Arctic-Alpine plants in Bulgarian mountains/ Taxones artico-alpinos en las montanas de Bulgaria.
Many cold-adapted species are naturally distributed in both Arctic and the mountain ranges of Europe. The species with current occurrence limited to the high latitudes of Arctic and high altitudes of mountain ranges of Central and Southern Europe, particularly in the Alps, are referred as "arctic-alpine" or "alpine-arctic" plants (OBERDORFER, 1994). Because of past, climate-related species shifts, the highest mountains of southern Europe represent an important refuge for many survived species, which are widely distributed in the northern Palaearctic (Willis, 1994; WILLIS & VAN ANDEL, 2004; MEDAIL & DIADEMA, 2009). The high mountains of the Balkan Peninsula are a good example of regional refuge for arctic-alpine species (ASSENOV, 2006; STEVANOVIC & al., 2009). Some of these species are proven relics, based on macrofossil and pollen evidences (BIRKS & WILLIS, 2008). Others can be interpreted also as relics, survived in the Balkans during the cold stages of glaciations (STEVANOVIC & al., 2009; SCHMIDTT & al., 2010).
In recent years, arctic-alpine species have been the target of many studies, especially with regard to climate change (for overview, see e.g. THEURILLAT & GUISAN, 2001; PAULI & al., 2007). Other studies are focused on the genesis (STEHLIK, 2003; BIRKS, 2008; BHAGWAT & WILLIS, 2008; OZENDA, 2009; HABEL & al., 2010), species biology and ecology (BILLINGS & MOONEY, 1968; TASCHLER & NEUNER, 2004; IVERSEN & al., 2009; LARCHER & al., 2010), with special attention to their habitats and species relationships (HEEGAARD & VANDVIK, 2004; POMPE & al., 2010; FERNANDEZ & MOLERO, 2011; GAVILAN & al., 2012).
However, there are many gaps in the knowledge about the ecology and distribution of these species in Bulgaria. Therefore, the aims of the present study are (1) to identify the arctic-alpine element in the Bulgarian mountains, and (2) to ascertain the distribution patterns of these species in respect to their ecology and phytosociological affinity.
MATERIALS AND METHODS
A list of arctic-alpine species occurring in Bulgaria was created following chorotype determination by ASSYOV & PETROVA (2012) with corrections (of some boreal chorotypes) according to MEUSEL & al. (1965, 1978) and OBERDORFER (1994). Species with contemporary occurrences also in Scandinavia, and especially in Norway were objects of field observation. Data about species distribution in the country were extracted from literature (STOJANOFF, 1940; DELIPAVLOV & al., 2003; ASSYOV & PETROVA, 2012).
Following the information about known occurrences of these species as well as our previous experience, we focused on the highest mountains in Bulgaria--Rila (2925 m asl), Pirin (2914 m asl) and Stara Planina (2376 m asl) (Figure 1). Climate of the study areas is characterised by relatively high rainfall (1000 mm annual precipitation) and low temperatures (mean January--10.9[degrees]C, July 5[degrees]C). Snow cover lasts 190-200 days (Maateva, 2002). The study areas represent typical alpine surface of rocky slopes, mountain cliffs, and high mountain shrubs and pastures. They were chosen as to comprise different conditions of exposure, inclination and micro-habitat characteristics. The study area in Rila was 6.65 [km.sup.2], in Pirin 4.12 [km.sup.2] and in Stara Planina 13.75 [km.sup.2]. The localities were systematically sampled by 16 m2 plots, following the Braun-Blanquet approach (WESTHOFF & VAN DERMAAREL, 1978). We sampled a total of 219 plots. Distinct locations for the same species were considered those, outlying at least 50 m. In each plot we collected latitude/longitude, altitude and aspect using GPS (Garmin Etrex) and slope (inclinometer). field data was collected during 2009 and 2010.
The relationship between the number of plants, selected for observation and the vegetation cover of accompanying plants in the sample plots, was tested by simple linear regression. Spearman's rank correlation coefficient was calculated in order to test the dependence between, number of species and the cover of accompanying plants. The analyses were performed by Statistica 9.0 (Statsoft Inc).
