Significant Habitat Loss of the Black Vanilla Orchid (Nigritella Nigra S.L

Uniwersytet Gdaski

University of Gdask

https://repozytorium.bg.ug.edu. pl

Significant habitat loss of the black vanilla orchid (Nigritella nigra s.l., Orchidaceae) and Publikacja / shifts in its pollinators availability as results of global warming, Publication Kolanowska Marta, Rewicz Agnieszka, Nowak Sawomir DOI wersji wydawcy / http://dx.doi.org/10.1016/j.gecco.2021.e01560 Published version DOI Adres publikacji w Repozytorium URL / https://repozytorium.bg.ug.edu.pl/info/article/UOG2ae4b8dd19b94d7c91e5f64aea8de4a9/ Publication address in Repository Data opublikowania w 14 kwi 2021 Repozytorium / Deposited in Repository on Rodzaj Uznanie Autorstwa - Uycie Niekomercyjne - Bez utworów zalenych (CC-BY-NC-ND licencji / Type of licence 4.0) Kolanowska Marta, Rewicz Agnieszka, Nowak Sawomir: Significant habitat loss of the Cytuj t wersj / black vanilla orchid (Nigritella nigra s.l., Orchidaceae) and shifts in its pollinators Cite this availability as results of global warming, Global Ecology and Conservation, Elsevier BV, version vol. 27, 2021, pp. 1-20, DOI:10.1016/j.gecco.2021.e01560 Global Ecology and Conservation 27 (2021) e01560

Contents lists available at ScienceDirect

Global Ecology and Conservation

journal homepage: www.elsevier.com/locate/gecco

Original Research Article Significant habitat loss of the black vanilla orchid (Nigritella nigra s.l., ]] Orchidaceae) and shifts in its pollinators availability as results of ]]]]]]]] global warming

Marta Kolanowskaa,b, Agnieszka Rewiczc,⁎, Sławomir Nowakd a University of Lodz, Faculty of Biology and Environmental Protection, Department of Geobotany and Plant Ecology, Banacha 12/16, 90-237 Lodz, Poland b Department of Biodiversity Research, Global Change Research Institute AS CR, Bělidla 4a, 603 00 Brno, Czech Republic c University of Lodz, Faculty of Biology and Environmental Protection, Department of Biogeography, Paleoecology and Nature Conservation, 1/3 Banacha Str., 90-237 Lodz, Poland d University of Gdansk, Faculty of Biology, Department of Plant Taxonomy and Nature Conservation, Wita Stwosza 59, 80-308 Gdańsk, Poland article info abstract

Article history: The black vanilla orchid (Nigritella nigra s.l.) is a perennial plant found in the main European Received 27 May 2020 mountain ranges. It occurs in large numbers in the Alps, but it has become a rare and Received in revised form 26 March 2021 endangered species in Scandinavia. Two subspecies of N. nigra s.l are recognized by most Accepted 26 March 2021 authors – the nominal subspecies which is restricted in its distribution to Scandinavia and Available online xxxx N. nigra subsp. austriaca which is found in the alpine region. Some taxonomists postulated that these two taxa should be considered as separated species. The N. nigra s.l. is pollinated Keywords: Nigritella nigra mostly by Lepidoptera. As a mainly montane species it is especially fragile to global warming, Niche modeling however, some previously published reports indicated that the climate changes will not Pollinators significantlyaffect northern populations of this species. The aim of this study was to evaluate Bioclimatic preferences the differences in the climatic niche preferences between Scandinavian and central European Global warming populations of the black vanilla orchid and to estimate the impact of global warming on the distribution of this species using (ENM). Additionally, the predicted future location and extent of suitable climatic niches of insects pollinating studied orchid was modeled in order to estimate the availability of pollinators for this montane plant. This approach was applied as the persistence of an orchid population depends on pollination and subsequent seed production. Our analyses showed that the northern and southern populations differ in bio climatic preferences and geographical distribution of these orchids together with variations in their chromosomes number and morphological discrepancies, suggest that N. nigra in not homogenous taxon as postulated by some authors and this approach should be also applied in assessing conservation priorities in Europe. Both, northern and southern population of N. nigra, will face significant habitat loss as a result of the global warming. In the best case scenario (rcp2.6) only 31.7% and 60.5% of the currently suitable niches will be still available for N. nigra respectively. The most damaging rcp8.5 scenario will cause the extreme decline of the coverage of orchid and just 2.3% of the habitats will be still suitable for N. nigra in the North and 18% for N. nigra in the South. Within the future potential range of N. nigra and N. nigra subsp. austriaca some pollinators will be still available for orchids, mostly for the latter taxon. Considering that the flowering time of the orchid seems to overlap with the

⁎ Corresponding author. E-mail addresses: [email protected] (M. Kolanowska), [email protected] (A. Rewicz), [email protected] (S. Nowak). https://doi.org/10.1016/j.gecco.2021.e01560 2351-9894/© 2021 The Author(s). Published by Elsevier B.V. CC_BY_NC_ND_4.0

Pobrano z https://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 M. Kolanowska, A. Rewicz and S. Nowak Global Ecology and Conservation 27 (2021) e01560

activity of pollinators for the last 70 years we not expect significant desynchronization of these events which could prevent pollen transfer. Noteworthy as the Scandinavian popula tions N. nigra is characterized by lower genetic diversity than in the alpine region of central Europe, species seems to be more endangered in the North (Moen and Øien, 2002) and the future loss of habitats predicted in our study together with limited availability of pollinators can led to loss of the unique gene pool of this orchid. In our opinion this fact should be considered in the establishment of nature protection projects and the conservation efforts should focus on areas which in the future will be still suitable for occurrence of this species and its pollen vectors. © 2021 The Author(s). Published by Elsevier B.V. CC_BY_NC_ND_4.0

1. Introduction

Nigritella nigra (L.) Rchb. f. (syn. Gymnadenia nigra (L.) Rchb. f.), known also as the black vanilla orchid (Fig. 1) is a perennial representative of Orchidaceae found in the main European mountain ranges, extending from the Pyrenees to the Alps and the Balkans, and up to Central Scandinavia (Moen and Øien, 2002; Delforge, 2006). The disjunctive arctic-alpine range is relatively common in both plants and animals and it is a result of various biogeographical patterns of the vicariance and/or dispersal

Fig. 1. Black vanilla orchid in its natural habitat. (A–B) Etang de Lers, Ariege, S France (photos: Mark Lunn), (C) Schwefelbergbad, Kanton Bern, Switzerland (photo: Christian Kobel), (D–E) Marieby near Östersund, Jämtland, Sweden (photos: Marco Klüber/ www.m-klueber.de).

