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 : 346-351

MURAENINAE

Gill-arch skeleton Figures 1–4

Fourth pharyngobranchial (Pb4).—

‘‘The most anterior portion of the fourth epibranchial is connected to the center of a well-developed fourth pharyngobranchial bone, which is endowed with two rows of 14–16 sharply recurved teeth.’’ (M&W: 606)

The distinction between the fourth pharyngobranchial and the fourth upper pharyngeal toothplate was clarified by Nelson (1968: 489–491), and as shown by Nelson (1966), there is no fourth pharyngobranchial (a cartilaginous element) in anguilliform eels. The precise composition of the toothed element in muraenids is difficult to determine without ontogenetic evidence (currently not available for muraenids) but most likely includes elements of the second and third pharyngobranchials and associated toothplate and possibly the fourth upper pharyngeal toothplate. Fusion of adjacent pharyngobranchial elements is not common but has been demonstrated in some stomiiform fishes ( Schnell and Johnson, 2012). Nelson referred to it as UP3-4, noting ( Nelson, 1966: table 1) that the two elements were ‘‘probably fused.’’ Given the uncertainty without ontogeny, I refer to it as the upper pharyngeal toothplate (UPT). As described by M&W, the anterior end of Eb4 articulates with the medial surface of a dorsal flange at about the mid-length of UPT. Posteroventrally, Eb4 articulates with the posterodorsal end of Cb4.

Extrinsic gill-arch muscles

Internal levators.— ( Figs. 3–5 )

‘‘In muraenines, four external levators are present (1–4)’’ and ‘‘have their sites of insertion on the dorsal surface of the corresponding epibranchials (1–4). The external levators converge to form a single bundle of muscle fibers just below the origination site on the parasphenoid.’’ (M&W: 610)

‘‘Levator externus 4, the longest, runs dorsally along the epibranchial bone and inserts on the posterior portion of the dorsal side of the fourth epibranchial.’’ (M&W: 609– 610)

Whereas the first three external levators insert as described by M&W, none of them originate on the parasphenoid (but rather on the occipito/otic region of the cranium; also see Eagderi, 2010), and the putative fourth (considered here to be the posterior subdivision of LI2) has no association with the fourth epibranchial and inserts instead on the dorsal surface of the posterior portion of the upper pharyngeal toothplate. As noted above in Results, the four species of the subgenus Neomuraena (not examined by M&W) are exceptional in having an LE4 and an undivided LI2. According to M&W (table 1), LE4 is the muscle that Nelson called protractor posterior, and they stated, ‘‘The levator externus 4 is an important dorsal protractor. We presume that elongation of the levator externus 4 resulted in the synonym protractor posterior ( Nelson, 1967).’’ However, Nelson (table 2, fig. 11) reported that the posterior protractor (his PP) is absent in muraenines. Nelson reported PP to be present only in uropterygiines, though I see no reason not to call that muscle in uropterygiines LE4 ( Fig. 8A, B ), which is also present in other non-muraenine eels (e.g., see Springer and Johnson, 2015). Nelson did report and illustrate a second internal levator (LI2, not mentioned by M&W), that would be the correct identity of the muscle labeled external levator 4 by M&W, given its insertion on UPT. As discussed above (see levator internus 2 in Results), I consider this the posterior subdivision of LI2 (see Figs. 2–5 ).

‘‘There is a single internal branchial levator, levator internus 4, that originates from the posterior part of the parasphenoid just behind the bundle of levator externi and inserts on the dorsal side of the fourth pharyngobranchial just anterior to the Pb4/Eb4 joint.’’ (M&W: 610, shown correctly inserting on UPT in their fig. 4, mistakenly labeled there as LI1 but described in the legend as LI4, where it is said to insert on Eb4).

