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BIOLOGICAL FLORA OF THE BRITISH ISLES* No. 274 List Vasc. Pl. Br. Isles (1992) no. 107, 4, 3 Biological Flora of the British Isles: Eryngium maritimum Maike Isermann1† and Paul Rooney2 1 Vegetation Ecology and Conservation Biology, Department of Ecology, Bremen University, Leobener Strasse, 28359 Bremen, Germany, and 2Sand Dune and Shingle Network, Department of Geography, Liverpool Hope University, Hope Park, Liverpool L16 9JD, UK Running head: Eryngium maritimum * Nomenclature of vascular plants follows Stace (2010) and, for non-British species, Flora Europaea. † Correspondence author. Email: [email protected] 64 Summary 1. This account presents information on all aspects of the biology of Eryngium maritimum L. (Sea Holly) that are relevant to understanding its ecological characteristics and behaviour. The main topics are presented within the standard framework of the Biological Flora of the British Isles: distribution, habitat, communities, responses to biotic factors, responses to environment, structure and physiology, phenology, floral and seed characters, herbivores and disease, history, and conservation. 2. Eryngium maritimum is a native perennial hemicryptophyte, with a large taproot, spiny and leathery leaves, and a pale bluish inflorescence. It has a more or less continuous distribution in suitable habitats along the coasts of Great Britain and Ireland up to about 55° N but it is more scattered further north. On the west coast it is found south of the Hebrides and on the east coast, with some exceptions, south of Yorkshire. In Europe it has a wide, but mainly southern-temperate, European distribution along the coasts of the Atlantic Ocean, the Baltic, the Mediterranean, and the Black and Azov Seas. Its northern distribution limit is at c. 60° N. 3. Eryngium maritimum grows typically on sand and shingle beaches, foredunes and yellow dunes, as well as in semi-fixed grey dunes. Its habitats have full sunlight and are more or less dry. It occurs in many coastal plant communities from the beach inland and, because of its wide European distribution, it occurs with members of several different biogeographic species-groups. 4. Protected from grazing by its spininess and sclerophylly, E. maritimum is nevertheless vulnerable to direct damage by trampling. It supports few insect herbivores, probably because of chemical defences. Historically, it has had a great number of medicinal uses. 5. Eryngium maritimum is unable to withstand competition from faster and more densely growing plant species. In many coastal regions, in both temperate mediterranean parts of Europe, it is one of the rarest and most threatened plant species, mainly because of habitat loss and land-use changes. Key-words: climatic limitation, communities, conservation, ecophysiology, geographical and altitudinal distribution, germination, herbivory, mycorrhiza, parasites and diseases, reproductive biology, soils 64 Sea Holly. Apiaceae subfamily Saniculoideae. A long-lived, perennial herb with a long, welldeveloped tap-root and thick and fleshy rhizomes extending laterally from buried stems. Reproductive stems 0.15-0.60 m; lower part often root-like and buried in the sand; arial part pale below but with bluish tinge above, erect, robust, terete or sulcate, glabrous, solid and widely branched above so that the plant forms an open cushion. Basal leaves several; lamina 4-10 x 15-20 cm, leathery, glabrous, intensely glaucous, subrotund in outline and palmately 3(-5) lobed; base truncate or cordate; venation palmate and reticulate, the veins thick, prominent; margin thick, cartilaginous, with large spinose teeth; petioles about as long as the lamina, with swollen bases. Cauline leaves similar but sessile and progressively smaller upwards. Vegetative individuals c.15 cm tall, consisting of a few basal leaves. Inflorescence a dense capitulum with spiny bracts. Capitula borne at apices of stems and branches, globose to broadly ovoid; peduncles stout, 3.5-5 cm. Bracts 5-7, ovate to ovatelanceolate, leaf-like. Bracteoles 2.5-4 mm, purplish blue, tricuspidate, spiny, longer than the flowers. Flowers 25-50, mainly hermaphrodite, with nectaries on a disc at the base. Sepals 5, 4-6 mm, exceeding the petals, bluish, lanceolate, with a prominent midrib which is excurrent as a stout spine. Petals 5, 3-4 mm, oblong, pale bluish white, emarginate. Stamens 5; filaments purplish to bluish; anthers yellow. Styles 2. Fruit a schizocarp, 8-14(15) mm, with persistent sepals, consisting of two mericarps each containing one seed; mericarps 6-7 mm, densely covered in narrow white scales and 5 ridges, the 3 dorsal ridges indistinct, the 2 lateral ridges more prominent and with airfilled cells. Eryngium maritimum is native to the British Isles, occuring widely on maritime sand and shingle. I. Geographical and altitudinal distribution Eryngium maritimum is a coastal species throughout its range. It occurs more or less continuously along the west coast of England and in Ireland up to latitude 56° N, whereas along the east coast the contiguous distribution reaches only 54° N (Fig. 1). In N.E. England and Scotland it occurs in scattered localities; it was found as far north as Shetland until 1884 near Fitful Head probably at the Bay of Quendale (Scott 2011), its recorded world northern limit. In Britain the distribution is orientated to the South (South-North Index 2.5, where the value of the most southerly and westerly distributed species was defined as 0, and those of the most northerly and easterly as 10; Fitter & Peat 1994). It is more abundant on the west coast, although formerly there was probably no western preference (East-West Index of 5.73). The distribution of E. maritimum in northern Britain is limited by the lack of suitable of dune systems (Doody 2008). 64 Eryngium maritimum has a wide native distribution in Europe and adjacent parts of northern Africa and Middle East (Hegi 1975; Hultén & Fries 1986; Fitter & Peat 1994; Preston & Hill 1997), occurring the shores of the Atlantic Ocean, the Baltic, the Mediterranean, Black and Azov Seas (Fig. 2). Around the southern Baltic Sea E. maritimum is distributed in Denmark, Germany, Poland (Łabuz 2007), the Kaliningrad region, Lithuania, Latvia to Estonia, along the Skagerrak (Fries et al. 1971), and on the Swedish islands of Öland and Gotland (Fröman 1930). It occurs only in the southern parts of Norway (Fremstad & Moen 2001) and reaches a north-eastern distribution limit in the Gulf of Bothnia (Hegi 1975), a little north of 56° N in Sweden (Tyler 1969), and north-eastward up to the southern part of the Saaremaa Islands in Estonia (Rebassoo 1975; Olsauskas 1996). In Scandinavia it belongs to a southerly group of species (Pedersen 1990). Eryngium maritimum is distributed along the northern Mediterranean coast, including Malta and Gozo (Scapini 2002), and extends along that of the Black Sea (Uphof 1941; Eberle 1979; Van der Maarel & Van der Maarel-Versluys 1996). Its distribution along the southern Black Sea coast and the Azov Sea is scattered (Avižienė, Pakalnis & Senzikaite 2008). The species is absent from the shores of the Caspian Sea, the Canaries and Azores (Ridley 1930; Hultén & Fries 1986). On the southern Mediterranean coast it is recorded from Algeria, Egypt, Libya, Morocco and Tunisia (Turmel 1948; Hanifi, Kadik & Guittonneau 2007). In western Asia it occurs on Cyprus and Crete, and in Georgia, Israel, Lebanon, Syria, and Turkey (Chater 1968; Lakkis et al. 1996; Jawdat et al. 2010; USDA ARS, National Genetic Resources Program 2010; Akalin Uruşak et al. 2013). Eryngium maritimum has been introduced into parts of eastern North America (Hultén & Fries 1986): e.g. to Camden, New Jersey before 1881 (Britton 1881) and to Ellis Island, New York in 1922 (Mathias & Lincoln 1941), where it was used as ornamental plant for seashore restoration (Lieberman & O’Neill 1988). It is naturalised along the eastern seaboard of Canada (Ontario) and the USA (Virginia, New York, New Jersey, North Carolina; USDA, NRCS 2012) but is not considered invasive in New Jersey (New Jersey Invasive Species Council 2009). Eryngium maritimum has been introduced to Australia with plantings of Ammophila arenaria (Weeda 1987) and is naturalised in southeast Australia (Pálá-Paúl et al. 2006) where it occurs at 5 sites on the coast of New South Wales (Hnatiuk 1990; eFloraSA 1999). It is considered a potential weed in Australia (Csurhes & Edwards 1998), but no dominant stands have been recorded recently and it grows in similar habitats to those in Europe (Graham Prichard, pers. comm.). II. Habitat (A) CLIMATIC AND TOPOGRAPHICAL LIMITATIONS 64 Eryngium maritimum is a member of the EuropeanSouthern-temperate floristic biogeographic element (Preston & Hill 1997), confined to regions with mild winters. Bournérias & Wattez (1990) classified it as a member of the Mediterranean-Atlantic phytogeographical element but this differs from Preston & Hill’s definition of this element, as it scarcely extends further north in western Europe than it does in the east (Fig. 2). The Gulf Stream facilitates its distribution along the Atlantic coast. According to Clausing, Vickers & Kadereit (2000) the northern distribution limit of E. maritimum in Europe corresponds approximately with the 8 °C January and the 14 °C July isotherm. However, its northern limit in southern Norway and Sweden (Hultén & Fries 1986; Fitter & Peat 1994; Preston 2007) corresponds with the 0 °C January and 15 °C July isotherms (Bengtsson, Appelqvist & Lindholm 2009). In the British Isles the 10 x 10 km squares (hectads) occupied by E. maritimum have a January mean temperature of 4.7 °C, a July mean temperature of 15.2 °C and annual precipitation of 1010 mm (Hill et al. 2004). Eryngium maritimum is a member of a group of British plant species, characterised by Crithmum maritimum, whose area of distribution has the second highest mean January temperature (5.2 °C) among the groups in Britain and Ireland recognized by Preston et al. (2013). (B) SUBSTRATUM Eryngium maritimum grows on beaches, foredunes and yellow dunes, as well as grey dunes, (Forey et al. 2008). In Wales it is considered as an obligate dune species or one strongly associated with sand dunes (Rhind & Jones 1999). However, it does occur on shingle, especially where there is some sand content and on similar soils where Ammophila arenaria and Euphorbia paralias occur (Scott 1963; Moore & Wilson 1999; Doody 2001; Hitchmough, Kendle & Paraskevopoulou 2001; Doody & Randall 2003). It occurs especially on dunes and sandy shingle where blown sand is less active than on the beach, but where sand accretion is still relatively high; this results in open vegetation which receives nutrients from sea-spray, carbonates from mollusc shells and material blown from the driftline. Eryngium maritimum is also recorded from dry-deflation (blow out type) features that form as depressions between moving dune ridges (Ėringis & Pancekauskienė 1995). The driftline itself does not favour the establishment of E. maritimum. Very rarely, it is found on rocky coasts (Eberle 1979), probably where there is some sand, or on sandy patches between artificial hard coastal protection features that have similar structural qualities to shingle e.g. at Hall Road on the Sefton coast, north west England (Maike Isermann pers. obs.). Soil on foredunes mainly consists of sand, with low silt and clay contents, for example 89.8% sand, 6.0% silt and 4.2% clay in Iğneada, Turkey, Black Sea (Ali Kavgaci pers. comm.). Foredune soils with E. maritimum along the Saros Gulf (north Aegean Sea, Turkey) contain 95% sand, with 64 about 70% medium to fine grained sands (0.5-0.215 mm), 23% with sand grains below 0.215 mm, and 2.1-2.6% classed as clays and silts (Özcan et al. 2010). Soils where Eryngium maritimum occurs have a neutral or somewhat higher soil pH. In Britain soil pHs of 6.9 - 7.7 are typical (Moore 1931). More broadly, ranges of pH are 6.2 - 8.5 with means c. 6.7, but exceptionally as low as 4.5 (Pancekauskienė 2003; Avižienė, Pakalnis & Senzikaite 2008; Forey et al. 2008; Andersone et al. 2011; Ali Kavgaci pers. comm.). The CaCO3 content of these soils can be as high as 18.0% (Greiß et al. 1995), but is usually lower, e.g. at sites in Turkey with 8.42% (Ali Kavgaci pers. comm.) and on the Isle of Man with 2.73% (Moore 1931). At low pH, E. maritimum presumably occurs on dunes with even lower carbonate contents. Soil organic matter content is generally low; 0 - 1.3% (means 0.4-0.7%) especially where there is low grass cover (Pancekauskienė 2003; Avižienė, Pakalnis & Senzikaite 2008; Andersone et al. 2011; Ali Kavgaci pers. comm.). An organic matter content of about 0.86% was measured on the Isle of Man (Moore 1931). Dune soils supporting E. maritimum are generally low in nutrients (Fitter & Peat 1994), but can be enriched for example by the addition of driftline material or shells. There are low concentrations of total nitrogen (0-320 mg kg-1) and total potassium (19-85 mg kg-1, n = 66). Total phosphorus concentrations vary (typically146-200 mg kg-1;Andersone et al. 2011) but may be much higher, between 578 and 1000 mg kg-1 (mean 732 mg kg-1; Pancekauskienė 2003; Avižienė, Pakalnis & Senzikaite 2008). Total concentrations of elements on Turkish dunes were determined as: Na 33, K 19, Ca 1550, Mg 55, P 2 mg kg-1 (Ali Kavgaci pers. comm.). Salt content, expressed as chloride compounds, reaches values of 4500 - 6700 mg kg-1 in dunes along the Danish North Sea coast (Greiß et al. 1995); in contrast, Andersone et al. (2011) reported Cl- concentrations of only 13-20 mg kg-1 (equivalent to 21-33 NaCl mg kg-1). Sites are more or less dry, with a well-drained soil (Forey et al. 2008). These environmental conditions are reflected in the ecological indicator values for E. maritimum (Appendix S1. Sources for Table 2: Biogeographical species-groups distinguished by TWINSPAN classification of species frequency in 8 biogeographic regions from Europe and adjacent countries. Appendix S2. Additional acknowledgements. 