Morphological features of the flower of Symphoricarpos species (Caprifoliaceae) introduced to Ukraine

With the help of light and scanning electron microscopy, the features of inflorescences and flowers of six species of the genus Symphoricarpos introduced to Ukraine were studied, and the peculiarities of their structure were specified. Morphological peculiarities of the calyx, corolla, stamens, and style, differentiating S.  albus (including S. racemosus and S. rivularis), S. hesperius, S. mollis, S. occidentalis, S. orbiculatus, and S. oreophilus var. utahensis, were determined. The obtained data are important for identification of the species and taxonomy of the genus Symphoricarpos. In particular, the results of our study showed that flowers of S. racemosus, S. rivularis, and S. albus share common features and this supports their synonymy under the name S. albus. Other five Symphoricarpos species showed differences in their floral morphology. Among the important features for identification of Symphoricarpos species introduced to Ukraine, which were not mentioned in available literature sources we can list: the number of flowers in the inflorescence, features of pedicels, shape and features of bracts pubescence, shape of calyx teeth and their pubescence, presence or absence of corolla tube convexity, presence of ovoid projection of anther’s connective, and size of all the floral elements. Symphoricarpos oreophilus var. utahensis has unique features of floral morphology. Its single flowers located in the axis of the leaves on the pendent pubescent pedicels; the calyx is elongated, fusiform; the corolla is narrowly tubular, without a convex at the base; the stamens are shorter than the corolla tubule or rarely of the same length, with a clear ovoid projection on the apex.


Introduction
The genus Symphoricarpos Duhamel includes 9 to 15 species, and belongs to the family Caprifoliaceae Juss. of the order Dipsacales Juss. ex Bercht. & J. Presl (Takhtajan, 1997(Takhtajan, , 2009. Today numerous molecularphylogenetic studies are actively performed on different representatives of this order. Thereafter, active discussion regarding the evolution of the reproductive organs of these representatives is ongoing (Bell et al., 2001;Zhang et al., 2003;Theis et al., 2008).
Dipsacales demonstrates the number of evolutionary changes that may be of interest in understanding the morphology of flower in general. The modern representatives of this order have from five (the most common) to three lobes of corolla, and the number of stamens vary from one to ten (most often there are five or four stamens per flower). The ancestor of the recent Caprifoliaceae is still unknown. Modern representatives of the family have funnel-shaped or campanulate flowers with four or five lobes, small calyx, four or five Floral morphology of Symphoricarpos species introduced to Ukraine stamens, elongated style, and capitate or lobed stigma. Probably before that, they were slightly different, and had symmetrical flowers with large calyxes, tubular corollas with five lobes at the apex, five stamens, elongated styles, and capitate stigmas. Among some species of the genus Symphoricarpos, the reduction to four lobes of the corolla and four stamens happened. In general, five types of flower shape were suggested for Caprifoliaceae, and the genus Symphoricarpos has been classified as those having radially symmetrical flowers (Roels & Smets, 1996;Donoghue et al., 2003;Zhang et al., 2003;Howarth & Donoghue, 2005;Hauser, 2007;Theis et al., 2008).
The genus Symphoricarpos includes shrubs with multicolored fruits, and therefore these plants are often used as ornamental.
According to Mosyakin & Fedoronhuk (1999), S. albus (L.) S.F. Blake (= S. racemosus Michx. and S. rivularis Suksdorf.) is widespread in Ukraine as an ornamental plant. While S. occidentalis Hook. and S. orbiculatus Moench. are rarely applied for landscaping in gardens and parks of Ukraine (Barbarych, 1961). Some other species of the genus (i.e., S. hesperius G.N. Jones, S. mollis Nutt., S. oreophilus Gray) were also introduced to Ukraine, and their specimens are stored at the herbarium of the M.M. Gryshko National Botanical Garden of the NAS of Ukraine.
Due to the wide introduction of Symphoricarpos in Ukraine, it is important to study their morphological features in more details, with special emphasis on the structure of their reproductive organs and identify taxonomic diagnostic features. However, the literature provides little information on their morphological features of inflorescence, flower, and fruits of Symphoricarpos species, which are represented in some local floras (Leroy & Stinchfield Ferris, 1960;Barbarych, 1961;Welsh et al., 1987Welsh et al., , 1993Gilbert, 1995;McWilliams, 2000;Sell & Murrell, 2006;Yang, 2011).
Hence, we decided to clarify the features of the flower of Symphoricarpos introduced to Ukraine, and identify additional features, which could be applied in the taxonomy of the genus.

