Biological Flora of the British Isles: Orchis mascula (L.) L

Journal of Ecology

2009,

97

, 360–377 doi: 10.1111/j.1365-2745.2008.01473.x

© 2009 The Authors. Journal compilation © 2009 British Ecological Society

-Blackwell Publishing Ltd

BIOLOGICAL FLORA OF THE BRITISH ISLES* No. 252

List Vasc. PI. Br. Isles (1992) no.

162, 20, 2

Biological Flora of the British Isles:

Orchis mascula

(L.) L.

Hans Jacquemyn

1

†, Rein Brys

2

, Olivier Honnay

1

and Michael J. Hutchings

3

1

Division of Plant Ecology and Systematics, University of Leuven, Arenbergpark 31, B-3001 Heverlee, Belgium;

2

Research Institute for Nature and Forest, Kliniekstraat 25, B-1070 Brussels, Belgium; and

3

School of Life Sciences, University of

Sussex, Falmer, Brighton, Sussex, BN1 9QG, UK

Summary

1.

This account presents information on all aspects of the biology of

Orchis mascula

(L.) L. (earlypurple orchid) relevant to understanding its ecological characteristics and behaviour. The maintopics are presented within the 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 characteristics, herbivores and disease, history and conservation.

2.

Orchis mascula

is a native herb of the British flora. It is mostly found in woodland, copses, grasslandsand open pastures, mostly on neutral or base-rich soils. It can also occur in hedgerows, scrub, on roadsidesand railway banks, in grikes on limestone pavement and on moist cliff ledges. It is absent from very acidor very wet sites. It tolerates a sparse to moderately dense canopy, but it does not flower in deep shade.

3.

Orchis mascula

is a non-bulbous geophyte with little or no capacity for vegetative spread. Themain perennating organ is a tuber (strictly a rootstem tuber). In most years the tuber generates arosette of expanded leaves, and, at the end of every year of the plant’s life, the tuber is replaced byat least one new tuber. Dormancy, the failure of above-ground parts to appear in a growing season,and the subsequent reappearance of full-sized photosynthetic plants in subsequent seasons, hasbeen observed, but does not last longer than 1 year. The species is long-lived: it takes at least 4 yearsfrom first appearance above-ground to achieve flowering for the first time. The maximum recordedlifetime after first appearance is 13 years.

4.

Orchis mascula

is not autogamous and pollinators are necessary for successful pollination andfruit set. Flowers are nectarless, and pollinated by deceit, mainly by bumblebees and solitary bees.Natural levels of fruit set are usually < 20%. Hand-pollination can increase fruit set to approxi-mately 80%, indicating that seed production is strongly pollen-limited. The lowest four flowers aremore likely to be pollinated than the upper flowers, probably because pollinators learn to avoid thespecies after discovering that it offers no reward.

5.

As in most other European countries,

Orchis mascula

has declined in the British Isles, although it isnot at threat of extinction at a national level. Most sites from which it has been lost are in central Englandand Scotland. Most losses have been caused by woodland clearance and coniferization, intensificationof grassland management and ploughing. The cessation of traditional coppicing practises has also ledto a decline in the abundance of

O. mascula

. Since the species is slow to colonize new forest stands orgrasslands, management should focus mainly on conservation of ancient forest habitats and grasslandsin which fertility is moderate to low and grazing is absent or low in intensity. Restoration of traditionalcoppicing practices could also lead to higher chances of the species flowering and surviving in the long-term.

Key-words:

ancient woodland, communities, conservation, coppicing, germination, pollination, soils

*Nomenclature of vascular plants follows Stace (1997) and, for non-British species,

Flora Europaea

. More recent orchid taxonomy, based onmolecular phylogeny (Bateman

et al

. 2003), is given in parenthesis in the text.†Correspondence author. E-mail: [email protected]

Orchis mascula

(L.) L.

361

© 2009 The Authors. Journal compilation © 2009 British Ecological Society,

Journal of Ecology

,

97

, 360–377

Early purple orchid. Orchidaceae, genus

Orchis

, subgenus

Masculae

, section

Masculae

.

Orchis mascula

is a polycarpicperennial herb with two ellipsoid to sub-globose tubers,15–35

×

10–20 mm, positioned 3–10 cm underground; rootsfew, rather slender. Stem 20–60 cm, erect, stout, cylindrical,pale green, often purplish, and angled above, sometimes hollowat the base, with 3–5 leaves in lower half and with sheathsabove. Leaves 5–20 cm long, 0.5–3 cm wide, bright or greyish-green, broadly to narrowly oblong–lanceolate to oblong, acuteor obtuse at apex, keeled, usually with rounded black–purplespots, the lower leaves spreading, the upper more erect andclasping. Inflorescence a spike, 4–15

×

3–5 cm, ovoid or cylin-drical, rather lax, especially below, with 10–45 flowers. Bracts12–20 mm long, 1.0–1.5 cm wide, usually as long as ovary,purple-tinged, narrowly linear-lanceolate, long-acute at apex,membranous, one-veined or the lower three-veined. Flowersreddish-violet, magenta, lilac, rose, pale pink or white, scent-less or with an unpleasant smell of cats. No nectar is produced.Outer perianth segments 6–8 mm long, ovate or oblong-lanceolate, the two lateral deflexed, the median more or lesserect; inner obliquely ovate-lanceolate. Labellum 8–15

×

7–18 mm, deep reddish-violet to pale rose or magenta, paler atthe base and dotted with darker purple, three-lobed; lateral lobes1.2–3.7

×

1.7–5.9 mm, ovate or orbicular, obtuse, crenulatetowards the apex, middle lobe 1.7–5.1

×

2.5–7.9 mm, almostsquare, slightly larger, truncate to two-lobed, crenulate witha ± distinct central notch and sometimes with a lateral notchon either side. Spur 10–15

×

1–3.5 mm, at least as long as ovary,stout, cylindrical, straight or curved upwards, horizontal orascending, blunt or truncate. Column short, with a small pointat the apex. Anthers ovate 1.2–2.5 mm, purplish or greenish-grey;pollinia 2, dark green, or yellow when the flowers are white;caudicles 1.4

×

0.15 mm, yellow and transparent, enclosed ina rose-violet bursicle, strongly elastic. Two stigmas, confluenton the roof and sides of the chamber, edged with a purplishline. Rostellum three-lobed. Ovary sessile, purple-tinged.Capsule 17–20.3

×

4.4–5.2 mm, erect. Seeds very numerousand tiny (length: 0.39 (± 0.13) mm, width: 0.18 (± 0.03) mm),mean volume 6.43 (± 3.98)

×

10

−

3

mm

3

; testa transparent.

Orchis mascula

shows considerable variation throughoutits range (Kretzschmar

et al

. 2007). In Britain, leaves of plantsin Scotland are less likely to bear spots than those of plants inEngland (Foley & Clarke 2005). White-flowered specimens arenot rare and can be found in virtually all larger populations.Occasionally, pink-coloured individuals can be observed.Pankhurst & Mullin (1991) report that small forms of

O

.

mascula

are found on Taransay, South Harris and Fuday inthe Outer Hebrides and that these have been distinguished asvar.

ebudicum

J. W. H. Harrison. Although the status ofsome subspecies and varieties is still under debate, mostrecent accounts report five subspecies and several varieties(Kretzschmar

et al

. 2007), as follows:

1.

Orchis mascula

ssp.

mascula

. Spike dense, many-flowered.Perianth segments usually purple, obtuse, acute or shortlyacuminate. Lateral lobes of labellum not deflexed; middlelobe up to 1.5 times as long as the lateral lobe. Spur usually aslong as ovary. Mainly western and western-central Europe.

2.

Orchis mascula

ssp.

ichnusae

Corrias. Spike oval to conical,few-flowered. Perianth-segments lilac, the outer with brown-ish-purple veins, obtuse. Lateral lobes of labellum deflexed;middle lobe up to 1.5 times as long as the lateral lobe. Spurusually as long as the ovary or slightly longer. Leaves unspotted.Endemic to Sardinia.

3.

Orchis mascula

ssp.

speciosa

(W.D.J. Koch) Hegi. Spikedense, many-flowered. Perianth-segments purple, aristate-acuminate, the outer often deflexed at apex. Lateral lobes oflabellum not deflexed; middle lobe up to twice as long as thelateral lobe. Spur as long as the ovary. Central, south and east-ern Europe.

4.

Orchis mascula

ssp.

scopulorum

(Summerh.) H. Sund.Spike pyramidal, short and dense. Perianth-segments palepink or reddish, obtuse. Lateral lobes of labellum notdeflexed; middle lobe up to 1.5 times as long as the laterallobe. Spur a third or half of the length of the ovary, horizon-tal. Endemic to Madeira.

5.

Orchis mascula

ssp.

laxifloraeformis

Rivas Goday andBellot. Spike lax, many-flowered. Perianth-segments obtuse,purple. Lateral lobes of labellum not deflexed; middle lobeslightly longer than the lateral lobe. Spur shorter than, to aslong as, the ovary. Central Pyrenees and mountains ofsouth-western Spain.

