SELECTIVE ATTRACTION OF MALE EUGLOSSINE BEES TO ORCHID FLORAL FRAGRANCES AND ITS IMPORTAXCE IN LOXG DISTANCE POLLEN FLOW
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1 SELECTIVE ATTRACTION OF MALE EUGLOSSINE BEES TO ORCHID FLORAL FRAGRANCES AND ITS IMPORTAXCE IN LOXG DISTANCE POLLEN FLOW :'\ORRIS H. WILLIAMS' AND CALAWAY H. DODSON Department of Biology, University of Miami, Coral Gables, Florida 3312 Received February 26, 1971 It has been known for some time that male bees of the tribe Euglossini visit and often pollinate various orchid flowers (Dodson and Frymire, 1961a, 1961b; Dodson, 1962, 1967; Vogel, 1963, 1966; van der Pijl and Dodson, 1966; Dressler, 1967, 1968a, 1968b). The syndrome of "euglossine pollination" was discussed by Dress Ier (1968b). He noted that the orchid flowers that are pollinated exclusively by male euglossine bees are very fragrant, but are almost always lacking in nectar; therefore, no food is present. The source of the attraction was recognized as the fragrance of the flower, but the identity of the odor components was not known for a number of years. Eleven compounds from orchid floral fragrances were identified (Hills et al., 1968), but only some of the compounds were shown to be attractants of male euglossine bees (Adams, 1968; Dodson et al., 1969). Adams showed that some of the compounds from orchid fragrances modified the attraction potential of other fragrance components, and that some of the compounds were not attractive to male euglossine bees. Several additional compounds have been identified from orchid floral fragrances (Dodson and Williams, unpublished), some of which have been demonstrated in field tests to be active attractants of male euglossines, while other compounds have been shown to modify or reduce the attraction potential of various other odor components. The behavior of the bees on the flowers and at the isolated odor components has 'Current address: Visiting Research Associate in the Department of Botany, Smithsonian Institution, Washington, D.C. 26. EVOLUTION 26:8-9. March 1972 been discussed in detail elsewhere (Vogel, 1966; Dressler, 1968b; Dodson et al., 1969). The detailed description of the motor patterns of the bees as they transfer the collected chemicals from the front tarsi to the hind tibiae has also been discussed elsewhere (Evoy and Jones, 1971). The chemicals to which the male euglossine bees are attracted are found in other plant families (Gesneriaceae, Araceae, and Solanaceae) which are pollinated to a limited extent by male euglossine bees (Dodson, Dressler, Hills, and Williams, unpublished). For the most part the floral fragrance components are commonly occurring plant products, either terpenoids or aromatic compounds. The identification and availability of various pure forms of orchid odor components has made it possible to attract large numbers of male euglossine bees in a given area. In many cases poorly known or seemingly very rare species have been collected in large number when attracted to the odor components. The use of odor components as attractants has also made it possible to obtain a much better idea of geographical distributions of many species. The experiments reported here were designed to test the effects of mixtures of compounds on the attraction of euglossine bees. An experiment was also designed to test the effects of combining two (or more) known attractants. Several compounds which had seemed to be poor attractants in previous field trials (ocimene, beta-pinene) were tested to determine if they had any effect on reducing the attraction potential 8 of known attractants. In some cases the compounds have not been positively identified in orchid floral fragrances, but are
2 ECGLOSSI:\'E BEES A:\'D ORCHID FLORAL FR.-\GRA:';CES 8 TABLE l. Euglossine bees collected at jlowers at Dtnoa, Gu yana. Female bees are marked with all asterisk. Bees!1 <>. Flowers...': ;; '" :::- e " ee " "-. ;:.:z.': 7 -e.".s "".,"!1!1 ",. t "'" 1 ;; " ;; ;; " ; E t..l "..., U U U c, " G Euglossa augaspis E. chlorosoma E. cognata 1 E. cordata 1 E. liopoda 19 E. mixta 1 E. sp. UM-lO 1 E. sp. RD Eulaema bombijormis E. cingulata * 1* E. aff. luteola 1 E. meriana E. mimetica 1* E. mocsaryi 2* E. peruviana Euplusia elegans 2* E. sp. UM-2 1 Totals :\'. species attracted structurally similar to compounds which have been identified from orchid floral fragrances. For example, methyl isoeugenol is not known to occur naturally in orchid fragrances, but is similar to eugenol, and methyl ionone is similar to ionone. MATERIALS AND 1\IETHODS Chemicals which had been identified from orchid floral fragrances (Hills et al., 1968) by gas chromatography were purchased from various organic