Cities and Disturbed Areas as Man-made Shelters for Orchid Communities

Many species from the family Orchidaceae spread in anthropogenic habitats and numerous studies documenting this process are known. Unfortunately, such data are scattered throughout various papers and reports, sometimes fragmentary and hard to reach (the ‘grey literature’). Scientific elaboration on this topic still lacks a comprehensive review and summary of the scale of this phenomenon. Therefore, the main aim of this study was to gather, review and analyse such data, seeking the answer to the question whether the man-made habitats can be considered as refugee for orchids. The paper summarises data on the occurrence of orchid species in man-made habitats in Europe originating from published and unpublished sources. The particular emphasis was placed in urban habitats. For this purpose, the floristically data from 42 European cities were used. The conducted studies showed that the apohytism phenomenon in the family Orchidaceae was more widespread than had been previously reported. As a result, 70 species of orchids in the distinguished man-made habitats were found. The majority of the species grow on sand and clay pits. The most common species were Epipactis helleborine and Dactylorhiza majalis. The gathered data have confirmed that man-made habitats become refugee for many orchid species in the aftermath of the loss of their natural habitats. Thus, protection of sites transformed by man with orchid occurrence should be taken into consideration. These sites can become a source of very useful information for biogeographically and phylo-geographically analyses of many valuable and endangered species.


Introduction
Increasing anthropogenic impact on the environment and the related environmental transformation may result in the shrinking of areas of natural habitats or in the creation of substitute habitats novel in terms of ecological conditions (Jongman, 2002;Walker, 2007;Brun, 2009;Lundholm and Richardson 2010;Yamaura et al., 2012).Plants often respond to the anthropogenic pressure by e.g.: a decline in the number of localities; the disappearance of entire populations; the breakdown of ecological connections, as well as changes of morphological and genetic diversity (Andrews, 1990;Hollingsworth and Dickson, 1997;Vitousek et al., 1997;Reisch, 2006;Walker, 2007;Van Calster et al., 2008;Niedrist et al., 2009;Rewicz et al., 2016;Zielińska et al., 2016).However, a couple of indigenous species found suitable conditions in anthropogenic habitats (Formant et al., 2009;Efimov, 2011;van Kleef et al., 2012;Yamaura et al., 2012).Those new habitats, often created by man, give many plant species a chance to survive.Moreover, the most flexible species may increase the number of localities and expand within, even outside the original geographical range.
Europe.In this paper, recent as well as historical data about orchids occurring in man-made habitats were reviewed to draw attention to this phenomenon and to provide a basis for future research.Besides the predominant review function of this paper, the final data set was used to address the question whether transformed areas can be important substitute sites for orchid species endangered in their natural landscape, and also to define the spectrum of anthropogenic habitats occupied by the species.

Data sources
The complete list of orchid species occurring in man-made habitats was prepared based on available literature data, including information published in scientific articles and data from the "grey literature", such as local monographs or technical reports.The paper included all types of anthropogenic habitats where orchids were found.The analyses covered only such species of orchids which had the apophyte status in the city i.e. native plants established in anthropogenic habitats (Jackowiak, 2006;Sukopp, 2006).We did not take into account species found in nontransformed areas which sometimes lie inside the urban areas, for example: protected areas or forest complexes located within administrative boundaries of cities.The distinguished anthropogenic habitats were grouped into eight categories: (A) forests influenced by industrial emissions; (B) industrial terrains; (C) industrial waste places; (D) greenery -parks, hedges, etc.; (E) plantations of ecologically alien trees; (F) plantations of nonnative trees; (G) roadsides and embankments; (H) sand pits, clay pits and quarries.
For the analysis of occurrence of orchids in urban habitats, we selected available materials comprising complete lists of urban flora of 42 European cities, mainly from the area of Central and Northern Europe (Table 1).
Orchids occurring in urban habitats were grouped into frequency classes of the following categories (the number of occurrences of the species in all of the cities): I -up to 20%, II -20-39%, III -40-59%, IV -60-79%, V -80-100%.
Due to somewhat diversified extent of floristic studies carried out at various locations, data on species occurrence was encoded in a binary fashion (0-1, absent-present), without taking into account the degrees of quantitative occurrence.

Data analysis
Spearman's rank correlation coefficients were used for the analysis of the correlation between the area of the examined cities and the number of orchid species and between the total numbers of vascular plants in particular cities and the number of orchids.The results were considered to be statistically significant for p < 0.05.The Detrended Correspondence Analysis (DCA) was used to assess variability within individual habitats in terms of occurrence of species from the Orchidaceae family.The software package STATISTICA PL. ver. 10 and Canoco ver.4.5 were used for all the above-mentioned numerical analyses (Statsoft Inc, 2013;Leps and Smilauer, 2003).