Recent phylogenetic data (Bateman

et al

. 2003) haveshown that the former ssp.

olbiensis

(Reut. ex Gren.) Asch.and Graebn. should be granted the status of a species. It isconsidered as the sister to an extinct representative of thesection

Masculae

, from which all other species of thissection have developed. Thus it is an isolated positionwithin the section and it is also older than

Orchis mascula

(Kretzschmar

et al

. 2007). The former ssp.

pinetorum

(Boiss &Kotschy) E. G. Camus, Bergon & A. Camus and ssp.

tenera

(Landwehr) Del Prete, on the other hand, can only beassigned the possible status of variety. Recently, ssp.

long-

icalcarata

Akhalkatski, H. Baumann, R. Lorenz, Mosulishviliand R. Peter and ssp.

maghrebiana

B. Baumann and H.Baumann have been described (Akhalkatski

et al

. 2005;Baumann & Baumann 2005), but their status is under debateand some (Kretzschmar

et al.

2007) argue that these taxacan be granted, at most, the status of a variety. Fora more thorough description of the

O. mascula

complex, seeKretzschmar

et al.

(2007).

Orchis mascula

is a native herb occurring in moist meadowsand pastures, open woods, copses, thickets or on rock-ledges,mostly on neutral or base-rich soils. It also occurs inhedgerows and scrub, on roadsides and railway banks, ingrikes on limestone pavement, and on moist cliff ledges. Itis absent from sites that are very acidic or very wet. It toleratesa light canopy, but it does not flower in deep shade. Thetraditional management of coppiced woodland appearsto have created particularly favourable conditions for itssurvival.

Orchis mascula

is common in traditional coppice-with-standards woodlands on circumneutral soils, but itgenerally does not occur in the acid sessile-oak coppice woodsthat are very widespread up and down the western side ofBritain.

362

H. Jacquemyn

et al.


Journal of Ecology

,

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, 360–377

I. Geographical and altitudinal distribution

Orchis mascula

is widespread throughout the British Isles,although it is more common in the southern half of England.In the period 1987–1999,

O. mascula

was recorded from1416 10-km squares in Great Britain (about 50% of thetotal; Preston

et al

. 2002) (Fig. 1). It has been recorded in allvice-counties in Britain (Stace

et al

. 2003), including thenorthern isles of Orkney and Shetland, and all Irish vice-counties (Scannell & Synnott 1987).

Orchis mascula

has alsobeen recorded in the Channel Islands. Areas in which it isinfrequent or absent include the treeless reclaimed fens ofEast Anglia, and acidic, species-poor uplands of centralWales and the Southern Uplands of Scotland. In Ireland it isprominent in the Burren, but very rare in the adjacent acidicareas of Connemara (Webb & Scannell 1983).

Orchis mascula

has a very wide distribution in Europe andalso occurs in parts of Asia. It is found throughout most ofEurope – with the exception of northern Russia, mainlandFinland and a large part of Sweden – in North Africa andeastwards to Iran, the Caucasus and western Siberia (Fig. 2;Ziegenspeck 1936; Meusel

et al

. 1965; Sundermann 1970;

Hultén & Fries 1986). In Norway,

O. mascula

has beenrecorded in Karlsøy as far as 70

°

N and it also occurs in theLofoten Islands. In Sweden, it only occurs in Halland,Blekinge, Schonen, Småland, Dalarne, Upland and Vester-gotland. It is widespread in western Estonia, including theislands of Saaremaa, Hiiumaa and Muhu. In the Mediterra-nean, several subspecies have been recognized (Castroviejo

et al

. 2005) and in Asia Minor the spp.

pinetorum

(Boiss &Kotschy) E. G. Camus, Bergon & A. Camus is found, occur-ring through the Pontus up to the Caucasus and Persia andprobably into Syria as well (Ziegenspeck 1936).

The altitudinal range of

O. mascula

in the British Isles isfrom sea level to 880 m a.s.l. in Caenlochan, Angus (Pearman& Corner 2004). In Spain it occurs between sea level and1750 m (Castroviejo

et al

. 2005). In the Alps it has beenrecorded at approximately 2000 m (Hegi 1975): 2200 m inPuschlav (Switzerland), 2500 m in the area around Bernina(Italy), 2000 m in Wallis (Switzerland), 1900 m in Tirol (Austria)and 1600 m in the Karawanken Mountains on the borderbetween Austria and Slovenia (Ziegenspeck 1936). In themountains of Albania, the species is mostly found between1600 and 2100 m altitude (Ziegenspeck 1936).

Fig. 1. The distribution of Orchis mascula inthe British Isles. Each dot represents at leastone record in a 10 km square of the Nationalgrid. Native: (�) native post-1970; (�) nativepre- and including 1970; (+) non-native post-1970; (×) non-native pre- and including 1970.Mapped by Stephanie Ames, using Dr A.Morton’s DMAP software, Biological RecordsCentre, Centre for Ecology and Hydrology,Wallingford, mainly from data collected bymembers of the Botanical Society of theBritish Isles.

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(L.) L.

363


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, 360–377

II. Habitat

(

A

)

CL IMATIC

AND

TOPOGRAPHICAL

L IMITATIONS

In Britain,

Orchis mascula

does not encounter any climaticlimits. Its northern limit within Europe coincides approxi-mately with the

−

6

°

C January isotherm (Ziegenspeck 1936).Dahl (1998) gives

−

5

°

C as the mean temperature of thecoldest month calculated for the lowest altitudes in the

Atlas

Florae Europaeae

squares where

O. mascula

occurs. Hill

et al

.(2004) report that the mean January and mean July temper-atures, and mean annual precipitation in the 10-km squaresoccupied by

O. mascula

in Britain are 3.5

°

C, 14.7

°

C and1073 mm, respectively. Preston & Hill (1997) and Grime

et al

.(2007) assign

O. mascula

to the European Temperate elementin the British flora (i.e. mainly occurring in Europe and notextending east of 60

°

East, and associated with the cool-temperate deciduous forest zone).

(

B

)

SUBSTRATUM

Orchis mascula

grows on a variety of soils in the British Isles,but is most common on basic and calcareous soils, often on

moderately nutrient-rich substrates (Rackham 2003). It canalso be found on clayey neutral soils or even slightly acid soils(Summerhayes 1951). It is reported as very characteristic oflimestone dales in Derbyshire (Clapham 1969), but sparselydistributed in the Magnesian limestone dales of County Dur-ham (Graham 1988). In Glamorgan it is found on limestonesea-cliffs (Wade et al. 1994) and in Warwickshire it is con-centrated on Lower Lias limestone substrate (Cadbury et al.1971). In Dorset it is characteristic of heavier soils includingupper chalk sediments (Good 1948), and in Hertfordshireand Norfolk it is frequent in woods on heavy boulder clay(Dony 1967; Beckett & Bull 1999). Edees (1972) reports itsoccurrence in Staffordshire on Keuper marl. In the Shrop-shire region, Sinker et al. (1985) state, that it is most commonon damp loams and clays, but only under well-drainedconditions. It is found on fixed sand dunes, as in Kent (Philp1982) and the Isle of Man (Allen 1984), and it grows in grikesin almost bare limestone in the Burren and elsewhere onlimestone pavement (Foley & Clarke 2005). In Shetland itoccurs on ultrabasic rocks, growing on bare, dry serpentinegravel on Unst and Fetlar (Scott & Palmer 1987).

Grime et al. (2007) give the median pH of substratessupporting O. mascula as between 6.25 and 6.75. Ziegenspeck

Fig. 2. European distribution of Orchis mascula sensu lato. Reproduced from Hultén & Fries (1986) Atlas of North European Vascular PlantsNorth of the Tropic of Cancer, Volume II, by permission of Koeltz Scientific Books, Koenigstein, Germany. Key: � isolated, fairly exactlyindicated occurrences common or fairly common occurrence within the area, incompletely or approximately stated occurrences.

364 H. Jacquemyn et al.

© 2009 The Authors. Journal compilation © 2009 British Ecological Society, Journal of Ecology, 97, 360–377

(1936) reports pH values for O. mascula soils between 5.0and 7.7. Based on field measurements, he grouped O. mascula,O. morio (now regarded as Anacamptis morio) and Dacty-

lorhiza sambucina into an assemblage of orchid species thatcan grow in weakly acid conditions, although they are morecharacteristically found on strongly basic substrates.

