Low Levels of Fruit Nitrogen as Drivers for the Evolution of Madagascar's Primate Communities.

The uneven representation of frugivorous mammals and birds across tropical regions - high in the New World, low in Madagascar and intermediate in Africa and Asia - represents a long-standing enigma in ecology. Several hypotheses have been proposed to explain these differences but the ultimate drivers remain unclear. Here, we tested the hypothesis that fruits in Madagascar contain insufficient nitrogen to meet primate metabolic requirements, thus constraining the evolution of frugivory. We performed a global analysis of nitrogen in fruits consumed by primates, as collated from 79 studies. Our results showed that average frugivory among lemur communities was lower compared to New World and Asian-African primate communities. Fruits in Madagascar contain lower average nitrogen than those in the New World and Old World. Nitrogen content in the overall diets of primate species did not differ significantly between major taxonomic radiations. There is no relationship between fruit protein and the degree of frugivory among primates either globally or within regions, with the exception of Madagascar. This suggests that low protein availability in fruits influences current lemur communities to select for protein from other sources, whereas in the New World and Old World other factors are more significant in shaping primate communities.

Possible fruit protein effects on primate communities in madagascar and the neotropics.

BACKGROUND: The ecological factors contributing to the evolution of tropical vertebrate communities are still poorly understood. Primate communities of the tropical Americas have fewer folivorous but more frugivorous genera than tropical regions of the Old World and especially many more frugivorous genera than Madagascar. Reasons for this phenomenon are largely unexplored. We developed the hypothesis that Neotropical fruits have higher protein concentrations than fruits from Madagascar and that the higher representation of frugivorous genera in the Neotropics is linked to high protein concentrations in fruits. Low fruit protein concentrations in Madagascar would restrict the evolution of frugivores in Malagasy communities. METHODOLOGY/PRINCIPAL FINDINGS: We reviewed the literature for nitrogen concentrations in fruits from the Neotropics and from Madagascar, and analyzed fruits from an additional six sites in the Neotropics and six sites in Madagascar. Fruits from the Neotropical sites contain significantly more nitrogen than fruits from the Madagascar sites. Nitrogen concentrations in New World fruits are above the concentrations to satisfy nitrogen requirements of primates, while they are at the lower end or below the concentrations to cover primate protein needs in Madagascar. CONCLUSIONS/SIGNIFICANCE: Fruits at most sites in the Neotropics contain enough protein to satisfy the protein needs of primates. Thus, selection pressure to develop new adaptations for foods that are difficult to digest (such as leaves) may have been lower in the Neotropics than in Madagascar. The low nitrogen concentrations in fruits from Madagascar may contribute to the almost complete absence of frugivorous primate species on this island.

Tree dispersal strategies in the littoral forest of Sainte Luce (SE-Madagascar).

Zoochory is the most common mode of seed dispersal for the majority of plant species in the tropics. Based on the assumption of tight plant-animal interactions several hypotheses have been developed to investigate the origin of life history traits of plant diaspores and their dispersers, such as species-specific co-evolution, the low/high investment model (low investment in single fruits but massive fruiting to attract many different frugivores versus high investment in single fruits and fruit production for extended periods to provide food for few frugivores), and the evolution of syndromes which represent plant adaptations to disperser groups (e.g. birds, mammals, mixed). To test these hypotheses the dispersal strategies of 34 tree species were determined in the littoral forest of Sainte Luce (SE-Madagascar) with the help of fruit traps and tree watches. The impact of fruit consumers on the seeds was determined based on detailed behavioral observations. Phenological, morphological and biochemical fruit traits from tree species were measured to look for co-variation with different types of dispersal. No indication for species-specific co-evolution could be found nor any support for the low/high investment model. However dispersal syndromes could be distinguished as diaspores dispersed by birds, mammals or both groups (mixed) differ in the size of their fruits and seeds, fruit shape, and seed number, but not in biochemical traits. Five large-seeded tree species seem to depend critically on the largest lemur, Eulemur fulvus collaris, for seed dispersal. However, this does not represent a case of tight species-specific co-evolution. Rather it seems to be the consequence of the extinction of the larger frugivorous birds and lemurs which might also have fed on these large fruits. Nevertheless these interactions are of crucial importance to conserve the integrity of the forest.