Synopsis and Phylogenetic Analysis of the Pearlfish Subfamily Carapinae (Pisces: Carapidae)

Home , Carapinae, Echiodon, Onuxodon, Pearlfish

BULLETIN OF MARINE SCIENCE. 34(3): 386-397. 1984

SYNOPSIS AND PHYLOGENETIC ANALYSIS OF THE PEARLFISH SUBFAMILY CARAPINAE (PISCES: CARAPIDAE)

Jeffrey T. Williams

ABSTRACT Representatives of the pearlfish subfamily Carapinae are known from every ocean of the world except the Arctic Ocean. Four carapine genera are recognized: Echiodon, Onuxodon, Carapus and Encheliophis. The last contains the subgenera Encheliophis and Jordanicus. Members of the Carapinae share the following apomorphies: ossified interarcual element, reduced ventral process ofposttemporal bone and loss of pleural ribs. A phylogenetic analysis indicates that Echiodon and Onuxodon are sister groups, which together form the sister group of Carapus and Encheliophis. The subfamily and its included genera are diagnosed, and a key to all carapid genera is provided.

The family Carapidae, which includes the subfamilies Pyramodontinae and Carapinae, contains an ecologically diverse group of marine fishes. They range from tropical shallow water parasitic invertebrate symbionts to supposedly free- living fishes found on the continental shelf and slope of every major ocean except the Arctic Ocean (Arnold, 1956; Markle et aI., 1983; Trott, 1970). The last systematic review of the subfamily Carapinae was that of Arnold (1956). Since his study, additional material has been collected and many taxonomic problems have surfaced. A cladistic analysis of the group was undertaken to understand and define the relationships within the Carapinae. The numerous taxonomic problems at the species level are being examined by Douglas F. Markle and John E. Olney and will not be treated here. This paper diagnoses the subfamily and its genera, and proposes a hypothesis of the phylogenetic relationships among the carapine genera based on adult osteological and morphological characters.

METHODS

Extensive synonymies for genera and species are in Arnold (1956). Gill rakers refer to those on the first arch (sensu Cohen and Nielsen, 1978). Pelvic bones and cartilage refer to elements located inside the body immediately behind and between the ventral junction of the cleithra. Names of bones follow Courtenay and McKittrick (1970), Gosline (1960) and Tyler (1970). Osteological character states were based on specimens cleared and stained following Dingerkus' and Uhler's method (1977) and radiographs. Transverse processes are paired bony structures extending ventrolaterally from the precaudal centra (those centra without a distinct hemal spine). The transverse processes may articulate with their respective centra (usually those of centra 1-3 to 5), or be fused with the centra (Markle et aI., 1983). Pleural ribs are the bony elements (usually small in ophidiiforms) that articulate with the ventral edge of the transverse processes. Recurved cardiform teeth are those teeth that are bent in the middle in a posterior direction at a 90° angle to form an L-shaped tooth. Each tooth is loosely hinged to the premaxillary bone, directed laterally from the premaxillary, and concealed beneath the upper lip. Small fleshy flaps above the upper lip are approximately 0.2 mm lo'ng and extend into the groove between the premaxillary and maxillary bones, and, if present, are situated immediately anterior to the ventrally directed anteriormost pore of the supraorbital series (Markle et aI., 1983). The following institutional abbreviations are used; ANSP-Academy of Natural Sciences of Phila- delphia; BM(NH)-British Museum (Natural History), London; BPBM-Bernice P. Bishop Museum, Honolulu; CAS -California Academy of Sciences, San Francisco; FAKU - Fisheries Research Station, Kyoto University, Japan; ISH-Institut fur Seefischerei, Zoological Museum, University of Hamburg,

