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B. PacsaiDepartment of Nature Conservation Biology, Georgikon Campus, Hungarian University of Agriculture and Life Sciences, H-8360 Keszthely, Festetics u. 7, Hungary

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I. SisákInstitute of Plant Sciences and Environmental Protection, Faculty of Agriculture, University of Szeged, H-6800 Hódmezővásárhely, Andrássy u. 15, Hungary

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J. BódisDepartment of Nature Conservation Biology, Georgikon Campus, Hungarian University of Agriculture and Life Sciences, H-8360 Keszthely, Festetics u. 7, Hungary

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With 22 taxa reported from the country so far, Epipactis is the most species-rich orchid genus in Hungary. Many of them are rare, threatened species. To protect endangered species effectively, it is crucial to explore their ecology. Our work aimed to select and examine factors that are influencing the distribution of Epipactis species. Our data collection (2014–2018) was carried out in the Keszthely Hills, in the northeastern part of the Zala Hills and the Southern Bakony Mountains. We assigned ecologically relevant data from databases of local forestries, terrain models and geological maps to each occurrence. We examined the factors that result in the best differentiation between the studied species. At 1,261 localities, a total of 5,223 individuals of 15 taxa were found. We found three factors (tree species composition of the forest, genetic soil type, bedrock type) that significantly influenced the distribution of Epipactis species. Our results can help understand the distribution patterns of these species and allow for more effective, targeted protection of their potential habitats on a regional level.

Abstract

With 22 taxa reported from the country so far, Epipactis is the most species-rich orchid genus in Hungary. Many of them are rare, threatened species. To protect endangered species effectively, it is crucial to explore their ecology. Our work aimed to select and examine factors that are influencing the distribution of Epipactis species. Our data collection (2014–2018) was carried out in the Keszthely Hills, in the northeastern part of the Zala Hills and the Southern Bakony Mountains. We assigned ecologically relevant data from databases of local forestries, terrain models and geological maps to each occurrence. We examined the factors that result in the best differentiation between the studied species. At 1,261 localities, a total of 5,223 individuals of 15 taxa were found. We found three factors (tree species composition of the forest, genetic soil type, bedrock type) that significantly influenced the distribution of Epipactis species. Our results can help understand the distribution patterns of these species and allow for more effective, targeted protection of their potential habitats on a regional level.

INTRODUCTION

Epipactis (Orchidaceae) is one of the most species-rich orchid genera of the north temperate zone. In Hungary, nearly one-third of the native orchid species belong to this group. The genus currently is in a state of rapid speciation, which could be explained by the evolutionary effect of their recent radiation from the Mediterranean towards the north after the last glaciation (Delforge 2006, Tranchida-Lombardo et al. 2011). The high rate of autogamy – which is a good strategy during rapid colonisation – in this genus might also be the consequence of this progress (Hollingsworth et al. 2006, Squirrell et al. 2002). Epipactis species are also adapted to clonal growth, which is also a beneficial trait in environments where pollination is limited by the scarcity of potential partners (Eckert 1999).

Due to this ongoing speciation, the genus’ taxonomy is of high complexity, the number of accepted species greatly varies by authors and time as well (Delforge 1995, 2006, Molnár V. 2011).

Like every genus of Orchidaceae, Epipactis species also rely on symbiotic fungi during their germination, but often through their whole life cycle (Gonneau et al. 2014). Most of the known potential mycorrhizal partners of species in this genus are also ectomycorrhizal tree species (Schiebold et al. 2017). Although many Epipactis species have many potential fungi partners, this association is often highly specific. Many species have only one known mycorrhizal partner (Schiebold et al. 2017). Therefore, the distribution area of Epipactis species is limited not just by abiotic factors, but by the presence of their mycorrhizal partners, which is also affected by abiotic factors (Rasmussen and Whigham 1998, Taylor and Bruns 1999).

Partly due to their indirect dependence of particular tree species through their mycorrhizal partner, most Epipactis species are typically limited to only a few specific habitat types in their whole distribution area where the appropriate tree species occur (Hrivnák et al. 2014), in contrast with other orchid genera which often occur in diverse habitats at different parts of their distribution area (e.g., Ophrys, Dactylorhiza, Orchis spp.) (Abdullah 2018, Illyés et al. 2010). On the other hand, members of the Epipactis genus often considered pioneer species in general, since they frequently appear in secondary, disturbed habitats, like plantations or mines (Adamowski 2006, Jakubska-Busse et al. 2006, Rewicz et al. 2017, Shefferson et al. 2008, Süveges et al. 2020).

22 Epipactis species and subspecies were reported from Hungary according to recent publications, many of them only recently (Csábi and Halász 2016, Molnár V. 2011, Somlyay et al. 2016). Although in some cases their taxonomic rank is still disputed, we have some knowledge of the ecological preferences of the majority of these taxa. Most of these ecological data derives from descriptions attached to floristic data, though a few publications aimed to char-acterise and compare ecological preferences of certain Epipactis taxa (Hrivnák et al. 2014, Sulyok and Molnár V. 1998, Timpe and Mrkvicka 1996, Těšitelová et al. 2012) or orchid species in general (Djordjević et al. 2016).

The aim of our work was to determine if there are noticeable differences between ecological preferences of some Epipactis species in a relatively small area compared to their distribution area.

