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Folia Geobotanica

, Volume 52, Issue 3–4, pp 433–442 | Cite as

Accounting for clonality in comparative plant demography – growth or reproduction?

  • Zdeněk Janovský
  • Tomáš Herben
  • Jitka Klimešová
Article

Abstract

Clonal growth occurs in a high proportion of herbaceous plant species, but it is difficult to deal with in demographic transition matrix models. It is primarily a growth process, but in many cases gives rise to new individuals from the viewpoint of plant demography. In the present contribution, we review how clonality is treated in existing demographic studies of clonal species from the Central European flora. We based our analyses on publicly accessible data in the COMPADRE and CLO-PLA databases and compiling from these information on plant matrix population models (hereafter MPMs) and clonal traits. Out of the 55 species × study combinations of species with known clonality, ca 30% neglect clonality. Another 30% treat clonal growth as growth of mother ramet and only the remaining 40% address clonality as a separate reproductive pathway. However, but only about half of these studies (12; 22% of total) reported a separable submatrix of clonal transitions necessary for comparative analyses. Here we show that failure to report clonal transitions separately leads to a serious bias in estimation of many demographic characteristics derived from MPMs, such as generation time. Shoot ontogeny (namely shoot lifespan and its branching architecture) largely determined whether clonality was neglected, treated as growth or treated as reproduction. Additionally, species with long runners were under-represented in demographic studies relative to their proportion in the Central European clonal flora. To conclude, we discuss how to construct MPMs for species with varying degree of ramet integration. We recommend that demographic analyses should focus on ramets – the smallest unit capable of living through all life-cycle stages of the species – as a sampling and study unit of plant populations.

Keywords

CLO-PLA COMPADRE Cyclicity Population projection matrix Ramet Shoot lifespan Shoot ontogeny 

Introduction

Plant population biology bridges the gap between our understanding of individual drivers of plant life transitions and large-scale analyses of population responses to environment conditions (Caswell 2001; Adler et al. 2014; Salguero-Gómez et al. 2016). An important advantage of demographic analysis is the ability to capture the richness of life histories in a framework of transition matrix population models (hereafter MPMs) allowing comparative analyses (Silvertown et al. 1993; Ehrlén and Lehtilä 2002; García et al. 2008; Salguero-Gómez et al. 2016). Such analyses have benefited from the release of the COMPADRE database, which summarizes data from 819 published demographic studies of 695 species worldwide (version 4.0.1; Salguero-Gómez et al. 2015).

However, the incorporation of plant clonality into MPMs is challenging in many species, since new individuals in the population of a clonal species may arise both by generative reproduction and clonal growth. Clonal growth can gives rise to new rooting units (daughter ramets; Harper 1977), which may potentially become independent (see Klimeš et al. 1997 for a review). Since daughter ramets can at least potentially undergo all life-cycle transitions, an individual of clonal plant species consisting of two ramets needs to be seen as two individuals (albeit genetically identical) from the viewpoint of plant demography. Thus, clonality constitutes an important axis of variation of perennial herb life histories (Aarssen 2008; Klimešová et al. 2015) and its effects on plant population dynamics are likely to be profound (Söyrinki 1938; Herben et al. 2015).

Plant demographers have utilized several approaches for incorporation of clonal growth into MPMs. Some consider clonality negligible and do not include daughter ramet production into MPM (compare Fig. 1ab). Alternatively, daughter ramets may be considered a part of mother ramet size and contribute to criteria used for delimitation of life-cycle stages (Fig. 1c). Finally, clonality may be recorded as production of new demographic individuals similar to generative reproduction. Clonal growth transitions may be either summed up with individual development transitions (Fig. 1d) or the whole MPM may be reported as a set of three distinct submatrices of transitions (as indicated by different fonts in Fig. 1a).
Fig. 1

Representations different approaches to including clonality in MPM for a hypothetical clonal plant species. a – The actual species’ life cycle – two separate reproduction pathways, a matrix comprises of three submatrices of transitions: individual development (plain), generative reproduction (italics) and clonal growth (bold); b – Model, where clonal growth is considered negligible or ignored by the author; c – Clonal growth modelled as changes in mother ramet size (sampling unit is a clump of ramets contrary to a single ramet in a, b, d); d – Clonal growth added to individual development transitions (mmissing clonal submatrix). Empty cells denote impossible transitions (i.e. structural zeros). Abbreviations: sdl – seedling; veg – vegetative, single ramet; flow – flowering, single ramet; veg2+ –vegetative, two or more ramets; flo2+ – flowering, two or more ramets.

