Introduction
Bryophytes, the pioneer plants of different substrate types, are one of the most important component of forest ecosystems (Longton 1992,Baldwin and Bradfield 2005,Ezer 2017,Mellado-Mansilla et al. 2017). Bryophytes are poikilohydric organisms whose their moisture content rapidly equilibrating with environmental conditions (Green and Lange 1994). Therefore, they are highly sensitive to environmental factors (Schofield 2001). In particular, abiotic ecological factors such as humidity directly or indirectly affect the colonization and the distribution of bryophytes in the epiphytic habitat (Mazimpaka and Lara 1995,Schofield 2001,Mishler 2003,Mazimpaka et al. 2009). In addition to environmental drought, phorophyte-type, physical and chemical properties of bark characteristics such as rugosity, water retention capacity, bark pH, and dust deposition are also important for the spatial distribution of bryophytes on epiphytic habitats (Lara and Mazimpaka 1998,Mazimpaka et al. 2010,Ezer 2017).
Some studies on the succession of epiphytic bryophyte communities have revealed that the succession gradient of epiphytes is highly complex due to changes in positive and negative interactions among species within epiphytic communities as trees age (Mazimpaka et al. 2010,Ódor et al.2013,Bargali et al. 2014,Ezer 2017,Ezer et al. 2019).
Although phytosociological studies on epiphytic bryophytes in Türkiye have made progress in the last decade (Alataş et al. 2017,2021,Alataş 2018,Can Gözcü et al. 2018), few studies have been done on the spatial distributions and community composition of epiphytic bryophytes in successional stages (Ezer and Kara 2013,Ezer 2017,Ezer et al. 2019).
The present study focuses on the vertical distribution patterns of epiphytic bryophytes and community composition in the successional stages on trunks of B. sempervirens trees in Fırtına Valley. This study aimed to reveal the successional trends of bryophyte communities on the epiphytic habitats of boxwood trees and to contribute to bryo-ecological studies in Türkiye.
The study area
The Çamlıhemşin (Rize, Türkiye) District, in which the study area is located, is surrounded by Pazar and Ardeşen to the north, Çayeli, Hemşin and İkizdere districts to the west, and Artvin Province Yusufeli district to the east. The distance of the district to Rize city center is 62 km. The B. sempervirens forests, located in the Fırtına Valley and within the boundaries of the Çamlıhemşin District, are located within the A4 square according to the Henderson (1961) grid-square system and are in the colchic zone of the Euro-Siberian phytogeographic region (Anşin 1983,Fig. 1).
The Fırtına Valley, which exhibits a unique phytological diversity, hosts many rare species due to the presence of all the main habitats of the region. Buxus sempervirens, which has a very wide distribution in the Euro-Siberian Phytogeographic Region, forms remarkable communities in the valley (Kurdoğlu et al. 2004). Moreover, in 1999, the WWW (World Wildlife Fund) identified Europe’s 100 forest areas valuable in terms of biodiversity and in urgent need of protection (Myers et al. 2000). Nine of these areas, which are called “Hot Spots of European Forests”, are located in Türkiye (Satar and Güneş 2014). One of these nine hot spots is the Fırtına Valley. Only one study on bryophytes has been conducted in the valley so far (Abay et al. 2006).
Fırtına Valley, like the whole of the Eastern Black Sea Region, is an area very open to natural disasters such as landslides, rockfalls and avalanches due to the very steep slopes, rainy climatic conditions and, soil cover (Tunçel 1990).
Lithologically, there are units from almost all geological times in the valley (Bayrakdar 2006). In Türkiye, not rich in current glaciers, Kaçkar Mountains (3932 m) located to the south of the Fırtına Valley are one of the regions where current glaciers are found (Çiner 2003). The Kaçkar Mountains, the Verçenik (Üçdoruk) Mountain, the Bulut Mountains and, the Altınparmak Mountains are mountain ranges that limit the study area in the SW-NE direction. In the valley, which is also very rich in terms of rivers, Fırtına Stream is divided into branches at various degrees and forms the smaller Tunca, Hala, Palovit, Haçivanak and Hemşin creeks. These creeks also forked among themselves and surround the valley like a net system.