chemical supply houses (Eastman Organic Chemicals, Aldrich Chemical Company, K & K Laboratories, Matheson Coleman Bell). The commercially obtained compounds were checked for purity by gas chromatography using the techniques outlined in Hills et al. ( 1968). The parameters of the gas chromatograph and the methods of component identification have been previously published (Hills et al., 1968). Due to technical difficulties, it is more practical to use commercially obtained reagents than to try to obtain the components directly from the orchid flowers. The odor components were presented on two-inch square pads of blotter paper and attached to trees in the area being sampled. Each pad was saturated with a given chemical in liquid form and was replenished as the liquid evaporated. It is only those compounds that still attract after several hours that are not replenished every ten-fifteen minutes. An average time interval is about 2 minutes, but some are replenished more often and others less often. In all cases the pads are replenished well before they become dry and
3 86 N. H. WILLIAMS AND C. H. DODSON TABLE 2. Male euglossine bees collected at chemical compounds at Dtnua, Guyana. Chemicals ṣ ṩ."" "" o s ' Bees...r: c. :;;: Aglae caerulea Eujriesea pulchra Euglossa augaspis E. chalybeata E. chlorosoma E. cognata E. cordata E. aff. crassipunctata E. aff. cyanaspis E. decorata E. im perialis E. intersecta E. liopoda E. mix/a E. stilbono/a E. /ridentata E. sp. UM-lO E. sp. UM-11 E. sp. UM-12 E. sp. :l.d-92 E. sp. RD-11 E. sp. RD-l18 Eulaema bombijormis E. dngulats E. meriana E. mocsaryi E. nigrita Euplusia auriceps Exaerete smaragdina E. /rocan/erica Total No. species attracted well before bees cease to come to the pads. The following laboratory experiment also supports our sampling technique. We have saturated pads with a variety of chemicals such as cineole and eugenol. The pads were then placed in separate sampling jars, and after a period of equilibration the "head space" of each jar was analyzed by gas chromatography. Such sampling was repeated over long time periods. Chemicals such as cineole evaporate rapidly from the pads, while eugenol does not; the gas chromatographic analyses confirm this. We have consistently replenished our pads before they dry out. We have obtained similar results using bottles of the chemicals with wicks attached. While our intervals of replenishment are somewhat subjective, we feel that they are more than adequate for field work of this nature. All
4 EUGLOSSI:\E BEES A:\D ORCHID FLORAL FRAGR.\:\CES 87 TABLE 3. Male euglossine bees collected at mixtures of compounds at Dauia, Guyana. Benzyl acetate (BA); methyl salicylate (MS); methyl cinnamate (Me); eugenol (E); stock (.8% alpha-pinene,.1% beta-pinene, 3% myrcene, 9% cineole)...;; Compounds u ::;.. - '" :::.... -e- g" e " " E" - '" - '. " '.. < -e < -e s ' ".:l " - c :& 1 "... c < -e -r. :fl lfj c Bees Vi Vi Vi Vi Vi ::'l ::'l ;::: ::; Z :fi Eujriesea pulchra 3 Euglossa augaspis E. chalybeata E. chlorosoma E. cordata E. intersecta 1 1 E. ioprosopa E. liopoda E. mixta 2 E. stilbonota 2 3 E. tridentata 3 E. sp. RD-92 E. sp. RD Eulaema bombijormis E. cingulata 8 2 E. meriana 1 8 Exaerete smaragdina Total :\. species attracted "" bees that landed on the pads were captured for identification, since microscopical examination is necessary for the identification of most species. Moure's (1967) treatment of the euglossine bees is followed for the most part in this paper. These experiments were conducted at the Dawa Field Station, Dawa, Republic of Guyana, during late March and early April, 197. Dawa is located about twenty miles from the Atlantic coast in degraded tropical rain forest. Much of the area has been cut over and allowed to grow up in second growth vegetation. The area is at an approximate elevation of 3 meters with very small hills and a generally sandy substrate. During the first several days of collecting at Dawa, the area was sampled using pure chemical compounds which had been identified as components of orchid floral fragrances. Male euglossine bees were also collected at all orchid flowers that were in bloom at that time which possess the "euglossine syndrome." Several bees were also collected visiting food plants for nectar. This collecting was done to establish a background count of species which were present in the area during the time of the experiments and to obtain an idea of which species of bees would be likely to visit the mixtures of compounds which were to be presented later. RESULTS AND INTERPRETATIONS Most of the euglossine bees collected at Dawa (see Tables 1-) were caught as
