BULLETIN OF MARINE SCIENCE, 34(1): 21-59,1984
DESCRIPTION OF PORKFISH LARVAE (ANISOTREMUS VIRGINICUS, HAEMULIDAE) AND THEIR OSTEOLOGICAL DEVELOPMENT
Thomas Potthoff, Sharon Kelley, Martin Moe and Forrest Young
ABSTRACT Wild-caught adult porkfish (Anisotremus virginicus, Haemulidae) were spawned in the laboratory and their larvae reared. A series of 35 larvae 2.4 mm NL to 21.5 mm SL from 2 to 30 days old or older (larvae of unknown age) was studied for pigmentation characteristics. Cleared and stained specimens were examined for meristic and osteological development. Cartilaginous neural and haemal arches develop first anteriorly, at the center, and posteriorly, above and below the notochord, but ossification of the vertebral column is from anterior in a posterior direction. Epipleural rib pairs develop from bone, but pleural rib pairs develop from cartilage first and then ossify. The second dorsal, anal and caudal fins develop rays first and simultaneously, followed by first dorsal fin spine development. The pectoral and pelvic fins are the last of all fins to develop rays. All bones basic to a perciform pectoral girdle develop with cartilaginous radials present between the pectoral fin ray bases. Development and structure of pre dorsal bones and dorsal and anal fin pterygiophores were studied. All bones basic to a perciform caudal complex developed and no fusion of any of these bones was observed in the adults. Radial cartilages developed ventrad in the hypural complex. The hyoid arches originated from cartilage but the branchiostegal rays formed from bone. The development and anatomy of the branchial skeleton were studied. Spines develop on the four bones of the opercular series in larvae and juveniles but are absent in the adults.
There are two species of Anisotremus in the north Atlantic Ocean: A. virginicus and A. surinamensis. In the north Pacific Ocean there is only one species A. davidsoni (Robins et a1., 1980). Recently, a third species A. moricandi has been redescribed for the north Atlantic Ocean by Acero p, and Garzon F. (1982), The larvae of the porkfish (Anisotremus virginicus) belonging to the percoid family of grunts (Haemulidae) have not been described previously, except by de Sylva (1970) who illustrated a 16.5 mm SL porkfish. Knowledge of the osteological development of A. virginicus is also lacking. The larvae of only two grunt species are described. Hildebrand and Cable (1930) described larvae of'the pigfish (Orthopristis chrysopterus) and Watson 1 (manu- script) is redescribing them. Saksena and Richards (1975) described laboratory- reared white grunt larvae (Haemulon plumien) with data on meristics and osteo- logical development. Courtenay (1961) described 13 species of juvenile grunts of the genus Haemulon from the western Atlantic. All aspects of the early life history of the porkfish are unknown. In this paper we describe the early life history stages including osteological development so that larvae caught in ichthyoplankton surveys can be distinguished from other similar- looking haemulid, sparid (Houde and Potthoff, 1976), or lutjanid larvae (Johnson, 1978). The detailed study of osteological development presented here may be useful in future studies of percoid relationships.
I Marine Ecological Consultants of Southern California, 533 Stevens Avenue, Solana Beach, CA 92075.
21 22 BULLETIN OF MARINE SCIENCE, VOL. 34, NO. I, 1984
MATERIALS AND METHODS
Porkfish larvae were spawned and reared by M. Moe and F. Young in the Aqualife Research Corporation laboratory in the Florida Keys. Thirty-five larvae from 2.4 mm NL to 21.5 mm SL were killed and preserved in 5% formalin' 2, 4, 8, 9, 15, 21 and 30 days after hatching; three of the largest reared larvae were of unknown age (Table I). In addition, five adult porkfish from 140 to 168 mm SL, caught in South Florida waters with a spear gun or hook and line during our study in 1981, were used in the study. Of the reared larvae, 26 were preserved for 3 years in 5% formalin and six were preserved for 2 years before our study began. For the largest three larvae the length of preservation was unknown. A. virginicus larvae were measured for notochord length (NL, prellexion and lIexion stage) or standard length (SL, postllexion stage). The methods of measurement and the preparation and treatment of larvae,juveniles and adults for and during the study are given in Potthoffet a!. (1980) in the Materials and Methods section. In clearing and staining we followed the methods of Taylor (1967) and Dingerkus and Uhler (1977), In the following text the reared larvae will be referred to by length; their ages can be obtained from Table I. For the caudal complex we use a composite terminology following Gosline (1961a; b), Nybelin (1963) and Monod (1968). For the terminology ofthe branchial and hyoid arches we follow McAllister (1968), Nelson (1969) and Rosen (l973). These terminologies have been previously used by Potthoff and Richards (1970), Potthoff(1974, 1975), Houde and Potthoff(1976), Fritzsche and Johnson (1980), Potthoff (1980), Potthoff et a!. (i 980), Johnson (1981) and Potthoff and Kelley (1982).
Spawning and Rearing
Adult porkfish, A. virginicus, were collected live on Coffins Patch reef off Marathon in the Florida Keys on 8 November 1978 and 4 November 1979 for experimental spawning. The fish were spawned on the evening of the day of capture. Most of the females were reproductively active and the eggs hydrated and ovulated naturally so hormone injections were unnecessary, The eggs were expressed manually shortly after ovulation into a small bowl and sperm from a male was immediately added. Salt water of the same salinity and temperature as the holding tank was added to the bowl and the eggs and salt water were stirred. Water temperature for spawning and rearing was 27° ± 2°C, The eggs were placed in the rearing tanks soon after first cleavage was observed. The fish were reared in 946-1 circular-polyethylene tanks with conical bottoms. Constant lighting was provided by two 122 cm, 40 watt daylight spectrum lIuorescent bulbs. Salinity was 350/00 throughout the rearing. For the destruction of protozoan fish parasites and the reduction of bacterial levels, treated natural sea water was used for the first 4 to 6 weeks of larval rearing. Water treatment consisted of an overnight application, about 14 h, of 4 to 6 ppm of free chlorine with subsequent dechlorination with sodium thiosulphate and filtration through sand and activated carbon before addition to the rearing tank. Water changes of about 50% of the volume of the rearing tank were made once a week. Larval foods during the first 3 weeks consisted of wild plankton, cultured rotifers, copepods and brine shrimp nauplii, Large brine shrimp, commercial tropical fish lIake foods finely ground and fine particles of shrimp lIesh were added to the diet as the fish became large enough to accept them. At 5 to 6 weeks of age the young porkfish were transferred to 1,361-1 grow-out tanks supplied with a constant lIow of filtered sea water.
PIGMENTATION Two or 3 years elapsed between the time that larvae from the two spawnings were preserved in 5% formalin and subsequently examined. The preservation period did not affect pigmentation noticeably. Head Region. -All larvae 2.4-2.8 mm NL had unpigmented eyes. Of these, three out of five larvae lacked pigment in the head region and two had three to four stellate melanophores on the snout and forebrain as shown in Figure 1 for the 2.5 mm NL specimen. All A. virginicus 2.4-2.6 mm NL had stellate melanophores on the snout and forebrain. Two specimens had one to two melanophores on the
2 Use of any product used in this paper does nol imply endorsement by the National Marine Fisheries Service, NOAA. POTTHOFF ET AL.: ANISOTREMUS LARVAL DEVELOPMENT 23
Table 1. Fin spine and ray counts of 35 laboratory-reared Anisotremlls virginiclls larvae and 5 captured adults from the Florida Keys (specimens above dashed line have an unflexed notochord, those below the dashed line have a flexed notochord)
Pelvic Caudal Fin Rays Pectoral Fin Dorsal Fin Anal Fin Fin Rays Rays Principal Secondary Cleared NL or Days After Spines and Spines (One (Upper/ (Upper/ Total and SL, mm Hatching Rays and Rays Right Left Side) Lower) Lower) Number Stained 2.4 4 0 0 0 0 0 0 0 0 No 2.4 4 0 0 0 0 0 0 0 0 No 2.5 4 0 0 0 0 0 0 0 0 No 2.5 4 0 0 0 0 0 0 0 0 No 2,6 4 0 0 0 0 0 0 0 0 No 2.7 2 0 0 0 0 0 0 0 0 No 2.7 2 0 0 0 0 0 0 0 0 No 2.7 2 0 0 0 0 0 0 0 0 No 2.8 2 0 0 0 0 0 0 0 0 No 3.2 9 0 0 0 0 0 0 0 0 No 3.4 9 0 0 0 0 0 0 0 0 No 3.5 9 0 0 0 0 0 0 0 0 Yes 3,7 9 0 0 0 0 0 0 0 0 Yes 3.8 9 0 0 0 0 0 0 0 0 Yes 3.9 8 0 0 0 0 0 0 0 0 Yes 4.3 8 0 0 0 0 0 0 0 0 Yes ------5.7 15 0,12 2,7 0 0 0 9/8 0/1 18 Yes 5,9 15 No 6.2 15 IV-2,16 1-1,10 0 0 0 9/8 1/1 19 Yes 6.4 15 V-3,16 I-I, I0 6 6 0 9/8 2/2 21 Yes 7.1 21 X-2,16 11-1,10 11 11 1,3 9/8 4/4 25 Yes 7.5 21 XI-l,16 11-1,10 15 15 1,4 9/8 5/5 27 Yes 8.2 21 X-2,17 11-1,10 16 16 1,5 9/8 6/6 29 Yes 8.6 30 XII,16 11-1,10 17 17 1,5 9/8 8/7 32 Yes 8.7 30 XII,16 11-1,10 16 16 1,5 9/8 7/7 31 Yes 8.8 21 XI-I,17 II-I,ll 15 1,5 9/8 7/7 31 Yes 9,0 30 XI-I,15 11-1,10 17 17 1,5 9/8 9/8 34 Yes 9,6 30 XI-I,17 11-1,10 17 16 1,5 9/8 9/9 35 Yes 9,6 30 XI-I,16 11-1,10 16 17 1,5 9/8 8/8 33 Yes 9.8 30 XI-1,I5 IT-I,IO 16 17 1,5 9/8 9/9 35 Yes 10.1 30 XI-I,16 II-I, II 17 16 1,5 9/8 9/8 34 Yes 10.4 30 XI-I,16 IT-I,IO 16 16 1,5 9/8 10/9 36 Yes 20,2 Unknown XII,16 III, 10 17 17 1,5 9/8 13/12 42 Yes 20.4 Unknown XII,15 11,11 17 16 1,5 9/8 13/12 42 Yes 21.5 Unknown XIII,16 III, 10 17 17 1,5 9/8 13/12 42 Yes 140 Not reared XIT,16 III, 10 17 17 1,5 9/8 11/12 40 Yes 158 Not reared XI,18 III, 10 18 18 1,5 9/8 13/12 42 Yes 159 Not reared XII,16 III, 1I 18 18 1,5 Yes 164 Not reared XII,16 III, 10 18 18 1,5 9/8 12/12 41 Yes 168 Not reared XII,16 1II,10 17 1,5 9/8 13/12 42 Yes
