Avian dispersal of "mimetic seeds" of Ormosia lignivalvis by terrestrial granivores: Deception or mutualism?

Abstract

Several tropical forest legume species producing hard and brightly-colored seeds, which apparently evolved as mimics of fleshy fruit and arillate-seed models, have been presumed to be dispersed by avian frugivores through non-mutualistic interactions involving sensorial deception. Here we examine the interactions between a typical so-called "mimetic seed" species and its potential dispersers in an Amazonian forest site, and propose that such interactions are best interpreted as mutualistic. Ormosia lignivalvis (Leguminosae: Papilionaceae) is a relatively rare but widespread canopy tree producing naked seeds with a conspicuous, bicolored (scarlet and black) hard seed coat, containing no nutrient rewards to its putative dispersers. Mature seeds are gradually released from dehiscent pods in a piecemeal fashion, during an extended fruiting period of up to 8 months, but may be retained by persistent funicles throughout the year. Intact Ormosia seeds were found in stomach contents of large-bodied terrestrial birds - including one tinamou, one trumpeter, and two cracid species which appear to be the main dispersers. On the other hand, a total of 185 h of vigils of 5 fruiting tree crowns failed to result in any observed cases of seed removal by arboreal frugivores. Laboratory measurements of seed resistance, elasticity, and hardness showed that Ormosia seeds are extremely hard, and could, therefore, aid in the mechanical breakdown of softer seeds which make up a large proportion of the diet of these terrestrial granivores. We argue that the hard, non-elastic O. lignivalvis seeds, and perhaps a number of other so-called mimetic-seed species, can function as similarly shaped and sized mineral grit universally swallowed by large gallinaceous birds, in that they help to crush and grind the mostly pliable seeds digested by their dispersers. This interaction is thus best described as a mutualism in that (1) Ormosia germination is greatly enhanced by the abrasive gut treatment of avian granivores, and (2) such birds would otherwise find no adequate gizzard grit substitutes in environments conspicuously lacking small pebbles, such as the lowland rainforests of sedimentary river basins of Amazonia.