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Origin of Insect Pollination the Figure) SCIENTIFIC CORRESPONDENCE its proboscis to suck the droplets (c, din Origin of insect pollination the figure). Moths visiting male strobili sometimes probed the nectar secreted SIR - The Gnetales, a bizarre order of secretion started at about 18:00 h, and among male flowers and then their prob­ gymnosperms thought to be a sister group ceased by 21:00 h in male and by 20:00 h in osces touched the microsporangia. Moths of angiospermsu, comprise three distinct female strobili, respectively. If droplets fluttered slowly between strobili and the genera, Ephedra, Welwitschia and Gne­ remained intact, the mean standing crop mean time spent on a strobili was 485 s tum; the first two are xerophytic and of a droplet increased to 0.164 in male and (n=5, range 72-1, 155). Moth visits per pollinated mainly by wind and partly by to 0.190 J.ll in female strobili at 21:00 h (a, strobilus per night were more frequent on 3 insects . Gnetum is restricted to tropical bin the figure). We did not observe rapid a male (1.74 ± 0.62, n=6) than a female rain forests and its pollination mechanism withdrawal of droplets after pollination. strobilus (0.67±0.28, n=3). Each male has not been definitely established. We The droplets contained sugar, the con­ and female strobilus was visited about 8. 7 have observed insect visits to a dioecious centration of which ranged from 3 to 13%, and 3.4 times on average respectively shrub. Gnetum gnemon, in a lowland which is lower than that of an entomophi­ during the flowering period, which is mixed dipterocarp forest in Sarawak, lous Ephedra (72- 80%) 7 but is higher than about 5 days. Malaysia. Pollination droplets were sec­ that of anemophilous conifers (for exam- The pollen grains are inaperturate and reted from ovules on female strobili and sticky while a pollenkitt is absent. All the from sterile ovules on male strobili in the 18 moths collected on male strobili had evening and were consumed by nectar­ pollen grains attached on probosces and seeking moths ofPyralidae and Geometri­ antennae and, much less frequently, on dae. Sticky pollen was attached on prob­ tarsi of legs. Although there were no osces and antennae of these moths. The pollen grains attached on a moth collected moth attraction in Gnetum would have on a female flower , the same species was arisen from unspecialized entomophily, collected on male strobili. which is thought to be an original pollina­ Most Gnetum species, even tall clim­ tion system of early Gnetales and early bers, flower in the understory of rain 4 angiosperms . forests where the humid habitat is least One hypothesis of the angiosperm di­ suitable for anemophily. Gnetum strobili, versification in the Cretaceous is the adop­ by emitting droplets as a nectar reward 5 tion of insect pollination . Recent and odour as an attractant, attract noctur­ palaeobotanical evidence suggests that nal moths. Gnetum does not have typical early Gnetales and early angiosperms co­ moth flowers in a classical anthecological occurred in mesic floodplain habitats and sense because petals are absent and the had similar vegetative morphology (small nectar reward is exposed. However, the 6 herbs or shrubs) , similar ecological toler­ nocturnal pattern of droplet secretion, the ances and similar reproductive biology low sugar concentration of the droplet and (flowers simple and pollinated by wind or fragrancy coincide with the moth­ 4 unspecialized nectar-seeking insects) . pollinated flower syndrome. High relative Thus, pollination systems of extant One­ humidity and stillness of surrounding air tales may hold the key to the problem of in the evening favour this pollination angiosperm radiation. Among the three system , which is also adopted in Nepen­ genera of the Gnetales, anemophily is th es (Nepenthaceae) in the Palaeotropics 10 prevalent in Ephedra and entomophily is . We believe that the moth attraction in known in only a few species of Ephedra7 Gnetum derived from unspecialized en­ and rarely in Welwitschi{[' . Gnetum is an tomophily as observed in Ephedra and enigmatic genus: little is known of its Welwitschia after the divergence of long­ pollination biology, although there are tongued lepidopterans which coevolved Strobili of Gnetum gnemon in the evening in a some morpholo~ical indications that point with deep angiosperm flowers in the late to entomophily . tropical rain forest in Sarawak. a, Sterile Cretaceous. ovules emitting droplets (male strobilus); b, MakotoKato In the Malayan region, 16 species of fertile ovules emitting droplets (female strobi­ Gnetum are known; two are trees or lus); c, a male strobilus visited by a pyralid Biological Laboratory, Yoshida College, shrubs and others are woody climbers. We moth, Herpetogramma sp.; d, a female strobi­ Kyoto University, Sa kyo, Kyoto 606-01, studied the Floral biology of a dioecious lus visited by a pyralid moth, Hedylepta sp. Japan shrub, Gnetum gnemon Linne var. tener­ Tamljllnoue um Markgraf, in a lowland mixed dipter­ ple, Pinus, 1.2 %)~. The sugar concentra­ Centre for Ecological Research, Kyoto ocarp forest in Lambir Hills National tion of the droplet was affected by the University, Shimosakamoto, Otsu 520-01, Park, Malaysia W 2' N, 113° 50' E, relative humidity of the surrounding air, Japan altitude 60 m) . We observed Flowering which usually increased to more than 95% throughout the year, but the flowering in the evening in the forest floor habitat. 1. Crane. P. Ann. M. Bot. Gdn72. 716-793(1985). 2 . Doyle, J. A. & Donoghue. M.J. Paleobiology19. period of individual shrubs was less than 3 Nectar was also secreted among micros­ 141- 167 (1993). weeks. In preliminary observations made porangiphores on male strobili, although 3 . Kub ltzki K. in The families and genera of vascular plants vol.1 (eds Kramer. K. U. &Green, P. S.) 378-391 in the daytime between 21 and 30 Novem­ in very small amounts. (Springer. Berlin. 1990). ber 1992, we found no flower visitors. We Male strobili secreting droplets had a 4. Lloyd. D. G. &Wells. M. S. Pl. Syst. Evo/.181, 77- 95 made night observations between 5 and 31 strong odour, whereas female strobili (1992) 5 Friis. E. M. eta/. (eds.) The Origins ofAngiosperms and August 1993. were less fragrant. Probably attracted by Their Biological Consequences (Cambridge Univ. Press. Ovules on female strobili and sterile the odour, nocturnal moths of Pyralidae 1987). 6. Crane. P.R. eta!. Am. J. Bot. 74.1722-1736 (1987). ovules on male strobili secreted pollina­ and Geometridae visited the strobili be­ 7. Sino. R. J. eta/. Proc. Koninkle Nederl. Aka d. Wetensch. tion droplets in the evening. Sequential tween 18:00 and 21:00 h. We found nine C87,1·-24 (1984). 8. vanderPijl, L.Ann. Bogor. 1. 77- 99(1953). sampling of droplets of pollinator­ pyralid and four geometrid species. Each 9. McWillian.J. R. Bot. Gaz. 120.109-117 (1955). excluded strobili showed that droplet moth landed on a strobilus and extended 10. Kato , M. Am.J. Bot. 80.924- 927 (1993). NATURE · VOL368 · 17 MARCH 1994 195 © 1994 Nature Publishing Group.
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