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Enchytraeid communities in successional habitats (from meadow to forest)
Pedobiologia 45, 497–508 (2001) © Urban & Fischer Verlag http://www.urbanfischer.de/journals/pedo
Enchytraeid communities in successional habitats (from meadow to forest) Ewa Nowak* Polish Academy of Sciences, Institute of Ecology, Department of Landscape Ecology, Dziekanów Les’ny, 05-092 Lomianki, Poland Submitted: 29. September 2000 Accepted: 14. May 2001
Summary The study was conducted in two successional series: natural on mesotrophic soils (a meadow, two birch woods and a mixed coniferous forest), and human-made on sandy soils (old field, birch plantation and pine forest). In both these series species richness and diversity of enchytraeid communities decreased with advancing succession. In the first two successional stages, enchytraeid communities showed a high degree of similarity (the meadow and 30-year-old birch thicket, ore the old field and 10-year-old birch plantation). Variation in soil in the same plant communities cause differences in animal communities. The abundance of enchytraeids varied from 14 to 51 x 103 m-2 individuals. In the majority of habitats C. sphagnetorum was the dominant species. Soil pH showed a positive correlation with species diversity and negative with number of C. sphagnetorum. The body size of this species was small at low pH (presumably as a result of frequent reproduction). It is suggested that the way of reproduction of the dominant species could confer a competitive advantage, thereby accounting for the simplification of enchytraeid communities in later stages of succession. Key words: Secondary succession, Enchytraeidae, Cognettia sphagnetorum, density, species composition
*E-mail corresponding author: [email protected]
0031–4056/01/45/06–497 $ 15.00/0
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Introduction Succession is a process fascinating ecologist for years. Many mechanisms of succession have already been described in textbooks. It is known how nutrient resources in the soil change during plant succession, and how life strategies of species vary in this process (Begon et al. 1990). But even now new description of this process appear either as a results of long-term studies (Koehler 1998; Petersen 1995) or, more often, due to comparing communities in different stages of succession. The latter, applied in this study, is simpler but less correct and sometimes yielding to misleading conclusions (Pizˇl 1992, 1999). Few descriptions of succession relate to soil organisms (Wardle & Giller 1997; Ohtonen et al. 1997) for two reasons. The first is that the biology of soil organisms is relatively little known, so that changes occurring in their communities are difficult to explain. Secondly, the soil is a conservative habitat so that, as a consequence of buffering mechanisms, physical and chemical changes in soil can be slow and more obscure than changes in plant cover. Despite these difficulties there are a number of papers in soil zoology that relate successional replacement of species with their life strategies (e.g. Petersen 1995; Wasilewska 1998), to the increasing diversity of microhabitats (e.g. Petrov 1997) or changes in quality of food (e.g. Frouz 1997). This paper describes enchytraeid communities in habitats that represent different stages of succession on mineral soil or on soil subjected to rapid mineralisation. The aim of this study was to what extent the changes in this group of saprophages paralleled changes in plant communities.
Materials and Methods The study was conducted in the Kampinos Forest, north-west of Warsaw. In 1959 it was designated a national park, so mowing of meadows ceased and forest succession began on many areas earlier subject to agricultural management. The study plots were situated in the strictly preserved area called Sieraków, in the north-eastern part of the forest. Four plots were established: A – a meadow classified as Stellario-Deschampsietum many years ago (Traczyk 1966) and still representing a community predominated by Deschampsia cespitosa (L) developed on moorsh (hydromorphic) soils (Wicik 1997). At this site, the rate of plant succession is slow because of a high ground water table (it may be flooded in spring and autumn). B – a young, 20–30 years old birch thicket. It grows at the central, drier part, where site A was located also. This part is now overgrown with birches at a density of 35 trees per 10 m2. C – a birch wood. In 1964, this site was described as a clump of trees (oaks and birches) within a meadow (Traczyk 1966). After years of succession this clump covers a much larger area so that it forms a small wood. The experimental plot was located in a birch wood 50 years old with a typical moorsh soil. Density of trees was 15 per 10 m2 with a dominance of birches (13 trees per 10 m2). The samples on this site were taken only in 1998 year. In 1997 samples were taken in the oldest part of the wood predominated by oaks (site Cd). The soil of this part had a large admixture of sand, was highly acidic- pH 3.9, and differed from the soil types at other sites. D – a mixed coniferous forest, Pino-Quercetum. This is a climax community for Deschampsietum (Traczyk 1966). This site was located more than 1 km from the remaining sites. The soils were mineral-moorsh (Solon 1997). Out of 12 trees growing on average per 10 m2 of this site, 4 were pines and 2 were birches.
