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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
1Vegetation 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]
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
Sea Holly. Apiaceae subfamily Saniculoideae. A long-lived, perennial herb with a long, well-
developed 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 ovate-
lanceolate, 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 air-
filled 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).
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 in Europe (Graham Prichard, pers. comm.).
II. Habitat
(A) CLIMATIC AND TOPOGRAPHICAL LIMITATIONS
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
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 isn 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.).
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. Where rates of sand accretion are not too high, Eespecially 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 this 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).
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
13
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
communities contain species of classes typical for nutrient rich stands like Artemisietea vulgaris,
Epilobietea angustifolii and Galio-Urticetea; or in spatial associated communities like Festuco-
Brometea, 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
14
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
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
15
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,
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
16
by acid deposition, pollutants and eutrophication (Van der Laan 1985). Where the dune area is
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, Gallego-
Fernández & 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
17
1895; Eberle 1979; Avižienė, Pakalnis & Senzikaite 2008). Moreover, the rootstock may have
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 This is 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 well-
developed 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).
18
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).
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
19
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
1994). Although Eryngium maritimum and Pancratium maritimum co-occur in Mediterranean
semi-fixed 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 quite rarereduced
(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).
20
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
(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).
21
(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
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 polyhydroxy-
triterpenoid 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%), 2,3,4-
trimethyl-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 α-
pinene, 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
22
possess antimicrobial (Meot-Duros, Le Floch & Magné 2008), mainly antimycotic, qualities
(Barbara Thiem pers. comm.).
VII. Phenology
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 above-
ground 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
23
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
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).
24
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.
(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 long-
tongued 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
25
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).
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
26
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
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).
27
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
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 trade-
off 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
28
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
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
29
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
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 rarely found 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
30
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;
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
31
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
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 lalong 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 printed 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.
32
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).,
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 &
33
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). Vvarious 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).
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
34
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).
However, it is difficult to distinguish the cause from inof the decline, a complex of environmental
changes, including combined effects of climate and landuse change and as well as habitat loss.
Climate change with concomitant rise in realtive 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).
35
Restoration measures
Regeneration, based on the natural soil seed bank appears not to be a reliable method for re-
establishment 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
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 re-
established 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
36
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. The large number of other people from many
countries who helped is listed in Appendix S2.
37
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Supporting information
Additional Supporting Information may be found in the online version of this article:
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.
61
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).
Cerain 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 1-4 or 5
Indicator UK N.W. Europe Netherlands GreeceL - light 9 9 full lightT - temperature 6 6 moderate to warm 4 extreme warmK - continentality 3 3 oceanic to suboceanicF - moisture 4 4 dry to moderate fresh 4.52 (3.00-6.48) 2 very dry habitatsR - soil pH 6 7 slightly acid to basic 6.44 (4.00-7.50) 5 calcifugeN - nitrogen 5 4 poor to moderate 4.54 (2.50-7.20)S - salinity 3+ ? 3 facultative halophyte
62
Table 2. Biogeographical species-groups distinguished by TWINSPAN classification of species frequency (%) in 8 biogeographic regions. It includes
3605 relevés from Europe and adjacent countries. Names of syntaxa follow Mucina (1997). Sources are given in Appendix S1
Biogeographic region
Bla
ck S
ea, M
edit.
Sea
, SW
A
tlant
ic
NW
Atla
ntic
, Nor
th S
ea,
Bal
tic S
ea
Bla
ck S
ea
S Eu
r. A
tlant
ic a
nd
Med
iter.
Sea
NW
Eur
. Atla
ntic
and
N
orth
Sea
N N
orth
Sea
and
B
altic
Sea
NE
Bla
ck S
ea
SW B
lack
Sea
NE
and
cent
ral N
Med
it
S Eu
r. A
tlant
ic, N
W a
nd S
M
edit.