Pobrano z https://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 M. Kolanowska, A. Rewicz and S. Nowak Global Ecology and Conservation 27 (2021) e01560 events (Schmitt et al., 2010). In such disconnected populations the opportunity for allopatric speciation increase (Hoelzer et al., 2008) and the detailed genetic analyses are useful in assessing the proper taxonomic status of taxa characterized by dis continuous geographical ranges (Medrano and Herrera, 2008). Without a doubt, the effective conservation strategies should be focused on appropriate taxonomical units, but evolutionarily and genetically divergent lineages within threatened species are often not recognized (Llorens et al., 2015). Teppner and Klein (1990) suggested separation of two subspecies within N. nigra based on spur length and chromosomes number. In this taxonomic concept the nominal subspecies of N. nigra occurs only in two areas in Scandinavia while the alpine region of central Europe is occupied by N. nigra subsp. austriaca Teppner and Klein. The same authors (Teppner and Klein, 1993) further separated N. nigra representatives occurring in the Pyrenees as N. nigra subsp. iberica Teppner and Klein. The genetic studies (Hedrén et al., 2017) supported approach with heterogenous concept of N. nigra, but in spite of minor differences in morphology (Teppner, 2004) and allozymes (Hedrén et al., 2000), only delineation of subsp. nigra and subsp. austriaca seemed to be justified (Hedrén et al., 2017). Delforge et al. (1991) raised both taxa to the species rank. In our work, we proceeded from the concept of N. nigra s.l. because much of the pollination and occurrence data were and are often attributed to this taxon. In our opinion, without a detailed analysis of the material studied, which is often impossible, it would be imprudent to assign the data a priori to one taxon or the other. However, we also discuss the results obtained in the context of the aforementioned concepts of N. nigra. It is worth to notice that a decade ago it was proposed to lump Nigritella Rich. in Gymnadenia R. Br. (Bateman, 2009) despite clear morphological differences between these taxa (Moore, 1980; Baumann et al., 2006; Kellenberger et al., 2019) and results of molecular research (Ståhlberg, 1999; Hedrén et al., 2000). More recently the phylogenetic and genetic studies confirmed the separateness of these two genera (Hedrén et al., 2017; Brandrud et al., 2019). However, there is still not complete agreement on the classification of the two genera, as detailed by Bateman (2021), who clearly advocates accepting the genus Gymnadenia s.l. The black vanilla orchid is nectariferous plant pollinated by butterflies (Pridgeon et al., 2001), however, numerous Scan dinavian populations are apomictic (Timpe and Mrkvicka, 1991; Hedrén et al., 2000). So far seven Lepidoptera species were reported as transferring pollen of the studied orchid. Also an unidentified species of Zygaena was observed as pollinator (Godfery, 1933). The butterflies are probably attracted to orchid flower by presence of vanillin (Tava et al., 2012). Moreover, a single Diptera representative was reported as pollinator of the black vanilla orchid (Table 1). The studied species grows usually in grassland and meadows but can also be found in open wooded pastures and dry fens. As most Orchidaceae, it is included in Annex II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). The black vanilla orchid occurs in large numbers in the Alps, but it has become a rare and endangered species in Scandinavia due to the loss of suitable habitats (Björkbäck and Lundqvist, 1996; Moen and Øien, 2002) and it is considered as endangered in Norway (Bjørndalen, 2015). While global warming affects the composition and dynamic of ecosystems across the world, the montane bionetworks are particularly sensitive to climate changes because their biota is generally limited by low temperatures (Parmesan and Yohe, 2003; Neilson et al., 2005; Vanneste et al., 2017). Temperature rise leads to increase of aboveground biomass, loss of species richness, and shifts in plant community composition (Berauer et al., 2019). It was suggested in the “Åtgärdsprogram för Brunkulla, 2013–2017″ report of the Naturvårdsverkets that the impacts of climate change is of minor importance for N. nigra persistence in Sweden (Holmberg, 2020) but this statement was presented without any experimental confirmation. The aim of our research was to estimate the impact of global warming on the dis tribution of northern and southern populations of N. nigra s.l. (N. nigra subsp. nigra and N. nigra subsp. austriaca) and to evaluate the predicted future location and extent of suitable climatic niches of insects pollinating the black vanilla orchid in order to estimate the availability of pollinators for this montane plant species. For the first time the evaluation of future distribution of suitable habitats for nectariferous orchid and its pollen vectors is presented. This approach seems to be crucial for obtaining any reliable assessment of the actual impact of climate change on Orchidaceae because persistence of any orchid population is strongly depended on its pollination and subsequent seed production (Jacquemyn et al., 2005; Štípková et al., 2020). The additional objective of the present study was to evaluate the discrepancies in the climatic niche preferences between Scan dinavian (N. nigra subsp. nigra) and central European populations of N. nigra (N. nigra subsp. austriaca) to verify if the two

Table 1 Pollinator species of Nigritella nigra included in the study.

Species Source

Adscita statices L. Müller (1874) and Kaiser (1993) Boloria euphrosyne L. Müller (1874) Crambus perlella Scop. Müller (1881) and Vöth (1999, 2000) Crocota tinctaria Hübner Müller (1881) Diasemia litterata Scop. Müller (1874, 1881) and Vöth (1999, 2000) Lasionycta imbecilla Fab. Müller (1881) and Vöth (1999) Leucania comma L. Godfery (1933) Thricops aculeipes Zett Müller (1881)

Pobrano z https://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 M. K olanowska, A Pobrano zhttps://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 . Rewicz and S. N owak 4 Global Ecology and Conserva tion Fig. 2. Localities of N. nigra s.l. georeferenced with precision of at least 2 km (red spots) and records used in the analyses (black stars) (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article). 27 (202 1) e0 1 560 M. K olanowska, A Pobrano zhttps://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 . Rewicz and S. N owak 5 Global Ecology and Conserva

Fig. 3. Localities of N. nigra s.l. pollinators used in the analyses. tion 27 (202 1) e0 1 560 M. Kolanowska, A. Rewicz and S. Nowak Global Ecology and Conservation 27 (2021) e01560 subspecies differs ecologically which would support their separateness postulated by Delforge et al. (1991). If in fact, these are two different taxa, the conservation actions should be proposed separately for each species and nature protection activities should be focused on areas which will be suitable for Nigritella and its pollinators occurrence in the future. Nigritella nigra as a species with unclear taxonomic status and discontinuous distribution range may pose a great challenge to conservation and therefore was selected as an object of this study. Moreover, it is a mountain species and therefore po tentially the most threatened during global climate change.

2. Material and methods

2.1. Localities of studied species

The database of localities of N. nigra s.l. and its pollinators was compiled based on data available in GBIF (2018). From the total of 3324 localities of the studied orchid and 127,143 of eight insect species only records georeferenced with the precision of at least 2 km were used. Numerous localities in the databases were overlapping with each other or were located in a close proximity giving little analytical value. The initial catalogue was therefore thinned to remove duplicate records and to reduce bias caused by sampling in more accessible areas (Reddy and Davalos, 2003; Reese et al., 2005; Phillips et al., 2009) and finally included only records distanced one from another for at least 10 km. The final database contained 69 localities of southern and 26 of northern populations of N. nigra s.l. (Fig. 2) which is more than the minimum number of records required to obtain reliable predictions in MaxEnt (Pearson et al., 2006; Wisz et al., 2008). The list of pollinators localities included a total of 5584 records (A. statices – 1104, B. euphrosyne – 2410, C. perlella – 874, C. tinctaria – 13, D. reticularis – 84, L. imbecilla – 84, L. comma – 996, T. aculeipes – 19; Fig. 3). While terrestrial orchids like Orchis, Ophrys, Gymnadenia and Nigritella (Piñeiro Fernández et al., 2009) attract a broad range of floral visitors, the list of pollinators used in our study was compiled based on previously published reports on pollen vectors (Table 1) and the insects which were found on flowers of the black vanilla orchid but did not transfer pollen were not included in the modeling.

2.2. Climatic preferences of northern of southern populations of N. nigra

The Principal Components Analysis (PCA) was used to evaluate the differences between southern and northern populations of N. nigra s.l. based on 19 bioclimatic variables (Hijmans et al., 2005; Booth et al., 2014) in software package STATISTICA PL v. 13.3 (StatSoft, Inc., 2013). The data matrix was transformed (square root) before performing the ordination analysis. The results of PCA analysis were used to decide whether the species distribution models should be conducted using records from the whole range of N. nigra s.l., or using two different datasets (separated for northern and southern populations).

