Intensified Grazing Affects Endemic Plant and Gastropod

Biologia, Bratislava, 62/4: 438—445, 2007 Section Zoology DOI: 10.2478/s11756-007-0086-4

Intensiﬁed grazing aﬀects endemic plant and gastropod diversity in alpine grasslands of the Southern Carpathian mountains (Romania)

Bruno Baur1,CristinaCremene1,2, Gheorghe Groza3,AnatoliA.Schileyko4, Anette Baur1 & Andreas Erhardt1

1Section of Conservation Biology, Department of Environmental Sciences, University of Basel, St. Johanns-Vorstadt 10, CH-4056 Basel, Switzerland; e-mail: [email protected] 2Faculty of Biology and Geology, Babes-Bolyai University, Str. Clinicilor 5–7, 400006 Cluj-Napoca, Romania 3Department of Botany, University of Agricultural Sciences and Veterinary Medicine, Calea Manastur 3–5, 400372 Cluj- Napoca, Romania 4A.N. Severtzov Institute of Problems of Evolution and Ecology of the Russian Academy of Sciences, Leninski Prospect 33, 119017 Moscow, Russia

Abstract: Alpine grasslands in the Southern Carpathian Mts, Romania, harbour an extraordinarily high diversity of plants and invertebrates, including Carpathic endemics. In the past decades, intensive sheep grazing has caused a dramatic de- crease in biodiversity and even led to eroded soils at many places in the Carpathians. Because of limited food resources, sheep are increasingly forced to graze on steep slopes, which were formerly not grazed by livestock and are considered as local biodiversity hotspots. We examined species richness, abundance and number of endemic vascular plants and terrestrial gastropods on steep slopes that were either grazed by sheep or ungrazed by livestock in two areas of the Southern Carpathians. On calcareous soils in the Bucegi Mts, a total of 177 vascular plant and 19 gastropod species were recorded. Twelve plant species (6.8%) and three gastropod species (15.8%) were endemic to the Carpathians. Grazed sites had lower plant and gastropod species richness than ungrazed sites. Furthermore, grazed sites harboured fewer gastropod species endemic to the Carpathians than ungrazed sites. On acid soils in the Fagaras Mts, a total of 96 vascular plant and nine gastropod species were found. In this mountain area, however, grazed and ungrazed sites did not differ in species richness, abundance and number of endemic plant and gastropod species. Our findings confirm the high biodiversity of grasslands on steep slopes in the Southern Carpathian Mts and caution against increasing grazing pressure in these refuges for relic plants and gastropods as well as for other invertebrates. Key words: Alpine grassland; biodiversity; Bucegi Mts; Gastropoda; grazing; Fagaras Mts; vascular plants

Introduction adjusted to the local conditions to identify and imple- ment the best strategy of biodiversity conservation. Alpine grasslands are unique habitats for a variety of In contrast to the general trend of grassland aban- plant and invertebrate species (Körner 1999; Nagy et donment in remote areas, land use is increasingly in- al. 2003). Seasonal pastoral activities have been prac- tensified in easily accessible mountain areas (Tasser & ticed for many centuries on accessible areas of these Tappeiner 2002). Transhumant shepherding, the sea- natural grasslands (Messerli & Ives 1997). To increase sonal migration of sheep to suitable grazing grounds, is grazing areas, semi-natural grasslands have been cre- the traditional use of subalpine and alpine grasslands in ated in mountain areas belowthetreelinebyforest the Southern Carpathian Mts (Romania). For example, logging (Ellenberg 1996; Coldea 2003). Although vas- historical records document sheep grazing in the Bucegi cular plant species richness of various natural and semi- Mts since the beginning of the sixteenth century (Bar- natural grasslands in general increases under moderate bulescu & Motca 1983). In these mountains, the sheep grazing (Collins et al. 1998; Sternberg et al. 2000), ef- flocks have always been large, forcing the animals to fects of grazing on biodiversity vary considerably among graze also in adjacent forests, which were clearcut to ecosystems and among different taxa (Niemelä&Baur extend the pastures in the 19th century (Coldea 2003). 1998; Balmer & Erhardt 2000; Cremene et al. 2005; More recently, the size of the sheep flocks has increased Baur et al. 2006). Moreover, patterns of biodiversity further as a consequence of the altered socio-economic and their driving processes obviously vary with spatial situation since 1989. Detrimental effects of overgrazing and temporal scale (Crawley & Harral 2001; Dullinger and trampling on plant diversity and vegetation struc- et al. 2003). Pasture management should therefore be ture, and eroded soils have been reported on the plateau

