Introduction
Secondary dry grassland communities in the Mediterranean have a zoo-anthropogenic origin; they have developed over centuries or even millennia of traditional land use, featuring practices such as mowing, grazing, temporary abandonment of arable fields, and/or other disturbance regimes (Apostolova et al. 2014,Valkó et al. 2018). Mediterranean and sub-Mediterranean dry grasslands are considered to be among the floristically richest vegetation types (Apostolova et al. 2014) and, at the same time, a very important habitat for endangered, rare and endemic species, so they are included in the list of Habitats of European Interest (Council Directive 92/43/EEC on the conservation of natural habitats and of wild fauna and flora, 1992), as well as the European Red List of Habitats (Janssen et al. 2016). Compared to other parts of Europe, dry grasslands of the Balkan peninsula are still well preserved (Apostolova et al. 2014).
The Balkan peninsula is well known for its rich flora and well-preserved vegetation, because it was a glacial refuge for animal and plant species (Griffiths et al. 2004). Its biodiversity is considered to be among the highest in Europe (Apostolova et al. 2014). The peninsula is characterized by the presence of a broad spectrum of dry grasslands (e.g.,Horvat et al. 1974,Jovanović et al. 1986,Apostolova et al. 2014,Terzi 2015,Aćić et al. 2015,Matevski et al. 2018). In some Balkan countries (Slovenia, Serbia, Bulgaria, Croatia, North Macedonia), dry grassland vegetation has been intensively researched (Apostolova et al. 2014,Matevski et al. 2018). In contrast to these countries, research into this type of vegetation in Montenegro has considerable discontinuity, and comprenhensive studies, especially in the sub-Mediterranean and Mediterranean region, are rare (Pulević and Bulić 2012).
In our study, we focused on research into Asphodelus ramosus-dominated vegetation. Asphodelus ramosus is a species native to the Mediterranean and Macaronesian regions: southern Europe, northern Africa, the Middle East, Mediterranean islands and Canary Islands. It can be found in forest edges and grasslands, generally on basic soils of a certain depth, forming very dense populations in grazed areas, from the coast up to 1000 m, occasionally reaching 2150 m in the mountain systems of North Africa (Diaz-Lifante and Valdés 1996). It is unpalatable for grazing animals.
Research into plant communities dominated by Asphodelus spp. (and Asphodelus ramosus in particular) has become very intensive in recent years, especially in the western and central Mediterranean (Allegrezza et al. 2015,Biondi et al. 2016,2017). In the Balkan peninsula, similar vegetation has been described from Albania (Fanelli et al. 2015) and Croatia (Horvatić 1934,1939,1963,Šegulja 1969,1970,Hećimović 1984,Jasprica and Ruščić 2013,Jasprica et al. 2016).
Today, there are different opinions about the syntaxonomical classification of Asphodelus ramosus dominated vegetation in Europe and its position in the landscape (as grasslands or fringe (saum) communities). In the eastern Adriatic, these communities have been classified within the grassland class Festuco-Brometea, while in the central and western Adriatic, they have been classified as heliophilous edge vegetation of Trifolio-Geranietea sanguinei (Biondi et al. 2014,Allegrezza et al. 2015) or recently into a new class Charybdido pancratii-Asphodeletea ramosi Biondi et al. 2016 (Biondi et al. 2016,2017).
The aim of this study was to (i) contribute to knowledge of the composition of dry grasslands dominated by Asphodelus ramosus in Montenegro and (ii) compare examples of Asphodelus ramosus dominated vegetation along the Adriatic and its syntaxonomical classification and classification into Natura 2000 habitat types.
Material and methods
Study area
Ćemovsko polje is a part of Zetska ravnica plain in Montenegro, between the rivers Morača, Cijevna and Ribnica. It covers 165 km2 and extends from Podgorica, the capital of Montenegro, to Skadar Lake. The altitude of the investigated area ranges from 12 to 30 m a.s.l. During the Pleistocene period, moraine material eroded from the mountains was carried along the rivers Morača and Cijevna into the area of Ćemovsko polje (Radojičić 2015). The dominant types of soil are eutric cambisol and rendzina, which are formed on fluvio-glacial deposits, and consequently are often shallow and skeletoid (Burić et al. 2017). The area of Ćemovsko polje has a Mediterranean climate with hot summers – Csa (Burić and Micev 2008). A grassland ecosystem is dominant in this area. The studied Asphodelus ramosus-dominated vegetation occurs in pastures used for grazing by cattle and sheep. A significant area of Ćemovsko polje is occupied by vineyards and plantations of peach and other kinds of fruit (Radojičić 2015). The area investigated has also recently been heavily impacted by urbanization (Burić et al. 2017).