The list of arctic-alpine plant species represented in bulgaria includes 38 taxa (Table 1). All species are distributed exceptionally in the mountains at the altitudinal range between 800 and 2900 m. The frequency of arctic-alpine plants increases at higher altitudes (figure 2). Different number of species was registered across mountain systems (figure 3). The highest number of arctic-alpine species is located in Rila Mt., followed by Pirin and Stara Planina Mts. Their spatial distribution is uneven and principally reflects their rarity. We registered 16 species from the list within the study sites. The most frequently occurring were Juncus trifidus, Poa alpina, Dryas octopetala, Bistorta vivipara, Antennaria dioica and Omalotheca supina (Figure 4).
The highest number (42.3%) of localities were facing north, regardless of the fact that study areas share all possible aspects. On southern slopes were placed 33.2% of the localities, while these facing east (17.3%) and west (3.7%) were less presented. Bistorta vivipara, Carex atrata, Empetrum nigrum and Oxyria digyna were registered only on north facing slopes. None of the observed species was discovered on southern slopes only. Detailed species distribution over the main directions is shown on Figure 5. The slope inclination varies between 3 and 46 degrees, most often it is 23.
All listed species have short growing period and are adapted for flowering within 2-3 months (Table 1). Seventy percent of listed arctic-alpine plants develop rhizomatous root system, which provides resources for fast growing and seed production in limited vegetation period.
In 77 plots (35.2%) there was only one arctic-alpine species, while in 142 plots (64.8%) more than one species were registered. High association with arctic-alpine plants exhibit Balkan endemic Dianthus microlepis Boiss. and Alpic-Carpathic-Balkanic Primula minima L. These species were registered in 25.6% and 16.4% of all sampled plots respectively. Endemics Primula deorum Velen and Geum bulgaricum Pancic, were observed together with other listed species in Rila Mt., while Papaver degenii (Urum. et Javorka) Kuzmanov was sampled locally in Pirin Mt.
Total vegetation cover in the sampled plots varies between 15 and 98%. The median of these values is 85%. In almost all plots there was moss layer covered from 1% to 40% of the plot. Bare rocks also were presented in some plots reaching up to 8% of the area. We established that besides Dianthus microlepis and Primula minima other plants, which accompany arctic-alpine species share a relatively small part of the total species cover in the vegetation. In case of high number of arctic-alpine plants in a sample plot, the group of other co-occurring plants has lower cover value. In the sample plots with highest abundance of arctic-alpine plants (7-10 species) the cover of accompanying species varies between 1 % and 48 %. Figure 6 shows the relationship between the cover of accompanying plants and the number of arctic-alpine species in studied plots.
GENERAL TRENDS IN DISTRIBUTION OF ARCTIC-ALPINE PLANTS IN BULGARIAN MOUNTAINS
Balkan Peninsula is known as one of the refuges for plant survival during glaciations (BIRKS & WILLIS, 2008). At this time both Rila and Pirin Mts were covered by ice, while Stara Planina Mt. was considered not permanently glaciated (VLASKOV, 2002). It is believed that during ice persistence many species from high latitudes have migrated southward and survived in the southern Europe, particularly in Balkans (OZENDA, 2009). Palynological data proves that during late glacial period steppe-mountain vegetation has been developed in high Balkan mountains (STEFANOVA & AMMAN, 2003; TONKOV & al., 2006). After ice withdrawal, the species demanding higher humidity and cold resistant started to climb up mountain slopes. This process was simultaneously accompanied by other local species, which certainly had more thermophilous nature, and thus influenced the ascent of current arctic-alpine plants. During following periods steppe-mountain vegetation was partly replaced by pines and temperate deciduous trees. In mountains of lower altitude such as Sredna gora Mt. (highest peak 1604 m) forest vegetation persist to date and provides very few suitable habitats for arctic-alpine plants. Eroded places and secondary grasslands there host only Antennaria dioica and Phleum alpinum.
