Functional Morphology of the Feeding Apparatus in Simenchelys parasitica (Simenchelyinae: Synaphobranchidae), an Alleged Parasitic Eel
The Pugnose Eel, Simenchelys parasitica (family Synaphobranchidae, subfamily Simenchelyinae), is a deep-water species described as both being a parasite and a scavenger that can bite off large chunks of flesh. Little, however, is known about its cranial morphology, including to what degree its feeding apparatus is modified to allow feeding specializations. We provide a detailed description of the cranial morphology of S. parasitica, comparing it with that of more closely related synaphobranchid species, for which no parasitic behavior has been reported, i.e., Ilyophis brunneus (Ilyophinae) and Synaphobranchus brevidorsalis (Synaphobranchinae). Pugnose Eels have stretchable skin around a small, terminal mouth, as well as teeth with a clear cutting edge, a mouth-closing apparatus equipped with large jaw muscles, a large tongue-like secretory structure, and well-developed hyoid and branchial arches to facilitate the transport of large food items in the buccal cavity. A comparison with other species provides several lines of evidence supporting the hypothesis that Pugnose Eels have a feeding apparatus that is equipped for biting off chunks of flesh from prey (irrespective of whether prey is dead or alive), most likely by using rotational feeding.
Neurocranium of Simenchelys parasitica. (A) Dorsal view and (B) ventral view. af susp A, anterior suspensorial articulation facet; af susp P, posterior suspensorial articulation facet; fr-Olf, foramen olfactorius; fr-Tri.fac, foramen trigemino-facialis; o-BOc, basioccipital; o-BSph, basisphenoid; o-Epi, epioccipital; o-ExOc, exoccipital; o-F, frontal; o-Par, parietal; o-Et, ethmoidal complex; o-Pro, prootic; o-PSph, parasphenoid; o-Pt, pterotic; o-PtSph, pterosphenoid; o-SOc, supraoccipital; o-Sph, sphenotic; o-V, vomer.
Cranial skeleton of Simenchelys parasitica (lateral view). (A) Complete skull except the circumorbital bones (right side), (B) suspensorium (right side), and (C) position of the skull in the head. ac Op, opercular articular condyle; ac susp A, anterior suspensorial condyle; ac susp P, posterior suspensorial condyle; a.l.d.Mx, anterolateral depression of maxilla; d m-Et, distance between anterior tip of mouth and ethmoidal complex (soft tissue); l-CH-Ang, ceratohyalo-angular ligament; l-Iop-Ang, interoperculo-angular ligament; l-Op-IOp, operculo-interopercular ligament; l-prim, primordial ligament; o-BSph, basisphenoid; o-D, dentary complex; o-Epi, epioccipital; o-Et, ethmoidal complex; o-F, frontal; o-Hm, hyomandibula; o-IOp, interopercle; o-Mx, maxillary bone; o-Nas, nasal; o-Op, opercle; o-Par, parietal; o-Pg, ectopterygoid; o-POp, preopercle; o-Pt, pterotic; o-PtSph, pterosphenoid; o-Q, quadrate; o-SOc, supraoccipital; o-SOp, subopercle; o-Sph, sphenotic; o-V, vomer; Orb, orbit; Pr Hm, hyomandibular lateral process.
3D reconstruction of the skull, illustrating the cranial lateral line system of Simenchelys parasitica. (A) Position of the canals in relation to the skull (right side, lateral view), and (B) lateral view of the nasal bone, preorbital bone, infraorbital bone, and first postorbital bone (right side). c IO, infraorbital canal; c POM, preopercular mandibular canal; c SO, supraorbital canal; c T, temporal canal; Cm F, frontal commissure; cm ST, supratemporal commissure; o-InfOrb, infraorbital; o-D, dentary complex; o-F, frontal; o-Hm, hyomandibula; o-Nas, nasal; o-Op, opercle; o-PoOrb, postorbital; o-POp, preopercle; o-POrb, preorbital.
Jaws of Simenchelys parasitica (right side). (A) Lower jaw; medial view, and (B) maxilla; medial view. af Md, mandibular articulation facet; af Mx-Et, maxillo-ethmoidal articular facet; l-CH-Ang, ceratohyalo-angular ligament; l-IOp-Ang, interoperculo-angular ligament; o-Ang, angular complex; o-cMec, coronomeckelian; o-D, dentary complex; o-Mx, maxillary bone; o-ra, retroarticular; Pr Cor, coronoid process.
