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1983

Reproductive-Biology Of The Blueline Tilefish, Caulolatilus- Microps, Off North-Carolina And South-Carolina

Jeffery L. Ross

John Merriner Virginia Institute of Marine Science

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Recommended Citation Ross, Jeffery L. and Merriner, John, "Reproductive-Biology Of The Blueline Tilefish, Caulolatilus-Microps, Off North-Carolina And South-Carolina" (1983). VIMS Articles. 628. https://scholarworks.wm.edu/vimsarticles/628

This Article is brought to you for free and open access by W&M ScholarWorks. It has been accepted for inclusion in VIMS Articles by an authorized administrator of W&M ScholarWorks. For more information, please contact [email protected]. REPRODUCTIVE BIOLOGY OF THE BLUELINE TILEFISH, CA ULOLATILUS MICROPS, OFF NORTH CAROLINA AND SOUTH CAROLINAI

JEFFREY L. Ross' AND JOHN V. MERRINER'

ABSTRACT

Blueline tilefish, Caulolati/us microps, were obtained by hook and line fishing and port sampling operations offNorth Carolina and SouthCarolina from 1972 to 1977. Caulolati/us microps spawn off the Carolinas from April through October, with peak activity offNorth Carolina inMay-June and September-October. Multiple spawnings by individual females were indicated by multimodel size distributions ofova; this is complement­ ed by the continuous production of spermatozoa in testes, which is facilitated by dynamic spermatogenic tubules. Fecundity is best predicted by fish weight: In Fecundity = 0.016 + 1.832 In Weight. Fecundity estimates ranged from 0.2 mil\ion ova for a412 mm TL (0.82 kg) fish t04.1 mil\ion ova fora 736 mm TL (4.85 kg) fish. Females attained sexual maturity between 425 and 450 mm TL(age IV- V). Males showed pronounc­ ed testicular development after age V (500 mm TL). Females were more abundant from 300 to 500 mm TL; the sex ratio was 1:1 between 500 and 600 mm TL; males predominated in size classes greater than 600 mm TL. Protogynous sex reversal in three juvenile specimens (156-202 mm TL) was indicated by transitional gonads or testes with residual oocytes. Previtellogenic oocytes in 8 of 42 mature males (436-700 mm TL) further suggest protogyny, although no adult fish with transitional gonads were observed. Whether blueline tilefish are strictly juvenile or functional hermaphrodites has yet to be determined.

The blueline tilefish, Caulolatilus microps Goode and The reproductive biology ofC. microps is previously Bean, is a semitropical demersal branchiostegid that undescribed. Dooley (1978) reported the capture of constitutes a significant componentofthe deepwater ripe females in January and May through September grouper-snapper fishery off North Carolina and off North Carolina. Brief notes on reproduction for South Carolina (Huntsman 1976). It inhabits the other branchiostegids suggest protracted spawning outer continental shelf, shelf edge, and upper slope seasons for C. princeps (Fitch and Lavenberg 1971), (70-235 m) from Cape Charles, Va., to Key West, C. affinis (Dooley 1978), Lopholatilus chameleon· Fla., and in the Gulf of Mexico from Pensacola, Fla., ticeps (Freeman and Turner 1977; Grimes·), and to Campeche, Mexico (Dooley 1978). Branchiostegus japonicus japonicus (Hayashi 1977). In 1972 scientists atthe SoutheastFisheries Center Dooley and Paxton (1975) related the presence of of the National Marine Fisheries Service (NMFS) several size classes ofova inmaturingB. wardi andB. began studying the biology, community relation· serratus to multiple spawning and found anomalous ships, and population dynamics of the offshore sex ratios within size classes. Pelagic eggs and larvae demersal (reef) fishes off the southeastern United of Caulolatilus sp. and L. chameleonticeps have been States, ultimately to provide effective management collected off the Carolinas and in the northwest of this fishery (Huntsman 1976). The reproductive Atlantic (Freeman and Turner 1977; M. Fahay5). biology ofblueline tilefish was investigated as part of that program, and is herein described with respectto MATERIALS AND METHODS 1) spawning seasonality, 2) descriptive gonado­ genesis, 3) fecundity, 4) age/size of sexual maturity, Blueline tilefish were captured over rugged pre· 5) sex ratio with size, and 6) sexual transition. cipitous bottoms as well as gently sloping sections of the shelf edge (Fig. 1). Specimens were obtained by 'Contribution No. 1083, Virginia Institute of Marine Science, hook.and line fishing with electric reels and rods from Gloucester Point, Va. Based on a thesis by Jeffrey L. Ross, submit­ ted to the School of Marine Science, College of Wil\iam and Mary, Williamsburg, Va., December 1978. ]Virginia Institute of Marine Science, Gloucester Point, Va.; pre­ "Churchill B. Grimes, Assistant Professor, Department ofEnviron­ sentaddress: North Carolina Division ofMarine Fisheries, P.O. Box mental Resources, Rutgers University, P.O. Box 231, New Bruns­ 967. Manteo. NC 27954. wick, NJ 08903, pers. commun. February 1982. 'Virginia Institute ofMarine Sciences, GloucesterPoint, Va.; pres­ 'Michael Fahey, Fishery Biologist, Northeast Fisheries Center ent address: Southeast Fisheries Center Beaufort Laboratory, SandyHookLaboratory,National Marine FisheriesService, NOAA, National Marine Fisheries Service, NOAA, Beaufort, NC 28516. Highlands, NJ OZ732, pers. commun. February 1982.

