Filtration at the mega-scale: Exploring the filter morphology and filtration mechanisms in the cartilaginous fishes

Abstract

Suspension feeding in the cartilaginous fishes evolved approximately 66-22 million years ago and is manifest in four independently evolved lineages of fishes (Cetorhinidae, Megachasmidae, Rhincodontidae, and Mobulidae). The mechanisms of filtration used by fishes are reflective of the morphology and composition of the filtering tissues. I found the filter morphology and the mechanisms of filtration in the 11 species of devil rays are different from all other filtering fishes. I used a combination of gross anatomical descriptions, scanning electron microscopy (SEM), histology, modeling, and live performance data to describe the anatomy and filtration mechanisms in the devil rays. The filter pads are offset, chevron-shaped, rigid, cartilaginous structures composed of repeating filter lobes located on the anterior (toward the incoming flow) and posterior (toward the esophagus) surfaces of the epibranchial and ceratobranchial arches. SEM and histology show that the ultrastructure of the leaf-like, ascending filter lobes varies between species; however, most are keratinous and can be either smooth or covered in cilia and some include the presence of denticles. The shape and surface of the terminal filtering lobes are distinct in each species and may be used as a tool for species identification. In some species, the stratified squamous epithelium contains a high density of mucus cells, likely serving as a mechanism for sticky sieve filtration while in others the mucus producing cells are absent. Fluid flow in the devil rays is unusual; it does not follow a continuous, parallel trajectory through the buccopharyngeal cavity as in other suspension feeding fishes. Instead there is an abrupt 90° turn from the initial inflowing path to move through the laterally directed branchial filter pores, over the gill tissue, and out the ventrally located gill slits. The deviation from the incoming flow results in tangential shearing stress (cross-flow) across the filter surface. This implies that devil rays can use cross-flow filtration to clear the filter after particles are caught by inertial impaction, direct interception, and/or sieving mechanisms.