Seed dispersers shape the pulp nutrients of fleshy-fruited plants

Abstract

The dispersal-syndrome hypothesis posits that fruit traits are a product of selection by frugivores. Although criticized as adaptationist, recent studies have suggested that traits such as fruit or seed size, colour and odour exhibit signatures that imply selection by animal mutualists. These traits imply nutritional rewards (e.g. lipid, carbohydrate), attracting frugivores; however, this remains incompletely resolved. Here, we investigated whether fruit nutrients (lipid, sugar, protein, vitamin C, water content) moderate the co-adaptation of key disperser-group mutualisms. Multivariate techniques revealed that fruit nutrients assembled non-randomly and grouped according to key dispersal modes. Bird-dispersed fruits were richer in lipids than mammal-dispersed fruits. Mixed-dispersed fruits had significantly higher vitamin C than did mammal- or bird-dispersed fruits separately. Sugar and water content were consistently high irrespective of dispersal modes, suggesting that these traits appeal to both avian and mammalian frugivores to match high-energy requirements. Similarly, protein content was low irrespective of dispersal modes, corroborating that birds and mammals avoid protein-rich fruits, which are often associated with toxic levels of nitrogenous secondary compounds. Our results provide substantial over-arching evidence that seed disperser assemblages co-exert fundamental selection pressures on fruit nutrient trait adaptation, with broad implications for structuring fruit-frugivore mutualism and maintaining fruit trait diversity.

Keywords: dietary switching; fleshy-fruited plants; fruit pulp; fruit–frugivore mutualism; nutrient traits; seed dispersal syndromes.

Figure 1.

Variations in water content and in the concentration of four fruit pulp nutrients (%) based on dry pulp mass. Numbers in histograms represent sample size. Error bars show standard deviation (s.d.) of the mean.

Figure 2.

The percentage of four fruit pulp nutrient concentrations based on dry pulp mass, along with water content based on fresh pulp mass in mammal-, bird- and mixed-dispersed fruits. (a–e) Lipid, protein, water, sugar and vitamin C, respectively. Error bars show standard deviation (s.d) of the mean. Different letters above bars indicate significant differences.

Figure 3.

The results of principal coordinate analysis (PCoA) of a pairwise distance matrix. Each seed dispersers guild category is represented as a coloured dot: bird-dispersed fruits (red), mammal-dispersed fruits (green) and mix-dispersed fruits (blue). The x-axis and y-axis represent two dimensions of percentage variation explained by the PCoA. Ellipses are included for visualization purposes. The significance of analysis of similarities is shown within the figure. (Online version in colour.)