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Effects of management cessation on grassland butterflies in southern Poland
Agriculture, Ecosystems and Environment 121 (2007) 319–324 www.elsevier.com/locate/agee
Effects of management cessation on grassland butterflies in southern Poland Piotr Sko´rka a,*, Josef Settele b, Michal Woyciechowski a a
Institute of Environmental Sciences, Jagiellonian University, Gronostajowa 7, 30-387 Krako´w, Poland b Department of Community Ecology, Helmholtz Centre for Environmental Research-UFZ, Theodor-Lieser-Str. 4, D-06120 Halle, Germany Received 23 November 2005; received in revised form 18 October 2006; accepted 2 November 2006 Available online 5 December 2006
Abstract The effects of natural succession and invasions of indigenous reed Phragmites australis and alien goldenrods Solidago sp. on butterfly communities of wet grassland were investigated in Krako´w (southern Poland) after management cessation. The total number of species and individuals, mean number of species per survey and a species diversity (Shannon-Wiener index) were highest in fallow lands, old fallow lands and young forests, and the lowest in fallow lands invaded by reed and goldenrod and in mature forests. These results (1) reveal the importance of extensively mown meadows and fallow land for butterflies, (2) indicate that meadow restoration is still possible even several decades after abandonment and (3) show that invasion of reed and non-native goldenrods should be prevented. A few very rare species included in the Habitat Directive (Lycaena dispar, Lycaena helle, Maculinea teleius and Maculinea nausithous) were common on the wet grasslands in Krakow, thus the area should be protected. Moreover, it was shown that the presence and relative abundance of Maculinea butterflies were good indicators of general butterfly species richness and abundance in the investigated wet grasslands. # 2006 Elsevier B.V. All rights reserved. Keywords: Butterflies; Land management; Invasion; Bioindicators
1. Introduction On grasslands, the main habitat for butterflies in Europe, two major but antagonistic changes in land use pattern may affect butterfly populations. The first is intensification of agriculture (van Swaay and Warren, 1999; van Swaay, 2002), including intensive mowing and/or overgrazing. The second is the cessation of management practices in places where e.g. food production is no longer profitable (van Swaay and Warren, 1999; van Swaay, 2002; Verburg et al., 2006). Wet fallow lands undergoes natural succession and are often invaded by reed Phragmites australis or non-native goldenrods (Solidago sp.) (Voser-Huber, 1992; Weber, 2001; Bartoszuk, 2003). * Corresponding author. Tel.: +48 12 6645129; fax: +48 12 6646912. E-mail address: [email protected] (P. Sko´rka). 0167-8809/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2006.11.001
In this paper the effects of natural succession (appearance of shrubs and trees) as well as invasion of reed and nonnative goldenrods on butterfly communities inhabiting fallow land in southern Poland were analyzed.
2. Study area and methods The study was carried out in a vast complex of wet grasslands (ca. 16 km2) located in the western part of the city of Krako´w (southern Poland). The grassland is a mosaic of various types of meadows (with a prevailing Molinietalia association including characteristic plant species like Deschampsia caespitosa, Achillea ptarmica, Angelica sylvestris, Carex hartmannii, Cirsium palustre, Galium uliginosum, Lychnis flos-cuculi, Trollius europaeus, Sanguisorba officinalis) differing in management scheme, fallow lands and
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land (Table 1), however, shrubs and young trees were very numerous (especially young B. pendula, Salix sp. and Crataegus sp.). The density of shrubs was on average four individuals per 100 m2. Young forest appears about 20 years after management has ceased. This habitat type covered about 10% of the study area. It was characterised by the presence of a young tree layer (about 6 m tall) and a lower layer of youngest trees and shrubs (1–2 m tall). The main tree species were B. pendula, Populus sp. and A. glutinosa. Frangula alnus dominated among shrubs (Table 1). Mature forest was about 50 years old (Table 1). This is an expected stage of long-term succession in the study area. The main tree species were similar to those of young forest, however, much taller (15 m), with a visible canopy level. Other tree species included Carpinus betulus, Quercus spp. and planted Pinus sylvestris. Fallow land invaded by reed covered approximately 30% of the grassland area. Reed is very expansive on the investigated grasslands. It overgrows other plants species and reaches over 2 m in height (Table 1). Fallow meadows invaded by non-native goldenrods covered over 10% of the grassland area. Goldenrod starts to grow in late May, and in the middle of June it overgrows other plant species (Table 1). Goldenrods start blooming in late July or in the beginning of August.
small wooded areas. The meadows are occasionally flooded by the river Vistula, mainly during spring. In the last 10–20 years, most of the meadows were abandoned and therefore vast areas are not grazed or mown at all, resulting in the appearance of shrubs or young trees (mainly Betula pendula, Alnus glutinosa, Crataegus sp.). Alternative to shrub succession, an invasion of reed P. australis and/or non-native goldenrods Solidago sp. on fallow land has been observed. The following distinct types of habitats representing consecutive stages of natural succession were established: mown grassland, fallow land, old fallow land, young forest and mature forest. Fallow land with common reed as well as with non-native goldenrods were also included (Table 1). Mown meadows covered only about seven percent of the grasslands. They were mown once a year, usually at the end of July or during August and rarely grazed by cows. No fertiliser or herbicide were applied by farmers. The main plant species were grasses D. caespitosa, Arrhenatherum elatius, Dactylis glomerata, Festuca pratensis, Poa pratensis, Anthoxanthum odoratum and some other plants, mainly Cardamine pratense, Taraxacum officinale, Ly. flos-cuculi (Table 1). Early stages of fallow land covered about 30% of the total area of grasslands. Management was discontinued about 10 years ago, however, only single shrubs were present. The plants were rather tall (Table 1), and many flowering herb species occurred there, e.g. S. offcinalis, Ranunculus acris, Galium verum, Geranium pratense, Stellaria media. However, grasses still covered a substantial part of the ground (80–90% on average). Old fallow lands (about 10–20 years after abandonment) with shrubs were very similar to recently developed fallow
2.1. Butterfly censuses At first several (up to 10) patches of similar size (of about 6–10 ha) of each habitat type were selected. Then three
Table 1 General characteristic of the investigated transects Transect
Total number of butterfly species and individuals (in bracket)
Total number of plant species
Mean height of herb layer (cm) S.D.