64 Table 1. Indicator values for Eryngium maritimum for light (L), temperature (T), continentality (K), moisture (F), soil pH (R), nitrogen (N) and salinity (S) in different parts of its range. UK (range 1-9, except F 1-12; Hill et al. 1999); N.W. Europe (range 1-9, except F 1-12; Ellenberg et al. 1991). Indicator values for the eastern parts of its distribution are missing (Ramensky et al. 1956). Values of The Netherlands (Bakkenes et al. 2002) are recalibrated on the basis of the Dutch vegetation database, giving mean, minimum and maximum values. Values for Greece (Böhling 1995) range 14 or 5 Indicator UK L - light 9 T - temperature 6 K - continentality 3 F - moisture 4 R - soil pH 6 N - nitrogen 5 S - salinity 3+ 9 6 3 4 7 4 N.W. Europe Netherlands full light moderate to warm oceanic to suboceanic dry to moderate fresh 4.52 (3.00-6.48) slightly acid to basic 6.44 (4.00-7.50) poor to moderate 4.54 (2.50-7.20) ? Greece 4 extreme warm 2 very dry habitats 5 calcifuge 3 facultative halophyte Table 2. Biogeographical species-groups distinguished by TWINSPAN classification of species frequency (%) in 8 biogeographic regions. It includes Black Sea S Eur. Atlantic and Mediter. Sea NW Eur. Atlantic and North Sea N North Sea and Baltic Sea NE Black Sea SW Black Sea NE and central N Medit S Eur. Atlantic, NW and S Medit. Sea NW Atlantic-S North Sea, SW Baltic North Sea NE and central S Baltic Sea N North Sea and NW Baltic Sea Twinspan step Number of relevés Eryngium maritimum Black Sea, Mediterranean Sea, S.W. Atlantic Polygonum maritimum Salsola kali Euphorbia peplis Xanthium strumarium Cakile maritima Elytrigia juncea Euphorbia paralias Medicago marina L. Pancratium maritimum Echinophora spinosa L. Sporobolus pungens (Schreb.) Kunth Achillea maritima Ammophila arenaria (L.) Link ssp. arundinacea H.Lindb. Cyperus capitatus Vand. Crucianella maritima L. Black Sea Crambe maritima NW Atlantic, North Sea, Baltic Sea Biogeographic region Black Sea, Medit. Sea, SW Atlantic 3605 relevés from Europe and adjacent countries. Names of syntaxa follow Mucina (1997). Sources are given in Appendix S1 1 2250 100 2 1355 100 1,1 240 100 1,2 2010 100 2,1 1219 100 2,2 136 100 1,11 155 100 1,12 85 100 1,21 1496 100 1,22 514 100 2,11 953 100 2,12 266 100 2,21 132 100 2,22 4 100 13 23 11 18 31 62 32 36 31 28 27 23 1 9 1 0 14 33 14 1 1 1 1 2 13 30 12 36 28 11 4 3 2 . . 1 13 22 11 16 32 68 36 39 34 31 30 25 1 9 1 . 15 37 16 2 1 1 1 3 . 4 . 3 5 2 . . . . . . 6 28 10 35 36 6 4 3 1 . . 2 26 32 16 39 13 21 5 5 2 . . . 12 25 13 20 35 69 32 42 34 36 35 26 15 11 4 2 23 64 46 33 35 15 17 24 1 10 1 . 18 31 13 2 1 1 1 2 . 5 0 . 5 58 25 . . . . 6 . 4 . 3 5 2 . . . . . . . . . . . . . . . . . . 22 21 10 . 0 0 . 1 . 24 23 11 . 0 0 . . . . . . . 2 . 21 27 5 35 11 26 . 0 0 . . . . . . . . . 4 3 41 0 3 1 46 32 . 0 4 0 . 25 64 Lactuca tatarica 4 Euphorbia seguieriana Neck. 2 Linaria dalmatica 2 Alyssum hirsutum M.Bieb. 1 Cynanchum acutum L. 2 Artemisia tschernieviana Besser 3 Gypsophila perfoliata L. 2 Melilotus albus 3 Artemisia santonicum L. 2 Carex ligerica J.Gay 1 Phragmites australis 4 Seseli tortuosum L. 4 Elymus elongatus (Host) Runemark 2 Centaurea arenaria M.Bieb. ex Willd. 3 Medicago sativa 2 Secale sylvestre Host 1 Silene thymifolia Sm. 2 Chondrilla juncea L. 2 N.E. Black Sea Glycyrrhiza glabra L. 1 Bromus squarrosus 1 Astrodaucus littoralis (M.Bieb.) Drude 1 Galium humifusum M.Bieb. 1 Polygonum arenarium 1 Salsola soda L. 1 Argusia sibirica (L.) Dandy 1 Suaeda maritima 1 Cynodon dactylon 7 S.W. Black Sea Silene conica 1 S. European Atlantic and Mediterranean Sea Calystegia soldanella 27 Lotus cytisoides L. 8 Cutandia maritima (L.) Barbey 8 S. European Atlantic, N.W. and S. Mediterranean Sea Lotus creticus L. 6 Malcolmia littorea (L.) R.Br. 3 3 . 0 . . . . 1 . 0 2 . . . 1 . . 2 38 19 16 12 11 25 18 17 14 13 11 10 10 30 19 13 11 10 0 . 0 . 1 . . 1 . . 3 3 2 . 0 0 0 1 3 . . . . . . 1 . . 2 . . . 1 . . 3 . . 2 . . . . . . 1 . . . . . . . . 34 15 7 14 10 38 27 21 22 16 15 16 14 15 5 6 . 5 44 26 33 8 12 2 2 9 . 7 4 . 1 59 44 26 31 18 0 . 0 . 1 . . 2 . . 3 3 2 . 0 0 1 2 . . . . 0 . . . . . 1 3 . . . . . 1 4 . . . . . . 1 . . 3 . . . 1 . . 3 . . . . . . . 1 . . . . . . . . . . . . 2 . . . . . . 1 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0 . 1 3 9 9 9 8 8 8 8 7 6 1 0 . . 0 0 0 0 8 . . . . . 0 . 1 3 . . . . . . . . . 14 14 14 13 12 12 12 10 10 . . . . . . . . . 1 0 . . 0 1 0 1 9 . . . . . . . 0 2 . . . . . 0 . 1 4 . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 6 0 2 . 2 13 0 . 3 . . . 18 . . . . . 30 10 9 21 . . . . . . . . . . . 26 9 10 43 10 9 19 . . 27 . . . . . . . . . . . . 7 4 . . . . . . . . 3 0 17 13 . . . . . . . . 64 Aetheorhiza bulbosa Helichrysum stoechas (L.) Moench N.W. Atlantic, North Sea, Baltic Sea Ammophila arenaria Festuca rubra Carex arenaria Honckenya peploides Leymus arenarius X Calammophila baltica Galium album N.W. European Atlantic and North Sea Hypochaeris radicata Sedum acre Taraxacum sect. Ruderalia Lotus corniculatus Sonchus arvensis Galium verum Cerastium semidecandrum Leontodon saxatilis Phleum arenarium Plantago lanceolata Hippophae rhamnoides Poa pratensis Ononis repens Senecio jacobaea L. S North Sea Cerastium diffusum Tripleurospermum maritimum North Sea and Baltic Sea Hieracium umbellatum Corynephorus canescens Jasione montana Viola tricolor Artemisia campestris Lathyrus japonicus ssp. maritimus Festuca polesica Zapall. Linaria odora (M.Bieb.) Fisch. 5 4 . 2 . . 6 4 . 2 . . . . . . 4 2 12 12 . 2 . . . . . . 17 . 1 1 0 . . 67 63 43 29 24 10 10 16 . . . 3 . . 17 . 1 1 . . . 68 63 44 29 24 10 10 60 57 32 25 23 15 8 . . . . . . . 45 . . . 9 . . 17 . . . . . . 16 . 5 6 . . . 69 65 46 26 29 12 13 65 56 36 42 5 0 2 60 56 31 25 20 16 8 50 100 75 25 100 . . 3 0 . 1 0 . 0 1 1 1 0 . . . 25 25 19 18 16 16 16 15 14 14 12 11 9 10 . . . . 1 . 0 . . . . . . . 3 0 . 1 . . . 2 2 1 0 . . . 28 27 21 20 18 18 17 16 16 15 13 12 10 11 1 7 2 1 1 3 2 2 . . 3 3 . . . . . . . . 1 . . . . . . . . . . . 2 . . . . . . . . . 4 0 . 1 . . . . 2 1 0 . . . 1 0 . . . . . 6 . 0 . . . . 24 30 20 14 21 16 20 16 18 13 16 11 9 8 42 14 27 39 6 25 8 17 9 25 1 18 12 23 2 5 2 . . 2 2 2 . . 3 2 . . . 50 25 25 50 50 . . . . . 50 . . 0 0 8 7 . . 0 0 8 8 . . . . . . . . 1 1 6 6 16 12 . . . . . 1 0 . 4 . . 0 31 20 16 12 12 7 3 2 . . . . 3 . . . . 1 0 . 4 . . 0 26 18 14 10 6 5 0 . 78 40 32 26 59 28 23 18 . . . . 1 . . . . . . . 6 . . . . . 0 . 1 . . 0 . 4 0 . 11 . . . 34 22 17 12 8 6 1 . . 2 2 4 . 1 . . 80 42 33 27 61 27 23 19 25 . . . . 50 . . 64 Helichrysum arenarium (L.) Moench Calamagrostis epigejos N.E. and central S. Baltic Sea Thymus serpyllum Festuca lemanii Salix daphnoides Tragopogon floccosus Waldst. & Kit. N. North Sea and N.W. Baltic Sea Potentilla anserina Elytrigia repens Atriplex prostrata Arrhenatherum elatius Plantago maritima Linaria vulgaris Atriplex littoralis Sedum telephium Vicia cracca . 1 3 4 . 7 . . 2 3 18 13 . 6 . 8 . . . . 2 3 . . 18 13 . . . . . . 3 1 1 1 . . . . . . . . 2 . . . 9 9 9 9 . . . . . . . . . . . . . . . . 3 . . . . . . . 9 9 9 9 . . . . . 0 1 . 0 0 . . 0 4 7 5 1 2 3 2 1 1 . 2 3 . 3 2 . . . . 0 1 . . . . . 0 4 7 5 1 2 3 2 1 1 2 3 2 1 1 1 1 1 1 . 3 4 . 4 3 . . . . . . . . . . . . . 0 1 . . . . . 0 . . 1 . . . . . . 3 9 6 2 2 4 3 1 1 7 . 2 . 2 . . . . . 2 1 . 1 1 1 . . 75 50 50 50 25 25 25 25 25 III. Communities In Great Britain Eryngium maritimum is scattered in shingle and strandline communities (Fig. 3a) such as the Honckenya peploides-Cakile maritima strandline community (SD2, Rodwell 2000). The community occurs above the tidal limit as patchy strips of pioneer vegetation with Cakile maritima and Honckenya peploides on sand and fine shingle strandlines. Additions of driftline material also support the growth of nitrophilous ephemeral species. In contrast to Crambe maritima, Honckenya peploides, Lathyrus japonicus ssp. maritimus and Silene uniflora, that are capable of withstanding large amounts of burial by sand, E. maritimum grows on shingle and dunes that have low rates of sand accumulation (Scott 1963). On dunes, Eryngium maritimum is found in the Elymus farctus ssp. boreali-atlanticus foredune community (SD4, Rodwell 2000; Fig. 3b), the pioneer vegetation on foredunes, with Elytrigia juncea (E. farctus) as dominant. Ammophila arenaria can establish on the raised foredunes and, with ongoing sand accumulation, the foredune community develops continously into the Ammophila arenaria mobile dune community (SD6, Rodwell 2000), in which A. arenaria is dominant. Especially in more southern parts of Britain, E. maritimum is a characteristic species in this community (Rodwell 2000). With reduced sand accumulation, vegetation cover increases and the Ammophila arenaria-Festuca rubra semi-fixed dune community (SD7, Rodwell 2000) develops successively at the back of the first dune ridge. Where rates of sand accretion are not too high, many other plant species co-occur. Eryngium maritimum can persist in the semi-fixed dune community, which is dominated by Ammophila arenaria and short grasses like Festuca rubra, and has increasing numbers of herbs such as Anthyllis vulneraria, Sonchus arvensis, and Viola tricolor, as well as bryophytes such as Brachythecium albicans (Rhind & Jones 1999; Rodwell 2000). In warmer, southerly stands of Ammophila arenaria communities on the coast in Britain, Eryngium maritimum is associated with Calystegia soldanella and more thermophilous species such as Euphorbia paralias and E. portlandica, providing a link with the dune vegetation of the Atlantic coast further south in Europe (Rodwell 2000). Comparison of the floristic composition of plant communities with Eryngium maritimum from all over Europe, including 3605 relevés, reveals distinct biogeographical species groups (Table 2). Characteristic communities of the Black Sea and the Mediterranean Sea include Cakile maritima, Elytrigia juncea, Euphorbia paralias, Medicago marina and Pancratium maritimum. In Italy, for example, most of these species characterise different communities on embryonic and on yellow dunes (Ciccarelli, Bacaro & Chiarucci 2012, Prisco et al. 2012). 13 Around the Black Sea Eryngium maritimum communities typically contain Artemisia tschernieviana, Crambe maritima, Lactuca tatarica and Xanthium strumarium at higher frequencies than in E. maritimum communities along the S. European Atlantic and Mediterranean Sea (Table 2). Different species-groups are characteristic of the N.E. Black Sea (e.g. with Astrodaucus littoralis and Galium humifusum) and the S.W. Black Sea coasts (e.g. with Centaurea arenaria, Medicago sativa and Secale sylvestre). Typical species in Eryngium maritimum communities of the southern European Atlantic and the Mediterranean Sea are Achillea maritima (Otanthus maritimum), Ammophila arenaria ssp. arundinacea, Calystegia soldanella, Cutandia maritima, Echinophora spinosa, Elytrigia juncea, Euphorbia paralias, Medicago marina, Pancratium maritimum and Sporobolus pungens. In the south European Atlantic, N.W. Mediterranean and the south Mediterranean Sea, species such as Aetheorhiza bulbosa, Helichrysum stoechas, Malcolmia littorea and Lotus creticus are more frequent than in the north-east Mediterranean Sea area. Communities of the N.W. European Atlantic, the North Sea and the Baltic Sea are characterised, for example, by Ammophila arenaria, Carex arenaria, Festuca rubra, Hieracium umbellatum, Honckenya peploides, Leymus arenarius and Sedum acre. Within this group, communities of the N.W. European Atlantic and the North Sea are differentiated from S.W. Baltic communities by Cerastium semidecandrum, Galium verum, Hypochaeris radicata, Leontodon saxatilis, Lotus corniculatus, Phleum arenarium, Sedum acre and Sonchus arvensis. The biogeographic species group of the northern North Sea and the Baltic Sea is characterised for example by Artemisia campestris, Festuca polesica, Hieracium umbellatum and Lathyrus japonicus ssp. maritimus. Along the central south and the N.E. Baltic Sea Festuca lemanii, Salix daphnoides, Thymus serpyllum and Tragopogon floccosus are more frequent. The most northern communities more frequently include Arrhenatherum elatius, Atriplex littoralis, Atriplex prostrata, Elytrigia repens, Linaria vulgaris, Potentilla anserina, Sedum telephium and Vicia cracca. Eryngium maritimum is most frequent in mobile dunes and is usually categorised as a characteristic species of the class Ammophiletea Br.