2.3. Ecological niche modeling

The ecological niche modeling was conducted using the maximum entropy method in MaxEnt version 3.3.2 (Phillips et al., 2004, 2006; Elith et al., 2011) based on presence-only data. Considering the outputs of previous studies (e.g. Barve et al., 2011) the area of ENM analyses was restricted to 12°W–45°E and 74°−34°N. The correlation between 19 bioclimatic variables was calculated using the Pearson correlation coefficient and the final dataset consisted of 12 layers (Table 2) in 2.5′ (±21.62 km2 at the equator) of interpolated climate surface (Hijmans et al., 2005; Booth et al., 2014) obtained from WorldClim (version 1.4, www.worldclim.org) for which calculated correlation coefficient factor was lower than 0.9.

Table 2 Variables – codes of climatic variables used in the analyses.

Code Description

bio1 Annual Mean Temperature bio2 Mean Diurnal Range = Mean of monthly (max temp − min temp) bio3 Isothermality (bio2/bio7) *100 bio4 Temperature Seasonality (standard deviation * 100) bio8 Mean Temperature of Wettest Quarter bio9 Mean Temperature of Driest Quarter bio10 Mean Temperature of Warmest Quarter bio12 Annual Precipitation bio14 Precipitation of Driest Month bio15 Precipitation Seasonality (Coefficient of Variation) bio18 Precipitation of Warmest Quarter bio19 Precipitation of Coldest Quarter

Pobrano z https://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 M. Kolanowska, A. Rewicz and S. Nowak Global Ecology and Conservation 27 (2021) e01560

Predictions of the future coverage of the climatic niches of the black vanilla orchid and its pollinators in 2070 were modeled using climate projections of the Community Climate System Model (CCSM4) for four representative concentration pathways (RCPs: rcp2.6, rcp4.5, rcp6.0, rcp8.5). These scenarios describe future climate of the Earth considering various emission of greenhouse gases (Moss et al., 2008; Weyant et al., 2009). In all analyses the maximum number of iterations was set to 10,000 and convergence threshold to 0.00001. The “random seed” option which provided a random test partition and background subset for each run was applied. 10% of the samples were used as test points. The run was performed as a bootstrap with 1000 replicates, and the output was set to logistic. All operations on GIS data were carried out on ArcGis 10.6 (Esri, Redlands, CA, USA). The evaluation of the created models was made using the most common metric – the area under the curve (AUC; Mason and Graham, 2002; Evangelista et al., 2008).

2.4. Changes in the distribution of suitable niches

SDMtoolbox 2.3 for ArcGIS (Kremen et al., 2008) was used to visualize changes in the distribution of suitable niches of studied orchid and its pollinators caused by global warming. To compare distribution model created for current climatic conditions with future models all SDMs were converted into binary rasters and projected using Albers EAC as projection. The presence threshold was estimated based on the values of grids in which studied species occur in models created using present- time data – for southern populations of the black vanilla orchid and all pollinators the threshold was set as 0.4 and for the northern group of the orchid as 0.3. Moreover, the binary models of predicted occurrence of studied plant were compared with future distribution of its pollinators niches and number of grid cells in which both orchid and insect can occur was calculated to estimate the pollinator availability.

3. Results

3.1. Climatic preferences of northern and southern populations of N. nigra s.l

The PCA indicated significantdifferences in bioclimatic preferences between northern and southern populations of the black vanilla orchid. Occurrence of orchids in the north was correlated especially with bio4 and bio6. The distribution of southern populations was correlated especially with bio10, bio12 and bio14. The PCA analysis revealed that the first two principal components explained 72.3% (49.8% and 22.5% respectively) of the total variance (Fig. 4).

3.2. Models evaluation and limiting factors

The AUC for created models received high values of 0.819–0.966 with a standard deviation of 0.001–0.012 (Table 3). According to the analyses the two groups of the black vanilla orchid populations differ in the factors limiting their distribution.

Fig. 4. Ordination diagram of the Principal Component Analysis (PCA) between northern populations of N. nigra (black dots) and southern populations of N. nigra (green dots) based on 12 bioclimatic variables (For interpretation of the references to color in this figurelegend, the reader is referred to the web version of this article).

Pobrano z https://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 M. Kolanowska, A. Rewicz and S. Nowak Global Ecology and Conservation 27 (2021) e01560

Table 3 The average training AUC and standard deviation values (in bracket) for the replicate runs for created models.

present rcp2.6 rcp 4.5 rcp 6.0 rcp 8.5

N. nigra N 0.996 (0.001) 0.996 (0.001) 0.996 (0.001) 0.996 (0.001) 0.996 (0.001) N. nigra S 0.992 (0.001) 0.992 (0.002) 0.992 (0.002) 0.992 (0.001) 0.992 (0.002) Adscita statices 0.902 (0.002) 0.901 (0.002) 0.902 (0.002) 0.902 (0.002) 0.902 (0.002) Boloria euphrosyne 0.822 (0.002) 0.819 (0.002) 0.819 (0.002) 0.821 (0.002) 0.823 (0.002) Crambus perlella 0.896 (0.003) 0.895 (0.003) 0.894 (0.003) 0.892 (0.003) 0.894 (0.003) Crocota tinctaria 0.980 (0.011) 0.979 (0.011) 0.978 (0.012) 0.978 (0.011) 0.978 (0.012) Diasemia reticularis 0.992 (0.001) 0.992 (0.001) 0.993 (0.001) 0.992 (0.001) 0.992 (0.001) Lasionycta imbecilla 0.970 (0.006) 0.972 (0.005) 0.970 (0.005) 0.970 (0.005) 0.971 (0.005) Leucania comma 0.924 (0.002) 0.923 (0.002) 0.926 (0.002) 0.924 (0.002) 0.926 (0.002) Thricops aculeipes 0.986 (0.005) 0.986 (0.004) 0.985 (0.005) 0.987 (0.004) 0.985 (0.005)

While the highest contribution to the MaxEnt models of northern group was given by bio1 (33.9%), bio10 (18.6%), and bio4 (11.3%), in case of southern plants the most important bioclimatic factors were bio18 (44.7%), bio12 (13.3%), and bio3 (13.1%).

3.3. Current distribution and of bioclimatic niches suitable for N. nigra s.l. and its pollinators

The current distribution of the suitable niches of the black vanilla orchid is consistent with the known geographical range of this species, however, some additional niches were detected in the Caucasus, some parts of the Carpathians and far north of Scandinavia where so far this orchid was not recorded (Fig. 5). Potential distribution of the pollinators of the studied species is presented in Fig. 6. In the model created for Adscita statices the suitable niches which seems to be outside the known distribution of this orchid were detected in the Dinaric Alps and the Pyrenees. The potential distribution of Boloria euphrosyne, Crambus perlella, Lasionycta imbecilla, and Leucania comma is con sistent with the reported occurrence of these insects with the exception of the eastern Carpathians and small parts of the Dinaric Alps. Some additional niches of Leucania comma are also located in the coastal areas if northern Europe. The projected range of Crocota tinctaria is overestimated which may be a result of insufficient records used in the analyses. The known populations of this species occur only in the Alps while the created model indicated also the Pyrenees, the Dinaric Alps, part of Great Britain and northern Scandinavia as suitable for the existence of this insect. In case of Diasemia reticularis the model designated the Caucasus as an area suitable for this species presence but so far this species was not found in this region. The model of the potential distribution of Thricops aculeipes is generally consistent with the known range of this insect, however, some scattered suitable areas were also detected in southern Europe.

