熊蜂盗蜜的花色偏好及对长距忍冬繁殖适合度的影响

doi:10.17520/biods.2024554

生物多样性 ›› 2025, Vol. 33 ›› Issue (4): 24554. DOI: 10.17520/biods.2024554 cstr: 32101.14.biods.2024554

• 研究报告: 植物多样性 • 上一篇下一篇

熊蜂盗蜜的花色偏好及对长距忍冬繁殖适合度的影响

王顺雨¹^,²(), 李杨¹^,²(), 吕晓琴¹^,³(), 李欣¹(), 范权秀¹(), 王晓月¹^,³^,^*()()

1.贵州师范大学生命科学学院, 贵阳 550025
2.贵州师范大学贵州省植物生理与发育调控重点实验室, 贵阳 550025
3.贵州师范大学西南喀斯特山地生物多样性保护国家林业和草原局重点实验室, 贵阳 550025

收稿日期:2024-12-09 接受日期:2025-03-03 出版日期:2025-04-20 发布日期:2025-03-10
通讯作者: *E-mail: wang.xiaoyue1989@163.com
基金资助:
国家自然科学基金(32360262);国家自然科学基金(31901208);贵州省重大科技成果转化项目([2022]010);喀斯特石漠化水肥耦合与生物多样性恢复项目(黔教技〔2023〕004)

The color preference of bumblebee nectar robbing and its impact on the reproductive fitness of Lonicera calcarata

Wang Shunyu¹^,²(), Li Yang¹^,²(), L‌ü Xiaoqin¹^,³(), Li Xin¹(), Fan Quanxiu¹(), Wang Xiaoyue¹^,³^,^*()()

1 College of Life Sciences, Guizhou Normal University, Guiyang 550025, China
2 Key Laboratory of Plant Physiology and Development of Guizhou Province, Guizhou Normal University, Guiyang 550025, China
3 Key Laboratory of Southwest Karst Mountain Biodiversity Conservation of National Forestry and Grassland Administration, Guizhou Normal University, Guiyang 550025, China

Received:2024-12-09 Accepted:2025-03-03 Online:2025-04-20 Published:2025-03-10
Contact: *E-mail: wang.xiaoyue1989@163.com
Supported by:
National Natural Science Foundation of China(32360262);National Natural Science Foundation of China(31901208);Guizhou Provincial Program on Commercialization of Scientific and Technological Achievements([2022]010);Water-Fertilizer Coupling and Biodiversity Restoration in Karst Rocky Desertification(QianJiaoJi [2023]004)

摘要/Abstract

摘要：

植物开花过程中花色的变化作为一种指示信号会引导传粉者偏好访问变色前的花, 那么花色的变化能否影响昆虫盗蜜, 目前还不清楚。为了探究盗蜜者是否偏好变色前的花以及盗蜜对植物繁殖适合度的作用, 我们以忍冬属长距忍冬(Lonicera calcarata)为研究对象, 其花期3天, 花色从白变为黄, 再变为橘红, 野外记录访花昆虫的访问行为, 计算合法访问和盗蜜的频率; 统计不同居群3种颜色花的盗蜜率, 测量它们正常和盗蜜花朵的形态特征, 测量开花中正常和盗蜜花朵的花蜜现存量和糖浓度, 统计正常和盗蜜的花苞中花粉和胚珠总数, 进行不同人工授粉处理统计结实率。长距忍冬的访花者有尺蛾、蝶和熊蜂, 其中熊蜂可以合法地访花和对不同颜色的花盗蜜, 总的盗蜜频率高于合法访花频率; 橘红色和黄色花的盗蜜率、盗洞大小显著高于白色花; 盗蜜花的形态特征(尤其是唇瓣和花药)整体上小于正常花, 盗蜜减少单花的花蜜分泌量, 但不影响其糖浓度; 盗蜜不影响花苞中的花粉总数、胚珠数和植株的结实率。该研究表明盗蜜者熊蜂没有偏好访问变色前的花, 盗蜜会减少花蜜分泌量, 没有直接显著影响植物的雌雄适合度。植物花色变化对访花昆虫行为的影响需要更深入和持续的研究。

关键词: 盗蜜, 繁育适合度, 传粉者, 盗蜜者, 长距忍冬, 花色变化

Abstract

Aims:The color change of flowers during their blooming process can serve as a cue that guides pollinators to preferentially visit pre-change color flowers. However, it remains unclear whether this color change influences nectar robbers’ behavior.

