Metabarcoding dietary analysis of coral dwelling predatory fish demonstrates the minor contribution of coral mutualists to their highly partitioned, generalist diet

Abstract

Understanding the role of predators in food webs can be challenging in highly diverse predator/prey systems composed of small cryptic species. DNA based dietary analysis can supplement predator removal experiments and provide high resolution for prey identification. Here we use a metabarcoding approach to provide initial insights into the diet and functional role of coral-dwelling predatory fish feeding on small invertebrates. Fish were collected in Moorea (French Polynesia) where the BIOCODE project has generated DNA barcodes for numerous coral associated invertebrate species. Pyrosequencing data revealed a total of 292 Operational Taxonomic Units (OTU) in the gut contents of the arc-eye hawkfish ( Paracirrhites arcatus), the flame hawkfish ( Neocirrhites armatus) and the coral croucher ( Caracanthus maculatus). One hundred forty-nine (51%) of them had species-level matches in reference libraries (>98% similarity) while 76 additional OTUs (26%) could be identified to higher taxonomic levels. Decapods that have a mutualistic relationship with Pocillopora and are typically dominant among coral branches, represent a minor contribution of the predators’ diets. Instead, predators mainly consumed transient species including pelagic taxa such as copepods, chaetognaths and siphonophores suggesting non random feeding behavior. We also identified prey species known to have direct negative interactions with stony corals, such as Hapalocarcinus sp, a gall crab considered a coral parasite, as well as species of vermetid snails known for their deleterious effects on coral growth. Pocillopora DNA accounted for 20.8% and 20.1% of total number of sequences in the guts of the flame hawkfish and coral croucher but it was not detected in the guts of the arc-eye hawkfish. Comparison of diets among the three fishes demonstrates remarkable partitioning with nearly 80% of prey items consumed by only one predator. Overall, the taxonomic resolution provided by the metabarcoding approach highlights a highly complex interaction web and demonstrates that levels of trophic partitioning among coral reef fishes have likely been underestimated. Therefore, we strongly encourage further empirical approaches to dietary studies prior to making assumptions of trophic equivalency in food web reconstruction.