P1. Syst. Evol.

169, 177-207 (1990)

slant
stematics
and
Evolution
by Springer-Verlag 1990
Pollination of Ophrys (Orchidaceae) in Cyprus
H. F. PAULUS and C. GACK
Received October 28, 1988
Key words: Angiosperms, Orchidaceae, Ophrys; bees, Melecta, Eucera, Anthophora, An-
drena. - Pollination, pseudocopulation. - Flora of Cyprus.
Abstract: In the southern part of Cyprus the pollinator- Ophrys (Orchidaceae) rela-
tionships and its specifity have been investigated from the end of February until the middle
of March 1986. 12 Ophrys spp. were found. To date, only a single pollinator reference has
been reported from this island. We found the following pollinators: Melecta tuberculata
(Ophrys kotschyi), Eucera dimidiata (Ophrys flavomarginata), Eucera gaullei (Ophrys um-
bilicata), Eucera paulusi (Ophrys bornmuelleri), Anthophora erschowi (Ophrys elegans), An-
drena torda (Ophrys sicula = O. lutea subsp, minor), Andrena cinereophila (Ophrys fusca,
small-flowered), Andrena flavipes (Ophrys israelitica), Andrena morio (Ophrys iricolor and
Ophrys transhyrcana), Andrena bimaculata (Ophrys sphegodes aggr., probably formerly
confused with O. transhyrcana). Most interestingly, it could be verified that O. flavomar-
ginata/O, umbilicata, O. bornmuelleri/O, levantina and O. transhyrcana/O, sphegodes aggr.
(possibly O. sintenisii) are different biospecies. This is a result of genetic isolation due to
varying pollinators, and of differences in flower morphology.
Flowers of the European orchid genus Ophrys imitate important sexual releasing
signals of hymenopterous females that stimulate the males to attempt copulation
with these flowers. This phenomenon was discovered by POUYANNE (1917) and
later treated by KULLEN~ERG (1961). Several new findings have been published by
KULLENBERG (1973), KULLENBERG & BERGSTROM (1976), KULLENBERG & al.
(1984), PAULUS & GACK (1980, 1981, 1983a, b, 1986), VOTH (1984, 1985), and
VOGEL (1976).
The labellum of the Ophrys flower produces several hundred chemical com-
pounds which attract males by imitating the effect of the sexual pheromones pro-
duced by the pollinator female. Other important signals of the flower for allurement
or orientation are optical and tactile. The allurement is usually highly species-
specific, such that one Ophrys species is only attractive for males of a single bee
species and in some cases for one or several closely related species. This specifity
is derived from a specific chemical compound mixture exhibited by each Ophrys
species. Only some of the chemical compounds are identical with those found in
the imitated pollinator female (BORO-KARLSON 1985, for further literature). In-
formation regarding the attractive efficiency of the optical or the tactile signals of
the flower is scant. In some cases the overall similarity of the Ophrys flower to the
178 H. F. PAULUS 8 C. GACK:
Table 1. List of the known pollinators from Ophrys spp. in Cyprus
Ophrys species Pollinator Family/tribus
O. kotschyi FLEISCHMANN
& So6 (1926)
O. flavomarginata (RENz)
BAUMANN 8 KONKELE (1981)
O. umbilicata DESV. (1807)
O. bornmuelleri SCHULZE (1898)
O. elegans (RENz)
BAUMANN 8 Kf2NKELE (1981)
O. sicula TINEO (= minor)
O.fusca LINK (1800) (very small-
flowered species)
O. israelitica
BAUMANN 8Z; KI)NKELE (1988)
O. iricolor DESF. (1807)
O. transhyrcana
CZERNIAKOVSKA (1923)
O. sphegodes aggr. (sintenisii
FLEISCHMANN & BORN-
Mr?LEER 19237)
O. mammosa DESF. (1807)
O. levantina G6Lz &
REINHARD (1985)
Melecta tuberculata LIEFTINCK
Eucera (s. str.) dimidiata BRULLE
Eucera (Atopeueera) gaullei VACHAL
Eucera ( Pteneucera) paulusi TKALK~
Anthophora erschowi F~DTSCH~NKO
Andrena ( Cordandrena) torda WARNCKE
Andrena ( Chlorandrena) cinereophila
WARNCKE
Andrena ( Zonandrena) flaripes Pz.
Andrena (Melandrena) morio BR.
Andrena (MeIandrena) morio BR.
Andrena ( Plastandrena)
bimaculata (KIRBY)
supposed pollinator:
Andrena (Melanapis) fuscosa ERICHS.
(Cyprus?)
supposed pollinator:
Eucera spec.
Anthophoridae,
Melectini
Anthophoridae,
Eucerini
Anthophoridae ,
Eucerini
Anthophoridae,
Eucerini
Anthophoridae,
Anthophorini
Andrenidae
Andrenidae
Andrenidae
Andrenidae
Andrenidae
Andrenidae
Andrenidae
Anthophoridae,
Eueerini
pollinator female is very impressive [e.g., Ophrys vernixia ( = O. speculum), PAULUS
1978]. In most cases, however, the optical mimicry must evidently be limited to
certain releasing signals. The most i mport ant tactile signal is the orientation of the
hairs on the labellum which determines the position of the pollinator thus leading
to either abdomen pollination (in Ophrys fusca-lutea aggregation) or head polli-
nat i on (in all other Ophrys spp.) (KULLENBERQ 1961).
Ophrys flowers never produce nectar and are exclusively pollinated by hyme-
nopterous males (solitary bees, in some cases scoliids or sphecids). The flowers are
never attractive to females, which is a result of the mode of attraction employed.
The Ophrys flower is a sexual deception flower and the pollination mechani sm has
been called "pseudocopul at i on". Ophrys is the only example of this occurring in
the European flora, however, it has developed convergently in several Australian
Pollination of Ophrys
Table 2. Ophrys spp. occurring in Cyprus and their further distribution
179
Ophrys species Floral element Distribution
Anatolia/ E.
Middle East Europe
W,
Europe
O. kotschyi Cyprus endemic
O. elegans E. Medit. +
O. flavomarginata E. Medit. +
O. sphegodes
aggr. (sintenisii?) E. Medit. +
O. bornmueIleri E. Medit. +
O. levantina E. Medit. +
O. transhyrcana E. Medit. +
O. israelitica E. Medit. +
O. umbilicata/attica E. Medit. +
O. iricolor E. Medit. +
O. mammosa E. Medit. +
O. (cinereophila)fusca E. Medit. +
O. sicula/minor Medit. +
O. apifera Medit. +
O. holoserica Medit. +
+
+ (Sardinia?)
+
+
+ +
+ +
+ +
and S. Amer i can orchi ds (VAN DER P1JL DODSON 1969; STOUTAMIRE 1975, 1983;
BEARDSELL & BERNHARDT 1982).
Sexual decept i on flowers use t he existing sexual behavi oural pat t er ns of t he
pol l i nat or species. Dur i ng their evol ut i on t hey acqui red signals whi ch mi mi c t hose
of t he female and release mal e sexual behavi our, l eadi ng to successful pol l i nat i on.
This pol l i nat i on mechani sm, t herefore, is not a consequence of co-evol ut i on (in t he
sense of PAULUS 1978, 1988 a; JANZEN 1980), but represent s a compl et el y one-si ded
evol ut i on of t he flower in acqui ri ng adapt at i ons l eadi ng to t he pol l i nat i on mech-
ani sm of ps eudocopul at i on. I n this sense t he flowers parasitize t he instinctive sexual
behavi our al pat t er ns of t he decei ved males (VOGEL 1975).
