Tourism and recreation: a common threat to IUCN red-listed vascular plants in Europe

Author Ballantyne, Mark, Pickering, Catherine Marina

Published 2013

Journal Title Biodiversity and Conservation

DOI https://doi.org/10.1007/s10531-013-0569-2

Copyright Statement © 2013 Springer. This is an electronic version of an article published in Biodiversity and Conservation, December 2013, Volume 22, Issue 13-14, pp 3027-3044. Biodiversity and Conservation is available online at: http://link.springer.com/ with the open URL of your article.

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1 Tourism and recreation: a common threat to IUCN red-listed vascular 1 2 3 4 2 plants in Europe 5 6 7 8 3 *Mark Ballantyne and Catherine Marina Pickering 9 10 11 12 4 Environmental Futures Centre, School of Environment, Griffith University, Gold Coast, 13 14 5 Queensland 4222, Australia 15 16 17 18 6 *Corresponding author email: [email protected], telephone: +61(0)405783604 19 20 21 7 22 23 8 24 25 9 26 27 28 10 29 30 11 31 32 12 33 34 13 35 36 37 14 38 39 15 40 41 16 42 43 17 44 45 46 18 47 48 19 49 50 20 51 52 21 53 54 55 22 56 57 23 58 59 24 60 61 62 63 64 65 25 Abstract 1 2 3 4 26 Tourism and recreation are large industries employing millions of people and contribute over 5 6 27 US$2.01 trillion to the global economy. Unfortunately they also have diverse and sometimes severe 7 8 28 environmental impacts affecting many species, including those that are rare and threatened. To 9 10 11 29 assess the extent to which these industries threaten vascular plants, we reviewed data in the IUCN 12 13 30 Red List for 462 Critically Endangered, Endangered and Vulnerable European species. Tourism and 14 15 16 31 recreation were listed as threatening 42% (194 species) of these species from across 50 families, 17 18 32 mostly herbs (70%). They were listed as threatening plants in 9 of the 10 bioregions in Europe and in 19 20 33 25 of the 40 countries assessed. Popular tourism destinations such as the Canary Islands (41 species) 21 22 23 34 and mainland Spain (40 species) had the greatest diversity of species listed as threatened by tourism 24 25 35 and recreation. The most common of these threats were trampling (61 species), plant collection (59), 26 27 36 the maintenance/construction of tourist infrastructure (43) and habitat degradation due to the 28 29 30 37 urbanisation of tourist sites (13). Additional species assessments and more research on the impacts 31 32 38 of tourism and recreation may add to these values. It is clear that these industries pose an important 33 34 35 39 threatening process on plants in Europe based on the IUCN Red List data and hence deserve greater 36 37 40 recognition in terms of research, conservation and management. 38 39 40 41 Key Words 41 42 43 42 Endangered species, vegetation trampling, plant collecting, infrastructure impacts, Mediterranean 44 45 46 43 flora 47 48 49 44 Introduction 50 51 52 53 45 Tourism and recreation are large, rapidly expanding global industries (Cornelissen 2005; McCool and 54 55 46 Moisey 2009; WTTC 2012). During 2011 there were 983 million tourist arrivals worldwide; up 4.6% 56 57 58 47 from 2010 (UNWTO 2012). In Europe, tourism and recreation contributed 8% to gross domestic 59 60 48 product in 2011, with an expenditure of >US$1,700 billion and the provision of nearly 10 million jobs 61 62 63 64 65 49 (WTTC 2012). In the same year Europe experienced the most rapid growth in tourism globally, 1 2 50 receiving 504 million tourist arrivals; over half of all international tourist arrivals worldwide (UNWTO 3 4 5 51 2012). This growth is likely to continue with tourist arrivals predicted to reach 628 million by 2022 6 7 52 (WTTC 2012). Within Europe, tourism is highly concentrated in a few particular hotspots with the 8 9 53 majority of international arrivals in the Mediterranean (Amelung and Viner 2006). 10 11 12 13 54 The benefits of tourism and recreation come with costs including those from a range of negative 14 15 55 environmental impacts on water, soil, animals and plants (Liddle 1997; Myers et al. 2000; Van der 16 17 56 Duim and Caalders 2002; Butchart et al. 2010; Steven et al. 2011). Damage to plants includes 18 19 20 57 obvious effects of vegetation removal and changes to soils during the construction and maintenance 21 22 58 of tourist and recreational infrastructure such as coastal resorts, golf courses and ski-runs (Buckley 23 24 59 et al. 2000; López-Pujol et al. 2003; Peñas et al. 2011). However, even comparatively low-key nature- 25 26 27 60 based activities such as hiking can trample plants reducing vegetation cover, biomass and height 28 29 61 (Liddle 1997; Cole 1995; Cole 2004; Pickering et al. 2011). Some visitors to natural areas harvest 30 31 32 62 flowers and other plant parts threatening charismatic species such as rare orchids (Ballantyne and 33 34 63 Pickering, 2012a). In addition, there are other less obvious impacts such as tourists spreading weeds 35 36 64 and pathogens, altering fire regimes and degrading habitat quality and functioning (Benninger-Truax 37 38 39 65 1992; Kelly et al. 2003; Buckley et al. 2004; Pickering and Mount 2010; Müllerová et al. 2011). As a 40 41 66 result, sensitive plant communities and species may decline while resistant species such as weeds 42 43 67 dominate modified ecosystems (Liddle 1997; Cole 2004; Leung and Marion 2000; Pickering and Hill 44 45 46 68 2007a; Hamberg et al. 2008; Pickering et al. 2010; Monz et al. 2010). These impacts can be 47 48 69 particularly severe for species and communities already threatened with extinction (Kelly et al. 2003; 49 50 51 70 Lavergne et al. 2005; Rossi et al. 2009; Moxham and Turner 2011). 52 53 54 71 Despite such well recognised environmental impacts, there is limited specific, experimental and 55 56 72 quantitative research on the impacts of tourism and recreation on threatened plants (Pickering and 57 58 59 73 Hill 2007a; Ballantyne and Pickering 2012a). A few exceptions include work in the USA (Maschinski et 60 61 62 63 64 65 74 al. 1997), Spain (Peñas et al. 2011) and Italy (Fenu et al. 2013). The majority of available information 1 2 75 is observational, and this data is often used within threatened species listings and for comparative 3 4 5 76 reviews. These listings have been drawn upon for comparing threats to plant families (Ballantyne 6 7 77 and Pickering 2012a) as well as threats to plant species within countries (Kelly et al. 2003), but few 8 9 78 have used them to assess impacts to plant species across larger continents or bioregions. 10 11 12 13 79 Europe has high biodiversity including around 20,000 species of vascular plants (Euro+Med 14 15 80 Plantbase 2012), many of which are endemic and many of socio-economic value (Kell et al. 2008; 16 17 81 Sharrock and Jones 2009; Bilz et al. 2011). With the cessation of traditional farming practises and the 18 19 20 82 increase in intensified modern agriculture and urbanisation, populations of many plant species are 21 22 83 declining (Luijten et al. 2000; Walker et al. 2004; Raijmann et al. 2006; Peñas et al. 2011; Bilz et al. 23 24 84 2011). By 1997, around 3,250 species (30% of them from Spain) had been listed as threatened to 25 26 27 85 some degree (Walter et al. 1997) and today 650 species are documented as extinct or facing 28 29 86 extinction (Planta Europa, 2008). 30 31 32 87 The contribution of tourism and recreation to this process is not widely recognised nor addressed in 33 34 35 88 conservation policy documents such as the current European Strategy for Plant Conservation. A few 36 37 89 reports (Montmollin and Strahm 2005; Bilz et al. 2011) briefly mention tourism and recreation as an 38 39 40 90 important threat and highlight that the expansion of these industries must be closely monitored and 41 42 91 managed if they are to develop sustainably. 43 44 45 92 Here we advance on this knowledge by reviewing the extent to which tourism and recreation 46 47 48 93 threaten IUCN red-listed European plants. Using the European database for the International Union 49 50 94 for the Conservation of Nature (IUCN), we assess: i) the number of species threatened by tourism 51 52 95 and recreation, ii) where these species are threatened, iii) the types of plants most at risk, iv) the 53 54 55 96 common types of threats from tourism and recreation and v) the implications for future tourism, 56 57 97 recreation and plant conservation in Europe. 58 59 60 61 62 63 64 65 98 Methodology 1 2 3 4 99 Critically Endangered, Endangered and Vulnerable vascular plant species and subspecies from 5 6 100 Europe were identified from the IUCN Red List (available at http://www.iucnredlist.org/) during April 7 8 101 and May 2012. In the current study we used ‘Europe’ to refer to the 10 million km2 of continental 9 10 11 102 land and islands that extends from the Azores and Iceland in the Atlantic Ocean as far east as the 12 13 103 border with Asian Russia, Turkey and the Caucasus and as far north as Svalbard (Norway) and south 14 15 16 104 to the Canary Islands in the Atlantic and Cyprus in Mediterranean Sea. Within this area there are 10 17 18 105 recognised bioregions: Alpine, Atlantic, Black Sea, Boreal, Continental, Macaronesia, Mediterranean, 19 20 106 Pannonian, Steppe and Arctic (European Commission 2012). We did not look at species from Turkey 21 22 23 107 and Russia as their floras are also largely part of the Asian region. The Spanish and Portuguese island 24 25 108 territories of Macaronesia, however, were included as they form part of the European geopolitical 26 27 109 area. National level assessments and other red lists were not used for this initial listing as: i) a 28 29 30 110 species may be threatened in one country but not throughout its entire distribution, ii) there are 31 32 111 inconsistencies in the classification of threat statuses among national lists and iii) they often lack 33 34 35 112 information on threatening processes for individual species (Sharrock and Jones 2009; Bilz et al. 36 37 113 2011). 38 39 40 114 For each species identified on the IUCN Red List as native to Europe, information was entered into a 41 42 43 115 database including scientific and common names (incl. synonyms), growth-form, IUCN status, 44 45 116 population trend, listing year, native distribution (countries), whether the species was a national or 46 47 117 regional endemic, habitat type and bioregion. The Angiosperm Phylogeny Group III system was 48 49 50 118 consulted for information on each species’ family (Angiosperm Phylogeny Group, 2013). Growth 51 52 119 form was determined either from the in-text IUCN profile information for each species or by 53 54 120 researching each species in online herbaria or botanical journals. For those species whose 55 56 57 121 distribution overlapped two or more bioregions, the one with the majority of populations was used. 58 59 122 Furthermore, plants were only listed in the Alpine bioregion if they were recorded growing between 60 61 62 63 64 65 123 the tree-line (roughly 1,800m) and the permanent snow line (roughly 2,500m) of Europe’s Alps, 1 2 124 Carpathians, Pyrenees and Apennines. 3 4 5 125 Using the details provided within the IUCN Red List, information about tourism and recreation as a 6 7 8 126 threatening process was entered for each species. The criteria we used for listing tourism as a threat 9 10 127 were either that the terms ‘tourism’ and/or ‘recreation’ were specifically stated as a threat in the 11 12 13 128 Red List, or if one or more populations of the species were stated to be directly threatened by 14 15 129 tourism and recreation activities, impacts or infrastructure. Plant collecting was included as a threat 16 17 130 only if the listing stated that the plants were being collected by visitors, tourists or enthusiasts and 18 19 20 131 not for medicinal or commercial purposes and the populations where they were being collected 21 22 132 were in protected areas or tourism hotspots. Despite tourism and recreation contributing to the 23 24 133 spread of weeds and pathogens (Pickering and Mount 2010; Pickering and Hill 2007a), we did not 25 26 27 134 include these types of threats in our analysis because detailed information was not provided on 28 29 135 whether they were a result of tourism or recreation. Similar IUCN Red List-based methods have also 30 31 32 136 been used for other comprehensive reviews on the threats, and benefits, of tourism and recreation 33 34 137 toward birds, frogs and mammals (Steven et al. 2011; Morrison et al. 2012; Buckley et al. 2012). 35 36 37 138 Initially, 425 species were identified as threatened by tourism and recreation based on the IUCN Red 38 39 40 139 List, but when this was cross-checked with the European Red List of Vascular Plants (Bilz et al. 2011) 41 42 140 an additional 64 species were identified that had IUCN threat profiles but which were not identified 43 44 141 using the search engine, and an additional 59 species were identified which did not have IUCN 45 46 47 142 profiles but were listed as threatened within Europe under EU or regional policy instruments 48 49 143 (namely CITES, EU Habitats Directive, Bern Convention and EU Wildlife Trade Regulation). These 50 51 144 species were often not restricted to Europe and/or were subspecies for which official nomenclature 52 53 54 145 is ambiguous (e.g. Anchusa crispa subspecies). Of this expanded list of 548 species in the database, 55 56 146 the 59 species without IUCN profiles and a further 27 species which lacked information on threats 57 58 59 147 were excluded from further analysis leaving a final total of 462 species that could be assessed. 60 61 62 63 64 65 148 Data Analysis 1 2 3 4 149 The total number and proportion of species listed by growth form that were threatened by tourism 5 6 150 and recreation in Europe was calculated. Chi-square tests were performed to determine whether 7 8 151 there were significant differences in threats depending on growth form. The total number of 9 10 11 152 threatened species and number specifically threatened by tourism and recreation were calculated 12 13 153 for each country and compared with the size of the national floras, the number of endemics and the 14 15 16 154 percentage of land in protected areas. The numbers of species threatened by different types of 17 18 155 tourism or recreational activities, impacts, and infrastructures were also calculated. 19 20 21 22 156 Results 23 24 25 157 Tourism and recreation was considered to threaten 194 (42%) of the 462 species assessed based on 26 27 28 158 the information within the IUCN Red Listings. The terms ‘tourism’ and ‘recreation’ were used in the 29 30 159 listing documents for 180 of these species and could be inferred based on details of threats for a 31 32 160 further 14 species (online resource). Of this total, 136 species were herbs reflecting their high 33 34 35 161 diversity in Europe and the large number of threatened herbs on the IUCN Red List (Table 1). There 36 37 162 was only a handful of ferns (2 species) and aquatic plants (5) threatened by tourism and recreation 38 39 163 but few of these plants were actually listed by the IUCN anyway. As a result, there was no significant 40 41 42 164 difference among growth forms and in the likelihood that tourism and recreation was a threat 43 44 165 among the red-listed species (Chi-square test, p > 0.05). 