Larval development of laboratory-reared Green mandarinfish, Synchiropus splendidus (Teleostei: Callionymidae).
Dragonets of the genus Synchiropus Gill, 1859, are small, bottom-dwelling fishes from the tropical Indian and Pacific Oceans and comprise approximately 27 species (Fricke 1983). The Green Mandarin, Synchiropus splendidus (Herre, 1927), is a small (6 cm) species that occurs in shallow protected lagoons and reefs in the western Pacific; it is distributed from the Ryukyu Islands of southern Japan to New Caledonia and Australia (Myers 1999). Together with S. picturatus (Peters, 1877), S. stellatus Smith, 1963, and S. ocellatus (Pallas, 1770), S. splendidus is hugely popular in the world aquarium trade. To date, all specimens offered in the trade are captured from the wild, and concern over the sustainability of this selective fishery has been raised (Sadovy et al. 2001, Vincent & Sadovy 1998).
Despite initial successes in the propagation and rearing of Synchiropus spp. (Wittenrich 2009; Mai 2000, 2006; Sadovy et al. 2001; Wilkerson 1996), limited descriptive information is available pertaining to the development of these popular fishes. Improved larval rearing techniques and knowledge of the life-history requirements of Synchiropus have recently enabled continuous production of larval and juvenile S. splendidus for observation. Sadovy et al. (2001) described the fishery, reproduction, and early life history of S. splendidus. Herein, we expand on their description of larval development and describe for the first time the development of certain osteological features. We describe morphology, color pattern, and growth of larvae and juveniles to 50 days post-hatching (DPH). Additionally, we compare larval S. splendidus to known larvae of other Callionymidae. Developmental characters may be of value in future phylogenetic investigations of callionymid fishes. We hope that this information will prove useful in providing a rearing protocol for future scientific investigations and hatchery applications. Aquaculture potential and protocols will be addressed in future work. Cultured fish do indeed exhibit long-term success in aquariums and commercial production is underway at one US-based commercial hatchery, based on Wittenrich (2009).
MATERIALS AND METHODS
Larvae described herein were obtained from natural spawnings of two wild-collected pairs of Synchiropus splendidus. Eggs were collected shortly after spawning and transferred to cylindrical incubation tanks (15 1) provided with gentle aeration from an open-ended air diffuser. Two days after fertilization embryos were transferred to 150 l black conical rearing tanks and reared at densities of no more than 1.5 larvae [l.sup.-1]. Water quality in each rearing tank was maintained by a biological filter tower, ultraviolet sterilizer, and protein skimmer with an exchange rate of 0.5 [l.sup.-1 min]. Natural seawater filtered through a 10 [micro]m closed-pore filter was maintained at 26[degrees]C, salinity 35 ppt, pH 8.2, [NH.sub.3] and [NO.sub.2] < 0.02 ppm, and [NO.sub.3] < 10 ppm (Red Sea marine lab test kit). Water changes were performed every other day by replacing 10% of the total system water from the sump. Photoperiod was maintained at 14 hrs light and 10 hrs dark with two 40W fluorescent bulbs (6500 K) mounted 20 cm above the water surface. Greenwater was maintained in the rearing tanks during all trials by adding 0.5 ml of diluted Nannochloropsis oculata algae paste (Reed Mariculture) to the tanks each morning.
Larvae were provided with rotifers (Brachionus plicatilis, average lorica length ranged from 180-277 [micro]m) and copepod-dominated, size-sorted wild plankton (55-90 [micro]m) as initial feed 4 DPH and subsequently provided with larger copepod-dominated, size-sorted wild plankton (110-500 [micro]m) 8 DPH through settlement. Prey density of rotifers was maintained from 3-5 DPH at 10 [ml.sup.-1] and subsequently lowered to 5 [ml.sup.-1] until 12 DPH when rotifers were removed from the diet. Wild plankton was maintained at 2 [ml.sup.-1] throughout the larval period.
Beginning at hatching (0 DPH), 20 larvae were sampled from the rearing tank, initially every other day and subsequently every 2-6 days, anesthetized with tricaine methanosulphonate (MS-222) and fixed in 5% seawater-buffered formalin for 24 hours before transfer to 70% ethanol for later analysis. Notochord length (NL) or standard length (SL) of freshly collected larvae was measured using an ocular micrometer fitted to a stereomicroscope prior to preservation. Twelve larvae from samples taken at 5, 7, 9, 12, 15, 17 and 23 DPH were cleared and stained following the methods described by Potthoff (1984). Elements of the viscerocranium were described following Hunt Von Herbing et al. (1996), Liu (2001) and Moteki (2002). References to osteological development were standardized to body length. Preserved specimens of Paradiplogrammus bairdi from Belize referenced in the "Discussion" are from ongoing larval-fish studies at the Smithsonian's marine station at Carrie Bow Cay.
