Uropterygiinae, Fowler, 1925

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 : 353-354

Uropterygiinae

‘‘There is no dorsal retractor that spans the posterior portion of the epibranchial and the vertebral column, suggesting that retraction of the jaws is accomplished primarily by the esophagus and the pharyngocleitheralis [sic].’’ (M&W: 614)

As described by Nelson, all eels have a dorsal retractor, but only in muraenines does it attach posteriorly to the vertebral column. This anchoring of DR posteriorly undoubtedly strengthens the retraction force of this muscle, and this makes sense for muraenines, given the exceptional protraction and retraction kinematics described by M&W. Because non-muraenid eels are not known to move the pharyngeal jaws in this extreme fashion, the lack of attachment of DR to the vertebral column seems reasonable. As M&W noted (614), both the esophagus and the pharyngocleithralis are involved in pharyngeal-jaw retraction, but it seems that the longitudinal fibers of the sphincter oesophagi would not be as effective in extensive retraction of the UPT in uropterygiines as they are in muraenines without being anchored to the vertebral column. However, in uropterygiines retraction is further facilitated by the presence of an additional retractor (my hypaxial retractor, HR), not previously described, which, because of its more ventral position and insertion on the posterior end of Eb4, might function to retract the upper pharyngeal toothplate in a somewhat more ventral direction than the dorsal retractor of muraenines. In that case it would seem that it might tend to open the gape of the pharyngeal jaws wider at a time when it should be closing. It will be interesting to see what detailed functional analyses can tell us about the two quite different retraction mechanisms in muraenines and uropterygiines.

As for protraction, the insertion of an LE4 on the posterior end of Eb4 suggests that UPT could extend even farther into the oral cavity than in muraenines. Unfortunately, Mehta and Wainwright never had access to live uropterygiines to watch them feed. The same would seem to apply to Neomuraena , and perhaps future studies can address protraction in these taxa.

Functional summary

Contrary to M&W, I suggest that there are three distinct mechanisms of protraction and retraction of the upper pharyngeal jaws involving dorsal gill-arch muscles in Muraenidae (the role of LI 1 in all three remains unclear):

Muraeninae (except Neomuraena ): Protraction is achieved by contraction of the two sections of LI2, which originate on the occipito/otic region of the braincase and insert on the anterior and posterior ends of UPT, although this cannot fully explain its extreme protraction to a point ventral to the orbit documented by M&W. Retraction is achieved by contraction of the dorsal retractor, which originates on the vertebral column and inserts on UPT. Rhinomuraena is exceptional in that the dorsal retractor does not originate on the vertebral column.

Neomuraena : Protraction is achieved by contraction of LI2 and LE4, both of which originate on the occipito/otic region of the braincase. The former inserts on the anterior end of UPT, and the latter inserts on the posterior end of Eb4. Retraction is achieved as in Muraeninae . This anatomical distinction warrants consideration of elevation of the subgenus Neomuraena ( Girard, 1859) to generic status. It is otherwise diagnosed by having three vs. four infraorbitals and comprises four species restricted to the western Atlantic ( Böhlke et al., 1989).

Uropterygiinae : Protraction is achieved by contraction of LI2 and LE4 as in Neomuraena . Unlike muraenines, the dorsal retractor has no attachment to the vertebral column, but its effectiveness in retraction is augmented by contraction of the hypaxial retractor (HR), which originates in the hypaxialis and inserts on the posterior end of Eb4.

Sternohyoideus

As documented and discussed by M&W, ventral flexion of the neurocranium in muraenids is an integral part of pharyngeal protraction. Their figure 7, based on videos, clearly shows that this occurs in the protraction phase. It is also obvious that there is considerable contraction along the horizontal axis (compare the position of the opercular opening in fig. 7A, D with the protraction phases, B–D). Exactly how this is accomplished is not entirely clear, but I suggest that it must involve the epaxialis, hypaxialis, and sternohyoideus. In their paper on biting in morays, Mehta and Wainwright (2007b: 500–501) found that feeding morays rely on directly biting prey rather than capturing it with suction, noting that the cleithrum and hyoid arch (by which they meant ceratohyal) are thin and flexible and that the latter does not seem strong enough to withstand strong forces such as that necessary to depress the ventral region of the oral cavity. Despite the obvious weakness of the ceratohyal, M&W proposed that it can withstand a force strong enough to protract the lower pharyngeal jaws, and I agree, though the muscle involved is the subpharyngealis, not the rectus communis. They also stated (498) that ‘‘The sternohyoideus is small compared to other teleosts and the fibers appear continuous with the hypaxialis.’’ The primary subject of their comparison was Anguilla , but they provided no quantification of the sternohyoideus mass, nor any comparative illustrations. Eagderi (2010) illustrated the sternohyoideus of several eels, including Anguilla and two muraenids, Gymnothorax (fig. 6.13c) and Anarchias (fig. 6.16c). Comparison of that of Anguilla (fig. 4.9d) with that of the two morays shows that the sternohyoideus is deeper posteriorly in the former, but also substantially shorter. It is undoubtedly more robust in Anguilla than in muraenids, but there are two additional notable differences.

First, as noted by Mehta and Wainwright (2007b: 498), unlike Anguilla and other eels, the muraenid sternohyoideus is essentially an extension of the hypaxialis and has little or no attachment to the extremely thin cleithrum. A more striking and undoubtedly functionally significant morphological difference is the absence of the urohyal, its normal site of attachment, in muraenids. The urohyal is not strictly part of the hyoid arch but an unpaired sesamoid ossification of the anterior tendon of the sternohyoideus ( Arratia and Schultze, 1990). In most teleosts, it attaches by two short ligaments to the ventral hypohyals. Because eels lack hypohyals, the sternohyoideus attaches to the anterior tip of the anterior ceratohyals. Accordingly, contraction of the sternohyoideus generates a median posteroventral pull on the ceratohyals where they attach to the ventral gill arches, which are then also pulled in that direction. Absence of the urohyal in morays was not mentioned by Mehta and Wainwright (2007b), and their figure 1 confusingly labels both the urohyal in Anguilla and the anterior ceratohyals in the two morays ‘‘UH,’’ presumably urohyal, though the abbreviation of that given in the legend is ‘‘U.’’ Absence of the urohyal is, in fact, a unique apomorphy of muraenid eels, and would seem to be a critical feature in their feeding mechanics not considered by Mehta and Wainwright (2007b) or M&W. Unlike other eels, in the absence of the urohyal, the sternohyoideus inserts along the length of each ceratohyal ( Fig. 7A, B ; Eagderi, 2010: figs. 6.13c, 6.16c), and because the median elements of the ventral arches are absent those bones have no median point of attachment. Thus the effect of contraction of the sternohyoideus must be quite different. This muscle is often continuous posteriorly with the hypaxialis (Winterbottom, e.g., Elops , fig. 27), and its more extensive origin there in morays would not necessarily weaken its ability to retract the anteroventral elements of the head. However, its insertion on the reduced and free ceratohyals would certainly affect the way in which it does this compared to other eels. Documentation of horizontal contraction of this region by M&W is irrefutable, but further investigation is needed to identify the precise mechanics involved. Because contraction of the internal levators cannot alone explain the extreme protrusion of UPT (particularly in muraenines), understanding the role of the sternohyoideus (and subpharyngealis) is paramount.

Figures

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.