midbrain. Eye pigmentation was acquired at 2.8 and 3.2 mm NL. The snout and forebrain melanophores were lost in larvae 3.2-4.3 mm NL and reacquired in larvae 5.7-6.4 mm SL (Figs. 1-4, Table 2). New pigment in the head region for larvae 3.2-4.3 mm NL was in the hindbrain region, tip and ramus of the upper and lower jaws, angle of the jaws, gular membrane and around the eyes (Figs. 2, 3, Table 2). The forebrain pigments were reacquired and pigments on the midbrain appeared in larvae 5.7-6.4 mm SL (Fig. 4, Table 2). Melanophore density in the head region increased greatly in 7.1-21. 5 mm SL A. virginicus (Figs. 5-7). 24 BULLETIN OF MARINE SCIENCE, VOL. 34, NO. I, 1984
I I ,25mm
Figure L Laboratory-reared Anisotremus virginicus larva, 2.5 mm NL, 4 days old. Top: left lateral view; center: dorsal view; bottom: ventral view,
Trunk and Tail Region.-Larvae 2.4-2.8 mm NL had several stellate melano- phores on the anterior portion of the yolk sac, two to seven melanophores along the dorsal body margin, some lateral body pigment, pigment below the gut and just anterior to the anus and two to seven melanophores along the ventral midline posterior to the anus (Fig. 1, Table 2). Some larvae 3.2-4.3 mm NL had one to three stellate melanophores on the nape and in the dorsal body margin opposite the vent (Figs. 2, 3). These larvae also had stellate melanophores on the pectoral symphysis, above, on the sides and below the gut and along the ventral tail margin. Trunk and tail pigmentation did not appreciably increase in the 5.7-10.4 mm SL A. virginicus, except for some lateral musculature pigment in specimens 8.6-10.4 mm SL (Figs. 4-6). Specimens 20.2-21.5 mm SL showed appreciable increase in dorsal, lateral and ventral trunk and tail pigmentation (Fig. 7). Caudal Region.-Specimens 2.4-2.8 mm NL had one melanophore below the tip of the notochord. In larger 3.2-4.3 mm NL un flexed larvae, one large and several small melanophores were seen below the notochord in the caudal fin anlage. Postflexion A. virginicus 5.7 mm SL and larger had a cluster of melanophores at the midline near the distal portion of the hypural bones and near the bases of the caudal fin rays forming a characteristic tail spot (Figs. 1-7, Table 2). Fins. - Melanophores on the fin rays (except for the distinctive caudal spot) and on the fin membrane were first seen on the anal fin of an 8.2 mm SL larva. All specimens longer than 9.0 mm SL had pigmentation on the anal fin rays and fin membrane (Figs. 5-7, Table 2). The second dorsal fin rays and membrane acquired pigmentation at 9.6-10.4 mm SL (Figs. 6, 7, Table 2). The caudal fin had scattered melanophores on the posterior portions of the upper and lower lobes at 20.2 mm SL (Fig. 7, Table 2). The first dorsal fin had only 3 to 6 melanophores in the 20.2- 21.5 mm SL specimens. The pectoral and pelvic fins were unpigmented in all specimens to 21.5 mm SL. POTTHOFF ET AL.: ANISOTREMUS LARVAL DEVELOPMENT 25
I ·5mm
Figure 2. Laboratory-reared AnisOlremus virginicus larva, 3.5 mm NL, 9 days old. Top: left lateral view; center: dorsal view; bottom: ventral view.
OSTEOLOGICAL DEVELOPMENT Vertebral Column. - Before notochord flexion, cartilaginous neural and haemal arches and spines were observed in the smallest cleared and stained 3.5 mm NL A. virginicus. These cartilaginous neural arches and spines were found anteriorly, at the center, and posteriorly on the notochord as shown in Figure 8 for the 3.8 mm NL specimen. Fragmentation of the notochord was first observed anteriorly in the 4.3 mm NL specimen. In the next larger 5.7 mm SL larva the entire vertebral column was ossifying (Fig. 8). Ossification of the neural and haemal arches and spines proceeded from anterior in a posterior direction (Fig. 8). Ossification of individual arches and spines started at the base of the arch and proceeded distad. Then, at the tip of the cartilaginous neural or haemal spine a bony tip appeared also growing distad (Figs. 8-10). All neural and haemal arches were ossifying in the 8.6 mm SL specimen. Later during development, between 10 and 20 mm SL, neural pre- and postzygapophyses developed on the centra (Figs. 9, 10). Neural prezygapophyses developed on centra two or three posteriorly to centrum 26 (urostyle) (Figs. 9, 10), neural postzygapophyses started on centrum four or five and extended posteriorly on all centra to centrum 23 or 24 (Figs. 9, 10). Haemal prezygapophyses were found on all centra from centrum 14 or 15 to centrum 24 and haemal postzygapophyses were observed starting either on centrum 9, 10, II or 12 occurring posteriorly on all centra to centrum 23 (Fig. 10). Miller and Jorgenson (1973) reported 26 or 27 vertebrae for A. virginicus. All specimens examined by us had 26 vertebrae, 10 precaudal and 16 caudal. Pre caudal centra can be distinguished from the caudal centra by noting the position of the first anal pterygiophore. This pterygiophore is always just anterior to the first haemal 26 BULLETIN OF MARINE SCIENCE, VOL. 34, NO. I, 1984
·5mm
~------'h'" ~
_.'t:: ._._,,_._. __ ••._~
Figure 3. Laboratory-reared Anisotremus virginicus larva, 4.3 mm NL, 8 days old. Top: left lateral view; center: dorsal view; bottom: ventral view.
1mm
Figure 4. Laboratory-reared Anisotremus virginicus larva, 5.9 mm SL, 15 days old. Top: left lateral view; center: dorsal view; bottom: ventral view. POTTHOFF ET AL.: AN/SOTREMUS LARVAL DEVELOPMENT 27
Table 2. Lengths and days after hatching at which melanophores develop in 35 laboratory-reared Anisotremus I'irginicus (2.4 mm NL-21.5 mm SL). First: appearance of melanophores in some spec- imens; All: melanophores present in all specimens of the indicated value or larger. Numbers in parentheses denote pigment acquired in young larvae which are lost but later reacquired
Length. mm NL or SL Days after Hatching First All First All Forebrain 5.7 (2.7) 5.7 15(2) IS Midbrain 5.7 (2.5) 7.1 IS (4) 21 Hindbrain 3.2 10.1 9 30 Tip and ramus upper jaw 3.9 (2.7) 7.1 8 (2) 21 Tip and ramus lower jaw 3.2 7.1 9 21 Angle of jaw 3.2 3.2 8 8 Gular membrane 3.2 3.2 8 8 Around eye 4.3 10.4 8 30 Dorsal margin (nape to peduncle) 2.4 8.8 2 30 Lateral midline (pectoral insertion to peduncle) 2.4 10.4 2 30 Caudal spot 2.4 3.2 2 8 Ventral margin (vent to peduncle) 2.4 2.4 2 2 Gut (dorsal and ventral surface) 2.4 2.4 2 2 Pectoral symphysis 3.2 3.2 8 8 First dorsal fin > 10.4, <20.2 > 10.4, <20.2 Not known Not known Second dorsal fin 9.6 10.4 30 30 Anal nn 8.2 9.0 21 30 Caudal fin (but not caudal spot) > 10.4, < 20.2 > 10.4, <20.2 Not known Not known
spine of the first caudal vertebra (Fig. 8). The first closed haemal arch (Fig. II) was found on the 7th or 8th centrum in larvae 5.7 mm SL or longer. In 18 specimens >5.7 mm SL it occurred 14 times on the 7th and 4 times on the 8th vertebra, but in five adults it occurred only on the 8th vertebra (Table 3). In larvae <5.7 mm SL the haemal arch was developing on the individual vertebrae in an anterior direction and was found on the 11th and 10th centra (Table 3). Epipleural and Pleural Ribs. - In juvenile and adult A. virginicus, precaudal centra 1 and 2 each support a pair of epipleural ribs and precaudal centra 3 to 10 support a pair of epipleural and pleural ribs which articulate with the parapophyses. Pleural ribs were first developing in the 7.1 mm SL A. virginicus on precaudal vertebrae 3 and 4 and epipleural ribs were first seen in the 8.2 mm SL specimen on precaudal vertebrae 1 and 2 (Fig. 8, Table 3). Addition of more epipleural and pleural rib pairs was in a posterior direction. The full adult complement of 12 pairs of epipleural ribs on vertebrae 1 to 12 and of 8 pairs of pleural ribs on vertebrae 3 to 10 was attained between 10 and 20 mm SL (Table 3). Individual pleural ribs were seen developing from cartilage first and then ossifying. Pectoral Fin and Supports. -Buds of pectoral fins were present in newly hatched larvae 2 and 4 days old (Fig. 1), which developed to cartilaginous blades and finfolds (Figs. 2-4, 12). The finfolds containp.d actinotrichia, and pectoral rays began to develop dorsad in the finfold first in a 6.4 mm SL specimen and addition of rays was in a ventral direction (Tables 1, 4, 5). The adult pectoral fin ray complement from 16 to 18 rays was first observed in an 8.2 mm SL specimen and all A. virginicus longer than 8.8 mm SL had the adult count (Tables 1, 5) (Hoese and Moore, 1977). Fully developed A. virginicus have 12 bones on each side in their pectoral girdles and suspensoria (Figs. 12, 13). These are one supratemporal-intertemporal 28 BULLETIN OF MARINE SCIENCE, VOL. 34, NO. I, 1984
I---< 1mm
Figure 5, Laboratory-reared Anisotremus virginicus larva, 8.6 mm SL, 30 days old. Top: left lateral view; center: dorsal view; bottom: ventral view.