45 46 47 166 Tourism and recreation threatened a diverse range of plants from 50 families. Those with the most 48 49 50 167 species threatened by tourism and recreation include the Asteraceae (32 species), Orchidaceae (15), 51 52 168 Caryophyllaceae (15), Fabaceae (14), Brassicaceae (11) and Poaceae (6). Among the Asteraceae 53 54 169 some genera had several species threatened by tourism and recreation including six species of star- 55 56 57 170 thistle (Centaurea), four species of rock-centaury (Cheirolophus) and three species of everlasting 58 59 171 daisy (Helichrysum): all from the Mediterranean or Macaronesia. Orchids threatened by tourism and 60 61 62 63 64 65 172 recreation included four species of vanilla orchid (Gymnadenia) from the Alps and four species of 1 2 173 helleborine (Epipactis) from central Europe. Four sandworts (Moehringia) from the Caryophyllaceae 3 4 5 174 family were also threatened by tourism and recreation and all from southern Europe. 6 7 8 175 The vast majority of species threatened by tourism and recreation were single country endemics 9 10 176 (87%) with only 15 species’ native distributions extending beyond Europe into North Africa or West 11 12 13 177 Asia. There was a geographical bias in the location of plants threatened by tourism and recreation 14 15 178 (Table 2). Many were from the Canary Islands (41 species), mainland Spain (40), Greece (17), 16 17 179 mainland Portugal (16), Italy (16), Sardinia (11) and Madeira (11). As these locations are part of the 18 19 20 180 Mediterranean and Macaronesian bioregions, the two bioregions had proportionally more red-listed 21 22 181 species threatened by tourism and recreation; 51% and 29%, respectively (Table 3). In contrast there 23 24 182 were few species threatened by tourism and recreation in the Alpine (15 species), Continental (12), 25 26 27 183 Steppic (4), Black Sea (4), Pannonian (3), Atlantic (1), Boreal (1) and Arctic (0) bioregions. For the 28 29 184 latter 3 bioregions, this partly reflects their naturally low plant diversity. 30 31 32 185 When the proportion of red-listed species threatened by tourism and recreation was calculated out 33 34 35 186 of the total species listed per country, a different pattern emerged (Table 2). In this case, countries 36 37 187 where most, or all, IUCN red-listed listed species were threatened by tourism and recreation 38 39 40 188 included Slovakia (100%), Switzerland (100%), Montenegro (100%), Slovenia (86%), Portugal (82%) 41 42 189 and Austria (75%) although all of them, other than Portugal, also had few species listed (Table 2). 43 44 45 190 A total of 35 species were listed as threatened by tourism and recreation but did not include details 46 47 48 191 specifying how. For those species where details were provided, there were 15 types of activities, 6 49 50 192 impacts and 5 types of tourism and recreation infrastructure listed as threats (Table 4). Two thirds 51 52 193 (65) of the species were threatened by more than one activity, impact and/or infrastructure. The 53 54 55 194 most commonly listed threatening activities were collecting plants (59 species), rock-climbing and 56 57 195 mountaineering (12), driving recreational vehicles (10), camping/picnicking (5), horse-riding (5), and 58 59 196 trail/mountain-biking (3). Among tourism and recreation impacts, those frequently listed were 60 61 62 63 64 65 197 trampling (61 species), habitat degradation resulting from urbanising tourist sites (13), altered fire 1 2 198 regimes (3), physical vegetation damage (3) and erosion by walkers (2). The maintenance and/or 3 4 5 199 creation of tourist infrastructure (including ski-runs, hotels, pools, restaurants and golf-courses) 6 7 200 affected 43 species while the construction/maintenance of walking tracks, roads and car-parks for 8 9 201 tourism and recreation threatened 16 species. 10 11 12 13 202 Plant collection threatened many charismatic and showy plants such as orchids (Epipactis and 14 15 203 Gymnadenia), fritillaries (Fritillaria) and daffodils (Narcissus) but was also important for other 16 17 204 families such as the Fabaceae and Plantaginaceae. Collecting was a threat to 52% of listed bulb or 18 19 20 205 pseudobulb species. Trampling frequently threatened low-growing herbs, sub-shrubs and shrubs 21 22 206 including members of the Asteraceae (9 species), Boraginaceae (5), Plumbaginaceae (5), Fabaceae (5) 23 24 207 and Campanulaceae (3). The maintenance and construction of tourist infrastructure threatened a 25 26 27 208 wide variety of growth forms and families but particularly daises (Asteraceae, 10 species). Habitat 28 29 209 degradation as a result of urbanising tourist sites was a threat for rare grasses (Poaceae) on the 30 31 32 210 Black Sea coast. Driving of recreational vehicles threatened herbs and bulbs such as the plantain 33 34 211 Plantago almogravensis, the bugloss Anchusa crispa and the Corsican Saffron (Colchicum corsicum). 35 36 212 As would be expected water-sports and riparian activities threatened aquatic plants while rock- 37 38 39 213 climbing/mountaineering threatened cliff-dwelling (rupicolous) species such as Borderea chouardii. 40 41 42 214 Many species threatened by tourism and recreation had populations within publicly-accessible 43 44 215 protected areas. For 38 red-listed species, >75% of their remaining populations were in protected 45 46 47 216 areas (supplementary material) with the populations of 19 of them listed as being in rapid decline. 48 49 217 Therefore, despite the conservation benefits of many protected areas in mitigating threats such as 50 51 218 urbanisation and forestry, tourism and recreation as allowed activities in these locations may yet 52 53 54 219 remain an issue for many red-listed plants. 55 56 57 220 Discussion 58 59 60 61 62 63 64 65 221 Tourism and recreation poses a significant threat to at least 42% of European IUCN red-listed 1 2 222 vascular plants. It is considered to threaten species in 9 of Europe’s 10 bioregions and in 25 out of 3 4 5 223 the 40 countries and territories assessed, ranging from Finland in the north to the Canary Islands in 6 7 224 the south and from the Azores in the west to the Ukrainian steppe in the east. It is considered to 8 9 225 threaten plants from 50 families and a variety of growth forms, predominantly herbs. Even if those 10 11 12 226 species for which threats were inferred are excluded, tourism and recreation were still directly-listed 13 14 227 threats for 39% (180) of European red-listed vascular plants. 15 16 17 228 The number of species identified here may be an underestimate of those currently threatened by 18 19 20 229 tourism and recreation in Europe. We only included species where specific information about 21 22 230 threats was included in the listing documents. It may be likely that some listed species for which 23 24 231 details about threats were not available, are also threatened by tourism and recreation. In addition, 25 26 27 232 tourism and recreation may threaten species that have not yet been assessed, particularly as some 28 29 233 countries and regions in Europe, particularly the Balkans, have not conducted extensive surveys of 30 31 32 234 threats to biodiversity (Griffiths et al. 2004; Convention on Biological Diversity 2008). Furthermore, 33 34 235 the political instability of countries such as Kosovo has meant that monitoring threats to biodiversity 35 36 236 has not been of primary concern. Further research on the impacts of tourism and recreation on 37 38 39 237 plants is likely to identify more species threatened and more ways in which tourism and recreation 40 41 238 threaten them (Kelly et al. 2003; Pickering and Hill 2007a). 42 43 44 239 Recognition of the generality of threats posed by tourism and recreation is important, as the 45 46 47 240 industry and its impacts are increasing in intensity and spread across Europe (WTTC 2012). For 48 49 241 example, more people are now travelling to previously poorly-visited destinations such as the 50 51 242 former Yugoslav republics, Albania and northern Cyprus (WTTC 2012; Bramwell 2004; Page and 52 53 54 243 Connell 2009; Doda 2012). These regions have few protected areas and, even where species do 55 56 244 occur in such reserves, they are still at risk of increasing disturbance from the rise in visitation. 57 58 59 60 61 62 63 64 65 245 Without adequate recognition of the magnitude of the problem, it’s hard to effectively manage 1 2 246 these threats either in-situ or via legislative processes. 3 4 5 247 Unfortunately, tourism and recreation as threatening processes are not well recognised in many 6 7 8 248 Europe-wide and national policy documents (Secretariat on the Convention on Biological Diversity 9 10 249 2009; CBD 2012a). One of the few exceptions is the European Red List of Vascular Plants (Bilz et al. 11 12 13 250 2011), where tourism and recreation was listed as the second-most important threat for the species 14 15 251 assessed. Many were threatened by the development of tourist infrastructure and activities as well 16 17 252 as the wider-scale damage due to urbanisation of coastlines for tourism. Similarly, a report on 50 of 18 19 20 253 the most endangered plants in the Mediterranean bioregion found tourism and recreation 21 22 254 developments and coastal urbanisation in general to be the most important threats to plant species 23 24 255 (Montmollin and Strahm 2005). However, the report by Bilz et al. 2011 does not give details of 25 26 27 256 exactly how, where and which species are affected by tourism and recreation, and the latter by 28 29 257 Montmollin and Strahm 2005 is limited to just 50 species in one bioregion. 30 31 32 258 The threats from tourism and recreation are not evenly spread over Europe. Here we have shown 33 34 35 259 that tourism and recreation threaten at least 98 species of plants in the Mediterranean bioregion 36 37 260 and 56 species in the Macaronesian bioregion of which 86 (44%) were from Spain and its island 38 39 40 261 territories. Tourism and recreation, however, threaten only 4 species each in the Steppic and Black 41 42 262 Sea bioregions and 1 each in the Boreal and Atlantic. Three factors may be contributing to the 43 44 263 apparent concentration of tourism and recreation threats in the Mediterranean and Macaronesian 45 46 47 264 bioregions. They have high biodiversity, contain many popular tourism destinations, and there is 48 49 265 comparatively more information and research effort about threats to species in these bioregions 50 51 266 than others in Europe. 52 53 54 55 267 The Mediterranean basin contains 25,000 native plant species of which 13,000 are endemic, making 56 57 268 it a biodiversity hotspot containing 4.3% of the global flora (Mooney 1988; Médail and Quézel 1997; 58 59 269 Myers et al. 2000; Francisco-Ortega et al. 2000; Cuttelod et al. 2008). The Macaronesian region also 60 61 62 63 64 65 270 has many endemic, rare and threatened species (Bramwell 1990; Bilz et al. 2011). The Canary Islands 1 2 271 alone have 570 endemic plants, of which 20% are endangered (Francisco-Ortega et al. 2000). Many 3 4 5 272 are African palaeoendemic relicts that evolved unique lineages on the islands (Cronk 1997). 6 7 8 273 The Mediterranean is also one of the most visited tourist destinations globally with visitation ranging 9 10 274 from 100 million to 246 million tourists annually (Amelung and Viner 2006; Cuttelod et al. 2008). The 11 12 13 275 Mediterranean attracts so many visitors largely due to ease of access for many people from the rest 14 15 276 of Europe, its favourable climate and attractive coastline (Davenport and Davenport 2006). The 16 17 277 robust growth of Europe’s tourism economy during 2011 was largely driven by visitation to the 18 19 20 278 Mediterranean region with Greece, Portugal and Spain attracting the most tourists (UNWTO 2012). 21 22 279 Tourism in these places has contributed to the removal of native vegetation through urbanisation of 23 24 280 coastlines (López-Pujol et al. 2003; Montmollin and Strahm 2005; Cuttelod et al. 2008) and the 25 26 27 281 construction and use of popular tourism infrastructures such as resorts and golf courses (Fenu et al. 28 29 282 2011; Peñas et al. 2011). Other impacts come from trampling (Andrés-Aballán et al. 2006), plant 30 31 32 283 collecting (Cuttelod et al. 2008) and other types of physical damage such as beach contouring, 33 34 284 cleaning and path maintenance (Mus and Rita Larrucea, 2006). Environmental impacts associated 35 36 285 with mass tourism and urbanisation along the Mediterranean coast contribute to declines in many 37 38 39 286 species particularly around the popular Iberian peninsula (López-Pujol et al. 2003; Sharrock and 40 41 287 Jones 2009; Fady and Conord 2010). 42 43 44 288 The Macaronesian islands are also very popular, with the Canary Islands receiving 12 million visitors 45 46 47 289 in 2002, which contributed >50% of the islands’ GDP (Garín-Muñoz 2006). These islands have one of 48 49 290 the most urbanised, crowded coastlines in Europe and the highest road density of all European 50 51 291 islands (Gil 2003; Delgado et al. 2007). Due to their isolation, post-settlement change has largely 52 53 54 292 been driven by tourism with pronounced effects on biodiversity from tourist infrastructure and the 55 56 293 spread of weeds (Arévalo et al. 2005; Delgado et al. 2007; Arteaga et al. 2009). 57 58 59 60 61 62 63 64 65 294 The third factor contributing to the apparent geographical bias is the greater research effort 1 2 295 ascribed to many western European countries and the limited effort and data from other parts of 3 4 5 296 Europe. For instance, countries such as Bosnia-Herzegovina have high floral biodiversity (including 6 7 297 over 30% of entire Balkan-endemic flora) and rapidly increasing tourism and recreation industries 8 9 298 (Fady and Conord 2010; Doda 2012; Convention on Biological Diversity 2012b) but the threat status 10 11 12 299 of many species has not been assessed (Sharrock and Jones 2009; Convention on Biological Diversity 13 14 300 2012b). These types of geographical biases due to differential sampling effort affect many 15 16 301 international conservation databases and hence the primary targets of many conservation strategies 17 18 19 302 (Hortal et al. 2007; Planta Europa 2008; Secretariat on the Convention on Biological Diversity 2009). 20 21 303 Following the hotspot approach (Myers et al. 2000) it is important that we focus on areas of high 22 23 24 304 botanical diversity across the European continent in order to logistically direction conservation 25 26 305 approaches for wild plant species. Such an effort will require extensive site surveys of these regions 27 28 306 for centres of biodiversity (Pérez-García et al. 2012) as well as hotspots of tourism and recreation 29 30 31 307 impacts. Committing to such an inventory on a continental scale will require scientific rigour as well 32 33 308 as political collaboration, but will improve on a largely western-biased, observation-based 34 35 309 knowledge as it stands. 36 37 38 39 310 There was variation in how tourism and recreation threatens plants in Europe. Trampling by hikers 40 41 311 and other visitors threatens at least 61 species. Impacts of trampling by hikers has been documented 42 43 312 for many plant species and communities in Europe (Lemauviel and Rozé 2003; Davenport and 44 45 46 313 Davenport 2006; Grunewald 2006; Rossi et al. 2009; Bernhardt-Römermann et al. 2011) as well as 47 48 314 other continents (Rickard et al. 1994; Maschinski et al. 1997; Cole 2004; Pickering and Hill 2007b; 49 50 51 315 Pickering et al. 2011). Impacts include direct damage from trampling as well as impacts due to 52 53 316 changes in soil ecology such as compaction and alteration of nutrient and hydrological cycles (Cole 54 55 317 2004; Pickering and Hill 2007b; Light and MacConaill 2007). Plants vary in their resistance to 56 57 58 318 trampling and in how rapidly they recover; hence their tolerance to this type of disturbance (Rickard 59 60 319 et al. 1994; Leung and Marion 2000; Hill and Pickering 2009). Herbs threatened by trampling in 61 62 63 64 65 320 Europe included the lily Lilium rhodopeum in Bulgaria and the pink Dianthus diutinus in Hungary. 