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Early Ontogeny and Systematics of Bothidae, Pleuronectoidei

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Early Ontogeny and Systematics of Bothidae, Pleuronectoidei BULLETIN OF MARINE SCIENCE, 60(1): 192-212,1997 EARLY ONTOGENY AND SYSTEMATICS OF BOTHIDAE, PLEURONECTOIDEI Atsushi Fukui ABSTRACT Of the 20 bothid genera, larvae of the following 16 genera are presently known: Taeniop- settinae, (1) Taeniopsella, (2) Engyophrys, (3) Trichopsetta; Bothinae, (4) Parabothus, (5) Tosarhombus, (6) Crossorhombus, (7) Engyprosopon, (8) Bothus, (9) Grammatobothus, (10) Asterorhombus, (11) Psellina, (12) Lophonectes, (13) Arnoglossus, (14) Monolene, (15) Laeops, (16) Chascanopsetta, This study reviews the early ontogeny and systematics of bothids of the world. A cladistic analysis of 16 characters results in 25 equally parsimonious trees. A strict consensus tree for these 25 trees is shown. It has resolved two monophyletic groups and unresolved polytomy at basal nodes. The two monophyletic groups indicate that (1) Asterorhombu,\' and Engyprosopon except sp.2 of the subfamily Bothinae are sister group for the subfamily Taeniopsettinae, (2) Arnoglossus and Engyprosopon is not monophyletic, and (3) Taeniopsetta, Engyophrys, and Trichopsetta of the subfamily Taeniopsettinae are monophyletic. Fishes of the family Bothidae, suborder Pleuronectoidei, are very diverse, being comprised of 20 genera in two subfamilies, four in Taeniopsettinae and 16 in Bothinae (Amaoka, 1969; Ahlstrom et aI., 1984), The larvae of this family have a transparent, extremely compressed, body. The dorsal fin begins anterior to the eye, its second ray being elongated. The pelagic larvae are the largest among the pleuronectoid fishes, e.g., Chascanopsetta lu- gubris with 120-mm larvae, Many studies have been made on bothid larvae, e.g" Amaoka (1964, 1970, 1971a, 1972, 1973, 1974, 1976), Futch (1977), and Hensley (1977). Ahlstrom et aI. (1984) reviewed these studies. However, early development of bothids is still poorly understood, because the early and middle postlarvae are nearly unknown, After the publication by Ahlstrom et aI. (1984), Ozawa and Fukui (1986) made extensive studies on the early ontogeny of bothids based on numerous larvae collected in the western North Pacific, My present study reviews the early ontogeny and systematics of bothids of the world, and discusses phylogenetic information provided by larval characters. METHODS The larval period was divided into the following five stages: stage I, before flexion of notochord; stage II, until completion of notochord flexion or of caudal fin ray formation; stage IlIa, until disap- pearance of air bladder; stage IUb, until completion of right-eye migration to left side; stage IV, after metamorphosis, Metamorphosis is the period of right-eye migration. Morphometric measurements follow Ozawa and Fukui (1986). Definitions of the terms used in the present study are as follows: rostrum above snout, anterior projection of dorsal fin; interspine base of dorsal (anal) fin, along the dorsal (anal) edge of the epaxial (hypaxial) musculature; interspinous region of dorsal (anal) fin, region of dorsal (anal) fin pterygiophores. GENERAL FEATURES OF THE DEVELOPMENT OF BOTHID LARVAE Of the 20 bothid genera, the larvae of 16 are known (Table lA, B; Figs. 1-6). Larvae of four of the genera, Parabothus, Tosarhombus, Grammatobothus, and Asterorhombus, were identified after Ahlstrom et al. (1984). Early larvae (stages I or II) are known for the following 12 genera: Engyophrys and Trichopsetta in 192 FUKUI: ONTOGENY AND SYSTEMATICS OF BOTHIDAE 193 o o o 0 o ... w o 0 o o o 000 o o > > :r -'7 194 BULLETIN OF MARINE SCIENCE, VOL. 60, NO. I, 1997 o o o o o o 0.. <Il o o o 000 o 0 00 000 FUKUI: ONTOGENY AND SYSTEMATICS OF BOTHIDAE 195 Figure 1. Larvae of Bothidae. (A) Taeniopsetta ocel/ata, 59.0 mm SL, from Amaoka, 1970; (B) Trichopsetta ventralis, 21.9 rom SL, from Evseenko, 1982; (C) Engyophrys senta, 12.3 mm SL, from Hensley, 1977; (D) Asterorhombus sp. 1, 11.0 mm SL; (E) Asterorhombus sp. 2 7.80 mm SL; (F) Epiotic spines of Asterorhombus (left, A. sp. 1; right, A. sp. 2). Taeniopsettinae; Crossorhombus, Engyprosopon, Bothus, GrammatobiJthus, As- terorhombus, Psettina, Amoglossus, Monolene, Laeops, and Chascanopsetta in Bothinae. General features of bothid larvae are summarized below. Bothid larvae have a body that is very laterally compressed and deep to fairly slender and long dorsal and anal fin bases with many slender rays. The dorsal fin origin is anterior to the eyes and its second ray becomes elongated in stages I ]96 BULLETIN 0 F MARINE SCIENCE , VOL ,60, NO, I, 1997 Figure 2 L . arvae of B th' fiI E ]4.] mm SL- 0 Idae. (A) En SL; (F) E, s~. ~~)9~Om;:~is:~~ma,, (G) Grammatobothus14.!:r::;:o:~~ lb~r;iSqUama,. sp. 1, 19.54.08mmmmSL'SL'(~)Bk . grandisquama sp., 10.5 mm SL; (H) G. sp., 27.1. sp. mm2, 9.54SL. m~ FUKUI: ONTOGENY AND SYSTEMATICS OF BOTHIDAE 197 Figure 3. Larvae of Bothidae. (A) Crossorhombus kobensis, 2.88 mm SL; (B) C. kobensis, 15.4 mm SL; (C) C. azureus (=kanekonis), 15.1 mm SL; (D) Lophonectes gallus, 18.5 mm SL, from Ahlstrom et al. 1984; (E) Psettina gigantea, 18.0 mm SL; (F) P. iijimae. 