INTRODUCTION
Lutjanus russellii (Bleeker, 1849), the Russell's snapper, is a widely distributed lutjanid species in the Indo-West Pacific region, ranging from the Fiji Islands to East Africa, and from Australia to southern Japan, and is important in commercial and recreational fisheries (Allen, Reference Allen1985; Newman, Reference Newman2002). It is found in offshore coral reefs and also inshore rocky and coral reefs (Sommer et al., Reference Sommer, Schneider and Poutiers1996). Juveniles frequent mangrove estuaries and nearshore rocky reef areas and are sometimes found near seagrass beds (Newman & Williams, Reference Newman and Willams1996; Nuraini et al., Reference Nuraini, Carballo, van Densen, Machiels, Lindeboom and Nagelkerke2007). Knowledge of the early life history of this species is particularly limited. Liu & Hu (Reference Liu and Hu1980) described the eggs of laboratory-reared L. russellii. Later, Kojima & Mori (Reference Kojima, Mori and Okiyama1988) illustrated a 19.6 mm juvenile of this species. The goal of the present study, therefore, was to examine the morphological development of laboratory-reared L. russellii from the yolk-sac larvae to the early juvenile stages. An attempt was made to establish ontogenetic intervals for the species, based on the development of the characters examined.
MATERIALS AND METHODS
Eggs and larvae were obtained on 30 August 2008 from spontaneous spawning of a pair of captive brooders maintained in a 3000-ton concrete pond at the National Museum of Marine Biology and Aquarium (NMMBA), Taiwan (22°03′N 120°41′E). The broodfish were fed daily with various trash fishes, such as carangid and scombrid species, and squid (Illex argentinus Castellanos, 1960). Lighting schedules during the preconditioning and spawning period were ambient. Fertilized eggs were collected from the spawning pond with a fine dip net (100 μm mesh size). The eggs were then transferred into a 500 l circular fibreglass tank at a density of 100 eggs l−1 for incubation and larval rearing. The feeding scheme for the resulting larvae and juveniles was as follows: s-type rotifers (Brachionus rotundiformis Tschugunoff, 1921) at a density of 5–10 individuals ml−1, from two days after hatching (DAH) to 30 DAH; copepods (Euterpina acutifrons Dana, (1847)), 1–3 individuals ml−1, from 15 DAH to 30 DAH; and artificial diet, from 25 DAH until the termination of the experimental rearing period on 50 DAH. During the experiment, water temperatures ranged from 26.6 to 29.8°C and salinity from 27.6 to 32.4 ppt. Larvae were sampled with a pipette and euthanized in MS-222 (approximately 20 mg l−1) for measurement and photography. These specimens were observed and measured under a Leica stereomicroscope equipped with a calibrated ocular micrometer (to the nearest 0.01 mm) or measured with an absolute digimatic caliper (to the nearest 0.1 mm), photographed by a Leica MPS30 photomicrographic system and preserved in 5% buffered formalin, transferred to 70% ethanol. Terminology generally follows Kendall et al. (Reference Kendall, Ahlstrom, Moser, Moser, Richards, Cohen, Fahay, Kendall and Richardson1984) and Leis & Rennis (Reference Leis, Rennis, Leis and Carson-Ewart2004). Specimens examined were deposited at NMMBA, with the collection numbers NMMBLF 00102–00104.
RESULTS
Egg, larvae and juveniles in different developmental stages are presented in Figure 1. The fertilized eggs were transparent, spherical and buoyant (diameter = 0.80 mm, range 0.71–0.84 mm, standard deviation (SD) = 0.04; N = 50), and contained a single oil globule (diameter = 0.16 mm, range 0.15–0.17 mm, SD = 0.01; N = 50) (Figure 1A). The perivitelline space was narrow, the chorion clear and unsculptured, and the yolk homogeneous and unsegmented. Melanophore and xanthophore pigments were visible on the surface of the embryonic body and yolk. Hatching occurred 26 hours 50 minutes after fertilization at a temperature of 24.7°C. The hatching rate varied from 46.9% to 83.5% with an average of 70.4%. Embryonic development of Lutjanus russellii was found to be similar in appearance to that of other previously documented specimens of this species (Liu & Hu, Reference Liu and Hu1980) and will not be described further.

