Pollination of Ophrys (Orchidaceae) in Cyprus

P1. Syst. Evol. 169, 177-207 (1990) s•lant 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 umbilicata), 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. flavomarginata/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 compounds 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 important 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 pollination (in all other Ophrys spp.) (KULLENBERQ 1961).

Ophrys flowers never produce nectar and are exclusively pollinated by hymenopterous 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 mechanism has been called "pseudocopulation". 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. American orchids (VAN DER P1JL • DODSON 1969; STOUTAMIRE 1975, 1983; BEARDSELL & BERNHARDT 1982).

Sexual deception flowers use the existing sexual behavioural patterns of the pollinator species. During their evolution they acquired signals which mimic those of the female and release male sexual behaviour, leading to successful pollination. This pollination mechanism, therefore, is not a consequence of co-evolution (in the sense of PAULUS 1978, 1988 a; JANZEN 1980), but represents a completely one-sided evolution of the flower in acquiring adaptations leading to the pollination mechanism ofpseudocopulation. In this sense the flowers parasitize the instinctive sexual behavioural patterns of the deceived males (VOGEL 1975).

The relation between the Ophrys spp. and their pollinators is very specific and has been tested in numerous cases in the field (PAULUS & GACK 1981, 1983 b, 1986; VOTH 1984, 1985) (Table 1). The Ophrys pollinator serves as a pregamic isolating mechanism since it effectively isolates the gene-pool of each Ophrys species (PAULUS & GACK 1983 a). Therefore, by identifying the pollinator we can determine the taxonomic status of the p l a n t - a method resulting from the application of the biospecies concept which is unusual in botanical investigations. Application of the biospecies concept to Ophrys leads in most cases to a clear differentiation; however in some cases, attention must also be given to other facts (PAULUS & GACK 1983 a).

In the present work we summarize our observations and tests during a visit to the southern part of the eastern Mediterranean isle of Cyprus during February 28th to March 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, WILHY~ 1975/1976) (Table 2). We found all the species except the late-flowering O. apifera, O. holoserica, and O. mammosa. Only a single case of poll ination has been reported on this island (Andrena flavipes on O. israelitica- cited as O. fusca, BAUMANN & HALX 1972).

Methods

We always try to observe spontaneous visits and pseudocopulations of the pollinator in the natural habitat of the Ophrys plants. As this occurs very rarely we look for swarming sites of males or for flower visiting bee males of the possible pollinators and there we put the Ophrys to test. To test the specifity we often offer several Ophrys spp. together to give the males the choice. Tests and observations were carried out in the field as often as there was the opportunity in order to make the results reproducible for different times and places.

A special bee species only is considered the pollinator after careful observations of its behaviour on the Ophrys flower.

(1) The male has to show intense pseudocopulation behaviour, e.g., a specific, fast and determined approach to the flower, the extrusion of the genital apparatus, copulation movements with the abdomen, in some species humming with the wings.

(2) Another criterion is the removal of pollinia or a pollination with pollinia from a flower visited earlier. Both only happens when the male's behaviour and size is corresponding to the flowers.

(3) Indications of a pollination relationship are given by caught males who carry pollinia of Ophrys on the head or the abdomen. With reservations it is possible to relate these species to certain Ophrys spp. due to the systematical position of the bee.

(4) Some bee species even show pseudocopulation behaviour when they are put into a glass tube together with a flower. This has to be estimated critically as artificial conditions may cause abnormous reactions.