Although many floristic studies have been performed in the area of Ćemovsko polje (Černjavski et al. 1949,Hadžiablahović 2010, 2018,Stešević et al. 2014), the vegetation has remained poorly studied (Černjavski et al. 1949,Hadžiablahović 2018). Potential natural vegetation of the wider area of Podgorica and Lake Skadar is Apulian-southeast Adriatic meso-supra-Mediterranean Quercus trojana forests with Pistacia species (Bohn et al. 2000-2003) or precisely Macedonian oak forest ‘Quercetum trojanae montenegrinum Blečić et Lakušić 1975’ (recte: Quercetum trojanae Em 1958). Illyrian sub-Mediterranean rocky grasslands on shallow calcareous soils of the alliance Chrysopogono grylli-Koelerion splendentis Horvatić 1973 prevail in the area of Ćemovsko polje (Hadžiablahović 2010).
Sampling and data analysis
From April to June 2019, we sampled Asphodelus ramosus-dominated plant communities on Ćemovsko polje according to the Braun-Blanquet method (Braun-Blanquet 1964). We made 17 relevés and the size of plots was 25 m2. The minimum distance between plots was 100 m. The minimum coverage value of Asphodelus ramosus for it to be considered dominant was 25%. Each plot was visited in April and again in June. Cover values of species and total vegetation cover are based on the summer aspect (Tab. 1, Appendix 1). GPS coordinates were recorded for each plot (Appendix 2). All relevés made during fieldwork and relevés from the literature were entered into the Turboveg (Hennekens and Schaminée 2001) database. Relevés from the literature were used for comparison with vegetation data from our fieldwork (Appendix 3).
We obtained characteristic species of the association Bromo erecti-Chrysopogonetum grylli according to Horvatić (1963). Diagnostic taxa of alliance and order were assigned according to Terzi (2015), while the diagnostic taxa of classes were determined according to Terzi (2015) for the class Festuco-Brometea, Mucina et al. (2016) for other classes and Biondi et al. (2016) for the class Charybdido pancratii-Asphodeletea ramosi.
Non-metric multidimensional scaling (NMDS,Kruskal 1964) was used to examine the overall variation in the species composition in the whole relevé dataset. Hellinger transformation of percentage cover values (5=87.5%, 4=62.5%, 3= 37.5%, 2=12.5%, 1=2.5%, +=0.5%, r=0.1%) was used and Bray-Curtis as a measure of dissimilarity. NMDS was performed using the R package ‘vegan’ (Oksanen et al. 2017). For ecological interpretation of vegetation patterns, ecological indicator values (Pignatti et al. 2005) were passively projected onto the NMDS graph. Weighted by species cover, mean indicator values were calculated for each relevé using JUICE software (Tichý 2002).
The nomenclature of taxa is in accordance with Euro+Med (2006) and the nomenclature of higher syntaxa according to Mucina et al. (2016).The taxonomy of Asphodelus ramosus species was sometimes ambiguous. Previously, the species Asphodelus microcarpus Viv. was accepted as valid by many authors but, after a taxonomic revision of the genus Asphodelus in the western Mediterranean (Diaz-Lifante and Valdés 1996), it has been considered a synonym of Asphodelus ramosus L. (Euro+Med 2006).
Results
The Asphodelus ramosus plant community from Ćemovsko polje (Montenegro) is represented by 17 relevés in the phytosociological table (Tab. 1). The dominant species of the association are Asphodelus ramosus and Chrysopogon gryllus, while the most frequent species are Asphodelus ramosus, Sanguisorba minor, Poa bulbosa, Teucrium capitatum, Sideritis romana subsp. purpurea, and Anacamptis papilionacea. Asphodelus ramosus is also considered to be the only characteristic species of the association. The community develops in two clear phenological aspects. In the spring aspect (Fig. 2A), the dominant species is Asphodelus ramosus, while in summer (Fig. 2B), dominance is taken by the tall grass Chrysopogon gryllus. The spring aspect is also characterised by high frequency and coverage of Anemone hortensis, Poa bulbosa and Sanguisorba minor, and the summer one by Bupleurum veronense and Teucrium capitatum.