386 WILLIAMS: SYNOPSIS OF CARAPINAE 387

West Germany; SIO-Scripps Institution of Oceanography, La Jolla; UF -Florida State Museum, University of Florida, Gainesville; USAIC- University of South Alabama Ichthyological Collection, Mobile; USNM-National Museum of Natural History, Smithsonian Institution, Washington, D.C. Material Examined.-Pyramodon ventralis: off Isla San Felix, Chile: USNM 231353 (I). Snyderidia bothrops: off French Guiana: USNM 214035 (I cleared & stained). Carapus bermudensis: Dry Tortugas, Florida: UF 11825 (I cleared & stained). Carapus mourlani: Oahu, Hawaiian Islands: BPBM 17341 (I), 17821 (I). Carapus parvipinnis: Ifaluk Atoll, Caroline Islands: CAS 48978 (12 + 2 cleared & stained). Carapus variegalUs: Israel, Gulf of Aqaba: ANSP 72147 (I para type cleared & stained). Echiodon owasianus: Owase, Japan: FAKU 34517-34519 (3). Echiodon exsi/ium: Baja California Sur: SIO 65-292 (8 + I cleared & stained). Echiodon dawsoni: eastern Gulf of Mexico: USAIC 6279 (I paratype cleared & stained), UF 30886 (I para type cleared & stained). Echiodon drummondii: off northern Scotland: BM(NH) 1967.5.4: 3-5 (2 + I cleared & stained). Echiodon cryomargarites: off Argentina: ISH 1818/68 (I + I cleared & stained). Encheliophis (E.) jordani: Buena Vista, Baja California Sur: UF 34264 (I cleared & stained). E ncheliophis (E.) vermicularis: Belau Island, Caroline Islands: BPBM 11379 (I). Encheliophis (Jordanicus) gracilis: Oahu, Hawaiian Islands: BPBM 4997 (4), 4998 (I), 4999 (I); Fanning Island, Line Islands: BPBM 25714 (2); Tutuila, Samoa Islands: BPBM 5000 (I); Guam, Marianas Islands: UF 34265 (I + I cleared & stained); Ambon Island, Moluccas: BPBM 19426 (I); Seychelles Islands: BM(NH) 1981.2.24.19 (I). Onuxodon margaritiferae: Fatu Hiva, Marquesas Islands: BPBM 11674 (I); Moorea, Society Islands: CAS 13524 (I cleared & stained); Christmas Island, Line Islands: BPBM 5001 (I); Maldive Islands: CAS 48975 (2), 48976 (I cleared & stained). Onuxodon parvibrachium: Fiji: ANSP 91016 (I paratype); Seychelles Islands: ANSP 109210 (I cleared & stained). Brotuia barbata: off Aransas, Texas: UF 34271 (I cleared & stained). Otophidium omostigmum: northeastern Gulf of Mexico: UF 34270 (2 cleared & stained). Ophidion holbrooki: Cedar Keys, Florida: UF 948 (3 + I cleared & stained). Lepophidium jeannae: northeastern Gulf of Mexico: UF 26817 (3 + I cleared & stained). Parophidion schmidti: Providencia Island Group, Colombia: UF 25086 (7 + I cleared & stained). Ophisternon aenigmaticum: Mexico: UF 16209 (I I).

KEY TO CARAPID GENERA

la. Pectoral-fin rays 24-30, precaudal vertebrae 15 or fewer 2 lb. Pectoral. fin rays 23 or fewer, precaudal vertebrae 17-35 3 2a. Pelvic fins present pyramodon 2b. Pelvic fins absent Snyderidia 3a. Large recurved canines isolated at tips of both jaws; no strongly recurved cardiform teeth hidden under upper lip . 4 3b. No large recurved canines isolated at tips of both jaws; row of strongly recurved cardiform teeth hidden under upper lip 5 4a. Median rocker bone present at anterior end of swim bladder (found by inserting sharp probe through tissues of posterior part of gill cavity); body width about 3 in depth; no small fleshy tabs above upper lip at snout tip Onuxodon 4b. No median rocker bone at anterior end of swim bladder; body width about 2 in depth; 2-3 small fleshy tabs above upper lip at snout tip Echiodon 5a. Posterior margin of maxillary free Carapus 5b. Maxillary adnate ...... •...... 6 6a. Pectoral fin not apparent externally Encheliophis (Encheliophis) 6b. Pectoral fin apparent externally Encheliophis (Jordanicus)

Subfamily Carapinae Jordan and Fowler, 1902 Diagnosis. - lnterarcual element ossified; ventral process of posttemporal bone reduced or absent (Fig. 1); no pleural ribs; pectoral-fin rays 23 or fewer; precaudal vertebrae 17-35; pseudobranchial filaments 2-3. Comments. - Travers (1981) found an ossified interarcual element in the Carapi- dae (sensu Arnold, 1956) and in the Synbranchidae, but it was either cartilaginous 388 BULLETIN OF MARINE SCIENCE, VOL. 34, NO.3, 1984