Methods:To explore whether nectar robbers prefer pre-change color flowers and the impact of nectar robbing on plant reproductive success, we used Lonicera calcarata (Caprifoliaceae) as the study subject. Its flowering period lasts for three days, during which the flower color changes from white to yellow and then to orange-red. We recorded the visitation behavior of flower-visiting insects in the field and calculated the frequencies of legitimate visits and nectar robbing. We also analyzed the nectar robbing rates of flowers of three colors in different populations, measured the morphological traits of normal and robbed flowers, assessed the nectar volume and sugar concentration in both normal and robbed flowers during blooming, and examined the total number of pollen grains and ovules in flower buds from normal and robbed flowers. Finally, we performed different artificial pollination treatments to calculate seed set.

Results:Flower visitors to L. calcarata included moths, butterflies, and bumblebees, among which bumblebees could both legitimately visit the flowers and rob nectar from flowers of different colors. The overall nectar robbing frequency was higher than the frequency of legitimate visits for bumblebees. Nectar robbing rates of L. calcarata varied across different populations, with the nectar robbing rate of orange-red and yellow flowers being significantly higher than that of white flowers. The floral traits of robbed flowers were smaller than normal flowers in general, especially the lip and anther size. The holes in nectar spurs of orange-red and yellow flowers were significantly larger than those in white flowers. In all the three phases, nectar robbing significantly reduced the nectar volume of one flower, but did not affect the nectar sugar concentration. There were no significant differences in the total number of pollen grains in the buds between robbed and normal flower, as well as the ovules. Seed sets of pollen grains from normal and robbed flowers pollinated on the stigmas of normal flowers were not significantly different. Likewise, the seed sets of pollen from normal flowers pollinated on the stigma of normal and robbed flowers showed no significant differences.

Conclusion:This study preliminarily indicates that nectar robbing bees, particularly bumblebees, do not preferentially visit pre-change color flowers. Nectar robbing reduces nectar secretion and it does not directly affect the plant’s female and male fitness. The influence of flower color change on flower-visiting insect behavior requires further and more sustained investigation.

Key words: nectar robbing, reproductive fitness, pollinator, nectar robber, Lonicera calcarata, floral color change

王顺雨, 李杨, 吕晓琴, 李欣, 范权秀, 王晓月 (2025) 熊蜂盗蜜的花色偏好及对长距忍冬繁殖适合度的影响. 生物多样性, 33, 24554. DOI: 10.17520/biods.2024554.

Wang Shunyu, Li Yang, L‌ü Xiaoqin, Li Xin, Fan Quanxiu, Wang Xiaoyue (2025) The color preference of bumblebee nectar robbing and its impact on the reproductive fitness of Lonicera calcarata. Biodiversity Science, 33, 24554. DOI: 10.17520/biods.2024554.

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图/表 6

图1 长距忍冬的花序、单花以及昆虫的访花行为。A. 长距忍冬枝条白色、黄色和橘红色的花; B. 花蜜距被盗蜜现象(以白色花为例, 红色箭头指向盗洞); C. 花部特征测量方法的示意图(a: 上唇长; b: 上唇宽; c: 下唇长; d: 下唇宽; e: 花开口直径; f: 花筒直径; g: 花筒深; h: 花蜜距长; i: 花蜜距直径; j: 雌蕊长; k: 柱头直径; l: 柱头厚度; m: 雄蕊长; n: 花药长; o: 花药宽; p: 花药厚度; q: 盗洞长; r: 盗洞宽); D. 黑尾熊蜂从花冠开口进入花中吸取花蜜(合法地访花行为); E. 黑尾熊蜂将喙从花蜜距的基部盗洞深入蜜距, 直接盗取花蜜; F. Bombus eximius在合法地访花; G. B. eximius从花蜜距基部盗取花蜜; H. 楚南熊蜂合法地访花; I. 楚南熊蜂从花蜜距基部盗取花蜜; J. 完善绢粉蝶在合法地访花; K. 尺蛾类在合法地访花。

