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Article

Diversity, Ecology and Phytogeography of Bryophytes across Temperate Forest Communities—Insight from Mt. Papuk (Croatia, SE Europe)

by
Antun Alegro
1,
Vedran Šegota
1,*,
Anja Rimac
1 and
Beáta Papp
2
1
Division of Botany, Department of Biology, Faculty of Science, University of Zagreb, Marulićev trg 20/II, 10000 Zagreb, Croatia
2
Botanical Department, Hungarian Natural History Museum, Pf 222, H-1476 Budapest, Hungary
*
Author to whom correspondence should be addressed.
Plants 2023, 12(19), 3346; https://doi.org/10.3390/plants12193346
Submission received: 6 August 2023 / Revised: 11 September 2023 / Accepted: 19 September 2023 / Published: 22 September 2023
(This article belongs to the Section Plant Ecology)
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Abstract

:
It has been widely documented that the complex structure of forest ecosystems supports considerable bryophyte species and functional diversity. In this study, we assessed the diversity, distribution and ecological and phytogeographical features of bryophytes across a gradient of temperate forest types on Mt. Papuk. This is the largest and highest mountain in the lowland, Pannonian part of Croatia, with high geological diversity and various temperate forests covering 95% of the mountain. According to the predominant tree species (oak vs. beech), geological bedrock (calcareous vs. siliceous) and soil reaction (alkaline vs. acidic), 21 study plots were classified into four distinct forest types. In all, 184 bryophyte species (35 liverworts and 149 mosses) were recorded. Although the forest types investigated did not differ significantly with respect to species richness, each was characterized by a considerable number of diagnostic bryophyte species. According to our results, one of the main ecological factors determining the variability of the forest bryophyte composition was geological bedrock and the associated soil reaction. Basiphilous forests developed on carbonate bedrock harbored more thermophilous and nitrophilous bryophytes and were characterized by southern-temperate and Mediterranean–Atlantic biogeographic elements. In contrast, acidophilous forests growing on silicate bedrock were characterized by wide-boreal and boreo-arctic–montane elements, i.e., bryophytes indicating cooler habitats and nitrogen-deficient soils. Based on the results, we hypothesized that the main latitudinal biogeographic distinction between southern and northern biogeographic elements is driven more by geological substrate than by the main tree species in forest communities. The present study confirmed previous findings that bryophytes are good and specific habitat indicators and show associations with different forest types, which can help to understand the complexity, ecological microconditions and biogeographic characteristics of forest communities.

1. Introduction

Bryophytes are a significant component in forest ecosystems, which, due to their complex structure, provide many different substrates and niches supporting considerable bryophyte species richness and functional diversity [1,2,3,4,5,6]. Bryophytes serve several important functions in the forest ecosystem. They are colonists of bare soil and they are capable of absorbing moisture quickly, retaining it and releasing it slowly, acting as a water reservoir [7]. In temperate forests, their water storage capacity prevents the rainwater run-off and ensures that nutrients from the rainwater are fed into the ecosystem [8]. Furthermore, the bryophytes contribute significantly to the overall energy flow and nutrient cycling in the woodland environment [7]. For example, mosses represent 49% of the annual phytomass production, and they contribute 75% to the phosphorus supply of the forest ecosystem [8]. However, they provide a habitat for a huge number of invertebrates, fungi and other microorganisms [7]. Furthermore, mosses that form mat-like colonies help to prevent soil erosion, and they create seed beds influencing tree growth by either enhancing or prohibiting seedling survival [9,10].
The bryophyte species composition and richness in forest ecosystems are primarily driven by macroclimatic factors such as air temperature and precipitation [11], longitudinal and altitudinal gradients [12,13], microrelief diversity [14] and forest integrity [15], as well as forest management and silviculture practices [16,17,18,19]. On a smaller scale, the microclimatic conditions (shade, humidity), substrate availability and light conditions determined by forest structure significantly affect bryophyte diversity and cover [6,20,21,22,23,24]. In addition, soil properties, especially soil reaction, also affect forest floor bryophyte assemblages and their diversity [25,26,27,28]. Finally, anthropogenic impacts such as habitat disturbance caused by logging can have a considerable influence on forest bryophyte diversity [29,30].
In temperate and boreal forests, vascular plants and forest floor bryophytes are major components of understory vegetation [31]. Both groups are often considered equally important components of plant communities and are thus both included in the vegetation relevés and used as diagnostic species of the same community types [32]. According to several authors [33,34,35], bryophyte composition is significantly correlated to different environmental conditions, making bryophytes reliable indicators of forest condition and naturalness [19,36]. Ewald [31,37] showed that bryophyte composition in mountain forests is significantly correlated to environmental conditions, but less so than vascular plants. Although Diekmann [33] assumed that this limited indication potential of bryophytes is a consequence of their low species numbers in deciduous forests, Ewald [31] showed that the higher indication potential of vascular plants is not principally due to their higher species diversity but can be attributed to a more pronounced response of vascular plants to ecological gradients. Furthermore, he concluded that forest floor bryophytes do not contribute substantially to bioindication in terms of Ellenberg’s indicator values in mountain forests.
Nevertheless, plenty of studies have shown that bryophytes have high indication potential. They can be considered as good indicators of environmental conditions in natural forest communities [38] and promising indicators of forest integrity [15]. The richness and composition of bryophytes have a high indication value for conservation strategies of set-aside forests [39] and bryophyte community composition is known to indicate fragmentation in temperate rainforests [40]. It was shown on a large data set that, in Central Europe (Poland), bryophytes are good indicators of habitat conditions and show associations with different types of forests [41]. Similar patterns were obtained for Slovenian forests; it was demonstrated that, in close-to-nature managed forests, bryophyte species composition varied considerably among five forest types of different tree layer composition (broadleaved vs. conifers) and bedrock and soil type (calcareous vs. siliceous) [42]. Similarly, bryophyte species richness and species composition in Alpine forests were best explained by substrate and forest type [4]. In addition, it was elaborated that tree species composition (deciduous vs. coniferous) determines bryophyte species richness and cover and that soils with lower pH and macronutrient content support larger bryophyte cover [43]. However, it was demonstrated that the stand structure of temperate deciduous forests was more influential on forest floor bryophyte diversity than soil characteristics [44].
However, to date, there has been no research on bryophyte diversity nor their ecological and phytogeographical features across forest communities in Croatia. Moreover, Croatia is bryologically still quite underexplored. Therefore, the aim of this work was to obtain a detailed insight into the diversity of the bryophyte flora of Mt. Papuk. Since this area harbors considerable geological and vegetational diversity, we further wanted to explore the phytogeographical, coenological and ecological structure of bryophyte flora in relation to different temperate forest communities in order to assess the indication potential of forest bryophytes.