(fused from two bones during development), one posttemporal, one supraclei- thrum, one cleithrum, two postcleithra, one scapula, one coracoid and four radials. The scapula and the four ossified radials supported the fin rays. Each fin ray also had a cartilaginous radial between its bifurcate base. The supratemporal-inter- temporal and posttemporal accommodated the laterosensory canal (Harrington, 1955). A bony cleithrum, a coraco-scapular cartilage and a cartilaginous blade were present in the smallest cleared and stained specimen 3.5 mm NL. The cleithrum was a rod-shaped bone at first but developed a large posterior process dorsad and a sagittal keel ventrad (Figs. 12, 13). The coraco-scapular cartilage first had a long dorsal and a long posterior process and a very short anterior process (Figs. 12, 13) (Swinnerton, 1905; Starks, 1930). The short anterior process elongated during ontogeny and after ossification became part of the coracoid, whereas the long posterior process shortened during ontogeny and also became part of the coracoid. The dorsal process of the coraco-scapular cartilage acquired a foramen during ontogeny at 5.7 mm SL (Table 4). Part of the POTTHOFF ET AL.: ANISOTREMUS LARVAL DEVELOPMENT 29
~ 1mm
Figure 6. Laboratory-reared Anisotremus virginicus larva, 10.4 mm SL, 30 days old. Top: left lateral view; center: dorsal view; bottom: ventral view. dorsal process with the foramen ossified into the scapula at 8.2 mm SL (Fig. 12). Ventrad the dorsal process ossified into part of the coracoid also at 8.2 mm SL (Fig. 12, Table 4). In adults the scapula and coracoid are separated by a narrow strip of cartilage (Fig. 13). Four radials develop from the cartilaginous blade. The blade was a semicircular sheet of cartilage at first in the 3.5 mm NL specimen. A cleavage developed in the middle of the semicircle of the blade in the 3.8 mm NL specimen similar as shown for the 4.3 mm NL specimen in Figure 12 (Fritzsche and Johnson, 1980). At 5.7 mm SL, two more cleavages developed on either side of the first cleavage in the center (Fig. 12). The three cleavages elongate during development reaching the margins of the blade and thus separating the blade into four radials at 7.1 30 BULLETIN OF MARINE SCIENCE, VOL 34, NO.1, 1984
H 1mm
Figure 7, Laboratory-reared Anisotrernus virginicus juvenile, 20.4 mm SL, age unknown. Top: left lateral view; center: dorsal view; bottom: ventral view, mm SL. Ossification of the four cartilaginous radials started at 8.6 mm SL with the dorsalmost radial number 1. All four radials were ossifying in the 10.4 mm SL specimen (Fig. 12). The supratemporal of dermal origin was first observed in an 8.6 mm SL spec- imen and the intertemporal also of dermal origin in the 20.2 mm SL specimen (Fig. 12, Table 4). We did not have any material between the 10.4 mm SL and the 20.2 mm SL specimens, but we believe the intertemporal developed after 10.4 mm SL but before 20.2 mm SL. In adults the supratemporal is fused with the POTIHOFF ET AL.: AN/SOTREMUS LARVAL DEVELOPMENT 31
2 4 6 8 10 12 14 16 18 20 22 24 26 I I I I I I I I I I I I I
I I I I I I I I I I I I I I 2 4 6 8 10 12 14 16 18 20 22 24 26
Figure 8. Schematic representation of vertebral column, dorsal and anal fin, and pterygiophore development in laboratory-reared porkfish (Anisotremus virginicus). Cartilage, white; ossifying, stip- pled. Scale represents interneural and interhaemal space number and vertebra number.
intertemporal forming the tubular supratemporal-intertemporal bone of the laterosensory canal. The canal connects through the posttemporal (Fig. 13). The posttemporal, suprac1eithrum and the two postc1eithra are of dermal origin and were first observed at 5.7 mm SL (Table 4). Pelvic Fin and Supports. - Pelvic fin buds were first observed in the 6.4 mm SL specimen as very small protuberances postero-ventrad to the pectoral symphysis, but no basipterygia or fin rays could be seen. The next larger 7.1 mm SL A. virginicus had a cartilaginous basipterygium and a fin ray count of 1,3 (Tables 1, 4, 5). Pelvic rays were added from the outer edge of the fin toward the inside and adult fin ray counts ofl,5 were first obtained at 8.2 mm SL (Tables 1, 5). Ossi- fication of the basipterygia was first observed at 8.2 mm SL (Figs. 12, 13, Ta- ble 4). 32 BULLETIN OF MARINE SCIENCE, VOL. 34, NO. I, 1984
I ~m
I I I I : Nc I I I I I I I t- I
Figure 9. Left lateral view of the 5th precaudal centrum from AnisOlremus virginicus showing the ontogeny. Starting from the left the specimens' lengths (NL or SL) in mm were: top row, 4.3, 5.7, 7.5; bottom row, 10.1, 21.5, 168. EPL epipleural rib; NPo, neural postzygapophysis; NPr, neural prezy- gapophysis; Ns, neural spine; Pa, parapophysis; PI, pleural rib. Cartilage, white; ossifying, stippled.
First Dorsal Fin. - First dorsal fin elements developed first in a 6.2 mm SL spec- imen, which already had all second dorsal rays. Four elements were spines with pointed distal tips and two were rays with broad distal ends of a frayed appearance (Fig. 8, Tables I, 5) (Houde and Potthoff, 1976). The four spines were at the anteriormost and the rays were at the posteriormost portion of the fin with finfold and actinotrichia in between. The adult count of 12 elements (10 spines anteriorly followed by two rays) was obtained from a 7.1 mm SL specimen. All rays of the first dorsal fin develop into spines in specimens between 10.4 and 20.2 mm SL (Table I). Of 20 specimens with a full count of first dorsal fin elements (spines POTTHOFF ET AL.: ANISOTREMUS LARVAL DEVELOPMENT 33
~ , , , , ~ \).lmm
Figure 10. Left lateral view of the 13th centrum (3rd caudal) from Anisotremus virginicus showing the ontogeny. Starting from the left the specimens' lengths are the same as in Figure 9. C, centrum; HPo, haemal postzygapophysis; Hs, haemal spine. For other abbreviations see Figure 9. Cartilage, white; ossifying, stippled.
and rays), 18 had 12 elements, one had 11 and another had 13 (Table 1) (Miller and Jorgenson, 1973; Hoese and Moore, 1977). The base of all individual first dorsal fin spines was closed in adults (Fig. 14). First Dorsal Fin Supports. - In larvae of A. virginicus, cartilaginous first dorsal fin pterygiophores and three predorsa1 cartilages were first present in a 5.7 mm SL specimen (Figs. 8, 15). The fin spines had not formed in this larva. The next larger cleared and stained specimen 6.2 mm SL also had three cartilaginous predorsa1s and all first dorsal fin pterygiophores in cartilage. In this specimen the anteriormost two and the 7th, 8th, and 9th fin spines were not formed. Ossification of first 34 BULLETIN OF MARINE SCIENCE, VOL. 34, NO. I, 1984
Figure 11. Views of two centra from a 158 mm SL adult Anisotremus virginicus. The views and centra from left to right are: left lateral view of 7th precaudal centrum; anterior view of 7th precaudal centrum; lateral view of 8th precaudal centrum; anterior view of 8th precaudal centrum. Ha, first haemal arch. For other abbreviations, see Figure 9. dorsal fin pterygiophores first started with the predorsals and the anteriormost pterygiophores in larvae 8.2-8.8 mm SL. Ossification of the pterygiophores under the first dorsal fin was from anterior in a posterior direction on the proximal radials only. Distal radials were ossifying under the first dorsal fin at 20.2 mm SL (Figs. 8, 15, 16). Individual pterygiophores under the first dorsal fin and the three predorsals each originated from one piece of cartilage, except the first anteriormost pteryg- iophore, which originated from two pieces (Figs. IS, 16). On each pterygiophore a piece of distal radial cartilage separated from the proximal radial cartilage after fin spine formation. The cartilages then ossified to a distal and proximal radial (Figs. 15, 16). During ontogeny lateral and sagittal keels were added to the proximal radials and the anterior surfaces of the distal radials ankylosed to the proximal radials. The proximal ventral tips of the proximal radials remained cartilage in adults. The distal radials under the first dorsal fin developed posterior projections which hooked into the closed bases of the fin spines (Figs. 14, 16). On the first anteriormost pterygiophore, which developed from two pieces of cartilage, three distal radial projections developed for the support of three fin spines. The two anterior projections curved ventrad during ontogeny so that in adult A. virginicus the first two spines were held by ring-like structures atop the first pterygiophore (Fig. 14). Second Dorsal Fin. - Second dorsal fin rays developed first in the 5.7 mm SL specimen before first dorsal fin spines, but concurrently with anal fin spines and rays (Fig. 8, Tables 1, 5). Because in this 5.7 mm SL specimen the first anterior pterygiophore of the second dorsal fin and five posterior pterygiophores did not yet support rays we assumed that second dorsal fin rays develop from the center outward in an anterior and posterior direction. The next larger 6.2 mm SL A. virginicus had the full adult count of 16 rays with every second dorsal fin pteryg- iophore supporting a fin ray. All 21 specimens larger than 6.2 mm SL had the full second dorsal fin count of 15 to 18 rays (Tables 1, 5) (Miller and Jorgenson, 1973; Hoese and Moore, 1977); three A. virginicus had 15, 15 had 16, three had 17 and one had 18 rays. The last posteriormost second dorsal fin ray supported POTTHOFF ET AL.: ANISOTREMUS LARVAL DEVELOPMENT 35
'";:,: :::: ce ,~ ooooooo~o~"''''~'''~~'''~~o~oooooo :::: •. 111111111-1------M M~MMMMMMMMIMI I I I I I "'" M (""')M(""')f1")Mtt"'l '-0 ~ :; "0 ______N-N-NNNN o;S --.---...-..-..-- NVNVM~V~VV------"0 OOOOOOOOO~~~~~~~~~~~~~~~~~~ e:l .1.1111111------i5. ------111 I 1 I 1 1 o;S u
