Soil fauna of a reclaimed lignite open-cast mine of the Rhineland: improvement of soil quality by surface pattern

Ecological Engineering 17 (2001) 307– 322

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Soil fauna of a reclaimed lignite open-cast mine of the Rhineland: improvement of soil quality by surface pattern Werner Topp a,*, Markus Simon a, Guido Kautz a, Ulf Dworschak b, Frank Nicolini a, Stephanie Pru¨ckner a a

Department of Zoology, Terrestrial Ecology, Uni6ersity of Cologne, Weyertal 119, D-50923 Cologne, Germany b Rheinbraun AG, Forstamt, Friedrich-Ebert-Str. 104, D-50374 Erftstadt, Germany Accepted 19 August 2000

Abstract Reclaimed lignite open-cast mine areas in the Rhineland are covered by a mixture of loess and sand deposits containing organic material that originates from the upper quartary soil which has been taken from the front of the mining path. Consequently, the soil fauna that has established itself on the reclaimed open-cast mine areas may result from the primary succession and also from species that are carried to the dumping mines and are able to survive the dumping process. The reclaimed landscape consists of a regular structural pattern of crests and troughs. The troughs provide appropriate habitats for establishing a rich and diverse fauna with higher densities of almost all animal groups investigated, with enhanced microbial activity and higher values of available macronutrients. In terms of plant growth, the physical and chemical conditions found in the troughs exceeded the conditions found on the crests. From laboratory studies we made the following conclusions: (1) environmental conditions in the troughs were improved not only by erosion, but additionally by the soil fauna that directly enhanced microbial activity and indirectly increased the availability of macronutrients; (2) soil animals improved soil quality by increasing the pH-values, increasing the ammonium–nitrogen content and decreasing the content of aluminium ions; and (3) a multiple-species system is able to improve soil quality more effectively than a single-species system. © 2001 Elsevier Science B.V. All rights reserved. Keywords: Open-cast mine; Reclamation; Afforestation; Soil fauna; Microorganisms; Macronutrients

1. Introduction In the Rhineland the established restoration practices for reclaiming lignite open-cast mines are primarily aimed at coverage of surface mines. * Corresponding author. Tel.: + 49-221-4703152; fax: +49221-4705038. E-mail address: [email protected] (W. Topp).

An optimal substrate for plant growth following the process of dumping is either pure loess or a mixture of subsurface loess and sand (‘Forstkies’) from the quartary epoch layer (Kunde and Mu¨llensiefen, 1998). Following the practices derived from the hard coal mines, the overburden was initially deposited as a regular hill with slopes and benches. The ‘Sophienho¨he’ is one of these artificial overburden

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dumps with a height of about 200 m above ground level. The following question arose: how do we create a landscape which looks more natural? Several experiences lead to a modified dumping technique (Fig. 1), omitting the final levelling process and compressing the subsurface substrate, particularly within areas where afforestation took place. After dumping is finished, afforestation is carried out within the next planting season using tree species from natural ecosystems in that geographic region (Dilla and Mo¨hlenbruch, 1998; Wolf, 1998). Afforestation is completed soon after dumping in order to minimize degradation by natural processes and to allow the new land to be used as soon as possible. New land uses include recreation areas, almost natural forests that support the development of wildlife and commercial forests. Cover plants are added to optimize tree growth. Thus, the principles of Higgs (1997), e.g. a restored ecosystem must strongly resemble the structure and composition of the so-called natural ecosystem, were not strictly applied even when the goal of restoration as demanded in the Rhineland is to create a self-sustaining rehabilitation area (cf. Majer, 1989).

For our studies the following questions were addressed: 1. Which soil animals settle the reclaimed and afforested open-cast mines? 2. What are their densities? 3. How does a surface pattern with crests and troughs influence faunal diversity? 4. Does the soil fauna improve soil properties during the initial phase of succession?

2. Material and methods The investigations were carried out in a lignite open-cast mine of the Rhineland. The studies concentrated on 3- and 7-year-old afforested sites which were covered by a mixture of sand and loess (‘Forstkies’) to a thickness of at least 4 m. The coverage was not leveled. The surfaces of all sites were formed by a modified dumping technique that produced crests and troughs, differing in height by about 80 cm, with a distance of about 150 cm between crests. The characteristics of the chosen sites were as follows:

Fig. 1. Dumping of a mixed soil which contains sand, loess and organic material as coverage for reclaimable areas. The surface of the reclaimable areas in which afforestation took place was not leveled and retains a structured pattern with crests and troughs which improves self-sustaining rehabilitation (photograph courtesy of Rheinbraun AG).

