Specialized seed dispersal in Neotropical Vanilla reveals fruit unpalatability to omnivores

Flowering plants are essentially sessile organisms that disperse their genes through pollination, expanding their areas of occurrence through seed dispersal. In orchids, seed dispersal is commonly mediated by air currents. Conversely, members of several genera have evolved seeds adapted to endozoochory. This is the case for Vanilla, the most economically important genus in the orchid family. The role of indehiscent fruits in the attraction and rewarding of Vanilla seed dispersers was investigated based on field observations, analysis of fragrances, reward substances, and investigation of seed viability through the digestive tract. Indehiscent Vanilla fruits are consumed exclusively by herbivores, i.e. agoutis. Besides providing nutritional rewards, the fruits are rich in polyphenols that are unpalatable to omnivores. The most dominant compound in fruits is attractive only to agoutis. This is the first study showing synzoochory in Orchidaceae and specificity of seed dispersal in orchids. Indehiscent fruits may have evolved early in Neotropical Vanilla in response to selection pressures mediated by large herbivores as the genus emerged ca. 34 Mya in South America, concomitantly with megafauna diversification in the Oligocene. Extinction of the megafauna during the Pleistocene has left agoutis as inheritors of seed dispersal in species with large fleshy fruits. Apart from the effects on omnivores, this study shows that indehiscent fruits of V. chamissonis are consumed exclusively by agoutis, providing the first evidence of target mutualism in orchid seed dispersal.