1 2 321 Unfortunately peak visitation to the areas where these species grow coincides with peak flowering 3 4 5 322 reducing seed production and hence threatening population viability (Rossi et al. 2009; Bazos and 6 7 323 Petrova 2011; Király and Stevanović 2011). Similarly alpine and upland species such as the stork’s-bill 8 9 324 Erodium rupicola and the daffodil Narcissus nevadensis are threatened by trampling because they 10 11 12 325 have peak growth and flowering during summer months. Summer tourism and recreation in 13 14 326 mountain regions worldwide is growing and diversifying and this may increase trampling effects on 15 16 327 such plants which are often sensitive to disturbance (Liddle, 1997; Buckley et al. 2000; Geneletti and 17 18 19 328 Dawa 2009). 20 21 22 329 Trampling also threatens many sub-shrubs in Europe including the rock-rose Helianthemum 23 24 330 teneriffae, the trefoil Lotus kunkelii and the rock-centaury Cheirolophus falcisectus reflecting the 25 26 27 331 general low trampling tolerance of woody, sclerophyllous plants (Rusterholz et al. 2004; Andrés- 28 29 332 Aballán et al. 2006; Bernhardt-Römermann et al. 2011). Recreational vehicles are a threat to herbs 30 31 32 333 and shrubs in part because of the greater mass load of vehicles compared to other recreational 33 34 334 activities such as hiking and climbing (Rickard et al. 1994; Kutiel et al. 2000). 35 36 37 335 Plant collecting was a particular threat for bulbs and herbs including orchids potentially due to their 38 39 40 336 rarity and aesthetic appeal to enthusiasts (Oldfield 1984; Ballantyne and Pickering 2012a). The 41 42 337 collection of orchids by tourists, including botanical tourists, has been documented in Europe and 43 44 338 elsewhere and for many different species (IUCN/SSC Orchid Specialist Group 1996; Kelly et al. 2003; 45 46 47 339 Ballantyne and Pickering 2012a). Lilies are especially attractive to collectors and many once- 48 49 340 widespread species are becoming increasingly rare in Europe due to intensive collection (Mascarello 50 51 341 et al. 2011). Collecting particularly unusual and charismatic flora such as Metlesics' Orchid 52 53 54 342 (Himantoglossum metlesicsianum) and the succulent Euphorbia handiensis was reported from 55 56 343 popular tourist locations in the Canary Islands (Mesa Coello et al., 2004; Marrero Gómez and Carqué 57 58 59 344 Alamo). Such unusual species have particular appeal to botanical tourists and this increases the risk 60 61 62 63 64 65 345 of harvesting by collectors (Ballantyne and Pickering 2012a). Obtaining exact details of whom, why 1 2 346 and when such plants are harvested by visitors is challenging however, due to the illicit nature of the 3 4 5 347 activity (Kelly et al. 2003; Ballantyne and Pickering 2012a). 6 7 8 348 Rock-climbing and water-sports threatened plants restricted to cliffs (rupicolous) and riparian 9 10 349 (riverine) habitats respectively. Climbing on the limestone cliffs of the Jura Mountains in Switzerland, 11 12 13 350 for example, has reduced populations of rare rupicolous herbs and shrubs and in some cases 14 15 351 catalysed a shift in composition towards novel, disturbance-tolerant communities (Rusterholz et al. 16 17 352 2004). Here we found that species affected by rock-climbing in Europe included the bedstraw 18 19 20 353 Galium sudeticum in Poland, the cat’s-ear Tolpis glabrescens on Tenerife, the mouse-ear Cerastium 21 22 354 dinaricum in Slovenia and two catchfly (Petrocoptis) species in Spain (Bilz, 2011; Martín Cáceres et al. 23 24 355 2011; Garbajal et al. 2011; Villar et al. 2011). Water-sports and boating threaten the quillwort 25 26 27 356 Isoetes boryana in France and the Bodensee Forget-me-not (Myosotis rehsteineri) in Austria 28 29 357 (Commission of the European Communities, 2009; Lansdown, 2011). Much of the damage to aquatic 30 31 32 358 and riparian plants can be attributed to the effects of wave-action and propeller turbulence on 33 34 359 inland waters (Liddle et al. 1980; Vermaat and de Bruyne 1993; Mosisch and Arthington 1998). 35 36 37 360 A range of plants were threatened by the development and expansion of tourist infrastructure in 38 39 40 361 Europe. The critically endangered herb Centranthus amazonum (a valerian) that is endemic to 41 42 362 Mount Oliena, Sardinia is reduced to a few populations of just 50-100 plants which are threatened 43 44 363 by the development of tourist trails and roads (IUCN Red List 2012). Also on Sardinia, the daisy 45 46 47 364 Nananthea perpusilla is threatened by the construction of a campsite on one of its four remaining 48 49 365 populations (Jeanmonod and Gamisans 2007). The catchfly Silene nocteolens, restricted to Teide 50 51 366 National Park, Tenerife is threatened by the creation and use of walking trails (IUCN Red List 2012; 52 53 54 367 Marrero-Gómez et al. 2003). There are just 97 isolated plants of the Canarian endemic tree, Myrica 55 56 368 rivas-martinezii and they are threatened by infrastructure development and weed introduction 57 58 59 369 (Bañares Baudet et al. 2011). Golf-course expansion contributed to declines in populations of the 60 61 62 63 64 65 370 Sandarac Gum Tree (Tetraclinis articulata) in Spain (Sánchez-Gómez et al. 2012). Golf courses and 1 2 371 other resort amenities contributed to declines in other species in Europe, largely as a result of 3 4 5 372 fragmentation which decreases the quality of remaining habitat (Leyva et al. 2006; Peñas et al. 2011). 6 7 373 Walking and cycle-track development affects at least 10 European plants in this study, most of which 8 9 374 were herbs. Impacts from tracks occur from the destruction of vegetation during construction, from 10 11 12 375 the leaching of trail materials into the surrounding ecosystem over time and from internal habitat 13 14 376 fragmentation (Godefroid and Koedam 2004; Müllerová et al. 2011; Ballantyne and Pickering, 2012b). 15 16 17 377 Tourism and recreation is not always bad for plants, with some conservation benefits arising directly 18 19 20 378 and indirectly including in Europe. One critically endangered species, the soapwort Saponaria jagelii, 21 22 379 for example, can benefit directly from tourism. Where access is restricted during the plants’ 23 24 380 flowering season but allowed during seeding, walkers can facilitate seed dispersal within its littoral 25 26 27 381 habitat. In some cases, volunteer and other types of specialist tourism directly contribute to the 28 29 382 conservation of rare plants in Europe by protecting them from vandalism and collection (Ballantyne 30 31 32 383 and Pickering 2012a) and via other active conservation measures such as habitat restoration 33 34 384 (Halpenny and Caissie 2003). More generally, tourism and recreation, particularly nature-based and 35 36 385 eco-tourism, can provide economic and social support for the establishment and funding of 37 38 39 386 protected areas which can help safeguard rare and threatened species (Leung and Marion 2000; 40 41 387 Shackley 2004; Hamilton and Hamilton 2006; Buckley et al. 2012). 42 43 44 388 This work has provided evidence that the industries of tourism and recreation pose great pressures 45 46 47 389 for some of Europe’s rarest plants. However, it is important to recognise that these impacts do not 48 49 390 act in isolation. Nearly all of the species here described are also threatened by other, more widely 50 51 391 researched anthropogenic factors such as agricultural intensification, urbanisation and 52 53 54 392 overexploitation. Europe has seen some of the most drastic modifications of natural ecosystems 55 56 393 worldwide and there are a number of documents that illustrate the resultant impacts and what can 57 58 59 394 be done about them (Planta Europa, 2008; Bilz et al. 2011). The Mediterranean in particular has 60 61 62 63 64 65 395 experienced some of the greatest land-use change and hence, biodiversity loss (Falcucci et al. 2007). 1 2 396 We suggest that in order to further improve policy guidance for managing increasing threats, more 3 4 5 397 quantitative and comparative research should be undertaken. In addition to simply listing impacts, 6 7 398 sometimes based solely on observational work, frameworks should provide rankings of impact 8 9 399 severity for individual threatened species and compare them between threats. If a standardised 10 11 12 400 methodology was employed, such an approach would provide useful, integrated information on a 13 14 401 continental basis and highlight which impacts are of greatest concern and where. It is likely, such an 15 16 402 approach will take considerable political co-operation, but with increasing concern over biodiversity 17 18 19 403 loss in Europe, it might be increasingly timely to initiate such an effort, using IUCN red-listed plants 20 21 404 to ‘pave the way’. 22 23 24 405 Conclusions 25 26 27 28 406 Tourism and recreation appear to be common threats to a wide variety of European IUCN red-listed 29 30 407 plants, and are likely to threaten other plants in other popular tourism destinations as well. Greater 31 32 408 emphasis should therefore be given to minimising the range of negative impacts from unsustainable 33 34 35 409 tourism and recreation use, particularly in biodiversity hotspots such as the Mediterranean. 36 37 410 Management plans for protected areas, and recovery plans for red-listed species need to more 38 39 40 411 specifically address these types of threats. Moreover, in order to do so, increasing quantitative and 41 42 412 experimental species-specific research should be undertaken to add rigour to the current, often 43 44 413 observational-based listings. Finally, as tourism and recreation industries continue to grow in Europe, 45 46 47 414 there needs to be more recognition and reduction of their impacts, particularly if they are to protect 48 49 415 their triple bottom line (environmental, social and economic benefits) and reduce their contribution 50 51 416 to the endangerment of Europe’s flora. 52 53 54 55 417 Acknowledgements 56 57 58 59 60 61 62 63 64 65 418 The authors would like to thank Clare Morrison, Julien Grignon and Daniela Guitart of Griffith 1 2 419 University for their comments on this manuscript as well as Nicholas Turland of the Botanischer 3 4 5 420 Garten und Botanisches Museum, Berlin-Dahlem for his review. 6 7 8 421 References 9 10 11 12 422 Amelung B, Viner D (2006) Mediterranean tourism: exploring the future with the tourism climatic 13 14 423 index. 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Annals of 49 50 681 Tourism Research 29(3): 743-761. 51 52 53 682 Vermaat JE, de Bruyne RJ (1993) Factors limiting the distribution of submerged water plants in the 54 55 56 683 lowland River Vecht (The Netherlands). Freshw Biol 30(1): 147-157. 57 58 59 60 61 62 63 64 65 684 Villar L, Goñi Martínez D, Ferrández J (2011). Petrocoptis pseudoviscosa. In: IUCN 2013 Red List of 1 2 685 Threatened Species, Version 2013.1. IUCN Red List website. 3 4 5 686 http://www.iucnredlist.org/details/162059/0. Accessed 23 July 2013. 6 7 8 687 Walker KJ, Stevens PA, Stevens DP, Owen JO, Manchester SJ, Pywell RF (2004) The restoration and 9 10 688 re-creation of species-rich lowland grassland on land formerly managed for intensive agriculture in 11 12 13 689 the UK. Biol Conserv 19: 1-18. 14 15 16 690 Walter KS, Gillett HJ (1997) The 1997 IUCN red list of threatened plants. IUCN Publishing, Gland, 17 18 691 Switzerland. 19 20 21 692 WTTC - World Travel and Tourism Council (2012) Travel & tourism: economic impact 2012 report. 22 23 24 693 WTTC website. http://www.wttc.org/site_media/uploads/downloads/world2012.pdf. Accessed 25 25 26 694 June 2012. 27 28 29 695 30 31 32 33 696 34 35 36 697 37 38 39 698 40 41 42 699 43 44 45 46 700 47 48 49 701 50 51 52 702 53 54 55 56 703 57 58 59 704 60 61 62 63 64 65 705 Table 1: The most common forms of tourism and recreation-related threats in relation to the totals 1 2 706 of different growth-forms of red-listed vascular plants listed by the IUCN in Europe. The numbers of 3 707 species affected by each activity are given in brackets. T&R = threatened by tourism and recreation. 4 5 6 Growth Form Total Total threatened by T&R Most common threats 7 8 Tree 26 5 Maintenance/construction of tourist 9 10 infrastructure (3); Trampling (2) 11 Shrub 55 11 Trampling (5); Non-specified (4); Collection of 12 13 plants (3) 14 15 Sub-shrub 53 21 Trampling (10); Collection of plants (8); Non- 16 17 specified (3) 18 19 Climber 3 0 Rock-climbing/mountaineering (1) 20 Herb 289 137 Collection of plants (46); 21 22 Maintenance/construction of tourist 23 24 infrastructure (40); Trampling (39); Non- 25 26 specified (21); Habitat degradation from 27 urbanising tourist sites (10); Walking/cycle-track 28 29 development (9); Rock- 30 31 climbing/mountaineering (8) 32 33 Succulent 9 6 Collection of plants (4); Trampling (2) 34 35 Aquatic 7 5 Water-sports/swimming (1); Leisure fishing (1); 36 Trampling (1); Walking/cycle-track development 37 38 (1) 39 40 Fern 2 2 Collection of plants (1); Trampling (1) 41 42 Graminoid 17 7 Habitat degradation from urbanising tourist 43 44 sites (3); Maintenance/construction of tourist 45 infrastructure (2); Rock- 46 47 climbing/mountaineering (1) 48 49 708 50 51 52 709 53 54 55 710 56 57 58 59 711 60 61 62 63 64 65 712 Table 2: Total number of native and endemic plants per country in relation to the number listed as 1 2 713 threatened (equiv. Critically Endangered, Endangered, Vulnerable) on national red lists, the IUCN 3 714 Red-list and those found to be threatened specifically by tourism and recreation in this study. 4 5 715 Proportions of national red-listed species also listed by the IUCN are given. 6 7 8 Country/Territory* Total Endemic National IUCN IUCN % national % of land 9 10 red lists Red List T&R red list on in PAs 11 IUCN 12 13 Albania 3,245 177 363 1 0 0.3 9.8 14 15 Austria 2,950 167 1,151 12 8 1 22.9 16 17 Belarus 2,100 - 173 0 0 0 7.2 18 19 Belgium 1,400 - 448 1 0 0.2 13.8 20 Bosnia-Herzegovina 4,569 450 63 1 0 1.6 0.6 21 22 Bulgaria 3,900 186 158 5 3 3.2 9.2 23 24 Croatia 5,347 485 760 7 4 0.9 13 25 26 Cyprus 1,738 143 238 19 6 8 10.5 27 Czech Republic 2,700 - 1,161 10 7 0.9 15.1 28 29 Denmark 1,000 - 197 2 0 1 4.9 30 31 Estonia 1,500 - 188 0 0 0 20.4 32 33 Finland 1,240 - 180 2 1 1.1 9 34 35 France 4,700 - 486 20 8 4.1 16.5 36 Corsica 9 5 37 38 Germany 3,242 85 875 15 4 1.7 42.4 39 40 Greece 5,500 1,000 900 34 17 3.8 16.2 41 42 Crete 12 4 43 Aegean Islands 1 0 44 45 Hungary 2,200 695 605 8 6 1.3 5.1 46 47 Iceland 483 - 52 0 0 0 19.7 48 49 Ireland 900 - 68 1 0 1.5 1.8 50 51 Italy 6,711 1,314 1,020 28 16 2.7 15.1 52 Sicily 21 6 53 54 Sardinia 18 11 55 56 Capraia 1 0 57 58 Latvia 1,937 - 426 0 0 0 18 59 Liechtenstein 1,531 - 379 0 0 0 42.4 60 61 62 63 64 65 Lithuania 1,796 - 339 0 0 0 14.5 1 2 Luxembourg 1,323 - 354 1 0 0.3 20 3 Macedonia 3,700 117 500 0 0 0 4.9 4 5 Malta 1,200 25 255 4 1 1.6 17.3 6 7 Moldova 1,989 - 242 2 1 0.8 1.4 8 9 Montenegro 3,250 223 415 1 1 0.2 13.3 10 11 Netherlands 1,490 - 335 0 0 0 12.4 12 Norway 1,253 - 181 2 0 1.1 14.6 13 14 Poland 2,468 - 506 10 4 2 22.4 15 16 Portugal 3,600 200 254 35 16 13.8 8.3 17 18 Madeira 33 11 19 Azores 10 5 20 21 Romania 3,700 57 210 4 2 1.9 7.1 22 23 Serbia 3,662 165 171 3 2 1.8 6 24 25 Slovakia 3,352 - 747 3 3 0.4 23.2 26 27 Slovenia 3,175 22 304 7 6 2.3 13.2 28 Spain 8,500 4,080 1,275 68 40 7.5 8.6 29 30 Balearic Islands 15 5 31

