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

Abstract

Hypophthalmichthys molitrix, silver carp, is an invasive Asian carp that has become increasingly widespread and ecologically destructive within the upper Mississippi River Basin. Its complex trophic anatomy may help explain the apparent efficiency with which they consume phytoplankton, outcompeting native filter feeders. This cypriniform species is characterized by trophic synapomorphies that include a palatal organ, loss of upper pharyngeal jaws, and a hypertrophied lower pharyngeal jaw. However, in silver carp these structures have become greatly modified and diverge from the more basal condition that characterizes species such as goldfish. The trophic apparatus of silver carp is composed of discrete structures that are functionally coupled: filtering plates, paired epibranchial organs (EBO), a modified palatal organ composed of large muscular folds that interdigitate with the filtering plates, and hypertrophied lower pharyngeal jaws and teeth. The filtering plates fill a significant portion of the buccal cavity, especially since the distal parts of these filtering plates make up a key component of the EBOs. EBOs, food aggregating structures found in many teleosts, are thought to have independently evolved at least six times. Ranging in complexity from small slits on the dorsal wall of the pharyngeal cavity to exceedingly intricate spiraling structures, EBOs are morphologically diverse among filter‐feeding fishes. Despite this morphological diversity and broad taxonomic distribution, little is known regarding the functional anatomy of the EBO. Moreover, the EBO in silver carp is distinct from the organs previously described in other species, being created by four independent pharyngeal involutions (instead of the more typical one or two) that form spiral‐shaped pharyngeal tubes surrounded by circumferential muscle. On each side of the head greatly hypertrophied hyomandibulae and opercles are connected to the anterior cartilaginous caps of the bilateral EBOs via enlarged muscles. Given that these fish are pump filter feeders we hypothesize that the opercula may compress and expand the EBOs during pumping causing food to be moved posteriorly toward the pharyngeal jaws.

Developmental ecomorphology of the epibranchial organ of the silver carp, Hypophthalmichthys molitrix

“…This may explain why the organ develops early in ontogeny (<15 mm SL) but is not functional until much later (80 mm SL). We previously proposed (Cohen & Hernandez, 2018b) from the suspensorium, yet still retain its overall shape as stated in our previous studies (Cohen & Hernandez, 2018a,b).…”

“…The trophic apparatus of silver carp is composed of fusedfiltering plates (Cohen & Hernandez, 2018a), bilaterally paired epibranchial organs (EBOs) (Cohen & Hernandez, 2018b; Howes, 1981; Verigin, 1957), a palatal organ (PO), and a greatly modified and hypertrophied pharyngeal jaw (Cohen & Hernandez, 2018b) (Figure 1a,b). During the course of development each of these structures becomes functionally coupled, playing an integral role in foraging success.…”

“…Silver carp possess the most anatomically complex EBO yet described (Bertmar et al ., 1969; Boulenger, 1901; Cohen & Hernandez, 2018b; Fang, 1928; Howes, 1981; Miller, 1969). Their EBOs are bilaterally paired and supported by modified epibranchials (EB) and infrapharyngeobranchials (IPB) from branchial arches I–IV (Figure 1a–c).…”

“…The filtering plates are composed of fused, individual rakers and begin at the rostral end of the ceratobranchial (CB; Figure 1b) and continue onto the end of the EB. Near the entry of the EBO the filtering plates become detached from the base of the EB and wind through the muscular tubes of the EBO (Figure 1b,d); at this point they are no longer referred to as filtering plates, but instead as gill raker sets to delineate their new function inside the EBO (Cohen & Hernandez, 2018a,b). The gill raker sets terminate in a mucus‐rich sac deep within the body of the EBO.…”

“…Silver carp possess the most anatomically complex EBO yet described (Bertmar et al, 1969;Boulenger, 1901;Cohen & Hernandez, 2018b;Fang, 1928;Howes, 1981;Miller, 1969). Their The gill raker sets terminate in a mucus-rich sac deep within the body of the EBO.…”