Manuscript accepted November 1982. 553 FISHERY BULLETIN: VOL. 81, NO.3, 1983. FISHERY BULLETIN: VOL. 81, NO.3

.------__-,37°00·

36°00'

N.C. 35°00'

,, ,

34°00' s.c.

33°00'

32°00'

31°00'

FIGURE 1.- Distribution of Cau/o/ati/us microps off North Carolina and South Carolina (noted by hatch marked area).

1972 to 1977 in the northern and central portions of GW Onslow Bay aboard the RV Onslow Bay (NMFS). GSI= WX 100 Fishing was most successful when baits were main­ where GW = preserved gonad weight (0.1 g) and W = tainedas close tothe bottom as possible. Totallength total body weight (g). GSI was used to determine (TL, mm) and total weight (W, g) were recorded for spawning seasonality and sexual maturity. each fish, gonads excised and stored in 10% For­ Sex was determined by gonad examination since malin6 and otoliths removed and stored in glycerine. blueline tilefish apparently exhibit no sexually Sampling of headboats fishing out of North Carolina dimorphic characteristics. Ovaries and testes were and South Carolina ports provided ancillary records staged macroscopically and histologically after pre­ of total length and total weight, and samples of servation in 10% Formalin (Tables 1,2). Ova stages gonads and otoliths. corresponded to those described by Moe (1969) for A gonosomatic index (GSI) was calculated accord­ red grouper, Epinephelus moria: oogonia, 2-8 }L; stage ing to the formula I, early oocytes, 20-50 }L; stage II, previtellogenic oocytes, 40-170 }L; stage III, early vitellogenic "Reference to trade names does not imply endorsement by the oocytes, 11 0-260 }L; stage IV, active vitellogenic National Marine Fisheries Service, NOAA. oocytes, 215-650}L; stage V, mature ova, 735-910}L 554 ROSS and MERRINER: REPRODUCTIVE BIOLOGY OF BLUELINE TILEFISH with 140-196 P. oil globule. Spermatogenic stages to determine the relative frequency of each size were analogous tothose described by Moe (1969) for group. red grouper and Hyder (1969) for Tilapia. Routine Well-Developed and Ripe ovaries from fish cap­ histological methods were used for slide pre­ tured from April through September were used for parations from Formalin-fixed gonads. fecundity estimates. One ovary randomly selected Frequency distributions ofova diameters were plot­ from each pair was weighed to the nearest 0.1 g. The ted by gonad stage to determine individual spawning ova were teased free of the ovarian tunic. Two sub­ patterns. Representative females were selected for samples were removed and all vitellogenic ova each ovarian stage. The diameterof50 ova from each (stages m- V; determined by relative size andopacity occurring stage (previtellogenic, early vitellogenic, of cytoplasm) were counted. The sample and sub­ active vitellogenic, and mature oocytes) were samples were oven dried and weighed to the nearest measured from each sample using a gridded petri 0.001 g. The formula dish and a magnification of 70X. A ratio of the four stages was then determined by reducing the magni­ (W) (wJ fication to 20X and counting two or more entire ¥= (WJ (w) y grids until about 500 ova were counted. This ratio was reduced to a base of200 and combined with ova was used to estimate fecundity, with ¥= total num­ diameter frequencies per stage data using the ratio ber of eggs in both ovaries, W = wet weight of both ovaries, Wi = wet weight ofselected ovary, Wi = total frequency of ova stage X ova diameter frequency dryweight, w = total dry weight ofsubsamples, andy 200 50 = number of ova in subsamples (Manooch 1976).

