Orobanche caryophyllacea Sm . ( OROBANCHACEAE ) IN POLAND : CURRENT DISTRIBUTION , TAXONOMY , PLANT COMMUNITIES AND HOSTS

The paper presents the current distribution of Orobanche caryophyllacea Sm. in Poland based on a critical revision of herbarium and literature data as well as the results of my field studies. The majority of localities are in south and south-eastern Poland: Ma opolska Upland, Lublin Upland, Roztocze, Przemy l Foothills, Pieniny Mts, rarely in the valleys of the Lower Vistula and Oder rivers or Wolin island. The distribution map in Poland is included. The taxonomy, biology and ecology of the species are discussed.

The aim of this study was to identify the present distribution of Orobanche caryophyllacea in Poland based on field investigations and verified herbarium and literature data.Preferred habitats, communities, hosts and threats are also discussed below.308.Linnaeus received the same from Siberia" [26].
In the traditional division, Orobanche caryophyllacea is included in grex Galeatae Beck, containing species having the corolla with a curved dorsal line, a galeate upper lip, large flowers, 17-35 mm, yellow-brown, purple, lilac, usually purpurescent towards the margin, with high colour variability [22,23].The species is placed in the section Orobanche Teryokhin, subsection Galeatae (Beck) Teryokhin [27], in the most recent approach.In Central Europe, Orobanche lutea and O. teucrii also belong to the subsection Galeatae.In an older approach, these species were included in grex Galeatae together with O. gamosepala and O. latisquama [23].At present, the former is placed in a separate section, Gamosepalae, [27] while O. latisquama has been placed in the genus Boulardia latisquama [28][29][30].O. clausonis Pomel, which is classified in grex Minores [23], is a very similar species; however, the diagnostic characters indicate it should be included in grex Galeatae.It also parasitizes Rubiaceae (e.g.Asperula hirsuta, Rubia peregrina), occurring in the Mediterranean Region, mainly on the Iberian Peninsula [31,32].A recent phylogenetic study has shown that O. clausonis (section Orobanche) is closer to the taxa of the section Trionychon [33].
In Central Europe, determination errors are mostly made between Orobanche lutea and O. teucrii.Unlike O. caryophyllacea, O. lutea nearly always has a wax-coloured or yellow stigma, the dorsal line of the corolla is curved from its base, slightly convex, but the corolla is not swollen and with a considerably less open throat.It parasitizes the Medicago genus and is scentless or the scent is very delicate.The dorsal line of the corolla in O. teucrii is straight or weakly convex; the inflorescence is short and with few flowers.It parasitizes species of the Teucrium genus.Photographs and descriptions of the species are available in several studies [20,21].O. teucrii was incorrectly reported from the Polish part of the Pieniny Mts [34] and from the Lublin region [35].The species was identified as O. caryophyllacea on herbarium and field verification.
Phenotypic variability of shoots is very high in Orobanche caryophyllacea, especially of flowers and stems, with a wide range of colours from albinotic, brigh yellow, light pink and purple to violet.The colour of the pistil stigma is also variable.Typically, it is purple-coloured, but forms having orange, yellow and pink stigmas are known.The intensity of pubescence and metric characters are also observed.One population can comprise even a few colour forms.Many varieties have been described: var.typica G. Beck, var.incurvata G. Beck, var.buhsei (Reuter) G. Beck, var.gymnantha G. Beck, and over 30 lower units depending on the colour, pubescence and calyx structure [22,23].Specimens with large flowers (2.5-3.5 mm), lax and multi-flower inflorescence, were determined in Poland, especially in Silesia, as var.laxiflora (= O. laxiflora Reichenb., f. macrantha (Dietrich) G. Beck), while specimens with a lemon-coloured corolla and a purple pistil stigma from the area of Krynica were determined as f.citrina (Dietrich) G. Beck [36].Specimens having a lemon-coloured corolla and a pistil stigma can also be infrequently observed in the Nida Basin (e.g. S dziejowice), corresponding to the described form f. strobiligena (Reichenbach) G. Beck.Intensly-coloured purple individuals, described as f.orphinia G. Beck, can also be encountered in the same populations at scattered localities in Poland.Albinotic specimens have also been observed in shaded sites, such as the specimen in the Grabowiec reserve in the Nida Basin [5].An albinotic form was described as f.albiflora Baguet and reported so far from Belgium [23].