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This sequence of four sites represents a successional series on mesotrophic soils and was studied in 1997, 1998 years. In 1998, additional samples were taken at three sites on old fields in the buffer zone at the south-eastern edge of the Kampinos Forest: Ao – old field aged three-years, predominated by Antoxantum aristatum Boiss; a species typical of poor old fields (Kotowska, personal communication); Bo – a 10 year-old birch plantation adjoining Ao. Sometimes the samples were taken from the belt of moist, gleyed soil crossing this site. This samples were not removed but analysed only ocasionally and denoted as Bom. Do – a 50 year-old pine wood planted on the site of a mixed coniferous forest, that is, on the most fertile soil in this series. This sequence of sites can be considered a series of secondary succession formed by human activity on the oligotrophic sandy soils. In both years of study the season of 1997 (1 April – 30 September) was wetter and cooler than that of 1998. The sum of precipitation was 456 mm in 1997 and 386 mm in 1998. The mean seasonal air temperature was 14.4 °C in 1997 and 15.0 °C in 1998. In four main habitats (A, B, C, and D), the quantity and quality of food resources and their variability were estimated once in season, in winter 1997. The amount of litter were estimated by taking nine 225-cm2 samples from each site. The weight of the litter, and the proportions of different plant species were assessed (Table 1). Also samples 0–15cm deep and 10 cm2 in area were taken to estimate contents of C, N and soil moisture (Table 2). Variability of soil characteristics was expressed by the coefficient of variation CV = SD % (Table 2). X
Table 1. Mass (g dw m-2) and composition (% dw) of standing crop of litter at the study sites Site Litter mass Litter composition: grasses, forbes, soft leaves birch leaves oak leaves pine needles C/N ratio
A
B
C
D
400
650
530
560
93.4
21.2
14.1
10.6
6.6 – – 24
78.8 – – 23
67.9 17.3 0.7 25
6.5 24.0 58.9 25
Table 2. Chemical properties of soil (and litter- 0–15 cm layer) -a, and their spatial heterogenity CV% -b. The number of samples is shown in parentheses Site
A
B
C
D
a
pH %C %N
5.5 12.91 0.538
5.6 16.72 0.727
5.1 11.92 0.477
4.2 9.90 0.396
b
litter mass (9) soil moisture (5) pH (9) C content (7)
27 5 2 21
29 7 11 21
29 7 9 47
34 18 2 24
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Based on these variables, the birch thicket B can be considered as the richest habitat, with the highest litter fall and low C/N of the litter. On the habitats Ao, Co and Do only soil moisture and pH were estimated. The species composition and abundance of enchytraeids were estimated four times a year, using 15 samples 10 cm2 in area and 15 cm deep from each site. The samples were divided into three 5-cm layers, and the animals were extracted by using the O’Connor method. Live animals were identified (Kasprzak 1986) and measured to the nearest 0.5 mm. Their biomass was calculated from the body length by using the formula w = 6.22x1.55 (Makulec 1983), where w is the fresh weight of an individual in µg, and x is the body length in mm. Shannon index H’ (log2, Krebs 1989) was used to determine the diversity of the communities. Two indices of similarity were applied: 1) Marczewski – modified Sörensen, (Kasprzak & Niedbal/ a 1981), w/a + b – w %, where w is the number of common species, and a or b are total numbers of species in the compared habitats, respectively; and 2) Morisita index (Krebs 1989), 2∑xy/∑x2 +∑y2, where x or y are proportions of successive species in the total number of individuals in respective habitats. Marczewski’s index considers only the presence of a species, thus it is sensitive to occasional species, whereas the Morisita’s index largely depends on the similarity in the dominance structure of the compared communities. The results were tested by using Student’s t- and u-test (difference in numbers, in body sizes and in proportion), correlation coefficients, and analysis of variance (difference in body sizes).
Results The structure of enchytraeid community A total of 24 enchytraeid species was recorded. Most of them were eurytopic, but only one, Cognettia sphagnetorum, was present at all sites (Table 3) and in both study years. This was a dominant species at four sites. Two other species, Acheta camerani and Enchytronia parva, were almost equally common. E. parva was found at all sites except for the mixed coniferous forest D, although according to literature data (Pilipiuk 1993) it can occur in this habitat. In 1997, the proportion of this typically not abundant species was very high (38%) in the acid, sandy part of the birch wood (site Cd). A. camerani occurred also at six sites, although at one of them, birch thicket B, its presence can be considered as accidental (it was not found in 1997). In both years this species was not found in the meadow A. Three species were found at only one site. Two of them, Cognettia glandulosa and Mesenchytraeus armatus, were present in the moist meadow A, and one, Mesenchytraeus glandulosus, in the mixed coniferous forest D which was a relatively dry site. The percentage of the species of two genera, Buchholzia sp. and Fridericia sp., decreased progressively along the main successional series and Acheta sp. increases along both series. The two areas of the Kampinos Forest where the study was conducted showed a distinctive character, probably as a consequence of rather specific soil conditions. In addition to eurytopic C. sphagnetorum, two species, Marionina argentea and B. appendiculata, were abundant in moorsh soils. In sandy soils, numbers of Henlea heleotropha were high (from moorsh soils it was recorded only once), and Enchytraeus norvegicus was found only in October but in large numbers (Table 3). The species richness of enchytraeids varied widely from 6-species communities (Do), to 19- (20 in 1997) species communities in the moist meadow A (Table 3). At
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Table 3. Species composition of enchytraeid communities in 1998. (Relative numbers %; + < 1%) Site
A
B
C
D
Ao
Bo
Do
Mesenchytraeus armatus (Lev.) Mesenchytraeus glandulosus (Lev.) Cˇernosvitoviella atrata (Bret.) Buchholzia appendiculata (Buchh.) Cognettia sphagnetorum (Vejd.) Cognettia glandulosa (Mich.) Marionina argentea (Mich.) Marionina sp. Enchytraeus buchholzi Vej Enchytraeus christenseni Niel.et Chr Enchytraeus norvegicus Abrah Fridericia bulbosa (Rosa) Fridericia striata Issel Fridericia maculata Issel Fridericia leydigi (Vejd.) Fridericia bisetosa (Lev.) Fridericia ratzeli Eis Fridericia sp. Enchytronia parva Niel.et Christ. Henlea perpusilla Friend Henlea heleotropha Steph Henlea nasuta (Eis) Henlea ventriculosa (d’Udek.) Acheta camerani Cog. Acheta bohemica (Vejd.) Acheta eiseni Vejd.
