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Home , Chloranthaceae, Sarcandra, Sarcandra glabra

J. Res. 114: 423-427,2001 Journal of Plant Research 0 by The Botanical Society of 2001

Pollination of glabra () in Natural Populations in Japan

Yayoi Tosaki', Susanne S. Rennet and Hiroshi Takahashi3*

1 Laboratory for Plant Natural History, Faculty of Science, Kanazawa University, Kanazawa, 920-1192 Japan 2 Department of Biology, University of Missouri-St. Louis, St. Louis, MO 63121, U.S.A. 3 Department of Biology, Faculty of Education, Gifu University, Gifu, 501-1193 Japan

The pollination biology of was inves- compatible. Here we report the first field data on the tiiated in its natural habit in Japan. were pollination and mating system of S. glabra. protogynous and receptivity dropped off significantly following anther dehiscence. Female-stage and bisexual- Materials and Methods stage flowers were visited by beetles, bees, hemiptera, flies, and rarely ants that foraged for and/or small droplets Field investigations were conducted at Aka0 (40m alt.), of liquid that occasionally were secreted by the carpels and Takatomi-cho, Yamagata-gun, Gifu Prefecture, and at axes. At least the beetles, bees, and Uruno (50 m alt.), Kozagawa-cho, Higashimuro-gun, Wa- hemiptera commonly touched the stigmas and likely effect- kayama Prefecture. The flowering process was observed in ed pollination. Rowers were self-compatible, and auto- thirty flowers at the Aka0 site in July of 1997. Insects visits matic selfing sometimes occurred when pollen fell from were recorded at the Aka0 site for about 130 hours and at apical flowers onto the stigmas of lower flowers. the Uruno site for about 20 hours. Each inflorescence usually consists of four spikes (cf. Balthazar and Endress Key words: Bees - Beetles - Chloranthaceae - 1999), and each was used for only one pollination experi- Flies - Pollination - Sarcandra glabra - Self-compatibility ment. Experimental crossings and selfings were performed on female-stage flowers and bisexual-stage flowers from the middle of the spikes. Pollen for cross-pollination was Chloranthaceae are a family of angiosperms that collected from newly opened anthers on more than 10 has received much attention from morphologists and m away. Pollen for self-pollination of female-stage flowers phylogeneticists because of their unusual flowers and fossil was collected from newly opened anthers on the same record that goes back to the Early (e.g., Endress inflorescence. Pollen for self-pollination of flowers in the 1986,1987, Friis et a/. 1986, Crane et a/. 1989, Herendeen et bisexual stage came from the of the same . a/. 1993, Brenner 1996). Less is known about their pollina- Anther dehiscence could usually be predicted based on tion and breeding systems. Chloranthaceae comprise four anther color (Results) and flower position because there is an genera of which two, Chloranthus with 15species and almost regular progression in anther opening from the apical Sarcandra with three species, are endemic in lndomalaysia flowers of a spike downwards. This regular progression of and Eastern Asia. Both appear to be insect-pollinated, spike flowering enabled us to emasculate flowers just before although only Chloranthus has been studied in the field and they shed their pollen. All flowers used in experimental greenhouse (Ma et a/. 1997, Luo and Li 1999, Wang et a/. crossings and apomixis tests were emasculated. With the 1999, Balthazar and Endress 1999, see Endress 2001 for a exception of open-pollinated controls, were recent summary). Phylogenetically, Sarcandra and Chlor- bagged with I-mm or finer mesh polyethylene screens before anthus are sistergroups (Qiu et al. 1999) and derived relative their stigmas became receptive. Bags were removed when to the other two genera, and Ascarha, which stigmas had dried up. likely are wind-pollinated (Endress 1987, 2001). The average number of pollen grains per flower was Mating systems in Chloranthaceae have been examined in calculated by placing mature anthers on glass slides and the greenhouse for Sarcandra chloranthoides, S. glabra, and flushing pollen grains from the thecae with about 0.3 ml of Chloranthus spicatus (Balthazar and Endress 1999), and in 70% ethanol. After removal of the empty anther and evapo- the field for C. fortunei, C. henwi, C. holostegius, and C. ration of the ethanol, grains were immersed in a 1 : 1 mixture serratus (Ma et al. 1997, Luo and Li 1999, Wang et a/. 1999). of glycerin and water with aniline blue and counted under a With the exception of C. spicatus, all were found to be self- microscope. Ovules in the same flowers were counted under a binocular. Voucher specimens of Sarcandra glabra have been de- * Corresponding author: takahash@ cc.gifu-u.ac.jp posited in the herbarium of Gifu University, which also 424 Y. Tosaki et al.

