Functional impact and trophic morphology of small, sand-sifting fishes on coral reefs

Abstract

Oligotrophic tropical coral reefs are built on efficient internal energy and nutrient cycling, facilitated by tight trophic interactions. In the competition for available prey, some small fishes have evolved to feed on apparently barren sand patches that connect hard-substratum patches in many reef habitats. One strategy for obtaining prey from a particulate matrix is to sift out small prey items from the sediment (often called ‘winnowing’). Yet, the trophic link between small winnowing consumers and their prey are poorly resolved, let alone the morphological specialisations that enable this foraging behaviour. We used aquarium-based feeding experiments to quantify the impact of winnowing by two sand-dwelling goby species (Valenciennea sexguttata and Valenciennea strigata) on meiobenthos abundance and diversity and examined their actual ingestion of meiobenthos using gut content analysis. To identify potential morphological structures involved in winnowing, we investigated the gobies' feeding apparatus with electron microscopy (SEM) and micro-computed tomography (micro-CT). After 4 days of sifting through the sand matrix, the two species significantly reduced meiobenthic prey abundance by 30.7% ± 9.2 SE (V. sexguttata) and 46.1% ± 5.1 SE (V. strigata), but had little impact on the meiobenthic diversity. The most abundant prey groups (copepods and annelids) experienced the greatest reduction in number, suggesting selection by size, shape and density of prey items. Furthermore, gut content analysis confirmed that winnowing gobies can efficiently separate meiobenthic prey from heavier inorganic particles (sand), likely facilitated by a specialised epibranchial lobe, pharyngeal jaws and highly abundant papillose taste buds in the oropharyngeal cavity. Our results provide important background on the trophic link between the meiobenthos and winnowing gobies on coral reefs. The revealed specialisations of the goby feeding apparatus facilitate sand-sifting foraging behaviour and access to an otherwise inaccessible trophic niche of microscopic prey. By having evolved a specialised strategy to obtain nutritious and highly abundant prey from seemingly barren sand, we suggest that winnowing gobies act as an important conduit for sand-derived energy to higher trophic levels. Read the free Plain Language Summary for this article on the Journal blog.