2 – 10 12 19 2 28 1 1 3 – 2 – 4 2 2 2 – 1 5 + 3 1 – – –
– – 1 9 4 – 37 6 5 8 – 3 – 3 3 3 3 – 3 5 – 4 3 + – –
– – – 9 68 – 3 + – 1 – – – 1 1 1 1 – 6 – – 3 1 5 – 1
– + – + 55 – + – – – – – + – – – – – – – – – – 27 4 14
– – – – 58 – – – – – 4 – – + – + – + 7 – 21 – – 2 – 8
– – – – 27 – – – – – 10 – – – + 2 – + 1 – 51 – – 2 – 7
– – – 3 76 – – – – – – – – – – – – – + – 1 – – 10 – 10
Total number of identified animals Total number of species H’
522 402 603 694 263 251 236 19 17 14 8 9 9 6 3.34* 3.33 1.89 1.62 1.82* 2.00 1.24
* Not significant difference between neighbouring site. The other differences were significant at p = 0.01
this site, the index of species diversity reached a maximum value of 3.36 in 1997. In both years and in both sequences, the most diverse enchytraeid communities occurred in habitats covered with herbaceous plants (A and Ao), whereas the least diverse communities occurred in both forest habitats, mixed coniferous forest D and planted pine forest Do. A comparison of species diversity (Table 3) with habitat heterogenity (Table 2) of the four main habitats yielded unexpected results. No relationship was found between the species richness of enchytraeid communities and the range of variation in chemical properties (pH and N content in soil) or in physical properties (litter fall and mois-
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ture). Nor can a relationship be expected between the species richness and soil fertility because the latter decreased in one successional series and increased in the other series. It seems that the simplification of the enchytraeid community is related to decreasing soil pH. Linear correlation between this factor and the number of enchytraeid species (Fig.1) was r = 0.86, and for the Shannon index r = 0.80, both these values being significant at p < 0.02. The regression line was fitted according to the formula Y = 8.4X – 29 and y = 1.3X – 4.4 where X-soil pH, Y-number of enchytraeid species, y-diversity H’. Similarity of enchytraeid communities The enchytraeid communities of different sites were considered to be similar if their similarity indices approximated to for the same habitat in two successive years. The values of the Morisita index for between-year comparisons ranged from 0.94 for forest D to 0.88 for meadow A. The range of the Marczewski index was from 53 for forest D to 88 for birch wood C/Cd. Accepted similarity limit was 0,70 for the Morisita and 50 for the Marczewski index. According to the Morisita index the following pairs of sites were similar: D/Do, A/B, and, a little less, Ao/Bo and Ao/D (Table 4a). According to the Marczewski index all sites on sandy soils were similar (Ao, Bo, Do, and the old field and birch plantation even identical), and also A/B and B/C (Table 4b). With respect to the dominance structure and species composition, the similarity was confirmed for two habitat pairs, A/B and Ao/Bo, that is, between the habitat with herbaceous plants and young, 10- or 30-year-old birch thicket. These two initial stages of succession were similar, and then their similarity was declining with time (e.g. meadow to birch thicket A/B 0.85, meadow to birch wood A/C 0.48, meadow to coniferous forest A/D 0.39). Low similarity indices of enchytraeid communities were obtained for the same plant communities at sites with differential substrate. The Morisita index for sites
Fig. 1. Relationship between the soil pH and the number of enchytraeid species. Sites: meadow A, birch thicket B, birch wood C, coniferous forest D, old field Ao birch plantation Bo, pine wood Do
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Table 4. Similarity of enchytraeid communities in the Morisita (a) and Marczewski (b) indices for the successional sites (bold – similar communities) a – Morisita coefficient, 1998 year Site
B
C
D
Ao
Bo
Do
A B C D Ao Bo
0.85
0.48 0.15
0.39 0.09 0.45
0.41 0.09 0.52 0.79
0.21 0.05 0.44 0.43 0.74
0.28 0.09 0.52 0.92 0.46 0.46
b – Marczewski coefficient, 1998 year Site
B
C
D
Ao
Bo
Do
A B C D Ao Bo
80
50 63
12 19 29
30 31 35 31
17 25 28 30 100
19 21 33 40 55 55
C/Cd (that is, for parts of birch wood on moorsh and on more sandy soils) was 0.56, and for sites Bo/Bom (that is, for parts of the birch plantation on sandy and on moist, gleyed soils) was 0.39. Numbers and biomass of enchytraeids Numbers of enchytraeids at different sites showed a moderate variation by a factor of no more than 3.3 (Fig. 2). At most sites (B, C, A, Do), mean numbers were not high, 14–27 103 individuals m-2. They were abundant only at sites D and Ao, 51 103 indiv. m-2 and 43 103 indiv. m-2, respectively. Both these sites – the mixed coniferous forest D and old field Ao are considered to be the least fertile in their successional series. No rank correlation was found between soil fertility and enchytraeid numbers (Spearman test, r = 0.4). A negative correlation between the soil pH and enchytraeid numbers was significant (r = –0.81, p = 0.05). Even less differences between sites were found in the biomass of enchytraeids, as estimated from mean body sizes at each site. Differences in body sizes were statistically significant (p < 0.01). In 1997 enchytraeid biomass at different sites differed by a factor of 2.4 and in 1998 by a factor of 1.7, the order of sites remaining the same (Fig. 2). Numbers and biomass of enchytraeids were generally a little lower in 1997, which was more humid and cool than 1998 (rather moist habitats were compared and the sum of precipitation was not fully reflected in soil moisture). Spatial variation in enchytraeid numbers was very high. At site D in 1997, the value of CV reached even 149%. Some similarity exists between this variation and spatial heterogenity of the sites, but not obvious. In both, 1997 and 1998, the highest
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Fig. 2. Population density (a) and biomass (b) of enchytraeids at the study sites. Density N x 103 m-2. Sites: meadow A, birch thicket B, birch wood C, coniferous forest D, old field Ao birch plantation Bo, pine wood Do. * not significant differences in numbers between neighbouring sites. The other differencs were significant at p = 0.01
variation in numbers occurred at site D, that is, in the habitat where physical factors were most diverse (Table 2). The lowest variation (CV 80% and 94% in two years, respectively) was on the meadow A with least variable physical factors. Vertical distribution of enchytraeids Vertical distribution of enchytraeids varied and it seems to reflect soil moisture. The upper soil layer (0–5 cm) of the moist meadow A was inhabited by 89% of enchytraeids in 1997 and 91% in the year 1998. These values ranged from 59% in May to 97% in July 1997. In the drier coniferous forest D, the upper soil layer was inhabited by 62% of enchytraeids in 1997 and 74% in 1998. The range was from 39% in May 1997 to 85% in May 1998. All soil animals most readily occupy the upper layer, rich in food and oxygen. In this layer there were 68 to 90% of C. sphagnetorum but only 51 to 69% Acheta sp. (Table 5). This implies that Acheta not always can find place in the preferred upper layer and that these two genera divide the soil space between themselves.
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Table 5. Relative numbers of C. sphagnetorum and Acheta sp. in the upper soil layer (0–5 cm) (%) Site
B
C*
D
Do
C. sphagnetorum Acheta sp. Both
85 51 66
68 69 69
88 58 74
90 67 96
* Not significant differences in distribution of species. The other differences in depth distributions were significant at p = 0.01
Cognettia sphagnetorum Numbers of this dominant species varied from 600 indiv. m-2 to 28 x 103 indiv. m-2 and were negatively correlated with soil pH (r = –0.96, p = 0.02). The regression line was fitted according to the formula y = 112.0 – 19.8x where x-pH, y- number of C. Sphagnetorum x 103 m-2. The largest population in the mixed coniferous forest D, was infected with gregarine (3.3% of the population); a parasite found in addition only in one individual from meadow A. The frequency distribution of the size of C. sphagnetorum showed site-related differences. The mean body size varied from 3.6 mm in the mixed coniferous forest D to 5.1 in the meadow A. The largest individuals were in the class of 10–11mm at sites D and Do, and in the class of 14.5–15.5 mm in the meadow A (Fig. 3). Statistically significant differences were found in the distribution of body sizes between the meadow and the birch wood (A and C) and the forests and the old field (D, Do, Ao), whereas differences within this two groups were statistical not significant (analysis of variance). Variation in the mean body size can reflect the frequency of divisions. This species reproduces through architomy – the more frequent reproduction (divisions), the smaller the mean individual and the lower the size range. These size distributions were also related to soil pH. The correlation coefficient between pH and the mean size of an individual was week r = 0.84, p = 0.03. The regression line was fitted according to the formula Y = 1.4 + 1.2 pH. As numbers of C. sphagnetorum, like the number of species in the enchytraeid community, both were correlated with soil pH, they were expected to be correlated with each other. This linear, negative correlation, however, was statistical not significant (r = –0.8, p = 0.06).
