Trade-offs in an ant–plant–fungus mutualism

• Published in: Proceedings of the Royal Society. B, Biological sciences Vol. 284; no. 1850; p. 20161679
• Main Authors: Orivel, Jérôme, Malé, Pierre-Jean, Lauth, Jérémie, Roux, Olivier, Petitclerc, Frédéric, Dejean, Alain, Leroy, Céline
• Format: Journal Article
• Language: English
• Published: England The Royal Society 15.03.2017; The Royal Society Publishing; Royal Society, The
• Edition: Royal Society (Great Britain)
• Subjects: Animal behavior; Animals; Ants; Ants - physiology; Ant–plant–fungus Interaction; Coexistence; Colonies; Cultivation; Dispersal; Fitness; Foliage; Formicidae; French Guiana; Fungi; Fungi - physiology; Galleries; Growth rate; Herbivores; Herbivory; Host plants; Investment; Life Sciences; Mutualism; Plant protection; Plants; Plants (botany); Prey; Queens; Special Feature; Species; Species Coexistence; Symbiosis; Tradeoffs; dispersal; Hirtella; allomerus; ant–plant–fungus interaction; mutualism; species coexistence; écologie végétale; champignon; hirtella
• ISSN: 0962-8452; 1471-2954
• DOI: 10.1098/rspb.2016.1679

Species engaged in multiple, simultaneous mutualisms are subject to trade-offs in their mutualistic investment if the traits involved in each interaction are overlapping, which can lead to conflicts and affect the longevity of these associations. We investigate this issue via a tripartite mutualism involving an ant plant, two competing ant species and a fungus the ants cultivate to build galleries under the stems of their host plant to capture insect prey. The use of the galleries represents an innovative prey capture strategy compared with the more typical strategy of foraging on leaves. However, because of a limited worker force in their colonies, the prey capture behaviour of the ants results in a trade-off between plant protection (i.e. the ants patrol the foliage and attack intruders including herbivores) and ambushing prey in the galleries, which has a cascading effect on the fitness of all of the partners. The quantification of partners' traits and effects showed that the two ant species differed in their mutualistic investment. Less investment in the galleries (i.e. in fungal cultivation) translated into more benefits for the plant in terms of less herbivory and higher growth rates and vice versa. However, the greater vegetative growth of the plants did not produce a positive fitness effect for the better mutualistic ant species in terms of colony size and production of sexuals nor was the mutualist compensated by the wider dispersal of its queens. As a consequence, although the better ant mutualist is the one that provides more benefits to its host plant, its lower host–plant exploitation does not give this ant species a competitive advantage. The local coexistence of the ant species is thus fleeting and should eventually lead to the exclusion of the less competitive species.