III. Communities

Within the British Isles, Orchis mascula is a species of bothwoodlands and open conditions, including a variety ofcoastal and inland grasslands, pastures and wastelands. Espe-cially in the eastern counties, O. mascula is mainly a woodlandplant. In the north and west it becomes common in unshadedhabitats. It is common on grassy road verges in Devon, occa-sionally spectacularly so. In northern England, Scotland andIreland it is found on montane cliff ledges, being frequent inthis habitat in parts of Scotland (McCallum Webster 1978;Duncan 1980). It is also a component of the flora of grikesin limestone pavements, in which it is protected from grazing,and it occurs with other woodland relict species in ravines inheavily grazed areas such as Rum (Pearman et al. 2008). Itis infrequent in communities of skeletal habitats, althoughit may be abundant on walls where lime mortar has beenused in south-west Waterford (Green 2008). Grime et al.(2007) give the mean number of species with which it is asso-ciated in the Sheffield region as between 18 and 22 m−2.

In Britain, O. mascula is commonly a species of fertilewoodlands with moderate shade. It occurs with both lowconstancy and low abundance in Fraxinus excelsior–Acer

campestre–Mercurialis perennis woodland communities (W8)(Rodwell 1991), including Primula vulgaris–Glechoma hederacea

(W8a), Anemone nemorosa (W8b) and G. robertianum (W8e)sub-communities (Rodwell 1991). These woodlands arewidespread in lowland Britain and occur on calcareous mullsoils where annual rainfall is < 1000 mm. It is also commonlyfound in F. excelsior–Sorbus aucuparia–M. perennis commu-nities (W9). This woodland community is characteristic ofmoist brown soils derived from calcareous bedrocks in thesub-montane climate of north–west Britain (Rodwell 1991).Orchis mascula is also an occasional constituent of beechwoods,oakwoods and oak-hornbeam woods (Salisbury 1916;Summerhayes 1951). It has been recorded in several ofPeterken’s (1981) ancient semi-natural woodland types,including 1Ba (wet F. excelsior-Ulmus glabra woodland,heavy soil form), 2Aa (wet F. excelsior-A. campestre wood-land) at a frequency of 1–10%, and in type 7G (Alnus glutinosa

woodlands with seasonal or persistent standing water) at afrequency of 11–20% (E. P. Mountford, pers. comm.).

In eastern Britain, woodland populations of O. mascula arestrongly associated with ancient woods (i.e. woods thatoriginated before 1600) and the species is slow to colonizerecently-established woods (Peterken & Game 1984). Similarobservations have been made in Germany (Zacharias 1994)and by Hermy et al. (1999), who reviewed 22 Europeanstudies and classified O. mascula as an indicator of ancientwoodland. However, it is probably associated with ancient

woods because their pattern of management up till recenttimes has provided congenial habitat for O. mascula (perhapsespecially the regular disturbance of the coppicing cycle), notbecause of their age as such. A meta-analysis of studiesinvestigating colonization ability of woodland herbs acrosswoodland communities in Europe indeed indicated that theprobability of O. mascula occurring in woods is not significantlydetermined by woodland age (Verheyen et al. 2003). Honnayet al. (1998) and Sciama (2000) have found that O. mascula

had a higher probability of occurrence in recently-establishedwoods than in ancient woods in Belgium and France, respectively.

Orchis mascula is also a component of several grasslandcommunities (Rodwell 1992). These include Dryas octopetala–

Carex flacca calcicolous sub-montane heath grasslandcommunities (CG13), including the Hieracium pilosella–

Ctenidium molluscum (CG13a) and Salix repens–Empetrum

nigrum ssp. nigrum sub-communities (CG13b). It has higherconstancy (21–40%) in the latter sub-community than inthe former. It is also a component of Festuca ovina–Avenula

pratensis (CG2) and F. ovina–Agrostis capillaris–Thymus

praecox grasslands (CG10). Among mesotrophic grasslandsit is recorded in Anthoxanthum odoratum–G. sylvaticum

communities (MG3), particularly the Briza media sub-community (MG3b), in which its constancy is 21–40%. Itis also a minor component (1–20% frequency) of Luzula

sylvatica–Geum rivale calcifugous tall herb grassland com-munities (U17), including the Geranium sylvaticum (U17b),Agrostis capillaris–Rhytidiadelphus loreus (U17c) and Primula

vulgaris–Hypericum pulchrum (U17d) sub-communities, withcover values between 4% and 10% in U17 and U17b.

Outside Britain, O. mascula can be found in a wide varietyof meadow and forest communities. In Scandinavia and theBaltic, the species is a constituent of alvar grassland com-munities. On the Estonian islands of Saaremaa, Hiiumaa andMuhu, for example, O. mascula occurs with Ophrys insectifera,Orchis militaris and O. (Neotinea) ustulata. Co-occurring grassand sedge/graminoid species are Sesleria caerulea, Danthonia

decumbens, Carex pulicaris, C. capillaris and C. acutiformis.Other frequently observed associates are Filipendula vul-

garis, Scorzonera humilis, Geum rivale, Dianthus superbus andTofieldia calyculata (Ziegenspeck 1936). In the Baltic, it isalso a component of species-rich wooded meadows and alvarforests. Here it occurs with Sesleria caerulea, Filipendula

vulgaris, Galium verum, Primula veris, Hepatica nobilis, Melica

nutans, Brachypodium pinnatum, Calamagrostis arundinacea

and Carex montana (T. Kull, pers. comm.).In the Netherlands, where it is an endangered species,

O. mascula only occurs in forest commuities. Although wide-spread at the beginning of the 20th century, it has now becomevery rare due to cessation of traditional coppice management.Stortelder et al. (1998) distinguish two different associationsin which O. mascula occurs. The first, Stellario–Carpinetumorchietosum, occurs on rather steep slopes where the lime-stone is within 60 cm of the soil surface and the pH rangesfrom 6.5 to 7.5; it is characterized by a species-rich treelayer consisting primarily of Fraxinus excelsior and Quercus

robur. In the shrub layer, Clematis vitalba, Corylus avellana,

Orchis mascula (L.) L. 365


Carpinus betulus, Crataegus monogyna, Rosa canina, Rubus

caesius, Ligustrum vulgare, R. arvensis and Acer pseudoplat-

anus can be regularly found. Listera (Neottia) ovata, Paris

quadrifolia, Actaea spicata, Brachypodium sylvaticum, Viola

reichenbachiana, Sanicula europaea, Campanula trachelium,Carex digitata and Eurhynchium striatum are also abundantin these communities. The second association, Orchio–cornetum, develops after clearance of forests of the formerassociation. In the first years after a clear-cut, several speciesthat occurred in a vegetative state under the closed canopytake advantage of increased light at soil level, and start flow-ering abundantly. After a few years, the canopy closes again.Characteristic species for this association are Orchis purpurea,Hypericum hirsutum, Rosa arvensis, Cephalanthera damaso-

nium and Ophrys insectifera.In central Europe, O. mascula is a species of beech forests

on chalk (Sundermann 1970). Dominant species within theseforest communities are Brachypodium sylvaticum, Melica nutans,M. uniflora, Carex ornithopoda, C. digitata, Vicia dumetorum,Dictamnus albus, Hypericum hirsutum, Peucedanum officinale,Lithospermum purpureocaeruleum, Melittis melisophyllum

and Tanacetum corymbosum. Other orchid species that canoften be encountered together with O. mascula are Neottia

nidus-avis, Epipactis helleborine, Cephalanthera damasonium,C. rubra, L. (Neottia) ovata and Plantanthera chlorantha. Orchis

mascula can also be found in small brushwoods and groves.These thickets mostly consist of Prunus spinosa, Crataegus

monogyna, Sorbus torminalis, S. aria, Rosa spp., Rhamnus

cathartica, Cornus mas and Lonicera xylosteum, and are oftenlocated between dry meadows and closed woods. They areparticularly rich in orchid species, including Himantoglossum

hircinum, Ophrys insectifera, O. sphegodes, O. apifera, Orchis

militaris, O. pallens, O. purpurea and O. (Neotinea) ustulata.Orchis mascula is a constituent of xeric grasslands (Sunder-

mann 1970), where it often occurs with Ophrys insectifera,O. apifera, O. fuciflora, Orchis militaris, and O. purpurea. Othercharacteristic species in these communities are Gentianella

germanica, G. ciliata, Pulsatilla vulgaris and Polygala comosa.When these grasslands are no longer grazed, they developinto scrub, with Corylus avellana, Cornus spp., Crataegus spp.and Fagus sylvatica becoming dominant. Within these com-munities, Cephalamnera damasonium becomes the dominantorchid, and, in addition to O. mascula, O. purpurea, L. (Neottia)

ovata and Platanthera chlorantha are often found. Ziegenspeck(1936) mentions that O. mascula is also part of Xerobrometumrhenanum, a species-rich community in which Bromopsis

(Bromus) erecta, Carex caryophyllea, Anthyllis vulneraria,Hippocrepis comosa, Onobrychis viciifolia, Sanguisorba minor

and Peucedanum oreoselinum make up the dominant species.At higher altitudes, O. mascula is part of the Seslerieto-Semperviretum and Semperviretum calciphilum communities.Carex sempervirens, Sesleria caerulea, Anthoxanthum odoratum,Agrostis canina and F. ovina are the most important grass spe-cies, whereas Ranunculus bulbosus, Arabis alpina, Potentilla

erecta, Alchemilla glabra, Medicago lupulina, Anthyllis vulner-

aria, Lotus corniculatus, Hippocrepis comosa, Polygala amara

and Gentiana verna are the most important forbs.

