An update to the genus Bolboschoenus in Bulgaria - species diversity, distribution and phytosociological affinities

The current study presents new data on the distribution of the representatives of the genus Bolboschoenus in Bulgaria and gives a brief description of their communities. It is based on revision of herbarium materials, field observations and phytosociological samples. Morphological characteristics and ecological traits of the studied taxa are commented. A synopsis of all collected chorological information is attached.


Introduction
The account of the genus Bolboschoenus (Asch.)Palla (Cyperaceae) for the Bulgarian flora [1] includes only B. maritimus (L.) Palla with seven varieties (monostachys, polystachys, compactus, macrostachys, bornmulleri, maritimus, and laxiflorus).These varieties were distinguished solely on the basis of differences in inflorescence structure.For the Flora Europaea, DeFilipps [2] had adopted broader concept including Bolboshoenus in Scirpus L. at section level, recognizing two subspecies S. maritimus L. subsp.maritimus and S. maritimus subsp.affinis (Roth) T. Norlindh for the territory of the Old World.Over the last 25 years, research on the genus has largely clarified its taxonomy and established species diversity of sixteen species worldwide [3], six of which are represented in Europe [4].It became clear that carpological characters are most important in discrimination of species within the genus and inflorescence features are of lower significance since the latter being often affected by ecological conditions [5], [6], [7].The accumulation of new taxonomic information and improvement of classification of Bolboschoenus induced many regional studies especially in Europe [6], [7], [8], [9], [10].However, diversity, distribution and phytosociological affinities of Bolboschoenus spp. in Bulgaria have been not summarized according newly accepted taxonomy.
Among the European species, Bolboschoenus glaucus (Lam.) S. G. Smith and B. planiculmis (F.Schmidt) T.V. Egorova has been already reported to Bulgaria [11], [12], though without reference to representative material.Further extensive revision of herbarium collections at the indexed Bulgarian herbaria SO and SOM [13] raised the number of species in Bulgaria to four [5], adding B. laticarpus Marhold, Hroudová, Duchácek & Zákr to already noted B. planiculmis, B. glaucus and B. maritimus s. str.Yet, in the most recent floristic synopses on the flora of Bulgaria [14], [15], [16], the novel data on the taxonomic and biogeographic limits of the species within Bolboschoenus were incompletely amended.
Data on the distribution of Bolboschoenus maritimus s. l. in Bulgaria could be traced in many published floristic and phytosociological works and several MSc or PhD theses.Most important of

Results and Discussion
The present study confirms the results of previous studies [5] on occurrence of four species of genus Bolboschoenus in Bulgaria.The most important characters used for discrimination of the individual taxa within the genus are indeed, those related to achene morphology and anatomy.The identification keys proposed by various authors [5], [6], [7], [16] has been proved useful and reliable for differentiation of Bolboschoenus taxa within Bulgarian populations.