(A) Cross section of the head and mucosal histology of Simenchelys parasitica: (A) overview section at the level of the anterior part of the lower jaw; (B) overview section at the level of the anterior part of the ventral oral valve; (C) detail of the mucosal tissue with multiple goblet cells at the base of the ventral oral valve (scale bar 100 μm); (D) multilayered epithelial mucosa of buccal cavity roof in the same region as C (scale bar 50 μm); (E) detail of mucosal tissue in the roof of the buccal cavity, at the level of the vomeral bone, showing localized epithelial proliferation with goblet cells (scale bar 200 μm); and (F) detail of the buccal mucosa in the posterior region of the buccal cavity floor, showing epithelial cells producing large mucus vacuoles (scale bar 50 μm). (C and D come from different sections than that in image B, but for clarity their position is indicated in B with the corresponding, labeled arrows.) c POM, preopercular mandibular canal; l-IOp-Ang, interoperculo-angular ligament; m-A2α, ventral subsection of A2; m-A2β, dorsal subsection of A2; m-A3, A3 section of the adductor mandibulae muscle complex; m-AAP, adductor arcus palatini muscle; m-HH inf, hyohyoideus inferioris muscle; m-LAPa, anterior subsection of levator arcus palatini muscle; m-PH, protractor hyoidei muscle; m-SH, sternohyoideus muscle; m-SPH, pharyngocleithralis muscle; o-D, dentary complex; t-A2β, tendon of A2β.
Opercular series and hyoid apparatus of Simenchelys parasitica: (A) Opercular series; lateral view (right side), and (B) hyoid apparatus; ventral and dorsal views of the dorsal hypohyal, ventral hypohyal, anterior ceratohyal and posterior ceratohyal bones, ventral and dorsal views of urohyal, and dorsal view of basihyal. af Hhy, hypohyal articular facet; af Op, opercular articular facet; ac Hhy, hypohyal articular condyle; l-CH-Ang, ceratohyalo-angular ligament; o-BH, basihyal; o-CH A, anterior ceratohyal bone; o-CH P, posterior ceratohyal bone; o-Hhy D, dorsal hypohyal bone; o-Hhy V, ventral hypohyal bone; o-IOp, interopercle; o-Op, opercle; o-POp, preopercle; o-SOp, subopercle; o-UH, urohyal; Pop W, preopercular wing; Pr UH, urohyal process.
Gill arches of Simenchelys parasitica. (A) Dorsal view of the ventral part and the ventral view of the dorsal part of the gill arch, and (B) gill arch muscles. m-APTp, pharyngeal tooth plate adductor muscle; m-Le, levator externus muscle; m-Li, levator internus muscle; m-PHC, pharyngocleithralis muscle; m-SPH, subpharyngealis muscle; m-Trans.v, transversus ventralis muscle; o-Bb, basibranchial bone; o-Cb, ceratobranchial bone; o-Eb, epibranchial bone; o-Hb, hypobranchial bone; o-Ib, infrapharyngobranchial bone; o-LP, lower pharyngeal tooth plates; o-UP, upper pharyngeal tooth plates.
The cranial muscles of Simenchelys parasitica. (A) Skin removed (lateral view), (B) sections A2 except for the medial fibers of subsection A2α, hyohyoideus muscle, hyohyoideus inferioris muscle, epaxial muscles, hypaxial muscles, ventral muscles of the head, and primordial ligament are removed (lateral view), (C) subsection A2α, section A3, lateral fibers of the levator arcus palatini muscle and levator operculi muscle are removed (lateral view), and (D) ventral muscles of head (sagittal left cut), hyohyoideus muscle is removed. l-Iop-Ang, interoperculo-angular ligament; l-prim, primordial ligament; m-A2α, ventral subsection of A2; m-A2β, dorsal subsection of A2; m-A2αm, medial fibers of vental subsection of A2; m-A3, A3 section of the adductor mandibulae muscle complex; m-AAP, adductor arcus palatini muscle; m-AO, adductor operculi muscle; m-DO, dilatator operculi muscle; m-Epax, epaxial muscles; m-HH inf, hyohyoideus inferioris muscle; m-HH sup, hyohyoideus superior muscle; m-LAPa, anterior subsection of levator arcus palatini muscle; m-LAPp, posterior subsection of levator arcus palatini muscle; m-LO, levator operculi muscle; m-PH, protractor hyoidei muscle; m-PHC, pharyngocleithralis muscle; m-SH, sternohyoideus muscle; m-SPH, subpharyngealis muscle; m-Trans.v, transversus ventralis muscle; o-Cb, ceratobranchial bone; o-CH A, anterior ceratohyal bone; o-Cl, cleithrum bone; o-D, dentary complex; o-Et, ethmoidal complex; o-F, frontal bone; o-Hb, hypobranchial bone; o-Hhy V, ventral hypohyal bone; o-Mx, maxillary bone; o-Op, opercle; o-Par, parietal bone; o-Pg, ectopterygoid bone; o-POp, preopercle; o-SOp, subopercle; t-A2β, tendon of A2β; t-DO, tendon of dilatator operculi muscle; t-LAPa, tendon of anterior subsection of levator arcus palatini; t-LAPp, tendon of posterior subsection of levator arcus palatini; t-LO, tendon of levator operculi.
