A REVISION OF DISTRIBUTION AND HISTORICAL ANALYSIS OF PREFERRED HOSTS OF Orobanche ramosa ( Orobanchaceae ) IN POLAND

The Polish localities of Orobanche ramosa L., branched broomrape, are either extinct or have not been confirmed for many years. This paper presents two new localities of O. ramosa in Poland from the Pła skowyż Proszowicki plateau (Wyżyna Małopolska upland) and the Nizina Nadwiślańska lowland (Kotlina Sandomierska basin). Habitat preferences and the abundance at the sites are described. A revised map of the distribution and a historical analysis of preferred hosts in Poland are included. The taxonomy, biology, ecology and control methods of O. ramosa are also discussed.


INTRODUCTION
Orobanche ramosa L., branched broomrape, belongs to the parasitic family Orobanchaceae.Of approximately 200 species of the genus Orobanche (Pusch and Günther, 2009), six parasitize crop plants: O. aegyptiaca, O. cernua, O. crenata, O. cumana, O. minor and O. ramosa (S a u e r b o r n , 1991; P a rk e r , 1994).O. ramosa, O. crenata and O. cumana are the prominent species that increasingly cause agricultural problems in Southern and South-Eastern European countries.O. ramosa has long been known in Central Europe as a parasite of hemp and tobacco but it did not have a major agricultural impact; it has recently become an aggressive weed that adapts to new hosts and causes considerable crop losses (W e g m a n n , 2004).
Orobanche ramosa is a widespread species.Its range extends in Europe and Western Asia (J ä g e r and W e r n e r , 2002).It occurs in Central (northwards to England, the Netherlands, northern Germany, Poland, Estonia and the former USSR) and Southern Europe, in Asia, northern and southern Africa, north America and southern Australia.The species probably travelled to Central Europe from Asia with hemp crops ca.500 BC (K r e u t z , 1995; P u s c h and G ü nt h e r , 2009).
The Polish localities of Orobanche ramosa are rare and mostly extinct or have not been confirmed for many years.O. ramosa is red-listed in Poland as a rare, potentially threatened species (R) (Z a r z y ck i and S z e l ą g , 2006).It is classified as a species of indeterminate status (I) in the Kujawy-Pomeranian region (R u t k o w s k i , 1997), as extinct (Ex) in Western Pomerania and Wielkopolska (Ż u k o w s k i and J a c k o w i a k , 1995), regionally extinct (RE) in Gdańsk Pomerania (M a r k o w s k i and B u l i ń s k i , 2004; O l s z e w s k i and M a r k o w s k i , 2006), and extinct (Ex) in the Kraków Voivodeship (Z a j ą c and Z a j ą c , 1998).
The aim of this study is to present the current distribution of Orobanche ramosa in Poland based on a critical revision of literature and herbarium data and the results of my field studies.Issues related to the taxonomy, biology, ecology and control methods of O. ramosa are also discussed.High variability is also observed within Orobanche ramosa subsp.ramosa, especially for the length or colour of flowers which may range from whitish to pale blue or intensely blue.The height and branching, if present, of shoots may also differ.The stem and inflorescence are branched in f. polyclonos Wallroth (var.robusta Čelakovsky), while f.monoclonos Wallroth (var.simplex Noulet, Kopsia ramosa Dum.f. monoclonos Béguinot, Phelipaea ramosa var.monoclonos Rouy) has a single inflorescence and stem.The colour of the corolla distinguishes f. cyanea G. Beck (Kopsia ramosa f. cyanea Béguinot), which has an intensely blue-purple corolla, from f. albiflora (Godr.et Gren.)G. Beck (Phelipaea ramosa var.alba Webb et Berthel, Kopsia ramosa f. albiflora Béguinot, Phelypaea ramosa var.alba (Webb et Berth.)Rouy) which has a white corolla.Corolla size and shape may also vary.F. gracillima G. Beck is distinguished by a 1-1.2 cm long corolla, while the corolla is 7 mm long in f. proboscistyla Bianca (Kopsia ramosa var.proboscistyla Béguinot) (B e c k , 1930).These morphological differences are caused by different hosts or habitat conditions.The taxonomic rank of internal taxa within O. ramosa requires further investigations, including ecological-geographic and molecular examinations.