2. Results

In all, 184 bryophyte species—35 liverworts and 149 mosses—were recorded within the forest communities studied (Table A1 and Table S1). The most frequent species across the sampling plots was Hypnum cupressiforme (81%), followed by Polytrichum formosum (52%), Isothecium alopecuroides (48%), Dicranella heteromalla (48%), Brachythecium rutabulum (48%), Plagiochila porelloides (48%) and Metzgeria furcata (43%). Nevertheless, as many as 74 species appeared on only one sampling plot. Noteworthily, several species recorded, such as Microlejeunea ulicina, Rhabdoweisia fugax, Sciuro-hypnum flotowianum, Dicranum spurium and Syntrichia calcicola, are known in Croatia only from Mt. Papuk. Furthermore, species listed in Annex V of the Habitats Directive [45], Leucobryum glaucum and Sphagnum quinquefarium, were recorded as well, with the population of S. quinquefarium from Papuk being the largest known in Croatia.
Diagnostic species (Table A1) for acidophilous beech forests (FA) were Isothecium alopecuroides, Plagiochila porelloides, Metzgeria furcata, Rhizomnium punctatum and Lophocolea heterophylla and diagnostic species for basiphilous beech forests (FB) were Mnium stellare, Plagiomnium rostratum, P. undulatum, Brachythecium tommasinii, Conocephalum salebrosum and Homalothecium philippeanum. Diagnostic species for acidophilous oak forests (QA) were Polytrichum piliferum and Ceratodon purpureus, while the basiphilous oak forests (QB) had a larger set of diagnostic species comprising Leucodon sciuroides, Barbula unguiculata, Tortula muralis, Encalypta streptocarpa, Homalothecium lutescens, H. sericeum, Didymodon acutus, Grimmia pulvinata, Tortella tortuosa and Flexitrichum flexicaule.
Although the distinction between forest types based on bryophyte diversity (species richness, Shannon diversity index and Margalef’s richness index) was not supported by the Kruskal–Wallis test, or by the Mann–Whitney pairwise test (Table S2), the beech forests exhibited higher diversity indices than oak forests (Figure 1). However, considering the species number, the richest site, with 51 species, was within an acidophilous oak forest, followed by two sites in acidophilous beech forests (50 species each) and by one site in a basiphilous beech forest (48 species) (Table S1). It was the complex structure of microhabitats observed in these sites (rocks, rock crevices and peat deposits) that ensured such a high number of species.
Ellenberg’s indicator values of bryophyte flora (EIVs) and measured pH (Figure 2) values showed clear differences between the studied forest types, which were supported by the Kruskal–Wallis test (p < 0.05 in all cases). The subsequent Mann–Whitney pairwise test revealed the differences between particular forest types (Table S2). Both groups of oak forests (QA and QB) were characterized by higher light values (L), i.e., by more heliophytic bryophyte flora, and by lower moisture values (F) indicating drier habitats, with QB being the driest and significantly different from all other types. Semi-shade species of moderately moist to moist soils were specific for beech forests, while species of well-lit places (occurring also in partial shade) and well-drained soils were characteristic for oak forests. Both basiphilous forest types (FB and QB) had significantly higher pH values than beech forests, which were supported by higher bryophyte EIVs for soil reaction (R). Furthermore, oak forests showed higher bryophyte EIVs for temperature (T) and nutrient content (N).
All these tendencies were furthermore corroborated by DCA analysis (Figure 3A). Furthermore, acidophilous beech forests (FA) were grouped mainly along the moisture vector (F), while basiphilous oak forests (QB) were the most distant from other forest types and grouped in the directions of vectors for temperature (T), soil reaction (R), nutrients (N) and light (L). Additionally, acidophilous oak forests (QA) were separated from the acidophilous beech forests (FA) along the light vector.
The DCA graph representing the relationship between sampling plots and the bryophyte major biome elements (Figure 3B) indicates that basiphilous and acidophilous forests were biogeographically clearly distinguished. The basiphilous ones were characterized by different temperate elements, as well as Mediterranean–Atlantic bryophyte elements, whereas acidophilous forests were characterized by boreal bryophyte elements.
The bryophyte biogeographic spectrum regarding distribution throughout the major biomes (E1) (Figure 4) showed that the dominant element in all forest types was boreo-temperate, but with the highest ratio in acidophilous beech forests (51.8%). The share of boreo-arctic–montane and wide-boreal elements was the highest in acidophilous oak forests (7.7 and 21.3%, respectively). By contrast, the highest shares of southern-temperate (22.9%) and wide-temperate elements (18.4%) were in basiphilous oak forests, while the highest shares of temperate (35.7%) and Mediterranean–Atlantic species (7.5%) were characteristic of basiphilous beech forests. The Mediterranean–Atlantic element was absent in both acidophilous forest types, whereas the southern-temperate element was represented with only 0.8% in acidophilous beech forests. Generally, oak had more complex spectra of bryophyte biogeographical elements than beech forests.
In the DCA graph (Figure 3C) showing the relationship of the forest sampling plots and the bryophyte eastern limit (E2), basiphilous oak forests are shifted toward the vectors representing Eurosiberian and Eurasian elements, and basiphilous beech forests toward European and suboceanic elements. The latter element also characterized acidophilous beech forests, while acidophilous oak forests were shifted toward the vector representing a circumpolar element.
When the spectrum of the eastern limit category of bryophyte species distribution was considered (Figure 5), the circumpolar element was dominant in all forest types, with the highest share in acidophilous oak forests (79.1%). An exception was found in basiphilous beech forests, where the European element (48.9%) dominated. The Eurasian element was present exclusively in the oak forests (5.8% in QB and 4.1% in QA), while, in the beech forests, it was absent (FB) or marginally present (0.57% in FA). Bryophyte species of the suboceanic element were more frequent in beech (9.4% in FB and 7.6% in FA) than in oak forests (5.8% in QB and 3.3% in QA). Finally, the Eurosiberian element had by far the highest share in basiphilous oak forests (8.3%), but was present with less than 2% in all other forest types.
The correlation between the ecology and the biogeography of forest bryophytes was demonstrated by the Mantel test. Correlations between the matrix of bryophyte Ellenberg’s indicator values and both biogeographical matrices were high (r (E1) = 0.7 and r (E2) = 0.5) and statistically significant (p < 0.001). A positive association between matrices was also indicated by the randomization test.

3. Discussion

The results of this study show that bryophyte flora corresponds with forest vegetation both ecologically and biogeographically and that the interconnection between bryophytes and forest vegetation observed on a small scale in this study demonstrates the same patterns detected on mid- [4] and large national scales [41,42]. Noteworthily, the total number of recorded bryophyte species in our study (184 spp.) corresponds closely with the overall forest bryophyte diversity of similar Slovenian (199 spp.) [42] and Polish forests (173 spp.) [41].
Diagnostic bryophyte species could be defined for all studied forest types and their number ranged in our study from 2 to 10, which is in line with the number of diagnostic species for Central European forests, which ranged from 1 to 12 [41]. However, the φ-coefficient threshold was conservatively set much higher in our study (40% vs. 15%). The presence of valid diagnostic bryophyte species, as well as their quite high number in our study, corroborates previous findings on the relationship between bryophyte assemblages and forest communities [4,35,42,46,47,48]. By contrast, Stefańska-Krzaczek et al. [41] found a low number of diagnostic bryophyte species, suggesting their subordinate position compared to vascular plants in vegetation classification, as already noted by some authors [31,46]. However, many forest communities, especially those that are acidophilous, contain a low number of diagnostic vascular plant species and, in these cases, bryophytes can substantially contribute to the vegetation classification [49,50].
Although in our study the species richness did not differ significantly among investigated forest types, a pattern in which beech forests have both significantly higher bryophyte EIVs for moisture (F) and also higher diversity indices than oak forests was evident. This is consistent with the findings of Stefańska-Krzaczek et al. [41] that the moisture index is the most important predictor of the number of forest bryophyte species.
One of the main ecological factors determining the variability of the forest bryophyte flora is soil reaction [25,26,27,28]. According to our results, basiphilous forest communities, either beech or oak, include more thermophilous and nitrophilous bryophyte species, which can be explained by more aerated and therefore warmer soil due to a porous and fragmented carbonate or dolomite bedrock. Good aeration and non-acidic soil reaction enhance the mineralization of organic matter, which in turn makes these habitats suitable for colonization by more nitrophilous species. In terms of biogeography, these basiphilous forests were characterized by southern-temperate (Frullania dilatata, Didymodon acutus, D. fallax, Gymnostomum calcareum, Grimmia pulvinata, Homalothecium lutescens, H. sericeum, Trichostomum crispulum, Syntrichia calcicola, Tortula muralis) and Mediterranean–Atlantic biogeographic elements (Plasteurhynchium striatulum, Tortella squarrosa, Didymodon sinuosus, Rhynchostegiella teneriffae and Trichostomum brachydontium). However, acidophilous forest communities were characterized by wide-boreal (Jungermannia pumila, Dicranum scoparium, Hylocomium splendens, Polytrichum commune, P. juniperinum) and boreo-arctic–montane elements (Blepharostoma trichophyllum, Cynodontium polycarpon, Dichodontium pellucidum, Pogonatum urnigerum), i.e., bryophytes indicating cooler habitats and nitrogen-deficient soils. Acidic substrates are mostly siliceous, nonporous and less aerated. This implies a relatively cool soil in comparison to the carbonate and dolomite soils in the same region, and a slower mineralization of organic matter, not only due to the cooler conditions but, and primarily, because of the acidic soil reaction. This, therefore, may suggest that the main latitudinal biogeographic distinction between southern and northern biogeographic elements is driven by geological substrate and not by the main tree species in forest communities.
The distinction between longitudinal eastern and western biogeographic elements is observable in the oak–beech dichotomy. While the oak forests feature bryophyte flora with higher indicator values for light and lower values for moisture, the opposite is true for the beech forests. This may be explained by the density of forest stands and the relief of their habitats. Namely, in our study, which included zonal temperate forest, oak forest stands were, as expected, less dense than beech. This is partially a consequence of looser canopy closure and partially due to the relatively thin soil layer on often steep and inclined positions on which the oak stands investigated are developed [49]. For these reasons, water is a limiting factor, preventing the development of dense forest stands, which in turn drives the colonization of light-demanding bryophyte species of well-drained soils. The presence of Eurasian and Eurosiberian species (e.g., Brachythecium glareosum, Homomallium incurvatum, Homalothecium sericeum, Leucodon sciuroides) almost exclusively within the oak forests investigated reflects a continental, more “eastern” climate with a pronounced dry summer period and a high annual temperature amplitude. On the other hand, the European (e.g., Ctenidium molluscum, Plagiomnium rostratum, P. undullatum, Thamnobryum alopecurum) and suboceanic (Bazzania trilobata, Calypogeia fissa, Diplophyllum albicans, Atrichum angustatum, Heterocladium heteropterum, Pseudotaxiphyllum elegenas, etc.) species were the most abundant in the beech forests. Such a biogeographic spectrum makes the beech forests more “western” than the oak forests, indicating microclimatic conditions with more constant humidity and temperature.
The present study confirmed the previous findings that bryophytes are good and specific habitat indicators and that they show a clear association with different forest types [4,41,42,43], which is useful for the understanding of the complexity, ecological microconditions and biogeographic characteristics of the forest communities. It is important to note that non-vascular plants are rarely included in floristic and vegetation assessments since their importance as indicators of the plant communities is still not truly recognized [51]. Consequently, there has been little systematic study of their biogeography and community ecology [52]. Ewald [31], based on research into mountain forests in the Bavarian Alps, concluded that combining vascular plants and bryophytes yielded very similar or even slightly less stringent relationships with the environment than using vascular plants only. Moreover, he showed that bryophyte-based indicator values do not significantly predict the residuals of measured ecological variables against vascular-plant-based Ellenberg indicator values. On the other hand, Bagella [52], from a review of twenty-seven papers, concluded that vascular plants cannot be used as habitat indicator surrogates for bryophytes without carefully considering habitat type, environmental and human-induced factors and assessment scale. This conclusion is strongly supported by the fact that, in some cases, richness in two taxonomic groups is affected similarly by the same environmental factors, and differently by others. Several studies pointed out that the species richness of these groups responds similarly to precipitation [53] and moisture [54], but differently to pH, conductivity and water level dynamics [55].
The results of this study can improve forest conservation strategies and management plans. Ecological and biogeographical analysis of bryophyte flora has shown that acidophilic beech forests, especially moist ones, stand out with a high proportion of boreal and boreal–arctic–montane species, which are rare in Croatian flora due to its geographical position. Protection of their habitats is one of the priorities while preserving the peculiarities of bryophyte flora and generally the biodiversity in Croatia. In addition, some of these habitats are unique in Croatia, e.g., beech forests with dominating peat moss Sphagnum qiunquefarium (plot 18 in Table S1), which is also the only place in Croatia where Dicranum spurium and some other rare bryophytes are found. It is worth noting that some of them (e.g., Bazzania trilobata, Calypogeia fissa, Diplophyllum albicans, Pseudotaxiphyllum elegans) belong to the rare subocanic element. Such forest habitats with permanent soil moisture enabling the survival of northern and oceanic elements should be exempted from any timbering and coppicing. Moreover, they are the most threatened by climate change due to their wetter and mostly cooler microclimate in comparison to the general climate of the area. The analyses of climatic data have shown that changes in the temperature and precipitation regime have already begun in Croatia [56]. In eastern Croatia, where the study area is situated, a considerable increase in the temperature of the coldest and the warmest months is expected, as well as a decrease in the precipitation in the driest and the wettest months [56]. On the other hand, oak forests harbor a high proportion of thermophilous and light-demanding species belonging to the temperate and southern temperate elements. These forests often form a mosaic landscape with former extensive dry pastures. Abandonment of these pastures and their encroachment into thickets also affect the forests due to the spread of the successional species into the forests, which could change forest structure, light conditions and microclimate. Therefore, to preserve these forests in the mosaic landscape and their specific biodiversity, it is necessary to prevent the succession of grasslands. These oak forests are, according to the models, also susceptible to climate change, which can alter their spatial distribution and cause their possible disappearance and substitution with other forest types [56].
The use of bryophytes as indicators is strongly supported by our results, as they broaden the understanding of the complexity, biogeography and environmental conditions of plant communities.
Our research was restricted to only one mountain in the Peripannonian area. Future research, including the broader area and neighboring mountains, will give a more complete insight into the diversity and ecology of forest bryophytes in that unique area that connects two biogeographical regions, Pannonian and Dinaric.

