2023PLoS BiologyOpen access

When cheating turns into a stabilizing mechanism of plant–pollinator communities

François Duchenne, Stéphane Aubert, Elisa Barreto, Emanuel Brenes, María A. Maglianesi, Tatiana Santander, Esteban A. Guevara, Catherine H. Graham

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Abstract

Mutualistic interactions, such as plant-mycorrhizal or plant-pollinator interactions, are widespread in ecological communities and frequently exploited by cheaters, species that profit from interactions without providing benefits in return. Cheating usually negatively affects the fitness of the individuals that are cheated on, but the effects of cheating at the community level remains poorly understood. Here, we describe 2 different kinds of cheating in mutualistic networks and use a generalized Lotka-Volterra model to show that they have very different consequences for the persistence of the community. Conservative cheating, where a species cheats on its mutualistic partners to escape the cost of mutualistic interactions, negatively affects community persistence. In contrast, innovative cheating occurs with species with whom legitimate interactions are not possible, because of a physiological or morphological barrier. Innovative cheating can enhance community persistence under some conditions: when cheaters have few mutualistic partners, cheat at low or intermediate frequency and the cost associated with mutualism is not too high. Under these conditions, the negative effects of cheating on partner persistence are overcompensated at the community level by the positive feedback loops that arise in diverse mutualistic communities. Using an empirical dataset of plant-bird interactions (hummingbirds and flowerpiercers), we found that observed cheating patterns are highly consistent with theoretical cheating patterns found to increase community persistence. This result suggests that the cheating patterns observed in nature could contribute to promote species coexistence in mutualistic communities, instead of necessarily destabilizing them.

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Mutualistic interactions, such as plant-mycorrhizal or plant-pollinator interactions, are widespread in ecological communities and frequently exploited by cheaters, species that profit from interactions without providing benefits in return. Cheating usually negatively affects the fitness of the individuals that are cheated on, but the effects of cheating at the community level remains poorly understood. Here, we describe 2 different kinds of cheating in mutualistic networks and use a generalized Lotka-Volterra model to show that they have very different consequences for the persistence of the community. Conservative cheating, where a species cheats on its mutualistic partners to escape the cost of mutualistic interactions, negatively affects community persistence. In contrast, innovative cheating occurs with species with whom legitimate interactions are not possible, because of a physiological or morphological barrier. Innovative cheating can enhance community persistence under some conditions: when cheaters have few mutualistic partners, cheat at low or intermediate frequency and the cost associated with mutualism is not too high. Under these conditions, the negative effects of cheating on partner persistence are overcompensated at the community level by the positive feedback loops that arise in diverse mutualistic communities. Using an empirical dataset of plant-bird interactions (hummingbirds and flowerpiercers), we found that observed cheating patterns are highly consistent with theoretical cheating patterns found to increase community persistence. This result suggests that the cheating patterns observed in nature could contribute to promote species coexistence in mutualistic communities, instead of necessarily destabilizing them.

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Available abstract

Mutualistic interactions, such as plant-mycorrhizal or plant-pollinator interactions, are widespread in ecological communities and frequently exploited by cheaters, species that profit from interactions without providing benefits in return. Cheating usually negatively affects the fitness of the individuals that are cheated on, but the effects of cheating at the community level remains poorly understood. Here, we describe 2 different kinds of cheating in mutualistic networks and use a generalized Lotka-Volterra model to show that they have very different consequences for the persistence of the community. Conservative cheating, where a species cheats on its mutualistic partners to escape the cost of mutualistic interactions, negatively affects community persistence. In contrast, innovative cheating occurs with species with whom legitimate interactions are not possible, because of a physiological or morphological barrier. Innovative cheating can enhance community persistence under some conditions: when cheaters have few mutualistic partners, cheat at low or intermediate frequency and the cost associated with mutualism is not too high. Under these conditions, the negative effects of cheating on partner persistence are overcompensated at the community level by the positive feedback loops that arise in diverse mutualistic communities. Using an empirical dataset of plant-bird interactions (hummingbirds and flowerpiercers), we found that observed cheating patterns are highly consistent with theoretical cheating patterns found to increase community persistence. This result suggests that the cheating patterns observed in nature could contribute to promote species coexistence in mutualistic communities, instead of necessarily destabilizing them.

Key concepts: Cheating, Mutualism (biology), Biology, Ecology, Persistence (discontinuity), Geotechnical engineering, Engineering

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