The rel at i on bet ween t he Ophrys spp. and t hei r pol l i nat ors is very specific and
has been t est ed in numer ous cases in t he field (PAULUS & GACK 1981, 1983 b, 1986;
VOTH 1984, 1985) (Table 1). The Ophrys pol l i nat or serves as a pr egami c i sol at i ng
mechani s m since it effectively isolates t he gene-pool of each Ophrys species (PAULUS
& GACK 1983 a). Therefore, by i dent i fyi ng t he pol l i nat or we can det er mi ne t he
t axonomi c st at us of t he p l a n t - a me t hod resul t i ng f r om t he appl i cat i on of t he
biospecies concept whi ch is unusual in bot ani cal investigations. Appl i cat i on of t he
biospecies concept to Ophrys leads in most cases to a clear di fferent i at i on; however
in some cases, at t ent i on must also be given to ot her facts (PAULUS & GACK 1983 a).
I n t he present wor k we summar i ze our observat i ons and tests dur i ng a visit to
t he sout her n par t of t he east ern Medi t er r anean isle of Cypr us dur i ng Febr uar y
28t h to Mar ch 14th 1986. The Ophrys flora of this isle is relatively well known and
consists of 14 species (BALZINGER 1982, BAUMANN & KONKELE 1982, DAVIS 1954,
GOLZ & REINHARD 1985, GUMPRECHT 1964, HERMJAKOB 1969, MHKLE 1985, RENZ
180 H. F. PAULUS & C. GACK:
1929, So(3 1929, WI LHY~ 1975/ 1976) ( Ta bl e 2). We f o u n d all t he speci es e xc e pt
t he l a t e - f l owe r i ng O. apifera, O. holoserica, a n d O. mammosa. On l y a si ngl e cas e
o f p o l l i n a t i o n h a s b e e n r e p o r t e d o n t hi s i s l a nd (Andrena flavipes o n O. israeli-
t i ca- c i t e d as O. fusca, BAUMANN & HALX 1972).
Methods
We always t ry t o observe s pont aneous visits and pseudocopul at i ons of t he pol l i nat or i n
t he nat ur al habi t at of t he Ophrys plants. As this occurs very rarely we l ook for swarmi ng
sites of males or for flower visiting bee males of t he possible pol l i nat or s and t here we put
t he Ophrys t o test. To test t he specifity we of t en offer several Ophrys spp. t oget her t o give
t he males t he choice. Test s and observat i ons were carri ed out in t he field as of t en as t here
was t he oppor t uni t y in or der t o make t he results reproduci bl e for di fferent t i mes and places.
A special bee species onl y is consi dered t he pol l i nat or after careful observat i ons of its
behavi our on t he Ophrys flower.
(1) The mal e has t o show i nt ense ps eudocopul at i on behavi our , e.g., a specific, fast and
det er mi ned appr oach t o t he flower, t he ext rusi on of t he genital appar at us, copul at i on
movement s wi t h t he abdomen, in some species hummi ng wi t h t he wings.
(2) Anot her cri t eri on is t he r emoval of pol l i ni a or a pol l i nat i on wi t h pol l i ni a f r om a
flower visited earlier. Bot h onl y happens when t he mal e' s behavi our and size is cor r espondi ng
t o t he flowers.
(3) I ndi cat i ons of a pol l i nat i on rel at i onshi p are given by caught males who carry pol l i ni a
of Ophrys on t he head or t he abdomen. Wi t h reservat i ons it is possible t o relate these
species t o cert ai n Ophrys spp. due t o t he systematical posi t i on of t he bee.
(4) Some bee species even show ps eudocopul at i on behavi our when t hey are put i nt o a
glass t ube t oget her wi t h a flower. Thi s has t o be est i mat ed critically as artificial condi t i ons
ma y cause a bnor mous reactions.
Results
Ophrys kotschyi ( Fi g. 1). O. kotschyi was j u s t b e g i n n i n g i t s a n t h e s i s i n ear l y Ma r c h .
Th i s b e a u t i f u l speci es i s - as f ar as is k n o w n - e n d e mi c t o Cy p r u s . T h e l ar ge b l a c k
a n d wh i t e p a t t e r n e d f l owe r s ( Fi g. 1 a, b) s h o w a gr e a t s i mi l a r i t y t o t h e Ae g e a n O.
cretica (VIERr~.) NELSON a n d f o r t hi s r e a s o n b o t h we r e c o n s i d e r e d s ubs pe c i e s wi t h i n
t h e s a me speci es (NELSON 1962, SUNI~RMANbr 1980). Ho we v e r , RENZ (1929) a n d
l at er DANESCtt & DANESCH (1972: 42) a n d CAMPBELL (1982) e l u c i d a t e d t he r el a-
t i o n s h i p t o t h e Ophrys umbilieata-oestrifera aggr . Re c e n t l y GOLz & REINttARD
(1985) c o n d u c t e d a b i o me t r i c a l a na l ys i s r e ve a l i ng a l a r g e " S i p p e n d i f f e r e n z " b e t we e n
O. kotschyi a n d O. cretica wh i c h d o e s n o t f a v o u r t he i de a o f speci es i d e n t i t y a n d
p o s s i b l y n o t e ve n a cl ose r e l a t i o n s h i p . T h e s u p p o s e d p o l l i n a t o r , Melecta tuberculata
LIEFTINCK, is o n l y k n o w n f r o m c o l l e c t i o n ma t e r i a l wi t h p o l l i n i a a t t a c h e d t o t he
h e a d ( Cy p r u s , Rh o d e s , a n d Cr et e) (LIEFTINCK 1980). F r o m o u r k n o wl e d g e o n t he
p o l l i n a t i o n o f O. cretica f r o m Cr e t e , we s u p p o s e d t h a t M. tuberculata mi g h t be
t he p o l l i n a t o r o f O. kotschyi (PAULUS & GACK 1986). I n f act , i n Cy p r u s we o b s e r v e d
p s e u d o c o p u l a t i o n s o n O. kotschyi by Melecta tuberculata ( Fi g. 1 c) ( Agi os Ge o r g i o s
Ma r c h 4 t h 1986, s ever al o b s e r v a t i o n s u n d e r e x p e r i me n t a l c o n d i t i o n s i n t he fi el d;
Ac r o t i r i , 4 ma l e s wi t h pol l i ni a ; ma n y o b s e r v a t i o n s u n d e r ar t i f i ci al c o n d i t i o n s i n a
h o t e l r o o m) . F r o m t he s e f i n d i n g s i t is a b s o l u t e l y cl ear t h a t t hi s l a r ge Melecta is
t he ef f ect i ve p o l l i n a t o r o f O. kotschyi. T h e s a me bee speci es we f o u n d t o be t h e
p o l l i n a t o r o f t h e l a t e - f l owe r i ng e a s t e r n " f o r m" o f O. cretica i n Cr e t e ( Za g r o s 30.
3. 1986, L a n g a d a a n d Pi l a l i ma t a 1. 4. 1986, PAULUS 1988b) . T h e ot he r , ear l y-
Pollination of Ophrys 181
Fig. 1. Ophrys kotschyi, a Flower, b several flowers differing with respect to the patterns
of the labella, c Melecta tuberculata male during pseudocopulation; note the protruded
genital apparatus and the tuft of pollinia attached to the bee's head
flowering "f or m" of O. cretica (referred to by NELSON 1962 as O. cretica subsp.
karpathensis or subsp, naxia) is pollinated by Melecta albifrons (PAULUS & GACK
1983 b, 1986). According to the above ment i oned concept, same pol l i nat or - s ame
Ophrys spp., this should be an adequate reason for considering O. kotschyi and O.
