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4 September 2021

The Epipactis helleborine Group (Orchidaceae): An Overview of Recent Taxonomic Changes, with an Updated List of Currently Accepted Taxa

,
,
and
1
Department of Botany, Faculty of Biological Sciences, University of Wroclaw, 50-328 Wroclaw, Poland
2
Institute of Environmental and Agricultural Biology (X-BIO), Tyumen State University, 625003 Tyumen, Russia
3
Joint Directorate of the Mordovia State Nature Reserve and National Park “Smolny”, 430005 Saransk, Russia
*
Authors to whom correspondence should be addressed.
Plants2021, 10(9), 1839;https://doi.org/10.3390/plants10091839
This article belongs to the Special Issue Advance in Orchidaceae Research
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Abstract

The Epipactis helleborine (L.) Crantz group is one of the most taxonomically challenging species complexes within the genus Epipactis. Because of the exceptionally high levels of morphological variability and the ability to readily cross with other species, ninety different taxa at various taxonomic ranks have already been described within its nominative subspecies, but the taxonomic status of most of them is uncertain, widely disputed, and sometimes even irrelevant. The present review is based on results of the most recent research devoted to the E. helleborine group taxonomy. In addition, we analysed data about taxa belonging to this group presented in some research articles and monographs devoted directly to the genus Epipactis or to orchids in certain area(s). Based on the reviewed literature and data collected in four taxonomic databases available online, we propose an updated list of the 10 currently accepted taxa in the E. helleborine group (two species, six subspecies, and two varieties), which includes E. helleborine (L.) Crantz subsp. helleborine; E. helleborine subsp. bithynica (Robatsch) Kreutz; E. helleborine subsp. distans (Arv.-Touv.) R.Engel and P.Quentin; E. helleborine subsp. neerlandica (Verm.) Buttler; E. helleborine var. tangutica (Schltr.) S.C.Chen and G.H.Zhu; E. helleborine subsp. tremolsii (Pau) E.Klein; E. helleborine subsp. voethii (Robatsch) Jakubska-Busse, Żołubak, and Łobas, stat. nov.; E. condensata Boiss. ex D.P.Young; E. condensata var. kuenkeleana (Akhalk., H.Baumann, R.Lorenz, and Mosul.) Popovich; and E. cupaniana C.Brullo, D’Emerico, and Pulv.

1. Introduction

The long and turbulent history of changes in taxonomy of the genus Epipactis Zinn, 1757 (Orchidaceae) is well documented [1,2,3,4,5,6,7,8,9,10,11,12]. The most widely contested aspect of its taxonomy is whether to treat many of its morphologically different but poorly defined taxa as new species or if is more appropriate to transfer some of them to lower taxonomic ranks, such as subspecies, variety, or form [13,14]. The currently adopted classification system of Epipactis does not take sufficient account of the variation range of morphological characters within its taxa, nor does it explain the underlying sources of this variability. Moreover, the species delimitation within Epipactis is often complicated by the ease with which the interspecific hybrids are formed in the locations inside the native ranges of the parental species, the existence of which is a common cause of taxa misidentification [15,16,17,18,19,20,21]. The fluidity of the morphological boundaries between various Epipactis species causes serious difficulties in determinig the diagnostic characters useful in species identification [22,23,24]. As a result, there is still no official account of the species included within the genus Epipactis. The estimates range from a few to several dozen depending on the source (e.g., [6,17,25,26,27,28,29,30,31,32,33,34,35,36,37,38]).
The primary aim of taxonomic research is to provide a comprehensive classification system, which reflects the observed relationships between the taxa at the morphological, geographical, and genetic levels [39]. The major impediment in achieving a taxonomic consensus within the genus Epipactis is its exceptionally high morphological variability, which is still insufficiently documented and requires further clarification [11,14]. The main source of this variability, referred to the phenotypic plasticity, is manifested in natural populations of many Epipactis species through the slight differences observed in the vegetative (e.g., shoots and leaves) and generative (i.e., flowers and their separate elements) parts of the individual plants [4,15,40,41,42]. This broad spectrum of morphological variation also provided a wide range of characters that delimitate and group the species within the genus Epipactis over the past few decades (e.g., [14,17,21,23,28,29,30,31,32,43,44,45,46,47,48,49,50,51,52,53,54]). As a consequence, a large number of morphologically similar species and infraspecific taxa (i.e., subspecies, varieties, or forms), usually of local or narrowly restricted occurrence, have been described within Epipactis [17,23,31,55]. However, the taxonomy and systematic position of the majority of these taxa are still not well understood and highly debated [4,11,13,24,42,56,57,58,59].
One of these taxonomically problematic species is Epipactis helleborine (L.) Crantz, native to Eurasia and North Africa and widely naturalised in North America [27,31,32,58,60]. It is a common cross-pollinating (allogamous) orchid species with a very wide ecological amplitude. It grows in areas with nutrient rich soils and a broad pH spectrum (usually in alkaline conditions) and, unlike the other species of Epipactis, has a highly variable habitat preference. Its natural populations are usually found in forests, amongst shrubs, or in partly disturbed vegetation sites, ranging from lowland floodplains to mountain spruce forests up to the altitude of 2200 m a.s.l. [31,37,51,52,53,61,62,63]. It is also increasingly observed in the areas strongly impacted by human activity, such as roadsides, cemeteries, railway embankments, gravel pits, gardens, and urban parks [64,65].
The recently increased interest in the evolutionary history of the genus Epipactis has resulted in some significant changes in its taxonomy [11]. The most important and widely challenged one of them is considered the present division of this genus into nine morphologically distinct species complexes [66,67,68,69]. Among them, there is also a group devoted to E. helleborine, for which the circumscription has already been reorganized by numerous scientists [3,5,8,10,17,23,30,31,47,70,71]. Interestingly, the taxonomic status of individual taxa included in this group is still chaotic and in need of clarification.
Because of the general confusion concerning the taxonomy of the genus Epipactis, caused mainly by the frequent changes in its infrageneric classification, we aimed to present here an updated list of the 10 currently accepted taxa included in the E. helleborine group. As a decisive criterion for the selection of individual taxa to our circumscription, we used the results of recent genetic and morphometric analysis in relation to the total 41 taxa that have been included in this group.