3.4. Future changes in the distribution and extent of bioclimatic niches suitable for N. nigra s.l

In all predicted scenarios the total coverage of the suitable niches of the studied orchid will decline (Table 4 and Fig. 7). The total habitat loss vary between 39.37% and 82.55% in case of southern populations and 67.80–97.64% for northern group. The most damaging will be rcp8.5 scenario in which just 2.3% of the suitable habitats of northern and 18% of southern populations will be available. The rcp2.6 scenario should be the least harmful, with 31.7–60.5% habitat still available for the black vanilla orchid. Considering the coverage of these suitable niches, 39,468–67,750 km2 of the currently suitable niches will be lost in Central Europe and the northern part of the range will contract for 63,096–86,856 km2. Noteworthy, in both cases the small expansion of potentially available habitats will be observed – 2664–8426 km2 in the south and 1370–3734 km2 in the north (Table 4; Figs. 8 and 9).

3.5. Future changes in the distribution and extent of bioclimatic niches suitable for pollinators of the black vanilla orchid

Overall, all pollinators of studied orchid will face habitat loss as a result of the climate changes (Table 5; Annexes 1 and 2). The highest range contraction will be observed in Boloria euphrosyne – in most damaging climate change scenario, rcp8.5, this species will lose 857,599 km2 of the suitable niches. The coverage of the potentially available habitat of Adscita statices will decline for 3,755,312 km2 (rcp8.5) to 461,699 km2 (rcp4.5). Relatively significant range contraction will be also observed for Crambus perlella which will lose 458,171 km2 (rcp2.6) – 696,349 km2 (rcp8.5). Somewhat smaller decline in the coverage of the suitable niches will be observed in Leucania comma (205,598–322,970 km2). Crocota tinctaria will lose 14,113–65,235 km2 of the habitats and the reduction ranging from 15,802 km2 to 96,314 km2 will be recorded in Lasionycta imbecilla. The coverage of areas available for Thricops aculeipes will also decline (58,629–92,636 km2). The potential range of one species, Diasemia reticularis, will be slightly larger in rcp4.5 scenario than currently observed (expansion of ca 20,287 km2).

Fig. 6. Current distribution of suitable niches of Adscita statices (A), Boloria euphrosyne (B), Crambus perlella (C), Crocota tinctaria (D), Diasemia reticularis (E), Lasionycta imbecilla (F), Leucania comma (G), Thricops aculeipes (H).

Pobrano z https://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 M. Kolanowska, A. Rewicz and S. Nowak Global Ecology and Conservation 27 (2021) e01560

Table 4 Comparison of the model of current potential range of N. nigra with the predicted climate change scenarios (rcp2.6, rcp4.5, rcp6.0, and rcp8.5). Changes are expressed as area (km2) of the range expansion (−1), no occupancy (0), no change (1) and range contraction (2).

change rcp2.6 rcp4.5 rcp6.0 rcp8.5 habitat loss [%]

N. nigra N –1 3734.734 3246.779 2101.961 1370.028 67.80% 0 9,433,881.486 9,434,369.441 9,435,514.259 9,436,246.192 84.59% 1 24,454.062 10,247.059 10,791.316 694.398 85.27% 2 63,096.358 77,303.361 76,759.103 86,856.022 97.64% N. nigra S –1 8426.611 6906.443 3378.151 2664.986 39.37% 0 9,437,897.733 9,439,417.901 9,442,946.192 9,443,659.357 41.54% 1 39,374.230 39,186.555 23,834.734 11,091.597 65.48% 2 39,468.067 39,655.742 55,007.563 67,750.700 82.55%

3.6. Future pollinator availability

The general maps presenting potential range of the black vanilla orchid and its pollinators in various climate change scenarios are presented in Fig. 10 and the calculated number of grid cells where both, the orchid and insects can occur in the future are presented in Table 6. Adscita statices will not be available for northern populations of studied orchid and very limited for southern group – overlapping localities will be found only in 0.19–3.53% of the predicted orchid potential range. Boloria euphrosyne will be the most important pollinator for both geographical groups of N. nigra. This insect will be available in 69.45–93.93% of northern and in 74.84–90.29% of southern populations range. Crambus perlella will be available only for the maximum of 0.46% of northern populations of the black vanilla orchid and for 17.21–42.97% of southern group. Crocota tinctaria will play important role for southern populations (present in 21.68–44.36% of orchid range). Diasemia reticularis and Leucania comma will be available exclusively for southern populations of studied orchid (22.09–58.03% and 9.11–34.25% respectively). While the overlapping area of the occurrence of the black vanilla orchid and Lasionycta imbecilla will constitute only up to 1.02% of the northern potential range of N. nigra, the area shared with pollinator in the south will be much higher (43.14–68.30%). Thricops aculeipes will not play important role in pollination of northern (0.48–13.44%) or southern (0–2.77%) populations of N. nigra s.l. Based on data published in GBIF the overlap of flowering time of the black vanilla orchid and its pollinators was evaluated for five different time periods: before 1950, 1951–1970, 1971–1990, 1991–2010, and 2011–2020. The monthly observations in each period are presented in Fig. 11.

4. Discussion

As showed in our analyses the northern and southern populations of the black vanilla orchid differ in bioclimatic pre ferences. The two groups delineated in our study correspond to the subspecies designated by Teppner and Klein (1990). Considering various geographical distribution of these orchids, variation in the chromosomes number (in N. nigra subsp. aus triaca 2n = 80 and in N. nigra subsp. nigra 2n = 60) and morphological disparities (spur length and length of perigon parts), the two taxa could be treated as separated species as postulated by Delforge et al. (1991) as well. According to Joffard et al. (2019) speciation is higher in deceptive than in nectar-producing orchids (as Nigritella). Since the two studied Nigritella species share the same pollination strategy, their speciation could be prompted by the large-scale and long-term geographic isolation, however, the more detailed genetic research should be conducted to confirm that. Global warming will be harmful for the black vanilla orchid which will face the significant habitat loss. In the best case scenario (rcp2.6) only 31.7% of the suitable niches will be still available for N. nigra in the North and 60.5% in the South. The most damaging rcp8.5 scenario will cause the dramatic decline of the coverage of orchid niches and just 2.3% of the habitats will be still suitable for northern population of N. nigra and 18% southern population. It is generally accepted that alpine species which occupy extreme habitats characterized by colder climate, low night temperatures, short growing-season and high winds due to their physiological tolerance or requirement for cold conditions and/or their intolerance to competition with taller, more rapidly growing lowland or montane plants (Körner, 2003, 2016). Undoubtedly, montane ecosystems are among the most vulnerable when global warming is considered (Guisan et al., 1995) and scenarios of upward species migration and vegetation shifts were widely discussed in the literature (e.g. Grabherr et al., 1994; Freeman et al., 2018). Geppert et al. (2020) reported recently consistent decline of some alpine orchid species and concluded that rear-edge populations of these plants are more vulnerable due to multiple threats (global warming, habitat modification, and loss of specific ecological relationships). Range shifts in response to climate change are a phenomenon that is observed not only for species but also for plant formations (Dainese et al., 2017; Lamprecht et al., 2018). However, in the case of orchids, which are often specialists, this possibility is limited (Geppert et al., 2020). Montane species would be at greatest risk of local extinction, whereas species with a large elevation range would run the lowest risk (Guisan and Theurillat, 2000; Scherrer and Körner, 2010). Nigritella nigra s.l. is montane species,

Pobrano z https://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 M. Kolanowska, A. Rewicz and S. Nowak Global Ecology and Conservation 27 (2021) e01560

Fig. 7. Distribution of suitable niches of N. nigra s.l. according to various climate change scenarios – rcp2.6 (A, E), rcp4.5 (B, F), rcp6.0 (C, G), and rcp8.5 (D, H). (A–D) – northern populations of N. nigra, (E–H) – southern populations of N. nigra.