A C E A G E

~ ~ U ~ ~

0 F B 0 F B~ D ~

Figure 1. (Left) Posttemporal bone of carapine genera. Left lateral view, front of fish is to the left. A, Carapus berrnudensis(UF 11825); B, Carapus parvipinnis (CAS 48977); C, Enche/iophis (E.)jordani (UF 34264); D, Enche/iophis (Jordanicus) gracilis (UF 34265); E, Echiodon cryornargarites (ISH 1818/ 68); F, Onuxodon rnargaritiferae (CAS 13524) (note reduction or absence of ventral strut). Figure 2. (Right) Shape of supracleithrum of carapine genera. Left lateral view, front of fish is to the left. A, Carapus berrnudensis (UF 11825); B, Carapus parvipinnis (CAS 48977); C, Enche/iophis (E.) jordani (UF 34264); D, Enche/iophis (Jordanicus) graci/is (UF 34265); E, Echiodon cryornargarites (ISH 1818/68); F, Onuxodon rnargaritiferae (CAS 13524).

or absent in all other groups he examined. He concluded that the ossified condition is more highly derived. This element is cartilaginous in pyramodontines. The inclusion of the Pyramodontinae in the Carapidae (Williams, 1983) is based primarily on the sharing ofa unique planktonic vexillifer larval stage (Markle and Olney, 1981; Olney and Markle, 1979) during ontogeny. As the synbranchids are most closely related to the mastacembeloids (Robert A. Travers, pers. comm.), the ossified interarcual element is considered as being independently derived in carapines and synbranchids. Thus a sister-group relationship between carapines and pyramodontines is supported by the shared vexillifer larval stage.

Carapus Rafinesque, 1810

Carapus Rafinesque, 1810 (type species based on Opinion 42 of the International Commission on Zoological Nomenclature Gyrnnolus acus Linnaeus). A list of 12 generic synonyms and a discussion of the nomenclatural history were given by Arnold (1956: 260-262). Diagnosis. - Premaxillaries with row of recurved cardiform teeth (under upper lip) external to polyserial band of small conical teeth, caninoid teeth sometimes present anteriorly; dentaries with polyserial band of conical teeth, some teeth of outer series may be caninoid, but canines never isolated at symphyses; vomer usually with enlarged caninoid teeth on crest; no fleshy flaps above upper lip at snout tip; posterior edge of maxillaries not adnate (rarely adnate in anomalous specimens according to Trott, 1970); pectoral fins present; three developed gill rakers on first arch; gill opening extends dorsally above mid-body on each side; no median rocker bone; pelvic bones present; posttemporal bone with ventral WILLIAMS: SYNOPSIS OF CARAPINAE 389 process reduced to a small knob (Fig. I); supracleithrum rod-shaped dorsally with a posteroventrally projecting bony flange giving ventral margin shape ofa shallow inverted U (Fig. 2); transverse processes of centrum 3 expanded posteriorly into a broad flat bony plate extending along lateral surface of swimbladder to beneath centrum 4; transverse processes of centrum 4 overlie respective modified transverse processes of centrum 3, and are about 112 length of transverse processes of centrum 5; neural spines of centra 2-4 rod-shaped; first hemal spine not modified; lateral-line ossicles present or absent (Carapus parvipinnis has a flattened, some- what rectangular ossicle associated with each segment, but these are lacking in other Carapus species examined); predorsal bone present or absent, when present, not associated with first dorsal-fin ray. Comments.-Based on radiographs of Carapus specimens, Arnold (1956) and Trott (1970) concluded that the transverse processes of centra 3 and 4 were fused. Courtenay and McKittrick (1970) found an independent, reduced fourth transverse process overlying a greatly expanded third transverse process on each side in C. bermudensis. All Carapus specimens I examined had a reduced, but independent, fourth transverse process. It seems likely that the statements about fused transverse processes resulted from the loss of resolution inherent in radiographs. Arnold (1956) and Trott (1970) described a calcified ligament connecting the first neural spine to the skull. Courtenay and McKittrick (1970) did not mention such a structure, and I have not found one in any of my material. In most radiographs of carapids, the slender posttemporal bones appear to connect the first neural spine to the skull, and could easily be mistaken for a calcified ligament. I found an outer row of recurved cardiform teeth on the upper jaw of every Carapus specimen examined. Trott (1970) noted the presence of these teeth in specimens of Encheliophis (Jordanicus) gracilis and Encheliophis (E.) jordani, but apparently overlooked them in his Carapus bermudensis specimens. This is not surprising since these teeth are completely covered by the upper lip. I have found these highly modified teeth only in members of carapid genera (Carapus and Encheliophis) that are symbiotic primarily with holothurians and asteroids (Cohen and Nielsen, 1978, for a more complete list of hosts). These teeth project laterally from the premaxillae and may be used to facilitate burrowing through host tissues to gain entry into the coelomic cavity. I did not find these teeth in specimens of Onuxodon, a molluscan commensal. Distribution. - The genus Carapus is circum tropical in distribution. Taxonomic Notes. -Of the 15 species of Carapus listed by Cohen and Nielsen (1978), C. owasianus is attributable to Echiodon (Williams, 1984) and there are taxonomic problems associated with the remaining species of Carapus that are being examined by John E. Olney and Douglas F. Markle (pers. comm.). Etymology. -As discussed by Arnold (1956) and Williams and Shipp (1982), the generic name Carapus is derived from the native Brazilian word c;arapo, which is a common name for the gymnotoid fishes. Gender is masculine.

