Contributions to the genus Riccia L. (Ricciaceae) in Turkey

This study provides an identification key to the species of Riccia in Turkey and also gives information about detailed morphological and anatomic characters, reproductive forms, detailed photos of Riccia species and their spores, ecological preferences, and distribution patterns in the Mediterranean, Europe, and Southwest Asia. The number of Riccia taxa in Turkey has reached 27 including R. atromarginata, reported for the first time from Turkey in this study. Additionally, the presence of R. gougetiana var. armatissima and R. trabutiana in Turkey is confirmed here. This study reports other distribution areas of the species R. bicarinata, R. ciliata, R. ciliifera, R. crystallina, and R. papillosa, which were added to the country`s flora some years ago, beyond previously known locations. Riccia rhenana recorded from Isikli Lake, Denizli, by Walter has not been reported again from the original locality or other areas in Turkey. Within this study, all previously recorded localities and surroundings were searched in detail for the species without success. Different localities have often led to the expansion of knowledge on where these species particularly disperse all over the Mediterranean climate regions in Turkey. Additionally, in this study, Turkish names are proposed for four newly reported taxa.

to the Riccia specimens deposited in the herbaria mentioned above. A number of Riccia species were also examined in the Dahlem Botanical Garden and Botanical Museum (Berlin-Germany) (BGBM); in the Botany Unit of the Department of Animal Biology, Plant Biology, and Ecology at the Universitat Autònoma de Barcelona-BCB (Spain); and in the Institute of Biodiversity and Ecology Research, Bulgarian Academy of Sciences (Bulgaria).
The descriptions of taxa given in previous studies of the species are expanded (Jovet-Ast, 1986;Schumacker and Váňa, 2000;Bischler, 2004;Frey et al., 2006;Kürshner and Frey, 2011;Özenoğlu Kiremit et al., 2016). Morphological examinations are also included based on the length and type of rosette; colors of thallus; number of bifurcations, width, and shapes of ultimate branches; median groove width and length; the presence or absence of cilia, numbers, shape, length, structure, or presence of tubercles; and ventral scale color, position, shape, and cell size. Anatomical examinations were based on the thallus section height and width; epidermal and subepidermal cell size, color, and wall thickness; chlorenchyma and parenchyma height; and cell sizes, whether or not air chambers are considered. Moreover, sexual condition and reproductive examinations were based on sporophyte status; capsule, archegonial and antheridial neck lengths; and spore size, color, distal and proximal face shape, and wing size. The related resources were used for the distribution of taxa (Jovet-Ast, 1986;Schumacker and Váňa, 2000;Bischler, 2004;Frey et al., 2006;Ros et al., 2007;Kürshner and Frey, 2011;Özenoğlu Kiremit et al., 2016;Söderström et al., 2018).
Additionally, a key to the Turkish species of Riccia was prepared on the basis of the methods of Casas et al. (2009) and Kürschner and Frey (2011). All distinguishing characters of the specimens collected in Turkey were used in the key. The list, synonyms (Jovet-Ast, 1986), types, descriptions, habitats, and distributions of the species are given in the Appendix. Although Turkish names were given to all Turkish bryophyte taxa by Güner et al. (2017), we have proposed Turkish names for four newly reported taxa, which are Riccia atromarginata (Levier), R. beyrichiana (Hampe), R. cavernosa (Hoffm.), and R. crinita (Taylor).
Photographs were taken in the natural environment of the species during the field trips. Microstructure of spore surfaces of the species was studied using a scanning electron microscope (SEM) at Selçuk University. Crosssections of thalli and general overviews of spores were photographed under a light microscope (N2203720 Olympus CX41RF-5 Trinocular Microscope). Digital photographs were used for anatomical measurement and anatomical drawing (Adobe Illustrator CS5). New records are marked by asterisks.

