during three seasons (1984 - 1986) at three locations: Ma'ale Ephraim, Ein-Gedi and .... London: Academic Press. Addresses of the authors: REUVEN DUKAS, ...
Plant
P1. Syst. Evol. 169, 65-68 (1990)
Systematics and Evolution © by Springer-Verlag 1990
Buzz-pollination in three nectariferous Boraginaceae and possible evolution of buzz-pollinated flowers REUVEN DUKAS and AMOTS DAFNI Received August 7, 1988; in revised form April 12, 1988 Key words: Angiosperms, Boraginaceae, Onosma gigantea, Trichodesma africana, Trichodesma boissieri. - Buzz-pollination. Abstract: Buzz-pollination was observed in three nectariferous Boraginaceae spp. : Onosma gigantea LAM., Trichodesma africana (L.) R. BR. and T. boissieri PosT. An evolutionary pathway from usual nectariferous flowers to typical buzz-pollinated flowers is suggested.
While the anthers of most flowering plants open longitudinally, those of about 20 000 species are poricidally dehiscent (BuCHMANN 1983). In the poricidal flowers, bees are unable to collect pollen by the usual method of brushing and grooming. Only certain bees and syrphid flies are able to collect pollen from these flowers by vibrating the anthers; this behavior is called buzz-pollination (BucHMaN~ 1983). Usually, buzz-pollinated flowers are nectarless (VOGEL 1978, BUCHMANN 1983). Although buzz-pollinated flowers represent about ten percent of the flowering plants, their evolution is still unclear (cf. BUCHMANN 1985). Based on new evidence of buzz-pollination in some nectariferous flowers, we suggest an evolutionary pathway from usual nectariferous flowers to typical buzz-pollinated flowers. Material and methods
The buzz-pollinated nectariferous species observed are the Boraginaceae Onosma gigantea LAM., Trichodesma africana (L.) R. Bm and T. boissieri PosT. Observations were made during three seasons (1984 - 1986) at three locations: Ma'ale Ephraim, Ein-Gedi and Jericho in eastern Israel. Voucher specimens of the plants investigated are deposited in the herbarium of The Hebrew University of Jerusalem. Results
The tube of the pendulous flower of Onosma gigantea contains and conceals the stamen cone. Tube length is 22.6 + 0.8 m m (mean -4- one S.D., n = 25). The lower parts of the introrse anthers are combined and create an annulus, while the upper parts form a cone above the style; the stigma protrudes from the tube. Bees can reach the nectar only by pushing their tongues through the narrow spaces between the filaments. A similar structure is found in several other boraginaceous genera (e.g., Podonosma, Symphytum, Cerinthe); the usual nectar collecting pattern in these genera
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is the same as above. However, in Onosma gigantea two bee species, Cubitalia boyadjiani VACHAL,and Eucera trasalis LEPELETIER(Anthophoridae) were observed hanging upside down on the flowers and vibrating the anther cones. An average visit of C. boyadjiani lasted 0.84 + 0.28 sec (n = 25). Vibration of flowers by the bees forced pollen grains out of the anthers and onto the bees' body. Bees also collected nectar from the flowers. The nectar in Trichodesma africana and T. boissieri is concealed near the base of the ovary in the short flower tube. Access to the nectar is through the grooves between the tube and the exposed stamens. Stamens are introrse and the elongated connectives create a cone around the style; the cone ends with a pore. The flowers are protandrous; in the male stage pollen is dispersed in the hollow cone head, and in the female stage the stigma extends beyond the connectives. Two bee species, Anthophora tarsalis PRIESNER (Anthophoridae) and Hoplitis spec. (Megachilidae), vibrated the flowers of Trichodesma africana and collected pollen in addition to nectar. This is probably the only second evidence of buzzpollination behavior by a megachilid bee (NEFF • SIMPSON 1988). It should be noted that another megachilid bee, Chalicodoma incretum visited the flowers frequently, but for nectar only. In T. boissieriwhich has larger flowers compared to T. africans, buzz-pollination is carried out by several large and medium sized species of Anthophora and Amegila (Anthophoridae) which collect nectar as well. In both Trichodesma spp., buzzing is carried out during the male phase, whereas pollination occurs when bees touch the stigma during nectar collection in the female stage.