Eggs and hatching (Fig. 1)
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Eggs were released singly or clumped together in chains, breaking apart as they swelled with water and drifted in currents. Those released singly were spherical, whereas those that remained clumped were oblong with triangular adhesion points to adjoining eggs. In situ the eggs were clear and positively buoyant. They measured 0.8 mm in diameter and lacked oil globules. The chorion had a distinctive polygonal mesh-like appearance. Hatching began 13-16 hours post fertilization.
Morphological development (Table I; Figs 2-7)
Table I. Mean measurements of laboratory-reared Synchiropus splendidus larvae. Measurements are expressed as a fraction of body length (notochord length, NL). DPH = days post-hatch. A dash indicates the measurement could not be made. Pelagic Benthic stage juvenile Age (DPH) 5 7 9 12 15 17 23 Mean body 2.01 NL 2.19 2.64 2.99 3.08 NL 3.33 3.26 length NL NL NL NL NL Proportions Snout to anus 0.45 0.55 0.57 0.53 0.55 0.55 0.62 length Snout to - - - 0.43 0.42 0.39 0.46 dorsal length Snout to - - - 0.33 0.32 0.30 0.34 pectoral length Head length 0.27 0.28 0.31 0.34 0.35 0.34 0.37 Head width 0.15 0.16 0.21 0.30 0.30 0.33 0.36 Body depth 0.25 0.25 0.25 0.28 0.28 0.26 0.29 Eye diameter 0.11 0.11 0.12 0.13 0.14 0.14 0.15
Newly hatched larvae measure 1.56 [+ or -].04 mm and possess a large oval yolk without oil globules. The yolk is 52% body length. Eye placodes are present. At 2 DPH the larvae measure 1.67 [+ or -].05mm, and the yolk has been reduced to 34% body length, giving the larvae a streamlined appearance. The anal pore and gut are visible, but are not connected to the finfold. At 3 DPH, pectoral-fin buds are visible, the anal pore has opened to the finfold and the mouth is beginning to form. As the larva grows, the body thickens, and the head becomes broad. At 12 DPH the head width is 30% body length and expands to 36% body length by 23 DPH. Age and growth of larvae and early juveniles to 50 DPH is illustrated in Fig. 2.
[FIGURE 2 OMITTED]
Newly hatched larvae mostly drifted motionless but swam in rapid short bursts a few times per minute. First feeding occurred 4 DPH at 26[degrees]C when the larvae measured 1.74 [+ or -].06 mm and the yolk was depleted. At approximately 12 DPH, larvae exhibited a conspicuous behavior that persisted until settlement: when a larva approached prey, the posterior portion of the body curled to one side of the body, which potentially aids maneuverability and steering (Sadovy et al. 2001). Intermittent settling behavior was exhibited near 12 DPH when the larvae rested on the vertical walls and floor of the rearing tank for short periods before returning to the open water. Most larvae settled to the floor of the rearing tank by 16-20 DPH. In subsequent larval rearing trials sufficient wild zooplankton densities were difficult to collect due to storm events. During those times, when prey concentration in the open water of the rearing tank was limited, larval settlement occurred earlier, around 14 DPH.
Body pigmentation (Figs 3-7)
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At hatching, the body and yolk are covered with stellate and dendritic xanthophores, with a heavy concentration on the dorsal and anal finfolds posterior to the yolk. Scattered melanophores are present along the dorsal surface of the yolk, on the dorsal finfold and on the head and trunk. The notochord tip and caudal finfold lack pigment. By 3 DPH the clear posterior finfold tip is conspicuous relative to the rest of the body, which is largely yellow. The head and trunk are primarily covered by stellate xanthophores, whereas the posterior portion of the body, beyond the yolk, is dominated by dendritic xanthophores interlaced with larger melanophores. Dense xanthophores are present on the ventral finfold edge from the anal pore to the last myomere, forming a distinct yellow edge. This yellow edge is mirrored on the dorsal finfold by a matching posterior yellow line. A similar, but smaller yellow edge is present on the dorsal finfold above the posterior edge of the yolk. The body is almost solid yellow at 4 DPH, at which time eye pigmentation first appears and the iris iridophores reflect silver. The dorsal and anal finfolds are densely covered with clusters of xanthophores, and the distinctive yellow edges are lost. The anal pore is bright yellow. The posterior finfold, beyond the last myomere, remains unpigmented. Melano - phores remain sparse. Between 6 and 8 DPH, melanophores increase in density, and the body becomes almost solid orange. A conspicuous brown spot appears on the trunk over the posterior edge of the gut and anal pore. The head and trunk are a dense, dark, uniform orange by 12 DPH, and the dark trunk spot fades. The median fins are clear. By 8 DPH iris iridophores reflect gold, which then darkens through settlement.