Present distribution of arctic-alpine species in Bulgarian mountains reflects the migration routes and available space. Major routes are illustrated by STEVANOVIC & al. (2009). The number of species for Vitosha Mt. and the Rhodopes is the same, but Vitosha has much smaller territory, that ranks it up as mountain area with relatively high concentration of arctic-alpine plants. Its close proximity to Rila and similarity of rock types gives reason to assume existence of long lasting historical migration routes between them for many species. The Rhodopes are characterized by huge coniferous forests, much more similar to Boreal region than Arctic.
Our findings demonstrate that the studied plants establish and survive in high altitudes, at wind exposed northern slopes, as in other southern Europe mountains. The overall vegetation cover is low there and plenty of open space is available. Many authors (e.g. TASHLER & NEUNER, 2004; LARCHER & al., 2010; HABEL & al., 2010) suppose that the high ability to resist severe winds and low temperatures together with weak competition ability are the major driving mechanisms for arctic-alpine species occurrence. Observed species occupy the area above the timberline (with few exceptions as Diphasiastrum alpinum, Epilobium anagallidifolium, Omalotheca norvegica, Saxifraga paniculata, Phleum alpinum, Selaginella selaginoides and Antennaria dioica). This observation is in conformity with the overall arctic-alpine plant distribution at the southern range, reported also by other authors (TOMASELLI, 1991; BRUUN & al., 2006; GUTIERREZ & GAVILAN, 2010; VITTOZ & al., 2010).
Most of the studied species develop in rock and scree habitats. Natural or human induced disturbances provide additional space for plants demanding openings, such as Antennaria dioica and Omalotheca supina which are closely tied to patches, disturbed by erosion. On plane or slightly inclined terrains the surface is covered by soil of up to 20 cm depth and provides opportunity for development of tussock grasses as for example Nardus stricta, Sesleria comosa, Sesleria latifolia and Festuca nigrescens. The only arctic-alpine species registered there were Phleum alpinum and Bistorta vivipara. Considering the statement of GRABHERR (1989) that the "alpine grasslands can be defined as build of one or few keystone species and a couple of associates which are weak competitors", we could perceive as "keystone species" among listed plants only Juncus trifidus.
It is noteworthy that arctic-alpine species grow closely to each other and this is why they were often registered together in the sample plots. Such species association is justified by common ecological requirements (BILLINGS & MOONEY, 1968; Iversen & al., 2009; LARCHER & al., 2010). Juncus trifidus, Bistorta vivipara, Poa alpina, Dryas octopetala, Bartsia alpina and Omalotheca supina manifest the highest association ability. Dianthus microlepis and Primula minima should be mentioned as strong companions to the arctic-alpine plants in Bulgarian mountains.
Despite the fact that arctic-alpine species occupy small number of habitats, they take part in different syntaxa. According to our current knowledge (HORVAT & al., 1937; SIMON, 1958; MUCINA & al., 1990; ROUSSAKOVA, 2000; HAJEK & al., 2008), 7 classes should be mentioned as characteristic for the arctic-alpine plants in Bulgaria (see Table 1). Salicetea herbaceae is presented in Rila and Pirin Mts only. Carici rupestris-Kobresietea bellardii is registered only in Rila. Communities of Juncetea trifidi, occupying the highest alpine zone in Rila, Pirin, Stara Planina, Vitosha, Rhodope and Osogovo are broadly distributed. Vegetation tied to rocks and scree habitats is included in Asplenietea trichomanis and Thlaspietea rotundifolii, reported so far for Rila and Pirin, but our recent, not published data show their distribution in other mountains too. The alpine scree communities are extremely rich in rare and endemic species. Scheuchzerio-Caricetea nigrae and Montio-Cardaminetea are presented in all mountains but, occupy very limited areas.