W. Topp et al. / Ecological Engineering 17 (2001) 307–322

I. Age: 3 years. Soil: 70% sand, pH 5.39 0.5. Plantation: Quercus robur, Tilia cordata, Sorbus aucuparia, Prunus a6ium covered by Alnus glutinosa. II. Age: 7 years. Soil: 70% sand, pH 6.090.2. Plantation: Q. robur, T. cordata covered by A. glutinosa. III. Age: 7 years. Soil: 70% sand, pH 4.790.3. Plantation: Q. robur, T. cordata covered by Populus sp. IV. Age: 7 years. Soil: characterized by loess,B 35% sand, pH 7.290.1. Plantation: Q. robur, T. cordata covered by A. glutinosa. The properties of crests and troughs of each site were measured. The sites were selected based on the existence of parameters that could be responsible for differences between sites. The parameters were: (1) the age of the reclaimed sites (I vs. II); (2) the species used as cover-plants (II vs. III); and (3) the texture of the coverage (II vs. IV). Physical and chemical parameters of the soil from the study sites were taken every second month from April to December 1997. Soil moisture and dry weight of leaf litter were measured gravimetrically. The organic carbon content of soil was determined by a total carbon analyzer (Stro¨hlein Instruments); total nitrogen was measured by a Kjeldahl apparatus; nitrate — N, ammonium — N and phosphate — P were extracted according to Steubing and Fangmeier (1992); for further macronutrients we used the methods described by Hornburg et al. (1995). The soil biota were obtained by different methods which were appropriate for each group. Earthworms were extracted by dilute formalin (0.2%) — two infusions within 30 min, 5 l each, applied to a 1/4 m2 sample area (n = 12 for each site) in December 1997. The litter and vegetation cover were removed before the infusion of formalin, and animals present in this material were extracted over a 3-week period using Tullgrenfunnels. Enchytraeidae were obtained by wet extraction from soil cores=55.4 cm2, 4 cm deep, n=16 (O’Connor, 1962, modified by Koehler, 1993). Macroarthropods such as Coleoptera and Diptera adults, as well as Isopoda and Diplopoda were obtained by soil photo-eclectors (Funke,

309

1971) with a surface area of 1/4 m2 (n=8 for each site). The photo-eclectors remained on the chosen sites for the whole season (May –October). Diptera larvae were extracted by a modified flotation apparatus as described by Healey and Russel-Smith (1970) and Heynen (1990). Collembola were sampled by dry extraction (MacFadyen, 1962, modified by Koehler, 1993). Extractions were taken every second month from April to December 1997. The area of soil cores for each arthropod group and the number of replicate samples for each site were as follows: Diptera larvae: soil core= 200 cm2, n=20, Collembola: soil core= 31.2 cm2, n=16. Depth of soil cores was 4 cm. Microbial activity (n= 12) was measured by CO2 released after an incubation period in permanent darkness (Anderson, 1989). The moisture content of the soil samples was first adjusted to 50% water potential (n=6). Microbial biomass (n= 24) was obtained by a fumigation-extraction method (Vance et al., 1987). Both microbial parameters were carried out with a total carbon analyzer. Feeding experiments were carried out in containers with a surface area of 55 cm2. These containers were deposited under constant laboratory conditions of 15°C and a light/dark cycle of 12h/12h. A loamy sand (75% sand, 19% silt, 6% clay) was used as a substrate and adjusted to 50% water potential. One earthworm and five pre-adult Isopoda were fed separately or together with 2.5 g leaf litter per container. For each trial, we used seven replicates. The experiments lasted 8 weeks and five measurements were taken at fixed intervals each fortnight. The parameters of litter disappearance and content of macronutrients were calculated by y=ae − Kt + b(a, b=const., K is the rate of increase, t is the duration of experiments). Activities of micro-organism were fitted to sigmoidal response curves. The curve fitting was done using Prism® 2.01. The data sets presented in Tables 3 and 4 are expressed as means per square meter to allow comparisons with data from the literature. Because the data obtained from the different treatments were not normally distributed, data are also represented as median9median absolute devia-

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Table 1 Organic litter layer and chemical properties of soil (median 9 MAD) for different sites (see Section 2) of a lignite open-cast mine in the Rhinelanda Sites

I

II

III

IV

Crest/trough

c

t

c

t

c

t

c

t

Org. litter layer (g/m2) Corg (%) Nt (mg/g) NH+ 4 –N (mg/g) NO− 3 –N (mg/g) PO3− 4 –P (mg/g)

32 9 12

32 9 8

1889 76**

900 920

1169 12**

284 9 144

1529 44*

3529 124

0.41 90.06*** 0.68 90.18 0.40 9 0.03*** 0.60 9 0.08 0.8 9 0.3 0.5 9 0.2

0.72 9 0.15*** 2.52 9 0.97 0.61 9 0.14*** 1.83 9 0.53 0.9 9 0.4*** 3.6 9 0.3

0.46 9 0.08*** 1.30 9 0.28 0.41 9 0.03*** 0.97 9 0.11 1.1 90.2 1.29 0.3

1.26 9 0.26*** 2.69 9 0.73 1.05 9 0.14*** 1.98 9 0.19 2.2 9 0.4*** 2.8 9 0.6

0.9 90.9**

2.3 91.7

3.6 9 0.9***

14.5 9 6.6

0.5 9 0.5

0.69 0.6

6.8 9 0.9***

15.8 9 3.4

7.0 9 0.9***

8.9 9 1.1

5.4 9 0.8***

10.5 9 0.9

4.5 90.5***

9.9 9 1.6

15.1 9 2.9***

27.2 9 3.0

a

Significant differences between crests (c) and troughs (t) within the sites are indicated (n = 32): *PB0.05, **PB0.01, ***PB0.001.

