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Effect of litter removal on species richness and acidification of a mixed oak-pine woodland
Biological Conservation 106 (2002) 389–398 www.elsevier.com/locate/biocon
Effect of litter removal on species richness and acidification of a mixed oak-pine woodland Zbigniew Dzwonko*, Stefan Gawron´ski Institute of Botany, Jagellonian University, ul. Lubicz 46, 31-512 Krako´w, Poland Received 6 June 2001; received in revised form 7 November 2001; accepted 4 December 2001
Abstract Eutrophication of woodland ecosystems and disappearance of acidophilous species have often been observed in central and western Europe over recent decades. Considerable increase in air-borne nitrogen and sulphur has been invoked as responsible for these processes in most studies. Historic data indicate that for hundreds of years man removed litter and fodder from many woodlands in these areas. As a result, woodland soils became poorer and more acid than they were originally. Cessation of the removal of materials may resulted in soil enrichment and eutrophication of many woods. This hypothesis was tested in a 16-year litter removal experiment in an acidophilous mixed oak–pine wood in southern Poland. It was found that litter removal resulted in substantial impoverishment of soil. After 16 years soil of the litter removal plots contained significantly less P, Mg and Ca, and had a lower cation exchange capacity (CEC) in the epihumus subhorizon, and less Ca and a lower CEC in the humus and lessivage horizons than soil in the control plots. Vascular plant species and bryophytes colonized the litter removal plots much more frequently. Within 16 years species richness increased in the field layer of these plots, but abundance of dominant species and character of vegetation remained unchanged, while vegetation of the control plots changed from acidophilous to neutrophilous. Disappearance in the control plots of vascular plants species and mosses common in mixed woodlands was caused by thick litter layer which impeded seed germination and seedling development, and by competition of dominant species. The results obtained suggest that acidophilous vegetation in the field layer of the study wood was associated with material removal by man over a long time, and its eutrophication largely resulted from the cessation of traditional methods of management. # 2002 Elsevier Science Ltd. All rights reserved. Keywords: Air pollution; Oak–pine woodlands; Permanent plots; Southern Poland; Vegetation change
1. Introduction Eutrophication, just like acidification, has been one of the most often observed processes occurring in woodland ecosystems in many European countries over recent decades (cf. Pearson and Stewart, 1993; Binkley and Ho¨gberg, 1997; Bobbink et al., 1998). An increase in the number or frequency of nitrophilous species in deciduous and mixed woodlands in western, north-western and central Europe has been noted by many authors (Falkengren-Grerup, 1986; Wilmanns et al., 1986; Tyler, 1987; Thimonier et al., 1992; Thimonier et al., 1994; Brunet et al., 1997). Moreover, decline and extinction of acidophilous species were observed in * Corresponding author. Tel.: +48-12-4241780; fax: +48-124230949. E-mail address: [email protected] (Z. Dzwonko).
deciduous, coniferous and mixed woods growing on less fertile soils (Kuhn et al., 1987; Mitka, 1993; Fangmeier et al., 1994; Walther, 1997; van Tol et al., 1998). Medwecka-Kornas´ and Gawron´ski (1990, 1991) found that during 30 years, from 1958 to 1988, vegetation in most of mixed oak–pine wood stands in the Ojco´w National Park (southern Poland) changed from acidophilous into neutrophilous, as a result of dieback of coniferous trees and extinction of acidophilous mosses and vascular plant species in the field layer. Considerable increase in air-borne nitrogen and sulphur, observed in the last decades, has been invoked as responsible for eutrophication of woodland communities in most studies. Coniferous trees growing in polluted areas suffer most of all. Their dieback may result in canopy thinning in mixed woods and, consequently, in increasing light flux to the forest floor and higher soil temperature, which leads to an increase in microbial
0006-3207/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved. PII: S0006-3207(01)00266-X
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activity and nitrogen mineralization (Ellenberg, 1988). This creates favourable conditions for nitrophilous species (cf. Falkengren-Grerup and Tyler, 1991). However, observations in south Poland proved that gaps in mixed woods were often filled with broad-leaved trees and light conditions remained substantially the same (Medwecka-Kornas´ and Gawron´ski, 1990, 1991). Many authors suggest other explanation of eutrophication, that is an increased atmospheric nitrogen deposition, which may promote litter decomposition and nitrogen mineralization (Falkengren-Grerup, 1986; Wilmanns et al., 1986; Kuhn et al., 1987; Thimonier et al., 1994; Diekmann and Dupre´, 1997). Diekmann et al. (1999) pointed out that nitrogen deposition in deciduous woodlands of south Sweden likely caused an increase in nitrification rate and nitrification ratio, which had substantial influence on species composition. Various observations of sites with higher nitrogen deposition as well as long-term experiments based on substantial enrichment of woodland soils with nitrogen resulted not only in an increase of nitrophilous species, but also in a reduction of biomass and the extinction of some acidophilous species, e.g. Vaccinium myrtillus and V. vitis-idaea, and bryophytes (Mitka, 1987; Mitka et al., 1987; Becker et al., 1992; Bobbink et al., 1998). Extinction of acidophilous species in woodlands and their eutrophication may also arise from other processes. For hundreds of years woods in central Europe have been strongly influenced by human activities. Still in the first half of the twentieth century farmers removed litter and grazed domestic animals in many woods (Miklaszewski, 1928; Ehwald, 1957; Ellenberg, 1988). Regular litter removal resulted in substantial impoverishment of soils in nitrogen and other nutrients and could lead to considerable reduction of woodland productivity (Mitscherlich, 1955). According to Ellenberg (1988), as a consequence of material removal, woodland soils in central Europe became less fertile and more acid than they were originally. Yet during the first few decades after World War II litter was removed and animals were grazed in deciduous woods in various parts of Poland (Jakubowska-Gabara, 1993). Cessation of these traditional methods of management coincided with the beginning of air pollution growth. It is possible then that changes in species composition of mixed woods also arose from the accumulation of organic matter and occurrence of thick litter layer. Decomposition of larger quantities of matter enriched soil in nutrients, and thick litter layer could restrict seed germination and development of many species. This is suggested by the studies on the influence of litter on soil and on seed germination and species distribution in deciduous woodlands (Sydes and Grime, 1981; Wilke et al., 1993; Eriksson, 1995). The purpose of this study was to determine whether eutrophication of soil and vegetation in acidophilous mixed woods depends on litter
accumulation, and to what degree the regular removal of litter influences soil, floristic composition and species richness.
2. Study area The study were carried out in an oak-pine mixed woodland with Quercus robur, Pinus sylvestris and Fagus sylvatica (Pino–Quercetum), situated in the Wierzbano´wka valley, in the northern part of Carpathian foothills, at 270 m a.s.l., 25 km southwest of Krako´w (southern Poland; 49 540 N, 19 420 E). In this area the mean annual temperature is 7.8 C, and the mean temperatures in January and July are 3.3 C and 17.9 C, respectively. The mean annual precipitation is 748 mm. The study wood grows on soil lessive´s transitional to podzolized soil (Langer, 1988), in central part of wooded area containing ancient and recent deciduous and mixed woods on the total area of 27.5 ha. Oak– hornbeam wood with Quercus robur and Carpinus betulus (Tilio–Carpinetum) occurs here on brown soils. Pino–Quercetum and Tilio–Carpinetum are considered as the regional climax communities (Medwecka-Kornas´ et al., 1988). More details of the floristic composition and species richness of these woods are given by Dzwonko (1993) and Dzwonko and Gawron´ski (1994). A perusal of historical maps and documents shows that although the study wood was managed it may be recognized as ancient because it is a remnant of woodland which in the first half of the fifteenth century covered almost the entire valley. According to the information obtained from local farmers and foresters, litter was regularly removed from the study wood until the end of the 1950s, and occasionally even in the 1960s. Over the last 145 years the frequency of various tree species has changed in this wood due to selective cutting and planting. Among other species Q. robur was felled, and Picea abies and Larix decidua were planted. These managements led to a reduction of the canopy cover and increase in the light available to the field layer in some places. Such changes, especially when litter removal had been discontinued, favoured the colonization of these places by Carex brizoides, which spreads rapidly by vegetative propagation. Now this sedge is very frequent in the study wood. In the past few decades, a considerable decrease of frequency of acidophilous species, particularly Vaccinium myrtillus, has been observed. Already in the early 1980s sites with greater cover of this species were very rare.