Encheliophis MUller, 1842

Enche/iophis MUlier, 1842: 205 (type species by monotypy Encheliophis vermicularis MUlier). lordanicus Gilbert, 1905: 656 (type species by monotypy Fierasfer umbratilis Jordan and Evermann, 1903). E ncheliophiops Reid, 1940: 47 (type species by original designation Encheliophiops hancocki Reid, 1940). 390 BULLETIN OF MARINE SCIENCE, VOL 34. NO, 3, 1984

Diagnosis.-Premaxillaries with row of recurved cardiform teeth (under upper lip) external to single row of slender conical teeth; dentaries with single row of slender conical teeth; vomer with slender conical teeth (no granular teeth); no fleshy flaps above upper lip at snout tip; maxillaries adnate; pectoral fins present (subgenus Jordanicus), or not apparent externally (subgenus Encheliophis with rudimentary elements present beneath skin); gill rakers reduced and without denticulations; gill opening not extending dorsally above mid-body on either side; no median rocker bone; pelvic bones present; posttemporal bone with ventral process reduced to a small knob (Fig. 1); supracleithrum rod-shaped dorsally with posteroventrally projecting bony flange giving ventral margin shape of a shallow inverted U (Fig. 2); each transverse process of centrum 3 expanded posteriorly into a broad flat bony plate extending along lateral surface of swimbladder to beneath centrum 5; transverse processes of centrum 4 overlie respective modified transverse processes of centrum 3, and are about lh length of transverse processes of centrum 5; transverse processes of centra 4 and 5 overlie, but are not fused to, modified third transverse processes; neural spines of centra 2-4 modified into broad, laterally-flattened bony plates as long as their centra; first hemal spine not modified; flat, rounded lateral-line ossicles present (one per segment); slender predorsal bone over centrum 4, and closely associated with neural spines 3 and 4; first dorsal-fin ray not associated with predorsal bone. Comments. -As discussed in the Carapus account, Arnold (1956) and Trott (1970) concluded that Encheliophis and Jordanicus have the modified third transverse processes fused to the fourth and fifth transverse processes on each side. In my specimens of these genera, each of these transverse processes is independent, the fourth is reduced in size, the fifth is normal size, and both overlie the modified third process. In addition, the slender calcified ligament described by Arnold (1956: fig. 5) is not present. The neural spines of centra 2-4 are modified into bony plates that almost touch each other, but do not have the appearance of Arnold's calcified ligament. Distribution. Encheliophis is known to occur in the tropical and subtropical Pacific and Indian Oceans. Taxonomic Notes. Arnold (1956) reduced Jordanicus and Encheliophiops to subgenera of Encheliophis, and recognized three species in the subgenus Encheliophis: E. (E.) hancocki, E. (E.) jordani, and E. (E.) vermicularis; and two species in the subgenus Jordanicus: E. (J.) gracilis and E. (J.) sagamianus. Trott (1970) synonymized E. (E.) hancocki with E. (E.) jordani. Smith (1955) synonymized E. (J.) sagamianus with E. (J.) gracilis, but did not give his reasons for doing so. Arnold (1956) chose to recognize both species, while Trott (1970) chose to follow Smith (1955). Trott (1981) later included E. (J.) sagamianus in a list of valid carapine species. Until the different geographic populations of E. (J.) gracilis are thoroughly studied, the status of E. (J.) sagamianus will be in doubt. Whether Jordanicus should be given generic or subgeneric taxonomic status has been a controversial subject. Smith (1955) and Trott (1981) gave it full generic status primarily on the basis of its having a pectoral fin and Encheliophis lacking one. Arnold (1956) and Cohen and Nielsen (1978) considered the loss of pectoral fins as a subgeneric character not sufficient to distinguish Encheliophis and Jor- danicus as full genera. My cleared and stained Encheliophis (E.) specimen has a rudimentary pectoral fin consisting of one or more cartilage radial(s) supporting 3-4 minute, but ossified, fin rays. This assemblage is beneath the skin and is not WILLIAMS: SYNOPSIS OF CARAPINAE 391 evident in unstained specimens. The reduced condition of the pectoral fin in the subgenus Encheliophis and the loss of conical teeth in the upper jaw in the subgenus Jordanicus represent highly derived conditions that help to establish monophyly for their included species. On the basis of the above information, Jordanicus and Encheliophis are considered to represent two distinct subgenera in the genus E ncheliophis. Etymology. - The generic name Encheliophis is apparently derived from the Greek enchelys, meaning eel, and the Greek ophis, meaning serpent or reptile, presumably referring to its elongate body. Gender is masculine.

