BIOLOGICAL FLORA OF THE BRITISH ISLES*
No. xxx
List Vasc. Pl. Br. Isles (1992) no. 162.23.2
Biological Flora of the British Isles: Ophrys sphegodes
Hans Jacquemyn1† and Michael J. Hutchings2
1
KU Leuven, Department of Biology, Plant Population and Conservation Biology,
Kasteelpark Arenberg 31, B-3001 Heverlee, Belgium; and 2School of Life Sciences,
University of Sussex, Falmer, Brighton, Sussex, BN1 9QG, UK
Running head: Ophrys sphegodes
* Nomenclature of vascular plants follows Stace (2010) and, for non-British species, Flora
Europaea.
†Correspondence author. E-mail: [email protected]
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Summary
1. This account presents information on all aspects of the biology of Ophrys sphegodes Mill.
that are relevant to understanding its ecological characteristics and behaviour. The main
topics 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. Ophrys sphegodes is native to Britain. It used to be more widely distributed throughout
south-eastern England, but is now mainly restricted to the counties of Dorset, East Sussex
and Kent. Ophrys sphegodes is widespread throughout the western parts of central and
southern Europe, and is common in Spain, France, and Italy. Further east it occurs in
Bulgaria and Greece, including most of the Mediterranean islands, and extends into
southern Russia, Turkey and northern Iran.
3. Ophrys sphegodes grows on calcareous, nutrient-poor substrates, and rarely under any
shade. It is most common in ancient, heavily-grazed grassland on chalk and Jurassic
limestone, but it also occurs in disturbed habitats, horizontally-oriented rock floors in
limestone quarries, on old limestone quarry spoil heaps, and in lightly trampled calcareous
grasslands on maritime cliffs.
4. Ophrys sphegodes multiplies predominantly by sexual reproduction. Vegetative
multiplication occasionally occurs through survival or splitting of the old tuber. In the
UK, the species is almost exclusively pollinated by males of the solitary bee Andrena
nigroaenea, although other Andrena species have also been observed visiting O.
sphegodes flowers. Male bees are attracted by complex floral bouquets emitted by the
flowers that strongly resemble pheromones produced by female A. nigroaenea. Fruit
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production is generally low and in most populations <15% of the flowers produce
capsules.
5. Ophrys sphegodes is reproductively isolated from other species in the genus by strong
pre-mating barriers, most notably temporal (differences in flowering time) and floral
(different pollinators) isolation. In particular, differences in floral odour appear to underlie
floral isolation. Nonetheless, several hybrids involving O. sphegodes have been described
in Britain and elsewhere in Europe.
6. The range of Ophrys sphegodes in Britain showed a dramatic decline in the twentieth
century, with the species becoming extinct in twelve vice-counties. Most losses were due
to ploughing of grassland and changes in fertilizer and grazing regimes. Its range has
increased somewhat in recent years. Increases in spring temperature due to climate
warming may seriously threaten the species by disrupting the close relationship between
O. sphegodes flowering time and the phenology of flight of its prime pollinator in the UK,
leading to reproductive failure.
Key-words: calcareous grasslands, conservation, dispersal, Ophrys, germination, mycorrhiza,
Orchidaceae, pollination, seed characteristics
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Early spider orchid. Orchidaceae. Ophrys sphegodes is a winter-green, short-lived, perennial
tuberous herb. Root tubers 2(3), ovoid to subglobose. Roots short, rather thick. Flowering
stem (15-) 25-40 (-60) cm tall, yellowish-green, erect, glabrous; leaves 4-10 × 0.5-1.5 cm, the
lower green or greyish-green, elliptical-oblong to ovate-lanceolate, rather obtuse at apex,
often mucronate, entire, spreading or recurved, with 1-14 veins, the upper narrower and more
acute at apex. Inflorescence a spike 4-10 × 1.5-4.0 cm, lax, with (2-) 5-9 (-12) flowers; bracts
10-30 × 1-4 mm, pale green, lanceolate, more or less obtuse at apex, concave, with 7-9 veins.
Flower scent not detectable by humans, rapidly fading after anthesis. Outer perianth segments
6-10 (-12) mm, green, whitish green, yellowish or olive-green, rarely white or pink, oblongovate to oblong-lanceolate, obtuse at apex, edges rolled back, the lower spreading, the upper
erect and slightly arched forwards. Inner perianth segments 4-8 (-10) × 2.5-4 (-5) mm,
greenish-yellow to olive-green or brownish, rarely pink, spreading, hairless, of variable shape,
oblong, lanceolate, oval, sometimes obovate or falcate, margins ± strongly undulate,
sometimes straight, 1-veined. Labellum suborbicular or ovate, subentire or rarely 3-lobed, the
lateral lobes small, with basal protuberances, the central lobe entire or emarginated, usually
with no terminal appendage, 10-16 × 9-18 mm (when spread), blackish to pale reddish-brown,
with a brownish submarginal band of hairs, sometimes shorter on distal half, and bordered by
a hairless margin, often narrow, lighter, sometimes yellow, often turned down, sometimes
reflexed, centre velvety, convex, with basal swelling absent or ± well marked. Speculum
greyish to bluish, glabrous, sometimes finely edged whitish, often forming a ± thickened H or
horseshoe shape. Appendage small to lacking, inserted into a distinct notch. Stigmatic cavity
and basal field rather reduced, colouration dull reddish brown or pale olive-green, paler than
centre of lip; stigmatic cavity rounded, constricted at base, floor with a greyish specular stage,
only slightly contrasting. Pseudo-eyes iridescent greenish-grey, sometimes encircled with pale
greenish edge; external walls of stigmatic cavity tinted green, ochre or reddish, slightly
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contrasting. Anther like the head of a bird with yellowish eyes, and a short, obtuse beak.
Pollinia 2, yellow. Caudicles yellow. Viscidia enclosed in bursicles. Fruit 2-2.5 × 0.7-0.9 cm.
Seeds 0.2-0.35 mm.
The species is highly variable. Clapham, Tutin & Moore (1987) state that the
description given above applies to ssp. sphegodes, and that this is the only subspecies native
to the British Isles. Considerable variation can be found in labellum shape, with rounded and
long-pointed examples sometimes occurring on the same inflorescence. Abnormalities in
labellum and perianth segments are also frequent. Based on variation in labellum features and
the size of plants, Hegi (1975) mentions several varieties on the Continent, including var.
genuina Rchb., var. araneola Rchb., var. fucifera Rchb., var. fissa Moggr., var. flavescens M.
Schulze, var. euchlora Murr., var. virescens Moggr., and var. atrata Rchb. Pedersen &
Faurholdt (2007) recognize 12 subspecies (O. sphegodes subsp. sphegodes, subsp. litigiosa,
subsp. atrata, subsp. passionis, subsp. sipontensis, subsp. spruneri, subsp. helenae, subsp.
epirotica, subsp. aesculapii, subsp. mammosa, subsp. cretensis and subsp. gortynia) that
differ from each other with regard to distribution, flowering season and/or habitat preferences
(Supporting Information Table S1). Finally, Delforge (2006) lists 33 subspecies of O.
sphegodes, to most of which he has assigned the rank of species (Table S2). On the other
hand, detailed molecular analyses of a large subset of species within the genus Ophrys has
shown that relationships within the O. sphegodes group are poorly resolved (Devey et al.
2008), suggesting that the species delimitation presented by Delforge (2006) may not be
warranted and that further research is needed before definitive statements can be made about
the taxonomic status of any of these putative (sub)species.
Ophrys sphegodes is a lowland native species of ancient, species-rich, heavily-grazed
grassland on chalk and limestone substrates. It can, however, tolerate some taller grassland
community types, and it can rapidly colonise disturbed ground, and suitable transient habitats,
5
horizontally-oriented rock floors in limestone quarries, and old spoil heaps. It is also found on
grazed and trampled maritime cliff grassland vegetation. On the European mainland it can be
found in a wide range of habitats, including garrigue, roadside verges, open woods, grassland
and pesticide-free olive groves.
I. Geographical and altitudinal distribution
Although O. sphegodes was once recorded from a considerable part of south-eastern England,
including Cornwall, Northamptonshire, Bedfordshire, Cambridgeshire, Essex, Oxfordshire
and Denbighshire, its range suffered a sharp contraction during the twentieth century, and it
no longer occurs in these counties (Fig. 1) (Summerhayes 1951). It has also been lost from
Breckland (Trist 1979), Jersey (Stace 1991) and probably Hampshire (Brewis, Bowman &
Rose 1996). The Atlas of the British Flora (Perring & Walters 1962) reported that O.
sphegodes had been recorded in 53 10 × 10-km national grid squares prior to 1930 (Hutchings
1987a), but it is probable that the records for only 46 of these squares were reliable (C. D.
Preston, pers. comm.). By 1975 the number of squares in which the species persisted had
fallen to 20, and between 1975 and 1987 a further fall in persistence occurred, with the
species remaining in only ten squares (Hutchings 1987a). Preston et al. (2002) recorded O.
sphegodes in 17 national grid squares (see also Kull & Hutchings 2006), and the most recent
distribution map, prepared from information collected up to 2002 (Fig. 1), records the species
in 19 grid squares. Some of the new records suggest that O. sphegodes is colonising suitable
sites further north than its 1987 UK range limits, perhaps as a consequence of climate
warming.
At present, the only populations in Britain that contain more than a few plants are in
Dorset, west and east Sussex and Kent. Most populations are near the coast, but there are
isolated populations in Gloucestershire, Wiltshire and West Suffolk (Fig. 1, Lang 1989;
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Harrap & Harrap 2005). Byfield (1983) estimated that the populations in Dorset collectively
numbered over 13 500 plants, and accounted for almost 70% of all the plants of O. sphegodes
in Britain. His estimated total number of plants in Dorset, Sussex and Kent (almost 20 000
altogether) was certainly an underestimate, as it was based only on counts of flowering plants,
omitting both vegetative and dormant plants, which can account for a considerable proportion
of any population in any year (Hutchings 1987a, 2010). The largest population of O.
sphegodes in East Sussex alone exceeds Byfield’s estimated number several-fold (Hutchings,
personal observation), and a newly-recorded population in Kent increased from 67 plants in
1998 to 11 500 flowering plants in 2012. In contrast, many other populations consist of very
few plants, and in some cases only a single plant is present (e.g. Wolley-Dod 1937, Burton
1983).
