Early osteological development of the fins in the hatchery-reared red porgy,Pagrus pagrus(L. 1758)

Abstract

Journal of Applied IchthyologyVolume 25, Issue 1 p. 26-32 Free Access Early osteological development of the fins in the hatchery-reared red porgy, Pagrus pagrus (L. 1758) D. Çoban, D. Çoban Faculty of Fisheries, Department of Aquaculture, Ege University, Bornova, Izmir, TurkeySearch for more papers by this authorC. Suzer, C. Suzer Faculty of Fisheries, Department of Aquaculture, Ege University, Bornova, Izmir, TurkeySearch for more papers by this authorH. O. Kamaci, H. O. Kamaci Faculty of Fisheries, Department of Aquaculture, Ege University, Bornova, Izmir, TurkeySearch for more papers by this authorŞ. Saka, Ş. Saka Faculty of Fisheries, Department of Aquaculture, Ege University, Bornova, Izmir, TurkeySearch for more papers by this authorK. Firat, K. Firat Tire Kutsan Vocational School, Ege University, Tire, Izmir, TurkeySearch for more papers by this author D. Çoban, D. Çoban Faculty of Fisheries, Department of Aquaculture, Ege University, Bornova, Izmir, TurkeySearch for more papers by this authorC. Suzer, C. Suzer Faculty of Fisheries, Department of Aquaculture, Ege University, Bornova, Izmir, TurkeySearch for more papers by this authorH. O. Kamaci, H. O. Kamaci Faculty of Fisheries, Department of Aquaculture, Ege University, Bornova, Izmir, TurkeySearch for more papers by this authorŞ. Saka, Ş. Saka Faculty of Fisheries, Department of Aquaculture, Ege University, Bornova, Izmir, TurkeySearch for more papers by this authorK. Firat, K. Firat Tire Kutsan Vocational School, Ege University, Tire, Izmir, TurkeySearch for more papers by this author First published: 16 February 2009 https://doi.org/10.1111/j.1439-0426.2008.01165.xCitations: 7 Author’s address: Deniz Çoban, Faculty of Fisheries, Department of Aquaculture, Ege University, TR-35100 Bornova, Izmir, Turkey.E-mail: deniz.coban@ege.edu.tr AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Summary The present study was undertaken to establish the normal, healthy features of morphological structures at various developmental stages as achieved under well-defined environmental culture conditions (temperature between 16 and 21°C, salinity 36 ppt, pH around 7.6, and oxygen saturation over 95%) common in aquaculture of the species. The pectoral fin supports began to develop at 2.90 mm total length (TL), followed by those of dorsal fins at 5.5 mm TL, caudal fins at 5.6 mm TL, pelvic fins at 5.9 mm TL and anal fins at 6.0 mm TL. The pelvic fins appeared fully at 7.4 mm TL. Development of dorsal lepidotrichia was first observed at 6.9 mm TL, attaining their final number at 7.6 mm TL. The dorsal spines first appeared at 6.5 mm TL and were complete at 7.4 mm TL. The anal lepidotrichia appeared during the development phase from 6.8 to 8.6 mm TL. At 5.6 mm TL, the upward flexion of the urostyle was initiated. The caudal lepidotrichia formed within the primordial fin at 5.6 mm TL and reached the final count at 7.4 mm TL. The caudal dermatotrichia first appeared at 7.3 mm TL and all forms were observed by 15.5 mm TL. The development pattern of fin supports found in Pagrus pagrus is quite similar to that described for other Sparid species. Introduction The red porgy, Pagrus pagrus, is a promising candidate species in marine aquaculture. It is a commercially important demersal marine sparid found in the Mediterranean Sea, in the eastern Atlantic from the British Isles to Senegal, and in the western Atlantic from North Carolina to Mexico and from Venezuela to Argentina (FAO, 1973; Manooch and Huntsman, 1977). In commercial fisheries, the red porgy is highly appreciated for its appearance and meat quality. This, together with a growing concern on over-fishing of this species (Vaughan and Prager, 2002), makes red porgy a very suitable