Anatomical and physiological studies of bigheaded carps demonstrate that the epibranchial organ functions as a pharyngeal taste organ

Abstract

The epibranchial organ (EO) is an enigmatic tubular organ found in the pharyngeal cavity of many filter-feeding fishes. We investigated whether it might function as a taste organ that mediates aggregation and ingestion of planktonic food within the buccal cavity. The EO and associated structures of bighead and silver carps, two successful and invasive planktivorous fishes, were examined using histological and electrophysiological techniques. Both species possess finely structured gill rakers that extend directly via a series of protrusions into each of the four blind canals which are organized as the muscular EO, suggesting that the gill rakers and EO probably function in an integrated manner. Both the interior and exterior surfaces of the EOs of both species are covered with high densities of taste buds and solitary chemosensory cells (SCCs) as well as mucous cells. Conversely, taste buds are scarce in both the buccal cavities and external portions of the head and mouth of both species. Electrophysiological recordings from a caudal branch of the vagus nerve (cranial nerve X) found to innervate the EO showed it to be sensitive to chemicals found in a planktonic diet. L-Amino acids accounted for some, but not all of the neural activity. We conclude that taste buds and SCCs located on the EO and gill rakers probably serve to chemically detect food particles, which the EO then aggregates by mucus secretion before eventually expelling them onto the floor of the pharynx for ingestion. This specialized, pharyngeal chemosensory structure may explain the feeding success of these, and perhaps other planktivorous, filter-feeding fishes.

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

“…This final involution at the posterior end of the EBO creates a final exit between the posterior median triangular fold (#5, Figure a) and the pharyngeal jaws (Figure c). Contrary to results (for both bighead and silver carp) published by Hansen, Ghosal, Caprio, Claus, and Sorensen () no taste buds were found inside the EBO. Particles aggregated within the EBO are deposited onto the pharyngeal jaws.…”

Body condition (Wr) and reproductive potential of bighead and silver carp hybrids: Postzygotic selection in the Mississippi River Basin

“…The gill raker and pharyngeal apparatus of bighead and silver carp is a highly specialized system for filtering and funneling food particles into the pharynx (Hansen, Ghosal, Caprio, Claus, & Sorensen, 2014;Walleser, Howard, Sandheinrich, Gaikowski, & Amberg, 2014;Wilamovski, 1972). Up to 88% of early generation bighead hybrids have deformed gill rakers (Lamer et al, 2010;Marian et al, 1986).…”

Sensory cutaneous papillae in the sea lamprey (Petromyzon marinus L.): I. Neuroanatomy and physiology

“…The SCC distribution is variable from one vertebrate species to the other. In aquatic vertebrates, they are widely distributed on the skin, gills, nasopharynx, or oropharynx (hagfish—Braun, , ; Braun & Northcutt, ; lampreys—Baatrup & Døving, ; Fox et al, ; Whitear & Lane, ; chondrichthyes—Peach, ; Whitear & Moate, ; bony fish—Codina et al, ; Hansen et al, ; Kotrschal, ; Kotrschal et al, , , ; Kuciel et al, ; Peters et al, , ; Silver & Finger, ; see Whitear, for a review). In terrestrial vertebrates, on the other hand, SCCs seem restricted to specific anatomical locations (e.g., the airways) (amphibians—Osculati & Sbarbati, ; Whitear, ; but see also for putative skin SCCs Koyama et al, ; Nagai et al, ; reptiles—Hansen, ; mammals—Finger et al, ; Saunders et al, ; Sbarbati et al, , ; Sbarbati & Osculati, ; Tizzano et al, , ).…”

“…However, it is only with the work of Whitear on the skin of teleost fish that the innervation, and thus sensory nature, of these cells was demonstrated (Lane & Whitear, ; Whitear, , , ). Subsequently, studies have reported putative SCCs on the barbels and nasopharynx of hagfish (Braun, , ; Braun & Northcutt, ), on the skin surface of brook lampreys ( Lampetra planeri Bloch) and river lampreys ( Lampetra fluviatilis L.), including the oral, gill pore, dorsal fin and genital regions (Baatrup & Døving, ; Fox, Lane, & Whitear, ; Whitear & Lane, ), on the skin, gills, and oropharynx of chondrichthyes and bony fish (Codina et al, ; Hansen, Ghosal, Caprio, Claus, & Sorensen, ; Kotrschal, ; Kotrschal, Krautgartner, & Hansen, ; Kotrschal, Peters, & Atema, ; Kotrschal, Whitear, & Adam, ; Kuciel et al, ; Peach, ; Peters, Kotrschal, & Krautgartner, ; Peters, Van Steenderen, & Kotrschal, ; Silver & Finger, ; Whitear & Moate, ). Other studies have described SCCs on the skin and in the oral cavity of amphibians (Koyama, Nagai, Takeuchi, & Hillyard, ; Nagai, Koyama, Von Seckendorff Hoff, & Hillyard, ; Osculati & Sbarbati, ; Whitear, ), and in the airways of reptiles and mammals (Finger et al, ; Hansen, ; Saunders, Christensen, Finger, & Tizzano, ; Sbarbati, Crescimanno, Benati, & Osculati, ; Sbarbati, Crescimanno, Bernardi, & Osculati, ; Sbarbati & Osculati, ; Tizzano et al, ; Tizzano, Merigo, & Sbarbati, ).…”