c 2007 Institute of Zoology, Slovak Academy of Sciences Intensified grazing in the Southern Carpathians 439 of the Bucegi Mts (Barbulescu & Motca 1983; Coldea north of the Balea Nature Reserve. The flora of this val- 2003). As a result, grazing pressure has increased on so ley is characteristic for the alpine region of the Southern far extensively used, adjacent steep mountain slopes. Carpathians and includes several Carpathic endemic species This is of particular concern as the Southern Carpathi- (Puscaru-Soroceanu et al. 1981; Barbulescu & Motca 1983). ans harbour a high number of endemic and relic plant The Balea Nature Reserve is considered as relatively species- poor in invertebrates (www.ipmsb.ro/rezervnat.htm#balea; and invertebrate species (ICAS 1996; Ioras 2003). accessed 28.02.2006). However, some Carpathic endemic in- The aim of the present study was to examine effects vertebrates can still be found in this area, e.g. the land snail of intensified grazing on these steep slopes, so far only Arianta aethiops aethiops (Bielz, 1851) (Baur et al. 2000). occasionally grazed by sheep and wildlife (chamois). In both mountain areas we investigated similar sites As indicators of biodiversity we used vascular plants that differed in grazing intensity. In July 2003, we surveyed and terrestrial gastropods, which both have been shown the diversity and abundance of vascular plants and ter- to be sensitive indicators of habitat change (Ellenberg restrial gastropods on steep slopes at five sites intensively 1996; Labaune & Magnin 2002). We assessed the species grazed by sheep (hereafter grazed sites) and at five sites only diversity and species abundance of vascular plants and occasionally grazed by chamois (hereafter ungrazed sites) in terrestrial gastropods in both intensively grazed sites the Bucegi Mts (Table 1). Grazed study sites were parts of pastures repeatedly visited by large flocks of sheep (> 500 and in sites only occasionally grazed by chamois in two individuals). Ungrazed study sites were situated on the same areas in the Southern Carpathians, Romania. In partic- slopes but separated from grazed sites either by rock walls ular, we addressed the following questions: (1) How are or stands of Pinus mugo. Each study site measured approx- plant and gastropod diversity and abundance affected imately 20 × 30 m. Similarly, we examined four grazed and by intensified sheep grazing on steep slopes? (2) How four ungrazed sites in the Fagaras Mts (Table 1). Grazed do endemic and threatened (red-listed) species respond and ungrazed sites were situated 110–2600 m apart in the to intensive grazing? (3) Are responses to grazing cor- Bucegi Mts and 120–1530 m in the Fagaras Mts. related between plants and gastropods? For plants we compiled a species list of grasses and forbs for each site. In addition to presence/absence, we also recorded the abundance of each species in a subplot of 10 × Material and methods 10 m using the Braun-Blanquet method (1964). Walking in × Study areas and sampling a zigzag line over the entire study site (20 30 m) the list The effect of intensified pastoral management on the alpine of plant species was completed by recording all new species plant and gastropod diversity was examined in two areas in observed. Plant identification followed Tuttin et al. (1964– the Southern Carpathians in Romania: in the Bucegi Mts 1980) and Ciocarlan (2000). (45◦24 N, 25◦31 E) 30 km SSW of Brasov and in the Fa- Species richness and relative abundance of terrestrial garas Mts (45◦37 N, 24◦37 E) 40 km SE of Sibiu. The gastropods were assessed by visually searching for living two mountain areas are 80 km apart from each other and snails and slugs and for empty shells. Five people searched × differ in the underlying bedrock: the investigated slopes of in each 20 30 m plot for a total of 120 minutes. Field- the Bucegi Mts consist of limestone, while the sites in the work was only conducted under conditions favourable for Fagaras Mts are situated on siliceous bedrock. gastropod activity (moist vegetation and high air humidity). The Bucegi Mts are built of Mesozoic sedimentary Identification of gastropods followed Grossu (1981, 1983). rocks (mainly limestones, sandstones and conglomerates), At each study site, the following ecological variables which are exposed to erosion since middle Tertiary. This were measured: elevation (in metres above sea level, ex- resulted in complex tectonic and morphological structures, tracted from topographical maps; Bucegi Mts, scale 1 : with numerous small valleys and ridges on steep slopes. In 53,000; Fagaras Mts, scale 1 : 60,000), exposure (degrees the Bucegi Mts, the first protected areas were established from south using a compass), inclination (average of six in 1943 (www.bucegipark.ro; accessed 15.02.2006). The pro- measurements), soil pH (average of six soil samples using tected areas were several times enlarged, resulting in the the Hellige method; AVM Analyseverfahren, Freiburg, Ger- Bucegi Nature Park with a total area of 326.6 km2, includ- many), two measures of vegetation height (average height ing 13 nature reserves (ca. 90 km2) in 2000. A significant of the forb and the grass layer, both based on six measure- part of the nature reserves is located on the steep moun- ments), and the percentage area covered by rock and scree tain slopes, while the gently inclined slopes on the plateau, (estimated to the nearest 10%). which are heavily overgrazed at many places and contain In the Bucegi Mts, grazed and ungrazed study sites did huge areas of eroded soil, are not protected. Our study was not differ in elevation, soil pH and area covered by rocks and conducted on natural alpine grasslands at the border of the scree (Table 1; t-tests, in all comparisons, P > 0.35). How- Abruptul Prahovean Nature Reserve (Table 1). ever, grazed sites faced slightly more to north-east, whereas The Bucegi Nature Park contains approximately 30% ungrazed sites tended to face to south-east (Mardia-Watson- of the total plant diversity in Romania. The steep slopes of Wheeler-test, P = 0.05). Furthermore, grazed sites occurred ◦ ◦ the Bucegi Mts harbour a most interesting flora with nu- on slightly flatter slopes than ungrazed sites (33.8 ± 3.8 ◦ ◦ merous Carpathic endemic and glacial relic plants (Coldea (SD) vs 39.2 ± 1.9 ; t8 = 2.94, P = 0.0188). As expected, & Cristea 1998). At places with calcareous bedrock, the gas- the vegetation was shorter at grazed sites than at ungrazed tropod fauna is rich with several species endemic to the ones (forb height: 7.0 ± 2.7 cm vs 23.0 ± 2.7 cm, t8 = 9.24, Carpathians (Grossu 1981, 1983). P < 0.0001; grass height: 18.0 ± 4.5 cm vs 30.0 ± 0cm,t8 The Fagaras Mts are a traditional area for Romanian = 6.00, P = 0.0003). shepherds, who have been practicing transhumant pastoral- In the Fagaras Mts, grazed and ungrazed sites did not ism for many centuries (Puscaru-Soroceanu et al. 1981). Our differ in exposure, elevation, inclination, soil pH and area study sites were located on crystalline bedrock with brown covered by rocks and scree (Table 1; t-tests, in all compar- acid soils in subalpine, man-made grasslands in the valley isons, P > 0.14). Again, the vegetation was shorter at grazed 440 B. Baur et al.

