Synchronized Protandry and Hermaphroditism in a Tropical Secondary Forest Tree, Schefflera Heptaphylla (Araliaceae)
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Plant Syst Evol (2011) 296:29–39 DOI 10.1007/s00606-011-0474-7 ORIGINAL ARTICLE Synchronized protandry and hermaphroditism in a tropical secondary forest tree, Schefflera heptaphylla (Araliaceae) Nancai Pei • Zhonglai Luo • Mark A. Schlessman • Dianxiang Zhang Received: 23 March 2011 / Accepted: 10 May 2011 / Published online: 4 June 2011 Ó Springer-Verlag 2011 Abstract Selection favoring avoidance of stigma clog- than those in earlier-maturing (first and second order) ging, pollen discounting, self-fertilization, and other neg- umbellets. Floral visitors were primarily flies (Chrysomya ative effects of self-pollination can produce intricate sp. and Syrphinae sp.) and wasps (Vespula sp. and Eu- patterns of intra- and interfloral dichogamy in plants menes sp.). Flowers produced nectar during both the male bearing numerous flowers. Here we report an extensive (pollen presentation) and female (stigma receptivity) stages study of the relationships among dichogamy, floral sex of their development, and the volume of nectar production allocation (pollen-to-ovule ratios), nectar production, floral was higher in the female stage. Nevertheless, flowers visitors, mating system, and fruit set in natural populations received fewer visits in the female stage than they did in of Schefflera heptaphylla, a widespread paleotropical sec- the male stage, and natural fruit set was low, especially in ondary forest tree that produces thousands of flowers in a first and third order umbellets. Fruit set from hand cross- blooming season. Each tree produces 15–30 sequentially and self-pollinations was significantly higher than natural blooming, paniculate, compound inflorescences. Each fruit set, indicating pollen limitation of fruit set. Schefflera compound inflorescence has up to three orders of umbel- heptaphylla has also been reported to be andromonoecious. lets, which also bloom sequentially. While hand-pollina- Both hermaphroditism and andromonoecy are consistent tions showed that S. heptaphylla was capable of self- with theoretical predictions for variation in sex allocation fertilization, our observations of thousands of flowers among sequentially maturing flowers in protandrous showed that strong intra- and interfloral protandry severely species. Further studies comparing hermaphroditic and restricts both autogamous and geitonogamous self-polli- andromonoecious populations of S. heptaphylla could nation. All flowers were bisexual, thus the sexual system of elucidate the selective factors affecting sex expression, the populations we studied was hermaphroditism. The nectar production, and fruit set in species with numerous pollen-to-ovule (P/O) ratios were characteristic of out- flowers displaying both intra- and interfloral dichogamy. crossing species, and P/O ratios of flowers in the last- maturing (third order) umbellets were significantly higher Keywords Araliaceae Á Dichogamy Á Hermaphroditism Á Phenology Á P/O ratios Á Protandry N. Pei Á Z. Luo Á D. Zhang (&) Key Laboratory of Plant Resource Conservation and Sustainable Utilization, South China Botanical Garden, Introduction The Chinese Academy of Sciences, Guangzhou 510650, People’s Republic of China Flowering plants are under strong selective pressure to e-mail: [email protected] synchronize pollen export and stigma receptivity among N. Pei individuals in order to maximize both male and female The Graduate University of the Chinese Academy of Sciences, reproductive success. In addition to increased levels of Beijing 100049, People’s Republic of China successful pollination and outcrossing, synchronous flow- M. A. Schlessman ering and fruiting of individuals within a population may Vassar College, Poughkeepsie, NY 12604, USA satiate predators and allow more seeds and seedlings to 123 30 N. Pei et al. escape predation (Janzen 1974; Kelly and Sork 2002; complex cycles of dichogamy, have been documented in Michalski and Durka 2007). At the same time, individual the genera Polyscias (Henwood 1986; Schlessman et al. plants are typically under selective pressures to separate 1990b), Raukaua (Merrett 2005), and Arthrophyllum, pollen release and stigma receptivity of their own flowers, Delarbrea, and Schefflera (Schlessman et al. 1990a). in order to reduce stigma clogging, and in genetically self- However, observations are often limited to just a few compatible species, also pollen discounting, self-fertiliza- individuals or populations per species, and typically only tion, and inbreeding depression (Lloyd and Webb 1986). to portions of extended flowering seasons. Consequently, As a result, angiosperms often exhibit intricate phenolog- data on floral visitors to tropical araliads are also limited. ical patterns involving dichogamy, the