Pobrano z https://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 M. Kolanowska, A. Rewicz and S. Nowak Global Ecology and Conservation 27 (2021) e01560

Fig. 8. Changes in the distribution of suitable niches of northern populations of N. nigra s.l. [range expansion (−1), no occupancy (0), no change (1) and range contraction (2)] according to various climate change scenarios – rcp2.6 (A), rcp4.5 (B), rcp6.0 (C), and rcp8.5 (D).

however, it grows in lower altitudes and can be found even at elevation of 1000 m, hereby the complete extinction of these species is not currently expected. The nature of the orchid–pollinator relationship is complex. The most common animals transferring pollinia of Orchidaceae are Hymenoptera, but other insects (e.g. Lepidoptera, Diptera, Coleoptera) and small birds were also reported as orchid pollinators (Gorham, 1976; Gutowski, 1990; van der Cingel, 2001; Micheneau et al., 2010; Gaskett, 2011). While some orchid species can be pollinated by numerous taxa, other are specialized and only one pollinator species can transfer the pollen. Orchids with more specific interactions with pollinators have more efficient pollen transfer than species relying on multiple pollinators, but on the other hand the absence of particular animal can significantly reduce their reproductive success. Without the doubt, the relationship between plant and its pollen vectors should be considered to improve conservation strategies (Phillips et al., 2020) by assuring the cross-pollination of vanilla orchids. Outcrossing via deceptive pollination stimulate higher genetic diversity in orchids (Zhang et al., 2019). Transfer of pollinia guarantees connectivity between sub-populations and counteracting the genetic erosion at local scales. While plants which are predominantly cross-pollinated are generally expected to preserve higher population genetic diversity (Castro and Singer, 2019), such taxa usually undergo more significant losses of genetic variation when gene flowbetween populations is compromised following habitat fragmentation or decline (Honnay and Jacquemyn, 2007; Aguilar et al., 2008). Within the future potential range of N. nigra some pollinators will be still available for orchids, mostly for the latter taxon. Boloria euphrosyne will be the most important pollinator for both Nigritella species. On the other hand the role Thricops aculeipes as pollen vector will be very limited. In the northern population, Nigritella nigra will lost Adscita statices as pollen vector and the role of Crambus perlella and Lasionycta imbecilla will be very limited as these insects will

Pobrano z https://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 M. Kolanowska, A. Rewicz and S. Nowak Global Ecology and Conservation 27 (2021) e01560

Fig. 9. Changes in the distribution of suitable niches of southern populations of N. nigra s.l. [range expansion (−1), no occupancy (0), no change (1) and range contraction (2)] according to various climate change scenarios – rcp2.6 (A), rcp4.5 (B), rcp6.0 (C), and rcp8.5 (D).

Table 5 Habitat loss [km2] of pollinators of N. nigra. The numbers are differences between area of range contraction and range expansion as calculated in SDMToolbox.

Scenario Adscita statices Boloria Crambus Crocota Diasemia Lasionycta Leucania Thricops euphrosyne perlella tinctaria reticularis imbecilla comma aculeipes

rcp2.6 382,707.00 330,796.08 458,171.15 14,113.16 3622.13 36,803.08 205,598.04 58,629.69 rcp4.5 461,699.44 537,107.28 582,749.86 45,999.16 –20,287.67 37,966.67 301,406.16 73,718.77 rcp6.0 442,237.53 539,791.04 539,791.04 35,883.47 4128.85 15,802.24 297,859.10 84,078.43 rcp8.5 375,312.60 857,600.00 696,349.58 65,235.85 25,805.32 96,314.84 322,970.02 92,636.41

be available for orchid in very constrained part of its geographical range. In southern populations Crambus perlella and Crocota tinctaria will still be able to pollinate N. nigra within respectively 17.21–42.97% and 21.68–44.36% of plant range, Lasionycta imbecilla will remain important pollen vector as it will occur in 43.14–68.30% of orchid range, and Adscita statices will serve as a pollinator in very restricted areas (0.19–3.53% of orchid range). Noteworthy, apomixis which allows plants to reproduce in time when pollinators are scarce was previously reported for N. nigra in Scandinavia (Timpe and Mrkvicka, 1991). Unfortunately, this pathway of reproduction can result in loss of genetic diversity in populations causing genetic erosion which is potentially a great

Pobrano z https://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 M. K olanowska, A Pobrano zhttps://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 . Rewicz and S. N owak 1 5 Global Ecology and Conserva tion Fig. 10. Distribution of N. nigra s.l. (blue shade) and its pollinators (green shade) in various climate change scenarios – rcp2.6 (A), rcp4.5 (B), rcp6.0 (C), and rcp8.5 (D) (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article). 27 (202 1) e0 1 560 M. Kolanowska, A. Rewicz and S. Nowak Global Ecology and Conservation 27 (2021) e01560

Table 6 Number of grid cells in MaxEnt models where both N. nigra and its pollinators occur in the present time and in which they will be present according to various climate change scenarios (rcp2.6, rcp4.5, rcp6.0, rcp8.5).

present rcp2.6 rcp4.5 rcp6.0 rcp8.5

Adscita statices & N. nigra N 0 0 0 0 0 Adscita statices & N. nigra S 6 6 65 64 14 Boloria euphrosyne & N. nigra N 4958 1969 1027 1207 158 Boloria euphrosyne & N. nigra S 3150 2401 2496 1637 724 Crambus perlella & N. nigra N 2 0 6 0 0 Crambus perlella & N. nigra S 888 552 848 779 209 Crocota tinctaria & N. nigra N 86 26 3 1 8 Crocota tinctaria & N. nigra S 1581 1423 921 393 284 Diasemia reticularis & N. nigra N 164 0 0 0 0 Diasemia reticularis & N. nigra S 2754 1400 1484 1052 211 Lasionycta imbecilla & N. nigra N 318 29 3 7 0 Lasionycta imbecilla & N. nigra S 2295 2191 1543 1222 412 Leucania comma & N. nigra N 0 0 0 0 0 Leucania comma & N. nigra S 973 1001 936 621 87 Thricops aculeipes & N. nigra N 1317 110 175 9 1 Thricops aculeipes & N. nigra S 70 89 42 23 0