Table 1. Characteristics of the sites surveyed in the Bucegi and Fagaras Mts, Southern Carpathians, Romania.

Mountain Site Grassland Elevation Exposure Inclination Soil pH Forb / grass height Rock cover area management (m a.s.l.) (◦)(cm)(%)

Bucegi 1 U 2220 E–ESE 38 6.5 25 / 30 10 2 U 2080 S–SE 37 6.0 20 / 30 20 3 U 2120 S–SSE 40 7.0 20 / 30 20 4 U 2040 E–SE 42 6.5 25 / 30 20 5 U 1910 E–ESE 39 6.5 25 / 30 25 6 G 2070 NE 31 6.5 5 / 20 10 7 G 2120 NNE 32 6.5 5 / 10 15 8 G 2100 ENE 34 6.5 10 / 20 20 9 G 2070 NNE 32 6.5 5 / 20 15 10 G 1940 NE 40 5.5 10 / 20 20

Fagaras 1 U 1700 W 29 4.0 20 / 50 1 2 U 1750 W–WSW 35 4.0 30 / 40 15 3 U 1750 W 24 4.5 15 / 30 15 4 U 1820 WNW 35 4.5 10 / 30 5 5 G 1620 WSW 27 4.5 10 / 30 5 6 G 1650 W 30 4.0 7 / 20 5 7 G 1700 W 22 4.0 5 / 20 15 8 G 1780 WSW 20 4.0 5 / 20 10

Explanations: U – ungrazed; G – grazed. than at ungrazed sites (forb height: 6.8 ± 2.4 cm vs 18.8 ± their frequencies (Eilertsen et al. 1990). DCA was performed 8.5 cm, t6 = 2.71, P = 0.0352; grass height: 22.5 ± 5.0 vs using CANOCO version 4.5 (ter Braak & Smilauer 2002). 37.5 ± 9.6 cm, t6 = 2.78, P = 0.0321). In plants, comparisons of species richness and number of endemic and red-listed species are based on the species list Data analyses of each study site (20 × 30 m), whereas comparisons of The StatView program package (SAS Institute 1998) was communities are based on abundance data of 10 × 10 m used for statistical analyses. Means ± 1 SD are given un- subplots. less otherwise stated. In all analyses we considered the study To examine whether grazed and ungrazed sites dif- sites as the unit of investigation. As calcareous and siliceous fered in the number of endemic plants or gastropods, we soils are known to harbour a different flora and fauna, we assigned each species to one of the following categories: analysed data from the Bucegi and Fagaras Mts separately. Romanian Carpathic endemic (occurring exclusively in the Data on species richness, number of gastropod individu- Carpathians of Romania), Eastern European endemic (Bal- als, and number of endemic and red-listed species were log- canic, Pontic, Carpathic and/or Dacic distributions) and transformed (if necessary log(x + 1)). widespread (naturally occurring in large areas of one or more Because the grazed and ungrazed sites examined in the continents). Total cover of plants endemic to the Carpathi- Bucegi Mts slightly differed in exposure, we used analyses ans was calculated for each site as the sum of the cover of covariance (ANCOVA, type III model) with grazing/no values of all Carpathic endemic plants (see above). In Ro- grazing as factor and exposure as covariate to examine pos- mania, a red list exists for plants (Boscaiu et al., 1994) but sible differences in species richness, number of gastropod not for terrestrial gastropods. individuals, and number of endemic and red-listed species. We used Pearson’s correlations to examine possible cor- Similarly, data from the Bucegi Mts were analysed using the relations between species richness and numbers of endemic same ANCOVA-model with inclination as covariate. How- and red-listed species within and between plants and gas- ever, in no case did inclination have a significant influence tropods. For data of the Bucegi Mts, we calculated partial on the examined variables. Therefore, these analyses are not correlations, keeping exposure constant. presented. In the Fagaras Mts, the grazed and ungrazed sites examined differed neither in exposure nor in inclination. For Results this area we used unpaired t-tests to examine possible differences between grazed and ungrazed sites in species richness, number of gastropod individuals, and number of endemic and red-listed species. Plant and gastropod species richness We used detrended correspondence analysis (DCA) to A total of 177 plant species was recorded at the study examine differences in plant and gastropod communities be- sites of the Bucegi Mts. Grazed sites had a lower plant tween grazed and ungrazed study sites (Hill & Gauch 1980). species richness (57.8 ± 10.9; mean ± SD) than un- DCA was preformed separately for both groups of organ- grazed sites (64.2 ± 8.6; ANCOVA: F1,6 = 6.44, P = ism and both mountain areas. For the DCA, the vegetation 0.0443). The exposure of the sites did not affect the cover-abundance code adapted from Braun-Blanquet (1964) number of plant species (P = 0.51), but there was a was applied using the following weights: 0.1 for ‘R’, 0.5 for tendency for an interaction between grazing and expo- ‘+’, 3 for the category 1, 7.5 for the category 2, 15 for the category 3, 25 for the category 4, and 40 for the category 5 sure (P = 0.0573). Nineteen different gastropod species (see Buschmann et al. 2005). Prior to ordination, the data were recorded at the study sites of the Bucegi Mts. were log-transformed. Species that were less frequent than Grazed sites harboured fewer gastropod species (5.4 ± the median frequency were down-weighted in proportion to 3.5) than ungrazed sites (8.4 ± 2.3; ANCOVA: F1,6 = Intensified grazing in the Southern Carpathians 441