Results and discussion
The family Ricciaceae includes two genera, both known in Turkey: Riccia and the monotypic Ricciocarpos Corda. Ricciocarpos, a monotypic genus, with Ricciocarpos natans (L.) Corda, was registered in Sakarya Province by Seçmen et al. (1989). Ricciocarpos is separated from Riccia by its long pendant scales with serrate margins and the presence of oil cells in the scales and the thallus.
Turkish name: Çatalcık. Lectotype: Riccia glauca L., fide Hässel Menendez in Opera Lilloana 7: 208 (1963); Na-Thalang, Brunonia 3: 71 (1980). Riccia plants are mostly small (thalli generally 0.5-4 mm wide, 2-30 mm long), dichotomously branched and often forming rosettes, terrestrial or sometimes floating; upper side and margins are sometimes with cilia or papillae; groove median is deep or shallow, along the length of branches or only apical. Epidermis is persistent or decaying, epidermal pores are more visible among epidermal cells; assimilatory tissue or chlorenchyma is compact, in vertical cell columns, enclosing narrow air channels, open at top, or spongy, with one to three layers of air chambers; storage tissue cells or parenchyma are rounded, occupying ventral 1/2 or less of thallus; oil bodies are absent; scales vestigial to conspicuous, hyaline or variously colored, lateral or ventral, usually imbricate, sometimes absent; rhizoids smooth or tuberculate, usually numerous, absent in floating plants. Typical gemmae are unknown.
In some species, asexual reproduction can be seen with one or several apical or ventral tubers. Monoicous or dioicous; antheridial and archegonial necks are often protruding. The genus has a simple sporophyte that is embedded and virtually hidden in the tissues of the vegetative thallus. There is no foot or seta, and at maturity the spherical sporophyte consists merely of capsule wall without thickenings with spores enclosed that are released when the capsule wall disintegrates. Spores with tetrads are separated at maturity, 40-200 µm in diameter, distal and proximal faces are alveolate, tuberculate or nearly smooth, with distinct triradiate mark; wing has with several dimensions and shapes.
The genus comprises 250 species with a worldwide distribution from the Arctic to the Antarctic (Söderström et al., 2016).

Key to the species of Riccia in Turkey
The Turkish Riccia key was prepared based on the methods of Kürschner and Frey (2011) and Casas et al. 5* Thallus bluish green, dorsally crystalline, sparingly dichotomous; dorsal surface with small pores air chambers, the thalli with large alveolate only with age; spores 65-80 µm in diameter, light brown, distal face regularly areolate, margins here and there with a pore; on shaded soil in fields, on paths mainly in anthropogenic landscapes but also on mud by ponds ..  Figure 1L) 7* Thallus branches to 2 mm wide, 5-8 times as wide as thick, with coarse areolation; branches short, usually lingulate; marginal cells of thallus 25 × 40-50 µm; cells of ventral scales to 65 µm long; in pools and on mud at edges of drying-out ponds .   This study was planned to determine the status of the Turkish Riccia. Additionally, detailed morphologic and anatomic characteristics, reproductive forms, detailed photos of Riccia species and spores in SEM, distribution patterns, and ecological preferences are given.
Previous studies on the genus in Turkey reported 26 taxa. Additionally, R. atromarginata was recorded for the first time during this study, raising the present number to 27 taxa (25 species and 2 varieties). The presence of R. gougetiana var. armatissima and R. trabutiana in Turkey is also confirmed by this study.
R. atromarginata can be distinguished from the rest of the members of the Riccia subgenus by its finger-like papilla on thallus. However, it is considerably similar to R. trabutiana in spite of some slight differences in comparison of thallus color, the presence of papilla, and rounded margins of lobes and spores.
After Walter (1967) recorded the species R. rhenana from Işıklı Lake, Denizli, as an aquatic form found in the lake, no new record of the species has been reported. Within this study, all localities and surroundings that were previously recorded for the species were searched in detail for the species; however, nothing was found.
An aquatic form of Riccia fluitans has been recorded only in water bodies of Kazan Lake (called Kazangöl) (Selçuk/İzmir). Although we carefully searched for the species in similar water bodies, we never found aquatic forms of the species in any other locations. Kazan Lake is slightly salty. The locality where the species was collected is an area facing pollution under the influence of intense human activities; thus, the known locality is also under threat.
This study reports new localities of species (R. bicarinata, R. ciliata, R. ciliifera, R. crystallina, and R. papillosa), which were recorded among the country's flora a number of years ago. R. ciliifera, which was first recorded from Bursa by Bornmüller in 1931, has never been recollected and recorded until now. Our study reports that the species were found to be widespread on volcanic tuff along with R. michelii and Oxymitra incrassata and were collected from the hillside of Demirköprü Dam Lake near the town of Sindel (Salihli/Manisa). Thus, the known distribution of the species in Turkey has been expanded. Recording of R. cavernosa from the transition zone between the Middle Black Sea and the Central Anatolia regions in Turkey is significantly worth mentioning in terms of the zone having a Mediterranean climate. R. cavernosa is easily characterized by its sponge-like structure. Records of R. crinita from Turkey filled the distribution gap missing between Europe and the Middle East.
An overall evaluation for all recorded localities in general showed that the genus Riccia prefers Mediterranean-type localities. However, it is also observed that species (R. bifurca, R. papillosa, R. trabutiana) might be distributed in different habitats with variable climate types, such as alpine zones and plateaus with high altitudes (e.g., Trabzon and Van). Different localities have often led to the expansion of knowledge of species distribution all over the Mediterranean climate regions in Turkey.
Riccia species that occur only in the Mediterranean Region and its surroundings in Turkey can be found in the period of time between December and March. On the other hand, the species occurring in alpine zones were found only between June and August, along with their spores. Therefore, this is a significant detail to consider when planning a field study to collect the species. It is also observed that Riccia species often prefer to be present in open fields such as roadsides, soil floors, and footpaths, which are under the influence of human activities, but not in dense vegetation. Furthermore, it becomes increasingly difficult to find and collect the species when the open areas in question are covered by other herbaceous plants. Most of the localities recorded in this study face habitat loss due to anthropogenic pressure factors such as migration, urbanization, commercial activities, and pollution along with fire events and also soil drying in relation to global climatic changes.
Studies relevant to Riccia are limited and will definitely contribute to studies on the Turkish bryoflora. Moreover, the identification key designed here for the genus in question will be a useful referral source for interested researchers. Plants forming incomplete rosettes or crowded mats; thallus bluish green, dark purplish on the rounded margins ( Figure 1A); thalli 2-3 furcate, ultimate branches 1-1.6 mm wide, obovate, narrowed from apex towards base, rounded apically; median groove shallow, often narrow, widening to 1/3 branch width, distinct almost to base; papillae numerous, hyaline, finger-like, rounded at top, intensely on margins, seldom on dorsal side of thallus, 120-180 µm, straight or curved, intensely curved; ventral scales pink or purplish; rhizoids smooth and internally tuberculate. Thallus sections of lobes as wide as high near top of lobes, 1.5 times wider than high below, contain colored idioblast cells; epidermis of 2 layers, subepidermal cell thin-walled; ventral scale cells 20-25 × 28-38 µm. (Appendix Figure 1). Dioicous. Archegonial necks purple; spores 90-110 µm, dark brown, distal face with 12-18 alveoli across diameter, limited by thick walls with tubercles at wall corners ( Figure 2A1), proximal faces similarly ornamented ( Figure 2A2), without wing, crenulate on margin by projecting tubercles.
Riccia atromarginata was found in subalpine vegetation. It was growing on soil in the grassland area near the lake. Accompanying species is Riccia trabutiana.
Riccia atromarginata can be distinguished from other members of the subgenus Riccia by its finger-like papillae on thallus. It is closely allied to R. trabutiana, from which it differs in color of the thallus, presence of papillae, and rounded margins of lobes.  (Sérgio and Melo, 2015).