4. Materials and Methods

4.1. Study Area

The field survey of the forest bryophytes was conducted on Mt. Papuk, which is situated in the eastern part of Croatia, on the southern border of the large Pannonian plain, within the Peripannonian biogeographic region characterized by a wetter climate than that of the Pannonian region (Figure 6). In this region, Papuk is the largest and highest mountain; the peaks reach between 800 and 953 m a.s.l. Unlike the majority of Croatian mountains, which are built of Mesozoic limestone, Papuk has a high geological diversity dominated by metamorphic rocks, granites and different types of schists. The climate is temperate but moderately warm without an explicit dry period. Depending on the elevation, the annual mean temperature is between 8 and 11 °C and annual precipitation varies between 800 and 1300 mm. Ninety-five per cent of the area is covered with beech forests with dominant acidophilous beech communities of the suballiance Luzulo luzuloidis-Fagenion (Lohm. et Tx. 1954) Oberd. 1957 and the beech–fir community (ass. Festuco drymeiae-Abietetum Vukelić et Baričević 2007). The basiphilous beach forests are less frequent, belonging to ass. Vicio oroboidi-Fagetum sylvaticae (Horvat 1938) Pocs et Borhidi in Borhidi 1960 and developed above patches of carbonate and dolomite rocks. Similarly, oak forests are also either acidophilous (several communities from the alliance Quercion robori-petraeae Br.-Bl. 1932) or basiphilous (Quercion pubescenti petraeae Br.-Bl. 1932) [49,57]. Mt. Papuk, with an area of 33,600 ha, has been protected as a Nature Park since 1999, and recently as a NATURA 2000 site [58].

4.2. Methods

Forest bryophytes were collected during a four-year period (2009–2013) from the forest floor, rocks and stones, living wood (bark of living trees) and deadwood (stumps, lying logs and standing dead trees). In total, 22 sampling plots (each 200 m2) were selected so that the four main forest communities present on Papuk (Figure 7 and Table A2) were represented in proportion to their frequency within the area. These types, defined by the main tree species, soil reaction and bedrock type (calcareous vs. siliceous), are:
  • FA—acidophilous beech forests (suballiance Luzulo luzuloidis-Fagenion (Lohm. et Tx. 1954) Oberd. 1957 and ass. Festuco drymeiae-Abietetum Vukelić et Baričević 2007);
  • FB—basiphilous beech forests (ass. Vicio oroboidi-Fagetum sylvaticae (Horvat 1938) Pocs et Borhidi in Borhidi 1960 from the suballiance Epimedio-fagenion (Borhidi 1963) Martinček et al. 1993);
  • QA—acidophilous oak forests (ass. Festuco drymeiae-Quercetum petrae (Janković 1968) Hruška-Dell’Uomo 1975, ass. Molinio arundinaceae-Quercetum petraeae Šugar 1972 and Quercus petraea-Calluna vulgaris community, all three belonging to the alliance Quercion robori-petraeae Tx. (1931) 1937);
  • QB—basiphilous oak forests (Lathyro nigri-Quercetum petraeae Horvat (1938) 1958, Fraxino orni-Quercetum pubescentis Klika 1938, both from the alliance Quercion pubescenti-petraeae Br.-Bl. 1932).
On each sampling plot, the geological bedrock was documented and a composite soil sample was collected for soil reaction (pH) measurement in suspension with distilled water according to a standard protocol [59].
The bryophyte specimens are deposited in the Herbarium of the Botanical Department of the Faculty of Science in Zagreb (ZA) and the Herbarium of the Hungarian Natural History Museum in Budapest (BP). Nomenclature of the bryophyte taxa follows Hodgetts et al. [60].
In the statistical analyses, bryophyte species recorded on different substrates in each plot were analyzed together.
The forest types were analyzed with the respect to species composition. For each species within a particular forest type, frequency (f) was calculated, as was the fidelity (φ) coefficient, tested for significance with the Fisher test (Table A1), using Juice 7.1 [61]. These were used to define diagnostic species (f ≥ 50%; φ ≥ 40%, p < 0.05).
Ellenberg’s indicator values (EIV) for light (L), moisture (F), reaction (R), nitrogen (N) and temperature (T) were used in the ecological analysis [62], while chorological analysis followed the system proposed by Hill and Preston [63], which was elaborated in Hill et al. [64] and recently summarized by van Zuijlen et al. [62]. Both biogeographic elements, reflecting the major biomes (E1) and the eastern limit in Eurasia (E2), were used. Spectra of EIVs and biogeographic elements were calculated for each sampling site and for each group of forest communities (FA, FB, QA and QB).
Bryophyte alpha diversity indices (species richness, Shannon diversity index and Margalef’s richness index) of different forest types were calculated in Past 4.12 software [65]. Furthermore, the Kruskal–Wallis test for equal medians followed by the pairwise Mann–Whitney test were performed using the same software to compare alpha diversity indices, bryophyte EIVs and measured pH among the forest types.
EIVs, pH values and alpha diversity indices were visualized through boxplot graphs in SPSS 22.0 software.
Community structure was assessed using the indirect ordination method, detrended correspondence analysis (DCA). In DCA, EIVs and both biogeographical elements (E1 and E2) were passively projected over ordination of plots to assess possible environmental and biogeographical gradients. DCA revealed that the data were compositional with a gradient longer than 3.0 SD units, confirming that analysis based on a unimodal model, such as DCA, was suitable for describing the data [66]. The procedure was performed in CANOCO 5.0 [66,67].
The Mantel test, a permutation test for correlation between two distance or similarity matrices, was used to test the possible relationship between ecology (described by EIVs) and biogeography (biogeographical elements E1 and E2). The analysis was performed using the Sorensen distance measure and 999 randomized runs. The calculated R value is the Pearson correlation coefficient among all the entries in the two matrices and it was retained as significant if p < 0.001. The test was performed in PcOrd 7.0 [68].