3. Methods In 1983, three pairs of permanent plots, each 55 m in size, were established in the study wood in sites with
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homogeneous vegetation, where acidophilous species were still growing or had occurred shortly before. Plots of each pair were placed at 3 m distance. V. myrtillus occurred in four plots, while C. brizoides dominated on two plots. From 1983 to 1998 every year by the end of October, litter was raked and removed from one plot of each pair. In 1985 and 1988, mean air-dry mass of removed litter was measured and the obtained results were 384 g m2 and 240 g m2, respectively. From 1984 to 1999 abundance of species according to the 6-degree Braun-Blanquet scale (Westhoff and van der Maarel, 1978), and the percentage cover of tree, shrub, field and bottom (bryophytes) layers were estimated in each plot during August. The nomenclature of vascular plant species is that used in Flora Europaea by Tutin et al. (1964–1980), and the nomenclature of mosses follows Ochyra and Szmajda (1978). A few days prior to litter raking in 1984, 1992, 1996 and 1999 soil was sampled for chemical analyses. In 1984 and 1992 one soil sample was taken from each of four and six plots, respectively, while in 1996 and 1999 five samples were taken from each plot, from the Hlayer (epihumus subhorizon), the A-layer (humus horizon) and lessivage horizon (depth ranging from 8 to 25 cm). At the same time the thickness of the F-layer (fermenting, fragmented litter), and that of the H-layer and the A-layer was measured. Air-dry samples were analysed for pH (in aqueous solution), available phosphorus (P), potassium (K) and magnesium (Mg) in ammonium lactate extraction according to Egner et al. (1960), exchangeable calcium (Ca) by spectrophotometry in 1 N ammonium acetate, total nitrogen (N) by the Kjeldahl method, and total carbon (C) by the Tiurin method. Cation exchange capacity (CEC) was calculated as the sum of different cations measured with a flame photometer and a spectrophotometer in 1 N ammonium acetate. In order to characterize the environmental preferences of the species in the plots, mean characteristic Ellenberg indicator values for reaction and nitrogen were calculated (Ellenberg et al., 1991) using the 6-degree coverabundance scale and only presence or absence of species. Differences in soil characteristics in 1992, 1996 and 1999 in the litter removal and control plots were analysed by non-parametric analysis of variance, the Friedman test (Sokal and Rohlf, 1998), whereas for estimating the differences between soil and community characteristics in the same years in different plots the Mann–Whitney U test was applied. The soil data from 1984 was not taken into consideration in calculations as they referred only to four plots. Rate of changes in the field and bottom layers in the litter removal and control plots were characterized by mean percentage dissimilarities in the species composition and abundance in the plots with reference to the first year of observation. Floristic dissimilarities
391
between plots were calculated using the transformed Jaccard formula (D=1 S), and the dissimilarities in the abundance of species (the symbol+on the BraunBlanquet scale was replaced by 0.5) using its quantitative equivalent: D=1 [i min (xij, xik)/i max (xij, xik)]. The Mantel test (Sokal and Rohlf, 1998) was used to examine whether differences in species composition and abundance between plots in different years were related to litter removal. This technique allows the computation of a correlation coefficient between the elements of two dissimilarity matrices. The first matrix contained all pairwise dissimilarity between plots, computed using the transformed Jaccard formula or its quantitative equivalent. The second matrix had a value of 0 for each element where plots were treated in the same way, and values of 1 elsewhere (cf. Burgman, 1987). Data from two successive years was taken into account in calculations, since only then was the number of compared entities sufficient for carry out a sampled permutation test (cf. Sokal and Rohlf, 1998). Canonical Correspondence Analysis (CCA, CANOCO program, Ter Braak and Sˇmilauer, 1998) with time as a constraining variable was used to assess the significance of changes in species composition and abundance during 16 years (from 1984 to 1999) in the field and bottom layers of the litter removal and control plots. Monte Carlo permutation test under the reduced model with the split-plot design option was done in each case. As the analyses covered three time series, 999 permutations, restricted to the cyclic shifts within time series were carried out. The total changes in community compositions were characterized by the length of gradient for the first axis of Detrended Canonical Correspondence Analysis (DCCA) with detrending by segments and time as variable. To infer which species changed considerably in the plots during 16 years, results of Redundancy Analysis (RDA) for species abundance with time as constraining variable were used. In this case the species scores along the first RDA axis are correlations of the species with the constrained variable (cf. Ter Braak and Sˇmilauer, 1998).
4. Results 4.1. Change in soil properties The removal of litter resulted in considerable soil impoverishment. Over the period between 1984 and 1999 pH Ca and CEC distinctly decreased in all three examined soil horizons of the raked plots (Table 1). During this period pH dropped also in the H-layer and lessivage horizon of the control plots, but soil here remained substantially richer in nutrients than in the raked plots. In 1992, 9 years after the litter removal had been commenced, the F-layer and H-layer of the raked
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Table 1 Comparison of soil variables for the litter removal and control plotsa Litter removal plots Variables Number of samples Depth of F-layer (cm)
1984
1992
Control plots 1996
1999
P
1984
1992
1996
1999
P
2 1.00
3 1.67
15 1.70
15 4.07
NS
2 1.00
3 0.50
15 0.38---
15 0.00---
NS
H-layer Depth (cm) pH CEC Ca Mg K P Total N (%) Total C (%) C/N
3.50 4.28 5.74 4.50 7.10 22.85 13.50 0.51 8.82 17.65
2.67 3.91 3.61 1.50 13.20 30.53 23.73 0.73 16.85+ 16.10
2.43-3.58 3.62--2.44--30.31-31.47 11.05 0.58 12.27 20.97
2.13--3.61 1.96--1.16--18.67--13.92 4.17 0.61 12.33 20.31
NS NS NS NS < 0.05 NS < 0.05 NS NS NS
3.50 4.51 3.52 2.07 7.70 23.65 18.65 0.42 7.71 18.20
3.33 3.87 5.40 3.08 16.00 29.13 20.27 0.69 11.51 16.60
3.43 3.74 10.72 9.01 39.39 39.13 13.32 0.64 13.00 20.39
3.30 3.61 4.48 3.58 31.59 12.85 5.17 0.65 12.79 20.43
NS NS NS NS <0.05 <0.05 NS NS NS NS
A-layer Depth (cm) pH CEC Ca Mg K P Total N (%) Total C (%) C/N
3.50 4.08 1.20 0.83 1.68 4.30 2.15 0.14 3.16 23.15
3.00 3.88+ 1.45 0.42 6.00 10.17 15.07 0.15 2.63 17.27
3.03 3.56 0.58--0.35--4.44 14.68 5.05 0.17 3.94 23.41
3.30 3.58 0.43--0.23--2.05 8.77 3.42 0.18 3.79 22.42
NS NS < 0.05 NS NS NS NS NS NS NS
3.50 4.05 0.97 0.58 1.14 7.35 2.25 0.18 4.14 22.50
3.00 3.45 1.74 0.60 4.90 8.70 13.20 0.16 2.56 15.03
3.20 3.68 1.30 1.07 2.07 14.69 2.36 0.19 4.11 21.70
2.57 3.53 0.86 0.68 1.75 10.16 3.61 0.21 3.75 22.47
NS NS NS NS NS <0.05 <0.05 NS NS NS
Lessivage horizon pH CEC Ca Mg K P Total N (%) Total C (%) C/N
4.90 0.76 0.43 0.90 6.30 1.80 0.07 1.28 18.60
4.34 1.08 0.28 4.70 5.17 6.53 0.07 1.02 15.57
3.97 0.34 0.24 1.06 4.15-2.17 0.08 1.60 20.94
3.86 0.24--0.10--0.60 11.03 4.76 0.06 1.73 27.89
NS NS NS NS NS < 0.05 NS NS < 0.05
5.04 0.48 0.23 0.90 7.75 1.95 0.08 1.02 13.10
4.20 0.73 0.18 3.20 6.17 6.73 0.08 1.14 13.40
3.97 0.47 0.34 1.08 5.85 3.07 0.07 1.53 21.79
3.93 0.45 0.29 1.04 10.09 5.69 0.07 1.83 26.95
NS NS NS NS NS NS NS NS NS
a Values are means. Ca, Mg, K and P are expressed as mg 100 g1 soil, cation exchange capacity (CEC) as me 100 g1 soil. P denotes the probability of no differences between years (Friedman two-way test). +/ indicate lower/higher values at P40.05 (Mann–Whitney U test) than in the control plots in the same years -P40.01 --P40.001
plots were considerably thinner, and the H-layer was significantly poorer in Ca and CEC than in the control plots. After 13 years, in 1996, differences were already much more greater. In the H-layer of the raked plots there was significantly less P, Mg, Ca and CEC, and the A-layer and lessivage horizon contained significantly less Ca and CEC than those in the control plots. The same features of soils varied considerably in the compared plots also after another 3 years, in 1999. For both groups of the plots a substantial increase in P in the Hlayer, and P and Mg in the A-layer and lessivage horizon was observed in 1992. It is assumed that this was a result of particularly intensive mineral fertilization of fields adjacent to the study woodland in 1991 and 1992.
Fertilizers spread by wind and washed by rainwater from the fields at higher altitude enriched woodland soils with the above mentioned elements. 4.2. Rate of changes in communities During 16 years tree and shrub covers on the compared plots were rather similar (Fig. 1a). In this period vegetation of the field and bottom layers changed substantially. The highest rate of change in the raked plots was within 6 years after the litter removal had been commenced. Over that period floristic composition changed by 66% and species abundance by 60%, as compared to the first year of observations (Fig. 2). The
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393
Fig. 1. Mean cover of the tree and shrub layers (a), mean cover of species in the field and bottom layers (b), and mean number of species in the field (c) and bottom (d) layers in the litter removal (&, *) and control (&, *) plots during 1984–1999. * Indicates significant difference (P40.05; Mann– Whitney U test).