-Bl. et R. Tx. ex Westhoff et al. 1946 (synon: Ammophiletea R. Tx. in Knapp 1943, Ammophiletea Br.-Bl. et R. Tx. 1943, Helichryso-Crucianelletea maritimae J.-M. Géhu et al. in Bon et J.-M. Géhu 1973, Helichryso-Crucianelletea maritimae J.-M. Géhu et al. in J.-M. Géhu 1975, Euphorbio-Ammophiletea arundinaceae J.-M. Géhu et J. Géhu 1988) (Mucina 1997). However, E. maritimum is recognised in various other phytosociological classes: communities of Cakiletea maritimae that occur on driftlines, those of Honckenyo-Elymetea on sandy beaches and shingle, of Koelerio-Corynephoretea on semi-fixed and fixed dunes, of Saginetea maritimae on transition zones to salt marshes, of Crithmo-Staticetea representing chasmophytic coastal vegetation under salt-spray influence on rocks and sand. Often these 14 communities contain species of classes typical for nutrient rich stands like Artemisietea vulgaris, Epilobietea angustifolii and Galio-Urticetea; or in spatial associated communities like FestucoBrometea, Juncetea maritima, Puccinellio-Salicornietea and Salicornietea fruticosae; in older successional stages of first shrubs and trees, in classes such as Rhamno-Prunetea and Quercetea ilicis. Eryngium maritimum is affiliated to a functional group of plant species adapted to harsh environmental conditions, including the low nutrient content of the soils, across their whole range. This group includes perennials (or summer annuals) which are larger than 0.15 m, and mostly scleromorphs that grow in full light, have below-ground storage of reserves, are mostly dispersed by sea water, withstand sand burial, and show leaf succulence or reinforced cuticles (García-Mora, Gallego-Fernández & García-Novo 1999; 2000; Gallego-Fernández, García Mora & de Seoane 2003). IV. Response to biotic factors Grazing Eryngium maritimum is protected from grazing to a degree by its spininess and biochemical defences e.g. terpenes, which deter herbivores such as rabbits (Hicks 1895). Nevertheless, under strong grazing pressure, populations probably decline (Olsson & Tyler 2001), as the similar species E. campestre and E. nudicaule have been shown to be more frequent in areas without rabbits (Pucheta et al. 1998; Katona et al. 2004). However, grazing indirectly favours E. maritimum through the removal of potential competitors, as well as by the creation of open areas (Pedersen & Høiland 1989). Disturbance may result in the growth of new shoots from nodal root meristems (Andersone et al. 2011). Trampling Eryngium maritimum is vulnerable to direct damage from trampling both by humans and by larger grazing animals because its stems and roots are brittle (Stasiak 1986; Vökler 1992; Tzatzanis, Wrbka & Sauberer 2003). Trampling damage, especially to the rootstock, results in dieback of the plant. A decrease of grazing animals and therefore of direct damage by trampling resulted in a slight increase of Eryngium maritimum on Gotland (Lars Fröberg, pers. comm.). Trampling by humans in regions with high tourism pressure often causes a decline and local extinction (Stasiak 1986; Weber & Kendzior 2006; Żółkoś et al. 2007). Nevertheless, E. maritimum occurs frequently in and around dune blowouts (Mir-Gual et al. 2013). Thus, E. maritimum can grow on open, bare sand where fixed dunes have been destroyed (Tansley 1911; Heukels 2000), where there is some sand deposition (Forey et al. 2008). It is probably favoured by light human pressure, for example 15 along pathways to the beach where the vegetation cover is sparse and competition with other plant species reduced, and where some nutrient input occurs due to footpath management with straw mulches etc. (Weeda 1987). Competition Eryngium maritimum is a poor competitor (Stasiak 1986). It generally occupies open areas because it is out-competed, especially by densely growing species such as Carex arenaria in northern Europe. It declines when habitats are invaded by shrubs such as Elaeagnus commutata, Hippophae rhamnoides, Rosa rugosa (Fig. 3c) and Salix repens, because of shading effects. Similarly, in Portugal Acacia longifolia excludes Eryngium maritimum (Stasiak 1986; Pedersen & Høiland 1989; Bruun 2005; Stephan 2006; Bengtsson, Appelqvist & Lindholm 2009). On the south-eastern coast of France, the non-native species Carpobrotus edulis forms dense mats that out-compete E. maritimum (Suehs, Médail & Affre 2003). In Italy, the frequency of E. maritimum decreased by nearly 80% in embryonic and yellow dunes, when these dune types were dominated by Carpobrotus acinaciformis (Attorre et al. 2013). V. Response to environment (A) GREGARIOUSNESS The size of Eryngium maritimum populations varies greatly, from a single plant to more than several hundred individuals, and rarely to more than 1000 individuals (Burmester 2007; Curle, Stabbetorp & Nordal 2007). Large populations can exist even in regions where the species is rare (Halvorsen & Lima 1984). Fertile individuals show a 70-75% probability of surviving to the following year (Curle, Stabbetorp & Nordal 2007). The survival of small, vegetative individuals is low (26-37%) in comparison to that of large sterile and fertile individuals (70-100%) (Curle, Stabbetorp & Nordal 2007). Stems of reproductive individuals are (0.15)0.20-0.60 m tall, erect and branched in the upper part (Stace 2010; Jäger & Werner 2005; Avižienė, Pakalnis & Senzikaite 2008), whereas vegetative individuals are about 0.15 m tall (Fitter & Peat 1994). Eryngium maritimum is generally is long-lived (10-15 years) (Curle, Stabbetorp & Nordal 2007), and individuals may live to 30 or more years (Eberle 1979; Stephan 2006). Flowering and fruiting sometimes starts in the second year (Clausing, Vickers & Kadereit 2000), but often not until the fourth to sixth year (Curle, Stabbetorp & Nordal 2007; Avižienė, Pakalnis & Senzikaite 2008). In a situation of sand accumulation, juveniles need longer for the development of a first inflorescence, probably because internodal stem elongation is necessary to bring the rejuvenation bud near to the substrate surface (Burmester 2010). Because of the high mortality of juvenile individuals, several growing seasons are necessary to establish a stable or growing population (Frisendahl 1926; Curle, 16 Stabbetorp & Nordal 2007). Plants which have reached maturity and flowered at least once may fail to flower in some years in which conditions are adverse (Weeda 1987), i.e. poor nutrient availability, unusual temperature extremes or dry weather in spring and early summer etc. In general, the fraction of reproductive individuals characterizes the stability of a population; stable or growing populations are dominated by vegetative individuals (Curle, Stabbetorp & Nordal 2007). Long-term studies between 1968 and 1999, at the Curonian Spit, Lithuania and along the German Baltic coast, have suggested declining populations (Pancekauskienė 2003; Burmester 2007). (B) PERFORMANCE IN VARIOUS HABITATS Habitat suitability for Eryngium maritimum varies along the zonation from the driftline to fixed dunes. The best conditions for E. maritimum occur in areas where abiotic conditions are less harsh and there is also reduced competition by dense vegetation in the older successional stages. Storms and high tides characterise the environment of driftlines: substrate instability, salinity and water content probably constrain the growth of E. maritimum. In dry dune succession, under favourable environments, it first establishes on dunes that are between 3-10 years of age (Pignatti & Ubrizsy Savoia 1989). Eryngium maritimum is regarded as intermediate between competitor and stress-tolerant strategies (Grime 1979; Hitchmough, Kendle & Paraskevopoulou 2001). It establishes larger populations and grows more vigorously on yellow dunes than on foredunes, because of the more stable substrate and reduced effects of wind and blown sand (Łabuz 2007). Individuals may flower for many years favourable in sites (Burmester 2010), but sometimes individuals flower only once (Hegi 1975). Eryngium maritimum declines in older successional stages, such as on grey dunes (Prat & Salomon 1997; Stankevičiūtė 2006), where it is out-competed by dense grass or scrub. However, because of its rootstock it can persist vegetatively for long periods in older successional stages. The species benefits from moderate dune dynamics that create open sites (Stasiak 1986). In contrast to more western sites, in Poland, E. maritimum is found more frequently on grey dunes: about 40% of the individuals occur in foredunes and yellow dunes, 46% in open grey dunes and 14% in older grey dunes adjacent to Pinus forests (Stasiak 1988). In Poland its distribution has shifted during the last century from the yellow dunes to the grey dunes (Stasiak 1986; 1988). These changes were probably caused by the retreat of many parts of the coast, as well as by erosion of yellow dunes, and the establishment of seeds of E. maritimum blown inland along paths in grey dunes. The development of vegetation as well as soil conditions towards older successional stages is enhanced by acid deposition, pollutants and eutrophication (Van der Laan 1985). Where the dune area is 17 relatively small and only a few ridges occur, such along the Baltic Sea, seeds often are blown towards the forest where they are not able to establish (Łabuz 2007). (C) EFFECT OF FROST, DROUGHT, ETC. Coastal beaches, foredunes and yellow dunes worldwide are regularly subjected to similar types of environmental stress: salt spray, episodic over-wash, highly permeable substrates, low field capacity, high temperatures, drought, strong winds and substrate mobility (García-Mora, GallegoFernández & García-Novo 1999). Frost The above-ground parts of Eryngium maritimum probably tolerate short periods of light frost, but young shoots and seedlings are susceptible to frost particularly in spring. Therefore, in northern Europe the increased number of days with frost and the reduced length of the growing season limits the distribution of Eryngium maritimum (Halvorsen 1982; Bakker 1976; Curle, Stabbetorp & Nordal 2007). Sand mobility Moving sand is mostly a threat during seedling establishment, especially because of the disruption to root development (Eberle 1979). Eryngium maritimum is able to cope with a little sand burial, typically only up to 0.18 m (Walmsley 1995; Walmsley & Davy 2001), probably by shoot elongation (Frisendahl 1926; Turmel 1947; Salisbury 1952; Eberle 1979; Łukasiewicz 1985). The depth of sand burial tolerated by E. maritimum is less than that tolerated by Glaucium flavum (0.20 m), Lathyrus japonicus ssp. maritimus (0.37 m) and Honckenya peploides (0.41 m), but more than Crambe maritima (0.16 m) and Rumex crispus (0.15 m) (Walmsley 1995; Walmsley & Davy 2001). Its leaf characteristics provide good protection from wind and blown sand (Eberle 1979). Although high levels of sand accumulation may be disadvantageous to the survival of adult individuals, surface lowering may result in mechanical damage of the brittle roots by wind and water, and lead to death (Łabuz 2007). Eryngium maritimum tolerated surface lowering of about 0.19 m, less than Crambe maritima (0.22 m) and Honckenya peploides (0.26 m) but more than Glaucium flavum (0.04 m), Lathyrus japonicus ssp. maritimus and Rumex crispus (0.08 m) (Walmsley 1995; Walmsley & Davy 2001). Drought Eryngium maritimum occurs in very dry to moderately dry conditions. It has a well-developed taproot (Avižienė, Pakalnis & Senzikaite 2008), on average about 1.5 m long (Salisbury 1952), but can reach a length of 3(-5) m (Fig. 3d). This facilitates the absorption and storage of water (Hicks 1895; Eberle 1979; Avižienė, Pakalnis & Senzikaite 2008). Moreover, the rootstock may have 18 access the water table, which in dunes is frequently about 3-4 m below the surface (Ranwell 1972), although this varies with site and season. The more or less thick taproot enables the species to hold water reserves (Meyer & Van Dieken 1947) and thus it is able to survive dry periods. Water uptake is hampered in upper parts of the soil, especially in young plants, by salinity. Coarse substrates lead to water stress, and therefore probably limit the distribution of E. maritimum on shingle beaches (Walmsley 1995). The less favourable growing conditions of high precipitation and low temperatures mean that at the northern range of its distribution there is a decline of photosynthetic productivity (Andersone et al. 2011). Reduced