Chorological data
Among the Bulgarian species, B. glaucus is the most widespread.It occupies 77 (10x10 km) UTM grid squares within the most of the floristic regions of the country, excluding Strandzha, The Rhodopes (West) and (Central), Rila, Pirin (North), Belasitsa, Slavyanka, Struma Valley (North), Znepole and Sofia Regions (Figure 1A).It is recognized by the inflorescence bearing many rays, and the achenes -smallest among all of the representatives of the genus in Bulgaria.The exocarp, visible in transverse section of achene made across upper 1/3 -very thin, outer surface smoot and glossy.The exocarp/mesocarp ratio is about 1:5 (1:8) (Figure 2A-A1).Compared to the other representatives, the species is more thermo-and xerophilic.It is often seen in shallow, temporarily wet depressions that completely dry out in summer.The flowering period begins comparatively earlier of about 2 to 4 weeks, thus ripe fruits may be collected as early as mid-June.However, the letter observation need to be supported with additional phenological studies.The vertical limits of the species reaches 710 m a.s.l at 'Arkata' reservior (Appendix B).In Europe B. laticarpus is most frequent in its central region, while it is restricted on South [5], [19], which is the reason it is the most rare representative of the genus in Bulgaria -lack of optimal conditions at the periphery of its range limits its distribution in the country.It has been confirmed to Bulgaria from four locations only, three of which are known only from herbarium records (Appendix A).It is registered at four UTM grid squares and the floristic regions Black Sea coast (South), Tundzha Hilly Country, and Forebalkan (West) (Figure1B).A single population has been registered at the field during the present study (Appendix B).The species is most similar to B. glaucus and it is hardly distinguished from the latter at in situ environment based only on general morphology.The achene length/width ratio is ca.3x2 mm, achene surface somewhat dull, a bit larger than and not as shiny as in B. glaucus.The exocarp/mesocarp ratio is mostly 1:3 (1:2) (Figure 2B-B1).The observed population consisted of several groups of individuals each covering an area of 1-2 m 2 , distributed in about 50 m section of a small river.At the locality, the species was associated with Phragmites australis, Schoenoplectus lacustris, Typha latifolia, Iris pseudacorus, Paspalum distichum, Cyperus longus, Calamagrostis epigejos, Xanthium orientale subsp.italicum, Sonchus arvensis subsp.uliginosus, Stachys palustris, Lycopus exaltatus, and Urtica dioica.
B. maritimus was found frequently and with high population density mostly along the Black Sea coast and to a certain extent in SE Bulgaria, while in the remaining regions, explored during present study it was found significantly less frequently and with low abundance.The area of occupancy includes 30 UTM grid squares and the floristic regions of the Black Sea coast, Northeast Bulgaria, The Balkan Mts (East), Tundzha Hilly Country, Thracian Lowland, and Sofia (Figure 1C).It has been found mainly on the shores of brackish water bodies, which shows its higher salt tolerance comparing with the rest of the Bulgarian species of the genus, which is in line with previous studies [5], [7].Beside the exhibit salinity tolerance the species is recognized by its (sub-)sessile inflorescence, occasionally bearing 1-3 rays, each with 1-3(-4) spikelets.The achenes are relatively large, surface more or less dull, with conspicuous smooth polygonal reticulation, exocarp/mesocarp ratio usually 2:1 (Figure 2C-C1).
In Bulgaria B. planiculmis has been registered at 30 UTM grid squares and Struma Valley (North), Znepole, Sofia, Thracian Lowland, Sredna gora Mts (West), Balkan Mts (East), Northeast Bulgaria, The Black Sea coast (North), Forebalkan, and The Danubian plain floristic regions (Figure 1D).It is recognized by its slender habit, inflorescence often (sub-) sessile with predominantly bifid styles, often formed by a single spikelet.Achenes length/width 3-3.5 x 2-2.5 mm, usually broader in comparison to the rest Bolboschoenus spp. in Bulgaria, biconcave or flat-concave in cross section, exocarp/mesocarp ratio 1:1 (Figure 2D-D1).It is more common and abundant in Northwest and South-central Bulgaria.It is often found along with B. glaucus at the peripheries of artificial ponds, e.g.reservoirs, gravel pits, fishponds, or ricefields.However, in such cases both species usually colonize different parts of littoral zone.B. glaucus, being more xerophilous, colonize the upper littoral zone that drains earlier in the season, while B. planiculmis is commonly observed in the lower littoral zone, often semi-submerged in shallow (0.05-0.20 cm) water.