Ophrys sphegodes is widespread throughout the western parts of central and southern
Europe (Fig. 2), extending northwards to Belgium, central Germany (although it is absent
from north Germany) and the Czech Republic. It is common in the western Mediterranean
area (Spain, France, Italy) and occurs further east in Bulgaria and Greece, including most of
the Mediterranean islands, into southern Russia, Crimea, Turkey, northern Iran and north
Africa. It is widely distributed in France, where it is only absent from a few departments in
the north and Limousin. It does not occur in Corsica (Bournérias & Plat 2005). In the
Netherlands, O. sphegodes occurred at a single site in calcareous grassland in Zuid-Limburg
between 1970 and 1980. It has not been recorded at this location since then, suggesting that
this population has become extinct (Kreutz & Dekker 2000). Although the exact history of
this population is unclear, it is not thought to have been artificially introduced. In Belgium, O.
sphegodes is currently restricted to the southernmost part of the country, where a few isolated
populations can still be found. In northern Belgium (Flanders), O. sphegodes was known from
two localities, one between Blankenberge and Heist (last sighting in 1926) and one in the
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vicinity of the Sint-Pietersberg (last sighting in 1869) (Ziegenspeck 1936; Van de Vijver
2006).
II. Habitat
(A) CLIMATIC AND TOPOGRAPHICAL LIMITATIONS
Summerhayes (1951) lists Ophrys sphegodes as a member of the European element of the
British flora, while Hill & Preston (1997) assign it to the Submediterranean-Subatlantic
element of the British flora. The January mean temperature of the national grid squares in
which the species is found is 4 °C, the July mean temperature is 16.3 °C and the annual
precipitation is 729 mm. The northern distribution of O. sphegodes in the British Isles is
therefore probably limited by low temperatures.
In the UK, Ophrys sphegodes is essentially a lowland species (< 100 m a.s.l.). On the
Continent, it can occur at up to 800 m elevation in Germany and Switzerland (Hegi 1975), up
to 1300 m a.s.l. in France (Delforge 2006) and to 1500 m in Spain (Castroviejo et al. 2005).
(B) SUBSTRATUM
The substrates on which O. sphegodes is found, both in the UK and in most other countries in
which it occurs, overlie chalk or Jurassic limestone. Its Ellenberg number for substrate
reaction is 9, reflecting its requirement for basic substrates (Hill, Preston & Roy 2004). In
addition, it has been assigned Ellenberg numbers of 4 for moisture (i.e. it is a species of drier
rather than damp substrates) and 3 for nitrogen, indicating a requirement for a more-or-less
infertile substrate. Although its Ellenberg number for salt tolerance is 0, suggesting complete
or almost complete intolerance of salt, a considerable number of the sites in which it is found
in the UK are very close to the coast, and several of them are maritime cliff grassland
communities, sometimes within metres of the cliff edge, where deposition of wind-borne salt
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in spray is inevitable. A large population of O. sphegodes has established itself at Samphire
Hoe, Kent, on a low-lying, landscaped platform of chalk marl extracted from the Channel
Tunnel excavations. This habitat is certainly subjected to frequent, substantial deposition of
salt spray, suggesting that the proposed Ellenberg number (S = 0) may be an underestimate of
salt tolerance in O. sphegodes.
III. Communities
In the United Kingdom, Ophrys sphegodes is limited to grassland communities with a short,
grazed turf or an open structure, overlying calcareous or limestone substrates (Rodwell 1992).
Although large populations of several thousand plants occur in a few locations, the species
always has a low percentage cover. The community in which it is most characteristic is sheepor rabbit-grazed Festuca ovina – Avenula pratensis (CG2) grassland with continuous closed
turf, where there is a species-rich mixture of small grasses and dicotyledonous herbs
intimately mingled at a high species density. Of the grasses, F. ovina and F. rubra are
constants, with the former usually more abundant. Agrostis stolonifera, Avenula pratensis, A.
pubescens, Briza media, Cynosurus cristatus, Dactylis glomerata, Holcus lanatus, Koeleria
macrantha and Trisetum flavescens are also often present. Bromopsis erecta and
Brachypodium pinnatum may displace these small-statured grasses and become abundant,
especially in highly grazed sites, because they are avoided by grazing animals. Ophrys
sphegodes is most often a component of the Succisa pratensis – Leucanthemum vulgare
(CG2b) sub-community, in which Asperula cynanchica, Cirsium acaule and Hippocrepis
comosa are constants, and Carex caryophyllea, Medicago lupulina, Plantago media, Prunella
vulgaris and Trifolium pratense are common. Preferential species include Centaurea nigra
sensu lato, Leucanthemum vulgare, and Succisa pratensis.
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Ophrys sphegodes is also found in more rank and tussocky Bromus erectus
(Bromopsis erecta) – Brachypodium pinnatum (CG5) communities, primarily the Typical
(CG5a) sub-community, in which Avenula pratensis, Briza media, Carex flacca, Festuca
ovina and Koeleria macrantha are also constant and abundant. Grasses are more dominant in
this community than in CG2 grasslands. The dicotyledonous species that are constant and
sometimes locally abundant include Anthyllis vulneraria, Asperula cynanchica, Campanula
rotundifolia, Cirsium acaule, Hippocrepis comosa, Leontodon hispidus, Lotus corniculatus,
Pilosella officinarum, Pimpinella saxifraga, Poterium sanguisorba, Scabiosa columbaria and
Thymus polytrichus. There are also records of Ophrys sphegodes in more open and tussocky
Festuca ovina – Carlina vulgaris (CG1) grasslands, and in more rank Bromus erectus
(Bromopsis erecta) (CG3) and Brachypodium pinnatum (CG4) grasslands. In the last of
these, in which cover of B. pinnatum exceeds 10%, species richness is greatly reduced,
although Carex flacca and Festuca ovina are constants, and Briza media, Linum catharticum
and Poterium sanguisorba may persist. Despite its usual avoidance of taller vegetation, O.
sphegodes is one of the few other species that can be found in such vegetation, with weak and
etiolated flowering stems being supported by, and often penetrating above, a dense mat of B.
pinnatum vegetation and litter.
Finally, O. sphegodes is an occasional constituent of Brassica oleracea (MC4)
maritime cliff-ledge grassland communities. It is confined to the Ononis repens (MC4b) subcommunity which is found only in Kent and Dorset (Rodwell 2000). Brachypodium
pinnatum, Dactylis glomerata and Festuca rubra are the dominant grasses, and Centaurea
scabiosa, O. repens, Rumex acetosa and Silene nutans are constants. Brachypodium
pinnatum, Brassica oleracea, Daucus carota, Festuca rubra, Pilosella officinarum, Plantago
lanceolata, Sonchus oleraceus and Teucrium scorodonia may be frequent.
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On the European mainland, O. sphegodes can be found in a wide range of
communities, including calcareous grasslands, dry meadows, garrigue, pesticide-free olive
groves, scrub and open woodlands (Oberdorfer 1977; Delforge 2006; Pedersen & Faurholdt
2007). Oberdorfer (1977) states that O. sphegodes is a characteristic species of the
Mesobromion communities. In Peninsular Italy, O. sphegodes can also be found in coastal
sandy areas (Breitkopf et al. 2013). Within the Mediterranean, it often co-occurs with other
representatives of the genus and hybridization may occur frequently (see section VIII B).
IV. Response to biotic factors
The leaves of O. sphegodes are closely appressed to the ground. Because of this, the species is
rarely able to persist in communities in which taller species intercept a high proportion of the
available light. Despite its intolerance of shading by competitors, it is one of the few species
that can persist in grassland where the competitive, tussock-forming grass Brachypodium
pinnatum achieves moderate cover. O. sphegodes produces leaves in September or October,
and much of its carbon fixation is achieved by photosynthesis during the winter months when
many other species are dormant and their foliage has died back.
O. sphegodes suffers from grazing, especially by molluscs, rabbits and sheep (see
section IX).
V. Response to the environment
(A) GREGARIOUSNESS
Even in large populations, Ophrys sphegodes never achieves high percentage cover. In
addition, dense clusters of rosettes are uncommon. Nevertheless, groups of two or more
adjacent rosettes can be found occasionally (Fig. 3). Although this could be the result of the
establishment of plants from seed, the usual cause is that the old tuber has conserved enough
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resources, after production of the current year’s above-ground growth, to produce an
additional new tuber in the following year. These tubers are often very small in size, and may
only produce a single leaf when they first emerge following such multiplication. They may
not produce any leaves for one or more years because of insufficient resources. Hutchings
(1987a) suggested that, in any year, up to 5% of emergent rosettes might have arisen by such
vegetative propagation, but the criterion used for this assessment is likely to have overestimated the number of cases in which this occurred.
(B) PERFORMANCE IN VARIOUS HABITATS
In the Sussex population of Ophrys sphegodes studied by Hutchings (1987a), mean number of
leaves per rosette varied over a 10-year period from approximately 3 to 4.5, mean height of
flower spikes from 4.5 to 10.0 cm, and mean number of flowers per inflorescence from 2.5 to
3.25. Inflorescence height was positively correlated with total rainfall between leaf emergence
and flowering (October – May).
Although similar values for these measures of plant size are seen in many populations
of O. sphegodes in the UK, certain circumstances result in plants performing very differently.
Populations of plants growing in the very thin substrate overlying horizontally-oriented rock
floors in abandoned limestone quarries in the Isle of Purbeck in Dorset have such short
inflorescence spikes that the few flowers produced are in contact with the ground. These
plants flower about one month earlier than O. sphegodes elsewhere in the UK, presumably
because of elevated temperatures on sunny days at the soil/air interface. In contrast, some
plants in the population growing on chalk marl extracted from the Channel Tunnel
excavations at Samphire Hoe, Kent, can be over 40cm in height, and bear as many as twelve
(-17) flowers (Gay & Philp 1999). It is not known whether genetic differences also contribute
to the differences in performance between any of these populations. Plants of O. sphegodes
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from populations in the Mediterranean region are usually taller (10-70 cm) than those in the
UK, and produce between 3 and 10 (-15) flowers (Castroviejo et al. 2005).