5 88 X. H. WILLIAMS AD C. H. DODSOX they visited pure samples of orchid floral fragrance components, although a few species were collected visiting orchid flowers or the flowers of food plants. Of the species in six genera, several species are yet undescribed but previously known from other areas, while a few appear to be previously unknown species (Dodson, Dressler, and Williams, unpublished). All bees which were collected while visiting flowers are listed in Table 1. The four species of Catasetum which are listed were visited only by male euglossines, as would be expected from previous knowledge of the genus (Dodson, 1962; Dressler, 1968b). The non-orchidaceous flowers were visited by both male and female bees searching for food. Food in the form of nectar is offered in illandevilla spp. (Apocynaceae), Odontadcnia sp. (Apocynaceae), and Palicourca sp. (Rubiaceae). Food in the form of pollen is present in the species of Cassia (Leguminosae ), which was visited only by female bees. Table 2 lists the more than bees which were collected at Dawa which were attracted to pure chemical compounds. These data show that certain compounds are better attractants than others. Benzyl acetate, cineole, eugenol, and methyl salicylate are all identified as present in orchid floral fragrances, and all are very good attractants. Vanillin, 2-phenylethyl acetate. and ocimene are also found in orchid fragrances, but are not good general attractants. Methyl isoeugenol and methyl ionone are not known to occur in orchid fragrances and are not good attractants. Table 3 lists the species of bees which were collected during a three day experiment to determine the effect of mixtures of compounds as attractants. "Stock" is a mixture of four compounds in the percentages found in a number of euglossine-pollinated orchids (.8% alpha-pinene,.1% beta-pinene, 3% myrcene, and 9% cineole). Table 3 shows the striking effect that several odor components have on the attraction potential of other odor components. Euglossa chalybeata is attracted to stock TABLE. Male euglossines collected at various chemicals and mixtures at Dawa, Guyana. Chemicals <- ] l.. "'6 - en w - ;., <O!I <O!I ec if) Bees ;:;; ;:;;... w" Eujriesea pulchra 7 3 Euglossa augas pis 3 E. chalybeata E. chlorosoma 3 E. cognate 1 E. aff. crassipunctata 1 E. im perialis 1 E. liopoda 21 E. mixta 3 2 E. stilbonota 3 2 E. sp. RD Eulaema bombijormis 9 E. cingulata 3+ E. meriana 9 8 E. mocsaryi 1 Euplusia auriceps 1 Exacrete trochonterica 2 Total X o. species attracted (Table 3) and pure cineole (Table 2); it comes to a 3: 1 mixture of stock and benzyl acetate in low numbers but not at all to 1: 1 mixtures (Table 3) or to pure benzyl acetate (Table 2). Euglossa chlorosoma (a species allied to E. chalybcata) is attracted to pure benzyl acetate (Table 2): it comes to 1: 1 and : 1 mixtures of benzyl acetate and beta-pinene in low numbers (Table 3) and to 1: 1 mixtures in slightly larger numbers (Table 3). For simplicity of discussion Table 3 is broken down into Tables and. Table shows the reciprocal effects of eugenol and methyl salicylate on the attraction potential of each other, as well as the effects of stock on the attraction potential of methyl salicylate. Eugenol in combination with methyl salicylate destroys the attraction of all species which were attracted to methyl salicylate alone, with the exception of one specimen of
6 EUGLOSSIE BEES A:'\D ORCHID FLORAL FRAGRA:,\CES 89 TABLE. Male bees collected at cineole, stock, ocimene, and mixtures at Dawa, Guyana. Attractants " ".. "8 " '" '" ". Bees U " <7l <7l <7l -t- Ql.ll: C... (,) Ql III bil >. >.... :::I.ll:.J: U III.-I Ql.-I (,)... Ql III III.-I... III III E III E It') E Euglossa augasips 1 E. chalybeata E. chlorosoma 1 E. cordata 6 1 E. afl cyanaspis 6 E. im perialis 1 E. intersecta 1 3 Ei liopoda E. stilbonota E. tridentata 3 2 E. sp. UM-lO E. sp. UM-ll 2 E. sp. UM-12 E. sp. RD Eulaema meriana E. nigrita 1 Exaeret e smaragdina Total :'\. species attracted 1 8 'Yo species attracted to cineole % species attracted to stock which are repelled by ocimene Eulaema bombiiormis. Methyl salicylate destroys the attraction of all species which were attracted to eugenol alone, i.e., Eulaema cingulata. Six species which are attracted to methyl salicylate alone are not attracted to a : 1 mixture of methyl salicylate and stock. The attraction of at least four additional species (Eufriesea pulchra, Euglossa chalybeata, Euglossa liopoda, and Eulacma bombiiormisi is reduced by the : 1 mixture of methyl salicylate and stock. Eulaema meriana is attracted to both cineole and methyl salicylate (Table 2) and is attracted to stock in low numbers (Table 3): it is attracted to methyl salicylate and to a : 1 mixture of methyl salicylate and stock in approximately equal numbers 1 \ FIG. 1. The effects of stock, methyl salicylate, and eugenol on the attraction of Euglossa chlorosoma (open squares) and E. cholybeata (solid squares). When two good attractants (stock and methyl salicylate) are combined Euglossa cholybeata is attracted in reduced numbers. The combination of eugenol and methyl salicylate failed to attract either of these species.