Fig. 2. Mean percentage floristic dissimilarity and mean percentage dissimilarity in species abundance of the litter removal (&) and control (&) plots with reference to the first year of the study.
greatest changes in the composition (71%) and abundance (64%) of species occurred after 10 and 9 years, respectively. The rate of change in the control plots was much slower. In this case the greatest changes in species composition (57%) were observed after 14 years, and in species abundance (62%) after 16 years. The Mantel test showed that already in the third and fourth year of observations, the litter removal and control plots had significantly different species composition of vascular plants and bryophytes, and from the fifth
and sixth year they also significantly differed in vascular plants species (Table 2). Corresponding differences in species abundance were from the fifth and sixth year, and from the seventh and eighth year. Increasing values of the standardized Mantel coefficients in successive years indicate that the differences in vegetation between the litter removal and control plots increased with time. The litter removal plots were much more frequently colonized by species of vascular plants and bryophytes than the control plots (Table 3). Already in the sixth
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Table 2 Results of the Mantel test for different yearsa Years
1984–1985 1986–1987 1988–1989 1990–1991 1992–1993 1994–1995 1996–1997 1998–1999
All species
Vascular plant species
Presence/absence
Cover/abundance
Presence/absence
Cover/abundance
r
P
r
P
r
P
r
P
0.14 0.29 0.57 0.69 0.73 0.77 0.76 0.73
0.112 0.026 0.002 0.003 0.005 0.003 0.002 0.003
0.06 0.15 0.43 0.56 0.65 0.69 0.76 0.77
0.199 0.127 0.010 0.003 0.004 0.001 0.001 0.002
0.09 0.13 0.20 0.40 0.40 0.44 0.45 0.45
0.253 0.128 0.049 0.001 0.004 0.001 0.005 0.005
0.01 0.01 0.12 0.24 0.39 0.41 0.51 0.54
0.358 0.560 0.104 0.053 0.020 0.005 0.004 0.002
a Values are standardised Mantel coefficients (r) and probabilities (P) that there is no association between species composition and abundance in the plots and treatments, based on 1000 permutations.
Table 3 Species turnover in the litter removal and control plots during 1984– 1999a
Persistent species Extinct species Immigrant species Transient species
Litter removal plots
Control plots
P
8.3 0.7 14.0 6.0
5.7 2.3 5.3 0.7
NS NS <0.05 NS
(25) (2) (42) (18)
(17) (7) (23) (2)
a Values are mean species numbers and total numbers of species occurrences (in parentheses). Persistent species: present from 1984 to 1999. Extinct species: present in 1984 and extinct before 1999. Immigrant species: absent in 1984 but later appearing and present until 1999. Transient species: absent in 1984 later appearing and extinct before 1999. P denotes the probability of no difference (Mann– Whitney U test).
year of observations the mean number of vascular plant species in the raked plots was much higher, and in the 11-th year significantly higher in comparison with the control plots (Fig. 1c). From the fifth year also significantly more bryophyte species grew in the raked plots; their cover at that time exceeded 30% (Fig. 1b, d). During 16 years the number of vascular plant species only slightly increased in the control plots, but cover of the field layer increased markedly, and in the last three years was significantly higher than in the litter removal plots. However, more species became extinct in the control than in the litter removal plots (Table 3), including all species of mosses which disappeared during the first 8 years.
vegetation during the study period were greater. In these plots both species abundance and floristic composition changed significantly. The results of RDA with time as variable showed that the role of more abundant species (Carex brizoides, Vaccinium myrtillus, Majanthemum bifolium, Luzula pilosa and Milium effusum) did not change markedly in the litter removal plots during 16 years, while frequency of 21 other vascular plant species and bryophytes increased considerably; their correlation coefficients were 0.25 or higher (Table 5). Eighteen of these species were absent in the first year of observation. Only one species (Poa nemoralis) had considerable negative correlation with time in the litter removal plots. At the same time frequency or abundance of 12 species increased distinctly in the control plots, including three more abundant species (Carex brizoides, Milium effusum and Rubus hirtus) and six other species which appeared also in the litter removal plots. However, in the course of 16 years the role of as many as six species considerably decreased in the control plots, including three vascular plant species common in acidophilous mixed woodlands: Vaccinium myrtillus, Majanthemum bifolium and Luzula pilosa, as well as mosses: Atrichum undulatum, Polytrichum formosum and Dicranella heteromalla. The mean Ellenberg indicator value for acidity, calculated with consideration of species abundance, distinctly increased here; in the 11th year of the experiment it was significantly higher than in the litter removal plots (Fig. 3). Also the mean indicator value for nitrogen slightly increased in the control plots.
4.3. Temporal variation in community composition CCA with the Monte Carlo permutation test revealed significant changes in species composition and lack of such changes in species abundance in the litter removal plots (Table 4). Comparison of gradient lengths along the first DCCA axes shows that in the case of the control plots relative changes in the field and bottom layer
5. Discussion This study has shown that regular litter removal restrains eutrophication of mixed woodland ecosystem. It causes soil impoverishment and favours preservation of acidophilous vegetation in the field layer; after 13
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395
Table 4 Results of the CCA with time as a constraining variablea l1
r
P
Gradient length
Presence/absence of species Litter removal plots Control plots
0.10 0.20
0.87 0.93
0.035 0.007
1.20 1.54
Cover/abundance of species Litter removal plots Control plots
0.07 0.18
0.87 0.87
0.072 0.005
0.90 1.36
a Eigenvalue (l1) corresponds to the first CCA axis. r indicates species-environment correlations. P denotes the probability of changes in species composition and abundance in the litter removal and control plots during 1984–1999. Gradient length corresponds to the first DCCA axis.
Fig. 3. The mean Ellenberg indicator values for reaction (mR) and nitrogen (mN) in the litter removal (&) and control (&) plots during 1984–1999. * Indicates significant difference (P40.05; Mann–Whitney U test).
years of litter removal all soil layers were considerably poorer in nutrients. These results agree with the conclusions reports of Ehwald (1957), Ellenberg (1988) and other authors, on impoverishment and acidification of woodland soils in central Europe resulting from longterm removal of matter by farmers. Wilke et al. (1993) showed that in case of woodland soils with low calcium content, similar effects were obtained due to regular, natural litter removal by wind. These authors found decrease of pH in the top soil layer in such sites and its increase in the case of thicker litter layer in deciduous woodlands in Kaiserstuhl and Schwarzwald. Changes occurring in soil influence species composition of the
field layer. Falkengren-Grerup and Tyler (1993) pointed out that many species of mesophilous deciduous woodlands are sensitive to increase soil acidity and may gradually diminish or disappear at acidified woodland sites. In the last 15 years pollution of air with nitrogen oxides in the vicinity of Krako´w has not changed reaching approximately 30 mg m3. On the other hand during that time air pollution with sulphur dioxide substantially decreased; its content between 1982 and 1989 was ranging from 69 to 100 mg m3, while in 1998 it was only 17 mg m3. Also the deposition of dust containing mainly calcium decreased from 73 to 137 g m2 year1 between 1986 and 1992 to values ranging from 45 to
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Table 5 Frequency of species in the litter removal and control plots in 1984 and 1999a Species
Vascular plant species Quercus robur Frangula alnus Sorbus aucuparia Dryopteris carthusiana Fagus sylvatica Populus tremula Rubus idaeus Trientalis europaea Picea abies Carpinus betulus Polygonatum multiflorum Salix caprea Corylus avellana Carex digitata Hieracium argillaceum Betula pendula Deschampsia caespitosa Carex pallescens Agrostis capillaris Hypericum perforatum Epilobium angustifolium Rubus hirtus Carex brizoides Milium effusum Pteridium aquilinum Calamagrostis arundinacea Hedera helix Prunus avium Poa nemoralis Vaccinium myrtillus Majanthemum bifolium Luzula pilosa Bryophytes Plagiothecium nemorale Plagiothecium laetum Plagiothecium denticulatum Pleurozium schreberi Pohlia nutans Plagiomnium rostratum Lepidozia reptans Brachythecium salebrosum Atrichum undulatum Polytrichum formosum Dicranella heteromalla
R
x 4 4 4 x x x 3 x x 6 7 x x 4 x x 4 4 6 5 x 4 5 3 4 x 7 5 2 3 5
N
x x x 3 x x 6 2 x x 5 7 5 4 2 x 3 3 4 3 8 x 3 5 3 5 x 5 4 3 3 4
Litter removal plots
Control plots
1984
1999
S
r
1984
1999
S
r
0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 3 2 1 1 0 0 1 2 2 2
3 3 3 3 1 1 3 2 2 1 1 1 1 1 1 1 1 1 0 0 0 1 3 3 1 1 0 0 0 2 3 3
2.3 2.7 2.3 1.0 0.7 v0.3 3.0 v1.3 1.3 0.3 0.3 0.3 0.3 0.7 0.3 1.0 0.3 1.3 0.7 0.3 0.3 v8.0 0.0 1.7 0.0 0.0 0.0 0.0 0.3 0.3 4.3 1.0
0.83 0.78 0.80 0.79 0.33 0.40 0.35 0.51 0.39 0.41 0.39 0.36 0.36 0.31 0.30 0.25 0.25 0.24 0.12 0.10 0.08 0.14 0.02 0.05 0.00 0.20 – – 0.43 0.00 0.18 0.12
0 1 1 1 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 3 2 1 0 0 1 0 2 2 1
3 3 2 2 1 1 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 2 1 1 1 0 1 2 1
1.7 1.0 1.0 0.3 0.7 v0.7 0.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 v2.0 0.0 1.3 v0.7 0.3 v0.3 0.0 0.0 0.0 0.7 0.3
0.70 0.63 0.25 0.27 0.41 0.39 0.07 – – – – – – – – – – – – – – 0.56 0.34 0.30 0.29 0.32 0.39 0.00 – 0.58 0.47 0.36
0 2 0 0 0 2 0 0 2 2 2
2 3 1 1 1 2 0 0 3 3 3
1.0 0.3 0.7 0.7 1.0 0.0 0.3 0.7 2.3 2.0 1.3
0.60 0.25 0.25 0.24 0.22 0.08 0.04 0.19 0.49 0.23 0.12
0 0 0 0 0 0 0 0 2 2 1
0 0 0 0 0 0 0 0 0 0 0
0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
– – – – – – – – 0.58 0.58 0.32
a
Species occurring in the plots shorter than 3 years were omitted. S denotes mean number of seedlings or shoots spread vegetatively (v) from plants growing outside of the plots. r indicates correlation of the species abundance with time according to RDA. Values greater than 0.25 are in bold type. Ellenberg indicator values for reaction (R) and nitrogen (N ) are given.