Phytosociological affinities
Representatives of the genus on the territory of Bulgaria often dominate a wide range of wet habitats, including coastal and inland salt marshes, coastal zones of freshwater bodies and temporarily wet pools on the periphery of arable land.They inhabit mostly disturbed sites with considerable silt accumulation.The preliminary analysis, based only on differences in floristic composition and ecological traits of 27 phytocenological samples collected during the present study shows differentiation of four groups of communities with dominance or high abundance of Bolboschoenus spp.
The communities with B. maritimus develop on sandy or sand-mud substrates mainly along the Black Sea coast and along Tundzha River.The species composition of these communities varies significantly even in neighbouring stands.It is mostly poor, including many typical hygrophytes and (sub-) halophilic species, as well as ruderals, such as Phragmites australis, Typha spp., Tripolium pannonicum, Symphyotrichum squamatum, Polypogon monspeliensis, Artemisia santonicum, Xanthium orientale subsp.italicum, Pulicaria dysenterica, Elymus elongatus, Suaeda maritima, Samolus valerandi, Centaurium spicatum, Equisetum ramosissimum, Bromus diandrus, Solanum dulcamara, etc.According to the recent classification of inland Bolboschoenus-dominated vegetation [23], saline Bolboschoenus associations of coastal areas are classified to the alliance Scirpion maritimi Dahl et Hadač 1941, while inland freshwater communities dominate by Bolboschoenus spp.were grouped into Meliloto dentati-Bolboschoenion maritimi Hroudová, Hrivnák & Chytrý 2009.Two type of communities with B. maritimus could be recognized also in Bulgaria.However, the species composition of the Bulgarian communities is somewhat different from those in Central Europe, therefore at present assignment to a lower syntaxonomic units is not considered due to insufficient data set.
B. glaucus dominated communities in Bulgaria were noted mostly in the periphery of freshwater basins in the interior of the country, often observed over the shallow banks and at the inflow zone of artificial ponds, in wet depressions of alluvial terraces at lower course of many rivers, roadside ditches, and at the margins of arable land.B. glaucus was noted at the margins of rice paddy fields, although it is rarely abundant in such communities.The substrates were often clayey, retaining moisture even during dry period.The colonies are often dense and monospecific.In the hot months of the year B. glaucus stands are often grazed, since it is nearly the only fresh source of fodder available in the lowlands during dry period.This explain why these communities are influenced by many ruderal species.The species composition includes Phragmites australis, Typha spp., Schoenoplectus spp., Mentha aquatica, M. pulegium, Pulicaria dysenterica, Cyperus longus, Agrostis stolonifera, Rumex spp., Epilobium tetragonum, E. hirsutum, Carex cuprina, C. muricata aggr., Lythrum salicaria, L. virgatum, Xanthium orientale subsp.italicum, Eleocharis palustris, E. uniglumis, Cirsium vulgare, C. arvense, C. creticum, Sonchus arvensis subsp.uliginosus, Phacelurus digitatus, Beckmannia eruciformis, Sparganium erectum, Bidens spp., Oxybasis rubra, Jacobaea aquatica, Amaranthus blitum aggr., Erigeron canadensis, etc.The preliminary data indicate that described communities correspond to ass.Bolboschoenetum glauci Grechushkina, Sorokin et Golub 2011 of the all.Eleocharito palustris-Sagittarion sagittifoliae Passarge 1964 [24], [25].Communities with B. planiculmis develop in the periphery of freshwater basins in the interior of the country, more often in North-West Bulgaria.As it was already pointed, the optimum of these communities is displayed at flooded conditions and water layer with depth of 0.05-0.2m [26], so to form helophytic coenoses.The substrates are mostly sand-loamy.The species composition includes many of the representatives characteristic of B. glaucus communities.In contrast, phytocoenoses with B. planiculmis are relatively open, which allows entering of some annual ephemeral vascular plants and mosses, such as Cyperus fuscus, C. glaber, Crypsis alopecuroides, C. schoenoides, Persicaria spp., Lindernia dubia, Riccia cavernosa, R. frostii, and Physcomitrella patens.
The collected phytosociological data is insufficient for conclusive syntaxonomic decision.However, the studied communities with B. planiculmis most probably, belong also to all.Eleocharito palustris-Sagittarion sagittifoliae Passarge 1964, as they share similar species pool with the communities of B. glaucus and often both species co-occur at the field.Though, at community level the ass.Tripleurospermo inodori-Bolboschoenetum planiculmis Hroudová et al. 2009, from Central Europe is sufficiently ecologically and floristically different to encompass the Bulgarian communities with B. planiculmis [23].

Conclusion
The occurrence of four species of the genus Bolboschoenus in Bulgaria has been confirmed.B. glaucus is the most widespread, thermophilous and dry tolerant.It is the earliest flowering and fruiting amongst all studied taxa.In contrast, B. paniculmis is less dry tolerant, and it is flowering/fruiting latter in the season.On the territory of the country the letter is mostly found in flooded habitats.B. maritimus has been found mostly at the coastal regions while it is relatively scattered inland.B. laticarpus has been registered in a single site with small numbers of individuals, so it is the rarest representative of the genus.The preliminary analysis of 27 phytocenological samples shows the differentiation of four groups of communities of Bolboschoenus spp. in Bulgaria, belonging to cl.Phragmito-Magnocaricetea Klika in Klika et Novák 1941.However, more samples should be collected prior final analysis and classification of these communities in Bulgaria, which will be subject of a further study.

Figure 1 .
Figure 1.Distripution map of Bolboschoenus spp. in Bulgaria: A) B. glaucus; B) B. laticarpus; C) B. maritimus; D) B. planiculmis.Yellow grid squares indicate localities extracted from herbarium records; white grid squares show localities registered at the field; orange grid squares display both respectively.