Functional Morphology of the Pharyngeal Jaw Apparatus in Moray Eels
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JOURNAL OF MORPHOLOGY 269:604–619 (2008) Functional Morphology of the Pharyngeal Jaw Apparatus in Moray Eels Rita S. Mehta* and Peter C. Wainwright Section of Evolution and Ecology, University of California, Davis, California 95616 ABSTRACT Moray eels (Muraenidae) are a relatively eels comprise roughly 95% of the taxonomic diver- large group of anguilliform fishes that are notable for sity and species richness within the Elopomorpha. their crevice-dwelling lifestyle and renowned for their Muraenids, otherwise known as moray eels, are a ability to consume large prey. Morays apprehend their clade within the anguilliforms. They include prey by biting and then transport prey by extreme pro- roughly 200 species and represent one of the larg- traction and retraction of their pharyngeal jaw appara- tus. Here, we present a detailed interpretation of the est clades within the anguilliforms. Within the mechanisms of pharyngeal jaw transport based on work muraenids, two monophyletic subgroups are recog- with Muraena retifera. We also review what is known of nized: Uropterygiinae and Muraeninae. These sub- the moray pharyngeal jaw apparatus from the literature groups are based on morphological characters of and provide comparative data on the pharyngeal jaw ele- the gill arch region and the development of the ments and kinematics for other moray species to deter- median fin (Bo¨hlke et al., 1989). Uropterygiines mine whether interspecific differences in morphology contain the genera Anarchias, Channomuraena, and behavior are present. Rather than comprising broad Scuticaria, and Urotperygius, while roughly twelve upper and lower processing tooth plates, the pharyngeal genera are thought to comprise the muraenines jaws of muraenine and uropterygiine morays, are long (see McCosker and Randall, 2007 for new genus, and thin and possess large, recurved teeth. Compared with the muraenines, the pharyngobranchials of the Diaphenchelys). uropterygiines do not possess a horn-shaped process and In addition to being extremely elongate with a their connection to the fourth epibranchial is dorsal reduced cross-sectional area, a body plan that is rather than medial. In addition, the lower tooth plates shared by all anguilliform fishes, morays exhibit do not exhibit a lateral groove that serves as a site of many morphological specializations for a crevice muscle attachment for the pharyngocleitheralis and the dwelling lifestyle such as the absence of scales, the ventral rather than the lateral side of the lower tooth ability to exude copious amounts of body mucus plate attaches to the fourth ceratobranchial. In all mor- (Randall et al., 1981), the loss of pectoral and pel- ays, the muscles positioned for protraction and retrac- vic fins (Bo¨hlke et al., 1989), gill arch reduction tion of the pharyngeal apparatus have undergone elon- and extreme posterior placement of the gill arches gation, while maintaining the generalized attachment sites on the bones of the skull and axial skeleton. Urop- (Nelson, 1966). These additional characteristics terygiines lack a dorsal retractor muscle and we pre- appear to allow morays to effectively move and sume that retraction of the pharyngeal jaws is achieved hunt in the crevices of coral heads and rocky reefs. by the pharyngocleitheralis and the esophagus. The fifth Unlike the majority of anguilliforms, some species branchial adductor is greatly hypertrophied in all spe- of morays can attain standard lengths of up to 3.9 cies examined, suggesting that morays can strongly m (Myers, 1991). The ability of morays to attain adduct the pharyngeal jaws during prey transport. The great size is ecologically interesting, especially in kinematics of biting behavior during prey capture and light of their high density that has been reported transport resulted in similar magnitudes of cranial in certain areas in the Caribbean (Randall, 1963; movements although the timing of kinematic events was Gilbert et al., 2005). Surveys in the Virgin Islands significantly different and the duration of transport was twice as long as prey capture. We speculate that morays (Randall, 1963) and those that took place recently have evolved this alternative prey transport strategy as in Barbados (Gilbert et al., 2005), suggest that a means of overcoming gape constraints, while hunting in the confines of coral reefs. J. Morphol. 