2 2 A B 8 5 2 4 4 3 5 3 10 1

2 8 Axis 2 Axis Axis 2 Axis 1 7 9 7 6 0 6 0

02Axis 1 0 Axis 1 3

2 C D 4 8 8 1 4 1 9 5 2

5 Axis 2 Axis Axis 2 Axis 1 3 2 3 6 6 7 10 7 0 0

0 Axis 1 2 03Axis 1

Fig. 1. Ordination diagram based on detrended correspondence analysis of plants and terrestrial gastropods in grazed and ungrazed grasslands in the Southern Carpathians, Romania, displaying the major variation in species composition: A – plants in the Bucegi Mts; B – plants in the Fagaras Mts; C – terrestrial gastropods in the Bucegi Mts; D – terrestrial gastropods in the Fagaras mountains. Open dots indicate ungrazed sites and full dots grazed sites. Numbers refer to the study sites (see Table 1).

6.00, P = 0.0498). Again, site exposure did not influ- value = 0.534) explained 40.0% of the variance in gas- ence the number of gastropod species (P = 0.29), and tropod species data (together with the second axis there was a tendency for an interaction between grazing 59.1%). and exposure (P = 0.0573). In all, 96 plant species were found in the study sites Abundance of gastropods on siliceous bedrock in the Fagaras Mts. Grazed (29.3 A total of 1,611 gastropod individuals were recorded ± 6.4) and ungrazed (30.8 ± 4.6) sites did not differ (1,496 in the Bucegi Mts and 115 in the Fagaras Mts). in plant species richness (t6 = 0.46, P = 0.66). At the In the Bucegi Mts, on average 114.6 ± 62.9 individ- same sites, a total of 9 gastropod species was recorded. uals were found in grazed sites and 184.6 ± 47.6 in- Grazed sites (3.3 ± 2.2) and ungrazed sites (3.8 ± 1.3) dividuals in ungrazed sites. However, due to the large did not differ in gastropod species richness (t6 = 0.68, within-treatment variation in number of individuals the P = 0.52). difference in gastropod abundance was not significant (ANCOVA: F1,6 = 1.16, P = 0.32). The exposure of the Community structure site did not influence the number of gastropod individ- In plants growing in the Bucegi Mts, the DCA ordi- uals recorded (P = 0.80) and there was no interaction nation revealed a separation of grazed and ungrazed between grazing and exposure (P = 0.52). Similarly, study sites, except that one grazed site (#10) was grazed and ungrazed sites in the Fagaras Mts did not positioned among ungrazed sites (Fig. 1A). The first differ in the number of gastropod individuals (15.8 ± axis (Eigenvalue = 0.379) explained 25.1% of the vari- 4.0 vs 13.0 ± 9.8; t6 = 0.92, P = 0.39). ance in species data (together with the second axis In the Bucegi Mts, the number of recorded gastro- 37.7%). In plants of the Fagaras Mts, grazed and un- pod individuals increased with increasing grass height grazed sites were clearly separated (Fig. 1B). The first (partial correlation, exposure kept constant: r = 0.82, axis (Eigenvalue = 0.683) explained 28.4% of the vari- n = 10, P = 0.0086). No similar relationship between ance in plant species data (together with the second number of gastropods recorded and vegetation height axis 39.6%). Similarly, in terrestrial gastropods liv- was found in the Fagaras Mts (r = −0.17, n =8,P = ing in the Bucegi Mts, the DCA ordination revealed 0.70). a clear separation of grazed and ungrazed study sites The two mountain areas differed also in the pro- (Fig. 1C). The first axis (Eigenvalue = 0.273) explained portion of slugs (gastropods without shell) found. In 27.7% of the variance in species data (together with the Bucegi Mts, only 14 (0.9%) out of the 1496 individ- the second axis 35.7%). In gastropods of the Fagaras uals recorded were slugs, whereas in the Fagaras Mts Mts, however, there was no separation between grazed 88 (76.5%) of the 115 gastropod individuals were slugs and ungrazed sites (Fig. 1D). The first axis (Eigen- (chi square = 1028.8, df = 1, P < 0.0001). 442 B. Baur et al.