The forest formation, which starts at 200 m in the north of the study area, is very rich in terms of under-forest flora, depending on the oceanic and temperate climatic conditions in all seasons. This forest formation, which is dominated by broadleaf trees, loses its colchic feature with the increase in altitude and gives way to mixed forests and then to coniferous forests (Özçağlar et al.2006). The vegetation in the Fırtına Valley shows a distinct difference from other valleys, especially with its particular forest formations and flora richness. There are basically three types of forest formation such as alluvial forests, hardwood forests found in river floodplains and regularly flooded for a portion of the growing season; boxwood forests; and old growth forest formations in the Fırtına Valley (Kurdoğlu et al. 2004).
The B. sempervirens forests spread along the Fırtına Stream and its tributaries, between 200-1500 meters of the study area. Although these forests are seen along the streams, they are also found in large groups on the valley slopes. These forests are widely found between 900-1300 meters along the Çamlıhemşin-Meydan road, in Şimşirlik place, within the Gito Forests and Palovit Valley.
The study area generally has a temperate Oceanic climate. The annual average precipitation is 2192 mm and, the annual average temperature is 8.3 ºC in Çamlıhemşin. The hottest month of the year is August and the coldest is January. The absence of a dry season indicates that the Fırtına Valley is under the influence of an Oceanic climate (Akman 2011).
Material and methods
Field sampling procedures
The epiphytic bryophyte specimens were collected from the living trunks of B. sempervirensin Fırtına Valley during field studies in 2020. The locality details are given inTab. 1. A total of 60 sampling plots were taken from the trunks of 20 boxwood trees of different ages in the valley. Spatial distributions and community structures of epiphytic bryophytes in successional stages on boxwood trees were investigated according to tree diameter at breast height (dbh) and tree age. The trees were divided into three age classes using an indirect method as young (dbh 20-35 cm, 21 plots), middle-aged (dbh 40-50 cm, 18 plots), and aged trees (dbh 60-80 cm, 21 plots). Each boxwood tree was divided into the lower base zone (0 - 40 cm from the ground), the middle zone (40 - 120 cm), and the upper zone (120 - 180 cm) as proposed by Moe and Botnen (2000).
Sampling plots from tree zones were defined by 20 × 20 cm2, determined according to species diversity on the living trunks of B. sempervirens. In the present study the branches of the boxwood trees did not provide sample plots, only the trunks. The percentage cover of the species within the each sample plot was visually estimated and ecological data such as humidity, aspect and light of the epiphytic habitat were recorded.
The nomenclature of the epiphytic bryophyte species determined within the sample plots follows Ros et al. (2013) and Hodgetts et al. (2020) (Tab. 2). Habitat affinity types of bryophytes were established following Mazimpaka and Lara (1995) and Draper et al. (2003). Life forms of the taxa were determined according to Mägdefrau (1982). Voucher specimens were deposited in the herbarium of Niğde Ömer Halisdemir University.
Data analysis
The relative frequency of each taxon in the sample plots was determined by the index of ecological significance (IES) described by Lara and Mazimpaka (1998), Albertos et al. (2001) and Mazimpaka et al. (2009). The formula used to calculate the IES values for each taxon is as follows:
IES = F (1 + C)
C = Σ ci / x
where F is the relative frequency (100 x / n), and C is the cover of the taxon (Σ ci / x), while x represents the number of sample plots containing the taxon, n is total number of sample plots, and ci is cover class assigned to the taxon in each sample plot.