5. Conclusions

The present study confirmed previous findings that bryophytes are good, specific habitat indicators, and show associations with different forest types. We defined diagnostic species for each forest type based on frequency and fidelity index and their number varied from two in the acidophilous oak forests to 10 in basiphilous beech forests. Two main ecological and biogeographical gradients were recognized—latitudinal and longitudinal. The main latitudinal biogeographic distinction between southern and northern biogeographic elements is driven largely by geological substrate rather than by the main tree species in forest communities. Basiphilous forests developed on carbonate bedrock harbored more thermophilous and nitrophilous bryophytes and were characterized by southern-temperate and Mediterranean–Atlantic biogeographic elements. By contrast, acidophilous forests developed on silicate bedrock were characterized by wide-boreal and boreo-arctic–montane elements, i.e. bryophytes indicating cooler habitats and nitrogen-deficient soils. Furthermore, the latitudinal distinction between eastern and western biogeographical elements was observed in the oak–beech dichotomy. While the oak forests featured bryophytes with higher indicator values for light and lower values for moisture, the opposite was true for beech forests. The presence of Eurasian and Eurosiberian species was almost exclusively limited to oak forests. On the other hand, the European and suboceanic species were the most abundant in beech forests. The findings of this study can have direct applications in conservation and forest management, suggesting a strong need for the controlled exploitation of beech stands with permanent soil moisture, as well as a need for the suppression of vegetation succession in dry pastures, which are mosaically intermixed with some oak forests.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/plants12193346/s1, Table S1: List of species recorded at investigated localities; Table S2: Results of the Kruskal–Wallis test for equal medians and pairwise Mann–Whitney; for investigated forest types for alpha diversity indices, Ellenberg’s indicator values and measured pH.

Author Contributions

Conceptualization, methodology, resources, funding acquisition, data analysis, writing—original draft preparation, A.A.; data collection and sampling, A.A., V.Š. and B.P.; identification of the plant material, A.A., A.R. and B.P.; validation and project administration, V.Š.; writing—review and editing, V.Š. and A.R.; visualization, A.A. and A.R. All authors have read and agreed to the published version of the manuscript.

Funding

This research was partially funded by Public Institution Papuk Nature Park.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We are grateful for the hospitality provided by Papuk Nature Park and for the kind help and logistic support in our fieldwork. We are deeply indebted to the EU Synthesys2 grant, which funded the first author’s research visit to the Hungarian Natural History Museum (project No. HU-TAF-1485) during which many specimens were identified or revised. Special thanks to Vlasta Ćosović for the identification of geological samples.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A. Synoptic Table with Percentage Frequency and Fidelity Index ϕ-Coefficients