Sea
NW
Atla
ntic
-S N
orth
Sea
, SW
Bal
tic
Nor
th S
ea
NE
and
cent
ral S
Bal
tic S
ea
N N
orth
Sea
and
N
W B
altic
Sea
Twinspan step 1 2 1,1 1,2 2,1 2,2 1,11 1,12 1,21 1,22 2,11 2,12 2,21 2,22Number of relevés 2250 1355 240 2010 1219 136 155 85 1496 514 953 266 132 4Eryngium maritimum 100 100 100 100 100 100 100 100 100 100 100 100 100 100Black Sea, Mediterranean Sea, S.W. AtlanticPolygonum maritimum 13 1 13 13 1 . 6 26 12 15 1 . . .Salsola kali 23 9 30 22 9 4 28 32 25 11 10 5 4 .Euphorbia peplis 11 1 12 11 1 . 10 16 13 4 1 0 . .Xanthium strumarium 18 0 36 16 . 3 35 39 20 2 . . 3 .Cakile maritima 31 14 28 32 15 5 36 13 35 23 18 5 5 .Elytrigia juncea 62 33 11 68 37 2 6 21 69 64 31 58 2 .Euphorbia paralias 32 14 4 36 16 . 4 5 32 46 13 25 . .Medicago marina L. 36 1 3 39 2 . 3 5 42 33 2 . . .Pancratium maritimum 31 1 2 34 1 . 1 2 34 35 1 . . .Echinophora spinosa L. 28 1 . 31 1 . . . 36 15 1 . . .Sporobolus pungens (Schreb.) Kunth 27 1 . 30 1 . . . 35 17 1 . . .Achillea maritima 23 2 1 25 3 . 2 . 26 24 2 6 . .Ammophila arenaria (L.) Link ssp. arundinacea H.Lindb. 22 . . 24 . . . . 21 35 . . . .Cyperus capitatus Vand. 21 0 1 23 0 . . 2 27 11 0 . . .Crucianella maritima L. 10 0 . 11 0 . . . 5 26 0 . . .Black SeaCrambe maritima 4 3 41 0 3 1 46 32 . 0 4 0 . 25
Lactuca tatarica 4 3 38 0 3 . 34 44 0 . 4 . . .Euphorbia seguieriana Neck. 2 . 19 . . . 15 26 . . . . . .Linaria dalmatica 2 0 16 0 . 2 7 33 0 . . . 2 .Alyssum hirsutum M.Bieb. 1 . 12 . . . 14 8 . . . . . .Cynanchum acutum L. 2 . 11 1 . . 10 12 1 0 . . . .Artemisia tschernieviana Besser 3 . 25 . . . 38 2 . . . . . .Gypsophila perfoliata L. 2 . 18 . . . 27 2 . . . . . .Melilotus albus 3 1 17 1 1 . 21 9 2 . 1 1 . .Artemisia santonicum L. 2 . 14 . . . 22 . . . . . . .Carex ligerica J.Gay 1 0 13 . . 1 16 7 . . . . 1 .Phragmites australis 4 2 11 3 2 . 15 4 3 1 3 . . .Seseli tortuosum L. 4 . 10 3 . . 16 . 3 3 . . . .Elymus elongatus (Host) Runemark 2 . 10 2 . . 14 1 2 . . . . .Centaurea arenaria M.Bieb. ex Willd. 3 . 30 . . . 15 59 . . . . . .Medicago sativa 2 1 19 0 1 . 5 44 0 . 1 . . .Secale sylvestre Host 1 . 13 0 . . 6 26 0 . . . . .Silene thymifolia Sm. 2 . 11 0 . . . 31 1 . . . . .Chondrilla juncea L. 2 2 10 1 3 . 5 18 2 1 3 . . .N.E. Black SeaGlycyrrhiza glabra L. 1 . 9 1 . . 14 . 1 . . . . .Bromus squarrosus 1 . 9 0 . . 14 . 0 . . . . .Astrodaucus littoralis (M.Bieb.) Drude 1 . 9 . . . 14 . . . . . . .Galium humifusum M.Bieb. 1 . 8 . . . 13 . . . . . . .Polygonum arenarium 1 . 