Two Types of Pelagic Larvae of <I>Bembrops</I> (Trachinoidea

BULLETINOFMARINESCIENCE.60(1): 152-160. 1997

TWO TYPES OF PELAGIC LARVAE OF BEMBROPS (TRACHINOIDEA: PERCOPHIDAE), WITH NOTES ON THEIR PHYLOGENETIC IMPLICATION

Muneo Okiyama

ABSTRACT A larva and a pelagic juvenile of Bembrops curvalura are identified and described from Japanese waters. These pelagic larvae are remarkable in developing a transparent enlarged dermal space over the head, i.e., so-called "bubblemorph," which disappears by 15.8mm SL through metamorphosis. Pigmentation is scant, but a peritoneal pigment section over the gut is distinct. Occurrence of a similar larva of Bembrops in Australian waters probably referable to another species is also recorded, although its specific identification cannot be made. In contrast, the Atlantic congener, B. anatiroslris, is known to lack bubblemorph stage (Richards, 1990), revealing at least two types of pelagic larvae in the genus. Possible significances of this peculiar larva] morph are discussed. Known larvae of the Percophidae including Bem- brops, Chrionema, Spinapsaron. Hemerocoeles, and Matsubaraea are compared and based on ]arval morphology the monophy]y of the family is questioned.

The Suborder Trachinoidea contains more than 200 species of (tropical) marine fishes placed in 13 families (Nelson, 1994). Although the monophyletic integrity of the group sensu Pietsch and Zabetian (1990) is doubtful (Johnson, 1993), the hypothesis that Trichonotidae, Creediidae and Percophidae form a monophyletic assemblage has gotten general support (Pietsch and Zabetian, 1990; Johnson, 1993). More than 10 years ago, the ontogeny and systematics of the Trachinoidea (excluding Pholidichthyidae and Ammodytidae) were reviewed by Watson et al. (1984), revealing the paucilty of early life history data on these taxa. At that time, only a single larva of Hemerocoetes sp. had been described (Crossland, 1982). Subsequently, Mori (1988) described a series of early developmental stages of Spinapsaron sp. in detail. Recently, an unusual pelagic bubblemorph larva from Japanese waters was identified as Bembrops. A comparison of the morphology of this larva with that of the Atlantic congener, B. anatirostris, (Richards, 1990), led me to further investigate the current knowledge of early life history stages of the Percophidae including examination of specimens not described in the literature, The revision of Bembrops (Das and Nelson, 1996) provided reliable information on the systematic status of each species in this complex genus. In this paper, emphasis is placed on the phylogenetic significance of the larval bubblemorph of Bembrops and the generic interrelationships of the family Per- cophidae based on ontogeny.

MATERIALS AND METHODS

Materials for this study came from various sources. Two pelagic individuals, a larva and a juvenile of Bembrops curvalura were collected from the Sagami Bay, Centra] Japan, during the cruises of the R/V TANSEIMARU(KT88-2; 10.3 mm SL; II Dec. 1988) and the R/V HAKUHOMARU(KH89-1; 15.8 mm SL; 11 Sept. 1989). These collections were made using 3.3-m-IKPT towed obliquely from the surface to less than 100 m. These specimens are held in the Ocean Research Institute (ORI). Additional materials were borrowed from other institutions or sorted from my collections, as follows: Bemhrops sp.: CSIRO uncatalogued; 10.0 mm SL; 13 Oct. 1983; ]9°15'S, 116°10'E; 2-m-IKMT, oblique tow, 0-100 m. Chrionema cf. pallidum: NMFS-Honolulu T8-1-16; 16.3 mm SL; 24-25 Jan. 1977; 14°00'S, 150000'W; 3-m-IKMT, oblique tow, 0-275 m; Identified by Dr. B. C. Mundy; to be held in the Los Angeles County Museum. Malsubaraea fusiforme: ORI uncatalogued, 8.6 mm SL (cleared and stained); 17 Sept. 1979; Fukui harbor, the Sea of Japan; Maruchi larva net, horizontal