MATERIAL AND METHODS

Study areas

Data collection was carried out in six Natura 2000 sites in Western Hungary (Table 1, Fig. 1), as these areas represent well most natural habitats in this region.

Table 1

The sampled Natura 2000 sites and some details of the data collection.

RegionSiteNatura 2000 site codeArea (km2)Data collection
Keszthely HillsKeszthelyi-hegységHUBF20035149.02014–2018
South Bakony HillsKab-hegyHUBF2000380.82017–2018
Agár-tetőHUBF2000451.42016–2018
Zala HillsZalaegerszegi Csácsi erdőHUBF2005311.32016
Nagykapornaki erdőHUBF200546.42016
RemetekertHUBF200559.72016
Fig. 1
Fig. 1

Map of the study area and the sample sites

Citation: Acta Botanica Hungarica 64, 3-4; 10.1556/034.64.2022.3-4.10

The Keszthely Hills has two main parts with significant differences in their rock composition and habitat types, the Keszthely Plateau and the Tátika Group. The Keszthely Plateau is mainly composed of upper Triassic dolomite, on which rendzina, Eutric Cambisol and Lithic Leptosol are typical (Dövényi 2010). In this area, closed and open thermophilous oak woodlands and beech (Fagus sylvatica) forests are the most common (Bölöni and Bauer 2010).

The Tátika Group is of volcanic origin, mainly composed of basalt on which Eutric Cambisol and Haplic Luvisol are distinct soil types (Dövényi 2010). Besides beech forests, sessile oak (Quecus petraea) – hornbeam (Carpinus betulus) and lowland oak-hornbeam woodlands are the most common forest habitats in this area (Bölöni and Bauer 2010, Bölöni et al. 2011).

The two sites located in the Southern Bakony Hills (Kab-hegy, Agártető) are composed of volcanic rocks (mainly basalt) deposited on dolomite and limestone. Eutric Cambisol and Haplic Luvisol are the most frequent soil types in this area and rendzina are also prevalent (Dövényi 2010). The most common woodland habitats in this area are Fagus sylvatica and sessile oakhornbeam woodlands with some uncharacteristic hardwood forests and plantations (Bölöni and Bauer 2010, Bölöni et al. 2011).

Zala Hills are composed of loam and loess deposited on Pannonic calcareous bedrock, on which Haplic Luvisol and Chromic Cambisol are typical (Dövényi 2010). The most common woodland habitats are sessile oak-horn-beam and beech woodlands, with many riverine ash-alder forests (Bölöni and Bauer 2010).

Methods

The data collection was done between 2014 and 2018; the position and the number of individuals occurring at one locality were recorded. The minimum distance between localities of one species was 100 m, all localities were documented once. If we found two or more Epipactis species on one point (which happened frequently), we recorded the localities separately, which means only one species belongs to each locality. We recorded 1261 localities altogether (Table 2).

Table 2

The number of localities and the number of shoots (in parentheses) of the occurring species in the three regions. The species involved in the analysis are in bolditalics.

SpeciesBakony MtsZala HillsKeszthely Hills
Epipactis albensis Nováková et Rydlo008 (31)
Epipactis atrorubens Hoffm. ex Besser0010 (217)
Epipactis helleborine (L.) Crantz21 (123)1 (2)352 (1244)
Epipactis leptochila Godfery016 (78)42 (118)
Epipactis microphylla (Ehrh.) Sw.13 (34)5 (8)71 (212)
Epipactis moravica P. Batoušek007 (58)
Epipactis muelleri Godfery007 (27)
Epipactis neglecta Kümpel22 (41)058 (235)
Epipactis nordeniorum Robatsch44 (249)33 (136)57 (197)
Epipactis palustris (L.) Crantz0022 (116)
Epipactis peitzii H. Neumann et Wucherpf.0042 (163)
Epipactis pontica Taubenheim005 (32)
Epipactis purpurata Sm.23 (75)162 (321)9 (17)
Epipactis tallosii A. Molnár et Robatsch0086 (1047)
Epipactis voethii Robatsch1 (3)17 (35)129 (407)

We attempted to map the six sites near systematically by foot during fieldwork, which resulted in an 8.1 km/km2 average sampling density (more than 2,500 km walk between May and September). In the study sites, the presence of 15 Epipactis species was detected (Table 2). We followed the nomenclature of Molnár V. (2011) and Somlyay et al. (2016).

We included in the statistical analysis those species which were found at least at eight localities. In that way, E. pontica, E. muelleri and E. moravica were excluded from the analysis. E. palustris was also excluded from the analysis given that it is not a forest species (unlike the other species studied), typically occurring in wet meadows and marshes.

To each of the localities, we have assigned geographical attributes [altitude (m), slope (°)], soil (soil type, bedrock) and forestry data [tree species composition, forest stand age and the canopy cover] based on the digital elevation model of the Department of Geodesy Remote Sensing and Land Offices, the geological map of the Geological Institute of Hungary and the databases of the three local forestries, Verga Ltd, Bakonyerdő Ltd and Zalaerdő Ltd.