In the absence of calcareous rock, O. mascula can be foundtogether with Traunsteinera globosa, Dactylorhiza sambucina,D. elata, O. militaris, Gymnadenia conopsea, and Coeloglossum

viride (D. viridis). Helictotrichon pubescens and A. odoratum

are the dominant grass species. Scorzonera humilis, Polygona-

tum odoratum, Potentilla alba, Lathyrus montanus and Galium

boreale are the most frequent herbs. Lilium martagon, Lychnis

viscaria, Thesium bavarum, Trollius europaeus, Pulsatilla patens,Aquilegia vulgaris, Trifolium montanum, G. sanguineum,Gentiana pneumonanthe, Pulmonaria angustifolia and otherspecies can also be found. In Albania, O. mascula has also beenobserved in the Ericetum carneae at an altitude of 2100 m onserpentine soils, where it occurs with Stipa pulcherrima,Sesleria heufleriana, Brachypodium retusum, Lilium albanicum,Cytisus pseudoprocumbens, Hypericum richeri, Viola dukadjinica

and Thymus praecox ssp. zygiformis.

In less dry conditions, it is also a constituent of the Meso-brometum gentianetosum ciliatae. In this community, Bromopsis

(Bromus) erecta is no longer the dominant grass species, butBrachypodium pinnatum and, to a lesser extent, Festuca rubra

and Poa angustifolia become more prominent. Associatedspecies include Carex caryophyllea, Ranunculus bulbosus,Potentilla neumanniana, Sanguisorba minor, Ononis spinosa,Lotus corniculatus, Linum catharticum, Polygala vulgaris,Viola hirta, Pimpinella saxifraga, Gentianella ciliata, Galium

verum, Cirsium acaule and Scabiosa columbaria. Related to thiscommunity are semi-dry grasslands that are partly occupiedwith shrubs and in which O. mascula occurs with Ophrys

insectifera, O. apifera, Orchis militaris, Gymnadenia conopsea,Platanthera chlorantha and Listesa (Neottia) ovata. Bunium

bulbocastanum and Danthonia decumbens are also notablein this community. Bromus erectus is replaced mainly byHelictotrichon pratense, and Brachypodium pinnatum,Festuca ovina, Carex caryophyllacea and C. flacca are alsopresent.

A final community type in which O. mascula is found is theflower-rich meadows that are dominated by Narcissus poe-

ticus ssp. radiiflorus (N. angustifolius) in the KarawankenMountains along the Slovenian-Austrian border. Many orchidspecies co-occur, including Dactylorhiza maculata, D. sambucina,D. traunsteineri, D. elata, Orchis mascula, O. (Anacamptis)morio, O. (Neotinea) ustulata, Ophrys insectifera, Nigritella

nigra and Coeloglossum viride (D. viridis). Crocus vernus ssp.albiflorus and Trollius europaeus are also important componentsof this community (Ziegenspeck 1936).

IV. Response to biotic factors

Orchis mascula is rare in many suitable places such as wood-lands and old marl-pits where grazing takes place. However,when grazing and trampling are reduced, it has been shown toincrease in abundance, indicating that it is sensitive to grazingand trampling (Brewis et al. 1996). In grassland, it favoursestablishment in places where moss grows up beneath thegrass. Its occasional occurrence on road verges in spectacularabundance, declining again after a few years, also suggeststhat particular disturbance events may favour it.



V. Response to the environment

(A) GREGARIOUSNESS

Orchis mascula can form vast populations. On Öland, popu-lations of O. mascula can sometimes exceed a million individ-uals (Nilsson 1983). Within populations, it often grows in clumpsof 2–5 individuals (Möller 1987). Jacquemyn et al. (2009a)used spatial point pattern analysis to investigate whetherO. mascula individuals showed a non-random spatial distri-bution by mapping the position of each individual to thenearest measurement (cm) in two populations. In bothpopulations, adult O. mascula plants showed a pronouncedsmall-scale aggregation, with groups of two to five adultplants growing very close to each other, confirming the earlierfindings of Möller (1987). The cluster radii ranged from 20 to39 cm. Seedling densities can be quite high. In Germany,for example, Möller (1987) has reported densities of 400–500seedlings m−2. In their study populations, Jacquemyn et al.(2009a) showed that seedlings were also clustered aroundadult plants, with approximately 90% of all recruits locatedwithin 16 and 24 cm of the adults in the two populations.Limited seed dispersal (see VIII C) and/or distance-dependentgermination with respect to adult plants (Diez 2007; Jacque-myn et al. 2007) are the probable reasons for the sizes of theobserved clusters. Occasionally, clusters of O. mascula mayarise as a result of vegetative propagation, although thecapacity for this seems to be limited (Jacquemyn et al. 2009a;see also VI C).

(B) PERFORMANCE IN VARIOUS HABITATS

Orchis mascula is shade tolerant, but ill-adapted to life in thedeep shade of undisturbed woodland and it appears to bereliant on frequent opening of the canopy for its long-termpersistence (Tamm 1972; Jacquemyn et al. 2008). It isstimulated to flower after coppicing, probably as a result ofthe increased light penetration to the herbaceous layer.Mason & MacDonald (2001) recorded that the percentage oflight penetrating to the soil in July varied between 60% and80% in the first year after coppicing, declined to approximately25% in the third year after coppicing, and was < 1% 5 yearsafter coppicing when the canopy had closed again. Using dataon the demographic structure of 15 populations, Jacquemynet al. (2008) showed that in the year after coppicing a mean of42.9% of all individuals in O. mascula populations flowered,whereas in undisturbed woodland only 20.8% of all individ-uals flowered. In undisturbed woodland, 42.8% of adultplants were non-flowering, whereas in coppiced woodland13.3% of adult plants did not flower (Fig. 3a). However, inflo-rescence size and the number of flowers per inflorescence didnot differ significantly in the coppiced and undisturbedwoodland (mean number of flowers per inflorescence= 16.5 ± 7.2 and 14.0 ± 4.6 in the coppiced and undisturbedwoodlands, respectively; Jacquemyn et al. 2008).

Coppicing can also have a large impact on fruit set, as theopen and sunny conditions in coppiced woodland may attract

more potential pollinators. Jacquemyn et al. (2008) showedthat the percentage of flowering plants that did not set fruitvaried between 0% and 25% (mean: 6.9%) in coppicedwoodland and was significantly lower than in undisturbedwoodland (mean: 31.2%, range: 22.2–37.5%). Fruitingsuccess also increased significantly with population size incoppiced woodland, whereas in closed woodland there wasno relationship between fruiting success and population size(Fig. 3b). The probability of setting at least one fruit wassignificantly determined by inflorescence size (measured asnumber of flowers in the inflorescence), and to a lesser extentby the interaction between inflorescence size and woodlandtype. Large inflorescences had a higher probability of settingat least one fruit than smaller ones. Inflorescences with 15flowers had a 90% probability of setting at least one fruit inrecently coppiced wood, whereas in undisturbed woods inflo-rescences had to produce 34 flowers to have a 90% probabilityof setting at least one fruit (Fig. 3c). The mean number offruits per plant varied between 1.75 and 12.1 (mean: 6.17)among populations in recently coppiced woodland and wassignificantly higher than that for populations in undisturbedwoodland (mean: 1.66, range: 1.36–2.06). The proportion offlowers setting fruit varied between 20.5% and 55.5% inrecently coppiced woodland and between 8.8% and 13.2% inundisturbed woodland. Percentage fruit set also increasedsignificantly with increasing population size in recentlycoppiced woodland, whereas in undisturbed woodlandpercent fruit set was independent of population size(Fig. 3d).

Because changes in forest management strongly affect localenvironmental conditions, coppicing can also affect thedistribution of genetic variation among populations, throughevolutionary processes including selection, differential geneexchange and chance associations caused by genetic drift andfounder effects. Natural selection can adapt populations tothe variable photon flux densities at forest soil level, resultingin micro-geographical variation in genetic variation associatedwith different types of forest management. Genetic heteroge-neity can also be the result of differential gene exchange causedby differences in flowering probabilities between forests managedin different ways. Studying 15 populations, Jacquemyn et al.(2009b) showed lower genetic variation and greater geneticdifferentiation between O. mascula populations in woods thatwere left undisturbed for several decades compared to popu-lations in woods that were regularly coppiced. Because ananalysis of molecular variance showed no between-group dif-ferentiation, the possibility that selection for shade tolerancein undisturbed populations affected genetic differentiation isunlikely, because in that case genetic variation should to someextent be related to the type of forest management. Geographicallocation also did not affect the patterns of genetic variation,because isolation by distance was not observed (Jacquemynet al. 2009b). These results indicate that a lack of coppicingleads to decreased genetic diversity and increased differenti-ation in this orchid species, probably as the result of geneticdrift following demographic bottlenecks. Both the geneticand demographic data also indicate that coppicing plays an



important role in maintaining viable woodland populationsof O. mascula in the long-term (Jacquemyn et al. 2008, 2009b).