threat for studied orchid (Hamilton, 2009; Barrett et al., 2014). The flowering times of N. nigra seem to overlap with the activity of the pollinators for the last 70 years hereby we not expect significant desynchronization of these events which could prevent pollen transfer in the next 50 years. Also the daily activity of pollinators, even if disturbed by global warming, should not have an impact on fruit set of N. nigra because the flowers of Nigritella individuals are opening in succession and they last for several days (Paušič, 2015). Noteworthy, the gene pool of N. nigra in the Scandinavian and Central European regions differ significantlyand the exchange of genetic material between these populations probably does not occur (Hedrén et al., 2017). Nigritella nigra in the North is characterized by lower genetic diversity than in the South (Hedrén et al., 2000, 2017). Pfeifer et al. (2009) revealed in a study on another species with a disjunctive distribution in Europe that not only historical changes, mainly post-glacial, are important for the genetic structure of a population. It turns out that an important role is played by climate change, which could shape the geographic genetic structure, so genetic differences between N. nigra s.l. populations may still increase in the future. Nowadays Scandinavian orchids seem to be more endangered (Moen and Øien, 2002) and the significant future habitats loss predicted in our study together with decreased pollinator availability can led to extinction of N. nigra. In our opinion this fact should be considered in the establishment of nature protection projects. It is especially important to preserve areas which were indicated in our models as suitable for occurrence of this species and its pollinators (Fig. 18). However, as Pfeifer et al. (2010) point out, in the case of climate change, different conservation approaches should be used for areas where the species expands or shifts its range and for areas where the species retreats. In new areas, many other factors may come into play that will affect the survival of the species, while relict areas may be characterized by high stability, allowing the taxon to persist much longer. While according to our study the Scandinavian and Central European populations of the black vanilla orchid should be considered as separated species based on the differences in preferred climatic niches, we can not exclude the possibility that more detailed genetic analyses will indicate that N. nigra is a species with disjunct distribution and should not be divided into smaller taxa. Without a doubt, taxonomy plays important role in establishing nature conservation actions and for that reason in this paper we discussed the impact of climate change in both parts of the black vanilla orchid so our findingswill be relevant for any taxonomic concept of N. nigra.

Funding

This work was supported by the Ministry of Education, Youth and Sports of Czech Republic within the CzeCOS program, grant number LM2018123.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have ap peared to influence the work reported in this paper.

Fig. 11. Flowering time of N. nigra and its pollinators activity time. M. Kolanowska, A. Rewicz and S. Nowak Global Ecology and Conservation 27 (2021) e01560

Acknowledgments

We are grateful to Mark Lunn, Christian Kobel and Marco Klüber for providing photos of black vanilla orchid used in this paper.

Appendix A. Supporting information

Supplementary data associated with this article can be found in the online version at doi:10.1016/j.gecco.2021.e01560.

References

Aguilar, R., Quesada, M., Ashworth, L., Herrerias-Diego, Y., Lobo, J., 2008. Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol. Ecol. 17, 5177–5188. Barrett, S.C.H., Arunkumar, R., Wright, S.I., 2014. The demography and population genomics of evolutionary transitions to self-fertilization in plants. Philos. Trans. R. Soc. B 369 (1648), 20130344. Barve, N., Barve, V., Jimenez-Valverde, A., Lira-Noriega, A., Maher, S.P., Peterson, A.T., Soberóna, J., Villalobos, F., 2011. The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecol. Model. 222, 1810–1819. https://doi.org/10.1016/j.ecolmodel.2011.02.011 Bateman, R.M., 2009. Evolutionary classification of European orchids: the crucial importance of maximizing explicit evidence and minimizing authoritarian speculation. J. Eur. Orch. 41, 243–318. Bateman, R.M., 2021. Phenotypic versus genotypic disparity in the Eurasian orchid genus Gymnadenia: exploring the limits of phylogeny reconstruction. Syst. Biodivers. 1–23. https://doi.org/10.1080/14772000.2021.1877845 Baumann, H., Künkele, S., Lorenz, R., 2006. Orchideen Europas. Ulmer Naturführer. Berauer, B.J., Wilfahrt, P.A., Arfin-Khan, M.A.S., Eibes, P., von Heßberg, A., Ingrisch, J., Schloter, M., Schuchardt, M.A., Jentsch, A., 2019. Low resistance of montane and alpine grasslands to abrupt changes in temperature and precipitation regimes. Arct. Antarct. Alp. Res. 51 (1), 215–231. https://doi.org/10.1080/ 15230430.2019.1618116 Björkbäck, E., Lundqvist, J., 1996. Some new and interesting localities for Nigritella nigra in Jamtland, central Sweden. Sven. Bot. Tidskr. 90, 301–306. Bjørndalen, J.E., 2015. Protection of Norwegian orchids – a review of achievements and challenges. Eur. J. Environ. Sci. 5 (2), 121–133. Booth, T.H., Nix, H.A., Busby, J.R., Hutchinson, M.F., 2014. BIOCLIM: the first species distribution modelling package, its early applications and relevance to most current MAXENT studies. Divers. Distrib. 20, 1–9. https://doi.org/10.1111/ddi.12144 Brandrud, M.K., Paun, O., Lorenz, R., Hedrén, M., 2019. Restriction-site associated DNA sequencing supports a sister group relationship of Nigritella and Gymnadenia (Orchidaceae). Mol. Phylogenet. Evol. 136, 21–28. Castro, J.B., Singer, R.B., 2019. A literature review of the pollination strategies and breeding systems in Oncidiinae orchids. Acta Bot. Bras. 33 (4), 618–643. https://doi.org/10.1590/0102-33062019abb0111 van der Cingel, N.A., 2001. An Atlas of Orchid Pollination: America, Africa, Asia and Australia. Balkema, Rotterdam. Dainese, M., Aikio, S., Hulme, P.E., Bertolli, A., Prosser, F., Marini, L., 2017. Human disturbance and upward expansion of plants in a warming climate. Nat. Clim. Chang 7 (8), 577–580. Delforge, P., 2006. Orchids of Europe, North Africa and the Middle East. Timber Press, Portland. Delforge, P., Devillers-Terschuren, J., Devillers, P., 1991. Contributions taxonomiques et nomenclaturales aux Orchidees d′Europe. Nat. Belg. 72, 99–101. Elith, J., Phillips, S.J., Hastie, T., Dudík, M., Chee, Y.E., Yates, C.J., 2011. A statistical explanation of MaxEnt for ecologists. Divers. Distrib. 17, 43–57. https://doi.org/ 10.1111/j.1472-4642.2010.00725.x Evangelista, P.H., Kumar, S., Stohlgren, T.J., Jarnevich, C.S., Crall, A.W., Norman III, J.B., Barnett, D.T., 2008. Modelling invasion for a habitat generalist and a specialist plant species. Divers. Distrib. 14, 808–817. https://doi.org/10.1111/j.1472–4642.2008.00486.x Freeman, B.G., Lee‐Yaw, J.A., Sunday, J.M., Hargreaves, A.L., 2018. Expanding, shifting and shrinking: The impact of global warming on species’ elevational distributions. Glob. Ecol. Biogeogr. 27, 1268–1276. https://doi.org/10.1111/geb.12774 Gaskett, A.C., 2011. Orchid pollination by sexual deception: pollinator perspectives. Biol. Rev. Camb. Philos. Soc. 86 (1), 33–75. https://doi.org/10.1111/j.1469- 185X.2010.00134.x GBIF, 2018. GBIF Occurrence Download. https://doi.org/10.15468/dl.xyfl4n (Accessed 4 November 2018). Geppert, C., Perazza, G., Wilson, R.J., Bertolli, A., Prosser, F., Melchiori, G., Marini, L., 2020. Consistent population declines but idiosyncratic range shifts in Alpine orchids under global change. Nat. Commun. 11, 5835. https://doi.org/10.1038/s41467-020-19680-2 Godfery, M.J., 1933. Monograph and iconograph of the native British Orchidaceae, Cambridge. Gorham, J.R., 1976. Orchid pollination by Aedes Mosquitoes in Alaska. Am. Midl. Nat. 95 (1), 208–210. Grabherr, G., Gottfried, M., Paul, H., 1994. Climate effects on mountain plants. Nature 369, 448. Guisan, A., Holten, J.I., Spichiger, R., Tessier, L., 1995. Potential Ecological Impacts of Climate Change in the Alps and Fennoscandian Mountains, An Annex Report to the Second Assessment Report (SAR) of the Intergovernmental Pannel on Climate Change (IPCC). Conservatoire et jardin botaniques de la Ville de Genève. Guisan, A., Theurillat, J.P., 2000. Assessing alpine plant vulnerability to climate change: a modeling perspective. Integr. Assess. 1, 307–320. https://doi.org/10. 1023/A:1018912114948 Gutowski, J.M., 1990. Pollination of the orchid Dactylorhiza fuchsii by longhorn beetles in primeval forests of Northeastern Poland. Biol. Conserv. 51 (4), 287–297. https://doi.org/10.1016/0006-3207(90)90114-5 Hamilton, M.B., 2009. Population Genetics. Wiley-Blackwell, West Sussex. Hedrén, M., Klein, E., Teppner, H., 2000. Evolution of Polyploids in the European Orchid Genus Nigritella: evidence from Allozyme Data. Phyton 40 (2), 239–275. Hedrén, M., Lorenz, R., Teppner, H., Dolinar, B., Giotta, C., Griebl, N., Hansson, S., Heidtke, U., Klein, E., Perazza, G., Ståhlberg, D., Surina, B., 2017. Evolution and systematics of polyploid Nigritella (Orchidaceae). Nord. J. Bot. 36 (3), 01539. https://doi.org/10.1111/njb.01539 Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., Jarvis, A., 2005. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978. https://doi.org/10.1002/joc.1276 Hoelzer, G.A., Drewes, R., Meier, J., Doursat, R., 2008. Isolation-by-distance and outbreeding depression are sufficient to drive parapatric speciation in the absence of environmental influences. PloS Comput. Biol. 4 (7), e1000126. https://doi.org/10.1371/journal.pcbi.1000126 Holmberg, B.J., 2020. A Case Study of a Natural Habitat for Gymnadenia Nigra in Vålådalen, Jämtland, Using Remote Sensing and GIS (Bachelor of Science Thesis). University of Gothenburg. Honnay, O., Jacquemyn, H., 2007. Susceptibility of common and rare plant species to the genetic consequences of habitat fragmentation. Biol. Conserv. 21, 823–831. Jacquemyn, H., Brys, R., Hermy, M., Willems, K.H., 2005. Does nectar reward affect rarity and extinction probabilities of orchid species? An assessment using historical records from Belgium and the Netherlands. Biol. Conserv. 121, 257–263.