In total, 34 tree species were found in forest subcompartments in which we recorded Epipactis species. We included the 11 most common tree species in the statistical analysis. Slavonian oak (Quercus robur subsp. slavonica) distinguished in the forestries’ databases was merged into the pedunculate oak (Quercus robur), based on taxonomic consideration. The other 21 species, which were neglected in the statistical survey, were found in a few cases (< 10) and/or in low proportion (< 5%) in the examined forest subcompartments. Their combined share in the tree canopy cover did not reach 3%.

Seven genetic soil types occurred in more than five cases; these were included in the analysis. Based on the geological map, a total of 32 bedrock types were assigned to Epipactis localities. For practical purposes, we classified these highly specific classes into seven main categories (dolomite, scree, loess, sediment, sand, basalt, marl).

To determine the extent of differences in each species’ examined factors, in cases of each continuous variable (e.g., canopy closure and age of forest subcompartments), we used a single-variable analysis of variance (ANOVA). For each categorical variable (e.g., bedrock types, tree species composition of the forest subcompartments), we used multivariate logistic regression.

Spatial calculations and data management were done with ArcGIS 10.2 software. Analysing simultaneous responses of many species to several factors is often a task for ecologists that requires a multivariate analysis. The traditional approach is to use parametric multiple analysis of variance. For ecological applications, however, nonparametric approaches may be preferred. Several nonparametric multivariate methods for use in biology, ecology and the social sciences have been proposed. For these, a test statistic is obtained directly from distances calculated among sampling units where distance measure other than the Euclidean distance may be used.

Legendre and Anderson (1999) have proposed a method called distance-based redundancy analysis. It has the double advantage that it can be based on any distance measure of choice and it can provide a multivariate partitioning to test any individual term in a multifactorial design. This is a significant development, because it is precisely such designs that are most often used in ecological studies, due to the inclusion of several interacting factors.

The statistical analyses were performed using redundancy analysis (RDA) and variance partition (varpart). In the case of trees, we used their canopy cover percentages in the investigation. All analyses and the presentation of the results were done with R software version 3.5.3 (R Core Team 2019) and vegan package version 2.5-6 (Oksanen et al. 2019).

RESULTS

By redundancy analysis we found that although all examined factors had significant effect (p > 0.01 at 999 permutations) on occurrences of Epipactis species, particularly three factors (tree species composition of forest subcompartments, soil type and bedrock type) contributed to the explained variance with a total adjusted R² of 0.119 (Fig. 2). These three factors unique effects were comparable with the sum of variances explained together by one or two other explanatory variables.

Fig. 2
Fig. 2

Venn diagram showing the effects of tree species composition of forest subcompartments, soil type and bedrock type on Epipactis occurrences. The values indicate the adjusted R², as calculated from variation partitioning by RDA

Citation: Acta Botanica Hungarica 64, 3-4; 10.1556/034.64.2022.3-4.10

The relationships between tree species composition and Epipactis species

Out of the examined factors, tree species composition of forest stands was the best predictor of occurrences of Epipactis species (RDA, adjusted R2 =0.0667, p = 0.001 at 999 permutations). Along the first RDA1 axis (Fig. 3) there is a distinct gradient with almost 2.5 times as much variance explained than by axis RDA2. E. helleborine, E. muelleri and E. atrorubens preferred Quercus pubescens and Fraxinus ornus or Pinus nigra stands, while E. purpurata, E. nordeniorum, E. leptochila and E. albensis preferred Fagus sylvatica, Carpinus betulus and Quercus robur forest stands. Besides these two marked orientations, E. microphylla and E. peitzii preferred Quercus cerris and E. nordeniorum had preferences towards small-leaved lime. We found E. tallosii mainly in Quercus robur and Carpinus betulus forests, but the largest population was associated with a Populus stand mixed with Quercus robur. The other four species did not have defined preferences, but they disfavour thermophilous habitats with Pinus nigra, Quercus pubescens and Fraxinus ornus.

Fig. 3
Fig. 3

Biplot of redundancy analysis (RDA) showing the correlations between tree- and Epipactis species. Tree species are represented by arrows and with grey text: Carbet, Carpinus betulus; Fagsyl, Fagus sylvatica; Fraorn, Fraxinus ornus; Lardec, Larix decidua; Quepet, Quercus petraea; Quepub, Quercus pubescens; Querob, Quercus robur; Querub, Quercus rubra; Pinnig, Pinus nigra; Pinsyl, Pinus sylvestris; tilcor, Tilia cordata. Epipactis species (represented by black circles): alb, E. albensis; atr, E. atrorubens; hel, E. helleborine; lep, E. leptochila; mic, E. microphylla; neg, E. neglecta; nor, E. nordeniorum; pei, E. peitzii; pur, E. purpurata; tal, E. tallosii; voe, E. voethii

Citation: Acta Botanica Hungarica 64, 3-4; 10.1556/034.64.2022.3-4.10

The relationships between soil types and Epipactis species

We also found soil type as a significant factor influencing Epipactis occurrences (RDA, adjusted R2 = 0.0566, p = 0.001 at 999 permutations), but to a less extent than forest composition.

There were three distinct gradients (Fig. 4), with E. purpurata preferring Haplic Luvisols, E. helleborine, E. peitzii and E atrorubens preferring Rendzic Leptosols and E. muelleri was associated with Lithic Leptosols. Also, notable the preference of E. nordeniorum towards Eutric Leptosol.