Endemism als (P = 0.54) nor was there any interaction (P = 0.89). Twelve (6.8%) of the 177 plant species recorded in Considering single species, the Carpathic endemic A. the Bucegi Mts were endemic to the Carpathians livida and the Eastern European endemic F. faustina (Cerastium transsilvanicum Schur, Dianthus gelidus occurred in most of the sites examined. The abundance Schott, Nyman and Kotschy, Dianthus tenuifolius of both species did not differ between grazed and un- Schur, Gypsophila petraea (Baumgarten) Reichenbach, grazed sites (ANCOVA, P =0.71andP = 0.92, respec- Hypericum richeri ssp. transsilvanicum Celakovsky, tively). However, the abundance of another Carpathic Koeleria macrantha ssp. transsilvanica Schur, Ono- endemic, C. venerabilis was affected by sheep grazing: brychis montana ssp. transsilvanica Simonkai, Oxytro- 5.4 ± 7.8 individuals were found in grazed sites and 70.0 pis carpatica von Uechtritz, Phyteuma wagneri Kerner, ± 39.1 individuals in ungrazed sites (ANCOVA: F1,6 = Saxifraga demissa Scott and Kotschy, Thlaspi dacicum 10.54, P = 0.0175). The abundance of C. venerabilis was Heuffel and Thymus pulcherrimus Schur) and another not significantly influenced by the exposure of the site 20 species (11.3%) were endemic to Eastern Europe. (ANCOVA: P = 0.07), but there was an interaction be- The number of plant species endemic to the Carpathi- tween grazing and exposure (F1,6 = 7.09, P = 0.0374), ans tended to be lower in grazed sites (3.0 ± 2.6) than indicating that this species was differently influenced by in ungrazed sites (4.0 ± 1.4; ANCOVA: F1,6 = 5.18, the combined effects of grazing and exposure. C. vener- P = 0.0632). The number of Carpathic endemic plant abilis occurred in all five ungrazed sites and in two of the species was not affected by the exposure of the sites five grazed sites. The other two endemics (A. canescens (P = 0.21), but there was a significant interaction be- and O. inopinatus) were only found at a single site each. tween grazing and exposure (P = 0.0494), indicating None of the nine gastropod species found in the that the number of endemic plant species in grazed ar- study sites of the Fagaras Mts was endemic to the eas was differently influenced by the combined effects Carpathians. of grazing and exposure. Furthermore, the total cover of Carpathic endemic plants was lower in grazed (1.0 ± Red-listed species 1.5%) than in ungrazed sites (3.9 ± 3.8%; ANCOVA: In the Bucegi Mts, four vulnerable and 19 nearly threat- F1,6 = 10.03, P = 0.0194). The exposure of the sites ened (rare) plant species were recorded in the sites ex- did not influence the total cover of endemic plants (P amined (no critically endangered or endangered species = 0.89), but there was a tendency for an interaction be- occurred in these sites). Grazed and ungrazed sites did tween grazing and exposure (F1,6 = 5.94, P = 0.0506). not differ in the number of red-listed plant species (to- Two (2.1%) of the 96 plant species recorded in the tal of species considered as vulnerable or nearly threat- Fagaras Mts were endemic to the Carpathians (Hyper- ened; grazed sites 10.4 ± 2.4%, ungrazed sites 8.2 ± icum richeri ssp. transsilvanicum and Thymus pulcher- 3.3%; ANCOVA: F1,6 = 3.86, P = 0.10). The exposure rimus) and another nine species (9.4%) were endemic of the sites did not influence the number of red-listed to Eastern Europe. Grazed and ungrazed sites did not species (P = 0.78), and there was no interaction be- differ in the number of Carpathic endemic plant species tween grazing and exposure (P = 0.09). (1.3 ± 1.0 vs 0.5 ± 0.6; t6 = 1.15, P = 0.29). Neither In the Fagaras Mts, one vulnerable and four nearly did the grassland types differ in total cover of plants threatened plant species were found in the study sites. endemic to the Carpathians (grazed: 0.2 ± 0.3%, un- Grazed and ungrazed sites did not differ in the number grazed: 0.8 ± 1.5%; t6 = 0.11, P = 0.92). of red-listed plant species (2.0 ± 1.6 vs 1.8 ± 1.0; t6 = Three (15.8%) of the 19 gastropod species recorded 0.04 P = 0.97). in the Bucegi Mts were endemic to the Carpathi- ans [Alopia canescens (Charpentier, 1852), Alopia Correlations between plants and gastropods livida (Menke, 1830) and Chondrula venerabilis (Pfeifer, Plant species richness was positively correlated with 1853)] and two further species [Oxychilus inopina- gastropod species richness in the Bucegi Mts (partial tus (Ulicny, 1887) and Faustina faustina (Rossmässler, correlation, keeping exposure constant, r = 0.67, n = 1835)] were endemic to Eastern Europe. The number 10, P = 0.0480), but not in the Fagaras Mts (r = −0.48, of gastropod species endemic to the Carpathians was n = 10, P = 0.25). In the Bucegi Mts, plant species lower in grazed than in ungrazed sites (1.5 ± 0.5 vs richness was also positively correlated with the number 2.2 ± 0.4; ANCOVA: F1,6 = 6.67, P = 0.0416). Site of plants endemic to the Carpathians (partial correla- exposure did not influence the number of endemic gas- tion r = 0.91, n = 10, P = 0.0003) and the number tropod species (P = 0.17), and there was no interac- of Carpathic endemic gastropods (partial correlation r tion between grazing and exposure (F1,6 = 5.59, P = = 0.77, n = 10, P = 0.0116). However, the number 0.06). Considering the number of gastropod individuals of red-listed plant species was neither correlated with endemic to the Carpathians, on average 81.4 ± 53.7 in- plant species richness nor with the number of endemic dividuals were found in grazed sites and 109.2 ± 33.4 plants or gastropods. Furthermore, none of these vari- in ungrazed sites. However, because of the large within- ables were intercorrelated in the Fagaras Mts. treatment variation in number of endemic individuals, this difference was not significant (ANCOVA: F1,6 = Discussion 0.29, P = 0.61). Furthermore, there was no effect of site exposure on the number of endemic gastropod individu- Over the past centuries, pastoralism has taken up much Intensified grazing in the Southern Carpathians 443 of the grasslands in the Southern Carpathians (Bar- significant differences between grazed and ungrazed bulescu & Motca 1983). Due to the high grazing pres- sites. Furthermore, slugs are presumably less sensitive sure, the grassland areas were stepwise enlarged by to livestock trampling than shelled gastropods (Boschi clear-cutting forests and