tion (MAD). Statistical tests were generally carried out using non-parametric tests. Significance of differences was tested using the Mann – Whitney U-test. Laboratory tests were examined by Friedman’s test following the Wilcoxon test. ANOVA is the most straightforward technique for evaluating the extent to which site characteristics (age of reclaimed area, cover plant, texture) influence species distribution. When variances were heterogeneous (Cochran, P B0.1) even after transformation, only those factors with P B0.001 were regarded (Sachs, 1992). SPSS® procedures were used for all statistical tests.

3. Results

3.1. The soil en6ironment The coverage of loess and sand used for recultivation exhibits a thickness of at least 4 m and contains a sufficient content of some macronutrients for tree growth. In the first year after dumping, the content of available potassium was on average 50 mg/kg, for magnesium, average values of between 80 and 100 mg/kg were obtained, and the content of calcium within the loess layer

mostly surpassed the requirements for plant growth (Dumbeck, 1995). Limitations in the first phase after recultivation were related to levels of carbon, nitrogen and phosphorus. We found an accumulation of organic carbon, total nitrogen, nitrate nitrogen and phosphorus in the troughs of all experimental sites (Table 1) when compared to the crests. Significant differences (P B 0.05) between crests and troughs were found for most macronutrients (Simon and Topp, 1999). In the troughs of 7-yearold sites the content of available phosphorus and all other nutrients reached (sites II and III) and surpassed (site IV, loess soil with a minor content of sand particles) the limitations for plant growth (Wilde, 1962; Schlichting et al., 1995). Analyses of variances (two-way ANOVA) revealed that the chemical properties were largely explained by influences of the soil relief (R 2 = 0.19 –0.56). The texture, the age of sites after recultivation and the influence of cover tree species were of lesser importance (Table 2). Measurements of soil water content by the gravimetric method revealed differences in field capacity within and between sites. Fig. 2 shows the average values of the actual water content as found during the year. Differences were signifi-

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311

Table 2 Two-way analysis of variance for data on organic carbon (Corg), nitrate — N and phosphate — Pa Corg

Site I 6s. II Main factors Age Relief Interaction Model Site II 6s. III Main factors Cover plant Relief Interaction Model Site II 6s. IV Main factors Texture Relief Interaction Model

nitrate — N

phosphate — P

F

R2

110.5 125.2 51.8

0.27*** 0.30*** 0.13*** 0.70

48.8 68.7 26.0

0.20*** 0.29*** 0.11*** 0.60

0.9 209.0 52.6

52.7 180.0 22.3

0.14*** 0.48*** 0.06*** 0.67

130.0 64.9 57.0

0.37*** 0.19*** 0.16*** 0.72

1.8 318.9 6.5

4.7 144.3 3.7

0.52*** 0.55

R2

F

0.2 124.8 3.7

0.56*** 0.58

F

R2

0.46*** 0.11*** 0.57

0.61*** 0.63

1144.8 480.7 111.8

0.59*** 0.25*** 0.06*** 0.90

a Factors were soil relief (crest and trough), age after recultivation (3 and 7 years), cover plant (alder and poplar) and soil texture (sand and loess). Significance values are indicated (***PB0.001).

cant between crests and troughs of each site and also between most sites.

3.2. Soil macrofauna The organic material of the substrate can contain eggs, cocoons of earthworms, juveniles and even adult soil animals that were transported to the reclaimed land. Another source that facilitates the initial invasion of species in reclaimed areas may be the soil material which remains attached to the roots of those plants used for afforestation. The texture of the deposits and the quality of organic material are the main influences on animal survival at the beginning of succession (Heuser and Topp, 1989). Earthworms (Table 3), including the deep burrowing, surface-casting species Lumbricus terrestris, were already found in such high numbers at the 3-year-old site (Table 3, site I) that it is hard to believe they originated exclusively through invasion and multiplication within reclaimed areas. Population densities of earthworms in the 7-year-

old sites is possibly even higher than in central European broad leafed forests (Zajonc, 1971). We assume that colonization of rehabilitated opencast surface mines, at least by earthworms, may be influenced by the species density and composition of animals which reach these dumping areas

Fig. 2. Actual water content of soil (median 9MAD, n =25) measured from April to December 1997. Differences between crests (c) and troughs (t) of sites I – IV (see Section 2) are indicated, *P B0.05, ***PB0.001.