physiological conditions are probably related to the increased clonal growth of E. maritimum in northern regions (Andersone et al. 2011). Nutrient supply Some nutrient availability arising from moderate amounts of driftline material seems to support the growth of Eryngium maritimum. However, raised soil nutrient concentrations caused by gull faeces have led to the decline or extinction of species such as E. maritimum, Artemisia caerulescens, Calystegia soldanella and Polypogon maritimus on the Riou archipelago near Marseille, France (Vidal et al. 1998). In recent decades the atmospheric deposition of nutrients, especially nitrogen and phosphate, has led to the increase of both dense, short and tall grasslands in dunes, and caused a decline in open dune areas, in north-west Europe (Veer & Kooijman 1997). Therefore, atmospheric deposition of nutrients reduces the habitat quality and indirectly promotes the decline in E. maritimum. Light Eryngium maritimum is a light-demanding plant, and thus grows only on open sites (Ćwikliński 1972). It is protected against high insolation, as well as the high levels of light reflection from the sand, by its equifacial leaves with multilayered palisade parenchyma (Eberle 1979). VI. Structure and physiology (A) MORPHOLOGY Eryngium maritimum is a slightly succulent xerophyte (Fig. 4) with adaptations including a welldeveloped root system and other scleromorphological traits (Delf 1912; Hanson 1950; Hegi 1975). Thus, the above-ground parts are more or less fleshy and, due to surface waxes, are greyish-blue sometimes greenish, or bluish throughout (Mathias & Lincoln 1941). The root and stem have a thick cambium with internal phelloderm and a very thick secondary cortex develops (Wolff 1913). The cortex and the pith/medulla of the napiformed taproot contain many oil channels (Eberle 1979). The stele/vascular bundles of the stem are interfascicular. The secondary bark has clearly visible medullary rays/vascular rays, and oil channels. Glands with calcium oxalate occur in the secondary bark as well as in the cortical parenchyma/cortex and in the pith (Erikson 1896). 19 A leaf cuticle with epicuticular waxes, in the form of massive wax rodlets (Fig. 5), protects the plant from water loss, and together with the cartilaginous margin, the cuticle protects the plant from the erosive effect of blown sand. The epicuticular waxes of Eryngium maritimum are similar to the so-called Strelitzia wax type, with massive projections composed of various wax crystalloids and rodlike subunits (Fröhlich & Barthlott 1988). The wax layer develops during the year (Samsone et al. 2007), giving the plant has a more or less bluish appearance at the end of the growing season. Epicuticular waxes are characteristically found in species such as Brassica oleracea, Crambe maritima, Leymus arenarius, Medicago maritima, Pancratium maritimum, and Salsola kali, which are pioneer colonists of open sites such as beaches (Neinhuis & Barthlott 1997). The stomata are counter-sunk in the two-plied epidermis (Chermezon 1910; Eberle 1979). Stomata are on both surfaces of the leaf (amphistomatous) as in most other dune and shingle species (Davy, Willis & Beerling 2001). The stomatal density (mm-²) on the upper (adaxial) surface varies between 243 (Delf 1912), 102 (Iversen 1936), 90 (Davy, Willis & Beerling 2001), 67 (Fitter & Peat 1994) , 60 (Erikson 1896) and 35 (Burmester 2010); correspondingly, on the lower (abaxial) surface it is between 149 (Delf 1912), 102 (Iversen 1936), 81 (Davy, Willis & Beerling 2001), 59 (Fitter & Peat 1994), 52 (Erikson 1896) and 38 (Burmester 2010). Thus, the ratio between upper and lower surface varies between 1:0.6 and 1:1.1. Like Eryngium maritimum, other coastal beach and dune species, particularly those that are somewhat succulent, have similar numbers on both leaf sides or more stomata on the upper leaf surface. In the northern distribution area, the stomatal density of Eryngium maritimum on the upper/lower surface (60/52, 90/81) is lower than in Lathyrus japonicus ssp. maritimus (70/80, 96/95), Petasites japonicus (88/130) (Erikson 1896), and Crambe maritima (102/104) (Davy, Willis & Beerling 2001). The higher the stomatal density, the greater the stomatal index (Salisbury 1952; Davy, Willis & Beerling 2001) and the stomatal index for shingle species is on average 16.8%. On the other hand, the stomatal density of the upper/lower surfaces is higher than in many other species of similar habitats (Honckenya peploides 49/80, 71/65, Salsola kali 71/0, Cakile maritima 127/163) (Delf 1912; Iversen 1936; Davy, Willis & Beerling 2001). The stomatal index of Eryngium maritimum is low (11.0/11.2) in comparison with other species (Davy, Willis & Beerling 2001). The leaves are xeromorphic; both upper and lower epidermes have thickened cell walls (Chermezon 1910; Burmester 2010). The leaf epidermis is collenchymatic, about 12-14 µm thick, and is thus similar to Petasites japonicus (9-12 µm) but much thicker than in Honckenya peploides (6 µm) (Erikson 1896). Under the two-layered epidermis of both the upper and the lower leaves, a 2-3 layered palisade mesophyll occurs. Between the two palisade parenchymas there are 2-3 layers of isodiametric cells forming the lacunary tissue. Therefore, the leaf has an equifacial structure as in Cakile maritima (Grigore & Toma 2008). Leaf areas range between 0.001-0.01 m² (Fitter & Peat 20 1994). Although Eryngium maritimum and Pancratium maritimum co-occur in Mediterranean semifixed coastal dunes, E. maritimum has a much greater leaf area index than P. maritimum (Table 3). In comparison with P. maritimum, E. maritimum, has fewer larger leaves (Gratani & Fiorentino 1988). (B) MYCORRHIZA Arbuscular mycorrhiza (AM) occurs in about 70% of species of coastal, sandy habitats, including Eryngium maritimum (Giovannetti & Nicolson 1983; Giovannetti 1985; Harley & Harley 1987; Maremmani et al. 2003; Nikopoulos et al. 2006). AM colonisation in E. maritimum is 3-18% of the total root length (Puppi & Riess 1987; Harley & Harley 1990; Çakan & Karataş 2006), but there are individuals that reach 70-90% (Read 1989, Andersone et al. 2011). Furthermore, the percentage of individuals with mycorrhiza is only about 33% (Puppi & Riess 1987), so it is facultatively mycorrhizal (Harley & Harley 1987). A number of species of AM fungi occur in coastal dunes (Giovannetti & Avio 1983; Błaszkowski, Adamska & Czerniawska 2003). The highest number spores of Glomus spp., Gigaspora gregaria and Gigaspora calospora occurred with Ammophila arenaria, Helichrysum spp. and Eryngium maritimum in Italian sand dunes: under Eryngium maritimum up to 102 spores 100 g-1 of sand was recorded (Giovannetti & Avio 1983). Colonization of E. maritimum with AM varies during the year in relation to photosynthetic activity, and inversely with leaf chlorophyll content (Andersone et al. 2011). Colonisation increases from late winter/early spring until the beginning flowering season in early summer, decreases during summer, and stays relatively constant in autumn and winter (Giovanetti 1985; Andersone et al. 2011). (C) PERENNATION: REPRODUCTION Eryngium maritimum shows both sexual and vegetative reproduction. Mediterranean populations appear to be more age-differentiated, with large numbers of seedlings and young plants (Stasiak 1986), whereas in the northern part of its range seed production appears to be reduced (Stasiak 1986; Stephan 2006; Bengtsson, Appelqvist & Lindholm 2009), and populations seem to be maintained by vegetative reproduction (Stasiak 1986). This probable change from sexual to vegetative reproduction in the northern distribution area suggests reduced fitness of the species at the climatic extremes of its geographical range (Stasiak 1986). Vegetative reproduction by offshoots from rhizomes or root fragments, which are possibly distributed by the sea, seems to be common particularly in the case of burial by sand (Frisendahl 1926; Blackman 1935; Turmel 1947; Wołk 1973; Walmsley 1995). E. maritimum is a clump former 21 (Hitchmough, Kendle & Paraskevopoulou 2001), and juveniles growing 2-3 m from a stock/maternal plant, may be connected to it deep in the sand (Frisendahl 1926; Stasiak 1986; Avižienė, Pakalnis & Senzikaite 2008). A possible sequence of clonal growth starts with branches attached to the mature plant, and then with sand accumulation the shoots develop into separate individuals (Andersone et al. 2011). Vegetative reproduction is used in horticulture, where root cuttings are taken in winter (Christopher 2006). (D) CHROMOSOMES The chromosome number is 2n = 16 (Wulff 1937; Maude 1939; Bowden 1945 (cultivated plants); Malheiros-Gardé & Gardé 1951; Hamel 1955; Skalińska et al. 1964; Valdés-Bermojo 1979; Perdigó Arisó & Llauradó Miravall 1985; Al-Bermani et al. 1993; Wörz 1999; Curle, Stabbetorp & Nordal 2007). A high degree of heterozygosity implies that the species is probably tetraploid with a basic chromosome number x = 4 (Curle, Stabbetorp & Nordal 2007). Genetic variation and geographic distribution along the European coasts are well correlated (see X History. Phylogeography). (E) PHYSIOLOGICAL DATA The photosynthetic pathway is assumed to be C3 (Fitter & Peat 1994). Predictions of transpiration rate, photosynthetic rate and water-use efficiency were made from stomatal measurements (Davy, Willis & Beerling 2001). In comparison to other shingle species, Eryngium maritimum has a slightly higher photosynthetic rate (17.6 µmol m-2 s-1, mean 17.5), a clearly lower water vapour conductance (812 mmol m-2 s-1, mean 1054.5), a lower transpiration rate (6.5 mmol m-2 s-1, mean 8.1) and a higher photosynthetic water use efficiency (2.7 mmol CO2/mol H2O, mean 2.33) (Davy, Willis & Beerling 2001). Comparing it with the dune species Ammophila arenaria, Anthemis maritima, Cakile maritima, Elytrigia juncea, Ononis variegata and Pancratium maritimum, Eryngium maritimum had the highest leaf area (0.0067 m²) and ranked third for leaf mass area (14.6 mg cm-2). Eryngium maritimum has the second highest succulence index (81.5 mg cm-2) behind Cakile maritima, with values of the species studied between 28.3 and 96.4 mg cm-2 (Gratani, Varone & Crescente 2009). E. maritimum produced greatest biomass during experiments at 25/15 °C day/night-temperature treatments, and growth was lower in 20/10 °C and 30/20 °C treatments (Arve 2008). (F) BIOCHEMICAL DATA In common with other Eryngium species, E. maritimum contains bioactive secondary metabolites. Flavonoids, polyacetylenes and essential oils are present in aerial parts, while triterpene saponins 22 and monoterpenoid glycosides are observed mainly in the roots. Saponin complexes are also found in aerial parts, but their composition is different. Phenolic acids are present in a whole plant and coumarins in fruits and roots. Triterpene saponins occur mainly as saponin complexes with ester structures such as polyhydroxytriterpenoid glycosides and phenolic acids, e.g. rosmarinic acids and its derivates, chlorogenic acid and caffeic acid (Hiller 1971; Hiller, von Mach & Franke 1976; Kartal et al. 2005; 2006; Le Claire et al. 2005; Thiem & Wiatrowska 2007; Kikowska, Thiem & Krawczyk 2009; Thiem & Kikowska 2009). Some saponins possess anti-inflammatory properties, anti-HIV-1 protease activity and cytotoxicity for tumour cells (Roberg 1937; Zhang et al. 2008). Flavonoids were identified from the above-ground parts of Eryngium maritimum (Hiller, Pohl & Franke 1981; Kartnig & Wolf 1993; Hohmann et al. 1997), particulary flavonol glycosides (kaempferol and quercetin derivatives) and poliacetylenes (falcarinol, falcarinon, falcarinolon) (Hegnauer 1973; Lam, Christensen & Thomasen 1992; Christensen & Brandt 2006). Essential oils are frequent in species of Apiaceae. The genus Eryngium, belonging to the subfamily Saniculoideae, does not contain large amounts of essential oil (Aslan & Kartal 2006; Djarri et al. 2008). The average oil content of the seeds is 31% (Barclay & Earle 1974). The essential oil composition of E. maritimum consists of several dozen compounds, varied in their amount and concentration in different parts of the plant (Palá-Paúl 2002, 2006; Ayoub, Kubeczka & Nawwar 2003; Brophy et al. 2003; Ayoub et al. 2006). The main components of the aerial parts are germacrene D (43%) and 9-muurolen-15-aldehyde (20%) and in the roots γ-guaiene (40%), 2,3,4trimethyl-benzylaldehyde (24%) and germacrene D (10%) (Palá-Paúl et al. 2005 a; b). Major compounds consisting of more than 2% of the total amount of essential oils in the leaves are αpinene, germacrene D, bicyclogermacrene, germacrene B and δ-cadinene (Machado et al. 2010). Further components are described by Muckensturm et al. (2010). Eryngium species contain coumarins (Erdelmeier & Sticher 1985), betaines (Adrian-Romero et al. 1998) and tannins (Dinan, Savchenko & Whiting 2001). Eryngium species are well-known worldwide in traditional medicine. They provide raw materials for Eryngii herba and