Mean flower spike height, mean number of flowers per flowering plant and mean
number of leaves in the rosette were all highest in plants between 4 and 7 years after first
emergence, and declined in older plants (Hutchings 1987b).
(C) EFFECT OF FROST, DROUGHT, ETC.
Frost
The leaves of O. sphegodes are winter-green, being produced in September or October, and
they may not die back until after flowering in May or June. However, they often exhibit
severe frost damage, with much of the lamina being blackened and desiccated before spring.
The bases of leaves that have been damaged in this way appear to remain photosynthetically
functional.
Drought
Ophrys sphegodes is among the earliest orchid species to flower both in England and on the
European mainland. Like other members of the Submediterranean-Subatlantic element of the
British flora, it flowers, sets seed, and dies back to a dormant state before the warmest part of
the year, thus avoiding activity during the months when availability of water is at its lowest.
As in many species of orchid, alkanes and alkenes in the plant cuticle may reduce the
evaporation of water (Schiestl & Cozzolino 2008).
Shade
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O. sphegodes is a light-loving species. It is rarely found even in moderate shade, and does not
tolerate heavy shade. Its Ellenberg number for light is 8 (i.e. it is rarely found where relative
illumination in summer is less than 40%; Hill, Preston & Roy 2004).
VI. Structure and physiology
(A) MORPHOLOGY
Species of the genus Ophrys are usually small rosette plants with small inflorescences that
contain only a few flowers (Fig. 4). Plants have two ovoid-elliptoid tubers, one of which has
supported the growth of the current rosette, and is in a phase of depletion, while the other is
whiter, usually smaller, firmer in texture and clothed with fine hairs. This latter tuber gives
rise to the next rosette that is produced. A number of large, white roots originate from the
main stem axis above the tuber (Fig. 4). These roots are replaced annually and are colonized
by mycorrhizal fungi (Rasmussen 1995). The leaves are green, sometimes greyish or silvery,
and range in shape from oblong to lanceolate, obovate or falcate (Fig. 4). Flowers are
produced in early spring. In the British Isles, plants tend to produce few flowers, but plants in
many countries produce inflorescences containing between five and nine flowers.
Occasionally, plants with >12 flowers can be found.
(B) MYCORRHIZA
As in most other European tuberous orchids with a similar life history (e.g. those in the genera
Orchis, Neotinea, Anacamptis), the roots of O. sphegodes are colonized by mycorrhizal fungi.
Molecular investigation has shown that the most common fungal associates belong to
members of the Tulasnellaceae and Ceratobasidiaceae (Jacquemyn et al. 2015), confirming
other reports that Tulasnella fungi are important symbionts in Ophrys (Clements et al. 1986;
Andersen 1990, Pecoraro et al. 2015).
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(C) PERENNATION: REPRODUCTION
Ophrys sphegodes is a winter-green, short-lived perennial geophytic herb in which vegetative
spread is limited. The main perennating organ is a tuber. The tuber is usually completely
replaced every year by a new tuber, from which the whole functional plant arises on the next
occasion that the plant emerges above ground. In some cases, however, the old tuber is not
completely exhausted by producing the above-ground parts. Under such circumstances it can
support the development of a new rosette in the following year. When this happens, two
rosettes of leaves can develop in very close proximity. Occasionally, clusters of several small
rosettes, and even single leaves rather than multi-leaved rosettes, can arise in this way,
presumably having been produced by extremely small tubers.
However, neither new tubers, nor the remains of old tubers, necessarily produce
rosettes of leaves in the next year. As in many other tuberous species, both in the Orchidaceae
and in other families, plants may remain in a state of adult dormancy (Shefferson 2009), in
which no aboveground parts are produced for one or more years. Failure to produce
aboveground parts is common in O. sphegodes, and plants can continue in this condition for
one or more years. Hutchings (2010) reported that, over the course of a demographic study of
over thirty years’ duration, an average of 28.7 ± 2.7 (SE) % of the population was in
dormancy in any given year, with the proportion of the population in dormancy ranging from
as low as 10% to as high as 67.7% in different years. Almost 80% of all episodes of dormancy
were ≤2 years in duration and almost all were <4 years in length, but dormancy of as long as 8
years was observed. Although plants could undergo more than one episode of dormancy
during their lives, this was not the case for most plants, because their life-spans from first
emergence until death were too short. The probability of O. sphegodes emerging above
ground in any year declined significantly as plant age increased (Hutchings 1987b).
15
Following seed germination, plants embark on a subterranean phase of life as a
protocorm. This stage appears to last for up to two years. After first emergence aboveground, most plants have short lives. However, some plants live for as long as 10 (-20) years.
Analysis of age-specific survivorship data produced a half-life of 2.25 years from first
emergence above ground (Hutchings 2010).
(D) CHROMOSOMES
As in most other species in the genus Ophrys (d’Emerico et al. 2005), O. sphegodes is
diploid, with a basic chromosome number 2n = 36 (Greilhuber & Ehrendorfer 1975; Bianco et
al. 1989; Xu et al. 2011; Sedeek et al. 2014). Sedeek et al. (2014), however, mention one
individual that appeared to be triploid.
(E) PHYSIOLOGICAL DATA
Investigation of the plastids in the leaves of O. sphegodes has shown that they have two
different forms (Lux & Hudák 1987). Plastids in the vascular parenchyma cells are either
globular in shape or cup-shaped, and are generally smaller than mesophyll chloroplasts, which
have well-developed grana and scattered plastoglobuli. The cavities of cup-shaped plastids
frequently contain irregularly-shaped plastid material, and are lacking in thylakoids.
(F) BIOCHEMICAL DATA
Pollination in the genus Ophrys is achieved by sexual deception. Although the flowers of
many species of Ophrys bear a physical resemblance in colour, shape and hirsuteness to the
females of pollinating species of hymenoptera, this is not the case for O. sphegodes. Despite
the English name of the species (early spider orchid – because of a resemblance of the
labellum to the head, thorax and abdomen of a leg-less spider), there are no records of
16
arachnids pollinating this species. The main stimulus involved in achieving pollination is
olfactory, but Devey et al. (2008) suggest that visual deception, and even tactile deception,
involving variation in pilosity across the labellum of the flowers, also play a role.
Gas chromatographic-electroantennographic detection techniques have demonstrated
the presence of identical alkanes and alkenes in both the floral bouquet emitted by the
labellum of Ophrys sphegodes flowers and the cuticle of females of the bee Andrena
nigroaenea, which is the prime pollinator of O. sphegodes in the UK and in most other
regions (Schiestl et al. 1997, 1999, 2000). Moreover, the odours emitted in both cases contain
almost identical relative amounts of the compounds responsible for inducing copulatory
responses in male A. nigroaenea. The alkenes (unsaturated hydrocarbons) attract the male
bees that pollinate the orchid, while the alkanes (saturated analogues of the alkenes) act
synergistically, intensifying the male response. In total, Ayasse et al. (2000) identified over
100 compounds emitted by the labellum of O. sphegodes, of which 24 were biologically
active in the olfactory receptors of male bees of A. nigroaenea. The biologically active
compounds exhibited less intraspecific variation than the non-active compounds, which was
suggested to be a result of higher selective pressure on the pollinator-attracting
communication signal than on non-signaling odour components.
Ayasse et al. (2000) also recorded variation both in the chemical composition of the
floral bouquets emitted by flowers at different positions within inflorescences of O.
sphegodes, by different plants within populations, and by plants from different populations.
Male bees were shown to be able to distinguish the odour bouquets of individual flowers with
which pseudocopulation had already been attempted, enabling avoidance of previously-visited
flowers but not deterring the visitation of other, previously unvisited flowers either on the
same plant or on different plants.
17
Schiestl & Ayasse (2001) analysed the floral bouquet emitted by flowers of O.
sphegodes following pollination. They recorded changes in the composition of the odour
plume which reduced the attractiveness of pollinated flowers to A. nigroaenea males.
Pollinated flowers emitted greater absolute and relative amounts of all-trans-farnesyl (F) and
all-trans-farnesyl hexanoate (F6) than unpollinated flowers, and lower quantities of the odour
components responsible for attracting male bees. Farnesyl hexanoate is secreted by the brood
cells of fertilised female A. nigroaenea, and this results in a smaller number of attempts by
male bees to copulate with these females. Experimental tests were conducted by Schiestl &
Ayasse (2001) to compare the attractiveness to male bees of flowers treated only with a
neutral solvent, and flowers that were artificially scented with farnesyl hexanoate at a
concentration equivalent to that emitted by flowers after pollination. The flowers emitting
higher farnesyl hexanoate concentrations were significantly less attractive to male bees,
leading the authors to propose that this compound acts as a signal to divert pollinators away
from pollinated flowers and towards unpollinated flowers in the inflorescence. Although the
production of F and F6 by pollinated flowers of O. sphegodes is enough to deter further
attempts at pseudocopulation, Schiestl & Ayasse (2001) suggest that the absolute amounts
emitted are so small that male bees that approach the plant may still visit unpollinated flowers
in the same inflorescence that are still emitting chemical sexual attractants, rather than flying
to another plant. This may increase the proportion of flowers that are pollinated within
inflorescences.
Variation in the floral bouquet emitted by different flowers and plants encourages
cross-fertilisation as it allows both learned avoidance of the odour chemistry of previouslyvisited unrewarding flowers, and increases the likelihood that a given pollinator will visit
numerous different flowers and plants both within populations and in different populations.
18
Finally, Manzo et al. (2014) have reported differences in the floral bouquets emitted
by flowering individuals of Ophrys sphegodes under field conditions and after picking. These
two sets of plants differed in the proportions of a range of terpenes emitted. Picked
individuals also emitted more ά-pinene than plants growing under field conditions.