Abundance of flowers a
Cover of grasses (%) b
Mown meadow 1 Mown meadow 2 Mown meadow 3 Fallow land 1 Fallow land 2 Fallow land 3 Old fallow land 1 Old fallow land 2 Old fallow land 3 Young forest 1 Young forest 2 Young forest 3 Mature forest 1 Mature forest 2 Mature forest 3 Meadow invaded by Meadow invaded by Meadow invaded by Meadow invaded by Meadow invaded by Meadow invaded by
21 21 19 29 22 29 25 30 37 25 29 29 12 13 13 9 5 9 10 15 19
19 18 16 27 18 27 17 20 35 30 26 22 10 9 7 21 17 16 17 15 21
69.2 16.0 53.2 11.8 73.9 9.2 84.0 14.3 139.6 12.0 99.1 19.4 112.7 23.0 79.5 16.5 96.3 30.0 94.5 17.7 82.4 19.2 93.2 24.9 39.2 9.5 31.1 17.1 33.6 10.9 179.5 18.1 175.6 17.9 188.4 22.5 156.6 21.2 134.4 24.5 120.8 35.3
205 475 235 560 400 505 300 425 630 360 355 380 95 95 70 485 330 405 205 475 235
70–80 80–90 80–90 70–80 80–90 80–90 70–80 80–90 80–90 50–60 70–80 50–60 30–40 10–20 30–40 70–80 60–70 60–80 10–20 10–20 10–20
a b
reed 1 reed 2 reed 3 goldenrods 1 goldenrods 2 goldenrods 3
(84) (99) (78) (144) (85) (139) (111) (195) (161) (98) (135) (96) (60) (44) (45) (20) (12) (19) (22) (35) (52)
Sum of the lower limits of the established categories noted in 10 round plots in each transect, see also text for further explanation. Modal category of the noted in 10 round plots in each transect, see also text for further explanation.
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patches in each habitat type were randomly chosen. In each patch, a 200 m transect was established for butterfly surveys (Pollard and Yates, 1993). Therefore, there were 21 transects in total for the seven habitat types (Table 1). Each transect was located in the middle of the given patch, at least 50 m from the patch boundary, to avoid edge effects and the impact of surrounding areas. Butterflies were counted on each transect from the beginning of May to the beginning of September on 11 occasions (Pollard and Yates, 1993). The butterflies were surveyed between 9 a.m. and 16 p.m. during favourable weather conditions (maximum wind: three in Beaufort scale, cloud cover up to 25%). The order in which the transects were checked was random. 2.2. Plant counts Ten round plots of 1 m diameter (0.79 m2) were randomly selected on each transect. Plant species richness, flower abundance and vegetation height were estimated within these plots. Plant species were counted twice—in the middle of May and in the middle of July. During the same surveys the abundance of flowers of each plant species was estimated as a categorical variable: <5 flowers/inflorescences per 0.79 m2, 5–10, 11–15 and 16–30. In case of grasses, because of identification problems, only ground cover was measured (in categories: 0–10, 11–20, . . ., 91–100%). Finally, the total number of plant species noted for each transect during the two surveys was estimated and flower abundance. Vegetation height was measured in each plot. Ten herbs were randomly selected in each plot. Then mean from means for each round plot within the transect was used in calculations.
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Separate regression models for each species were also built (but only when sample sizes were sufficient) in order to investigate factors affecting their presence and abundance. Again, forward stepwise regression with the aforementioned variables was applied, but additionally, an index of larval host plant abundance was used (flower/inflorescence abundance of the host-plant) or ground cover of grasses (in case of butterflies with grass as the host plants). For a few species (Celastrina argiolus, Goenopteryx rhamni, Nymphalis antiopa, Thecla betulae, Apatura ilia), which rely on shrubs or trees, only the presence/absence of these host plants was examined. As several butterfly species occurred only in some transects, the vegetation characteristics were used to predict the presence/absence of particular butterfly species. A generalized linear model with a logit link-function was used (Quinn and Keough, 2002). All analyzes were performed in Statistica 6.0 (StatSoft, 2003).
3. Results Altogether 1732 individuals belonging to 51 species were recorded during transect surveys (supplementary electronic
2.3. Data analysis and statistics One-way analysis of variance (ANOVA) with Tukey post hoc tests were used to analyze the effects of different stages of succession and invasion of reed and goldenrod on total number of butterfly species and total number of individuals noted during all surveys as well as on a species diversity (Shannon-Wiener index). Repeated-measures ANOVA was used to analyze these effects on the mean number of butterfly species per count. To examine how vegetation characteristics explain variation within the data, multiple stepwise regression with forward variable selection was used (Quinn and Keough, 2002). It was examined how the number of plant species, flower abundance and vegetation height (independent variables) affect butterfly species richness, number of individuals and the species diversity index (dependent variables). As the number of plant species was strongly correlated with flower abundance (r2 = 0.633; p < 0.01), a simple regression between these variables was performed and only residuals of flower abundance not explained by plant species number were used in the multiple regression analysis.