182 H. F. PAULUS & C. GACK:
cretica as synonymous. However, there are good reasons - flower morphol ogy and
the statistical analysis of GOLz & REINHARD ( 1985) - whi ch indicate a convergence
between these two Ophrys "f or ms". If true, the similarity woul d be the consequence
of identical selection pressures worki ng i ndependent l y and allopatrically t hrough
the same pol l i nat or species Melecta tuberculata. Similar explanations could be
demonst rat ed for O. apulica - O. heldreichii - O. episcopalis ( = O. holoserica
var. maxima) and O. atlantica - O. bertolonii - O. ferrum-equinum (PAULUS &
GACK 1986). To confi rm the hypothesis of convergence between O. cretica and O.
kotschyi more details on pl ant morphol ogy, enzymology, and above all the com-
position of the chemical compounds in the labella should be investigated.
Ophrys elegans (Fig. 2 a, c). This species is rare and had nearly finished its
flowering period by the beginning of March, 1986. Ophrys elegans is distributed
only in the most eastern part of the Medi t erranean area and can be found in Cyprus
and eventually southeastern Turkey. It is a species closely related to Ophrys argolica
FLEISCHM. (Fig. 2 b), whi ch occurs in Greece. Flowers of O. elegans (Fig. 2 a) are
relatively small, the sepals are light or dar k rose-coloured, and in most cases
markedl y curved backwards. The lateral edges of the labellum are mostly so t ucked
under t hat the lip is pointed. The labellum is dark brown-red and shows a char-
acteristic design in the form of a transverse dumb-bell or spectacles. But there is
variability: sometimes the two ends of the dumb-bell are j oi ned by a circle directed
t owar d the tip of the labellum; sometimes the design is reduced to two separate
rhombi c spots. Similar designs can be found in Ophrys argolica, O. delphinensis 0.
E. DANESCH, O. crabronifera MAURI and O. biscutella O. & E. DANESCH. We
found Anthophora retusa (L.) to be the pol l i nat or of O. biscutella (1985, sout hern
Italy) and Anthophora plagiata ILL. to be t hat of O. delphinensis (N. Peloponnesus,
Delphi) (PAULUS & GACK, unpubl.). For this reason we expected to find anot her
Anthophora species as the pol l i nat or of O. elegans. I n fact, we discovered the small,
silver grey Anthophora erschowi FEDT., an E. Eur opean representative of this genus,
to be the pol l i nat or on Cyprus (Fig. 2 c). This is now the t hi rd Anthophora species
as pol l i nat or within this Ophrys group with a spectacles-design on the labellum.
This result is remarkabl e since it suggests t hat this design is an i mpor t ant optical
releaser for some species of the genus Anthophora. For this reason we expect t hat
even the pollinators of O. argolica and O. crabronifera should be species of An-
thophora. All members of this Ophrys group wi t h such a labellum design could be
considered typologically as closely related. But at t ent i on must be pai d to the pos-
sibility ofconvergences as demonst rat ed in O. cretica - O. kotschyi or O. bertolonii
- O. atlantica - O. ferrum-equinum (PAULUS & GACK 1986).
Opbrys flavomarginata (Fig. 3 a - c ) and Opbrys umbilicata (Fig. 3d, e). These
two species are distributed in the eastern Medi t erranean area. O. flavomarginata,
originally described as a col our vari at i on of O. umbilicata, was first investigated
at the species level by BAt:MANN & K~NKELE (1982). It has been report ed on
Cyprus, Israel, and, accordi ng to BUTXLER (1986), also Jordan. O. umbilicata (incl.
attica) has a wider distribution area over Israel, Lebanon, and Turkey to Greece.
0. flavomarginata was at the end of its flowering period in early Mar ch 1986,
whereas O. umbilicata was in full flower. The flowers of O. flavomarginata are, in
compari son to those of O. umbilicata (Fig. 3 a, b, e), larger and wider. The labellum
is surrounded by a broad, mostly yellow margi n and shows a nearly quadrat i c or
rect angul ar shape. The sepals are always green. The flowers of O. umbilicata are
Pollination of Ophrys 183
Fig. 2. Ophrys spp. a Flower of O. elegans from Cyprus, b flower of O. argolica from
Peloponnesus; note the similar dumb-bell-like pattern of the labella, c Anthophora erschowi
during pseudocopulation on O. elegans
184 H. F. PAULUS & C. GACK:
smaller and more graceful. The lateral margi n of the labellum is bent up t owar d
the back side, so t hat the front side of the labellum is oval. The colours of the
sepals vary from green to white and different shades of pink. Pi nk is the domi nat i ng
col our in the mount ai nous regions. In spite of these differences the two species
often resemble each ot her (al t hough differentiating between these two in the field
seldom leads to any problems) which was the reason for groupi ng bot h as subspecies
of the same species. GOLz & REINHARD (1985) only found a small "Sippendifferenz"
using a statistical met hod of biometrical discrimination analysis. But considering
O. flavomarginata as a subspecies of O. umbilicata ignores their syntopic distri-
bution. If these two forms are really different species t hen bot h should have different
pollinators acting as isolating mechani sms to mai nt ai n their respective gene-pools.
Pollinators of bot h species are still unknown. In Cyprus we found males of the
green-eyed l ong-horn bee Eueera dimidiata BR. pseudocopul at i ng wi t h flowers of
O.flavomarginata (Fig. 3 c) and males of the smaller bright brown (freshly emerged)
or grey (old) haired Eucera gaullei VACI4. pseudocopul at i ng with flowers of O.
umbilicata (Fig. 3 d). I n choice tests bot h bee species reacted specifically, i.e., Eucera
dimidiata pseudocopul at ed only with O. flavomarginata and Eucera gaullei only
with O. umbilicata. This shows a clear reproductive isolation of the two Ophrys
spp. and confirms their biospecies status. There is no record of hybrids; their
identification woul d be very difficult any way. It is interesting t hat Eucera gaullei
did not prefer one col our form of O. umbilicata to the other. The pseudocopul at i ons
were of the same intensity on plants with green, white or pinkish sepals, even on
plants from the mount ai nous areas, whi ch share a great similarity with O. scolopax
or O. oestrifera in t hat the mi ddl e sepalum is sometimes erected (Fig. 3 d) instead
of t urned t oward the lip (Fig. 3 e). This infers t hat the forms previously discriminated
as O. umbilicata, O. carmeli, O. orientalis and even the O. oestrifera-like plants are
all conspecific, at least on Cyprus.
Anot her interesting fact is t hat the pol l i nat or of O. flavomarginata, Eucera
dimidiata, also pollinates O. tenthredinifera in Crete (PAULUS 1988 b). Accordi ng
to TKALCU (1978) this bee is distributed t hr oughout N. Africa, Greece, Crete,
Cyprus, and the Middle East. This relationship may explain the absence of O.
tenthredinifera in Cyprus. The pol l i nat or of O. tenthredinifera in Greece and the
western Medi t erranean is the l ong-horn bee Eucera nigrilabris (KtJI.LENBERG 1961,
KULLENBEe,~ & al. 1984, SCUP, EMMER 1960, PAULUS & GACK 1980, V~STH 1984).
This species does not occur, as far as is known, on Crete or Cyprus.
Ophrys bornmuelIeri and Ophrys levantina (Fig. 4). It has long been known t hat
O. bornmuelleri occurs in two different "forms": small-flowered O. bornmuelleri
(s.str.) and large-flowered O. bornmuelleri subsp, grandiflora FLEISCHMANN & 806.