152 OKIYAMA: TWO TYPES OF LARVAL Bt.MBROPS 153 tow, 5-m depth. Spinapsaron sp.: ORI uncatalogued, 12.2 mm SL (cleared and stained); 13 June 1969; Sado strait. the Sea of Japan; Triangle larva net, horizontal tow, 25-m depth. Larvae were measured under a stereo microscope using an ocular micrometer according to the meth- od of Okiyama (1988). Drawings were prepared with the aid of camera lucida. Larval and juvenile specimens of Bembrops curvatura were cleared and stained for osteological study following Dingerkus and Uhler (1977).

RESULTS

Bembrops curvatura Okada et Suzuki Figure 1 Identification.-Despite its unusual bubblemorph appearance, the 1O.3-mmlarva can readily be referred to Bembrops, in having meristic characters and the external as well as internal pigmentation patterns similar to those of the metamorphosed pelagic juvenile, which resembles the pelagic larvae of Bembrops anatirostris reported by Richards (1990), and it bears the small incipient skin flap at the posterior end of the maxilla diagnostic for Bembrops. Recently, 13 species of Bembrops were recognized as valid(Das and Nelson, 1996), three of which are recorded from the Japanese waters. Their meristic characters are shown in Table 1, together with those of the unnamed Japanese species (Okamura, 1985) which was not mentioned in Das and Nelson (1996). Both the larval and juvenile pelagic specimens described herein can be ascribed either to Bembrops curvatura or to B. caudimacula from the meristics (Table 1). However, the] 5.8-mm juvenile exhibits "the lateral line descending abruptly over pectoral fin" which is diagnostic for B. curvatura (Das and Nelson, 1996). The number of lateral line scales (about 46) and rows of scales between lateral line and origin of anal fin (3) also fall within the ranges of B. curvatura.

Description.-] 0.3 MM LARVA(FIG. 1 A-C). Measurements in percentage of SL and meristic data: Head length 47.5, head width 43.7, head depth 33.0, snout ]6.5, maxillary 18.2, eye diameter ]5.0 X 12.1, preanus 63.1; D VI-14, A 14, PI 23/23, P2 6, C 7+7+7+3, Vertebrae 28. GENERALMORPHOLOGY.Body stubby, with exceptionally massive and bulbous head created by envelope of flaccid skin. Head long, but deep and wide. Head oval in dorsal view with large eyes located latero-ventrally at widest part. Anlage of brain and arrangement of oculomortor muscles clearly visible through thick but transparent envelope. Transparent gelatinous layer deep, lacking any visible structures except widely spaced strands running vertically between surface and base of skull. Strands usually branched just above skull and spread towards surface of skin. Ovoidal eyes (long/short axis = 1.25) located at middle of head with long axis dorsally titled to horizontal plane. Nostrils small, single, deep cups formed near tip of long snout close to maxillae. Mouth large and inferior in position due to bulged forehead. Maxillae reach posteriorly to vertical through anterior part of eye. Membranous flap absent on posterior end of maxillae. Premaxillae edentulous with complicated articulation anteriorly with maxillae, but anterior spinous pro- jection not present. Dentary teeth also lacking. No spinous elements on head. In contrast to head, trunk and tail laterally compressed. Abdomen distended ventrally within framework of bubblemorph. Tail decreases in depth toward caudal fin which again deepens near base. Full compliment of rays present in all fins, although first dorsal fin still small and separated widely from second. Dorsal- and anal-fin rays similarly long and 154 BULLETIN OF MARINE SCIENCE. VOL. 60. NO. I, 1997

Figure 1. Pelagic larva (bubblemorph) and juvenile of Bembrops curvatura, collected from Sagami Bay, central Japan. A-C, Left lateral, dorsal and ventral views of larva, 10.3 mm SL; D-F, the same of juvenile, 15.8 mm SL. Internal pigment on gut omitted in dorsal view. OKiYAMA: TWO TYPES OF LARVAL BEMBROPS 155