Fig. 4
Fig. 4

Biplot of redundancy analysis (RDA) showing the correlations between Epipactis species and soil types on which they occurred. Arrows and grey text represent soil types: lLep: Lithic Leptosol; eLep: Eutric Leptosol; rLep: Rendzic Leptosol; hLuv: Haplic Luvisol; cCam: Chromic Cambisol; eCam: Eutric Cambisol; eGle: Eutric Gleysol. Epipactis species (represented by black circles): alb, E. albensis; atr, E. atrorubens; hel, E. helleborine; lep, E. leptochila; mic, E. microphylla; neg, E. neglecta; nor, E. nordeniorum; pei, E. peitzii; pur, E. purpurata; tal, E. tallosii; voe, E. voethii

Citation: Acta Botanica Hungarica 64, 3-4; 10.1556/034.64.2022.3-4.10

The relationships between bedrock types and Epipactis species

Bedrock type was a significant predictor as well (RDA, adjusted R2 = 0.0418, p = 0.001 at 999 permutations), but it explained the least variation of the three factors described above.

In the case of bedrock type preferences, RDA analysis showed one strong gradient between loess and dolomite along with sand (x-axis explains four times as much variability as y-axis). There is a weaker gradient in the direction of sediments (Fig. 5). E. atrorubens, E. helleborine and E. peitzii had a marked preference towards sand and dolomite. E. nordeniorum, E. purpurata, E. leptochila and E. albensis preferred loess, although E. albensis in a less pronounced way and E. purpurata had a distinct preference towards basalt also. The other seven species mostly preferred sediments.

Fig. 5
Fig. 5

Biplot of redundancy analysis (RDA) showing the correlations between Epipactis species and bedrock types on which they occurred. Bedrock types (represented by arrows and with grey text): dolom, dolomite; limest, limestone; sedim, sediment; Epipactis species (represented by black circles): alb, E. albensis; atr, E. atrorubens; hel, E. helleborine; lep, E. leptochila; mic, E. microphylla; neg, E. neglecta; nor, E. nordeniorum; pei, E. peitzii; pur, E. purpurata; tal, E. tallosii; voe, E. voethii

Citation: Acta Botanica Hungarica 64, 3-4; 10.1556/034.64.2022.3-4.10

Single-variable factors affecting the distribution of Epipactis species

Although we found that all examined single-variable factors had significant effect on distributions of Epipactis species, in most cases they behave similarly, only a few of them preferred considerably different conditions by some factors (Fig. 6).

Fig. 6
Fig. 6

Boxplots of elevation (a), slope (b), forest subcompartment age (c) and forest subcompartment average canopy closure (d) assigned to Epipactis spp. localities. Epipactis species: alb, E. albensis; atr, E. atrorubens; hel, E. helleborine; lep, E. leptochila; mic, E. microphylla; neg, E. neglecta; nor, E. nordeniorum; pei, E. peitzii; pur, E. purpurata; tal, E. tallosii; voe, E. voethii

Citation: Acta Botanica Hungarica 64, 3-4; 10.1556/034.64.2022.3-4.10

By the elevation where Epipactis species occurred, there were several visible differences between some species (Fig. 6). Still, it had a less pronounced effect on their distribution (RDA, adjusted R2 = 0.0111, p = 0.001 at 999 permutations). E. peitzii, E. neglecta and E. microphylla had a significant preference towards higher altitudes (p = 0.001 at 999 permutations), while E. tallosii preferred lower situated habitats. Age, canopy closure and slope had also significant effect, but only with adjusted R2 of 0.0035; 0.0027 and 0.00084, respectively. All studied species occurred predominantly in forest stands of 50–80 years. Still, in some cases, significant number of occurrences were found in younger (e.g. E. helleborine, E. microphylla, E. neglecta, E. nordeniorum, E. purpurata) and much older (e.g. E. atrorubens, E. helleborine, E. neglecta, E. voethii) stands as well. Most examined Epipactis species occurred principally in stands with high (85–95%) canopy closure. Only E. atrorubens preferred forests with somewhat more open canopies as well. All species occurred mostly on slopes between 0° and 15° without many differences between the preferences of each species. Only E. atrorubens preferred more steep terrain.

DISCUSSION

The number of recorded localities showed remarkable differences in the three regions. The number of recorded species and individuals was significantly higher in the Keszthely Hills than in the other two areas. It is partly because the Keszthely Hills is the largest among the sample sites and hosts more habitat types, thus many species with different habitat preferences can find their favourable conditions in this relatively small area. Another factor that could influence this difference is that we collected data in the Keszthely Hills for the most extended period (Table 1) thus we had more chance finding populations that might appear dormant in years with less favourable conditions.

Dissimilarities between ratios of occurring Epipactis species on sites with different characteristics were observed. This phenomenon is most distinct in areas with diverse habitat types, as we experienced in Keszthely Hills, where besides E. helleborine and E. voethii, the two most common species, further 13 species were found. In Zala Hills E. purpurata was the most common species by far with many occurrences of E. nordeniorum and E. leptochila also, whereas E. helleborine was remarkably uncommon in the area. In Bakony Mts, we found the least number of species, of which E. nordeniorum was the most common. Out of the 15 species, only E. nordeniorum had a considerable number of occurrences in the study areas in all three regions, which is interesting, since according to present knowledge, this species has a small distribution area, confined to the Carpathian Basin and its immediate surroundings (Delforge 2006), particularly to Transdanubia (Molnár V. 2011).