59 g m2 year1 in 1998 (Grodzin´ska, 1994; Turzan´ski, 1999). It seems that decrease in soil pH observed on the control plots in the study wood may be related to these changes in air pollution. However, comparison of vegetation in the raked and control plots revealed that changes in species cover and composition were determined first of all by removal of litter. After just a few years the litter removal plots were much richer in species
of vascular plants and bryophytes than the control plots. Various observations show that the litter has a negative effect on the recruitment of the majority, if not all species in deciduous woodlands (Sydes and Grime, 1981; Persson et al., 1987; Facelli and Pickett, 1991; Eriksson, 1995; Dzwonko, 2001). Eriksson (1995) found that removal of litter in deciduous wood in central Sweden increased both seedling number per unit area
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and species diversity among seedlings. Positive effects of litter removal on species richness and cover of bryophytes in deciduous woodlands were demonstrated by Wilke et al. (1993), and in coniferous woodlands by Taoda (1988). De Vries et al. (1995) and Baar and Kuyper (1998) proved that litter and humus layer removal in pine woods resulted also in increase of species richness and sporocarp density of ectomycorrhizal fungi. During the study period cover of the field layer increased distinctly in the control plots, although the number of vascular plant species increased only slightly here in comparison with the litter removal plots. These results may lead to the conclusion consistent with the suggestion of Xiong and Nilsson (1999), resulting from the analysis of various studies, that litter affects species richness much more than above-ground biomass. Our results also confirm the opinion of Facelli and Pickett (1991) that litter constitutes not only a transitory bank of nutrients, but it is also an important factor influencing community organization and dynamics. In the 16-year period the number of species increased in the litter removal plots, but abundance of dominant species and character of vegetation did not change distinctly, while in the control plots vegetation of the field layer changed from rather acidophilous to neutrophilous. These studies indicate that Luzula pilosa, Majanthemum bifolium and Vaccinium myrtillus, species common in acidophilous mixed woodlands, declined due to restriction by litter of the germination of seeds and the establishment of seedlings and competition of other species, mainly Carex brizoides, growing rapidly in sites richer in nutrients. This sedge forms a dense and thick layer of tillers, leaves, and rhizomes, which hinders the establishment of seedlings and growth of shoots of many other species. The results obtained induced us to infer that the characteristic floristic composition and acidophilous character of the field layer vegetation in the study mixed wood largely resulted from litter removal by man for a long period. Eutrophication of this wood results first of all from the cessation of traditional methods of management in the past 40 years, and to much lower extent from increase of air pollution and mineral fertilization of the adjacent fields. The same causes could lead to the extinction of acidophilous species in other mixed woods, also in protected areas where air pollution has not been large enough to become the main or only reason of woodland dieback. The Ojco´w National Park, established in 1956, about 22 km NNW of Krako´w, may presents an example of such a situation. Medwecka-Kornas´ and Gawron´ski (1990, 1991) showed that recent changes in the structure and composition of the Pino–Quercetum, the only acidophilous forest in this area, are so great that most of its stands do not represent this community any more. An evident retreat during 30 years of such acidophilous
397
woodland species as Vaccinium myrtillus, Luzula luzuloides, Majanthemum bifolium, Melampyrum pratense, Orthilia secunda, Veronica officinalis, Lycopodium annotinum, Polytrichum formosum and Pleurozium schreberi was noted there. Similar changes have been observed also on other sites in southern Poland. In consequence, species richness of many woodlands and local diversity of woodland communities decrease. The disappearance of acidophilous species in mixed woodlands of southern Poland may result in a high degree from the increased accumulation of dead matter on the forest ground. The results of our study suggest that periodic removal of litter can diminish this process. Since litter removal is not a feature of modern management practices it may be expected that many acidophilous mixed woods will strongly change in some decades even if air pollution was be substantially reduced. Acknowledgements We would like to thank Barbara Szczepanowicz for her assistance with laboratory work. We also thank two anonymous referees for valuable comments and suggestions.
References Baar, J., Kuyper, Th.W., 1998. Restoration of aboveground ectomycorrhizal Flora in stands of Pinus sylvestris (Scots pine) in the Netherlands by removal of litter and humus. Restoration Ecology 6, 227–237. Becker, M., Bonneau, M., Le Tacon, F., 1992. Long-term vegetation changes in an Abies alba forest: natural development compared with response to fertilization. Journal of Vegetation Science 3, 467–474. Binkley, D., Ho¨gberg, P., 1997. Does atmospheric deposition of nitrogen threaten Swedish forests? Forest Ecology and Management 92, 119–152. Bobbink, R., Hornung, M., Roelofs, J.G.M., 1998. The effects of airborne nitrogen pollutants on species diversity in natural and seminatural European vegetation. Journal of Ecology 86, 717–738. Brunet, J., Falkengren-Grerup, U., Ru¨hling, A˚., Tyler, G., 1997. Regional differences in floristic change in South Swedish oak forests as related to soil chemistry and land use. Journal of Vegetation Science 8, 329–336. Burgman, M.A., 1987. An analysis of the distribution of plants on granite outcrops in southern Western Australia using Mantel tests. Vegetatio 71, 79–86. De Vries, B.W.L., Jansen, E., van Dobben, H.F., Kuyper, Th.W., 1995. Partial restoration of fungal and plant species diversity by removal of litter and humus layers in stands of Scots pine in the Netherlands. Biodiversity and Conservation 4, 156–164. Diekmann, M., Dupre´, C., 1997. Acidification and eutrophication of deciduous forests in northwestern Germany demonstrated by indicator species analysis. Journal of Vegetation Science 8, 855–864. Diekmann, M., Brunet, J., Ru¨hling, A., Falkengren-Grerup, U., 1999. Effects of nitrogen deposition: results of a temporal-spatial analysis of deciduous forests in South Sweden. Plant Biology 1, 471–481. Dzwonko, Z., 1993. Relations between the floristic composition of isolated young woods and their proximity to ancient woodland. Journal of Vegetation Science 4, 693–698.