temporal separation Here we report an extensive study of the floral phenol- of anther dehiscence, and stigmatic receptivity, both within ogy, sex expression, mating system, and fruit set of the individual flowers (intrafloral) and among different flowers widespread tropical araliad tree, Schefflera heptaphylla. on the same plant (Lloyd and Webb 1986; Bertin and Our study spanned two flowering seasons, and we exam- Newman 1993). There are two forms of dichogamy: prot- ined thousands of flowers among numerous individual trees andry, in which anthers dehisce before stigmas become in three distinct populations. We documented floral phe- receptive, and protogyny, in which stigmas become nology, pollen and ovule production, nectar secretion, receptive before anthers dehisce (Sprengel 1793). floral visitors, self-fertility, and fruit set. We predicted Marked, synchronized, intra- and interfloral protandry is that (1) like other species with small, white to greenish- characteristic of the primarily tropical and woody Aralia- yellowish flowers, S. heptaphylla would be pollinated by ceae (Schlessman et al. 1990a, 2010). Individual plants small, generalized insects (Willemstein 1987; Bawa 1990; may produce hundreds to thousands of small, white to Proctor et al. 1996); (2) like other araliads, S. heptaphylla greenish-white flowers, which are typically borne on would exhibit both self-fertility and intra- and interfloral compound inflorescences composed of two or more struc- protandry that limited opportunities for both autogamy and turally distinct flower clusters (Philipson 1970; Frodin and geitonogamy (Schlessman et al. 1990a); and (3) the pollen- Govaerts 2003). The way that interfloral dichogamy is to-ovule ratios of S. heptaphylla flowers would be within expressed in these compound inflorescences, i.e., whether the range reported for animal-pollinated, primarily out- orders of umbels mature synchronously or sequentially, crossing species (Cruden 2000). We proposed that her- appears to be key in determining the sexual system. Syn- maphroditism was consistent with theoretical predictions chrony among umbel orders is correlated with hermaph- for variation in sex allocation among sequentially maturing roditism (all flowers bisexual), while sequential maturation flowers in protandrous species. is correlated with andromonoecy (Schlessman et al. 1990a, 2010). However, the most comprehensive studies of araliad Materials and methods floral phenology to date have been conducted on eastern North American herbaceous species of the temperate gen- Study species and populations era Aralia and Panax, and the latter is unusual in that it lacks compound inflorescences. Aralia hispida exhibits Schefflera heptaphylla (L.) Frodin (Araliaceae), the ‘‘ivy multiple cycles of protandry as sequentially maturing tree,’’ is a winter-flowering species common in tropical or cluster of flowers (umbels) open, and this temporal sepa- subtropical evergreen broadleaved forests. It is widely ration of male and female function is thought to reduce distributed in Fujian, Guangdong, Guangxi, Guizhou, opportunities for self-pollination, promote out-breeding, Hunan, Jiangxi, Xizang, Yunnan, Zhejiang, and Taiwan in and intensify competition among staminate flowers for China, and also in the neighboring countries India, Japan, ovules (Thomson and Barrett 1981; Thomson et al. 1982; Thailand, and Vietnam (He and Zeng 1974; Xiang and Barrett 1984). In the simple, single umbel inflorescences of Lowry 2007). Individual trees range from 2 to 8 m in Panax quinquefolius, intra- and interfloral protandry height, and the trunk diameter at breast height can exceed reduces opportunities for selfing but does not entirely 0.30 m. Mature trees typically produce 15–30 compound, prevent it (Lewis and Zenger 1983; Schlessman 1985; paniculate inflorescences during a flowering season. A Anderson et al. 1993; Mooney and McGraw 2007). Simi- typical compound inflorescence consists of a first order larly, marked intra- and interfloral protandry restricts aut- (primary, terminal) umbel, 15.55 ± 0.67 branches ogamous and geitonogamous selfing in the simple (mean ± SE, n = 20) terminating in second order (sec- inflorescences of Panax trifolius (Schlessman 1990). ondary, lateral) umbels, and 7.45 ± 0.40 third order (ter- Studies of the floral biology of the more common and tiary, sublateral) umbels (n = 20) on each branch. Each representative tropical Araliaceae have been somewhat umbellet is composed of 11.70 ± 0.53 small (ca. 5 mm narrow in scope. Intra- and interfloral protandry, along with diameter) flowers (n = 20). Thus, a single compound 123 Synchronized protandry of Schefflera heptaphylla 31 inflorescence may have 1,337.60 ± 86.40 flowers (abscising), or all fallen; stamens with anthers undehis- (n = 20), and trees typically produce thousands of flowers ced, dehiscing (exposing pollen), or empty