.478

P (water-soluble) 0.525 0.240 −0.700 −0.278

Cox 0.316 0.686 0.216 −0.281

P. nigra soil.

MI increased as succession pro-gressed and were somewhat lower in semi-natural pine forest. Changes in the values of PPI were negligible. The B/F ratio had the highest value in DDO. The

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est value of B(F+RF) was in SD and decreased in older pine forests.

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Ro-Table 4

Seasonal changes of abundance of soil nematodes, enchytraeids, rotifers, and tardigrades (×103_{individuals/m}2_{) in pine forests}

Date/locality WB BB SD MR DDM DDO NP

Nematoda

Spring 1997 19 548 452 707 666 1089 1591 Autumn 1997 128 518 927 442 503 317 1343 Spring 1998 1239 372 454 200 526 597 1160 Autumn 1998 908 558 681 661 299 372 1117

Enchytraeidae

Spring 1997 3 16 3 7 28 22

Autumn 1997 5 5 2 39 13 28

Spring 1998 3 2 14 20 30 30

Autumn 1998 4 3 9 5 15 6

Rotifera

Spring 1997 62 16 27 19 38 146

Autumn 1997 4 27 27 11 31 34 182

Spring 1998 11 18 17 21 32 37 90

Autumn 1998 50 18 29 51 10 35 37

Tardigrada

Spring 1997 11 100 21 47 70 114

Autumn 1997 9 9 9 19 16 17 154

Spring 1998 4 24 14 88 92 37 80

Autumn 1998 5 4 6 27 20 23 48

tifera and Tardigrada occurred in semi-natural pine forest.

4. Discussion

succes-sional stages in these sites, with 32% of the nema-todes being omnivores in a six-year-old pine forest in Poland.

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pine trees, the second axis with humus contents and total P, and the third axis with pH and available P.

An important phenomenon was the increase in pop-ulation densities of Filenchus species in the succession studied. It is well known that the genus Filenchus (or

Tylenchus s.l.) is dominant in pine soil and that

pop-ulation densities increase with the age and maturity of pine forest ecosystems (Wasilewska, 1970; Arpin and Ponge, 1986; Slepetiene, 1986; De Goede et al., 1993b). Magnusson (1983b) observed feeding of

Ty-lenchus on hyphae of ecto-mycorrhizal Suillus granu-latus (L. ex Fr.) O. Kuntze. Sohlenius and Wasilewska

(1984) found the numbers of fungal-feeding nema-todes correlated with metabolically-active fungal biomass. In spruce forests, Filenchus populations con-centrate in mycorrhizae (Hánˇel, 1998). It is also known from laboratory studies that Filenchus species can feed and reproduce on fungal cultures, including my-corrhizal species (Ruess and Dighton, 1996; Brzeski, 1998). Therefore, increase in abundance of the genus

Filenchus in the succession studied could indicate an

increase in populations of mycorrhizal fungi and es-tablishment of ectomycorrhiza. Increasing population densities of Filenchus in BB could also indicate faster development of mycorrhizal mycoflora in the planta-tion of P. nigra than in plantaplanta-tions of P. sylvestris of similar age on the coal-mining sands investigated. The genus Ditylenchus inhabited all successional stages and it is known that most species of Ditylenchus can feed on various fungi (Yeates et al., 1993).

Some other genera also had greater abundance in older successional stages: Metateratocephalus,

Cervidellus, Drilocephalobus, Eumonhystera, Tera-tocephalus, Alaimus, Geomonhystera, Eucephalobus, Tylolaimophorus, Deladenus, Thonus, and Aporce-laimellus. Their C-P values, according to Bongers

(1990), ranged from 1 to 5 and the weighted means of their C-P values (MI andP

Drilo-cephalobus 3, Tylolaimophorus 4–5, Filenchus 3. On

the other hand, Aporcelaimellus can colonise rela-tively young successional stages more easily than

Eudorylaimus as shown in the primary succession

studied here or in the secondary succession investi-gated by Hánˇel (1995). In the succession studied by Wasilewska (1970) Aporcelaimellus obtusicaudatus (Bastian, 1865) increased in population density in older pine forests. De Goede et al. (1993b) reported

Eudorylaimus to be highly dominant in young as well

as older successional stages, whereas the dominance of Aporcelaimellus decreased in older stages. This indicates that different species of the genus

Eudory-laimus and different populations of A. obtusicaudatus

can adopt variable strategies when inhabiting similar ecosystems in different areas with particular pedolog-ical and climatologpedolog-ical conditions.

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perseg-nis Bastian, 1865) or recurred in older stages (e.g. Prismatolaimus intermedius Bütschli, 1873).

How-ever, the major trend was the diversification of ne-matode communities as succession progressed, at least in the range of pine tree age classes studied. The increase in food-web complexity and symbiotic relationships in more mature successional stages is also mirrored by changes in nematode communities (increase in abundance of omnivores+predators, in-crease in abundance of Filenchus, greater number of species and genera). On the other hand, nematodes classified as r-strategists (or colonisers) also had im-portant positions in the nematode communities found in older successional stages (values of MI andP

MI were relatively low).

or-ganic matter. In the pine sites studied here, the mean individual biomass of nematodes increased with Cox

(r=0.713, P<0.10, n=7). This increase in individual biomass was associated with increase in population densities of Plectus, Eudorylaimus, Aporcelaimellus, and Prionchulus (bacterivores, omnivores, predators). In the semi-natural pine forest, high population den-sities of Aphelenchoides and Filenchus (fungal and root-fungal feeders) resulted in a decreased mean body size of an individual nematode in the community. It can be hypothesised that in successive pine forests of the area studied the body size of nematodes in the community increases from initial to relatively young forests and then decreases, reflecting changes in the nematode diet that occur during succession.