32 Canary Islands 119 41 33 34 Sweden 1,638 - 261 4 1 1.2 10.9 35 Switzerland 3,144 - 1,066 2 2 0.2 24.9 36 37 Ukraine 6,086 - 439 18 8 2.1 3.5 38 39 United Kingdom 1,756 - 52 5 1 9.6 26.4 40 41 Gibraltar 1 1 42 716 43 44 45 717 *Information on number of species in each country, number of endemic species and number of species on 46 47 48 718 national red-lists gained from most recent National Reports and National Biodiversity and Action Plans under 49 50 719 Convention on Biological Diversity (DBD) signatory accessed at http://www.cbd.int/convention/parties/list/ 51 52 720 and through information provided by European Information Platform for Plants accessed at 53 54 721 http://www.plantaeuropa.org. Andorra, Kosovo, Monaco, San Marino and the Vatican City were not included 55 56 722 in this database because they did not have any species profiles native to those regions and are not signatory 57 58 723 nations to the CBD. Hyphens denote information that could not be found in the literature or policy documents. 59 60 61 62 63 64 65 724 Island territories belonging to signatory countries (e.g. Sardinia, Crete and Madeira) are italicised and apart 1 2 725 from the number of plants on the IUCN Red List and tourism threat data, information is maintained within 3 4 726 governing country’s statistics. Percentage of land in protected areas based on 2010 data issued by the World 5 6 727 Bank for terrestrial protected areas (% of total land area) accessed at 7 8 728 http://data.worldbank.org/indicator/ER.LND.PTLD.ZS. T&R = number of species threatened by tourism and 9 10 11 729 recreation, PAs = protected areas. 12 13 14 730 15 16 17 731 18 19 20 732 21 22 23 733 24 25 26 734 27 28 29 735 30 31 32 736 33 34 35 737 36 37 38 738 39 40 41 739 42 43 44 740 45 46 47 741 48 49 50 742 51 52 53 743 54 55 56 744 57 58 59 745 60 61 62 63 64 65 746 Table 3: Total number of vascular plant species affected by tourism and recreation (T&R) across the 1 2 747 10 European bioregions as set out by the European Commission. The most common tourism and 3 748 recreation threats are also listed with total number of species affected given in brackets. 4 5 6 Bioregion Total Most common threats 7 8 Alpine 15 Non-specified (5); Collection of plants (5); Rock- 9 10 climbing/mountaineering (2) 11 Arctic 0 n/a 12 13 Atlantic 1 Maintenance/construction of tourist infrastructure (1) 14 15 Black Sea 4 Habitat degradation from urbanising tourist sites (4) 16 17 Boreal 1 Non-specified (1) 18 19 Continental 12 Non-specified (6); Trampling (3); Rock-climbing/mountaineering (3); 20 Driving recreational vehicles (2) 21 22 Macaronesia 56 Collection of plants (25); Trampling (25); Maintenance/construction of 23 24 tourist infrastructure (9); Non-specified (5); Walking/cycle-track 25 26 development (5) 27 Mediterranean 98 Maintenance/construction of tourist infrastructure (32); Collection of 28 29 plants (31); Trampling (29); Non-specified (14); Habitat degradation 30 31 from urbanising tourist sites (8); Driving recreational vehicles (7); 32 33 Walking/cycle-track development (6) 34 35 Pannonian 3 Trampling (3); Horse-riding (1); Para-gliding/ballooning (1) 36 Steppic 4 Non-specified (4) 37 38 749 39 40 41 750 42 43 44 45 751 46 47 48 752 49 50 51 753 52 53 54 754 55 56 57 58 755 59 60 61 62 63 64 65 756 Table 4: Total number of IUCN Red-listed European vascular plant species threatened by different 1 2 757 types of tourist or recreational activities, impacts and infrastructures. 3 4 5 Threat Total 6 7 Non-specified 35 8 9 Activities 10 11 Collection of plants 59 12 13 Rock-climbing and mountaineering 12 14 Driving of recreational vehicles 10 15 16 Camping/picnicking 5 17 18 Horse-riding 5 19 20 Water-sports/swimming 3 21 Winter-tourism/skiing 3 22 23 Trail/mountain-biking 3 24 25 Picking flowers 2 26 27 Game-driving 2 28 29 Riding of non-motorised recreational vehicles 2 30 Beach cleaning for tourists 2 31 32 Paragliding 1 33 34 Motor-biking/quad-biking 1 35 36 Leisure fishing 1 37 Impacts 38 39 Trampling 61 40 41 Habitat degradation as a result of urbanising tourist sites 13 42 43 Vegetation damage by tourists 3 44 45 Altered fire regimes 3 46 Erosion by walkers 2 47 48 Littering 1 49 50 Infrastructure 51 52 Maintenance/construction of tourist infrastructure 43 53 Walking/cycle-track development 10 54 55 Building of tourist roads 3 56 57 Tourist car-parks 2 58 59 Expansion of golf-courses 1 60 61 62 63 64 65 758 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 Table (Supplementary Material)