Bot h "f or ms" have been considered as being conspecific wi t h O. holoserica (SUN-
I~EI~MANN 1980). Wi t h a biometrical discrimination analysis GOLZ & REINHARD
Fig. 3. a Two flowers of Ophrys umbilicata (left) and two flowers of O. flavomarginata
(right) showing, respectively, the ovale and rectangular shape of the labella and the vari-
ability of the labellum pattern; b flowers of O. flavomarginata, note the different labellum
patterns even on the same plant; e Eueera dimidiata pseudocopulating on O.flavomarginata,
the light green eyes of the bee appear white; d Eucera gaullei pulling out the pollinia of an
O. umbilicata; note the erected middle sepalum; e O. umbilicata, lateral view
Pollination of Ophr2s 185
186 H. F. PAULUS & C. GACK:
Fig. 4. a Flowers of Ophrys bornmuelleri (left) and O. levantina (right); note the triangular
and rectangular shape, respectively, of the labella and the different width of the stigmatic
groove, b Eucera paulusi, during pseudocopulation; one pollinium is attached to the bee's
head
(1985) showed that bot h "forms" are different species which are well separated
from each other as well as from similar species by a large "Sippendifferenz". They
regarded the large "f or m" as a new species, O. levantina (GoLz & REINHARD 1985).
We concur with this idea and assume that the differences in morphol ogy (e.g., size,
shape) between O. bornmuelleri and O. levantina are due to the different selective
pressure of two different pollinator species. We have demonst rat ed similar cases
for O. fusca in Spain (PAULUS & GACK 1981, 1983 a) and O. holoserica on Crete
(PAULUS & GACK 1986). O. bornmuelleri and O. levantina occur in the eastern
Mediterranean. But their exact distribution needs further confirmation especially
since there may be additional "forms" (e.g., we found two "forms" of O. born-
muelleri in Israel, one of t hem was similar but much smaller t han O. levantina in
Cyprus). Both species are very common in Cyprus. O. levantina was in full flower
until the middle of March 1986, while the flowering period of O. bornmuelleri had
just started. The flowers of O. levantina are usually larger t han those of O. born-
muelleri and their labella are oriented vertically, while those of O. bornmuelleri are
oriented horizontally. The labellum of O. levantina is quadratic, that of O. born-
muelleri triangular (Fig. 4 a). Anot her marked distinction between the two species
are the two humps on the labellum which are pointed and orientated parallel to
the gynost emi um in O. bornmuelleri but are rounded and oriented at an obtuse
angle to the gynost emi um in O. levantina (GOLz & REINHARD 1985, WILLING &
WILLING 1975/76).
We found only one of the two supposed pollinators in Cyprus. Eucera paulusi
TKALCU, a very small long-horn bee, is the pollinator of O. bornmuelleri (Fig. 4 b).
In several choice tests the males of this species chose only O. bornmuelleri and
Pol l i nat i on of Ophrys 187
Tabl e 3. Known pol l i nat or s of Ophrys lutea aggr. a I n PAULUS 8,2 GACK (1986) er r oneousl y
refered t o as A. cinereophila W. b Several males wi t h abdomi nal pol l i ni a were caught , but
no ps eudocopul at i on was observed. Size of t he bee, its phyl ogenet i c rel at i onshi p (subgenus)
and t he locality where it was caught i ndi cat e t hat t he pol l i ni a are deri ved f r om t he respective
Ophrys species, c I ncl udi ng t hose pl ant s f r om Pugl i a wi t h flowers very similar t o Ophrys
melena f r om S. Greece. We refer t o these pl ant s as mel enoi d sicula (minor) and not as O.
melena RENZ
Ophrys species Pollinator(s) Local i t y of obser vat i on
O. lutea A. (Chlorandrena) cinerea BR. Spain, France, Greece, Italy,
Mor occo
S. Spain, Algeria
S. Italy, S. Greece
O. sicula
O. melena
A. (Chlorandrena) senecionis PER.
A. (Chlorandrena) humilis IMn.
A. ( Chlorandrena) panurgimorpha
MAVR. a
A. (Lepiandrena) dorsalis BR. b
A. (Chrysandrena) hesperia SMITH
A. (Chrysandrena) merula WARNCKE
A. (Euandrena) bicolor F.
A. (Euandrena) vulpecula KRI~CnB.
A. (Cordandrena) torda WARNCKE
A. (Simandrena) transitoria MOR.
Cret e
S. It al y
Greece, S. It al y , Crete,
Lebanon, Rhodes
Israel
S. It al y b
S. It al y
Cyprus
S. Greece (NOTH 1985)
n e v e r O. levantina. Th i s c o n f i r ms t he s e p a r a t i o n o f t h e t wo Ophrys speci es as
s u g g e s t e d b y GOLZ & REINI~ARD (1985).
Ophrys sicula ( = O. galilaea FLEISCHMANN & BORNM~LLER). PAULUS & GACK
(1986) e l e v a t e d t he s ma l l f l o we r e d O. lutea s ubs p, minor t o speci es s t a t us b e c a u s e
i n all o u r t es t l ocal i t i es i n t h e Me d i t e r r a n e a n a r e a (S. I t al y, Gr e e c e , Cr e t e , Rh o d e s ,
et c. ) t he t wo O. lutea " f o r ms " ( l ar ge- a n d s ma l l - f l owe r e d) h a v e d i f f e r e n t p o l l i n a t o r s .
Un f o r t u n a t e l y , we d i d n o t p a y a t t e n t i o n t o t he f a c t t h a t o n t he speci es l evel t he
n a me "minor" d o e s n o t h a v e p r i o r i t y o v e r "galilaea". Ac c o r d i n g t o BAUMANN &
KONKELE (1986) t he s ma l l O. lutea s h o u l d be n a me d O. galilaea, a t l eas t i n i t s
e a s t e r n a r e a o f d i s t r i b u t i o n . We s u p p o s e t h a t al l t he s ma l l - f l o we r e d O. lutea " f o r ms " ,
u s u a l l y cal l ed O. lutea s ubs p, minor, r e p r e s e n t a s i ngl e bi os peci es , s e p a r a t e d f r o m
t h e l a r g e r - f l o we r e d O. lutea. Bu t t h e t a x o n o my is still unc l e a r . Ac c o r d i n g t o PAULUS
(1988 b) O. galilaea is s y n o n y mo u s wi t h O. sicula.
0. sicula is t he o n l y speci es wi t h i n t h e O. lutea g r o u p i n Cy p r u s . Th e f l owe r s
ar e s mal l - t o mi ddl e - s i z e d, t h e l i ps ar e l i ght y e l l o w- g r e e n i n s t e a d o f c a n a r y - y e l l o w
as i n O. / u r e a . T h e p o l l i n a t o r s o f O. sicula ar e s ever al cl os el y r e l a t e d Andrena s pp.
o f t he s ubg. Chrysandrena. T h e mo s t c o m m o n speci es is A. hesperia (PAULUS &
GACK 1986, WARNCKE & KULLENBERG 1984). I n Cy p r u s s ever al p s e u d o c o p u l a t i o n s
by Andrena torda we r e o b s e r v e d , b u t o n l y a t a s i ngl e l o c a t i o n . Thi s speci es is a
r e p r e s e n t a t i v e o f t he s ubg. Cordandrena, wh i c h is, a c c o r d i n g t o WARNCKE (1968),
cl os el y r e l a t e d t o t h e Micrandrena-Euandrena-Chrysandrena g r o u p s . We ar e c on-
v i n c e d t h a t t he l e g i t i ma t e p o l l i n a t o r wi l l be a n o t h e r speci es o f Chrysandrena, ma y b e
A. hesperia or A. merula. T h e k n o w n p o l l i n a t o r s o f O. sicula ar e gi ve n i n Ta b l e 3.
188 H. F. PAULUS & C. GACK:
Fig. 5. a Andrena morio male during pseudocopulation on Ophrys iricolor flower, note the
pollinia attached to the bee's head which are removed from O. transhyrcana; b Andrena
morio during pseudocopulation on O. iricoIor; the pollinia are glued to the viscid stigmatic
groove
Ophrys iricolor (Fig. 5). O. iricolor has a wide distribution in the eastern Med-
iterranean area and is a biospecies within the O. fusca aggr. The pollinator is the
large blue-black Andrena morio BR. Pseudocopul at i on has been observed in Aegina
(VOTH 1984) and in Crete (PAULUS & GACK 1986) and male bees with pollinia
have been caught from Crete (VOOEL 1976), Rhodes (WAP.NCKE & KULLENBEP.O
Pollination of Ophrys 189
~D

~D


,4
r ~
~
(
j ' l I
: . . L' L' . . . .