candidate for aquaculture (Van der Salm et al., 2004). A close relative, the red sea bream (Pagrus major), has been cultured successfully for many years in Japan, where it is the most important cultured species of the Sparidae family (Foscarini, 1988; Watanabe and Kiron, 1995). The ontogeny of fish is the most vulnerable time of their lives, in both wild and culture conditions. The entire life cycle of an organism reflects environmental conditions during early ontogeny. Different meristic characters are common among individual fish in the same population, even among young obtained from the same parents when embryos or larvae are exposed to different environmental conditions (Lindsey, 1988; Blaxter, 1992). Knowledge of the developmental osteology of a species is important not only from the embryological point of view but also for fisheries biology and aquaculture (Koumoundouros et al., 2000). In fish culture, precise developmental knowledge is a prerequisite for the early detection and elimination of skeletal deformations common under rearing conditions (Divanach et al., 1996, 1997; Koumoundouros et al., 1997a,b). Numerous studies relate to the osteology of sparids such as Pagrus major (Matsuoka, 1982, 1985), Pagellus erythrinus (Sfakianakis et al., 2004), Dentex dentex (Koumoundouros et al., 1999, 2001a), Sparus aurata (Koumoundouros et al., 1997a; Faustino and Power, 1998, 1999), Diplodus sargus (Koumoundouros et al., 2001b), Diplodus puntazzo (Sfakianakis et al., 2005), whereas there are no published studies on the osteological development of P. pagrus. The aim of the present study was to describe the development of ontogeny of the pelvic, dorsal, anal, caudal, and pectoral fins in red porgy, P. pagrus, under intensive culture conditions for later use as a reference tool in assessing larval quality. Materials and methods Larval rearing Pagrus pagrus broodstocks were selected from wild breeders. They were fed frozen cuttlefish (Sepia officinalis) and prawn (Palaemon elegans) as a daily primary food source. Broodstocks were maintained at the local photoperiod and temperature conditions (38°92′N; 27°05′E). Maturation and spawning occurred spontaneously. Eggs were incubated in 50-L incubators at an initial stocking density of 1500 eggs L−1 with a gentle flow of seawater. Larval rearing was carried out in a closed seawater system. Initial stocking density was 100 larvae L−1 in a cylindrical tank (6 m3). During the larval period, oxygen saturation was 95%, salinity 36 ppt, photoperiod 24 h−1 (100 lx), and pH 7.6. Water temperature range during the embryonic and yolk-sac larval stage was altered from 16 to 17°C and then varied between 20 and 21°C in later stages. Larvae were fed three times daily from day 4 (when the mouth opened) to day 15 with rotifers (Brachionus rotundiformis and Brachionus plicatilis) cultured with algae and enriched (DHA Protein Selco; Artemia Systems SA, Ghent, Belgium) at a density of 10–15 ind ml−1. The microalgae Isochrysis galbana and Tetraselmis suecica were supplied from days 3 to 26 each morning to achieve an initial concentration of 30–35 × 104 cells ml−1. From days 8 to 46, larvae were fed three times daily with Artemia nauplii (AF 480 INVE Aquaculture) and Artemia metanauplii at 0.5–1.5 ind L−1. From day 32, a commercial powdered dry diet was administered with a ratio ranging from 3% to 8% body weight. Larval rearing conditions and growth are schematized in Fig. 1. Figure 1Open in figure viewerPowerPoint Growth, temperature (°C) and feeding regime of Pagrus pagrus (□, standard deviation; —, mean; , maximum; ⊥, minimum) Sampling and staining Development of the fin was conducted on samples of minimum 30 specimens per every third day during the larval stages (days 1–46; Table 1). Larvae were anaesthetized with ethylenglycol-monophenylether (Merck, 0.2–0.5 