Table 1. Selected meritistic characters for four species of Bembrops recorded from Japanese waters (Okamura, 1985; Nakabo, 1993, Das and Nelson, 1996)

Species 2nd dorsal fin Anal fin Pectoral fin Lateral 1. scales B. caudimacula 13-15 14-17 19-25 42-54 B. curvatura 14-15 15 19-25 40-49 B. filifer 14-16 16-18 22-25 60-69 B. sp.* 15 17 22-28 65-67 Pelagic specimens 14 14-15 23-24 ca. 46 • Okamura (1985). segmented. Pelvic fins in jugular position and broadly separated at base. Pelvic rays shorter than those of pectoral fin. Pectoral fins have broad base and blade with rays directed posterodorsally. Pigmentation: Aside from black eyes, pigmentation light, particularly on head, where small dots visible only on opercular flaps, on hind brain and halfway along ventral edge of dentaries. On the trunk, dots of various sizes on pectoral fin blade and around pelvic fin base posterior to cleithral symphysis. On caudal peduncle, pigments concentrated on dorsal and ventral mar- gins and midlaterally near caudal-fin base. Most conspicuous of these occurs along each side of ventral midline. In addition, series of internal melanophores present along most of dorsal border of vertebrae. Fin pigmentation restricted to pelvic fins, which bear dots on proximal halves of membranes between 1st to 4th rays laterally. Single large peritoneal patch of pigment covers nearly half of dorsal surface of gut excluding rectum. 15.8 MMPELAGICJUVENILE(FIG.1 D-F). Measurements in % of SL and meristic data: Head length 47.5, head width 34.2, head depth 19.0, snout 11.7, eye diameter 13.6, preanus 60.8; D VI-14, A 15, PI 24/24, P2 6, C 4+7+7+4, L.L.S. ca 46, Vertebrae 28. GENERALMORPHOLOGY.Larval bubblemorph completely transformed into juvenile form with extremely depressed and long head. Relative size of head unchanged in length, but decreased in width due to loss of bubblemorph. Dorsal profile of forehead straight, forming pointed long snout. Eyes similarly large, produced laterally, and oval in shape with longer axis in parallel with horizontal plane. Top of skull remained transparent as in previous larva. Nostrils incom- pletely separate into two narrow openings. Small teeth formed on edges of both jaws throughout gape. Abdominal profile straight, and caudal peduncle deep. All fin rays fully formed with distinct first dorsal fin closely spaced with second dorsal fin. Pectoral rays directed posteriad. Body surface except head, mostly covered with small scales. Lateral-line scales fully formed, descending abruptly over pectoral fin (not shown in Fig. 1). PIGMENTATION.Pigmentation patterns almost unchanged from previous larva, whereas each spot densely pigmented or extended. Dorsal surface of head unpigmented except for small dots along preopercular margin and upper jaws. Some- what dense pigmentation on lateral side of dentary. Melanophores chiefly added along midlateral part of body.

Bembrops sp. Figure 2 Identification.- The top three species listed in Table 1 also represent the Bem- brops fauna in the northwestern waters of Australia where this larva was collected 156 BULLETIN OF MARINE SCIENCE, VOL. 60, NO. I. 1997

Figure 2. Pelagic larva (bubblemorph) of Bembrops sp. 10.0 mm SL, collected from the Australian NW shelf. Figure 2 was prepared with minor corrections.