Settlement-stage larvae become mottled with dark orange to brown irregular bands on the trunk. After settlement the body turns pale tan to brown with darker vertical bands and blotches across the body. The pelvic and anal fins are the first to gain partial brown pigment near 25 DPH. At 30 DPH the tan and brown mottled pattern has become more conspicuous and faint green bands are present on the head and eyes. Forty-day old juveniles exhibit well-delimited brown bars on the body, faint green banding on the head and brown anal and pelvic fins. The caudal, dorsal and pectoral fins remain clear. At 50 DPH the body color has turned bright orange with a characteristic blue banding pattern resembling the adult. The dorsal, anal, pelvic, and caudal fins are now bright orange with a blue outline.
Body pigmentation of 5-17 DPH larvae fades quickly after alcohol preservation. Small melanophores are scattered loosely on the frontal, gut, and anus of 5 DPH larvae. Concentrated melanophores also appear on the dorsal and ventral edges of the trunk. From 8-17 DPH melanophore concentration increases on the frontal and nape regions, dorsal and ventral melanophore stripes become more prominent and a midbody stripe appears. Large melanophores appear scattered over the opercular region in 12 DPH larvae, and a dark spot is visible on the dorsal trunk below the dorsal anlagen.
Settlement-stage larvae, from 23-50 DPH, have brown body pigmentation, and scattered melanophores on the frontal, nape and operculum. The spot below the dorsal fin remains until near 50 DPH. Dorsal, anal and midbody stripes have disappeared. At 50 DPH the body pigmentation resembles the adult, and while the color intensity fades in preservative the banding pattern remains.
Skeletal Development (Table I-III; Fig. 8)
Table II. Mean counts of laboratory-reared Synchiropus splendidus larvae. DPH = days post-hatch. Pelagic Benthic juvenile Age (DPH) 5 7 9 12 15 17 23 Neural arches 4 15 18 18 18 18 18 Haemal arches 0 7 13 12 13 13 13 Dorsal 0 0 0 12 12 12 12 pterygiophores Anal 0 0 0 6 7 6.5 7 pterygiophores Dorsal-fin rays 0 0 0 0,4 0,6 IV,8 IV, 8 Anal-fin rays 0 0 0 4 7 7 7 Pelvic-fin rays 0 0 0 6 6 6 6 Pectoral-fin 0 0 0 0 0 0 0 rays Caudal-fin rays 0 0 0 6 11 12 15
[FIGURE 8 OMITTED]
Jaws. Meckel's cartilage is present in 5 DPH larvae (1.95 mm [+ or -].21mm NL). The dentary and retroarticular begin to differentiate at 9 DPH (2.5 [+ or -].19 mm NL) and are beginning to ossify at 12 DPH (2.85 [+ or -].39 mm NL). The premaxilla and maxilla are visible at 9 DPH (2.5 [+ or -].19 mm NL). Neither the upper nor lower jaw is completely ossified at 23 DPH (3.51 [+ or -].23 mm SL). The premaxilla and dentary lack teeth throughout larval development.
Suspensorium. The hyomandibulosymplectic cartilage, consisting of cartilaginous precursors to the hyomandibular and symplectic, is visible at 5 DPH. The palatoquadrate cartilage is present at 9 DPH. Dorsal and ventral ossification of the hyomandibular and initial ossification of the symplectic, palatine and quadrate are evident by 23 DPH (3.51 [+ or -].23 mm SL). The cartilaginous metapterygoid begins to ossify by 17 DPH (3.05 [+ or -].23 mm SL). The ectopterygoid and endopterygoid first appear as ossifying bone at 23 DPH (3.51 [+ or -].23 mm SL).
Hyoid arch. Rudimentary hyoid bars are present at first feeding. Ceratohyal and epihyal cartilages continually expand until 9 DPH when the hyoid reaches its maximum depth and has the full complement of six branchiostegal rays. The interhyal and epihyal begin ossifying at 17 DPH followed by the ceratohyal and basihyal at 23 DPH.
Opercular series. All elements of the opercular series form as dermal bone. The opercle is the first to appear, at 15 DPH, followed by the interopercle and subopercle at 17 DPH. The preopercle appears at 23 DPH. The preopercular spine is not present until the juvenile stage, approximately 30 DPH.