Echiodon Thompson, 1837

Echiodon Thompson, 1837: 55 (type species by monotypy Echiodon drummondii Thompson, 1837). Diagnosis.-Each premaxillary with 1-3 large recurved fangs at tip followed by polyserial band of small conical teeth; each dentary with 1-2 large recurved fangs at tip followed by polyserial band of small conical teeth (some species have a distinct untoothed gap behind fangs, but others have small conical teeth close behind fangs); vomer covered with conical teeth, those on crest sometimes larger than others, but never caninoid; 2-3 small fleshy flaps above upper lip on each side of snout tip; posterior edge of maxillaries not adnate; pectoral fins well- developed; three developed gill rakers on first arch; gill opening extends above mid-body on each side; no median rocker bone; no pelvic bones or cartilage; posttemporal bone rod-shaped, no ventral fork (Fig. I); suprac1eithrum rod-shaped, no posteroventrally directed bony flange, ventral margin convexly rounded (Fig. 2); each transverse process of centrum 3 only slightly expanded posteriorly, its posterior margin not extending beyond about middle of centrum 4, plane of each flattened third transverse process at about a 45° angle to longitudinal axis of body with ventralmost edge of each process directed inward to constrict swim bladder, and flattened part directed posterolaterally (Markle et al., 1983); transverse processes of centrum 4 about same length as those of centrum 5 (i.e., not reduced); neural spines of centra 2-4 rod-shaped; first hemal spine not modified; no lateral- line ossic1es; predorsal bone present or absent, when present, associated with first dorsal-fin ray.

Comments. - The inward angling of the third transverse processes to constrict the swimbladder is found only in species of Echiodon. This condition, shared by all examined Echiodon species, is considered to be a derived state and suggests a monophyletic origin for the included species. All other carapines have greatly expanded third transverse processes that extend posteriorly along the sides of the swimbladder, and parallel to the longitudinal axis of the body. I have found the size of the diastema in the lower jaw (Arnold, 1956) to be variable within the genus and of questionable value as a generic character. Williams (1984) gives diagnostic characters of 10 named species (two new) and two problematic populations. Distribution. - The genus Echiodon is represented in every major ocean except the Arctic Ocean (Williams, 1984). Etymology. - The name Echiodon is a combination of the Greek echis, meaning viper or adder, and the Greek odous (odon) meaning tooth, in reference to the large fangs at the tips of the jaws. Gender is masculine. 392 BULLETIN OF MARINE SCIENCE, VOL. 34, NO.3, 1984