(Das and Nelson, 1996). Despite similarity to the bubblemorph, this specimen revealed different pigmentation from larval B. curvatura described above. Al- though meristic counts of this larva most closely fit with those of B. caudimacula, its distinction from B. filifera remains to be solved. 10.0 mm larva, bubblemorph (Fig. 2).-Measurements in % of SL and meristic data: Head length 51.0, head width 42.3, head depth 31.0, snout 14.5, eye diameter 13.5, preanus 61.0; D VI-14, A 16, PI 22/22. P2 6, C 9+7+7+7. GENERALMORPHOLOGYANDPIGMENTATION.Due to poor preservation, head of this specimen slightly distorted. Since this larval bubblemorph closely resembles 1O.3-mm larva of previous species, only differences are listed. Snout shorter due to slightly more anterior placement of eyes and dorsal profile of snout concave due to extension of premaxillae. First dorsal fin well developed. Pigments occur on the anterior and posterior portion of upper jaws, besides internal melanophores on articular head of maxillae. Dorsal edge of caudal peduncle unpigmented, but proximal half of caudal fin moderately dotted. Small spot present on ventral midline just anterior to anus.

DISCUSSION Significance of the Larval Bubblemorph.-Striking contrasts in larval morphs among Bembrops species (Figs. 1-3) raises questions about the possible significance of the bubblemorph, a larval stage which disappears completely with metamorphosis. It is obvious that this unusual feature represents one of the extremes of larval specialization (Kendall, 1984). The term "larval bubblemorph" has rarely been used in early life history stud- ies. Marliave and Peden (1989) were the first to pay special attention to the significance of this peculiar morph, when they compared the ontogeny of two species of Liparis, one with and one without a distinct bubblemorph stage from various aspects, including adaptation strategy and phylogeny. They concluded that presence of a larval bubblemorph in Liparis is an adaptive, rather than a historical, feature, and therefore not indicative of relationships. So far as is known, larval bubblemorphs are restricted to several unrelated acanthomorph groups, Ceratoidei (Bertelsen, 1951), Cyclopteridae (Able et aI., 1984; Marliave and Peden, 1989), and Percophidae. Whereas there are differences in these morphs with respect to the extent of relevant specialization and the re- tention of gelatinous balloon-like skin after transformation, "stubby body with large and broad head" seems the necessary condition responsible for developing OKIY AMA: TWO TYPES OF LARV AL BEMBROPS 157

Figure 3. Pelagic larva and juvenile of Bembrops anatirostris collected from the central western Atlantic. A-B, Left lateral and dorsal view of larva, 6.3 mm SL; C, Left lateral view of juvenile, 9.4 mm SL (after Richards, 1990). the larval bubblemorph. It is natural to consider that this peculiar morph would compete with the formation of, at least, head spination which is among the most prominent and common larval characters (Kendall, 1984). Therefore, certain phylogenetic constraints may be associated with this ontogenetic event. It is of particular interest that two contrasting larval morphs are present in this monophyletic genus. Of course, the larval bubblemorph in Bembrops can be in- terpreted as a floating mechanism associated with the prolonged pelagic larval life, but it can also be considered suggestive of some phylogenetic meaning, although it remains to be determined if this remarkable larval morph is a syn- apomorphy due to indistinct relationships of the relevant two species. Interrelationships of the family Percophidae-According to Nelson (1994), CUf- rent systematics of the Percophidae are summarized as follows: Subfamily Percophinae Genus: Percophis Subfamily Bembropinae Genus: Bembrops*, Chrionema* Subfamily Hemerocoetinae 158 BULLETIN OF MARINE SCIENCE, VOL. 60, NO.1, 1997

Figure 4. Larvae and juveniles of the Percophidae. A, Chrionema cr. palllidum, 16.3 mm SL, collected from central Pacific near Tahiti; B, Matsubaraeafusiforme, 8,3 mm SL, collected from the Sea of Japan; C, Hemerocoetes sp., 16,0 mm SL (after Watson et aI., 1984); D, Spinapsaron sp" 12,2 mm SL, collected from the Sea of Japan; E, dorsal view of head of Spinapsaron sp.; F-G, lateral and dorsal views, respectively, of articular head of left maxillary of Spinapsaron sp. (arrowhead indicates snout spine).