Figs. 1-6. Sarcandm glabra flowers and their insect visitors, bar=l mm. 1. A female-stage flower, showing the single stamen to the left and the receptive stigma to the upper right. 2. Ladybird beetle (Coccinel- lidae) visiting male-stage flowers. 3. Alticinae beetle on bisexual-stage flowers. 4. Pseudomordellis- tena kaguyahime beetle on female-stage flowers. 5. Glipostenoda rosseola beetle on bisexual-stage flowers. 6. A cerambycid beetle on female-stage flowers. Pollination of Sacandra glabra 425 I.

1

Figs. 7-10. Insects visiting Sarcandra glabra flowers, bar4 mm. 7 and 8. Pentatomid hemipterans visiting the flowers. 9. A syrphid fly visiting female-stage flowers. 10. A Lasiogbssum bee visiting male- stage flowers. houses some of the insects collected. Additional insect 8 days. Flowers emit a weak fragrance just prior to anther vouchers have been deposited in the Osaka Museum of dehiscence and a stronger fragrance thereafter. Small Natural History. droplets of liquid were occasionally observed on carpels and inflorescence axes. Results Insect visitors Flowering in Sarcandra glabra Table 1 lists the insects collected on the flowers of Sarcan- Each spike of Sarcandra glabra has 6-14 flowers, and dra glabra. Small, between 1.5 and 6 mm long, beetles (Figs. flowering normally proceeds from the top of a spike down- 2-6), hemiptera (Figs. 7,8),flies (Fig. 9), bees (Fig. lo), and wards over two to three days. The carpels are green, and rarely ants visited inflorescences and flowers just prior to the crenate stigmas become moist several days before anther dehiscence and during the two days after dehis- anther dehiscence (Fig. 1). Mature but still indehisced sta- cence. The beetles probed carpels and spike axes, appar- mens have a creamish white connective and cream thecae, ently to take up the droplets secreted there, and they also which turn orange or reddish-brown upon opening (Figs. 2,4, foraged for pollen in older flowers. They often touched the 10). Anther dehiscence occurs several days after the stig- stigmas, carried numerous pollen grains on their bodies, and mas become receptive, mainly in the early morning (6-8 frequently switch between plants. The Ceratina, Lasioglos- a.m.), but occasionally also throughout the day. Thecae are sum, and Hylaeus bees foraged for pollen in bisexual-stage emptied within a few days, and the fall off after 2 to flowers and also touched the stigmas while moving on and 426 Y. Tosaki et a/.

Table 1. Insects foraging on the flowers of Sarcandra glabra Table 2. Experimental pollination in Sarcandra glabra

Flower Fruit set Insects Foraging Treatment stage,, Flower Fruits objects" ("0)