Riccia beyrichiana
The discovery of R. beyrichiana is a significant extension range to the eastern border of its known range. Easternmost localities of R. beyrichiana (of Greece and Turkey) appear rather isolated compared with the bulk of localities in Portugal, Spain, France, and North Africa. The discovery is also a new record for Southwest Asia.
Riccia bicarinata can be distinguished from other members of the subgenus Riccia by its spoon-like thallus lobes, marginal cilia triangular enlarged at base and connate in groups of two to three.
Riccia bifurca was growing on soil in olive tree, Pinus brutia L., and Quercus coccifera plantations.  Konya, Hadim, Beyreli Plateau (1956 m), and Van, Nebirnav Plateau (2920 m). These alpine localities are very different from the Mediterranean climate type and these localities are very important as extended Riccia distribution areas and types.
Riccia canaliculata can be distinguished from other members of the subgenus Ricciella by the narrow chambered thalli with the apex of the branches distinctly narrowed and covered by the apical ventral scale.

Riccia cavernosa
Riccia cavernosa has been found on wet soils in river banks, in Populus alba L., Rubus sp., and Salix sp. plantations. The species was growing on wet soil and sandy rock ledges in the lowlands (Özenoğlu Kiremit et al., 2016).
Riccia cavernosa can be distinguished from other members of the subgenus Ricciella by the irregular perforations on dorsal side. R. crystallina is a similar species to R. cavernosa, but R. cavernosa differs from R. crystallina as the thalli dorsal surface is strongly alveolate and spore distal face with imperfect areolation. In R. crystallina, the thalli dorsal surface is alveolate only with age and spore distal face regularly areolate.
The specimen was collected from the transition zone between the Middle Black Sea and Central Anatolia, which has a Mediterranean climate.
Distribution: Riccia cavernosa is widely distributed in warmer regions of all continents (Jovet-Ast, 1986). It occurs in various parts of the world with the exception of the high Arctic and Antarctic (Borovichev and Bakalin, 2016).