Fig. 1. Development of egg, larvae and juveniles of Lutjanus russellii: (A) late stage egg, 0.80 mm diameter; (B) newly-hatched larva, 1.92 mm total length (TL); (C) 3 days after hatching (DAH), 2.88 mm TL; (D) 7 DAH, 3.77 mm TL; (E) 13 DAH, 4.48 mm TL; (F) 15 DAH, 5.70 mm TL; (G) 20 DAH, 8.04 mm TL; (H) 30 DAH, 15.52 mm TL; (I) 38 DAH, 23.41 mm TL.
A description of the key characteristics of each developmental stage are summarized in Table 1. Newly hatched larvae measured 1.86 mm total length (TL, range 1.66–2.04 mm, SD = 0.10; N = 10; Figure 1B) with 24 (10 + 14) myomeres and were slightly curved around the yolk sac. The oil globule, in the majority of specimens, was located in the ventro-anterior area of the yolk sac. The eyes were unpigmented at this stage, melanophores and branched xanthophores were scattered on the head, body, yolk, oil globule and the dorsal finfold surface. At 2 DAH (length = 2.61 mm, range 2.35–2.88 mm, SD = 0.17; N = 10), a single cluster of external xanthophores appeared on the half of the dorsal finfold above the 9–10 myomeres, melanophores on the ventral side of the trunk and tail arranged in two rows. At 3 DAH (length = 2.74 mm, range 2.39–2.95 mm; SD = 0.17; N = 10; Figure 1C), the yolk sac was almost completely absorbed and the oil globule reduced to a negligible size, the mouth and anus were opened, the gas bladder inflated and the eyes were fully pigmented. The maxilla and mandible were functional but still not fully developed. Melanophores joined together to form anteriorly an oblique blotch covering the dorsal part of the gut and posteriorly a single row composed of stellate melanophores. The new relatively large and branched melanophores were developed on the ventral surface of the abdominal cavity. In live specimens at this stage, a cluster of external xanthophores appeared on the half of the dorsal finfold above the 10 myomeres (indicated by arrow on Figure 1C). At 7 DAH (length = 3.50 mm, range 3.06–4.03 mm; SD = 0.29; N = 10; Figure 1D), the nostrils had appeared. One stellate melanophore appeared on the cleithral symphysis. At 10 DAH (length = 3.93 mm, range 3.48–4.30 mm; SD = 0.26; N = 10), the buds of the second dorsal and pelvic-fin spines had appeared. The stellate melanophores on the ventral side of the tail became distinct and decreased in number. At 13 DAH (length = 4.32 mm, range 3.72–5.21 mm; SD = 0.43; N = 10; Figure 1E), dorsal-fin rays IV, pelvic ray I/0–1, the mouth and eyes were completely differentiated. The second dorsal and pelvic-fin spines had begun to elongate. The soft rays of the dorsal and anal-fins had begun to develop. One dark brown, honeycomb-shaped cluster of melanophores appeared on the top of rear-brain. At 15 DAH (length = 5.81 mm, range 4.86–7.40 mm; SD = 0.66; N = 10; Figure 1F), dorsal-fin rays VII/9–10, anal rays II/6–7, pelvic ray I/3. The ratios of the second dorsal and pelvic-fin spine lengths to total length attained their maximum, 40% and 36%, respectively. The second dorsal and pelvic-fin spines were triangular in cross-section, with serrations beginning to develop on each ridge, and the notochord was slightly flexed. Hypural bones and the soft rays of the caudal-fin had begun to develop. At 20 DAH (length = 6.91 mm, range 5.85–8.30 mm; SD = 0.84; N = 10; Figure 1G), dorsal-fin rays VIII/14 anal rays II/8, pelvic ray I/5. The hypural bones were shown at a vertical position. At 25 DAH (length = 9.12 mm, range 7.62–11.93 mm; SD = 1.19; N = 10), dorsal-fin rays IX/14, anal rays III/8, pelvic ray I/5. The second dorsal and pelvic-fin spine lengths had decreased. The nostrils had become separated into two pores. At 30 DAH (length = 14.02 mm, range 10.67–16.75 mm; SD = 1.91; N = 10; Figure 1H), dorsal-fin rays X/14–15, anal rays III/8, pelvic rays I/5, pectoral rays 16, caudal rays 17. The overall adult number of spines and soft rays was complete. The entire body was still translucent, but melanophores were spread over the top of the head. The larval habitat shifted from the surface or middle layers to