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Table 3 Macrofauna (individuals/m2, mean values) of soil for different sites (see Section 2) of a lignite open-cast mine in the Rhineland Sites

I

II

Crest/trough

c

t

c

t

c

t

c

t

Lumbricidae, total Dendrobaena octaedra Dendrodrilus rubidus Lumbricus castaneus Lumbricus rubellus Lumbricus terrestris Lumbricus n. det. (juv.) Allolobophora chlorotica Aporrectodea caliginosa Diplopoda, total Iulus scandina6ius Chordeuma sil6estre Polydesmus angustus Isopoda (Trachelipus rathkii )

251 123 – – 31 1 92 – 4 4 4 – – –

457 258 1 2 25 8 163 – 1 22 16 – 6 20

275 112 33 29 7 2 91 1 – 65 31 14 20 –

521 131 67 64 16 5 229 9 1 142 82 22 38 –

103 2 24 – 25 – 53 – – 11 7 3 1 2

125 3 33 – 25 – 65 – – 108 72 13 23 1

358 177 13 25 5 15 118 6 – 205 69 59 77 40

723 303 43 63 12 16 278 7 – 220 46 83 91 40

alive and find appropriate places to survive. Our studies revealed a correlation between the number of earthworms and the biomass of dry weight of the litter layer (rs = 0.43, P = 0.003, n = 48). In addition, a correlation between earthworms and microbial activity was found (rs =0.71, P = 0.05, n=8). Isopoda were mostly represented by Trachelipus rathkii. Diplopoda (Table 3), represented by Iulus scandina6ius, Chordeuma sil6estre and Polydesmus angustus, confirmed the assumption that the number of individuals was correlated with the biomass of dry weight of the litter layer (rs =0.77, P = 0.027, n=8). Earlier investigations have shown that the isopod T. rathkii is a characteristic species which occurs during the first phase of succession but which fails in forests. The millipedes mentioned belong to a list of species which usually predominate within rehabilitated areas older than 10 years (Neumann, 1971).

3.3. Soil mesofauna Among soil mesofauna, highest densities were observed for Collembola and Enchytraeidae. For Collembola, significant differences (P B 0.05) between crests and troughs were shown for all sites except for loess site (IV). Density of Enchytraei-

III

IV

dae revealed significant differences (P B 0.05) between crests and troughs for sites II and IV with the highest numbers in the troughs (Table 4). Dipteran larvae were also found mostly within the troughs. However, differences in densities between crests and troughs were not significant at sites I and III. Significant differences were found between crests and troughs for site II (P B 0.001) and site IV (PB 0.05). In contrast to the number of individuals, the biomass values of Diptera revealed significant differences for all sites (not indicated). Among families of Diptera, the microphytophageous and saprophageous species of Chironomidae and the predaceous species of Dolichopodidae characterized the 3-year-old sites. Individuals of these families (PB 0.001 and P B 0.05) predominated on the crests at 7-year-old sites, as observed at site III. The troughs of all sites were characterized by Sciaridae. Significant differences between crests and troughs (P B 0.05) occurred for all sites except for loess site IV. The troughs of the 7-year-old sites which are characterized by sandy material (sites II and III) were additionally settled by the predaceous Empididae. The differences in density between crests and troughs were highly significant (PB 0.001). Two-way analysis of variance revealed that the greatest influence on distribution of Diptera (to-

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313

tal) and most families of Diptera was the relief (crest and trough). Age of sites had the greatest influence on the distribution pattern of Tipulidae and Limoniidae. Limoniidae were additionally influenced by the cover-tree species, whereas the distribution pattern of Empididae depended on all factors investigated (Table 5).

C-mineralization, calculated as microbial activity per quantity of organic carbon, gave almost the same values for crests and troughs and also between sites. Because we found a significant increase (PB 0.001) of organic carbon in the troughs of all sites in comparison to crests (Table 1), this means that generally higher rates of Cmineralization occurs within the troughs.

3.4. Soil microflora

3.5. Epigeic insects

At all sites, the microbial activity measured in the troughs was significantly higher (P B 0.001) than on the crests (Fig. 3). Microbial activity seemed to be mainly influenced by the litter layer and the effect of bioturbation by soil animals. The correlation between microbial activity and the content of organic carbon within the soil layer was highly significant (rs =0.87, P B0.001, n = 240). These studies also revealed that the microbial biomass was always higher in the troughs than on the crests. The correlation between microbial activity and microbial biomass was rs =0.86 (PB 0.001, n=240). Consequently, the specific metabolism (microbial activity/microbial biomass) calculated for crests and troughs was almost the same when the 3-year-old site (I) and the 7-yearold loess site (IV) were compared. Specific metabolism in the troughs of the 7-year-old sandy sites (II and III) was slightly higher than on the crests (PB 0.05).