Flowering time
The species flowers from March in Southern Europe.It flowers from (VI) VIII until IX (X) in Central Europe (K r e u t z , 1995; Z á z v o r k a , 1997, 2000; P u s c h and G ü n t h e r , 2009).It flowers from late August until late October in Poland.

Productivity, seed dispersal and vitality
A single fruit of Orobanche ramosa can produce between 700 and 4 000 seeds.Every plant can produce 35 000-500 000 durable and very small seeds, leading to a dramatic increase of the Orobanche seed bank in the soil (S a u e r b o r n , 1991; B u s c hm a n n , 2004).Seed shape ranges from ellipsoid to ovoid, 0.33-0.52x 0.19-0.33mm in size (P l a z a et al. 2004).200 000 seeds per gram can be produced (Q ua s e m and K a s r a v i , 1995; Q u a s e m , 1998).Humans, machinery, water or wind can easily disperse these seeds (B u s c h m a n n et al. 2005).Seeds can lie dormant in the soil for up to 13 years (B u s c h m a n n , 2004).Seed life expectancy in broomrapes varies considerably depending on the soil type and climatic conditions.Broomrape viability can probably be longer in drier conditions (T e r y o k h i n , 1997).

Habitat and phytocoenoses
Orobanche ramosa occurs in root crop fields, in sown fields, fallows, sandy fields, especially in root crop cultures, on roadsides, in ruderal pastures, on alkaline, nutrient-rich sandy or loamy soil (M ą d a ls k i , 1967, T z v e l e v , 1981, K r e u t z , 1995).
It is mostly a lowland species.The highest site of its occurrence in Central Europe was reported from Wallis in Switzerland, at ca. 1 600 m a. s. l. (P u s c h and G ü n t h e r , 2009).It has also been reported from mountainous areas, e.g.

Control methods
As Orobanche ramosa can cause considerable crop losses, a range of eradication methods have been developed.However, it is a persistent weed and control strategies described in the literature are not always universal or fully effective.The main control methods are described below.
Some success has been obtained using chemical   (2002).The nomenclature of syntaxa is based on M a t u s z k i e w i c z ( 2006).The localities are listed in ATPOL cartogram units, 10 x 10 km (Z a j ą c , 1978); units are given in alphabetical order.Data collected by me and the localities documented in the herbarium materials and reported in the literature are included.Abbreviations of the hosts of O. ramosa are based on the information in the herbarium materials and in the available literature (in brackets after the location of the site): hc -headed cabbage (Brassica oleracea subsp .capitata), h -hemp (Cannabis sativa), p -potato (Solanum tuberosum), tb -tobacco (Nicotiana tabaccum), tm -tomato (Lycopersicon esculentum), s -strawflower (Helichrysum bracteatum), u -stinging nettle (Urtica dioica).

All available herbarium materials of
During the floristic investigations conducted between 2008 and 2010, two new localities of Orobanche ramosa were recorded: in the Płaskowyż Proszowicki plateau (Wyżyna Małopolska upland) and the Nizina Nadwiślańska lowland (Kotlina Sandomierska basin) (Fig. 1).The location of these sites, the abundance of individuals within populations and the preferred host at the new localities are specified, and the habitats are briefly described.Soil tests were performed at the Regional Chemical-Agricultural Station in Kielce.
Specimens collected at the new localities were deposited in the Herbarium of the Jan Kochanowski University in Kielce (KTC).

