生物多样性 ›› 2018, Vol. 26 ›› Issue (5): 498-509.doi: 10.17520/biods.2018046

• 研究报告 • 上一篇    下一篇

荒漠短命植物异喙菊的小花异形性及繁殖特性

吉乃提汗·马木提1, 成小军1, 谭敦炎1, 2, *()   

  1. 1 新疆农业大学草业与环境科学学院, 新疆草地资源与生态重点实验室及西部干旱荒漠区草地资源与生态教育部重点实验室, 乌鲁木齐 830052
    2 吉首大学生物资源与环境科学学院, 湖南吉首 416000
  • 收稿日期:2018-02-09 接受日期:2018-05-15 出版日期:2018-05-20
  • 通讯作者: 谭敦炎 E-mail:tandunyan@163.com
  • 作者简介:

    # 共同第一作者

  • 基金项目:
    国家自然科学基金(U1603231, 31460128, 31760060)

Heteromorphism of florets and reproductive characteristics in Heteracia szovitsii (Asteraceae), a desert ephemeral annual herb

Jannathan Mamut1, Xiaojun Cheng1, Dunyan Tan1, 2, *()   

  1. 1 Xinjiang Key Laboratory of Grassland Resources and Ecology & Ministry of Education Key Laboratory for Western Arid Region Grassland Resources and Ecology, College of Grassland and Environment Sciences, Xinjiang Agricultural University, Ürümqi 830052;
    2 College of Biology and Environmental Sciences, Jishou University, Jishou, Hunan 416000
  • Received:2018-02-09 Accepted:2018-05-15 Online:2018-05-20
  • Contact: Tan Dunyan E-mail:tandunyan@163.com
  • About author:

    # Co-first authors

异喙菊(Heteracia szovitsii)是分布于新疆北部荒漠、具短寿命花和多态果实的菊科一年生短命植物。本文对该物种的开花式样和花部特征以及繁育系统与昆虫传粉特性进行了研究, 以期明确其头状花序中小花的形态差异及其与多态果实间的关系、揭示其在短的花寿命内的繁殖特性。结果表明: 该物种头状花序中发育成多态果实的3类小花在数量、冠毛的有无以及舌片长/宽、子房宽、花柱裂片长和子房喙长之间均存在不同程度的差异, 且3类小花冠毛的有无以及子房宽和喙长与多态果实的形态一致, 说明多态果实的数量与形态在小花发育过程中就已完成分化。花序中的小花每天集中在上午开放, 使花序在功能上犹如一朵花, 可快速增大花展示和对传粉者的吸引, 以使异交在开花后短时间内完成; 3类小花的自花花粉均可在花柱裂片上萌发并长出花粉管, 说明该物种自交亲和。3类小花不去雄套袋后均能结实, 且自然授粉后的结实率显著高于不去雄套袋的, 说明该物种能自主自花授粉, 且异花授粉促进了结实。3类小花通过雄性先熟以及次级花粉呈现中的泵/刷机制, 将花粉呈现在花柱上部和未展开的柱头裂片外侧刷状毛上以及裂片顶端, 延长了花粉呈现(雄性阶段)持续的时间, 减少了花内雌雄功能间的干扰, 有利于传粉者异花传粉, 提高了雄/雌性适合度; 同时, 柱头裂片展开时可将自花花粉落置到裂片上, 以完成自主自花授粉。主要传粉者六显甜花蜂(Halictus sexnotatulus)的访花时间与花序开放时间、花粉活力最高期和柱头最佳授粉期高度吻合, 有利于雄性阶段花粉的输出以及雌性阶段柱头接受花粉, 保障授粉在开花后短时间内快速有效地完成以及异交成功。在新疆北部荒漠的春季环境中, 具短寿命花的异喙菊既可在低温多风导致传粉者不足或活动受限时, 通过快速自主自花授粉及自交亲和机制来提供繁殖保障, 也可在传粉者活动正常时, 通过集中开花、雄性先熟及次级花粉呈现等机制来快速完成异交, 提高雌/雄性及后代的适合度。

