Why Does the Flower Stalk of Pulsatilla Cernua (Ranunculaceae) Bend During Anthesis?1
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American Journal of Botany 89(10): 1599±1603. 2002. WHY DOES THE FLOWER STALK OF PULSATILLA CERNUA (RANUNCULACEAE) BEND DURING ANTHESIS?1 SHUANG-QUAN HUANG,2,3,5 YOSHITAKA TAKAHASHI,3 AND AMOTS DAFNI4 2College of Life Sciences, Wuhan University, Wuhan 430072, China; 3Department of Livestock and Grassland Science, National Agricultural Research Center for Western Region, Oda, Shimane 694-0013 Japan; and 4The Institute of Evolution, University of Haifa, Haifa 31905, Israel Flower stalks of Pulsatilla cernua, an early spring herb in north temperate Asia, changed position from erect to pendulous and back to erect during 6±10 d anthesis. We tested three possible explanations for this movement. Our results showed that (1) this movement is unlikely to be a mechanism to attract pollinators or enhance pollen output, because no pollinator preference was observed between erect and pendulous ¯owers and we found no buzz-pollination in this species; (2) hand self-pollination yielded higher seed set than open pollination in the ®eld, but spontaneous sel®ng rarely occurred. Among open-pollinated ¯owers, seed set was depressed by emasculation, indicating that in the presence of insects, self-pollen provided reproductive assurance in this protogynous and self- compatible species. However, the change in ¯ower orientation cannot be explained as reproductive assurance in that even self-polli- nation largely depended on pollinator visits rather than gravity. (3) A pollen germination experiment indicated that pollen damage by water is serious in this species. We deduced that the bending of the ¯ower stalk during anthesis was to avoid rain damage to pollen grains in this species. During the 3±6 d period of pollen presentation, the petals elongated and were covered with unwettable hairs. Together with ¯ower stalk movement, this was enough to protect the organs inside the ¯ower from rain. This movement of the ¯ower stalk seems to be important to maintain pollen viability in a rainy habitat with a scarcity of pollinators. Key words: adaptation; ¯ower orientation; ¯ower stalk; pollen viability; pollination; Pulsatilla cernua; rain; Ranunculaceae. Floral traits such as color, shape, size, and symmetry have productive assurance by enhancing self-pollination. (3) Does been interpreted as adaptations to pollinators (e.g., Waser, the ¯ower stalk bend to avoid rain? Rain can damage pollen 1983; Stanton, Snow, and Handel, 1986; Nilsson, 1988; Dafni viability and constrain pollination success (Corbet, 1990; Daf- and Kevan, 1997; Neal, Dafni, and Giurfa, 1998). However, ni, 1996; Jacquemart, 1996; Bynum and Smith, 2001). Pul- the roles of extra¯oral structures in pollination have largely satilla cernua's ¯owering period, from April to May, is also been ignored. For example, in some species, movement of the the rainy season. ¯oral stalk during anthesis may in¯uence pollination and re- productive success (Eisikowitch and Rotem, 1987). MATERIALS AND METHODS One aspect of ¯ower orientation, heliotropism, has been in- vestigated (e.g., Kevan, 1975). Sun tracking increases intra¯o- Study speciesÐPulsatilla cernua (Thunb.) Spreng. (Ranunculaceae) is a ral temperature and pollinator activity at low ambient temper- perennial herb distributed in Northeastern China, Korea, and Japan. It is a atures. This cannot explain the movement of the ¯ower stalk common early spring ¯ower in China but is an endangered plant in Japan in Pulsatilla cernua (Ranunculaceae), an early spring plant, in because of a rapid decline of populations in the last two decades (Naito and which the ¯ower stalks bend distinctly during anthesis but Nakagoshi, 1994; Environment Agency of Japan, 2000). Individual plants may produce several ¯owers each year. The six petals are dark purplish red and which occasionally brings the ¯owers upright to track solar are covered with white silky-villose hairs. The androecium, with numerous radiation. One-®fth of the ¯owers of P. alpina remained in the stamens, is bright yellow at the beginning of anthesis and becomes paler with upright position, and it was reported to be heliotropic during age. The outer short club-shaped stamens are always sterile (staminodes) and periods of direct solar radiation (Luzar and Gottsberger, 2001). secrete nectar, as in the other Pulsatilla species (Jonsson, Rosquist, and Wid- In this study, we explore why the ¯ower stalk of Pulsatilla en, 1991). The pistils are numerous and borne on a conical receptacle. Each cernua bends during anthesis. We have tested several adaptive pistil has one ovule with a long purple style covered with hairs. After polli- possibilities as follows. (1) Is the movement attractive to pol- nation, the style will continue to grow, reaching 4±5 cm when the achenes linators? What ¯oral orientation do pollinators prefer to visit? mature. If buzz-pollination exists, a pendulous orientation might in- crease pollen output (Corbet, Chapman, and Saville, 