Table A1. Diagnostic species (f ≥ 50.00; ϕ ≥ 40.00%) are marked in bold.
Table A1. Diagnostic species (f ≥ 50.00; ϕ ≥ 40.00%) are marked in bold.
Forest TypeFAFBQAQB
Number of Relevés11244
Hypnum cupressiforme Hedw.10044.7. 100 50
Polytrichum formosum Hedw.64 . 100 .
Isothecium alopecuroides (Lam. ex Dubois)7352.6. 25 25
Dicranella heteromalla (Hedw.) Schimp.64 . 75 .
Brachythecium rutabulum (Hedw.) Schimp.55 100 25 25
Plagiochila porelloides (Torr. ex Nees)7342.850 25 .
Metzgeria furcata (L.) Corda7364.9. 25 .
Dicranum scoparium Hedw.45 . 50 25
Hedwigia ciliata (Hedw.) P.Beauv.36 50 50 .
Pseudanomodon attenuatus (Hedw.) Ignatov45 50 25 .
Sciuro-hypnum populeum (Hedw.) Ignatov &45 50 25
Oxyrrhynchium hians (Hedw.) Loeske27 100 50
Alleniella complanata (Hedw.) S.Olsson,36 50 25 .
Rhizomnium punctatum (Hedw.) T.J.Kop.5568.8. .
Thamnobryum alopecurum (Hedw.) Gangulee36 100 .
Ctenidium molluscum (Hedw.) Mitt.27 100 25
Plagiothecium cavifolium (Brid.) Z.Iwats45 . 25 .
Lophocolea heterophylla (Schrad.) Dumort4562. .
Anomodon viticulosus (Hedw.) Hook. & Tay27 50 25
Pseudotaxiphyllum elegans (Brid.) Z.Iwat36 . 25 .
Frullania dilatata (L.) Dumort.27 . 50 .
Radula complanata (L.) Dumort.36 . 25 .
Atrichum undulatum (Hedw.) P.Beauv.27 . 50 .
Polytrichum piliferum Hedw.9 . 10094.3.
Atrichum angustatum (Brid.) Bruch & Schi27 . 25 .
Plagiomnium cuspidatum (Hedw.) T.J.Kop.36 . .
Metzgeria conjugata Lindb.27 . 25 .
Mnium stellare Hedw.18 10089.2 .
Plagiomnium rostratum (Schrad.) T.J.Kop.18 10089.2 .
Pogonatum urnigerum (Hedw.) P.Beauv.27 . 25 .
Frullania tamarisci (L.) Dumort.27 . 25 .
Eurhynchium angustirete (Broth.) T.J.Kop27 . 25 .
Thuidium delicatulum (Hedw.) Schimp.18 . 50
Brachytheciastrum velutinum (Hedw.) Igna36 . .
Diplophyllum albicans (L.) Dumort.27 50 .
Plagiomnium undulatum (Hedw.) T.J.Kop.18 10089.2 .
Brachythecium tommasinii (Sendtn. ex Bou)9 10081.325 .
Ptychostomum capillare (Hedw.) Holyoak &9 50 25 25
Didymodon fallax (Hedw.) R.H.Zander. 50 25 50
Ceratodon purpureus (Hedw.) Brid.. . 7566.725
Leucodon sciuroides (Hedw.) Schwägr.. . 25 7566.7
Hylocomium splendens (Hedw.) Schimp.27 . .
Pogonatum aloides (Hedw.) P.Beauv.27 . .
Solenostoma gracillimum (Sm.) R.M.Schust18 . 25 .
Plagiothecium nemorale (Mitt.) A.Jaeger27 . .
Pseudotaxiphyllum elegans (Brid.) Z.Iwat18 . 25 .
Pleurozium schreberi (Willd. ex Brid.) M18 . 25 .
Dicranum fulvum Hook.27 . .
Conocephalum salebrosum Szweyk., Buczk.9 10094.3 .
Pedinophyllum interruptum(Nees) Kaal.18 . 25 .
Plagiomnium affine (Blandow ex Funck) T.9 50 25 .
Pterigynandrum filiforme Hedw.27 . . .
Paraleucobryum longifolium (Hedw.) Loesk18 . . 25
Scapania nemorea (L.) Grolle27 . . .
Leucobryum juniperoideum (Brid.) Müll.Ha9 . 50 .
Blepharostoma trichophyllum (L.) Dumort.18 . 25 .
Lepidozia reptans (L.) Dumort.18 . 25 .
Lophozia ventricosa (Dicks.) Dumort.18 . 25 .
Brachythecium salebrosum (Hoffm. ex F.We18 . . 25
Exsertotheca crispa (Hedw.) S.Olsson, En9 50 . 25
Homalothecium philippeanum (Spruce) Schi9 10094.3. .
Orthotrichum cupulatum Brid.9 . 25 25
Barbula unguiculata Hedw.. . . 7583.2
Tortula muralis Hedw.. . . 7583.2
Encalypta streptocarpa Hedw.. . . 7583.2
Diplophyllum obtusifolium (Hook.) Dumort18 . . .
Mnium marginatum (Dicks.) P.Beauv.18 . . .
Chiloscyphus polyanthos (L.) Corda18 . . .
Plagiochila asplenioides (L.) Dumort18 . . .
Dichodontium pellucidum (Hedw.) Schimp.18 . . .
Cirriphyllum crassinervium (Taylor) Loes18 . . .
Bartramia pomiformis Hedw.18 . . .
Pohlia nutans (Hedw.) Lindb.9 . 25 .
Dicranella varia (Hedw.) Schimp.9 . . 25
Antitrichia curtipendula (Hedw.) Brid.9 . 25 .
Plagiothecium denticulatum (Hedw.) Schim18 . . .
Calypogeia fissa (L.) Raddi18 . . .
Pellia neesiana (Gottsche) Limpr.9 50 . .
Solenostoma hyalinum (Lyell) Mitt.18 . . .
Cephaloziella divaricata (Sm.) Schiffn.9 . 25 .
Homalia trichomanioides (Hedw.) Brid.18 . . .
Mnium hornum Hedw.18 . . .
Heterocladium heteropterum (Brid.) Schim18 . . .
Polytrichastrum alpinum (Hedw.) G.L.Sm.9 . 25 .
Conocephalum conicum (L.) Dumort.18 . . .
Polytrichum juniperinum Hedw.9 . 25 .
Hylocomiadelphus triquetrus (Hedw.) Ochy9 . . 25
Fissidens dubius P.Beauv.9 . . 25
Dicranoweisia cirrata (Hedw.) Lindb.9 . 25 .
Orthotrichum anomalum Hedw.9 . 25 .
Syzygiella autumnalis (DC.) K.Feldberg,9 . 25 .
Grimmia trichophylla Grev.9 . 25 .
Pseudoleskeella catenulata (Brid. ex Sch9 . 25 .
Lewinskya striata (Hedw.) F.Lara, Garill9 . 25 .
Rhabdoweisia fugax (Hedw.) Bruch. & Schi9 . 25 .
Platygyrium repens (Brid.) Schimp.9 . 25 .
Orthotrichum stramineum Hornsch. ex Brid9 . 25 .
Lewinskya speciosa (Nees) F.Lara, Garill9 . 25 .
Cynodontium polycarpon (Hedw.) Schimp.9 . 25 .
Schistidium crassipilum H.H.Blom9 . . 25
Cephalozia bicuspidata (L.) Dumort.. 50 25 .
Fissidens taxifolius Hedw.. 50 . 25
Thuidium recognitum (Hedw.) Lindb.. . 25 25
Didymodon rigidulus Hedw.. . 25 25
Hypnum cupressiforme var. lacunosum Brid.. . 25 25
Homalothecium lutescens (Hedw.) H.Rob.. . . 5065.5
Didymodon acutus (Brid.) K.Saito. . . 5065.5
Homalothecium sericeum (Hedw.) Schimp.. . . 5065.5
Grimmia pulvinata (Hedw.) Sm.. . . 5065.5
Tortella tortuosa (Hedw.) Limpr.. . . 5065.5
Flexitrichum flexicaule (Schwägr.) Ignat. . . 5065.5
Plagiothecium platyphyllum Mönk.9 . . .
Leskea polycarpa Hedw.9 . . .
Grimmia hartmanii Schimp.9 . . .
Porella arboris-vitae (With.) Grolle9 . . .
Dicranum spurium Hedw.9 . . .
Diphyscium foliosum (Hedw.) D.Mohr9 . . .
Leucobryum glaucum (Hedw.) Ĺngstr.9 . . .
Jungermannia pumila With.9 . . .
Polytrichum commune Hedw.9 . . .
Sphagnum quinquefarium (Braithw.) Warnst9 . . .
Porella platyphylla (L.) Pfeiff.9 . . .
Pseudoscleropodium purum (Hedw.) M.Fleis9 . . .
Dicranum polysetum Sw. ex anon.9 . . .
Bazzania trilobata (L.) Gray9 . . .
Porella baueri (Schiffn.) C.E.O.Jensen9 . . .
Lewinskya affinis (Schrad. ex Brid.) F.L9 . . .
Callicladium imponens (Hedw.) Hedenäs, S9 . . .
Ulota bruchii Hornsch. ex Brid.9 . . .
Campylopus pyriformis (Schultz) Brid.9 . . .
Plagiothecium succulentum (Wilson) Lindb9 . . .
Plagiothecium laetum Schimp.9 . . .
Microlejeunea ulicina (Taylor) Steph.9 . . .
Amblystegium serpens (Hedw.) Schimp.9 . . .
Tritomaria exsectiformis (Breidl.) Schif9 . . .
Isothecium myosuroides Brid.9 . . .
Sciuro-hipnum flotowianum (Sendtn.) Ignatov9 . . .
Sciuro-hypnum plumosum (Hedw.) Ignatov &9 . . .
Taxiphyllum wissgrillii (Garov.) Wijk &9 . . .
Pellia epiphylla (L.) Corda. 50 . .
Plasteurhynchium striatulum (Spruce) M.F. 50 . .
Rhynchostegiella teneriffae (Mont.) Dirk. 50 . .
Gymnostomum calcareum Nees & Hornsch.. 50 . .
Liochlaena lanceolata Nees. 50 . .
Conardia compacta (Drumm. ex Müll.Hal.) H. 50 . .
Seligeria pusilla (Hedw.) Bruch & Schimp. 50 . .
Plagiomnium ellipticum (Brid.) T.J.Kop.. 50 . .
Barbilophozia barbata (Schmidel ex Schre. . 25 .
Funaria hygrometrica Hedw.. . 25 .
Orthotrichum pallens Bruch ex Brid.. . 25 .
Amphidium mougeotii (Schimp.) Schimp.. . 25 .
Grimmia muehlenbeckii Schimp.. . 25 .
Ulota crispula Bruch. . 25 .
Abietinella abietina (Hedw.) M.Fleisch.. . . 25
Ptychostomum rubens (Mitt.) Holyoak & N. . . 25
Ptychostomum moravicum (Podp.) Ros & Maz. . . 25
Syntrichia montana Nees. . . 25
Trichostomum brachydontium Bruch. . . 25
Tortella inclinata (R.Hedw.) Limpr.. . . 25
Thuidium assimile (Mitt.) A.Jaeger. . . 25
Encalypta vulgaris Hedw.. . . 25
Didymodon vinealis (Brid.) R.H.Zander. . . 25
Tortula lindbergii Broth.. . . 25
Weisia longifolia Mitt.. . . 25
Homomallium incurvatum (Schrad. ex Brid.. . . 25
Bryum argenteum Hedw.. . . 25
Brachythecium glaerosum (Bruch ex Spruce. . . 25
Campyliadelphus chrysophyllus (Brid.) R.. . . 25
Bryum ruderale Crundw. & Nyholm. . . 25
Weisia controversa Hedw.. . . 25
Didymodon spadiceus (Mitt.) Limpr.. . . 25
Syntrichia ruralis (Hedw.) F.Weber & D.M. . . 25
Tortella fasciculata (Culm.) Culm.. . . 25
Syntrichia calcicola J.J.Amann. . . 25
Tortella squarrosa (Brid.) Limpr.. . . 25
Bryoerythrophyllum recurvirostrum (Hedw.). . . 25
Didymodon sinuosus (Mitt.) Delonge. . . 25
Pulvigera lyellii (Hook. & Taylor) Pláše. . . 25
Dicranella howei Renauld & Cardot. . . 25
Trichostomum crispulum Bruch. . . 25
Campylophyllopsis calcarea (Crundw. & Ny). . . 25
Streblotrichum convolutum (Hedw.) P.Beau. . . 25
Didymodon cordatus Jur.. . . 25
Weissia brachycarpa (Nees et Hornsch.) J. . . 25