MATERIALS AND METHODS
Field research was conducted in 1999-2013, with the investigations being intensified between 2006 and 2013.All the herbarium materials of Orobanche caryophyllacea available in Poland were reviewed.The materials are deposited in the herbaria CHRZ, KRA, KRAM, KTC, KTU, LBL, LOD, OPOL, POZ, TRN, UGDA, WA, WRSL, WSRP, and also in Germany (B, GLM).Herbarium acronyms are given after M i r e k et al. [37] and H o l m g r e n and H o l m g r e n [38].The nomenclature of vascular plants follows M i r e k et al. [39].The nomenclature of syntaxa is based on M a t u s z k i e w i c z [40].The localities are organized as ATPOL cartogram units, 10 km × 10 km [41, see http://www.ib.uj.edu.pl/chronpol/], in alphabetical order.Probably incorrect localities or not confirmed by the field or herbarium investigations are marked with the symbol "?" per square number.The localities are described as follows: ATPOL grid unit, geographic location, habitat description, abundance in brackets.The following information is also given for most localities: geographic coordinates and altitude (above sea level), and for revised exsiccata the collector and collection date, exsiccatum number and the herbarium acronym.
Host plants were observed by delicately exposing the soil with a gardening shovel.A total of 80 soil pits were observed in the field and in the analysis of herbarium materials containing an attached host.
Symbols and abbreviations: ecol.[47,48].Many incorrect reports also concerned the Ma opolska Upland and adjacent areas [e.g.49-53, unpublished data from the ATPOL database].Some literature data could not be verified as the herbarium material was lacking or despite investigations in the field (especially old German data, with not strictly defined localities).These uncertain data are marked with a special symbol on the map (Fig. 1).Attempts are still made to find and verify many of them in the field.

Host preferences
Prior to my study, Orobanche caryophyllacea was reported from Poland as a parasite of the Rubiaceae family, genera Galium, Asperula and Sherardia [135].A total of 80 soil pits were investigated in the field between 2006 and 2013.Herbarium materials were analyzed if a specimen was collected together with the host.My analysis has shown that in Poland O. caryophyllacea parasitizes exclusively species of the family Rubiaceae.It infects G. mollugo in 80% of cases, seldom G. verum and very rarely G. boreale, e.g. in S dziejowice or Kików in the Nida Basin.Parasitism on G. odoratum was noted only in the "Grabowiec" reserve in the Nida Basin [5] and in Carpathian beech forests in the Pieniny Mts (leg.K. Zarzycki, 26.06.1966,KRAM; see list of localities).The species parasitized Cruciata glabra only at one locality on the margin of the "Grabowiec" reserve [5] (Fig. 2).Symptoms of host weakening by the parasite were not observed.