the tank bottom. The cannibalistic behaviour appeared at this stage. At 38 DAH (length = 23.1 mm, range 19.66–27.1 mm; SD = 2.66; N = 8; Figure 1I), the body had become whitish colour, and serrations on the dorsal, pelvic, and anal-fin spines reduced. The squamated area of the body extended along the midline of the trunk from the posterior of the operculum to the caudal peduncle. Four dark brown stripes and a round black spot on the lateral line below the anterior portions of the soft dorsal-fin were visible on the body. At 50 DAH (length = 44.3 mm, range 38.3–50.8 mm; SD = 4.5; N = 9), the juvenile habitat shifted gradually to the bottom and when startled, sought shelter immediately. A summary of growth of L. russellii from hatching through 50 DAH is shown in Figure 2. Larvae and juveniles were reared between 26.6 and 29.8°C. An exponential equation: Y = 2.18e0.06X (where Y is mean TL (mm) and X represents days after hatching) was found to provide the best fit of the observed data and explained 99.34% (e.g. R 2 = 0.9934, P < 0.001) of the variation in growth obtained over the course of the 50 days in culture.

Fig. 2. Summary of observed growth of Lutjanus russellii over the course of 50 days in culture. Error bars indicate standard deviation of the mean.
Table 1. Key morphological characteristics at each developmental stage of Lutjanus russellii, cultured at 26.6–29.8°C.

PF, post fertilization; DAH, days after hatching.
DISCUSSION
The early life history of snappers has been thoroughly reviewed by Leis (Reference Leis, Polovina and Ralston1987). Eggs, larvae and early juveniles are only known for a few species (Richards et al., Reference Richards, Lindeman, Lyczkowski-Shultz, Leis, Röpke, Clarke and Comyns1994). There are no data about larvae of Lutjanus russellii in the literature. With reference to the fertilized eggs and newly hatched larvae, 17 species should be compared with L. russellii (Table 2). The diameters of fertilized eggs (0.70–0.84 mm) were similar to those observed for same lutjanids: Lutjanus griseus Linnaeus (1758) (Damas et al., Reference Damas, Borrero, Millares and González1978; Cabrera et al., Reference Cabrera, Rosas and Millán1997), Lutjanus kasmira Forsskål (1775) (Suzuki & Hioki, Reference Suzuki and Hioki1979), Lutjanus campechanus Poey (1860) (Rabalais et al., Reference Rabalais, Rabalais and Arnold1980), Lutjanus vitta Quoy & Gaimard (1824) (Lu, Reference Lu1981), Lutjanus johnii Bloch (1792) (Lim et al., Reference Lim, Cheong, Lee and Heng1985), Lutjanus lutjanus Bloch, 1790 (Zhang et al., Reference Zhang, Lu, Zhao, Chen, Zhang and Jiang1985), Pristipomoides typus Bleeker, 1852 (Zhang et al., Reference Zhang, Lu, Zhao, Chen, Zhang and Jiang1985), Lutjanus stellatus Akazaki, 1983 (Hamamoto et al., Reference Hamamoto, Kumagai, Nosaka, Manabe, Kasuga and Iwatsuki1992), Lutjanus argentimaculatus Forsskål (1775) (Doi et al., Reference Doi, Kohno, Taki, Ohno and Singhagraiwan1994; Leu et al., Reference Leu, Chen and Fang2003) and Lutjanus cyanopterus Cuvier (1828) (Heyman et al., Reference Heyman, Kjerfve, Graham, Rhodes and Garbutt2005). Moreover, the diameter was relatively bigger than Lutjanus synagris Linnaeus (1758) (Borrero et al., Reference Borrero, González, Millares and Damas1978; Clarke et al., Reference Clarke, Domeier and Laroche1997) and Lutjanus rivulatus Cuvier (1828) (Senoo et al., Reference Senoo, Baidya, Shapawi and Rahman2002). Yet, the diameter was generally smaller than Lutjanus erythopterus Bloch, 1790 (Zhang et al., Reference Zhang, Lu, Zhao, Chen, Zhang and Jiang1985), Ocyurus chrysurus Bloch (1791) (Riley et al., Reference Riley, Holt and Arnold1995; Clarke et al., Reference Clarke, Domeier and Laroche1997), Lutjanus analis Cuvier (1828) (Watanabe et al., Reference Watanabe, Ellis, Ellis, Chaves and Manfredi1998), Lutjanus sebae Cuvier (1816) (Imanto et al., Reference Imanto, Melianawati and Suastika2006) and Lutjanus guttatus Steindachner (1869) (Boza-Abarca et al., Reference Boza-Abarca, Calvo-Vargas, Solis-Ortiz and Komen2008).