VII. Phenology
Ophrys sphegodes is a short-lived perennial in which the above-ground parts are analogous to
those of a winter annual. Leaves start to emerge above ground from early September
(Hutchings 1987a; Sanger & Waite 1998), and by the end of November most plants that will
not spend a year or more in a vegetatively dormant condition have appeared above ground.
Plants that flowered in the previous year are more likely to emerge early than plants that did
not flower (Sanger & Waite 1998). A second peak of recruitment may occur between March
and May, implying that in early May some individuals within a population have been above
the ground for six months, whereas others have only been emergent for 2 months. Some
plants that emerge in November-December may not remain above-ground in May, indicating
that annual censuses at the time of flowering could underestimate total emergent population
size and incorrectly assume that some plants are dormant or dead (Sanger & Waite 1998).
Ophrys sphegodes is one of the earliest orchids to flower in the UK. Plants start
flowering at the end of April or the beginning of May, and flowering continues throughout the
greater part of May (Summerhayes 1951; Lang 1989). In some years, flowering plants can
still be observed during the first week of June. Populations of O. sphegodes from more
westerly locations, where spring temperatures tend to be higher, flower significantly earlier
than those from more easterly locations (Robbirt et al. 2011). Short-statured plants at Worth
Matravers in Dorset can be in flower in early April. The number of inflorescences bearing
capsules containing ripening seed reaches a peak at the end of June (Sanger & Waite 1998).
19
Flowering plants that fail to develop ripe seed capsules, and vegetative plants, die back earlier
than those that produce seeds (Sanger & Waite 1998). Very few plants still possess either
green or dead above-ground parts by the end of July.
A large-scale, 32-year study of a population of Ophrys sphegodes demonstrated that
flowering was advanced following years in which temperature was higher, but delayed
following winters with many night frosts (Hutchings 2010). Both mean inflorescence height
and mean number of leaves in rosettes were greater in years in which precipitation was higher
during inflorescence extension (March – May). Mean inflorescence height and leaf number
were lower following years with higher temperature and more sunshine hours. A smaller
proportion of the population flowered in years in which periods of higher temperature
preceded the flowering season (Hutchings 2010). Flowering was advanced by 6 days oC-1
increase in spring (March – May) temperature (Robbirt et al. 2011), and over the 32-year
period from 1975 – 2006, the timing of flowering advanced by approximately 2.5 weeks
(Hutchings 2010).
Detailed investigations using both information collected from herbarium specimens
and field data have demonstrated additional strong impacts of weather on the phenology of
Ophrys sphegodes (Hutchings 2010; Robbirt et al. 2011). The data from the herbarium
specimens, collected between 1848 and 1958, corroborate the field data, which were collected
from 1975-2006, in also showing an advancement of peak flowering time of 6 days oC-1 rise
in average spring (March – May) temperature (Fig. 5). The field study showed that the date of
peak flowering of O. sphegodes advanced by an average of 0.5 day annum-1 between 1975
and 2006 (Hutchings 2010). Advancement of flowering date in O. sphegodes is greater than
the mean advancement of first flowering date (4.4 days °C-1 rise in temperature) reported for
243 species growing at a single locality in the UK (Fitter et al., 1995), but falls within the
20
range (2-10 days °C-1 rise in temperature) reported for 24 species across the UK by Sparks et
al. (2010).
It is possible that climate change could have far-reaching effects on pollination of
Ophrys sphegodes if the phenology of flowering and the phenology of emergence of Andrena
nigroaenea, the bee that pollinates the orchid, respond differently both to the spring
temperature preceding flowering in any year, and to a long-term increase in temperature as a
consequence of climate change (Robbirt et al. 2014; Willmer 2014). Robbirt et al. (2014)
carried out a comprehensive analysis of the effects of temperature on the phenology of
flowering in O. sphegodes and the date of emergence of male and female A. nigroaenea. They
showed that the flight date of the male bees was significantly earlier than the peak flowering
date of the orchid, and that the timing of male bee emergence was more responsive than the
orchid to spring temperature (Fig. 6a). More importantly, emergence date of female bees was
even more responsive to spring temperature than either orchid flowering or male bee
emergence (Fig. 6b). The data strongly suggested that, in years with warmer springs, the flight
date of female bees could coincide with, or even precede, orchid flowering. As climate
warming proceeds, the frequency of warmer springs in which this could happen is likely to
increase. The expectation would be that, if female bees have emerged before the orchid
flowers, male A. nigroaenea will be less likely to be deceived into pseudocopulation with
orchid flowers that mimic the scent of female bees. Instead, there is a greater probability that
they will copulate with female bees, or that there will at least be competition between the
orchid and female bees for the attention of male bees. Pollination of the orchid is therefore
likely to become less frequent because the essential phenological relationships between the
orchid and its pollinator will be disrupted. Consequently, because of its highly specialised
relationship with a single pollinator species, climate change may be the most serious threat to
the long-term future of O. sphegodes. Failure of pollination, even over a short sequence of
21
consecutive years, would be disastrous for this short-lived species, in which reproductive
success is already low, establishment from seed is precarious, and vegetative propagation is
uncommon (Hutchings 2010).
VIII. Floral and seed characters
(A) FLORAL BIOLOGY
The flowers of Ophrys species mimic receptive females of usually one pollinator species.
Males of this species are attracted primarily by the odour of the flower (Pouyanne 1917;
Kullenberg 1961; Paulus & Gack 1980). In O. sphegodes, the most conspicuous part of the
flower is the labellum (Fig. 7). This has a mean surface area of 91 mm2 (Schiestl & Cozzolino
2008), and resembles the abdomen of a spider. It emits compounds that attract males of the
solitary bee Andrena nigroaenea. As in other Ophrys species that are pollinated by Andrena
and males of the hymenopteran genus Colletes (Colletidae), the key pollinator attractants are
primarily alkenes, a class of unsaturated, long-chain hydrocarbons, which are produced by
sub-cuticular cells in the epidermis of the plant tissue (Samuels, Kunst & Jetter, 2008).
Alkanes and alkenes are the major constituents of the wax layer of all plant tissues, serving as
a waterproof barrier that helps regulate tissue water content (Riederer & Müller, 2006 and
references therein). They are also found in significant amounts on the surface of leaves, stems
and sometimes even sepals, albeit with different composition in each case. Detailed
comparisons of the different compounds emitted by female bees and by the flowers of O.
sphegodes showed that they are emitted in almost exactly the same proportions (Table 1)
(Schiestl et al. 1999).
There is wide variation between plants, both in flower form and labellum markings.
Populations of O sphegodes from Dorset included individuals with double lips and columns,
and with inverted flowers (Lang 1980). The latter variation is also found in Sussex
22
populations, as are flowers in which the labellum is concave instead of convex.
One
population in Sussex contained several plants in which the labellum and lateral sepals were
fused, the upper petals were greatly reduced, and the whole flower was smooth and green in
colour (Lang 1980).
The pollen grains of O. sphegodes are packed in two pollinia and do not separate
easily. Each pollinium is 315.0 ± 46.44 (SE) µm long and 151.1 ± 28.44 µm wide. Pollen
grains range in shape from monoaperturate to porate, tenuate-porate, tectate-perforate,
regulate-fossulate and irregularly scabrate (Aybeke 2007).
There is a wide consensus that O. sphegodes is mainly pollinated by Andrena
(Melandrena) nigroaenea; Apidae (Kullenberg 1961; Kullenberg & Bergström 1976;
Gumprecht 1977; Paulus 1998, 2006; Paulus & Gack 1986, 1990a,b,c, 1995, 1999; Vöth
1999; Hirth 2005; Schiestl 2005). The distribution range of Andrena nigroaenea in England
extends far beyond that of Ophrys sphegodes, and strongly overlaps with it. The primary
trigger of the flower’s sexual attraction for the bee is the floral bouquet emitted by
unpollinated flowers. During pseudocopulation, the pollinia detach at the base of the
caudicles, and become firmly glued to the head of a visiting male bee (cephalic
pseudocopulation - Paulus & Gack 1990a). Pollen is transferred to the stigmatic surface of
subsequently-visited flowers.
Several reports have documented other pollinators of Ophrys sphegodes. In western
France, Lorella, Mahé & Séité (2002) recorded that over a period of several years O.
sphegodes was pollinated by several species of Andrena (A. barbilabris, A. cineraria and A.
thoracica). Paulus & Gack (1990a, d) also mention A. bimaculata and A. limata as
pollinators, whereas Gumprecht (1977) has observed A. ovatula visiting flowers of O.
sphegodes. Kullenberg (1991) states that the digger wasp Argogorytes mystaceus, which is the
prime pollinator of the related O. insectifera, is capable of pollinating O. sphegodes as well.
23
Pedersen & Faurholdt (2007) mention that O. sphegodes subsp. sipontensis and subsp.
spruneri are pollinated by the xylocopid bee Xylocopa iris. These observations support
previous statements that indicate that the supposedly highly specific pseudocopulatory
pollination syndrome of Ophrys is demonstrably ‘leaky’, and support suggestions that the
genus may have been substantially over-divided at the species level by some authorities
(Devey et al. 2008). Breitkopf et al. (2013) sought evidence of early stages of evolutionary
divergence between populations of O. sphegodes by examining Adriatic populations that were
pollinated by Andrena nigroaenea and Tyrrhenian populations that were primarily pollinated
by A. bimaculata. The floral bouquets emitted by flowers from these populations were
significantly different, both in total composition and in the amounts of the components that
elicited sexual attraction in the pollinators. Despite clear differences in floral bouquets and in
pollinator attraction between populations from these regions, there was little genetic
differentiation between them, implying that they are at best at a very early stage of
divergence, and that a high level of gene flow between them is countering the tendency
towards speciation.
