Biodiversity Science ›› 2019, Vol. 27 ›› Issue (4): 373-379.doi: 10.17520/biods.2019003

• Original Papers • Previous Article     Next Article

Adaptive significance of yellow flowered Bombax ceiba (Malvaceae)

Xiang Wenqian, Ren Mingxun()   

  1. Center for Terrestrial Biodiversity of the South China Sea, College of Ecology and Environment, Hainan University, Haikou 570228
  • Received:2019-01-07 Accepted:2019-05-04 Online:2019-06-05
  • Ren Mingxun

Bombax ceiba is a tall tree species with predominantly red flowers and is normally pollinated by birds. In some populations, a yellow flowered variety occurs. Honeybees frequently visit these uncommon yellow flowers but how this adaptation affects the life history of this variant remains unexplored. In the present study, floral syndrome and pollination mechanism of yellow flowers were compared with red flowers of B. ceiba populations on Hainan Island, southern China. The results showed that main nectar components of two floral phenotypes are both glucose and fructose dominated, and the volatile chemicals are mainly alkanes, esters, phenols and acids with no significant difference between the two phenotypes. The relative spectral reflectance showed that both birds and honeybees could detect the yellow flowers, suggesting visitation by honeybees can compensate for times when bird visitation is low. Compared with red flowers, yellow flower had a lower degree of dichogamy, which might increase selfing possibilities and provide reproduction assurance when red flowers receive low bird visitation. Interestingly, yellow flowers had a relatively higher degree of herkogamy, i.e. stigmas are much higher than anthers when compared to the red flowers. Greater herkogamy in yellow flowers may reflect an adaptation to decreased dichogamy, avoiding autonomous selfing and interference between female and male organs. Fruit set of the yellow phenotype (1.08 ± 0.56)% was lower than that of red phenotype (3.27 ± 0.93)%, suggesting pollen-limitation in B. ceiba. We propose that yellow flowers, with greater herkogamy but lower dichogamy, promote pollination via attracting diverse pollinators and protect red flowers from disturbance of honeybees.

Key words: bird-pollination, sexual interference, reproductive assurance, dichogamy, herkogamy

Fig. 1

Floral syndromes of red and yellow flowers of Bombax ceiba (I-L, I-S, P represent inner long stamen, inner short stamen and peripheral stamen, respectively)"

Fig. 2

Pollen viability and stigma receptivity of red and yellow flowers of Bombax ceiba"

Fig. 3

Relative spectral reflectance of red and yellow flowers of Bombax ceiba. The short dashed lines are spectral sensitivities of bees, the dotted line are spectral sensitivities of birds."

Table 1

Nectar volume, nectar components and volatile substances (%) of red and yellow flowers of Bombax ceiba. Data are mean ± standard. Different small letters mean significant difference at 0.05 level among treatments."

Red flower
Yellow flower
花蜜产量 Nectar volume (mL) 7.46 ± 1.05a 7.78 ± 0.84a
果糖 Fructose (mg/mL) 13.30 ± 1.89a 13.09 ± 2.79a
葡萄糖 Glucose (mg/mL) 26.71 ± 0.86a 28.25 ± 2.04a
烷烃类 Hydrocarbon (%) 67.42 ± 13.92a 54.75 ± 7.78a
脂类 Lipids (%) 6.59 ± 0.54a 7.08 ± 0.98a
2,4-二叔丁基苯酚 2,4-Di-tert-butylphenol (%) 5.88 ± 1.53a 6.42 ± 0.93a
5-羟基-2,4-二叔丁基苯基酯戊酸5-hydroxy-pentanoic acid (% ) 0.79 ± 0.09a 0.55 ± 0.11a

Table 2

Pollinator visitation and fruit set (%) of red and yellow flowers of Bombax ceiba. Data are mean ± standard. Different small letters mean significant difference at 0.05 level among treatments."