Results

Ophrys kotschyi (Fig. 1). O. kotschyi was just beginning its anthesis in early March. This beautiful species i s - as far as is k n o w n - endemic to Cyprus. The large black and white pat terned flowers (Fig. 1 a, b) show a great similarity to the Aegean O. cretica (VIERr~.) NELSON and for this reason both were considered subspecies within the same species (NELSON 1962, SUNI~RMANbr 1980). However, RENZ (1929) and later DANESCtt & DANESCH (1972: 42) and CAMPBELL (1982) elucidated the rela- t ionship to the Ophrys umbilieata-oestrifera aggr. Recently GOLz & REINttARD (1985) conducted a biometrical analysis revealing a large"Sippendifferenz" between O. kotschyi and O. cretica which does not favour the idea of species identity and possibly not even a close relationship. The supposed pollinator, Melecta tuberculata LIEFTINCK, is only known from collection material with pollinia at tached to the head (Cyprus, Rhodes, and Crete) (LIEFTINCK 1980). F r o m our knowledge on the poll ination of O. cretica f rom Crete, we supposed that M. tuberculata might be the poll inator of O. kotschyi (PAULUS & GACK 1986). In fact, in Cyprus we observed pseudocopulat ions on O. kotschyi by Melecta tuberculata (Fig. 1 c) (Agios Georgios March 4th 1986, several observations under experimental condit ions in the field; Acrotiri, 4 males with pollinia; many observations under artificial condit ions in a hotel room). F r o m these findings it is absolutely clear that this large Melecta is the effective poll inator of O. kotschyi. The same bee species we found to be the poll inator of the late-flowering eastern " fo rm" of O. cretica in Crete (Zagros 30. 3. 1986, Langada and Pilalimata 1. 4. 1986, PAULUS 1988b). The other, early-

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 "form" 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 mentioned concept, same po l l ina to r - same Ophrys spp., this should be an adequate reason for considering O. kotschyi and O.


cretica as synonymous. However, there are good reasons - flower morphology and the statistical analysis of GOLz & REINHARD (1985)- which indicate a convergence between these two Ophrys "forms". If true, the similarity would be the consequence of identical selection pressures working independently and allopatrically through the same pollinator species Melecta tuberculata. Similar explanations could be demonstrated for O. apulica - O. heldreichii - O. episcopalis (= O. holoserica var. maxima) and O. atlantica - O. bertolonii - O. ferrum-equinum (PAULUS & GACK 1986). To confirm the hypothesis of convergence between O. cretica and O. kotschyi more details on plant morphology, 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 Mediterranean area and can be found in Cyprus and eventually southeastern Turkey. It is a species closely related to Ophrys argolica FLEISCHM. (Fig. 2 b), which occurs in Greece. Flowers of O. elegans (Fig. 2 a) are relatively small, the sepals are light or dark rose-coloured, and in most cases markedly curved backwards. The lateral edges of the labellum are mostly so tucked under that 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 joined by a circle directed toward the tip of the labellum; sometimes the design is reduced to two separate rhombic 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 pollinator of O. biscutella (1985, southern Italy) and Anthophora plagiata ILL. to be that of O. delphinensis (N. Peloponnesus, Delphi) (PAULUS & GACK, unpubl.). For this reason we expected to find another Anthophora species as the pollinator of O. elegans. In fact, we discovered the small, silver grey Anthophora erschowi FEDT., an E. European representative of this genus, to be the pollinator on Cyprus (Fig. 2 c). This is now the third Anthophora species as pollinator within this Ophrys group with a spectacles-design on the labellum. This result is remarkable since it suggests that this design is an important optical releaser for some species of the genus Anthophora. For this reason we expect that even the pollinators of O. argolica and O. crabronifera should be species of An- thophora. All members of this Ophrys group with such a labellum design could be considered typologically as closely related. But attention must be paid to the pos- sibility ofconvergences as demonstrated 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 Mediterranean area. O. flavomarginata, originally described as a colour variation of O. umbilicata, was first investigated at the species level by BAt:MANN & K~NKELE (1982). It has been reported on Cyprus, Israel, and, according 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 March 1986, whereas O. umbilicata was in full flower. The flowers of O. flavomarginata are, in comparison to those of O. umbilicata (Fig. 3 a, b, e), larger and wider. The labellum is surrounded by a broad, mostly yellow margin and shows a nearly quadratic or rectangular shape. The sepals are always green. The flowers of O. umbilicata are


