Chin J Plan Ecolo ›› 2015, Vol. 39 ›› Issue (7): 753-761.doi: 10.17521/cjpe.2015.0072

• Orginal Article • Previous Articles     Next Articles

Floral morphology and pollination mechanism of Salvia liguliloba, a narrow endemic species with degraded lever-like stamens

HUANG Yan-Bo1, WEI Yu-Kun1,*(), WANG Qi1, XIAO Yue-E1, YE Xi-Yang2   

  1. 1Shanghai Chenshan Botanical Garden, Shanghai Chenshan Plant Science Research Center, Chinese Academy of Sciences, Shanghai 201602, China
    2Zhejiang A&F University, Hangzhou 311300, China
  • Online:2015-07-22 Published:2015-07-01
  • Contact: Yu-Kun WEI
  • About author:

    # Co-first authors

Abstract: Aims Diverse stamen structures and interactions with pollinators make Salvia the model plants for studying evolutionary changes in plant pollination mechanisms. The dorsal pollination mechanism of lever-like stamens has been extensively investigated as a classic example for precise interactions between plants of Salvia genus and their pollinators. However, there are many atypical lever-like structures and pollination mechanisms among Salvia species. For example, Salvia liguliloba has floral organ structures and a pollination mechanism characterized by degenerated lever-like stamens. The aim of this work was to understand the selection pressure and ecological significance of Salvia plants that have the atypical staminal level mechanism. Methods In this study, we described the morphological features of S. liguliloba, a plant species endemic to the Tianmu Mountains, and investigated its pollination ecology in detail. Various components of the flower of S. liguliloba were measured, which included the corolla, corolla tube, corolla entrance, filament, connective and pistil. Flower-visiting insects, pollinators, and the pollination process were observed and recorded by a digital video camera. Furthermore, we focused on comparing the floral organ structures and the pollination characteristics of S. liguliloba with those of S. digitaloides, which has a short-lever stamen. The relative frequency of insects, visiting time per flower, activity rate and visitation rate were measured and compared with the data from our previous study of S. digitaloides, for which the flower structure and pollination features were well concluded. Important findings Salvia liguliloba has smaller corolla length, tube width, and shorter filament and pistil than S. digitaloides (p < 0.05). The only effective pollinator was Bombus trifasciatus, and its average relative visiting frequency and the visiting time per flower were (0.959 ± 0.065) and (1.54 ± 0.60) s. The degenerated lower arm and limited moving space in the upper arm of the stamen restrict the pollinating insects from pushing the stamens in a lever-like motion. Thus, bumblebees completed pollination with the aid of their heads. Compared with the structure of the lever-like stamen and the pollination mechanism of S. digitaloides, the structural features of the floral organs of S. liguliloba make it adapt to a more specific pollinator with shorter visiting time and higher activity rate. The results suggested that the species with degraded lever-like stamens might be different from other typical Salvia species in their evolution direction and reproductive strategy.

Key words: adaptive evolution, forehead pollination, short-lever stamen, Salvia liguliloba, Bombus trifasciatus

Fig. 1

Photographic images of Salvia liguliloba and its visiting insects. A, Habitat. B, Plant. C, Lateral view of flower. D, Longitudinal section of flower. E, Pistil. F, Front view of flower. G, Stamens. H, Fruits. I, Bombus trifasciatus (pollinator). J, Ventral visiting by a species of Halictidae. K, Dorsal visiting by a species of Halictidae. L, A visitor of Sphingidae species. Bar = 2 mm."

Fig. 2

Diagram of Salvia liguliloba flower measurement. A, Corolla length. B, Corolla width. C, Corolla height. D, Tube length. E, Entrance height. F, Entrance width. G, Filament length. H, Connective length. I, Pistil length. Bar = 2 mm."

Fig. 3

Comparisons of morphometric data between Salvia liguliloba (A to D) and S. digitaloides (E to H). A, E, Lateral view of a flower. B, F, Longitudinal section of a flower. C, G, Front view of a flower. D, H, Stamens. Bar = 5 mm."