190 H.F. PAULUS & C. GACK:
1984), and At t i ca (PAULUS & GACK, unpubl . ). In Cypr us O. iricolor was in full
bl oom and we also f ound A. morio as t he pol l i nat or (Fig. 5 a, b).
This Ophrys species, like all member s of t he O. fusca/lutea group, at t aches t he
pol l i ni a to t he tip of t he bee' s abdomen. I n Cypr us we f ound t wo males of A. morio
wi t h pollinia not onl y on t he abdomen but also wi t h addi t i onal Ophrys pollinia
at t ached to t he head (Fig. 5 a). It is obvi ous t hat these t wo i ndi vi dual s visited t wo
di fferent Ophrys species. As we will see later, t he head pollinia ori gi nat ed f r om O.
transhyrcana. Pr ovi ded t hat A. morio visits bot h Ophrys spp. regularly, it can act
as an i sol at i ng mechani sm for t wo synt opi c Ophrys spp. flowering at t he same time.
Similar si t uat i ons are known f r om t ropi cal Euglossina bees as pol l i nat ors of Ca-
tasetum (Orchidaceae) (DREsSLER 1968, DODSON 1975).
Ophrys israelitica(= O. fleischmanniip.p.) (Figs. 6, 7, and 8; Table 4). I n Cypr us
this species, bel ongi ng to t he O. fusca/lutea group, was in full bl oom dur i ng t he
first t wo weeks of Mar ch 1986 (Fig. 6 a, b). Accor di ng to BAUMANN & DAFNI (1981)
"O. fleischmannii" is di st ri but ed f r om Crete, sout her n At t i ca, most of t he Aegean
islands, west ern and sout her n coast of Tur key to Syria, Lebanon and Israel. The
pol l i nat or was first di scovered by BAUMANN & HALX (1972) in Cyprus. They t ook
pi ct ures of pseudocopul at i ng Andrena flavipes on "O. fleischmannii" (cited as O.
fusca). Thi s coul d be conf i r med by PAULUS & GACK (1986) in nor t her n Israel
( numer ous observat i ons of pseudocopul at i ons) (Fig. 7 a) and now in Cypr us as well
after numer ous observat i ons of A. flavipes males wi t h abdomi nal pol l i ni a *. Since
t he flower mor phol ogy of "O. fl ei schmanni i " f r om Israel and Cypr us is very di fferent
f r om t hat of O. fleischmannii f r om Crete (Fig. 7 b, c), we post ul at ed t wo di fferent
pol l i nat ors and supposed t hat "O. fleischmannii" f r om Cypr us and Israel is a new,
still unna me d species (PauLuS & GACK 1986). Meanwhi l e, t he pol l i nat or of t he
Crete O. fleischmannii coul d be f ound and i dent i fi ed as Anthophora sicheli RAD.,
a species whi ch had al ready been f ound wi t h pollinia by VOGEL (1976) on Crete.
(However, based on t he condi t i ons of t he locality, he consi dered t he pol l i ni a to
have ori gi nat ed f r om O. iricolor.) This confi rms our supposi t i on t hat t he O. fleisch-
mannii f r om Crete and t hose f r om Cyprus/ Israel are di fferent species. O. fleisch-
mannii f r om Crete has been descri bed by HAYEK (1926). The new species now has
been descri bed as O. israelitica (BAUMANN & K~NKELE 1988).
Due to our own i nvest i gat i ons we are able to give some addi t i onal i nf or mat i on
to t he descri pt i on of O. israelitica. This new species is di st ri but ed over Cyprus, N.
Israel, Lebanon (KULLENBERG1961), and SE. Anat ol i a (VOTn 1967, SUNDERMANN
& TAUBENI-IEIM 1978 as O. omegaifera) (DAvis 1984). The descri pt i on of O.fleisch-
mannii given f r om Naxos and Siros in BAUMANN & DAFNI (1981) refers per haps
to a di fferent O. fusca-form but not to these t wo species, as t he original fot os f r om
* A. flavipes is the pollinator of the so-called O. flavipes-fusca (kleine fusca of PAULUS
& GACK 1980, 1986) in the western Mediterranean area, Greece and Crete (PAULUS 1988 b).
Therefore we supposed that no O. flavipes-fusca should exist on Cyprus, but rather other
O. fusca "forms".
Fig. 6. Ophrys israelitica, a Several plants in full bloom; b - e flowers, note the wide stigmatic
groove and the velvet-like short hairs on the dark brown parts of the lip; fseveral flowers
showing relatively little variability of shape
Pollination of Ophrys 191
192 H. F. PAULUS & C. GACK:
Fig. 7. a Andrena flavipes pulling out the pollinia from Ophrys israelitica (Israel); b O.
israelitica (foto REINI-IARD), Cyprus, 10. 3. 1985; c O. fleischmannii, Crete
Fig. 8. Ophrys israelitica ( a- d), O. fleischmannii ( e- h), SEM fotos; a and d in comparison
with e and h: the "speculum-area" of O. israelitica (a) shows long hairs which point markedly
towards the stigmatic groove (d) whereas the corresponding area of O. fleischmannii (e)
shows shorter hairs without any orientation (h); b in comparison with f ' frontal view of
the hairy surface of the brown parts of the lips; the hairs of O. israelitica (b) are very long
and show no recognizable orientation, the corresponding hairs of O. fleischmannii (f) are
much shorter and in the middle of the area they point towards the stigmatic cavity; c in
comparison with g: side view of the same flowers; note the same characteristics as in b and f
Pollination of Ophrys 193
194
8
H. F. PAULUS & C. GACK:
s z
O
t t 3 ~ 3
,.,_#
oo
o oc~
r~
Ctl
c q~ d
cm o~
~
~<, . d
2:
Pollination of Ophrys 195
a tD
!
b
J
cl
1era
Fig. 10. Flower analysis of OphrysJTeischmannii, a Ophrys heldreichii, Osterr. Bot. Z. 74:
182, tab. II, fig. 6 (1925), nora. illeg. Kreta: Distr. Khania, Akrotiri, Hagia Triadha, 3. 3.
1924, leg. I. DORFLER Nr. 154 (WU, W). = O. fleischmanii in Feddes Repert. 22: 388
(1926). Size as in the publication of H. FLEISCHMANN. b Comparison of flower size between
O.fleischmannii (right), Crete: Thrifti, 4. 4. 1972, leg. J. FORSTER and O. omegaifera (left),
Crete: Melambes, 31. 3. 1972 ( HR 17205). Nat ural size. c Ophrysfleischmannii, Crete:
Nomos Lasithion, Thrifti, 4. 4. 1972, leg. J. FORSTER, Winterthur. ( HR 17205). Size c. 2 : 1.
d O. sitiaca, Crete: Nomos Lasithion, Thrifti Ori, lower forest region, 500 m, 19.2. 1988,
leg. H. F. PAULUS (holotype) (from PAULUS 1988 b)
196 H. F . PAULUS & C. GACK:
%
o o o o o o o e o o o e o o o e e e o e ~ a o
~ e o o o
o o e e e o e
.~''...-
i?..