Distribution in Poland
Orobache ramosa occurred in Poland at a few scattered localities, mostly in the lowland, in Pomerania, Kujawy, Wielkopolska, Silesia, the Wyżyna Małopolska upland, the Nizina Sandomierska lowland, Wyżyna Lubelska upland, Podkarpacie, in Podolia and Volhynia within the Polish borders in the interwar period (S z a f e r et al. 1924; M ą d a l s k i , 1967; F i j a ł k o w s k i , 1995; Z a j ą c and Z a j ą c , 2001) (Fig. 1).A vast majority of data were reported in the late 19 th and the early 20 th centuries.The species has not been observed in recent years; only a massive occurrence of O. ramosa in several tomato crops in the Sandomierz region in 1999 was reported but the location was not specified (B o r k o w s k i and R o b a k , 2000,2002).

New localities of Orobanche ramosa 1. Płaskowyż Proszowicki plateau, Zysławice.
The locality is in a field, in a tobacco crop, Zysławice village near Wojsławice, S of Kazimierza Wielka, on loamy-sandy soil.Soil pH is alkaline (pH in KCl = 7.3), the content of P is very high (31 mg/100 g soil), Mg -medium (6.7 mg), and a low content of K (10.9 mg).The broomrape was observed intermittently by the field owners for over 20 years.Broomrape infestation occurred only when tobacco was planted as part of crop rotation.O. ramosa is accompanied by its host and common weeds: Galinsoga parviflora, Echinochloa crus-galli, Elymus repens, Chenopodium album, Polygonum aviculare, Equisetum arvense, Setaria pumila, Convolvulus arvensis.The community may be included in the Polygono-Chenopodietalia order (Stellarietea mediae class) with species belonging to the Agropyretea intermedio-repentis class.Over fifty, mostly large tufts consisting of ten to some 30 shoots, were recorded.The flowering optimum was observed in the second half of August and in the first half of September 2008.Individual specimens also flowered in late September and early October.ATPOL: EF53; GPS: 50 o 11'25.1''N,20 o 30'58.7''E,220 m a.s.l.

Nizina Nadwiślańska lowland, Szewce.
The locality is ca.0.5 km SE of the S border of the Szewce village, in the Vistula valley.The field borders on an unnamed tributary of the Koprzywianka river to the east.Over 1 000 specimens of O. ramosa occur in a tomato crop covering an area of ca. 150 m 2 .It is accompanied by common weeds: Chenopodium album, Echinochloa crus-galli, Capsella bursa-pastoris, Stellaria media, Galinsoga parviflora.Observations were conducted on 25.09.2010.Ca. 50% of the population was withered; the remaining population was in full bloom or was beginning to flower.ATPOL: FE91; GPS: 50 o 37'37.6''N,21 o 37'44.2''E,129 m a.s.l.

A historical outline of preferred hosts of Orobanche ramosa in Poland
Orobanche ramosa was probably introduced to Central Europe shortly after hemp cultivation began and can be regarded as an archaeophyte (traces of hemp cultivations date from the Iron Age ca.500 BC) (P u s c h and G ü n t h e r , 2009).The oldest information concerning the use of hemp goes back to China, ca.5500-4500 BP.Hemp spread in Asia and reached Europe through Scythian tribes who used it as a drug.As in Europe, the oldest records of hemp in Poland were described from the Roman period but the plant gained importance in the early Middle Ages (L it y ń s k a -Z a j ą c , 1997; L i t y ń s k a -Z a j ą c and W a s y l i k o w a , 2005).Tobacco was imported from North America (in Europe since ca.1560) and the parasite was probably distributed in Central Europe with its seeds (P u s c h and G ü n t h e r , 2009).
First documented reports on its occurrence in Poland date back to the beginning of the 19 th century from a hemp crop (F i e k , 1881, after Starke -probably before 1800) and a tobacco crop (R e b e n t i s c h , 1804).Ho wever, the most abundant records were observed between the 1850s and the 1960s in hemp crops where it reached the occurrence optimum in Poland.Less numerous occurrence has also been reported from tobacco and potato crops.It has been reported from a single locality on stinging nettle, strawflower and on headed cabbage.At present, it is observed only on tobacco and tomatoes as hemp cropping has been discontinued.Based on available data on the hosts of O. ramosa, a diagram of individual host species is presented, specifying the time and the number of localities (Fig. 2).A considerable drop in the number of localities (the disappearance) of O. ramosa in recent years is also caused by more efficient methods of seed purification, crop rotations and the application of plant varieties resistant to infection.Similar causes of the disappearance of the species have been described from the Czech Republic after hemp cultivation was discontinued in the 1950s and following the quarantine act in 1964-1996 (Z á z v o r k a , 2000).