Cover classes of taxa were established using the six-point Lara and Mazimpaka (1998) scale: [0.5 (< 1%), 1 (1-5%), 2 (6-25%), 3 (26-50%), 4 (51-75%) and, 5 (76-100%)]. In addition, the IES values were combined in the following abundance classes: very scarce (< 25), scarce (26-50), moderately abundant (51-100), abundant (101-200), and dominant (> 200).
Here, TWINSPAN and DECORANA (Hill 1979,Seaby and Henderson 2007) were used to explore the community composition and spatial patterns of epiphytic bryophyte communities and their relationship with the associated environmental factors of the epiphytic habitat. In this context, TWINSPAN and DECORANA were applied to the matrix of cover in 60 sample plots according to the computer program CAP (Community Analysis Package-5) of Seaby and Henderson (2007).
Results
Floristical results
Twenty-nine species belonging to 17 families and 25 genera were determined as a result of the identification of 362 specimens. Among them 24 are mosses (21 pleurocarpous and 3 acrocarpous), and 5 are liverworts. Neckeraceae (6 species, 20.6%) and Brachytheciaceae (5 species, 17.2%), both pleurocarpous moss families, are the most species-rich families found in epiphytic habitats on boxwood trees in the study area (Tab. 2). Exsertotheca crispa (Hedw.) S.Olsson, Enroth & D.Quandt is the most common species in the B. sempervirens forests of Fırtına Valley.
Ecological results
Six different life forms were determined. Among them, the mat life form prevailed (34.4%), followed by the weft life form (24.1%). The dendroid life form was negligible (3.4%) (Tab. 2). In addition, four different habitat affinity categories as cortico-saxicolous, indifferent, customary epiphyte and preferentially not corticolous were determined belonging to the species. While cortico-saxicolous species were the most common with 51.7% within the sample plots, the preferentially not corticolous type habitat affinity is least common with one species (Tab. 2).
Lower base zone
The spatial distributions and community structures analyses showed that a total of 11 species, all of them are mosses, were found on the base zone of young boxwood trees (dbh 20-35 cm). Among of the mosses E. crispa was the most frequent and the most dominantm with the highest IES value (271). Isothecium alopecuroides was co-dominant with 214 IES values. Homalia trichomanoides and Sciuro-hypnum flotowianum were abundant species with 171 and 143 IES values on the lower base of trunks of B. sempervirens. Brachythecium rutabulum, S. populeum and Thamnobryum alopecurum which have the lowest IES values (43) were scarce on the lower base (Tab. 3). Whereas the weft life form was the most dominant (36.3%) in the base zone, the life forms mat and fan were co-dominant (27.2%). Also, the cortico-saxicolous type habitat affinity of the species was the most common with 54.5% on the base zones of young boxwood trees.
Fifteen mosses were collected from the lower base of the middle-aged B. sempervirens (dbh 40-50 cm). Among them, E. crispa (266 IES value) and H. trichomanoides (216 IES value) were the two most dominant species. Sciuro-hypnum flotowianum was the most abundant on the base zones of the middle-aged trees with the 183 IES value. Anomodon viticulosus, Pseudoleskeella nervosa and S. populeum were scarce with the lowest IES values (33). Moreover, Ctenidium molluscum and P. nervosa were only found on the lower bases of middle-aged trees (Tab. 3). While the fan life form is the most dominant (33.3%), the life forms mat and weft were co-dominant (26.6%) on the lower base of middle-aged boxwood trees. Cortico-saxicolous type affinity of epiphytic habitats (60%) were the most common on the basal zone of middle-aged trees.
Twelve species (11 mosses, one liverwort) were determined on the lower bases of aged boxwood trees (dbh 60-80 cm). Exsertotheca crispa was still the most frequent and the most dominant with the highest IES value (371). This value is also the highest among all tree-size groups (Tab. 3). While, Hypnum cupressiforme, I. alopecuroides, Pseudanomodon attenuates and, S. flotowianum were abundant, Fissidens serrulatus, Oxyrrhynchium hians and, Plagiothecium nemorale usually not epiphytic, were scarce with the lowest IES values (28). The mat life form was the most dominant with 41.6% and cortico-saxicolous species (50%) were still the most common on base zones of aged B. sempervirens.