8 0 . . 12 . 0 . . . . .Salsola soda L. 1 0 8 0 0 . 12 . 1 . 0 . . .Argusia sibirica (L.) Dandy 1 . 8 0 . . 12 . 0 . . . . .Suaeda maritima 1 1 7 0 1 . 10 . 1 0 1 . . .Cynodon dactylon 7 3 6 8 3 . 10 . 9 2 4 . . .S.W. Black SeaSilene conica 1 2 6 0 2 . 2 13 0 . 3 . . .S. European Atlantic and Mediterranean SeaCalystegia soldanella 27 18 . 30 21 . . . 26 43 19 27 . .Lotus cytisoides L. 8 . . 10 . . . . 9 10 . . . .Cutandia maritima (L.) Barbey 8 . . 9 . . . . 10 9 . . . .S. European Atlantic, N.W. and S. Mediterranean SeaLotus creticus L. 6 . . 7 . . . . 3 17 . . . .Malcolmia littorea (L.) R.Br. 3 . . 4 . . . . 0 13 . . . .
64
Aetheorhiza bulbosa 5 . . 6 . . . . 4 12 . . . .Helichrysum stoechas (L.) Moench 4 2 . 4 2 . . . 2 12 2 . . .N.W. Atlantic, North Sea, Baltic SeaAmmophila arenaria 17 67 16 17 68 60 . 45 17 16 69 65 60 50Festuca rubra . 63 . . 63 57 . . . . 65 56 56 100Carex arenaria 1 43 . 1 44 32 . . . 5 46 36 31 75Honckenya peploides 1 29 . 1 29 25 . . . 6 26 42 25 25Leymus arenarius 0 24 3 . 24 23 . 9 . . 29 5 20 100X Calammophila baltica . 10 . . 10 15 . . . . 12 0 16 .Galium album . 10 . . 10 8 . . . . 13 2 8 .N.W. European Atlantic and North SeaHypochaeris radicata 3 25 . 3 28 1 . . 4 1 24 42 2 .Sedum acre 0 25 . 0 27 7 . . 0 0 30 14 5 50Taraxacum sect. Ruderalia . 19 . . 21 2 . . . . 20 27 2 25Lotus corniculatus 1 18 . 1 20 1 . . 1 . 14 39 . 25Sonchus arvensis 0 16 1 . 18 1 . 2 . . 21 6 . 50Galium verum . 16 . . 18 3 . . . . 16 25 2 50Cerastium semidecandrum 0 16 0 . 17 2 1 . . . 20 8 2 .Leontodon saxatilis 1 15 . 2 16 2 . . . 6 16 17 2 .Phleum arenarium 1 14 . 2 16 . . . 2 . 18 9 . .Plantago lanceolata 1 14 . 1 15 . . . 1 0 13 25 . .Hippophae rhamnoides 0 12 . 0 13 3 . . 0 . 16 1 3 .Poa pratensis . 11 . . 12 3 . . . . 11 18 2 50Ononis repens . 9 . . 10 . . . . . 9 12 . .Senecio jacobaea L. . 10 . . 11 . . . . . 8 23 . .S North SeaCerastium diffusum 0 8 . 0 8 . . . . 1 6 16 . .Tripleurospermum maritimum 0 7 . 0 8 . . . . 1 6 12 . .North Sea and Baltic SeaHieracium umbellatum . 31 . . 26 78 . . . . 34 . 80 25Corynephorus canescens 1 20 . 1 18 40 . . . 4 22 2 42 .Jasione montana 0 16 . 0 14 32 . . 0 0 17 2 33 .Viola tricolor . 12 . . 10 26 . . . . 12 4 27 .Artemisia campestris 4 12 3 4 6 59 1 6 1 11 8 . 61 .Lathyrus japonicus ssp. maritimus . 7 . . 5 28 . . . . 6 1 27 50Festuca polesica Zapall. . 3 . . 0 23 . . . . 1 . 23 .Linaria odora (M.Bieb.) Fisch. 0 2 . 0 . 18 . . 0 . . . 19 .
