Loranthus europaeus (Loranthaceae) in Ukraine: an overview of distribution patterns and hosts

Updated information on geographic distribution patterns and hosts of Loranthus europaeus in Ukraine is presented as a list of known localities and a schematic map based on data of field observations, herbarium collections, and literature sources. The field study areas with eight localities directly surveyed by the authors included: Chernivtsi Region (Hertsayivs'ky and Kelmenets'ky districts), Zakarpattia (Transcarpathian) Region (Rakhivs'kyi District) and Khmelnyts'kyi Region (Kamianets-Podils'ky District) of Ukraine. In Ukraine L. europaeus has been recorded since the 19 century. In total, it was reported from ca. 30 localities in Ukraine, mostly in the southwestern regions of the country at the northeastern limits of the Eastern European part of its range. The records from Kyiv Region and Crimea remain questionable. Within its range in Ukraine, L. europaeus parasitizes Quercus species as its primary hosts. In our opinion, this mistletoe species is not expected to become a noxious pest causing considerable damage for the Ukrainian forests, unlike the European mistletoe, Viscum album. Moreover, L. europaeus is recommended for special protection in Khmelnyts'kyi Region and is included in the list of regionally rare plants of administrative units of Ukraine.


Introduction
Mistletoes, which is an English vernacular name for many species of obligate hemiparasitic plants belonging to several currently recognized genera (e.g., Viscum L., Arceuthobium M. Bieb., Tupeia Cham. & Schltdl., Phoradendron Nutt., Strutanthus Mart., Loranthus Jacq., etc.) and even families of Santalales (e.g., Viscaceae, Santalaceae, Loranthaceae, etc.), are aerial hemiparasites of woody plants distributed widely from tropical to boreal physiographic zones (Beylin, 1986;Aukema, 2003;Mathiasen et al., 2008;Nickrent, 2010;Kuijt, 2015). Their role in forests and other habitats/ ecosystems is considered to be ambivalent, or even contradictory. First, mistletoe fruits, due to their persistence in cold seasons in temperate regions, are usually consumed by birds and other animals. At the same time, mistletoes compromise trees' water balance and photosynthetic activity as pests by pirating water due to the haustorial connection of their endophytes to the host vascular system (Watson, 2001). Ornithochory favors an aggregated spatial distribution of infected trees (Glatzel, Geils, 2008). The infestation patterns are mostly discrete and distance-dependent (Matula et al., 2015).
The taxonomic circumscription of Loranthus Jacq. (Loranthaceae) considerably changed over time, and it remains problematic even now. Various authors recognized in the genus from ca. 500 or even 600 species (Krüssmann, 1977, and earlier authors) to ten (Nickrent et al., 2010) or just two (Kujit, 2015) species. In earlier literature the genus encompassed most species of mistletoes parasitizing representatives of phylogenetically distant taxa (Krüssmann, 1977). Recently, according to the fundamentally revised phylogenetic classification of Santalales by Nickrent et al. (2010) based on nucleotide sequence data, it is widely accepted that subtribe Loranthinae Engl. includes just two genera: monotypic Cecarria Barlow with the only species C. obtusifolia (Merr.) Barlow inhabiting the Philippines, New Guinea, New Britain, and the Solomon Islands, and Loranthus Jacq. with ca. ten species occurring from Europe to southern China, and Sumatra. This classification is supported by palynomorphological data, since the genus Loranthus from subtribe Loranthinae, clade G, have pollen of Type B (Grímsson et al., 2018). However, Kuijt (2015) recognized only two species of Loranthus. Moreover, phylogenetic analysis of L. europaeus mitochondrial genome performed for the studies of the mitochondrial genome evolution places this species in the Santalales as sister to Gaiadendron G. Don (Loranthaceae) (Zervas et al., 2019), though the taxonomic classification of Nickrent et al. (2010) separates Loranthus and Gaiadendron into different clades, and places these two genera in two different tribes, Lorantheae та Gaiadendreae, respectively.
Loranthus europaeus is widely distributed in Central and Southeastern Europe, the Eastern Mediterranean region, and also has several isolated populations in Asia Minor (Glatzel et al., 2016). In Ukraine, records of L. europaeus are quite scarce. These issues are addressed in the present article based on our revision of available specimens in the Ukrainian herbaria, relevant literature, and field observations made during 2005-2019.