As in other sexually deceptive orchid species (Edens-Meier & Bernhardt 2014),
pollination in Ophrys sphegodes is limited by the availability of pollinators and by the
frequency of pollinator visits. The populations studied by Breitkopf et al. (2013) were only
visited by pollinators in the morning. Few instances of pollinium removal were observed
despite lengthy periods of observation. Ayasse et al. (2000) reported that only 4.9% of plants
of Ophrys sphegodes were visited by pollinators. They also stated that 67% of male Andrena
nigroaenea visited more than one flower in visited inflorescences. Nevertheless, high levels
of geitonogamous pollen transfer are avoided because pollination can only be achieved if the
pollinia carried by the bee from one flower have rotated forward to contact the stigmatic
24
surface of the next flower visited. Claessens & Kleynen (2011) stated that it takes 161.9 ±
10.1 seconds (n = 10) for the caudicles to complete the bending required for this to happen.
Although flowers may be subjected to frenzied attacks by Andrena nigroaenea, this
does not always result in transfer of pollinia to the bee (MJH, pers. obs.). The proportion of
flowers that produce ripe seed capsules is very low in many populations. Delpino (cited in
Darwin 1877) reported reproductive success, measured as capsules set, of 0.03%,
Vandewoestijne et al. (2009) recorded 38-52% reproductive success in populations of less
than 15 plants distributed at low density, but only 2 - 4% in denser populations of between 45
and 66 plants. Lang (1980) and Neiland & Wilcock (1998) report that no more than 20% of
plants bear seed. Gay & Philp (1999) reported many visits and pseudocopulation attempts by
Andrena nigroaenea at a colony of O. sphegodes in Kent, but only 25% of capsules produced
seed. In the study by Vandewoestijne et al. (2009), only 18.3% of plants produced one or
more capsules.
As flowers age, it is common in those that have not had their pollinia removed for the
pollinia to drop onto the stigmatic surface. Although it is probable that autogamy is achieved
by this means, there appear to be no data to substantiate the fact. Claessens & Kleynen (2011)
report that autogamous pollination occurs in other Ophrys species (O. bombyliflora, O.
holoserica, O. incubacea, O. lutea, O. scolopax). However, Vandewoestijne et al. (2009) state
that Ophrys sphegodes is allogamous. Experimental study would be valuable to determine
whether the species is obligately allogamous.
Vandewoestijne et al. (2009) observed higher reproductive success in plants with taller
inflorescences, in those with more flowers in the inflorescence, and in plants with more
distant nearest neighbours, and higher rates of seed set for flowers in the lower half of
inflorescences. There was no significant difference in the reproductive success of populations
studied in two successive years.
25
(B) HYBRIDS
Ophrys is a species-rich genus. Over 140 species have been described by Delforge (2006).
However, there is still ongoing and vigorous debate about the taxonomy of the genus and the
species within it (e.g. Pedersen & Faurholdt 2007; Devey et al. 2008). Part of the taxonomic
complexity is caused by the fact that gene flow across proposed species boundaries appears to
occur and that evidence of introgression is regularly found where sympatric populations of
different Ophrys species occur (Soliva & Widmer 2003). In the British Isles, for example, a
hybrid between O. sphegodes and O. insectifera, known as O. × hybrida Pokorny ap. Rchb. f.,
has been recorded in Kent on a number of occasions (Foley & Clarke 2005; Stace, Preston &
Pearman 2015). In addition, Summerhayes (1951) and Stace et al. (2015) described hybrids
between O. sphegodes and O. fuciflora in Kent. These hybrids have the greenish sepals of O.
sphegodes and a labellum with markings, and a tri-lobed labellum appendage, reminiscent of
O. fuciflora. The hybrid between these species, which is known as O. × obscura Beck (O. ×
aschersonii Nanteuil), is believed to arise in unusual years in which the flowering periods of
O. sphegodes and O. fuciflora overlap (Foley & Clarke 2005). Finally, Burton (1983) refers to
Hanbury & Marshall’s (1899) Flora of Kent, in which possible hybrids between O. sphegodes
and O. apifera in the London area have been reported. However, all of these reported hybrids
should be treated with caution as their precise taxonomic status has not been scientifically
established.
Hybridization involving O. sphegodes may be more widespread on the European
mainland, although there is the same need for caution in accepting the status of reported
hybrids. For example, the range of the morphologically and phenologically highly variable
Ophrys × arachnitiformis (a partly stabilized hybrid complex between O. sphegodes and O.
fuciflora that probably involves several subspecies of both species) extends from northern
26
Spain across southern France, Corsica and Sardinia to the western and southern parts of
mainland Italy and the islands along the Dalmatian coast (Fig. 8a; Pedersen & Faurholdt
2007). The range of the hybrid Ophrys × flavicans, a partly stabilised hybrid complex
between O. bertolonii and O. sphegodes, extends from Cataluña across the Balearic Islands,
southern France and mainland Italy to Dalmatia, Sicily and Malta (Fig. 8b; Pedersen &
Faurholdt 2007).
Within the Gargano National Park (Puglia, Italy), where about 30 different Ophrys
species occur, several hybrids involving O. sphegodes have been described (Rossini &
Quitadamo 2003), including hybrids with O. archipelagi (O. × trombettensis), O.
bertoloniiformis, O. biscutella (O. × boscoquartensis), O. cornuta (O. × calenae), O.
garganica (O. × biancoae), O. incubacea (O. × todaroana) and O. tenthredinifera (O. ×
etrusca). In France, hybrids between O. sphegodes and O. apifera, O. fuciflora, O.
occidentalis, O. araneola, O. aurelia, O. sulcata, O. insectifera and O. scolopax have been
described (Bournérias & Pratt 2005), although in most cases, just as with the purported
hybrids reported in the UK, morphological and/or molecular data confirming hybridization
are lacking. In Spain, hybrids between O. sphegodes and O. aveyronensis, O. bertolonii
subsp. balearica, O. bertolonii subsp. catalaunica, O. fusca, subsp. bilunulata, O. fusca
subsp. fusca, O. insectifera, O. lutea, O. scolopax, O. speculum subsp. speculum and O.
tenthredinifera have been reported (Castroviejo et al. 2005).
Notwithstanding the apparently frequent possibilities of hybridisation events involving
Ophrys sphegodes, there is considerable evidence for mechanisms that are effective in
achieving reproductive isolation between species within the genus Ophrys. These isolating
mechanisms act predominantly pre-zygotically, whereas post-zygotic barriers appear to be
generally very weak (Scopece et al. 2007). Given that orchids of the genus Ophrys attract
male insects by sexual mimicry (see section VIIIA), the key requirement for the achievement
27
of reproductive isolation is chemical mimicry of the sex pheromone emitted by the female of
the pollinating species (Schlüter & Schiestl 2008; Schiestl & Schlüter 2009). Floral isolation
is strongest when the complex bouquet of the flower’s scent differs between species, which in
turn results in strong pollinator specificity and a low probability of interspecific gene flow
occurring (but see Soliva et al. 2001; Soliva & Widmer 2003).
Detailed investigations of the main reproductive barriers acting between O. sphegodes
and the closely related O. exaltata have shown that they were due to attraction of two
different, highly specific pollinator species. Other reproductive barriers were virtually absent
(Xu et al. 2011). Investigations of the floral bouquet of the two orchid species revealed that
they differed mainly in the double-bond position of their major alkenes (Mant et al. 2005),
suggesting that genes underlying this difference may be the key determinants affecting
reproductive isolation between these species. More particularly, O. sphegodes emitted higher
concentrations of 9- and 12-alkenes, which function as attractants of Andrena nigroaenea,
whereas O. exaltata produced higher concentrations of 7-alkenes, which attract Colletes
cunicularius (Mant et al. 2005). Schlüter et al. (2011) further showed that stearoyl-acyl
carrier protein desaturases were responsible for the difference in 9- and 12-alkenes between
O. sphegodes and O. exaltata, thereby contributing to differential pollinator attraction and
thus to reproductive isolation between the species. Further investigations involving O.
sphegodes, O. exaltata, O. garganica and O. incubacea confirmed that in hybrid
combinations involving O. sphegodes, strong post-pollination barriers were lacking, but that
differences in pollinators (floral isolation) and, to a lesser extent, differences in flowering time
(temporal isolation), were the prime factors leading to effective reproductive isolation of O.
exaltata from O. sphegodes (Sedeek et al. 2014). Biochemical analyses of the floral bouquets
emitted by each of the four species clearly separated them into four distinct clusters (Fig. 9),
28
supporting the hypothesis that differences in floral odour chemistry underlie the observed
reproductive barriers (Sedeek et al. 2014).
(C) SEED PRODUCTION AND DISPERSAL
Although individual fruits can produce 5000-10000 seeds (Soliva & Widmer 2003), both
Summerhayes (1951) and Lang (1980) report that only 6-18% of flowers set seed in
populations of Ophrys sphegodes in England. Claessens & Kleynen (2011) report fruit set
ranging from 0 - 21.1% (mean: 8.7%) for a number of populations on the Continent,
confirming that only a small proportion of the flowers set fruit. Seeds have the potential to be
dispersed over large distances. Compared to other species in the genus Ophrys, the seeds of
Ophrys sphegodes are small (length: 0.34 ± 0.10 mm, width: 0.09 ± 0.02 mm) and show an
irregular thickening on the periclinal walls (Aybeke 2007). The testa cells are rectangular and
are on average 11.98 µm long. The embryo is dark brown and is 0.08 ± 0.02 (SE) mm long
and 0.05 ± 0.02 mm wide, leading to a seed volume/embryo volume ratio of 6.40. The
percentage air space is 84.37 (Aybeke 2007).
(D) VIABILITY OF SEEDS: GERMINATION
Mead & Bulard (1975) conducted germination experiments on seeds of Ophrys sphegodes
using different culture media in the absence of mycorrhizal symbionts. They found that seeds
germinated best in darkness and on a basal medium that was supplemented with sucrose,
casein hydrolysate and the vitamins thiamine, pyridoxine, nicotinic acid and biotin. White
fluorescent light almost completely inhibited germination. In these experiments, some
germination occurred within a month, and most germination had occurred within 2 months.