Table 1

Comparison between Salvia liguliloba and S. digitaloides on flower features (mean ± SD) (mm)"

Entrance height
Filament length
Connective length
S. liguliloba
23.67 ± 0.74b 5.31 ± 0.34b 7.30 ± 0.67b 19.49 ± 0.8b 4.87 ± 0.61a 4.41 ± 0.52b 2.39 ± 0.14b 5.19 ± 0.33a 23.74 ± 0.43b
S. digitaloides
39.80 ± 2.60a 12.52 ± 1.49a 22.98 ± 2.62a 28.99 ± 2.01a 4.33 ± 0.68b 6.80 ± 0.72a 7.33 ± 0.46a 5.10 ± 0.43a 34.89 ± 2.30a

Table 2

Morphometric data of visiting insects from Salvia liguliloba in the study (mean ± SD) (mm)"

Visiting insect
Body length
Thorax width
Thorax thickness
Tongue length
三条熊蜂 Bombus trifasciatus (n = 10) 21.8 ± 1.29 7.35 ± 0.41 5.10 ± 0.24 11.0 ± 1.32
隧蜂科昆虫 Halictidae (n = 1) 6.88 1.91 1.66 0.73

Fig. 4

The pollination process of Bombus trifasciatus, an effective pollinator of Salvia liguliloba. A, Approaching to the corolla. B, Accessing to flower tube and the pollinator’s tongue is extending. C, B. trifasciatus is sucking nectar and its forehead touching the fertile anther. Bar = 2 mm."

Fig. 5

The daily dynamic of flower-visiting times for Salvia liguliloba by Bombus trifasciatus."

Table 3

Flower-visiting traits of pollinators from Salvia liguliloba and S. digitaloides (mean ± SD)"

