Muraeninae, Rafinesque, 1815

Johnson, G. David, 2019, Revisions of Anatomical Descriptions of the Pharyngeal Jaw Apparatus in Moray Eels of the Family Muraenidae (Teleostei: Anguilliformes), Copeia 107 (2), pp. 341-357 : 352-353

Muraeninae

‘‘The attachment of the levator externus 4 at a posterior (distal) location on the fourth epibranchial facilitates the extreme jaw protraction distance observed in morays. Contraction of the levator externus 4 pulls the posterior portion of the epibranchial toward its origin on the neurocranium’’ (M&W: 614) ‘‘The upper pharyngobranchial and fourth epibranchial are protracted anterior to the origin of the levator externus 4, resulting in the pharyngeal jaws protruding into the oral cavity.’’ (M&W: 613, legend of fig. 9).

Because the muscle identified as LE4 is actually a posterior branch of LI2 and inserts on UPT rather than a posterior location on Eb4, protraction of the upper pharyngeal elements into the oral cavity is not facilitated by a direct pull on the posterior end of EB4 ( Neomuraena is exceptional). According to figures 1b and 4b and the supplemental videos of Mehta and Wainwright (2007a) and 7c of M&W, UPT is protruded forward to a point where its anterior half is directly below the orbit. Because the internal levators originate well posterior to the orbit and insert on UPT rather than the much more posterior end of Eb4 ( Figs. 1 , 7 ), their contraction can hardly explain such an extreme anterior extension of UPT. When UPT is positioned below the orbit, the insertions of both internal levators will necessarily be well forward of their point of origin on the braincase (see Mehta and Wainwright, 2007a: fig. 4b). The extreme anterior extension of UPT in muraenines is clearly documented in the videos, but the explanation for exactly how this is accomplished given by M&W should be reevaluated.

‘‘As the upper pharyngobranchial is protracted further into the oral cavity, contraction of the fourth levator internus and obliquus dorsalis dorsally rotate the upper pharyngobranchial at the Pb4/Eb4 joint.’’ (M&W: 613) ‘‘ Contraction of the levator internus 4 positions the recurved teeth in an open orientation for ensnaring prey.’’ (M&W: 614)

The muscle inserting on UPT that M&W called LI4 is instead the anterior branch of LI2. The inappropriate terminology does not affect the mechanics; however, there are actually two sections of LI2, one inserting anterodorsally and one posterodorsally on UPT. Accordingly, any rotation of UPT by the two muscles is probably more complex than described by M&W. It would seem that the anterior branch would rotate UPT upward, whereas the posterior branch would rotate it downward. As for the obliquus dorsalis, it does not exist, so could have no role in rotating UPT.

‘‘In muraenines, there is a very elongate bundle of muscle fibers that runs from the posterior part of the fourth epibranchial to the ventral side of the vertebral column and attaches onto the 10th and 14th vertebrae. We call this muscle the dorsal retractor.’’ (M&W: 610) ‘‘Contraction of the dorsal retractor retracts the upper pharyngeal jaw....’’ (M&W: 613)

The dorsal retractor actually inserts on UPT and thus retracts UPT by pulling backward on that element rather than Eb4. If DR inserted on Eb4 to retract UPT (the prey capture implement), the connection between those two elements would need to be very firm to prevent their separation during retraction. In the scenario of M&W, the UPT/Eb4 connection would be reinforced by the obliquus dorsalis 4, but there is no OD4. I was initially puzzled by this, because the only other reference to the UPT/EB4 joint is to its flexibility, and their figure 4B, C (reproduced here in Fig. 11B, C ) shows no connective tissue reinforcing it. Nonetheless, I accept that the movements described by M&W do occur. As shown in Figure 11E, F , there is indeed a strong connective tissue (ligamentous) bond between these two elements, this tissue apparently having been scraped off in M&W’s figure and not discussed by them.