(C) EFFECT OF FROST, DROUGHT, ETC.

Leaves of O. mascula emerge above-ground in early winterand can withstand frost. The tubers contain salep, whichconsists mainly of mucilage and starch (Lawler 1984). Themucilage is water-retentive and reduces the freezing point of thetissue, rendering the tubers fairly drought- and frost-resistant(Jaretzky & Bereck 1938). However, O. mascula is to someextent sensitive to drought, particularly in the early growthphases. Rasmussen (1995) mentioned that seedlings ofO. mascula in shallow soil died after a very dry spring.Protocorms in the upper layer of the soil may also die fromdrying out during summer (Möller 1987), which may limit thespecies’ ability to persist in habitats with dry soils.

VI. Structure and physiology

(A) MORPHOLOGY

At the time of flowering (April–May), O. mascula has twounderground tubers: one, at the base of the leafy shoot, isslightly wrinkled and brown and in the process of depletion,while the other is whiter, usually smaller, firmer in texture andclothed with fine hairs (Fig. 4; Sharman 1939). The latter(daughter) tuber is attached to the parent tuber by a cylindri-cal connection, which is usually about 0.5 cm long, but mayreach 2.5 cm in length (Sharman 1939). Sharman (1939) alsonoted that older plants flowered earlier and had larger tubers,with the daughter tubers attached by shorter stalks. In aboutthe middle of August, the leaves of the parent plant die backand the connection between the adult and daughter tuberbreaks, leaving a brown ring on the daughter tuber. By this

Fig. 3. Demographic structure and fruit set of Orchis mascula populations in coppiced and undisturbed woodland. (a) Demographic stagestructure of populations of Orchis mascula occurring in coppiced and undisturbed woodland. Vertical bars, 1 SE. (b) The relationship betweenpopulation size (i.e. the number of flowering individuals) and the percentage of plants that failed to produce any fruits at all (fruiting failure).(c) The relationship between the number of flowers and the probability of setting at least one fruit for plants located in coppiced and undisturbedwoodland, respectively. (d) Percentage fruit set for 15 populations of Orchis mascula occurring in coppiced and undisturbed woodland. Verticalbars, ± 1 SE. (Data from Jacquemyn et al. 2008).



time, the tuber shows little external change, but the axillarybud that forms the daughter tuber for the following season isalready visible. The growth of the bud and tuber continuethrough the winter and in January the base of the subtendingscale splits, and the new daughter tuber protrudes through it.Throughout February and March, the tuber grows in lengthand diameter and pushes its way outwards and downwardsthrough the split in the subtending scale.

(B) MYCORRHIZA

Like almost all other Orchis species, O. mascula is mycorrhizaland a fungal symbiont is necessary for seed establishmentunder field conditions (Rasmussen 1995). In experiments setup by Borris & Voigt (1986), seeds of O. mascula did not ger-minate asymbiotically whether fresh mature seeds, after-ripened seeds or immature embryos from green capsules wereused, but when a fungus strain isolated from an adult plantwas introduced, seeds germinated well. Harley & Harley(1987) cite nine studies that have shown mycorrhizal associ-ations with O. mascula. Recent molecular investigations ofthe mycorrhizal diversity of O. mascula showed that several

closely-related species of the Tulasnellaceae are associatedwith O. mascula (S. Van Kerckhove & B. Lievens, pers. comm.).Thanatephorus orchidicola Warcup & Talbot has also beenisolated from O. mascula, but its ability to induce germi-nation has not been confirmed (Warcup & Talbot 1966).

(C) PERENNATION: REPRODUCTION

Orchis mascula is a non-bulbous geophyte showing limited orno vegetative spread. The main perennating organ is a tuber(strictly a rootstem tuber) that is considered homologous witha polystelic axillary shoot (Sharman 1939; Rasmussen 1995).Each year the tuber is wholly replaced by at least one newdaughter tuber. In most years the parent tuber generates arosette of expanded leaves. In individuals that flower, anunbranched stem elongates from within the rosette andtypically generates additional leaves that become sequen-tially smaller and increasingly bract-like. Eventually, thebracteoidal leaves are succeeded by true bracts subtendingspirally arranged flower buds to generate the racemoseinflorescence.

Dormancy, that is, the failure of above-ground parts toappear in a growing season, followed by reappearance offull-sized photosynthetic plants in subsequent growingseasons, has been observed in O. mascula, but appears not tolast longer than 1 year (Inghe & Tamm 1988). The speciesappears to be long-lived: it takes at least 4 years from firstappearance for plants to flower for the first time (Möller1987), although in general the first flower spike will not beproduced until the plant is even older (Kretzschmar et al.2007). Plants may persist in a vegetative condition for severalyears in places where the habitat has become overgrown, forexample as a result of re-growth of coppice or invasion byRubus fruticosus agg. and light penetration to the ground isvery low. Flowering can resume in the year immediatelyfollowing coppicing or clearance (Jacquemyn et al. 2008).The maximum recorded lifetime of O. mascula after firstappearance is 13 years (Inghe & Tamm 1988).

(D) CHROMOSOMES

A chromosome number of 2n = 42 has been repeatedlyreported for O. mascula (Hagerup 1938; Heusser 1938; Ver-meulen 1949; Skalinska et al. 1957; Gadella & Kliphuis 1963;Kliphuis 1963; Mrkvicka 1992; Oberdorfer 1994; Wisskirchen &Haeupler 1998; Bässler 2002; Cozzolino et al. 2004).

(E) PHYSIOLOGICAL DATA

Specific leaf area of O. mascula is 15–20 mm2 mg−1 and leafdry matter content is < 15%. Salisbury (1928) reported a meanof 45 stomata mm−2 (range 33–67 mm−2) on the lower (abaxial)leaf surfaces, but that there are no stomata on the upper(adaxial) leaf surfaces. Canopy structure is semi-basal (i.e.with stems erect or ascending, and leafy, but with the largestleaves towards the base). Canopy height is 100–300 mm, andlateral spread is < 100 mm in diameter.

Fig. 4. Adult plant of Orchis mascula in April. (a) roots, (b) brownring, (c) old tuber, (d) new tuber, (e) flowering stalk.



(F) B IOCHEMICAL DATA

Chemical analyses of the floral fragrance produced by O.

mascula were made by Nilsson (1983) and Salzmann et al.(2007). Monoterpene hydrocarbons make up the largest partof the emitted scent (up to 90% according to Nilsson (1983),83% according to Salzmann et al. (2007)). Tricyclene, α-pineneand trans-β-ocimene made up 69.7% of the observed monot-erpenes (Nilsson 1983). Only about 2.4% of the scent consistsof monoterpene alcohols, of which linanool makes up thelargest fraction. However, there seems to be considerable var-iation in scent both within and between populations, and onlya few compounds, including nonanal, (E)-ocimene, myrcene,cis-linalool oxide, and linalool were common to most individ-uals (Salzmann et al. 2007). There were no compounds com-mon to the scent emitted by all sampled individuals (n = 76)and individuals displayed high quantitative variation in scentprofiles. This high variation in the chemical composition ofemitted scents may be a strategy for promoting reproductivesuccess in food-deceptive species. As with other floral signalssuch as colour, rare morphs may be proportionally morepollinated, and thus experience higher fitness than morecommon morphs (Salzmann et al. 2007). As a result, negativefrequency-dependent selection may maintain high variationin floral scent within these populations, although preliminaryresults of manipulative experiments conducted by the sameauthors did not support this hypothesis. Relative fitness, cal-culated as the number of capsules/number of flowers averagedfor all plants within a plot, was not related to the total amountof scent or the number of different compounds in the scentemitted, suggesting that odour differences do not arisethrough selective pressures imposed by pollinators on odourcompounds, but are to a certain extent the result of randomprocesses or differences in environmental conditions such assoil, humidity and temperature (Salzmann et al. 2007).

VII. Phenology

Leaf phenology is vernal (Grime et al. 2007). The lower leavesof the rosette emerge in late winter, followed by more erectbasal leaves that expand and surround the developing inflo-rescence later in spring (Foley & Clarke 2005). Summer-greenplants, with leaves unfolding early in spring, have beenreported in Denmark (Rasmussen 1995). When plants ofO. mascula from winter-green populations on Öland, Sweden,were transplanted next to summer-green plants in the Copen-hagen Botanical Gardens, they sprouted in autumn, whereasthe leaves of the adjacent Danish plants did not develop theirleaves until spring, possibly reflecting different ecological races(Rasmussen 1995).

