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      Asymmetrical disassortative pollination in a distylous primrose: the complementary roles of bumblebee nectar robbers and syrphid flies

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          Abstract

          Heterostyly is a floral polymorphism characterized by reciprocal herkogamy maintained through high levels of mating between morphs, serviced by appropriate pollinators. We studied how differential efficiency and abundance of distinct pollinators affect plant female reproduction in self- and intra-morph incompatible distylous Primula secundiflora. Bumblebees and syrphid flies were found to be the most abundant floral visitors. Bumblebees frequently exhibited nectar-robbing behavior. Because the robbing holes were always situated between the high- and low-level organs on both morphs, nectar-robbing bumblebees only pollinated S-styled flowers. L-styled flowers set four times as many seeds as did S-styled flowers after being visited by pollen-collecting syrphid flies. The natural female fecundity and the magnitude of pollen limitation varied between the morphs within populations because of the mosaic distribution of nectar-robbing bumblebees and syrphid flies. L-styled flowers and S-styled flowers set the same number of seeds after supplemental hand pollination, indicating equivalent female reproductive potential. We suggest that bumblebee nectar robbers and syrphid flies play an important role in sustaining the floral dimorphism of heterostyly in P. secundiflora because of their complementary roles in the pollination system.

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          Pollen flow in the distylous Palicourea fendleri (Rubiaceae): an experimental test of the Disassortative Pollen Flow Hypothesis.

          The Disassortative Pollen Flow Hypothesis proposed by Darwin postulates that the relative position of anthers and stigmas in distylous flowers enhances pollen flow between flowers of different morphs (legitimate pollination), in comparison to flow between flowers of the same morph (illegitimate pollination). In order to test this hypothesis, we measured pollen transport, mediated by a trained Copper-rumped Hummingbird (Amazilia tobaci), between flowers of the distylous Palicourea fendleri under laboratory conditions. In individual tests, we offered to the hummingbird a pollen donor flower and two emasculated recipient flowers in a controlled sequence. After each foraging bout, we counted the number of pollen grains transported from the donor flower to the stigmas of both recipient flowers. In agreement with Darwin's hypothesis, we found that hummingbirds transport pollen of "pin" flowers in significantly higher numbers to legitimate "thrum" stigmas, even if previously visiting a "pin" flower. However, "thrum" pollen was deposited in greater numbers on illegitimate "thrum" stigmas. We interpret this asymmetry largely as the consequence of floral morphology; pollen flow was greater between anthers and stigmas that exhibit greater spatial matching. In P. fendleri, the position of floral organs along the corolla tube does not always precisely correspond. In our experimental system, the probability that the pollinator extracts a pollen grain from the anther and the probability of self-pollination were both dependent on the type of floral morph. We discuss the relevance of the latter findings in relation to other studies of pollen flow in heterostylous species.
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            Pollinator shifts and the loss of style polymorphism in Narcissus papyraceus (Amaryllidaceae).

            Darwin proposed that the driving force for the evolution of style polymorphisms is the promotion of cross-pollination between style morphs, through accurate placement of pollen on the pollinator's body. This hypothesis has received much attention, but the effect of different pollinators in the fitness of morphs remains poorly understood. Narcissus papyraceus is a style dimorphic species (long -L- and short -S- styled) with isoplethic (1 : 1) and L-monomorphic populations, mainly visited by long-tongued (LT) nocturnal and short-tongued (ST) diurnal pollinators, respectively. We studied natural female fertility of morphs, and assessed the role of diurnal and nocturnal pollinators. We also quantified female fertility of the morphs in experimental populations with different morph ratio, exposed to predominately long- or short-tongued pollinators. We found that with LT pollinators, both morphs were successfully pollinated in all morph ratio conditions, suggesting that these insects could be involved in maintenance of the polymorphism, although other factors may also play a role. However, with ST pollinators, S-plants displayed less fertility than L-plants, and mating among L-plants was favoured, implying that the polymorphism is lost. These results underscore the role of pollinators on variations in style polymorphism.
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              Relative Stability of Core Groups in Pollination Networks in a Biodiversity Hotspot over Four Years

              Plants and their pollinators form pollination networks integral to the evolution and persistence of species in communities. Previous studies suggest that pollination network structure remains nested while network composition is highly dynamic. However, little is known about temporal variation in the structure and function of plant-pollinator networks, especially in species-rich communities where the strength of pollinator competition is predicted to be high. Here we quantify temporal variation of pollination networks over four consecutive years in an alpine meadow in the Hengduan Mountains biodiversity hotspot in China. We found that ranked positions and idiosyncratic temperatures of both plants and pollinators were more conservative between consecutive years than in non-consecutive years. Although network compositions exhibited high turnover, generalized core groups – decomposed by a k-core algorithm – were much more stable than peripheral groups. Given the high rate of turnover observed, we suggest that identical plants and pollinators that persist for at least two successive years sustain pollination services at the community level. Our data do not support theoretical predictions of a high proportion of specialized links within species-rich communities. Plants were relatively specialized, exhibiting less variability in pollinator composition at pollinator functional group level than at the species level. Both specialized and generalized plants experienced narrow variation in functional pollinator groups. The dynamic nature of pollination networks in the alpine meadow demonstrates the potential for networks to mitigate the effects of fluctuations in species composition in a high biodiversity area.
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                Author and article information

                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group
                2045-2322
                12 January 2015
                2015
                : 5
                : 7721
                Affiliations
                [1 ]Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden , Chinese Academy of Sciences, Mengla, 666303, China
                [2 ]University of Chinese Academy of Sciences , 10049, China
                [3 ]Kunming Institute of Botany, Chinese Academy of Sciences , Kunming, 650204, China
                Author notes
                Article
                srep07721
                10.1038/srep07721
                4289899
                25579323
                a03b66eb-dd36-47f7-98e8-82aefe8ed4c7
                Copyright © 2015, Macmillan Publishers Limited. All rights reserved

                This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder in order to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/4.0/

                History
                : 29 May 2014
                : 08 December 2014
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