There is no fourth internal levator in any actinopterygian, and there is no reason that the muscle identified as LI4 by M&W should not be considered equivalent to Nelson’s internal levator 2, given its insertion on UPT. Muraenines are unique among eels in having three separate muscle bundles inserting on UPT (LI1 and two sections of LI2), identified by Nelson as internal levators 1 and 2 and the protractor medialis. Muraenids have no separate Pb2, the normal insertion site of LI1, but because one of these muscles is broad and strap-like and originates in the epaxial musculature, it is readily identifiable as LI1 (see Internal levators section in Results). M&W did not report, and therefore I presume that they did not see, the prominent strap-like LI1 and instead identified the two sections of LI2 as LI4 and LE4 (LI1 appears only once in M&W, in their fig. 4, where, as mentioned above, it appears that it was mislabeled). Moreover, LI2 originates on the occipito/otic region of the braincase (see also Eagderi, 2010: 103) and not on the parasphenoid as they indicated. M&W identified the anterior branch of LI2 as the ‘‘fourth internal levator’’ concluding that it is the muscle that Nelson called ‘‘protractor medialis.’’ Because actinopterygians have no fourth internal levator (see S&J and Springer and Johnson, 2015), there is no justification for that surmise. Consequently, that muscle should be considered equivalent to Nelson’s internal levator 2, given its insertion on UPT. Nelson (358, fig. 11) described four muscles inserting on UPT. As discussed below, I was unable to find one of these, his protractor lateralis (LP). Of the remaining three, one is LI1, and he identified one of the other two as levator internus 2 (LI2) and called the other protractor medialis (his MP) with no explanation. His LI2 inserts on UPT posteriorly and his MP inserts on UPT anteriorly. Because these muscle bundles are continuous at their origin together with the external levators of the occipito/otic region of the braincase, it is most parsimonious to interpret them as subdivisions of the second internal levator (LI2), and I am unable to explain why Nelson chose to call the anterior one protractor medialis. This posterior division inserts on the dorsolateral side of the posterior end of UPT and the anterior one on the dorsomedial side of its anterior end ( Figs. 2C , 3A , 4 ). For other instances of subdivided internal levators see S&J (46, 58, pls. 46, 49) and Stiassny (1996: 407, fig. 1).

The unusual origin of LI 1 in the epaxialis deserves further attention. I have confirmed this origin of LI1 to be as Nelson (349) described for Conger in anguillids, muraenids, ophichthids and chlopsids. Among the other anguilliform families I have examined, I found that it exhibits the primitive state (origin on the braincase) in protanguillids and synaphobranchids. Previous studies (e.g., Johnson et al., 2012; Tang and Fielitz, 2013) placed those two families as sequential sister taxa to all remaining anguilliforms. Pending investigation of the origin of LI 1 in all eel families, I propose that the distribution of its unique origin from the epaxialis should be further investigated as a potential morphological synapomorphy for a yet-to-be-determined clade of derived eels, one that excludes at least Protanguilla and the synaphobranchids.

Summarizing, M&W did not refer to the two traditionally known muscles that Nelson illustrated and labeled as LI1 and LI2. Nelson (table 2, fig. 11) listed and illustrated in muraenines ( Gymnothorax ) four ‘‘protractor’’ muscles, two internal levators, a protractor medialis, and a ‘‘protractor lateralis.’’ As discussed above, there are only two dorsal ‘‘protractor’’ muscles—LI1 originating in the epaxialis and LI2 consisting of two sections with a common origin on the braincase. The fourth muscle, the ‘‘protractor lateralis’’ (LP) Nelson (358) described as ‘‘extending between UP3-4 and the ventral part of the hyoid arch (attaching there in common with the ventral muscles LA1 (adductor lateralis 1), OAl-2 (attractores obliqui),’’ the latter of which Nelson recognized as subdivisions of the subpharyngealis, a sheet of longitudinal fibers dorsal to the ventral arch elements. I was unable to locate Nelson’s protractor lateralis or understand it from his illustration. Winterbottom also appears to have been confused by it, listing the muscle as questionably a synonym of an internal levator. This is the only fundamental point about muraenines in which I disagree with Nelson—the difference in my UPT and his UPT3-4 is not significant, as I agree that there could have been fusion of the two elements. As for his protractor medialis, I used a parsimony argument to postulate that it is most likely to be a subdivision of LI2, thus there is no need to give it a separate name. Nelson apparently did not see the hypaxial retractor in uropterygiines (see below). I agree with his descriptions of LE4 and LI2 there, but again, I cannot explain why he decided to rename them as protractor posterior and protractor medialis, respectively.

Dorsal retractor (DR).— ( Figs. 2–6 )

‘‘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)

According to M&W, this is the muscle that Nelson called lateral retractor. However, Nelson made no mention of a lateral retractor, and, in fact, he also called this muscle dorsal retractor (his table 2 and fig. 11) and accurately described it as inserting on UPT (his UP3-4). Contrary to M&W, the dorsal retractor in muraenines completely bypasses the fourth epibranchial to insert on the upper pharyngeal toothplate, as does the retractor dorsalis in neoteleosts. M&W (see above) apparently misidentified the anterior portion of the dorsal retractor as the obliquus dorsalis (OD4/OBL.DIV). Their (fig. 1) diagrammatic depiction of the dorsal retractor as fully exposed and separate from the sphincter oesophagi, as is the retractor dorsalis of neoteleosts, is inaccurate; DR only emerges from the sphincter oesophagi directly below its attachment to the vertebral column ( Fig. 6 ). It is more accurately depicted in the diagrammatic sequence in their figure 9, except that in A of that figure it is not attached to the vertebral column.