Fig. 1. Effects of natural succession on (a) total number of butterfly species and (b) species diversity index. Codes for habitat stages: G, fallow land invaded by goldenrods; R, fallow land invaded by reed; M, mown meadows; A, fallow land; S, old fallow land; Y, young forest; F, mature forest. The arrow indicates the direction of successional changes in time. The dashed line separates fallow lands invaded by reed or goldenrods as alternative effects of meadow abandonment. Means with 95% confidence intervals are presented. Tukey post hoc test showed the following significant differences at p < 0.05: (a) G–A, G–S, G–Y, R–M, R–A, R–S, R–Y, M–F, A–F, S–F, Y– F and (b) R–M, R–A, R–S, R–Y, M–F, A–F, S–F, S–F.
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material 2). The most abundant species were Aphanthopus hyperantus (14.8%), Brenthis ino (12.9%), Anthocharis cardamines (7.3%), Coenonympha pamphilus (5.6%), Maculinea teleius (4.7%) and Pieris brassicae (4.6%). On average, the largest number of species was noted on fallow lands, old fallow lands and in young forest (one-way ANOVA F 6,14 = 18.516, p < 0.001; Fig. 1a). The number of species in these habitats was significantly higher than in meadows invaded by reed and goldenrods as well as in mature forest (Fig. 1a). Moreover, old fallow land had statistically higher species richness than mown meadows (Fig. 1a). Mown meadows had relatively poor butterfly species richness, however, statistically higher than fallow lands invaded by reed (Fig. 1a). Almost the same pattern was noted when the total number of individuals was analyzed (one-way ANOVA F 6,14 = 14.094, p < 0.001; see supplementary electronic material 1). When the mean number of species per survey was analyzed, a pattern similar to the one above was found (repeated measures ANOVA, F 6,14 = 29.774, p < 0.001), however, the number of species noted during surveys on mown meadows did not differ from old fallow land and simultaneously was significantly higher than on meadows invaded by reed, goldenrods and in mature forest (supplementary electronic material 1). In case of the species diversity index on fallow lands, old fallow lands and young forest had higher values than on fallow lands invaded by reed and mature forest (one-way ANOVA F 6,14 = 8.018, p < 0.001; Fig. 1b). Mown meadows did not have statistically different values than other habitats, with the exception of fallow lands with reed, where values of the index were exceptionally low (Fig. 1b). Forward stepwise multiple regression analysis showed that the total number of butterfly species was positively affected by the number of plant species (beta = 0.830, t17 = 7.116, p < 0.0001) and negatively by vegetation height (beta = 0.581, t17 = 4.194, p < 0.001). The final model explained quite a large proportion of variation (r2 = 0.74, F 3,17 = 20.076, p < 0.0001). In case of the number of individuals, the final model (including the aforementioned variables) also explained a large proportion of the variation in the data (r2 = 0.70, F 3,17 = 13.283, p < 0.0001). The number of individuals was affected positively by number of plant species (beta = 0.736, t17 = 5.417, p < 0.0001) and negatively by vegetation height (beta = 0.681, t17 = 4.211, p < 0.001). On the other hand, the only variable influencing the species diversity index was plant species number (beta = 0.521, t17 = 2.544, p < 0.001), and the model explained only 24% of data variation (F 3,17 = 2.789, p = 0.05). Models predicting presence/absence and abundance of each species explained on average less variation (38% and 36%, respectively) than regression models built for the total number of species and total number of individuals (see above, supplementary electronic material 2). In presence/ absence models, variables that were significant most often
included the number of plant species (16 cases), vegetation height (six), and index of abundance of host plant (four). Only in one case (Ochlodes sylvanus), was the residual number of flowers significant (supplementary electronic material 2). Moreover, in 15 species none of the variables predicted presence/absence on transects. In contrast, in models predicting butterfly abundance the most important factors appeared to be vegetation height (eight cases) and number of plant species (seven). The index of host plant abundance appeared significant in five cases and the residual of flower abundance was significant in three cases. Only in three species were none of the variables significant (supplementary electronic material 2). Vegetation height influenced negatively both abundance and the probability of presence within the transect (no species showed a significant opposite trend). All the remaining variables positively affected both presence/absence and abundance of species. The grassland complex was habitat for many interesting species of which probably the most important were four species included in Appendix II of the Habitats’ Directive: M. teleius, Maculinea nausithous, Lycaena dispar and Lycaena helle. Other species from these genera included M. alcon, L. hippothoe, L. tityrus and L. phlaeas. The highest abundances of M. teleius, M. nausithous and M. alcon were found on old fallow land and, in contrast, L. dispar and L. helle reached their highest abundance on mown meadows (two-way ANOVA, interaction genus habitat type: F 4,20 = 3.561, p < 0.05; see supplementary electronic material 3). It is noteworthy that Maculinea species achieved the highest abundance in the same habitats that harboured the largest number of butterfly species and individuals.
