红姜花(姜科)同步大量开花的适应意义

doi:10.3724/SP.J.1003.2012.10034

摘要/Abstract

摘要：

两性花植物同步大量开花增加了个体花展示大小, 能吸引更多的传粉者, 使植株获得更多的交配机会, 但也不可避免地带来不同程度的同株异花授粉, 进而对被子植物的性资源分配、花部性状以及雌雄异株的进化等产生重要的影响。本文以姜科红姜花(Hedychium coccineum)为研究对象, 通过人工授粉和操控试验、传粉动物的观察、自然结果率和自然居群的大小和密度的调查, 探讨红姜花同步大量开花的适应意义。结果表明: (1)红姜花的穗状花序由57.33 ± 1.68(n = 30)个蝎尾状聚伞小花序组成, 每个小花序具3.8 ± 0.15(n = 30)朵花, 同一花序上所有的小花序同步开花, 不同小花序内的花按轮次同步开放, 使花序在整个开花期间保持有数十朵花同时开放, 花序水平上的花展示极为显著; (2)红姜花为自交亲和植物, 但不存在自动自花授粉, 自然居群存在严重的传粉者限制, 其结实也存在着资源限制; (3)多型蓝凤蝶(Papilio memnon)、小矩翅粉蝶(Dercas lycorias)和黑角尖翅粉蝶云南亚种(Appias indra aristoxemus)是红姜花的有效传粉者, 3种蝴蝶对红姜花不同大小花序的访问频率都显著不同, 随着花序花展示大小的增加其访问频率也显著增加; (4)红姜花同一个体小花序内不同轮次花之间的胚珠数随轮次显著减少, 而花粉数前3轮随轮次显著增加。胚珠数的递减及结实存在着资源限制, 说明红姜花一个花序开大量的花并不是为了增加结实, 而花粉数前3轮的递增, 有利于花粉的分散输出, 提高个体的雄性适合度。

关键词: 姜花属, 花展示, 花寿命, 开花格局, 同株异花授粉, 花序结构, 性资源分配

Abstract

Hermaphroditic plants that simultaneously display multiple flowers may attract more pollinators and create more chances for mating. However, this may also lead to geitonogamy, which may have major impacts on evolution of sex allocation, floral characteristics, and dioecy. To explore adaptive significance of mass-flowering in Hedychium coccineum, we conducted studies on pollination biology of H. coccineum, via hand-pollination and manipulated experiments, pollinator observation, and investigations on population density and natural fruit sets. Overall, inflorescences of H. coccineum were composed of terminal spikes containing 57.33 ± 1.68 (n = 30) cincinnus, and each cincinnus possessed 3.8 ± 0.15 (n = 30) flowers. Flowers in each cincinnus opened in turn, and the same round flowers among each cincinnus within inflorescences opened in successive synchronous cycles. This provided a spike that kept a mass of flowers blooming simultaneously throughout the flowering period. H. coccineum displayed a large floral display at the inflorescence level. Additionally, H. coccineum was self-compatible, and spontaneous self-pollination did not occur. Fruit production of H. coccineum in natural populations was severely pollinator-limited. Meanwhile, H. coccineum was also resource-limited in fruit production. Three butterflies, Papilio memnon, Dercas lycorias, and Appias indra aristoxemus were effective pollinators of H. coccineum. Visiting frequencies of these butterfly species to three inflorescences with different floral display size were obviously different and visitation frequencies increased as the inflorescence increased in floral display size. Pollen grains and ovules of H. coccineum varied significantly among flowers of different rounds in the cincinnus. Ovule production decreased significantly from the first to the fourth round, but pollen grains increased significantly from the first round to the third round. The decrease in ovules and resource limitation in fruit production indicated that mass-flowering in H. coccineum was not for increasing fruit production. The increase in pollen grains from the first round to the third round benefits pollen export and increases male fitness.

Key words: Hedychium, floral display, floral longevity, flowering pattern, geitonogamy, inflorescence structure, sex allocation

高江云, 盛春玲, 杨淑霞 (2012) 红姜花(姜科)同步大量开花的适应意义. 生物多样性, 20, 376-385. DOI: 10.3724/SP.J.1003.2012.10034.

Jiangyun Gao, Chunling Sheng, Shuxia Yang (2012) Adaptive significance of mass-flowering in Hedychium coccineum (Zingiberaceae). Biodiversity Science, 20, 376-385. DOI: 10.3724/SP.J.1003.2012.10034.

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.biodiversity-science.net/CN/10.3724/SP.J.1003.2012.10034

https://www.biodiversity-science.net/CN/Y2012/V20/I3/376

图/表 6

图1 红姜花的花序和访花昆虫。(a)红姜花的花序由许多蝎尾状聚伞小花序组成, 小花序内的花依次开放, 整个花序同时有大量花开放; (b)一只多型蓝凤蝶正访问红姜花的花序; (c)一只小矩翅粉蝶正访问红姜花; (d)一只访花的小矩翅粉蝶翅膀上粘有大量红姜花的花粉。箭头指示花粉。

Fig. 1 Inflorescence and visitors of Hedychium coccineum. (a) An inflorescence of Hedychium coccineum contains many cincinnus, and flowers in a cincinnus blooms on turn, and many flowers bloom on an inflorescence at the same time. (b) A Papilio memnon is visiting the inflorescence of H. coccineum. (c) A Dercas lycorias is visiting the inflorescence of H. coccineum. (d) A number of pollen grains of H. coccineum are stuck on the wing of a visiting Dercas lycorias. The arrow indicates the pollen grains.