Supplementary Material – Table 1: List of 194 IUCN Red-listed vascular plant species affected by tourism and recreation in Europe. Threats include those from activities, impacts and infrastructure associated with tourism and recreation. The threats are listed as either ‘stated’ (i.e. IUCN classification scheme uses the words ‘tourism’ and/or ‘recreation’ to describe threats to the species) or ‘inferred’ (i.e. threats were a result of activities, impacts or infrastructure in a public protected area of tourism hotspot from which the threats were likely derived). Family taxonomy according to Angiosperm Phylogeny Group III system.

Family Name Species Name Stated Inferred Tourism/recreational impact Protected Area (PA) % population in PA Native Range Alismataceae Alisma wahlenbergii X Non-specified Finland; Sweden Amaryllidaceae Allium corsicum X Non-specified Corsica Amaryllidaceae Galanthus reginae-olgae X Habitat degradation resulting Greece; Sicily; from urbanising tourist sites Montenegro Amaryllidaceae Narcissus alcaracensis X Collection of plants by visitors Unnamed protected ? Spain area Amaryllidaceae Narcissus longispathus X Collection of plants by visitors Unnamed protected ? Spain area Amaryllidaceae Narcissus nevadensis X Trampling by tourists; collection Spain of plants by visitors Amaryllidaceae Narcissus nevadensis ssp. X Trampling by tourists Spain enemeritoi Amaryllidaceae Narcissus radinganorum X Collection of plants by visitors Spain