Branchial arch. Cartilaginous basibranchial and ceratobranchials 1 and 2 are present at 5 DPH, but do not begin ossifying until approximately 17 DPH. Epibranchials and hypobranchials differentiate around 12 DPH. Ossification of the gill arches is not complete by 23 DPH.
Appendicular skeleton. The cleithrum, present at first feeding as a thin band, thickens with growth. At 9 DPH, the post- and supracleithrum are visible. All cleithral elements begin to ossify around 12 DPH. The scapula and coracoid are visible at 5 DPH. Neither element begins to ossify until after settlement, near 4 mm SL. Pectoral radials are not formed at 23 DPH. Pectoral-fin rays have not begun differentiating at 23 DPH. The pelvic basipterygium is visible at 9 DPH and begins ossifying at the distal end at approximately 17 DPH. Pelvic-fin rays appear at 12 DPH.
Axial skeleton. Two to five neural arches are visible in 5 DPH specimens, 15 are present at 7 DPH and 18 by 9 DPH. At 7 DPH five to seven haemal arches are present and number 13 by 9 DPH. Initial ossification of the vertebrae and neural and haemal spines is observed at 9 DPH and progresses in an anterior-to-posterior direction. All but the two posteriormost vertebral centra, neural and haemal arches are ossified in 12-15 DPH specimens.
Caudal complex. Development of the caudal complex begins at 9 DPH when the cartilaginous parhypural appears anterior to a small triangular ventral hypural plate. The cartilaginous neural arch and spine of PU2 (NPU2) is present opposite the parhypural. At 12 DPH the ventral hypural plate has expanded and supports three to five caudal rays. The notochord is straight and elongate, the tip accounting for roughly 20% body length. The dorsal hypural plate is now visible as a thin cartilage projection and supports a single caudal ray. NPU2 has expanded dorsally from its attachment point on the vertebra, and the autogenous, cartilaginous epural is present. At 15 DPH the ventral hypural plate supports five caudal rays, and the parhypural supports a single ray. The dorsal hypural plate is now a triangle of cartilage that supports three caudal rays. Notchord flexion is evident at 17 DPH as a weak upward bend from the horizontal. At 23 DPH, flexion is complete, and the posterior edges of the hypural plates form a vertical margin. The urostyle is now less than 5 % body length. Ossification of the caudal complex is not apparent at 23 DPH. The full complement of caudal-fin rays (15) is present at 23 DPH.
Dorsal and anal fins. Dorsal and anal anlagen appear at 9 DPH, and the full complement of cartilaginous ptergyiophores is present at 12-15 DPH. At 23 DPH, the full complement of dorsal and anal-fin elements is present.
Comparisons with early life-history stages of other callionymids
Egg and larval development of S. splendidus is similar to that described for other callionymids (Leis & Rennis 1983, Houde 1984, Powell & Greene 2000, Sadovy et al. 2001). Callionymid eggs are typically spherical, colorless, pelagic, range in size from 0.55-0.97 mm and are released at the height of a spawning ascent from single-pair spawning events (Leis & Rennis 1983, Thresher 1984, Houde 1984, Sadovy et al. 2001). Sadovy et al. (2001) reported that eggs of S. splendidus are lightly adhesive, buoyant and remain together as they drift away with passing currents. Takita (1983) reported that eggs of Callionymus calliste Jordan & Fowler, 1903, are shed in adhesive masses that break apart into individual pelagic eggs as they near hatching. In our experience, S. splendidus, as well as S. picturatus, S. ocellatus, and S. stellatus (M. L. Wittenrich, unpublished data) spawn in a similar fashion with eggs being shed singly or clumped together in long chains that break apart shortly after spawning. Eggs lack oil globules, have a partially separated yolk, and most species exhibit a polygonal mesh-like sculpturing on the chorion. Sadovy et al. (2001) suggested that the mesh-like appearance of the S. splendidus chorion is more disjunct than that of other callionymids. Hatching of S. splendidus embryos is influenced by temperature and ranges from 12.5 h at 28.5[degrees] C to 16 h at 24[degrees] C (Sadovy et al. 2001). Incubation time in the present study was 13-16 h at 26 [degrees]C.