ml L−1; Koumoundouros et al., 1999) and fixed in phosphate-buffered 10% formalin (pH 7.4) for 24–48 h (Taylor and Van Dyke, 1985). Specimens were immediately processed or preserved in 100% ethanol for later use. Staining procedures followed those of Pothoff (1984). The following procedures were carried out: Table 1. Days after hatching (DAH), number of sampled larvae, total length (TL) mean ± SD and total length range in Pagrus pagrus DAH n TLmean+SD Range (mm) 1 113 3.09 ± 0.09 2.86–3.26 4 56 3.61 ± 0.88 3.50–3.85 7 64 4.05 ± 0.82 3.84–4.14 10 61 4.23 ± 0.19 3.77–4.61 13 106 4.32 ± 0.29 3.94–4.98 16 121 4.95 ± 0.26 4.54–5.72 19 46 5.12 ± 0.31 4.50–5.82 22 50 5.58 ± 0.42 4.99–6.87 25 74 6.06 ± 0.69 4.75–7.55 28 46 6.24 ± 0.56 5.27–7.37 31 72 7.72 ± 0.80 6.03–9.37 34 37 8.22 ± 0.63 7.13–9.39 37 31 10.40 ± 1.09 9.21–12.17 40 34 13.07 ± 1.55 9.30–15.34 43 35 14.72 ± 1.16 12.01–16.10 46 41 15.84 ± 1.32 13.77–17.85 (i) Dehydration for 2 days (50% distilled H2O, 50% of 95% ethanol). (ii) Cartilage staining for 1 day (70 ml absolute ethanol, 30 ml acetic acid, 20 mg alcian blue). (iii) Neutralization for half a day (sodium borate). (iv) Bleaching for 40 min (15 ml 3% H2O2, 85 ml 1% KOH). (v) Trypsin in a solution until 60% clear (35 ml sodium borate, 65 ml H2O, trypsin powder). (vi) Bone-staining for 1 day (1% KOH with alizarin red S). (vii) Destaining for 2–4 days (35 ml sodium borate, 65 ml H2O, trypsin powder). During the study, 987 larvae were stained individually; deformed larvae were not analysed. TL measurements were carried out from the first day after hatching (DAH) to 46 DAH before fixation of individuals to the nearest 0.01 mm. The TL at which more than 50% of the individuals displayed a certain characteristic was used as the reference point in the description of the ontogeny. The anatomical terminology relating to the skeletal structures was followed as described by Houde and Potthoff (1976), Matsuoka (1985, 1987), Balart (1995) and Koumoundouros et al. (2001a,b) to determine the skeleton systems of the red porgy larvae. Results Developmental sequences of all fin supports and rays against total length in P. pagrus are shown in Fig. 2. Figure 2Open in figure viewerPowerPoint Developmental sequence of fin supports and rays in Pagrus pagrus. Stippled bar, appearance of cartilaginous element. Solid bar, appearance of ossified bone or beginning of ossification of cartilaginous element. Δ full complement of elements Development of pectoral fin supports The pectoral girdle was the first fin support to develop in P. pagrus. The ontogeny of the pectoral fins started at the yolk-sac larval stage with formation of the cleithrum (Cl). The needlelike cleithrum and coracoid (Co)–scapula (Sca) complex were present at 2.90 mm TL, and the cartilaginous fin plate closely followed. At this period, the coracoid–scapula and fin plate were in close contact with each other. At 3.5 mm TL the cartilaginous fin plate had separated from the coracoid–scapula complex and a crevice had developed in the anterior mid-region of the fin plate. The coracoid and scapula commenced ossifying on the primordial coracoid–scapula cartilage at 8.0–8.4 mm TL, respectively. The second and third crevices were present at 6.1 and 6.3 mm TL, respectively. Propterygium formed above the fin plate cartilage at 6.5 mm TL. Distal radials and rays were visible as was the scapular foramen and the lower ossified post-cleithrum. The four proximal pterygiophores (Prx) were formed in a ventrad direction on the primordial fin plate at 7.3, 7.5, 7.9 and 8.1 mm TL, respectively. The ossification of proximal pterygiophores began at 9.5 mm TL with Prx1, whereas the last to begin ossifying was Prx4 at 13.9 mm TL. The pectoral lepidotrichia developed at 6.5 mm TL, simultaneously with appearance of the propterygium cartilage. The lepidotrichia