Among the insects collected by photo-eclectors, the Coleoptera and Diptera revealed the highest densities. Individuals of both orders were more common within the troughs than on the crests (Table 6). These differences were usually not significant for the beetles. However, except for the relief of the loess site (IV), they were highly significant (PB 0.001) for the dipterans. The ground beetles (Carabidae) were found in the highest densities within the troughs of the 3-yearold site. Here the most common species were Bradycellus 6erbasci and Harpalus rufipes. Calathus melanocephalus predominated on the crests. The troughs of the loess site (IV) were characterized by Trechus obtusus, Bembidion obtusum and Pterostichus strenuus, whereas the crests of the same site were mostly inhabited by C. melanocephalus. Thus, the differences which were significant (PB 0.05 –0.001) between trough and crest for sites I–III would have been even more

Table 4 Mesofauna (individuals/m2, mean values) of subsurface coverage for different sites (see Section 2) of a lignite open-cast mine in the Rhineland Sites

I

II

III

IV

Crest/trough

c

t

c

t

c

t

c

t

Oligochaeta, Enchytraeidae Collembola Diptera larvae, total Tipulidae Limoniidae Chironomidae Sciaridae Cecidomyidae Empididae Dolichopodidae

714 7555 942 19 1 470 60 216 9 110

489 12 127 1556 9 16 909 250 277 11 31

147 1476 446 58 34 12 81 179 10 12

387 2238 1838 205 175 7 258 336 61 5

3876 2695 943 56 46 274 207 120 59 102

3981 7475 1256 40 3 22 584 320 165 37

966 8117 717 22 21 76 182 231 67 14

2244 7411 1372 80 120 26 550 291 77 5

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314

Table 5 Two-way analysis of variance with data on the abundance of selected groups of Diptera larvaea Diptera

Site I 6s. II Main factors Age Relief Interaction Model Site II 6s. III Main factors Cover plant Relief Interaction Model Site II 6s. IV Main factors Texture Relief Interaction Model

Tipulidae

Limoniidae

Empididae

F

R2

F

R2

F

R2

F

R2

4.3 27.6 6.3

50.2 3.3 8.1

0.51***

0.37***

87.7 32.6 7.5

0.54*** 0.20***

13.6 17.4 10.1

0.18*** 0.23***

0.51

2.6 27.2 8.5

0.37***

0.63

10.1 3.7 7.4

0.52

0.1 26.5 3.0

0.40***

0.78

38.9 0.7 45.9 0.37

13.1 18.5 0.0

0.45

0.19*** 0.27*** 0.47

5.5 27.8 0.5

0.32*** 0.38*** 0.70

0.40*** 0.48

0.53

17.6 35.1 0.1

0.20*** 0.39*** 0.59

17.7 17.6 9.8

0.22*** 0.22*** 0.56

a Factors were soil relief (crest and trough), age after recultivation (3 and 7 years), cover plant (alder and poplar) and soil texture (sand and loess). Significance values are indicated (***PB0.001).

pronounced if the differentiations had been made on the species rather than at the family level. Significant differences in the densities of rove beetles (Staphylinidae) between troughs and crests were found only between sites I and III. Aleochara sparsa was most common within the troughs of site I. This species was not present on the crests of the same site. However, this species, which is an endoparasite on dipteran larvae, characterized all 7-year-old sites. The troughs of site III additionally revealed a high abundance of the polyphageous Omalium ri6ulare and Atheta triangulum. The mycetophageous Lathridiidae preferred the moist troughs of the loess site (IV). The introduced Lathridius bifasciatus (n =78) was found almost exclusively in this biotope. The congeneric L. nodifer, which was even more common (n = 195) within the troughs of site I, showed a much wider distribution pattern and was found, albeit sometimes in low numbers, within each sample area. The distribution pattern of Lathridiidae was highly aggregated. Despite the high differences found for the total numbers (Table 6), the densi-

ties for the crests and troughs were never significantly different (P\ 0.05). The abundance of Glischrochilus hortensis mainly influenced the high densities found within the Nitidulidae. G. hortensis preferred the crests of

Fig. 3. Microbial activity of soil (median 9 MAD, n =30) as measured from April to December 1997. Differences between crests (c) and troughs (t) of sites I – IV (see Section 2) are indicated, ***PB 0.001.

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315

Table 6 Density (individuals/m2, mean values) of Coleoptera, Diptera (adults) and of selected families from these orders collected by photo-eclectors Sites

I

Crest/trough

c

Coleoptera (total) Carabidae Staphylinidae Lathridiidae Cryptophagidae Nitidulidae Diptera (total) Chironomidae Sciaridae Cecidomyidae Tipuloidea Phoridae Empididae

