The Chemical Ecology of Primate Seed Dispersal

Many tropical angiosperms rely on frugivores for seed dispersal and evolved fleshy fruits to attract them. Although both sides of the interaction are generalists, frugivores do not feed on the full range of fruit species in their habitats and angiosperms rely on the dispersal services of only a share of the frugivore community. This observation led to the “Dispersal Syndrome Hypothesis”, which postulates that over time fruits evolve to specialize on certain guilds of frugivorous seed dispersers and consequently their traits evolve in response to the dietary and sensory capacities of their main dispersal agents. Fruit traits such as size, seed size and husk thickness have been shown to be malleable to selection pressures exerted by their main seed-dispersal vectors. Additionally, due to competition for dispersal services and the need to promote consumption of ripe fruits and thus dispersal of mature seeds, fruits are also under selection pressures to provide reliable signals for ripeness. A prime example is fruit color, which has evolved independently in many bird-dispersed species to signal ripeness and possibly nutrient content. Fruit odor, similarly, has been speculated to be a signaling system between plants and frugivores with elaborated olfactory capabilities, but this has only recently received support in figs (genus Ficus) dispersed by bats. Yet data are still restricted to the narrow bat-fig model system and it is not clear whether fruit olfactory signaling has evolved in other plant genera and in the communication with other taxa, and thus indeed a recurring component of some Dispersal Syndromes. Primates are one of the most important seed dispersal vectors in the tropics. Until recently, their olfactory capabilities were considered low and thus irrelevant for the study of their feeding ecology. This view has been utterly revisited over the past years and primates are now known to possess high olfactory capacities. Therefore, under the framework of the Dispersal Syndrome Hypothesis, it is likely that fruits whose seeds they disperse evolved olfactory signals for ripeness, too. This thesis explores the evolution and functions of fruit aroma in the communication between primates and plants. The first chapter is a theoretical review regarding the roles of olfaction in primate feeding ecology. It concludes, based on available behavioral works, that frugivory is the dietary category that requires most reliance on olfaction in feeding primates, and that olfactory cues are used solely for the function of fruit selection from very short distances. So, primate-dispersed fruits are expected to be under pressure to provide signals that are not necessarily carried away to long distances, but rather maximize the ability to identify ripe fruits from close proximity. The second chapter is a comparative analysis of fruit odor in four Neotropical plant species, two dispersed by primates and two by birds. It demonstrates that ripe primate-dispersed fruits bear odors that are strong, compound-rich and significantly different from the odors of unripe fruits. Thus, their odors provide a reliable signal for ripeness that could be used for fruit selection. In contrast, bird-dispersed fruits emit relatively weak and compound-poor odors that are not different from the odors of unripe fruits. Hence, their odor profiles are not informative regarding their level of ripeness. Since each bird-dispersed species is phylogenetically closer to one primate-dispersed species than they are to one another, these patterns of odor release are independent of phylogeny. Therefore, the chapter concludes that fruit odor as a reliable signal for ripeness evolved in these two primate-dispersed species, independent of phylogeny and hence it is likely to constitute an adapted communication system with seed-dispersing primates. The third chapter reports olfactory-discrimination experiments that confirmed that primates indeed “understand” the signal – that they can physiologically discriminate between odors of ripe and unripe primate-dispersed fruits and choose ripe fruits based on their odor in the absence of cues from other trajectories. It further reports experiments which show that no single compound or compound class in the odor of fruits is significantly more important than others to allow ripe-fruit recognition. The final section provides a synthesis of the results and a framework for integrating the study of primate olfaction and fruit chemistry into a new “chemical ecology of primate-plant interactions”