DISCUSSION
Orobanche ramosa in Poland, also in Central Europe, is probably an archaeophyte.The first documented reports on the occurrence of O. ramosa in Poland date back to the early 19 th century, mostly from hemp, tobacco and potato cultivation.Its preferred habitats include root crops where host species occur as well as tobacco and tomatoes, in communities of the Polygono-Chenopodietalia order (Stellarietea mediae class) at the newly discovered localities.
The flowering optimum was observed at the new sites between late August and late September (October).The species did not flower homogenously.Withered specimens and specimens flowering or beginning to flower occurred simultaneously in individual populations.O. ramosa sporadically occurs singly; it usually grows in tufts consisting of between several and some 30 shoots.
As reported by local residents in the Szewce village and its vicinity, Orobanche ramosa usually occurs more abundantly in dry summers.Farmers have noticed a drop in tomato fitness when mass infection by the parasite takes place.In 2010, however, an abundant occurrence of O. ramosa in a tomato field was also observed in a post-flood area.
An analysis of the distribution map in Poland shows that the species mainly occurs along the valleys of larger rivers (Fig. 1
(USA) for the first time (M u s s e l m a n and B o l i n , 2008).It has also been spreading in western France, where it parasitizes Brassica napus subsp.napus (G ib o t -L e c l e r c et al. 2003).
from the Czech Republic (Tepelské vrchy) 650-690 m (Z á z v o r k a , 2000), Tyrol up to 883 m, Abkhazia 850 m, northern Persia 3200 m, Eritrea 2480 m, Italy up to 1000 m (P i g n a t t i , 1982; U h l i c h et al. 1995).In Europe the species has been recorded in Eragrostion, Caucalidion lappulae, Polygono-Chenopodietalia, Bidentetalia tripartitae, Tribulo-Eragrostion, Secalietea (O b e r d o r f e r , 1990; U h l i c h et al. 1995; Z a z v o r k a , 2000; J ä g e r and W e r n e r , 2002; K r o p á č , 2006).A separate segetal community with Orobanche ramosa has been distinguished in Ukraine (Crimea region), Orobancho ramosae-Stachydetum annuae, Stellarietaea mediae class (B a g r ik o v a , 1996).
control (L o l a s , 1994; Q a s e m , 1998; B o r k o ws k i et al. 2007a; B o r k o w s k i and R o b a k , 2000, 2002; G o l d w a s s e r et al. 2003), resistant varieties (Perez-de-Luque et al. 2004) and agronomical practices (H a i d a r and S i d a h m e d , 2000).Crop rotation for a period of at least five years is recommended in fields affected by Orobanche ramosa (M a ł u s z y ń s k a et al. 1998).Many researchers have investigated the effect of organic fertilizers on the seed germination of a variety of plants (H a i d a r et al. 1999; H a i d a r and S i d a h m e d , 2000).H a i d a r et al. (2003) reported that goat manure significantly reduced broomrape infestation.Broomrape seeds can also be destroyed by soil solarization (A b d e l -R a h m a n and A l -T aw a h a , 2005; S a h i l e et al. 2005).Another control method is the use of drip irrigation systems.Results reported in the literature indicate that broomrape infestation in tobacco and potato can be suppressed by drip irrigation (S a b r a , 2000; V ee r a p u t h i r a n and K a n d a s m y , 2001; K a r k an i s et al. 2007).Biocontrol methods with insects or pathogens are still being researched.Studies have been conducted on the use of Phytomyza orobanchiae (Diptera: Agromyzidae).P. orobanchiae is an oligophagous species and feeds on Orobanche spp.(K l e i n and K r os c h e l , 2002).The larvae of P. orobanchia mine in Orobanche shoots and capsules, feed on the seeds and also damage the stalks of the plant (S p e n c e r , 1973).Aphis gossypii also stunts growth and flowering of O. ramosa in greenhouse conditions (B o r k o w s k i et al. 2007b).Studies on growth-inhibiting pathogens, such as many species of the genus Fusarium, Ulocladium atrum, Rhizoctonia solani, Alternaria and Sclerotinia sp., are increasingly popular.Myrothecium verrucaria or Fusarium compactum were isolated from diseased O. ramosa plants collected, e.g., in southern Italy to find potential biocontrol agents of this parasitic weed (Z o n n o and V u r r o , 2002; A b o u z e i d a et al. 2004; A n d o l f i et al. 2005).
Orobanche ramosa in Poland and Germany deposited in herbaria GLM, KTC, KRA, KRAM, LBL, TRN, WA were reviewed.Herbarium acronyms are given after M i r e k et al. (1997) as well as H o l m g r e n and H o l m g r e n (1998).The nomenclature of vascular plants follows M i r e k et al.

