Recent studies about mutualism consider the complexity and versatility of the relationship, in addition to highlighting the importance of the cost/benefit balance between the two protagonists. Because species interactions are highly dependent on the environment, the climate changes foreseen for the coming years are expected to have significant impacts on the evolution of mutualistic interactions. Among mutualisms, the aphid–ant interaction is well documented, partly explained by the pest status of aphids. This literature review focuses on the impact of climate change (particularly atmospheric carbon dioxide concentration and temperature) on aphid biology and the potential consequences with respect to their mutualistic interactions with ants. We provide an overview of the published reports concerned with the effects of temperature and carbon dioxide on aphids, for which a positive, a negative or no effect has been highlighted. We then discuss how climatic changes can alter four major components of aphid biology that are shaping their interaction with ants: (i) aphid population growth; (ii) aphid behaviour and mobility; (iii) honeydew production and composition; and (iv) semiochemistry. Finaly, we discuss the limitations of such studies on aphid–ant mutualism, as well as the information that is still needed to predict how climate change might impact this type of relationship.
Honeydew is considered a cornerstone of the interactions between aphids and their natural enemies. Bacteria activity occurring in aphid honeydew typically results in the release of volatile organic compounds (VOCs) that are used by the natural enemies of aphids to locate their prey. Because atmospheric carbon dioxide (CO2) concentration directly impacts the physiology of plants, we raise the hypothesis that elevated CO2 concentrations impact the quantity of honeydew produced by aphids, as well as the diversity and quantity of honeydew VOCs, leading to cascade effects on the foraging behavior of aphids’ natural enemies. Using solid-phase microextraction, we analyzed the VOCs emitted by honeydew from pea aphids (Acyrthosiphon pisum Harris) reared under 450 ± 50 ppm of CO2 (aCO2) or 800 ± 50 ppm CO2 (eCO2). While the total amount of honeydew excreted was only slightly reduced by eCO2 concentrations, we detected qualitative and quantitative differences in the semiochemistry of aphid honeydew between CO2 conditions. Three VOCs were not found in the honeydew of eCO2 aphids: 3-methyl-2-buten-1-ol, 2-methyl-1-butanol, and isobutanol. However, no difference was observed in the searching and oviposition behaviors of hoverfly (Episyrphus balteatus (De Geer)) females exposed to plants covered with honeydew originating from the different CO2 conditions. The present work showed the effect of a particular aspect of atmospheric changes, and should be extended to other abiotic parameters, such as temperature.
Chemically mediated interaction through so-called infochemicals (Hay, 2009;, often also referred to as semiochemicals, is arguably the oldest and most widespread form of communication (Wyatt, 2003). Infochemicals provide the basis for the vast majority of ecological processes across the tree of life in both terrestrial and aquatic ecosystems (Brönmark & Hansson, 2012;Wyatt, 2014), serving as cues or signals released into the surroundings or present on the surface of organisms (Wyatt, 2014). They cover a broad range of functions, mediating
1. Climate change will likely affect the association between species interacting at different trophic levels. However, studies focusing on the impact of an elevation of temperature on ant-hemipteran mutualism remain scarce. 2. In the present study we investigated, in laboratory conditions, the foraging behaviour of the ant Lasius niger and its mutualistic interaction with the aphid Aphis fabae under three conditions of temperatures (i.e. 20 ∘ C, 23 ∘ C, and 26 ∘ C), as predicted by climatic scenarios. 3. Aphids were more mobile but as likely to release honeydew droplets at higher temperatures. As regards the ants, a moderate 3 ∘ C increase of temperature positively impacted their mutualistic interaction with aphids. Such reinforcement was achieved through an increase in the walking speed of ant foragers, in the number of mobilised ants as well as in the total amount of honeydew harvested by the colony. 4. A further elevation of temperature to 26 ∘ C reduced the benefits gained by the aphid-tending ants, in terms of lower amount of collected honeydew. 5. Based on our results, we hypothesise that, in temperate regions, a moderate increase of ambient atmospheric temperature by 3 ∘ C will benefit to the L. niger-A. fabae mutualistic interaction. A more marked elevation of 6 ∘ C may represent a threshold thermal value above which a switch of partners or a disruption of the interaction may occur under the temperatures predicted for the end of the century. These results demonstrate the fragility of mutualistic interactions, and more particularly their sensitivity to temperature increases predicted by realistic forecast models.
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