‘‘The rectus communis, which connects the hyoid arch to the anteroventral margin of the fourth ceratobranchials, protracts the lower pharyngeal jaw.’’ (M&W: 614) ‘‘Contraction of the rectus communis produces a bulge in the ventral side of the skull directly posterior to the position of the hyoid.’’ (M&W: 612)

My observations agree with those of Nelson (348, table 1) that there is no rectus communis in muraenines. This is not surprising, as there are no hypobranchials, on which they typically insert. I surmise (as did Nelson: 363) that the muscle mass responsible for retracting the lower pharyngeal jaws consists of subdivisions of the subpharyngealis (particularly the larger one of the fourth arch), which originate on the posterior ends of ceratobranchials and terminate on the anterior and posterior ceratohyals (the ‘‘hyoid’’ or ‘‘hyoid arch’’ of Nelson and M&W). These muscles lie dorsal to the skeletal elements of the ventral arches (including the LPT), and the bulge in the ventral side of the skull described by M&W could presumably be produced by ventral depression of the anterior tip of LPT as the lower ceratobranchials are pulled forward from their posterior portions. Such a bulge would not result if the main protractive force originated at the tip of LPT.

Although I agree that this muscle plays an important role in protraction of the LPT, this would require that a substantial force be applied against the very thin ceratohyal, about which Mehta and Wainwright (2007b: 501) said, ‘‘the slender hyoid bar does not seem able to withstand the forces necessary to depress the ventral region of the buccal cavity....’’. I am not suggesting that an equivalent force is required to protract the pharyngeal jaws, but wonder why M&W did not refer to this potential conundrum. The role of this very slender ceratohyal in protraction of the pharyngeal jaws is discussed further in Functional Summary.

Also missing from M&W’s (612–613) Functional Interpretation is the action of the prominent, sling-like LI1 that originates in the epaxialis directly above UPT and inserts on the anterior portion of its dorsal surface midway along its length. This muscle, not seen or described by M&W, is unique among teleosts to several eel families. It undoubtedly plays a role in the mechanics of pharyngeal jaw movements in muraenid eels, and without it the scenario is incomplete. Because its resting position is directly above UPT, speculation on its role in protraction/retraction is challenging. One thing seems clear—it could not play the usual protractive role of an internal levator. Does it assist in widening the pharyngeal gape, retracting UPT, both, or have some other function?

Figures

Fig. 1. (A) Gymnothorax buroensis, USNM 141541, 170 mm, left lateral view of head of cleared and stained specimen showing posterior position of gill arches. (B) Muraena lentiginosa, USNM 318298, 210 mm, left lateral view of gill arches in situ, showing external levators and first internal levator; second internal levator occluded. Cb, ceratobranchial; Eb, epibranchial; Ep, epaxialis; LE, levator externus; LI, levator internus; Sh, sternohyoideus.

Fig. 7. Muraena argus, USNM 318316, 250 mm. Left lateral view, gill arches in situ. (A) Entire gill arches exposed, sternohyoideus intact. (B) Close up of A. (C) First three arches and sternohyoideus removed, pharyngocleithralis exposed. Note absence of well-defined muscle bundle from anterior tip of LPT to hyoid and presence of fan-like subpharyngealis (Sph). Aa, anguloarticular; AD, adductor dorsalis; Cb, ceratobranchial; Ch, anterior and posterior ceratohyal; Cl, cleithrum; De, dentary; DP, dorsal process of UPT; Eb, epibranchial; Ep, epaxialis; LI, levator internus; LPT, lower pharyngeal toothplate; Mx, maxilla; Pcl, pharyngocleithralis; Sh, sternohyoideus; SO/DR, sphincter oesophagi/dorsal retractor; Sph, subpharyngealis; UPT, upper pharyngeal toothplate. Red star marks origin of LI1 within epaxialis.

Fig. 11. Photographs of left medial view of alizarin-stained bone showing association between UPT and EB4. (A–D) Muraena retifera, with muscles and connective tissue removed, from figure 4 of Mehta and Wainwright (2008). (C, D) Muscles drawn in—modified, red boxes indicate misidentification of obliquus dorsalis—there is no major muscle spanning the joint between Eb4 and UPT. Given the angle and point of insertion, the element labeled LI1 is probably LI1, a muscle otherwise not recognized, illustrated, or discussed by M&W. (E, F) Gymnothorax pindae, USNM 443783, 200 mm, arrows point to the strong connective tissue that binds the two elements together. LI, levator internus; OBL.D, obliquus dorsalis.