Genus: Dactylopsaron, Enigmapercis, Matsubaraea*, Squamicreedia, Acan- thaphritis, Branchiopsaron, Hemerocoetes*, Osopsaron, Pteropsaron, Spi- napsaron* Generic confusion seems to exist in the Hemerocoetinae, because Suzuki and Nakabo(1995) consider Spinapsaron and Branchiosparon as possible junior syn- onyms of Acanthaphritis. In the review of ontogeny and systematics of the Trachinoidea, Watson et al. (1984) revealed the paucity of early life history data, including only a single larva of Hemerocoetes sp. from the Percophidae. Now, relevant information has in- OKIYAMA: TWO TYPES OF LARVAL BEMBROPS 159

Table 2. Summary of early life history (mostly pelagic juvenile) characters by genus in the Perco- phidae (compiled from Watson et aI., 1984; Mori, 1988; and this paper). Derived conditions are in bold.

Bembropinae Hemerocoelinae

Character Bembrops Chrionema Sp;napsaron Hemerocoetes Matsubaraea

Body shape stubby less stubby elongate elongate elongate Head large moderate, less small, small, less small depressed depressed depressed depressed depressed Larval bubblemoph present/absent absent? absent absent absent Snout spine absent absent present present present Opercular spine absent absent present absent absent Pelvic fin short elongate short short short Body pigmentation light heavy light light * Peritoneal pigment section present absent absent absent * Pelvic fin pigment present present absent absent * '"Means unavailable due to cleared material.

creased remarkably to cover five genera (Figs. 1, 2, 4) indicated by asterisks in the above list of systematics. Since most of the available specimens are pelagic juveniles, morphological comparisons among genera were mostly restricted to that stage (Table 2). In discussing relationships among five genera of the Percophidae, the Tricho- notidae and the Creediidae were tentatively selected as out groups, because these three families are considered to form a monophyletic assemblage, but with unclear associations among them (Pietsch and Zabetian, 1990; Johnson, 1993). Character states not shared with either of these out-group families (Leis, 1982; Leis and Rennis, 1983; Mori, 1988) were considered as derived for the Percophidae. With the exception of the opercular spine which is absent in the Trichonotidae and present and highly specialized in the Creediidae, all characters could be un- equivocally polarized based on the outgroup criterion. Of five genera, Bembrops and Chrionema have only autapomorphic specializations. The remaining three genera share synapomorphies, the presence of a snout spine and the pelvic fin pigmentation (except, perhaps, Matsubaraea whose pigmentation pattern was unavailable due to cleared material). As shown in Figure 4G, the snout spine is derived from the protruding articular head of the maxilla. Despite variable anlages of this spine, three genera of the Hemerocoetinae distinctly share it. Therefore, the division of this subfamily into two groups according to the presence or absence of the nasal spine in adults (the spine is absent in adult Matsubarae; Nelson, 1994) is not corroborated by the larval evidence. It may safely be said from the stand point of larval morphology that the Per- cophidae is a diverse, probably polyphyletic or paraphyletic group. Perhaps, the two genera included in the Bembropinae are more distantly related than previously considered. The two distinct larval morphologies in Bembrops suggest that two lineages may be present in that genus.

ACKNOWLEDGMENTS

I thank T. A. Clarke, J. M. Leis, T. Nagasawa, and T. Noichi for loaning us specimens in their care. W. J. Richards provided unpublished information on Bembrops anatirostris. Y. Kitagawa illustrated larva and juvenile of B. curvatura. M. Hara and Y. Tsukamoto helped me with the preparation of the manuscript. Critical comments from anonymous reviewers are particularly appreciated. 160 BULLETIN OF MARINE SCIENCE, VOL. 60, NO. I, 1997

LITERATURE CITED

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DATE ACCEPTED: April15, 1996,

ADDRESS: Ocean Research Institute, University of Tokyo, Minamidai 1-15-1, Nakano·ku, Tokyo 164, Japan.