4. Discussion Our results reveal that the succession process on abandoned wet grasslands has a positive effect on butterfly species richness, abundance and diversity index in its early stages. Fallow lands, old fallow lands and young forest supported the highest number of species and individuals. The importance of fallow lands for butterflies was recognized by Erhardt (1985) and Balmer and Erhardt (2000) on calcareous grasslands in Switzerland. Our results confirm their observations and also indicate that fallow land is very important for butterflies. However, the results of our study differ considerably from Balmer and Erhardt (2000) in two aspects. First, our results show that the young forest also supports a large number of species, whereas in the aforementioned study, the authors observed a considerable decrease in species number and abundance. These contradictory data result most probably from differences in vegetation structure in young forest growing on wet and calcareous habitats. The latter is covered by very dense bushes of Prunus spinosa, reducing visibility and area for butterflies, which could also be observed on calcareous grasslands in our study region. Young forests in wet habitats
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were not as dense as bushes of Pr. spinosa, and often had small gaps with flowering plants, which probably created favourable conditions for butterflies. Moreover, the presence of trees and shrubs may protect butterflies from adverse weather conditions (especially wind) and permits longer and more effective foraging (Dover, 1997; Merckx and van Dyck, 2002). Second, in contrast to Balmer and Erhardt (2000), succession on wet meadows seems to be much slower; our fallow land was 10–15 years old with almost no trees and only sparse shrubs. However, the most important conclusion is that meadow restoration is still possible even after a few decades after management abandonment. The plant species richness in old fallow land and young forest is high, therefore removing trees and shrubs is probably sufficient practice in this case. As fallow land, old fallow land and young forest support such a high number of butterfly species and individuals, it is also reasonable to maintain a mosaic of habitats in different successional stages, which was also pointed out by other authors for different habitats and animals (Corbet, 1995; Pain and Pienkowski, 1997; Cremene et al., 2005). This suggestion is supported by our finding that some very rare species reach their highest abundance in different habitat types, some seem to prefer old fallow land (Maculinea butterflies; compare Johst et al., 2006), other mown meadows (Lycaena species; for L. dispar see Loritz and Settele, 2002; for L. helle, however, quite different from habitat requirements in Western Europe, see e.g. Ebert and Rennwald, 1991) (supplementary electronic material 3). This study is the first to document the harmful effects of common reed and non-native goldenrods on the number of butterfly species and individuals, therefore the invasion of these plants should be prevented as far as butterfly communities are concerned. The finding that vegetation height negatively affects butterfly species richness and abundance is somewhat surprising (Collinge et al., 2003). It may be explained by tall vegetation preventing flight among flowers. Moreover, if vegetation is very tall not every flower is in fact available, because some plant species overgrow others. Contrary to species number and abundance, the diversity index was correlated only with the number of plant species. The models for individual species also showed that the number of plant species and vegetation height were the most significant variables explaining variation in abundance and presence on transects. The models included abundance of larval food plant and residual abundance of flowers as significant variables for relatively few species. The significant correlation between residual flower abundance and abundance or presence/absence of butterfly species indicates that in reality the relationship may be even stronger, as this variable is well correlated with number of plant species. However, for 15 species (35%) out of 41 for which sample size was appropriate, none of the variables in presence/absence models were significant, whereas in case of the models for abundance only three species (12%) out of 26 showed no response to the investigated variables.
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The wet meadows in Krako´w are characterised by a large number of species, often rare ones such as L. dispar, L. helle, M. teleius or M. nausithous. These species sometimes reach extraordinarily high abundances as in case of M. teleius, which is one of the most common in the region. A recent study on population sizes of Maculinea butterflies in the study area showed that about 150,000 individuals live here and almost all potentially suitable patches are inhabited (Nowicki, P., unpublished data). This group of butterflies occurred and was also the most abundant in habitats with the highest species richness, abundance and species diversity. This suggests that Maculinea species may be good indicators for biodiversity in wet meadows, at least for butterfly communities (one of the hypothesis of Settele et al., 2002). The wet grasslands in Krako´w as well as in other parts of Poland support many species, not only of butterflies but also of birds and plants, therefore many researchers stress that they should be protected (e.g. Denisiuk et al., 1991). Moreover, these wet meadows represent mainly Molinietalia associations, belonging to the most endangered habitats in Europe (Denisiuk et al., 1991). Therefore, to cover conservation priorities for both plants, birds and butterflies, a mosaic of mown (grazed) and of different stages of fallow land should be created. This could be achieved by a rotational management often quoted for such situations (Cremene et al., 2005). Acknowledgements Authors are grateful to A. Erhardt, H. Szentgyorgyi, M. Witek and an anonymous referee for critical comments on earlier version of the manuscript and also to P. Nowicki for access to his unpublished data and valuable comments on the manuscript. The study was financed by the MacMan Project (EVK2-CT-2001-00126). PS was a beneficiary of the Grant for Young Scientist of Foundation for Polish Science.
Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/ j.agee.2006.11.001.
