Integrating ecological roles and trophic diversification on coral reefs: multiple lines of evidence identify parrotfishes as microphages

Coral reef ecosystems are remarkable for their high productivity in nutrient-poor waters. A high proportion of primary production is consumed by the dominant herbivore assemblage, teleost fishes, many of which are the product of recent and rapid diversification. Our review and synthesis of the trophodynamics of herbivorous reef fishes suggests that current models underestimate the level of resource partitioning, and thus trophic innovation, in this diverse assemblage. We examine several lines of evidence including feeding observations, trophic anatomy, and biochemical analyses of diet, tissue composition and digestive processes to show that the prevailing view (including explicit models) of parrotfishes as primary consumers of macroscopic algae is incompatible with available data. Instead, the data are consistent with the hypothesis that most parrotfishes are microphages that target cyanobacteria and other protein-rich autotrophic microorganisms that live on (epilithic) or within (endolithic) calcareous substrata, are epiphytic on algae or seagrasses, or endosymbiotic within sessile invertebrates. This novel view of parrotfish feeding biology provides a unified explanation for the apparently disparate range of feeding substrata used by parrotfishes, and integrates parrotfish nutrition with their ecological roles in reef bioerosion and sediment transport. Accelerated evolution in parrotfishes can now be explained as the result of (1) the ability to utilize a novel food resource for reef fishes, i.e. microscopic autotrophs; and (2) the partitioning of this resource by habitat and successional stage.