Ants are less attracted to the extrafloral nectar of plants with symbiotic, nitrogen‐fixing rhizobia

Abstract

Plants simultaneously maintain mutualistic relationships with different partners that are connected through the same host, but do not interact directly. One or more participating mutualists may alter their host's phenotype, resulting in a shift in the host's ecological interactions with all other mutualists involved. Understanding the functional interplay of mutualists associated with the same host remains an important challenge in biology. Here, we show belowground nitrogen-fixing rhizobia on lima bean (Phaseolus lunatus) alter their host plant's defensive mutualism with aboveground ants. We induced extrafloral nectar (EFN), an indirect defense acting through ant attraction. We also measured various nutritive and defensive plant traits, biomass, and counted ants on rhizobial and rhizobia-free plants. Rhizobia increased plant protein as well as cyanogenesis, a direct chemical defense against herbivores, but decreased EFN. Ants were significantly more attracted to rhizobia-free plants, and our structural equation model shows a strong link between rhizobia and reduced EFN as well as between EFN and ants: the sole path to ant recruitment. The rhizobia-mediated effects on simultaneously expressed defensive plant traits indicate rhizobia can have significant bottom-up effects on higher trophic levels. Our results show belowground symbionts play a critical and underestimated role in determining aboveground mutualistic interactions.

Effects of Soil Organisms on Aboveground Plant-Insect Interactions in the Field: Patterns, Mechanisms and the Role of Methodology

“…However, this is not necessarily the case, as rhizobia have been shown to also affect plant defense responses directly (e.g., Thamer et al, 2011) and indirectly (Godschalx et al, 2015). The latter is illustrated by a study with potted plants placed in the field that reported positive effects of the addition of Rhizobium sp.…”

“…Ants can act as natural enemies of herbivores and this study suggests that rhizobia can interfere with this indirect plant defense mechanism. In the presence of rhizobia, cyanogenesis (a chemical defense in legumes) is increased, and this may reduce the need for the plant to produce extrafloral nectar to attract ants (Godschalx et al, 2015).…”

“…Plant nutritional value (most importantly, nitrogen and sugar content) in the field can be positively affected by soil organisms (Gange and West, 1994;Gange et al, 2005a,b;Younginger et al, 2009;Moon et al, 2013;Brunner et al, 2015;Godschalx et al, 2015;Ryalls et al, 2016). Moreover, plant secondary defense metabolites, that play a role in the palatability of host plants, can be affected by soil organisms in the field (Wurst et al, 2008;Megías and Müller, 2010).…”

Multiple mutualist effects on genomewide expression in the tripartite association between Medicago truncatula, nitrogen‐fixing bacteria and mycorrhizal fungi

“…; Godschalx et al . ), so much so that most organisms interact with many different mutualists simultaneously or sequentially throughout their lives. Empirical studies have recognized that complementarity and conflict among multiple mutualist can have substantial and diverse effects on the success of organisms that cannot be detected based on pairwise studies (Champawat ; Lau & Galloway ; Ness ; Bracken et al .…”

Microbial Root Mutualists Affect the Predators and Pathogens of Herbivores above Ground: Mechanisms, Magnitudes, and Missing Links

“…For example, in Vicia faba, association with AMF reduces extrafloral nectaries, which may result in reduced protection by ants against herbivores (Laird and Addicott, 2007). Similarly, rhizobia reduce extrafloral nectar production by lima beans (Phaseolus lunatus), leading to fewer ants attracted to rhizobia associated plants (Godschalx et al, 2015). Here, the mechanistic basis underlying the tri-trophic interaction above ground appears to be a tradeoff in plant resource allocation between root mutualists and indirect defense rewards.…”