Onuxodon Smith, 1955

Onuxodon Smith, 1955: 405 (type species by original designation Carapus parvibrachium Fowler, 1927). Diagnosis.-Each premaxillary with 1-2 large recurved fangs at tip followed by an edentate gap, then by a po1yseria1band of small concical teeth; each dentary with 1-2 large recurved fangs at tip followed by a short edentate gap, then a polyserial band of small conical teeth; vomer covered with small conical teeth; no fleshy flaps above upper lip at tip of snout; posterior edge of maxillaries not adnate; pectoral fins visible externally (reduced in one species, but still evident); three developed gill rakers on first arch; gill opening extends above mid-body on each side; median rocker bone present at anterior end of swimbladder; no pelvic bones or cartilages; posttemporal bone rod-shaped, no anteromedially directed bony flange, ventral margin slightly rounded (Fig. I); supracleithrum rod-shaped, no posteroventrally directed flange, ventral margin convexly rounded (Fig. 2); transverse processes of centrum 3 extensively modified, anteriorly connected to each other by a ridge of bone extending beneath centrum 3, each transverse process expanded into a bony plate that extends along side of swimbladder to beneath front of centrum 5 (Courtenay and McKittrick, 1970); no transverse processes on centrum 4; neural spines of centra 2-4 rod-shaped; modified first hemal spine long, laterally flattened, and bent anteriorly at middle of length (Tyler, 1970; fig. 3); no lateral-line ossicles along body; predorsal bone situated immediately in front of first dorsal-fin ray. Comments.-Courtenay and McKittrick (1970) examined the sound-producing structures associated with the swimbladder of Onuxodon, and suggested common ancestry of carapine (pyramodontines do not possess similar structures) and ophi- diids based on their "pattern of sound-producing muscles and their association with the swimbladder." The nature of the expanded third transverse processes of Onuxodon, while different, bears some similarity to that found in other carapines. The expanded part superficially resembles that of Carapus and Encheliophis, but these genera do not possess the bony bar connecting the transverse processes of each side. Echiodon does not have the posterior expansion, but has an inwardly directed component constricting the swimbladder that could be a precursor to the bony bar of Onuxodon. In addition, the third transverse processes of Onuxodon have the expansion directed anteriorly from the thickened part of the process, while Carapus and Encheliophis have the expansion directed posteriorly from the thickened part (see illustrations in Courtenay and McKittrick, 1970). Echiodon also has a slight anteriorly-directed expansion of the third transverse processes that vaguely resembles that of Onuxodon. Distribution, - Known from the western Indian Ocean to the Philippine and Mar- quesas Islands. Taxonomic Notes.-Arnold (1956) recognized Onuxodon as a subgenus of Car- apus including Carapus (Onuxodon) parvibrachium and C. (0.) margaritiferae. Tyler (1970) and Courtenay and McKittrick (1970), based on anatomical studies, returned Onuxodon to generic status. The highly derived sound-producing structures illustrated by Courtenay and McKittrick (1970) support a sister-group relationship between the included species, O. parvibrachium and O. margaritiferae. Smith's (1955) description and figure of Carapus reedi appear to represent a tenuis larva (as defined by Arnold, 1956) of Onuxodon margaritiferae, but this WILLIAMS: SYNOPSIS OF CARAPINAE 393 needs to be confirmed by examination of the holotype to see if a median rocker bone is present. Etymology. -Smith (1955) did not provide his derivation of the name Onuxodon, but it appears to be a combination of a prefix that could have several different derivations (possibly from the Greek onyx meaning claw or talon), and the Creek odous (odon), meaning tooth. Gender is masculine.