Pobrano z https://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 M. Kolanowska, A. Rewicz and S. Nowak Global Ecology and Conservation 27 (2021) e01560

Joffard, N., Massol, F., Grenié, M., Montgelard, C., Schatz, B., 2019. Effect of pollination strategy, phylogeny and distribution on pollination niches of Euro‐Mediterranean orchids. J. Ecol. 107 (1), 478–490. https://doi.org/10.1111/1365-2745.13013 Kaiser, R., 1993. Vom Duft der Orchideen. Olfaktorische und chemische Untersuchungen. Editiones Roche. Kellenberger, R.T., Byers, K.J., Francisco, R.M.D.B., Staedler, Y.M., LaFountain, A.M., Schönenberger, J., Schiestl, F.P., Schlüter, P.M., 2019. Emergence of a floral colour polymorphism by pollinator-mediated overdominance. Nat. Commun. 10, 63. Körner, C., 2003. Alpine Plant Life: Functional Plant Ecology of High Mountain Ecosystems, second ed. Springer,, Berlin. https://doi.org/10.1007/978-3-642- 18970-8 Körner, C., 2016. Plant adaptation to cold climates. F1000Research, 5, F1000 Faculty Rev-2769. https://doi.org/10.12688/f1000research.9107.1. Kremen, C.A., Cameron, A., Moilanen, S.J., Phillips, C.D., Thomas, H., Beentje, J., Dransfield, B.L., Fisher, F., Glaw, T.C., Good, G.J., Harper, R.J., Hijmans, D.C., Lees, E., Louis Jr., R.A., Nussbaum, C.J., Raxworthy, A., Razafimpahanana, G.E., Schatz, M., Vences, D.R., Vieites, M., Zjhra, L., 2008. Aligning conservation priorities across taxa in Madagascar with high-resolution planning tools. Science 320, 222–226. https://doi.org/10.1126/science.1155193 Lamprecht, A., Semenchuk, P.R., Steinbauer, K., Winkler, M., Pauli, H., 2018. Climate change leads to accelerated transformation of high‐elevation vegetation in the central Alps. N. Phytol. 220 (2), 447–459. Llorens, T.M., Macdonald, B., McArthur, S., Coates, D.J., Byrne, M., 2015. Disjunct, highly divergent genetic lineages within two rare Eremophila (Scrophulariaceae: Myoporeae) species in a biodiversity hotspot: implications for taxonomy and conservation. Bot. J. Linn. Soc. 177 (1), 96–111. https://doi.org/10.1111/boj. 12228 Mason, S.J., Graham, N.E., 2002. Areas beneath the relative operating characteristics (ROC) and relative operating levels (ROL) curves statistical significance and interpretation. Q. J. R. Meteorol. Soc. 128, 2145–2166. https://doi.org/10.1256/003590002320603584 Medrano, M., Herrera, C.M., 2008. Geographical structuring of genetic diversity across the whole distribution range of Narcissus longispathus, a habitat-specialist, Mediterranean narrow endemic. Ann. Bot. 102 (2), 183–194. https://doi.org/10.1093/aob/mcn086 Micheneau, C., Fournel, J., Warren, B.H., Hugel, S., Gauvin-Bialecki, A., Pailler, T., Strasberg, D., Chase, M.W., 2010. Orthoptera, a new order of pollinator. Ann. Bot. 105 (3), 355–364. https://doi.org/10.1093/aob/mcp299 Moen, A., Øien, D.I., 2002. Ecology and survival of Nigritella nigra, a threatened orchid species in Scandinavia. Nord. J. Bot. 22 (4), 435–461. https://doi.org/10. 1111/j.1756-1051.2002.tb01398.x Moore, D.M., 1980. Gymnadenia R.Br., Nigritella L.C.M. Richard. In: Tutin, T.G., Heywood, V.H., Moore, D.M., Valentine, D.H., Walters, S.M., Webb, D.A. (Eds.), Flora Europea. vol. 5. Cambridge University Press, pp. 332–333. Moss, R., Babiker, W., Brinkman, S., Calvo, E., Carter, T., Edmonds, J., Elgizouli, I., Emori, S., Erda, L., Hibbard, K., Jones, Roger, N., Kainuma, M., Kelleher, J., Lamarque, J.F., Manning, M., Matthews, B., Meehl, J., Meyer, L., Mitchell, J., Nakicenovic, N., ONeill, B., Pichs, R., Riahi, K., Rose, S., Stouffer, R., van Vuuren, D., Weyant, J., Wilbanks, T., van Ypersele, J.P., Zurek, M., 2008. Towards New Scenarios for Analysis of Emissions, Climate Change, Impacts, and Response Strategies. Intergovernmental Panel on Climate Change. Müller, H., 1874. Fertilisation of flowers by insects. Nature 11, 110–112. https://doi.org/10.1038/011110a0 Müller, H., 1881. Alpenblumen, ihre Befruchtung durch Insekten und ihre Anpassung an dieselben. W. Engelmann, Leipzig. Neilson, R.P., Pitelka, L.F., Solomon, A.M., Nathan, R., Midgley, G.F., Fragoso, J.M.V., Lischke, H., Thompson, K., 2005. Forecasting regional to global plant migration in response to climate change. Bioscience 55, 749–759 https://doi.org/10.1641/0006-3568(2005)055[0749:FRTGPM]2.0.CO;2. Parmesan, C., Yohe, G., 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42. https://doi.org/10.1038/ nature01286 Paušič, I., 2015. Confirmation of the Austrian vanilla orchid, Nigritella austriaca (Teppner & E. Klein) P. Delforge (Orchidaceae) a new Species in the Slovenian flora. Folia Biol. Geol. 56 (1), 115–123. Pearson, R.G., Raxworthy, C.J., Nakamura, M., Townsend Peterson, A., 2006. Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J. Biogeogr. 34, 102–117. Pfeifer, M., Passalacqua, N.G., Bartram, S., Schatz, B., Croce, A., Carey, P.D., Kraudelt, H., Jeltsch, F., 2010. Conservation priorities differ at opposing species borders of a European orchid. Biol. Conserv. 143 (9), 2207–2220. Pfeifer, M., Schatz, B., Xavier Pico, F., Passalacqua, N.G., Fay, M.F., Carey, P.D., Jeltsch, F., 2009. Phylogeography and genetic structure of the orchid Himantoglossum hircinum (L.) Spreng. across its European central–marginal gradient. J. Biogeogr. 