"0'" c "0 o;S Figure 12. Left lateral external view of the pectoral girdle from Anisotremus virginicus showing the ontogeny. Starting from the left the specimens' lengths were: top row, 4.3 mm NL, 5.7 mm SL; bottom row, 10.4 mm SL, 20.4 mm SL. A, anterior process of the coraco-scapular cartilage; B I, cartilaginous pectoral blade; Cl, cleithrum; Cor, coracoid; D, dorsal process of the coraco-scapular cartilage; Fnfld, pectoral finfold; P, posterior process of the coraco-scapular cartilage; Pelv, pelvic basipterygium; PstCl, postcleithrum; Pt, posttemporal; r, cartilaginous pectoral radials; R, major pectoral radials; Sc, scapula; ScF, scapular foramen; SCI, supracleithrum; St, supratemporal-intertemporal. Cartilage, white; ossi- fying, stippled. POTTHOFF ET AL.: ANISOTREMUS LARVAL DEVELOPMENT 37 Table 4. Development of bones and fin rays of the pelvic and pectoral girdles for 22 laboratory- reared Anisotremus virginicus 3.5 mm NL-21.5 mm SL Length at First Appearance in Length at First Evidence of Part Cartilage, mm NL or SL, Days Ossification, mm NL or SL, Days Cleithrum dermal origin? not known Scapula not known 8.2,2] Scapular foramen 5.7, ]5 Coracoid not known 8.2,2] Radials 1-4 7.],21 8.6-10.4,30 Supratem poral- intertem poral dermal origin Suprat. 8.8-10.1, 21-30; intert. > 10.4 but <20.2, >30 Posttemporal dermal origin 5.7, 15 Supracleithrum dermal origin 5.7, ]5 Postcleithrum I, 2 dermal origin 5.7, ]5 Pectoral fin rays 6.4, 15 Pelvic fin buds 6.4, 15 Pelvie fin rays 7.1,21 Pelvic basi pterygium 7.1,21 8.2,21 serially by a single pterygiophore was double (Fig. 17). All rays of the second dorsal fin had a bifurcated (open) base (Fig. 14). Second Dorsal Fin Supports. - Cartilaginous second dorsal fin pterygiophores were not developed in the 4.3 mm NL A. virginicus but were all present in the next longer 5.7 mm SL specimen (Fig. 8). Ossification of second dorsal fin pterygiophore proximal radials was first noticed in the 8.6 mm SL A. virginicus. However, not all specimens from 8.6 to 10.4 mm SL had ossifying proximal radials under the second dorsal fin. In the next larger 20.2 mm SL specimen all second dorsal fin proximal radials were ossified (Fig. 18). Ossification of the distal radials under the second dorsal fin was not observed in any of the laboratory-reared specimens Table 5. Summary offin development in laboratory-reared cleared and stained larvae of Anisolremus virginicus (PCR, principal caudal rays; SCR, secondary caudal rays) Length NL or SL. mm, Days All Specimens First Appearance of Have Spines Full Complement Number of Rays in Fin Spines or Rays or Rays of Spines or Rays Fully Developed Fin Caudal >4.3 but <5.7, 5.7, 15 >10.4 but <20.2, >30 12-13 + 9 + >8 but <15 8+12=41-42 PCR >4.3 but <5.7, 5.7, 15 5.7, IS 9+8 >8but<15 SCR 5.7, 15 5.7, 15 >10.4 but <20.2, >30 13 dorsal 12 ventral Pectoral 6.4, 15 6.4, 15 8.2-8.8,21 ]6-]8 Pelvic 7.1,21 7.1,21 8.2,21 1,5 First dorsal 6.2, 15 6.2, IS 7.1,21 Xl-XIII; most often Xll Second dorsal 5.7, 15 5.7, 15 6.2, 15 15-18; most often 16 Anal 5.7, 15 5.7, 15 7.1,21 III, 10-1 I; most often III, 10 38 BULLETIN OF MARINE SCIENCE, VOL. 34, NO. I, 1984 Figure 13. Left lateral external view of the pectoral girdle from an adult 158 mm SL A nisotremus virginicus. For abbreviations, see Figure 12. Cartilage, white; bone, stippled. 21.5 mm SL or smaller. The distal radials were fully ossified in the smallest available adult 140 mm SL. Ossification of the second dorsal fin pterygiophore proximal radials was from anterior in a posterior direction following the ossifi- cation of the proximal radials under the first dorsal fin (Fig. 8). Individual second dorsal fin pterygiophores originated from a single piece of cartilage. After fin ray formation a distal radial cartilage pinched off the pteryg- iophore cartilage, resulting in proximal and distal radial cartilages (Figs. 17, 18). These cartilages then ossified to the proximal and distal radials. During devel- opment lateral and sagittal keels were added to the proximal radials. The cartila- ginous second dorsal distal radials ossified to a bilateral two-bone structure (Fig. 14) which were held in adult A. virginicus between the bifurcate bases of the fin rays. The posteriormost second dorsal (and anal) fin pterygiophore had a stay, which is an extension of the proximal radial cartilage (Fig. 17). This stay ossified late during development between 21.5 and 140 mm SL. Middle radials did not develop on posterior pterygiophores of the second dorsal fin. Anal Fin.-Anal fin rays developed first in the 5.7 mm SL specimen (Tables 1, 5). The anteriormost spine and posteriormost double ray were not developed at POTTHOFF ET AL.: ANISOTREMUS LARVAL DEVELOPMENT 39 A R 1mm 1mm s C D Figure 14. Left lateral view of selected pterygiophores and anterior view of associated spines and rays from an adult Anisolremus virginicus, 168 mm SL. A, Ist and 2nd anteriormost first dorsal fin pterygiophores, three spines associated with first pterygiophore have been removed and are shown in anterior view. B, Ist three anteriormost anal pterygiophores, three spines associated with 1st pteryg- iophore and one ray associated with 2nd pterygiophore have been removed and are shown in anterior view. C, 4th anterior pterygiophore in second dorsal fin, the serially associated ray and distal radial have been removed and are shown in anterior view. D, 5th and 6th anterior pterygiophores in first dorsal fin, the serially associated spines have been removed and are shown in anterior view. D, distal radial; P, proximal radial; R, fin ray; S, fin spine. Cartilage, white; bone, stippled. 40 BULLETIN OF MARINE SCIENCE, VOL. 34, NO. I, 1984 .1mm 5mm Figure IS. Left lateral view of predorsal cartilages or bones and pterygiophores inserting into inter- neural spaces one to three showing the ontogeny in Anisotremus virginicus. Starting from the top the specimens' lengths in mm SL were: left side, 6.4, 6,2, 7.5; right side, 10.4,21.5, 168. Int, interneural space; Pd, predorsal cartilage or bone. For other abbreviations see Figure 14. Cartilage, white; ossifying, stippled. this size. In longer A. virginicus the anteriormost spine was not developed, but the double ray was. The 7. I mm SL specimen had the anteriormost spine. Two spines (e.g., the second and third) are at first rays and later develop into spines (Figs. 8, 19, Table I). Adult counts of 13 anal fin elements were first obtained in the 7.1 mm SL A. virginicus. The 20.4 mm SL specimen had only two spines and a fully developed ray; all three were supported by the first anal pterygiophore as were the three anal spines in all longer specimens (Fig. 19, Table I). In adults the three anal fin spines have a closed base similar to the first dorsal fin spines and the 10 anal rays have a bifurcated base similar to the second dorsal fin rays (Fig. 14) (Miller and Jorgenson, 1973; Hoese and Moore, 1977). POTTHOFF ET AL.: AN1SOTREMUS LARVAL DEVELOPMENT 41 Figure 16. Left lateral view of the 5th and 6th first dorsal fin pterygiophores showing the ontogeny in Anisotremus virginicus. The anterior spine shown is secondarily associated with the 5th pterygio- phore whereas the following spine is serially associated with the 5th pterygiophore. Starting from the left the specimens' lengths in mm SL were: top row, 6.4, 7.5, 10.4; bottom row, 21.5,168. Ns, neural spine. For other abbreviations, see Figures 14 and 15. Cartilage, white; ossifying, stippled. Anal Fin Supports. -Cartilaginous anal fin pterygiophores were not developed in the 4.3 mm NL A. virginicus but were all present in the next longer 5.7 mm SL specimen. Ossification of anal fin pterygiophore proximal and distal radials was the same as described for the second dorsal fin. Individual anal fin pterygiophore development of the proximal and distal radials and the stay was the same as described for the second dorsal fin pterygiophores, except for the anteriormost anal fin pterygiophore, which develops similar to the 42 BULLETIN OF MARINE SCIENCE, VOL. 34, NO.1, 1984 ~ '~". '---.-. lmm Stay Figure 17. Left lateral view of the posteriormost second dorsal fin pterygiophore showing the ontogeny in Anisotremus virginicus. Starting from the left the specimens' lengths in mm SL were: top row, 7.5, 10.1, 21.5; bottom, 168. For abbreviations, see Figure 14. Cartilage, white; ossifying, stippled. anteriormost first dorsal fin pterygiophore from two pieces of cartilage (Figs. 15, 19). A difference was noted, however, in the distal radial of the third spine. In adults this distal radial was free from the anteriormost proximal radial of the anal fin (Fig. 14). Middle radials did not develop on posterior anal fin pterygiophores. Fin Spine and Ray and Pterygiophore Associations. - Three spines were associated with the first anteriormost dorsal and anal fin pterygiophores (Figs. 14, 15, 19, 20). Two anterior spines were secondarily associated, the posterior spine was serially associated. The 21.5 mm SL A. virginicus had four spines associated with the anteriormost first dorsal fin pterygiophore (Fig. 15). The other dorsal and anal fin spines and rays were serially associated with one pterygiophore and secondarily Figure 18. Left lateral view of the 4th anterior second dorsal fin pterygiophore showing the ontogeny in Anisotremus virginicus. Starting from the left the specimens' lengths in mm SL were: 6.2, 10.1,21.5, 168. For abbreviations, see Figure 14. Cartilage, white; ossifying, stippled. POTTHOFF ET AL.: ANISOTREMUS LARVAL DEVELOPMENT 43 Figure 19. Left lateral view of the anteriormost two anal pterygiophores inserting into interhaemal spaces II and 12 showing the ontogeny in Anisolremus virginicus. Starting from the left the specimens' lengths in mm SL were: top row, 6.4, 7.5; center row, 10.4,21.5; bottom, 168. Hs, haemal spine. For other abbreviations, see Figure 14. Cartilage, white; ossifying, stippled. associated with the following posterior proximal radial (Figs. 15, 16, 19, 20). The posteriormost double ray ofthe dorsal and anal fins had no secondary association. The pterygiophores and predorsal bones of A. virginicus inserted into interneural and interhaemal spaces (Figs. 14-16, 19,20). The spaces were delineated by neural and haemal spines, but the first interneural space was anteriorly bounded by the skull and posteriorly by the first neural spine. The first interhaemal space was anteriorly bounded by the gut and posteriorly by the first haemal spine. In Figure 20, interhaemal spaces were numbered the same as the oppositely located inter- 44 BULLETIN OF MARINE SCIENCE, VOL. 34, NO.1, 1984 PR EDD.