Appendix B. Investigated Localities

Table A2. List of investigated localities and habitat characteristics.
Table A2. List of investigated localities and habitat characteristics.
LocalityCoordinates WGS84Habitat Characteristics
No.NameyxGeological BedrockForest TypeVegetationpH (H2O)pH (KCl)
1.Šimića put—Molišće45.4870417.64151quartziteQAFestuco drymeiae-Quercetum petrae4.053.46
2.Vrhovački mlin45.4632517.57752sandstone interlayed with algal limestoneQBFraxino orni-Quercetum pubescentis8.807.97
3.Vranovo45.4891717.56697phylliteFALuzulo luzuloidis-Fagenion5.323.95
4.Čarugin kamen45.5130617.53556migmatiteFALuzulo luzuloidis-Fagenion4.674.13
5.Točak (below peak)45.5758417.53478amphiboliteFALuzulo luzuloidis-Fagenion, with several Qurecus petrea trees4.303.94
6.Dva hrasta45.5667117.50290migmatiteFAFestuco drymeiae-Abietetum, with only scattered low Abies alba trees4.934.02
7.Rupnica45.6051317.53190albitic rhyoliteQBLathyro nigri-Quercetum petraeae6.545.91
8.Gudnoga45.5743517.63108graniteFALuzulo luzuloidis-Fagenion4.423.95
9.Kovačica brook, near Jankovac45.5314917.69876gneissFALuzulo luzuloidis-Fagenion5.365.07
10.Mala Rijeka45.4646717.86223phylliteFALuzulo luzuloidis-Fagenion4.173.82
11.Remetska Rijeka45.4746117.86411chlorite schistsFALuzulo luzuloidis-Fagenion4.683.79
12.Djedov nos45.4936917.86581dolomitic breccia-conglomeratesQBLathyro nigri-Quercetum petraeae7.787.40
13.Šaševa—Rastova kosa45.4953717.81560slate, quartziteQAQurecus petraea-Calluna vulgaris community3.893.13
14.Viljevačka kosa45.5100017.80319schistQAFestuco drymeiae-Quercetum petrae4.343.47
15.Pištanska kosa45.5134017.76675sand with grains of schits and phyllitesQAMolinio arundinaceae-Quercetum petraeae4.793.98
16.Jankovac, near brook spring45.5186717.68675limestone, tuffaFBVicio oroboidi-Fagetum sylvaticae8.488.01
17.Jankovac45.5230417.68300limestone, tuffaFBVicio oroboidi-Fagetum sylvaticae8.128.04
18.Svinjarevac45.5009817.52846quartzite, gneissFA 4.273.32
19.Radovanovačke Sokoline45.4772317.62205quartziteFALuzulo luzuloidis-Fagenion, with Quercus cerris and Q. petera3.933.49
20.Velika Pliš45.4695617.64227dolomitesQBLathyro nigri-Quercetum petraeae with patches of Fraxino orni-Quercetum pubescentis7.347.23
21.Velika Raduča, Crni virovi45.5300517.72536slate, quartziteFALuzulo luzuloidis-Fagenion4.704.13