II t

c

III t

c

IV t

c

t

218 60 28 9 13 6

426 194 102 29 0 18

257 13 116 75 29 2

328 46 160 23 16 7

384 16 104 160 14 67

365 88 178 14 6 11

690 79 360 61 18 99

940 103 305 335 35 17

262 23 60 69 4 19 1

2564 630 1406 115 7 92 45

641 8 391 65 42 26 28

4620 4 3358 122 732 66 69

1291 45 801 89 2 19 10

3908 15 2950 330 13 92 111

1212 2 555 210 23 151 45

1541 15 500 199 295 85 64

sites II and IV and exhibited higher densities within these areas (P \0.01) than within the troughs. The same significance pattern for the Diptera (total) was found for the individuals of the most common dipteran family, the Sciaridae. The Chironomidae were the most common (P \ 0.001) within the troughs of the 3-year-old sites, whereas the Tipuloidea characterized the troughs of the 7-year-old sandy site (II) and the loess site (IV) in which A. glutinosa grew as a cover-tree. The variances of the individuals of the latter family were influenced either by the age of the sites, the covertree, or the relief of the sites. This was in contrast to the results found for Diptera (total) and for Sciaridae, in which variances of individuals were mostly explained by the relief of the sites (Table 7). For Cecidomyidae (Table 6), significant differences in densities (P \0.05) were only obvious within the sandy 7-year-old site (III). Phoridae were most common within the loess site (IV); significant differences between crest and trough were revealed in the 3-year-old site (I). Using ANOVA, the main factors, relief and texture, were found to have significant influence on the occurrence of Phoridae (R 2 =0.10 – 0.11).

3.6. Functional response of soil macrofauna The soil macrofauna is known to have different effects on its environment, which could either be beneficial or detrimental (Abbott, 1989). Significant beneficial effects of soil animals on soil structure are achieved mainly by a few groups of larger soil invertebrates. In the lignite open-cast mine, the earthworms and the ants influenced the physical properties of the soil most extensively (Topp, 1999b). In particular, the burrows of the earthworms contributed to macroporosity and so increased water infiltration. Anecic species (L. terrestris) that live in burrows opening to the soil surface and feed at that surface, create almost vertical channels for effective water infiltration, even within 3-year-old sites. Additionally, the endogeic species (Allolobophora spp., Octolasion lacteum) that burrow more horizontally with intersecting networks of macropores were able to contribute significantly to the hydraulic conductivity of a saturated loess soil (Topp, 1999b). However, after an 18-week study we found no significant effect on the hydraulic conductivity by the earthworm L. rubellus, which is mostly epigeic when the soil surface of the feeding area is covered by a litter layer.

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316

The water retention capacity of a homogenized loess soil was also enhanced by earthworms. Of the soil column experiments, the epigeic L. rubellus increased the water retention capacity after 18 weeks by 1%, whereas the endogeic O. lacteum caused an increase of 3% (Skambracks et al., 1997). These results were obtained when the population density of earthworms was equivalent to 100 individuals/m2. Enhancement of the water retention capacity by earthworms may be due to an accumulation of organic material, bioturbation of the soil and/or faeces deposited within the burrows. Laboratory experiments carried out with L. rubellus, which feeds on a combination of organic matter and inorganic material, revealed evidence that ingestion rates and bioturbation were influenced by the quality of leaf litter and the texture of soil particles (Heuser and Topp, 1989). The relatively high consumption rates of soil particles by endogeic species in comparison to that of epigeic species may explain the higher increase of the water retention capacity as observed in the experiments with O. lacteum.

Additional studies were carried out to test the influence of the geophageous O. lacteum on different soil microbial parameters such as soil respiration, microbial biomass, specific respiration and mineralization of organic carbon. All of these parameters increased with earthworm density. However, the enhancement of microbial parameters by earthworms was also dependent on soil texture. A soil substrate that was characterized by a low percentage of loess gave a higher increase in the microbial parameters of the soil than did a soil substrate characterized by a high percentage of loess. The latter showed higher initial values of microbial activity, even when no earthworms inhabited the soil (Topp, 1999b). Similarly, the isopod Porcellio scaber enhanced the recovery of microbial communities of either substrates (Kautz and Topp, 2000). In further laboratory studies, we used a loamy sand as a substrate and a litter of Q. robur or A. glutinosa or both simultaneously as nutrition for the saprophageous earthworm L. rubellus and for the saprophagheous isopod P. scaber. In addi-

Table 7 Two-way analysis of variance with data on the abundance of selected groups of epigeic arthropodsa Carabidae

Site I 6s. II Main factors Age Relief Interaction Model Site II 6s. III Main factors Cover plant Relief Interaction Model Site II 6s. IV Main factors Texture Relief Interaction Model

Diptera

Sciaridae

Tipulidae

F

R2

F

R2

F

R2

F

R2

30.1 29.1 1.5

0.20*** 0.19***

3.0 61.6 0.4

8.1 37.9 0.5

0.27***

16.2 4.8 4.4

0.14***

0.39***

0.40

0.4 18.8 0.0

0.17***

0.41

0.0 35.8 0.0

0.17

11.9 5.1 3.0

0.11***

0.18

0.28***

0.34

0.8 36.6 1.0

0.28

1.0 14.3 9.2

0.12*** 0.20

0.28***

0.22

14.4 5.8 3.3

0.28

0.5 11.3 15.5

0.09*** 0.13*** 0.24

0.12***

0.20

0.9 11.9 0.0

0.11*** 0.12

a Factors were soil relief (crest and trough), age after recultivation (3 and 7 years), cover plant (alder and poplar) and soil texture (sand and loess). Significance values are indicated (***PB0.001).