The aim of this paper is to review the ways in which clonal growth has been included in matrix population models and discuss what consequences this may have for comparative demographic analyses. We end up by presenting some recommendations about the way clonal growth should be considered in studies of plant demography. We focused our analysis on Central European flora, because there is detailed knowledge of clonal species and their traits in this flora and demography of a number of clonal species from this flora has been studied as well. As a part of our analysis, we also determined proportional representation of different types of clonal growth among available studies given that some types are more challenging to study than others.

Material and Methods

To conduct this analysis we excerpted from the comprehensive COMPADRE 4.0.1 database of MPMs all studies focusing on clonal species listed in the CLO-PLA database (version 3.0; Klimešová et al. 2017), which covers complete Central European flora with exception of geographically limited apomictic taxa (e.g. Rubus sp. div.). Having compiled this list, we then reviewed the original studies to determine how (or if) they had included clonality in the MPM construction.

We focused on five key traits related to clonality: mean annual daughter ramet production (a measure of clonal growth rate), extent of lateral spread (i.e. length of spacers), persistence of clonal connections for more than one season as well as bud bank size and depth. The last two are proxies of potential for clonal growth in response to disturbance or injury. All clonal traits except for persistence (0/1 variable) were log-transformed prior to all analyses.

This search resulted in a set of 47 species from 45 studies covering only 3.2% of 1,486 Central European clonal species. For some species, there were data by different authors (who often treat species’ clonality differently) yielding 55 species × study combinations, which we take as a unit for analysis and discussion. We do not take into account the phylogenetic structure of the data, as we were studying coverage of clonal species trait-space (i.e. representativeness of sampling of clonal species for demographic studies) and not evolutionary relationships.

Results and discussion

How is clonality incorporated into MPMs

Our search revealed that in about 32% of species × study combinations (18 out of 55; Table 1), the authors did not consider clonality in MPM construction claiming that the species was not clonal or exhibited clonal growth only very rarely. While this is reasonable in some species (e.g. Corallorhiza trifida or Epipactis atrorubens; Iriondo et al. 2009; Jäkäläniemi et al. 2011), an important life-cycle process may be omitted in others. For example, the seedlings and daughter ramets formed from frequently produced bulbils were not distinguished in the study of three species of genus Pinguicula (Svensson et al. 1993). Failure to distinguish clonal growth from generative reproduction of the species precludes any assessment of their relative roles.
Table 1

Summary of how clonal growth is treated in published demographic studies of Central European clonal species

Species

Treatment of clonality

Shoot ontogeny type

Reference

Actaea spicata L.

1

S-mono

Fröberg and Eriksson 2003

Agrimonia eupatoria L.

1

S-mono

Kiviniemi 2002

Allium vineale L.

1

S-mono

Burns et al. 2013

Anthericum liliago L.

3

S-poly

Černá and Münzbergová 2013

Anthericum ramosum L.

3

S-mono

Černá and Münzbergová 2013

Artemisia genipi Weber ex Stechm.

2

S-poly

Marcante et al. 2009

Aster amellus L.

3

S-poly

Münzbergová 2007

Bothriochloa ischaemum (L.) Keng

2

S-mono

Gabbard 2003

Carex bigelowii Torr. ex Schwein.

3s

S-poly

Carlsson and Callaghan 1991

Centaurea jacea L.

3s

S-mono

Jongejans and de Kroon 2005

Chaerophyllum aureum L.

1

S-mono

Magda et al. 2004

Cirsium acaule (L.) A.A.Weber ex Wigg.

3

S-poly

Münzbergová 2005

Cirsium dissectum (L.) Hill

3s

S-poly

Jongejans et al. 2008

Cirsium pannonicum (L.f.) Link

3

S-poly

Münzbergová 2005

Colchicum autumnale L.

3s

S-poly

Winter et al. 2014

Corallorhiza trifida Châtel.

1

S-mono

Iriondo et al. 2009

Cypripedium calceolus L.

2

S-mono

García et al. 2010

Cypripedium calceolus L.