28.0 mm SL; (G) P. tosana, 3.12 mm SL; (H) P. tosana, 23.2 mm SL. 198 BULLETIN OF MARINE SCIENCE. VOL. 60. NO. I. 1997 Figure 4. Larvae of Bothidae. (A) Bothus myriaster, 8.90 mm SL; (B) B. myriaster 23.8 mm SL; (C) B. pantherinus, 32.0 mm SL; (D) B. mancus, 24.6 mm SL; (E) B. oceLlatus, 16.2 mm SL. from Evseenko. 1976; (F) Tosarhombus octoculatus, 26.7 mm SL. and II. The mouth is small and the eyes are elliptical, generally small and sub- tended by a lunate choroid tissue. The urohyal is widely exposed and the posterior basipterygial process is slender and borders the lower part of the abdominal cavity. Most of the abdominal cavity is filled with the gut and liver. The pelvic fin is FUKUI: ONTOGENY AND SYSTEMATICS OF BOTHIDAE 199 Figure 5. Larvae of Bothidae. (A) Arnoglossus tenuis, 24.0 mm SL; (B) A. japonicus, 34.6 mm SL; (C) A. yamanakai, 8.00 mm SL; (D) A. yamanakai, 49.0 mm SL; (E) A. sp. 1, 39.2 mm SL; (F) A. sp. 2, 35.0 mm SL; (G) A. debilis, ca. 59 mm SL, from Ahlstrom et al. 1984; (H) A. [aterna, 16 mm SL, from Russell, 1976. supported by a triangular cartilaginous anterior basipterygial process between the urohyal and posterior basipterygial process. After pelvic fin rays develop, those in the left fin move anteriorly to the fixed adult position, the first ray of the right fin being opposite to the second one of left fin in Taeniopsettinae, and to third or fourth (rarely second) in Bothinae. In 10 genera, minute short spines are devel- 200 BULLETIN OF MARINE SCIENCE, VOL. 60, NO. I, 1997 Figure 6, Larvae of Bothidae. (A) Monolene sessilicauda, 14,3 mm SL, from Futch, 1971; (B) Laeops nigromaculatus, 56.6 mm SL; (C) L. kitaharae, 5,00 mm SL; (D) L. kitaharae, 64,5 mm SL; (E) Chascanopsetta lugubris lugubris, 8,20 mm SL; (F) C. lugubris lugubris, 66,8 mm SL; (G) C. micrognathus, ]0,8 mm SL; (H) Parabothus sp., 22,8 mm SL, from Tsukamoto et aI., 1991. FUKUI: ONTOGENY AND SYSTEMATICS OF BOTHIDAE 201 oped on the posterior basipterygial process, urohyal, cleithrum, and epiotic. Body melanophores are generally absent or small. The air bladder disappears during development. During metamorphosis, the right eye migrates through a slit or hole formed below the origin of the dorsal fin base. Size at metamorphosis ranges from 13 to 125 mm, being the largest in the Pleuronectiformes. Many changes occur rapidly during metamorphosis, differentiation of pecrtoral fin rays, degeneration of spines, and appearance of many melanophores, etc. (Ozawa and Fukui, 1986: 334). Among the above characters, the extremely compressed body, elongated second dorsal fin ray in stages I and II, elliptical eye with choroid tissue, and asymmetric pelvic fin placement are the diagnostic characters for bothid larvae. Larval char- acters of the Bothidae are summarized in Table 2. Features of GenUs.-TAENIOPSETT1NAE.In the taeniopsettine genera, spines are developed on the posterior basipterygial process, urohyal, cleithrum, and epiotic. References are shown in Table 1. Taeniopsetta Gilbert Larvae of stages llIb and IV of T. ocellata and T. radula are known. Diagnosis.-Body oval; three epiotic spines; masses of melanophores present on left side of body after end of stage llIb (about 60 mm SL); elongated dorsal fin ray short; metamorphosis occurring at about 60 mm SL; vertebrae 10 + 32-33 = 42-43. Engyophrys Jordan et Bollman The early ontogeny of E. senta and E. sancti-Iaurentii is known. Diagnosis.-Body oval in stages II-IIIb; three or four epiotic spines until 8 mm SL, four after 8 mm SL; melanophores present on head, urohyal, and ventral margin of intestinal coiling only in stage I; elongated dorsal fin ray becomes short after about 10 mm SL; metamorphosis occurring at about 20 mm SL; vertebrae 10 + 27-31 = 37-41. Trichopsetta Gill The early ontogeny of T. ventralis is known. Diagnosis.-Body oval in stage IlIa; two or three epiotic spines until 16 mm SL, three after 16 mm SL; masses of melanophores present on interspinous regions of dorsal and anal fins, and on midlateral line after 17 mm SL; elongated dorsal fin ray remains until about 21 mm SL; largest collected larvae 29 mm SL; ver- tebrae 10-11 + 30-33 = 40-43. Features of the Genus Bothinae Parabothus Norman Larvae of stage IIIb referable either to P. coarctatus or P. kiensis are known. Diagnosis.-Body moderately slender; rostrum above snout developed; spines present on posterior basipterygial process and urohyal; melanophores absent; sec- ond to 11th dorsal fin rays elongated; largest collected larvae 23mm SL; vertebrae 10 + 30-36 = 40-46.
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