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 margin of the labellum is bent up toward the back side, so that the front side of the labellum is oval. The colours of the sepals vary from green to white and different shades of pink. Pink is the dominating colour in the mountainous regions. In spite of these differences the two species often resemble each other (although differentiating between these two in the field seldom leads to any problems) which was the reason for grouping both as subspecies of the same species. GOLz & REINHARD (1985) only found a small "Sippendifferenz" using a statistical method of biometrical discrimination analysis. But considering O. flavomarginata as a subspecies of O. umbilicata ignores their syntopic distribution. If these two forms are really different species then both should have different pollinators acting as isolating mechanisms to maintain their respective gene-pools. Pollinators of both species are still unknown. In Cyprus we found males of the green-eyed long-horn bee Eueera dimidiata BR. pseudocopulating with flowers of O.flavomarginata (Fig. 3 c) and males of the smaller bright brown (freshly emerged) or grey (old) haired Eucera gaullei VACI4. pseudocopulating with flowers of O. umbilicata (Fig. 3 d). In choice tests both bee species reacted specifically, i.e., Eucera dimidiata pseudocopulated 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 would be very difficult any way. It is interesting that Eucera gaullei did not prefer one colour form of O. umbilicata to the other. The pseudocopulations were of the same intensity on plants with green, white or pinkish sepals, even on plants from the mountainous areas, which share a great similarity with O. scolopax or O. oestrifera in that the middle sepalum is sometimes erected (Fig. 3 d) instead of turned toward the lip (Fig. 3 e). This infers that 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.

Another interesting fact is that the pollinator of O. flavomarginata, Eucera dimidiata, also pollinates O. tenthredinifera in Crete (PAULUS 1988 b). According to TKALCU (1978) this bee is distributed throughout N. Africa, Greece, Crete, Cyprus, and the Middle East. This relationship may explain the absence of O. tenthredinifera in Cyprus. The pollinator of O. tenthredinifera in Greece and the western Mediterranean is the long-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 that O. bornmuelleri occurs in two different "forms": small-flowered O. bornmuelleri (s.str.) and large-flowered O. bornmuelleri subsp, grandiflora FLEISCHMANN & 806. Both "forms" have been considered as being conspecific with O. holoserica (SUN- I~EI~MANN 1980). With 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 variability 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


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 both "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 "form" as a new species, O. levantina (GoLz & REINHARD 1985). We concur with this idea and assume that the differences in morphology (e.g., size, shape) between O. bornmuelleri and O. levantina are due to the different selective pressure of two different pollinator species. We have demonstrated 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. bornmuelleri in Israel, one of them was similar but much smaller than 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 than those of O. bornmuelleri and their labella are oriented vertically, while those of O. bornmuelleri are oriented horizontally. The labellum of O. levantina is quadratic, that of O. bornmuelleri triangular (Fig. 4 a). Another marked distinction between the two species are the two humps on the labellum which are pointed and orientated parallel to the gynostemium in O. bornmuelleri but are rounded and oriented at an obtuse angle to the gynostemium 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


Table 3. Known pollinators of Ophrys lutea aggr. a In PAULUS 8,2 GACK (1986) erroneously refered to as A. cinereophila W. b Several males with abdominal pollinia were caught, but no pseudocopulation was observed. Size of the bee, its phylogenetic relationship (subgenus) and the locality where it was caught indicate that the pollinia are derived from the respective Ophrys species, c Including those plants from Puglia with flowers very similar to Ophrys melena from S. Greece. We refer to these plants as melenoid sicula (minor) and not as O. melena RENZ

Ophrys species Pollinator(s) Locality of observation

O. lutea A. (Chlorandrena) cinerea BR. Spain, France, Greece, Italy, Morocco

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.

Crete S. Italy

Greece, S. Italy °, Crete, Lebanon, Rhodes

Israel S. Italy b S. Italy ° Cyprus

S. Greece (NOTH 1985)

never O. levantina. This confirms the separation of the two Ophrys species as suggested by GOLZ & REINI~ARD (1985).

Ophrys sicula ( = O. galilaea FLEISCHMANN & BORNM~LLER). PAULUS & GACK (1986) elevated the small flowered O. lutea subsp, minor to species status because in all our test localities in the Medi terranean area (S. Italy, Greece, Crete, Rhodes, etc.) the two O. lutea " forms" (large- and small-flowered) have different pollinators. Unfortunately, we did not pay at tent ion to the fact that on the species level the name "minor" does not have priori ty over "galilaea". According to BAUMANN & KONKELE (1986) the small O. lutea should be named O. galilaea, at least in its eastern area of distribution. We suppose that all the small-flowered O. lutea "forms" , usually called O. lutea subsp, minor, represent a single biospecies, separated f rom the larger-flowered O. lutea. But the t axonomy is still unclear. According to PAULUS (1988 b) O. galilaea is synonymous with O. sicula.