Discussion
As far there are only vague ideas about the evolution of buzz-pollinated flowers. BUCHMANN (1985) suggested that poricidal anthers evolved from regular anthers of pollen flowers in which bees were vibrating while collecting pollen. Most of the Solanum-type flowers (sensu VOGEL 1978) evolved from oligandrous nectariferous flowers. Evidence supporting this idea can be found in the rudimentary nectaries in some of these flowers (VOGEL 1978). Therefore, there must be an evolutionary pathway from the nectariferous flowers to the SoIanum-type flowers. The existence of buzz-pollination in the Borago-type (sensu FAEGRI 1986) oligoandrous nectariferous species as the ones mentioned here and others (e.g., CORBET & al. 1988) elucidate a possible evolutionary pathway leading to the pollination syndrome of buzz-pollination in the Solanum-type flowers (Fig. 1). The reduction of stamen number may result in a lower investment in pollen production (VOGEL 1978). Additional ways to lower investment in pollen production are: (1) compact pollen organized in masses (pollinia in Orchidaceae and Asclepiadeceae); (2) nototrobic pollination in which some of the pollen is not accessible to the pollinators (in many Labiatae and Scrophulariaceae; MACIOR 1967, 1974); and (3) concealed stamens protected in the floral tube by hair or scales (mainly Boraginaceae and Bignoniaceae). In a case of pollen shortage, bees could collect pollen from concealed stamens by occasional vibration, in addition to typical nectar sipping. This could lead toward new floral adaptations resulting in an obligate buzz-pollinated flower.
Buzz-pollination in some Boraginaceae Polyandrous
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nectariferous
flowers
Reduced pollen production
Oligandrous nectariferous with regular stamens
flowers
Reduced pollen production
Flowers with pollinia
Nototrobic flowers
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NO change
Concealed stamens in a narrow or closed tube
Bees vibrate flowers for pollen, in addition to nectar sipping
Higher pollen production accompanied by reduction of nectar production
Typical buzz-pollinated flowers
Fig. 1. Possible evolution of buzz-pollinated flowers We thank A. SHMIDA,Y. IVRI, A. WALDENBERG,and R. GILL for comments and help in the field observations. Special thanks go to C. O'TOOLE and D. BAKER who identified the bees. References
BUCHMANN,S. L. 1983: Buzz pollination in angiosperms. - In JONES, C. E., LITTLE,R. J., (Eds.) : H a n d b o o k of experimental pollination biology, pp. 73 - 113. - New York: S. & E. Scientific and Academic Editions. 1985: Bees use vibration to aid pollen collection from non-poricidal flowers. - J. Kansas Entomol. S o c . 5 8 : 5 1 7 - 525. CORBET, S. A., CHAPMAN,H., SAVILLE,N., 1988: Vibratory pollen collection and flower form: bumble-bees on Actinidia, Syrnphytum, Borago, and Polygonatum. - Functional Ecology 2: 1 4 7 - 155.
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FAE~RI, K., 1986: The solanoid flower. - Bot. Soc. Edinburgh (50th Anniversary suppl.), pp. 51 - 59. MACIOR, L. W. 1967: Pollen foraging behavior of Bombus in relation to pollination of nototrobic flowers. - Amer. J. Bot. 54: 359-364. 1974: Behavioral aspects of coadaptation between flowers and insect pollinators. Ann. Missouri Bot. Gard. 61: 760-769. NEFF, J. L., SIMPSON, B. B., 1988: Vibratile pollen-harvesting by Megachile mendica CRESSON (Hymenoptera, Megachilidae). - J. Kansas Entomol. Soc. 61: 242-244. VO~EL, S., 1978: Evolutionary shifts from reward to deception in pollen flowers. - In RICHARDS, A. J., (Ed.): The pollination of flowers by insects, pp. 89-96. - London: Academic Press.
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Addresses of the authors: REUVEN DUKAS, Department of Botany, The Hebrew University of Jerusalem, Jerusalem 91904, Israel. Present address: Department of Zoology, North Carolina State University, Raleigh, NC 27695-7617, U.S.A. - AMOTSDAFNI, Institute of Evolution, University of Haifa, Haifa, Israel.