1988). (2) Flower morphology during anthesisÐThirty ¯owers of cultivated plants, If the ¯owers are self-compatible and pollen limited due to a derived from seeds collected from the ®eld, were observed daily in pots out- scarcity of pollinators, a pendulous position might bring re- doors in April 2000. Six ¯oral parameters of each ¯ower were recorded to describe ¯ower morphological changes during anthesis as follows (Fig. 1): 1 Manuscript received 30 November 2001; revision accepted 7 May 2002. length of stem (S1), length of ¯ower stalk (S2), length of the longest petal (PL), The authors thank Yan-Wen Zhang, Chen-Chuan Liu, Bo Zhang, Tao Zhang, corolla width (CW), height of the longest pistil above the androecium (SH), and Norio Otaki, Yuko Kurihara, Ichiroku Hayashi, and Yasuyuki Ide for their help the angle from erect to the direction of the pistils (a). The status of the stamens in the ®eld and laboratory; Sarah A. Corbet for correcting the English and and ¯oral nectar was examined when we observed these ¯owers. reviewing the earlier draft; and Dwight Kincaid and an anonymous reviewer for their helpful comments on the manuscript. This study was partly supported by a grant from Ministry of Agriculture, Forestry and Fisheries, Japan and by Pollinator behaviorÐObservations of pollinator behavior were carried out JSPS Research Fellowships for S.-Q. H. from April to May in ®ve populations, two in northeastern China in 2000 and 5 Author for reprint requests (e-mail: [email protected], or three in Japan in 2001. We observed each population on at least 5 d in the [email protected]). ®eld. Various insects were observed visiting the ¯owers of Pulsatilla cernua 1599 1600 AMERICAN JOURNAL OF BOTANY [Vol. 89 RESULTS Flower morphology during anthesisÐAnthesis of a single ¯ower lasted from 6 to 10 d. During anthesis all ¯ower stalks of the cultivated plants bent markedly, though a few ¯owers in the ®eld did not bend the ¯ower stalk. Accompanying the movement of the ¯ower stalk, ¯ower orientation changed from 08 to 1808 and back to 08 with age. According to the angle of ¯ower from vertical (a), seven ¯owering stages were identi®ed (Fig. 2, Table 1). Most ¯owers were not vertically oriented, and only 16% (N 5 150) of the ¯owers were erect when they began to open. When the upper stamens of the androecium dehisced, the ¯ower angle was usually $908. When pendulous ¯owers began to become upright in the later stages of anthesis, all anthers had opened, the Fig. 1. Parameters measured for Pulsatilla cernua during anthesis. S1 5 ®laments had begun to wilt, and the ¯owers no longer contained length of stem; S2 5 length of ¯ower stalk; PL 5 length of the longest petal; nectar (Table 1). At the same time, the petals stopped growing CW 5 corolla width; SH 5 height of the longest pistil above androecium; and the corolla width decreased rapidly, but the ¯ower stalks and and a5the angle from erect to the direction of pistils. the pistils grew longer quickly (Fig. 3). Pollinator behaviorÐBumble bees (Bombus spp.) and soli- in these ®ve populations (S.-Q. Huang et al., unpublished manuscript). Visi- tary bees were the main pollinators. Some syrphids also visited tors carrying pollen of P. cernua observed moving between the ¯owers are the ¯owers but they seldom carried pollen grains. Bumble bees considered as pollinators in this study. To assess whether visitors prefer pen- and solitary bees were observed foraging for nectar and car- dulous to upright ¯owers, we recorded the number of visits to ¯owers at rying pollen grains. The bumble bees pushed their bodies into different stages of anthesis and the visitors' behavior within ¯owers. the ¯ower between petals and the androecium and seemed to forage mainly for nectar. When they crept more or less inside Pollination treatmentsÐTo examine incompatibility and the possibility of the ¯ower, pollen grains became attached to their legs and ab- self-pollination in this species, three pollination treatments were carried out domen. These pollen grains could be transferred to the stigmas at Sugadaira, Nagano Prefecture, Japan (368319 N, 1388259 E) at an elevation during a continuous visit to the ¯ower of P. cernua. Bees were of 1400 m above sea level in 2000. To investigate spontaneous self-pollina- observed moving around the androecium to collect pollen grains tion, eight ¯owers were covered by nylon mesh bags to exclude pollinators as well as foraging for nectar. Buzz-pollination by bumble bees before the ¯owers opened. To investigate hand self-pollination, ten bagged or solitary bees was not observed in this species. ¯owers were arti®cially pollinated by self-pollen after anther dehiscence. All Pollinators preferred to visit ¯owers at early stages with bags for these two treatments were removed after about 10 d, just after an- nectar (Table 1), but did not prefer downward to upward ¯ow- thesis ended. To investigate emasculation, the anthers were removed from ten ers. Visit frequencies (mean 6 1 SE) to upward and downward ¯owers after ¯owers had opened before anther dehiscence.