The presence of casein hydrolysate and the four vitamins significantly increased percentage
germination and produced vigorous protocorms that were thickly covered with hairs, many of
29
which were >3 mm in length. In the absence of casein hydrolysate, protocorms were small
and had very few, short (<1.5 mm) epidermal hairs. In general, mortality of transplanted
protocorms was high 7 - 12 months after sowing. Moreover, the course of development was
variable, with some protocorms producing one or several plantlets or new protocorms, each
developing individually, and others producing callus-like structures, from which one or two
protocorms emerged and developed into plantlets (Mead & Bulard 1975). Following this type
of development, vigorous plants with green leaves 4-7 cm long were obtained if casein
hydrolysate was added to the medium. These plants produced numerous roots and about 50%
of them produced tubers >1cm in diameter. When transplanted aseptically on fresh medium,
these tubers produced a new plantlet and a new tuber.
Hutchings (2010) found that annual recruitment of new plants showed a significant
positive correlation with the number of flowering plants of Ophrys sphegodes in the
population in each of the previous two years, suggesting that some seeds take as long as two
years from dispersal to germinate and emerge above ground. The number of new recruits in
each year was positively correlated (r = +0.38) with mean temperature over the previous year,
but more strongly correlated (r = +0.55) with temperature during the year preceding that.
Number of recruits was negatively correlated (r = -0.41) with number of frosts in the previous
winter.
IX. Herbivory and disease
(A) ANIMAL FEEDERS OR PARASITES
The animal feeders that cause most damage to Ophrys sphegodes are molluscs, rabbits and
sheep, all of which feed on the leaves. Damage can be substantial. Plants from which either
the majority of the leaves, or the leaf tips, have been removed are common. All of the
herbivores mentioned above may remove flower spikes. In the case of molluscs, the flower
30
spike is often severed at its base, but the stem and flowers are not consumed. Hutchings
(1987a) reported removal of a very high proportion of the flower spikes from a population of
O. sphegodes that was exposed to sheep grazing during the flowering period.
Alkanes and alkenes produced by the plant’s cuticular layer may limit herbivore
activity (Eigenbrode & Espelie 1995: Schiestl & Cozzolino 2008).
(B) & (C) PLANT PARASITES AND DISEASES
No data.
X. History
According to Clarke (1900) and Marren (1999), the first record of Ophrys sphegodes in the
UK is dated 1650. How (1650) stated that the species was discovered by Dr Bowle “Upon an
old stone pit ground….hard by Walcot a mile from Barnack”. This site was probably at
Barnack Hills and Holes, Northamptonshire. Marren (1999) also mentions Gerard (1633)
writing of “a wasp orchid” with flowers “the colour of a dry oken leafe”, and speculates that
this description is also of O. sphegodes. Other early references to the species are its first
records in Cambridgeshire in 1663 (Ray 1663), Breckland in 1773 (Trist 1979) and in Sussex
in 1834 (Wolley-Dod 1937), a single record for Bedfordshire in about 1800 (Dony 1976), and
a reference to it being native to Surrey in 1670 (Lousley 1976).
XI. Conservation
In comparison with its distribution range prior to 1930, the most recent available information
suggests that there has been a contraction of at least 60% in the range of Ophrys sphegodes in
the UK. O. sphegodes is listed as a Schedule 8 species under the Wildlife and Countryside
Act of 1981. Although formerly classified as Near Threatened in Great Britain (Wigginton
31
1999), it is now regarded as of Least Concern (Cheffings & Farrell 2005). On the European
mainland, the species is widespread, especially in the Mediterranean region, and not
considered to be threatened.
The main causes of loss of populations of O. sphegodes in the UK include ploughing
of grassland, in some cases followed by re-seeding and fertilisation, and either cessation of
grazing or the introduction of inappropriate grazing regimes. The inability of O. sphegodes to
compete successfully for light against taller species with leaves located above ground level
commonly leads to its rapid loss from rank vegetation. Perring & Farrell (1983) expressed the
opinion that much of the decline in the species’ range that occurred in the twentieth century,
or even earlier, preceded the pre- and post-war ploughing of large areas of chalk and
limestone grassland, and that the attractiveness of the flowers, and the accessibility of many
of the sites where the species occurred, were also significant contributory factors. They also
suggested that some of the largest populations of O. sphegodes in the UK, especially those in
Dorset, and the habitats in which they were located, were suffering serious damage from
trampling. Byfield (1983) listed re-seeding of ploughed grassland habitats, cessation of
grazing and invasion of coarse species, including Brachypodium pinnatum, among the causes
of the species’ decline.
A long-term study of a population of Ophrys sphegodes in Sussex (Hutchings
1987a,b; Waite & Hutchings 1991) showed that winter grazing by cattle caused a rapid loss of
plants, with the number of deaths exceeding recruitment every year. The main causes were (i)
the manner in which cattle graze, which causes whole plants, including their underground
parts, to be wrenched out of the substrate, (ii) the mechanical damage suffered by fleshy
underground plant parts such as tubers, which is caused by the heavy impact of cattle on thin
rendzina soils, and (iii) the tendency of cattle to cause severe soil slippage on hill slopes,
especially in wet weather. This dislodges tubers and destroys the intimate connections
32
between the plant’s roots, its mycorrhizal associates, and the substrate. Detailed analysis of
recruitment and death of plants in the population demonstrated that grazing of the site by
cattle for more than a few consecutive years would push the population towards extinction
(Hutchings 1987a, 2010; Waite & Hutchings 1991).
In comparison, grazing by sheep, which is the traditional form of management on
many of the chalk downland habitats in which O. sphegodes has been recorded, causes much
less mechanical damage to the species and its substrate. Sheep nibble leaves, including those
of O. sphegodes, very close to the soil surface, leaving a short turf, in which competition for
light is minimal, and there is a high proportion of bare ground. Crucially, sheep leave tubers
intact and therefore able to regenerate leaves and flowering stems. Hutchings (2010)
demonstrated that sheep-grazing throughout the year apart from the three months during
which plants flowered and set seed (approximately May – July), reversed the decline in the
population. Recruitment of new individuals considerably exceeded deaths in many years of
the study, such that the population rapidly recovered its original numbers and then continued
to increase in size (Waite & Hutchings 1991; Hutchings 2010). It is vital to withdraw sheep
grazing during the months of flowering and seed setting, as sheep graze the flower spikes of
O. sphegodes. The short life span of the species, combined with a low probability of
successful establishment from seed, and the near-absence of vegetative propagation, makes it
imperative that, if possible, such a management prescription is rigidly followed to create
conditions that are conducive to the production of as much seed as possible in every year.
Many of the habitats in which O. sphegodes can thrive are transient in nature, and the
species possesses many weedy characteristics, including a short life-span and the potential for
producing large numbers of very small seeds. These features also make it essential that at
least some bare ground is maintained in which establishment from seed can occur. However,
even with all these management precautions in place, several years may pass before an
33
increase in the numbers of emergent plants is apparent (Hutchings 2010), because newly
germinated plants potentially spend from one to several years in a subterranean phase before
they produce any leaves or flowers.
Byfield (1983) suggested that other threats to Ophrys sphegodes include aerial crop
and herbicide spraying, the illegal collection of whole plants and plant parts, trampling, and
even, in the case of plants located near cliff edges, coastal erosion. Although these all
represent realistic hazards to conservation of the species, Byfield estimated that 76% of the O.
sphegodes plants in Dorset were located in sites that were already afforded at least some
measure of formal protection, and that this was also true for all but one of all the British
populations of more than 1000 plants.
Further threats to Ophrys sphegodes in the UK can be predicted as a consequence of
its reliance for pollination on a single insect species, Andrena nigroaenea. A. nigroaenea is
widespread and relatively common in the UK. Nevertheless, in common with other orchid
species that rely on sexual deception for pollination, Ophrys sphegodes achieves very low
reproductive success, even when it occurs in large populations. It is likely that very small
populations of the orchid, and newly-established populations, will be unable to reliably attract
A. nigroaenea to the sites they occupy, and therefore will regularly fail to produce seeds.
Recent analyses of the responses of Ophrys sphegodes and Andrena nigroaenea to
temperature suggest that climate warming could also be a major threat to the survival of the
orchid in the UK. Flowering time in O. sphegodes has shown a dramatic advance in recent
decades (Hutchings 2010). Warmer springs are at least partially responsible for this (Robbirt
et al. 2011). There are significant differences between the effects of warmer spring
temperature on flowering time in the orchid and on the dates on which both the male and
female bees of A. nigroaenea emerge from their winter nesting sites (Robbirt et al. 2014). The
threat is that as warmer springs become more frequent, orchid flowering is less certain to
34
precede emergence of the female bees. Pollination of O. sphegodes by male A. nigroaenea
depends on there being few female bees on the wing to distract male bees from attempting
pseudocopulation with the orchid flowers. If warmer springs reduce the number of attempted
pseudocopulation events, or reduce the frequency of years in which pseudocopulation occurs,
seed production will be at least reduced, and may fail completely in some years. This in turn
will lower or even prevent future recruitment of plants into populations. As O. sphegodes has
such a short life span, it will not take many years for the extinction of populations that are not
recruiting new plants regularly. This may be the biggest long-term threat to the conservation
of this species.
On a more positive note, the weedy characteristics of Ophrys sphegodes allow the
possibility that, given suitable habitat conditions and an influx of seeds, the establishment of
new populations can occur, as recent expansion of the species’ range attests. Indeed, it is
possible for new populations to reach very high numbers very quickly. For example, a
population discovered at Samphire Hoe, Kent, in 1998, has contained several thousand
flowering plants every year for well over a decade. Populations of this size are a precious
resource that should be managed with the utmost care to ensure the continued survival of O.
sphegodes in the British Isles.
Acknowledgments
We thank Tony Davy and five reviewers for their constructive comments on previous drafts
of this manuscript. This research was supported by the European Research Council (ERC
starting grant 260601 – MYCASOR).
35
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44
Table 1 Electrophysiologically active compounds in cuticle extracts of virgin Andrena
nigroaenea females and labellum extracts of Ophrys sphegodes flowers (data from Schiestl et
al. 1999).
