Indirect defense in a highly specific ant–plant mutualism

Abstract

Although associations between myrmecophytes and their plant ants are recognized as a particularly effective form of protective mutualism, their functioning remains incompletely understood. This field study examined the ant-plant Hirtella physophora and its obligate ant associate Allomerus decemarticulatus. We formulated two hypotheses on the highly specific nature of this association: (1) Ant presence should be correlated with a marked reduction in the amount of herbivory on the plant foliage; (2) ant activity should be consistent with the "optimal defense" theory predicting that the most vulnerable and valuable parts of the plant are the best defended. We validated the first hypothesis by demonstrating that for ant-excluded plants, expanding leaves, but also newly matured ones in the long term, suffered significantly more herbivore damage than ant-inhabited plants. We showed that A. decemarticulatus workers represent both constitutive and inducible defenses for their host, by patrolling its foliage and rapidly recruiting nestmates to foliar wounds. On examining how these activities change according to the leaves' developmental stage, we found that the number of patrolling ants dramatically decreased as the leaves matured, while leaf wounds induced ant recruitment regardless of the leaf's age. The resulting level of these indirect defenses was roughly proportional to leaf vulnerability and value during its development, thus validating our second hypothesis predicting optimal protection. This led us to discuss the factors influencing ant activity on the plant's surface. Our study emphasizes the importance of studying both the constitutive and inducible components of indirect defense when evaluating its efficacy and optimality.

Trade-offs in an ant–plant–fungus mutualism

“…Nonetheless, it should be noted that, although its presence is less beneficial for the plant, A. decemarticulatus remains a mutualist, as the net outcome experienced by H. physophora from the interaction is positive. These ants also protect the foliage by patrolling on leaves, so that host plants have a better level of fitness when associated with A. decemarticulatus than when devoid of ants [24,29]. The fitness of both ant species (R 2 in figure 1) should be qualitatively affected in a similar way by the differential growth rate of their host plant as their colony growth is highly correlated with plant size.…”

“…All Allomerus species are specialist plant-ants inhabiting a variety of myrmecophytic hosts [27]. Concerning the A. octoarticulatus and A. decemarticulatus species studied thus far, the workers protect their host plant from defoliators through their predatory behaviour [9,28,29]. On the other hand, these two ant species are also known to impose costs on their host plants through their castration behaviour, which favours the vegetative growth of the plant and thus the production of more nesting space [30][31][32][33].…”

“…R. Soc. B 284: 20161679 but still tender, leaves per plant between 13.00 and 15.00, a timeframe that corresponds to the species' main period of activity [29,34]. Statistical comparisons were conducted, using GLMM with plant ID as a random effect.…”

Dynamics of the association between a long-lived understory myrmecophyte and its specific associated ants

“…Control and ant-excluded plants were compared according to either their total vegetative or reproductive investments during the 16-month period. We started the census 2 months after removing the ants because Grangier et al (2008) demonstrated that excluding the ants has no eVect on the rate of herbivory after 40 days.…”

Ecologia comportamental e de interações entre <i>Pseudomyrmex concolor</i> Smith (Hymenoptera, Formicidae, Pseudomyrmecinae) e sua planta hospedeira <i>Tachigali myrmecophila</i> Ducke (Fabaceae: Caesalpinioideae) na Amazônia amapaense

“…Portanto, formigas enquanto defesa biótica induzida devem ser eficazes em resguardar partes mais custosas (e.g. folhas jovens) para o desenvolvimento das plantas com as quais interagem de forma mutualista (Janzen, 1972;Brouat et al, 2000;Grangier et al, 2008;Heil & McKey, 2003;Dáttilo et al, 2015).…”