Fig. 1 Inflorescence and single flower of Lonicera calcarata and the visiting behavior of insects. A. White, yellow and orange-red flowers on the branch of L. calcarata; B. Nectar robbing phenomenon (using the white flower as an example, the hole marked with a red arrow); C. Diagram showing the measurement of floral traits (a, Upper lip length; b, Upper lip width; c, Lower lip length; d, Lower lip width; e, Floral opening diameter; f, Floral tube diamete; g, Floral tube depth; h, Nectar spur length; i, Nectar spur diameter; j, Pistil length; k, Stigma diameter; l, Stigma thickness; m, Stamen length; n, Anther length; o, Anther width; p, Anther thickness; q, Robbing hole’ length; r, Robbing hole’s width); D. Bombus melanurus forages the nectar through the corolla opening (legitimate visit); E. B. melanurus inserts its proboscis into the nectar spur’s base to rob nectar; F. B. eximius visits the flowers legitimately; G. B. eximius robs the nectar from the base of the nectar spur; H. B. sonani visits the flowers legitimately; I. B. sonani robs the nectar from the base of the nectar spur; J. Aporia agathon visits the flowers legitimately; K. Moths visits the flowers legitimately.

表1 长距忍冬7个野生居群的位置以及每一个居群中白色花、黄色花和橘红色花盗蜜率的比较(广义线性模型分析)。同一行中标注不同的小写字母的数值表示在该居群不同颜色花的盗蜜率存在显著性差异。

Table 1 The locations of the seven wild populations of Lonicera calcarata and comparison of nectar robbing rates of white, yellow, and orange-red flowers in each population (generalized linear model analysis). Different lower case letters in the same row indicate significant differences in nectar robbing rate among the different color flowers.

居群 Population	位置 Location			盗蜜率 Nectar robbing rate (%)			Wald χ²	df	P
	纬度 Latitude (°N)	经度 Longitude (°E)	海拔 Altitude (m)	白色花 White flowers	黄色花 Yellow flowers	橘红色花 Orange-red flowers	Wald χ²	df	P
1	23.14	104.81	1,939	15.81 ± 5.30^b	58.53 ± 13.36^a	60.88 ± 14.68^a	12.107	2	0.002
2	23.24	104.91	1,953	41.67 ± 22.05^b	89.71 ± 7.55^a	96.97 ± 3.03^a	12.895	2	0.002
3	23.16	104.82	1,920	32.82 ± 3.41^b	80.16 ± 8.40^a	83.33 ± 9.62^a	26.701	2	< 0.001
4	23.19	104.86	1,930	16.90 ± 6.91^b	34.17 ± 19.73^a	75.35 ± 9.01^a	22.566	2	< 0.001
5	23.29	104.76	1,941	11.97 ± 4.93^b	65.19 ± 17.12^a	72.50 ± 7.25^a	56.944	2	< 0.001
6	22.69	105.76	1,817	35.42 ± 7.38^b	32.97 ± 7.67^ab	58.78 ± 8.58^a	8.746	2	0.013
7	22.19	105.16	1,761	0.00 ± 0.00^c	20.00 ± 16.33^b	38.89 ± 18.59^a	42.372	2	< 0.001

