The importance of phylogenetic distance and functional-trait dissimilarity between alien and native plant species in the formation of novel pollination mutualisms
Final Report Abstract
When exotic species conquer new regions, new combinations of exotic and native species interact. For flowering plants, exotic species, once they have invaded a region, can often successfully compete with native species for pollinators. However, local plant species may facilitate the initial establishment of closely related exotic species by providing them with a large range of existing pollinators. As one would expect that plant species which are related or have similar flowers will attract similar flower visitors, we tested if evolutionary relatedness and floral similarity of exotic to native plants influenced their ability to attract flower visitors. In a field experiment, we simulated an early stage of plant invasion by introducing potted exotic plants into native plant communities. Using multiple species (34 exotics and 20 natives), we could manipulate the degrees of evolutionary relatedness and floral similarity between exotic and native plants. We paired each exotic plant with a native plant, observed the frequency of floral visits to them, and assessed the composition of the flower visitors. Evolutionary relatedness and floral similarity to local species influenced the frequency of floral visits to exotic species in different ways. Exotic plants that were either closely related or distantly related to local plants, and with intermediate floral similarity to natives, received most floral visits. Exotic plants that were distantly related to native plants, and with either low or high floral similarity to natives, received more similar flower visitors to locals. Native plants may help closely related exotic plants to attract existing flower visiting insects, and exotic plants that are distantly related to locals can avoid competing for flower visitors with them. Exotic plants with flowers that are not too different to those of native plants are likely to receive floral visits, and their flowers are not too similar to those of the natives to compete with them. These findings illustrate how an interplay of facilitation and competition for flower visiting insects can simultaneously explain indirect interactions between exotic and native plants. Competition for pollinators between plants that share pollinators may also increase movements of pollen between different plant species by shared pollinators. Such pollen transfer between different species can have negative consequences on plant reproduction due to the deposition of foreign pollen. Foreign pollen deposition on the stigma can interfere with the fertilization of ovules by pollen from the same species, and lead to a reduced fruit and seed production. As foreign pollen from exotic plants can interfere with the reproduction of native plants by reducing fruit and seed production, pollen interference has been proposed as a mechanism contributing to the success of exotic plants. In our study, we also investigated the opposite interaction. We did a large multi-species experiment in which we used nine exotic and 11 native species as both pollen donors and recipients (in 81 species combinations), and considered the degrees of evolutionary relatedness and floral trait similarity between pollen recipients and donors in our analysis. We found that both exotic and native recipients suffered from foreign pollen from donors of the opposite status in terms of fruit and seed production. Evolutionary relatedness did not affect fruit and seed production. However, style-length distance decreased, while pollen-size distance increased pollen interference. We conclude that pollen interference affects both native and exotic recipients, thus indirectly altering community composition. Importantly, we found that pollen interference can be a mechanism that increases biotic resistance of natives against exotics. The experimental studies in this project provide new insights on the indirect interactions mediated by pollinators between exotic and native plants. The findings highlight that the influence of evolutionary relatedness measured as phylogenetic distance and floral trait similarity on the outcomes of species interactions do not need to be consistent, as evolutionary relatedness and floral similarity may reflect different ecological mechanisms. Seemingly opposing mechanisms such as pollinator facilitation and competition for pollinators can simultaneously act to engage the formation of novel pollination interactions.
Publications
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(2018) Phenological shifts and flower visitation of 185 lowland and alpine species in a lowland botanical garden. Alpine Botany 128:23-33
Razanajatovo M., Föhr C., van Kleunen M. & Fischer M.
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(2019) Autofertility and self-compatibility moderately benefit island colonization of plants. Global Ecology and Biogeography 28: 341-352
Razanajatovo M., van Kleunen M., Kreft H., Dawson W., Essl F., Pergl J., Pyšek P., Winter M. & Weigelt P.
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(2020) Do floral traits and the selfing capacity of Mimulus guttatus plastically respond to experimental temperature changes? Oecologia 192: 261-272
Razanajatovo M., Fischer L. & van Kleunen M.
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(2020) Reciprocal heterospecific pollen interference among alien and native species
Malecore, E.M., Berthelot, S., van Kleunen, M., Razanajatovo, M.
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(2021) The role of phylogenetic relatedness on alien plant success depends on the stage of invasion. Nature Plants
Omer A., Fristoe T., Yang Q., Razanajatovo M., Weigelt P., Kreft H., Dawson W., Dullinger S., Essl F. Pergl J., Pyšek P. & van Kleunen M.
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(2021) Widespread vulnerability of flowering plant seed production to pollinator declines. Science Advances 7: eabd3524
Rodger, J. G., Bennett, J. M., Razanajatovo, M., Knight, T. M., Kleunen, M. v., Ashman, T.-L., Steets, J. A., Hui, C., Arceo-Gómez, G., Burd, M., Burkle, L. A., Burns, J. H., Durka, W., Freitas, L., Kemp, J. E., Li, J., Pauw, A., Vamosi, J. C., Wolowski, M., Xia, J. & Ellis, A. G.
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(2021). Reciprocal heterospecific pollen interference among alien and native species. Perspectives in Plant Ecology, Evolution and Systematics 50, 125610
Malecore E. M., Berthelot, S., van Kleunen, M., & Razanajatovo, M.
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(2022) Flower visitation of alien plants is non-linearly related to phylogenetic and floral similarity to native plants
Razanajatovo M., Rakoto Joseph F., Rajaonarivelo Andrianina P. & van Kleunen M.