Visiting insects
Relative frequency
Visiting time per flower (s)
Activity rate
Visitation rate
Pollination mode
Pollinator of S. liguliloba
Bombus trifasciatus
0.959 ± 0.065
(n = 7)
1.54 ± 0.60
(n = 1 035)
18.2 ± 3.12
(n = 10)
17.45 F
Pollinators of S. digitaloides
Psithyrus sp.
0.57 8.68 ± 0.90 - 3.94 D
小雅熊蜂 B. lepidus 0.20 15.57 ± 1.20 - 0.77 D/V
B. infrequens < 0.20 - - - D
[1] Claßen-Bockhoff R, Speck T, Tweraser E, Wester P, Thimm S, Reith M (2004). The staminal lever mechanism in Salvia L. (Lamiaceae): A key innovation for adaptive radiation?Organisms Diversity & Evolution, 4, 189-205.
[2] Claßen-Bockhoff R, Wester P, Tweraser E (2003). The staminal lever mechanism in Salvia L. (Lamiaceae)—A review.Plant Biology, 5, 33-41.
[3] Fang Q, Huang SQ (2014). Progress in pollination ecology at the community level.Chinese Science Bulletin, 59, 449-458.
(in Chinese with English abstract) [方强, 黄双全 (2014). 群落水平上传粉生态学的研究进展. 科学通报, 59, 449-458.]
[4] Feng JM, Wang XP, Xu CD, Yang YH, Fang JY (2006). Altitudinal patterns of plant species diversity and community structure on Yulong Mountains, Yunnan, China.Journal of Mountain Science, 24, 110-116.
(in Chinese with English abstract) [冯建孟, 王襄平, 徐成东, 杨元合, 方精云 (2006). 玉龙雪山植物物种多样性和群落结构沿海拔梯度的分布格局. 山地学报, 24, 110-116.]
[5] 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.]
[6] Huang SQ (2007). Studies on plant-pollinator interaction and its significances.Biodiversity Science, 15, 569-575.
(in Chinese with English abstract) [黄双全 (2007). 植物与传粉者相互作用的研究及其意义. 生物多样性, 15, 569-575.]
[7] Huang SQ, Guo YH (2000). New advances in pollination biology.Chinese Science Bulletin, 45, 225-237.
(in Chinese) [黄双全, 郭友好 (2000). 传粉生物学的研究进展. 科学通报, 45, 225-237.]
[8] Huang YB, Wei YK, Ge BJ, Wang Q (2014). Pollination Mechanisms of genus Salvia (Lamiaceae) in East Asia (China).Acta Ecologica Sinica, 34, 2282-2289.
(in Chinese with English abstract) [黄艳波, 魏宇昆, 葛斌杰, 王琦 (2014). 鼠尾草属东亚分支的传粉模式. 生态学报, 34, 2282-2289.]
[9] Li QQ, Li MH, Yuan QJ, Cui ZH, Huang LQ, Xiao PG (2013) Phylogenetic relationships of Salvia (Lamiaceae) in China: Evidence from DNA sequence datasets.Journal of Systematics and Evolution, 51, 184-195.
[10] Talavera S, Bastida F, Ortiz PL, Arista M (2001). Pollinator attendance and reproductive success in Cistus libanotis L. (Cistaceae).International Journal of Plant Sciences, 162, 343-352.
[11] Wang Q, Wei YK, Huang YB (2015). Research on distribution pattern of Subg. Salvia Benth. (Lamiaceae), an important group of medicinal plants in East Asia.Acta Ecologica Sinica, 35, 1470-1479.
(in Chinese with English abstract) [王琦, 魏宇昆, 黄艳波 (2015). 中国弧隔鼠尾草亚属(唇形科)的分布格局. 生态学报, 35, 1470-1479.]
[12] Wei YK, Wang Q, Huang YB (2015). Species diversity and distribution of Salvia (Lamiaceae).Biodiversity Science, 23, 3-10.
(in Chinese with English abstract) [魏宇昆, 王琦, 黄艳波 (2015). 唇形科鼠尾草属的物种多样性与分布. 生物多样性, 23, 3-10.]
[13] Xin HJ, He YQ, Li ZX, Wang SJ, Du JK, Wang CF, Pu T, Zhang W (2012). Inter-annual variation of temperature and precipitation gradient at the Eastern slope of Yulong Snow Mountain. Earth Science-Journal of China University of Geosciences, 37(Suppl.), 188-194.
(in Chinese with English abstract) [辛惠娟, 何元庆, 李宗省, 王世金, 杜建括, 王春凤, 蒲焘, 张蔚 (2012). 玉龙雪山东坡气温和降水梯度年内变化特征. 地球科学——中国地质大学学报, 37(Suppl.), 188-194.]
[14] Xin HJ, He YQ, Zhang T, Niu HW, Du JK (2013). The features of climate variation and glacier response in Mt. Yulong, southeastern Tibetan Plateau.Advances in Earth Science, 28, 1257-1268.
(in Chinese with English abstract) [辛惠娟, 何元庆, 张涛, 牛贺文, 杜建括 (2013). 青藏高原东南缘丽江玉龙雪山气候变化特征及其对冰川变化的影响. 地球科学进展, 28, 1257-1268.]
[15] Yang FC (1992). Comprehensive Investigation Report on Natural Resource of Tianmu Mountain Nature Reserve. Zhejiang Science and Technology Press, Hangzhou.
(in Chinese) [杨逢春 (1992). 天目山自然保护区自然资源综合考察报告. 浙江科学技术出版社, 杭州.]
[16] Zhang B, Claßen-Bockhoff R, Zhang ZQ, Sun S, Luo YJ, Li QJ (2011). Functional implications of the staminal lever mechanism in Salvia cyclostegia (Lamiaceae).Annals of Botany, 107, 621-628.
[17] Zhang B, Li QJ (2014). Phenotypic selection on the staminal lever mechanism in Salvia digitaloides (Labiaceae).Evolutionary Ecology, 28, 373-386.
[18] Zhang B, Sun S, Fang QE, Bai XM (2012). Evolutionary response of staminal lever mechanism of different species in Salvia to spatial variation in pollinators.Chinese Journal of Plant Ecology, 36, 681-689.
(in Chinese with English abstract) [张勃, 孙杉, 方强恩, 白小明 (2012). 鼠尾草属不同物种的雄蕊杠杆机制对传粉者空间变异的进化响应. 植物生态学报, 36, 681-689.]
[19] Zhang B, Sun S, Zhang ZQ, Li QJ (2010). A review of the evolutionary and ecological significance of lever-like stamens.Chinese Journal of Plant Ecology, 34, 89-99.
(in Chinese with English abstract) [张勃, 孙杉, 张志强, 李庆军 (2010). 杠杆状雄蕊及其进化生态学意义. 植物生态学报, 34, 89-99.]
[1] TAN Ke, DONG Shu-Peng, LU Tao, ZHANG Ya-Jing, XU Shi-Tao, REN Ming-Xun. Diversity and evolution of samara in angiosperm [J]. Chin J Plan Ecolo, 2018, 42(8): 806-817.
[2] Jun-Wei YE, Yang ZHANG, Xiao-Juan WANG. Phylogeographic breaks and the mechanisms of their formation in the Sino-Japanese floristic region [J]. Chin J Plan Ecolo, 2017, 41(9): 1003-1019.
[3] Yukun Wei, Yanbo Huang, Guibin Li. Reproductive isolation in sympatric Salvia species sharing a sole pollinator [J]. Biodiv Sci, 2017, 25(6): 608-614.
[4] Zhenna Qian,Qianwan Meng,Mingxun Ren. Pollination ecotypes and herkogamy variation of Hiptage benghalensis (Malpighiaceae) with mirror-image flowers [J]. Biodiv Sci, 2016, 24(12): 1364-1372.
[5] Zhenna Qian,Mingxun Ren. Floral evolution and pollination shifts of the “Malpighiaceae route” taxa, a classical model for biogeographical study [J]. Biodiv Sci, 2016, 24(1): 95-101.
[6] Qianghua Xu,Zhichao Wu,Liangbiao Chen. Biodiversity and adaptive evolution of Antarctic notothenioid fishes [J]. Biodiv Sci, 2014, 22(1): 80-87.
[7] Bao-Rong Lu, Hui Xia, Wei Wang, Xiao Yang. Impacts of natural hybridization and introgression on biological invasion of plant species [J]. Biodiv Sci, 2010, 18(6): 577-589.
[8] YU Xiang-Qin, FENG Yu-Long, LI Qiao-Ming. Review of research advances and prospects of invasive Chromolaena odorata [J]. Chin J Plan Ecolo, 2010, 34(5): 591-600.
[9] Jing Wang;Ting Wang*;Yingjuan Su;Lin Sen;Bing Zhang;Yongxia Yang. Adaptive Evolution in the PHY-PAS1 Domain of PHYP in Gymnosperms [J]. Chin Bull Bot, 2009, 44(05): 608-618.
[10] Yifei Liu;Hongwen Huang*. Gene Flow Dynamics and Related Adaptive Evolution in Plant Populations [J]. Chin Bull Bot, 2009, 44(03): 351-362.
[11] Yuan Gao;Li Tian;Song Qin* . Positive Selection in Plant Evolution [J]. Chin Bull Bot, 2008, 25(04): 401-406.
Full text