0. sicula is the only species within the O. lutea group in Cyprus. The flowers are small- to middle-sized, the lips are light yellow-green instead of canary-yellow as in O./urea. The poll inators of O. sicula are several closely related Andrena spp. of the subg. Chrysandrena. The most c o m m o n species is A. hesperia (PAULUS & GACK 1986, WARNCKE & KULLENBERG 1984). In Cyprus several pseudocopulat ions by Andrena torda were observed, but only at a single location. This species is a representative of the subg. Cordandrena, which is, according to WARNCKE (1968), closely related to the Micrandrena-Euandrena-Chrysandrena groups. We are con- vinced that the legitimate pol l inator will be another species of Chrysandrena, maybe A. hesperia or A. merula. The known pollinators of O. sicula are given in Table 3.


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. Pseudocopulation 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


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1984), and Attica (PAULUS & GACK, unpubl.). In Cyprus O. iricolor was in full bloom and we also found A. morio as the pollinator (Fig. 5 a, b).

This Ophrys species, like all members of the O. fusca/lutea group, attaches the pollinia to the tip of the bee's abdomen. In Cyprus we found two males of A. morio with pollinia not only on the abdomen but also with additional Ophrys pollinia attached to the head (Fig. 5 a). It is obvious that these two individuals visited two different Ophrys species. As we will see later, the head pollinia originated from O. transhyrcana. Provided that A. morio visits both Ophrys spp. regularly, it can act as an isolating mechanism for two syntopic Ophrys spp. flowering at the same time. Similar situations are known from tropical Euglossina bees as pollinators of Ca- tasetum (Orchidaceae) (DREsSLER 1968, DODSON 1975).

Ophrys israelitica(= O. fleischmanniip.p.) (Figs. 6, 7, and 8; Table 4). In Cyprus this species, belonging to the O. fusca/lutea group, was in full bloom during the first two weeks of March 1986 (Fig. 6 a, b). According to BAUMANN & DAFNI (1981) "O. fleischmannii" is distributed from Crete, southern Attica, most of the Aegean islands, western and southern coast of Turkey to Syria, Lebanon and Israel. The pollinator was first discovered by BAUMANN & HALX (1972) in Cyprus. They took pictures of pseudocopulating Andrena flavipes on "O. fleischmannii" (cited as O. fusca). This could be confirmed by PAULUS & GACK (1986) in northern Israel (numerous observations of pseudocopulations) (Fig. 7 a) and now in Cyprus as well after numerous observations of A. flavipes males with abdominal pollinia *. Since the flower morphology of "O.fleischmannii" from Israel and Cyprus is very different from that of O. fleischmannii from Crete (Fig. 7 b, c), we postulated two different pollinators and supposed that "O. fleischmannii" from Cyprus and Israel is a new, still unnamed species (PauLuS & GACK 1986). Meanwhile, the pollinator of the Crete O. fleischmannii could be found and identified as Anthophora sicheli RAD., a species which had already been found with pollinia by VOGEL (1976) on Crete. (However, based on the conditions of the locality, he considered the pollinia to have originated from O. iricolor.) This confirms our supposition that the O. fleischmannii from Crete and those from Cyprus/Israel are different species. O. fleischmannii from Crete has been described by HAYEK (1926). The new species now has been described as O. israelitica (BAUMANN & K~NKELE 1988).

Due to our own investigations we are able to give some additional information to the description of O. israelitica. This new species is distributed over Cyprus, N. Israel, Lebanon (KULLENBERG1961), and SE. Anatolia (VOTn 1967, SUNDERMANN & TAUBENI-IEIM 1978 as O. omegaifera) (DAvis 1984). The description of O.fleischmannii given from Naxos and Siros in BAUMANN & DAFNI (1981) refers perhaps to a different O. fusca-form but not to these two species, as the original fotos from

* 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


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


194

8 H. F. PAULUS & C. GACK:

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o oc~ r~

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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). Natural 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 oooooo eoooe o o o ee e o e ° ° ~ a o ° °

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/~ O. fleischmannii

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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 omitted 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 middle 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; Anatolia fot. TAUBENHEIM; Cyprus fot. PETER; as O. fleischmannii); FEINBRUN-DOTHAN (1986: Flora Palaestina 4, Tafelband fig. 520).