7 9 N. H. WILLIAMS AND C. H. DODSON 8 Q) Q) c c Q) c Q) Q) u Q). E IV till o u Q) E >. ;j CIl c Q) s: >. en... Q)....,. u U Gl U U... U Q) en en... c u IV en E en E 1 E u III III III \ D-D. D 12 FIG. 3. The effects of cineole, stock, ocimene, and combinations of stock and ocimene on the attraction of Euglossa chlorosoma (open squares) and E. chalybeata (solid squares). The concentration of cineole is decreasing from left to right and the concentration of ocimene is increasing from left to right. FIG. 2. The effects of stock, methyl salicylate, and eugenol on the number of species (circles) and the number of individuals (triangles) attracted. Stock and methyl salicylate are both potent attractants, but when combined the mixture attracted fewer individuals and fewer species than either attractant did alone. (Table ). The effects of stock, methyl salicylate, and eugenol on the attraction of Euglossa chlorosoma and E. chalybeata are shown in Figure 1. The addition of a small amount of stock to methyl salicylate (Table ) reduced the number of individ-
8 EUGLOSSINE BEES AND ORCHID FLORAL FRAGRACES CIl.:.:: 1 u C.. u l>. en CIl C CIl CIl C CIl E E u u CIl.. CIl c.:.::.:.:: u... u E.... u en en FIG.. The effects of cineole, stock, ocimene, and combinations of stock and ocimene on the number of individuals (triangles) and species (circles) attracted to cineole. The concentration of cineole is decreasing from left to right and the concentration of ocimene is increasing from left to right. uals attracted from 83 to 3, and the number of species from 1 to 9 (Fig. 2). Table shows the effects of combining stock and ocimene and the effects of the minor components of stock on the attractant cineole. Seven species which are attracted to cineole are not attracted to stock. Four additional species which are attracted to cineole (Euglossa cordata, E. stilbonota, Euglossa sp. RD-92, and Eulaema mcriana) are attracted in reduced numbers to stock. Exaerete smaragdina is attracted to stock in larger numbers than it is attracted to cineole. Three species which are attracted to stock are not attracted to a 1: 1 mixture of stock and ocimene; two additional species (Euglossa chlorosoma and E. chalybeata) which are attracted to stock are attracted in low numbers to a 1: 1 mixture of stock and ocimene. Five species which are attracted to stock are not attracted to a : 1 mixture of stock and ocimene. Three species which are attracted to a 1: 1 mixture of stock and ocimene are not attracted to a : 1 mixture of stock and ocimene. Euglossa chalybeata is attracted to cineole, stock, and mixtures of stock and ocimene in decreasing numbers but is not attracted to pure ocimene (Fig. 3). One species (Euglossa tridentata) was attracted to stock with ocimene but not to stock alone. Ocimene is a very poor attractant and attracted only one individual each of four species. One species (Euglossa stilbonota) was attracted to cineole, stock, ocimene, and mixtures of stock and ocimene. Of the species which are attracted to stock, ocimene in low concentration ( 1: 1 stock: ocimene) reduces the attraction of 37.% of the species, and ocimene in high concentration (: 1 stock:ocimene) reduces the attraction of 62.% of the species. The presence of alpha-pinene, betapinene, and myrcene in cineole to form stock reduced the number of individuals attracted from 83 to and the number of species from 1 to 8 (Table ). The additional presence of ocimene in the stock solution reduced the number of species attracted by approximately % and the numbers of individuals attracted by 2 3% (Fig. ). The initial approach of the bees to the mixtures of compounds is similar to their