In addition to the species characteristic for the class Festuco-Brometea, there are several species of annual and ephemeral grasslands of the classes Stipo-Trachynietea distachyae and Helianthemetea guttate, and seasonal perennial and ephemeroid pastures of the class Poetea bulbosae, all indicating the Mediterranean and grassland character of the studied plant community. The impact of grazing is evident from the many ruderal species: Avena barbata, Scandix pecten-veneris, Daucus guttatus, Scolymus hispanicus, Bromus squarrosus, Euphorbia exigua, Sonchus oleraceus (Tab. 1). The studied stands constitute an open grassland community, which develops on stony soil and is used for grazing (cattle and sheep). Total vegetation coverage is 60 – 80% in the summer aspect. Stones and pebbles have dimensions of up to 20 cm and their cover is 5 – 40%. If the stones are removed and these areas are used for mowing, the vegetation changes into dry grasslands of the alliance Vulpio-Lotion (Hadžiablahović 2018).
Using various numerical classifications, we tried to classify the association Bromo erecti-Chrysopogonetum grylli into subassociations. This kind of vegetation is fairly uniform in the study area, and there were no ecologically evident/logical subunits.
A comparison of the studied Asphodelus community from Montenegro with Asphodelus ramosus-dominated communities from around the Adriatic (Fig. 1) revealed two distinct vegetation groups (Tab. 2,Fig. 3). Communities from Albania, Croatia and Montenegro form one group, with abundant grassland species of the class Festuco-Brometea, which are not present in the second group of edge communities from Italy. Two dimensional solution of the NMDS ordination attained a minimum stress of 0.21. The NMDS ordination clearly distinguishes the two groups along gradients of nutrients, light and soil reaction. Edge communities from Italy thrive on more nutrient-rich, shaded sites (Fig. 3).
Based on floristic composition and all the comparative analyses, we decided to classify the studied stands dominated by Asphodelus ramosus into the already described grassland association Bromo erecti-Chrysopogonetum grylli.
Discussion
In recent years, several studies on the distribution and dynamics of plant communities with Asphodelus ramosus have been performed, especially in the central and western Mediterranean (Biondi et al. 2016,Biondi et al. 2017). In contrast, this type of vegetation has been poorly studied in Montenegro.
The association Bromo erecti-Chrysopogonetum grylli was described for the first time in Croatia (Island of Pag,Horvatić 1934), with two subassociations (Bromo-Chrysopogonetum grylli dorycnietosum herbacei and Bromo-Chrysopogonetum grylli asphodeletosum microcarpi), and classified in the alliance ‘Chrysopogoneto-Satureion subspicatae Horvat i Horvatić 1934’ (recte: Chrysopogono grylli-Koelerion splendentis), order ‘Brometalia erecti Br. Bl.’ Subsequently, Bromo-Chrysopogonetum grylli asphodeletosum microcarpi was raised by Horvatić (1963) to the rank of association, with the name Asphodelo microcarpi-Chrysopogonetum grylli, and included in the order ‘Scorzonero-Chrysopogonetalia H-ić et Ht (1956) 1958’ (recte: Scorzoneretalia villosae). The association has so far been reported in Montenegro and Albania (Černjavski et al. 1949,Fanelli et al. 2015,Hadžiablahović 2018). In his nomenclatural revision of the order ‘Scorzonero villosae-Chrysopogonetalia grylli Horvatić et Horvat in Horvatić 1963’, Terzi (2011) considered the associations Asphodelo-Chrysopogonetum grylli and Bromo-Chrysopogonetum grylli to be valid, while Terzi (2015) later united them and retained the earlier valid name, Bromo-Chrysopogonetum grylli (cf.Theurillat et al. 2021).