Apiaceae Apium bermejoi X Trampling by tourists; Minorca trail/mountain-biking

Apiaceae Bupleurum capillare X Winter tourism; Greece maintenance/construction of tourist infrastructure Apiaceae Bupleurum kakiskalae X Rock-climbing/mountaineering Samaria Gorge 100 Crete National Park Apiaceae Ferula sadleriana X Trampling by tourists Unnamed protected 95 Hungary; Romania; area Slovakia Apiaceae Monizia edulis X Collection of plants by visitors Madeira

Apiaceae Thorella verticillato-inundata X Maintenance/construction of Portugal; Spain tourist infrastructure

Araceae Arum purpureospathum X Non-specified Crete

Apocynaceae Vincetoxicum pannonicum X Trampling by tourists; horse- Hungary riding; paragliding/ballooning Asparagaceae Asparagus arborescens X Non-specified Canary Islands

Asparagaceae Asparagus fallax X Non-specified Canary Islands

Asparagaceae Leopoldia gussonei X Maintenance/construction of Sicily tourist infrastructure Asteraceae Andryala crithmifolia X Collection of plants by visitors; Madeira maintenance/construction of tourist infrastructure

Asteraceae Aster pyrenaeus X Non-specified France; Spain

Asteraceae Atractylis arbuscula X Habitat degradation resulting Canary Islands from urbanising tourist sites; maintenance/construction of tourist infrastructure Asteraceae Calendula maritima X Picking of flowers Sicily

Asteraceae Centaurea akamantis X Non-specified Cyprus Asteraceae Centaurea borjae X Trampling by tourists; habitat Spain degradation resulting from urbanising tourist sites; maintenance/construction of tourist infrastructure Asteraceae Centaurea corensis X Maintenance/construction of Sardinia tourist infrastructure Asteraceae Centaurea corymbosa X Rock-climbing/mountaineering France Asteraceae Centaurea heldreichii X Trampling by tourists; rock- Greece climbing/mountaineering Asteraceae Centaurea peucedanifolia X Collection of plants by visitors; Greece walking/cycle track development Asteraceae Cheirolophus duranii X Game-driving Reserva Natural de 100 Canary Islands Mencáfete; Reserva Natural de Tibataje; Paisaje Protegido de Timijiraque Asteraceae Cheirolophus falcisectus X Trampling by tourists Reserva Natural ? Canary Islands Especial de Güígüí; Parque Rural del Nublo Asteraceae Cheirolophus junonianus X Trampling by tourists; driving of Monumento Natural 100 Canary Islands non-motorised vehicles, horse- de los Volcanes de riding; game-driving Teneguía Asteraceae Cheirolophus metlesicsii X Trampling by tourists; vegetation Parque Natural de 100 Canary Islands damage by tourists Corona Forestal Asteraceae Crepis purpurea X Non-specified Ukraine

Asteraceae Erigeron frigidus X Trampling by tourists; picking of Parque Nacional de 100 Spain flowers; vegetation damage by Sierra Nevada tourists Asteraceae Femeniasia balearica X Path clearing Minorca Asteraceae Helichrysum gossypinum X Building of roads in tourist area Paisaje Protegido de 100 Canary Islands La Geria; Paisaje Protegido Barranco de Tenegüime; Parque Natural Archipiélago Chinijo Asteraceae Helichrysum melitense X Collection of plants by visitors; Fungus Rock Nature ? Malta maintenance/construction of Reserve tourist infrastructure