Eryngii radix, both of which are herbal medicines. Extracts from aerial and root parts of Eryngium species show anti-inflammatory and antinociceptive activity, and are used in folk medicine as an antitussive, analgesic, diuretic, appetizer, stimulant and aphrodisiac (Lisciani et al. 1984; Küpeli et al. 2006; Thiem & Wiatrowska 2007). Moreover, Eryngium species possess antimicrobial (Meot-Duros, Le Floch & Magné 2008), mainly antimycotic, qualities (Barbara Thiem pers. comm.). VII. Phenology 23 Growth of Eryngium maritimum each year starts with the development of one or more basal leaves. A flowering stem develops at the centre of the basal rosette. In the northern part of its distribution, the basal leaves remain until late autumn, dying back as late as November (Eberle 1979), whereas in the Mediteranean the leaves die back during summer (Giovannetti 1985). In the southern part of Britain the flowering period extends from June/July to August (Tutin 1980; Fitter & Peat 1994). However, the flowering season varies with climatic region, according to temperature, with a gradient (Table 4) across Europe. Flowering starts as the average daily maximum temperature reaches 18-23 °C, and starting during April/May on the south Mediterranean coast. Along the north-east Mediterranean coast the flowering season starts about one month earlier than on the north west Mediterranean coast. Similarly, along the Atlantic coast in the south up to France, the flowering season begins about one month earlier than along the North Sea and the Northern Atlantic coasts. Along the coast of the Swedish Skagerrak (Bohuslän) the main flowering time is July to August (Korhonen 2011). It seems that along the northern Atlantic and the Baltic Sea coasts, the main flowering period is shorter. The time between anthesis and dissemination is on average 78.6 days (Burmester 2010). Ripening of seeds occurs along the German North Sea coast during September and October (Eberle 1979), and finally along the Baltic in late September and October (Olšauskas & Olšauskaite Urboniene 1999; Avižienė, Pakalnis & Senzikaite 2008). The onset of germination and the growing season show similar geographicaal patterns throughout Europe, again beginning in the Mediterranean area (Gratani, Fiorentino & Fida 1986). The decay of the aboveground parts of the plant starts in Italy as early as August (Gratani, Fiorentino & Fida 1986). VIII. Floral and seed characters (A) FLORAL BIOLOGY Flowers The flowering plant produces one terminal umbel that is larger and flowers earlier than the other umbels (Burmester 2010). The inflorescence is a dense, subglobose or ovoid capitulum, 1.5-3 cm in length and an average of 2 cm across (Bodkin 1986; Stace 2010) with ovate, spiny bracts. The inflorescence is pale blue to conspicuously amethystine. Each inflorescence contains 25-50, pedicellate, inconspicuous five-petalled flowers. Sepals are 4-5 mm long, ovate-lanceolate, aristate, and bluish. Petals are light blue, each about 10 mm long. Flowers are composed of purplish-bluish filaments, sometimes more pink (Sell & Murrell 2009). The bracteoles are 3-cuspidate, nearly three-lobed, greenish above and below, never bicoloured, 2.5-4 cm in length, herbaceous or coriaceous, and ovate or ovate-lanceolate (Mathias & Lincoln 1941). In the axils of the bracts, branches (paraclades) develop up to a third order, with further flower heads on these. Thus a whorl develops below the terminal umbel. Fertile seeds develop mainly in the upper flower heads. The 24 number of flower heads is usually, but not necessarily always, larger in older individuals (Burmester 2010). The close agglomeration of flowers in a flower head and the coloured bracts serve to attract insects (Hegi 1975). During the flowering season, cells enclose anthocyanins which cause the colour and dissipate with drying at the end of the growing season (Eberle 1979). The ovary is epigynous with an anatropous ovule. Nectar glands, with nectar of high glucose content (about 2%), occur on a disc at the base of the flowers (Eberle 1979). Flowering starts with the basal flowers of the inflorescence and procedes upwards (Eberle 1979). The flowers are protandrous (Bell 1971), and the style is receptive 3-5 days after anthesis (Burmester 2010). Flowers are usually cross-pollinated but selfing is possible (Klotz, Kühn & Durka 2002). Pollen Studies from the Mediterranean to the North Sea demonstrate homogeneity in the size of the pollen grains (polar axis and equatorial diameter) within one inflorescence but great variation within one plants and within populations (Van der Pluym & Hideux 1977). Pollen size varies in an individual plant, depending on the position of the flowers in the inflorescence, and the hierarchical level in the umbel (Van der Pluym & Hideux 1977). The pollen is subrectangular, with an endocolpus (transverse furrow vertical to the equatorial level), distinctly elongated, and sometimes fused into an endocingulum (describing a pollen grain with a continuous endoaperture around the equator). The ectocolpus is long, and the costae broad. The mean polar axis (P) (silicone oil/gylcerine jelly) is 44.5-50.5 µm, and the equatorial diameter (E) is 24.0-25.0 µm, resulting in a P/E ratio mean of 1.96-1.85 (Van der Pluym & Hideux 1977; Punt 1984). Van der Pluym & Hideux (1977) show light and scanning electron microscopy micrographs. Eryngium maritimum generally has low pollen production; thus in Turkey the pollen is a regular but minor component in honey and reaches 4% of the total amount (Silici & Gökceoglu 2007). Insects probably visit the flowers particularly for nectar (Bell 1971). Pollinators Eryngium maritimum is pollinated by generalist insects (Halvorsen 1982; Fitter & Peat 1994). Its sand-dune habitats are important for bees (e.g. Grace 2010), wasps and ants because they are mainly thermophilous. Bivoltine insects are especially dependent upon pollen and nectar produced by plants with long, or such as in the case of E. maritimum, late flowering periods (Howe, Knight & Clee 2010). Insects visiting E. maritimum include many Hymenoptera. Some species such as Colletes floralis E. show a preference for Apiaceae pollen, particularly in coastal areas (Westrich 2001). It is visited by bees such as Megachile maritima Kirby (De Rond 2009) and Sphecodes albilabris F., bumble bees including Bombus distinguendus Mor., B. lapidarius L., B. lucorum, B. soraensis F., and B. terrestris L., as well as diggerwasps such as Ammophila sabulosa L. and Cerceris arenaria L. 25 (Hegi 1975; De Rond 2009). The carpenter bee Ceratina cyanea Kirby was observed only once on Eryngium maritimum by Terzo, Iserbyt & Rasmont (2007). Diptera such as Syrphus ribesii L., S. umbellatarum F., and Sarcophaga carnaria L. are longtongued and could be pollinators of Eryngium maritimum (Hegi 1975). Among the Lepidoptera, the butterflies Cynthia cardui L., Lycaena semiargus Rott., Polygommatus phlaeas L., Pyrameis atalanta L. and Vanessa atalanta L., V. urticae L., and species of the Pieridae, as well as the moth Autographa gamma L., are pollinators of Eryngium maritimum (Eberle 1979; Hegi 1975). Coleoptera including Notoxus monoceros L. (Bucciarelli 1977) and Macrosiagon tricuspidatum Lepechin occur generally on the flowers of Apiaceae, but with preference for Eryngium maritimum (Zanella et al. 2009). The heteropteran Graphosoma semipunctatum F. also visits the flowers (Ribes & Sauleda 1979). (B) HYBRIDS Many species of the Eryngium are polyploids and thus natural hybrids are probably common (Calviño, Martínez & Downie 2008), but hybrids of E. maritimum are generally not known. However, there are records of a hybrid between E. maritimum and E. campestre (= Eryngium x rocheri Corb. ex Guétrot) in France (Stace 1975; Wörz 1999), and in the region of Valencia, Spain (Aparicio Rojo 2002). (C) SEED PRODUCTION AND DISPERSAL Seed production The terminal flower heads usually produce c. 35 fruits, each with two mericarps, whereas flower heads of the second order have c. 17 fruits. Individuals that flower for the first time and with one inflorescence can produce 100-150 fruits. Older, richly branched individuals with many inflorescences can produce c. 750 fruits, and rarely up to 4500 fruits (Burmester 2010). The fruit is a schizocarp consisting of two mericarps containing one seed each. Wings are absent or weakly developed, but the fruit has hooked bristles (Fig. 4e) (Stace 2010; Liu, van Wyk & Tilney 2003). In contrast to other species of the Apiaceae, carpophores are missing, and the mericarps are often dispersed together (Chater 1968; Wołk 1973; Halvorson 1982; Curle, Stabbetorp & Nordal 2007). As in other species of the subfamily Saniculoideae, the mesocarp contains scattered druse crystals of calcium oxalate, distuingishing E. maritimum from species of the Apioideae (Magee et al. 2010). The average individual mass seed (air-dry) is 17.5 mg (Royal Botanic Gardens Kew 2008) but dterminations vary between 11.5 mg and 14.4 mg (Fitter & Peat 1994; Hitchmough, Kendle & Paraskevopoulou 2001) up to 25.8 mg (Barclay & Earle 1974). 26 Seeds of plants growing on shingle risk destruction in such a high-energy environment, or may fall through the large voids in the coarsely textured substrate to a depth where germination or emergence will fail (Davy, Willis & Beerling 2001). Hence, shingle species tend to have significantly heavier seeds than phylogenetically related, non-shingle species (Salisbury 1974; Davy, Willis & Beerling 2001). The seed mass of Eryngium maritimum (12.9 mg) was found to be similar to Honckenya peploides (12.8 mg), but lower than the associated species Crambe maritima (146.0 mg) and Lathyrus japonicus ssp. maritimus (36.1 mg) (Davy, Willis & Beerling 2001). Dispersal The dispersal ecology of Eryngium maritimum has not been studied in detail. One main means of dispersal is by wind (Eberle 1979; Avižienė, Pakalnis & Senzikaite 2008). This requires the fruits to stay attached for a relatively long time on the flower head (Hegi 1975). At the end of the growing period the stems become brittle and break off easily (Curle, Stabbetorp & Nordal 2007). The dry plants as a whole may roll along the beach and other open areas, as a ‘tumbleweed’ (Curle, Stabbetorp & Nordal 2007), similarly to Cakile maritima. Seed dispersal may take place by sea (‘thalassochory’; Rappé 1996; 1997), and so it seems possible that long-distance dispersal occurs along the coast or between islands. Bouyancy of the fruits of E. maritimum in seawater is aided by their hooked bristles, soft inner wall with oil-bodies (Stace 2010) and long dry persistent sepals (Fig. 4e; Calviño, Martínez & Downie 2008). The ability to float lasts up to 14 days (Curle, Stabbetorp & Nordal 2007), with the mean floating period being between 2 and 4 days (Praeger 1913; Ridley 1930). Cold-treated fruits sank earlier than fruits without cold treatment (Curle, Stabbetorp & Nordal 2007). The generally poor buoyancy meants that long-distance dispersal in the sea is more limited than would be expected from its distribution range; the fragmented distribution of the species suggests that short-distance dispersal dominates, and that long-distance dispersal is probably unusual (Curle, Stabbetorp & Nordal 2007). Nevertheless, the geographic distribution of genetic lines indicates that, sea dispersal is the major means of long distance dispersal (Weising & Freitag 2007). The ability to float also enables Eryngium maritimum to colonize strandlines (Rappé 1996; 1997), together with similar sea-dispersed species such as Cakile maritima, Calystegia soldanella, Elytrigia juncea, Euphorbia paralias, E. peplis, Medicago marina, Achillea maritima, Pancratium maritimum and Salsola kali (García-Mora, Gallego-Fernández & García-Novo 1999). Such species tolerate exposure to seawater well. When 20 seeds of each species were experimentally floated in sea water for 40 days, the following germinated: Pancratium maritimum (14), Cakile maritima (13), Salsola kali (12), and Eryngium maritimum (10) (Praeger 1913; Ridley 1930). Epizoochorous dispersal by small animals such as mice and birds such as Carduelis carduelis L. (Goldfinch) seems 27 possible, because of the spiny attachments of the fruit (Lübbe 1909; Ridley 1930; Eberle 1979; Halvorsen 1982), but it has not been reported. (D) VIABILITY OF SEEDS: GERMINATION The percentage of infertile seeds varies from year to year from 11 to 34% (Walmsley & Davy 1997a) and is sometimes up to 60% (Avižienė, Pakalnis & Senzikaite 2008). Seed germination success is low in comparison to other coastal plant species e.g. Crambe maritima, Glaucium flavum, Lathyrus japonicus ssp. maritimus, and Rumex crispus and under field conditions achieves c. 5% (Walmsley & Davy 1997a; Walmsley 2004) or 11% (Jankevičienė 1978). The low germination rate is probably caused by the sclerenchymatous fruit wall not becoming moist enough for germination in dry sand (Frisendahl 1926; Curle, Stabbetorp & Nordal 2007). Cold