IMPLICATIONS FOR CONSERVATION
We consider the competition between arctic-alpine plants and expanding populations of shrubs and tussock grasses extremely important. Our study allows us to conclude that the presence of open spaces is an important condition for the existence of the observed species. The limited presence of grasses there is perhaps conditioned by the shallow and unstable soil substrate and strong winds. However, this factor does not influence shrub expansion (ERSCHBAAMER & al., 2009). Juniperus sibirica manifests intensive population increase as a result of deceased or abandoned grazing (VELEV & APOSTOLOVA, 2008). By analogy, to a lesser extent same is true for Pinus mugo. Presence of Juniperus sibirica was registered in the half of the sample plots, while Pinus mugo was registered only in four locations. A similar concern for shrub invasion in other European mountain systems was stated also by other researchers (CHOLER & al., 2001; SCHOB & al., 2009).
The anthropogenic impact might be evaluated as low for the whole group of arctic-alpine species due to their relatively difficult accessibility. However, their small populations and significant fragmentation, together with the increasing touristic activities in the mountains are factors that should be considered as threatening. According to the National Red List of vascular plants (PETROVA & VLADIMIROV, 2009) Juncus triglumis and Rhodiola rosea are evaluated as critically endangered, because the first is known from a single location while the second is subject to active collection as medicinal plant. Another 6 species (see Table 1) are endangered. Species that are represented in few localities or by scarce populations are listed in the National Biodiversity Act (2008) as well.
It should be mentioned that all arctic-alpine species somehow prefer wet environment. Actively launched idea for climate warming and xerophytisation puts in jeopardy these species as they may lose their contemporary habitats. Following this scenario, these species will not outlive further warming, because there are no more appropriate upward territories for migration (they already occupy the top of the mountains) which is the case in many south--European regions (BIRKS, 2008; PAROLO & ROSSI, 2008).
This work was financially supported by the EEA Grants, Project BG0034-GAE-00100-E-V1--EEA FM. We thank the two reviewers for all suggestions that helped us to improve earlier version of the manuscript.
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Received: 12 February 2013
Accepted: 19 October 2013
Iva Apostlova, Hristo Pedashenko, Desislava Sopotlieva, Nikolay Velev, Kiril Vassilev & Tenyo Meshinev (*)
* Institute of Biodiversity and Ecosystem Research. Bulgarian Academy of Sciences. Sofia 1113, Bulgaria. E-mail: firstname.lastname@example.org, email@example.com, firstname.lastname@example.org, email@example.com, firstname.lastname@example.org, email@example.com
Table 1 List of arctic-alpine plants in Bulgaria (* CR-critically endangered, EN-endangered, VU-vulnerable, NT-near threatened, BDA-biodiversity act; ** Data on phenology is extracted from cited local flora) Conservation Species Distribution status * range in altitude (m) Low High -- Arabis alpina L. 1000 2900 -- Antennaria dioica (L.) 1700 2900 Gaertner -- Aster alpinus L. 1300 2900 NT Bartsia alpina L. 2100 2600 -- Bistorta vivipara (L.) S. F. 1600 2750 Gray -- Carex atrata L. 2000 2600 -- Cerastium alpinum L. 1300 1500 -- Cerastium cerastoides (L.) 2000 2900 Britton VU, BDA Diphasiastrum alpinum (L.) J. 1700 2100 -- rlulUD Dryas octopetala L. 2000 2900 EN, BDA Empetrum nigrum L. subsp. 