In the case of E. helleborine we found a marked preference towards specific forests, bedrock and soil types as well, despite often being considered the most generalist species of the genus (Delforge 2006, Molnár V. 2011). However, there are large areas covered with Fagus sylvatica forests in all three regions, we found it frequently in thermophilous forests mainly composed of Quercus pubescens or Pinus nigra, which is uncommon among literature data (Aedo and Herrero 2005, Lorenz 2005).

Although previous publications indicate that E. atrorubens often occurs in Fagus sylvatica forests (Timpe 1995, Czarna et al. 2014) and this habitat type is common in our study area, we found this species predominantly in stands of Pinus nigra and P. sylvestris. Both tree species are non-native in the area, and they were used for afforestation of barren hilltops and southern hillsides in the region (Tamás 2003).

We found several E. tallosii occurrences in the Keszthely Hills site, mainly in humid stands of Quercus robur mixed with Carpinus betulus. Still, the largest population is partially situated in a canopy dominated by Populus. Since this habitat type is scarce in our study area (Populus spp. occurred only in two forest subcompartments with low proportions in the Keszthely Hills site), this might indicate a preference for Populus species. Lack of these habitat types not allowed to confirm it statistically, but it is supported by references in which E. tallosii were recorded from Populus stands and plantations (Molnár V. et al. 1998, Nagy 2015, Hadinec and Lustyk 2007).

We could find some significant differences between altitude preferences, although the highest and the lowest altitude in the study area had the difference of a mere 460 metres. Some of the studied species (e.g. E. atrorubens, E. leptochila, E. microphylla) occur in altitude ranges that are a multiple of this value (Delforge 2006), still we could indicate E. peitzii, E. neglecta and E. microphylla preferred higher altitudes and E. tallosii preferred lower situated habitats. The latter species often occurred in the vicinity of streams in the area, explaining their preference towards lower situated areas. This tendency towards riparian forest and lakeshores is also represented in literature data (Molnár V. 2011, Molnár V. et al. 1998).

Only one of the 11 studied species had pronounced slope preferences, E. atrorubens preferred more steep terrain. It might be influenced by the fact that most Epipactis occurrences were situated in valley bottoms or lower parts of valley sides. This factor’s effect is significantly reduced mainly by the vegetation cover.

Although we found that tree species composition of forests had the strongest influence on species occurrences, other single factors also had a marked effect. In the case of Epipactis purpurata it especially preferred loamy soils and E. atrorubens preferred dolomite and sand as a bedrock.

Our study statistically confirms descriptions of most species habitat preferences by previous references (Delforge 2006, Molnár V. 2011) and its in good accordance with field experiences.

Since we used sources, which are available in the same standardised form for the whole country, we believe these results not only add some valuable information to the knowledge on the habitat preferences of these species in general, but they might help in localising potentially suitable habitats of Epipactis species. However, these results could be used with the most accuracy on a regional level.

Acknowledgements

The authors are grateful to Iván Horváth, the Balaton Uplands National Park, Verga Zrt., Bakonyerdő Zrt., Department of Geodesy Remote Sensing and Land Offices and Geological Institute of Hungary for their kind assistance in data entry. The publication is supported by the EFOP-3.6.3-VEKOP-16-2017-00008 project. The project is co-financed by the European Union and the European Social Fund.

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  • Hrivnák, R., Hrivnák, M., Slezák, M., Vlčko, J., Baltiarová, J. and Svitok, M. (2014): Distribution and eco-coenotic patterns of the forest orchid Epipactis pontica in Slovakia.–Ann. Forest Res. 57(1): 5569.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Illyés, Z., Halász, K. and Rudnóy, Sz. (2010): Changes in the diversity of the mycorrhizal fungi of orchids as a function of the water supply of the habitat.–J. Appl. Bot. Food Quality 83(1): 2836.

    • Search Google Scholar
    • Export Citation
  • Jakubska-Busse, A., Malicka, M. and Malicki, M. (2006): New data on the apophytic occur-rence of Epipactis helleborine (L.) Crantz and Cephalanthera longifolia (L.) Fritsch in Populus ×canadensis plantation in Lower Silesia (south-western Poland).–Biodiv.: Res. Conserv. 1–2: 9698.

    • Search Google Scholar
    • Export Citation
  • Legendre, P. and Anderson, M. J. (1999): Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments.–Ecol. Monogr. 69: 124.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lorenz, R. (2005): Zur Artengruppe von Epipactis helleborine (Orchidaceae) in Südtirol.–Gredleriana 5: 103134.

  • Molnár V., A., Vidéki, R. and Vlčko, J. (1998): Adatok hazai Epipactis-fajok ismeretéhez. II.–Kitaibelia 3(2): 287289.

  • Molnár V., A. (2011): Magyarország orchideáinak atlasza. – Kossuth Kiadó, Budapest, 504 pp.

  • Nagy, T. (2015): Néhány florisztikai adat Kötcse környékéről (Dél-Dunántúl, NyugatKülső-Somogy).–Kitaibelia 20(1): 7480.