Discussion A high similarity was found in enchytraeid communities between the meadow and the birch thicket (Morisita index 0.85). Much larger differences occurred among patches that differed in soil type within the birch plantation (Morisita index 0.39) and within the birch wood (0.56). Thus, enchytraeid communities were more sensitive to soil variation within the same plant communities than to successional changes in the vegetation that occurred over several decades (20–13 years).
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Fig. 3. Frequency distribution of body sizes of C. sphagnetorum at the study sites. Mean body size category (mm), number in %, Ao – old field, Do – pine wood, D – mixed coniferous forest. A – meadow, C – birch wood. a – high density, b – low density
In the Czech successional series (Pizˇ l 1999) old field and thicket were not similar but the soil in thicket was without herbaceus layer, and hence some differences in results. The present data show that the number of enchytraeid species and their diversity decrease with plant succession. The number of species more often increases than decreases in the succession of soil organisms (Trojan et al. 1994; Kajak & Wasilewska 1997). Chalupsky (1994) described an increase in the number of enchytraeids in fertile brown soil. A different process occurs in the succession leading to coniferous forests. A decrease in the number of species during such a succession was also described by Pilipiuk 1995. The decline in species richness in relation to decrease in soil pH has been reported in other studies (Standen 1984). In the present study, soil pH can be correlated with almost all parameters of the enchytraeid community, specifically with the number of species, abundance of the dominant species, and with the mean body size of it. The range of pH variation at the study sites (from 4.2 to 5.6) did appear to exceed the tolerance of most enchytraeid species, including C. sphagnetorum (Healy 1980). The soil pH is related to the composition of soil microflora. The importance of fungi (their proportion in microflora) increases with soil acidity (Wallwork 1970). Moreover, the
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ratio of fungal to bacterial biomass increases with plant succession (Ohtonen et al. 1999). C. sphagnetorum, like Acheta, is saprofagous but shows preference for fungi (Kasprzak 1986; Hedlund & Augustsson 1995). The correlation between pH and the abundance of the dominant species may therefore be as a consequence of the availability of fungal food resources. C. sphagnetorum reproduces through architomy. This enables a rapid reproduction when food becomes available. That was important in the habitat where physical factor were diverse (e.g. D). This plasticity of Cognetia may confer advantage in competition with other species. Space allocation between Cognetia and Acheta may be a result of competitive exclusion of the latter from the upper soil layers, rather than a preference of Acheta for deeper layers (Didden & de Fluiter 1998). Nor does the correlation between the number of species and soil acidity seem to be an effect of the absence of species with tolerance of low pH (compare Healy 1980). Rather the relationship may be ascribed to competitive exclusion other species by C. sphagnetorum. The following scenario is suggested for the events described. A decrease (and not increase as in other groups) of species richness of enchytraeids in these successional stages occurred as the consequence of soil acidification by coniferous trees. This acidification, and also plant succession, may enhance the development of fungal biomass, which in turn promotes the fungivorous (saprophagous) enchytraeid C. sphagnetorum. Probably this species was capable of reducing populations of other species and simplifying the diversity of the enchytraeid community.
Acknowledgements I wish to thank J. Kotowska and A. Wasil/kowska, for phytosociological analysis of the study sites. I also thank I. Pilipiuk for her help with identifying enchytraeids and J. Górka for making available maps of the Kampinos National Park.
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Kasprzak, K., Nabagl/o, W. (1981) Wskaz´niki biocenotyczne stosowane przy porza˛dkowaniu i analizie danych. In: Górny, M., Grum, L., Metody stosowane w zoologii gleby. PWN pp. 483. Koehler, H. (1998) Secondary succession of soil mesofauna: A thirteen year study. Applied Soil Ecology 9, 81–86. Krebs, Ch. J. (1989) Ecological Methodology. Harper Collins Publishers, New York pp. 654. Makulec, G. (1983) Enchytraeidae (Oligocheta) of forest ecosystems. I. Density, biomass and production. Ekologia Polska 31, 9–56. Ohtonen, R., Aiko, S., Vare, H. (1997) Ecological theories in soil biology. Soil Biology and Biochemistry, 29, 1613–1619. Ohtonen, R., Fritze, H., Pennanen, T., Jumpponen, A., Trappe, J. (1999) Ecosystem properties and microbial community changes in primary succession on a glacier forefront. Oecologia 118, 239–246. Petersen, H. (1995) Temporal and spatial dynamics of soil Collembola during secondary succession in Danish heathland. Acta Zoologica Fennica 196,190–194. Pilipiuk, I. (1993) Enchytraeidae (Oligocheta) of pine forests in Poland. Fragmenta Faunistica 36, 75–107. Pilipiuk, I. (1995) Communities of Enchytraeidae (Oligocheta) in the pine forest succession sere of Puszcza Bial/owieska. Fragmenta Faunistica 38, 347–352. Petrov, P. (1997) The reactions of communities of oribatid mites to plant succesion on meadows. Ekologia Polska 45, 781–793. Pizˇ l, V. (1992) Succession of earthworm populations on abandoned fields. Soil Biology and Biochemistry 24, 1623–1628. Pizˇ l, V. (1999) Earthworm succession in abandoned fields – a comparison of deductive and sequential approaches to study. Pedobiologia 43, 705–712. Solon, J. (1997) Mapa ros´linnos´ci rzeczywistej. Plan Ochrony Kampinoskiego Parku Narodowego. [Map of plant communities. In: Plan of Conservation of Kampinos National Park.]. KPN Izabelin. Standen, V. (1984) Production and diversity of enchytraeidae, earthworms and plants in fertilized hay meadow plots. Journal of Applied Ecology 21, 293–312. Traczyk, T. (1966) Plant communities of Strzeleckie Meadows in Kampinos Forest. Ekologia Polska 14, 285–299. Trojan, P., Ban´kowska, R., Chudzicka, E., Pilipiuk, I., Skibin´ska, E., Sterzyn´ska, M., Wytwer, J. (1994) Secondary succession of fauna in the pine forests of Puszcza Bial/owieska. Fragmenta Faunistica 37, 3–104. Wallwork, J. A. (1970) Ecology of soil animals. Mc Graw Hill, London, New York, Sydney, Toronto, Johannesburg, Panama. pp 210. Wardle, D. A., Giller, K. E. (1997) The quest for a contemporary ecological dimension to soil biology. Soil Biology and Biochemistry 28, 1549–1554. Wasilewska, L. (1998) Changes in proportions of groups of bacterivorous soil nematodes with different life strategies in relation to environmental conditions. Applied Soil Ecology 9, 215–220. Wicik, B. (1997) Mapa gleb. Plan Ochrony Kampinoskiego Parku Narodowego. [Map of soil. In Plant of Conservation of Kampinos National Park.]. KPN Izabelin.