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Corbet, S.A., 1995. Insects, plants and succession: advantages of long-term set-aside. Agric. Ecosyst. Environ. 53, 201–217. Cremene, C., Groza, G., Rakosy, L., Schileyko, A.A., Baur, A., Erhardt, A., Baur, B., 2005. Alterations of steppe-like grasslands in Eastern Europe: a threat to regional biodiversity hotspots. Conserv. Biol. 19, 1606– 1618. Denisiuk, Z., Kalemba, A., Zaja˛c, T., Ostrowska, A., Gawlin´ski, S., Sienkiewicz, J., Rejman-Czajkowska, M., 1991. Interaction between agriculture and nature conservation in Poland. Environmental Research Series, IUCN. Dover, J.W., 1997. Conservation headlands: effects on butterfly distribution and behaviour. Agric. Ecosyst. Environ. 63, 31–49. Ebert, G., Rennwald, E., 1991. Die Schmetterlinge Baden-Wu¨rttembergs— Band 2 Tagfalter II. Ulmer, Stuttgart. Erhardt, A., 1985. Diurnal lepidoptera: sensitive indicators of cultivated and abandoned grassland. J. Appl. Ecol. 22, 849–861. Johst, K., Drechsler, M., Thomas, J.A., Settele, J., 2006. Influence of mowing on the persistence of two endangered large blue butterfly (Maculinea) species. J. Appl. Ecol. 43, 333–342. Loritz, H., Settele, J., 2002. Der große feuerfalter (Lycaena dispar Haworth, 1803) im queichtal bei landau/pfalz wirtspflanzenwahl und eiablagemuster. Mitt. Pollichia 89, 309–321. Merckx, T., van Dyck, H., 2002. Interrelations among habitat use, behavior, and flight-related morphology in two cooccurring satyrine butterflies, Maniola jurtina and Pyronia tithonus. J. Insect Behav. 15, 541–561.
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Effects of management cessation on grassland butterflies in southern Poland Piotr Sko´rka a,*, Josef Settele b, Michal Woyciechowski a a
Institute of Environmental Sciences, Jagiellonian University, Gronostajowa 7, 30-387 Krako´w, Poland b Department of Community Ecology, Helmholtz Centre for Environmental Research-UFZ, Theodor-Lieser-Str. 4, D-06120 Halle, Germany Received 23 November 2005; received in revised form 18 October 2006; accepted 2 November 2006 Available online 5 December 2006
Abstract The effects of natural succession and invasions of indigenous reed Phragmites australis and alien goldenrods Solidago sp. on butterfly communities of wet grassland were investigated in Krako´w (southern Poland) after management cessation. The total number of species and individuals, mean number of species per survey and a species diversity (Shannon-Wiener index) were highest in fallow lands, old fallow lands and young forests, and the lowest in fallow lands invaded by reed and goldenrod and in mature forests. These results (1) reveal the importance of extensively mown meadows and fallow land for butterflies, (2) indicate that meadow restoration is still possible even several decades after abandonment and (3) show that invasion of reed and non-native goldenrods should be prevented. A few very rare species included in the Habitat Directive (Lycaena dispar, Lycaena helle, Maculinea teleius and Maculinea nausithous) were common on the wet grasslands in Krakow, thus the area should be protected. Moreover, it was shown that the presence and relative abundance of Maculinea butterflies were good indicators of general butterfly species richness and abundance in the investigated wet grasslands. # 2006 Elsevier B.V. All rights reserved. Keywords: Butterflies; Land management; Invasion; Bioindicators
1. Introduction On grasslands, the main habitat for butterflies in Europe, two major but antagonistic changes in land use pattern may affect butterfly populations. The first is intensification of agriculture (van Swaay and Warren, 1999; van Swaay, 2002), including intensive mowing and/or overgrazing. The second is the cessation of management practices in places where e.g. food production is no longer profitable (van Swaay and Warren, 1999; van Swaay, 2002; Verburg et al., 2006). Wet fallow lands undergoes natural succession and are often invaded by reed Phragmites australis or non-native goldenrods (Solidago sp.) (Voser-Huber, 1992; Weber, 2001; Bartoszuk, 2003). * Corresponding author. Tel.: +48 12 6645129; fax: +48 12 6646912. E-mail address: [email protected] (P. Sko´rka). 0167-8809/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2006.11.001
In this paper the effects of natural succession (appearance of shrubs and trees) as well as invasion of reed and nonnative goldenrods on butterfly communities inhabiting fallow land in southern Poland were analyzed.
2. Study area and methods The study was carried out in a vast complex of wet grasslands (ca. 16 km2) located in the western part of the city of Krako´w (southern Poland). The grassland is a mosaic of various types of meadows (with a prevailing Molinietalia association including characteristic plant species like Deschampsia caespitosa, Achillea ptarmica, Angelica sylvestris, Carex hartmannii, Cirsium palustre, Galium uliginosum, Lychnis flos-cuculi, Trollius europaeus, Sanguisorba officinalis) differing in management scheme, fallow lands and
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land (Table 1), however, shrubs and young trees were very numerous (especially young B. pendula, Salix sp. and Crataegus sp.). The density of shrubs was on average four individuals per 100 m2. Young forest appears about 20 years after management has ceased. This habitat type covered about 10% of the study area. It was characterised by the presence of a young tree layer (about 6 m tall) and a lower layer of youngest trees and shrubs (1–2 m tall). The main tree species were B. pendula, Populus sp. and A. glutinosa. Frangula alnus dominated among shrubs (Table 1). Mature forest was about 50 years old (Table 1). This is an expected stage of long-term succession in the study area. The main tree species were similar to those of young forest, however, much taller (15 m), with a visible canopy level. Other tree species included Carpinus betulus, Quercus spp. and planted Pinus sylvestris. Fallow land invaded by reed covered approximately 30% of the grassland area. Reed is very expansive on the investigated grasslands. It overgrows other plants species and reaches over 2 m in height (Table 1). Fallow meadows invaded by non-native goldenrods covered over 10% of the grassland area. Goldenrod starts to grow in late May, and in the middle of June it overgrows other plant species (Table 1). Goldenrods start blooming in late July or in the beginning of August.