Subpharyngealis (Sph).— ( Figs. 2C , 7 )

‘‘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)

The rectus communis is an intrinsic muscle of the ventral gill arches. It lies ventral to the ventral gill-arch elements and has no association with the ceratohyal (the ‘‘hyoid’’ of M&W and Nelson). As described by Nelson and S&J, when present in eels it extends from the proximal end of Cb4 to one or more hypobranchials. I concur with Nelson ( Table 1) that there is no rectus communis in muraenids. There are, in fact, no hypobranchials in muraenines and no more than two in uropterygiines ( Nelson, 1966: table 1, figs. 41–44). M&W (table 1) inexplicably equated the rectus communis with Nelson’s ventral retractor, a muscle described above under dorsal retractor and illustrated in Figure 4 , because, as they proposed, it serves to move the pharyngeal jaws forward into the oral cavity. Thus, this muscle is a protractor, not a retractor. I can find no distinct, well-defined muscle bundle extending between the ceratohyal and the anteroventral margin of the lower pharyngeal toothplate (as described by M&W: 613) or fourth ceratobranchial in muraenines. I have not examined very large specimens, and it is possible, though unlikely, that there is an ontogenetic component to the muscle M&W described. Unfortunately, no sizes or collection numbers were given for the specimens they examined.

The major muscle bundle in this region inserting on the ceratohyal is the sternohyoideus, but it originates posteriorly in the hypaxialis near the cleithrum, not on the lower pharyngeal toothplate and thus could not function to protract the pharyngeal jaws. However, as described above, there is a fan-like array of muscle fibers extending from the dorsal surface of the posterior portions of two or three ceratobranchials to the anterior and posterior ceratohyals. These lie dorsal to the ventral arch elements and represent Nelson’s (fig. 10) subdivisions of the subpharyngealis ( Figs. 7 , 9 ; see also Springer and Johnson, 2015). As Nelson (362) described it, ‘‘Its position is distinctive, being internal to the skeletal elements rather than external as are the obliqui and recti. Probably the ventral musculature shifted from a relatively external to a relatively internal position with the reduction and loss of basibranchials. In any event, it assumed a sheetlike form, gradually encroaching upon the gill slits, which in the more advanced eels (e.g., the muraenids) are reduced to small round openings.’’

Intrinsic gill-arch muscles

Obliquus dorsalis (OD/OBL.DIV).— ( Fig. 2A )

‘‘The obliquus dorsalis, which medially spans the joint between the fourth epibranchial and the fourth pharyngobranchial is well developed.’’ (M&W: 610)

M&W (table 1) equated this muscle to Nelson’s obliquus inferior and superior. However, Nelson (table 2) reported those muscles to be absent in muraenids, and, in any case, the inferior obliquii only interconnect epibranchials. As reported by Nelson there are no obliqui dorsales in muraenids. The muscle bundle labeled as such by M&W (OBL.DIV, fig. 2A) is actually the anterior continuation of the sphincter oesophagi/dorsal retractor (SO/DR in Figs. 3–6 ). M&W apparently did not see that continuity, which has possible implications for their functional interpretation. Although they illustrate this as separate from AD4 (their AD5), it is also possible that they misinterpreted the anterior portion of that muscle as part of their obliquus dorsalis (see Fig. 2B and below).

Adductor dorsalis 4 (AD4).— ( Figs. 2–4 , 7C )

‘‘Adductor 5 is a very large muscle that originates on the posteromedial face of the fourth epibranchial and connects to the posterodorsal end of the fourth ceratobranchial.’’ (M&W: 610)

M&W (table 1) equated this muscle to Nelson’s obliquus posterior even though Nelson (table 2) reported this muscle as absent in muraenids. Adductors attach the epibranchials to the ceratobranchials of their corresponding arches, except, as described by S&J, ‘‘Ad5 attaches Cb5 variously to one or more of the following: Cb4, AC4, Eb4, or Eb5.’’ As reported by Nelson (1966: table 1), Cb5 is absent in muraenids (lower pharyngeal toothplate 5 having been transferred to Cb4). Accordingly, the large adductor attaching dorsally to the fourth epibranchial attaches ventrally to the fourth ceratobranchial (as described by M&W) and is adductor 4, not adductor 5. Nelson (tables 1–2, fig. 11) correctly reported AD5 ( Fig. 2 , Table 1) absent and AD4 present in muraenids. A very small portion of the fibers of AD4 bypass Eb4 to insert on the dorsal process of UPT.