图2 长距忍冬访花昆虫完善绢粉蝶、蛾类、黑尾熊蜂、B. eximius和楚南熊蜂的合法访问(即完成传粉过程)和盗蜜行为的访问频率的比较。不同大写字母表明不同的访花昆虫之间的合法访问的频率有显著性差异, 不同小写字母表示不同访花昆虫的盗蜜频率有显著性差异。ns表示同一种昆虫的合法访问频率和盗蜜频率没有显著性差异(P > 0.05), ***表示该昆虫的盗蜜频率显著高于访花的频率(P < 0.001)。

Fig. 2 Comparison of the frequency of legitimate visits (completing the pollination process) and nectar robbing behavior of Aporia agathon, moths, Bombus melanurus, B. eximius and B. sonani on Lonicera calcarata. Different uppercase letters indicate significant difference in the frequency of legitimate visits among different insects, while different lowercase letters indicate significant difference in the frequency of nectar robbing behavior among different insects. “ns” indicates no significant difference between the frequency of legitimate visit and nectar robbing behavior of the same insect (P > 0.05), while *** indicates that the nectar robbing frequency is significantly higher than the frequency of legitimate visits of the same insect (P < 0.001).

表2 长距忍冬白色、黄色和橘红色盗蜜的和正常的未被盗蜜的花的花部特征以及这3种颜色花的花蜜距中盗洞长和宽的比较(平均值士标准误，单位: mm,广义线性模”型)。同一颜色花中同一行不同的小写字母表示正常花和盗蜜花的该花部特征有显著性差异,较大的数值字体加粗表示。

Table 2 Comparison of floral characters between robbed and normal unrobbed flowers (white, yellow and orange-red) of Lonicera calcarata and nectar robbing hole size among these three colors flowers (mean土SE, units: mm, generalized linear model analysis). Different lowercase letters in the same row for one color flower indicate significant difference in the floral characters between robbed and normal flowers, with larger value in bold.

图3 长距忍冬正常花和盗蜜花在开花过程中3个时期花蜜的现存量(A)和糖浓度(B)的比较。不同的大写字母表明正常未被盗蜜的长距忍冬花蜜的现存量或者糖浓度在不同时期存在显著差异, 不同的小写字母表明盗蜜的长距忍冬花蜜的现存量或者糖浓度在不同时期存在显著性差异。***表明同一时期不同处理间存在显著性差异(P < 0.001), ns表明同一时期不同处理之间不存在显著性差异(P > 0.05)。

Fig. 3 Comparison of nectar volume (A) and sugar concentration (B) during three flowering stages of normal and robbed Lonicera calcarata flowers. Different uppercase letters indicate significant difference in nectar volume or sugar concentration of normal L. calcarata flowers at different stages. Different lowercase letters indicate significant difference in nectar volume or sugar concentration of robbed L. calcarata at different stages. *** indicates a significant difference (P < 0.001) between two treatments at the same stage, and “ns” indicates no significant difference (P > 0.05) between two treatments at the same stage.

图4 长距忍冬盗蜜的花苞和正常花苞中花粉总数(A)和胚珠总数(B)的比较, 以及长距忍冬不同授粉处理结实率的比较(C)。正常花粉授到盗蜜的柱头(缩写为NP*RS), 正常花粉授到正常的柱头(缩写为NP*NS), 盗蜜的花粉授到正常的柱头(缩写为RP*NS)。“ns”表示不同处理之间没有显著性差异(P > 0.05)。

Fig. 4 Comparison of total number of pollen grains (A) and ovules (B) between normal and robbed flower buds of Lonicera calcarata, and comparison of seed sets among different pollination treatments (C). Normal pollen * robbed stigma, abbreviated to NP*RS; normal pollen*normal stigma, abbreviated to NP*NS; robbed pollen * normal stigma, abbreviated to RP*NS. “ns” indicates no significant difference between the different treatments (P > 0.05).

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熊蜂盗蜜的花色偏好及对长距忍冬繁殖适合度的影响

The color preference of bumblebee nectar robbing and its impact on the reproductive fitness of Lonicera calcarata

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