  • Oksanen, J. et al. (2019): Vegan: community ecology package, ver. 2.5-6. – URL: http://r-forge.rproject.org/projects/vegan/.

  • Rasmussen, H. N. and Whigham, D. F. (1998): The underground phase: a special challenge in studies of terrestrial orchid populations.–Bot. J. Linn. Soc. 126: 4964.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rewicz, A., Jasku, R., Rewicz, T. and Tończyk, G. (2017): Pollinator diversity and reproductive success of Epipactis helleborine (L.) Crantz (Orchidaceae) in anthropogenic and natural habitats.–PeerJ 5: e3159.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • R Core Team (2019): R: A language and environment for statistical computing. – R Foundation for Statistical Computing, Vienna, Austria. URL: http://www.R-project.org/.

    • Search Google Scholar
    • Export Citation
  • Schiebold, J. M. I., Bidartondo, M. I., Karasch, P., Gravendeel, B. and Gebauer, G. (2017): You are what you get from your fungi: nitrogen stable isotope patterns in Epipactis species.–Ann. Bot. 119: 10851095.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Shefferson, R. P., Kull, T. and Tali, K. (2008): Mycorrhizal interactions of orchids colonizing Estonian mine tailings hills.–Amer. J. Bot. 95: 156164.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Somlyay, L., Makádi, S. and Csábi, M. (2016): Adatok Budapest környéke flórájának ismeretéhez II.–Kitaibelia 21(1): 3350.

  • Squirrell, J., Hollingsworth, P. M., Bateman, R. M., Tebbitt, M. C. and Hollingsworth, M. L. (2002): Taxonomic complexity and breeding system transitions: conservation genetics of the Epipactis leptochila complex (Orchidaceae).–Mol. Ecol. 11: 19571964.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sulyok, J. and Molnár V., A. (1998): Az Epipactis pontica Taubenheim Magyarországon.–Kitaibelia 1: 6670.

  • Süveges, K., Löki, V., Lovas-Kiss, Á., Ljubka, T., Fekete, R., Takács, A., Vincze, O., Lukács, B. A. and Molnár V., A. (2019): From European priority species to characteristic apophyte: Epipactis tallosii (Orchidaceae).–Willdenowia 49(3): 401409.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Tamás, J. (2003): The history of Austrian pine plantations in Hungary.–Acta Bot. Croat. 62(2): 147158.

  • Taylor, D. L. and Bruns, T. D. (1999): Population, habitat and genetic correlates of mycorrhizal specialization in the ‘cheating’ orchids Corallorhiza maculata and C. mertensiana.–Mol. Ecol. 8: 17191732.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Těšitelová, T., Těšitel, J., Jersáková, J., Rihová, G. and Selosse, M.-A. (2012): Symbiotic germination capability of four Epipactis species (Orchidaceae) is broader than expected from adult ecology.–Amer. J. Bot. 99: 10201032.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Timpe, W. (1995): Orchideen im südlichen Burgenland (IX). Epipactis (Stendelwurz)-Neufunde im Günser Gebirge.–Burgenländ. Heimatbl. 57: 125131.

    • Search Google Scholar
    • Export Citation
  • Timpe, W. and Mrkvicka, A. Ch. (1996): Beiträge zur Morphologie, Ökologie und Verbreitung von Epipactis nordeniorum, E. pontica und E. albensis in Südost-Österreich.–Florae Austr. Nov. 4: 110.

    • Search Google Scholar
    • Export Citation
  • Tranchida-Lombardo, V., Cafasso, D., Cristaudo, A. and Cozzolino, S. (2011): Phylogeo-graphic patterns, genetic affinities and morphological differentiation between Epipactis helleborine and related lineages in a Mediterranean glacial refugium.–Ann. Bot. 107: 427436.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Abdullah, W. R. (2018): Diversity and roles of mycorrhizal fungi in the bee orchid Ophrys apifera. – PhD thesis, University of Liverpool, Liverpool.

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  • Adamowski, W. (2006): Expansion of native orchids in anthropogenous habitats.–Polish Bot. Stud. 22: 3544.

  • Aedo, C. and Herrero, A. (2005): Flora Iberica 21. – Real Jardín Botánico, CSIC, Madrid, 366 pp.

  • Bölöni, J. and Bauer, N. (2010): Zalaapáti-hát; Tátika-csoport; Keszthelyi-fennsík; Kab hegy–Agártető-csoport. – In: Dövényi, Z. (ed.): Magyarország kistájainak katasztere. Második, átdolgozott és bővített kiadás. MTA Földrajztudományi Kutatóintézet, Budapest, p. 417 553 417, 533, 536, 553.

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  • Bölöni, J., Molnár, Zs. and Kun, A. (eds) (2011): Magyarország élőhelyei. Vegetációtípusok leírása és határozója, ÁNÉR 2011. – MTA Ökológiai és Botanikai Kutatóintézete, Vácrátót, 441 pp.

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  • Csábi, M. and Halász, A. (2016): Új orchideafaj a magyar flórában: Epipactis pseudopurpurata Mered’a.–Kitaibelia 21(1): 2732.