[1] Yan Xiao-hua Cai Zhu-ping. Effects of S-07, PP333 and Triadimefon on Peroxidaseisoentyme of Rice Seedling[J]. Chin Bull Bot, 1995, 12(专辑3): 109 -112 .
[2] . [J]. Chin Bull Bot, 1994, 11(专辑): 13 .
[3] Xiaomin Yu;Xingguo Lan;Yuhua Li. The Ub/26S Proteasome Pathway and Self-incompatible Responses in Flowering Plants[J]. Chin Bull Bot, 2006, 23(2): 197 -206 .
[4] WANG Ling-Li LIU Wen-Zhe. Contents of Camptothecin in Camptotheca acuminata from Different Provenances[J]. Chin Bull Bot, 2005, 22(05): 584 -589 .
[5] Dai Yun-ling and Xu Chun-hui. Advances in Research on Protein Components of Oxygen-evolving Complex[J]. Chin Bull Bot, 1992, 9(03): 1 -16 .
[6] . Advances in Research on Photosynthesis of Submerged Macrophytes[J]. Chin Bull Bot, 2005, 22(增刊): 128 -138 .
[7] Shaobin Zhang;Guoqin Liu. Research Advances in Plant Actin Isoforms[J]. Chin Bull Bot, 2006, 23(3): 242 -248 .
[9] MA Li-Hui, WU Pu-Te, and WANG You-Ke. Spatial pattern of root systems of dense jujube plantation with jujube age in the semiarid loess hilly region of China[J]. Chin J Plan Ecolo, 2012, 36(4): 292 -301 .
[10] PAN Yu-De, Melillo J. M., Kicklighter D. W., XIAO Xiang-Ming, McGuire A. D.. Modeling Structural and Functional Responses of Terrestria Ecosystems in China to Changes in Climate and Atmospheric CO2[J]. Chin J Plan Ecolo, 2001, 25(2): 175 -189 .