~~Al 8DN S FIRST DORSAL FIN SECOND DORSAL FIN 20 20 20 20 20 20 20 20 20 20 15 15 20 20 19 18 19 14 13 E o 0 3+1 1 1 1 1 1 1 1 1 2 2 2 2 2 222 0 1 2 2 1 1 1 1 1 1 1 1 2 2 2 2 2 222 C 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 8 /' 1'+~«11I 213 14 I 51 617 18 19110111112113114115116117118119120121122123124125126 11 12 13 14 15 16 17 18 19 8 ~ 1 1 1 1 1 2 2 2 0 C 3 1 1 1 1 2 2 200 19 19 20 19 19 20 17 15 18 E ANAL FIN Figure 20. Common arrangement of predorsal bones, pterygiophores, fin spines and rays in relation to the skull and vertebral column for 20 Anisotremus virginicus. Modified after Matsui (1967). A, skull and vertebrae numbers; B, interneural and interhaemal space numbers; C, number of pteryg- iophores in the respective interneural or interhaemal space; D, number of fin spines or rays associated with the pterygiophore; E, frequency of occurrence in 20 specimens for the pterygiophore number in the respective interneural or interhaemal spaces. ~: Hs Hy, : Ph >------< 025 Fnlld RC c S 025 Hy5 ~ 05c) ~ .1mm Figure 21. Left lateral view of the caudal complex showing the ontogeny in Anisotremus virginicus. Structure in square shows hypural 5 and associated radial cartilage enlarged from a 21.5 mm SL specimen. Starting from the left the specimens' lengths in mm SL were: top, 4.3, 5.7; bottom, 10.4, 20.4. Ep, epural; Fnfld, finfold; HPr, haemal prezygapophysis; Hs, haemal spine; Hy, hypural bone; "Na," specialized neural arch; Nc, notochord; NPr, neural prezygapophysis; Ns, neural spine; PCR, principal caudal rays; Ph, parhypural; Pu, preural centrum; r, basally shortened secondary caudal ray; R, posteriormost ventral secondary caudal ray with procurrent spur; RC, radial cartilage; SCR, sec- ondary caudal rays; Un, uroneural; Ur, urostyle. Cartilage, white; ossifying, stippled. POTIHOFF ET AL.: AN/SOTREMUS LARVAL DEVELOPMENT 45 Figure 22. Left lateral view of the caudal complex of an adult Anisotremus virginicus, 158 mm SL. For abbreviations, see Figure 21. Cartilage, white; bone, stippled. neural spaces; thus the first interhaemal space was designated number 11. Figure 20 shows the common pattern of the number of pterygiophores and predorsal bones inserting into each interneural and interhaemal space and the common number of spines and fin rays associated with the inserting pterygiophores. The insertion pattern was constant for the predorsal bones and first dorsal fin pteryg- iophores except the last one. There was variability of the insertion pattern under the second dorsal and above the anal fins. The second dorsal fin supports always terminated in the 19th interneural space, the anal fin supports terminated in 20 A. virginicus 18 times in the 18th and two times in the 19th interhaemal space. Caudal Fin. -Caudal fin rays were first seen in a 5.7 mm SL flexion larva (Tables 1, 5). This specimen had the full principal ray count (9/8) and one ventral sec- ondary ray. The dorsal and ventral secondary rays were added in an anterior direction. Full caudal counts of 41-42 rays were attained in larvae between 10.4 and 20.2 mm SL (Tables 1, 5). The low secondary caudal fin ray count obtained by Miller and Jorgenson (1973) was probably due to their examination of radio- graphs and not counting cleared and stained material, thus overlooking some small anterior secondary caudal rays. In juvenile and adult A. virginicus the upper caudal lobe usually had 22 rays whereas the lower lobe had 20. A procurrent spur (Johnson, 1975) on the posteriormost ventral secondary caudal ray and an an- teriorly adjacent basally shortened secondary ray (Figs. 21, 22) were present in juveniles and adults. The posteriormost ventral secondary ray was first present 46 BULLETIN OF MARINE SCIENCE, VOL. 34, NO. I, 1984 Table 6. Acquisition of cartilage and ossification of the various parts in the caudal complex of laboratory-reared Anisotremus virginicus Length Range (mm, NL or SL) Length Range (mm, NL or SL) of First Appearance in Canilage of First Evidence of Ossification PU) Centrum 6.2 Neural spine (PU» 5.7 6.2-9.0 PU2 Centrum 6.2 Specialized neural arch (PU2) 5.7 8.6-10.4 Epural, anterior 5.7 8.6-10.4 middle 5.7 8.6> 10.4<20.2 posterior 5.7 8.6> 10.4<20.2 Uroneurals 6.2-7.5 Hypural5 5.7 8.6 Hypural4 5.7 5.7-8.2 Hypural3 5.7 5.7-8.2 Hypural2 5.7 5.7-8.2 Hypural I 3.5-4.3 5.7-8.2 Parhypural 3.5-4.3 5.7-7.1 Urostyle 6.2 Haemal spine (PU2) 3.5-4.3 5.7-8.2 Haemal spine (PU) 5.7 5.7-6.4 Dorsal radial cartilage 6.2 Ventral radial cartilage 9.6 at 5.7 mm SL, but the procurrent spur on that ray was first seen in a 20.2 mm SL juvenile. The anteriorly adjacent basally shortened secondary ray was first observed in a 7.1 mm SL larva (Figs. 21, 22). Caudal Fin Supports. - The caudal fin rays were supported by some of the bones and cartilage of the caudal complex and three centra were involved in the support (Figs. 21, 22). The caudal complex bones and cartilage of A. virginicus were: urostyle, pre ural centrum 2 and preural centrum 3, one neural spine with distal articular cartilage, one specialized neural arch, three epurals, two pairs of uro- neurals, five autogenous hypural bones, one autogenous parhypural, two autog- enous haemal spines and three ventral radial cartilages (Figs. 21, 22). These bones and cartilages were seen during development and no ontogenetic fusion was ob- served. Between 2.4 and 4.3 mm NL, A. virginicus had a straight notochord in the caudal area. Notochord flexion was between 4.3 mm NL and 5.7 mm SL. Before notochord flexion in the 3.5 and 4.3 mm NL specimens, the haemal spine ofPU2, the parhypural and hypural 1 were seen developing from cartilage posteriorly and ventrad to the notochord (Fig. 21). The 3.8 and 3.9 mm NL specimens showed no caudal complex development. The 5.7 mm SL specimen had a flexed noto- chord. Posteriorly and ventrad, two autogenous haemal spines, a parhypural and hypurals 1-4 were just beginning to ossify and hypural 5 was present in cartilage. Dorsad, the neural spine of PU 3, the specialized neural arch of PU 2 and three epurals were present in cartilage. Two uroneural pairs were first present at 6.2 mm SL. The development and ossification sequence of all hypural complex parts is shown in Table 6. The two autogenous haemal spines of PU 3 and PU 2 are connected by cartilage to the centra, but this connection gets smaller and disappears during development POTTHOFF ET AL.: ANISOTREMUS LARVAL DEVELOPMENT 47 Figure 23. Left lateral view of the radial cartilages and their relationship to the haemal spines of the caudal complex during ontogeny of Anisotremus virginicus. Starting from the left the specimens'lengths in mm SL were: top row, 7.1, 10.4; bottom row, 20.4, 159. Art, articular cartilage. For other abbre- viations, see Figure 21. Cartilage, white; ossifying, stippled. (Figs. 21, 22). The parhypural and hypurals I to 5 developed from separate pieces of cartilage. Hypurals 5, 4 and 3 stayed separate during development, but hypurals 2, I and the parhypural were joined by cartilage at 5.7 mm SL. This cartilaginous connection gradually disappeared during development (Figs. 21, 22). Three radial cartilages were present ventrally in the hypural complex in larval, juvenile, and adult A. virginicus and were first observed in a 6.2 mm SL specimen (Figs. 21-23, Table 6). The anteriormost radial cartilage was the largest; in larvae it was situated proximally between the tips of the autogenous haemal spines of PU2 and PU) and three to four secondary caudal rays articulated with it (Figs. 21-23). Posterior to the largest radial cartilage and at the very tip of the autogenous haemal spine of PU 2 was the smallest piece of radial cartilage. The posteriormost cartilage was medium-sized and located between the proximal tips of the auto- genous haemal spine of PU2 and the parhypural. In larvae to 10.4 mm SL the Table 7. Distribution of the principal caudal rays over the bones of the hypural complex in 15 laboratory-reared larval (5.7-10.4 mm SL), 3 laboratory-reared juveniles (20.2-21.5 mm SL) and 5 captured adult (140-168 mm SL) Anisotremus virginicus Number of Principal Caudal Rays Larvae Juveniles Adults 4 a Hypural5 12 3 3 2 2 Hypural4 12 3 3 3 Hypural3 I 5 9 3 I 3 Hypural2 2 13 3 4 Hypurall 7 8 2 3 Parhypural 6 9 I 3 Radial cartilage 15 3 4 Haemal spine ofPU2 15 3 4 48 BULLETIN OF MARINE SCIENCE, VOL. 34, NO.1, 1984 Figure 24. Left lateral external view of the left hyoid arch showing ontogeny in Anisotremus virginicus. Starting from the left the specimens' lengths in mm NL or SL were: top row, 4.3, 7.5; center row, 10.1, 20.2; bottom row, 158. Br, branchiostegal ray; CH, ceratohyal; DHH, dorsal hypohyal; EH, epihyal; IH, interhyal; VHH, ventral hypohyal. Cartilage, white; ossifying, stippled. ventralmost principal caudal ray articulated with the posteriormost medium-sized cartilage (Fig. 21, Table 7). During development the three radial cartilages grad- ually changed position to between the autogenous haemal spines ofPU2 and PU3 as shown for the adult in Figures 22 and 23. Two separate pieces of cartilage at the proximal tips of the haemal spine of PU2 and the parhypural were only observed in adults (Fig. 23). Dorsally one radial cartilage was present in larvae, juveniles and adults at the distal tip of hypural 5 and between the base of the dorsalmost principal caudal ray (Fig. 21). This dorsal cartilage developed later than the ventral cartilages and was first seen in a 9.6 mm SL specimen (Table 6). The principal caudal rays articulated with the five hypural bones, the parhypural and the posteriormost radial cartilage in larval A. virginicus up to 10.4 mm SL (Fig. 21, Table 7). In juvenile specimens (20.2-21.5 mm SL) the ventral most principal caudal ray still articulated with the medium-sized radial cartilage, and in addition it also articulated with the haemal spine ofPU2 (Fig. 21, Table 7). In adult A. virginicus the ventralmost principal caudal ray only articulated with the haemal spine of PU 2, because the radial cartilage had moved between the haemal spines of PU2 and PU3 (Figs. 22, 23, Table 7). Branchiostegal Rays and Supporting Hyoid Arch. - Branchiostegal rays were pres- ent in all cleared and stained A. virginicus larvae> 3.5 mm NL (Fig. 24, Table 3). Specimens 5.7 mm NL and longer had the adult complement of 7 branchio- stegal rays on each side (Fig. 24, Table 3). Development of the rays was from posterior (epihyal) in an anterior direction (ceratohyal). POTTHOFF ET AL.: ANISOTREMUS LARVAL DEVELOPMENT 49 C1-5 @ UP3,4 ·5mm UP2-4 Figure 25. The branchial skeleton of two laboratory-reared Anisotremus virginicus; top, 3.9 mm NL; bottom, 5.7 mm SL. The dorsal view is shown for the lower left and right arches; the upper arches have been cut and the ventral view is shown for the left upper arch and the dorsal view is shown for the right upper arch. The infrapharyngobranchiall is not shown in the drawing at the top, it probably was lost during dissection. B, basibranchial; BC, basibranchial cartilage ofBI-3; C, ceratobranchial; E, epibranchial; H, hypobranchial; I, infrapharyngobranchial; IC, interarcual cartilage; PROC-E, pro- cess on epibranchial; UP, upper pharyngeal tooth plate ventrad on infrapharyngobranchial. Cartilage, white; ossifying, stippled. 