9 92 x. H. WILLIAMS AD C. H. DODSO); approach to pure compounds; however, bees will often approach a mixture of compounds, hover in front of the pad with the antennae moving slightly, vacillate in front of the pad, not quite touching the pad, and eventually flyaway without landing. This behavior has been observed in response to mixtures of compounds which contain an attractant for a given species with a certain amount of non-attractant, as well as for the compounds which are structurally similar to orchid floral fragrance components. DISCUSSION These experiments show in a simple way that a number of species of euglossine bees may be attracted to a pure compound from an orchid floral fragrance, but that the addition of one or a few additional compounds may reduce the attraction potential of the mixture of compounds. The effect of the reduction of the attraction potential may be seen in both the number of individuals and the number of species attracted (cf. Tables and, Figs. 1-). Dodson (197) showed that the presence of benzyl acetate with cineole reduced the number of individuals attracted from 18 to 2 in a total of six species. He also showed that the presence of alpha-pinene with cineole and benzyl acetate reduced the number of individuals attracted from 9 to 6 and the number of species attracted from 8 to 2. It is highly unlikely that the reduction of attraction of eight species in Table is due to sampling error. The probability that this reduction is due to chance alone is (%) H, or one chance in 26 that the presence of stock does not effect the attraction potential of methyl salicylate. The reduction of attraction could be explained on the basis of masking of one odor by another odor; however, we have shown that several species are able to detect minute quantities of a chemical (Dodson et al., 1969). "'hile odor masking is a possible explanation, it does not seem consistent with the experimental results. It is also possible that the reduction of attraction is due to a synergistic inhibition of receptors or an inhibition of the pathways of the central nervous system; we have no information either proving or disproving this idea. From the aspect of attracting a specific pollinator to a given species of orchid, the result is the same no matter how the chemicals work: a number of species of bees are not attracted when a fragrance contains certain additional compounds. The presence of a number of compounds in an orchid floral fragrance provides a means for attracting particular species of bees and not others. By attracting only one, or a limited number of species of bees, the floral odor can serve as an isolating mechanism between closely related species of orchids. The presence of some compounds may destroy the attraction to an entire group of bees, for example, the effect of eugenol on species attracted to methyl salicylate (Fig. 2). In 79 species in 1 genera of orchids which are pollinated by male euglossine bees, no species of orchid had eugenol and methyl salicylate in its floral fragrance (Hills et al., 1968). In many species the odors are very similar, but the presence of one additional compound may be sufficient to limit the attraction to only one species of bee. Euglossine bees are attracted to compounds which are structurally similar to the compounds found in natural orchid floral fragrances, but a slight modification of the molecule has a drastic effect on the attraction potential of the foreign compound (Table 2). Methyl isoeugenol is similar to eugenol and differs in the presence of an additional methyl group and the placement of a double bond in the side chain of the molecule. While eugenol attracted over 3 bees, methyl isoeugenol attracted only one bee. This is not surprising when one considers the effects of an additional hydroxyl on a molecule. Methyl salicylate, which has a hydroxyl group, attracted 11 species in central Panama, while methyl benzoate, which lacks the hydroxyl but is otherwise identical, attracted only
10 EUGLOSSIXE BEES AXD ORCHID FLORAL FRAGR.-\XCES 93 two species in the same area (Dodson, 197). Both of these compounds are present in orchid floral fragrances, often in the same species. These compounds may have the same effects on the attraction potential of each other as eugenol and methyl salicylate do on each other. Since naturally occurring compounds differing slightly have pronounced effects as attractants, it is not surprising that artificial modifications also have pronounced effects. Janzen's (1971) hypothesis of long distance pollination may be extended to include the visits of male euglossines to orchid flowers, as well as to flowers of other plant families which possess the "euglossine syndrome." Long distance pollination of orchids by male euglossine bees was first suggested by Dressler (1968b). Although the actual distances flown by male euglossines is not known, it is supposed that they have fairly wide flying ranges. Dodson (1966) noted that male euglossines leave the nest upon hatching and do not return to the nest. 