attained a final count of 14–16 at 11.2 mm TL. The first distal radials appeared at 6.3 mm TL and the final radial at 14.6 mm TL. Hypercleithrum formed at 4.9 mm TL followed by the post-temporal and the lower metacleithrum at 6.0 mm TL. The upper metacleithrum and lower extrascapula appeared at 7.2 and 14.1 mm TLs, respectively. The pectoral fin complex was completely formed at 14.66 mm TL (Fig. 3a). Figure 3Open in figure viewerPowerPoint Osteological features of (a) pectoral fin at 14.66 mm TL, (b) pelvic fin at 15.35 mm TL. Suc, Hypercleithrum; PocUp, Metacleithrum upper; Sca, Scapula; ScF, Scapular foramen; PocLo, Metacleithrum lower; Cl, Cleithrum; Co, Coracoid; Prx, Proximal radial; Rd, Distal radial; S, Hard spine; R, Lepidotrichia; Bp, Basipterygium. Scale bars indicate 1.0 mm Development of pelvic fin supports The basipterygium (Bp), located behind the pectoral girdle, gradually elongated in an anterior direction towards the cleithrum at 5.9 mm TL. The metapterygium developed as a small cartilaginous structure at 9.2 mm TL. Basipterygium ossification began at 9.0 mm TL. The lepidotrichia and spine first appeared at 7.4 mm TL and the tip of the basipterygium approached the cleithrum at 7.8 mm TL. Development of the pelvic fin was completed at 15.35 mm TL and was also observed as not fully ossified (Fig. 3b). Development of dorsal fin supports Development of the dorsal fin is illustrated in Fig. 4a–d. At 5.5 mm TL, three cartilaginous proximal radials (Prx) were visible dorsally (Prx2–Prx4) (Fig. 4a). The proximal radials developed in the caudal direction and by 7.5 mm TL all were formed (20–21 count); their ossification was first observed at 9.4 mm TL, and developed from the anterior to posterior. Predorsal (Prd 1) cartilage appeared in front of the proximal pterygiophores at 5.6 mm TL. The Prd 2 formed at 6.1 mm TL, followed by Prd 3 (6.4 mm TL). Their ossification began at 9.5 mm TL and was completed at 12.5 mm TL. Distal radial (Rd) first formed at 6.5 mm TL (Rd 1–3) and was completed at 7.8 mm TL. The cartilaginous distal radial began to ossify by 10.0 mm TL (Rd 1–4), but was still incompletely ossified at 17.9 mm TL. Development of the lepidotrichia (R) was first observed at 6.9 mm TL, attaining their final number (11–12 R) at 7.6 mm TL. Dorsal spines first appeared at 6.5 mm TL and were completely formed by 7.4 mm TL. Only the first proximal radial was supported by two spines. Three transitory elements appeared during the ontogeny of the dorsal fin. A cartilaginous process formed anterior to the proximal radial 1 at 6.8 mm TL, fusing to it to form one continuous element at 7.9 mm TL. The cartilage formed as a separate element posterior to the last proximal radial at 8.5 mm TL; these two elements fused at 10.1 mm TL. At 9.2 mm TL, the other separate cartilaginous element formed dorsally to the proximal radial 1 and fused with it at 10.3 mm TL. Figure 4Open in figure viewerPowerPoint Osteological features of anal, dorsal and caudal fins. (a) 5.5 mm TL; (b) 6.7 mm TL; (c) 8.2 mm TL; (d) 15.5 mm TL. Prx, Proximal radial; Rd, Distal radial; R, Lepidotrichia; Na, Neural arch; “Na” Specialized neural arch; SCR, Caudal dermatotrichia; PCR, Caudal lepidotrichia; Ep, Epural; Hy, Hypural; Ac, Accesory cartilage; Ur, Urostyle; Ha, haemal arch; PrH, parahypural; Pp, Parapophysis; Dr, Dorsal rib. Scale bars indicate 1.0 mm Development of anal fin supports Development of the anal fin is shown in Fig. 4a–d. The first proximal radials (Prx1) developed at 6.0 mm TL and all of them were formed by 6.8 mm TL. The ossification started with Prx1 at 7.2 mm TL and followed caudally. A cartilaginous process formed anterior to Prx1 at 6.9 mm TL and soon fused with it, forming one continuous element. Another separate cartilaginous element formed ventrally to Prx1 at 7.3 mm TL. The distal