As mentioned in PAULUS & GACK (1986) the flowers of the new species look 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


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5'o 6'o 7'o do 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 northern 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 presumably in Anatolia, O.israelitica grows syntopically with O. (einereophila)fusca (see the foot-note on p. 199) and perhaps with other O. fusca forms (except O. flavipes-fusca). But in the whole area O. omegaifera is lacking. From the typical O. fleischmannii HAYEK, which is endemic in Crete, O. israelitica can be distinguished by its colour, shorter hairs, and the surface of the lip, which is nearly plain (Fig. 8 a - h ) . BAUMANN ~; DAFNI (1981) did not distinguish between the genuine O. fleischmannii and O. israelitica. The colour 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 another picture of Acrotiri, which 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 found on Crete which is described as Ophrys sitiaca PAULUS & A. & C. ALIBERTIS (PAULUS 1988 b).

Electrophoretic enzyme analysis is a method to investigate genetic differences between populations and species. These differences possibly serve as taxonomic features (FER~USON 1980). On orchids this method 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 electrophoresis to construct dendrograms.

For Ophrys fleischmannii (Crete), O. israelitica (Cyprus), O. flavipes-fusca (S. Spain), O. kotschyi (Cyprus) 7 enzymes were compared by starch gel electrophoresis (for method see STEINBRUCK • al. 1986). All flowers and leaves investigated orig-


inated from plants which were cultivated in a greenhouse. The following enzymes were tested: Isocitratedehydrogenase (IDH), "Malic Enzyme" (ME), Phospho- glucomutase (Pgm), Phosphogluc'oisomerase (Pgi), Acidic Phosphatase (Acp), Superoxidismutase (SDM), Esterase (Substrate 4-Methylumbelliferyl-propionate) (ES).

Hardly any differences were found among the enzyme patterns of all the individuals of the species O. fleischmannii, O. israelitica, and O. fusca tested. In contrast to this result O. kotschyi shows a different pattern of bands for all enzymes investigated. Since only a few individuals have been tested, the existing data allow only preliminary conclusions. With the utmost caution we conclude that O. fleischmannii, O. israelitica, and O. fusca belong to a group which is genetically very uniform and shows clear differences to O. kotschyi. To delimitate O. fleischmannii and O. israelitica as species the existing data are not sufficient. For that purpose further investigation of more individuals and populations is needed.

Key o f the O. omegMfera aggr.

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 Longitudinal V-shaped furrow at the base of the lip long and distinct, stigmatic groove whose width is about 2 - 2.8 times the height, front edge of the speculum without "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 without a V-shaped furrow o r - if present - then very weak and

short; stigmatic groove whose width is at least 2.5 times, normally more than 3 times its height; front edge of the speculum always with a light "omega", which is seldom weak . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

2 Base of the lip with a flat, very short V-shaped furrow; stigmatic groove whose width is about 2.5 - 2.8 times its height, labellum flat, at its base weakly, sometimes markedly curved down. Lateral lobes very short, curved back. Lip light brown, often with a grey colouring, sometimes blueish. Front 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. Flowering time: J anua ry - March . . . . . . . . . . . . . . O. sitiaca H. F. PAULUS & C. + A. ALIBERTIS (Fig. 10 d)

- Base of the lip without a furrow. Stigmatic groove whose width is at least 3 times its height . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

3 Stigmatic groove whose width is about 4 - 4 . 5 times its height; lip flat, 11 - 15mm long, 8 -12 .5 ram broad, at its base hardly any curvature; lateral lobes extended, rarely turned backwards; speculum shiny, leaden-blue, sometimes blue, rarely brownish, very often marbled with dark and light spots; speculum edged with a whitish "omega". Phenology: January-March . Dis- tribution: Israel, Lebanon, Cyprus, SE. Anatolia. Pollinator: Andrena flavipes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . O. israelitica BAUMANN • KCINKELE

-- Stigmatic groove less broad; width about 3 - 3.5 times height. Lip clearly bent at its base and curved down, lateral lobes more or less close to the lip and curved back; speculum in most cases unicoloured without spots. Pollinators: species of the genus Anthophora . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4