stratification (8 weeks at 5-6 °C or 6 weeks at 2 °C) softens the pericarp and testa (Walmsley & Davy 1997a) and raises germination rates to c. 25% under a diurnal day/night temperature regime of 25/15 °C (Walmsley & Davy 1997a; Kļaviņa, Gailīte & Ievinsh 2006). Germination can be as high as 50% after warm stratification (2 weeks at 24 °C, and removal of the seeds from the seed coat) and following cold stratification (8 weeks at 5 °C) (Kļaviņa, Gailīte & Ievinsh 2006). Walmsley & Davy (1997a) found that further cold stratification up to 14 weeks resulted in a decline of the germination rate but Necajeva & Ievinsh (2013) reported an increasing rate up to 16 weeks. Like other shingle and sand-dune species such as Crambe maritima, Glaucium flavum, Honckenya peploides, Lathyrus japonicus ssp. maritimus and Rumex crispus, Eryngium maritimum germinates readily in diurnally alternating temperature regimes (Walmsley & Davy 1997a). For example, the germination rate of cold-stratified (8 weeks at 6 ºC) seeds of E. maritimum increased from 56% to 83% due to the change from a constant temperature (16 °C) to a diurnal temperature regime (23/9 °C) (Royal Botanic Gardens Kew 2008). The optimal germination of E. maritimum is in a diurnal temperature regime of 20/10 °C, which in Britain corresponds with temperatures during May and June (Walmsley & Davy 1997 a, b). This probably represents a limitation for its northern distribution (Curle, Stabbetorp & Nordal 2007). Eryngium maritimum, like other shingle and sand dune species, has innate seed dormancy and germinated in good numbers only in a relatively narrow temperature range of 15-23 °C (Walmsley & Davy 1997a), whereas Glaucium flavum and Lathyrus japonicus ssp. maritimus germinated well over a wider temperature range (9-30 °C) (Walmsley 1995). Germination rate was similar across a range of different substrates (Hitchmough, Kendle & Paraskevopoulou 2001). Increasing salinity reduced germination (Woodell 1985) and inhibited it at about 300 mM NaCl, as a result of osmotic effects limiting imbibition or toxic effects of absorption of ions such as Cl- (Walmsley & Davy 1997a). However, E. maritimum fruits can resist seawater 28 for long periods, and 55% - 73% of seeds kept in seawater for 36-40 days remained viable (Preuß 1911; Ridley 1930; Calviño, Martínez & Downie 2008). Seeds collected from the ground on 10 October 2009 on the island of Spiekeroog, Germany, were stored in moist conditions at 4 °C in a fridge. Four months later they were sown in sand collected from the field site and left in a greenhouse at c. 20 °C. Four weeks later on 9 March the first four seedlings sprouted, and five weeks later on eight additional seedlings sprouted; the last once germinated six weeks after sowing. These results are similar to other studies which found the first germination 18-28 days after sowing (Hitchmough, Kendle & Paraskevopoulou 2001; Kļaviņa, Gailīte & Ievinsh 2006; Curle, Stabbetorp & Nordal 2007), a peak at 131 days, and final emergence after 146 days (Hitchmough, Kendle & Paraskevopoulou 2001). The 19 weeks between the first and last germination represents the whole summer season in the field and probably represents a tradeoff between the risk of germinating too early and the loss of fecundity by starting too late in an unpredictable environment (Curle, Stabbetorp & Nordal 2007). Dry and cold conditions, especially in combination with deep sand burial during the first year, reduce seedling survival (Weeda 1987). However, moderate sand burial supports the establishment of seedlings (Bengtsson, Appelqvist & Lindholm 2009). In pot and laboratory experiments, seedling survival rates during the first 4 months are high, up to 100% of germinated seeds (Hitchmough, Kendle & Paraskevopoulou 2001; Kļaviņa, Gailīte & Ievinsh 2006). Eryngium maritimum maintains a persistent seed bank for at least three years, where 36% germinate in the first year, 11% in the second and 1.5% in the third year (Burmester 2010). Seed storage at a low temperature (5 °C) in the dark and at constant low humidity for 7 years did not break dormancy, but the percentage of viable seeds (TTC test) declined with storage time from about 80% after one year to only 20% after seven years (Walmsley & Davy 1997a; Walmsley 2002). (E) SEEDLING MORPHOLOGY Eryngium maritimum has epigeal germination (Erikson 1896). In experiments, seedling development was variable, probably in response to temperature. The cotyledons developed after 1 3 months (Fig. 6 a, b), the primary foliage leaf (Fig. 6 c) at 1.5 - 4 months, the second leaf (Fig. 6 d) at 2 - 5 months, and the third/fourth (6th) basal leaves within 4 - 7 months. During the first year, the seedling usually develops 3-4, rarely 5-6, leaves (Burmester 2010). The first internodes are close together, and the leaves are small (Erikson 1896). The primary foliage leaf has the typical dentate edge. The primary root thickens some weeks after germination to develop a rootstock for storing assimilated substances. Seedlings germinating in autumn probably show a higher mortality, in 29 contrast to adult plants with a well-developed rootstock (Pütz & Sukkau 2002), because of poor development of the primary root (Burmester 2010). IX. Herbivory and disease (A) ANIMAL FEEDERS OR PARASITES Invertebrates A small number of phytophagous insects is associated with Eryngium maritimum (Table 5). Only the micro-moth Agonopterix cnicella and the noctuid moth Agrotis ripae appear to be specific to E. maritimum. Caterpillars of the butterfly Papilio machaon have been reported as herbivores on the leaves in Sweden; however, in laboratory experiments, there was no oviposition and larvae did not feed on the leaves (Wiklund 1975). The essential oils in E. maritimum might confer some protection against invertebrates (Hicks 1895), particularly as agromyzids are absent. The exploitation by a microlepidopteran shows that chemical barriers are not entirely effective (Lawton & Price 1979). Similarly, the larvae of Papilio machaon feed on E. maritimum even though it contains the linear furanocoumarin xanthotoxin, which is toxic to generalist lepidopterous larvae (Crowden, Harborne & Heywood 1969; Berenbaum 1981). Phyto-ecdysteroids, presumed to be the cause of avoidance by invertebrate predators, occur in the seeds as well as in the leaves of Eryngium maritimum, and reach high concentrations, above 1 mg ecdysone equivalents g-1 in roots (Dinan, Savchenko & Whiting 2001). Although the spiny leaves are seen as defences agianst caterpillars and snails (Hegi 1975), in Portugal the snail Theba pisana was found on E. maritimum and on other dune species (Clarke & Beaumont 1992). Vertebrates Birds such as the Goldfinch Carduelis carduelis L. eat the seeds of Eryngium maritimum (Lübbe 1909). Some species of small rodents may also eat the seeds (Maike Isermann pers. obs.). The rootstocks, which are rich in carbohydrates, are also eaten by larger animals, for example by wild boars (Ursus arctos L.) in Lithuania (Avižienė, Pakalnis & Senzikaite 2008). (B) PLANT PARASITES Ascomycota Ascomycete fungi, such as Mycosphaerella eryngii (Fr. ex Duby) Johanson ex Oudem (Capnodiales), are probably more closely associated with Eryngium maritimum than the basidiomycetes. Pleospora herbarum (Pers.) Rabenh. (Pleosporales) fruits on E. maritimum leaves of the previous year (Stoykov & Assyov 2008; Jörg Albers pers. comm.). Another plurivorous 30 fungus, Diaporthopsis angelicae (Berk.) Wehm. (Diaporthales), is recorded from damaged plants of E. maritimum (Ellis & Ellis 1997). Many other fungi are host non-specific and occur on various dead or damaged plants species including E. maritimum (British Mycological Society 2012). Basidiomycota Entyloma eryngii (Corda) de Bary (Entylomatales) is associated with Eryngium maritimum, but is rare and mainly found in September (Ellis & Ellis 1997). Pleurotus eryngii (DC.) Quél. (Agaricales), an edible oyster mushroom, is associated with a wide range of genera of Apiaceae (Bresinsky et al. 1987). Pleurotus eryngii var. eryngii is associated with E. campestre (Hilber 1982) in Central Europe and, although not recorded on E. maritimum in the wild, it is grown on it experimentally (Lutz 1925; Hilber 1982; Bengtsson, Appelqvist & Lindholm 2009; Jörg Albers pers. comm.). Vascular plants Orobanche minor ssp. minor is parasitic on the roots of Eryngium maritimum in Britain and Ireland (Rumsey 1991; Hipkin 1992; O’Mahony 1992; Jackson 1995; Anderson 1997; Rumsey 2007), where it has a predominantly southern-eastern distribution that extends discontinuously west and north-west (Hipkin 1992). Despite its wide host range in coastal areas, it occurs nearly exclusively on E. maritimum in Ammophila arenaria communities on mobile dunes (Hipkin 1992). On Menorca, O. iammonensis similarly parasitizes E. maritimum (Pujadas-Salvà & Fraga I Arguimbau 2008). (C) PLANT DISEASES No diseases on Eryngium maritimum are known. X. History Records in the British Isles In the British Isles Eryngium maritimum was recorded first by W. Turner in The names of herbs (1548), where he noted that “Eryngium is named in englishe sea Hulver or sea Holly, it groweth plentuously in Englande by the sea syde” (Britten et al. 1965). Walcott (1861) describes many historical locations. It disappeared from many sites in north east England and eastern Scotland before 1930 and declined further up to 1986, with a change index score of -0.8 (Preston, Pearman & Dines 2002). Taxonomy Eryngium L. comprises about 250 species worldwide (Wörz 2005). Most occur in Central and South America, with 25-26 species in Europe (Stasiak 1986; Wörz 1999; 2004; Küpeli et al. 2006; 31 Muckensturm et al. 2010); the genus is absent from southern and tropical Africa (Heywood 1971). Taxonomic relationships within the genus Eryngium were studied by Jarvis et al. (1993) and Wörz (2004, 2005). Eryngium maritimum was described by Linnaeus in Species Plantarum I: 233 (1753). The name Eryngium derives from the Greek, probably based on Theophrastus (300 BC) who described it as a spiny plant, ‘Eryngion’ (Blindow 2006), or the name may have developed from the Greek ‘eruggarein’ meaning to eructate (belch), because the plant was used against various disorders (Huxley & Taylor 1989). Paleobotany Most pollen diagrams distinguish Apiaceae pollen, but records explicitly for Eryngium maritimum are not available even though the pollen is a distinctive morphotype together with E. alpinum (Beug 2004). Eryngium-type pollen is mentioned for Crete (Greece) (Bottema & Sarpaki 2003). The palaeobotanical study of ancient Carthage found Eryngium-type pollen that is possibly E. maritimum. This dates back to the Roman and Byzantine periods (Van Zeist, Bottema & Van der Veen 2001). Phylogeography Genetic and geographic distances along European coasts are well correlated, reflecting the fact that dispersal is mainly along the coast (Westberg 2005). Along the Latvian Baltic coast, there was no such correlation, suggesting little differentiation between populations at this smaller scale (Ievina et al. 2007). On the 150 km coastline of the Gulf of Gdańsk, genetic diversity is very low and genetic distance is related to the direction of sea currents influenced by the western winds (Minasiewicz et al. 2011). Taking the Baltic Coast from Poland to Finland, including the Swedish Islands Gotland and Öland, on the margin of the distribution range in Northern Europe the genetic diversity between and within populations is very low (Ievina et al. 2010). In Europe, the geographical clusters are more or less related to marine basins (Westberg 2005). There are two main geographical groups: an Atlantic and a Mediterranean one. Populations along the Atlantic, the North Sea and the Baltic Sea form a distinct group, which can divided into three subgroups: a southern Atlantic one from La Coruna to Cadiz, Spain; a W. Atlantic one around the Bay of Biscay and one from Brittany northwards to the Baltic Sea including the British Isles. The Mediterranean group is also divided into three subgroups: populations of the western Mediterranean Sea, from the strait of Gibraltar to the Adriatic Sea and to the Ionian Sea; the Aegean Sea; and the Black Sea. The genetic variation in the Atlantic group is slightly lower than in the Mediterranean group, and the correlation between genetic and geographic distance are marginally better in the Mediterranean cluster. The low genetic variation of the Atlantic group was caused by bottleneck events and founder effects during the colonisation history. Climatic changes during glaciations have played a 32 major role in determining the present patterns of genetic variation of E. maritimum. During recent glaciations (115,000-10,000 years ago), the southern limit of permafrost nearly reached Spain at the Atlantic Coast, and E. maritimum would have retracted from its present-day northern distribution area (Clausing, Vickers & Kadereit 2000). If E. maritimum disappeared