Within the British Isles, the timing of anthesis in O. mascula

varies with geographical location. Plants in the south canflower as early as April or early May, whereas those innorthern populations may not flower until 2–3 weeks later.The species makes a notable contribution to the floral displayin the Burren in the later half of May (Webb & Scannell 1983).In the Netherlands, flowering usually starts at the beginning

of May (Kreutz & Dekker 2000), whereas in Germany itbegins half way through April and lasts until the end of May(Möller 1967). In Central Europe, the peak of flowering is inMay (Kretzschmar et al. 2007). In all locations, flowering isusually finished by the end of June. More details wereprovided by Nilsson (1983), who studied the phenology ofO. mascula in Öland in Sweden. Anthesis started around 10May and continued until mid-June (Nilsson 1983). Inexposed alvar meadows, the flowering period lasted for about3 weeks and was 1 week earlier than in woods. In the latterhabitat, individual plants flowered for about 4 weeks. Themaximum number of open flowers was recorded between 26May and 2 June.

When monitored over consecutive years, Inghe & Tamm(1988) found that the proportion of flowering plants variedbetween 0% and 100%, largely because of successionalchanges to the vegetation in the habitat. With gradual succes-sion towards forest-like conditions in their study area, theproportion of plants flowering decreased until all plantswithin the plot eventually disappeared. Nonetheless, con-siderable year-to-year variation in percentage flowering wasobserved, and a substantial proportion of plants that floweredin a given year did not flower in the next, suggesting consid-erable costs of flowering. Warmth in May of the previous yearand drought in the previous June–August negatively affectedthe proportion of plants flowering in O. mascula (Inghe &Tamm 1988), suggesting that these results are interpreted assome kind of damage caused by drought. However, given thesmall sample size and the fact that these results were largelydependent on the biased positions of zero frequencies, theauthors were careful not to interpret their relationships asindicative of cause and effect.

VIII. Floral and seed characters

(A) FLORAL BIOLOGY

The floral biology of O. mascula has been described in greatdetail by Darwin (1867) and Nilsson (1983). The back sepaland the two side petals form a hood at the top of the flower,with the two side petals, one on each side, folded backwards.The three-lobed lip (labellum) forms a sloping convex plat-form at the front of the flower with, near its point of attach-ment, a long-tubular spur, which is oriented either almosthorizontally or in a nearly upright position. In the centre ofthe flower, within the hood and immediately above the mouthof the spur, is the column, which is very short and wide. Wherethe column is joined to the sides of the lip, a broad tube orantechamber leads to the spur proper. The central part of thecolumn is surmounted by the single stamen with its two bag-like pollen anther loculi (thecae) placed almost erect and sideby side. There are two pollinia, one lying loosely in each halfof the stamen. They consist in the upper part of a number ofsmaller masses of pollen attached lightly by threads to a centralspindle or axle, which is drawn out in the lower part to form along-stalk (caudicle), the whole being club-shaped. At its base,this stalk has a small round sticky disc (viscidium), which is



hidden within a purse-like container (bursicle). The bursicle,which is mounted on a part of the column (rostellum) pro-jecting downwards into the mouth of the spur, contains asticky liquid which prevents the disc from drying out until thewhole pollinium is removed by an insect visiting the flower.The viscidia, of which there is one to each pollinium, can beremoved separately, after which the flap, which is elastic, returnsto its original position, thus preventing viscidia that have notbeen removed from drying out.

The normal colour of O. mascula flowers ranges from lightto dark red-violet. The three-lobed lip has a slightly brightercolouring than the sepals and petals. A whitish or yellowishcolouring of the lip’s base, dotted with crimson spots, givesfurther contrast. In the insect visual spectrum, these coloursare insect-green to insect-yellowish-green. Most co-floweringspecies exhibit an array of different colours in the insect visualspectrum, suggesting that O. mascula does not mimic thecolouration of other co-occurring food-flowers (Nilsson1983). At least 31 insect species have been recorded carryingO. mascula pollinia (Table 1). Most of these species, whichmay serve as effective pollinators, are bumblebees and bees(Table 1), although Barile et al. (2006) showed that flowers ofO. mascula are also occasionally pollinated by moths (Table 1).It is therefore believed that O. mascula is a pollinator gener-alist (Nilsson 1983; Van der Cingel 1995). Because of the largenumber of solitary bees observed in Öland compared to othernorthern and north western European countries, and becauseof a much higher diversity of bees in southern Europe, theMediterranean and further east, Nilsson (1983) suggestedthat O. mascula is pollinated by, and specialized for, beepollination in these regions. The upward curve in the lengthyspur has also been considered as a specific adaptation topollination by solitary bees (Van der Cingel 1995). However,inspection of the potential pollinator guilds in Scandinaviaand the Mediterranean shows no differences in pollinatorassemblages between these regions, suggesting no specificspecialization and that O. mascula is a pollinator generalist.

The pollination process itself has been described in detailby Darwin (1867), Nilsson (1983) and Johnson & Nilsson(1999). When a visiting bee inserts its proboscis into theflower, its head usually presses against the mouth of the spurbecause the spur is usually longer than the proboscis. Whenthis happens, the bursicle swings backwards, and the sides ofthe insect’s head become enclosed by the walls while the stubis tightly squeezed so that the insect’s head rubs against theunderside of the viscidia. One or both viscidia stick to thehead or thorax. The fluid at the base of the viscidium driesand hardens within 30 s after contact, fixing it to the insect.The initially upward-pointing pollinia then rotate through90° to point forward, so that, when the insect enters anotherflower, the pollinia contact the stigma and pollination isachieved. Rotation of the pollinia does not occur untilapproximately 1 min after they have become fixed to theinsect (Johnson & Nilsson 1999), ensuring a high probabilitythat, as few flowers are visited before the bee moves to anotherinflorescence, the next flower visited will belong to a differentplant (Lang 1980).

Bumblebees typically probe only 1–2 flowers when visitinginflorescences of O. mascula. Artificial addition of nectarincreased the number of flowers probed per inflorescencefrom 1.7 ± 0.2 to 6.4 ± 0.8 (Johnson & Nilsson 1999). Bees spenta mean of 7.2 ± 1.8 s on control inflorescences and 57.6 ± 9.1 son nectar-enriched inflorescences. The mean time bees spentprobing individual flowers increased from 2.5 ± 0.5 s on con-trol flowers to 5.9 ± 0.7 s for nectar-enriched inflorescences.Mean transit times for bees between flowers of O. mascula

were 4.3 ± 3.5 s on nectar-enriched plants and 4.1 ± 3.5 onnectarless plants (not significantly different). The amountof pollen deposited on a sequence of emasculated flowersdecreased exponentially, with carryover proportions of 0.67,indicating that on average 33% of the pollen load is depositedon each sequential flower.

Table 1. Insect visitors to flowers of Orchis mascula

Species Source

HymenopteraBombus lapidarius Linnaeus 1, 2, 3, 4, 5B. terrestris Linnaeus 1, 2, 4, 5, 6B. pratorum Linnaeus 2, 4, 5B. hortorum Linnaeus 1, 2, 4, 5B. confusus Schenck 2B. pascuorum Scopoli 2, 4B. muscorum Linnaeus 7B. ruderatus Fabricius 5, 8B. sylvarum Linnaeus 4B. lucorum Linnaeus 4B. humilis Illiger 5B. ruderarius Müller 5B. rupestris Fabricius 5Psithyrus campestris Panzer 1, 2P. rupestris Fabricius 8P. vestalis Fourcroy 8P. barbutellus Kirby 4Osmia bicolor Schrank 4, 9Argogorytes mystaceus Linneaus 10Eucera hungarica Friese 5E. longicornis Linnaeus 4Halictus sexcintus 5Nomada marshamella Kirby 4Andrena nigroaenea Kirby 4A. helvola Linnaeus 4A. bicolor Fabricius 4

LepidopteraZygaena transalpina Esper 11Minucia lunaris (Denis & Schiffermüller) 11

DipteraEmpis tessellata Fabricius 12, 13Scatophagia stercoraria Linnaeus 14Anthomyiidae sp. 14

Sources: 1, Müller (1869); 2, Müller (1873); 3, Godfery (1933); 4, Nilsson (1983); 5, Cozzolino et al. (2005); 6, Selander & Bryant-Meisner (1909); 7, Darwin (1867); 8, Godfery (1918); 9, Maréchal & Petit (1955); 10, Kullenberg (1961); 11, Barile et al. (2006); 12, Hobby (1933); 13, Hobby & Smith (1961); 14, Willis & Burkill (1903).



