Mutualisms are important structuring forces in ecological communities that can mediate other biotic interactions. Yet, we still lack an understanding of the mechanisms that propagate the effects of mutualisms throughout community interaction networks. Legumes and aphids are both involved in mutualisms with microbial partners that mediate nitrogen (N) acquisition by the host. These mutualisms are linked by the antagonistic relationship between alfalfa aphids and their host plant. We studied the interaction between alfalfa (Medicago sativa) and aphids (Acyrthosiphon spp.) to determine whether soil N availability changes the strength of the respective host-microbe mutualisms, and whether this can affect the aphid-plant interaction. In particular, we asked whether the extent of rhizobial nodulation alters plant responses to aphid herbivory, and whether changes in plant N concentration or in the composition of N-based metabolites alter the aphid-Buchnera mutualism and resulting aphid herbivory. We addressed these questions by manipulating soil N availability in experimental barrels and pots and measuring plant chemistry, rhizobia nodulation rate, and plant and aphid biomass. This approach is complemented by data from an observational field study at a broad spatial scale.
Results/Conclusions
Variation in the strength of the alfalfa-rhizobia mutualism was correlated with plant chemistry and photosynthesis rate, but these effects were diminished—or reversed—when aphids are absent. Higher photosynthesis was linked to higher nodulation rates, but only when aphids were present. In addition, higher nodulation was linked to higher plant protein concentrations, but this effect was reversed in the presence of aphids. It appears that by acting as simultaneous carbon and N sinks, aphids subvert plant investment in their rhizobia mutualism by reducing positive N feedbacks from nodulation rates. At the same time, plants that had higher nodulation densities exhibited lower aphid densities, suggesting that the rhizobial mutualism could contribute to plant defense against aphids. Interestingly, at a given aphid density, aphids reduced plant protein more at higher nodulation densities, suggesting either that nodulation increased aphid N use efficiency, or that higher nodulation density shifts plant N allocation to compounds other than soluble proteins. Future work will explore whether this shift in defense strategy can affect aphid nutrition and the aphid-endosymbionnot relationship.