during glaciation from the Atlantic coast, the post-glacial re-colonisation from the Mediterranean refuge to northern Europe eventually occurred, stepwise, with a linear dispersal along the Atlantic coast. Thus a linear distribution modal could explain lower genetic diversity in Atlantic populations compared to Mediterranean populations, and the strong genetic differentiation between them probably reflects past geographical separation, even though the populations are now spatially continuous and probably connected by gene exchange (Clausing, Vickers & Kadereit 2000). The colder climate in the north western Mediterranean during glaciations did not result in extinction, but probably in a geographical isolation of Eryngium maritimum populations. Recent phylogenetic relations in the continuous Mediterranean distribution area are explained by the preferential seed and fruit dispersal by seawater in combination with present-day sea currents. This applies particularly to the Gibraltar gap, but also to differentiation between Adriatic and Aegean/Black Sea distributions (Clausing, Vickers & Kadereit 2000; Kadereit et al. 2005; Westberg 2005; Kadereit & Westberg 2007; Weising & Freitag 2007; Westberg & Kadereit 2009). Human culture Eryngium maritimum is often represented in paintings and other art e.g. scientific paintings in the Libri picturati collection (Vol. 27/folio 51, water-coloured) made in the Netherlands and stored in the Biblioteka Jagiellońska, Uniwersytet Jagielloński, Kraków, Poland. These paintings are from the second half of the 16th century and the beginnings of the 17th century and were annotated by the famous Flemish botanists like Charles de l’Écluse (Carolus Clusius) (1526–1609) (Zemanek & Zemanek 2006; Zemanek, Ubrzizsy Savoia & Zemanek 2007). Recent examples include works by the Irish artist Patrick O’Hara, the print on postage stamps such as the 1967 Belgian one franc stamp (Robyns 1976), and the 1969 twenty five pfennig stamp in the former German Democratic Republic. Eryngium maritimum is mentioned in plays and poems, notably the ‘The Merry Wives of Windsor’ by Shakespeare (Bloom 1903), and in the ‘Italian Journey’ by Goethe (Albrecht & Scheurmann 1997). Eryngium maritimum has been grown in gardens since medieval times, e.g. the gardens of the Westminster Abbey (Harvey 1992), in private gardens since at least 1525 (Harvey & Jones 1972; Harvey 1989), and in botanical gardens, since c. 1683 in the Physic Garden of Edinburgh (Robertson 2001). It is still used in gardens in the UK (Hamilton, Hart & Simmons 2000). 33 In Europe, the roots, young shoots and leaves of Eryngium maritimum were eaten particularly during the 17th and 18th centuries (Holland 1919; Facciola 1998; Pistrick 2002; Chatterjee 2005; Blindow 2006; Allen 2007), but they are still in use occasionally in Mediterranean regions (Della 2000). Eryngium maritimum has had numerous medical uses, especially during the medieval period. The roots in particular, but also the stems and leaves were used as an anti-toxin against various infections and diseases of humans as well as animals (Salisbury 1816; Woodward 1931; Liscani et al. 1984; Mathias 1994; Vonarburg 2001; Anderson 2004; Chatterjee 2005; Le Claire et al. 2005; Azaizeh et al. 2006; Meot-Duros, Le Floch & Magné 2008:258; Popov 2008; Watson & Preedy 2008). Furthermore, it was used in the Mediterranean against snake and scorpion bites (Sezik et al. 1997; Töngel & Ayan 2005; Küpeli et al. 2006; Çelik, Aydınlık & Arslan 2011). The medicinal use is based on saponins, essential oils, cumarins, flavonoids and organic acids present in the root (Vonarburg 2001). Dried roots for medicinal use are known as ‘Radix Eryngii maritimi’ (Hegi 1975). XI. Conservation In many coastal regions Eryngium maritimum is one of the rarest and most threatened plant species, and is therefore listed in Red Data Books (e.g. in Lithuania, Estonia, Norway, Israel, along the Russian Black Sea; Balevičius 1992; Paal 1998; Fremstad & Moen 2001; Sapir, Shmida & Fragman 2003; Seregin & Suslova 2007). However, in Britain it is assessed as not threatened (Leach & Rusbridge 2006) and its status is ‘least concern’ (Cheffings, Farrell & Dines 2005). Since the beginning of the 20th century Eryngium maritimum has been threatened with local extinctions in Europe (Krause 1906; Preuss 1911; Stasiak 1986) and it has been protected by law (Preuß 1906; Ćwikliński 1979; Avižienė, Pakalnis & Senzikaite 2008). In Germany (Bundesartenschutzverordnung 2005) and The Netherlands collection has been prohibited since 1973. However, it is not included in the EU Habitats and Species Directive (Council Directive 1992). In Europe there has been a drastic decline in the number of populations (Halvorsen 1982) as well as in the number of individuals (Balevičienė, Lazdauskaite & Rasomavicius 1995; Ėringis & Pancekauskienė 1995; Olsson & Tyler 2001; Żółkoś et al. 2007). Herbarium specimens provide evidence of the loss of many populations in Europe (Barriocanal & Blanché 2002; Skarpaas & Stabbetorp 2003). Various inventories document the decline, for example in Poland (Ćwikliński 1979; Piotrowska 2002; Łabuz 2007; Żółkoś et al. 2007), at the Curonian Spit (Olšauskas 1996; Olšauskas & Olšauskaite Urboniene 1999; Olšauskas & Urbonienė 2008), along the German Baltic coast (Burmester 2007), in Sweden (Bengtsson, Appelqvist & Lindholm 2009; Fröberg 2010), and in Norway (Halvorsen 1982; Pedersen 2002). 34 Threats Eryngium maritimum is threatened in several ways by human impacts. Collection for home decoration was, and still seems to be significant in some locations (Liebe 1880; Abromeit, Neuhoff & Steffen 1898; Preuß 1906; Stichting Duinbehoud 1983; Ćwikliński 1979; Weeda 1987; Moeslund 1994; Skarpaas & Stabbetorp 2003; Curle, Stabbetorp & Nordal 2007; Avižienė, Pakalnis & Senzikaite 2008). Habitat loss, disturbance, fragmentation and decline in habitat quality are the main threats to Eryngium maritimum. Coastal beaches, shingle and dunes can be destroyed by seaside tourism, recreational use, construction activities, waste disposal, agriculture, river dams, uncontrolled sand and gravel exploitation, beach management, afforestation, coastal erosion especially as a consequence of sea level rise, and coastal protection measures (Ćwikliński 1979; Piotrowska & Stasiak 1984; Piotrowska 1995; 2002; Urbanski 2001; Kull et al. 2002; Buskovic et al. 2004; Spanou et al. 2006; Łabuz 2004; 2007; Burmester 2007; Żółkoś et al. 2007; Avižienė, Pakalnis & Senzikaite 2008; Erginal et al. 2008; Speybroeck et al. 2008; O’Sullivan 2010; Rovira Rojas & Romagosa Casals 2010). Tourism and the growth of tourist infrastructure cause habitat loss for Eryngium maritimum (Goldsmith, Munton & Warren 1970; Łabuz 2007; Rovira Rojas & Romagosa Casals 2010). These changes often lead to increased trampling and other mechanical damage that threatens the plant (Eberle 1979; Olšauskas 1996; Olšauskas & Olšauskaite Urboniene 1999). Land-use changes are important. Stabilisation of dunes promotes older successional stages, for instance dense grasslands with Carex arenaria and shrublands with Hippophaë rhamnoides in which E. maritimum is outcompeted (Van der Laan 1985). Invasive species, such as Rosa rugosa (Fig. 3c) in north west Europe (Burmester 2007), Amorpha fruticosa along the Black Sea coast, Pinus spp. in various regions and Acacia longifolia on the Mediteranean coast have similar adverse impacts upon species of early successional stages. Woodland and forestry plantations, intended to stabilise dunes for coastal protection purposes have similar effects (Ćwikliński 1979; Piotrowska & Stasiak 1984; Stasiak 1986; Piotrowska 2002; Łabuz 2004; 2007). Eryngium maritimum is further threatened by a decline in livestock grazing (Stephan 2006; Burmester 2007), which supports open dune vegetation, although high densities of grazers such as rabbits Oryctolagus cuniculus L. are counter-productive (Burmester 2007; Bengtsson, Appelqvist & Lindholm 2009). The distribution of Eryngium maritimum will probably be affected by temperature changes related to projected climate change, extending (Metzing 2005), and increasing in frequency, northward (Bengtsson, Appelqvist & Lindholm 2009). However, it has declined in the Scotland and northern England in the last century and, recently, this has been associated with a trend towards higher rainfall since the 1950s (Ranwell 1972; Tutin 1980; Rich & Woodruff 1996; Preston 2007). 35 However, it is difficult to distinguish the cause of the decline, a complex of environmental changes, including combined effects of climate and landuse change as well as habitat loss. Climate change with concomitant rise in realtive sea level is leading to marine erosion in many. This may result in habitat loss for Eryngium maritimum. Moreover artificially reconstructed sea defences rarely allow the establishment of semi-natural dune vegetation it requires (Łabuz 2004; O’Sullivan 2010). The fragmented populations of Eryngium maritimum are threatened by their temporal and spatial variation in their population size (Curle, Stabbetorp & Nordal 2007). On the German Baltic coast, the two largest populations comprise about 80% of the total individuals (Burmester 2007), presenting an increased risk from stochastic disturbances and, probably, reduced fitness, effects that would be more significant at the margins of its range (Bengtsson, Appelqvist & Lindholm 2009; Tsaliki & Diekmann 2009). The level of genetic variation might affect population sustainability (Curle, Stabbetorp & Nordal 2007). Frequent suitable locations are necessary, with at least 50 individuals in the short term and at least 500 in the long term at any single site to ensure population viability. Because the genetic variability of Eryngium maritimum is low, relatively small numbers of individuals would be sufficient for survival at any one location (Bengtsson, Appelqvist & Lindholm 2009). Conservation measures Conservation measures should include protection against mechanical damage and the maintainenance of moderate sand accretion achieved through a naturally dynamic dune system (Bengtsson, Appelqvist & Lindholm 2009) and might embrace stock grazing, provided that this avoids damage by trampling at overly high stock densities (Weeda 1987). Where management damages Eryngium maritimum (Nordstrom 2000), it is advisable to collect seed before management operations for use in re-establishment afterwards, as is practised along parts of the German Baltic coast (Sonja Leipe pers. comm.). The removal of driftline material as a propagule source and nutrient supply for the establishment of new populations of Eryngium maritimum may also affect the maintenance of established populations (Bengtsson, Appelqvist & Lindholm 2009). Restoration measures Regeneration, based on the natural soil seed bank appears not to be a reliable method for reestablishment of Eryngium maritimum (Walmsley 1995; Walmsley & Davy 1997b; 2001). However, in some dune restoration schemes E. maritimum and other typical dune plants are known to establish spontaneously by natural regeneration from neighbouring sites (De Lillis et al. 2004; Escaray et al. 2010; Rozé & Lemauviel 2004; Schreck Reis, Antunes do Carmo & Freitas 2008). The method of sowing seeds in the field appears to be partially effective in re-establishing shingle and dune species. Eryngium maritimum germinated at Sizewell, Suffolk, UK between April 36 and June, after over wintering allowed natural stratification. Nevertheless, total seedling emergence and survival was low, probably because of drought and high temperature stress during the summer, and salt-spray effects and tidal inundation during winter (Walmsley & Davy 1997b; 2001). Planting of container-grown plants seems to be the most successful restoration method for Eryngium maritimum. Plantings of E. maritimum on a sandy shingle beach in Sizewell, Suffolk, Britain during April/May, have shown that planting location on the beach/dune profile is the most important factor that affected establishment; neither organic matter nor fertiliser had significant effects (Walmsley & Davy 1997c; 2001; Walmsley 2004). Eryngium maritimum has also been reestablished from dunes by plantings in Spain (Sanjaume & Pardo 1991; Escaray et al. 2010; Ley Vega de Seoane 2010). Young plants can be grown from root fragments (about 6 cm long) from the main root, as well as from offshoots from nursery plants. Root fragments buried horizontally in sandy soil during the winter, to a depth of 4-40 cm developed a root systems and leaves in a few months (Ley Vega de Seoane 2010, and pers. comm.). Nevertheless, there are documented unsuccessful transplantation efforts to re-establish E. maritimum in dunes restored from cultivation e.g. at Shingle Street, Suffolk, UK (Heath 1981). For the restoration of shingle vegetation in general, and Eryngium maritimum in particular, a well mixed shingle matrix with a good sand content, an available water source, and an area large enough to establish stable populations are important (Scott 1963; Fuller 1987; Walmsley & Davy 2001; Smith 2009). As E. maritimum is one of the more specialist species, occurring in a relatively narrow niche, habitat protection and management are important (Jukonienė & Stankevičiūtė 2005; Speybroeck et al. 2008). Therefore, beach, shingle and dune management must maintain, conserve and restore the natural values of habitats, having a full appreciation of the importance of the operation of natural processes to long term viability (Van der Meulen & Salman 1996). Acknowledgements The authors wish to record their thanks to Tony Davy for his great support, feedback and patience in the preparation of this paper. For extensive comments on an earlier manuscript, we thank particularly Chris Preston and Michael Proctor. We would also like to express our sincere gratitude to Barbara Thiem and Małgorzata Kikowska (K. Marcinkowski University of Medical Sciences in Poznań, Department of Pharmaceutical Botany and Plant Biotechnology) for rewriting the biochemical section of this paper. We thank Colin Harrower (Britain and Ireland) and Erik Welk (Europe) for preparation of the distribution maps. 