'Ye have repeatedly experienced difficulty in trying to mark and recapture male euglossines over periods of several days, even when large numbers of male bees were marked. This failure to recapture more than one or two of the male bees may be explained in three ways: 1) the bees are disturbed by the marking technique and do not return to the floral odors, 2) the bees are present in extremely large populations and the chance of recapturing a marked bee is very low, or,)) the bees move over a fairly large range during their search for food plants and flowers from which to collect the necessary odor chemicals. There is some evidence to reject the first alternative. When male bees which have been rubbing on a pad saturated with an orchid odor are captured, shaken violently (often with slight wing damage) and thrown into the air, a number of them will return in a few minutes to the pad. Tn some cases the bee would return immediately. This indicated that handling the bees does not disturb them enough to account for the lack of recaptures on the following days. Further, marking experiments in which the bees were not captured, but marked with a spot of paint while gathering the chemicals have given the same very low percentage of returns (Mrs. A. H. Powell, indirect pers. comm. via Dr. R. L. Dressler). The second alternative has been neither proven nor disproven. Proof must await further field experiments. If the third alternative is correct, even to a limited extent, male euglossine bees may serve as agents for gene dispersal in the orchids which they pollinate over fairly long distances. There are four areas in central Panama which are especially good localities for collecting both euglossine bees and orchids: the hills north of El Valle, the region around Cerro Campana, the Cerro Jefe region, and the logging road in the Cerro Santa Rita area. El Valle and Cerro Campana are several hours apart by road, but are only about 2 km from each other in a straight line, which should not be outside the range of a large male euglossine bee in one day. The distance from Cerro Jefe to Cerro Santa Rita (about km) should be in the flight range of a male bee, if not in one day certainly in a few days. The distance from Cerro Campana to Cerro Jefe or Cerro Santa Rita (8-9 km) should be within the range of a male bee in a few days or a week's flight time. It should be remembered that pollen of orchids is in one compact unit (the pollinarium) and is viable for long periods of time (up to a year, although usually less). The pollinarium is firmly attached to the bee and is not easily knocked or brushed from the bee, nor is it removed by wind. Long distance gene flow is more likely by the method of pollen flow (by means of pollen transfer by male bees) than by means of gene flow through seed dispersal. Although it is true that orchids have extremely small seeds which are easily carried about by wind currents, the chance of a seed germinating, or even landing in
11 9 x. H. WILLIAMS AND C. H. DODSON a favorable location for germination is probably quite small. The method of pollen flow is more likely to meet with favorable results, since the male euglossine bee is actively seeking the orchid flowers on the basis of selective attraction to the floral fragrance chemicals. The vicinity of the parent plant should be more favorable for germination than the habitats into which randomly wind dispersed seed might fall. While this method of gene dispersal is probably most important in terms of orchids pollinated by male euglossine bees, male euglossines also visit a number of other plants in several families. Male euglossines are important pollinating agents of certain members of the Gesneriaceae, Solanaceae, Apocynaceae, Convolvulaceae, Bignoniaceae, Araceae, Marantaceae, Costaceae, Rubiaceae, and possibly additional families. Although certain members of the Gesneriaceae, Araceae, and Solanaceae are visited by male euglossines for the purpose of collecting odor components, the remaining families are visited as food sources by males in search of nectar (these families are also visited-and probably more intensively-by foraging females). All the nectar producing flowers listed by Janzen ( 1971) are visited and pollinated by both male and female euglossine bees. In all of these families pollen is deposited on the bee and is carried for varying distances. While male bees may visit nectar producing flowers less intensively than the females, their contribution to long-distance pollination may be disproportionate if they are not tied to a fixed (even if large) foraging area as the females must be. There is little or no evidence to indicate that male euglossines return to a given area to sleep each night. Male euglossines are known to sleep in flowers (Dodson, 1966), and they may start foraging each day from a different locality. If this is true, male euglossines would have a wider foraging range than females, and would be more important than females as agents of long distance pollen flow. A number of plants