TABLE l.-Developmental stages of Caulolatilus microps ovaries.

Maturity stage External appearance Ova composition Immature Small, maroon. saUttsge to teardrop shaped hollow organs. Ovigerous lamellae composed of dense aggregations of undif­ (Btege 1) (>250 mm TL) ferentiated oogonia and primary Docytes. Resting Flaccid triangular sacs with translucent tunic and dark redJish Primarily "arly and previtellogenic oocytes with <1 % early vitel­ (stege 2) internal mass logenic oocytes. Developing Ovary becomes increasingly rotund while maintaining a basic Previtellogenic Docytes numerically dominant with some early (stage 3) triangular shape; yellowish orange appearance due to granula, and active vitellogenic Do.cytes, Well~developed ovaries contain ovigerous mass: tunic becomes more transparent, and ova afe an increasing number of vitellogenic oocytes evenly distributed dlscernable. over a large size range (215-650 MI.

Well·Developed Ovarian tunic becomes nearly transparent yellowish OV8 denaely Vitellogenic oocytes pr:edominant and evenly distributed over a (Blege 4) packed and discernable. large size range (215~650 M). Ripe May-August: Greatly distended. bulbous and occupying more Broad size distribution of vitellogenic oocytes. with a mode of IBtege 51 than 1/3 of the peritoneal cavity; very light orange to white in very large (420-640 M) vitellogenic oocytes together with slage color; 2·4% body weight. Ova clearly visible through delicate, III end smell (215-4001-') stege IVoocytes. Meture oocytes(785· nearly transparent tunic. 910 IJ.) characteristically contained in lumen. free of ovigerous lamellae. Seplember~October:Ovaries comparatively smaller. firm. more A mode of large stage IV oocytes with stage V oocytes present triangular though rotund; 1~2.4% body weight and relatively few small (215-400 ""I stage IV oocytes. Recently Spent­ Resemble deflated early developing ovaries: distinguished by Stage III and small stage IV oocytes occur together with some Redeveloping. inflamed ventral. posterior portion. otherwise cream colored. very large stage IV and stage V oocytes. the lattBr often in an IBtege 6-3) atretic state. Spent Flaccid. reduced in size; muscular tunic contracting and becom­ No evidence of vitellogenesis; stage IV and Voocytes are atretic: (stege 6) ing firm. inflamed. a few stage III oocytes occur.

TABLE 2.-Developmental stages of Caulolatilus microps testes.

Maturity atage External appearance 'Spennetogenic ectivity

Immature/Reating Ba.ically threadlike maroon organa with .Iight laterally com­ Spermatogenic tubules generally inactive. though spermatozoa prelSed expan.ion posteriorly above sperm duct. may occur in lumen of spermatogenic tubules and collecting tubules. Developing Maroon. thin, elongate, laterally compresaed, with widest por~ Spermatogenic tubules contain crypts 8t 811 developmental tion directly above .perm ducts, tapering rapidly to filamentous stages with spermatozoa collecting in the lumen and coll.ct~ anterior projection. ing tubules. Well­ More robust, triangular to nearly cornucopia shaped. tapering Extensive collections of spermatozoa in expanded lumens of Developed anteriorly. Maroon to creamy off-white color. actively developing spermatogenic tubules, with channeling of spermatozoa into media! collecting tubules. Ripe No running ripe testes observed