Compound
Abundance ± SE (%)
Andrena
Ophrys
Heneicosane
1.6 ± 0.5
1.8 ± 0.3
Docosane
0.6 ± 0.1
0.5 ± 0.1
Tricosane
28.7 ± 2.4
30.6 ± 1.8
Tetracosane
2.0 ± 0.2
3.1 ± 0.2
(Z)-9-pentacosene
3.4 ± 1.8
0.6 ± 0.1
Pentacosene
34.9 ± 2.2
20.2 ± 1.3
Hexacosene
1.6 ± 0.1
2.1 ± 0.2
(Z)-12 + (Z)-11-heptacosene
0.7 ± 0.3
6.0 ± 0.8
(Z)-9-heptacosene
5.1 ± 1.6
7.6 ± 1.0
Heptacosane
11.2 ± 1.1
11.5 ± 1.5
(Z)-12 + (Z)-11-nonacosene
3.7 ± 1.4
6.7 ± 1.0
(Z)-9-nonacosene
6.6 ± 0.4
9.4 ± 1.2
45
Fig. 1. Distribution of Ophrys sphegodes in the British Isles. Each dot represents at least one
record in a 10-km square of the national grid. Native: (●) 1970 onwards, (○) pre-1970, (×)
non-native pre-1970. Mapped by Colin Harrower, using Dr. A. Morton’s DMAP software,
Biological Records Centre, Centre for Ecology and Hydrology, Wallingford, mainly from the
data collected by the members of the Botanical Society of Britain and Ireland.
46
Fig. 2. European distribution of Ophrys sphegodes. Reproduced from Pedersen & Faurholdt
(2007) Ophrys. The bee orchids of Europe.
47
Fig. 3. The spatial distribution of emergent Ophrys sphegodes plants in a 20 × 20-m plot at
Castle Hill National Nature Reserve in Sussex (M. J. Hutchings, unpublished data). The data
are from 1993, in which the number of emergent plants was at its highest (n = 703).
48
Fig. 4. Morphology of Ophrys sphegodes (from Ross-Craig 1971). (a) Plant, (b) Flower, (c)
column and lip, (d) column in front view, (e) pollinia.
49
Time to flowering, in days from April 1
100
Herbarium data
Field data
80
60
40
20
0
7
8
9
10
Mean spring temperature (oC)
Fig. 5. Relationship between flowering date in Ophrys sphegodes (expressed as days after 1
April) and mean spring temperature (March–May). Closed symbols: herbarium records from
1855 to 1958 (y = 99.8 –5.66x, r2 = 0.134, P = 0.0016, n = 72). Open symbols: field data
from 1975 to 2006 (y = 97.7-5.68x, r2 = 0.586, P < 0.0001, n = 25). From Robbirt et al.
(2011).
50
160
(a)
140
120
100
80
Time to flight from 1 March (Days)
60
40
20
0
3
4
5
6
7
8
9
Mean (February to April) Temperature (°C)
160
(b)
140
120
100
80
60
40
20
0
7
8
9
10
Mean (March to May) Temperature (°C)
Fig. 6. Relationship between flight date of Andrena nigroaenea (days after 1 March) and
mean spring temperature from museum specimens. (a) males vs. mean February – April
temperature, 1893-2004 (y = 122.8 – 9.168x, r2 = 0.157, P < 0.0001, n = 208); (b) females vs.
mean March – May temperature, 1900-2007 (y = 202.3 – 15.64x, r2 = 0.167, P < 0.0001, n =
149). From Robbirt et al. (2014).
51
Fig. 7. Detailed picture of the flower of Ophrys sphegodes, which resembles the abdomen of a
spider (hence the English name for the species) and emits compounds that attract males of the
solitary bee Andrena nigroaenea.
52
Fig. 8a. Distribution of Ophrys × arachnitiformis (a partly stabilized hybrid complex between
O. sphegodes and O. fuciflora that probably involves several subspecies of both species) in
Europe. Reproduced from Pedersen & Faurholdt (2007).
53
Fig. 8b. European distribution of Ophrys sphegodes (black), O. bertolonii (blue) and their
hybrid (O. × flavicans) (red). Reproduced from Pedersen & Faurholdt (2007).
54
Fig. 9. Analysis of the differences in floral odour between four closely related Ophrys species.
Linear discriminant analysis (LDA) based on all identified compounds in the floral bouquet of
Ophrys exaltata (Exa), O. garganica (Gar), O. incubacea (Inc) and O. sphegodes (Sph)
separates the four species into four distinct clusters. Ctr. denotes the group centroid for each
species (from Sedeek et al. 2014).
55
Supporting Information
Table 1 Detailed description of the different subspecies of Ophrys sphegodes recognized by
Pedersen and Faurholdt (2007).
1. Ophrys sphegodes subsp. sphegodes. Plant slender, (10-)15-40(-60) cm tall with (2-)3-9(15) flowers in a lax spike. Sepals green to white, 8-14 × (2-)3-7 mm. Petals yellowish to
olive-green, 4-10(-11) × 2-4.5 mm. Lip with medium brown ground colour, occasionally
with a c. 1 mm-wide yellow margin, entire with rounded or truncate base, 9.5-16 × 9-18
mm, longer than the dorsal sepal, margin of the basal part more or less hirsute, margin of
the distal part velvety to subglabrous; front edge emarginated around a short terminal
point; protuberances almost absent to obliquely conical; mirror H-shaped. Eye-like knobs
of the column dark.
2. Ophrys sphegodes subsp. litigiosa. Plant robust, (10-)15-45 cm tall with 2-10(-15) flowers
in a lax to dense spike. Sepals (yellowish) green to white, 7-12 × 4-7 mm. Petals olivegreen to ochre-yellow, 5-8 × 2-4.5 mm. Lip with medium brown ground colour, often with
an up to 2 mm-wide, yellow to yellowish green margin, entire with rounded to truncate
base, 6.5-9.5 × 7.5-11.5 mm, shorter than the dorsal sepal, margin of the basal part more
or less hirsute, margin of the distal part velvety to subglabrous; front edge emarginated
around a short terminal point; protuberances absent or only weakly developed; mirror Hshaped to more complicated or marbled. Eye-like knobs of the column dark.
3. Ophrys sphegodes subsp. atrata. Plant relatively slender, 20-40(-60) cm tall with 2-8
flowers in a lax spike. Sepals green, 10-15.5 × 4-7.5 mm. Petals (olive-)green to muddy
ochre-yellow, 6.5-9 × 2.5-5 mm. Lip with dark brown to blackish brown ground colour,
entire with rounded to truncate base, (8-)10-14 × (8-)10-14.5 mm, shorter than the dorsal
56
sepal, with a thick, marginal, hirsute border of strikingly long hairs all around; front edge
emarginated around a short terminal point; protuberances obliquely conical; mirror Hshaped. Eye-like knobs of the column dark.
4. Ophrys sphegodes subsp. passionis. Plant relatively slender, 20-40(-45) cm tall with 4-8
flowers in a lax spike. Sepals green, 10-14 × 4-7 mm. Petals olive-green to ochre-yellow,
8-11 × 3.5-7 mm, nearly as wide as the sepals. Lip with dark brown ground colour, often
with a light reddish brown margin, entire with rounded to truncate base, 8-14 × 13-17 mm,
approximately as long as the dorsal sepal, the basal part more or less hirsute along the
margin, the distal part velvety to subglabrous along the margin; front edge emarginated
around a short terminal point; protuberances absent or weakly developed; mirror basically
H-shaped, but with two additional short arms from the base. Eye-like knobs of the column
dark.
5. Ophrys sphegodes subsp. sipontensis. Plant relatively slender, (15-)20-50(-60) cm tall
with 2-8 flowers in a lax spike. Sepals purplish violet to white, 10-15 × 4-7 mm. Petals
bright purplish violet to ruby, 7-12 × 3-7 mm, usually almost as wide as the sepals. Lip
with dark brown to blackish brown ground colour, entire with rounded to truncate base,
10-15 × 10-17 mm, approximately as long as the dorsal sepal, the basal part hirsute along
the margin, front edge emarginated around a short terminal point; protuberances absent or
weakly developed; mirror H-shaped or consisting of two parallel longitudinal bands. Eyelike knobs of the column dark.
6. Ophrys sphegodes subsp. spruneri. Plant slender to relatively robust, (10-)15-40(-50) cm
tall with 2-8 flowers in a lax (to dense) spike. Sepals purplish violet to white, the lateral
ones usually distinctly bicoloured (white/purplish violet) with the mid vein constituting a
boundary, 10-16.5 × (3-)5-6.5 mm. Petals bright purplish to ruby, (5-)8-11 × 2-4 mm,
approximately half as wide as the sepals. Lip with blackish brown ground colour, often
57
with a paler margin, three-lobed with rounded to truncate base, 10-15 × (10-)12-18 mm,
approximately as long as the dorsal sepal, the basal part velvety along the margin, the
distal part (sub)glabrous along the margin; front edge rounded with a short terminal point;
protuberances absent or weakly developed; mirror H-shaped or consisting of two lateral
bands. Eye-like knobs of the column dark.
7. Ophrys sphegodes subsp. helenae. Plant robust, 15-40 cm tall with 2-8 flowers in a dense
to relatively lax spike. Sepals pale green to yellowish green, often more or less suffused
with violet, 11-15.5 × 5-8 mm. Petals pale-green to ochre-yellow, 6-13 × 2-4 mm,
approximately half as wide as the sepals. Lip with purplish brown ground colour, entire
with rounded to truncate base, 11-18 × 15-23 mm, usually longer than the dorsal sepal, the
basal part shortly velvety to subglabrous, the distal part (sub)glabrous along the margin;
front edge emarginated with a short terminal point; protuberances absent or only weakly
developed; mirror absent or very obscure. Eye-like knobs of the column strongly reduced,
dark.
8. Ophrys sphegodes subsp. epirotica. Plant relatively slender, (15-)20-45 cm tall with 4-9(15) flowers in a lax to relatively dense spike. Sepals yellowish green to olive-green,
sometimes with purplish brown marking, 10-14 × 4-7 mm. Petals bright yellowish green,
6-9 × 2.5-4 mm, approximately half as wide as the sepals. Lip with light brown to
blackish brown ground colour, with a broad, reddish brown to yellow or yellowish green
margin, entire with rounded to truncate base, 10-14 × 10-17 mm, approximately as long as
the dorsal sepal, the basal part shortly velvety to subglabrous along the margin, the distal
part (sub)glabrous along the margin; front edge rounded to shortly acuminate with a short
terminal point; protuberances absent or weakly developed; mirror H-shaped or consisting
of two parallel longitudinal bands. Stigmatic cavity (almost) uniformly brown. Eye-like
knobs of the column greyish blue.