2

S-mono

Nicolé et al. 2005

Epipactis atrorubens (Hoffm.) Besser

1

S-mono

Jäkäläniemi et al. 2011

Eryngium maritimum L.

1

S-poly

Curle et al. 2004

Fritillaria meleagris L.

1

S-mono

Zhang and Hytteborn 1985

Geranium sylvaticum L.

2

S-poly

Ramula et al. 2007

Geum reptans L.

2s*

M

Weppler et al. 2006

Geum rivale L.

3

M

Kiviniemi 2002

Himantoglossum hircinum (L.) Spreng.

1

S-mono

Pfeifer et al. 2006

Hypochaeris radicata L.

3s

S-poly

Jongejans and de Kroon 2005

Lathyrus vernus (L.) Bernh.

1

S-mono

Ehrlén 1995

Molinia caerulea (L.) Moench

2

S-mono

Jacquemyn et al. 2005

Narcissus pseudonarcissus L.

3

M

Barkham 1980

Orchis purpurea Huds.

1

S-mono

Jacquemyn et al. 2010

Oxalis acetosella L.

3s

M

Berg 2002

Pinguicula alpina L.

1

S-poly

Svensson et al. 1993

Pinguicula villosa L.

1

S-mono

Svensson et al. 1993

Pinguicula vulgaris L.

1

S-mono

Svensson et al. 1993

Poa alpina L.

2s*

S-poly

Marcante et al. 2009

Potentilla anserina L.

3s

M

Eriksson 1988

Primula elatior (L.) Hill

2

S-poly

Jacquemyn and Brys 2008

Primula farinosa L.

3

S-poly

Lindborg and Ehrlén 2002

Primula veris L.

3

S-poly

Ehrlén et al. 2005

Primula veris L.

2

S-poly

Jacquemyn et al. 2012

Primula veris L.

3

S-poly

Lehtilä et al. 2006

Primula veris L.

2

S-poly

Brys et al. 2005

Primula veris L.

2

S-poly

Endels et al. 2005

Primula vulgaris Huds.

2

S-poly

Valverde and Silvertown 1998

Primula vulgaris Huds.

2

S-poly

Endels et al. 2007

Ranunculus acris L.

3s

S-poly

Sarukhán and Harper 1973

Ranunculus bulbosus L.

1

S-poly

Sarukhán and Harper 1973

Ranunculus repens L.

3s

S-poly

Sarukhán and Harper 1973

Sanicula europaea L.

3

S-poly

Gustafsson et Ehrlén 2003

Saxifraga cotyledon L.

3s

S-poly

Dinnétz and Nilsson 2002

Senecio jacobaea Gaertn.

2

S-poly

Forbes 1977

Succisa pratensis Moench

1

M

Mildén et al. 2006

Succisa pratensis Moench

3s

M

Jongejans and de Kroon 2005

Succisa pratensis Moench

1

M

Wallin and Svensson 2012

Trollius europaeus L.

3s

S-poly

Lemke and Salguero-Gómez 2016

Coding for treatment of clonality: 1 – clonality neglected, sampling unit shoot; 2 – daughter ramet part of mother ramet size, sampling unit group of shoots; 3 – clonality treated explicitly, sampling unit shoot; s – clonal submatrix separable from reported transition matrices. Shoot ontogeny type coded as: S-mono – sympodial branching, monocyclic shoots; S-poly – sympodial branching, polycyclic shoots; M – monopodial branching. Full citations for references are given in the Electronic Supplementary Material

Footnotes:

Clonal offspring mixed with generative offspring

* One form of clonal reproduction (daughter rosettes) treated as part of mother ramet size, another (bulbils, stolons) treated production of new individuals

In 15 species × study combinations (ca 27%), clonality was modelled as a part of the mother ramet size. This was common among species with short spacers between daughter and mother ramets (e.g. Geum reptans, Primula veris; Brys et al. 2005; Weppler et al. 2006). While this approach may be appropriate for modeling short-term population dynamics, it may produce errors as the distance between ramets often increases over time due to lateral growth and ramets become independent of each other (Fig. 2). How clonality is included in mother ramet size may also differ among studies, which creates challenges for comparative analyses (e.g. consider different possible delimitations of individuals in Fig. 2 top right).
Fig. 2

Clonal growth of species with different type of branching and shoot ontogeny type. Individuals are depicted in three successive time intervals (seasons) and all reproduce clonally in the second season (t2). Shoots and rhizomes are coloured according to the season of origin of a given module. Line and arrow types suggest possible ascriptions of shoots to individuals – see text for a more detailed explanation.