Riccia ciliifera
Riccia ciliifera was growing on volcanic tuff fall near the lake and on wet soil in streambeds. Verbascum sp. was very common in the habitat. Accompanying species were Oxymitra incrassata and R. michelii.
Riccia crinita can be distinguished from other members of the subgenus Riccia by the very long and numerous cilia at margins, on the dorsal side, and above capsule.  (Sérgio and Melo, 2015).

Riccia crystallina
Riccia crystallina grows on soil in open areas and was collected from olive grove, citrus garden, and antique city areas with anthropogenic pressure. Especially accompanying species is Sphaerocarpos texanus.
Riccia crystallina can be distinguished from other members of the subgenus Ricciella by glaucous-bluish green color, forming large thinly-shaped and flat rosettes, crystalline dorsal side with small perforation mainly in old parts.  Croatia, Czech Republic, Denmark, Egypt, England, Finland, France, Germany, Greece, the Netherlands, Hungary, Iraq, Iran, Israel, Italy, Latvia, Lebanon, Libya, Lithuania, Madeira, Malta, Morocco, Norway, Poland, Portugal, Romania, Russia, Sardinia, Serbia, Sicilia, Scotland, Slovenia, Spain, Sweden, Switzerland, Tunisia, Turkey, and Ukraine in the Mediterranean Region, Europe, and Southwest Asia.
In Turkey, the aquatic form of Riccia fluitans is only known from İzmir, Selçuk, Kazangöl. Kazangöl is a brackish water lake (Cl -= 1.179 mg mL -1 , Na + = 1540 mg L -1 , 88 mg CaCO 3 100 mL -1 water) (Aysel et al., 1998). Plant locality has a very narrow water basin and is under anthropogenic pressure. Compared to previous years, there is a marked reduction in R. fluitans population. Possible reason for this decrease in the lake is that the water comes from areas with heavy human exploitation, thus exposed to pollutants. Terrestrial form was collected on soil in a small streambed in Pinus brutia plantation. Accompanying species of terrestrial form are Lunularia cruciata, Reboulia hemisphaerica, Targionia hypophylla, Timmiella barbuloides (Brid.) Mönk., Didymodon insulanus, Didymodon acutus (Brid.) K. Saito, and Bryum sp. (Özenoğlu Kiremit and Kırmacı, 2012).
Terrestrial form of Riccia fluitans can be distinguished from other members of the subgenus Ricciella as the dorsal surface of dry plants is generally plane in R. fluitans, unlike the dry thalli of R. canaliculata, which are canaliculated with branch apices covered by ventral scales. R. perennis thalli are wider than in this species, with stalked terminal tubercules, which are for vegetative reproduction and not found in R. fluitans.

Riccia michelii
Riccia perennis grows in grasslands, in small streambeds, on wet soil that most probably are exposed to severe drought during hot months. Riccia perennis has been found in quite open olive tree and oak (Quercus L. sp.) plantation. The thalli grow often exposed to direct sun in imperfectly shaded localities. Direct associates include Corsinia coriandrina, Lunularia cruciata, Gongylanthus ericetorum (Raddi) Nees, Phaeoceros laevis, Riccia gougetiana var. armatissima, and R. subbifurca.
Riccia perennis can be distinguished from other members of the subgenus Ricciella by the size (very robust), color (yellowish tinge), lobe width (more than 1.7 mm wide), and tubers on apical ventral face of the thallus. No other species of the subgenus Ricciella has a thallus of more than 1.5 mm wide so identification is almost immediately possible even in the field.  (Hugonnot and Offerhaus, 2009;Özenoğlu Kiremit and Hugonnot, 2010).
The discovery of R. perennis is a significant extension of the range to the east. Possibly due to the lack of systematic floristic exploration, the easternmost localities of R. perennis (of Greece and Turkey) appear rather isolated compared with the bulk of localities of Portugal, Spain, Sardinia, and North Africa.
The species was until now considered a western Mediterranean endemic. The locality of Ukraine (Düll, 1983;Söderström et al., 2002), which appeared somewhat dubious (Jovet-Ast, 1986), should be reevaluated (if the specimen can be traced) in the light of the discovery of the species in Turkey. Taking into consideration the new locality provided in the present work, the species must be considered as a Mediterranean and Southwest Asiatic element.