269:604–619, 2008. Ó 2008 Wiley-Liss, Inc. Contract grant sponsor: NSF; Contract grant number: IOB- 0444554; Contract grant sponsor: American Association of Univer- KEY WORDS: moray eel; intra-oral transport; pharyngeal sity Women (AAUW) Fellowship. jaw apparatus; functional innovation *Correspondence to: Rita S. Mehta, Section of Evolution and Ecology, University of California, One Shields Ave, Davis, CA 95616. The Elopomorpha is a relatively large and early E-mail: [email protected] radiation of teleost fishes comprising species as Published online 14 January 2008 in diverse as tarpon, bonefish, halosaurs, spiny eels, Wiley InterScience (www.interscience.wiley.com) and anguilliform eels (Nelson, 2006). Anguilliform DOI: 10.1002/jmor.10612 Ó 2008 WILEY-LISS, INC. PHARYNGEAL JAW INNOVATION IN MORAY EELS 605 muraenids exhibit an average density of 5.6 fish pattern, following Winterbottom (1974). We also per 125 m22, which is similar to that of other large examine the kinematics of biting behavior in mor- predatory fishes for which densities have been ays and use Muraena retifera as our model for examined (Randall, 1963). Although morays are understanding the kinematic differences between known to feed on relatively large prey, dietary oral jaw biting during prey capture and transport. accounts in the literature are sparse and few stud- On the basis of anatomical characters and func- ies document prey consumed in relation to the size tional data for Muraena retifera and feeding obser- of the predator (Randall, 1967; Yukihira et al., vations for three other species, we make general- 1994; Young and Winn, 2003). How a relatively izations concerning the degree to which different large aquatic predator with a reduced cross-sec- morays use their pharyngeal jaws during trans- tional area, a large gape, and a noncircular mouth port. Lastly, we point out the skeletal changes that opening can consume large prey is interesting occurred that enabled the significant increase in from a biomechanical, physiological, and ecological protraction distance in the pharyngeal jaw appara- perspective. tus of morays and discuss how this pharyngeal In recent studies, we explored the functional innovation may be an adaptation for feeding in the morphology of prey capture and transport in confines of coral reefs. moray eels noting the marked reduction in move- able cranial elements and the small size of the hyoid bar, which are key characteristics of many MATERIALS AND METHODS suction-feeding fishes. We tested the effects of We studied the morphology and kinematics of the reticulated these reduced cranial elements on feeding kine- moray eel, Muraena retifera (Goode and Bean). Four adult Mur- aena retifera (Standard Lengths 35.5, 37.2, 34.32, and 40.3 cm) matics and concluded that morays do not use suc- were obtained commercially from Forest Young of Dynasty Ma- tion to capture prey, but rather, apprehend prey rine Associates in the Florida Keys. We recorded video of feed- with a bite (Mehta and Wainwright, 2007a). ing behavior for these individuals. After all kinematic sequen- Although other groups of teleosts are known to ces were obtained, the specimens were formalin-fixed and used apprehend prey by direct biting rather than by in- to examine the morphology and anatomy related to the pharyn- geal jaw apparatus. Two specimens were cleared and double- ertial suction feeding (Lauder, 1980a,b; Lauder stained for cartilage (Alcian blue) and bone (Alizarin red S) fol- and Norton, 1980; Alfaro et al., 2001; Porter and lowing a modification of Dingerkus and Uhler (1977). Speci- Motta, 2004; Janovetz, 2005; Konow and Bellwood, mens were examined with a Wild Heerbrugg dissecting micro- 2005) subsequent transport behaviors still involve scope. Following staining, the pharyngeal jaw apparatus of one of these specimens was disarticulated for photographs with a hydraulic, suction-based mechanisms (e.g., Lauder, digital Canon EOS. One formalin-fixed individual was X-rayed 1983). We discovered that moray eels have evolved and the radiograph was also used to examine the resting posi- an alternative mechanism of prey transport that tion of the pharyngeal jaws in relation to the skull. In addition involves extreme movement of their pharyngeal to the specimens of Muraena retifera, we studied preserved jaw region and we speculate that this novel func- specimens and cleared and stained specimens of two uroptery- giines: Anarchias seychellensis (Smith) (N 5 2) and Uroptery- tion enables morays to effectively swallow large gius macrocephalus (Bleeker) (N 5 3) and the following eight prey (Mehta and Wainwright, 2007b). However, muraenines: Echidna catenata (Bloch) (N 5 2), Echidna nebu- not all morays are known to consume large prey. losa (Ahl) (N 5 3), Echidna rhodochilus (Bleeker) (N 5 4), In fact, many morays feed mainly on crustaceans Enchelycore bayeri (Schultz) (N 5 2), Gymnothorax funebris and other soft and hard-shelled invertebrates (Ranzani) (N 5 2), Gymnothorax javanicus (Bleeker) (N 5 4), Gymnomuraena zebra (Shaw) (N 5 3), and Rhinomuraena (Myers, 1991). This variation in dietary patterns, quaesita (Garman) (N 5 3). in addition to the morphology-based sub-groupings Videofluoroscopy