Asteraceae Helichrysum monogynum X Driving of recreational vehicles Parque Natural 100 Canary Islands Archipiélago Chinijo; Paisaje Protegido de La Geria Asteraceae Lamyropsis microcephala X Maintenance/construction of Sardinia tourist infrastructure Asteraceae Leontodon microcephalus X Non-specified Spain Asteraceae Nananthea perpusilla X Maintenance/construction of Natural Reserve de ? Corsica; Sardinia tourist infrastructure Bouche de Bonifacio; Reserve des Finochiarola Asteraceae Onopordum carduelium X Trampling by tourists Reserva Natural 100 Canary Islands Especial Los Marteles Asteraceae Onopordum nogalesii X Collection of plants by visitors; Parque Natural de 100 Canary Islands maintenance/construction of Jandía tourist infrastructure Asteraceae Pericallis malvifolia X Non-specified Azores

Asteraceae Santolina elegans X Non-specified Spain

Asteraceae Senecio caespitosus X Trampling by tourists; Portugal maintenance/construction of tourist infrastructure Asteraceae Stemmacantha cynaroides X Collection of plants by visitors Parque Nacional de 100 Canary Islands Teide Asteraceae Sventenia bupleuroides X Walking/cycle track development Parque Natural de 100 Canary Islands Tamadaba Asteraceae Tanacetum ptarmiciflorum X Trampling by tourists; collection Paisaje Protegido de ? Canary Islands of plants by visitors Las Cumbres; Monumento Natural Riscos de Tirajana Asteraceae Tolpis glabrescens X Collection of plants by visitors; Parque Rural de ? Canary Islands rock-climbing/mountaineering Anaga; Reserva Natural Integral de Pijaral Betulaceae Betula pendula var. fontqueri X Non-specified Spain

Betulaceae Betula pendula var. X Maintenance/construction of Spain parvibracteata tourist infrastructure Boraginaceae Anchusa crispa X Trampling by tourists; driving of Corsica; Sardinia recreational vehicles; camping/picnicking; motor- biking; quad biking Boraginaceae Echium acanthocarpum X Trampling by tourists Parque Nacional de ? Canary Islands Garajonay; Parque Natural de Majona Boraginaceae Echium decaisnei ssp. X Trampling by tourists; driving of Canary Islands purpuriense recreational vehicles Boraginaceae Gyrocaryum oppositifolium X Trampling by tourists; collection Spain of plants by visitors Boraginaceae Myosotis rehsteineri X Camping/picnicking; water- Austria; Germany; sports; swimming Italy; Switzerland Boraginaceae Omphalodes littoralis ssp. X Trampling by tourists; car Spain gallaecica parking; driving of recreational vehicles; removal of beach materials; walking/cycle track development; maintenance/construction of tourist infrastructure

Brassicaceae Arabis kennedyae X Camping/picnicking; building of Troodos National 100 Cyprus roads in tourist area Forest Park, Pafos State Forest Brassicaceae Barbarea lepuznica X Trampling by tourists Vršačke Mountain ? Romania; Serbia Nature Park, Retezat National Park Brassicaceae Biscutella vincentina X Habitat degradation resulting Portugal from urbanising tourist sites; maintenance/construction of tourist infrastructure Brassicaceae Brassica macrocarpa X Trampling by tourists; Sicily maintenance/construction of tourist infrastructure; building of roads in tourist area Brassicaceae Cochlearia tatrae X Non-specified Poland; Slovakia

Brassicaceae Coincya rupestris X Non-specified Spain

Brassicaceae Crambe laevigata X Walking/cycle track development Rural Park Teno ? Canary Islands

Brassicaceae Diplotaxis vicentina X Walking track maintenance Portugal

Brassicaceae Isatis platyloba X Trampling by tourists Portugal; Spain

Brassicaceae Monanthes wildpretii X Collection of plants by visitors Parque Rural de Anaga 100 Canary Islands Brassicaceae Sinapidendron angustifolium X Maintenance/construction of Madeira tourist infrastructure Campanulaceae Azorina vidalii X Trampling by tourists Azores Campanulaceae Jasione lusitanica X Trampling by tourists; horse- Portugal riding; removal of beach materials; erosion by walkers; walking/cycle track development; maintenance/construction of tourist infrastructure Campanulaceae Musschia wollastonii X Trampling by tourists; collection Madeira of plants by visitors

Caryophyllaceae Arenaria bolosii X Trampling by tourists; collection Mallorca of plants by visitors; camping/picnicking; altered fire regime; habitat degradation resulting from urbanising tourist sites Caryophyllaceae Arenaria nevadensis X Erosion by walkers Sierra Nevada 100 Spain National Park Caryophyllaceae Cerastium dinaricum X Rock-climbing/mountaineering Slovenia

Caryophyllaceae Dianthus diutinus X Trampling by tourists Unnamed protected 80 Hungary; Serbia area in Hungary Caryophyllaceae Dianthus hypanicus X Non-specified Ukraine

Caryophyllaceae Dianthus morisianus X Trampling by tourists Sardinia

Caryophyllaceae Herniaria algarvica X Car parking; driving of Portugal recreational vehicles Caryophyllaceae Moehringia fontqueri X Walking/cycle track development Sierra Nevada 100 Spain National Park Caryophyllaceae Moehringia hypanica X Non-specified Ukraine

Caryophyllaceae Moehringia intricata ssp. X Collection of plants by visitors Parque Natrual de ? Spain tejedensis Tejeda, Alhama y Almijara Caryophyllaceae Moehringia tommasinii X Trampling by tourists; collection Italy, Croatia, of plants by visitors; rock- Slovenia climbing/mountaineering Caryophyllaceae Petrocoptis grandiflora X Rock-climbing/mountaineering Spain

Caryophyllaceae Petrocoptis pseudoviscosa X Rock-climbing/mountaineering Spain

Caryophyllaceae Saponaria jagelii X Trampling by tourists; driving of East Aegean Islands recreational vehicles Caryophyllaceae Silene nocteolens X Walking/cycle track development Parque National Teide 100 Canary Islands Chenopodiaceae Salicornia veneta X Non-specified Italy, Croatia, Slovenia Cistaceae Cistus heterophyllus ssp. X Non-specified Spain carthaginensis Cistaceae Helianthemum teneriffae X Trampling by tourists Parque Natural de la ? Canary Islands Corona Forestal Cistaceae Tuberaria major X Vegetation damage by tourists; Portugal littering; maintenance/construction of tourist infrastructure Colchicaceae Androcymbium rechingeri X Maintenance/construction of Crete tourist infrastructure

Colchicaceae Colchicum corsicum X Driving of recreational vehicles Corsica

Crassulaceae Aeonium balsamiferum X Trampling by tourists; collection Parque Rural de ? Canary Islands of plants by visitors Betancuria; Monumento Natural del Malpaís de La Arena; Parque Natural del Archipiélago Chinijo; Paisaje Protegido La Geria Crassulaceae Aeonium gomerense X Collection of plants by visitors Parque Nacional de 100 Canary Islands Garajonay; Parque Natural de Majona Crassulaceae Aichryson dumosum X Trampling by tourists Madeira

Cupressaceae Tetraclinis articulata X Golf-course expansion Malta; Spain

Dioscoreaceae Borderea chouardii X Rock-climbing/mountaineering Pyrénées National 100 Spain Park Dryopteridaceae Polystichum drepanum X Collection of plants by visitors Madeira

Euphorbiaceae Euphorbia bourgeana X Altered fire regime Parque Rural de ? Canary Islands Anaga; Parque Natural de la Corona Forestal; Parque Nacional de Garajonay Euphorbiaceae Euphorbia handiensis X Collection of plants by visitors Parque Natural de 100 Canary Islands Jandía Fabaceae Astragalus macrocarpus ssp. X Collection of plants by visitors; Cyprus lefkarensis maintenance/construction of tourist infrastructure Fabaceae Astragalus maritimus X Habitat degradation resulting Sardinia from urbanising tourist sites; maintenance/construction of tourist infrastructure

Fabaceae Astragalus setosulus X Non-specified Ukraine

Fabaceae Astragalus verrucosus X Maintenance/construction of Sardinia tourist infrastructure Fabaceae Dorycnium spectabile X Trampling by tourists; collection Parque Rural de Teno; 100 Canary Islands of plants by visitors Paisaje Protegido de las Siete Lomas Fabaceae Genista ancistrocarpa X Collection of plants by visitors National Park of 30 Spain Doñana Fabaceae Lotus kunkelii X Trampling by tourists SCI Jinamar 100 Canary Islands

Fabaceae Lotus maculatus X Trampling by tourists; collection Paisaje Protegido 100 Canary Islands of plants by visitors Costa de Acentejo Fabaceae Lotus pyranthus X Collection of plants by visitors Parque Natural de Las 100 Canary Islands Nieves Fabaceae Medicago saxatilis X Habitat degradation resulting Ukraine from urbanising tourist sites

Fabaceae Medicago kotovii X Habitat degradation resulting Ukraine; Moldova from urbanising tourist sites

Fabaceae Teline nervosa X Trampling by tourists; collection Paisaje Protegido de ? Canary Islands of plants by visitors; Pino Santo maintenance/construction of tourist infrastructure Fabaceae Vicia bifoliolata X Trampling by tourists; collection Minorca of plants by visitors Fabaceae Vicia costae X Non-specified Madeira