关键词: Heteracia szovitsii, 异形小花, 短寿命花, 自主自花授粉, 次级花粉呈现, 传粉

Heteracia szovitsii (Asteraceae) is a common ephemeral annual species occurring only in desert regions of northern Xinjiang in China, with short-lived florets and achenes within a single infructescence (capitulum) having three different morphs. To explore the relationship between morphological differences in florets and the polymorphic fruits and reproductive characteristics, we compared floral traits, flowering pattern, and flower visitors to the three floral morphs in H. szovitsii, and reproductive efforts by hand pollination treatments. The results showed that: Peripheral and intermediate florets did not have pappus, while central florets did. Number of florets and length and width of ligules were significantly different among the three floral morphs in a single capitulum. Further, the length of stigma lobes of peripheral florets was significantly greater than that of central florets, the length of ovary beaks of central florets was significantly greater than that of peripheral and intermediate florets. Differences in morphology with or without pappus, width of ovaries, length of ovary beaks among three morphs of florets were consistent with those of three morphs of achenes. These results indicated that the numbers of three morphs of achenes and their morphology had differentiated during the development period of three kinds of florets. The concentrated flowering pattern of blooming in the morning of three kinds of florets within capitulum, made the capitulum act as functional units, i.e. like a flower, thereby increasing flower display and attracting pollinators. Pollinator visits may facilitate outcrossing during the short flower longevity. Pollen grains of the three floral morphs could germinate and produce pollen tubes on their stigma lobes, indicating that this species is self-compatible. The three kinds of florets bagged without emasculation all can produce achenes, but fruit-set was all significantly lower than that of natural pollination, suggesting that this species could be autogamous and cross-pollination could increase fruit set. Due to the protandrous and the pump/bush mechanism of secondary pollen presentation, pollen of three floral morphs was present at the apex of the stigma and on the brush of hairs of both the upper part of style and outside lateral of the closed stigma lobes. This character prolonged the duration of pollen presentation (male stage), and reduced the interference between male and female functions within flower, promoted cross pollination, thereby improving male/female fitness. Meanwhile, it could allow the pollen deposition on the lobes when the stigma lobes expanded to complete self-pollination autonomously. Halictus sexnotatulus was the most frequent floral visitor, and the duration time among insects visiting, inflorescence opening, highest pollen viability and the highest stigma receptivity had a high degree of synchronicity. This strategy facilitated the output of pollen at the male stage and receipt of pollen on the stigma at the female stage, thus ensuring that pollination was completed quickly and effectively in a short time after flowering and that outcrossing was successful. In the desert spring environment of the northern Xinjiang, H. szovitsii with short-lived florets can not only provide reproductive assurance via autonomous self-pollination quickly under the condition of the lack of pollinators and/or limited activity due to low temperatures and windy conditions, but also can provide the opportunities for outcrossing, through concentrated flowering, protandry and secondary pollen presentation when environmental conditions became favorable for pollinator activities.

Key words: Heteracia szovitsii, heteromorphic florets, short-lived florets, autonomous self-pollination, secondary pollen presentation, pollination

图1

异喙菊头状花序与小花的形态、花粉呈现和访花昆虫。(A)头状花序纵剖面; (B)小花及其花粉呈现 (a: 外围小花, b: 过渡小花; c: 中央小花; d: 子房喙; e: 冠毛, f: 花粉呈现); (C)六显甜花蜂; (D)细腹食蚜蝇; (E)缘斑鼓额蚜蝇。"

表1

异喙菊3类小花在头状花序中的开放动态(平均值 ± 标准误差)"