Orchidaceae in anthropogenic habitats
As a result, 70 species of orchids in the investigated man-Generally, man-made areas are settled by common species demonstrating wide tolerance to habitat conditions (Latzel et al., 2011;Piekarska-Stachowiak et al., 2014).However, disturbed habitats could also function as a refuge for rare and endangered plants (Greenwood and Gemmell, 1978;Heindl and Ullmann, 1991;Ullmann et al., 1998;Brändle et al., 2003;Nowak, 2005Nowak, , 2006;;Nowak and Nowak, 2006;Esfeld et al., 2008;Kirpluk and Bomanowska, 2008;Reisch, 2006;van Kleef et al., 2012;Zielińska et al., 2016).Surprisingly, orchids are often found in the apophytes group, but they are still one of the most threatened plant groups in the world (Sharrock and Jones, 2009;Bliz et al., 2011; The IUCN Red List of Threatened Species 2015).The disappearance of natural habitats of orchids is well documented.Industrialisation and the related urbanisation are transforming natural habitats with side effects such as air, soil and water pollution, which are responsible for reducing orchid populations (McCormick et al., 2004;Pfeifer and Jetschke, 2006;Sukopp, 2006;Rewicz et al., 2015).On the other hand, numerous studies have revealed that some orchid species were found in a great number of individuals in anthropogenous habitats that were either grossly modified by man or entirely man-made (Davis, 1979;Adamowski and Conti, 1991;Hollingsworth and Dickson, 1997;Adamowski, 2002Adamowski, , 2006;;Heyde and Krug, 2000;Ehlers et al., 2002;Klimko et al., 2004;Light andMacConaill, 2005, 2006;Witting and Witting, 2007;Esfeld et al., 2008;Pedersen et al., 2013;Rewicz et al., 2016).Members of the family Orchidaceae can be found in varius types of anthropogenic habitats e.g.: roadsides, waste dumps, railway embankments, canal banks, poplar plantations, gravel pits, chalk and limestone quarries, lignite mining areas, etc. (e.g.: Davis, 1979;Adamowski, 2006;Esfeld et al., 2008).Such behaviour has been observed since the 19th century, when orchids were noticed on railway embankment and in sand limestone excavations in the United Kingdom for the first time (Prochazka and Velisek, 1983).According to Adamowski (2006), 53 orchid species occur in anthropogenically altered habitats, which is about 40% of the entire European flora of these plants.The most common taxa spread in secondary habitats in temperate Europe are species from the genus Epipactis and Dactylorrhiza.Those orchids have a shorter life cycle and broader ecological amplitudes in comparison to the other taxa (Adamowski, 2006).
Recently, in the scientific literature there are more and more reports indicating the appearance of orchids in urban areas (e.g.: Chronopoulos and Christodoulakis, 1996;Heinrich and Dietrich, 2008;Stefaniak et al., 2011;Barrico et al., 2012;Milović and Mitić, 2012;Tafra et al., 2012;Maslo, 2014;Stešević et al., 2014).This phenomenon needs special attention as towns and cities are a kind of conglomerates of transformed habitats which are not in the immediate vicinity of habitats natural for the analysed species.
Although the phenomenon of orchid species spreading onto transformed areas has been known for a long time and has been widely reported, there is a lack of research papers summarising the state of knowledge concerning this process.Therefore, the aim of the undertaken study was to complete the scattered data and to review the available information related to orchid species occurring in various man-made habitats, with a particular focus on urban habitats across made habitats were recorded (Table 2).The most common orchids occurring in the analysed anthropogenic sites were species from the genus Epipactis -E.helleborine, which occurred in all the types (8) of habitats, E. atrorubens recorded in six various habitats, and E. palustris observed in five (Fig. 1).
Numerous species were found in sand pits, clay pits, quarries (48), as well as on roadsides and embankments (35; Table 2).The most common species of orchids in these habitats were: E. helleborine (34) recorded 17 times on roadsides and embankments, E. palustris (18) recorded eight times in sand pits, clay pits and quarries, and E. atrorubens (18) recorded seven times on roadsides and embankments (Fig. 2).