Enchytraeid communities in successional habitats (from meadow to forest) Ewa Nowak* Polish Academy of Sciences, Institute of Ecology, Department of Landscape Ecology, Dziekanów Les’ny, 05-092 Lomianki, Poland Submitted: 29. September 2000 Accepted: 14. May 2001
Summary The study was conducted in two successional series: natural on mesotrophic soils (a meadow, two birch woods and a mixed coniferous forest), and human-made on sandy soils (old field, birch plantation and pine forest). In both these series species richness and diversity of enchytraeid communities decreased with advancing succession. In the first two successional stages, enchytraeid communities showed a high degree of similarity (the meadow and 30-year-old birch thicket, ore the old field and 10-year-old birch plantation). Variation in soil in the same plant communities cause differences in animal communities. The abundance of enchytraeids varied from 14 to 51 x 103 m-2 individuals. In the majority of habitats C. sphagnetorum was the dominant species. Soil pH showed a positive correlation with species diversity and negative with number of C. sphagnetorum. The body size of this species was small at low pH (presumably as a result of frequent reproduction). It is suggested that the way of reproduction of the dominant species could confer a competitive advantage, thereby accounting for the simplification of enchytraeid communities in later stages of succession. Key words: Secondary succession, Enchytraeidae, Cognettia sphagnetorum, density, species composition
*E-mail corresponding author: [email protected]
0031–4056/01/45/06–497 $ 15.00/0
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Introduction Succession is a process fascinating ecologist for years. Many mechanisms of succession have already been described in textbooks. It is known how nutrient resources in the soil change during plant succession, and how life strategies of species vary in this process (Begon et al. 1990). But even now new description of this process appear either as a results of long-term studies (Koehler 1998; Petersen 1995) or, more often, due to comparing communities in different stages of succession. The latter, applied in this study, is simpler but less correct and sometimes yielding to misleading conclusions (Pizˇl 1992, 1999). Few descriptions of succession relate to soil organisms (Wardle & Giller 1997; Ohtonen et al. 1997) for two reasons. The first is that the biology of soil organisms is relatively little known, so that changes occurring in their communities are difficult to explain. Secondly, the soil is a conservative habitat so that, as a consequence of buffering mechanisms, physical and chemical changes in soil can be slow and more obscure than changes in plant cover. Despite these difficulties there are a number of papers in soil zoology that relate successional replacement of species with their life strategies (e.g. Petersen 1995; Wasilewska 1998), to the increasing diversity of microhabitats (e.g. Petrov 1997) or changes in quality of food (e.g. Frouz 1997). This paper describes enchytraeid communities in habitats that represent different stages of succession on mineral soil or on soil subjected to rapid mineralisation. The aim of this study was to what extent the changes in this group of saprophages paralleled changes in plant communities.
Materials and Methods The study was conducted in the Kampinos Forest, north-west of Warsaw. In 1959 it was designated a national park, so mowing of meadows ceased and forest succession began on many areas earlier subject to agricultural management. The study plots were situated in the strictly preserved area called Sieraków, in the north-eastern part of the forest. Four plots were established: A – a meadow classified as Stellario-Deschampsietum many years ago (Traczyk 1966) and still representing a community predominated by Deschampsia cespitosa (L) developed on moorsh (hydromorphic) soils (Wicik 1997). At this site, the rate of plant succession is slow because of a high ground water table (it may be flooded in spring and autumn). B – a young, 20–30 years old birch thicket. It grows at the central, drier part, where site A was located also. This part is now overgrown with birches at a density of 35 trees per 10 m2. C – a birch wood. In 1964, this site was described as a clump of trees (oaks and birches) within a meadow (Traczyk 1966). After years of succession this clump covers a much larger area so that it forms a small wood. The experimental plot was located in a birch wood 50 years old with a typical moorsh soil. Density of trees was 15 per 10 m2 with a dominance of birches (13 trees per 10 m2). The samples on this site were taken only in 1998 year. In 1997 samples were taken in the oldest part of the wood predominated by oaks (site Cd). The soil of this part had a large admixture of sand, was highly acidic- pH 3.9, and differed from the soil types at other sites. D – a mixed coniferous forest, Pino-Quercetum. This is a climax community for Deschampsietum (Traczyk 1966). This site was located more than 1 km from the remaining sites. The soils were mineral-moorsh (Solon 1997). Out of 12 trees growing on average per 10 m2 of this site, 4 were pines and 2 were birches.