Middle zone
Twelve species (11 mosses, one liverwort) were determined on the middle zones of the young boxwood trees. Alleniella besseri and A. complanata were the most frequent and the most dominant with the highest IES values (328). While E. crispa was co-dominant with 314 IES values, Radula complanata (200), P. attenuatus (128) and, Palamacladium euchloron (128) were abundant on the middle parts of the trunks of the young B. sempervirens (Tab. 3). The mat life form with 33.3% and the cortico-saxicolous type habitat affinity with 83.3% were still most dominant on the middle parts of trunks of young boxwood trees.
Twelve species were collected from the middle zones of the middle-aged boxwood trees. Alleniella besseri was the most dominant with the highest IES values (316). Alleniella complanata andE. crispa were co-dominant, both with 266 IES values. Frullania tamarisci, I. alopecuroides and,Pseudoamblystegium subtile were scarce with the same IES values (33) on the middle zones of middle-aged trees (Tab. 3). The life form mat was the most dominant with 41.6% and cortico-saxicolous species were conspicuously the most common with the rate of 91.6% on middle parts of the middle-aged B. sempervirens.
A total of sixteen species, five of which were liverworts, were determined in the middle zones of the aged boxwood trees. All of the liverworts, which were determined in the epiphytic habitats of the boxwood forests, were found on the middle parts of the old trees. While A. complanata was the most frequent and the most dominant, with the highest IES value (342), E. crispa and A. besseri were co-dominant with the same IES values (314) (Tab. 3). The mat life form (50%) and the cortico-saxicolous type affinity (68.75%) were the most dominant on the middle zones of aged trees.
Upper zone
Ten species were found on the upper zones of young trees. Among them, eight were mosses and, two were liverworts. Exsertotheca crispa was still the most frequent and the most dominant with the highest IES value (357). Alleniella complanata, A. besseri and, Leucodon sciuroides were co-dominant with the higher IES values (>200) on the upper zones of the young B. sempervirens. While Orthotrichum pumilum (IES value 200), Ulota crispa (200) and, R. complanata (114) were abundant on these zones, S. flotowianum (28) was scarce with the least IES value (Tab. 3). The mat life form (40%) and the habitat affinity type cortico-saxicolous (70%) were the most common on the upper parts of young trees.
Eleven species (nine mosses, two liverworts) were collected from upper zones of the middle-aged boxwood trees. While E. crispa was still the most frequent and the most dominant with the highest IES value (366), A. besseri, A. complanata and, L. sciuroides were co-dominant (> 200). And also, U. crispa (167) was abundant on the upper zones of the middle-aged B. sempervirens (Tab. 3). The mats (45.45%) and cortico-saxicolous species (72.72%) were the most dominant.
A total of thirteen species were determined on the upper zones of the old B. sempervirens. Among them, four were liverworts and nine were mosses. Alleniella complanata was the most frequent and the most dominant with the highest IES value (342). While A. besseri (IES value 300), E. crispa (328) and, L. sciuroides (300) were co-dominant with the higher IES values, O. pumilum (200), R. complanata (143) and, U. crispa (200) were abundant on the upper parts of aged boxwood trees (Tab. 3). The life form mat (30.7%) and the habitat affinity type cortico-saxicolous (53.8%) were the most common again on the upper parts of old trees.