The remaining 22 species×study combinations (40%) recognise clonal formation of daughter ramets as an important separate process and the ramet was defined as a single shoot/ramet. However, only 12 species×study combinations report clonal reproduction in the form of a separable submatrix of clonal transitions. MPMs with inseparable submatrix of clonal transitions provide correct estimates of asymptotic population growth (λ), but other demographic characteristics are biased (e.g. generation time, survivorship function; see Cochran and Ellner 1992; Caswell 2001). This can be demonstrated by considering how generation time differs if it is estimated from a matrix with clonal transitions treated as a part of reproduction or wrongly from a matrix including clonal growth with individual development transitions (Fig. 3). Failing to treat clonal submatrix as new ramet production increases estimates of plant survival and leads to inflation of generation time on average by a factor of 2.64 (i.e. by 164%; P < 0.001; 95% CI = 1.78–3.93).
Fig. 3

Boxplots of generation times of 19 clonal plant species with clonal submatrices available (either from COMPADRE database or constructed from data provided in original articles). For each species, clonal submatrix either was left added up with individual development transitions (C-not accounted) or separated and treated as part of the reproduction (C-accounted). Please note that the y-axis is logarithmic.

Influence of shoot ontogeny type on clonal growth representation in MPMs

The parameters of an MPM highly depend on the demographer’s choice of sampling unit of a population of clonal species. For example in tussock-forming species, an individual can be defined as a single shoot or as a group of tightly-packed stems resulting in very different MPMs. Single shoots as sampling units seem to be more suitable for comparative analyses, because they are homologous across plant species. However, use of a single shoot has also two drawbacks. First, it may not correspond to an independent ramet, e.g. in species with multiple shoots and a single taproot such as Scorzonera humilis (Colling and Matthies 2004) or in species with strong shoot differentiation such as Carex bigelowii (Carlsson and Callaghan 1990). Second, shoot ontogeny type determines to a large degree the dynamics of shoot turnover, i.e. emergence, growth and flowering mortality (Serebriakova 1977).

Serebriakova (1977) defined three major types of shoot ontogeny (Fig. 2): (i) sympodially branching plants with annual shoots (16 species in our dataset; hereafter monocyclic species; terminology follows Klimešová et al. 2016), (ii) sympodially branching plants with long-lived shoots (24 species; hereafter polycyclic species), and (iii) monopodially branching plants with long-lived repeatedly flowering shoots (6 species; hereafter monopodial species). In monocyclic species, there is no continuity between the shoots in successive seasons. The belowground structure of rhizomes supporting the observed annual shoots typically remains unknown (Fig. 2a) and shoots need to be ascribed to demographic individuals more or less arbitrarily. Growth, survival and clonal reproduction of ramets of species with monocyclic shoots depends largely on how shoots are connected to ramets across seasons. Ascribing shoots to ramets is easier in species where new shoots appear close to the previous year’s shoot whereas species with new shoots emerging further away (e.g. Anemone nemorosa) are less likely to be studied due to challenge of shoot ascription.

On the contrary, the long-lived shoots of polycyclic species have well-defined year-to-year growth, survival and reproduction transitions from the demographer’s viewpoint. Shoot generations overlap with the younger shoots gradually replacing dead flowering shoots (in sympodially branching species, shoots die after flowering, since apical meristem differentiated into flowers). The majority of authors treats replacement by a younger shoot as continuation of the same ramet and so considers the two shoots as a single ramet (dashed line in Fig. 2b, Table 2). A minority of authors defines each shoot as a separate ramet and does not allow retrogression of flowering plants to vegetative stages (e.g. Carlsson and Callaghan 1991; Jongejans et al. 2008; dotted and dotted-and-dashed lines in Fig. 2b). The importance of clonal growth for population dynamics is inevitably higher under the second approach. A complete concordance between shoot census and ramet vital rates occurs only in monopodial species, where shoots can undergo multiple reproductive events and they can be identified as ramets without doubt (Fig. 2c – individuals depicted by different line types).
Table 2

