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Osteological Development of Wild-Captured Larvae and a Juvenile Sebastes Koreanus (Pisces, Scorpaenoidei) from the Yellow Sea Hyo Jae Yu and Jin-Koo Kim*

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Osteological Development of Wild-Captured Larvae and a Juvenile Sebastes Koreanus (Pisces, Scorpaenoidei) from the Yellow Sea Hyo Jae Yu and Jin-Koo Kim* Yu and Kim Fisheries and Aquatic Sciences (2016) 19:20 DOI 10.1186/s41240-016-0021-0 RESEARCH ARTICLE Open Access Osteological development of wild-captured larvae and a juvenile Sebastes koreanus (Pisces, Scorpaenoidei) from the Yellow Sea Hyo Jae Yu and Jin-Koo Kim* Abstract The osteological development in Sebastes koreanus is described and illustrated on the basis of 32 larvae [6.11–11.10 mm body length (BL)] and a single juvenile (18.60 mm BL) collected from the Yellow Sea. The first-ossified skeletal elements, which are related to feeding, swimming, and respiration, appear in larvae of 6.27 mm BL; these include the jaw bones, palatine, opercular, hyoid arch, and pectoral girdle. All skeletal elements are fully ossified in the juvenile observed in the study. Ossification of the neurocranium started in the frontal, pterotic, and parietal regions at 6.27 mm BL, and then in the parasphenoid and basioccipital regions at 8.17 mm BL. The vertebrae had started to ossify at ~7.17 mm BL, and their ossification was nearly complete at 11.10 mm BL. In the juvenile, although ossification of the pectoral girdle was fully complete, the fusion of the scapula and uppermost radial had not yet occurred. Thus, the scapula and uppermost radial fuse during or after the juvenile stage. The five hypurals in the caudal skeleton were also fused to form three hypural elements. The osteological results are discussed from a functional viewpoint and in terms of the comparative osteological development in related species. Keywords: Sebastes koreanus, Korean fish, Larvae, Juvenile, Osteological development Background Sebastes koreanus Kim and Lee 1994, in the family Osteological development in teleost fishes involves a Scorpaenidae (or Sebastidae sensu Nakabo and Kai sequence of remarkable morphological and functional 2013), is smaller than its congeneric species and is changes, occurring in different developmental stages regarded as endemic to the Yellow Sea (Kim and Lee (Löffler et al. 2008; Kang et al. 2012; Ott et al. 2012). 1994; Kim et al. 2005; Choi and Yang 2008). The species These ontogenetic changes strongly influence the feed- may be a good model fish with which to understand the ing, breathing, and swimming behaviors of both larvae phylogenetic relationships within the suborder Scorpae- and juveniles, and are therefore useful in functional and noidei, because the species is specifically adapted to ecological analyses and as a basis for phylogenetic infer- the unique marine environment of the Yellow Sea. ences about relationships among teleost taxa (Omori Comparisons of S. koreanus with other Sebastes species et al. 1996; Faustino and Power 1999; Koumoundouros have shown that S. koreanus collected in the wild exhibit et al. 2000, 2001a, b; Liu 2001; Lima et al. 2013; wide ontogenetic variations in their pigmentation patterns Voskoboinikova and Kudryavtseva 2014). Practically and in their head–spine development (Yu et al. 2015). speaking, an accurate knowledge of skeletal development In addition, the restricted distribution of the species is essential for the detection and elimination of skel- makes populations susceptible to collapse as a conse- etal deformities appearing during artificial seedling quence of environmental pollution and/or the influence of production and to promote effective aquacultural and climate change on the Yellow Sea. In this respect, resource management (Koumoundouros et al. 1997a, b). artificial seedling production presents a viable approach to the conservation of susceptible species. However, no studies have yet been conducted on the details of skeletal * Correspondence: [email protected] development in S. koreanus, except for studies of mor- Department of Marine Biology, Pukyong National University, 45, phological development and parturition season (Yu et al. Yongso-roNam-gu, Busan 608-737, South Korea © 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Yu and Kim Fisheries and Aquatic Sciences (2016) 19:20 Page 2 of 12 2015) and a small study of osteological development larvae (8.44–11.10 mm BL, n = 11; PKUI 388–398), and of reared larvae and juveniles in the Korea Strait a juvenile (18.60 mm BL, n = 1; PKUI 21). (Park et al. 2015). Also, we confirmed some differences in osteological development of S. koreanus when compared Results with reared larvae (Park et al. 2015) and wild-captured The osteological development of S. koreanus at vari- larvae from the Yellow Sea. Therefore, in this study, we ous developmental stages was described in the follow- describe in detail the early skeletal