/ ~ O. f l e i s c h m a n n i i
,,- O. o m e g a i f e r a
i~i O. i s r a e l i t i c a
" . !
Fig. 11. Distribution map of Ophrys spp. (for further comments see the text)
V(}TH show (VoTH, pers. comm.). For this reason, we have, for the time being
omi t t ed these points on the map of distribution (Fig. 11). Possibly the findings of
O. fleischmannii near Bodrum (SW. Anatolia, SUNDERMANN & TAUBENHEIM 1978)
and near Antalya (foto TAUBENHEIM) are of different O. fusca forms. Most of the
other distribution points on the map were obtained from BAUMANN DAFNI
(1981), ALTAN & HOFFMANN (1986), and from our own investigations in Israel,
Cyprus, Rhodes, and Crete. The plants are distributed mostly in Phrygana on
limestone hillsides and sparse pinewoods. Phenology: January (sometimes beginning
at the end of December) until the mi ddl e or the end of March. Pollinator: Andrena
flavipes PANZ. (Cyprus: BAUMANN 8 HALX 1972, PAULUS ~ GACK, the present
work; Israel: PAULUS 8 GACK 1986). The measurements of the lip are given in
Table 4 and Fig. 12, flower analysis see Figs. 9 and 10. Iconography: KULLENBERG
(1961: plate 1, fig. 13, 14; plate 42, fig. 12; plate 43, fig. 1; as O.fusca f. omegaifera);
BAUMANN ~ HALX (1972; as O.fusca); BAUMANN ~: DAFNI (1981: figs.: 9, 10, 11;
as O. fleischmannii); PAULUS & GACK (1986: colour table 3, fig. 6, p. 56, fig. 3 a;
as cf. O. fleischmannii; BUTTLER (1986: 173; Anat ol i a fot. TAUBENHEIM; Cyprus
fot. PETER; as O. fleischmannii); FEINBRUN-DOTHAN (1986: Fl ora Palaestina 4,
Tafelband fig. 520).
As ment i oned in PAULUS & GACK (1986) the flowers of the new species l ook
like an intermediate between O. fusca and O. omegaifera (Fig. 6 c - f ) . But the
distribution (Fig. 11) is inconsistent with a hybridization or a case of introgression.
In Israel no other species of the O.fusca aggr. (s.1.) except O. iricolor occurs [neither
Pollination of Ophrys 197
0 , 5 -
0,4-
0,3"
F
0,2-
o , t
Q
b
I
I
0 Ophrys fusca Link
] Ophrys omegaifera Fleischmann
Ophrys israelitica Baumann & K~nkele
/~ Ophrys fleischmannli Hayek
I
ii[
D
5' o 6' o 7' o d o c . m
Fig. 12. Graph showing that Ophrys israelitica is not an intermediate between O. fusca and
O. omegaifera; there is therefore no reason to believe that O. israelitica is of hybridogenous
origin
O. Jusca (s.str.) nor O. omegaifera]. In nort hern Israel O. israelitica is one of the
most common species, generally growing in sparse pine forests. We suppose the
same is true in Lebanon. In Cyprus and presumabl y in Anat ol i a, O.israelitica grows
syntopically with O. (einereophila)fusca (see the foot -not e on p. 199) and perhaps
with ot her O. fusca forms (except O. flavipes-fusca). But in the whole area O.
omegaifera is lacking. Fr om the typical O. fleischmannii HAYEK, whi ch is endemic
in Crete, O. israelitica can be distinguished by its colour, shorter hairs, and the
surface of the lip, whi ch is nearly plain (Fig. 8 a - h ) . BAUMANN ~; DAFNI (1981)
did not distinguish between the genuine O. fleischmannii and O. israelitica. The
col our picture in BAUMAN~ & OAFNI (1981) (foto VOTH) from the locus typicus
(Acrotiri) is not O. fleischmannii but O. omegaifera. Mr VOTH (pers. comm. ) gave
us anot her picture of Acrotiri, whi ch shows the real O. fleischmannii. A picture of
this species can also bee seen in LANDWEHR (1983: table 178, fig. 5). As far as we
know, O. israelitica does not occur in Crete and Rhodes. A similar new species
was f ound on Crete whi ch is described as Ophrys sitiaca PAULUS & A. & C. ALIBERTIS
(PAULUS 1988 b).
El ect rophoret i c enzyme analysis is a met hod to investigate genetic differences
between popul at i ons and species. These differences possibly serve as t axonomi c
features (FER~USON 1980). On orchids this met hod has been applied to characterize
hybrids (FELDMANN 1988, STEINBRUCK & al. 1986) and to identify species of the
genus Orchis and Dactylorhiza. Moreover, SCHLEGEL & al. (1989) used electro-
phoresis to const ruct dendrograms.
For Ophrys fleischmannii (Crete), O. israelitica (Cyprus), O. flavipes-fusca (S.
Spain), O. kotschyi (Cyprus) 7 enzymes were compar ed by starch gel electrophoresis
(for met hod see STEINBRUCK al. 1986). All flowers and leaves investigated orig-
198 H. F. PAULUS & C. GACK:
inated from plants which were cultivated in a greenhouse. The following enzymes
were tested: Isoci t rat edehydrogenase (IDH), "Mal i c Enzyme" (ME), Phospho-
glucomutase (Pgm), Phosphogluc' oisomerase (Pgi), Acidic Phosphat ase (Acp),
Superoxidismutase (SDM), Esterase (Substrate 4-Methylumbelliferyl-propionate)
(ES).
Hardl y any differences were found among the enzyme patterns of all the in-
dividuals of the species O. fleischmannii, O. israelitica, and O. fusca tested. In
cont rast to this result O. kotschyi shows a different pat t ern of bands for all enzymes
investigated. Since only a few individuals have been tested, the existing dat a allow
only prel i mi nary conclusions. Wi t h the ut most caut i on we concl ude t hat O. fleisch-
mannii, O. israelitica, and O. fusca belong to a group whi ch is genetically very
uni form and shows clear differences to O. kotschyi. To delimitate O. fleischmannii
and O. israelitica as species the existing dat a are not sufficient. For t hat purpose
further investigation of more individuals and popul at i ons is needed.
K e y o f t h e O. omegMfera a g g r .
The species of this group within the O. fusca aggr. (s.1.) are easy to recognize by
their lack of the longitudinal V-shaped furrow at the base of the lip, and by the
"omega" on the front edge of the speculum. This "omega" can also be found on
the lips of some O. fusca (s.str.) but these flowers always have the V-shaped furrow.