(B) HYBRIDS

Scopece et al. (2007) experimentally assessed pre-mating andpost-mating isolation barriers between a large suite of Euro-pean food-deceptive orchids, including O. mascula. Theyclearly demonstrated that in most species post-zygotic matingbarriers acted as effective barriers for hybridization in O.

mascula, with low fruit set and extremely low viable seedproduction when flowers were pollinated by a different species(Table 2). Pre-mating isolation, on the other hand, was weakbecause, like most food-deceptive orchid species, O. mascula

is a pollinator generalist, with the potential for pollinationby more than one insect species, and the capacity for sharinga considerable proportion of potential pollinating species(Cozzolino et al. 2005). Scopece et al. (2007) also investigatedcorrelations between reproductive isolation mechanisms andgenetic distance between species. In the case of O. mascula, nocorrelation was observed between genetic distance and pre-mating isolation (Spearman rank correlation: −0.33, P > 0.05)(Fig. 5a). In contrast, a strong correlation was observed betweencombined post-mating isolation and genetic distance (Spear-man rank correlation: 0.61, P = 0.01) (Fig. 5b).

Despite these strong post-mating barriers, several hybridsinvolving O. mascula have been described. For example,although they appear to be very rare, hybrids between Orchis

(Anacamptis) morio and O. mascula (O. × morioides Brand)have been recorded in the British Isles in open pasture andcliff-top habitats where both parent species occur (Godfery1918, 1933; Summerhayes 1951; Foley 1986; Graham 1988;Sell & Murrell 1996). The hybrids are intermediate between

the parent species, the spotted leaves of O. mascula beingsometimes combined with the green-veined sepals of O.(Anacamptis) morio (Summerhayes 1951). Experimentsconducted by Nilsson (1983) showed that no fruits or embryoswere formed when flowers of O. mascula were pollinated withpollen from O. (Anacamptis) morio. These results indicate thata complete barrier exists towards pollen from O. (Anacamptis)morio (Hildebrand 1865; Müller 1869; Scopece et al. 2007)and that hybrids with O. (Anacamptis) morio are thereforeprobably to be the result of pollen flow from O. mascula toO. (Anacamptis) morio (Hildebrand 1865; Nilsson 1983). Ahybrid between O. mascula and Gymnadenia conopsea

(× Orchigymnadenia belezei Fournier) has been reported froma site in County Durham where exposed conditions resultedin the synchronous flowering of these usually spring andsummer flowering species (Graham 1988).

Outside the British Isles, interspecific hybrids involvingO. mascula have been found repeatedly, most frequently withO. pauciflora, O. pallens, O. patens, O. provincialis ssp. provin-

cialis, O. provincialis ssp. pauciflora (treated subsequentlyas O. pauciflora) and O. spitzelii (Willing & Willing 1977;Steinbruck et al. 1986; Pellegrino et al. 2000; Cozzolino et al.2006; Kretzschmar et al. 2007). Pellegrino et al. (2005) hasconfirmed hybridization between sympatric island popula-tions of O. mascula and O. provincialis in Sardinia (Italy).Experimental crosses between hybrid individuals of O. mas-

cula and O. pauciflora and their parental species producedsome fruits and viable seeds (> 1%) (Scopece et al. 2008).Hybrid pollen was also able to trigger the development offruits in parental species. However, seed viability appeared to

Table 2. Pre-zygotic and post-zygotic mating barriers between Orchis mascula and other members of the Orchis genus and related genera (datafrom Scopece et al. 2007). The recent taxonomy used in the original paper, based on molecular phylogeny, has been retained

Species Pre-mating* Post-mating pre-zygotic† Post-mating post-zygotic‡ Combined post-mating§

Anacamptis laxiflora 0.75 1 − 1Anacamptis morio 0.25 0.51 1 1Anacamptis palustris 0.75 1 − 1Anacamptis papilionaceae 0.60 0.66 1 1Anacamptis pyramidalis 0.50 0.73 1 1Dactylorhiza romana 0.75 0.61 0.98 0.99Neotinea lactea − 0.51 0.94 0.97Neotinea tridentata 0.20 0.73 0.75 0.93Neotinea ustulata 0.80 1 − 1Orchis anthropophora 0.83 0.49 0.43 0.71Orchis italica 0.75 0.13 0.75 0.78Orchis pauciflora 0.25 0.06 0.20 0.25Orchis provincialis 0.75 1 − 1Orchis quadripunctata 0.75 0.52 0.16 0.59Orchis purpurea 0.80 1 − 1Orchis simia 0.62 0.62 0.59 0.85

*Premating isolation was calculated as 1 – (number of functional classes of pollinators shared by a species/total number of functional classes of pollinators of each species). Values of this index vary between 0 (no isolation) to 1 (complete isolation) (Scopece et al. 2007).†Post-mating pre-zygotic isolation was calculated as the proportion of fruits formed following interspecific pollinations, relative to the proportion of fruits formed following intraspecific pollinations within each parental species (McDade & Lundberg 1982).‡Post-mating post-zygotic isolation was calculated as the proportion of viable seeds obtained in interspecific pollinations relative to the proportion of viable seeds in intraspecific pollinations within each parental species.§Combined post-mating isolation was calculated as the linear sequential combination of pre-zygotic and post-zygotic isolation measures (Moyle et al. 2004): combined post-mating isolation = Postprezygotic + (1 − Postprezygotic) × Postpostzygotic.



be strongly reduced when compared with values of theintraspecific crosses of the parental species. Seed productionin parental species with hybrid pollen was 47.2%, whereas itwas 92.8% in intraspecific O. mascula crosses and 85.5% inO. pauciflora crosses (Scopece et al. 2008).

Investigation of the scent profiles of O. mascula, O. pauciflora

and their hybrid O. × colemanii showed that O. mascula andO. pauciflora were clearly differentiated, whereas most hybridsemitted an intermediate scent (Salzmann et al. 2007). Hybridi-zation is therefore unlikely to generate novel odour bouquetsthat may influence the pollinator response. Because scentprofiles and relative fitness were also not related, the odourdifferences between species were probably a neutral by-product of genetic drift rather than the result of pollinator-imposed selection.

(C) SEED PRODUCTION AND DISPERSAL

Orchis mascula is not autogamous and pollinators are neces-sary for successful pollination and fruit set. The flowers emit

a repellent odour, reminiscent of cats, which may act as anattractant for insects. Pollinator exclusion resulted in no fruitor seed production (Nilsson 1983). However, Nilsson (1983)reported that in hot and dry years when anthesis was faster,flowers quickly dried up and the viscidia were sometimesextracted by the collapsing lip. In a very few cases this causedthe pollinia to contact the stigma, resulting in self-pollination.Experimental hand-pollinations have also shown that a lowerpercentage of embryos is formed when flowers are self-pollinated (59.8 ± 18.8%) than when they are cross-pollinated(75.1 ± 18.9%) and that the mean size of the embryos is alsosmaller (Nilsson 1983).

Under natural conditions, approximately 50% of individualplants do not set fruit in a given year and percentage fruit setis mostly low (3–20%) (Skottsberg 1907; Ziegenspeck 1936;Nilsson 1983; Johnson & Nilsson 1999). About 88% of flow-ering plants produced three or fewer fruits. Experimentalpollination of flowers increased fruit set to approximately80%, indicating that fruit set is severely pollen-limited (Nilsson1983; Johnson & Nilsson 1999). The lowermost four flowersare more frequently pollinated than those higher up theinflorescence (Delpino 1873–1874; Nilsson 1983). Comparedto the lowest five flowers, flowers in positions higher than 20were less than half as successful at setting fruit. Delpino(1873–1874) explained these findings as a result of the bees’behavioural response to the fact that no reward is offered.He argued that pollination occurs mainly during the first 2 or3 days of anthesis before bees have learnt to avoid the unre-warding flowers of O. mascula. Nilsson (1983) showed thatanthesis of O. mascula covered a time period during which theunconditioned behaviour of various bee species towardsfood-sources can be fully exploited. This period coincideswith the inexperienced recovery-feeding stage of Bombus

queens, the early long-range patrolling by Eucera males, andthe first exploratory drives by naive solitary bees.

Because of their tiny size (length: 0.39 ± 0.13 mm, width:0.18 ± 0.03 mm), small volume (6.43 ± 3.98 × 10−3 mm3) and71% free air space in the testa (Arditti & Ghani 2000), seeds ofO. mascula appear to be well-adapted for long-distance seeddispersal by wind. Despite this, parentage analyses conductedin two populations of O. mascula indicated that most seedsfall in the direct neighbourhood of the mother plant (Jacque-myn et al. 2009a), with seed dispersal distances varyingbetween 0.01 and 7.21 m (median: 1.57 m) (Fig. 6). However,occasional long-distance seed dispersal seems to occur, asgenetic differentiation between populations is low (FST = 0.08,Scacchi et al. 1990; FST = 0.04, Jacquemyn et al. 2009b).

(D) V IABIL ITY OF SEEDS: GERMINATION

Embryos of O. mascula have an average length and width of0.21 ± 0.1 and 0.14 ± 0.01 mm, respectively and an averagevolume of 1.64 mm3 (Arditti & Ghani 2000). Using a modifiedtetrazolium test (Van Waes & Debergh 1986a), on average75.8% of embryos showed evidence of being viable (Van Waes& Debergh 1986b). Similar values were reported by Nilsson(1983).