日开放动态
Diurnal flowering dynamics
外围小花
Peripheral floret
过渡小花
Intermediate floret
中央小花
Central floret
F P
花冠舌片展开到柱头从聚药雄蕊筒中伸出持续时间
Duration time from corolla ligules expanding to stigma
exposure from sygensious stamen tube (min)
19.13 ± 0.60a 12.20 ± 0.59b 10.53 ± 0.45c 67.718 < 0.001
柱头伸出到柱头裂片完全开展持续时间 Duration time from stigma exposure until its lobes are completely expanded (min) 51.40 ± 0.98a 45.10 ± 1.28b 33.23 ± 0.80c 78.218 < 0.001
柱头裂片完全开展到花冠舌片萎蔫闭合持续时间
Duration time from stigma lobes completely expanded until
corolla ligules wilt and close (min)
110.20 ± 1.71a 57.40 ± 1.35b 18.83 ± 0.71c 119.43 < 0.001
单花开放持续时间 Anthesis duration time per floret (min) 173.81 ± 2.33a 109.77 ± 1.37b 74.47 ± 1.23c 855.503 < 0.001

表2

异喙菊头状花序中小花的数量特征(平均值 ± 标准误)"

花类型
Type of floret
外围小花
Peripheral floret
过渡小花
Intermediate floret
中央小花
Central floret
F P
每花序花数目 No. of florets per capitulum 8.02 ± 0.13a 10.10 ± 0.35b 15.60 ± 0.63c 100.09 < 0.05
冠毛 Pappi 数目 Number - - 44.85 ± 1.21 - -
长 Length (mm) - - 3.01 ± 0.04 - -
花冠 Corolla 舌片 Ligule 长 Length (mm) 4.89 ± 0.10a 4.28 ± 0.08b 3.92 ± 0.05c 37.82 < 0.05
宽 Width (mm) 1.84 ± 0.06a 1.56 ± 0.03b 1.37 ± 0.02c 46.02 < 0.05
花冠筒长 Length of corolla tubes (mm) 1.49 ± 0.05a 1.37 ± 0.07a 1.35 ± 0.06a 1.71 0.19
雄蕊 Stamen 花丝长 Length of filaments (mm) 1.07 ± 0.05a 1.02 ± 0.07a 1.04 ± 0.06a 0.17 0.85
花药长 Length of anthers (mm) 1.10 ± 0.04a 1.15 ± 0.03a 1.17 ± 0.04a 1.23 0.30
雌蕊 Pistil
子房 Ovary 长 Length (mm) 1.18 ± 0.06a 1.03 ± 0.05b 0.91 ± 0.03b 8.62 < 0.05
宽 Width (mm) 0.93 ± 0.04a 0.57 ± 0.03b 0.39 ± 0.02c 70.91 < 0.05
子房喙长 Length of ovary beaks (mm) 0.30 ± 0.02a 0.32 ± 0.02a 0.36 ± 0.01b 4.34 < 0.05
花柱长 Length of style (mm) 4.06 ± 0.15a 4.21 ± 0.14a 3.84 ± 0.15a 1.64 0.20
柱头裂片长 Length of stigma lobes (mm) 0.81 ± 0.03a 0.77 ± 0.03ab 0.72 ± 0.01b 3.13 < 0.05

图2

荧光显微镜下异喙菊花粉在柱头上落置、萌发及花 粉管生长情况。(A)花粉落置; (B)花粉萌发(a: 花粉; b: 花粉管)。"

图3

异喙菊3类小花的花粉活力动态变化曲线"

表3

异喙菊3类小花在不同处理下的结实率(%, 平均值 ± 标准误)"

花类型 Type of florets 自然传粉 Natural pollination 不去雄套纸袋 Bagged florets without emasculation F1 P
外围小花 Peripheral floret 90.16 ± 1.79Aa 79.05 ± 2.42Ab 6.08 < 0.001
过渡小花 Intermediate floret 88.14 ± 1.81Aa 74.60 ± 3.01Ab 7.90 < 0.001
中央小花 Central floret 87.87 ± 1.56Aa 77.58 ± 1.71Aa 8.16 < 0.001
F2 0.53 0.86
P 0.592 0.426

图4

异喙菊主要传粉者六显甜花蜂的访花频率"

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