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This sequence of four sites represents a successional series on mesotrophic soils and was studied in 1997, 1998 years. In 1998, additional samples were taken at three sites on old fields in the buffer zone at the south-eastern edge of the Kampinos Forest: Ao – old field aged three-years, predominated by Antoxantum aristatum Boiss; a species typical of poor old fields (Kotowska, personal communication); Bo – a 10 year-old birch plantation adjoining Ao. Sometimes the samples were taken from the belt of moist, gleyed soil crossing this site. This samples were not removed but analysed only ocasionally and denoted as Bom. Do – a 50 year-old pine wood planted on the site of a mixed coniferous forest, that is, on the most fertile soil in this series. This sequence of sites can be considered a series of secondary succession formed by human activity on the oligotrophic sandy soils. In both years of study the season of 1997 (1 April – 30 September) was wetter and cooler than that of 1998. The sum of precipitation was 456 mm in 1997 and 386 mm in 1998. The mean seasonal air temperature was 14.4 °C in 1997 and 15.0 °C in 1998. In four main habitats (A, B, C, and D), the quantity and quality of food resources and their variability were estimated once in season, in winter 1997. The amount of litter were estimated by taking nine 225-cm2 samples from each site. The weight of the litter, and the proportions of different plant species were assessed (Table 1). Also samples 0–15cm deep and 10 cm2 in area were taken to estimate contents of C, N and soil moisture (Table 2). Variability of soil characteristics was expressed by the coefficient of variation CV = SD % (Table 2). X
Table 1. Mass (g dw m-2) and composition (% dw) of standing crop of litter at the study sites Site Litter mass Litter composition: grasses, forbes, soft leaves birch leaves oak leaves pine needles C/N ratio
A
B
C
D
400
650
530
560
93.4
21.2
14.1
10.6
6.6 – – 24
78.8 – – 23
67.9 17.3 0.7 25
6.5 24.0 58.9 25
Table 2. Chemical properties of soil (and litter- 0–15 cm layer) -a, and their spatial heterogenity CV% -b. The number of samples is shown in parentheses Site
A
B
C
D
a
pH %C %N
5.5 12.91 0.538
5.6 16.72 0.727
5.1 11.92 0.477
4.2 9.90 0.396
b
litter mass (9) soil moisture (5) pH (9) C content (7)
27 5 2 21
29 7 11 21
29 7 9 47
34 18 2 24
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Based on these variables, the birch thicket B can be considered as the richest habitat, with the highest litter fall and low C/N of the litter. On the habitats Ao, Co and Do only soil moisture and pH were estimated. The species composition and abundance of enchytraeids were estimated four times a year, using 15 samples 10 cm2 in area and 15 cm deep from each site. The samples were divided into three 5-cm layers, and the animals were extracted by using the O’Connor method. Live animals were identified (Kasprzak 1986) and measured to the nearest 0.5 mm. Their biomass was calculated from the body length by using the formula w = 6.22x1.55 (Makulec 1983), where w is the fresh weight of an individual in µg, and x is the body length in mm. Shannon index H’ (log2, Krebs 1989) was used to determine the diversity of the communities. Two indices of similarity were applied: 1) Marczewski – modified Sörensen, (Kasprzak & Niedbal/ a 1981), w/a + b – w %, where w is the number of common species, and a or b are total numbers of species in the compared habitats, respectively; and 2) Morisita index (Krebs 1989), 2∑xy/∑x2 +∑y2, where x or y are proportions of successive species in the total number of individuals in respective habitats. Marczewski’s index considers only the presence of a species, thus it is sensitive to occasional species, whereas the Morisita’s index largely depends on the similarity in the dominance structure of the compared communities. The results were tested by using Student’s t- and u-test (difference in numbers, in body sizes and in proportion), correlation coefficients, and analysis of variance (difference in body sizes).
Results The structure of enchytraeid community A total of 24 enchytraeid species was recorded. Most of them were eurytopic, but only one, Cognettia sphagnetorum, was present at all sites (Table 3) and in both study years. This was a dominant species at four sites. Two other species, Acheta camerani and Enchytronia parva, were almost equally common. E. parva was found at all sites except for the mixed coniferous forest D, although according to literature data (Pilipiuk 1993) it can occur in this habitat. In 1997, the proportion of this typically not abundant species was very high (38%) in the acid, sandy part of the birch wood (site Cd). A. camerani occurred also at six sites, although at one of them, birch thicket B, its presence can be considered as accidental (it was not found in 1997). In both years this species was not found in the meadow A. Three species were found at only one site. Two of them, Cognettia glandulosa and Mesenchytraeus armatus, were present in the moist meadow A, and one, Mesenchytraeus glandulosus, in the mixed coniferous forest D which was a relatively dry site. The percentage of the species of two genera, Buchholzia sp. and Fridericia sp., decreased progressively along the main successional series and Acheta sp. increases along both series. The two areas of the Kampinos Forest where the study was conducted showed a distinctive character, probably as a consequence of rather specific soil conditions. In addition to eurytopic C. sphagnetorum, two species, Marionina argentea and B. appendiculata, were abundant in moorsh soils. In sandy soils, numbers of Henlea heleotropha were high (from moorsh soils it was recorded only once), and Enchytraeus norvegicus was found only in October but in large numbers (Table 3). The species richness of enchytraeids varied widely from 6-species communities (Do), to 19- (20 in 1997) species communities in the moist meadow A (Table 3). At
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Table 3. Species composition of enchytraeid communities in 1998. (Relative numbers %; + < 1%) Site
A
B
C
D
Ao
Bo
Do
Mesenchytraeus armatus (Lev.) Mesenchytraeus glandulosus (Lev.) Cˇernosvitoviella atrata (Bret.) Buchholzia appendiculata (Buchh.) Cognettia sphagnetorum (Vejd.) Cognettia glandulosa (Mich.) Marionina argentea (Mich.) Marionina sp. Enchytraeus buchholzi Vej Enchytraeus christenseni Niel.et Chr Enchytraeus norvegicus Abrah Fridericia bulbosa (Rosa) Fridericia striata Issel Fridericia maculata Issel Fridericia leydigi (Vejd.) Fridericia bisetosa (Lev.) Fridericia ratzeli Eis Fridericia sp. Enchytronia parva Niel.et Christ. Henlea perpusilla Friend Henlea heleotropha Steph Henlea nasuta (Eis) Henlea ventriculosa (d’Udek.) Acheta camerani Cog. Acheta bohemica (Vejd.) Acheta eiseni Vejd.
