Making a master filterer: Ontogeny of specialized filtering plates in silver carp (Hypophthalmichthys molitrix)

Abstract

Filter feeding fishes possess several morphological adaptations necessary to capture and concentrate small particulate matter from the water column. Filter feeding teleosts typically employ elongated and tightly packed gill rakers with secondary bony or epithelial modifications that increase filtering efficiency. The gill rakers of Hypophthalmichthys molitrix, silver carp, are anatomically distinct from and more complex than the filtering apparatus of other teleostean fishes. The silver carp filtering apparatus is composed of biserial, fused filtering plates used to capture particles ranging in size from 4 to 80 μm. Early in ontogeny, at 15-25 mm standard length (SL), silver carp gill rakers are reminiscent of other more stereotypical teleostean rakers, characterized by individual lanceolate rakers that are tightly packed along the entirety of the branchial arches. At 30 mm SL, secondary epithelial projections and concomitant dermal ossification begin to stitch together individual gill rakers. During later juvenile stages, dermal bone further modifies the individual gill rakers and creates a bony scaffold that supports the now fully fused and porous epithelium. By adulthood, the stitching of bone and complete fusion of the overlying epithelium creates rigid filtering plates with morphologically distinct faces. The inner face of the plates is organized into a net-like matrix while the outer face has a sponge-like appearance comprised of differently sized pores. Here, we present morphological data from an ontogenetic series of the filtering apparatus within silver carp. These data inform hypotheses regarding both how these gill raker plates may have evolved from a more basal condition, as well as how this novel architecture allows this species to feed on exceedingly small phytoplankton, particles that represent a greater filtering challenge to the typical anatomy of the gill rakers of fishes.

The complex trophic anatomy of silver carp, Hypophthalmichthys molitrix, highlighting a novel type of epibranchial organ

“…The filtering plates in silver carp develop from individual GR that become fused during early ontogeny (Cohen & Hernandez, ). Although, the GR in other teleosts undergo morphological changes throughout ontogeny, no other species is known to completely fuse individual GR into rigid plates.…”

“…The filtering plates in silver carp develop from individual GR that become fused during early ontogeny (Cohen & Hernandez, 2018).…”

“…Modified GR corresponding to branchial arches 1-5 are found within the EBOs(Figure 2a) and complete a set number of rotations before terminating into the blind ends of the pharyngeal tubes. These are referred to throughout as "modified gill rakers" to distinguish these structures from the filtering plates found within the buccal cavity (described byCohen & Hernandez, 2018).The bilaterally paired EBOs are completely embedded within and surrounded by the dorsal palatal organ(Figure 3a).Pharyngeal jaws are robust with four large compressed teeth extending from the tooth plate on the medial edge of each jaw(Figure 2d,e). The teeth are oriented medially with the flattened surface facing dorsally.…”

Channeling vorticity: Modeling the filter-feeding mechanism in silver carp using μCT and 3D PIV

“…In particular, silver carp feed on a broad range of particle sizes from 4 to 85 µm (Cremer and Smitherman, 1980;Battonyai et al, 2015;Zhou et al, 2009), making them an effective competitor for planktonic resources in the eutrophic rivers of the Mississippi River basin ecosystem (Freedman et al, 2012). Cohen and Hernandez (2018) hypothesized that the greatly modified filtering apparatus of silver carp aids in the capture of particles so small that they are generally only consumed by invertebrates.…”

“…1A). Early in ontogeny, individual gill rakers stitch together, creating a mesh-like plate that continues to fuse together with secondary dermal bone modifications (Cohen and Hernandez, 2018). In addition, the inner and outer faces of the filtering plates are morphologically distinct.…”