CHARACTER ANALYSIS lnterarcual Element. - The carapines and the synbranchids (Travers, 1981) have an ossified interarcual element, while it is cartilaginous in the pyramodontines and the comparative ophidiiforms. As discussed earlier, the ossified condition is considered the most highly derived state. The sharing of this state between the carapines and the synbranchids is considered homoplasious. Posttemporal Bone. -I have found three character states: (1) ventral wing well- developed, (2) ventral wing reduced to a small knob (Fig. 1A-D), and (3) ventral wing reduced to a small residual knob or lost (Fig. 1E, F). The pyramodontines and the comparative ophidiiforms have condition one, Carapus and Encheliophis have condition two, and Echiodon and Onuxodon have condition three. The above character states represent a transformation series with the loss (condition three) representing the most highly derived state. The reduction of the wing supports monophyly for the carapines, and the loss supports a sister group relationship between Echiodon and Onuxodon. Pleural Ribs. - The carapines have lost all pleural ribs. The pyramodontines and all comparative material examined have some pleural ribs. The loss of all pleural ribs is considered a derived state supporting monophyly for the carapines. Pelvic Bones and Cartilage.-Echiodon and Onuxodon have lost all pelvic elements. Carapus, Encheliophis, Pyramodon and other ophidiiform material examined have distinct pelvic bones. Snyderidia has a pelvic cartilage. The loss of pelvic bones and cartilage is considered to be a derived state supporting a sister group relationship between Echiodon and Onuxodon. The reduction from pelvic bones and cartilage to only pelvic cartilage in Snyderidia is difficult to assess, but appears to be independent of the condition in Echiodon and Onuxodon. Third Transverse Processes.-Echiodon and Onuxodon have a slightly (Echiodon) or greatly (Onuxodon) expanded part that is directed anteriorly from the thickened part ofthe process. Carapus, Encheliophis and the comparative material have the expanded part (if present) directed posteriorly from the thickened part of the process. The distinctively shaped third transverse process shared by all the species of Echiodon supports monophyly for the group. Onuxodon possesses a distinctive bony bar that extends beneath the third centrum to connect the third transverse processes. Whether this bar has been derived from the Echiodon condition or from the Carapus-Encheliophis condition is not clear. Since the conditions in Echiodon and Onuxodon both appear to be more derived than that in Carapus- Encheliophis, 1 treat them as independent synapomorphies for Echiodon and Onuxodon. Fourth Transverse Processes. - Three conditions exist for this character: (I) fourth processes about the same length as the fifth, (2) fourth processes about one half the length of the fifth, and (3) fourth processes lost. Echiodon, the pyramodontines, and the comparative ophidiiform material have condition one, which is consid- 394 BULLETIN OF MARINE SCIENCE, VOL. 34, NO.3, 1984 ered to be the plesiomorphic state. Carapus and Encheliophis have condition two, and Onuxodon has condition three. If these states represent a transformation series, then Onuxodon would be considered as the sister group to Carapus-En- cheliophis. Since Echiodon and Onuxodon share the extreme reduction or loss of the ventral wing of the posttemporal and the loss of all pelvic elements, I believe that these two derived characters support an Echiodon-Onuxodon sister group relationship over the single derived character that supports the Onuxodon-Car- apus-Encheliophis grouping. For this reason, I believe that the loss of the fourth transverse processes in Onuxodon was independently derived, and I have treated conditions two and three as independently derived synapomorphies. First Hemal Spine. - The first hemal spine of Onuxodon has a broad laterally- flattened ventral part that is directed anteroventrally from a point at about half the length of the spine, where it changes inclination from the posteroventrally directed upper half of the spine. All other material examined has a simple rod- shaped first hemal spine directed posteroventrally for its entire length. This character supports monophyly for the two species of Onuxodon. Median Rocker Bone. - This bone is found in Onuxodon, and was described by Courtenay and McKittrick (1970). No other carapids have it, but some species of Ophidion have a rocker bone (Courtenay and McKittrick, 1970; Rose, 1961). Examination of the rocker bones of Onuxodon and Ophidion holbrooki reveals several differences that suggest two independent derivations. The rocker bone of Onuxodon is solid and has a knob projecting from its dorsal surface (Courtenay and McKittrick, 1970: fig. 9), while that of Ophidion has an internal cavity into which the gas bladder penetrates (the gas bladder is external to the rocker bone of Onuxodon) and lacks a knob on the dorsal surface (Rose, 1961: fig. 5). Based on these differences, I believe the rocker bone of Onuxodon is a synapomorphy for the included species. Recurved Cardlform Teeth. - These upper-jaw teeth represent a synapomorphy linking Carapus and Encheliophis as sister groups. These teeth are not found in any of the other material examined. Supracleithrum. The two basic shapes of this bone are: (1) simple rod-shaped bone (Fig. 2E, F), and (2) lower part with a posteroventrally directed wing (Fig. 2A-D). Echiodon, Onuxodon, pyramodontines and other ophidiiform material examined have condition one (plesiomorphic). Carapus and Encheliophis share the derived condition two, which supports monophyly for these two genera. Neural Spines. - The second-fourth neural spines are modified into broad laterally-flattened plates in the subgenera of Encheliophis, while they are rod-shaped in all other material examined. The modified condition supports monophyly for Encheliophis. Gill Rakers. - The subgenera of Encheliophis have greatly reduced non-denticu- lated gill rakers on the first arch. In all other carapids, the first arch has three well-developed gill rakers with denticulations. The reduced condition is a synapomorphy of Encheliophis. Maxillaries. - The maxillaries are adnate in Encheliophis. All other specimens examined have a free posterior margin of the maxillaries. The adnate condition is a synapomorphy for Encheliophis. Gill Openings. - Encheliophis (Encheliophis) has the gill openings restricted to the lower half of the body. The gill openings extend to or above mid-body on each WILLIAMS: SYNOPSIS OF CARAPINAE 395