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Mitka, J., 1993. Eutrofizacja siedliska les´ nego Puszczy Niepoomickiej. II. Zmiany skadu chemicznego ros´ lin runa. Sylwan 137, 47–56. Mitka, J., Szczepanek, K., Zemanek, B., 1987. Changes in the herb layer biomass of the mixed oak–pine forest (Pino–Quercetum) in the Niepoomice Forest area effected by mineral fertilization with NPK and dolomite. Acta Agraria et Silvestria, Series Silvestris 26, 61–74. Mitscherlich, G., 1955. Untersuchungen u¨ber das Wachstum der Kiefer in Baden. 2. Teil: Die Streunutzung- und Du¨ngungsversuche. Allgemeine Forst und Jagdzeitung 126, 193–204. Ochyra, R., Szmajda, P., 1978. Annotated list of Polish mosses. Fragmenta Floristica et Geobotanica 24, 93–145. Pearson, J., Stewart, G.R., 1993. Tansley Review No 56. The deposition of atmospheric ammonia and its effects on plants. New Phytologist 125, 283–305. Persson, S., Malmer, N., Walle´n, B., 1987. Leaf litter fall and soil acidity during half a century of secondary succession in a temperate deciduous forest. Vegetatio 73, 31–45. Sokal, R.R., Rohlf, F.J., 1998. Biometry. Freeman and Company, New York. Sydes, C., Grime, J.P., 1981. Effects of tree leaf litter on herbaceous vegetation in deciduous woodland. Journal of Ecology 69, 237–248. Ter Braak, C.J.F., Sˇmilauer, P., 1998. CANOCO Reference Manual and User’s Guide to Canoco for Windows. Centre for Biometry, Wageningen. Thimonier, A., Dupouey, J.L., Timbal, J., 1992. Floristic changes in the herb-layer vegetation of a deciduous forest in the Lorraine Plain under the influence of atmospheric deposition. Forest Ecology and Management 55, 149–167. Thimonier, A., Dupouey, J.L., Bost, F., Becker, M., 1994. Simultaneous eutrophication and acidification of a forest ecosystem in North-East France. New Phytologist 126, 533–539. Taoda, H., 1988. Succession of Pinus thunbergii forest on coastal dunes, Hitotsuba Coast, Kyushu, Japan. Hikobia 10, 119–128. Turzan´ski, K.P., 1999. Raport o stanie s´ rodowiska w 1998 roku na obszarze wojewo´dztwa maopolskiego. Biblioteka Monitoringu S´rodowiska, Krako´w. Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valentine, D.H., Walters, S.M., Webb, D.A., 1964–1980. Flora Europaea. Cambridge University Press, Cambridge. Tyler, G., 1987. Probable effects of soil acidification and nitrogen deposition on the floristic composition of oak (Quercus robur L.) forest. Flora 179, 165–170. van Tol, G., van Dobben, H.F., Schmidt, P., Klap, J.M., 1998. Biodiversity of Dutch forest ecosystems as affected by recording groundwater levels and atmospheric deposition. Biodiversity and Conservation 7, 221–228. Walther, G-R., 1997. Longterm changes in species composition of Swiss beech forests. Annali di Botanica 55, 77–84. Westhoff, V., van der Maarel, E., 1978. The Braun-Blanquet approach. In: Whittaker, R.H. (Ed.), Classification of Plant Communities. W. Junk bv Publishers, The Hague, Boston, pp. 289–399. Wilke, B., Bogenrieder, A., Wilmanns, O., 1993. Differenzierte Streuverteilung im Walde, ihre Ursachen und Folgen. Phytocoenologia 23, 129–155. Wilmanns, O., Bogenrieder, A., Mu¨ller, W.H., 1986. Der Nachweis spontaner, teils autogener, teils immissionsbedingter A¨nderungen von Eichen-Hainbuchenwa¨ldern—eine Fallstudie im Kaiserstuhl/ Baden. Natur und Landschaft 61, 415–422. Xiong, S., Nilsson, C., 1999. The effects of plant litter on vegetation: a meta-analysis. Journal of Ecology 87, 984–994.
Effect of litter removal on species richness and acidification of a mixed oak-pine woodland Zbigniew Dzwonko*, Stefan Gawron´ski Institute of Botany, Jagellonian University, ul. Lubicz 46, 31-512 Krako´w, Poland Received 6 June 2001; received in revised form 7 November 2001; accepted 4 December 2001
Abstract Eutrophication of woodland ecosystems and disappearance of acidophilous species have often been observed in central and western Europe over recent decades. Considerable increase in air-borne nitrogen and sulphur has been invoked as responsible for these processes in most studies. Historic data indicate that for hundreds of years man removed litter and fodder from many woodlands in these areas. As a result, woodland soils became poorer and more acid than they were originally. Cessation of the removal of materials may resulted in soil enrichment and eutrophication of many woods. This hypothesis was tested in a 16-year litter removal experiment in an acidophilous mixed oak–pine wood in southern Poland. It was found that litter removal resulted in substantial impoverishment of soil. After 16 years soil of the litter removal plots contained significantly less P, Mg and Ca, and had a lower cation exchange capacity (CEC) in the epihumus subhorizon, and less Ca and a lower CEC in the humus and lessivage horizons than soil in the control plots. Vascular plant species and bryophytes colonized the litter removal plots much more frequently. Within 16 years species richness increased in the field layer of these plots, but abundance of dominant species and character of vegetation remained unchanged, while vegetation of the control plots changed from acidophilous to neutrophilous. Disappearance in the control plots of vascular plants species and mosses common in mixed woodlands was caused by thick litter layer which impeded seed germination and seedling development, and by competition of dominant species. The results obtained suggest that acidophilous vegetation in the field layer of the study wood was associated with material removal by man over a long time, and its eutrophication largely resulted from the cessation of traditional methods of management. # 2002 Elsevier Science Ltd. All rights reserved. Keywords: Air pollution; Oak–pine woodlands; Permanent plots; Southern Poland; Vegetation change
1. Introduction Eutrophication, just like acidification, has been one of the most often observed processes occurring in woodland ecosystems in many European countries over recent decades (cf. Pearson and Stewart, 1993; Binkley and Ho¨gberg, 1997; Bobbink et al., 1998). An increase in the number or frequency of nitrophilous species in deciduous and mixed woodlands in western, north-western and central Europe has been noted by many authors (Falkengren-Grerup, 1986; Wilmanns et al., 1986; Tyler, 1987; Thimonier et al., 1992; Thimonier et al., 1994; Brunet et al., 1997). Moreover, decline and extinction of acidophilous species were observed in * Corresponding author. Tel.: +48-12-4241780; fax: +48-124230949. E-mail address: [email protected] (Z. Dzwonko).
deciduous, coniferous and mixed woods growing on less fertile soils (Kuhn et al., 1987; Mitka, 1993; Fangmeier et al., 1994; Walther, 1997; van Tol et al., 1998). Medwecka-Kornas´ and Gawron´ski (1990, 1991) found that during 30 years, from 1958 to 1988, vegetation in most of mixed oak–pine wood stands in the Ojco´w National Park (southern Poland) changed from acidophilous into neutrophilous, as a result of dieback of coniferous trees and extinction of acidophilous mosses and vascular plant species in the field layer. Considerable increase in air-borne nitrogen and sulphur, observed in the last decades, has been invoked as responsible for eutrophication of woodland communities in most studies. Coniferous trees growing in polluted areas suffer most of all. Their dieback may result in canopy thinning in mixed woods and, consequently, in increasing light flux to the forest floor and higher soil temperature, which leads to an increase in microbial
0006-3207/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved. PII: S0006-3207(01)00266-X
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activity and nitrogen mineralization (Ellenberg, 1988). This creates favourable conditions for nitrophilous species (cf. Falkengren-Grerup and Tyler, 1991). However, observations in south Poland proved that gaps in mixed woods were often filled with broad-leaved trees and light conditions remained substantially the same (Medwecka-Kornas´ and Gawron´ski, 1990, 1991). Many authors suggest other explanation of eutrophication, that is an increased atmospheric nitrogen deposition, which may promote litter decomposition and nitrogen mineralization (Falkengren-Grerup, 1986; Wilmanns et al., 1986; Kuhn et al., 1987; Thimonier et al., 1994; Diekmann and Dupre´, 1997). Diekmann et al. (1999) pointed out that nitrogen deposition in deciduous woodlands of south Sweden likely caused an increase in nitrification rate and nitrification ratio, which had substantial influence on species composition. Various observations of sites with higher nitrogen deposition as well as long-term experiments based on substantial enrichment of woodland soils with nitrogen resulted not only in an increase of nitrophilous species, but also in a reduction of biomass and the extinction of some acidophilous species, e.g. Vaccinium myrtillus and V. vitis-idaea, and bryophytes (Mitka, 1987; Mitka et al., 1987; Becker et al., 1992; Bobbink et al., 1998). Extinction of acidophilous species in woodlands and their eutrophication may also arise from other processes. For hundreds of years woods in central Europe have been strongly influenced by human activities. Still in the first half of the twentieth century farmers removed litter and grazed domestic animals in many woods (Miklaszewski, 1928; Ehwald, 1957; Ellenberg, 1988). Regular litter removal resulted in substantial impoverishment of soils in nitrogen and other nutrients and could lead to considerable reduction of woodland productivity (Mitscherlich, 1955). According to Ellenberg (1988), as a consequence of material removal, woodland soils in central Europe became less fertile and more acid than they were originally. Yet during the first few decades after World War II litter was removed and animals were grazed in deciduous woods in various parts of Poland (Jakubowska-Gabara, 1993). Cessation of these traditional methods of management coincided with the beginning of air pollution growth. It is possible then that changes in species composition of mixed woods also arose from the accumulation of organic matter and occurrence of thick litter layer. Decomposition of larger quantities of matter enriched soil in nutrients, and thick litter layer could restrict seed germination and development of many species. This is suggested by the studies on the influence of litter on soil and on seed germination and species distribution in deciduous woodlands (Sydes and Grime, 1981; Wilke et al., 1993; Eriksson, 1995). The purpose of this study was to determine whether eutrophication of soil and vegetation in acidophilous mixed woods depends on litter
accumulation, and to what degree the regular removal of litter influences soil, floristic composition and species richness.