Preferred habitats and plant communities
In Poland Orobanche caryophyllacea mainly occurs in thermophilous habitats, from the southern sector of the horizon, seldom on west-or north-facing slopes, i.e. xerothermic grasslands of the Festuco-Brometea class, thermophilous meadows Molinio-Arrhenatheretea class.These communities vary considerably depending on the substrate, altitudinal aspect and regional location (Table 1).A description of phytocoenoses preferred by O. caryophyllacea in the regions with the highest density of its localities in Poland is given below.
Pieniny Mts.The properties of soils in the Pieniny Mts are different from the soils in the Carpathian Mts which formed from Carpathian flysch [136].This had a fundamental influence on the distrubtion of localities of the species belonging to the genus Orobanche.O. caryophyllacea occurs here on lime soils, shallow or medium deep and highly skeletal rendzinas, less often on brown soils [34].The species has been reported from thermophilous meadows, especially herbaceous meadows in the Pieniny Mts (Arrhenatheretum elatioris, Gladiolo-Agrostietum capillaris, Anthyllidi-Trifolietum montani associations), at higher altitudes Veratrum lobelianum-Laserpitium latifolium association, xerothermic grassland of the Festuco-Brometea class and alpine grasslands developing on calcareous substrate Seslerietea variae class (ecotones of the thermophilous rock grassland Festucetum pallentis, alpine rock grassland, endemic community Dendranthemo-Seslerietum variae associations, Seslerietea variae class) -community Calamagrostis varia: on slopes and screes of S-facing rock gorges, relict pine groves, thermophilous beech groves (Carici albae-Fagetum association), mountain sycamore maple forest Phyllitido-Aceretum association (Tilio platyphyllis-Acerion pseudoplatani alliance) [4,34,114,118,121].The current field research done by the authors could suggest that at present O. caryphyllacea occurs mostly in the Anthyllidi-Trifolietum montani association, thermophilous meadows with xerothermic plants, rarely in communities from Trifolio-Geranietea sanguinei and Rhamno-Prunetea classes, usually on mild slopes or at flat sites (Table 1).
Nida Basin.Orobanche caryophyllacea occurs in xerothermic grasslands, on hills, in pits often remaining after excavation or in quarries still operating in the area, of the Cirsio-Brachypodion pinnati alliance, especially in the Adonido-Brachypodietum pinnati, Thalictro-Salvietum pratensis, rarely Inuletum ensifoliae, and also on gypsum hills in locally differentiated communities Seslerio-Scorzoneretum purpureae and Carex glauca-Tetragonolobus maritimus ssp.siliquosus associations.The only locality in the "Grabowiec" reserve is on gypsum in the oak-hornbeam forest of the Querco-Fagetea class where it parasitizes Galium odoratum.The species has been rarely recorded in grassland communities of the Sisymbrio-Stipetum capillatae association.These preferred communities are often in mosaic segetal communities of the Stellarietea mediae, shrub communities Rhamno-Prunetea, fringe communities Trifolio-Geranietea sanguinei and ruderal communities Artemisietea vulgaris classes [5] (Table 1).
In the Opole province, it occurs at one locality on Góra Gipsowa Mt near Kietrz.The site has persisted since the 19 th century.The species grows on former gypsum extraction workings in xerothermic grassland of the Festuco-Brometea class with a high contribution of fringe species of the Geranion sanguinei alliance [104], (Table 1).
Pomerania.On the Lower Oder and Vistula rivers, Orobanche caryophyllacea is mostly found on rich moraine calcium carbonate in xerothermic grasslands of the Festuco-Stipion alliance, mainly in Potentillo-Stipetum capillatae associations, often occurring as a mosaic with meadow communities of the Molinio-Arrhenatheretea, fringe communities Trifolio-Geranietea sanguinei or shrub communities of the Rhamno-Prunetea classes (Table 1).
On Wolin island, the species occurs on strongly disturbed slopes of the Szczecin Lagoon (Lubin area), in thermophilous grassland communities with a high contribution of meadow and ruderal species.It is also encountered on the roadside in a cleared mixed forest towards Wapnica (see list of localities, Table 1).

I I
Carex flacca

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Festuca rupicola

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Adonis vernalis +

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Medicago falcata .