Frequency of approaches to treatment of clonality in demographic models in relation to the study species shoot ontogeny type (data based on Table 1)

Treatment of clonality

Shoot ontogeny type

Monocyclic

Polycyclic

Monopodial

Clonality neglected

12

4

2

Clonal offspring part of mother ramet size

4

10

1

Clonality treated explicitly

2

15

5

χ2-test: P < 0.001, d.f. = 2, monopodial species not included into the test due to lack of data

The decreasing (monopodial > polycyclic > monocyclic species) linkage between shoots and ramet vital rates translates into different ways how researchers treated clonal growth in demographic studies (Table 2). Clonality of monocyclic species is generally neglected in demographic analyses, while the overlapping ‘shoot generations’ of polycyclic species tend to be treated as a part of mother ramet size. Both in monocyclic and polycyclic clonal species (but not in monopodial), it is necessary to understand the connections between shoot dynamics and the dynamics of belowground structures to meaningfully delimit ramets for comparative analyses.

Are clonal species studied by demographers representative of the whole set of clonal species?

We used principal component analysis to summarise main gradients of variation among 1485 clonal species from Central Europe included in the CLO-PLA database. Into the resulting trait space, we projected which species have already been studied for their demography. The main gradients of clonal species trait variation were (i) extent and stability of below-ground structures (38.1% of total clonal trait variation) and (ii) intensity and spatial extent of clonal growth (additional 25.6% of variation). Species with studied demography were well represented along the first ordination axis, but less so along the second axis (Fig. 4). Univariate tests (Table 3) indicated that demographic studies were done on species with daughter ramets that appeared at shorter distances (geometric mean: 2.26 cm, 95% CI = 1.24–4.13), than the species that were not studied (4.84 cm, 95% CI = 4.34–5.39). This bias in selection of species for demographic analyses possibly reflects difficulties with tracking individuals in species (especially monocyclic) with long spacers (Fig. 2a; Klimešová et al. 2011). Studying the demography of clonal species with MPMs seems difficult, given that only 3.2% (47 out of 1,486) Central European clonal species have been used for such analysis, compared to 6.4% (43 out of 670) of non-clonal perennials studied (χ2-test, P < 0.001, d.f. = 1). The under-representation of clonal species in demographic analyses compared to non-clonal species is even more striking given that MPMs of only 22% of studied clonal species are reported in a way suitable for comparative analyses (i.e. clonality treated as a reproductive pathway separable into a distinct submatrix).
Fig. 4

Ordination diagram of principal component analysis of centred and scaled clonal traits; filled circles and shaded envelope indicate species with demographic data available, open circles indicate clonal species with no demographic data available. Arrows indicate relationship of clonal traits to each axis: connect. Persistence – persistence of clonal connections for > 1 year; bud bank size – mean number of buds; bud bank depth – mean depth of bud bank; ramet lateral spread – mean distance of mother and daughter ramet; daughter ramet production – mean number of daughter ramets produced per established individual and season. Data for clonal traits from CLO-PLA; analysis was undertaken in CANOCO 5 (ter Braak and Šmilauer 2012).

Table 3

Results of univariate tests of whether specific clonal traits differed between species used for demographic studies (listed in Table 1) and those not studied (using data from CLO-PLA)

Clonal trait

Resid. d.f.

i value

P-value

ramet lateral spread

1,442

5.96

0.015

bud bank size

1,483

1.18

n.s.

bud bank depth

1,473

0.05

n.s.

daughter ramet production

1,411

2.34

n.s.

persistence of clonal connections

1,434

n.s.

All response variables were log-transformed prior to analyses, except persistence of clonal connections, which was analysed by binomial generalised linear model due to its binary nature

How to overcome existing drawbacks and use existing data as much as possible

Our analysis revealed three main factors limiting the use of a MPM for comparative demographic analyses: i) clonality is neglected in MPM construction; (ii) clonality is treated only as part of individuals growth and not reproduction; (iii) clonal growth transitions are recognised as an alternative reproductive pathway but not reported in a separable submatrix. However, such MPMs can often still be used for some comparisons albeit more limited. Species whose clonality was neglected in MPM assembly cannot be used for any assessment of role on clonality in their life cycle, but the MPMs can be used for predictions of population growth/shrinkage for species, which reproduce clonally only rarely (e.g. orchids in our dataset).