58
9. Ophrys sphegodes subsp. aesculapii. Plant relatively robust, 15-40 cm tall with 3-12
flowers in a relatively dense (to lax) spike. Sepals pale green to yellowish green, often
with purplish brown markings, 9-14 × 3.5-5.5 mm. Petals yellowish green to olive-green,
5-8.5 × 2-3.5 mm, approximately half as wide as the sepals. Lip with (dark) brown to
blackish brown ground colour, with a broad, yellow to reddish brown margin, entire with
rounded to truncate base, 9-12 × 10-14 mm, approximately as long as the dorsal sepal, the
basal part shortly velvety to subglabrous along the margin, the distal part (sub)glabrous
along the margin; front edge rounded to shortly acuminate with a short terminal point;
protuberances
weakly developed; mirror
H-shaped. Stigmatic
cavity speckled
green/brown. Eye-like knobs of the column pale (yellowish) green.
10. Ophrys sphegodes subsp. mammosa. Plant relatively slender, (15-)20-60(-70) cm tall with
2-12(-18) flowers in a lax spike. Sepals olive-green to pale green and more or less
suffused with brownish violet, the lateral ones usually distinctly bicoloured (pale
green/purplish brown) with the mid vein constituting a boundary, 9-19 × 4-9 mm. Petals
yellowish green to olive-green or dull purplish brown, 5-13 × 1.5-4 mm, approximately
half as wide as the sepals. Lip with reddish brown to blackish brown ground colour, now
and then with a yellow margin, entire with rounded to truncate base, 9-18(-20) × 9-20(-22)
mm, approximately as long as the dorsal sepal, the basal part hirsute to velvety along the
margin, the distal part velvety to subglabrous along the margin; front edge rounded to
acuminate with a short terminal point; protuberances obliquely conical; mirror H-shaped
or consisting of two parallel longitudinal bands. Eye-like knobs of the column dark.
11. Ophrys sphegodes subsp. cretensis. Plant relatively slender, 20-50 cm tall with 6-11
flowers in a lax spike. Sepals pale green, or the lateral ones distinctly bicoloured (pale
green/pale purplish brown) with the mid-vein constituting a boundary, 8-11 × 4-5 mm.
Petals yellowish green to olive-green, 5-9 × 1.5-2.5 mm, approximately half as wide as the
59
sepals. Lip with brown ground colour, now and then with a narrow light brown to yellow
margin, entire with rounded to truncate base, 5-9 × 7-10 mm, shorter than the dorsal sepal,
the basal part shortly velvety to subglabrous, the distal part (sub)glabrous; front edge
rounded to shortly acuminate with a short terminal point; protuberances weakly developed
to obliquely conical; mirror H-shaped. Eye-like knobs of the column dark.
12. Ophrys sphegodes subsp. gortynia. Plant relatively slender, 15-35 cm tall with 3-6 flowers
in a lax spike. Sepals olive-green to pale green, rarely whitish, occasionally faintly
suffused with violet towards the base, 8-11 × 4-6 mm. Petals pale green to yellowish
green, 6-8 × 2.5-4 mm, approximately half as wide as the sepals. Lip with dark brown
ground colour, occasionally with a narrow light brown to yellow margin, entire with
wedge-shaped base, (8-)9-14 × 9-14 mm, usually longer than the dorsal sepal, the basal
(and to less extent the distal) part velvety along the margin; front edge rounded with a
short terminal point; protuberances weakly developed to obliquely conical; mirror Hshaped or consisting of two parallel longitudinal bands. Eye-like knobs of the column
dark.
60
Table S2 Overview of described subspecies of Ophrys sphegodes and their associated distribution area (data from Landwehr (1977) and
Delforge (2006)).
Subspecies
Species
Distribution area
O. sphegodes ssp. aesculapii (Renz) Sóo
Ophrys aesculapii Renz
Greece
O. sphegodes ssp. amanensis Nelson
Ophrys amanensis (E. Nelson ex Renz &
Turkey
Taubenheim) P. Delforge
O. sphegodes ssp. arachnitiformis
Ophrys arachnitiformis Grenier & Philippe
Spain, France, Italy
Ophrys argensonensis Guérin & Merlet
France
Ophrys incubacea Bianca ex Tod.
Spain, the Balearic Islands, southern France, Italy,
(Grenier & Philippe) Sundermann
O. sphegodes ssp. argensonensis (Guérin
& Merlet) Kreutz
O. sphegodes ssp. atrata (Lindl.) E.
Mayer
Corsica, Sardinia, former Yugoslavia, Albania and
Corfu
O. sphegodes ssp. aveyronensis J.J.
Ophrys aveyronensis (J.J. Wood) P.
Wood
Delforge
O. sphegodes ssp. caucasica (Woronow
Ophrys caucasica Woronow ex Grossheim
France
Anatolia, Russia
61
ex Grossheim) Sóo
O. sphegodes ssp. cephalonica B.
Ophrys cephalonica (B. Baumann & H.
Baumann & H. Baumann
Baumann) J. Devillers-Terschuren & P.
Greece
Devillers
O. sphegodes ssp. cretensis H. Baumann
Ophrys cretensis (H. Baumann & Kunkele)
& Kunkele
H.F. Paulus
O. sphegodes ssp. epirotica (Renz) Gölz
Ophrys epirotica (Renz) J. Devillers-
& H.R. Reinhard
Terschuren & P. Devillers
O. sphegodes ssp. garganica Nelson
O. passionis Sennen var. garganica (E.
Crete
Albania, Greece
Spain and Italy
Nelson ex O. Danesh & E. Danesh) P.
Delforge
O. sphegodes ssp. gortynia H. Baumann
Ophrys gortynia (H. Baumann & Künkele)
& Künkele
H.F. Paulus
O. sphegodes ssp. grammica (B. Willing
Ophrys grammica (B. Willing & E. Willing)
& E. Willing) Kreutz
J. Devillers-Terschuren & P. Devillers
O. sphegodes ssp. hebes Kalopissis
Ophrys hebes (Kalopissis) B. Willing & E.
Crete, Greece
Albania, Greece
Albania, Greece, former Yugoslavia
62
Willing
O. sphegodes ssp. helenae (Renz) Sóo
Ophrys helenae Renz
O. sphegodes ssp. herae (Hirth & Spaeth) Ophrys herae Hirth & Spaeth
Albania, Greece
Albania, Crete, Cyprus, Greece
Kreutz
O. sphegodes ssp. integra (Moggridge &
Ophrys arachnitiformis Grenier & Philippe
France, Spain, Italy
Ophrys araneola Reichenbach
France, northern Spain, south Germany,
Rchb. fil.) H. Baumann & Künkele
O. sphegodes ssp. litigiosa (Camus)
Becherer
O. sphegodes ssp. lunulata (Parlatore)
Switzerland, Italy, former Yugoslavia and Crete
Ophrys lunulata Parlatore
Sicily
O. sphegodes ssp. majellensis Daiss
Ophrys majellensis (Daiss) P. Delforge
Italy
O. sphegodes ssp. mammosa (Desf.) Sóo
Ophrys mammosa Desfontaines
Greece, Turkey, Cyprus, Lebanon and Crimea
O. sphegodes ssp. massiliensis (Viglione
Ophrys massiliensis Viglione & Véla
France, Italy
Ophrys melitensis (Salkowski) J. Devillers-
Malta
Sundermann
& Véla) Kreutz
O. sphegodes ssp. melitensis Salkowski
Terschuren & P. Devillers
63
O. sphegodes ssp. montenegrina H.
Ophrys montenegrina (H. Baumann &
Baumann & Künkele
Künkele) J. Devillers-Terschuren & P.
Former Yugoslavia
Devillers
O. sphegodes ssp. panormitana (Todaro)
Ophrys panormitana (Todaro) Sóo
Sicily, Italy
Ophrys passionis Sennen
France, Spain, Italy
Ophrys panormitana (Todaro) Sóo var.
Corsica, Sardinia
Kreutz
O. sphegodes ssp. passionis (Sennen)
Sanz & Nuet
O. sphegodes ssp. praecox Corrias
praecox (Corrias) P. Delforge
O. sphegodes ssp. provincialis H.
Ophrys provincialis (H. Baumann &
France, Italy, Spain
Baumann & Künkele
Künkele) H.F. Paulus
O. sphegodes ssp. sicula E. Nelson
Ophrys exaltata Tenore
Sicily and Italy
O. sphegodes ssp. sintenisii
Ophrys transhyrcana Czernakowska
Anatolia, Israel, Jordan, Lebanon, Syria, Russia
(Czernakowska) Buttler
O. sphegodes spp. sipontensis Gumprecht Ophrys sipontensis R Lorenz & Gembardt
Italy
O. sphegodes ssp. spruneri (Nyman)
Crete, Greece
Ophrys spruneri Nyman
64
Nelson
O. sphegodes ssp. tarquinia (P. Delforge)
Ophrys tarquinia P. Delforge
Italy
Ophrys mammosa Desfontaines
Albania, Anatolia, Bulgaria, Crete, Cyprus, Greece,
Kreutz
O. sphegodes ssp. taurica (Desfontaines)
Sóo
Israel, Jordan, former Yugoslavia, Russia, Turkey
O. sphegodes ssp. transhyrcana
O. sphegodes ssp. zeusii (Hirth) Kreutz
Ophrys negadensis G. Thiele & W. Thiele
Albania, Greece
65
Graphical abstract for online TOC
Ophrys sphegodes (early spider orchid) is a terrestrial orchid species with a narrow
distribution range in the British Isles. It grows mainly in full sunlight, rarely under shade, and
on nutrient-poor, calcareous substrates. Habitat destruction and conversion of calcareous
grasslands to arable land have led to a substantial decline of the species in the 20th century.
66