2. Recent Taxonomic Publications Devoted to the Epipactis helleborine Group

So far, a number of the research articles and monographs have been published by representing the description and taxonomic treatments of taxa of the Epipactis helleborine group [3,5,8,10,17,23,30,31,47,70,71] (see Table 1). At the beginning, Tyteca and Dufrêne [47] conducted the medium-scale biostatistical study of the genus Epipactis focused on only seven allogamous species (autogamous taxa were explicitly excluded) from the south-western limit of its distribution range in Europe. But the authors concluded that at least five species (i.e., E. helleborine s.str., E. distans Arv.-Touv., E. neerlandica (Verm.) Devillers-Tersch. and Devillers, E. tremolsii Pau, and E. lusitanica D.Tyteca) should be included within the E. helleborine group. Tyteca and Dufrêne [47] also used the results of multivariate analysis of 28 carefully chosen characters of floral and vegetative morphology (particularly the differences in the flower structure) to prove that the four taxa included in this group are sufficiently different from E. helleborine s.str. and should be treated as independent species rather than at the subspecific rank.
Table 1. Nomenclatural and taxonomic changes within the Epipactis helleborine group.
Later, the circumscription of the Epipactis helleborine group was delimited by a yet another set of clearly defined morphological characters, including the appearance of the shoot, labellum, ovary, and pedicel. However, the morphometric analysis of these characters was not as detailed as that of the other published taxonomic treatments (e.g., [23,47]). Delforge [30] divided the 23 species belonging to the E. helleborine group into three subgroups, i.e., the E. leptochila subgroup (five taxa), the E. helleborine subgroup (13 taxa), and the E. tremolsii subgroup (five taxa). Within the E. helleborine subgroup, this author included E. helleborine s.str. and 12 other morphologically similar species (Table 1). This subgroup was also further sub-divided into two additional sections: one with the cross-pollinating species and another with autogamous taxa only.
The increase in number of new taxa described within the genus Epipactis has led to some significant changes in its infrageneric classification. As a consequence, two new characters were added by Delforge [17] to the circumscription of the E. helleborine group, i.e., the leaf and the inflorescence morphology. Four of the previously used characters, i.e., the appearance of the shoot, labellum, ovary, and pedicel have also been redefined. Thus, Delforge’s newly circumscribed E. helleborine group included 13 taxa (11 at the rank of species and two varieties). Six of which were included in the author’s previous study [30], where one (i.e., E. helleborine var. youngiana A.J.Richards and A.F.Porter) Kreutz) has changed its taxonomic rank (Table 1).
Subsequently, Brullo et al. [23] have expanded the Epipactis helleborine group by including E. cupaniana C.Brullo, D’Emerico, and Pulv., a newly described endemic from the mesophilous Holm oak woods in north-central Sicily. Their circumscription of the E. helleborine group included 11 additional species and was broadly based on the system proposed by Delforge in 2006 (Table 1). The authors also conducted a morphometric analysis of a broad range of 37 characters of floral and vegetative morphology. The obtained results suggest that E. cupaniana does indeed belong to the E. helleborine group. This taxon is morphologically and karyologically different from E. helleborine s.str. and can be accepted as a separate species. Despite this conclusion, Delforge [31] did not include E. cupaniana in his latest concept of the E. helleborine group.
One year later, in 2014, Epipactis condensata subsp. kuenkeleana (Akhalk., H.Baumann, R.Lorenz, and Mosul.) Kreutz, Fateryga, and Efimov was published as a new combination for the species formerly known as E. viridiflora subsp. kuenkeleana Akhalk., H.Baumann, R.Lorenz, and Mosul. [8], where then Delforge raised this latter taxon to full species status (i.e., E. kuenkeleana (Akhalk., H.Baumann, R.Lorenz and Mosul.) P.Delforge) [72]. Thereafter, E. condensata subsp. kuenkeleana was put into synonymy with the nominative subspecies [10,70]. However, finally, in 2020, plants within the same taxon corresponding to the former subsp. kuenkeleana were considered as a phenotypic form, confined to shady forest communities, and described as E. condensata var. kuenkeleana (Akhalk., H.Baumann, R.Lorenz, and Mosul.) Popovich [70].
The most recent taxonomic treatment of the Epipactis helleborine group in Europe, North Africa, and the Middle East [31], is broadly based on an earlier account by the same author [17] and expands to comprise 17 taxa, five of which are included here for the first time, and one taxon (i.e., E. pontica Taubenheim) which is transferred to E. leptochila group (Table 1).