50 BULLETIN OF MARINE SCIENCE, VOL. 34, NO. I, 1984 81-4 H 1-3 c: IC "'" PROC-E1 PROC-E3 ~ E1-4 Figure 26. The branchial skeleton of a laboratory-reared 7.1 mm SL Anisotremus virginicus. For explanations of the views and abbreviations, see Figure 25. Cartilage, white; ossifying, stippled. The branchiostegal rays were directly and indirectly supported by a number of bones called the hyoid arch (McAllister, 1968). Anteriorly the hyoid arch con- nected with the dorsal and ventral hypohyal to basibranchial I of the branchial arch. Posterior to the hypohyals was the ceratohyal, which supported 5 branchi- ostegal rays (Fig. 24). Sutured posteriorly with the ceratohyal was the epihyal, which supported 2 rays. Articulating posterodorsad with the epihyal was the interhyal, which connected the hyoid arch to the hyomandibular bone. The bones in the hyoid arch developed from cartilage (Fig. 24), except the branchiostegal rays, which were of dermal origin. Only the interhyal cartilage ossified into a single bone. The hypohyal cartilage had a foramen and ossified into two hypohyal bones with the dorsal hypohyal retaining the foramen. The epi-ceratohyal cartilage ossified into two bones, the epihyal and the ceratohyal. These two bones sutured during ontogeny (Fig. 24). Gil/rakers and Branchial Skeleton. -Only outer row gillrakers of the first gill arch were counted in A. virginicus. The 3.9 and 4.3 mm NL larvae had no outer row first arch gillrakers developed (Fig. 25, Table 3). Three gillrakers were first ob- served in a 3.8 mm NL larva posteriorly on the ceratobranchial but not in the epi-ceratobranchial angle. Rakers were added on the ceratobranchial in an anterior direction. The raker in the epi-ceratobranchial angle and rakers on the posterior portion ofthe epibranchial were first observed in the 5.7 mm SL larva and rakers over the posterior portion of the hypobranchial first appeared in the 7.1 mm SL A. virginicus (Figs. 25, 26, Table 3). Addition of rakers on the epibranchial and hypobranchial was in an anterior direction. The ceratobranchial was the first bone to have the full count of 10 or 11 gillrakers at 6.2 mm SL (Table 3) and all specimens 8.6 mm SL and longer had the full ceratobranchial count. The full complement of 5 or 6 rakers over the hypobran- chial was first observed in the 20.2 mm SL specimen (Table 3). The full count of 10 to 12 rakers over the epibranchial was first seen in the 21.5 mm SL specimen. Total adult counts of 26 to 29 gillrakers were also first seen in the 21.5 mm SL specimen (Table 3) (Hoese and Moore, 1977). POTTHOFF ET AL.: ANISOTREMUS LARVAL DEVELOPMENT 51 UP2-4 Figure 27. The branchial skeleton of a laboratory-reared 10.4 mm SL Anisolremus virginicus. For explanations of the views and abbreviations, see Figure 25. Cartilage, white; ossifying, stippled. The branchial skeleton of A. virginicus (Figs. 25-29) consisted of a lower and upper portion. The lower portion had five paired ceratobranchials and three paired hypobranchials were found on arches 1 to 3. Single basibranchials were present on arches I to 4, the 4th basibranchial being cartilaginous in the adult (Fig. 29). Outer and inner rows of gillrakers of various shapes developed on each of the lower arches 1 to 4. The 5th arch, consisting only of a paired ceratobranchial, developed a tooth plate over its dorsal surface. The upper portion of the branchial skeleton had arches I to 4 consisting of four epibranchials and four infrapharyngobranchials. Outer row gillrakers developed on all four epibranchials; however, epibranchial 4 developed only one raker (Fig. 29). Inner row rakers developed on epibranchials I to 3; the inner row on epi- branchial 3 consisted of only one raker (Fig. 29). An autogenous tooth plate de- veloped posteriorly on the ventral surface on epibranchial 2 and a small non- autogenous toothplate developed on epibranchial 3 in the 21.5 mm SL specimen, but was absent in adults (Figs. 28, 29). Infrapharyngobranchial I served as a suspensory element and infrapharyngobranchials 2 to 4 developed the upper pharyngeal toothplates 2 to 4 on the ventral side (Figs. 25-29). A process was present anteriorly on epibranchial 1 and posteriorly on epibran- chial 3 (Figs. 25-29). Anteriorly to the epibranchial 1 process, connecting epi- branchial 1 dorsally with infrapharyngobranchial 2, was the interarcual cartilage. The process on epibranchial 3 extended dorsally to epibranchial 4. The branchial arches develop from cartilage (endochondral elements) with gill- rakers and toothplates (dermal elements) developing outside the cartilage (Figs. 25-29). Basibranchials 1 to 3 ossified from one piece of cartilage. The branchial skeleton was present in cartilage in the 3.7 mm NL specimen; the 3.5 mm NL specimen was not available for the examination of the branchial skeleton. Dermal 52 BULLETIN OF MARINE SCIENCE. VOL. 34. NO. I, 1984 Figure 28. The branchial skeleton of a laboratory-reared 21.5 mm SL Anisotremus virginicus. For explanations of the views and abbreviations, see Figure 25. Cartilage, white; ossifying, stippled. elements ossified first as upper pharyngeal tooth plates ventrad on the cartilaginous infrapharyngobranchials 3 and 4 (Fig. 25) followed by outer gillrakers on the ceratobranchials and a toothplate on infrapharyngobranchial 2 (Fig. 26). All en- dochondral skeletal parts (except basibranchial 4, which remains cartilaginous in adults) were ossifying when inner row rakers started forming first on ceratobran- chial 2 and 3 (Fig. 26). Later, inner row rakers developed on ceratobranchials 1 and 4 (Fig. 27). Last to develop were the inner row rakers on the epibranchials and the ventral toothplate on epibranchial 2 (Fig. 28). Opercular Series. - The dermal bones of the opercular series in A. virginicus were the opercle, subopercle, preopercle and interopercle (Fig. 30). The preopercle is the most visible in larvae not cleared and stained (Figs. 1-7) and developed first in larvae 3.5 mm NL. The interior shelf of the preopercle developed from 10 to 13 short spines (Fig. 30) in juvenile A. virginicus of about 20 mm SL. In adults the edge of the spine-bearing interior shelf became serrated. The exterior shelf of the preopercle (Fig. 30) had 2 or 3 small spines in larvae 3.5 mm NL-9.0 mm SL. These spines disappeared in larvae longer than 9.0 mm SL as the outer edge of the exterior shelffused to the interior shelf forming a canal of the laterosensory system. The opercle, subopercle and interopercle were first present in a 5.7 mm SL specimen. The opercle developed one inconspicuous spine at 9.0 mm SL, which is retained in adults (Fig. 30). The subopercle developed from 1 to 3 spines in specimens 5.7-10.4 mm SL, but the spines were overgrown by bone in the next longer 20.2-21.5 mm SLjuveniles. The interopercle developed 2 to 4 small spines, POTfHOFF ET AL.: ANISOTREMUS LARVAL DEVELOPMENT 53 11 Figure 29. The branchial skeleton of an adult 158 mm SL Anisotremus virginicus. For explanations of the views and abbreviations, see Figure 25. Cartilage, white; bone, stippled. which were present on the interopercles of the 20.2-21.5 mm SL juveniles but absent on the adult interopercles. DISCUSSION In the following we discuss the developmental and osteological features of Anisotremus virginicus, a percoid fish with few specializations, and compare them to the features of other perciform fish that we studied in the past. In external morphology, A. virginicus larvae most closely resemble sparids but have a distinctive caudal tail spot (Figs. 2-7) (Houde and Potthoff, 1976). A. virginicus larvae have 26 myomeres, the typical count for haemulids, which sep- arates haemulids from most other percoids in the North Atlantic. Of the percoid families in the North Atlantic examined by Miller and Jorgenson (1973), only four serranids, two carangids, one sciaenid, and the inermiids, kyphosids and pomacentrids had 26 vertebrae. Kendall (1979) reported all North American Serraninae and Epinephelinae with 24 vertebrae, but all Anthiinae and one gram- mistine genus with 26 vertebrae. First appearance and location of cartilaginous neural and haemal arches along the notochord have only recently been studied in fishes because of the late intro- duction of the cartilage staining technique with alcian blue by Dingerkus and Uhler (1977). Potthoff and Kelley (1982) described neural and haemal arch de- velopment in Xiphias gladius and Potthoff is now studying this development in istiophorids. Initial development of neural and haemal arches is the same in both billfish families but differs in A. virginicus. In billfish, appearance of dorsally opened neural arches is anterior on the notochord and addition of neural arches 54 BULLETIN OF MARINE SCIENCE, VOL. 34, NO. J, J 984 Figure 30, Left lateral external view of the opercular series showing the ontogeny in