Gentianaceae Centaurium somedanum X Collection of plants by visitors; Parque Natural de 90 Spain trail/mountain-biking; Somiedop; Espacio walking/cycle track development Natural Valle de San Emiliano Gentianaceae Gentianella bohemica X Non-specified Austria; Czech Republic; Germany; Poland Geraniaceae Erodium rupicola X Trampling by tourists; walking Parque Nacional de ? Spain track maintenance Sierra Nevada; Parque Natural de Sierra de Baza Iridaceae Crocus cyprius X Trampling by tourists Troodos National ? Cyprus Forest Park Iridaceae Iris boissieri X Collection of plants by visitors Parque Natural Baixa ? Portugal; Spain Limia-Serra do Xurés; Peneda-Geres National Park Isoetaceae Isoetes azorica X Leisure fishing; walking/cycle Azores track development Isoetaceae Isoetes boryana X Water sports France

Isoetaceae Isoetes fluitans X Waterway clearing Spain

Juncaceae Juncus sorrentinii X Habitat degradation resulting Greece; Italy; Sicily; from urbanising tourist sites Sardinia; Portugal; Spain Lamiaceae Rosmarinus tomentosus X Rock-climbing/mountaineering; Paraje Natural ? Spain swimming; Acantilados Maro- maintenance/construction of Cerro Gordo tourist infrastructure Lamiaceae Sideritis infernalis X Trampling by tourists Reserva Natural 100 Canary Islands Especial del Barranco del Infierno Lamiaceae Sideritis javalambrensis X Maintenance/construction of Spain tourist infrastructure Lamiaceae Sideritis marmorea X Collection of plants by visitors Reserva Natural 100 Canary Islands Especial de Puntallana Lentibulariaceae Pinguicula nevadensis X Trampling by tourists; Espacio Natural de ? Spain camping/picnicking Sierra Nevada

Liliaceae Fritillaria euboeica X Maintenance/construction of Greece tourist infrastructure Liliaceae Fritillaria obliqua X Collection of plants by visitors National Forest Park ? Greece of Parnitha Liliaceae Fritillaria rhodocanakis X Collection of plants by visitors Greece Liliaceae Lilium rhodopeum X Trampling by tourists; collection Unnamed protected ? Greece; Bulgaria of plants by visitors; area in Bulgaria maintenance/construction of tourist infrastructure Liliaceae Tulipa cypria X Collection of plants by visitors Cyprus

Marsileaceae Marsilea azorica X Trampling by tourists Azores

Myricaceae Myrica rivas-martinezii X Trampling by tourists Canary Islands

Orchidaceae Anacamptis boryi X Collection of plants by tourists Greece; Crete

Orchidaceae Dactylorhiza kalopissii X Collection of plants by tourists; Greece maintenance/construction of tourist infrastructure Orchidaceae Epipactis greuteri X Non-specified Austria; Bulgaria; Croatia; Czech Republic; Greece; Italy; Slovenia Orchidaceae Epipactis nordeniorum X Non-specified Austria; Croatia; Czech Republic; Germany; Hungary Orchidaceae Epipactis placentina X Non-specified Czech Republic; France; Hungary; Italy; Sicily; Slovenia; Switzerland Orchidaceae Epipactis tallosii X Non-specified Czech Republic; Hungary; Italy; Slovakia Orchidaceae Goodyera macrophylla X Trampling by tourists; collection Natural Park of 100 Madeira of plants by visitors Madeira Orchidaceae Gymnadenia archiducis- X Collection of plants by visitors Austria joannis Orchidaceae Gymnadenia lithopolitanica X Non-specified Austria; Slovenia

Orchidaceae Gymnadenia stiriaca X Non-specified Austria

Orchidaceae Gymnadenia widderi X Non-specified Austria; Germany; Italy Orchidaceae Himantoglossum X Collection of plants by visitors; Canary Islands metlesicsianum walking/cycle track development; maintenance/construction of tourist infrastructure Orchidaceae Ophrys argolica X Non-specified Greece Orchidaceae Orchis sitiaca X Collection of plants by visitors; Crete maintenance/construction of tourist infrastructure Orchidaceae Platanthera micrantha X Collection of plants by visitors; Azores maintenance/construction of tourist infrastructure

Plantaginaceae Antirrhinum lopesianum X Trampling by tourists; collection Parque Natural de ? Portugal; Spain of plants by visitors Arribes del Duero

Plantaginaceae Antirrhinum subbaeticum X Collection of plants by visitors Spain

Plantaginaceae Globularia ascanii X Non-specified Parque Natural de 100 Canary Islands Tamadaba

Plantaginaceae Linaria tonzigii X Collection of plants by visitors; Italy maintenance/construction of tourist infrastructure Plantaginaceae Plantago almogravensis X Trampling by tourists; collection Portugal of plants by visitors; driving of recreational vehicles Plantaginaceae Plantago famarae X Trampling by tourists Parque Natural del 100 Canary Islands Archipiélago Chinijo Plantaginaceae Veronica oetaea X Driving of recreational vehicles National Forest Park 100 Greece of Oiti Plumbaginaceae Armeria sampaioi X Trampling by tourists; skiing Portugal

Plumbaginaceae Limonium calabrum X Trampling by tourists; collection Italy of plants by visitors; maintenance/construction of tourist infrastructure Plumbaginaceae Limonium dendroides X Collection of plants by visitors Parque Rural de Valle 100 Canary Islands Gran Rey; Monumento Natural Barranco del Cabrito Plumbaginaceae Limonium fruticans X Trampling by tourists; collection Parque Rural de Teno ? Canary Islands of plants by visitors

Plumbaginaceae Limonium legrandii X Habitat degradation resulting France from urbanising tourist sites Plumbaginaceae Limonium perezii X Collection of plants by visitors Parque Rural de Teno 100 Canary Islands

Plumbaginaceae Limonium preauxii X Trampling by tourists; collection Paisaje Protegido de ? Canary Islands of plants by visitors Fataga; Parque Natural de Pilancones; Monumento Natural de Aguayro Plumbaginaceae Limonium strictissimum X Trampling by tourists; Parc Marin des ? Corsica; Sardinia maintenance/construction of Bouches de Bonifacio; tourist infrastructure Réserve Naturelle de l'Etang de Biguglia Poaceae Agropyron cimmericum X Habitat degradation resulting Ukraine from urbanising tourist sites Poaceae Agropyron dasyanthum X Habitat degradation resulting Ukraine from urbanising tourist sites

Poaceae Avenula hackelii X Maintenance/construction of Portugal tourist infrastructure

Poaceae Festuca brigantina X Non-specified Portugal; Spain

Poaceae Poa riphaea X Trampling by tourists; rock- Czech Republic climbing/mountaineering Poaceae Stipa veneta X Maintenance/construction of Italy tourist infrastructure

Polygalaceae Polygala helenae X Non-specified Greece Polygonaceae Rumex rupestris X Maintenance/construction of Unnamed protected 85 France, Spain, tourist infrastructure areas in France and United Kingdom the UK Primulaceae Primula apennina X Collection of plants by visitors Italy

Primulaceae Primula palinuri X Collection of plants by visitors; Italy altered fire regime; maintenance/construction of tourist infrastructure Pteridaceae Pteris incompleta X Trampling by tourists Natural Park of los ? Canary Islands; Alcornocales; Natural Gibraltar Parks of Garajonay, Majona and Tamadaba; Natural Reserve Tilos de Moya; Guelguen and del Pijaral; Rural Parks de Anaga and de Teno Ranunculaceae Aquilegia barbaricina X Collection of plants by visitors Sardinia

Ranunculaceae Callianthemum kernerianum X Trampling by tourists; soil- Italy removal for ski runs Ranunculaceae Delphinium caseyi X Collection of plants by visitors Karmi State Forest ? Cyprus Rosaceae Potentilla delphinensis X Collection of plants by visitors Parc National des 100 France Ecrins Rosaceae Prunus ramburii X Non-specified Sierra Nevada 100 Spain National Park Rosaceae Sorbus maderensis X Trampling by tourists; collection Madeira of plants by visitors; maintenance/construction of tourist infrastructure Rubiaceae Galium cracoviense X Trampling by tourists; driving of Poland recreational vehicles; driving of non-motorised vehicles; horse- riding; trail/mountain-biking Rubiaceae Galium sudeticum X Collection of plants by visitors; Karkonosze National ? Czech Republic; rock-climbing/mountaineering Park Poland Rubiaceae Galium viridiflorum X Trampling by tourists; horse- Parque Natural Sierra ? Spain riding de las Nieves; Parque Natural Sierras de Tejeda, Almijara y Alhama; Paraje Natural los Reales de Sierra Bermeja Saxifragaceae Saxifraga portosanctana X Collection of plants by visitors Madeira

Saxifragaceae Saxifraga presolanensis X Non-specified Italy Saxifragaceae Saxifraga tombeanensis X Collection of plants by visitors Alto Garda Bresciano ? Italy Park Scrophulariaceae Verbascum litigiosum X Trampling by tourists; habitat Portugal degradation resulting from urbanising tourist sites Thymelaeaceae Daphne rodriguezii X Non-specified Minorca

Valerianaceae Centranthus amazonum X Maintenance/construction of Sardinia tourist infrastructure Violaceae Viola athois X Maintenance/construction of Greece tourist infrastructure