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Festuca rubra

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Rosa sp.B

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Rosa sp.C

DISCUSSION
In Poland Orobanche caryophyllacea mainly occurs in the Ma opolska Upland (chiefly the Nida Basin and Middle Vistula River Valley), Lublin Upland, Roztocze, Przemy l Foothills, Sudeten Foreland, Silesian Basin, Pieniny Mts and Pomerania: Lower Vistula and Oder rivers, Wolin island.A total of 160 localities of O. caryophyllacea are known in Poland, of which ca. 120 have been confirmed and documented by herbarium specimens or photographs.Approximately 60 sites have been confirmed after 2000.Many sites were noted in the 19 th century and are now historical.O. caryophyllacea is one of the most sensitive species to changes in the phytoconoesis structure among species of the genus Orobanche found in Poland.The verification showed that the species had been incorrectly reported, for instance, from the l sko-Krakowska Upland, Ma opolska Upland and adjacent areas.It was usually confused with O. lutea and O. kochii, which are frequent there.A verified and updated distribution map (Fig. 1) of the ATPOL map [137,138] shows considerable differences and it is a result of errors and difficulties in determining the genus Orobanche.The herbarium revision and field investigations also showed that Orobanche teucrii reported from Poland in the Polish part of the Pieniny Mts [34,after Jasiewicz] or in the Lublin region [35] was reported incorrectly and the species was in fact O. caryophyllacea.
Orobanche caryophyllacea prefers xerothermic grasslands of the Festuco-Brometea class, fringe communities of the Trifolio-Geranietea sanguinei class, thermophilous meadows (Arrhenatherion elatioris alliance) of the Molinio-Arrhenatheretea class, rarely alpine grasslands Seslerietea variae class developing on calcareous substrate, cleared oak-hornbeam forests of the Querco-Fagetea class, such as sycamore maple in the Pieniny Mts, "Grabowiec" reserve in the Nida Basin.It colonizes soils such as shallow rendzinas, loess and chernozems.The species is recorded in lowland areas, from 29 m in Pomerania and Wielkopolska, 140-270 m in the belt of the Polish Uplands to 1050 m a.s.l. in the Pieniny Mts (Wysokie Ska ki).
Orobanche caryophyllacea is oligophagous and parasitizes species of the family Rubiaceae, genus Galium: G. mollugo, G. verum, rarely G. boreale, sporadically G. odoratum and Cruciata glabra.O. lutea and O. caryophyllacea are some of the earlierst flowering species of the genus Orobanche in Poland.The flowering peak is observed in late May and early June.O. caryophyllacea is characterized by the fact that it emits a strong scent resembling the smell of cloves.Representatives of the genus Bombus (Apidae) were the most frequently observed pollinating insects, al-though the genus Myrmica (Formicidae) and other genera were also noted (Piwowarczyk unpublished).
The abundance of Orobanche caryophyllacea populations varies regionally in Poland and fluctuates considerably annually.Its populations are usually not very abundant and mostly comprise 5 to 20 specimens.The most abundant populations are recorded in Lower Silesia (Kamienny Grzbiet) -over 300 specimens [88], in the Nida Basin, e.g.Kików and Chomentówek -200 specimens at each, Gartatowice, Samostrza ów, Grabowiec, Górki -100 specimens each [5].The populations in the Lublin Upland are also quite abundant and 50 specimens were recorded in K ty, Dobu ek or Przeorsk [17].
The progressing process of secondary succession of tree and shrub vegetation, the density of the herb layer and the cessation of former management methods are the main threats to Orobanche caryophyllacea.The localities are also often situated near arable fields where they are exposed to chemical agents.The influence of invasive species also poses a considerable threat.Heracleum sosnowskyi has been moving worryingly close to the O. caryophyllacea population (Gipsowa Góra).Mass self-sowing of Solidago gigantea and Calamagrostis epigejos are observed at many sites.Many localities are at disturbed sites or at operating excavation sites (limestone, serpentinite).Only a minority of localities are protected: within national parks -Wolin and Pieniny National Parks; reserves -e.g.Brodogóry, Stary Przylep, Bielinek, Zbocza P utowskie, Góra w.Wawrzy ca, Gipsowa Góra, Stawska Góra, Machnowska Góra, Skarpa Dobu a ska, Homole, Grabowiec, Zimne Wody; as ecological sites, e.g.Dwikozy, Owczary, or within Natura 2000 sites.This does not ensure the preservation of the species as active protection, which is not always introduced, is needed.At least some of the localities should be protected as ecological sites and active protection measures should be implemented: mowing or grazing of excessively developing field and herbaceous vegetation, while preserving the unique mosaic systems of grasslands and fringe communities, and nature monitoring.The abundance of the host species of the genus Galium should also be monitored.

Species biodiversity at the localities occupied by
Orobanche caryophyllacea is also high.Many species extremely rare in Poland were observed when phytosociological relevés were performed in the communities with O. caryophyllacea.These include: Achillea setacea, Adonis vernalis, Anthericum liliago, Cerasus fruticosa, Linum flavum, Orchis ustulata, Orobanche alba subsp.major, O. elatior, O.

Fig. 1 .
Fig. 1.Distribution of Orobanche caryophyllacea in Poland: -localities confirmed after 2000; -localities documented with herbarium collections, not confirmed after 2000; ?-localities not confirmed in the field, unsertain or probably doubtful, lack of herbarium materials.
42e list below presents only verified data.As my verification showed, the species was incorrectly reported from the Silesian -Krakow Upland [e.g.42-46, unpublished data from the ATPOL database].It was most often mistaken with O. lutea and O. kochii, which often occur in the area, infrequently with O. bartlingii and O. elatior and

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Orobanche caryophyllacea Sm. (Orobanchaceae) in Poland: current distribution, taxonomy, plant communities and hosts 111 © The Author(s) 2014 Published by Polish Botanical Society