Herbaria
The specimens from the main Ukrainian herbaria: KW The following herbaria were visited by the authors of the present article, and all specimens of Loranthus from Ukraine available in these herbaria were physically examined: KW, KWHA, and CHER.
We also received digital images of and/or information on available specimens from some other herbaria; that information was provided by their staff or other colleagues (see Acknowledgments), in particular: KWHU, LW, MSUD, and UU.
In the list of localities below we cite (1) herbarium specimens (the specimens physically studied in herbaria are marked with "!" following the herbarium acronym); (2) digital images of herbarium specimens provided from some herbaria (accompanied by the word "image"); (3) reliable publications (with relevant references given); (4) original observations of the authors of the present article, and (5) personal communications ("pers. comm.") of colleagues.
Herbarium acronyms are given following Index Herbariorum (Thiers, 2008-onward) and, if necessary, Index Herbariorum Ucrainicum (Shiyan, 2011). Specimens from the herbaria of the neighboring countries (e.g., Poland, Czech Republic, Slovakia) have not been studied. We hope that they will be analyzed in our further studies.

The survey areas
The field study areas directly surveyed by the authors included: Chernivtsi Region (Hertsayivs'ky and Kelmenets'ky districts), Zakarpattia (Transcarpathian) Region (Rakhivs'kyi district) and Khmelnyts'kyi Region (Kamianets-Podils'ky district) of Ukraine. Ca. 8 localities were attended during route and area surveys.

Mapping
The distribution range of L. europaeus is presented on a map according to the subdivision of Ukraine into administrative regions (in Ukrainian, singular: oblast, область) and districts (rayon, район). Chorological data (herbarium specimens, literature data and original observations) are presented here as a list of localities (alphabetically arranged within administrative units).

Morphological characteristics and biological peculiarities of Loranthus europaeus related to its hemiparasitism, distribution and dispersal
The occurrence of this deciduous mistletoe on host stems and/or branches can be diagnosed from the distance as it forms spherical tufts (clutches) ca. 60-80 cm in diameter, scattered on the host branches and/or stems ( Fig. 1; Fig. 2, A, B, C).
Fusiform malformations are present at sites of the old aerial exophyte (outer part) entry on host terminal branches (Fig. 2, B (arrow), F). Loranthus europaeus is green from early spring to late autumn (Fig. 2, A, B, E, G), then it loses leaves (Fig. 2, C, F) and bears yellow berries in winter (Fig. 2, D, O).
Flowering in Ukraine occurs in May-August, fruits ripen in November and persist during winter (Morozyuk, 1987). The seeds covered with sticky viscin ("bird glue") (  within the European range of L. europaeus (Cramp, Perrins, 1994).