Orchidaceae in urban areas
In 42 analysed cities, 79 species of the Orchidaceae family, which belong to 25 genera, were found.The majority of the species (17) belong to the genus Ophrys, 12 to the genus Dactylorhiza and 8 to the genus Epipactis respectively.
The number of occurrences of orchids in the cities ranged from 1 up to 33.The largest numbers of species of orchids were reported in Rome (33), and also in Chernivtsi ( 23), Podgorica (20), and Warsaw (19).In ten cities, only one species of Orchidaceae was found (Table 3).
The analysis of the frequency classes of the particular taxa occurrences showed that the majority of the specimens belong to the first two classes of frequency: 54 species belong to the I class and 14 to the II class (Table 3).Only four species: Epipactis helleborine, Dactylorhiza incarnata, Listera ovata and Platantera bifolia belong to the most frequent classes (IV-V; Table 3).
The correlation between the area of the cities and the number of orchid species (r=0.1871) and between the number of all the species and the number of the orchid species in the city (r=-0.1571)was not very strong and statistically not significant in each case (Spearman's rank correlation, p<0.05).
The analysis of the available data has shown that populations of some species remain on anthropogenic habitats for several years, hence they can be called euapophytes (apophytes sensu stricto, i.e. permanently established in anthropogenic habitats) (Jackowiak, 2006).The same phenomenon was confirmed in the studies conducted by Adamowski and Conti (1991) and Adamowski (2006) on Epipactis helleborine and Platanthera bifolia growing in poplar plantations.Their observations show that populations of these orchids have remained in disturbed habitats for up to 25 years.Similar results were obtained by Light andMacConaill (2005, 2006) on Epipactis helleborine, and also by Stark (2010) on Gymnadenia conopsea, and Wyrzykiewicz-Raszewska et al. (2001) on Epipactis palustris.
Anthropogenic habitats not only become refugia for species considered to be rare or even endangered, but often have an impact on the phenotypic plasticity of their specimens, as well as demographics and the life story of entire populations.Quintana-Ascencio et al. (2007) has proven that populations of endemic species of Hypericum cumulicola from Florida growing in disturbed populations are characterised by shorter life length, faster growth and earlier production of seeds while compared to natural populations.Similar conclusions concerning phenotypic variation and maintaining the population of Epipactis helleborine on roadsides were drawn by Rewicz (2015, unpublished data) and Rewicz et al. (2016).
Such a great number of orchid species in various anthropogenic habitats poses the question as to whether manmade habitats are an "ecological equivalent" to naturally occurring habitats.It is pointed out that anthropogenic sites can be considered as temporary shelters, rather than mainstays, from which plants can expand further.Frequently, these refugia play the role of corridors for expansion of species and links between natural populations (Nowak and Nowak 2006;Esfeld et al., 2008;van Kleef et al., 2012).Orchid species composition in anthropogenic habitats is a reflection of the species composition in the adjacent habitats, as well as of the geographical range of plants.Thus, it can explain the presence of the species from the genus Dactylorhiza and Epipactis in Eastern Europe, and the occurrence of the species from the genus Serapias and Ophrys in Western Europe.In the analysis of orchid occurrence in particular cities, it has also been observed that in Central European cities the species mentioned above dominate, while in the group of Balkan towns the species of the genus Ophrys and Serapias are dominant.This is due to the geographical ranges of the analysed taxa and the number of urban areas within the given part of Europe.In the case of the Balkans, the species of the Ophrys or Serapias genus are much more abundant, while in Central Europe and in the Ukraine those species do not occur (Delforge, 2006).The prevalence of orchids and other valuable plants in anthropogenic habitats should draw attention to the problem of maintaining rare and endangered species in non-natural ecological systems (van Kleef et al., 2012;Zielińska et al., 2016).Although currently there is no literature data about species conservation carried out in populations of orchids in anthropogenic habitats, such populations should be observed in terms of their condition and stability.
Furthermore, occurrence of orchids in anthropogenic habitats provides an opportunity to use those populations in the educational process.Very often, those species are protected by law, hence it is possible to make some nature trails and organise outdoor lessons, enhancing nature conservation knowledge.

Conclusions
The conducted review has shown that some man-made and disturbed habitats host many rare orchids and could provide a chance for survival of those rare and valuable plant species.The need for the protection of sites of valuable orchid species in habitats strongly transformed by man should be taken into consideration at the present time. 133

Fig. 1 .
Fig. 1.The most common orchid species in various distinguished types of man-made habitats Fig. 2. The most frequently orchid species in the distinguished types of man-made habitats.(A) forests influenced by industrial emissions; (B) industrial terrains; (C) industrial waste places; (D) parks, hedges etc. greenery; (E) plantations of ecologically alien trees; (F) plantations of non-native trees; (G) roadsides and embankments; (H) sand pits, clay pits and quarries

Fig. 3 .
Fig. 3. Ordination diagram based on Detrended Correspondence Analysis (DCA) showing connection of orchid species to the different types of man-made habitats.A, B... H -distinguished types/kinds of man-made habitats, see Fig. 2

Table 1 .
List of cities in which orchid species on man-made habitats were noted

Table 3 .
Orchids species noted in analyzed cities