2. Study area The study were carried out in an oak-pine mixed woodland with Quercus robur, Pinus sylvestris and Fagus sylvatica (Pino–Quercetum), situated in the Wierzbano´wka valley, in the northern part of Carpathian foothills, at 270 m a.s.l., 25 km southwest of Krako´w (southern Poland; 49 540 N, 19 420 E). In this area the mean annual temperature is 7.8 C, and the mean temperatures in January and July are 3.3 C and 17.9 C, respectively. The mean annual precipitation is 748 mm. The study wood grows on soil lessive´s transitional to podzolized soil (Langer, 1988), in central part of wooded area containing ancient and recent deciduous and mixed woods on the total area of 27.5 ha. Oak– hornbeam wood with Quercus robur and Carpinus betulus (Tilio–Carpinetum) occurs here on brown soils. Pino–Quercetum and Tilio–Carpinetum are considered as the regional climax communities (Medwecka-Kornas´ et al., 1988). More details of the floristic composition and species richness of these woods are given by Dzwonko (1993) and Dzwonko and Gawron´ski (1994). A perusal of historical maps and documents shows that although the study wood was managed it may be recognized as ancient because it is a remnant of woodland which in the first half of the fifteenth century covered almost the entire valley. According to the information obtained from local farmers and foresters, litter was regularly removed from the study wood until the end of the 1950s, and occasionally even in the 1960s. Over the last 145 years the frequency of various tree species has changed in this wood due to selective cutting and planting. Among other species Q. robur was felled, and Picea abies and Larix decidua were planted. These managements led to a reduction of the canopy cover and increase in the light available to the field layer in some places. Such changes, especially when litter removal had been discontinued, favoured the colonization of these places by Carex brizoides, which spreads rapidly by vegetative propagation. Now this sedge is very frequent in the study wood. In the past few decades, a considerable decrease of frequency of acidophilous species, particularly Vaccinium myrtillus, has been observed. Already in the early 1980s sites with greater cover of this species were very rare.
3. Methods In 1983, three pairs of permanent plots, each 55 m in size, were established in the study wood in sites with
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homogeneous vegetation, where acidophilous species were still growing or had occurred shortly before. Plots of each pair were placed at 3 m distance. V. myrtillus occurred in four plots, while C. brizoides dominated on two plots. From 1983 to 1998 every year by the end of October, litter was raked and removed from one plot of each pair. In 1985 and 1988, mean air-dry mass of removed litter was measured and the obtained results were 384 g m2 and 240 g m2, respectively. From 1984 to 1999 abundance of species according to the 6-degree Braun-Blanquet scale (Westhoff and van der Maarel, 1978), and the percentage cover of tree, shrub, field and bottom (bryophytes) layers were estimated in each plot during August. The nomenclature of vascular plant species is that used in Flora Europaea by Tutin et al. (1964–1980), and the nomenclature of mosses follows Ochyra and Szmajda (1978). A few days prior to litter raking in 1984, 1992, 1996 and 1999 soil was sampled for chemical analyses. In 1984 and 1992 one soil sample was taken from each of four and six plots, respectively, while in 1996 and 1999 five samples were taken from each plot, from the Hlayer (epihumus subhorizon), the A-layer (humus horizon) and lessivage horizon (depth ranging from 8 to 25 cm). At the same time the thickness of the F-layer (fermenting, fragmented litter), and that of the H-layer and the A-layer was measured. Air-dry samples were analysed for pH (in aqueous solution), available phosphorus (P), potassium (K) and magnesium (Mg) in ammonium lactate extraction according to Egner et al. (1960), exchangeable calcium (Ca) by spectrophotometry in 1 N ammonium acetate, total nitrogen (N) by the Kjeldahl method, and total carbon (C) by the Tiurin method. Cation exchange capacity (CEC) was calculated as the sum of different cations measured with a flame photometer and a spectrophotometer in 1 N ammonium acetate. In order to characterize the environmental preferences of the species in the plots, mean characteristic Ellenberg indicator values for reaction and nitrogen were calculated (Ellenberg et al., 1991) using the 6-degree coverabundance scale and only presence or absence of species. Differences in soil characteristics in 1992, 1996 and 1999 in the litter removal and control plots were analysed by non-parametric analysis of variance, the Friedman test (Sokal and Rohlf, 1998), whereas for estimating the differences between soil and community characteristics in the same years in different plots the Mann–Whitney U test was applied. The soil data from 1984 was not taken into consideration in calculations as they referred only to four plots. Rate of changes in the field and bottom layers in the litter removal and control plots were characterized by mean percentage dissimilarities in the species composition and abundance in the plots with reference to the first year of observation. Floristic dissimilarities
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between plots were calculated using the transformed Jaccard formula (D=1 S), and the dissimilarities in the abundance of species (the symbol+on the BraunBlanquet scale was replaced by 0.5) using its quantitative equivalent: D=1 [i min (xij, xik)/i max (xij, xik)]. The Mantel test (Sokal and Rohlf, 1998) was used to examine whether differences in species composition and abundance between plots in different years were related to litter removal. This technique allows the computation of a correlation coefficient between the elements of two dissimilarity matrices. The first matrix contained all pairwise dissimilarity between plots, computed using the transformed Jaccard formula or its quantitative equivalent. The second matrix had a value of 0 for each element where plots were treated in the same way, and values of 1 elsewhere (cf. Burgman, 1987). Data from two successive years was taken into account in calculations, since only then was the number of compared entities sufficient for carry out a sampled permutation test (cf. Sokal and Rohlf, 1998). Canonical Correspondence Analysis (CCA, CANOCO program, Ter Braak and Sˇmilauer, 1998) with time as a constraining variable was used to assess the significance of changes in species composition and abundance during 16 years (from 1984 to 1999) in the field and bottom layers of the litter removal and control plots. Monte Carlo permutation test under the reduced model with the split-plot design option was done in each case. As the analyses covered three time series, 999 permutations, restricted to the cyclic shifts within time series were carried out. The total changes in community compositions were characterized by the length of gradient for the first axis of Detrended Canonical Correspondence Analysis (DCCA) with detrending by segments and time as variable. To infer which species changed considerably in the plots during 16 years, results of Redundancy Analysis (RDA) for species abundance with time as constraining variable were used. In this case the species scores along the first RDA axis are correlations of the species with the constrained variable (cf. Ter Braak and Sˇmilauer, 1998).