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. 2. A and B based on figure 6B of Mehta and Wainwright (2008), modified. Red arrows point to indicated insertion points with which I disagree. (A) Red boxes indicate muscle identifications with which I disagree. (B) Muscles with my revised identifications in red letters. (C) Muscles redrawn based on my observations of Muraena lentiginosa, USNM 318298, epaxialis removed to match A and B, thus actual origin of LI (red star) within it is not shown; note origin of Sph on posterolateral surface of Cb4. AD, adductor dorsalis (?AD4? indicates the possibility that muscle as drawn could include part of AD4); Cb4, fourth ceratobranchial; Cl, cleithrum; DR, dorsal retractor; Hyo, hyoid (ceratohyal); LE, levator externus; LI, levator internus; OBL.DIV, obliquus dorsalis; Pcl (¼PHC. in panel A), pharyngocleithralis; R.C., rectus communis; SO, sphincter oesophagi; Sph, subpharyngealis. X indicates that there is no distinct muscle equivalent to the R.C. shown in A.

Fig. 3. Muraena lentiginosa, USNM 318298, 290 mm. (A) Slightly oblique left lateral view of fourth gill arch (first three removed) and associated musculature removed from body, sphincter oesophagi (SO/DR) intact; note two branches of LI2 and their insertion points on UPT. (B, C) Dorsal views of anterior ends of fourth epibranchials (C, close up of right side) deflected laterally to show that DR does not insert on them, but instead on UPT. AD, adductor dorsalis; Cb, ceratobranchial; DP dorsal process of UPT; DR, dorsal retractor; Eb, epibranchial; LI, levator internus; LPT, lower pharyngeal toothplate; Pcl, pharyngocleithralis; SO/DR, sphincter oesophagi/dorsal retractor; UPT, upper pharyngeal toothplate. (Subpharyngealis not shown.)

Fig. 4. Muraena lentiginosa, USNM 318298, 210 mm. (A) Left lateral view of left fourth gill arch and associated musculature, removed from body, circular fibers of SO removed to expose longitudinal fibers of DR; anterior section of LI2 occluded by posterior section. (B) Medial view of A; posterior section of LI2 exposed dorsal and ventral to anterior section. AD, adductor dorsalis; Cb, ceratobranchial; DP, dorsal process of UPT; DR, dorsal retractor; Eb, epibranchial; LI, levator internus; LPT, lower pharyngeal toothplate; UPT, upper pharyngeal toothplate.

Fig. 5. Muraena lentiginosa, USNM 318298, 290 mm. (A) Dorsal view of fourth gill arches and associated musculature, removed from body, SO/DR intact, showing anterior extension of DR to insert on UPT. (B) Ventral view of A showing insertion of VR on LPT, pharyngocleithralis removed. Cb, ceratobranchial; DR, dorsal retractor; Eb, epibranchial; LI, levator internus; LPT, lower pharyngeal toothplate; SO/DR, sphincter oesophagi/dorsal retractor; UPT, upper pharyngeal toothplate; VR, ventral retractor.

Fig. 8. Uropterygius alboguttatus, USNM 338657, 350 mm. (A) Left lateral view of left fourth gill arch and associated musculature, removed from body, circular fibers of SO removed to expose longitudinal fibers of DR, hypaxial retractor removed. (B) Medial view of A. Note insertion of single branch of LI2 on anterior end of UPT and posterior insertion point of LE4 near Eb4-Cb4 articulation. AD, adductor dorsalis; Cb, ceratobranchial; DR, dorsal retractor; Eb, epibranchial; LE levator externus; LI, levator internus; LPT, lower pharyngeal toothplate; UPT, upper pharyngeal toothplate.

Fig. 6. Muraena retifera, ANSP 103574, 165 mm. Left lateral view of tendinous attachment of DR to vertebral column (covered by epaxialis) as it exits SO. Cb, ceratobranchial; DR, dorsal retractor; Eb, epibranchial; Ep, epaxialis; SO, sphincter oesophagi.

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. 9. Uropterygius alboguttatus, USNM 338657, 310 mm. Left lateral view of left fourth gill arch and associated musculature in situ, posterior end of pharyngocleithralis and anterior end of hypaxialis excised at red lines to expose hypaxial retractor; LE4 passes medial to the insertion of HR to insert more posteriorly (see also Fig. 10). AD, adductor dorsalis; Cb, ceratobranchial; Eb, epibranchial; Ep, epaxialis; HR, hypaxial retractor; Hy, hypaxialis; LE levator externus; LI, levator internus; Pcl, pharyngocleithralis; SO/DR, sphincter oesophagi/dorsal retractor; Sph, subpharyngealis.