Material and methods
The material from the National Herbarium of the M.G. Kholodny Institute of Botany of the National Academy of Sciences of Ukraine (KW) and the Herbarium of the M.M Gryshko National Botanical Garden of the National Academy of Sciences of Ukraine (KWHA) has been used. The citations are provided accordingly to the original text of the labels. The flowers of 18 specimens of six Symphoricarpos species listed below were investigated. Macromorphological features were analyzed for all flowers present on the herbarium voucher (in average 3-5 flowers per voucher). For the micromorphological analysis, from 1-2 (S. hesperius, S. mollis, S. oreophilus) to 3-5 flowers were sampled (S. albus, S. occidentalis, S. orbiculatus) depending on the number of available vouchers.
Macromorphological features of the flowers were studied using MBS-9 binocular microscope. Floral elements were measured using AxioVision Rel. 4.8 software. For scanning electron microscopy (SEM, JSM-6060 LA) the specimens were fixed on the brass table, then these samples were goldcoated. The descriptions of floral elements follows terminology of Fedorov & Artiushenko (1975) and Zyman et al. (2004Zyman et al. ( , 2011

Results and discussion
Flowers of Symphoricarpos are actinomorphic, symmetrical, and small (about 10 mm long), with short ribbed pedicels (S. albus, S. orbiculatus, S. racemosus, S. rivularis) or pedicels without ribs (S. hesperius, S. mollis), grouped in short racemes, located in the axils of the upper leaves on the apical or lateral branches. At the base of the ovary of each flower of all studied species there are two opposite, small (0.5-1.5 mm long), ovate or triangular bracteoles, which are coalescent at the base (in S. oreophilus var. utahensis bracteoles are free), pubescent along the edges, or glabrous (S. hesperius, S. mollis, and S. occidentalis) (Tables 1 & 2).
There are (4-) 5 stamens with thin filaments and ellipsoidal anthers attached to the filaments in the middle; the length of the anthers is 1.0-1.5 mm. The stamens in most of the studied species are located in the tube of corolla; they are mostly equal in length or slightly longer than the corolla. However, S. occidentalis have stamens longer than the corolla, while the stamens of S. oreophilus var. utahensis are shorter than the corolla. We noted that the stamens of the studied Symphoricarpos species have an ovoid projection of the connective above the anthers; the length of this projection is about 0.5 mm (Fig. 4). The presence of such projections has been recently reported for Linnaea borealis L. (Tsymbaliuk et al., 2018).
The pistil has a thin style, which is usually shorter than the corolla. However, in S. occidentalis column is longer than the corolla, and in S. racemosus it is equal to the corolla. In all the investigated species, the stigma is capitate, about 0.5 mm in diameter (Tables 1 & 2).
Two close species (S. orbiculatus and S. occidentalis) showed some differences in their floral morphology. In particular, S. orbiculatus have short pedicels, whereas in S. occidentalis the flowers are sessile. S. orbiculatus bracteoles are sparsely pubescent, with small subulate hairs along the edges, while S. occidentalis bracteoles are glabrous. Each teeth of calyx in S. orbiculatus have a bundle of subulate hairs at the apex, whereas in S. occidentalis they are glabrous. The corolla lobes of S. orbiculatus are oval, with rounded apices, equal to 1/3 of the corolla length; these lobes in S. occidentalis are broadly oval, with acute apices, equal to     1/2 of the corolla length. We noted that the stamens and style exceed the corolla in length exclusively in S. occidentalis, hence it can be a diagnostic feature of this species (Tables 1 & 2). The following differences for other two similar species (S. hesperius and S. mollis) were found. The flowers of S. hesperius are with triangular calyx teeth, broadly bellshaped, and with a longer corolla; the tube of the corolla is crescent-shaped at the base; the filaments of stamens are glabrous. The calyx teeth of S. mollis flowers are deltoid; the corolla is campanulate and shorter; the stamen filaments pubescent by ribbon-like hairs.
Symphoricarpos oreophilus var. utahensis presents a peculiar floral morphology that distinguishes it from all the other studied representatives of the genus Symphoricarpos. It has solitary flowers on long (2-4 mm against 1 mm in other studied species) pendent pedicels, which are densely pubescent by simple bristly and glandular hairs. Other species have numerous flowers organized in racemes and placed on erect, glabrous pedicels. The calyx of S. oreophilus var. utahensis is elongated and spindle-shaped, unlikely to other species. Its corolla is narrowtubular, 2-4 mm in diameter and is much shorter than the tube. The tube is not convex at the base. The stamens are shorter or rarely of the same size as the corolla (Tables 1 & 2).

Conclusions
The micro-and macromorphological peculiarities of the flowers of six Symphoricarpos species introduced to Ukraine were specified. The morphological features of the calyx, corolla, stamens and style allowing distinguishing S. albus, S. hesperius, S. mollis, S. occidentalis, S. orbiculatus, and