Patterns of distribution of Loranthus europaeus in Ukraine
In the continental part of Ukraine L. europaeus occurs at the northeastern boarder of its range in Eastern Europe mostly in natural oak forests in Western and Central-Western Ukraine (Fig. 3). As compared to the continental climate of the most of Ukraine, in southwestern part it is milder, with snowy winters and average temperatures below freezing and higher precipitation during warm season (Peel et al., 2007  According to Fodor (1974), this hemiparasitic species resides mainly in the Transcarpathian Lowland, Foothills and the lower forest belt. Probably localities in Ukraine are in the northeastern border of the range of L. europaeus in Europe, and its distribution is limited by climatic factors.
Zawadzki in his Enumeratio plantarum Galiciae et Bucowinae (Zawadski, 1835) reported L. europaeus as parazitizing oaks near Lviv ("Auf Eichen um Lemberg"), though this record has not been confirmed later (Bordzilovskyi, Lonachevskyi, 1952), or probably the species has already disappeared in that locality. Тhus, the first reliable and confirmed record of L. europaeus in Ukraine was published by Herbich in his Stirpes rariores Bucovinae... (Herbich, 1853), where the species was reported "Im Walde bei Terescheni auf Eichen" (Hlybots'kyi District, Chernivtsi Region). In his later overview of the flora of Bukovina, Herbich (1859) confirmed the locality of L. europaeus mentioned in his previous publication: "Im Walde zwischen Terescheny und Oprischeny parasitisch auf Eichen". Moreover, in his book on plants of Galicia (Galychyna) and Bukovina Ueber die Verbreitung in Galizien und der Bukowina wildwachsenden Pflanzen Herbich (1861) summarized the data on plant species composition in this region, referring to his earlier works as well as to works of other botanists, including the publication of Zavadsky, who reported L. europaeus from Lviv (see above).
In turn, the first known records of L. europaeus in Ukraine were reported by V.V. Montresor, who collected it on 14 August, 1881 in Podillya (Latinized as Podolia) near Nova Ushytsya (see the cited specimen above). Montresor (1886: 59) reported Loranthus europaeus only for the current Khmelnyts'kyi Region as "Growing on old oaks near Mynkovets and Otrokova villages of Nova Ushitsya county (uyezd -уезд); near Nova Ushitsya by a postal road to Yampil city. August. Flowers yellow-greenish, fruits yellowish. The plant is parasitic [the archaic word "чужеядное" was used in the original Russian text], rarely occurring" (translated from Russian: Montresor, 1886). It is noteworthy that the hemiparasite persisted in the same area for more than 100 years, since it was recorded there also in 1985. In Murovanokurylivets'ky District, at Vysche-Olchadayivska sugar mill of Vyscheolchadayiv village, L. europaeus parasitized oaks at the edge of a forest near Mohylivs'ka ring road, what was observed on 30 September 1926 by N.O. Verner and M. Bilozor. The easternmost confirmed locality of L. europaeus in Ukraine and in Eastern Europe in general is in a "pure" (monodominant) oak forest near Bezvodne village (Vinnytsya Region, Yampils'kyi District), where the species was found on 21 June 1969. Schmalhausen (1886) provided general data on the range of L. europaeus and some localities in Kyiv and Khmelnyts'kyi regions: on oaks, rarely, Lipovetsky uyezd near Zabory farm in Ometyn'skyi forest near Novoushytskyi uyezd between Syvoroha and Kuzhelivka villages, Minkovtsy -in Koltun forest (Montresor!) [На дубах; редко. Киeв. Липов. у. около хутора Заборы в Ометинском лесу под. Новоуш. у. между дд. Сиворога и Кужелевка! Миньковцы -в лесу Колтун (Монтрезор!)].
The early collections of L. europaeus in the western part of Ukraine were done by the Romanian botanist Emilian Tsopa (Ţopa) in 1935 from the environs of Lomachyntsi village (Sokyrians'ky District, Chernivtsi Region); he reported it as a supposedly new species for the regional flora [of North Basarabia] (Ţopa, 1936). This locality was also recorded by Udra in 1985. Loranthus europaeus from Chernivtsi Region is also known from the Prut-Dnister interfluvial area (Prut-Dnistrovske Mezhyrichchya) in Kelmenets'ky and Sokyrians'ky districts and in Bukovynian Cis-Carpathia (Bukovyns'ke Prykarpattia) in Hertsayivs'ky and Hlybots'ky districts. Only 70 years after that record, a new locality of L. europaeus parasitizing Q. petraea was revealed near Hrushivtsi village (Kelmenets'ky District)  One of the largest surveyed populations of L. europaeus in Chernivtsi Oblast was revealed recently near Kulykivka village (Hertsayivs'ky District). The total area of parasitized 15-25 m-high stands of Quercus rubra was ca. 600 m 2 (150 x 50 m 2 ) located at the northern slopes (30-40° steepness). Besides Q. rubra, the forest comprised other trees and shrubs, such as Q. robur, Carpinus betulus, Acer platanoides L., Fagus sylvatica L., Populus tremula L., and Cerasus avium (L.) Moench (Prunus avium (L.) L.). It should be noted that one of exophytes of L. europaeus was 1.5-2 m in diameter, and many residual parasitic stems on the swollen host branches were revealed. However, only one parasitized tree of Q. robur with a low rate of infestation by L. europaeus was found in this locality, as compared with Q. rubra; though, at the plain part of that hill three more trees of Q. robur resided at the edge of a mixed Quercus-Fagus forest, having several L. europaeus exophytes on the upper thirds of trees. Thus, a tree 18 m tall and 30 cm in diameter had three yellow mistletoe exophytes, while the other two trees, being 15-18 m tall and 25-28 cm in diameter, had only one exophyte each.
A new site was revealed recently near Ivanivtsi village (Kelmenets'ky District, Chernivtsi Region) on 18 November 2018, where L. europaeus parasitized Q. robur trees (25-30-m tall and 50-100 cm in diameter) forming the first layer of a Carpinus -Quercus forest with the admixture of young Carpinus trees at the second one located at the comparatively flat top of the hill at the outskirts of the village towards Sokyryans'ky District. This population of L. europaeus occupied ca. 5 ha (100 x 500 m 2 ) of the forest with the central part with small growing trees lacking the parasite due to recent cuttings. Some exophytes reached 50-80 cm in diameter, and, additionally, had abundant maturating berries. The relative density of the infected trees was ca. one plant per 25-50 m 2 . Regarding the relatively rare occurrence of L. europaeus in Ukraine, and its residence at the northeastern boarders of the Eastern European part of the species range, this hemiparasitic species is recommended to be protected at regional level in Chernivtsi Region.
It is noteworthy that L. europaeus has been already included to the list of rare, relict and endemic species of the Eastern Podillya Region, namely, at the Сykivs'ky landscape protected area, Khmelnyts'kyi Region . In turn, the yellow dwarf mistletoe was revealed at Kamianets-Podil's'ky Region on oaks near Nygyn village, at Tovtry by Ol. Sokolovsky and V. Schidlovsky on 22.07.1935, also nearby, in a Quercus-Сarpinus forest, natural and planted Q. petraea oak forests in Podils'ky Tovtry National Nature Park (Novosad et al., 2009), and recently, on 25 January 2018, by D. Svyrydiuk, in the same national park. In Chemerovets'kyi District, near Cherche village this hemiparasitic species parasitizing Q. robur was recorded several times (23 July 1963, 18 October 1967, 10 September 1968. In Novoushitsky District I. Udra collected L. europaeus at slopes of the Dnister Reservoir near Rudkovtsy village on 6 June and 25 June 1985. In the Carpathians Mountains, two adjacent L. europaeus populations were recorded by R. Gleb on 11 May 2018 in the oak forests (50 х 25 m 2 ) comprised of Q. robur and Q. petraea located at one of ridges of the Svydovets' (near Velykyi Bychkiv village, Rakhivs'kyi district) at altitudes of 500-600 m a. s. l. Circa 30% of old Q. robur and Q. petraea trees on western slopes (steepness 10-20°) were parasitized mostly in the upper part of trees, ca. 5-10 aerial shoots per a host tree. It is noteworthy that most of old oaks survived cuttings. At the edge of a Fagus-Quercus deciduous forest, two infected trees of Q. robur located at some distance from each other were revealed on the western slope (steepness 5°). Six heavily infected Q. robur trees bearing 8-12 aerial shoots of L. europaeus at upper part of the crowns were found by the edge of a 90 m-long and 10-15 m-wide woodland belt on a northwestern slope (steepness 5°). Moreover, at the eastern slope (steepness 5-10°) at the edge of the oak forest, one Q. robur tree was parasitized by 5-10 L. europaeus individuals. In turn, on the western slope (steepness 5°) 8-10 hemiparasites were recorded on the upper part of Q. robur and Q. petraea tree crowns (8 trees in total). Furthermore, the largest L. europaeus samples (more than 50 cm in diameter), 8-12 individuals per a host tree, were observed on four Q. robur trees growing at the edge of Fagus-Quercus forest on western slope (steepness 5°).
In the Carpathian Biosphere Reserve, Chorna Hora Botanical Reserve (Vynohradivs'kyy district, near Vynohradiv city), L. europaeus was recorded in Q. robur and Q. petraea oak forests mixed with Fagus by R. Gleb on 25 February 2016. This population of the parasite resided at northern slopes (steepness 5-25°) at 230 m a.s.l., and circa 30% of the hosts were bearing L. europaeus aerial shoots. It is worth mentioning that approximately 50% of oaks were concomitantly infected by a transverse cancer accompanied by the massive wilting of oak trees in this locality.
The hemiparasite was also recorded at Mukachevo city environs, near the monastery,