Coleoptera Cross-pollination F 22 13 59.1 Cerambycidae B 36 6 16.7 1 sp. Self-pollination F 20 13 65.0 Chrysomllidae B a429 34.5 1 sp. p, 0 Bagged emasculated flowers - 50 0 0 Cocci nel lidae Bagged intact flowers - 40 13 32.5 1 sp. P. 0 Open pollination - 86 42 48.4 MordelI idae l) F, female stage; 6, bisexual stage. Glipostenoda rosseola Marseul p, 0 Pseudomordellistena kaguyahime Nomura et Kato p, 0 crossed and in selfed flowers (chi-square=11.16 for cross- 1 sp. P. 0 pollinated flowers, df=l, P< 0.005; chi-square=6.23 for Diptera self-pollinated flowers, df=l, P<0.025). None of the emas- Anthomyiidae culated flowers produced fruit, while bagged inflorescences 1 sp. P. 0 had a fruit set of 33%. Of the open-pollinated flowers, 48% Syrphidae set fruit, which was not significantly different from experi- 3 SPP. mentally crossed female-stage flowers (chi-square=0.74, Hemiptera df=l) and marginally higher than the fruit set in bagged Pentatomidae inflorescences (chi-square=2.96 df=l, P between 0.1 and Eysarcoris guniger Thunberg 0.05). 1 sp. Hymenoptera Pollen number Formicidae The average number of pollen grains in a stamen of Camponotus yamaokai Terayama et Satoh 0 Sarcandra g/abra was 22.6X102 (n=lO, range 41 X102 to 11 X Crematogaster brunnea teranishii Santschi 0 lo2; SD 7.35X102). Flowers contained one ovule, and the Apidae pollen/ovule ratio therefore was the same as the pollen number. Ceratina japonica Cockerell p, 0 Colletidae Hylaeus floralis Smith P Discussion Halictidae Fruit set in female-stage selfed or outcrossed Sarcandra P Lasioglmsum sp. glabra flowers was not significantly different, indicating that 1) P, foraging for pollen; 0, probing carpel surface. S. glabra is self-compatible. A study of two plants culti- vated in a greenhouse at the University of Zurich (Balthazar and Endress 1999) found that fruit set after selfing was between inflorescences. They carried large pollen loads. between 6 and 33% (crossings could not be carried out). The hemiptera visited female- and bisexual-stage flowers Based on stigma receptivity tests with 5% H202 and with and generally behaved much like the beetles except that KMn04,Balthazar and Endress suggested that stigmas were they did not touch the stigmas as frequently. Four species receptive several days prior to anther dehiscence and of anthomyiid and syrphid flies foraged for pollen or pr6bed remained receptive throughout the bisexual phase. Our the carpels (apparently for the small droplets of liquid some- results, however, indicate that stigma receptivity is signifi- times secreted there), but they rarely touched the stigmas. cantly higher in female-stage flowers than it is in bisexual- There were no differences in the visitor spectra between the stage flowers (59 vs. 17% in outcrossed flowers and 65 vs. Aka0 and the Uruno sites. 35% in selfed flowers). Bagged inflorescences that did not receive insect visits Breeding experiments still had 33% fruit Set, probably due to pollen from apical Results of the breeding experiments are given in Table 2. (older) flowers falling onto stigmas of the lower (younger) Fruit set after experimental crossing and selfing of female- flowers of an inflorescence as also observed by Balthazar stage flowers was not significantly different (59 and 65%, and Endress (1999). Thecae not visited by insects contain a respectively, chi-square=0.15, df=l, not significant). In lot of pollen, and we observed grains falling down when bisexual-stage flowers, however, selfing resulted in higher anthers received mechanical stimulation, for example, from fruit set than outcrossing (35 vs. 17%, chi-square=3.89, df= strong wind. 1, P<0.05). Fruit set in female-stage flowers was signifi- Based on the bisexual flowers, sticky pollen, and short cantly higher than fruit set in bisexual-stage flowers, both in single stamen, Endress (1986,1987) suggested that Sarcandra Pollination of Sarcandra glabra 427