individual (n = 5)
黄花植株 Yellow-flower individual (n = 5)
No. of flowers per tree
10,050 ± 4,452.25a 9,780 ± 2,031.50a
Bird visits per hour
79 ± 14.27a 34.80 ± 19.61b
Honeybee visits per hour
100.40 ± 63.79a 360 ± 114.67b
No. of fruits per tree
362 ± 102.32a 186.20 ± 66.52b
坐果率 Fruit set (%) 3.27 ± 0.93a 1.08 ± 0.56b
[1] Aluri JSR, Srungavarapu PR, Kone R ( 2005) Pollination by bats and birds in the obligate outcrosser Bombax ceiba L. (Bombacaceae), a tropical dry season flowering tree species in the Eastern Ghats forests of India. Ornithological Science, 4, 81-87.
doi: 10.2326/osj.4.81
[2] APG II ( 2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society, 141, 399-436.
doi: 10.1046/j.1095-8339.2003.t01-1-00158.x
[3] Barwick M ( 2004) Tropical and Subtropical Trees. Timber Press, Portland.
[4] Bergamo PJ, Rech AR, Brito VLG, Sazima M ( 2016) Flower colour and visitation rates of Costus arabicus support the ‘bee avoidance’ hypothesis for red-reflecting hummingbird-pollinated flowers. Functional Ecology, 30, 710-720.
doi: 10.1111/1365-2435.12537
[5] Chang SM, Rausher MD ( 1999) The role of inbreeding depression in maintaining the mixed mating system of the common morning glory, Ipomoea purpurea. Evolution, 53, 1366-1376.
doi: 10.1111/evo.1999.53.issue-5
[6] Chittka L, Waser N ( 1997) Why red flowers are not invisible to bees. Israel Journal of Plant Sciences, 45, 169-183.
doi: 10.1080/07929978.1997.10676682
[7] Cruden RW ( 1977) Pollen-ovule ratios: A conservative indicator of breeding systems in flowering plants. Evolution, 35, 964-974.
[8] Dafni A ( 1992) Pollination Ecology: A Practical Approach. Oxford University Press, Oxford.
[9] Dafni A, Maués MM ( 1998) A rapid and simple procedure to determine stigma receptivity. Sexual Plant Reproduction, 11, 177-180.
doi: 10.1007/s004970050138
[10] Davis TA, Mariamma KO ( 1965) Three kinds of stamens in Bombax ceiba L. (Bombacaceae). Botanic Garden Meise, 35, 185-211.
[11] Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD ( 2004) Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution,and Systematics, 35, 375-403.
doi: 10.1146/annurev.ecolsys.34.011802.132347
[12] Gigord LDB, Macnair MR, Smithson A ( 2001) Negative frequency-dependent selection maintains a dramatic flower color polymorphism in the rewardless orchid Dactylorhiza sambucina (L.) Soò. Proceedings of the National Academy of Sciences,USA, 98, 6253-6255.
doi: 10.1073/pnas.111162598
[13] Gong YB, Huang SQ ( 2007) On methodology of foraging behavior of pollinating insects. Biodiversity Science, 15, 576-583. (in Chinese with English abstract)
[ 龚燕兵, 黄双全 ( 2007) 传粉昆虫行为的研究方法探讨. 生物多样性, 15, 576-583.]
[14] Grunfeld E, Vincent C, Bagnara D ( 1989) High-performance liquid chromatography analysis of nectar and pollen of strawberry flowers. Journal of Agricultural and Food Chemistry, 37, 290-294.
doi: 10.1021/jf00086a003
[15] Irwin RE, Strauss SY, Storz S, Emerson A, Guibert G ( 2003) The role of herbivores in the maintenance of a flower color polymorphism wild radish. Ecology, 84, 1733-1743.
doi: 10.1890/0012-9658(2003)084[1733:TROHIT]2.0.CO;2
[16] Joseph N, Siril EA ( 2013) Floral color polymorphism and reproductive success in annatto (Bixa orellana L.). Tropical Plant Biology, 6, 217-227.
doi: 10.1007/s12042-013-9128-y
[17] Koski MH, Ashman TL ( 2016) Macroevolutionary patterns of ultraviolet floral pigmentation explained by geography and associated bioclimatic factors. New Phytologist, 211, 708-718.
doi: 10.1111/nph.13921
[18] Li QL, Ma XK, Cheng J, Luo YB ( 2012) Quantitative studies of floral color and floral scent. Biodiversity Science, 20, 308-316. (in Chinese with English abstract)
[ 李庆良, 马晓开, 程瑾, 罗毅波 ( 2012) 花颜色和花气味的量化研究方法. 生物多样性, 20, 308-316.]
[19] Majetic CJ, Raguso RA, Ashman T ( 2009) The sweet smell of success: Floral scent affects pollinator attraction and seed fitness in Hesperis matronalis. Functional Ecology, 23, 480-487.
doi: 10.1111/fec.2009.23.issue-3
[20] Raine NE, Chittka L ( 2007) The adaptive significance of sensory bias in a foraging context: Floral colour preferences in the bumblebee Bombus terrestris. PLoS ONE, 2, e556.
doi: 10.1371/journal.pone.0000556
[21] Ren MX ( 2008) Stamen fusion in plants: Diversity, adaptive significance, and taxonomic implications. Journal of Systematics and Evolution, 46, 452-466. (in Chinese with English abstract)
[ 任明迅 ( 2008) 植物雄蕊合生的多样性、适应意义及分类学意义初探. 植物分类学报, 46, 452-466.]
[22] Ren MX ( 2009) Intrafloral stamen differentiations and their adaptive significances. Chinese Journal of Plant Ecology, 33, 222-236. (in Chinese with English abstract)
[ 任明迅 ( 2009) 花内雄蕊分化及其适应意义. 植物生态学报, 33, 222-236.]
[23] Rodriguez-Riano T, Dafni A ( 2000) A new procedure to assess pollen viability. Sexual Plant Reproduction, 12, 241-244.
doi: 10.1007/s004970050008
[24] Schoonhoven LM, van Loon JJA, Dicke M ( 2007) Insect-Plant Biology. Oxford University Press, Oxford, UK.
[25] Stanton ML, Snow AA, Handel SN ( 1986) Floral evolution: Attractiveness to pollinators increases male fitness. Science, 232, 1625-1626.
doi: 10.1126/science.232.4758.1625
[26] Vaidya P, Mcdurmon A, Mattoon E, Keefe M, Carley L, Lee CR, Bingham R, Anderson JT ( 2018) Ecological causes and consequences of flower color polymorphism in a self- pollinating plant (Boechera stricta). New Phytologist, 218, 380-392.
doi: 10.1111/nph.14998
[27] Webb CJ, Lloyd DG ( 1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms II. Herkogamy. New Zealand Journal of Botany, 24, 163-178.
doi: 10.1080/0028825X.1986.10409726
[28] Zhang DY ( 2004) Plant Life-History Evolution and Reproductive Ecology. Science Press, Beijing. (in Chinese)
[ 张大勇 ( 2004) 植物生活史进化与繁殖生态学. 科学出版社, 北京.]
[29] Zhou ZL, Ma HC, Lin K, Zhao YJ, Chen Y, Xiong Z, Wang LY, Tian B ( 2015) RNA-seq reveals complicated transcriptomic responses to drought stress in a nonmodel tropic plant, Bombax ceiba L. Evolutionary Bioinformatics, 11, 27-37.
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