TWINSPAN classification
TWINSPAN classified the epiphytic bryophyte communities on the trunks of B. sempervirens in the Fırtına Valley at the second level into two main clusters (A and B) and three sub-clusters (A1, B1 and, B2) (Fig. 2). These main and sub-clusters were named according to the dominant, co-dominant and abundant species which were the distinctive species within the communities. The main cluster, A, occurred in lower-base communities and it was characterized by dominant species E. crispa and H. trichomanoides, co-dominant I. alopecuroides and abundant P. attenuatus and S. flotowianum. The second main cluster, B, occurred in middle and upper zone communities. Cluster B was characterised by dominant species A. besseri and A. complanata, co-dominant E. crispa and L. sciuroides, abundant species O. pumilum, P. euchloron, R. complanata, and U. crispa.
Epiphytic bryophyte communities
The A1 community was named Exsertotheca crispa-Isothecium alopecuroides due to the frequency, constancy and, dominancy of these species within the lower-base community. Both E. crispa and I. alopecuroides had the highest IES value on the lower bases of all tree-size groups (young, middle-aged and old boxwood trees) (Tab. 3). The community was represented with 19 moss species in a total of 20 sample plots. Moderately abundant R. complanata was the only liverwort in the lower-base community. Exsertotheca crispa-Isothecium alopecuroides community was co-dominated by H. trichomanoides. In this community, P. attenuatus and S. flotowianumwere also abundant. While the dominant life forms within the community were weft and mat (31.5%), cortico-saxicolous species (47.3%) were dominant and indifferent type affinity was also co-dominant (42.1%).
The B1 community was named Alleniella complanata-Exsertotheca crispa according to its dominant and co-dominant species. It was represented by 19 species (15 mosses, 4 liverworts) in a total of 17 sample plots from the middle parts of the young, middle-aged and old boxwood trees. The liverwort R. complanata was still present in the middle parts of the trunks with relatively high IES values. Also, P. euchloron was abundant in the community B1 on the middle zones, particularly of young and middle-aged trees particularly (Tab. 3). While mats were the most dominant with the rate of 42.1% within the middle parts of community B1, cortico-saxicolous species were the most common with 63.1%.
The B2 community was named Alleniella besseri-Leucodon sciuroidesaccording to its co-dominant species. This community, consisting of 17 species (13 mosses and four liverworts), was found on the upper zones of boxwood trees. The community B2 was represented by a total of 23 sample plots. Orthotrichum pumilum, R. complanata, and U. crispa were abundant species in the upper zones community. While mats were the most dominant with the rate of 41.1% within the middle parts of community B2, the cortico-saxicolous type habitat affinity was the most common with 70.5%.
DECORANA ordination
DECORANA grouped the sample plots on axis 1 and axis 2 according to the similarity and the environmental gradients (Fig. 3). While the DCA axis 1 was interpreted as gradient along the height of the epiphytic habitat (from the lower base to the upper zone) on trunks, the DCA axis 2 was interpreted as gradient of moisture (from mesic to xeric) (Fig. 3).
Discussion
When the epiphytic habitats on the boxwood trees in the Fırtına Valley were examined in terms of species diversity and species composition, the lower bases and the middle-parts were the richest zones with equal numbers of species (19 species), while the upper zones contain 17 epiphytic species.Large pleurocarp mosses such as E. crispa, H. trichomanoides, and I. alopecuroides were common on the basal parts of the trunks of B. sempervirens. These strong competitor members of pleurocarpous type mosses are more sensitive to drought, have a faster growth habit than acrocarpous mosses and spread horizontally in a carpet-like appearance on the substratum (Schofield 2001,Ezer 2017). The basal parts of the trunks are usually more humid and more nutrient rich than the other parts (middle and upper) due to soil proximity. Therefore, basal zones allow early establishment and rapid colonization of bryophytes due to higher water retention capacity, higher soil humidity, low evapotranspiration rate and low insolation (Lara and Mazimpaka 1998,Mazimpaka et al. 2009,Ezer and Kara 2013,Ezer 2017). In this respect, the lower base parts of the trees can be considered an extension of the forest floor (groundlayer) environment. For this reason, species such as B. rutabulum, C. molluscum, O. hians, P. nemorale,P. nervosa, S. populeum, T. alpecurum, Thuidium delicatulum, and F. serrulatus, which usually grows on the soil, were encountered only in this part. This caused the weft life form and indifferent type habitat affinity to co-dominate with the mats and cortico-saxicolous species were the strong competitor of robust pleurocarpous in basal parts of boxwood trees.