Unconfirmed and/or erroneous records
Loranthus europaeus from Vinnytsya Region (Nemyrivskyi District, Bratslav city) was mentioned in the Flora of Tultsyinshyna by Zhuravl (1929); however, no herbarium specimens were found. In Kyiv Region, the species was recorded on 10 August 1857 by A.S. [P.S.] Rogovych [Rogowicz] in Kagarlyts'ky District, Lipovets village, and the corresponding specimen is deposited at MSUD (personal collection of E.E. Lindemann), mentioned by Stankov and Taliev (1949) and later in the Atlas Florae Europaeae (1976): "…on Quercus robur branches -very rare, recorded for Kyiv environs. Hemi-parasite". Finally, the most challenging task still remains to confirm the observations from the Crimean Peninsula on Fagaceae mentioned by Morozyuk (1987) and Golubev (1996).
Generally, our data indicate that native (autochthonous) deciduous species of oaks are primary hosts for L. europaeus in Ukraine. Forty years ago the area of oak forests in Ukraine embraced 26% of the total forest cover in Ukraine (Shelyag-Sosonko, 1974), but now they declined due to several anthropic and natural factors. Species of Quercus often host both L. europaeus and Viscum album L. in the western regions of the country.
It is evident that this mistletoe species is not expected to become a noxious pest causing considerable damage to the Ukrainian forests, unlike Viscum album. Moreover, in Khmelnyts'kyi Region L. europaeus is even included in the list of regionally rare species (Kovalchuk, 2017). Following the Second Addendum to the Decision of the 5 th Session of the Council of Khmelnyts'kyi Region (Oblastna Rada) of 20 December 2006, No. 18-5/2006, L. europaeus is present in the "List of species recommended for special protection in Khmelnyts'kyi Region" (see Andriyenko, Peregrym, 2012).

Conclusions
The geographic distribution range of the aerial hemiparasitic plant species Loranthus europaeus in Ukraine is confined to the southwestern regions of the country. In total, this species was reported from ca. 30 localities in Ukraine, though the records from Kyiv Region and Crimea remain unconfirmed. Loranthus europaeus parasitizes Quercus species as its primary hosts within its range in Ukraine. Due to its hemiparasitic nature and limited distribution, L. europaeus is not expected to become a noxious pest; on the contrary, it is recommended to be protected in Ukraine at the regional level.