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Indicator values for Eryngium maritimum for light (L), temperature (T), continentality (K), moisture (F), soil pH (R), nitrogen (N) and salinity (S) in different parts of its range. UK (range 1-9, except F 1-12; Hill et al. 1999); N.W. Europe (range 1-9, except F 1-12; Ellenberg et al. 1991). Indicator values for the eastern parts of its distribution are missing (Ramensky et al. 1956). Values of The Netherlands (Bakkenes et al. 2002) are recalibrated on the basis of the Dutch vegetation database, giving mean, minimum and maximum values. Values for Greece (Böhling 1995) range 14 or 5 Indicator UK L - light 9 T - temperature 6 K - continentality 3 F - moisture 4 R - soil pH 6 N - nitrogen 5 S - salinity 3+ 9 6 3 4 7 4 N.W. Europe Netherlands full light moderate to warm oceanic to suboceanic dry to moderate fresh 4.52 (3.00-6.48) slightly acid to basic 6.44 (4.00-7.50) poor to moderate 4.54 (2.50-7.20) ? Greece 4 extreme warm 2 very dry habitats 5 calcifuge 3 facultative halophyte Table 2. Biogeographical species-groups distinguished by TWINSPAN classification of species frequency (%) in 8 biogeographic regions. It includes Black Sea S Eur. Atlantic and Mediter. Sea NW Eur. Atlantic and North Sea N North Sea and Baltic Sea NE Black Sea SW Black Sea NE and central N Medit S Eur. Atlantic, NW and S Medit. Sea NW Atlantic-S North Sea, SW Baltic North Sea NE and central S Baltic Sea N North Sea and NW Baltic Sea Twinspan step Number of relevés Eryngium maritimum Black Sea, Mediterranean Sea, S.W. Atlantic Polygonum maritimum Salsola kali Euphorbia peplis Xanthium strumarium Cakile maritima Elytrigia juncea Euphorbia paralias Medicago marina L. Pancratium maritimum Echinophora spinosa L. Sporobolus pungens (Schreb.) Kunth Achillea maritima Ammophila arenaria (L.) Link ssp. arundinacea H.Lindb. Cyperus capitatus Vand. Crucianella maritima L. Black Sea Crambe maritima NW Atlantic, North Sea, Baltic Sea Biogeographic region Black Sea, Medit. Sea, SW Atlantic 3605 relevés from Europe and adjacent countries. Names of syntaxa follow Mucina (1997). Sources are given in Appendix S1 1 2250 100 2 1355 100 1,1 240 100 1,2 2010 100 2,1 1219 100 2,2 136 100 1,11 155 100 1,12 85 100 1,21 1496 100 1,22 514 100 2,11 953 100 2,12 266 100 2,21 132 100 2,22 4 100 13 23 11 18 31 62 32 36 31 28 27 23 1 9 1 0 14 33 14 1 1 1 1 2 13 30 12 36 28 11 4 3 2 . . 1 13 22 11 16 32 68 36 39 34 31 30 25 1 9 1 . 15 37 16 2 1 1 1 3 . 4 . 3 5 2 . . . . . . 6 28 10 35 36 6 4 3 1 . . 2 26 32 16 39 13 21 5 5 2 . . . 12 25 13 20 35 69 32 42 34 36 35 26 15 11 4 2 23 64 46 33 35 15 17 24 1 10 1 . 18 31 13 2 1 1 1 2 . 5 0 . 5 58 25 . . . . 6 . 4 . 3 5 2 . . . . . . . . . . . . . . . . . . 22 21 10 . 0 0 . 1 . 24 23 11 . 0 0 . . . . . . . 2 . 21 27 5 35 11 26 . 0 0 . . . . . . . . . 4 3 41 0 3 1 46 32 . 0 4 0 . 25 63 Lactuca tatarica 4 Euphorbia seguieriana Neck. 2 Linaria dalmatica 2 Alyssum hirsutum M.Bieb. 1 Cynanchum acutum L. 2 Artemisia tschernieviana Besser 3 Gypsophila perfoliata L. 2 Melilotus albus 3 Artemisia santonicum L. 2 Carex ligerica J.Gay 1 Phragmites australis 4 Seseli tortuosum L. 4 Elymus elongatus (Host) Runemark 2 Centaurea arenaria M.Bieb. ex Willd. 3 Medicago sativa 2 Secale sylvestre Host 1 Silene thymifolia Sm. 2 Chondrilla juncea L. 2 N.E. Black Sea Glycyrrhiza glabra L. 1 Bromus squarrosus 1 Astrodaucus littoralis (M.Bieb.) Drude 1 Galium humifusum M.Bieb. 1 Polygonum arenarium 1 Salsola soda L. 1 Argusia sibirica (L.) Dandy 1 Suaeda maritima 1 Cynodon dactylon 7 S.W. Black Sea Silene conica 1 S. European Atlantic and Mediterranean Sea Calystegia soldanella 27 Lotus cytisoides L. 8 Cutandia maritima (L.) Barbey 8 S. European Atlantic, N.W. and S. Mediterranean Sea Lotus creticus L. 6 Malcolmia littorea (L.) R.Br. 3 3 . 0 . . . . 1 . 0 2 . . . 1 . . 2 38 19 16 12 11 25 18 17 14 13 11 10 10 30 19 13 11 10 0 . 0 . 1 . . 1 . . 3 3 2 . 0 0 0 1 3 . . . . . . 1 . . 2 . . . 1 . . 3 . . 2 . . . . . . 1 . . . . . . . . 34 15 7 14 10 38 27 21 22 16 15 16 14 15 5 6 . 5 44 26 33 8 12 2 2 9 . 7 4 . 1 59 44 26 31 18 0 . 0 . 1 . . 2 . . 3 3 2 . 0 0 1 2 . . . . 0 . . . . . 1 3 . . . . . 1 4 . . . . . . 1 . . 3 . . . 1 . . 3 . . . . . . . 1 . . . . . . . . . . . . 2 . . . . . . 1 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0 . 1 3 9 9 9 8 8 8 8 7 6 1 0 . . 0 0 0 0 8 . . . . . 0 . 1 3 . . . . . . . . . 14 14 14 13 12 12 12 10 10 . . . . . . . . . 1 0 . . 0 1 0 1 9 . . . . . . . 0 2 . . . . . 0 . 1 4 . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 6 0 2 . 2 13 0 . 3 . . . 18 . . . . . 30 10 9 21 . . . . . . . . . . . 26 9 10 43 10 9 19 . . 27 . . . . . . . . . . . . 7 4 . . . . . . . . 3 0 17 13 . . . . . . . . 64 Aetheorhiza bulbosa Helichrysum stoechas (L.) Moench N.W. Atlantic, North Sea, Baltic Sea Ammophila arenaria Festuca rubra Carex arenaria Honckenya peploides Leymus arenarius X Calammophila baltica Galium album N.W. European Atlantic and North Sea Hypochaeris radicata Sedum acre Taraxacum sect. Ruderalia Lotus corniculatus Sonchus arvensis Galium verum Cerastium semidecandrum Leontodon saxatilis Phleum arenarium Plantago lanceolata Hippophae rhamnoides Poa pratensis Ononis repens Senecio jacobaea L. S North Sea Cerastium diffusum Tripleurospermum maritimum North Sea and Baltic Sea Hieracium umbellatum Corynephorus canescens Jasione montana Viola tricolor Artemisia campestris Lathyrus japonicus ssp. maritimus Festuca polesica Zapall. Linaria odora (M.Bieb.) Fisch. 5 4 . 2 . . 6 4 . 2 . . . . . . 4 2 12 12 . 2 . . . . . . 17 . 1 1 0 . . 67 63 43 29 24 10 10 16 . . . 3 . . 17 . 1 1 . . . 68 63 44 29 24 10 10 60 57 32 25 23 15 8 . . . . . . . 45 . . . 9 . . 17 . . . . . . 16 . 5 6 . . . 69 65 46 26 29 12 13 65 56 36 42 5 0 2 60 56 31 25 20 16 8 50 100 75 25 100 . . 3 0 . 1 0 . 0 1 1 1 0 . . . 25 25 19 18 16 16 16 15 14 14 12 11 9 10 . . . . 1 . 0 . . . . . . . 3 0 . 1 . . . 2 2 1 0 . . . 28 27 21 20 18 18 17 16 16 15 13 12 10 11 1 7 2 1 1 3 2 2 . . 3 3 . . . . . . . . 1 . . . . . . . . . . . 2 . . . . . . . . . 4 0 . 1 . . . . 2 1 0 . . . 1 0 . . . . . 6 . 0 . . . . 24 30 20 14 21 16 20 16 18 13 16 11 9 8 42 14 27 39 6 25 8 17 9 25 1 18 12 23 2 5 2 . . 2 2 2 . . 3 2 . . . 50 25 25 50 50 . . . . . 50 . . 0 0 8 7 . . 0 0 8 8 . . . . . . . . 1 1 6 6 16 12 . . . . . 1 0 . 4 . . 0 31 20 16 12 12 7 3 2 . . . . 3 . . . . 1 0 . 4 . . 0 26 18 14 10 6 5 0 . 78 40 32 26 59 28 23 18 . . . . 1 . . . . . . . 6 . . . . . 0 . 1 . . 0 . 4 0 . 11 . . . 34 22 17 12 8 6 1 . . 2 2 4 . 1 . . 80 42 33 27 61 27 23 19 25 . . . . 50 . . 65 Helichrysum arenarium (L.) Moench Calamagrostis epigejos N.E. and central S. Baltic Sea Thymus serpyllum Festuca lemanii Salix daphnoides Tragopogon floccosus Waldst. & Kit. N. North Sea and N.W. Baltic Sea Potentilla anserina Elytrigia repens Atriplex prostrata Arrhenatherum elatius Plantago maritima Linaria vulgaris Atriplex littoralis Sedum telephium Vicia cracca . 1 3 4 . 7 . . 2 3 18 13 . 6 . 8 . . . . 2 3 . . 18 13 . . . . . . 3 1 1 1 . . . . . . . . 2 . . . 9 9 9 9 . . . . . . . . . . . . . . . . 3 . . . . . . . 9 9 9 9 . . . . . 0 1 . 0 0 . . 0 4 7 5 1 2 3 2 1 1 . 2 3 . 3 2 . . . . 0 1 . . . . . 0 4 7 5 1 2 3 2 1 1 2 3 2 1 1 1 1 1 1 . 3 4 . 4 3 . . . . . . . . . . . . . 0 1 . . . . . 0 . . 1 . . . . . . 3 9 6 2 2 4 3 1 1 7 . 2 . 2 . . . . . 2 1 . 1 1 1 . . 75 50 50 50 25 25 25 25 25 Table 3. Comparison of leaf traits of Eryngium maritimum and Pancratium maritimum. The mean and the standard deviation (SD) for 25 plants is shown. From Gratani & Fiorentino (1988) Eryngium maritimum Pancratium maritimum Mean SD Mean SD Leaf area per plant (m²) 0.00463 0.00136 0.00253 0.00019 Dry mass (kg m-2) 0.161 0.060 0.15119 0.06314 Number of leaves per plant 42.0 31.1 48.0 37.2 Height (m) 0.196 0.0927 0.237 0.0682 Leaf area index 2.63 0.87 0.61 0.27 67 Table 4. Timing and duration of flowering season in Eryngium maritimum in different areas of its distribution (based on Frisendahl 1926; Eberle 1979; Chater 1980; Bagella 1985; Gratani, Fiorentino & Fida 1986; Fitter & Peat 1994; Favennec 1998; Olšauskas & Olšauskaite Urboniene 1999; Heukels 2000; Hitchmough, Kendle & Paraskevopoulou 2001; Curle, Stabbetorp & Nordal 2007; Avižienė, Pakalnis & Senzikaite 2008; Korhonen 2011) South Mediterranean coast North-east Mediterranean coast North-west Mediterranean coast South Atlantic coast Southern North Sea, W. Baltic Sea North Atlantic, Irish Sea, Baltic Sea Flowering start April May June June July July Flowering end June August August August August-September August Duration (months) 2 3 3 3 1-2 1 68 Table 5. Invertebrate animals recorded as feeding on Eryngium maritimum Taxon ARTHROPODA, Insecta Hemiptera Aphididae Cavariella aegopodii (Scopoli) Coleoptera Scarabaeidae Polyphylla fullo L. Lepidoptera Oecophoridae Agonopterix cnicella Treitschke Tortricidae Aethes margarotana Duponchel Aethes williana Brahm Noctuidae Agrotis ripae Hübner Papilionidae Papilio machaon L. MOLLUSCA, Gastropoda Helicidae Theba pisana O.F. Müller Ecological notes Plant part Country Oligophagous on Apiaceae; overwinters as eggs on Salix spp. Larvae r) Larvae; monophagous on Eryngium maritimum; causes rolling, webbing and brown discolouration Reference 1 Roots Netherlands Shoots, leaves UK, Netherlands 2 3, 4 Larvae boring, webbing and mining. Causes brown discolouration larvae boring; feeds mainly on Daucus carota Noctuidae Larvae; monophagous Roots, upper Now extinct in stems, flowers UK Shoots, leaves UK 8 Caterpillar Leaves, roots Sweden 9 Leaves, stems? Portugal 10 Roots, lower stems UK 5 6, 7 References: 1, Börner (1952); 2, Huiting et al. (2006); 3, Emmet & Langmaid (2002); 4, Huisman et al. (2013); 5, Davidson et al. (1991); 6, Kimber (2013); 7, Razowski (1970); 8, Waring & Townsend (2003); 9, Wiklund (1975); 10, Clarke & Beaumont (1992). 69 Fig. 1. The distribution of Eryngium maritimum in the British Isles. Each dot represents at least one record in a 10-km square of the National Grid. (●) native 1970 onwards; (o) native pre-1970; (+) non-native 1970 onwards; (x) non-native pre-1970. Mapped by Colin Harrower, Biological Records Centre, Centre for Ecology and Hydrology, mainly from records collected by members of the Botanical Society of the British Isles, using Dr A. Morton’s DMAP software. 70 Fig. 2. The distribution of Eryngium maritimum in Europe and adjacent areas; compiled and mapped by E. Welk (AG Chorology, Departement Geobotany, Institute for Biology, Martin-LutherUniversity Halle Germany). Black dots represent recorded single occurrences; the dark grey line indicates coastal regions as mapped by Weinert in Meusel et al. (1978). 71 Fig. 3. Eryngium maritimum (a) on shingle, Shoreham Beach, West Sussex, UK (Photo: Dee Christensen, 2006), (b) on a yellow-dune with relatively high sand accumulation at the German island of Spiekeroog, (c) and threatened by Rosa rugosa on Spiekeroog (Photos: Maike Isermann, 2009). (d) Taproot of Eryngium maritimum on an eroding dune, Connemara, Galway, Republic of Ireland (Photo: Maike Isermann, 1991). (a) (b) (c) (d) 72 Fig. 4. Morphology of Eryngium maritimum: (a) Habit of an adult plant; details of (b) leaf, (c) shoot, (d) flower with bract, and (e) fruit (Drawings by Roland Spohn). (d) (c) (e) (b) (a) 73 (a) (b) (c) Fig. 5. Scanning EM micrographs of leaf surface structure with epicuticular waxes: (a) lower surface (b, c) upper surface (W. Barthlott). 74 (a) (b) (c) (d) (e) Fig. 6. Germination and developmment of Eryngium maritimum: (a) and (b) 2-cotyledon stage, at 4 weeks; (c) with primary foliage leaf, at 6 weeks; (d) with a small second foliage leaf, at 8 weeks; and (e) with four leaves, at c.12 weeks. Seeds collected from the German island of Spiekeroog, sown on the 9 March 2010 and maintained at c. 16 °C. (Drawings: Roland Spohn).