areas covered by shrubs and & Baur 2007). bushes (Puscaru-Soroceanu et al. 1981). However, the With our sampling approach we might have missed problem of overgrazing by large flocks of sheep grazing a few rare gastropod species (cf. Cameron & Pokryszko in relatively small areas remained. The huge number 2005). Our focus was, however, the comparison of two of sheep reduced plant diversity, and subsequently, the types of land use. Consequently, we applied the same soil became eroded, particularly on flatter parts of the sampling effort per plot in either land use type. The mountains (Coldea 2003). As a consequence, the orig- observed differences are conservative because the prob- inally wide-spread, species-rich grasslands can today ability of overlooking a snail is rather higher in tall only be found on the steeper slopes, which until recently vegetation of ungrazed sites than in short vegetation of were less intensively or not at all grazed by livestock. grazed sites. However, since 1989, the altered socioeconomic condi- Both investigated mountain areas harboured tions in Romania have favoured a further increase in species endemic to the Carpathians, but they were more the size of sheep flocks, which still have to graze on the numerous in the calcareous grasslands of the Bucegi same mountain pastures. As a result, grazing pressure Mts than in the Fagaras Mts. In the Bucegi Mts grazed has extended into these unique, species-rich grassland sites harboured fewer endemic gastropod species than remnants on the steep slopes. ungrazed sites. There was also a tendency for grazed Our study shows that in the Bucegi Mts species sites to contain fewer endemic plant species than un- richness of plants and terrestrial gastropods is lower grazed sites. Furthermore, the total cover of Carpathic in grasslands on steep, intensively grazed slopes com- endemic plants was lower on grazed slopes than on un- pared with sites only occasionally grazed by wildlife grazed slopes in this mountain area. Different endemic even though red-listed plant species were not affected. plant and gastropod species reacted differently to graz- Management by grazing is known to alter the botani- ing pressure. For example, the Carpathic endemic gas- cal composition and structure of grassland vegetation tropod Chondrula venerabilis is a specialized grassland (Morris 2000). Intermediate levels of disturbance are as- species, which showed a reduced abundance in grazed sumed to increase plant species richness and reduce the sites. By contrast, the Carpathic endemic Alopia livida dominance of competitive species (Curry 1994). How- and the Eastern European endemic Faustina faustina, ever, effects on gastropod communities are less well two gastropod species feeding on algae and lichens, oc- studied. Grazing may influence gastropods indirectly cur mainly on vertical rock surfaces and thus are less by altering the amount and quality of the food supply exposed to trampling by grazing livestock. Hence, the and by changing the microclimate, or directly by tram- abundance of both A. livida and F. faustina did not pling the snails’ shells (Baur 1986; Boschi & Baur 2007). differ between grazed and ungrazed sites. The latter is of particular importance for gastropods, Plant species richness was positively correlated because on steep slopes grazing sheep frequently move with that of terrestrial gastropods in the Bucegi Mts. pieces of stone that results in crushed snails (Baur et In steppe-like grasslands and their seral stages of suc- al. 2000). Our results indicate that the extent of dis- cession in Transylvania, Romania, no correlation be- turbance by grazing is too high to maintain the for- tween plant and gastropod species richness was found mer species-rich plant and gastropod communities in (Cremene et al. 2005). Similarly, the species richness of the Bucegi Mts. vascular plants was a poor indicator for species richness The effects of intensive sheep grazing on the plant of gastropods in nutrient-poor, dry calcareous grass- and gastropod communities of acid soils in the Fa- lands in Switzerland (Baur et al. 1996; Niemelä&Baur garas Mts were less pronounced. Areas with siliceous 1998). In the present study, plant diversity may not di- bedrock are generally less species-rich in plants and rectly influence gastropod diversity, but both may re- particularly in gastropods than areas with calcareous spond to similar environmental conditions. soils (Ellenberg 1996; Wäreborn 1970, 1992). Hence, in such areas an increased grazing pressure might not so Implications for conservation and management strongly affect species richness. However, in the present Our study shows that in the Bucegi Mts plant and study, species composition and abundance in plants gastropod diversity and abundance are significantly re- were altered in a characteristic and pronounced way duced by sheep grazing on formerly ungrazed, steep in the Fagaras Mts (Fig. 1B), suggesting that intensive slopes. This is of particular concern because the plateau sheep grazing affects the vegetation composition also of the Bucegi Mts is already heavily overgrazed, which on siliceous bedrock. has resulted in the local extinction of numerous indige- On acid soils only a limited number of gastropods nous plant species (Barbulescu & Motca 1983; Coldea can cope with the calcium carbonate deficiency. Slugs 2003). The grasslands investigated in our study be- (gastropods without shell) can better live under such long to the last remaining refuges for several endemic conditions. This may explain the high proportion of and relic plant and gastropod species. If overgrazing slugs in the Fagaras Mts. However, gastropod abun- by sheep should further extend into these particularly dance and species richness remained low, preventing valuable grassland remnants, their diverse flora and 444 B. Baur et al. fauna would be at risk. Thus, an appropriate manage- Boscaiu N., Coldea G. & Horeanu C. 1994. Lista rosie a plantelor ment should aim to protect these last refuges on steep vasculare disparute, amenintate sau vulnerabile din Roma- slopes from overgrazing. Most of these valuable grass- nia [The red list of extinct, endangered, vulnerable and rare vascular plants of the Romanian Flora]. Ocrotirea Naturii si lands are part of the 13 nature reserves of the Bucegi Mediului Inconjurator 38: 45–56. Nature