Plant-ants feed their host plant, but above all a fungal symbiont to recycle nitrogen

Abstract

In ant -plant symbioses, plants provide symbiotic ants with food and specialized nesting cavities (called domatia). In many ant -plant symbioses, a fungal patch grows within each domatium. The symbiotic nature of the fungal association has been shown in the ant-plant Leonardoxa africana and its protective mutualist ant Petalomyrmex phylax. To decipher trophic fluxes among the three partners, food enriched in 13 C and 15 N was given to the ants and tracked in the different parts of the symbiosis up to 660 days later. The plant received a small, but significant, amount of nitrogen from the ants. However, the ants fed more intensively the fungus. The pattern of isotope enrichment in the system indicated an ant behaviour that functions specifically to feed the fungus. After 660 days, the introduced nitrogen was still present in the system and homogeneously distributed among ant, plant and fungal compartments, indicating efficient recycling within the symbiosis. Another experiment showed that the plant surface absorbed nutrients (in the form of simple molecules) whether or not it is coated by fungus. Our study provides arguments for a mutualistic status of the fungal associate and a framework for investigating the previously unsuspected complexity of food webs in ant -plant mutualisms.

Plant-ants use symbiotic fungi as a food source: new insight into the nutritional ecology of ant–plant interactions

“…phylax workers do not feed their larvae with infrabuccal pellets, larvae nevertheless ingested fungal hyphae, suggesting active feeding on domatia fungi in this species at least. Behavioural observations [10], specificity of fungal strains with plant-ant species [15] and trophic flow from ants to domatia fungi [16] also suggest tight interaction between domatia fungi and plant-ants. The use of these fungi as a food source thus probably explains why ants maintain them within domatia.…”

“…Whether the ants depend on this resource still remains to be determined. Defossez et al [16] fed Pe. phylax ants with 15 N and showed that N was transferred to the fungal patch and the host plant within 10 days.…”

“…Recent molecular investigations showed that the fungi occupying domatia in a very diverse set of myrmecophytes from throughout the tropics all belong to the ascomycete order Chaetothyriales, and that each seems to be somewhat specific to a particular ant -plant symbiosis [10,15]. Moreover, recent characterization of trophic fluxes among the three partners showed that plant-ants provide their symbiotic fungi with nutrients, probably through the accumulation of waste products [16]. However, the role of fungi in these tripartite symbioses is not yet clear.…”

“…The symbiotic nature of the relationship between domatia-inhabiting fungi and plant-ants, and the peculiar behaviour of ants towards fungal patches [10,16], led us to consider that these interactions could be new cases of agriculture by insects. In this context, we tested the hypothesis that plant-ants consume the symbiotic fungi growing within domatia of their host plants.…”

Protein coadaptation and the design of novel approaches to identify protein–protein interactions

“…Thus, rhizobiales bacteria and AMF share some molecular pathways aimed at the establishment of a morphological link with their hosts and the transfer of nitrogen; reciprocally, the process activates similar molecular pathways in the plant, although the final symbiotic structures are different. Recently, two new and independent symbiotic systems of plant and ants have been found to involve a third mutualist species of a fungus that provides nitrogen to the plants (58,59). The study at the molecular level of these symbiotic systems might provide important insights in the evolution of symbioses that fix nitrogen in plants.…”