development of S. ing skeletal regions: neurocranium, jaw bones, palate koreanus in the context of functional changes, based series, opercular series, hyoid arch, pectoral girdle, on wild-captured larvae and juvenile. We also compare infraorbital bone, caudal skeleton, and vertebrae. The the osteological development of S. koreanus with that development results are summarized in Table 1. of congeneric species. Neurocranium Methods The development and ossification of the neurocranium All individuals were collected from the eastern margin for individuals at different developmental stages are of the Yellow Sea. Larvae of S. koreanus [6.11–11.10 mm illustrated in Figs. 1 and 2. In the smallest larvae body length (BL), n = 32] were collected off the Taean (6.11 mm BL; preflexion stage), no skeletal structures of Peninsula in May 2011 using a bongo net (0.6 m mouth the neurocranium were visible. Ossification of the opening, with 330 and 500 μm mesh size; bottom depth neurocranium started at 6.27 mm BL, with ossification 15–24 m). The juvenile of S. koreanus (18.60 mm BL, of the parietal, frontal, and pterotic bones (Fig. 1a); n = 1) was collected off Gang-hwa-do in July 2012 ossification of these elements appeared to begin at the using a stow net. The individuals were preserved in tips of the spines. In the 7.11 mm BL larva, the skeletal 5 % formalin immediately after collection. The speci- elements that had appeared in earlier stages continued mens fixed in formalin were washed with distilled to ossify, but no ossification of additional elements water and then preserved in 99 % ethanol. Before was observed (Fig. 1b). At 8.11 mm BL, the posterior staining, each sample was identified according to the of the parasphenoid and the anterior of the basiocci- morphological characteristics of Yu et al. (2015), pital had started to ossify, and the two elements were which were measured to the nearest 0.01 mm with joined. At the same time, the exoccipital began to ossify the stereomicroscope (Olympus SZX16, Japan). The along its posterior margin (Fig. 1c). At 9.06 mm BL, methods of measurement followed Leis and Carson-Ewart ossification of the frontal had extended to the dorsal (2000). The measured body parts included BL and area of the neurocranium, and then the frontal boundary total length (TL). The anatomical terminology relating line joined the parietal. In addition, the supraoccipital, to skeletal structures follows Russell (1976), and the sphenotic, and prootic elements had started to ossify terminology of developmental stages follows Kim et al. along their margins at this stage (Fig. 1d). At 10.20 mm (2011). The skeletal staining technique was derived BL, the lateral ethmoid had started to ossify along its from the double staining protocol of Darias et al. dorsal margin, and the parietal, pterotic, parasphenoid, (2010). After staining, the specimens were examined and basioccipital were almost fully ossified (Fig. 2a). on their right and dorsal sides with a stereomicro- At 11.10 mm BL, ossification of the frontal had extended scope and photographs taken with a camera lucida to most regions and ossification of the sphenotic and (Olympus SZX-DA, Japan) attached to the microscope. supraoccipital was complete. The epiotic, which appeared Drawings of the different skeletal parts were prepared relatively late compared with the other neurocranial from the photographs. We compared the skeletal elements, had started to ossify at this stage (Fig. 2b), and structures of the larvae and the juvenile with those of the vomer and medial ethmoid appeared simultaneously adult S. koreanus specimens, to observe the precise along their anterior margin. At this stage, although all locations and shapes of the skeletal elements. We also the elements of the neurocranium had started to ossify, compared stained specimens with a stained Sebastes some elements continued to ossify. In the juvenile inermis complex juvenile (17.06 mm BL, n = 1) collected stage (18.60 mm BL), the ossification of the neurocranium in the wild. The stained specimens were preserved in was fully complete (Fig. 2c). 100 % glycerin in glass bottles and were deposited at Pukyong National University (PKU). Jaw bones, palatine, and opercular series The development and ossification of the jaw bones, Materials examined palatine, and opercular series for individuals at differ- The examined materials included preflexion larvae ent developmental stages are illustrated in Fig. 3. No (6.11–6.27 mm BL, n = 2; PKUI 367–368), flexion larvae skeletal structures were visible in the smallest preflexion (6.43–8.40 mm BL, n = 19; PKUI 369–387), postflexion larva (6.11 mm BL). At 6.27 mm BL, the maxillary Yu and Kim Fisheries and Aquatic Sciences (2016) 19:20 Page 3 of 12 Table 1 Developmental sequence of ossification in Sebastes and premaxillary had both begun to ossify at their koreanus anterior and ventral margins, respectively (Fig.
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