was insect-pollinated, most likely by beetles. This first phylogenetic analysis of : compari- study of the natural pollination of a species of Sarcandra son and combination with molecular data. Int. J. Plant shows that the flowers are visited by a range of insects, Sci. 161 (6 Suppl.): S121-Sl53. including beetles, bees, pentatomid hemiptera, and flies, with Eklund, H., Friis, E.M. and Pedersen, K.R. 1997. Chloranth- at least the former three groups regularly touching the aceous floral structures from the Late Cretaceous of stigmas. We also found that, in addition to pollen, beetles, Sweden. Plant Syst. Evol. 207 13-42. Endress, P.K. Reproductive structures and hemiptera, and flies apparently take up minute droplets from 1986. phylogenetic significance of extant primitive angio- the carpels and inflorescence axes. In the greenhouse, sperms. Plant Syst. Evol. 152: 1-28. Balthazar and Endress did not observe droplets on carpels or Endress, P.K. 1987. The Chloranthaceae: reproductive ,spike axes of S. chloranthoides. However, they found that structures and phylogenetic position. Bot. Jahrb. Syst. bract apices secreted droplets through stomata (their Fig. 109 153-226. 5a-d). In S. glabra, we did not see droplets on the bracts (at Endress, P.K. 2001. The flowers in extant basal angio- a magnification of 150 times) nor did we find stomata on the sperms and inferences on ancestral flowers. Int. J. carpels that might have secreted the minute droplets. Plant Sci. 162: 1111-1140. Friis, E.M., Crane, P.R. and Pedersen, K.R. 1986. Floral We thank Dr. K. Yamauchi of Gifu University and Drs. S. evidence for Cretaceous chloranthoid angiosperms. Shiyake and S. Fujii of the Osaka Museum of Natural History Nature 320 163-164. for the identification of the insects, Dr. H. Takasu of Wa- Herendeen, P.S., Crepet, W.L. and Nixon, K.C. 1993. Chlor- kayama University for advice on the selection of study sites, anthus-like stamens from the Upper Cretaceous of New and Dr. Peter Endress for comments on the manuscript. Jersey. Amer. J. Bot. 80 865-871. This study was supported by a Grant-in-Aid for Scientific Luo, Y. and Li, 2. 1999. Pollination ecology of Chloranthus serratus (Thunb.) Roem. et Schult. and Cb. fortunei (A. Research from the Japan Society for the Promotion of Gray) Solms-Laub. (Chloranthaceae). Ann. Bot. 83: Science (10640680). 489-499. Ma, S-B.,Wang, Y-H. and Cui, M-K. 1997. A contribution References to the reproductive biology of Chloranthus holostegius (Chloranthaceae) in Mile population. Acta Bot Yun- Balthazar, M., von and Endress, P.K. 1999. Floral bract nanica 19: 415-422 (in Chinese with English abstract). function, flowering process and breeding systems of Qiu, Y., Lee, J., Bernasconi-Quadroni, F., Soltis, D.E., Soltis, Sarcandra and Chloranthus (Chloranthaceae). Plant P.S., Zanis, M., Zimmer, E.A., Chen, Z., Savolalnen, V. SySt. EvoI. 218: 161-178. and Chase, M.W. 1999. The earliest angiosperms: Brenner, G.J. 1996. Evidence for the earliest stage of evidence from mitochondrial, plastid and nuclear angiosperms pollen evolution: a paleoequatorial sec- genomes. Nature 402: 404-407. tion from Israel. In D.W. Taylor and L.J. Hickey, eds., Wang, Y-H., Yang, K. and Ma, S-B. 1999. Reproductive Origin, Evolution and Phylogeny, Chap- biology of Chloranthus henryi (Chloranthaceae)in north- man & Hall, New York, pp. 91-115. eastern Yunnan. Acta Bot Yunnanica 21: 218-224 (in Crane, P.R., Friis, E.M. and Pedersen, K.R. 1989. Repro- Chinese with English abstract). ductive structure and function in Cretaceous Chloranth- aceae. Plant Syst. Evol. 165: 211-226. (Received June 8, 2007; accepted September IS, 2001) Doyle, J.A. and Endress, P.K. 2000. Morphological