Fig. 2 .
Fig. 2. A comparison of preferred hosts of Orobanche ramosa and the time and number of localities recorded in Poland.
) and it may have spread during spring and autumn floods.Humans, however, play a role in the geographic spread of O. ramosa.Transport and seed exchange of host species are also important factors.Broomrape invasion into natural habitats or considerable crop losses have not been recorded in Poland to date.However, broomrapes often cause considerable economic losses in warmer climates.O. ramosa is a considerable threat to tomato crops in many countries, e.g.Turkey, Lebanon, Israel, Jordan, Sudan, Ethiopia (S a g h i r et al. 1983; D o n g o l a , 1995; Q a s e m , 1998; S a h i l e et al., 2005).It is especially noxious in tobacco fields in many countries in the Middle East, northern Africa, Cuba and Chile (A b u -I rm a i l e h , 1994, K o g a n , 1994, L a b r a d a , 1994).Numerous studies are conducted worldwide to control and eradicate the parasite.The majority of Polish species of Orobanche are rare and threatened plants that do not cause crop losses.All species of the genus Orobanche are strictly protected in Poland (Regulation of the Minister of Environment of 24 th July 2004).O. ramosa has not caused considerable crop losses so far and is a disappearing species in Poland.It is no longer listed as a quarantine parasite.However, the species should be closely monitored, especially near Sandomierz, one of the largest regions of vegetable production in Poland.A land register should be maintained to monitor the spread of O. ramosa.Poland participates in the international COST849 research programme investigating parasitic plants, including Orobanche, and control methods of plant parasites in crops (B o r k o w s k i and D y k i , 2008).
Orobanche ramosa Linnaeus 1753, Sp.Pl. 2: 633.Syn.: O. micrantha Wallr., O. cannabis Voucher ex Duby, O. albiflora Godr.et Gren.highlyvariable taxon.It comprises varieties and subspecies that are increasingly often recognized as separate species, mostly based on the length and shape of the corolla and the calyx: O. ramosa subsp.mutelii (F.W. Schultz) Coutinho, O. ramosa subsp.nana (Reuter) Coutinho, and O. ramosa subsp.ramosa (C h a t e r and W e b b , 1972).The first two occur mostly in southern Europe and parasitize wild plants.O. ramosa subsp.ramosa is usually a crop parasite.