W. Topp et al. / Ecological Engineering 17 (2001) 307–322

tional experiments both saprophageous species were fed together. Finally, we tested the influence of both invertebrates separately and together on litter disappearance, microbial parameters and soil chemical parameters. Population densities of both species in these laboratory eyperiments were equivalent to 180 individuals/m2 for L. rubellus and 900 individuals./m2 for P. scaber (Kautz, 1999). When both species were fed the litter of Q. robur together, the results were in accordance with our expectations for when both species were tested separately. The species did not influence each other. When fed together, the amount of litter disappearance did not significantly deviate from the sum of the values when both species were fed separately (Table 8). However, when the litter from A. glutinosa was offered, the disappearance by the joint effect of L. rubellus and P. scaber was significantly higher (increase of 271%, PB0.05) than that calculated by simply adding up the results obtained for both saprophageous species separately. An increase in consumption, defecation and bioturbation by soil animals may simultaneously increase the soil microbial properties and soil chemical values (Figs. 4 and 5). However, these experiments did not exclude any direct effect of the animals’ biomass on the disappearance of leaf litter. We assumed a linearity between the rate of disappearance and biomass of saprophages. The calculations included the results that were obtained by the control series (Table 8). An even greater increase in litter disappearance was measured when both invertebrate species and a litter of both plant species were provided together. In these series, the alder litter had already completely disappeared from the soil surface after 6 weeks. During the following 2 weeks of study, both saprophageous species fed on oak litter so intensively that the disappearance of oak litter in this series was 7% (P B 0.05) higher than the rate when oak litter was the only food source. The results on microbial activity and the availability of Ca++-ions for both saprophageous species are shown in Fig. 4. When feeding on both litter types, both species revealed an increase in microbial activity and the availability of Ca++. These results confirm the expectations derived

317

Table 8 Mean disappearance (mg) of leaf litter from Alnus glutinosa (2.5 g), Quercus robur (2.5 g), and from both litter types together (1.0 g A. glutinosa and 1.5 g Q. robur) over a time interval of 8 weeks in controls and when the woodlouse Porcellio scaber and the earthworm Lumbricus rubellus were added separately or togethera Litter disappearance (mg) Q. robur Control P. scaber L. rubellus P. scaber+ L. rubellus A. glutinosa Control P. scaber L. rubellus P. scaber+L. rubellus Q. robur+A. glutinosa Control P. scaber L. rubellus P. scaber+L. rubellus

Increase (%)

169 359 325 528

111 92 211

507 990 1096 1883

95 116 271

353 731 1053 1258

107 198 256

a Increases in litter disappearance (%) by soil fauna in comparison to the control series are indicated.

from the results cited above. However, we found remarkable differences between series when comparing the influence of leaf litter from different tree species. Feeding on the leaf litter from Q. robur, the common effect of L. rubellus and P. scaber was not significantly different from the results when the single effects of both species were added. However, when A. glutinosa was chosen as a food item, the common effect of both saprophageous species was greater (PB 0.05) than expected by the sum of the values which were obtained when the effects of both species were tested separately (Kautz and Topp, 1999). An interaction of both saprophageous species is assumed. In these experiments we also found that the substrate after litter consumption had a higher NH+ 4 –N content, higher pH-values and fewer soluble Al3 + -ions. Thus a more favourable soil environment was created. The effect of P. scaber was less pronounced than that of L. rubellus. The

318

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common effect of both species was significantly higher (PB0.05) than the effect of one single

species (Fig. 5). These results highlight the beneficial effects of soil invertebrates on soil quality.

4. Discussion

Fig. 4. Microbial activity and available Ca++-ions (median 9 MAD, n =7) in microcosm experiments when the woodlouse P. scaber and the earthworm L. rubellus were fed, either separately or together, litter from Q. robur or A. glutinosa. The values for microbial activity are adapted to exponential functions (above); the values for available Ca++- ions are adapted to sigmoidal functions (below). Different letters indicate significant differences (Wilcoxon-test: microbial activity,PB 0.01 and Ca++, P B0.001).