4. Results 4.1. Change in soil properties The removal of litter resulted in considerable soil impoverishment. Over the period between 1984 and 1999 pH Ca and CEC distinctly decreased in all three examined soil horizons of the raked plots (Table 1). During this period pH dropped also in the H-layer and lessivage horizon of the control plots, but soil here remained substantially richer in nutrients than in the raked plots. In 1992, 9 years after the litter removal had been commenced, the F-layer and H-layer of the raked
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Table 1 Comparison of soil variables for the litter removal and control plotsa Litter removal plots Variables Number of samples Depth of F-layer (cm)
1984
1992
Control plots 1996
1999
P
1984
1992
1996
1999
P
2 1.00
3 1.67
15 1.70
15 4.07
NS
2 1.00
3 0.50
15 0.38---
15 0.00---
NS
H-layer Depth (cm) pH CEC Ca Mg K P Total N (%) Total C (%) C/N
3.50 4.28 5.74 4.50 7.10 22.85 13.50 0.51 8.82 17.65
2.67 3.91 3.61 1.50 13.20 30.53 23.73 0.73 16.85+ 16.10
2.43-3.58 3.62--2.44--30.31-31.47 11.05 0.58 12.27 20.97
2.13--3.61 1.96--1.16--18.67--13.92 4.17 0.61 12.33 20.31
NS NS NS NS < 0.05 NS < 0.05 NS NS NS
3.50 4.51 3.52 2.07 7.70 23.65 18.65 0.42 7.71 18.20
3.33 3.87 5.40 3.08 16.00 29.13 20.27 0.69 11.51 16.60
3.43 3.74 10.72 9.01 39.39 39.13 13.32 0.64 13.00 20.39
3.30 3.61 4.48 3.58 31.59 12.85 5.17 0.65 12.79 20.43
NS NS NS NS <0.05 <0.05 NS NS NS NS
A-layer Depth (cm) pH CEC Ca Mg K P Total N (%) Total C (%) C/N
3.50 4.08 1.20 0.83 1.68 4.30 2.15 0.14 3.16 23.15
3.00 3.88+ 1.45 0.42 6.00 10.17 15.07 0.15 2.63 17.27
3.03 3.56 0.58--0.35--4.44 14.68 5.05 0.17 3.94 23.41
3.30 3.58 0.43--0.23--2.05 8.77 3.42 0.18 3.79 22.42
NS NS < 0.05 NS NS NS NS NS NS NS
3.50 4.05 0.97 0.58 1.14 7.35 2.25 0.18 4.14 22.50
3.00 3.45 1.74 0.60 4.90 8.70 13.20 0.16 2.56 15.03
3.20 3.68 1.30 1.07 2.07 14.69 2.36 0.19 4.11 21.70
2.57 3.53 0.86 0.68 1.75 10.16 3.61 0.21 3.75 22.47
NS NS NS NS NS <0.05 <0.05 NS NS NS
Lessivage horizon pH CEC Ca Mg K P Total N (%) Total C (%) C/N
4.90 0.76 0.43 0.90 6.30 1.80 0.07 1.28 18.60
4.34 1.08 0.28 4.70 5.17 6.53 0.07 1.02 15.57
3.97 0.34 0.24 1.06 4.15-2.17 0.08 1.60 20.94
3.86 0.24--0.10--0.60 11.03 4.76 0.06 1.73 27.89
NS NS NS NS NS < 0.05 NS NS < 0.05
5.04 0.48 0.23 0.90 7.75 1.95 0.08 1.02 13.10
4.20 0.73 0.18 3.20 6.17 6.73 0.08 1.14 13.40
3.97 0.47 0.34 1.08 5.85 3.07 0.07 1.53 21.79
3.93 0.45 0.29 1.04 10.09 5.69 0.07 1.83 26.95
NS NS NS NS NS NS NS NS NS
a Values are means. Ca, Mg, K and P are expressed as mg 100 g1 soil, cation exchange capacity (CEC) as me 100 g1 soil. P denotes the probability of no differences between years (Friedman two-way test). +/ indicate lower/higher values at P40.05 (Mann–Whitney U test) than in the control plots in the same years -P40.01 --P40.001
plots were considerably thinner, and the H-layer was significantly poorer in Ca and CEC than in the control plots. After 13 years, in 1996, differences were already much more greater. In the H-layer of the raked plots there was significantly less P, Mg, Ca and CEC, and the A-layer and lessivage horizon contained significantly less Ca and CEC than those in the control plots. The same features of soils varied considerably in the compared plots also after another 3 years, in 1999. For both groups of the plots a substantial increase in P in the Hlayer, and P and Mg in the A-layer and lessivage horizon was observed in 1992. It is assumed that this was a result of particularly intensive mineral fertilization of fields adjacent to the study woodland in 1991 and 1992.
Fertilizers spread by wind and washed by rainwater from the fields at higher altitude enriched woodland soils with the above mentioned elements. 4.2. Rate of changes in communities During 16 years tree and shrub covers on the compared plots were rather similar (Fig. 1a). In this period vegetation of the field and bottom layers changed substantially. The highest rate of change in the raked plots was within 6 years after the litter removal had been commenced. Over that period floristic composition changed by 66% and species abundance by 60%, as compared to the first year of observations (Fig. 2). The
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Fig. 1. Mean cover of the tree and shrub layers (a), mean cover of species in the field and bottom layers (b), and mean number of species in the field (c) and bottom (d) layers in the litter removal (&, *) and control (&, *) plots during 1984–1999. * Indicates significant difference (P40.05; Mann– Whitney U test).
Fig. 2. Mean percentage floristic dissimilarity and mean percentage dissimilarity in species abundance of the litter removal (&) and control (&) plots with reference to the first year of the study.
greatest changes in the composition (71%) and abundance (64%) of species occurred after 10 and 9 years, respectively. The rate of change in the control plots was much slower. In this case the greatest changes in species composition (57%) were observed after 14 years, and in species abundance (62%) after 16 years. The Mantel test showed that already in the third and fourth year of observations, the litter removal and control plots had significantly different species composition of vascular plants and bryophytes, and from the fifth
and sixth year they also significantly differed in vascular plants species (Table 2). Corresponding differences in species abundance were from the fifth and sixth year, and from the seventh and eighth year. Increasing values of the standardized Mantel coefficients in successive years indicate that the differences in vegetation between the litter removal and control plots increased with time. The litter removal plots were much more frequently colonized by species of vascular plants and bryophytes than the control plots (Table 3). Already in the sixth
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Table 2 Results of the Mantel test for different yearsa Years
1984–1985 1986–1987 1988–1989 1990–1991 1992–1993 1994–1995 1996–1997 1998–1999
All species
Vascular plant species
Presence/absence
Cover/abundance
Presence/absence
Cover/abundance
r
P
r
P
r
P
r
P
0.14 0.29 0.57 0.69 0.73 0.77 0.76 0.73
0.112 0.026 0.002 0.003 0.005 0.003 0.002 0.003
0.06 0.15 0.43 0.56 0.65 0.69 0.76 0.77
0.199 0.127 0.010 0.003 0.004 0.001 0.001 0.002
0.09 0.13 0.20 0.40 0.40 0.44 0.45 0.45
0.253 0.128 0.049 0.001 0.004 0.001 0.005 0.005
0.01 0.01 0.12 0.24 0.39 0.41 0.51 0.54
0.358 0.560 0.104 0.053 0.020 0.005 0.004 0.002
a Values are standardised Mantel coefficients (r) and probabilities (P) that there is no association between species composition and abundance in the plots and treatments, based on 1000 permutations.
Table 3 Species turnover in the litter removal and control plots during 1984– 1999a
Persistent species Extinct species Immigrant species Transient species
Litter removal plots
Control plots
P
8.3 0.7 14.0 6.0
5.7 2.3 5.3 0.7
NS NS <0.05 NS
(25) (2) (42) (18)
(17) (7) (23) (2)
a Values are mean species numbers and total numbers of species occurrences (in parentheses). Persistent species: present from 1984 to 1999. Extinct species: present in 1984 and extinct before 1999. Immigrant species: absent in 1984 but later appearing and present until 1999. Transient species: absent in 1984 later appearing and extinct before 1999. P denotes the probability of no difference (Mann– Whitney U test).
year of observations the mean number of vascular plant species in the raked plots was much higher, and in the 11-th year significantly higher in comparison with the control plots (Fig. 1c). From the fifth year also significantly more bryophyte species grew in the raked plots; their cover at that time exceeded 30% (Fig. 1b, d). During 16 years the number of vascular plant species only slightly increased in the control plots, but cover of the field layer increased markedly, and in the last three years was significantly higher than in the litter removal plots. However, more species became extinct in the control than in the litter removal plots (Table 3), including all species of mosses which disappeared during the first 8 years.
vegetation during the study period were greater. In these plots both species abundance and floristic composition changed significantly. The results of RDA with time as variable showed that the role of more abundant species (Carex brizoides, Vaccinium myrtillus, Majanthemum bifolium, Luzula pilosa and Milium effusum) did not change markedly in the litter removal plots during 16 years, while frequency of 21 other vascular plant species and bryophytes increased considerably; their correlation coefficients were 0.25 or higher (Table 5). Eighteen of these species were absent in the first year of observation. Only one species (Poa nemoralis) had considerable negative correlation with time in the litter removal plots. At the same time frequency or abundance of 12 species increased distinctly in the control plots, including three more abundant species (Carex brizoides, Milium effusum and Rubus hirtus) and six other species which appeared also in the litter removal plots. However, in the course of 16 years the role of as many as six species considerably decreased in the control plots, including three vascular plant species common in acidophilous mixed woodlands: Vaccinium myrtillus, Majanthemum bifolium and Luzula pilosa, as well as mosses: Atrichum undulatum, Polytrichum formosum and Dicranella heteromalla. The mean Ellenberg indicator value for acidity, calculated with consideration of species abundance, distinctly increased here; in the 11th year of the experiment it was significantly higher than in the litter removal plots (Fig. 3). Also the mean indicator value for nitrogen slightly increased in the control plots.
4.3. Temporal variation in community composition CCA with the Monte Carlo permutation test revealed significant changes in species composition and lack of such changes in species abundance in the litter removal plots (Table 4). Comparison of gradient lengths along the first DCCA axes shows that in the case of the control plots relative changes in the field and bottom layer
5. Discussion This study has shown that regular litter removal restrains eutrophication of mixed woodland ecosystem. It causes soil impoverishment and favours preservation of acidophilous vegetation in the field layer; after 13
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395
Table 4 Results of the CCA with time as a constraining variablea l1
r
P
Gradient length
Presence/absence of species Litter removal plots Control plots
0.10 0.20
0.87 0.93
0.035 0.007
1.20 1.54
Cover/abundance of species Litter removal plots Control plots
0.07 0.18
0.87 0.87
0.072 0.005
0.90 1.36
a Eigenvalue (l1) corresponds to the first CCA axis. r indicates species-environment correlations. P denotes the probability of changes in species composition and abundance in the litter removal and control plots during 1984–1999. Gradient length corresponds to the first DCCA axis.