ENCHELIOPHIS ENCHELIOPHIS ECHIODON ONUXODON CARAPUS (ENCHELIOPHIS) (JORDANICUS)

Figure 3. Cladogram of the Carapinae. Numbers refer to synapomorphies: I-ossified interarcual element, 2-reduced ventral process of posttemporal bone, 2'-extreme reduction or loss of ventral process of posttemporal bone, 3-10ss of pleural ribs, 4-loss of pelvic bones and cartilage, 5- distinctively modified third transverse processes, 6-third transverse processes connected by ossified bar beneath centrum 3, 7-loss offourth transverse processes (see text), 8-modified first hemal spine, 9-median rocker bone present, lO-strongly recurved cardiform teeth under upper lip, II-ossified posteroventrally directed wing of supracleithrum, 12-fourth transverse processes reduced to half length of fifth (see text), 13-neural spines 2-4 modified, 14-reduced gill rakers, 15-adnate maxillaries, 16- restricted gill openings, 17-extreme reduction of pectoral fins, 18- reduced premaxillary dentition. side in all other material examined. The restricted condition is a synapomorphy of the subgenus Encheliophis. Pectoral Fins. - The pectoral fins of Encheliophis (Encheliophis) are reduced to rudiments not visible externally. Pectoral fins are externally visible in all other material examined. The rudimentary condition is a synapomorphy of the subgenus E ncheliophis. Conical Teeth. -Encheliophis (Jordanicus) has lost all conical teeth in the upper jaw. At least one row of conical teeth is in the upper jaw of all other material examined. This loss of conical upper jaw teeth is a synapomorphy of the subgenus Jordanicus.

CLASSIFICAnON OF CARAPINAE The genera of the Carapinae form a monophyletic group defined by the following synapomorphies: ossified interarcual element, ventral process of posttemporal bone reduced or absent and pleural ribs lost. Based on the characters examined, the most parsimonious cladogram for the Carapinae is that shown in Figure 3. This phylogeny has Echiodon and Onuxodon as sister taxa that together form a sister group to Carapus and Encheliophis. I have not found a synapomorphy that will establish monophyly for Carapus. Carapus is the sister group of Encheliophis, which contains two monophyletic subgenera. An alternative tree with Echiodon as the sister group of all other carapines and Onuxodon as the sister group of Carapus and Encheliophis is supported by the reduction and loss of the fourth transverse process. This tree would require independent loss of pelvic elements and of the ventral wing of the posttemporal of Echiodon and Onuxodon. The previous tree requires only the independent loss 396 BULLETIN OF MARINE SCIENCE, VOL. 34, NO.3. 1984 of the fourth transverse processes of Onuxodon. If the uniquely modified third transverse processes of Onuxodon are derived from those of an ancestor of Echio- don, then this would support the c1adogram in Figure 3. Unfortunately, I cannot be certain about the derivation of the bony bar connecting the third processes of Onuxodon. A c1adogram of the Carapinae (Fig. 3) based on the above characters corresponds to Trott's (1970: fig. 7) evolutionary tree outlining the evolution of parasitism in the Carapidae. An additional test of this phylogenetic hypothesis will come from an analysis of larval characters that is being conducted by Douglas F. Markle and John E. Olney (pers. comm.).

ACKNOWLEDGMENTS

I thank the curators and staff of the institutions that provided study material. Specimens that were cleared, stained and dissected were kindly provided by D. M. Cohen, R. L. Shipp, G. Kreffi, C. R. Gilbert and W. N. Eschmeyer. I thank W. F. Smith- Vaniz for his hospitality and assistance during a visit to the ANSP, D. E. Rosen and R. A. Travers for discussions about the interarcual element and A. Wheeler for providing a cleared and stained specimen from the BM(NH). C. R. Gilbert, R. Win- terbottom and an anonymous reviewer provided helpful comments and suggestions. I thank G. Russell for preparing the typescript. The CAS provided a visiting scientist stipend during a visit to that institution, and a IO-week fellowship from the Smithsonian Institution supported my summer-198 I residence at the USNM.

LITERATURE CITED

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DATE ACCEPTED: August 12, 1983.

ADDRESS: Florida State Museum and Department of Zoology, University of Florida. Gainesville. FL 32611. PRESENT ADDRESS: Division of Fishes, National Museum of Natural History. Smithsonian Institution. Washington, D.C. 20560.