  • Czarna, A., Maćkowiak, Ł. and Woźniak, A. (2014): The occurrence of Epipactis albensis in the Lower Silesia province.–Chrońmy Przyrodę Ojczystą 70(6): 563566.

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  • Delforge, P. (1995): Orchids of Britain & Europe. – Harper Collins Publishers, London, 480 pp.

  • Delforge, P. (2006): Orchids of Europe, North Africa and the Middle East. – A&C Black Publishers Ltd, London, 640 pp.

  • Djordjević, V., Jakovljević, K. and Stevanović, V. (2016): Three taxa of Epipactis (Orchidaceae-Epidendroideae) new for the flora of Serbia.–Phyton; annales rei botanicae 56(1): 7789.

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  • Dövényi, Z. (2010): Magyarország kistájainak katasztere. Második, átdolgozott és bővített kiadás. – Magyar Tudományos Akadémia, Budapest, 876 pp.

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  • Eckert, C. G. (1999): Clonal plant research: proliferation, integration, but not much evolution.–Amer. J. Bot. 86: 16491654.

  • Gonneau, C., Jersáková, J., de Tredern, E., Till-Bottraud, I., Saarinen, K., Sauve, M., Roy, M., Hájek, T. and Selosse M.-A. (2014): Photosynthesis in perennial mixotrophic Epipactis spp. (Orchidaceae) contributes more to shoot and fruit biomass than to hypogeous survival.–J. Ecol. 102: 11831194.

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  • Hadinec, J. and Lustyk, P. (2007): Additamenta ad floram Reipublicae Bohemicae. VI.–Zpr. Českoslov. bot. společn. 42: 247337.

  • Hollingsworth, P. M., Squirrell, J. and Hollingsworth, M. L. (2006): Taxonomic complexity, conservation and recurrent origins of self-pollination in Epipactis (Orchidaceae). − In: Bailey, J. and Ellis, R. G. (eds): Current taxonomic research on the British and European flora. BSBI, London, pp. 2744.

    • Search Google Scholar
    • Export Citation
  • Hrivnák, R., Hrivnák, M., Slezák, M., Vlčko, J., Baltiarová, J. and Svitok, M. (2014): Distribution and eco-coenotic patterns of the forest orchid Epipactis pontica in Slovakia.–Ann. Forest Res. 57(1): 5569.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Illyés, Z., Halász, K. and Rudnóy, Sz. (2010): Changes in the diversity of the mycorrhizal fungi of orchids as a function of the water supply of the habitat.–J. Appl. Bot. Food Quality 83(1): 2836.

    • Search Google Scholar
    • Export Citation
  • Jakubska-Busse, A., Malicka, M. and Malicki, M. (2006): New data on the apophytic occur-rence of Epipactis helleborine (L.) Crantz and Cephalanthera longifolia (L.) Fritsch in Populus ×canadensis plantation in Lower Silesia (south-western Poland).–Biodiv.: Res. Conserv. 1–2: 9698.

    • Search Google Scholar
    • Export Citation
  • Legendre, P. and Anderson, M. J. (1999): Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments.–Ecol. Monogr. 69: 124.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lorenz, R. (2005): Zur Artengruppe von Epipactis helleborine (Orchidaceae) in Südtirol.–Gredleriana 5: 103134.

  • Molnár V., A., Vidéki, R. and Vlčko, J. (1998): Adatok hazai Epipactis-fajok ismeretéhez. II.–Kitaibelia 3(2): 287289.

  • Molnár V., A. (2011): Magyarország orchideáinak atlasza. – Kossuth Kiadó, Budapest, 504 pp.

  • Nagy, T. (2015): Néhány florisztikai adat Kötcse környékéről (Dél-Dunántúl, NyugatKülső-Somogy).–Kitaibelia 20(1): 7480.

  • Oksanen, J. et al. (2019): Vegan: community ecology package, ver. 2.5-6. – URL: http://r-forge.rproject.org/projects/vegan/.

  • Rasmussen, H. N. and Whigham, D. F. (1998): The underground phase: a special challenge in studies of terrestrial orchid populations.–Bot. J. Linn. Soc. 126: 4964.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rewicz, A., Jasku, R., Rewicz, T. and Tończyk, G. (2017): Pollinator diversity and reproductive success of Epipactis helleborine (L.) Crantz (Orchidaceae) in anthropogenic and natural habitats.–PeerJ 5: e3159.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • R Core Team (2019): R: A language and environment for statistical computing. – R Foundation for Statistical Computing, Vienna, Austria. URL: http://www.R-project.org/.

    • Search Google Scholar
    • Export Citation
  • Schiebold, J. M. I., Bidartondo, M. I., Karasch, P., Gravendeel, B. and Gebauer, G. (2017): You are what you get from your fungi: nitrogen stable isotope patterns in Epipactis species.–Ann. Bot. 119: 10851095.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Shefferson, R. P., Kull, T. and Tali, K. (2008): Mycorrhizal interactions of orchids colonizing Estonian mine tailings hills.–Amer. J. Bot. 95: 156164.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Somlyay, L., Makádi, S. and Csábi, M. (2016): Adatok Budapest környéke flórájának ismeretéhez II.–Kitaibelia 21(1): 3350.

