Abstract
Herbivores decrease plant fitness by consuming reproductive tissues, limiting resources, and/or affecting mutualisms. Although these mechanisms were extensively tested in chewing herbivores, the impact of other functional groups (e.g., sap-feeders) remains poorly understood. We investigated whether aphids affect plant reproduction via direct resource limitation on seed production and/or pollination interference. We compared plant traits and the seed set of naturally aphid-free vs. aphid-infested plants and then manipulated aphid presence and pollen receipt. We used path models to examine the links between variables. Nectar volume and seed set of aphid-infested plants was 54% and 42% lower than that of aphid-free plants. 72 h after removing aphids, nectar volume was restored to the level of aphid-free plants. When pollinators were excluded, the seed set of aphid-infested and aphid-free plants did not differ, suggesting that direct resource limitation on seed production was not the cause of reduced plant fitness. Manual addition of pollen restored the seed set of aphid-infested plants to the level of aphid-free plants, evidencing that plants were pollen limited. The path analysis showed a negative link between aphids and the seed set via nectar volume, supporting that nectar shortage caused by aphids may interfere with pollination and reduce plant fitness. Since aphids are crop pests and feed on a large number of animal-pollinated plants, the potential of these insects to influence pollination and plant fitness is high. This study emphasizes the ecological importance of aphids and the need to better understand the links between sap-feeding herbivory, pollination, and plant fitness.
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The datasets generated during and/or analyzed during the current study will be available in the Figshare Data Repository (https://figshare.com/).
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Acknowledgements
We thank MA Aizen and AG Farji-Brener for critical suggestions to earlier versions of this manuscript. We thank LL Ammassari for helping with seed counting, MA Oviedo-Diego for courageously helping in the field until late at night, M More and G San Blas for helping with moth identification, and J Ortego for helping with aphid identification. We thank Y Sasal for helping with path analyses and S Nanni for correcting the language. We appreciate the time spent by two anonymous reviewers who gave us helpful recommendations. AM Devegili is supported by a doctoral fellowship from the Consejo Nacional de Investigaciones Científicas y Técnicas of Argentina (CONICET) and VR Chalcoff is a researcher from the same institution.
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AMD and VRC conceived and designed the experiments; AMD and VRC collected the data and performed the experiments; AMD and VRC analyzed the data; AMD led the writing of the manuscript.
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Communicated by Monica Geber.
Herbivores are hypothesized to decrease plant fitness by consuming reproductive tissues, limiting resources, and/or affecting mutualisms, but few studies have focused on sap-feeding herbivores. Through a combination of field observations and experiments, we show that aphids reduce plant female fitness through an effect on pollination via the impoverishment of nectar rewards. This study contributes to a better understanding of the links between sap-feeding herbivory, pollination, and plant fitness, highlighting the ecological importance of aphids in flowering plant communities.
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Devegili, A.M., Chalcoff, V.R. Nectar shortage caused by aphids may reduce seed output via pollination interference. Oecologia 194, 321–332 (2020). https://doi.org/10.1007/s00442-020-04712-x
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DOI: https://doi.org/10.1007/s00442-020-04712-x