In Montenegro, Bromo erecti-Chrysopogonetum grylli was reported by Blečić and Lakušić (1976) in the coastal part of Montenegro, as well as in the vicinity of Podgorica, and by Černjavski et al. (1949) and Hadžiablahović (2018) in the area of Skadar Lake. These publications were not supported with phytosociological studies and it was not possible to make a comparison with our results from Ćemovsko polje. According to Černjavski et al. (1949), Bromo-Chrysopogonetum grylli is developed on stony hills with thin soils, while our researched stands are found in the lowlands of Ćemovsko polje on deeper alluvial soils. According to Černjavski et al. (1949)Bromo-Chrysopogonetum grylli is characterized by many species of shrub vegetation (Paliurus spina-christi, Salvia officinalis, Rubus ulmifolius, Euphorbia veneta, Helichrysum italicum, Ruscus aculeatus, Cyclamen neapolitanum, Arum italicum, Phlomis fruticosa, Cistus villosus, Cistus salviaefolius, Nephrodium filix-mas, Pteridium aqiulinum, etc.) and chasmophytic vegetation (Asplenium trichomanes, Edraianthus tenuifolius, Cardamine glauca, Silene quadridentata, Ceterach officinarum, Sedum album, Moltkea petraea, etc.) that were absent from our stands from Ćemovsko polje. Further investigation of the association Bromo-Chrysopogonetum grylli reported by Černjavski (1949) is needed to determine whether there are differences in relation to our community from Ćemovsko polje.
Fanelli et al. (2015) reported Asphodelo-Chrysopogonetum grylli in Albania in the Buna River protected landscape and it shows high similarity with associations from Montenegro and Croatia. The species Cytisus spinescens, which is a characteristic species of the association (Horvatić 1963) is not present in stands from Montenegro and Albania. Stands from Montenegro are also characterized by an absence of species characteristic of dry grasslands of the classes Festuco-Brometea – Salvia officinalis and Bromopsis erecta.
According to Horvatić (1934,1939), the development and distribution of Bromo-Chrysopogonetum grylli asphodeletosum microcarpi is conditioned by agro-pastoral activities, i.e., moderate grazing. In the case of Ćemovsko polje, it is grazed particularly by sheep and rarely by cattle. Intensive and permanent grazing leads to degradation of this community, which is especially evident from the absence of Asphodelus ramosus from relevés on Rab island (Horvatić 1939). Intensive grazing leads to a higher abundance of shrubs (Helichrysum italicum, Cytisus spinescens, Euphorbia spinosa, Salvia officinalis) (Horvatić 1934), or ruderal and subruderal species (Fanelli et al. 2015). Overgrazed stands can be included in the order Carthametalia lanatae (Artemisietea vulgaris) because of abundant therophytes: Carthamus lanatus, Dasypyrum villosum, Catapodium rigidum, Nigella arvensis, etc. (Fanelli et al. 2015). On the other hand, stands are abandoned, after which succession leads to Rhamno-Paliuretum Trinajstić 1996, or are turned into mowed grasslands of the Vulpio-Lotion Horvatić 1963 alliance (Hadžiablahović 2018).
In several localities in Croatia along the Adriatic coast, similar vegetation types with Asphodelus ramosus have been reported. Narcisso tazettae-Asphodeletum microcarpi was described in Istria (Šegulja 1970). The same association was later reported on the islands of Bobara and Mrkan (Hećimović 1984), Supetar (Jasprica and Ruščić 2013) and Olib (Jasprica et al. 2016). Originally, it was classified into Scorzonerion villosae, but was later moved to Chrysopogono grylli-Koelerion splendentis. Ecological conditions are different to those of Asphodelo ramosi-Chrysopogonetum grylli and it occurs on deep skeletoid soils and under the influence of salt spray (Šegulja 1969). According to Jasprica et al. (2016), the association is considered to be the most thermophilous grassland along the eastern Adriatic coast. The characteristic species of the association are Asphodelus ramosus, Narcissus tezzeta and Orchis papilionacea. Thermophilous grassland communities with domination of Asphodelus ramosus have a distribution along the eastern Adriatic, influenced by the Mediterranean climate.
There is a different situation along the western Adriatic coast, where Asphodelus ramosus-dominated communities are considered to be heliophilous fringe and tall-herb vegetation, which develops after the abandonment of agro-pastoral activities (Tesei et al. 2020). Comprehensive studies on heliophilous edge vegetation have been performed in Italy (Gargano peninsula, central part of the Apennines, northern part of Sardinia) and southern Spain (Biondi et al. 2016, 2017). As a result, a new class of edge vegetation Charybdido pancratii-Asphodeletea ramosi was described, focused on areas with a Mediterranean macrobioclimate (Biondi et al. 2016,2017).