4 Lip large, 13 - 21 mm long, with short hairs, chestnut coloured; speculum brownish with a touch of blue, "omega" grey-blue or blue, seldom whitish. Phenology: end of January (S. Crete) - April. Distribution; Crete, Carpatos, Rhodes, Samos, Kos. Pollinator: Anthophora atroalba subsp, agamoides . . . . . . . . . O. omegaifera

subsp, omegaifera FLEISCHM. - - Lip small, 10 - 15ram long, with long, furry white hairs . . . . . . . . . . . . . . . . . . . . . . 5 5 Species from Crete, speculum leaden-grey, "omega" grey or whitish blue. Phe-

nology: Feb rua ry - March (near the coast) until the end of April (in the mountains). Pollinator: Anthophora sicheli . . . . . . . . . . . . . . . . . . O. fleischmannii HAYEK

- - Species occurring in the SW. Mediterranean region: speculum reddish brown, brown, sometimes brown-violet, "omega" whitish, sometimes white-violet. Phe- nology: J a n u a r y - M a r c h (N. Africa), beginning of March -Apr i l (S. Spain), beginning of A p r i l - M a 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 could only find one species of the O. fusca aggr. (s.str.). It is possible that there are at least tw O species since GOi~z & RHNHAP, D (pers. comm.) have observed, in addition to the most common small-flowered plants, some plants with larger flowers. Most of the common O. fusca in Cyprus have small flowers which have a more or less broad yellow margin (Fig. 13 b, c), in some respects very similar to those from the Turkish coast, on Crete or Peleponnesus. This yellow margin can be bent over, in which case it is not visible from above. At the beginning of March O. fusca was in full bloom. At three different sites (Kandou, Vavla, and Acrotiri) we observed numerous pseudocopulations by An- drena cinereophila * (Fig. 13 a), even performed on flowers with variable size or with variable yellow coloured margins. This is the same species which was found to be the pollinator of a small-flowered O. fusca in southern 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 reaction to other O. fusca "forms". It never showed any interest for these plants. We suppose that this "cinereophila- fusca" is a well separated species distributed only in the eastern Mediterranean region.

Ophrys transhyrcana a n d O . mammosa ( F i g . 1 4 ) . According to previous authors (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 which CZERNIAKOVSKA (1923) described from Turkmenia in southern Russia. According to our findings in Cyprus, there is at least one other large-flowered species from the O. sphegodes aggr. which 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 mentioned above we captured Andrena morio with pollinia on both 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 pseudocopulation with removal of pollinia under natural conditions (Akrotiri), several peudocopulations under artificial conditions (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


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 pseudocopolatory behaviour than 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


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 contradict our previous interpretation since the pollinator of O. transhyreana in Cyprus is different from that 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 other similar cases more data are required to clarify this problem. Nonetheless we offer two alternative explanations:

(1) The flowers tested in Israel may not be O. transhyrcana but rather O. mammosa which are similar to O. transhyrcana in exhibiting a trilobe labellum. In this case the distribution of O. mammosa would reach as far as Israel. But in the Mt Carmel region we have found some plants which may have been genuine O. transhyrcana due to their extreme trilobic lips which were larger than those of plants previously tested. DAFNI & al. (1987) also suppose that there are both species in Israel, one of them a transhyrcanoid O. mammosa. We suppose that in Israel, the actual pollinator of the true O. transhyreana is also A. morio. If this is true, then O. transhyrcana and O. mammosa are different biospecies isolated by two different pollinators, A. (Melandrena) morio and A. (Melanapis) fuseosa, respectively:

(2) Both O. mammosa and O. transhyrcana may be pollinated by A. fuscosa but only allopatrically. With an overlapping (syntopic) distribution, e.g., in Cyprus, O. mammosa retains its pollinator A. fuscosa whereas O. transhyrcana switches to the new pollinator, A. morio, preventing cross-pollination. Similar evolutionary phe- nomena in zoology are known as character displacement (e.g., BRow~ & WILSON 1956). Therefore, characters which serve to isolate the gene-pools of two closely related species should be more different in syntopic areas than in allotopic areas (for further information see FENCHEL 1975, GRANT 1975, SLATKIN 1980). If character 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 natural test for the species status.

Ophrys sphegodes aggr. (Fig. 15). At different sites along the lower mountains of Cyprus-main ly in the region of Pano L e f k a r a - V a v l a - K a t o D h r y s - Mal l i a - Kissousa and Perapedhi - M a 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 Kato Dhrys we found hundreds of freshly opened flowers of this relatively unknown Ophrys which might 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 them as O. aesculapii which is certainly incorrect. According 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



extremely variable in shape and colour. The colour of the labellum varies from dark brown-red to light yellow-brown; the flattened edge of the lip varies in colour from entirely yellow to light brown or dark brown; it can be flat or turned backwards. The shape of the lip varies from clearly trilobic to completely unlobed like a typical O. sphegodes. Length and curvature of the connective varies greatly, like that of O. transhyrcana; the sepals are completely green or weakly to strongly bicoloured, such that the upper half is green and the lower reddish-brown (Fig. 15 a).