表1 红姜花的植株和花部特征

Table 1 Plant and floral characteristics of Hedychium coccineum

项目 Items	平均值±标准差 Mean ± SE	范围 Range	样本量 Simple size
株高 Plant height (m)	1.72 ± 0.05	1.2-2.3	30
小花序数 No. of cincinnus per inflorescence	57.33 ± 1.68	38-75	30
花数 No. of flowers per cincinnus	3.8 ± 0.15	2-6	30
花丝长度 Filament length (mm)	55.7 ± 0.66	49.82-62.11	30
花药长度 Anther length (mm)	10.08 ± 0.2	8-12.12	30
花柱长度 Style length (mm)	99.86 ± 0.90	88.72-105.27	30
花冠管长度 Corolla tube length (mm)	34.05 ± 0.48	29.61-39.82	30
唇瓣长度 Labellum length (mm)	27.55 ± 0.23	24.64-29.68	30
唇瓣宽度 Labellum width (mm)	17.55 ± 0.29	13.32-20.84	30
花粉数 No. of pollen grains	6,960.8 ± 168.2	3,600-11,775	90
胚珠数 No. of ovules	75.47 ± 1.59	45-118	90

图2 红姜花小花序内不同轮次花的花粉数和胚珠数。不同字母表示不同轮次花的花粉数(A、B或C)和胚珠数(a、b、c或d)差异显著(P < 0.001)。

Fig. 2 The pollen grains and ovule number of different round flowers in cincinnus of Hedychium coccineum. Statistically homogeneous grouping based on ANOVA analysis are indicated by the same letter (A, B or C for pollen grains and a, b, c or d for ovule number(P < 0.001).

图3 2005年和2006年红姜花不同授粉处理的结果率。不同字母表示不同授粉处理的结果率(2005年, A或B; 2006年, a、b或c)差异显著(P < 0.001)。

Fig. 3 The effects of pollination treatments on fruit set of Hedychium coccineum in 2005 and 2006. Statistically homogeneous grouping based on a one-way analysis of variance are indicated by the same letter (A or B for 2005 and a, b or c for 2006) above the bars(P < 0.001).

图4 红姜花不同授粉处理后花粉管的生长格局

Fig. 4 The growth pattern of pollen tube in the style of Hedychium coccineum under two pollination treatments

图5 多型蓝凤蝶、小矩翅粉蝶和黑角尖翅粉蝶云南亚种三种蝶类对红姜花3个不同大小花序的访问格局(2007年7月26-29日)

Fig. 5 The visitation patterns on the 3 different inflorescences of Hedychium coccineum by Papilio memnon, Dercas lycorias and Appias indra aristoxemus (26-29 July 2007)