The cranial muscles of Ilyophis brunneus. (A) Skin removed (lateral view); (B) sections A2, hyohyoideus muscle, lateral fibers of the levator/adductor operculi muscle, epaxial muscles, hypaxial muscles, maxillary bone, branchiostegal rays, and primordial ligament are removed (lateral view); (C) ventral view of the right side of the cranial muscles (Skin is removed and subpharyngealis muscle is cut). l-Iop-Ang, interoperculo-angular ligament; l-CH-Ang, cratohyalo-angular ligament; l-prim, primordial ligament; l-Mx-Et, maxillo-ethmoidal ligament; l-UH-BH, urohyalo-basihyal ligament; m-A2α, ventral subsection of A2; m-A2β, dorsal subsection of A2; m-A3, A3 section of the adductor mandibulae muscle complex; m-DO, dilatator operculi muscle; m-Epax, epaxial muscles; m-HH, hyohyoideus muscle complex; m-LAP, levator arcus palatini muscle; m-L/AOl, lateral fibers of levator/adductor operculi muscle; m-L/AOm, medial fibers of levator/adductor operculi muscle; m-PH, protractor hyoidei muscle; m-SH, sternohyoideus muscle; m-SPH, subpharyngealis muscle; o-CH A, anterior ceratohyal bone; o-Cl, cleithrum bone; o-D, dentary complex; o-F, frontal bone; o-IOp, interopercle; o-Mx, maxillary bone; o-Op, opercle; o-POp, preopercle; o-SOp, subopercle; o-UH, urohyal bone; t-A2β, tendon of A2β; t.a-PH, anterior tendon of protractor hyoidei muscle; t.p-PH, posterior tendon of protractor hyoidei muscle; t-SH, tendon of sternohyoideus muscle.
The cranial muscles of Synaphobranchus brevidorsalis. (A) Skin removed (lateral view), (B) sections A2, hyohyoideus muscle, levator operculi muscle, epaxial muscles, hypaxial muscles, maxillary bone, and primordial ligament are removed (lateral view), and (C) ventral muscles of head; left lower jaw, anterior and posterior ceratohyal, and left muscle bundle of the protractor hyoidei (m-PH), and sternohyoideus (m-SH) are removed. l-IOp-Ang, interoperculo-angular ligament; l-prim, primordial ligament; l-Pg-Q, pterygoideo-quadrate ligament; m-AAP, adductor arcus palatini; m-A2α, ventral subsection of A2; m-A2β, dorsal subsection of A2; m-A3, A3 section of the adductor mandibulae muscle complex; m-DO, dilatator operculi muscle; m-Epax, epaxial muscles; m-HH, hyohyoideus muscle complex; m-LAP, levator arcus palatini muscle; m-AO, adductor operculi muscle; m-LO, levator operculi muscle; m-PH.l, lateral fibers of protractor hyoidei muscle; m-PHC, pharyngocleithralis; m-SH, sternohyoideus muscle; o-BH, basihyal; o-CH A, anterior ceratohyal bone; o-Cl, cleithrum bone; o-D, dentary complex; o-Et, ethmoidal complex; o-F, frontal bone; o-Hhy, hypohyal bone; o-IOp, interopercle; o-Mx, maxillary bone; o-Op, opercle; o-Pg, ectopterygoid bone; o-SOp, subopercle; o-UH, urohyal bone; t-DO, tendon of dilatator operculi muscle; t-SH, tendon of sternohyoideus muscle.
Contributor Notes
Associate Editor: D. Buth.