Treatment of clonality as a growth process (i.e. including it into stage definitions) allows the use of MPMs for most tasks of short-term population modelling (e.g. in nature conservation). The drawbacks of such an approach become apparent at time scales over which sampled individuals consisting of clonally formed groups of ramets start to disintegrate or if more species with different growth forms are to be compared. Many of the population models in the studies we have reviewed could be relatively easily reworked to allow for comparative analyses by decoding clonality from stage classes and by treating retrogressions of flowering shoots of polycyclic species as clonal growth.

In contrast to the treatment of clonality as growth, treating clonality as a specific type of reproduction, but without a separable submatrix, provides correct estimates of population growth rates (λ), elasticities of λ to individual transitions and allows comparative analyses concerning the role of generative reproduction. On the other hand, age-based population characteristics are likely to be seriously biased (Fig. 3).

How to define demographic individuals in clonal plant species

The frequency of recording species life-cycle into MPM with clonality as reproduction and in a separable submatrix was higher in polycyclic species, whereas monocyclic species were much more likely to be recorded with neglected clonality (Table 2). This leads to a serious limitation for comparative analyses, because to date demographic analyses have been done (or made accessible) for only a single monocyclic species, eight polycyclic and three monopodial species; a very small proportion of the 1,485 clonal species in the Central European flora. Clearly, one of the main obstacles hampering demographic studies of clonal species is the problem of defining an individual, which is especially pronounced in monocyclic species (Fig. 2). In many cases, especially in situations where ramets of multiple genetic individuals mix together, it may not be possible to distinguish individuals without genotyping individual ramets (Widén et al. 1994; Suzuki et al. 1999; Jacquemyn et al. 2005; Honnay et al. 2006).

We have argued that treating shoots as individuals is preferable for comparative demographic studies for clonal species, because shoots (and corresponding belowground structures) of most species conform to the definition of ramet proposed by Harper (1977), i.e. structures that can potentially live through all life-cycle stages of the species. However, this may not hold true for some tussock plants (Wikberg and Svensson 2006), or species possessing extensive rhizomatous system (Carlsson and Callaghan 1990; Ott and Hartnett 2015), where ramet integration through belowground structures is very strong. For such species, we suggest that ramets be defined as the smallest multi-shoot integrated units conforming to the above-mentioned definition.

Although ca 73% of Central European clonal species forms between-ramet connections persisting for more than one season, we hypothesise that majority of these species with persistent connections do not exhibit the extreme ramet integration mentioned above. We suppose that possible milder integration of ramets of these species translates into differences among transition rates of the connected ramets (e.g. due to their position within the tussock; Münzbergová et al. 2005). MPMs are very well suited to evaluate impacts of such ramet integration on population performance (e.g. by defining separate stages for each ramet type).

Conclusion

Clonal growth can be treated as growth of the mother ramet, or in case of species exhibiting clonality only very rarely, it can be ignored in construction of matrix population models. However, if we aim to ask general questions about the role of clonality in plant demography, then clonal growth must be treated as a reproductive pathway analogous to generative reproduction, because it typically gives rise to new potentially independent demographic individuals. Only some 22% of analysed studies could be used for such comparative analyses without changes. This both limits evaluation of the role of clonality in population dynamics and contributes to strong under-representation of clonal species in existing plant demographic studies. Finally, shoot ontogeny type of the clonal species is a trait, which should be taken into account when designing demographic studies, because monocyclic shoot ontogeny type makes mistreatments of clonality more possible.

Notes

Acknowledgements

We thank Kay Gross for her valuable comments on the previous versions of manuscript. The research reported here was supported by grants from the Czech Science Foundation (16-19245S, Centre of Excellence 14-36079G PLADIAS).

Supplementary material

12224_2017_9301_MOESM1_ESM.doc (37 kb)
ESM 1 (DOC 37 kb)

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© Institute of Botany, Academy of Sciences of the Czech Republic 2017

Authors and Affiliations

  1. 1.Department of Botany, Faculty of ScienceCharles UniversityPraha 2Czech Republic
  2. 2.Institute of BotanyAcademy of Science of the Czech RepublicPrůhoniceCzech Republic
  3. 3.Institute of BotanyAcademy of Science of the Czech RepublicTřeboňCzech Republic

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