Neotropical Ant-Gardens: Behavioral and Chemical Ecology of an Obligate Ant-Plant Mutualism

Abstract

Seed dispersal mutualisms are essential for the survival of diverse plant species and communities worldwide. An outstanding but poorly understood ant-seed mutualism occurs in the Amazonian rainforest, where arboreal ants collect seeds of several taxonomically diverse plant species and cultivate them in nutrient-rich nests, forming abundant hanging gardens known as ant-gardens (AGs). AG ants and plants are dominant members of lowland Amazonian ecosystems, and their interaction is obligate and apparently species-specific. Though established AGs are limited to specific participants, it is unknown at what stage specificity arises. Seed fate pathways in AG epiphytes are undocumented, and the recognition cues that mediate the mutualism are unknown. Here the species specificity of the AG ant-seed interaction is assessed, and chemical cues are characterized that elicit seed-finding and seed-carrying in AG ants. To examine the specificity of the ant-seed interaction, general food baits and seeds of the AG plant <i>Peperomia macrostachya</i> were offered on alternate days at 108 bait stations. Seventy ant species were detected at food baits and could have interacted with AG seeds, but only three species collected <i>P. macrostachya</i> seeds, and 84% of observed seed removal by ants was attributed to the AG ant <i>Camponotus femoratus</i>. In a separate experiment, arthropod exclusion significantly reduced AG seed removal rates, but vertebrate exclusion did not. Thus species specific seed dispersal, rather than post-dispersal processes, appears to be the primary determinant of the distribution of AG plants. The results also begin to quantify factors that affect seed fate in this unusually specific plant-animal mutualism. To characterize behavioral cues on AG seeds, solvent extracts of three species (<i>Anthurium gracile</i>, <i>Codonanthe uleana</i>, and P. macrostachya</i>) were subjected to chromatographic fractionation. To test behavioral activity, each fraction was applied to other seeds that ants ordinarily ignore. At least one fraction of each seed extract elicited retrieval behavior in <i>C. femoratus</i>, but the active fractions of the three species differed in chemical composition, indicating that each plant species elicits seed-carrying with a different class of chemical attractants. Volatile attractants from <i>P. macrostachya</i> were further investigated using Y-tube olfactometer assays and gas chromatography-electroantennographic detection. In the olfactometer, <i>C. femoratus</i> preferred the odor of <i>P. macrostachya</i> seeds over that of control seeds, and <i>P. macrostachya</i> extract over solvent control. Five electrophysiologically active phenolic and terpenoid compounds from <i>P. macrostachya</i> extract were identified and combined in a synthetic blend, which was also preferred over solvent control and over a single component alone. Although seed dispersal by ants is common worldwide, this is the first documentation of volatile attractants from any ant-dispersed seed. Furthermore, the most abundant component of the attractive blend, geranyl linalool, is toxic to many ant species, hinting at one mechanism by which AG seeds may avoid being collected by inappropriate dispersers. Future studies of AGs should address costs and benefits of the interaction to its various participants, evaluate the consequences of the interaction for gene flow and population structure in the plants, and assess geographic variation in ant and seed traits that facilitate the interaction. Such studies would bear on central themes in the theory of mutualism, including the origin of mutualism, the evolution and coevolution of traits that facilitate the interaction, evolution and maintenance of species-specificity, and prevention of cheating. Furthermore, the taxonomic diversity of AG participants provides a unique opportunity to examine these questions in distantly related species that have all converged upon a similar mutualistic survival strategy.