Specific, non-nutritional association between an ascomycete fungus and Allomerus plant-ants.

Ant-fungus associations are well known from attine ants, whose nutrition is based on a symbiosis with basidiomycete fungi. Otherwise, only a few non-nutritional ant-fungus associations have been recorded to date. Here we focus on one of these associations involving Allomerus plant-ants that build galleried structures on their myrmecophytic hosts in order to ambush prey. We show that this association is not opportunistic because the ants select from a monophyletic group of closely related fungal haplotypes of an ascomycete species from the order Chaetothyriales that consistently grows on and has been isolated from the galleries. Both the ants' behaviour and an analysis of the genetic population structure of the ants and the fungus argue for host specificity in this interaction. The ants' behaviour reveals a major investment in manipulating, growing and cleaning the fungus. A molecular analysis of the fungus demonstrates the widespread occurrence of one haplotype and many other haplotypes with a lower occurrence, as well as significant variation in the presence of these fungal haplotypes between areas and ant species. Altogether, these results suggest that such an interaction might represent an as-yet undescribed type of specific association between ants and fungus in which the ants cultivate fungal mycelia to strengthen their hunting galleries.

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

Myrmecophytic symbioses are widespread in tropical ecosystems and their diversity makes them useful tools for understanding the origin and evolution of mutualisms. Obligate ant-plants, or myrmecophytes, provide a nesting place, and, often, food to a limited number of plant-ant species. In exchange, plant-ants protect their host plants from herbivores, competitors and pathogens, and can provide them with nutrients. Although most studies to date have highlighted a similar global pattern of interactions in these systems, little is known about the temporal structuring and dynamics of most of these associations. In this study we focused on the association between the understory myrmecophyte Hirtella physophora (Chrysobalanaceae) and its obligate ant partner Allomerus decemarticulatus (Myrmicinae). An examination of the life histories and growth rates of both partners demonstrated that this plant species has a much longer lifespan (up to about 350 years) than its associated ant colonies (up to about 21 years). The size of the ant colonies and their reproductive success were strongly limited by the available nesting space provided by the host plants. Moreover, the resident ants positively affected the vegetative growth of their host plant, but had a negative effect on its reproduction by reducing the number of flowers and fruits by more than 50%. Altogether our results are important to understanding the evolutionary dynamics of ant-plant symbioses. The highly specialized interaction between long-lived plants and ants with a shorter lifespan produces an asymmetry in the evolutionary rates of the interaction which, in return, can affect the degree to which the interests of the two partners converge.

Comparison between the anatomical and morphological structure of leaf blades and foliar domatia in the ant-plant Hirtella physophora (Chrysobalanaceae).

BACKGROUND AND AIMS: Myrmecophytes, or ant-plants, are characterized by their ability to shelter colonies of some ant species in hollow structures, or ant-domatia, that are often formed by hypertrophy of the internal tissue at specific locations (i.e. trunk, branches, thorns and leaf pouches). In Hirtella physophora (Chrysobalanaceae), the focal species of this study, the ant-domatia consist of leaf pouches formed when the leaf rolls over onto itself to create two spheres at the base of the blade. METHODS: The morphological and anatomical changes through which foliar ant-domatia developed from the laminas are studied for the first time by using fresh and fixed mature leaves from the same H. physophora individuals. KEY RESULTS: Ant-domatia were characterized by larger extra-floral nectaries, longer stomatal apertures and lower stomatal density. The anatomical structure of the domatia differed in the parenchymatous tissue where palisade and spongy parenchyma were indistinct; chloroplast density was lower and lignified sclerenchymal fibres were more numerous compared with the lamina. In addition, the domatia were thicker than the lamina, largely because the parenchymatous and epidermal cells were enlarged. CONCLUSIONS: Herein, the morphological and anatomical changes that permit foliar ant-domatia to be defined as a specialized leaf structure are highlighted. Similarities as well as structural modifications in the foliar ant-domatia compared with the lamina are discussed from botanical, functional and mutualistic points of view. These results are also important to understanding the reciprocal evolutionary changes in traits and, thus, the coevolutionary processes occurring in insect-plant mutualisms.

Comparative structure and ontogeny of the foliar domatia in three neotropical myrmecophytes.

The origin and timing of the appearance of leaf domatia during the ontogeny of plants are important evolutionary traits driving the maintenance of ant-plant associations. In this study conducted in French Guiana on Hirtella physophora, Maieta guianensis, and Tococa guianensis, we focused on the formation and development of leaf domatia having different morphological origins. We modeled the timing of the onset of these domatia, then compared their morpho-anatomical structure. Although the ontogenetic development of the domatia differed between species, they developed very early in the plant's ontogeny so that we did not note differences in the timing of the onset of these domatia. For H. physophora seedlings, a transitional leaf forms before the appearance of fully developed domatia, whereas in M. guianensis and T. guianensis the domatia forms abruptly without transitional leaves. Moreover, in all cases, the morpho-anatomical structure of the domatia differed considerably from the lamina. All three species had similar morpho-anatomical characteristics for the domatia, indicating a convergence in their structural and functional characteristics. This convergence between taxonomically distant plant species bearing domatia having different morphological origins could be interpreted as a product of the plant's evolution toward the morphology and anatomy most likely to maximize ant recruitment and long-term residence.