Table 2. Comparison of the eggs and yolk-sac larvae of lutjanids.

TL, total length; * size is measured in standard length (SL).
The size of the newly hatched larvae of L. russellii (1.66–2.2 mm) observed during this study is within the range recorded for L. synagris (Borrero et al., Reference Borrero, González, Millares and Damas1978; Clarke et al., Reference Clarke, Domeier and Laroche1997), L. kasmira (Suzuki & Hioki, Reference Suzuki and Hioki1979), L. campechanus (Rabalais et al., Reference Rabalais, Rabalais and Arnold1980; Minton et al., Reference Minton, Hawke and Tatum1983), L. johnii (Lim et al., Reference Lim, Cheong, Lee and Heng1985), and L. argentimaculatus (Doi et al., Reference Doi, Kohno, Taki, Ohno and Singhagraiwan1994; Leu et al., Reference Leu, Chen and Fang2003). The newly hatched larval size observed during this study is larger than the size recorded for L. vitta (Lu, Reference Lu1981), L. erythopterus (Zhang et al., Reference Zhang, Lu, Zhao, Chen, Zhang and Jiang1985), L. lutjanus (Zhang et al., Reference Zhang, Lu, Zhao, Chen, Zhang and Jiang1985) and P. typus (Zhang et al., Reference Zhang, Lu, Zhao, Chen, Zhang and Jiang1985); but is smaller than the size recorded for L. griseus (Damas et al., Reference Damas, Borrero, Millares and González1978; Cabrera et al., Reference Cabrera, Rosas and Millán1997), L. stellatus (Hamamoto et al., Reference Hamamoto, Kumagai, Nosaka, Manabe, Kasuga and Iwatsuki1992), O. chrysurus (Riley et al., Reference Riley, Holt and Arnold1995; Clarke et al., Reference Clarke, Domeier and Laroche1997), L. analis (Clarke et al., Reference Clarke, Domeier and Laroche1997), L. rivulatus (Senoo et al., Reference Senoo, Baidya, Shapawi and Rahman2002), L. sebae (Imanto & Melianawati, Reference Imanto and Melianawati2003) and L. guttatus (Boza-Abarca et al., Reference Boza-Abarca, Calvo-Vargas, Solis-Ortiz and Komen2008).