Fig. 5. Relationship between genetic distance and (a) pre-matingisolation and (b) combined post-mating isolation for 16 species (datafrom Scopece et al. 2007).



Borris and Voigt (1986) showed strong specificity in theeffectiveness of different mycorrhizal associations in pro-moting germination of O. mascula seeds. Fungi isolated fromseveral Dactylorhiza, Orchis, Platanthera, Listera (Neottia)

and Goodyera species did not promote germination, whereasmycorrhiza isolated from O. mascula itself were able to do so.The factor or complex of factors that promotes germinationis not known. Experiments with nicotinic acid amide, amember of the water-soluble vitamin B group known to influencegermination in members of the Vandea group, did not result inseed germination. Other germination-stimulating phytohor-mones such as gibberellins (gibberellin A4) and cytokinins(6-benzylaminopurine (BAP) and zeatin) also had no positiveeffect on seed germination (Borris & Voigt 1986). However,

addition of 2 ppm naphthaleneacetic acid (NAA), a planthormone in the auxin family, significantly increased seedgermination (Borris & Voigt 1986). Since fungi related toorchid mycorrhiza are known to produce auxins, it is notunlikely that the primary agents that promote germination ofO. mascula seeds are auxins.

Under natural conditions, seeds germinate in autumn andemerge above-ground in the following May (Ziegenspeck1936; Möller 1987).

(E) SEEDLING MORPHOLOGY

The period from seed germination to appearance above-ground lasts for about 10 months, and in good conditionsseedlings (4.5 × 6 mm) can first be observed in June (Beer1863; Möller 1987), although some authors report that thismay take more than 1 year (Stojanow 1916; Rasmussen 1995).At the time of emergence above-ground, the size of the tuberis approximately 6 × 8 mm, and the seedling weighs about300 mg. Germination takes place in the upper few centimetresof the soil. Möller (1987) distinguishes the following stages inthe seed germination process: (i) growth of a seed to a proto-corm; (ii) resource uptake and accumulation in a so-calledpre-tuber (G: Vorknolle); (iii) development of the leaves;(iv) development of the tuber (Fig. 7). According to Möller(1987), seedlings of O. mascula survive for about 10 monthsunderground. During that period, sugars are accumulated inthe pre-tuber without any photosynthesis. However, Rasmussen(1995) noted that without detailed anatomical and morpho-logical details it is difficult to say whether the pre-tuber rep-resents a perennial protocorm, a protocorm in the process ofproducing a tuber, or just the first tuber.

Leaf development takes place around mid-April. The sizeof the first leaf depends on local growth conditions. Whereaslight does not affect the first three developmental stages

Fig. 6. Seed dispersal distances in Orchis mascula obtained in twoplots using parentage analysis (data from Jacquemyn et al. 2009a).

Fig. 7. Stages in the development of seedsinto the seedling stage. (a–b): seed; (c) swollenseed; (d–e) protocorm; (f) protocorm withpre-tuber; (g) seedling.



(Fig. 7), it plays a major role in determining the future devel-opment of the tuber, because the seedling becomes autotrophicwhen the first leaf has developed. Further development andgrowth of the plant are dependent on the size of the leaf. In thesecond year, tubers have a mean size of 6 × 12 mm and freshmass of approximately 1.3 g (Möller 1987).

IX. Herbivory and disease

(A) ANIMAL FEEDERS OR PARASITES

There are no data in the Phytophagous Insects Database(D. Roy, pers. comm.). Browsing by muntjac deer (Muntiacus

reevesi) and sheep has been reported as damaging O. mascula

(Cooke & Farrell 2001). Slugs have been observed feeding onpetals of O. mascula. Inspection of the amount of herbivoredamage to the petals of O. mascula in a population growing inlimestone grassland in central England showed that the pro-portion of damage was < 1% across the whole population,but as high as 6% for individual plants (Breadmore & Kirk1998). In recent years there have been increasingly frequentreports of damage by wildlife, especially by wild boar feedingon the tubers (Kretzschmar et al. 2007).

(B) & (C) PLANT PARASITES AND DISEASES

No data available.

X. History

Orchis mascula has been used for centuries in the productionof salep, a drink made out of the dried and ground tubers. Itwas popular in Britain before the introduction of coffee andtea, and consumed in establishments devoted to the purpose(Grieve 1971). Salep consists mainly of mucilage and starch(Lawler 1984). In Turkey and Persia this has for many centu-ries been extracted from the tubers of various kinds of Orchis.Before coffee supplanted it, it used to be sold at stalls in thestreets of London, and was held in great repute in herbal med-icine, being largely employed as a strengthening and demul-cent agent (Grieve 1971). The best English Salep came fromOxfordshire, but the tubers were chiefly imported from theEast. The Royal College of Surgeons included orchid roots inthe aphrodisiac mixture recommended in their Pharmaco-poeia (Gray 1821, p. 27).

There are 96 common names for O. mascula (Grigson 1955).Sutherland (1683) reports that the common name for O. mas-

cula was Male Fools-stones (Robertson 2001). More ominousfolk names given to O. mascula are ‘Gethsemane’, ‘king’sfingers’, ‘bloody man’s fingers’ and ‘dead man’s thumbs’because the leaves have red markings which look like drops ofblood. Foley & Clarke (2005) claim that the name ‘Gethse-mane’ is taken from a legend that O. mascula grew below thecross of Christ, and that the markings on the leaves are dropsof Christ’s blood. The first record in Britain (Turner 1562)calls O. mascula adder grass, apparently because the spots onthe leaves were considered to resemble the pattern on the

snake. In the account of Ophelia’s death by drowning, it isreferred to as ‘long-purple’ by Queen Gertrude in Shake-speare’s Hamlet.

The ancient belief that the plant’s tubers resembled testiclesresulted in the species having a wide range of amorous andsexual associations, and its use was prescribed in treatmentsfor many ailments, especially of a sexual or amorous nature.Foley & Clarke (2005) report that the dying tubers were pre-scribed to cool ardour, and that the developing tubers wereprescribed to inflame it.

XI. Conservation

Although O. mascula is not much at threat except from hab-itat destruction and is currently not endangered in the UK, itsrange has declined here as in most western European coun-tries during the 20th century (Jacquemyn et al. 2005; Kull &Hutchings 2006). The New Atlas of the British and IrishFlora (Preston et al. 2002) records it in 1416 10-km squaresin Britain since 1987, compared with an overall total of1971squares, a decline of 28.2% (although some apparentlosses are doubtless due to under-recording in the latest timeperiod). In Ireland, a similar decline was observed (377 10-kmsquares since 1987 compared with a total of 475, an apparentdecline of 20.6%). Orchis mascula has been lost mostly fromthe London area, central England and parts of Scotland, andin Ireland it declined dramatically in Co. Dublin in the 20thcentury (Doogue et al. 1998). Most losses have been causedby woodland clearance and coniferization, intensification ofgrassland management and ploughing. However, becauseO. mascula is able to persist in open conditions, it can surviveclearance of woodland habitats. Because O. mascula has beenconsidered as an indicator of ancient forest (Peterken &Game 1984; Hermy et al. 1999), colonisation of new wood-land sites seems unlikely. There is very limited evidence for thespread of the species into new non-woodland sites. It appearsto have colonized the Isle of Man in the 20th century, as it wasfirst noticed in 1934 and spread subsequently on sand dunes(Allen 1984). Picking of flowers and uprooting of tubersmight also have contributed to the decline of the species.

The cessation of traditional coppicing practices has led to adecline in the abundance of this and other species with similarecological characteristics in Britain and elsewhere in Europe.The situation of O. mascula in the Netherlands may be illus-trative: having been one of the most abundant orchid speciesin Zuid-Limburg, the species has suffered dramatic declinesand most surviving populations today occur in woodland andconsist of few individuals, most of them in a vegetative state.The prospects for these populations are poor, as recruitmentof new individuals cannot be expected in the near future,unless traditional coppicing practices are restored (Willems1978). Results from Jacquemyn et al. (2009b) also suggestthat populations that have recently gone through a demo-graphic bottleneck due to prolonged lack of forest manage-ment harbour lower genetic diversity. Although the variationsurveyed was probably selectively neutral, its loss suggeststhat there is the potential for correlated loss of potentially



adaptive genetic variation. Low genetic diversity may also beassociated with decreased fitness through decreasing hetero-zygosity and the expression of deleterious alleles (Fischer &Matthies 1998; Keller & Waller 2002).

Acknowledgements

Authors are grateful to Stef Van Kerckhove and Bart Lievens for providinginformation on mycorrhizal associations. Tiiu Kull provided useful informa-tion on plant communities in the boreal zone, and Ed Mountford, OwenMountford and Peter Carey for information on community affiliations. Threeanonymous referees and Tony Davy provided very useful comments thatimproved the quality of this article. This research was funded by the Fund ofScientific Research (FWO) and the Research Fund K.U. Leuven.

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