3. List of Names of Infraspecific Taxa in Epipactis helleborine and its Current Taxonomic Status

The seemingly endless morphological variation observed across the entire distribution range of Epipactis helleborine s.str. is clearly reflected by the list of its infraspecific taxa presented below in Table 2.
Table 2. An overview of names of infraspecific taxa published in Epipactis helleborine.
As it turns out, in the light of the data collected in four taxonomic databases available online [73,74,75,76], as many as ninety morphologically similar taxa have been distinguished within Epipactis helleborine s.str. at various taxonomic ranks since its original description as Serapias helleborine L. by Carl Linnaeus in 1753 [33,77,78,79,80,81,82]. Among these, at the ranks of variety and subspecies have been classified respectively 37 and 36 names of taxa, and at the rank of form, 17 have been classified (Figure 1).
Figure 1. The current status of names of infraspecific taxa published in Epipactis helleborine categorised according to their taxonomic ranks, based on [73,74,75,76]. The number of names synonymised with E. helleborine s.l. and with other species is shown in parentheses.
It should be noted that most of them (64) were synonymised with Epipactis helleborine s.l. almost as soon as they were published and currently only five infraspecific taxa are accepted, i.e., E. helleborine (L.) Crantz subsp. helleborine, E. helleborine subsp. bithynica (Robatsch) Kreutz, E. helleborine subsp. neerlandica (Verm.) Buttler, E. helleborine var. tangutica (Schltr.) S.C.Chen and G.H.Zhu, and E. helleborine subsp. tremolsii (Pau) E.Klein [3,63,71,83,84]. The remaining 26 published names of taxa do not currently have a taxonomic relationship with E. helleborine s.l. (Figure 2).
Figure 2. The current status of names of infraspecific taxa published in Epipactis helleborine, based on [73,74,75,76]. The number of names synonymised with E. helleborine s.l. and to other species is shown in parentheses.