References

  1. Steel, J.B.; Wilson, B.; Anderson, B.J.; Lodge, R.H.E.; Tangney, R.S. Are bryophyte communities different from higher-plant communities? Abundance relations. Oikos 2004, 104, 479–486. [Google Scholar] [CrossRef]
  2. Grytnes, J.A.; Heegaard, E.; Ihlan, P.G. Species richness of vascular plants, bryophytes and lichens along an altitudinal gradient in western Norway. Acta Oecol. 2006, 29, 241–246. [Google Scholar] [CrossRef]
  3. Hofmeister, J.; Hošek, J.; Brabec, M.; Dvořák, D.; Beran, M.; Deckerová, H.; Burel, J.; Kříž, M.; Borovička, J.; Běťák, J.; et al. Value of old forest attributes related to cryptogam species richness in temperate forests: A quantitative assessment. Ecol. Ind. 2015, 57, 497–504. [Google Scholar] [CrossRef]
  4. Spitale, D. Forest and substrate type drive bryophyte distribution in the Alps. J. Bryol. 2017, 39, 128–140. [Google Scholar] [CrossRef]
  5. Wierzcholska, S.; Dyderski, M.K.; Pielech, R.; Gazda, A.; Smoczyk, M.; Malicki, M.; Horodecki, P.; Kamczyc, J.; Skorupski, M.; Hachułka, M.; et al. Natural forest remnants as refugia for bryophyte diversity in a transformed mountain river valley landscape. Sci. Total Environ. 2018, 640, 954–964. [Google Scholar] [CrossRef]
  6. Müller, J.; Boch, S.; Prati, D.; Socher, S.A.; Pommer, U.; Hessenmöller, D.; Schall, P.; Schulze, E.D.; Fischer, M. Effects of forest management on bryophyte species richness in Central European forests. For. Ecol. Manag. 2019, 432, 850–859. [Google Scholar] [CrossRef]
  7. Porley, R.; Hodgetts, N. Mosses and Liverworts; Collins: London, UK, 2005. [Google Scholar]
  8. Frahm, J.-P. Biologie der Moose; Spectrum Akademischer Verlag: Heidelberg/Berlin, Germany, 2001. [Google Scholar]
  9. Saxena, D.K.; Harinder. Uses of bryophytes. Resonance 2004, 9, 56–65. [Google Scholar] [CrossRef]
  10. Glime, J. The role of bryophytes in temperate forest ecosystems. Hikobia 2001, 13, 267–289. [Google Scholar]
  11. Sun, S.; Wu, Y.; Wang, G.; Zhou, J.; Yu, D.; Bing, H.; Luo, J. Bryophyte species richness and composition along an altitudinal gradient in Gongga Mountain. China. PLoS ONE 2013, 8, e58131. [Google Scholar] [CrossRef]
  12. Sveinbjörnsson, B.; Oechel, W.C. Controls on growth and productivity of bryophytes: Environmental limitations under current and anticipated conditions. In Bryophytes and lichens in a Changing Environment; Bates, J.W., Farmer, A.M., Eds.; Clarendon Press: Oxford, UK, 1992; pp. 77–102. [Google Scholar]
  13. Heilmann-Clausen, J.; Ande, E.; van Dort, K.; Christensen, M.; Piltaver, A.; Veerkamp, M.; Walleyn, R.; Siller, I.; Standovár, T.; Ódor, P. Communities of wood-inhabiting bryophytes and fungi on dead beech logs in Europe—Reflecting substrate quality or shaped by climate and forest conditions? J. Biogeogr. 2014, 41, 2269–2282. [Google Scholar] [CrossRef]
  14. Bruun, H.H.; Moen, J.; Virtanen, R.; Grytnes, J.A.; Oksanen, L.; Angerbjörn, A. Effects of altitude and topography on species richness of vascular plants, bryophytes and lichens in alpine communities. J. Veg. Sci. 2006, 17, 37–46. [Google Scholar] [CrossRef]
  15. Frego, K.A. Bryophytes as potential indicators of forest integrity. For. Ecol. Manag. 2007, 242, 65–75. [Google Scholar] [CrossRef]
  16. Bengtsson, J.; Nilsson, S.G.; Franc, A.; Menozzi, P. Biodiversity, disturbances, ecosystem function and management of European forests. For. Ecol. Manag. 2000, 132, 39–50. [Google Scholar] [CrossRef]
  17. Paillet, Y.; Bergés, L.; Hjältén, J.; Ódor, P.; Avon, C.; Bernhardt-Römermann, M.; Bijlsma, R.J.; de Bruyn, L.; Fuhr, M.; Grandin, U.; et al. Biodiversity differences between managed and unmanaged forests: Meta-analysis of species richness in Europe. Conserv. Biol. 2010, 24, 101–112. [Google Scholar] [CrossRef]
  18. Kantvilas, G.; Jarman, S.J.; Minchin, P.R. Early impacts of disturbance on lichens, mosses and liverworts in Tasmania’s wet eucalypt production forests. Aust. Forestry 2015, 78, 92–107. [Google Scholar] [CrossRef]
  19. Czerepko, J.; Gawryś, R.; Szymczyk, R.; Pisarek, W.; Janek, M.; Haidt, A.; Kowalewska, A.; Piegdoń, A.; Stebel, A.; Kukwa, M.; et al. How sensitive are epiphytic and epixylic cryptogams as indicators of forest naturalness? Testing bryophyte and lichen predictive power in stands under different management regimes in the Białowieża forest. Ecol. Indic. 2021, 125, 107532. [Google Scholar] [CrossRef]
  20. Márialigeti, S.; Németh, B.; Tinya, F.; Ódor, P. The effects of standstructure on ground-floor bryophyte assemblages in temperate mixed forests. Biodivers. Conserv. 2009, 18, 2223–2241. [Google Scholar] [CrossRef]
  21. Tinya, F.; Márialigeti, S.; Király, I.; Németh, B.; Ódor, P. The effect of light conditions on herbs, bryophytes and seedlings of temperate mixed forests in Őrség, Western Hungary. Plant Ecol. 2009, 204, 69–81. [Google Scholar] [CrossRef]
  22. Tinya, F.; Kovács, B.; Bidló, A.; Dima, B.; Király, I.; Kutszegi, G.; Lakatos, F.; Mag, Z.; Márialigeti, S.; Nascimbene, J.; et al. Environmental drivers of forest biodiversity in temperate mixed forests—A multi-taxon approach. Sci. Total Environ. 2021, 795, 148720. [Google Scholar] [CrossRef]
  23. Király, I.; Ódor, P. The effect of stand structure and tree species composition on epiphytic bryophytes in mixed deciduous–coniferous forests of Western Hungary. Biol. Conserv. 2010, 143, 2063–2069. [Google Scholar] [CrossRef]
  24. Tinya, F.; Ódor, P. Congruence of the spatial pattern of light and understory vegetation in an old-growth, temperate mixed forest. For. Ecol. Manag. 2016, 381, 84–92. [Google Scholar] [CrossRef]
  25. Vitt, D.H.; Li, Y.; Belland, R. Patterns of bryophyte diversity in peatlands of continental western Canada. Bryologist 1995, 98, 218–227. [Google Scholar] [CrossRef]
  26. Martinez, M.L.; Maun, M.A. Responses of dune mosses to experimental burial by sand under natural and greenhouse conditions. Plant Ecol. 1999, 145, 209–219. [Google Scholar] [CrossRef]
  27. Zamfir, M.; Dai, X.; van der Maarel, E. Bryophytes, lichens and phanerogams in an alvar grassland: Relationships at different scales and contributions to plant community pattern. Ecography 1999, 22, 40–52. [Google Scholar] [CrossRef]
  28. Erfanzadeh, R. Impact of phanerogam and soil characteristics on bryophyte assemblages with respect to restoration practices (case study: IJzermonding, Belgium). Ecopersia 2013, 1, 41–51. [Google Scholar]
  29. Nelson, C.R.; Halpern, C.B. Short-term effects of timber harvest and forest edges on ground-layer mosses and liverworts. Can. J. Bot. 2005, 83, 610–620. [Google Scholar] [CrossRef]
  30. Caners, R.T.; Macdonald, S.E.; Belland, R.J. Linking the biological traits of boreal bryophytes to forest habitat change after partial harvesting. For. Ecol. Manag. 2013, 303, 184–194. [Google Scholar] [CrossRef]
  31. Ewald, J. Epigeic bryophytes do not improve bioindication by Ellenberg values in mountain forests. Basic Appl. Ecol. 2009, 10, 420–426. [Google Scholar] [CrossRef]
  32. Berg, C.; Dengler, J. Moose und Flechten als diagnostische Arten von Pflanzengesellschaften—Eine Übersicht aus Mecklenburg-Vorpommern. Herzogia 2005, 18, 145–161. [Google Scholar]
  33. Diekmann, M. Use and improvement of Ellenberg’s indicator values in deciduous forests of the Boreo-nemoral zone in Sweden. Ecography 1995, 18, 178–189. [Google Scholar] [CrossRef]
  34. Düll, R. Zeigwerte von Laub- und Lebermoosen. In Zeigwerte von Pflanzen in Mitteleuropa, 3rd ed.; Ellenberg, H., Weber, H.E., Düll, R., Wirth, V., Werner, W., Eds.; Scripta geobotanica 18; Verlag Erich Goltze KG: Göttigen, Germany, 2001; pp. 9–166. [Google Scholar]
  35. Dierßen, K. Distribution, Ecological Amplitude and Phytosociological Characterization of European Bryophytes; Bryophytorum Bibliotheca; J. Cramer: Berlin, Germany, 2001. [Google Scholar]
  36. Sabovljević, M.; Vujičić, M.; Sabovljević, A. Diversity of saproxylic bryophytes in old-growth and managed beech forests in the Central Balkans. Plant Biosyst. 2010, 144, 234–240. [Google Scholar] [CrossRef]
  37. Ewald, J. Comparing indicator values of bryophyte and vascular understorey plants in mountain forests. Mitteilungen Der Arbeitsgemeinschaft Geobot. Schleswig-Holst. Und Hambg. 2008, 65, 117–126. [Google Scholar]
  38. Gabriel, R.; Bates, J.W. Bryophyte community composition and habitat specificity in the natural forests of Terceira, Azores. Plant Ecol. 2005, 177, 125–144. [Google Scholar] [CrossRef]
  39. Perhans, K.; Gustafsson, L.; Jonsson, F.; Nordin, U.; Weibull, H. 2007—Bryophytes and lichens in different types of forests set-asides in boreal Sweden. For. Ecol. Manag. 2007, 242, 347–390. [Google Scholar] [CrossRef]
  40. Baldwin, L.K.; Bradfield, G.E. Bryophyte responses to fragmentation in temperate coastal rainforests: A functional group approach. Biol. Conserv. 2007, 136, 408–422. [Google Scholar] [CrossRef]
  41. Stefańska-Krzaczek, E.; Swacha, G.; Żarnowiec, J.; Raduła, M.W.; Kącki, Z.; Staniaszek-Kik, M. Central European forest floor bryophytes: Richness, species composition, coexistence and diagnostic significance across environmental gradients of forest habitats. Ecol. Indic. 2022, 139, 108954. [Google Scholar] [CrossRef]
  42. Kutnar, L.; Kermavnar, J.; Sabovljević, M.S. Bryophyte diversity, composition and functional traits in relation to bedrock and tree species composition in close-to-nature managed forests. Eur. J. For. Res. 2023, 142, 1–18. [Google Scholar] [CrossRef]
  43. Rola, K.; Plášek, V.; Rożek, K.; Zubek, S. Effect of tree species identity and related habitat parameters on understorey bryophytes—interrelationships between bryophyte, soil and tree factors in a 50-year-old experimental forest. Plant Soil 2021, 466, 613–630. [Google Scholar] [CrossRef]
  44. Ilić, M.; Igić, R.; Ćuk, M.; Veljić, M.; Radulović, S.; Orlović, S.; Vukov, D. Environmental drivers of ground-floor bryophytes diversity in temperate forests. Oecologia 2023, 202, 275–285. [Google Scholar] [CrossRef]