Anisotremus virginicus. Starting from the left, the specimens' lengths in mm NL or SL were: top row, 4.3, 5.7, 9.6; bottom row, 20.4, 163, ES, exterior shelf; lOP, interopercle; IS, interior shelf; OP, opercle; POP, preopercle; SOP, subopercle. is in a posterior direction. Fritzsche and Johnson (1980) reported on neural and haemal arch development in species of Morone. The development of the arches in Morone differs from A. virginicus in that Morone develops dorsally opened neural arches from anterior to posterior, but haemal arches develop from a center anteriorly and posteriorly. [n contrast, A. virginicus develops dorsally opened cartilaginous neural arches anteriorly simultaneously with neural and haemal arches at the center of the notochord (Fig. 8). It is possible that the early devel- opment sequence of the neural and haemal arches in billfish represents an evo- lutionary advance over the different sequence of A. virginicus. Ossification se- quence of the neural and haemal arches is anterior to posterior in billfish, species of Morone, and A. virginicus as well as in the Scombridae (Potthoff, 1975), Spar- idae (Houde and Potthoff, 1976), Coryphaenidae (Potthoff, 1980), Scombrola- bracidae (Potthoff et aI., 1980). In the Scombridae (Potthoff, 1975), species of Marone (Fritzsche and Johnson, 1980), and Centropomidae (Lau and Shafland, 1982), as well as A. virginicus, the urostyle and preural centra 2 and 3 ossify from posterior to anterior. The arrangement of paired epipleural and pleural ribs in A. virginicus is typically POTTHOFF ET AL.: AN/SOTREMUS LARVAL DEVELOPMENT 55 percoid (Johnson, 1981). We found that in A. virginicus the pleural ribs develop initially as cartilage while the epipleural ribs develop initially as bone as in the species of Morone (Fritzsche and Johnson, 1980). Cartilaginous rib development also occurs in the highly modified ribs of Xiphias gladius (Potthoff and Kelley, 1982) and in the pleural ribs of istiophorids (Potthoff, personal observation). Emelianov (1935) determined histologically that rib development in bony fishes is variable. He reported that epipleural and pleural ribs may develop initially as cartilage, partially as cartilage and partially as connective tissue ossifications, or totally develop as connective tissue ossifications. Development of the pectoral fin and fin supports in A. virginicus does not differ (except in the absence or presence of a supratemporal-intertemporal bone and in the number of postdeithra) from other perciforms studied thus far (Houde and Potthoff, 1976; Fritzsche and Johnson, 1980; Potthoff, 1980; Potthoffet aI., 1980; Potthoff and Kelley, 1982). In their study on the species of Morone Fritzsche and Johnson (1980) were the first to describe a cartilaginous blade next to the coraco- scapular cartilage. This blade gives rise to the four major ossified proximal radials in perciforms (Potthoff and Kelley, 1982). In A. virginicus and in istiophorids cartilaginous distal radials occur between the bases of every pectoral fin ray and remain cartilaginous in the adults. The dorsalmost cartilaginous radial develops from the dorsal process of the coraco-scapular cartilage and the remainder develop from the distal edge of the cartilaginous blade. It is probable that most or all perciforms have these cartilaginous distal radials in the pectoral fin. The pelvic fin and basipterygia in A. virginicus develop last. Some perciforms studied by us have a reduced pelvic fin such as the istiophorids, gempylids and trichiurids or they lost their pelvic fin and basipterygia entirely such as Xiphias gladius. In A. virginicus the second dorsal and anal fins are the first to develop (Fig. 4). This is the most common developmental pattern among perciform fishes. Some examples are the Coryphaenidae (Potthoff, 1980; Shuzhen and Zhenran, 1981), Centropomidae (Lau and Shafland, 1982), Haemulidae (Orthopristis, B. Watson'sl manuscript), Xiphiidae (Potthoff and Kelley, 1982), Amarsipidae, Centrolophidae and Tetragonuridae (Ahlstrom et aI., 1976), Sphyraenidae (Houde, 1972), Spari- dae (Houde and Potthoff, 1976), Scombrolabracidae (Potthoff et aI., 1980), Mo- rone a primitive percoid (Fritzsche and Johnson, 1980), and most serranine Ser- ranidae (Kendall, 1979). In other perciform families, usually more advanced, dorsal fin rays or spines develop first anteriorly and second dorsal and anal finray development starts after the first dorsal fin is either fully or partially developed. Examples are the Istio- phoridae (Potthoff, personal observation), Scombridae (Matsumoto, 1959; Mat- sumoto et aI., 1972; Potthoff, 1975) except Scomber and Rastrelliger (Kramer, 1960; Matsui, 1963), Gempylidae (Voss, 1954), Nomeidae (Ahlstrom et aI., 1976), Lutjanidae (Laroche, 1977; Collins et aI., 1980; Richards and Saksena, 1980), and anthiine, epinepheline and grammistine Serranidae (Kendall, 1979). Predorsal bone and pterygiophore arrangement in A. virginicus exhibits the basic pattern of lower percoids where the predorsal bones occupy interneural spaces 1, 2, and sometimes 3, and where the first dorsal pterygiophore inserts into interneural space 3 (Smith and Bailey, 1961; Berry, 1969; Ahlstrom et aI., 1976; Houde and Potthoff, 1976; Kendall, 1976; Fritzsche and Johnson, 1980; Johnson, 1981). A few more specialized perciform families such as the Scombri- dae, Scombrolabracidae, Gempylidae (two exceptions), Trichiuridae, Xiphiidae, Istiophoridae and Coryphaenidae lack predorsal bones. In the Scombridae and Scombrolabracidae the anteriormost pterygiophore remains in the third inter- 56 BULLETIN OF MARINE SCIENCE, VOL. 34, NO. I, 1984 neural space, but it is found in the second interneural space in the Gempylidae, Trichiuridae and Xiphiidae, and in the first interneural space in the Istiophoridae and Coryphaenidae (Potthoff, 1975; 1980; Potthoff et al., 1980; Potthoff and Kelley, 1982; Potthoff, personal observation for Istiophoridae). The anteriormost dorsal and anal pterygiophore in A. virginicus supports two spines in a secondary association and one spine in a serial association as in the species of Marone (Fritzsche and Johnson, 1980). These pterygiophores were also fusions of two cartilages in A. virginicus and Marone. We believe the basic con- dition in Perciformes is when three spines are supported by the first dorsal and anal pterygiophores as shown by Kendall (1976) in the Serraninae and Anthiinae for the anteriormost dorsal pterygiophore. Loss of secondarily associated spines on the anteriormost dorsal pterygiophore apparently represents an evolutionary advance as found in some Carangidae and in the Scombridae, Scombrolabracidae, Gempylidae and Trichiuridae (Berry, 1969; Potthoff, 1975; Potthoff et al., 1980). In the Coryphaenidae and Xiphiidae the number of rays secondarily associated with the anteriormost dorsal pterygiophore varied from none to two (Potthoff, 1980; Potthoff and Kelley, 1982). Most perciforms have a large first anal pteryg- iophore (representing fusion of two cartilages), which supports two spines sec- ondarily and one spine serially. Examples are: Gempylidae (Potthoff, personal observation), Scombridae (Potthoff, 1975), Sparidae (Houde and Potthoff, 1976), and Scombrolabracidae (Potthoff et al., 1980). The Coryphaenidae (Potthoff, 1980) and Xiphiidae (Potthoff and Kelley, 1982) are exceptions where from none to two spines are secondarily supported by the anteriormost anal fin pterygiophore. A. virginicus develops a stay with the posteriormost dorsal and anal pterygio- phores (Fig. 17). Although stays have not been studied extensively in the perci- forms, most families develop them (G. D. Johnson, personal communication3). We know only of two examples without stays, the coryphaenids (Potthoff, 1980) and the carangid Elagatis (Berry, 1969). The pterygiophores in the posteriormost portions of the dorsal and anal fins lacked middle radials in A. virginicus, This is characteristic of haemulids and believed to be an advanced condition since most Perciformes have from one to many middle radials (Eaton, 1945; Berry, 1969; Potthoff, 1974; 1975; Houde and Potthoff, 1976; Potthoff et al., 1980; Johnson, 1981). Other fishes that do not develop middle radials are the Coryphaenidae (Potthoff, 1980) and the Xiphiidae (Potthoff and Kelley, 1982). The caudal fin and supporting elements in A. virginicus are typical of lower percoids (Gosline, 1961a; Johnson, 1981): preural centrum 3 with a neural spine tipped with cartilage and an autogenous haemal spine also tipped with cartilage, preural centrum 2 with a specialized neural arch and an autogenous haemal spine tipped with cartilage, urostyle with three epurals, two paired uroneurals, five hypurals and a parhypural. There is no fusion of adult caudal skeleton parts and a procurrent spur (Johnson, 1975) is present. Some examples of advanced caudal skeletons where fusions and loss of parts can be seen are in the coryphaenids (Potthoff, 1980), carangids (Berry, 1969), scombrids (Potthoff, 1975), xiphiids (Potthoff and Kelley, 1982), and many others (Monod, 1968). Radial cartilages were present in the caudal complex of A. virginicus ventrally anterior to the haemal spine of preural centrum 2 and dorsally distad to hypural 5. This condition is considered advanced since primitively radial cartilages are present dorsally an- :\ Marine Resources Research Institute, South Carolina Wildlife and Manne Resources Department, P.O. Box 12559, Charleston, SC 29412. POTTHOFF ET AL.: ANISOTREMUS LARVAL DEVELOPMENT 57 tenor to the neural spine of preural centrum 3 and ventrally anterior to the haemal spines of preural centra 2 and 3 in the Ambassidae, Apogonidae, Centrarchidae, Kyphosidae and Girellidae (Johnson, 1983). Lau and Shaftand (1982) reported the same primitive condition for the Centropomidae (but the preural centra were mislabeled by them in the figures and text) and Fritzsche and Johnson (1980) for Marone. Radial cartilages in the hypural complex of fishes have been studied only for a relatively short time but the systematic possibilities are large as Kendall pointed out in the American Society ofIchthyologists and Herpetologists meeting at Corvallis, Oregon in 1981 (Copeia 1981: 935). The branchial skeleton of A. virginicus is typical of other lower percoids as defined by Johnson (1981). However, we were able to determine, through a de- velopmental series of the branchial skeleton, that the endoskeletal element of infrapharyngobranchial 4 is present as a small cartilage to which the upper pha- ryngeal tooth plate developed ventrad; nonautogenous ossifications in the form of teeth developed on epibranchial 3 which are labeled TP-E3 in Figure 28. This epibranchial 3 toothplate is not present in the adult because it becomes overgrown by bone. ACKNOWLEDGMENTS We thank the following persons for reviewing the manuscript: B. B. Collette, E. D. Houde, G. D. Johnson, M. McGowan, P. Keener Ashe, W. J. Richards and W. Watson. G. D. Johnson discussed with T. Potthoff aspects of osteology and development. J. Javech drew Figures 6 and 1L 1. Cerwin recorded some osteological data. P. Fisher and G. L. Morina typed many manuscript drafts. This paper is contribution number 83-0 IM of the National Marine Fisheries Service, NOAA, Southeast Fisheries Center, Miami Laboratory. LITERATURE CITED Acero P., A. and J. Garz6n F. 1982. Rediscovery of Anisotremus moricandi (Perciformes: Hae- mulidae), including a redescription of the species and comments on its ecology and distribution. Copeia 1982: 613-618. Ahlstrom, E. H., J. L. Butler and B. Y. Sumida. 