Flower visitor networks: Reduced reproductive success driven by antagonists in a hummingbird-pollinated species

IF 16.4 1区 化学 Q1 CHEMISTRY, MULTIDISCIPLINARY
Irene Gélvez-Zúñiga, Fernanda V. Costa, Alberto L. Teixido, Lorena Ashworth, Ramiro Aguilar, G. Wilson Fernandes
{"title":"Flower visitor networks: Reduced reproductive success driven by antagonists in a hummingbird-pollinated species","authors":"Irene Gélvez-Zúñiga,&nbsp;Fernanda V. Costa,&nbsp;Alberto L. Teixido,&nbsp;Lorena Ashworth,&nbsp;Ramiro Aguilar,&nbsp;G. Wilson Fernandes","doi":"10.1111/btp.13342","DOIUrl":null,"url":null,"abstract":"<p>Flower–animal interactions encompass a <i>continuum</i> of mutualistic to antagonistic behaviors. Although the importance of pollinators in interaction networks has been widely reported, the role of floral antagonists remains overlooked. In <i>Collaea cipoensis</i>, an endemic shrub from southeastern Brazil, we modeled an individual-based network assessing the flower visitors' functional behavior and tested if plant centrality increases fitness. Centrality indicates how well-connected a given plant is with the rest of the conspecifics through shared flower visitors. Specifically, we tested if flower visitor interactions are amplified by many-flowered individuals, and whether the relationship between centrality and plant fitness encompasses the effects of mutualists or antagonists. Subsequently, we quantified each visiting species' effectiveness. Antagonistic interactions were the most frequent in the network (97% of visits), primarily conducted by the nectar-robbing bee <i>Trigona spinipes</i> (66%), which was also the most central species and detrimental antagonist. The hummingbirds <i>Colibri serrirostris</i> and <i>Eupatomena macroura</i> were the most efficient pollinators, with a high contribution to the quantity—floral visitation—and the quality—viable seeds—components, respectively. Many-flowered plants showed greater centrality, which boosted the plant's cohesion in the network and increased flower visitation. Accordingly, many-flowered plants were better connected, mainly due to antagonistic visitors. Thus, centrality increases were not positively translated into more reproductive success. Our results reinforce the dynamic scenarios of flower–animal interactions, with consequences to plant reproductive ecology. We highlight the importance of incorporating distinct types of interactions to unveil the complexity of interacting systems, that when not explored, hide potential evolutionary consequences for plant reproductive success.</p><p>Abstract in Portuguese is available with online material.</p>","PeriodicalId":1,"journal":{"name":"Accounts of Chemical Research","volume":null,"pages":null},"PeriodicalIF":16.4000,"publicationDate":"2024-05-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Accounts of Chemical Research","FirstCategoryId":"93","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/btp.13342","RegionNum":1,"RegionCategory":"化学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"CHEMISTRY, MULTIDISCIPLINARY","Score":null,"Total":0}
引用次数: 0

Abstract

Flower–animal interactions encompass a continuum of mutualistic to antagonistic behaviors. Although the importance of pollinators in interaction networks has been widely reported, the role of floral antagonists remains overlooked. In Collaea cipoensis, an endemic shrub from southeastern Brazil, we modeled an individual-based network assessing the flower visitors' functional behavior and tested if plant centrality increases fitness. Centrality indicates how well-connected a given plant is with the rest of the conspecifics through shared flower visitors. Specifically, we tested if flower visitor interactions are amplified by many-flowered individuals, and whether the relationship between centrality and plant fitness encompasses the effects of mutualists or antagonists. Subsequently, we quantified each visiting species' effectiveness. Antagonistic interactions were the most frequent in the network (97% of visits), primarily conducted by the nectar-robbing bee Trigona spinipes (66%), which was also the most central species and detrimental antagonist. The hummingbirds Colibri serrirostris and Eupatomena macroura were the most efficient pollinators, with a high contribution to the quantity—floral visitation—and the quality—viable seeds—components, respectively. Many-flowered plants showed greater centrality, which boosted the plant's cohesion in the network and increased flower visitation. Accordingly, many-flowered plants were better connected, mainly due to antagonistic visitors. Thus, centrality increases were not positively translated into more reproductive success. Our results reinforce the dynamic scenarios of flower–animal interactions, with consequences to plant reproductive ecology. We highlight the importance of incorporating distinct types of interactions to unveil the complexity of interacting systems, that when not explored, hide potential evolutionary consequences for plant reproductive success.

Abstract in Portuguese is available with online material.

Abstract Image

Abstract Image

访花者网络:蜂鸟授粉物种的拮抗剂导致繁殖成功率降低
花与动物之间的相互作用包括从互利到拮抗的一系列行为。尽管授粉者在互动网络中的重要性已被广泛报道,但花的拮抗剂的作用仍被忽视。在巴西东南部的一种特有灌木 Collaea cipoensis 中,我们建立了一个基于个体的网络模型,评估了访花者的功能行为,并测试了植物的中心性是否会提高适应性。中心性表明特定植物通过共享访花者与其他同种植物的联系程度。具体来说,我们测试了多花个体是否会放大访花者之间的相互作用,以及中心度与植物适应性之间的关系是否包括互利者或拮抗者的影响。随后,我们对每种访花物种的有效性进行了量化。拮抗作用在网络中最为频繁(97% 的访问),主要由采蜜蜂 Trigona spinipes 进行(66%),它也是最中心的物种和最有害的拮抗剂。蜂鸟 Colibri serrirostris 和 Eupatomena macroura 是最有效的授粉者,它们分别对数量--花朵访问量和质量--可存活种子--这两个部分做出了很大贡献。多花植物显示出更高的中心性,这提高了植物在网络中的凝聚力,增加了花的访问量。因此,多花植物的连接性更好,这主要是由于拮抗访花者造成的。因此,中心度的增加并没有积极地转化为更多的繁殖成功。我们的研究结果加强了花与动物相互作用的动态情景,并对植物繁殖生态学产生了影响。我们强调了纳入不同类型的相互作用以揭示相互作用系统复杂性的重要性,如果不对其进行探索,就会隐藏对植物繁殖成功的潜在进化后果。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Accounts of Chemical Research
Accounts of Chemical Research 化学-化学综合
CiteScore
31.40
自引率
1.10%
发文量
312
审稿时长
2 months
期刊介绍: Accounts of Chemical Research presents short, concise and critical articles offering easy-to-read overviews of basic research and applications in all areas of chemistry and biochemistry. These short reviews focus on research from the author’s own laboratory and are designed to teach the reader about a research project. In addition, Accounts of Chemical Research publishes commentaries that give an informed opinion on a current research problem. Special Issues online are devoted to a single topic of unusual activity and significance. Accounts of Chemical Research replaces the traditional article abstract with an article "Conspectus." These entries synopsize the research affording the reader a closer look at the content and significance of an article. Through this provision of a more detailed description of the article contents, the Conspectus enhances the article's discoverability by search engines and the exposure for the research.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信