4. Conclusions

Since the genus Epipactis has been divided into several species complexes based on morphological characters, more than forty taxa have been classified into the E. helleborine group (see Table 1). These contain such taxa as E. danubialis Robatsch and Rydlo, E. greuteri H.Baumann & Künkele, E. halacsyi Robatsch, E. leptochila (Godfery) Godfery, E. muelleri Godfery, E. naousaensis Robatsch, E. olympica Robatsch, E. pontica or E. purpurata Sm., which, because of their distinct morphological phenotype, were excluded from it over time and (in some cases) provided a basis for effective distinguishing of other groups. Despite the fact that 15 of these taxa were originally included as separate species, they are being considered currently as three out of the five infraspecific taxa published in E. helleborine (i.e., E. helleborine subsp. helleborine, E. helleborine subsp. neerlandica, and E. helleborine subsp. tremolsii). Furthermore, two other infraspecific taxa have been genetically confirmed as well-founded, i.e., E. helleborine subsp. distans (Arv.-Touv.) R.Engel and P.Quentin and E. helleborine subsp. voethii, although the latter one still has not been officially distinguished at this rank. As it appears, E. bugacensis Robatsch and E. rhodanensis Gévaudan and Robatsch have in fact a similarly close genetic relationship with E. dunensis (T.Stephenson and T.A.Stephenson) Godfery (originally included in the E. helleborine group), which, in our opinion, due to its floral morphologies (typical of autogamous taxa) should not be classified in this group. Although E. nordeniorum Robatsch was for a long time assigned to the E. helleborine group, as a result of recent genetic analysis it turned out to be molecularly similar to E. albensis Nováková and Rydlo, classified in a separate group. Some taxa, such as E. condensata Boiss. ex D.P.Young and E. cupaniana, based on results of a detailed morphological analysis of their floral and vegetative characters, should be retained in the E. helleborine group, although these taxa are still not included there in the most recently published accounts of the genus Epipactis.
The boundaries between individual species within the Epipactis helleborine group are unclear, making it difficult to determine reliable taxonomic characters useful in the construction of an identification key which would be unambiguously interpreted by different users. In the light of the scientific literature published worldwide, especially because of the impact of the genetic research on our current understanding of the boundaries between various species of Epipactis, we think it is appropriate to maintain the E. helleborine group, but we propose to update its circumscription to better reflect the taxonomic changes summarised in Table 1 that have occurred for its individual members over the past few decades.
Our proposed taxonomic circumscription of the Epipactis helleborine group therefore consists of the following only allogamous taxa: E. helleborine subsp. helleborine, E. helleborine subsp. bithynica, E. helleborine subsp. distans, E. helleborine subsp. neerlandica, E. helleborine var. tangutica, E. helleborine subsp. tremolsii, E. helleborine subsp. voethii (Robatsch) Jakubska-Busse, Żołubak, and Łobas, stat. nov., E. condensata, E. condensata var. kuenkeleana and E. cupaniana.
Although the proposed list of taxa in the Epipactis helleborine group seems to be appropriate at the moment, we treat it as legitimate until new methods of genetic and morphometric analysis are developed, which would allow more precise definition of the Epipactis separate species concept in the future.

Proposal of a New Status for Epipactis helleborine subsp. voethii

Epipactis helleborine subsp. voethii (Robatsch) Jakubska-Busse, Żołubak, and Łobas, stat. nov.
Basionym: Epipactis voethii Robatsch, Mitteilungen der Abteilung für Botanik am Landesmuseum Joanneum in Graz 21/22: 22 (1993).
Comments: This subspecies differs from typical Epipactis helleborine s.str. through few developed clinandrium, as well as the slight differences observed in the morphological characters, i.e., the green colour of stems, leaves, and flowers of the individual plants, which are almost lacking in any violet coloration. In the fruiting stage, taxa can be distinguished by the shape of the seeds: in E. helleborine s.str. the seeds are worm-like, and club-shaped in E. helleborine subsp. voethii.

Author Contributions

Conceptualization, Z.Ł. and A.J.-B.; methodology, Z.Ł., E.Ż. and A.J.-B.; investigation, Z.Ł., E.Ż. and A.J.-B.; writing—original draft preparation, Z.Ł., A.K., E.Ż. and A.J.-B.; writing—review and editing, Z.Ł., A.K., E.Ż. and A.J.-B.; visualization, E.Ż. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Publicly available datasets were analysed in this study.

Acknowledgments

The authors wish to thank to Jacek Wajer (Natural History Museum) for improving the English version of the text.

Conflicts of Interest

The authors declare no conflict of interest.

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