2 – 10 12 19 2 28 1 1 3 – 2 – 4 2 2 2 – 1 5 + 3 1 – – –
– – 1 9 4 – 37 6 5 8 – 3 – 3 3 3 3 – 3 5 – 4 3 + – –
– – – 9 68 – 3 + – 1 – – – 1 1 1 1 – 6 – – 3 1 5 – 1
– + – + 55 – + – – – – – + – – – – – – – – – – 27 4 14
– – – – 58 – – – – – 4 – – + – + – + 7 – 21 – – 2 – 8
– – – – 27 – – – – – 10 – – – + 2 – + 1 – 51 – – 2 – 7
– – – 3 76 – – – – – – – – – – – – – + – 1 – – 10 – 10
Total number of identified animals Total number of species H’
522 402 603 694 263 251 236 19 17 14 8 9 9 6 3.34* 3.33 1.89 1.62 1.82* 2.00 1.24
* Not significant difference between neighbouring site. The other differences were significant at p = 0.01
this site, the index of species diversity reached a maximum value of 3.36 in 1997. In both years and in both sequences, the most diverse enchytraeid communities occurred in habitats covered with herbaceous plants (A and Ao), whereas the least diverse communities occurred in both forest habitats, mixed coniferous forest D and planted pine forest Do. A comparison of species diversity (Table 3) with habitat heterogenity (Table 2) of the four main habitats yielded unexpected results. No relationship was found between the species richness of enchytraeid communities and the range of variation in chemical properties (pH and N content in soil) or in physical properties (litter fall and mois-
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ture). Nor can a relationship be expected between the species richness and soil fertility because the latter decreased in one successional series and increased in the other series. It seems that the simplification of the enchytraeid community is related to decreasing soil pH. Linear correlation between this factor and the number of enchytraeid species (Fig.1) was r = 0.86, and for the Shannon index r = 0.80, both these values being significant at p < 0.02. The regression line was fitted according to the formula Y = 8.4X – 29 and y = 1.3X – 4.4 where X-soil pH, Y-number of enchytraeid species, y-diversity H’. Similarity of enchytraeid communities The enchytraeid communities of different sites were considered to be similar if their similarity indices approximated to for the same habitat in two successive years. The values of the Morisita index for between-year comparisons ranged from 0.94 for forest D to 0.88 for meadow A. The range of the Marczewski index was from 53 for forest D to 88 for birch wood C/Cd. Accepted similarity limit was 0,70 for the Morisita and 50 for the Marczewski index. According to the Morisita index the following pairs of sites were similar: D/Do, A/B, and, a little less, Ao/Bo and Ao/D (Table 4a). According to the Marczewski index all sites on sandy soils were similar (Ao, Bo, Do, and the old field and birch plantation even identical), and also A/B and B/C (Table 4b). With respect to the dominance structure and species composition, the similarity was confirmed for two habitat pairs, A/B and Ao/Bo, that is, between the habitat with herbaceous plants and young, 10- or 30-year-old birch thicket. These two initial stages of succession were similar, and then their similarity was declining with time (e.g. meadow to birch thicket A/B 0.85, meadow to birch wood A/C 0.48, meadow to coniferous forest A/D 0.39). Low similarity indices of enchytraeid communities were obtained for the same plant communities at sites with differential substrate. The Morisita index for sites
Fig. 1. Relationship between the soil pH and the number of enchytraeid species. Sites: meadow A, birch thicket B, birch wood C, coniferous forest D, old field Ao birch plantation Bo, pine wood Do
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Table 4. Similarity of enchytraeid communities in the Morisita (a) and Marczewski (b) indices for the successional sites (bold – similar communities) a – Morisita coefficient, 1998 year Site
B
C
D
Ao
Bo
Do
A B C D Ao Bo
0.85
0.48 0.15
0.39 0.09 0.45
0.41 0.09 0.52 0.79
0.21 0.05 0.44 0.43 0.74
0.28 0.09 0.52 0.92 0.46 0.46
b – Marczewski coefficient, 1998 year Site
B
C
D
Ao
Bo
Do
A B C D Ao Bo
80
50 63
12 19 29
30 31 35 31
17 25 28 30 100
19 21 33 40 55 55
C/Cd (that is, for parts of birch wood on moorsh and on more sandy soils) was 0.56, and for sites Bo/Bom (that is, for parts of the birch plantation on sandy and on moist, gleyed soils) was 0.39. Numbers and biomass of enchytraeids Numbers of enchytraeids at different sites showed a moderate variation by a factor of no more than 3.3 (Fig. 2). At most sites (B, C, A, Do), mean numbers were not high, 14–27 103 individuals m-2. They were abundant only at sites D and Ao, 51 103 indiv. m-2 and 43 103 indiv. m-2, respectively. Both these sites – the mixed coniferous forest D and old field Ao are considered to be the least fertile in their successional series. No rank correlation was found between soil fertility and enchytraeid numbers (Spearman test, r = 0.4). A negative correlation between the soil pH and enchytraeid numbers was significant (r = –0.81, p = 0.05). Even less differences between sites were found in the biomass of enchytraeids, as estimated from mean body sizes at each site. Differences in body sizes were statistically significant (p < 0.01). In 1997 enchytraeid biomass at different sites differed by a factor of 2.4 and in 1998 by a factor of 1.7, the order of sites remaining the same (Fig. 2). Numbers and biomass of enchytraeids were generally a little lower in 1997, which was more humid and cool than 1998 (rather moist habitats were compared and the sum of precipitation was not fully reflected in soil moisture). Spatial variation in enchytraeid numbers was very high. At site D in 1997, the value of CV reached even 149%. Some similarity exists between this variation and spatial heterogenity of the sites, but not obvious. In both, 1997 and 1998, the highest
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Fig. 2. Population density (a) and biomass (b) of enchytraeids at the study sites. Density N x 103 m-2. Sites: meadow A, birch thicket B, birch wood C, coniferous forest D, old field Ao birch plantation Bo, pine wood Do. * not significant differences in numbers between neighbouring sites. The other differencs were significant at p = 0.01
variation in numbers occurred at site D, that is, in the habitat where physical factors were most diverse (Table 2). The lowest variation (CV 80% and 94% in two years, respectively) was on the meadow A with least variable physical factors. Vertical distribution of enchytraeids Vertical distribution of enchytraeids varied and it seems to reflect soil moisture. The upper soil layer (0–5 cm) of the moist meadow A was inhabited by 89% of enchytraeids in 1997 and 91% in the year 1998. These values ranged from 59% in May to 97% in July 1997. In the drier coniferous forest D, the upper soil layer was inhabited by 62% of enchytraeids in 1997 and 74% in 1998. The range was from 39% in May 1997 to 85% in May 1998. All soil animals most readily occupy the upper layer, rich in food and oxygen. In this layer there were 68 to 90% of C. sphagnetorum but only 51 to 69% Acheta sp. (Table 5). This implies that Acheta not always can find place in the preferred upper layer and that these two genera divide the soil space between themselves.