The proposal to update the EuroVegChecklist (Mucina et al. 2016) by adding this new class was provisionally rejected by the European Vegetation Classification Committee of the European Vegetation Survey working group of the International Association of Vegetation Science, due to the lack of evidence concerning a clear floristic delimitation of Charybdido pancratii-Asphodeletea ramosi from Lygeo sparti-Stipetea tenacissimae and Trifolio-Geranietea sanguinei (Biurrun and Willner 2020). Nonetheless, we can accept the existence of a new fringe class replacing Trifolio-Geranietea in the Mediterranean, but we are of the opinion that Bromo erecti-Chrysopogonetum grylli clearly represents grassland vegetation erroneously classified as fringe vegetation by Biondi et al. (2016). This is clearly indicated by the numerous species of Festuco-Brometea present in stands (Tab. 2) from eastern Adriatic Asphodelus-dominated communities. Fringe communities with Asphodelus ramosus from Italy, due to overgrazing, are dominated by monocotyledons, many of them toxic to animals, while in Montenegro these areas represent pastures. Another difference is the presence of shrub species with higher cover in stands of Charybdido-Asphodeletea ramosi (Paliurus spina-christi, Olea europaea, Pinus halepensis), missing in grasslands from the eastern Adriatic.
According to Biondi et al. (2016) the diagnostic species of the newly described class are Asphodelus ramosus subsp. ramosus, A. fistlosus, A. tenuifolius, A. ayardii, Charybdis pancration, C. maritima, C. glaucophylla, C. aphylla, C. hesperia, Thapsia garganica, Asparagus acutifolius, Ornithogalum etruscum subsp. umbratille, Anemone hortensis, Carlina corymbosa, Hypochoeris radicata, Iris planifolia, I. bicapitata, Asphodeline liburnica, A. lutea, Ferula communis, F. communis subsp. cardonae, F. glauca, F. arrigonii and Hermodactylis tuberosus. The diagnostic species group of Charybdido-Asphodeletea should also be revised, since many of them are attributed to other vegetation classes (Festuco-Brometea, Lygeo sparti-Stipetea tenacissimae, Ononido-Rosmarinetea etc.) according to Mucina et al. (2016). Asphodelus ramosus, Anemone hortensis, Carlina corymbosa and Hypochoeris radicata, which are considered to be character species by Biondi et al. (2016), are also very frequent in grassland vegetation of Bromo erecti-Chrysopogonetum grylli.
In terms of Natura 2000 habitat types (Council Directive 92/43/EEC on the conservation of natural habitats and of wild fauna and flora, 1992) there are differences between grassland and fringe communities dominated by Asphodelus ramosus. Heliophilous Asphodelus spp. edge communities in the western and central Mediterranean do not represent any habitats of European Community interest and a progressive increase in Asphodelus spp. cover in grasslands can result in the disappearance of grassland habitat types (Tesei et al. 2020). According to a report of habitat types of Montenegro important for the European Union (Petrović et al. 2019), Bromo erecti-Chrysopogonetum grylli is classified within the Eastern sub-Mediterranean dry grasslands (Scorzoneretalia villosae) habitat type (code 62A0). The same situation applies to Narcisso tazettae-Asphodeletum microcarpi in Croatia (Jasprica et al. 2016).
Syntaxonomical scheme
Based on the analyses performed, the following syntaxonomical scheme is proposed for Asphodelus ramosus-dominated communities in the Adriatic region.
Festuco-Brometea Br.-Bl. et Tx. ex Soó 1947
Scorzoneretalia villosae Kovačević 1959
Chrysopogono grylli-Koelerion splendentis Horvatić 1973
Bromo erecti-Chrysopogonetum grylli Horvatić 1934
Narcisso tazettae-Asphodeletum microcarpi Šegulja 1969
Artemisietea vulgaris Lohmeyer et al. ex von Rochow
Asphodelus ramosus community
Charybdido pancratii-Asphodeletea ramosi Biondi in Biondi et al. 2016
Asphodeletalia ramosi Biondi in Biondi et al. 2016
Charybdido pancratii-Asphodelion ramosi Biondi et al. 2016
Charybdido pancratii-Asphodeletum ramosi Biondi et al. 2016
Alkanno tinctoriae-Asphodeletum ramosi Biondi et al. 2016
Euphorbio characiae-Thapsietum garganicae Biondi et al. 2017
Asphodelo ramosi-Ferulion communis Biondi et al. 2016
Asphodelo ramosi-Feruletum communis Biondi et al. 2016
Asphodelino luteae-Feruletum communis Biondi et al. 2016