1976. Pelagic stromateoid fishes (Pisces, Perciformes) of the Eastern Pacific: kinds, distributions and early life histories, and observations on five of these from the Northwest Atlantic. Bull. Mar. Sci. 26: 285-402. Berry, F. H. 1969. Elagatis bipinulata (Pisces: Carangidae): morphology of the fins and other char- acteristics. Copeia 1969: 454-463. Collins, L. A., J. H. Finucane and L. E. Barger. 1980. Description of larval and juvenile red snapper Lutjanus campechanus. Fishery Bull. U.S. 77: 965-974. Courtenay, W. R., Jr. 196 L Western Atlantic fishes of the genus Haemulon (Pomadasyidae): sys- tematic status and juvenile pigmentation. Bull. Mar. Sci. Gulf Caribb. II: 66-149. de Sylva, D. P. 1970. Ecology and distribution of postlarval fishes of southern Biscayne Bay, Florida. Prog. Rept. to U.S. Environm. Protec. Agency, Div. Water Quality Res., Washington, D.C. 198 pp. Dingerkus, G. and L. D. Uhler. 1977. Enzyme clearing ofalcian blue stained whole small vertebrates for demonstration of cartilage. Stain Tech. 52: 229-232. Eaton, T. H., Jr. 1945. Skeletal supports of the median fins of fishes. 1. Morph. 76: 193-212. Emelianov, S. W. 1935. Die Morphologie der Fischrippen. Zool. Jahrb., Abt. Anat. Ontog. Tiere 60: 133-262. Fritzsche, R. A. and G. D. Johnson. 1980. Early osteological development of white perch and striped bass with emphasis on identification of their larvae. Trans. Am. Fish. Soc. 109: 387-406. Gosline, W. A. 1961a. The perciform caudal skeleton. Copeia 1961: 265-270. --. 1961b. Some osteological features of modern lower teleostean fishes. Smithson. Misc. Collns. 142: 1-42. Harrington, R. W. 1955. The osteocranium of the American cyprinid fish, Notropis bifrenatus, with an annotated synonymy of teleost skull bones. Copeia 1960: 210-215. Hildebrand, S. F. and L. E. Cable. 1930. Development and life history of fourteen teleostean fishes at Beaufort, N.C. Bull. U.S. Bur. Fish. 46: 383-488. 58 BULLETIN OF MARINE SCIENCE, VOL. 34, NO.1, 1984 Hoese, H. D. and R. H. Moore. 1977. Fishes of the GulfofMexico: Texas, Louisiana, and adjacent waters. Texas A&M University Press, College Station, Texas and London. 327 pp. Houde, E. D. 1972. Development and early life history of the northern sennet, Sphyraena borealis DeKay (Pisces: Sphyraenidae) reared in the laboratory. Fishery Bull. U.S. 70: 185-195. --- and T. Potthoff. 1976. Eggand larval development of the sea bream Archosargus rhomboidalis (Linnaeus): Pisces, Sparidae. Bull. Mar. Sci. 26: 506-529. Johnson, G. D. 1975. The procurrent spur: an undescribed perciform caudal character and its phylogenetic implications. Occ. Pap. Calif. Acad. Sci. (121): 1-23. ---. 1978. Development of fishes of the Mid-Atlantic Bight, an atlas of egg, larval and juvenile stages. Vol. IV. Carangidae through Ephippidae. U.S. Fish. Wildl. Serv., BioI. Servo Program, FWS/OBS-78/12. 314 pp. ---. 1981. The limits and relationships of the Lutjanidae and associated families. Bull. Scripps lnst. Oceanogr., Univ. Calif. Vol. 24. 114 pp. ---. 1983. Nithon spinosus: a primitive epinepheline serranid with comments on the monophyly and intrarelationships of the Serranidae. Copeia 1983: 777-787. Kendall, A. W., Jr. 1976. Predorsal and associated bones in serranid and grammistid fishes. Bull. Mar. Sci. 26: 585-592. ---. 1979. Morphological comparisons of North American sea bass larvae (Pisces: Serranidae). NOAA Tech. Rep. NMFS Circ. 428. 50 pp. Kramer, D. K. 1960. Development of eggs and larvae of Pacific mackerel and distribution and abundance of larvae 1952-56. Fishery Bull. Fish Wild\. Servo U.S. 60: 393-438. Laroche, W. A. 1977. Description of larval and early juvenile vermilion snapper, Rhomboplites aurorubens. Fishery Bull. U.S. 75: 547-554. Lau, S. R. and P. L. Shafland. 1982. Larval development of snook, Centropomus undecimalis (Pisces: Centropomidae). Copeia 1982: 618-627. Matsui, T. 1963. The larvae of Rastrelliger. Pages 59-69 in Southeast Asia Research Program, Univ. Calif. Scripps lnst. Oceanogr., ed. Ecology of the Gulf of Thailand and the South China Sea. Univ. Calif. SIO Ref. (63-6)1. ---. 1967. Review of the mackerel genera Scomber and Rastrelliger with description of a new species of Rastrelliger. Copeia 1967: 71-83. Matsumoto, W. M. 1959. Descriptions of Euthynnus and Au.xis larvae from the Pacific and Atlantic Oceans and adjacent seas. Dana-Rep. 50: 1-34. ---, E. H. Ahlstrom, S. Jones, W. L. Klawe, W. J. Richards and S. Ueyanagi. 1972. On the clarification of larval tuna identification particularly the genus Thunnus. Fishery Bull. U.S. 70: 1-12. McAllister, D. E. 1968. The evolution ofbranchiostegals and associated opercular, gular, and hyoid bones and the classification ofteleostome fishes, living and fossil. Bull. Nat. Mus. Canada 221 (BioI. Ser. No. 77): 1-239. Miller, G. L. and S. C. Jorgenson. 1973. Meristic characters of some marine fishes of the western Atlantic Ocean. Fishery Bull. U.S. 71: 301-312. Monod, T. 1968. Le complexe urophore des poissons teleosteens. Mem. lnst. Fond. Afr. Noire (81): 1-705. Nelson, G. J. 1969. Gill arches and the phylogeny of fishes, with notes on the classification of vertebrates. Bull. Am. Mus. Nat. Hist. 141(Art. 4): 475-552. Nybelin, O. 1963. Zur Morphologie und Terminologie des Schwanzskelettes der Actinopterygier. Ark. Zool. 15: 485-516. Potthoff, T. 1974. Osteologica] development and variation in young tunas, genus Thunnus (Pisces, Scombridae), from the Atlantic Ocean. Fishery Bull. U.S. 72: 563-588. --. 1975. Development and structure of the caudal complex, the vertebral column, and the pterygiophores in the blackfin tuna (Thunnus atlanticus, Pisces, Scombridae). Bull. Mar. Sci. 25: 205-23]. ---. 1980. Deve]opment and structure of the fins and the fin supports in the dolphin fishes Coryphaena hippurus and C. equiselis (Coryphaenidae). Fishery Bull. U.S. 78: 277-312. -- and S. Kelley. ]982. Development of the vertebral column, fins and fin supports, branchi- ostegal rays, and squamation in the swordfish, Xiphias gladius. Fishery Bull. U.S. 80: 161-186. -- and W. J. Richards. 1970. Juvenile bluefin tuna, Thunnus thynnus (Linnaeus), and other scombrids taken by terns in the Dry Tortugas, Florida. Bull. Mar. Sci. 20: 389-413. --, W. J. Richards and S. Ueyanagi. 1980. Development of Scombrolabrax heterolepis (Pisces, Scombrolabracidae) and comments on familial relationships. Bull. Mar. Sci. 30: 329-357. Richards, W. J. and V. P. Saksena. 1980. Description of larvae and early juveniles of ]aboratory- reared grey snapper, Lutjanus griseus (Linnaeus) (Pisces, Lutjanidae). Bull. Mar. Sci. 30: 515- 521. POTTHOFFETAL.:AN1SOTREMUS LARVALDEVELOPMENT 59 Robins, C. R., R. M. Bailey, C. E. Bond, J. R. Brooker, E. A. Lachner, R. N. Lea and W. B. Scott. 1980. A list of common and scientific names of fishes from the United States and Canada (4th edition). Am. Fish. Soc., Spec. Publ. (12): 1-174. Rosen, D. E. 1973. Interrelationships of higher euteleostean fishes. In P. H. Greenwood, R. S. Miles, and C. Patterson, eds. Interrelationships of fishes. Supplement No. I to the Zoological Journal of the Linnean Society Vol. 53. Academic Press, London, New York. 536 pp. Saksena, V. P. and W. J. Richards. 1975. Description of eggs and larvae of laboratory-reared white grunt, Haemulon plumieri (Lacepede) (Pisces, Pomadasyidae). Bull. Mar. Sci. 25: 523-536. Shuzhen, W. and C. Zhenran. 1981. On the larvae, juveniles and youngs of the pompano dolphinfish, Coryphaena equiselis Linnaeus, in the central part of South China Sea. Nanhai Studia Marina Sinica (2): 135-144. Smith, C. L. and R. M. Bailey. 1961. Evolution of the dorsal fin supports of percoid fishes. Pap. Mich. Acad. Sci. Arts Lett. 46: 345-363. Starks, E. C. 1930. The primary shoulder girdle of the bony fishes. Stanford Univ. Publ. BioI. Sci. 6: 147-240. Swinnerton, H. H. 1905. A contribution to the morphology and development of the pectoral skeleton of teleosteans. Q. J. Microsc. Sci., New Ser. 49: 363-382. Taylor, W. R. 1967. An enzyme method of clearing and staining small vertebrates. Proc. U.S. Natn. Mus. 122(3596): 1-17. Voss, N. A. 1954. The postlarval development of the fishes of the family Gempylidae from the Florida Current. I. Nesiarchus Johnson and Gempylus Cuv. and Val. Bull. Mar. Sci. GulfCaribb. 4: 120-159. DATEACCEPTED: September 7,1982. ADDRESSES:(T.P. and S.K.) Department of Commerce, National Oceanic and Atmospheric Admin- istration. National Marine Fisheries Service. Southeast Fisheries Center, Miami Laboratory, 75 Vir- ginia Beach Drive. Miami, Florida 33149; (M.M. and F. Y.) Aqualife Research Corporation, P.O. Box 3414, Marathon Shores, Florida 33052.