The larvae and juveniles of L. russellii examined in this study show many characters common to lutjanin species. These characters include: the body shape, the tightly coiled gut, small gas bladder, pigment pattern, and early formation of head spination and pelvic and dorsal-fin spines (Leis & Rennis, Reference Leis, Rennis, Leis and Carson-Ewart2004; Lindeman et al., Reference Lindeman, Richards, Lyczkowski-Shultz, Drass, Paris, Leis, Lara, Comyns and Richards2006; Leis, Reference Leis and Kendall2011). The melanophores covering the gut and gas bladder dorsally, along the membranes of the dorsal and pelvic-fin spines and along the ventral edge of the tail, is one of the pigmentation characteristics of lutjanid larvae. However, in just-hatched larvae, branched xanthophores on the head, body, yolk, oil globule and the dorsal finfold surface, present in L. russellii (Figure 1B), are absent in the other Lutjanidae (see above) (Borrero et al., Reference Borrero, González, Millares and Damas1978; Damas et al., Reference Damas, Borrero, Millares and González1978; Suzuki & Hioki, Reference Suzuki and Hioki1979; Rabalais et al., Reference Rabalais, Rabalais and Arnold1980; Lu, Reference Lu1981; Minton et al., Reference Minton, Hawke and Tatum1983; Lim et al., Reference Lim, Cheong, Lee and Heng1985; Zhang et al., Reference Zhang, Lu, Zhao, Chen, Zhang and Jiang1985; Hamamoto et al., Reference Hamamoto, Kumagai, Nosaka, Manabe, Kasuga and Iwatsuki1992; Doi et al., Reference Doi, Kohno, Taki, Ohno and Singhagraiwan1994; Clarke et al., Reference Clarke, Domeier and Laroche1997; Senoo et al., Reference Senoo, Baidya, Shapawi and Rahman2002; Imanto & Melianawati, Reference Imanto and Melianawati2003; Leu et al., Reference Leu, Chen and Fang2003; Boza-Abarca et al., Reference Boza-Abarca, Calvo-Vargas, Solis-Ortiz and Komen2008). Riley et al. (Reference Riley, Holt and Arnold1995) also observed the development of xanthophores located on the lateral surface of the body at midgut in <4.0 mm (3 DAH) O. chrysurus larvae. The xanthophores found on live or recently preserved specimens of these two snappers may be definitive characteristics for identification of the species; unfortunately, this light-coloured pigment was not visible after the 30-day preservation period in larvae and would not likely be detected in ichthyoplankton samples preserved in formalin or ethanol.
Furthermore, the body shape, pigment pattern, fin-spine morphology, and the fine serrations on the head spines of larval L. russellii are similar to larvae of Lutjanus malabaricus Bloch & Schneider (1801). However, the spines of the dorsal and pelvic-fins of L. malabaricus were strongly serrated in larvae between 4.3 and 16.3 mm (Leis & Rennis, Reference Leis, Rennis, Leis and Carson-Ewart2004). Lutjanus russellii larvae also have weak serrations on fin spines, but only in larvae between 5.1 and 7.4 mm, and between 7.4 and 15.0 mm these serrations were lost. Lutjanid larvae are relatively easy to identify to family but it is much more difficult to distinguish species. Identification of the larvae and juveniles of other lutjanid species is more difficult than that of L. russellii and L. malabaricus, since the meristic characters are very similar in most other species of lutjanids. At present time, lutjanid larvae <4.0 mm can be identified only to family. Laboratory rearing presents the most likely solution to the larval and juvenile lutjanid taxonomic problem since that is the primary method of examining and comparing larval fish to determine identifications of field-caught larvae. Advances in rearing series from known parents in the laboratory have greatly increased our knowledge, but more is unknown than known. In addition, the reared larvae in this study seem to have a slow rate of growth compared to the pelagic larval duration values of Zapata & Herron (Reference Zapata and Herron2002). It is not unusual for reared larvae to have slower growth than wild larvae, but it is an indication that improvements in culture procedures that give fast growth can be achieved. Information on age and size at larval transformation of intensively reared fish is valuable both in financial and logistics points of view. In the present study, L. russellii larvae grew completing metamorphosis in 30 DAH and transforming to juveniles, at 14.02 mm TL within a temperature range of 26.6–29.8°C.
ACKNOWLEDGEMENTS
The authors thank their colleague P.-J. Meng for constructive criticisms, and are grateful to G.-N. Chung, Fisheries Agency, Council of Agriculture, Executive Yuan, Taiwan, ROC, for collecting the broodstock. Heartfelt thanks go to C.-S. Huang, Graduate Institute of Marine Biodiversity & Evolutionary Biology, National Dong Hwa University, Taiwan, for assistance in larval rearing and sampling. We also thank the editor and anonymous referees for their constructive comments on the manuscript.
FINANCIAL SUPPORT
The National Museum of Marine Biology and Aquarium (NMMBA) provided financial support for this research as part of NMMBA Project No. 971003031.
Supplementary Material and Methods
The Supplementary Material referred to in this paper can be found online at journals.cambridge.org/mbi.