2200 2700 hermaphroditum (Hagerup) Boscher Epilobium anagallidifolium 800 2500 Lam. -- Festuca airoides Lam. 1400 1800 EN Gentiana nivalis L. 1800 2900 -- Juncus trifidus L. 2000 2900 CR, BDA Juncus triglumis L. 2000 2500 EN, BDA Kobresia myosuroides (All.) 2100 2700 W. Koch EN, BDA Lloydia serotina (L.) Reichenb. 900 2900 -- Omalotheca norvegica (Gunn.) 900 1000 Schultz-Bip. et F. Schul. -- Omalotheca supina (L.) DC. 2000 2900 -- Oxyria digyna (L.) Hill. 1800 2800 -- Oxytropis campestris (L.) DC. 2500 2500 EN Pedicularis oederi Vahl 2000 2900 -- Pedicularis verticillata L. 1000 2900 -- Phleum alpinum L. 1600 2500 -- Poa alpina L. 1500 2000 -- Poa laxa Haenke 2000 2900 -- Potentilla crantzii (Crantz) 1800 2700 Beck ex Fritsch CR, BDA Rhodiola rosea L. 1800 2600 -- Sagina saginoides (L.) Karsten 1500 2900 -- Salix herbacea L. 2400 2900 -- Salix reticulata L. 2500 2900 VU Saxifraga oppositifolia L. 2300 2900 -- Saxifraga paniculata Mill. 800 2500 -- Saxifraga stellaris L. 1800 2500 -- Selaginella selaginoides (L.) 2200 2800 Link EN Sibbaldia procumbens L. 2000 2800 -- Silene acaulis (L.) Jacq. 2200 2900 Conservation Occupancy in vegetation Start Fowering status * classes flowering duration (month) (months) ** ** -- Thlaspietea rotundifolii IV 5 -- Salicetea herbaceae, Juncetea trifidi, V 4 Thlaspietea rotundifolii -- Carici rupestris-Kobresietea VI 3 bellardii, Asplenietea trichomanis, Thlaspietea rotundifolii NT Salicetea herbaceae, VII 2 Thlaspietea rotundifolii VI 3 -- Juncetea trifidi -- Asplenietea trichomanis, VII 2 Thlaspietea rotundifolii -- Thlaspietea rotundifolii VII 2 -- Salicetea herbaceae, Scheuchzerio-Caricetea nigrae VI 3 VU, BDA Juncetea trifidi VII 3 -- Carici rupestris-Kobresietea VI 3 bellardii, Juncetea trifidi, Thlaspietea rotundifolii EN, BDA Thlaspietea rotundifolii VI 2 Salicetea herbaceae, VII 3 Scheuchzerio-Caricetea nigrae, Montio-Cardaminetea -- Juncetea trifidi VI 2 EN Carici rupestris-Kobresietea VII 2 bellardii, Juncetea trifidi -- Salicetea herbaceae, Carici VII 2 rupestris-Kobresietea bellardii, Juncetea trifidi, Thlaspietea rotundifolii CR, BDA Scheuchzerio-Caricetea nigrae VII 2 EN, BDA Carici rupestris-Kobresietea VI 3 bellardii, Thlaspietea rotundifolii EN, BDA Carici rupestris-Kobresietea VII 2 bellardii, Thlaspietea rotundifolii -- Asplenietea trichomanis, VI 4 Thlaspietea rotundifolii -- Salicetea herbaceae, Juncetea VI 4 trifidi, Asplenietea trichomanis, Thlaspietea rotundifolii -- Salicetea herbaceae, VII 2 Thlaspietea rotundifolii -- Carici rupestris-Kobresietea VII 3 bellardii, Thlaspietea rotundifolii EN Juncetea trifidi, Thlaspietea VI 2 rotundifolii -- Juncetea trifidi, Thlaspietea VII 2 rotundifolii -- Juncetea trifidi VIII 2 -- Juncetea trifidi, Thlaspietea VI 2 rotundifolii -- Juncetea trifidi, Thlaspietea VI 2 rotundifolii -- Juncetea trifidi VI 4 CR, BDA Thlaspietea rotundifolii VI 3 -- Salicetea herbaceae, VI 3 Juncetea trifidi -- Salicetea herbaceae VI 2 -- Salicetea herbaceae VI 2 VU Asplenietea trichomanis VII 2 -- Carici rupestris-Kobresietea V 2 bellardii, Asplenietea trichomanis -- Scheuchzeri-Caricetea nigrae, VII 3 Montio-Cardaminetea -- Juncetea trifidi, Thlaspietea VII 3 rotundifolii EN Salicetea herbaceae, VI 3 Asplenietea trichomanis, Thlaspietea rotundifolii -- Juncetea trifidi, VII 2 Thlaspietea rotundifolii
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|Title Annotation:||articulo en ingles|
|Author:||Apostlova, Iva; Pedashenko, Hristo; Sopotlieva, Desislava; Velev, Nikolay; Vassilev, Kiril; Meshinev|
|Date:||Jan 1, 2013|
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