Alleniella besseri, A. complanata and E. crispa were most dominant on the middle zones of the boxwood trees. Also, the mesophytic species P. euchloron, which was not present in the base zone, was abundant in the middle zone. Therefore, P. euchloron can be considered a characteristic and distinctive species of the communities in the middle zones. The customary epiphyte xerophytic species O. pumilum, which in the present study was generally abundant in the upper zones, in the present study was found for the first time only in the middle zones of old trees. As the middle and upper parts of the trunks move away from the soil effect, they are periodically exposed to higher insolation and desiccation that makes colonization of species on epiphytic habitats difficult (Moe and Botnen 2000). Therefore, as in the present study, small cushion-type mosses which have xerophytic characters such as Orthotrichaceae members and photophilous or heliophilous species such as A. besseri, A. complanata, and L. sciuroides are most common species within the middle and upper zone communities. Mat type life forms were predominant in the middle parts of old trees, due to the presence of cortico-saxicolous liverworts.
Although mesoscale climatic factors such as seasonal climatic variables are among the most important determinants of bryophyte species richness and species diversity, forest structure and habitat characteristics are also important for community compositions and spatial distributions of epiphytic bryophytes on epiphytic habitats (Medina et al. 2014,Ezer 2017). Species diversity and epiphytic cover on the upper zones were found to be lower than in the base and middle zones. The xerophytic robust pleurocarpic species L. sciuroides was dominant on the upper parts of all tree-size groups. Besides A. besseri, A. complanata and E. crispa there were other dominant pleurocarpic species in the upper zones of boxwood trees in the Fırtına Valley. Therefore, weak competitor species such as liverworts Frullania dilatata and Metzgeria furcata and small cushion-type mosses (such as O. pumilum and U. crispa) remain under these large pleurocarpous species and decreased or disappeared from the epiphytic habitats in the valley.
Some studies on the succession of epiphytic bryophyte communities have demonstrated that variables of the epiphytic bryophyte composition in the successional stages are closely related to tree age, trunk height (basal, middle and upper zones) and bark characteristics (Lara and Mazimpaka 1998,Mazimpaka et al. 2010,Ódor et al 2013,Bargali et al. 2014,Ezer 2017). However, in the present study, trunk height rather than tree age and bark characteristics were effective in the variability of epiphytic bryophyte composition in the per successional stage. Hygrophytic pleurocarpous species that usually grow on soil, such as B. rutabulum, C. molluscum, F. serrulatus, O. hians, P. nemorale P. nervosa, S. populeum, T. alpecurum, and T. delicatulum were particularly the pioneer colonizers in the early successional stages on the basal parts particularly of middle aged B. sempervirens. While the xerophytic small cushions O. pumilum and U. crispa were the pioneer colonizers in the early successional stages, the large pleurocarpous L. sciuroides was a secondary colonizer in the advanced stages on the upper parts of all tree-size groups. In addition, cortico-saxicolous species P. euchloron, a characteristic and distinctive species on the middle zones, was pioneer colonizer in the early successional stages on the middle parts of all tree-size groups. In this study, A. besseri, A. complanata, and E. crispa were other colonizers in the advanced successional stages on the middle zones. Considering the morphological physiognomy of the bryophyte communities on trunks of B. sempervirens in the Fırtına Valley; all communities were dominated by large pleurocarpous mosses. E. crispa was in particular the most constant and the most dominant within all communities in the B. sempervirens forests. In sum, the succession of the epiphytic bryophyte communities of the boxwood forests in the Fırtına Valley has reached the climax.