small wooded areas. The meadows are occasionally flooded by the river Vistula, mainly during spring. In the last 10–20 years, most of the meadows were abandoned and therefore vast areas are not grazed or mown at all, resulting in the appearance of shrubs or young trees (mainly Betula pendula, Alnus glutinosa, Crataegus sp.). Alternative to shrub succession, an invasion of reed P. australis and/or non-native goldenrods Solidago sp. on fallow land has been observed. The following distinct types of habitats representing consecutive stages of natural succession were established: mown grassland, fallow land, old fallow land, young forest and mature forest. Fallow land with common reed as well as with non-native goldenrods were also included (Table 1). Mown meadows covered only about seven percent of the grasslands. They were mown once a year, usually at the end of July or during August and rarely grazed by cows. No fertiliser or herbicide were applied by farmers. The main plant species were grasses D. caespitosa, Arrhenatherum elatius, Dactylis glomerata, Festuca pratensis, Poa pratensis, Anthoxanthum odoratum and some other plants, mainly Cardamine pratense, Taraxacum officinale, Ly. flos-cuculi (Table 1). Early stages of fallow land covered about 30% of the total area of grasslands. Management was discontinued about 10 years ago, however, only single shrubs were present. The plants were rather tall (Table 1), and many flowering herb species occurred there, e.g. S. offcinalis, Ranunculus acris, Galium verum, Geranium pratense, Stellaria media. However, grasses still covered a substantial part of the ground (80–90% on average). Old fallow lands (about 10–20 years after abandonment) with shrubs were very similar to recently developed fallow
2.1. Butterfly censuses At first several (up to 10) patches of similar size (of about 6–10 ha) of each habitat type were selected. Then three
Table 1 General characteristic of the investigated transects Transect
Total number of butterfly species and individuals (in bracket)
Total number of plant species
Mean height of herb layer (cm) S.D.
Abundance of flowers a
Cover of grasses (%) b
Mown meadow 1 Mown meadow 2 Mown meadow 3 Fallow land 1 Fallow land 2 Fallow land 3 Old fallow land 1 Old fallow land 2 Old fallow land 3 Young forest 1 Young forest 2 Young forest 3 Mature forest 1 Mature forest 2 Mature forest 3 Meadow invaded by Meadow invaded by Meadow invaded by Meadow invaded by Meadow invaded by Meadow invaded by
21 21 19 29 22 29 25 30 37 25 29 29 12 13 13 9 5 9 10 15 19
19 18 16 27 18 27 17 20 35 30 26 22 10 9 7 21 17 16 17 15 21
69.2 16.0 53.2 11.8 73.9 9.2 84.0 14.3 139.6 12.0 99.1 19.4 112.7 23.0 79.5 16.5 96.3 30.0 94.5 17.7 82.4 19.2 93.2 24.9 39.2 9.5 31.1 17.1 33.6 10.9 179.5 18.1 175.6 17.9 188.4 22.5 156.6 21.2 134.4 24.5 120.8 35.3
205 475 235 560 400 505 300 425 630 360 355 380 95 95 70 485 330 405 205 475 235
70–80 80–90 80–90 70–80 80–90 80–90 70–80 80–90 80–90 50–60 70–80 50–60 30–40 10–20 30–40 70–80 60–70 60–80 10–20 10–20 10–20
a b
reed 1 reed 2 reed 3 goldenrods 1 goldenrods 2 goldenrods 3
(84) (99) (78) (144) (85) (139) (111) (195) (161) (98) (135) (96) (60) (44) (45) (20) (12) (19) (22) (35) (52)
Sum of the lower limits of the established categories noted in 10 round plots in each transect, see also text for further explanation. Modal category of the noted in 10 round plots in each transect, see also text for further explanation.
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patches in each habitat type were randomly chosen. In each patch, a 200 m transect was established for butterfly surveys (Pollard and Yates, 1993). Therefore, there were 21 transects in total for the seven habitat types (Table 1). Each transect was located in the middle of the given patch, at least 50 m from the patch boundary, to avoid edge effects and the impact of surrounding areas. Butterflies were counted on each transect from the beginning of May to the beginning of September on 11 occasions (Pollard and Yates, 1993). The butterflies were surveyed between 9 a.m. and 16 p.m. during favourable weather conditions (maximum wind: three in Beaufort scale, cloud cover up to 25%). The order in which the transects were checked was random. 2.2. Plant counts Ten round plots of 1 m diameter (0.79 m2) were randomly selected on each transect. Plant species richness, flower abundance and vegetation height were estimated within these plots. Plant species were counted twice—in the middle of May and in the middle of July. During the same surveys the abundance of flowers of each plant species was estimated as a categorical variable: <5 flowers/inflorescences per 0.79 m2, 5–10, 11–15 and 16–30. In case of grasses, because of identification problems, only ground cover was measured (in categories: 0–10, 11–20, . . ., 91–100%). Finally, the total number of plant species noted for each transect during the two surveys was estimated and flower abundance. Vegetation height was measured in each plot. Ten herbs were randomly selected in each plot. Then mean from means for each round plot within the transect was used in calculations.
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Separate regression models for each species were also built (but only when sample sizes were sufficient) in order to investigate factors affecting their presence and abundance. Again, forward stepwise regression with the aforementioned variables was applied, but additionally, an index of larval host plant abundance was used (flower/inflorescence abundance of the host-plant) or ground cover of grasses (in case of butterflies with grass as the host plants). For a few species (Celastrina argiolus, Goenopteryx rhamni, Nymphalis antiopa, Thecla betulae, Apatura ilia), which rely on shrubs or trees, only the presence/absence of these host plants was examined. As several butterfly species occurred only in some transects, the vegetation characteristics were used to predict the presence/absence of particular butterfly species. A generalized linear model with a logit link-function was used (Quinn and Keough, 2002). All analyzes were performed in Statistica 6.0 (StatSoft, 2003).