We suppose that this Ophrys has been most often confused with O. transhyrcana and was earlier named O. sintenisii. LA~t~WEIqR (1983) shows a flower from Lebanon labelled as O. transhyrcana which resembles exactly those we found in Cyprus. Therefore we suppose that this O. sphegodes aggr. has a wider distribution, mainly in Turkey. It could clearly be demonstrated that this "form" represents a genuine species, since its pol l ina tor-Andrena bimaculata KIp,., a mid-sized brown or grey bee often with a reddish abdominal base - is different from that of O. transhyrcana. This bee species is closely related to A. fuscosa, the pollinator of O. rnamrnosa (WARNCKE 1968). At two sites (Perapedhi and Mandria) we could test the reactions of many male A. bimaculata to O. sphegodes aggr. (Fig. 15 b, c). They clearly showed a strong reaction by pseudocopulating and removing the pollinia almost in every case. Moreover one male with several pollinia attached to the head was caught near Mallia. In experiments A. bimaculata only reacted to O. sphegodes aggr. and never to O. transhyrcana. On the other hand A. morio never reacted to O. sphegodes aggr. From these findings two matters must be clarified. The first is which name should be given to this O. sphegodes aggr.? We agree with REINHARD (pers. comm.) that it is absolutely unclear which of the two species should be named O. transhyrcana. We think that identification of these two species from herbarium material alone might not be possible. Both species have a trilobic labellum and in most cases a long, bill-like prolongation of the connective. Thus the synonymity of O. sintenisii with O. transhyrcana must be reconfirmed. O. transhyrcana has been described by material from Turkmenia, Russia (CZERNIAKOVSKA 1923) and O. sintenisii by FLEISCHMANN (1923) from S. Turkey. The second matter is the reconfirmation of the identity of the so-called O. transhyrcana from S. Turkey, Cyprus, and Israel with the species distributed in southern Russia, northern Iran, and NE. Turkey. BERGEL (1987) gives two colour pictures of O. transhyrcana from N. Aserbeidschan in S. Russia which might confirm the identity of Russian O. transhyrcana with the E. Mediterranean 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.

References

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BALZINGER, E., 1982: Zypern und seine Orchideen. - Bull. Assoc. Philom. Alsace Loraine 19:65 - 70.


BAUMANN, H., DAFNI, A., 1981: Differenzierung und Arealform des Ophrys omegaifera- Komplexes im Mittelmeergebiet. - Beih. Ver6ff. Naturschutz und Landschaftspflege Baden-W/irtt. 19: 129- 153.

- HALX, G., 1972: Qphrys - die Pflanze mit ,,Sex". - Kosmos 68: 7 8 - 8 0 . - KONKELE, S., 1982: Die wildwachsenden Orchideen Europas. Kosmos-Naturfiihrer. -

Stuttgart: Franckh'sche Verlagshandl. 1986: Die Gattung Ophrys L. - eine taxonomische Obersicht. - AHO Mitt. B1.

Arbeitskr. Heim. Orchid. Baden-Wiirtt. 18: 305-688 . 1988: Neue Beitr/ige zur Taxonomie europ/iischer und mediterraner Orchideen. -

AHO Mitt. B1. Arbeitskr. Heim. Orchid. Baden-W/irtt. 20: 610-651 . BEARDSELL, D., BERNHARDT, P., 1982: Pollination biology of Australian terrestrial orchids.

- In WILLIAMS, E. G., KNOX, R. B., GILBERT, J. H., BERNHARDT, P., (Eds.): Pollination 1982, pp. 166- 183. - Parkville, Vic.: University of Melbourne Press.

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Address of the authors: Prof. Dr H. F. PAULUS and Dr C. GACK, Institut ffir Biologie I (Zoologie), Albertstrasse 21 a, D-7800 Freiburg, Federal Republic of Germany.

Documents

Pollination of Ophrys (Orchidaceae) in Cyprus