555 FISHERY BULLETIN: VOL. 81, NU.:J

Juvenile specimens were obtained for gonadal base of attachment along the medial surface. Each analysis from the Field Museum of Natural History, testis enters the urinary papilla by a separate Chicago, Ill., and the Institute of Marine Science, sperm duct. University of North Carolina, Morehead City, N.C. The structure and developmental pattern of the testes are similar to that described by Smith (1965) RESULTS as tubular. The primary spermatogenic units are radial spermatogenic tubules and spermatogenic Gonadal Development crypts. In cross section, the spermatogenic tubules are essentially a ring, one spermatogonium or one The paired ovaries of C. microps are suspended spermatogenic crypt thick (Fig. 2). An elastic con­ below the swim bladder by mesovarium in the most nective tissue, the Sertoli cells, encapsulates and posterior portion ofthe body cavity. The mesovarium maintains the integrity of the tubules and the in­ extends the length of the ovary and contains the dividual developing crypts. It presumably serves as ovarian arteries. Oogenesis and vitellogenesis occur the site of steroidogenesis (Lofts 1968; Hoar 1969). within the ovigerous lamellae which are distributed Development proceeds at vaJying rates within each evenly and project laterally and medially from the spermatogenic tubule, analogous to that in the tunica albuginea. The absence of lamellae from a ovigerous lamellae, so that active spermatogenic narrow band in the ventral portion ofthe ovary forms tubules usually contain clypls at all stages of an ovocoel. This facilitates ovarian expansion and development (Fig. 3). Spermatids were the most ad­ collection ofripe ova released from the lamellae prior vanced stage observed within a crypt. Spermio­ to extrusion through the common oviduct (Moe genesis, the morphogenesis of spermatid to sperma­ 1969). tozoa, occurred aJ'ound the time of pas age from Testes of blueline tilefish are solid, smooth tex­ crypt to the lumen of the spermatogenic tubule. tured, compressed laterally, and relatively more Whereas in many fishes the interstitial tissue elongate than ovaries. They are suspended from the separating the developing tubules breaks down at swim bladder by the mesorchium, which has a wide later stages of development resulting in extensively

FIGUHE 2.-C/'Oss section of Early-Developing testes f/'Om a 530 111m TL Cau/o/alilus mirrops collected 15 March 1977. Note radial spermatogenic tubules (SPT) composed principally of primary spermatogenia (SG1) with few developing crypts. and the presence of spermatozoa (SP) in the lumen of the spermatogenic tubules (Haematoxylin X 200).

556 ROSS and MERRINER: REPRODUCTIVE BIOLOGY OF BLUELINE TILEFISH

FIG RE 3.-Cross section of Developing testes from a 664 mm TL CoulD/ali/us microp.< capiUJ'ed 9 September 1974. Note spermatogenic tubules composed of the spectrum of developing crypt stage. with primary (SG i) spermatogonia; primary (SC I) and secondary (SC2) spermatocytes; spermatid (ST); and collections of spermatozoa (SP) in the lumen (Haemaloxylin and eosin X 200). packed sinuses of spermatozoa, the spermatogenic somedial migration of spermatogenic tubules and tubules of C. microps maintain their integrity. their merging with and releasing of spermatozoa into Drainage ofspermatozoa from the testes results from the collecting tubules. The collecting tubules chan­ the dynamic nature of the tubules. In the course of nel the spermatozoa posteriorly and ventrally into their development, they migrate medially from the the separate sperm ducts. lateral epithelium. Several observations support this hypothesis. In an early-developing male captured in Spawning Seasonality May (Fig. 4), the lateral spermatogenic tubules are undeveloped and inactive with small amounts of Cnu/o/n/i/u.~ microps spawn off orth Carolina and spermatozoa in the lumen. Those adjacentto the dor­ South Carolina between April-May and September­ somedial portions of the testes are also generally October. Monthly mean GSI values for 138 females inactive but contain larger collections of sper­ and 101 males captured off North Carolina exhibited matozoa. This suggests that longevity of sper­ peaks in May and September (Fig. 6). Early­ matogenic tubules exceeds one season and that Developing ovaries were predominant from Feb­ spermatogenic tubules generate from the peripheral ruary through April. High GSI values in May interstitium (Lofts 1968). The spermatogenic tu­ corresponded to the greatest incidence of Well­ bules adjacent to the dorsomedial connective tissue Developed and Ripe females (Fig. 7). The lower in developing testes are generally the most well mean GSI values observed in June, July, and August developed, and can be seen merging with the medial corre ponded with a diversity of gonad stages includ­ collecting tubules (Fig. 5). The collecting tubules ing Early-Developing, Well-Developed, Ripe, and have boundary cells that are essentially connective Recently Spent-Redeveloping ovaries. Ovaries were tissue, and contain only spermatozoa. The sper­ again synchronously Well-Developed or Ripe in Sep­ matogenic tubules can be distinguished, since they tember though con iderably smaller than gonads ob­ are bordered by active spermatogenic crypts. Tes­ served in May and June. Low GSI value from ticular drainage is thus accomplished by a dor- November through March reflect a period of gonad 557 FISHERY BULLETIN: VOL. 81, NO.3