pollinated by male euglossines have widely dispersed populations, often occurring as a single plant per acre (Dodson, unpublished), comparable to the thin distribution of a number of rain forest trees. Just as long distance pollination is important for these tree species, so must these herbaceous species depend upon long distance pollination. Their population structure is not explainable on the basis of pollination by insects with short flight ranges. Female euglossines may be attracted to the flowers by sight at close distances, or perhaps by odors at greater distances, but to our knowledge there is no evidence concerning the method of attraction of female euglossines to flowers other than random searching. However, we have presented here and elsewhere clear evidence that male euglossines are attracted by the odor components of these orchids. The odors of the flowers pollinated by male euglossines are therefore serving a dual purpose: they act as attractants of pollinators in dispersed populations by increasing the area of recognition of the flowers, and they also act as isolating mechanisms between interfertile species by selectively attracting one (or a very few) species as a pollinator. The placement of the pollinarium in orchids as an isolating mechanism was discussed by Dressler (1968b). SUMMARY Male euglossine bees may be attracted to pure chemicals which have been identified from orchid floral fragrances. The attraction of these bees may be reduced by the addition of other compounds which also have been identified from orchid floral fragrances. An additional compound may completely destroy the attraction of a species or group of species when present in a mixture with a potent attractant. Chemicals which are not known from orchid floral fragrances but which are structurally similar to orchid fragrance components attract a few bees, but these structurally
12 EUGLOSSI"E BEES A"D ORCHID FLORAL FRAGRA1\'"CES 9 similar compounds are not good attractants. Orchid floral fragrances may increase the area of recognition of flowers pollinated by male euglossine bees. It was suggested that male euglossine bees might be important agents for long-distance pollination of orchids and other plants which attract the bees to the floral odors, as well as plants which the male bees visit for food. ACKNOWLEDGMENTS "'e would like to thank Dr. Robert L. Dressler, Dr. Thomas E. Pliske, and Hans Wiehler for reading and criticizing the manuscript and for many useful discussions. The research reported here was supported by KSF grant GB to CHD. Kiat W. Tan and Katherine Gregg aided in the collection of some of the bees. LITERATURE CITED ADAlI1S, R. M The attraction of Euglossini (Hymenoptera: Apidae) to fragrance components of orchid flowers. Ph.D. dissertation, University of Miami, Coral Gables, Florida. DODSOX, C. H Pollination and variation in the subtribe Catasetinae (Orchidaceae). Ann. Mo. Bot. Gard. 9: Ethology of some bees of the tribe Euglossini (Hymenoptera: Apidae). J. Kansas Ent. Soc. 39: Relationships between pollinators and orchid flowers. Atas do Simposio sobre a Biota Amazonica : The role of chemical attractants in orchid pollination. Biochemical Coevolution. Oregon State University Press DODSON, C. H., AND G. P. FRYMIRE. 1961a. Natural pollination of orchids. Mo. Bot. Gard. Bull. 9: , AND b. Preliminary studies in the genus Stanhopea (Orchidaceae). Ann. Mo. Bot. Gard. 8: DODSON, C. H., R. L. DRESSLER, H. G. HILLS, R. M. ADAMS, AND N. H. WILLIAMS Biologically active compounds in orchid fragrances. Science 16: DRESSLER, R. L Why do euglossine bees visit orchid flowers? Atas do Simposio sobre a Biota Amazonica : a. Observations on orchids and euglossine bees in Panama and Costa Rica. Rev. BioI. Trop. 1: b. Pollination by euglossine bees. Evolution 22: Evov, W. H., AND B. P. JONES Motor patterns of male euglossine bees evoked by floral fragrances. Anim. Behav. 19:79-8. HILLS, H. G., N. H. WILLIAMS, AND C. H. DOD SON Identification of some orchid fragrance components. Amer. Orch. Soc. Bull. 37: JANZEN, D. H Euglossine bees as longdistance pollinators of tropical plants. Science 171:23-2. MOURE, J. S A checklist of the known euglossine bees (Hymenoptera, Apidae). Atas do Simposio sobre a Biota Amazonica :39 1. PIJL, L. VAN DER, AND C. H. DODSON Orchid flowers; their pollination and evolution. University of Miami Press. Coral Gables, Florida. 21 p. VOGEL, S Das sexuelle Anlockungsprinzip der Catasetinen-und Stanhopeen-Bliiten und die wahre Funktion ihres sogenannten Futtergewebes. Osterr. Bot. Zeitschr. 11: Parfiimsammelnde Bienen als Bestauber von Orchidaceen und Gloxinia. Osterr. Bot. Zeitschr. 113:
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