Reclaimed lignite open-cast mine areas in the Rhineland are obligatorily covered by loess or a mixture of loess and sand deposits originating from the upper quartary soil layers before mining in front of the mining face. Consequently, the diverse soil fauna that has established on the reclaimed landscape may not only be the result of primary succession, but also have been influenced by the density and composition of species which are carried to the overburden dumps and are able to survive the dumping process. When the soil coverage is not leveled and compressed, it shows a pattern of crests and troughs and the diversity of habitat structures is increased. Different habitat structures that will differentiate further through the influence of erosion give prerequisites for the establishment of a diverse fauna following primary succession and also increase the probability for survival of those species which follow secondary succession. From the results for the soil fauna presented in this study, we draw the following conclusions: (1) population densities of soil biota found in the troughs are higher than those on the crests; (2) the enhanced values of the chemical properties found in the troughs of the recultivated areas clearly indicate an improved soil quality (Table 1), obtained by the process of erosion and additionally by the activity of soil biota; and (3) diverse fauna and flora improve soil quality more effectively than is expected by the additive effects obtained by the influence of single species. This means that interactive processes between species contribute to improve soil quality, even within the initial phases of succession. From these results, it can be seen that the rate at which a proper substrate is improved depends on how soon diverse soil fauna colonize the substrate, their rate of survival, and their capability of attaining high densities. Different habitats will be appropriate for different species. Different organic resources associated with the different tree

W. Topp et al. / Ecological Engineering 17 (2001) 307–322

319

3+ Fig. 5. Content of NH+ -ions (median 9MAD, n =7) in microcosm experiments when the 4 –N, pH-values and content of Al woodlouse P. scaber and the earthworm L. rubellus were fed, either separately or together, litter from Q. robur or A. glutinosa. Different letters indicate significant differences (Wilcoxon-test, PB 0.05).

species used in afforestation possess different chemical and physical attributes, decompose at different rates even under controlled environmental conditions (Hutson, 1989), and serve as food sources of different qualities for saprohageous species (Table 8) (Zimmer and Topp, 1998). A physical environment formed by heterogenous structures plus a diverse litter quality which originates from different tree species will increase the probability that saprophages are able to find appropriate food items during all seasons of the year. Moreover, within a structured environment the troughs show a more balanced physical environment, with fewer extreme conditions during the

daily and annual cycle than the crests. Furthermore, they provide better food and cover than the crests, which explains the increased densities of most animal groups. In the areas investigated, we found a substantial re-establishment of the invertebrate fauna with high densities of Collembola, Diptera and Coleoptera which are known from the early stages of primary succession (Dunger, 1968, 1989). Additionally, we found earthworm species, woodlice or millipedes which are known to inhabit reclaimed areas during a second or third phase of succession (Topp et al., 1992; Dworschak, 1997). The distribution pattern of all of these species was highly aggregated and irregular. From these findings, we

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assume that the recolonization of mined areas, especially during their initial phase of succession, seems to be superimposed on several stochastic events comparable to the colonization of real islands (Topp, 1988, 1999a). Fluctuations in population densities in subsequent years may be due to methodical difficulties which arise from the erratic aggregation patterns of most of the species. A further explanation is given by influences of the physical environment such as frost or drought periods. Many species of soil fauna will die from desiccation or frost periods and this may lead to establishment, extinction and re-establishment of subpopulations (Den Boer, 1981). Species that are typical of the first phase of primary succession are adapted to extreme environmental conditions and maintain their chances of survival, even under adverse conditions (Gemesi and Topp, 1992). Species that usually invade reclaimed areas during a later phase of succession (e.g. endogeic earthworms) often lack the adaptive qualities needed in such extreme environments. These species may survive because of the habitat peculiarities found in the troughs, even during initial succession. The management of reclaimed land should clearly aim to encourage the soil fauna in order to help develop the soil and ultimately to aid plant growth with a minimum of additional fertilizers (Hutson, 1989). It is a widespread view that one way of encouraging soil fauna is enrichment with organic material so that the upper substrate used for recultivation is covered with a humus layer. In 1984, several experimental plots of the ‘Sophienho¨he’ were covered with added humus, originating from adjacent forests in the pre-mining area. This organic material was extended over the coverage of ‘Forstkies’ with a mean thickness of about 10 cm. The organic layer provided a rich source of seeds which increase plant diversity (Wolf, 1989, 1998). Similarly, abundance and diversity of soil fauna seemed to increase in areas where a humus layer was spread out. The investigations carried out 1 year after the humus layer was supplemented, revealed a diverse epigeic fauna with several key species living in the nearby forests (Glu¨ck, 1989). Four years later, a very high density of earth-

worms was found which was even higher than the values known from central European broad leafed forests (Topp et al., 1992). However, the epigeic indicator species (several carabids) from the nearby forests which were found 1 year after this rehabilitation were no longer present (Topp, 1998). Twelve years later, within the same plots, the densities of some groups of the soil mesofauna, the microbial colonization and some of the physical and chemical characteristics of the soil were measured. We did not find differences in most parameters in the untreated areas. From these results we concluded that treatments of reclaimed afforested lignite coal mining areas with a humus layer will barely improve soil quality more than a long-lasting fertilizer would (Ba¨nsch and Topp, 1999).

Acknowledgements We thank three anonymous reviewers for valuable contributions to this review. We also thank Fred Bartlett for proofreading the manuscript. This research was supported by grants from the Rheinbraun AG.

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.