Fig. 3. The mean Ellenberg indicator values for reaction (mR) and nitrogen (mN) in the litter removal (&) and control (&) plots during 1984–1999. * Indicates significant difference (P40.05; Mann–Whitney U test).
years of litter removal all soil layers were considerably poorer in nutrients. These results agree with the conclusions reports of Ehwald (1957), Ellenberg (1988) and other authors, on impoverishment and acidification of woodland soils in central Europe resulting from longterm removal of matter by farmers. Wilke et al. (1993) showed that in case of woodland soils with low calcium content, similar effects were obtained due to regular, natural litter removal by wind. These authors found decrease of pH in the top soil layer in such sites and its increase in the case of thicker litter layer in deciduous woodlands in Kaiserstuhl and Schwarzwald. Changes occurring in soil influence species composition of the
field layer. Falkengren-Grerup and Tyler (1993) pointed out that many species of mesophilous deciduous woodlands are sensitive to increase soil acidity and may gradually diminish or disappear at acidified woodland sites. In the last 15 years pollution of air with nitrogen oxides in the vicinity of Krako´w has not changed reaching approximately 30 mg m3. On the other hand during that time air pollution with sulphur dioxide substantially decreased; its content between 1982 and 1989 was ranging from 69 to 100 mg m3, while in 1998 it was only 17 mg m3. Also the deposition of dust containing mainly calcium decreased from 73 to 137 g m2 year1 between 1986 and 1992 to values ranging from 45 to
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Table 5 Frequency of species in the litter removal and control plots in 1984 and 1999a Species
Vascular plant species Quercus robur Frangula alnus Sorbus aucuparia Dryopteris carthusiana Fagus sylvatica Populus tremula Rubus idaeus Trientalis europaea Picea abies Carpinus betulus Polygonatum multiflorum Salix caprea Corylus avellana Carex digitata Hieracium argillaceum Betula pendula Deschampsia caespitosa Carex pallescens Agrostis capillaris Hypericum perforatum Epilobium angustifolium Rubus hirtus Carex brizoides Milium effusum Pteridium aquilinum Calamagrostis arundinacea Hedera helix Prunus avium Poa nemoralis Vaccinium myrtillus Majanthemum bifolium Luzula pilosa Bryophytes Plagiothecium nemorale Plagiothecium laetum Plagiothecium denticulatum Pleurozium schreberi Pohlia nutans Plagiomnium rostratum Lepidozia reptans Brachythecium salebrosum Atrichum undulatum Polytrichum formosum Dicranella heteromalla
R
x 4 4 4 x x x 3 x x 6 7 x x 4 x x 4 4 6 5 x 4 5 3 4 x 7 5 2 3 5
N
x x x 3 x x 6 2 x x 5 7 5 4 2 x 3 3 4 3 8 x 3 5 3 5 x 5 4 3 3 4
Litter removal plots
Control plots
1984
1999
S
r
1984
1999
S
r
0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 3 2 1 1 0 0 1 2 2 2
3 3 3 3 1 1 3 2 2 1 1 1 1 1 1 1 1 1 0 0 0 1 3 3 1 1 0 0 0 2 3 3
2.3 2.7 2.3 1.0 0.7 v0.3 3.0 v1.3 1.3 0.3 0.3 0.3 0.3 0.7 0.3 1.0 0.3 1.3 0.7 0.3 0.3 v8.0 0.0 1.7 0.0 0.0 0.0 0.0 0.3 0.3 4.3 1.0
0.83 0.78 0.80 0.79 0.33 0.40 0.35 0.51 0.39 0.41 0.39 0.36 0.36 0.31 0.30 0.25 0.25 0.24 0.12 0.10 0.08 0.14 0.02 0.05 0.00 0.20 – – 0.43 0.00 0.18 0.12
0 1 1 1 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 3 2 1 0 0 1 0 2 2 1
3 3 2 2 1 1 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 3 3 2 1 1 1 0 1 2 1
1.7 1.0 1.0 0.3 0.7 v0.7 0.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 v2.0 0.0 1.3 v0.7 0.3 v0.3 0.0 0.0 0.0 0.7 0.3
0.70 0.63 0.25 0.27 0.41 0.39 0.07 – – – – – – – – – – – – – – 0.56 0.34 0.30 0.29 0.32 0.39 0.00 – 0.58 0.47 0.36
0 2 0 0 0 2 0 0 2 2 2
2 3 1 1 1 2 0 0 3 3 3
1.0 0.3 0.7 0.7 1.0 0.0 0.3 0.7 2.3 2.0 1.3
0.60 0.25 0.25 0.24 0.22 0.08 0.04 0.19 0.49 0.23 0.12
0 0 0 0 0 0 0 0 2 2 1
0 0 0 0 0 0 0 0 0 0 0
0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
– – – – – – – – 0.58 0.58 0.32
a
Species occurring in the plots shorter than 3 years were omitted. S denotes mean number of seedlings or shoots spread vegetatively (v) from plants growing outside of the plots. r indicates correlation of the species abundance with time according to RDA. Values greater than 0.25 are in bold type. Ellenberg indicator values for reaction (R) and nitrogen (N ) are given.
59 g m2 year1 in 1998 (Grodzin´ska, 1994; Turzan´ski, 1999). It seems that decrease in soil pH observed on the control plots in the study wood may be related to these changes in air pollution. However, comparison of vegetation in the raked and control plots revealed that changes in species cover and composition were determined first of all by removal of litter. After just a few years the litter removal plots were much richer in species
of vascular plants and bryophytes than the control plots. Various observations show that the litter has a negative effect on the recruitment of the majority, if not all species in deciduous woodlands (Sydes and Grime, 1981; Persson et al., 1987; Facelli and Pickett, 1991; Eriksson, 1995; Dzwonko, 2001). Eriksson (1995) found that removal of litter in deciduous wood in central Sweden increased both seedling number per unit area
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and species diversity among seedlings. Positive effects of litter removal on species richness and cover of bryophytes in deciduous woodlands were demonstrated by Wilke et al. (1993), and in coniferous woodlands by Taoda (1988). De Vries et al. (1995) and Baar and Kuyper (1998) proved that litter and humus layer removal in pine woods resulted also in increase of species richness and sporocarp density of ectomycorrhizal fungi. During the study period cover of the field layer increased distinctly in the control plots, although the number of vascular plant species increased only slightly here in comparison with the litter removal plots. These results may lead to the conclusion consistent with the suggestion of Xiong and Nilsson (1999), resulting from the analysis of various studies, that litter affects species richness much more than above-ground biomass. Our results also confirm the opinion of Facelli and Pickett (1991) that litter constitutes not only a transitory bank of nutrients, but it is also an important factor influencing community organization and dynamics. In the 16-year period the number of species increased in the litter removal plots, but abundance of dominant species and character of vegetation did not change distinctly, while in the control plots vegetation of the field layer changed from rather acidophilous to neutrophilous. These studies indicate that Luzula pilosa, Majanthemum bifolium and Vaccinium myrtillus, species common in acidophilous mixed woodlands, declined due to restriction by litter of the germination of seeds and the establishment of seedlings and competition of other species, mainly Carex brizoides, growing rapidly in sites richer in nutrients. This sedge forms a dense and thick layer of tillers, leaves, and rhizomes, which hinders the establishment of seedlings and growth of shoots of many other species. The results obtained induced us to infer that the characteristic floristic composition and acidophilous character of the field layer vegetation in the study mixed wood largely resulted from litter removal by man for a long period. Eutrophication of this wood results first of all from the cessation of traditional methods of management in the past 40 years, and to much lower extent from increase of air pollution and mineral fertilization of the adjacent fields. The same causes could lead to the extinction of acidophilous species in other mixed woods, also in protected areas where air pollution has not been large enough to become the main or only reason of woodland dieback. The Ojco´w National Park, established in 1956, about 22 km NNW of Krako´w, may presents an example of such a situation. Medwecka-Kornas´ and Gawron´ski (1990, 1991) showed that recent changes in the structure and composition of the Pino–Quercetum, the only acidophilous forest in this area, are so great that most of its stands do not represent this community any more. An evident retreat during 30 years of such acidophilous
397
woodland species as Vaccinium myrtillus, Luzula luzuloides, Majanthemum bifolium, Melampyrum pratense, Orthilia secunda, Veronica officinalis, Lycopodium annotinum, Polytrichum formosum and Pleurozium schreberi was noted there. Similar changes have been observed also on other sites in southern Poland. In consequence, species richness of many woodlands and local diversity of woodland communities decrease. The disappearance of acidophilous species in mixed woodlands of southern Poland may result in a high degree from the increased accumulation of dead matter on the forest ground. The results of our study suggest that periodic removal of litter can diminish this process. Since litter removal is not a feature of modern management practices it may be expected that many acidophilous mixed woods will strongly change in some decades even if air pollution was be substantially reduced. Acknowledgements We would like to thank Barbara Szczepanowicz for her assistance with laboratory work. We also thank two anonymous referees for valuable comments and suggestions.
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