1 Longi t udi nal V-shaped furrow at the base of the lip long and distinct, stigmatic
groove whose wi dt h is about 2 - 2.8 times the height, front edge of the speculum
wi t hout "omega", sometimes weakly indicated . . . . . . . . . . . . . . . . . O. fusca (s.str.),
O. iricolor, O. lutea, O. sieula (= lutea subsp, minor), O. melena, O. pallida
- Base of the lip wi t hout a V-shaped furrow o r - if present - t hen very weak and
short; stigmatic groove whose wi dt h is at least 2.5 times, normal l y more t han
3 times its height; front edge of the speculum always with a light "omega",
whi ch is seldom weak . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2 Base of the lip with a flat, very short V-shaped furrow; stigmatic groove whose
wi dt h is about 2.5 - 2.8 times its height, labellum flat, at its base weakly, some-
times markedl y curved down. Lateral lobes very short, curved back. Lip light
brown, often wi t h a grey colouring, sometimes blueish. Fr ont edge of the
speculum with a whitish "omega". Hairs on the lip very short. Basal third of
the labellum nearly straight, only the distal edge curved backward. Distribution:
Crete. Pollinator: Andrena nigroaenea. Fl oweri ng time: J a n u a r y -
Mar ch . . . . . . . . . . . . . . O. sitiaca H. F. PAULUS & C. + A. ALIBERTIS (Fig. 10 d)
- Base of the lip wi t hout a furrow. Stigmatic groove whose wi dt h is at least 3
times its height . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3 Stigmatic groove whose wi dt h is about 4 - 4 . 5 times its height; lip flat,
1 1 - 15mm long, 8 - 1 2 . 5 r a m broad, at its base hardl y any curvature; lateral
lobes extended, rarely t urned backwards; speculum shiny, leaden-blue, some-
times blue, rarely brownish, very often marbl ed with dar k and light spots;
speculum edged wi t h a whitish "omega". Phenology: J a n u a r y - Ma r c h . Dis-
tribution: Israel, Lebanon, Cyprus, SE. Anatolia. Pollinator: Andrena flavipes
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . O. israelitica BAUMANN KCINKELE
-- Stigmatic groove less broad; wi dt h about 3 - 3.5 times height. Lip clearly bent
at its base and curved down, lateral lobes mor e or less close to the lip and
curved back; speculum in most cases uni col oured wi t hout spots. Pollinators:
species of the genus Anthophora . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
Pollination of Ophrys 199
4 Lip large, 13 - 21 mm long, with short hairs, chest nut coloured; speculum brown-
ish with a t ouch of blue, "omega" grey-blue or blue, seldom whitish. Phenology:
end of Januar y (S. Crete) - April. Distribution; Crete, Carpat os, Rhodes, Samos,
Kos. Pollinator: Anthophora atroalba subsp, agamoides . . . . . . . . . O. omegaifera
subsp, omegaifera FLEISCHM.
- - Lip small, 1 0 - 15ram long, with long, furry white hairs . . . . . . . . . . . . . . . . . . . . . . 5
5 Species from Crete, speculum leaden-grey, "omega" grey or whitish blue. Phe-
nology: Fe b r u a r y - Mar ch (near the coast) until the end of April (in the moun-
tains). Pollinator: Anthophora sicheli . . . . . . . . . . . . . . . . . . O. fleischmannii HAYEK
- - Species occurri ng in the SW. Medi t erranean region: speculum reddish brown,
brown, sometimes brown-violet, "omega" whitish, sometimes white-violet. Phe-
nology: J a n u a r y - Ma r c h (N. Africa), beginning of Ma r c h - Ap r i l (S. Spain),
beginning of Ap r i l - Ma y (NE. Spain). Distribution: NE. Spain, Mallorca, S.
Spain, S. Portugal, NW. Africa. Pollinator: Anthophora atroalba subsp, atroalba
(S. Spain), Anthophora balearica (Mallorca) . . . . . . . . . . . . . . . . . . . . . . O. omegaifera
subsp, dyr# (MAIRE) DEL PRETE
Ophrys fusca (Fig. 13). In 1986 we coul d only find one species of the O. fusca
aggr. (s.str.). It is possible t hat there are at least tw O species since GOi~z & RHNHAP, D
(pers. comm. ) have observed, in addi t i on to the most common small-flowered plants,
some plants with larger flowers. Most of the common O. fusca in Cyprus have
small flowers whi ch have a mor e or less br oad yellow margi n (Fig. 13 b, c), in some
respects very similar to those from the Turki sh coast, on Crete or Peleponnesus.
This yellow margi n can be bent over, in whi ch case it is not visible from above.
At the beginning of Mar ch O. f usca was in full bloom. At three different sites
( Kandou, Vavla, and Acrotiri) we observed numer ous pseudocopul at i ons by An-
drena cinereophila * (Fig. 13 a), even performed on flowers with variable size or
with variable yellow col oured margins. This is the same species whi ch was found
to be the pol l i nat or of a small-flowered O. fusca in sout hern Greece (Galaxidion,
VOa-H 1985), in Crete (PAULUS 1988 b), and Rhodes (PAULUS & GAC~, unpubl.).
Several times we were able to test this bee' s react i on to ot her O. fusca "f or ms". It
never showed any interest for these plants. We suppose t hat this "cinereophila-
f usca" is a well separated species distributed only in the eastern Medi t erranean
region.
Ophrys transhyrcana a n d O . mammosa ( F i g . 1 4 ) . Accordi ng to previous aut hors
(e.g., NELSON 1962, SUNDERMANN 1980) the large-flowered species O. mammosa
and O. sintenisii FLE~SCHM. & BORNM~LLER from the O. sphegodes aggr. occur in
Turkey and Cyprus. However, BAUMANN K~NKELE (1982) consider O. sintenisii
as conspecific with O. transhyrcana whi ch CZERNIAKOVSKA (1923) described from
Tur kmeni a in sout hern Russia. Accordi ng to our findings in Cyprus, there is at
least one ot her large-flowered species from the O. sphegodes aggr. whi ch is not
identical with O. transhyrcana or O. mammosa and which perhaps has been confused
in the past with O. transhyrcana-sintenisii (see below).
* Unfortunately in PAULUS & GACK (1986:50 and 65), A. cinereophila is cited as the
pollinator of Cretean O. lutea (large-flowered). The bee species pseudocopulating on O.
lutea (large-flowered) on Crete is A. panurgimorpha.
200 H. F. PAULUS 8 C. GACK:
Fig. 13. a Andrena cinereophila male pseudocopulating on Ophrys (cinereophila) fusca; b
flower of O. (cinereophila)fusca, note the yellow margins in a and b; c several flowers of
O. (cinereophila)fusca showing size and shape variability and a more or less visible yellow
margin
Cyprus is situated in an overlapping distribution zone of O. mammosa and O.
transhyrcana (BAUMANN ~ K~)NCKELE 1982). In 1986 we could find O. transhyrcana
only between March 1st and 14th (Fig. 14a). O. mammosa was not yet flowering
since it starts to flower in April on Cyprus (BAUMANN, GOLZ 8 REINHARD, pers.
comm.). As ment i oned above we captured Andrena morio with pollinia on bot h
the abdomen and the head. According to our tests, the pollinia on the abdomen
originated from O. iricolor, those on the head from O. transhyrcana. The latter is
based on the following observations: one pseudocopul at i on with removal of pollinia
under natural conditions (Akrotiri), several peudocopul at i ons under artificial con-
ditions (hotel room) (Fig. 14 b) and the capture of two A. morio males with pollinia
attached to the head and abdomen (Mallia, Vavla). In several artificial tests we
Pollination of Ophrys 201
Fig. 14. a Flowers of Ophrys transhyrcana (left) and O. sphegodes aggr. (right); b Andrena
morio during pseudocopulation on O. transhyrcana, the pollinium on the bee's abdomen
originates from O. iricolor (see Fig. 5)
observed that A. morio was attracted to O. iricolor and O. transhyrcana. In all tests
O. iricolor releases more intense pseudocopol at ory behaviour t han O. transhyrcana.
Pollination of O. transhyrcana has only been observed in Israel (PAULUS & GACK
1986). The pollinator bee in Israel is the black Andrena fuscosa which is also the
pollinator of O. mammosa on Crete, the Peloponnesus and Attica (PAuLus & GACK
202 H. F. PAULUS & C. GACK:
1986, and unpubl.). For this reason we considered the two species O. transhyrcana
and O. mammosa to be conspecific but members of two different geographical
races. BUTTLEe, (1986) also held this view, but for different reasons. Our new findings
cont radi ct our previous i nt erpret at i on since the pol l i nat or of O. transhyreana in
Cyprus is different from t hat in Israel. We tested the Cypriotic O. transhyrcana for
attractiveness to the Cypriotic A. fuscosa. The bee showed no interest.Thus the
two O. transhyrcana individuals tested may not be identical. As in ot her similar
cases more dat a are required to clarify this problem. Nonetheless we offer two
alternative explanations:
(1) The flowers tested in Israel may not be O. transhyrcana but rat her O.