  45. EU Habitats Directive (Council Directive 92/43/ECC). 1992. Available online: https://environment.ec.europa.eu/topics/nature-and-biodiversity/habitats-directive_en (accessed on 5 September 2023).
  46. Hokkanen, P.J. Bryophyte communities in herb-rich forests in Koli, eastern Finland: Comparison of forest classifications based on bryophytes and vascular plants. Ann. Bot. Fenn. 2004, 41, 331–365. [Google Scholar]
  47. Wolski, G.J.; Kruk, A. Determination of plant communities based on bryophytes: The combined use of Kohonen artificial neural network and indicator species analysis. Ecol. Ind. 2020, 113, 106160. [Google Scholar] [CrossRef]
  48. Staniaszek-Kik, M.; Żarnowiec, J.; Stefańska-Krzaczek, E. Diversity and composition of moss guilds on uprooted trees in Central European mountain forests: Effects of uprooting components and environmental variables. Ann. For. Sci. 2021, 78, 45. [Google Scholar] [CrossRef]
  49. Vukelić, J. Šumska Vegetacija Hrvatske. Forest Vegetation in Croatia; Šumarski Fakultet Sveučilišta u Zagrebu, Državni Zavod za Zaštitu Prirode: Zagreb, Croatia, 2012. [Google Scholar]
  50. Ellenberg, H. Vegetation Mitteleuropas mit den Alpen, 5th ed.; E. Ulmer Verlag: Stuttgart, Germany, 1996. [Google Scholar]
  51. Rapson, G.L. At what scales and in what vegetation types should we sample nonvascular plants? In Vegetation Structure and Function at Multiple Spatial, Temporal and Conceptual Scales; Box, E., Ed.; Springer International Publishing: Cham, Switzerland, 2016; pp. 389–403. [Google Scholar]
  52. Bagella, S. Does cross-taxon analysis show similarity in diversity patterns between vascular plants and bryophytes? Some answers from a literature review. C. R. Biol. 2014, 337, 276–282. [Google Scholar] [CrossRef] [PubMed]
  53. Möls, T.; Vellak, K.; Vellak, A.; Ingerpuu, N. Global gradients in moss and vascular plant diversity. Biodivers. Conserv. 2013, 22, 1537–1551. [Google Scholar] [CrossRef]
  54. Dynesius, M.; Zinko, U. Species richness correlations omong primary producers in boreal forests. Divers. Distrib. 2006, 12, 703–713. [Google Scholar] [CrossRef]
  55. Hájková, P.; Hájek, M. Bryophyte and vascular plant responses to base-richness and water level gradients in Western Carpathian Sphagnum-rich mires. Folia Geobot. 2004, 39, 335–351. [Google Scholar] [CrossRef]
  56. Ugarković, D.; Tikvić, I.; Mikac, S.; Stankić, I.; Balta, D. The influence of changing climate extremes on the ecological niche of pedunculated oak in Croatia. South-East Eur. For. 2016, 7, 143–148. [Google Scholar] [CrossRef]
  57. Škvorc, Ž.; Franjić, J.; Krstonošić, D.; Sever, K.; Alešković, I. Vegetacijska obilježja bukovih šuma Psunja, Papuka i Krndije—Vegetation Fetures of Beech Forests of Psunj, Papuk and Krndija Mountains. Croat. J. For. Eng. 2011, 32, 157–176. [Google Scholar]
  58. Government of the Republic of Croatia. Uredba o ekološkoj mreži [Regulation on Ecological Network]. Off. Gaz. 2013, 124. [Google Scholar]
  59. Mühlenberg, M. Freilandökologie, 3rd ed.; Quelle & Meyer: Heidelberg-Wiesbaden, Germany, 1993; pp. 45–47. [Google Scholar]
  60. Hodgetts, N.G.; Söderström, L.; Blockeel, L.; Caspari, S.; Ignatov, M.S.; Konstantinova, N.A.; Lockhart, N.; Papp, B.; Schröck, C.; Sim-Sim, M.; et al. An annotated checklist of bryophytes of Europe, Macaronesia and Cyprus. J. Bryol. 2020, 42, 1–116. [Google Scholar] [CrossRef]
  61. Tichý, L.; Holt, J.; Nejezchlebová, M. JUICE Program for Management, Analysis and Classification of Ecological Data. Program Manual; Masaryk University Brno: Brno, Czech Republic, 2006. [Google Scholar]
  62. Van Zuijlen, K.; Nobis, M.P.; Hedenäs, L.; Hodgetts, N.; Calleja Alarcón, J.A.; Albertos, B.; Bernhardt-Römermann, M.; Gabriel, R.; Garilleti, R.; Lara, F.; et al. Bryophytes of Europe Traits (BET) data set: A fundamental tool for ecological studies. J. Veg. Sci. 2023, 34, e13179. [Google Scholar] [CrossRef]
  63. Hill, M.O.; Preston, C.D. The geographical relationships of British and Irish bryophytes. J. Bryol. 1998, 20, 127–226. [Google Scholar] [CrossRef]
  64. Hill, M.O.; Preston, C.D.; Bossanquet, S.D.S.; Roy, D.B. Bryoatt—Attributes of British and Irish Mosses, Liverworts and Hornworts; NERC Centre for Ecology and Hydrology and Countryside Council for Wales: Huntigdon, UK, 2007. [Google Scholar]
  65. Hammer, Ø.; Harper, D.A.T.; Ryan, P.D. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Paleontol. Electron. 2001, 4, 9. [Google Scholar]
  66. ter Braak, C.; Šmilauer, P. Canoco Reference Manual and User’s Guide: Software for Ordination, Version 5.0; Microcomputer Power: Ithaca, NY, USA, 2012. [Google Scholar]
  67. Šmilauer, P.; Lepš, J. Multivariate Analysis of Ecological Data Using Canoco 5.0, 2nd ed.; Cambridge University Press: New York, NY, USA, 2014. [Google Scholar]
  68. McCune, B.; Mefford, M.J. PC-ORD. Multivariate Analysis of Ecological Data, Version 7.09; Wild Blueberry Media: Corvallis, OR, USA, 2018. [Google Scholar]
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Figure 1. Bryophyte alpha diversity indices across investigated forest types. FA—acidophilous beech forests, FB—basiphilous beech forests, QA—acidophilous oak forests, QB—basiphilous oak forests.
Figure 1. Bryophyte alpha diversity indices across investigated forest types. FA—acidophilous beech forests, FB—basiphilous beech forests, QA—acidophilous oak forests, QB—basiphilous oak forests.
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Figure 2. Box-plot graphs of bryophyte Ellenberg’s indicator values (EIVs) for temperature (T), light (L), moisture (F), reaction (R), nutrients (N) and measured soil pH across investigated forest types. FA—acidophilous beech forests, FB—basiphilous beech forests, QA—acidophilous oak forests, QB—basiphilous oak forests.
Figure 2. Box-plot graphs of bryophyte Ellenberg’s indicator values (EIVs) for temperature (T), light (L), moisture (F), reaction (R), nutrients (N) and measured soil pH across investigated forest types. FA—acidophilous beech forests, FB—basiphilous beech forests, QA—acidophilous oak forests, QB—basiphilous oak forests.
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Plants 12 03346 g003
Figure 3. DCA ordination graphs of investigated plots in different forest types with Ellenberg’s indicator values (A), biogeographic elements based on major biome (B) and eastern limit (C) passively projected as vectors. FA—acidophilous beech forests, FB—basiphilous beech forests, QA—acidophilous oak forests, QB—basiphilous oak forests; Ellenberg’s indicator values: T—temperature, L—light, F—moisture, R—reaction, N—nutrients; biogeographic elements: Temp–temperate, Boreo-temp—oreo-temperate, Boreal-m—boreal–montane, Boreo-ar—boreo-arctic–montane, Wide-bor—wide-boreal, Wide-temp—wide-temperate, S-temp—southern-temperate, Med-Atl—Mediterranean–Atlantic.
Figure 3. DCA ordination graphs of investigated plots in different forest types with Ellenberg’s indicator values (A), biogeographic elements based on major biome (B) and eastern limit (C) passively projected as vectors. FA—acidophilous beech forests, FB—basiphilous beech forests, QA—acidophilous oak forests, QB—basiphilous oak forests; Ellenberg’s indicator values: T—temperature, L—light, F—moisture, R—reaction, N—nutrients; biogeographic elements: Temp–temperate, Boreo-temp—oreo-temperate, Boreal-m—boreal–montane, Boreo-ar—boreo-arctic–montane, Wide-bor—wide-boreal, Wide-temp—wide-temperate, S-temp—southern-temperate, Med-Atl—Mediterranean–Atlantic.
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Figure 4. Spectrum of biogeographic elements regarding major biomes (E1) for the bryophyte flora of Mt. Papuk through forest types. FA—acidophilous beech forests, FB—basiphilous beech forests, QA—acidophilous oak forests, QB—basiphilous oak forests.
Figure 4. Spectrum of biogeographic elements regarding major biomes (E1) for the bryophyte flora of Mt. Papuk through forest types. FA—acidophilous beech forests, FB—basiphilous beech forests, QA—acidophilous oak forests, QB—basiphilous oak forests.
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Figure 5. Spectrum of biogeographic elements regarding eastern limit category (E2) for the bryophyte flora of Mt. Papuk through forest types.
Figure 5. Spectrum of biogeographic elements regarding eastern limit category (E2) for the bryophyte flora of Mt. Papuk through forest types.
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Figure 6. Geographical position of the study area in southeast Europe and Croatia and distribution of the investigated plots on Mt. Papuk.
Figure 6. Geographical position of the study area in southeast Europe and Croatia and distribution of the investigated plots on Mt. Papuk.
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Figure 7. Investigated forest types. (A)—acidophilous beech forest (FA); (B)—basiphilous beech forest (FB); (C)—acidophilous oak forests (QA); (D)—basiphilous oak forests (QB).
Figure 7. Investigated forest types. (A)—acidophilous beech forest (FA); (B)—basiphilous beech forest (FB); (C)—acidophilous oak forests (QA); (D)—basiphilous oak forests (QB).
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Alegro, A.; Šegota, V.; Rimac, A.; Papp, B. Diversity, Ecology and Phytogeography of Bryophytes across Temperate Forest Communities—Insight from Mt. Papuk (Croatia, SE Europe). Plants 2023, 12, 3346. https://doi.org/10.3390/plants12193346

AMA Style

Alegro A, Šegota V, Rimac A, Papp B. Diversity, Ecology and Phytogeography of Bryophytes across Temperate Forest Communities—Insight from Mt. Papuk (Croatia, SE Europe). Plants. 2023; 12(19):3346. https://doi.org/10.3390/plants12193346

Chicago/Turabian Style

Alegro, Antun, Vedran Šegota, Anja Rimac, and Beáta Papp. 2023. "Diversity, Ecology and Phytogeography of Bryophytes across Temperate Forest Communities—Insight from Mt. Papuk (Croatia, SE Europe)" Plants 12, no. 19: 3346. https://doi.org/10.3390/plants12193346

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