Park (www.bucegipark.ro). The findings of our Boschi C. & Baur B. 2007. The effect of horse, cattle and sheep study indicate that there is an urgent need to imple- grazing on the diversity and abundance of land snails in 8: ment the protection aims of the existing nature reserve. nutrient-poor calcareous grasslands. Basic Appl. Ecol. 55– 65. Furthermore, the restoration of overgrazed grasslands Braun-Blanquet J. 1964. Pflanzensoziologie, Grundzüge der Vege- should be promoted, even if this may require decades. tationskunde. Springer, New York, 865 pp. At present, the situation in the Fagaras Mts appears to Buschmann H., Keller M., Porret N., Dietz H. & Edwards P.J. be less critical, but should also be observed with atten- 2005. The effect of slug grazing on vegetation development and plant species diversity in an experimental grassland. tion. Funct. Ecol. 19: 291–298. In conclusion, our study confirms the high biodi- Cameron R.A.D. & Pokryszko, B.M. 2005. Estimating the species versity value of grasslands on steep slopes, not only for richness and composition of land mollusc communities: prob- endemic and relic plant and gastropod species, but also lems, consequences and practical advice. J. Conchol. 38: 529– 547. for more widespread species in the Carpathian Mts. It Ciocarlan V. 2000. Flora ilustrata a Romaniei – Pterydophyta si also shows the detrimental effects of intensified sheep Spermatophyta [Illustrated Flora of Romania – Pterydophyta grazing on these so far unthreatened grasslands, which et Spermatophyta]. Editura Ceres, Bucuresti, 1138 pp. were only occasionally grazed by wildlife. Other taxo- Coldea G. 2003. The alpine flora and vegetation of the south- eastern Carpathians, pp. 65–73. In: Nagy L., Grabherr G., nomic groups such as butterflies and moths may also Körner C. & Thompson D.B.A. (eds), Alpine Biodiversity in suffer under the increasing grazing pressure. For exam- Europe, Springer, Berlin. ple, populations of the moth Grammia quenseli Paykull, Coldea G. & Cristea V. 1998. Floristic and community diversity 1791, critically endangered in Romania, and a num- of sub-alpine and alpine grasslands and grazed dwarf-shrub 151/152: ber of other arctic-alpine moth species, declined ex- heaths in the Romanian Carpathians. Pirineos 73– 82. tremely during the last decades in the Bucegi Mts, and Collins S.L., Knapp A.K., Briggs J.M., Blair J.M. & Steinauer might even become extinct without conservation mea- E.M. 1998. Modulation of diversity by grazing and mowing sures (Rakosy et al. 2003; Dinca 2006). in native tallgrass prairie. Science 280: 745–747. Crawley M.J. & Harral J.E. 2001. Scale dependence in plant biodiversity. Science 291: 864–868. Cremene C., Groza G., Rakosy L., Schileyko A.A., Baur A., Er- Acknowledgements hardt A. & Baur B. 2005. Alterations of steppe-like grasslands in Eastern Europe: a threat to regional biodiversity hotspots. We thank L. Pop and M. Baur for field assistance, L. Rakosy Conserv. Biol. 19: 1606–1618. for advice, H.-P. Rusterholz and S. Zschokke for help with Curry J.P. 1994. Grassland Invertebrates Ecology, Influence on the data analyses, and J. Stöcklin, P. Stoll and two anony- Soil Fertility and Effects of Plant Growth. Chapman and Hall, mous reviewers for comments on the manuscript. This re- London, 437 pp. Dinca V. 2006. New data regarding several Lepidoptera species search was part of the scientific co-operation programme little known in Romania. Studia Universitatis ”Babes- between Switzerland and Eastern Europe (SCOPES) sup- Bolyai”, Biologia 50: 11–16. ported by the Swiss National Science Foundation. Dullinger S., Dirnböck T., Greimler J. & Grabherr G. 2003. A resampling approach for evaluating effects of pasture abandonment on subalpine plant species diversity. J. Veg. Sci. 14: References 243–252. Eilertsen O., Okland R.H., Okland T. & Pedersen O. 1990. Data manipulation and gradient length estimation in DCA ordina- Balmer O. & Erhardt A. 2000. Consequences of succession on tion.J.Veg.Sci.1: 261–270. extensively grazed grasslands for central European butter- Ellenberg H. 1996. Vegetation Mitteleuropas mit den Alpen. 5 fly communities: rethinking conservation practices. Conserv. edn. Eugen Ulmer, Stuttgart, 1096 pp. Biol. 14: 746–757. Grossu A.V. 1981. Gastropoda Romaniae. Ordo Stylommatopho- Barbulescu C. & Motca G. 1983. Pasunile muntilor inalti [The ra. Suprafams: Clausiliacea, Achatinacea. Universitatea din alpine pastures]. Editura Ceres, Bucuresti, 242 pp. Bucuresti, Bucuresti, 269 pp. Baur B. 1986. Patterns of dispersion, density and dispersal in Grossu A.V. 1983. Gastropoda Romaniae Ordo Stylommatophora Arianta arbustorum alpine populations of the land snail (L.) Suprafams: Arionaceae, Zonitaceae, Ariophantaceae si Heli- (Helicidae). Holarct. Ecol. 9: 117–125. caceae. Editura Litera, Bucuresti, 563 pp. Baur B., Joshi J., Schmid B., Hänggi A., Borcard D., Stary J., Hill M.O. & Gauch H.G. Jr. 1980. Detrended correspondence Pedroli-Christen A., Thommen G.H., Luka H., Rusterholz H.- analysis: an improved ordination technique. Vegetatio 42: 47– P., Oggier P., Ledergerber S. & Erhardt A. 1996. Variation in 58. species richness of plants and diverse groups of invertebrates ICAS. 1996. National Strategy and Action Plan for Biodiversity in three calcareous grasslands of the Swiss Jura mountains. Conservation and Sustainable Use of its Components in Ro- Rev. Suisse Zool. 103: 801–833. mania. ICAS, Bucuresti, Romania, 62 pp. Baur B., Schileyko A.A. & Baur A. 2000. Ecological observa- Ioras F. 2003. Trends in Romanian biodiversity conservation pol- tions on Arianta aethiops aethiops (Helicidae), a land snail icy. Biodivers. Conserv. 12: 9–23. endemic to the South Carpathian mountains. J. Molluscan Körner C. 1999. Alpine Plant Life. Springer, Berlin, 338 pp. Stud. 66: 285–289. Labaune C. & Magnin, F. 2002. Pastoral management vs. land Baur B., Cremene C., Groza G., Rakoszy L., Schileyko A.A., abandonment in Mediterranean uplands: impact on land snail Baur A., Stoll P. & Erhardt A. 2006. Effects of abandonment communities. Global Ecol. Biogeogr. 11: 237–245. of subalpine hay meadows on plant and invertebrate diversity Messerli B. & Ives J.D. 1997. Mountains of the World. The Pub- in Transylvania, Romania. Biol. Conserv. 132: 261–273. lishing Group, New York, 495 pp. Intensified grazing in the Southern Carpathians 445

