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

Abstract

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.

Signal and reward in wild fleshy fruits: Does fruit scent predict nutrient content?

“…Presumably, this and other effects may be weak enough if large amounts of protein in the pulp would result in large amounts of N/S compounds in the scent, which will mask other factors like microbial activity. Alas, protein levels in Malagasy fruits, in this study and in others (Donati et al, ; Ganzhorn et al, ; Valenta & Melin, ), are very low relative to fleshy fruits in other tropical systems. Not surprisingly, the scent of Malagasy fruits also tends to include fewer N/S compounds (Nevo & Valenta, ).…”

Effect of Site Attributes and Matrix Composition on Neotropical Primate Species Richness and Functional Traits: A Comparison Among Regions

“…Although such variation was weak for species retention, this was consistent in a global-scale study in which South America showed higher species richness than Madagascar for a given fragment size, and that species richness in Africa has no significant relationship with fragment size [34]. Primates from Madagascar face a limited dietary quality and this could decrease the likelihood of their persistence in small fragments [114]. The non-relationship in Africa is due to the extant taxa being resistant to anthropogenic landscape alterations [34].…”

Assessing the function of geophagy in a Malagasy rain forest lemur

“…Dietary supplementation is a well‐accepted explanation for primate geophagy (Table S2). While Madagascar's lemurs face unique nutritional challenges (Donati et al., ; Wright, ), geophagy patterns similar to those of other primates persist. Like sifakas, Formosan macaques exhibit no age or sex bias in soil consumption and annually consume soil from numerous sites (Hsu et al., ).…”

“…This difference is most significant during the austral winter months, when animals in unlogged forest spend up to 26% more time feeding on fruits/seeds than sifakas living in logged forest (Arrigo‐Nelson, ). Given the nutritional differences between fruits, seeds, and leaves ( e.g ., Altmann, Post & Klein, ; Arrigo‐Nelson, , Donati et al., ; Ganzhorn et al., ; National Research Council ), sifaka diets in logged forest likely contain not only fewer sugars and fats, but also fewer plant secondary metabolites (PSMs) from seeds than those in unlogged forest due to the lower proportion of fruits and seeds in their diet. PSMs, such as toxins ( e.g ., alkaloids) and protein inhibitors ( e.g ., tannins), may cause animals physiological harm or inhibit protein intake—costs that must be weighed against the nutritional benefits of a particular food item (Glander, ).…”