36 (12), 2353–2365. Phillips, S.J., Anderson, R., Schapire, R.E., 2006. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190, 231–259. https://doi.org/10. 1016/j.ecolmodel.2005.03.026 Phillips, S.J., Dudík, M., Elith, J., Graham, C.H., Lehmann, A., Leathwick, J., Ferrier, S., 2009. Sample selection bias and presence-only distribution models: implications for background and pseudo-absence data. Ecol. Appl. 19, 181–197. Phillips, S.J., Dudík, M., Schapire, R.E., 2004. A maximum entropy approach to species distribution modeling. in: ICML '04. Proceedings of the twenty-first international conference on Machine learning. ACM, New York. Phillips, R.D., Reiter, N., Peakall, R., 2020. Orchid conservation: from theory to practice. Ann. Bot. 126, 345–362. https://doi.org/10.1093/aob/mcaa093 Piñeiro Fernández, L., Byers, K.J.R.P., 2,3, Cai, J., Sedeek, K.E.M., Kellenberger, R.T., Russo, A., Qi, W., Fournier, C.A., Schlüter, P.M., 2009. A phylogenomic analysis of the floral transcriptomes of sexually deceptive and rewarding European Orchids, Ophrys and Gymnadenia. Front. Plant Sci. 10, 1553. Pridgeon, A.M., Cribb, P.J., Chase, M.W., Rasmussen, F.N., (Eds.), 2001. Genera Orchidacearum Volume 2: Orchidoideae (Part one). Oxford University Press, Oxford, pp. 294ff. Reddy, S., Davalos, L.M., 2003. Geographical sampling bias and its implications for conservation priorities in Africa. J. Biogeogr. 30, 1719–1727. Reese, G.C., Wilson, K.R., Hoeting, J.A., Flather, C.H., 2005. Factors affecting species distribution predictions: a simulation modeling experiment. Ecol. Appl. 15, 554–564. Scherrer, D., Körner, C., 2010. Infra-red thermometry of alpine landscapes challenges climatic warming projections. Glob. Chang. Biol. 16, 2602–2613. https://doi. org/10.1111/j.1365-2486.2009.02122.x Schmitt, T., Muster, C., Schönswetter, P., 2010. Are disjunct Alpine and Arctic-Alpine animal and plant species in the Western Palearctic Really “Relics of a Cold Past”? In: Habel, J.C., Assmann, T. (Eds.), Relict Species: Phylogeography and Conservation Biology. Springer-Verlag, Berlin and Heidelberg, pp. 239–252. Ståhlberg, D., 1999. Polyploid evolution in the European orchid genus Nigritella: evidence fromDNA fingerprinting. Unpublished MSD thesis, Institute för Systematisk Botanik, Lunds University. https://lup.lub.lu.se/record/2026859. StatSoft, Inc., 2013. STATISTICA (data analysis software system), version 13. 3. www.statsoft.com. Štípková, Z., Tsiftsis, S., Kindlmann, P., 2020. Pollination mechanisms are driving orchid distribution in space. Sci. Rep. 10, 850. https://doi.org/10.1038/s41598- 020-57871-5 Tava, A., Cecotti, R., Confalonieri, M., 2012. Characterization of the volatile fraction of Nigritella nigra (L.) Rchb. F. (Orchidaceae), a rare species from the Central Alps. J. Essent. Oil Res. 24 (1), 39–44. https://doi.org/10.1080/10412905.2012.645644 Teppner, H., 2004. A review of new results in Nigritella (Orchidaceae). – Sprawozdania z posiedzeń komisji naukowych [reports of the scientific committee] Polska Akademia Nauk 46 (2), pp. 111–116. Teppner, H., Klein, E., 1990. Nigritella rhellicani spec. nova und N. nigra (L.) Rchb. f. s. str. (Orchidaceae—Orchideae). Phyton 31, 5–26. Teppner, H., Klein, E., 1993. Nigritella gabasiana spec. nova, N. nigra subsp. iberica subsp. nova (Orchidaceae-Orchideae) und deren Embryologie. Phyton 33 (2), 179–209. Timpe, W., Mrkvicka, A.Ch, 1991. Zur Unterscheidung von Nigritella nigra (L.) Rchb.fil. subsp. austriaca Teppner & Klein und Nigritella rhellicani Teppner & Klein anhand makroskopischer Merkmale. Mitt. Bl. AHO Baden-Württ. 23 (3), 449–466.

Pobrano z https://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23 M. Kolanowska, A. Rewicz and S. Nowak Global Ecology and Conservation 27 (2021) e01560

Vanneste, T., Michelsen, O., Graae, B.J., Olsen Kyrkjeeide, M., Holien, H., Hassel, K., Lindmo, S., Erzsebet Kapás, R., De Frenne, P., 2017. Impact of climate change on alpine vegetation of mountain summits in Norway. Ecol. Res. 32 (4), 579–593. https://doi.org/10.1007/s11284-017-1472-1 Vöth, W., 1999. Lebensgeschichte und Bestäuber der Orchideen am Beispiel von Niederösterreich. Stapfia 65, 182–196. Vöth, W., 2000. Gymnadenia, Nigritella und ihre Bestäuber. J. Eur. Orch. 32, 547–573. Weyant, J., Azar, C., Kainuma, M., Kejun, J., Nakicenovic, N., Shukla, P.R., La Rovere, E., Yohe, G., 2009. Report of 2.6 Versus 2.9 Watts/m2 RCPP Evaluation Panel. IPCC Secr. Wisz, M., Hijmans, R.J., Li, J., Peterson, A.T., Graham, C.H., Guisan, A., 2008. Effects of sample size on the performance of species distribution models. Divers Distrib. 14, 763–773. Zhang, Z., Gale, S.W., Li, J.-H., Fischer, G.A., Ren, M.-X., Song, X.-Q., 2019. Pollen-mediated gene flow ensures connectivity among spatially discrete sub-popu lations of Phalaenopsis pulcherrima, a tropical food-deceptive orchid. BMC Plant Biol. 19, 597. https://doi.org/10.1186/s12870-019-2179-y

Pobrano z https://repozytorium.bg.ug.edu.pl / Downloaded from Repository of University of Gdańsk 2021-09-23