Larvae of callionymids are among the smallest recorded marine fish larvae at hatching, ranging from 1.0-2.1 mm in length (Leis & Rennis 1983, Houde 1984). Leis & Rennis (1983) noted that the small size, long notochord tip and heavy ventral pigmentation of larval callionymids distinguish them from larvae of other families. Larval S. splendidus are typical callionymid larvae in that newly hatched larvae are 1.5-1.6 mm TL, and the notochord accounts for 20% of the body length at 12 DPH. However, they are not so heavily pigmented ventrally as described and illustrated by Leis & Rennis (1983: 224, Fig. 66) for other callionymid larvae. Heavy ventral pigmentation may not be characteristic of most callionymids: for example, although larvae of the western Atlantic Diplogrammus pauciradiatus (Gill, 1865) have heavy ventral pigment on the lateral surface of the gut, larval Paradiplogrammus bairdi (Jordan, 1888) lacks heavy pigmentation ventrally (Powell & Green 2000). The 2.9- and 5.1-mm unidentified callionymid larvae illustrated by Leis & Rennis (1983: Fig. 66B-C) have three distinctive lines of pigment on the posterior portion of the body-one along the base of the dorsal fin, one along the base of the anal fin, and one along mid body. That same pattern of pigmentation is apparent in S. splendidus larvae (see Fig. 3B, D, F), but it is not present in preserved P. bairdi larvae from Belize, which may have melanophores along the lateral midline and a few blotches associated with the dorsal-fin base but lack melanophores along the anal-fin base.
Our description of osteology should serve as a baseline for future comparative work within the Callionymidae. Certain developmental features such as the elongate notochord tip and sequence of ossification should prove valuable in future studies of callionymid relationships.
We found the incidence of settlement was highest between 16-20 DPH, whereas Sadovy et al. (2001) reported settlement at 14 DPH at 24-26[degrees] C. One of the authors (MLW) noticed in subsequent rearing trials that food availability influenced time to settlement (although not quantified). When prey concentration in the open water of the rearing tank was low, larval settlement occurred near 14 DPH. Whether this is an artifact of captivity or suggestive of the ability of late-stage larvae to alternate between pelagic and benthic lifestyles to exploit food resources remains unknown. Settlement in callionymids in general ranges from 14-20 DPH at body lengths of 3.5-10 mm TL (Sadovy et al. 2001, Thresher 1984).
A notable observation of S. splendidus larvae is the ontogenetic color transformation (from yellow to orange) that occurs at 8 DPH. Sadovy et al. (2005) showed that the epidermis of adults is rich in mucous cells and has a distinct sacciform cell type that they proposed may secrete a noxious mucous functioning as a predator deterrent. The vibrant color pattern of adult S. splendidus may be a warning to potential predators. Little is known about ontogenetic color changes in live callionymid larvae because those colors fade in alcohol preservation. Settlement-stage (or nearly so) larvae of Paradiplogrammus bairdi from Belize are bright orange, but coloration of earlier larval stages is unknown, and adults are drab relative to adult S. splendidus. There are conspicuous xanthophores on the spinous dorsal fin in some P. bairdi larvae, and possibly smaller larvae are more uniformly yellow as are larvae of S. splendidus. The pelagic-stage coloration of bright orange that occurs in the Indo-Pacific S. splendidus and the Atlantic P. bairdi may represent a novel predator deterrent function and a conserved phylogenetic peculiarity.
The ontogenetic color change in S. splendidus is accompanied by the development of mucous cells. Although histological and chemical analyses were beyond the scope of this study, mucous production was evident during sampling and microscopy work. Orange has been suggested to be an aposematic warning color in the larvae of some marine organisms (e.g. Lindquist 2002, Young & Bingham 1987), and many marine organisms incorporate poisonous or noxious substances into gametes that serve as bitter or distasteful deterrents (e.g. McClintock & Vernon 1990, Gladstone 1987, Pillsbury 1957). Further investigation of the ontogenetic shift to orange in Synchiropus, including histological and chemical analyses, is needed.
We thank A. Didoha for assistance with raising larvae. This is contribution number 865 of the Caribbean Coral Reef Ecosystems Program (CCRE), Smithsonian Institution, supported in part by the Hunterdon Oceanographic Research Endowment.
Received: 24 September 2009 - Accepted: 3 January 2010
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Matthew L. Wittenrich (1), Carole C. Baldwin (2), Ralph G. Turingan (1)
(1) Florida Institute of Technology, Department of Biological Science, 150 W. University Blvd., Melbourne, FL, 32901, USA
(2) Division of Fishes, National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, Washington, DC 20013-7012, USA
* Corresponding author: Matthew L. Wittenrich, Phone: 321-674-7222, Fax: 321-674-7222. Email: email@example.com
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|Author:||Wittenrich, Matthew L.; Baldwin, Carole C.; Turingan, Ralph G.|
|Publication:||aqua: International Journal of Ichthyology|
|Date:||Jan 20, 2010|
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