radial was first observed at 6.2 mm TL. Full formation of the distal radial was completed at 7.5 mm TL and ossification began at 10.6 mm TL with the first distal radial. Lepidotrichia development appeared during the development phase from 6.8 to 7.6 mm TL, whereas the hard spines followed them. The Prx had three spines at 8.2 mm TL. Cartilage formed at 6.9 mm TL and fused to the last proximal radial at 10.2 mm TL. Development of caudal fin supports Development of the anal fin is shown in Fig. 4a–d. The notochord was straight in the yolk-sac and early larval stages of red porgy. The flexion of the notochord was observed at 5.6 mm TL. Development of the caudal complex was closely related to the flexion of the notochord. Hypural 1 (Hy) was the first visible element, appearing in a cartilaginous form in the preflexion stage at 4.7 mm TL, followed by hypural 2 at 4.9 mm TL, parhypural and hypural 3 at 5.1 mm TL, and hypural 4 at 5.4 mm TL. Hy1 and Hy2 were fused at their bases at 6.3 mm TL and subsequently with parhypural at 7.1 mm TL. The last cartilaginous bone, hypural 5, was observed at 7.6 mm TL. Epural 2 appeared at 5.2 mm TL and followed epural 1 and 3 at 5.6 mm TL. At this stage, the upward flexion of the urostyle was initiated and the caudal lepidotrichia formed within the primordial fin. The caudal lepidotrichia reached a final count at 6.7 mm TL. Dermatotrichia first appeared at 7.4 mm TL and all were formed by 15.5 mm TL. Uroneural 1 and uroneural 2 developed at 12.2 and 15.3 mm TLs, respectively. Ossification of hypural 1 started at 7.2 mm TL and followed Hy2 at 7.4 mm TL, Hy3 at 7.5 mm TL, parhypural at 7.6 mm TL, Hy4 at 8.3 mm TL, and Hy5 at 15.3 mm TL. Hy1–Hy4 and the parhypural were fully ossified by 17.7 mm TL. Discussion In the current study, we investigated the osteological development of fins (pectoral, pelvic, anal, dorsal, and caudal) examined in P. pagrus during early life development under culture conditions. It is commonly known that teleostei present a remarkable variability in respect to the developmental stage of the skeleton at hatching (Koumoundouros et al., 2001a). Additionally, skull and fin developments were observed in the Sparidae family after hatching (Matsuoka, 1985; Koumoundouros et al., 1997b, 2000, 2001a; Faustino and Power, 2001; Sfakianakis et al., 2004, 2005; present paper), whereas these were determined before hatching in Salmonidae (Kendall et al., 1984). Also, skeletal development in P. pagrus larvae was observed after hatching at 2.90 mm TL and compared with formation of the cleithrum and coracoid–scapula in D. dentex (Koumoundouros et al., 2001a), D. sargus (Koumoundouros et al., 2001b), S. aurata (Faustino and Power, 2001) and P. erythrinus (Sfakianakis et al., 2004). The cleithrum contributes to feeding functions, as it supports the sternohyoideus muscle, which is involved in opening the mouth (Matsuoka, 1987). Exploration of the food is mainly dependent on both prey localization and predator avoidance and presupposes the development of locomotive ability (Koumoundouros et al., 2001a). Also, the swimming of the larvae is initially carried out by movements of the primordial marginal finfold, assisted by the early-developed pectoral fin plates (Webb and Weish, 1986). The propulsive forces of the caudal part of the body increase as a result of the development of the corresponding fin (Matsuoka, 1987). These two developmental stages cause non-complex larval movements, thus carrying out vital functions for survival and feeding of larvae in early life development. While the caudal fin was formed for the first time in P. pagrus larvae, similar findings were reported in previous studies for Sparid species such as P. major (Matsuoka, 1982, 1985), P. erythrinus (Sfakianakis et al., 2004), D. dentex (Koumoundouros et al., 2000, 2001a), S. aurata (Koumoundouros et al., 2001a,b; Faustino and Power, 1999), D. sargus (Koumoundouros et al., 2001b) and D. puntazzo (Sfakianakis et al., 2005). Nevertheless, important differences were found in the profile of osteological development in the Sparidae family, depending on the size (in mm TL; Fig. 5). Although the ontogenic development of fins in P. erythrinus larvae was relatively faster than in the other Sparid fishes (Sfakianakis et al., 2004), pectoral and pelvic fin development were relatively slower (Fig. 5). Additionally, P. pagrus, P. erythrinus and P. major are similar in terms of morphological characteristics; however, formation and development-time of fins were different (Fig. 5). It is thought that one of the main factors affecting osteological development is the temperature of the culture water together with biological characteristics and requirements of larvae. Clearly, as commonly known, growth, notochord and fin development are relatively faster in higher water temperatures than in lower temperatures (Fuiman et al., 1998; Koumoundouros et al., 2001c). Figure 5Open in figure viewerPowerPoint Comparative diagram of the completion of caudal lepidotrichia, of dorsal and anal spines and lepidotrichia, of pectoral and pelvic lepidotrichia in Pagellus erythrinus (Sfakianakis et al., 2004; 21.0°C), Dentex dentex (Koumoundouros et al., 1999, 2001a,b,c; 16.9 ± 0.3 °C and 23.3 ± 0.5°C), Sparus aurata (Faustino and Power, 1999; 19.0 ± 1.0°C), Pagrus major (Matsuoka, 1985), Diplodus puntazzo (Sfakianakis et al., 2005; 21.4 ± 1.8°C), Diplodus sargus (Koumoundouros et al., 2001a,b,c; 22.0 ± 1.0°C) and Pagrus pagrus (Presented paper). , completion of the above meristic characters was present In teleost larvae, dorsal and anal fins and their fin supports were similar in ontogenic development (Faustino and Power, 1999). The proximal radials were the first structures to develop, followed by distal radials, predorsals, then rays and spines (Kohno and Taki, 1983). Nevertheless, these developmental stages were different both in the Sparidae family and among the same species. Moreover, in Pagrus pagrus, predorsal development was observed after formation of proximal radials, and the same results were determined in previous studies for P. major (Matsuoka, 1985), P. erythrinus (Sfakianakis et al., 2004), D. dentex (Koumoundouros et al., 2000, 2001a), S. aurata (Koumoundouros et al., 1997a; Faustino and Power, 1999), D. sargus (Koumoundouros et al., 2001b) and D. puntazzo (Sfakianakis et al., 2005). Conversely, completion of the predorsal formation (I–III) was observed before completion of the proximal formation. This is in agreement with other studies conducted on some Sparids, as mentioned above. It can be concluded that the ontogeny of the osteological fin developments in P. pagrus larvae followed the same general pattern described for most Sparidae species to date. Also, in both fisheries biology and aquaculture, osteological ontogeny serves to promote understanding of functional trends and environmental preferences of the various developmental stages (Fukuhara, 1992). Hence, osteological malformations were undesirable factors in fish culture. It would be beneficial to study osteological developmental processes in this species. The avoidance of skeletal deformities when rearing fish requires detailed knowledge of their ontogeny (Divanach et al., 1996, 1997; Koumoundouros et al., 1997a,b), which contributes to a better understanding of the species under aquacultural, systematic and ecological consideration (Koumoundouros et al., 2001a,b). Further studies on chondrification and ossification sequences will be useful in understanding how development and function interact, to influence a morphological program and create morphological diversity. 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