Morris M.G. 2000. The effects of structure and its dynamics on Tasser E. & Tappeiner U. 2002. Impact of land use changes on the ecology and conservation of arthropods in British grass- mountain vegetation. Appl. Veg. Sci. 5: 173–184. lands. Biol. Conserv. 95: 129–142. ter Braak C.J.F. & Smilauer P. 2002. CANOCO Reference Man- Nagy L., Grabherr G., Körner C. & Thompson D.B.A. (eds) 2003. ual and CanoDraw for Windows User’s guide: Software for Alpine Biodiversity in Europe. Springer, Berlin, 477 pp. Canonical Community Ordination (version 4.5). Microcom- Niemelä J. & Baur B. 1998. Threatened species in a vanishing puter Power, Ithaca. habitat: plants and invertebrates in calcareous grasslands in Tuttin G.T., Heywood H.V., Burges A.N., Valentine H.D., Wal- the Swiss Jura mountains. Biodivers. Conserv. 7: 1407–1416. ters M.S. & Webb H.D. 1964–1980. Flora Europaea. Volumes Puscaru-Soroceanu E., Csuros D., Puscaru D. & Popova-Cucu A. 1–5. University Press, Cambridge, United Kingdom, 2392 pp. 1981. Die Vegetation der Wiesen und Weiden des Fagaras- Wäreborn I. 1970. Environmental factors influencing the distri- Gebirges in den Südkarpaten. Phytocoenologia 9: 257–309. bution of land molluscs of an oligotrophic area in southern Rakosy L., Goia M. & Kovacs Z. 2003. Verzeichnis der Schmetter- Sweden. Oikos 21: 285–291. linge Rumäniens. Societatea Lepidopterologica Romana, Wäreborn I. 1992. Changes in the land mollusc fauna and soil Cluj-Napoca, 446 pp. chemistry in an inland district in southern Sweden. Ecogra- SAS Institute. 1998. StatView. Cary NC, USA, SAS Institute Inc. phy 15: 62–69. Sternberg M., Gutman M., Perevolotsky A., Ungar D. & Kigel J. 2000. Vegetation response to grazing management in a Received June 7, 2006 Mediterranean herbaceous community: a functional group ap- Accepted February 6, 2007 proach. J. Appl. Ecol. 37: 224–237.