3. Results Altogether 1732 individuals belonging to 51 species were recorded during transect surveys (supplementary electronic
2.3. Data analysis and statistics One-way analysis of variance (ANOVA) with Tukey post hoc tests were used to analyze the effects of different stages of succession and invasion of reed and goldenrod on total number of butterfly species and total number of individuals noted during all surveys as well as on a species diversity (Shannon-Wiener index). Repeated-measures ANOVA was used to analyze these effects on the mean number of butterfly species per count. To examine how vegetation characteristics explain variation within the data, multiple stepwise regression with forward variable selection was used (Quinn and Keough, 2002). It was examined how the number of plant species, flower abundance and vegetation height (independent variables) affect butterfly species richness, number of individuals and the species diversity index (dependent variables). As the number of plant species was strongly correlated with flower abundance (r2 = 0.633; p < 0.01), a simple regression between these variables was performed and only residuals of flower abundance not explained by plant species number were used in the multiple regression analysis.
Fig. 1. Effects of natural succession on (a) total number of butterfly species and (b) species diversity index. Codes for habitat stages: G, fallow land invaded by goldenrods; R, fallow land invaded by reed; M, mown meadows; A, fallow land; S, old fallow land; Y, young forest; F, mature forest. The arrow indicates the direction of successional changes in time. The dashed line separates fallow lands invaded by reed or goldenrods as alternative effects of meadow abandonment. Means with 95% confidence intervals are presented. Tukey post hoc test showed the following significant differences at p < 0.05: (a) G–A, G–S, G–Y, R–M, R–A, R–S, R–Y, M–F, A–F, S–F, Y– F and (b) R–M, R–A, R–S, R–Y, M–F, A–F, S–F, S–F.
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material 2). The most abundant species were Aphanthopus hyperantus (14.8%), Brenthis ino (12.9%), Anthocharis cardamines (7.3%), Coenonympha pamphilus (5.6%), Maculinea teleius (4.7%) and Pieris brassicae (4.6%). On average, the largest number of species was noted on fallow lands, old fallow lands and in young forest (one-way ANOVA F 6,14 = 18.516, p < 0.001; Fig. 1a). The number of species in these habitats was significantly higher than in meadows invaded by reed and goldenrods as well as in mature forest (Fig. 1a). Moreover, old fallow land had statistically higher species richness than mown meadows (Fig. 1a). Mown meadows had relatively poor butterfly species richness, however, statistically higher than fallow lands invaded by reed (Fig. 1a). Almost the same pattern was noted when the total number of individuals was analyzed (one-way ANOVA F 6,14 = 14.094, p < 0.001; see supplementary electronic material 1). When the mean number of species per survey was analyzed, a pattern similar to the one above was found (repeated measures ANOVA, F 6,14 = 29.774, p < 0.001), however, the number of species noted during surveys on mown meadows did not differ from old fallow land and simultaneously was significantly higher than on meadows invaded by reed, goldenrods and in mature forest (supplementary electronic material 1). In case of the species diversity index on fallow lands, old fallow lands and young forest had higher values than on fallow lands invaded by reed and mature forest (one-way ANOVA F 6,14 = 8.018, p < 0.001; Fig. 1b). Mown meadows did not have statistically different values than other habitats, with the exception of fallow lands with reed, where values of the index were exceptionally low (Fig. 1b). Forward stepwise multiple regression analysis showed that the total number of butterfly species was positively affected by the number of plant species (beta = 0.830, t17 = 7.116, p < 0.0001) and negatively by vegetation height (beta = 0.581, t17 = 4.194, p < 0.001). The final model explained quite a large proportion of variation (r2 = 0.74, F 3,17 = 20.076, p < 0.0001). In case of the number of individuals, the final model (including the aforementioned variables) also explained a large proportion of the variation in the data (r2 = 0.70, F 3,17 = 13.283, p < 0.0001). The number of individuals was affected positively by number of plant species (beta = 0.736, t17 = 5.417, p < 0.0001) and negatively by vegetation height (beta = 0.681, t17 = 4.211, p < 0.001). On the other hand, the only variable influencing the species diversity index was plant species number (beta = 0.521, t17 = 2.544, p < 0.001), and the model explained only 24% of data variation (F 3,17 = 2.789, p = 0.05). Models predicting presence/absence and abundance of each species explained on average less variation (38% and 36%, respectively) than regression models built for the total number of species and total number of individuals (see above, supplementary electronic material 2). In presence/ absence models, variables that were significant most often
included the number of plant species (16 cases), vegetation height (six), and index of abundance of host plant (four). Only in one case (Ochlodes sylvanus), was the residual number of flowers significant (supplementary electronic material 2). Moreover, in 15 species none of the variables predicted presence/absence on transects. In contrast, in models predicting butterfly abundance the most important factors appeared to be vegetation height (eight cases) and number of plant species (seven). The index of host plant abundance appeared significant in five cases and the residual of flower abundance was significant in three cases. Only in three species were none of the variables significant (supplementary electronic material 2). Vegetation height influenced negatively both abundance and the probability of presence within the transect (no species showed a significant opposite trend). All the remaining variables positively affected both presence/absence and abundance of species. The grassland complex was habitat for many interesting species of which probably the most important were four species included in Appendix II of the Habitats’ Directive: M. teleius, Maculinea nausithous, Lycaena dispar and Lycaena helle. Other species from these genera included M. alcon, L. hippothoe, L. tityrus and L. phlaeas. The highest abundances of M. teleius, M. nausithous and M. alcon were found on old fallow land and, in contrast, L. dispar and L. helle reached their highest abundance on mown meadows (two-way ANOVA, interaction genus habitat type: F 4,20 = 3.561, p < 0.05; see supplementary electronic material 3). It is noteworthy that Maculinea species achieved the highest abundance in the same habitats that harboured the largest number of butterfly species and individuals.