  • Squirrell, J., Hollingsworth, P. M., Bateman, R. M., Tebbitt, M. C. and Hollingsworth, M. L. (2002): Taxonomic complexity and breeding system transitions: conservation genetics of the Epipactis leptochila complex (Orchidaceae).–Mol. Ecol. 11: 19571964.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sulyok, J. and Molnár V., A. (1998): Az Epipactis pontica Taubenheim Magyarországon.–Kitaibelia 1: 6670.

  • Süveges, K., Löki, V., Lovas-Kiss, Á., Ljubka, T., Fekete, R., Takács, A., Vincze, O., Lukács, B. A. and Molnár V., A. (2019): From European priority species to characteristic apophyte: Epipactis tallosii (Orchidaceae).–Willdenowia 49(3): 401409.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Tamás, J. (2003): The history of Austrian pine plantations in Hungary.–Acta Bot. Croat. 62(2): 147158.

  • Taylor, D. L. and Bruns, T. D. (1999): Population, habitat and genetic correlates of mycorrhizal specialization in the ‘cheating’ orchids Corallorhiza maculata and C. mertensiana.–Mol. Ecol. 8: 17191732.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Těšitelová, T., Těšitel, J., Jersáková, J., Rihová, G. and Selosse, M.-A. (2012): Symbiotic germination capability of four Epipactis species (Orchidaceae) is broader than expected from adult ecology.–Amer. J. Bot. 99: 10201032.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Timpe, W. (1995): Orchideen im südlichen Burgenland (IX). Epipactis (Stendelwurz)-Neufunde im Günser Gebirge.–Burgenländ. Heimatbl. 57: 125131.

    • Search Google Scholar
    • Export Citation
  • Timpe, W. and Mrkvicka, A. Ch. (1996): Beiträge zur Morphologie, Ökologie und Verbreitung von Epipactis nordeniorum, E. pontica und E. albensis in Südost-Österreich.–Florae Austr. Nov. 4: 110.

    • Search Google Scholar
    • Export Citation
  • Tranchida-Lombardo, V., Cafasso, D., Cristaudo, A. and Cozzolino, S. (2011): Phylogeo-graphic patterns, genetic affinities and morphological differentiation between Epipactis helleborine and related lineages in a Mediterranean glacial refugium.–Ann. Bot. 107: 427436.

    • Crossref
    • Search Google Scholar
    • Export Citation
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  • Gy. BORBÉLY (Debrecen)
  • A. ČARNY (Ljubljana)
  • A. CSERGŐ (Dublin)
  • B. CZÚCZ (Paris)
  • M. HÖHN (Budapest)
  • K. T. KISS (Budapest)
  • A. KUZEMKO (Uman)
  • Z. LOSOSOVÁ (Brno)
  • I. MÁTHÉ (Szeged)
  • E. MIHALIK (Szeged)
  • S. ORBÁN (Eger)
  • R. PÁL (Butte)
  • Gy. PINKE (Mosonmagyaróvár)
  • T. PÓCS (Eger)
  • K. PRACH (České Budejovice)
  • E. S. RAUSCHERT (Cleveland)
  • E. RUPRECHT (Cluj Napoca)
  • G. SRAMKÓ (Debrecen)
  • A. T. SZABÓ (Veszprém)
  • É. SZŐKE (Budapest)
  • B. TOKARSKA-GUZIK (Katowice)
  • B. TÓTHMÉRÉSZ (Debrecen)
  • P. TÖRÖK (Debrecen)

Botta-Dukát, Zoltán
E-mail: botta-dukat.zoltan@okologia.mta.hu

or

Lőkös, László
E-mail: acta@bot.nhmus.hu
Institute: Botanical Department, Hungarian Natural History Museum
Address: Könyves K. krt. 40. H-1097 Budapest, Hungary

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2021  
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Scimago  
Scimago
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23
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0,392
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Ecology, Evolution, Behavior and Systematics (Q3)
Scopus  
Scopus
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2,5
Scopus
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Plant Science 205/482 (Q2)
Ecology, Evolution, Behavior and Systematics 322/687 (Q2)
Scopus
SNIP
1,046

2020  
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19
Scimago
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0,417
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Plant Science Q2
Ecology, Evolution, Behavior and Systematics Q3
Scopus
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155/89=1,7
Scopus
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Plant Science 221/445 (Q2)
Ecology, Evolution, Behavior and Systematics 374/647 (Q3)
Scopus
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260
Scopus
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22
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36%

 

2019  
Scimago
H-index
17
Scimago
Journal Rank
0,404
Scimago
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Plant Science Q2
Ecology, Evolution, Behavior and Systematics Q3
Scopus
Cite Score
164/91=1,8
Scopus
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Plant Science 209/431 (Q2)
Ecology, Evolution, Behavior and Systematics 358/629 (Q3)
Scopus
SNIP
0,699
Scopus
Cites
215
Scopus
Documents
23
Acceptance
Rate
30%

 

Acta Botanica Hungarica
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Acta Botanica Hungarica
Language English
French
German
Russian
Spanish
Size B5
Year of
Foundation
1954
Volumes
per Year
1
Issues
per Year
4
Founder Magyar Tudományos Akadémia
Founder's
Address
H-1051 Budapest, Hungary, Széchenyi István tér 9.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
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Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 0236-6495 (Print)
ISSN 1588-2578 (Online)

 

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