参考文献 39

[1]	Ashman TL, Schoen DJ (1994) How long should flowers live? Nature, 371, 788-791.
[2]	Augspurger CK (1980) Mass flowering of a tropical shrub (Hybanthus prunifolius): influence on pollinator attraction and movement. Evolution, 34, 475-488. DOI URL PMID
[3]	Beattie AJ, Culver DC (1979) Neighborhood size in Viola. Evolution, 33, 1226-1229. DOI URL PMID
[4]	Bell G (1985) On the function of flowers. Proceedings of the Royal Society of London B: Biological Sciences 224, 223-265.
[5]	Brunet J, Charlesworth D (1995) Floral sex allocation in sequentially blooming plants. Evolution, 49, 70-79.
[6]	Dafni A (1992) Pollination Ecology: A Practical Approach. Oxford University Press, New York.
[7]	de Jong TJ (2000) From pollen dynamics to adaptive dynamics. Plant Species Biology, 15, 31-41.
[8]	de Jong TJ, Klinkhamer PGL, Rademaker MCJ (1999) How geitonogamous selfing affects sex allocation in hermaphrodite plants. Journal of Evolutionary Biology, 12, 166-176.
[9]	de Jong TJ, Waser NM, Klinkhamer PGL (1993) Geitonogamy: the neglected side of selfing. Trends in Ecology and Evolution, 8, 321-325.
[10]	Gao JY, Zhang L, Deng XB, Ren PY, Kong JJ, Li QJ (2004) The floral biology of Curcumorpha longiflora (Zingiberaceae): a ginger with two-day flowers. American Journal of Botany, 91, 289-293.
[11]	Gao JY, Yang ZH, Ren PY, Li QJ (2006) Reproductive ecology of Rhynchanthus beesianus W. W. Smith (Zingib- eraceae) in south Yunnan, China: a ginger with bird pollination syndrome. Journal of Integrative Plant Biology, 48, 1294-1299.
[12]	Gentry AH (1974) Flowering phenology and diversity in tropical Bignoniaceae. Biotropica, 6, 64-68.
[13]	Harder LD, Barrett SCH (1995) Mating cost of large floral displays in hermaphrodite plants. Nature, 373, 512-515.
[14]	Harder LD, Barrett SCH (1996) Pollen dispersal and mating patterns in animal-pollinated plants. In: Floral Biology: Studies on Floral Evolution in Animal-Pollinated Plants (eds Lloyd DG, Barrett SCH), pp. 140-190. Chapman & Hall, New York.
[15]	Harder LD, Jordan CY, Gross WE, Routley MB (2004) Beyond floricentrism: the pollination function of inflorescences. Plant Species Biology, 19, 137-148.
[16]	Heinrich B, Raven PH (1972) Energetics and pollination ecology. Science, 176, 597-602.
[17]	Holsinger KE, Feldman MW, Christiansen FB (1984) The evolution of self-fertilization in plants: a population genetic model. The American Naturalist, 124, 446-453.
[18]	Holttum RE (1950) The Zingiberaceae of the Malay Peninsula. Garden's Bulletin Singapore, 13, 1-250.
[19]	Ippolito A, Armstrong JE (1993) Floral biology of Hornstedtia scottiana (Zingiberaceae) in a lowland rain forest of Australia. Biotropica, 25, 281-289.
[20]	Janzen DH (1971) Euglossine bees as long-distance pollinators of tropical plants. Science, 171, 203-205. URL PMID
[21]	Klinkhamer PGL, de Jong TJ, de Bruyn GJ (1989) Plant size and pollinator visitation in Cynoglossum officinale. Oikos, 54, 201-204.
[22]	Kunckel d’Herculais J (1910) Rapport des insects lepidopteres avec les fleurs des zingiberacees et en particulier avec celles des Hedychium. Comptes Rendus Hebdomadaires des Seances del Academie des Sciences, 1153-1155.
[23]	Levin DA (1981) Dispersal versus gene flow in plants. Annals of the Missouri Botanical Garden, 68, 233-253.
[24]	Li QJ, Xu ZF, Kress WJ, Xia YM, Zhang L, Deng XB, Gao JY, Bai ZL (2001) Flexible style that encourages outcrossing. Nature, 410, 432. DOI URL PMID
[25]	Müller F (1890) Miscellen Kreuzung von Hedychium. Abhandlungen Herausgegeben vom Naturwissenschaftlichen Vereine zu Bremen, 11, 444.
[26]	Price MV, Waser NM (1979) Pollen dispersal and optimal outcrossing in Delphinium nelsoni. Nature, 277, 294-297.
[27]	Queller DC (1983) Sexual selection in an hermaproditic plant. Nature, 305, 706-707.
[28]	Robertson AW (1992) The relationship between floral display size, pollen carryover and geitonogamy in Myosotis colensoi (Kirk) MacBride (Boraginaceae). Biological Journal of the Linnean Society, 46, 333-349.
[29]	Rodriguez-Riano T, Dafni A (2000) A new procedure to assess pollen viability. Sexual Plant Reproduction, 12, 241-244.
[30]	Schoen DJ, Ashman TL (1995) The evolution of floral longevity: resource allocation to maintenance versus construction of repeated parts in modular organisms. Evolution, 49, 131-139. URL PMID
[31]	Schmitt J (1980) Pollinator foraging behavior and gene dispe- rsal in Senecio (Compositae). Evolution, 34, 934-943. URL PMID
[32]	Snow AA, Spira TP, Simpson R, Klips RA (1996) The ecology of geitonogamous pollination. In: Floral Biology: Studies on Floral Evolution in Animal-Pollinated Plants (eds Lloyd DG, Barrett SCH), pp. 191-216. Chapman & Hall, New York.
[33]	Vogel S (1984) Blutensekrete als akzessorischer Pollenkitt. In: Mitteilungsband Botaniker-Tagung Wien (ed. Ehrendorfer F), p. 123. Institut fur Botanik, Universitat Wien, Vienna.
[34]	Wang YQ, Zhang DX, Renner SS, Chen ZY (2004) A new self-pollination mechanism. Nature, 431, 39-40.
[35]	Willson MF, Rathcke BJ (1974) Adaptive design of the floral display in Asclepias syriaca L. American Midland Naturalist, 92, 47-57.
[36]	Wu TL, Larsen K (2000) Zingiberaceae. In: Flora of China. (Vol. 24): Flagellariaceae Through Marantaceae (eds Wu ZY, Raven PH), pp. 346-347. Science Press, Beijing.
[37]	Zhang DY (张大勇) (2000) Research on Theoretical Ecology (理论生态学研究). Higher Education Press, Beijing. (in Chinese)
[38]	Zhang DY (张大勇) (2004) Plant Life-History Evolution and Reproductive Ecology (植物生活史进化与繁殖生态学). Science Press, Beijing. (in Chinese)
[39]	Zhang JH, Cao M (1995) Tropical forest vegetation of Xishuangbanna, SW China and its secondary changes, with special reference to some problems in local nature conservation. Biological Conservation, 73, 229-238.