4. Discussion Our results reveal that the succession process on abandoned wet grasslands has a positive effect on butterfly species richness, abundance and diversity index in its early stages. Fallow lands, old fallow lands and young forest supported the highest number of species and individuals. The importance of fallow lands for butterflies was recognized by Erhardt (1985) and Balmer and Erhardt (2000) on calcareous grasslands in Switzerland. Our results confirm their observations and also indicate that fallow land is very important for butterflies. However, the results of our study differ considerably from Balmer and Erhardt (2000) in two aspects. First, our results show that the young forest also supports a large number of species, whereas in the aforementioned study, the authors observed a considerable decrease in species number and abundance. These contradictory data result most probably from differences in vegetation structure in young forest growing on wet and calcareous habitats. The latter is covered by very dense bushes of Prunus spinosa, reducing visibility and area for butterflies, which could also be observed on calcareous grasslands in our study region. Young forests in wet habitats
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were not as dense as bushes of Pr. spinosa, and often had small gaps with flowering plants, which probably created favourable conditions for butterflies. Moreover, the presence of trees and shrubs may protect butterflies from adverse weather conditions (especially wind) and permits longer and more effective foraging (Dover, 1997; Merckx and van Dyck, 2002). Second, in contrast to Balmer and Erhardt (2000), succession on wet meadows seems to be much slower; our fallow land was 10–15 years old with almost no trees and only sparse shrubs. However, the most important conclusion is that meadow restoration is still possible even after a few decades after management abandonment. The plant species richness in old fallow land and young forest is high, therefore removing trees and shrubs is probably sufficient practice in this case. As fallow land, old fallow land and young forest support such a high number of butterfly species and individuals, it is also reasonable to maintain a mosaic of habitats in different successional stages, which was also pointed out by other authors for different habitats and animals (Corbet, 1995; Pain and Pienkowski, 1997; Cremene et al., 2005). This suggestion is supported by our finding that some very rare species reach their highest abundance in different habitat types, some seem to prefer old fallow land (Maculinea butterflies; compare Johst et al., 2006), other mown meadows (Lycaena species; for L. dispar see Loritz and Settele, 2002; for L. helle, however, quite different from habitat requirements in Western Europe, see e.g. Ebert and Rennwald, 1991) (supplementary electronic material 3). This study is the first to document the harmful effects of common reed and non-native goldenrods on the number of butterfly species and individuals, therefore the invasion of these plants should be prevented as far as butterfly communities are concerned. The finding that vegetation height negatively affects butterfly species richness and abundance is somewhat surprising (Collinge et al., 2003). It may be explained by tall vegetation preventing flight among flowers. Moreover, if vegetation is very tall not every flower is in fact available, because some plant species overgrow others. Contrary to species number and abundance, the diversity index was correlated only with the number of plant species. The models for individual species also showed that the number of plant species and vegetation height were the most significant variables explaining variation in abundance and presence on transects. The models included abundance of larval food plant and residual abundance of flowers as significant variables for relatively few species. The significant correlation between residual flower abundance and abundance or presence/absence of butterfly species indicates that in reality the relationship may be even stronger, as this variable is well correlated with number of plant species. However, for 15 species (35%) out of 41 for which sample size was appropriate, none of the variables in presence/absence models were significant, whereas in case of the models for abundance only three species (12%) out of 26 showed no response to the investigated variables.
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The wet meadows in Krako´w are characterised by a large number of species, often rare ones such as L. dispar, L. helle, M. teleius or M. nausithous. These species sometimes reach extraordinarily high abundances as in case of M. teleius, which is one of the most common in the region. A recent study on population sizes of Maculinea butterflies in the study area showed that about 150,000 individuals live here and almost all potentially suitable patches are inhabited (Nowicki, P., unpublished data). This group of butterflies occurred and was also the most abundant in habitats with the highest species richness, abundance and species diversity. This suggests that Maculinea species may be good indicators for biodiversity in wet meadows, at least for butterfly communities (one of the hypothesis of Settele et al., 2002). The wet grasslands in Krako´w as well as in other parts of Poland support many species, not only of butterflies but also of birds and plants, therefore many researchers stress that they should be protected (e.g. Denisiuk et al., 1991). Moreover, these wet meadows represent mainly Molinietalia associations, belonging to the most endangered habitats in Europe (Denisiuk et al., 1991). Therefore, to cover conservation priorities for both plants, birds and butterflies, a mosaic of mown (grazed) and of different stages of fallow land should be created. This could be achieved by a rotational management often quoted for such situations (Cremene et al., 2005). Acknowledgements Authors are grateful to A. Erhardt, H. Szentgyorgyi, M. Witek and an anonymous referee for critical comments on earlier version of the manuscript and also to P. Nowicki for access to his unpublished data and valuable comments on the manuscript. The study was financed by the MacMan Project (EVK2-CT-2001-00126). PS was a beneficiary of the Grant for Young Scientist of Foundation for Polish Science.
Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/ j.agee.2006.11.001.
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