mammosa which are similar to O. transhyrcana in exhibiting a trilobe labellum. In
this case the distribution of O. mammosa woul d reach as far as Israel. But in the
Mt Carmel region we have found some plants whi ch may have been genuine O.
transhyrcana due to their extreme trilobic lips whi ch were larger t han those of
plants previously tested. DAFNI & al. (1987) also suppose t hat there are bot h species
in Israel, one of t hem a t ranshyrcanoi d O. mammosa. We suppose t hat in Israel,
the actual pol l i nat or of the true O. transhyreana is also A. morio. I f this is true,
t hen O. transhyrcana and O. mammosa are different biospecies isolated by two
different pollinators, A. (Melandrena) morio and A. (Melanapis) fuseosa, respec-
tively:
(2) Bot h O. mammosa and O. transhyrcana may be pollinated by A. fuscosa but
only allopatrically. Wi t h an overlapping (syntopic) distribution, e.g., in Cyprus, O.
mammosa retains its pol l i nat or A. fuscosa whereas O. transhyrcana switches to the
new pollinator, A. morio, preventing cross-pollination. Similar evol ut i onary phe-
nomena in zoology are known as charact er displacement (e.g., BRow~ & WILSON
1956). Therefore, characters whi ch serve to isolate the gene-pools of two closely
related species should be more different in syntopic areas t han in allotopic areas
(for furt her i nformat i on see FENCHEL 1975, GRANT 1975, SLATKIN 1980). If char-
acter displacement operates in the pollination biology of O. transhyrcana and O.
mammosa, the two forms must be considered as well separated biospecies, since
they have different pollinators in their overlapping areas. Such areas serve as a
nat ural test for the species status.
Ophrys sphegodes aggr. (Fig. 15). At different sites along the lower mount ai ns
of Cypr us - ma i nl y in the region of Pano L e f k a r a - Va v l a - Ka t o Dh r y s -
Ma l l i a - Kissousa and Pe r a pe dhi - Ma n d r i a - we found one Ophrys species of the
O. sphegodes complex (Figs. 14 a and 15 a) which is different from O. transhyrcana
and O. mammosa. Especially near Vavla and Kat o Dhrys we found hundreds of
freshly opened flowers of this relatively unknown Ophrys which mi ght be identical
to the plants often considered as hybrids between O. mammosa and O. transhyrcana
(MEIKLE 1985). WOOD (1980) and LANGHE & D' HosE (1982) considered t hem as
O. aesculapii whi ch is certainly incorrect. Accordi ng to the description given by
BAUMANN & KCTNKEI~E (1982) it should be O. transhyrcana. But the flowers are
Fig. 15. a Several flowers of Ophrys sphegodes aggr., note the different colouration of the
sepals and of the margin around the lips; b Andrena bimaculata male pseudocopulating; c
two males of Andrena bimaeulata during pseudocopulation on the flowers of the same
plant; d flower, lateral view, note the unlobed lip
Pollination of Ophrys 203
204 H. F. PAULUS & C. GACK:
ext remel y variable in shape and col our. The col our of t he l abel l um varies f r om
dar k br own- r ed to light yel l ow-brown; t he fl at t ened edge of t he lip varies in col our
f r om entirely yellow to light br own or dar k brown; it can be flat or t ur ned back-
wards. The shape of t he lip varies f r om clearly trilobic to compl et el y unl obed like
a typical O. sphegodes. Lengt h and cur vat ur e of t he connect i ve varies greatly, like
t hat of O. transhyrcana; t he sepals are compl et el y green or weakl y to st rongl y
bi col oured, such t hat t he upper hal f is green and t he lower r eddi sh- br own (Fig. 15 a).
We suppose t hat this Ophrys has been most oft en conf used wi t h O. transhyrcana
and was earlier named O. sintenisii. LA~t~WEIqR (1983) shows a flower f r om Lebanon
labelled as O. transhyrcana whi ch resembles exactly t hose we f ound in Cyprus.
Therefore we suppose t hat this O. sphegodes aggr. has a wider di st ri but i on, mai nl y
in Turkey. It coul d clearly be demonst r at ed t hat this " f or m" represent s a genui ne
species, since its pol l i na t or - Andr e na bimaculata KIp,., a mi d-si zed br own or grey
bee oft en wi t h a reddi sh abdomi nal base - is di fferent f r om t hat of O. transhyrcana.
Thi s bee species is closely rel at ed to A. fuscosa, t he pol l i nat or of O. rnamrnosa
(WARNCKE 1968). At t wo sites (Perapedhi and Mandr i a) we coul d test t he react i ons
of many mal e A. bimaculata to O. sphegodes aggr. (Fig. 15 b, c). They clearly showed
a st rong react i on by pseudocopul at i ng and r emovi ng t he pollinia al most in every
case. Mor eover one mal e wi t h several pol l i ni a at t ached to t he head was caught
near Mallia. I n experi ment s A. bimaculata onl y react ed to O. sphegodes aggr. and
never to O. transhyrcana. On t he ot her hand A. morio never react ed to O. sphegodes
aggr. Fr om these findings t wo mat t ers mus t be clarified. The first is whi ch name
shoul d be given to this O. sphegodes aggr.? We agree wi t h REINHARD (pers. comm. )
t hat it is absol ut el y uncl ear whi ch of t he t wo species shoul d be named O. trans-
hyrcana. We t hi nk t hat i dent i fi cat i on of these t wo species f r om her bar i um mat eri al
al one mi ght not be possible. Bot h species have a trilobic l abel l um and in mos t cases
a long, bill-like pr ol ongat i on of t he connective. Thus t he synonymi t y of O. sintenisii
wi t h O. transhyrcana must be reconfi rmed. O. transhyrcana has been descri bed by
mat eri al f r om Tur kmeni a, Russi a (CZERNIAKOVSKA 1923) and O. sintenisii by
FLEISCHMANN (1923) f r om S. Turkey. The second mat t er is t he r econf i r mat i on of
t he i dent i t y of t he so-called O. transhyrcana f r om S. Tur key, Cyprus, and Israel
wi t h t he species di st ri but ed in sout her n Russia, nor t her n Iran, and NE. Turkey.
BERGEL (1987) gives t wo col our pi ct ures of O. transhyrcana f r om N. Aser bei dschan
in S. Russi a whi ch mi ght conf i r m t he i dent i t y of Russi an O. transhyrcana wi t h t he
E. Medi t er r anean O. transhyrcana sensu BAUMANN & K~NKELE (1982).
For assistance on Cyprus we thank our companion JOHN PLANT. For the establishment,
execution, and interpretation of electrophoresis we are very grateful to G. STEINBRi)CK,
M. SCHLEGEL, M. KLEMM, and M. KRAMER (Tfibingen). Also many thanks to CHRISTINE
GUTMANN who measured many flowers. H. REINHARD and P. G6LZ made flower analysis
available to us, gave us many hints for orchid localities and with many opportunities for
productive discussions. For the identification of the bees we thank B. TKALCU and K.
WARNCKE. Moreover we thank SABINE LANGNER and JOHN PLANT for correcting the English
manuscript.
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Addr ess of the aut hors: Prof. Dr H. F. PAULUS and Dr C. GACK, I nst i t ut ffir Biologie I
(Zool ogi e), Al ber t st r asse 21 a, D-7800 Fr ei bur g, Feder al Republ i c of Ger many.