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Table 5. Relative numbers of C. sphagnetorum and Acheta sp. in the upper soil layer (0–5 cm) (%) Site
B
C*
D
Do
C. sphagnetorum Acheta sp. Both
85 51 66
68 69 69
88 58 74
90 67 96
* Not significant differences in distribution of species. The other differences in depth distributions were significant at p = 0.01
Cognettia sphagnetorum Numbers of this dominant species varied from 600 indiv. m-2 to 28 x 103 indiv. m-2 and were negatively correlated with soil pH (r = –0.96, p = 0.02). The regression line was fitted according to the formula y = 112.0 – 19.8x where x-pH, y- number of C. Sphagnetorum x 103 m-2. The largest population in the mixed coniferous forest D, was infected with gregarine (3.3% of the population); a parasite found in addition only in one individual from meadow A. The frequency distribution of the size of C. sphagnetorum showed site-related differences. The mean body size varied from 3.6 mm in the mixed coniferous forest D to 5.1 in the meadow A. The largest individuals were in the class of 10–11mm at sites D and Do, and in the class of 14.5–15.5 mm in the meadow A (Fig. 3). Statistically significant differences were found in the distribution of body sizes between the meadow and the birch wood (A and C) and the forests and the old field (D, Do, Ao), whereas differences within this two groups were statistical not significant (analysis of variance). Variation in the mean body size can reflect the frequency of divisions. This species reproduces through architomy – the more frequent reproduction (divisions), the smaller the mean individual and the lower the size range. These size distributions were also related to soil pH. The correlation coefficient between pH and the mean size of an individual was week r = 0.84, p = 0.03. The regression line was fitted according to the formula Y = 1.4 + 1.2 pH. As numbers of C. sphagnetorum, like the number of species in the enchytraeid community, both were correlated with soil pH, they were expected to be correlated with each other. This linear, negative correlation, however, was statistical not significant (r = –0.8, p = 0.06).
Discussion A high similarity was found in enchytraeid communities between the meadow and the birch thicket (Morisita index 0.85). Much larger differences occurred among patches that differed in soil type within the birch plantation (Morisita index 0.39) and within the birch wood (0.56). Thus, enchytraeid communities were more sensitive to soil variation within the same plant communities than to successional changes in the vegetation that occurred over several decades (20–13 years).
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Fig. 3. Frequency distribution of body sizes of C. sphagnetorum at the study sites. Mean body size category (mm), number in %, Ao – old field, Do – pine wood, D – mixed coniferous forest. A – meadow, C – birch wood. a – high density, b – low density
In the Czech successional series (Pizˇ l 1999) old field and thicket were not similar but the soil in thicket was without herbaceus layer, and hence some differences in results. The present data show that the number of enchytraeid species and their diversity decrease with plant succession. The number of species more often increases than decreases in the succession of soil organisms (Trojan et al. 1994; Kajak & Wasilewska 1997). Chalupsky (1994) described an increase in the number of enchytraeids in fertile brown soil. A different process occurs in the succession leading to coniferous forests. A decrease in the number of species during such a succession was also described by Pilipiuk 1995. The decline in species richness in relation to decrease in soil pH has been reported in other studies (Standen 1984). In the present study, soil pH can be correlated with almost all parameters of the enchytraeid community, specifically with the number of species, abundance of the dominant species, and with the mean body size of it. The range of pH variation at the study sites (from 4.2 to 5.6) did appear to exceed the tolerance of most enchytraeid species, including C. sphagnetorum (Healy 1980). The soil pH is related to the composition of soil microflora. The importance of fungi (their proportion in microflora) increases with soil acidity (Wallwork 1970). Moreover, the
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ratio of fungal to bacterial biomass increases with plant succession (Ohtonen et al. 1999). C. sphagnetorum, like Acheta, is saprofagous but shows preference for fungi (Kasprzak 1986; Hedlund & Augustsson 1995). The correlation between pH and the abundance of the dominant species may therefore be as a consequence of the availability of fungal food resources. C. sphagnetorum reproduces through architomy. This enables a rapid reproduction when food becomes available. That was important in the habitat where physical factor were diverse (e.g. D). This plasticity of Cognetia may confer advantage in competition with other species. Space allocation between Cognetia and Acheta may be a result of competitive exclusion of the latter from the upper soil layers, rather than a preference of Acheta for deeper layers (Didden & de Fluiter 1998). Nor does the correlation between the number of species and soil acidity seem to be an effect of the absence of species with tolerance of low pH (compare Healy 1980). Rather the relationship may be ascribed to competitive exclusion other species by C. sphagnetorum. The following scenario is suggested for the events described. A decrease (and not increase as in other groups) of species richness of enchytraeids in these successional stages occurred as the consequence of soil acidification by coniferous trees. This acidification, and also plant succession, may enhance the development of fungal biomass, which in turn promotes the fungivorous (saprophagous) enchytraeid C. sphagnetorum. Probably this species was capable of reducing populations of other species and simplifying the diversity of the enchytraeid community.
Acknowledgements I wish to thank J. Kotowska and A. Wasil/kowska, for phytosociological analysis of the study sites. I also thank I. Pilipiuk for her help with identifying enchytraeids and J. Górka for making available maps of the Kampinos National Park.
References Begon, M., Harper, J. R., Towsend, C. R. (1990) Ecology. 2nd ed. Blackwell Scientific Publications. Boston, Oxford, London, pp. 945. Chalupsky´, J. (1994) Enchytraeids (Annelida, Enchytraeidae) in a secondary plant succession on a brown soil. European Journal of Soil Biology 30, 169–175. Didden, W. A. M., de Fluiter, R. (1998) Dynamics and stratification of Enchytraeidae in the organic layer of a Scots pine forest. Biology Fertility Soils 26, 305–312. Frouz, J. (1997) Changes in communities of soil dwelling dipteran larvae during secondary succession in abandoned fields. European Journal of Soil Biology 33, 57–65. Healy, B. (1980) Distribution of terrestrial Enchytraeidae in Ireland. Pedobiologia 20, 159–175. Hedlund, K., Augustsson, A. (1995) Effects of enchytraeidae grazing on fungal growth and respiration. Soil Biology and Biochemistry 27, 905–909. Kajak, A., Wasilewska, L. (1997) Changes in meadow ecosystems as consequence of secondary succession and plant diversity (synthesis of research). Ekologia Polska 45, 839–859. Kasprzak, K. (1986) Ska˛poszczety wodne i glebowe II. Klucze do oznaczania bezkre˛gowców Polski T.V. [Soil and water Oligocheta. II. Key to identification invertebrates of Poland V.]. PWN Warszawa, pp. 366.
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