65
Helichrysum arenarium (L.) Moench . 3 . . 2 18 . . . . 2 . 18 .Calamagrostis epigejos 1 4 7 . 3 13 6 8 . . 3 . 13 .N.E. and central S. Baltic SeaThymus serpyllum . 3 . . 2 9 . . . . 3 . 9 .Festuca lemanii . 1 . . . 9 . . . . . . 9 .Salix daphnoides . 1 . . . 9 . . . . . . 9 .Tragopogon floccosus Waldst. & Kit. . 1 . . . 9 . . . . . . 9 .N. North Sea and N.W. Baltic SeaPotentilla anserina . 4 . . 4 2 . . . . 3 7 . 75Elytrigia repens 0 7 2 0 7 3 3 . 0 . 9 . 2 50Atriplex prostrata 1 5 3 1 5 2 4 . 1 1 6 2 1 50Arrhenatherum elatius . 1 . . 1 1 . . . . 2 . . 50Plantago maritima 0 2 3 . 2 1 4 . . . 2 2 1 25Linaria vulgaris 0 3 2 . 3 1 3 . . . 4 . 1 25Atriplex littoralis . 2 . . 2 1 . . . . 3 . 1 25Sedum telephium . 1 . . 1 1 . . . . 1 . . 25Vicia cracca 0 1 . 0 1 1 . . 0 . 1 . . 25
66
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 maritimumMean SD Mean SD
Leaf area per plant (m²) 0.00463 0.00136 0.00253 0.00019Dry mass (kg m-2) 0.161 0.060 0.15119 0.06314Number of leaves per plant 42.0 31.1 48.0 37.2Height (m) 0.196 0.0927 0.237 0.0682Leaf area index 2.63 0.87 0.61 0.27
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)
Flowering start Flowering end Duration (months)South Mediterranean coast April June 2North-east Mediterranean coast May August 3North-west Mediterranean coast June August 3South Atlantic coast June August 3Southern North Sea, W. Baltic Sea July August-September 1-2North Atlantic, Irish Sea, Baltic Sea July August 1
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Table 5. Invertebrate animals recorded as feeding on Eryngium maritimum
Taxon Ecological notes Plant part Country Reference
ARTHROPODA, InsectaHemipteraAphididaeCavariella aegopodii (Scopoli) Oligophagous on Apiaceae;
overwinters as eggs on Salix spp. 1
ColeopteraScarabaeidaePolyphylla fullo L. Larvae Roots Netherlands 2
LepidopteraOecophoridaeAgonopterix cnicella Treitschke Larvae; monophagous on
Eryngium maritimum; causes rolling, webbing and brown discolouration
Shoots, leaves UK, Netherlands 3, 4
TortricidaeAethes margarotana Duponchel Larvae boring, webbing and
mining. Causes brown discolouration
Roots, upper stems, flowers
Now extinct in UK 5
Aethes williana Brahm larvae boring; feeds mainly on Daucus carota
Roots, lower stems
UK 6, 7
NoctuidaeAgrotis ripae Hübner Larvae; monophagous Shoots, leaves UK 8PapilionidaePapilio machaon L. Caterpillar Leaves, roots Sweden 9
MOLLUSCA, GastropodaHelicidaeTheba pisana O.F. Müller Leaves, stems? Portugal 10
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-Luther-
University 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).
(d)(a)
(b)
(c)
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).
(a)
(b)
(e)
(d)
(c)
73
(a)
(c)
(b)
74
Fig. 5. Scanning EM micrographs of leaf surface structure with epicuticular waxes: (a) lower
surface (b, c) upper surface (W. Barthlott).
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).
(a) (b) (c) (d) (e)
75
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