FIGURE 4.-Cross section of Hesting testes from a 410 mm TL C(Iu/u/ali/us mic/'{/p., collected 15 March 1977. Note undeveloped state of latcral (L) spcrmatogenic tu buies and incrcased collections ofspermatozoa (S?) in spel'll1alogenic lubules and collecling tubules (CT) located along dorsomedial (OM) region (Hacmatoxylin and eosin X 78).

FIGLJIlE 5.-Cross seclion of Developing leSles from a 664 mm TL ('(III/o/aii/lls micl'Ops collected 9 Seplember 1974. ote spermatogenic tubules (SPT) composed of active crypts merging with and channeling spcrmalozoa into collecting tubules (CT) which occur along the dorsomedial (OM) lunica albuginea (HaematoxyJin and eosin X 256).

558 ROSS and MERRINER; REPRODUCTIVE BIOLOGY OF BLUELINE TILEFISH

E N= 0 3 6 9 8 21 35 19 26 5 0 3 .2' Photoperiod 100..---r-r-h...., >. III C 90 '0 80 f i~ :::J 0 ~70 :r c Ql " 100 Meters :::J 60 Ql 24 Bollom Water Temperature • 200 Meters 'tl ~ ,r­ u. 50 f! 20 .- .2' _-----...... -..------...... "" ,~ C 'E .... 40 Ql 16 fl o ~-~-~~-/~.~-._- _-_._-~~~~~-::~~/" ~ o .. .. Q. 30 12 20 0.25 Males " North Carolina 10 .. • South Carolina ~0.20 c ;; 0.15 co g010 FIGURE 7.-Percent frequency histogram of gonad developmental 0.05 ~ ...-... ---1 " stages observed each month for female Cau/o/ali/us microps from North Carolina and South Carolina.

3.5 Females and early vitellogenic oocytes (Fig. 9). Ripe females 3.0 " North Carolina from May and June exhibited modes of pre­ • South Carolina vitellogenic oocytes, early vitellogenic oocytes, late .. 2.5 Ql 'tl vitellogenic oocytes, and mature eggs. This indicated E 2.0 continuous development from the residual stock of 'tl co 1.5 C oocytes occurred when spawning was imminent. 0 , .0 Early vitellogenic ova are predominant in Spent­ " Redeveloping ovaries and cooccur with residual 0.5 3 3 mature, atretic mature, and late vitellogenic oocytes. 0.0 Late vitellogenic oocytes were again the predomi­ Jan Feb Mar Apr May Jun Jul Aug Sept Oct Nov Dec nant oocytes in Well-Developed ovaries during Sep­ Months tember. There was also a decreased proportion of early vitellogenic oocytes in comparison with Well­ FIGURE 6.--Monthly mean gonad index values for male and female ('all/o/ali/lI,' microps from North Carolina and South Carolina, mean Developed gonads from May. bottom temperatures off Beaufort, N.C. (Stefansson and Atkinson Males accommodate the protracted season of 1967), and photoperiod. oogenesis by maintaininga constantstate ofdevelop­ ment during the spawning season. The two peaks in regression and early development. Ripe females were GSI of testes coincided with those observed for captured off South Carolina during April and July, ovaries (Fig. 6). Testes contained some spermatozoa which could indicate a more continuous or three­ in all months sampled and observed histologically, peaked spawning season. Monthly mean GSI as well while those from April through September generally as mean standard length were greater for females off contained large quantities of spermatozoa in the South Carolina, but data are too limited to draw any collecting tubules. However, we never captured any further conclusions. males with free-running milt. Analysis of ova development within individual ovaries suggested that blueline tilefish are multiple Fecundity spawners (Fig. 8). Ovaries considered Resting characteristically contained primary oocytes and We estimated the fecundity of blueline tilefish from previtellogenic oocytes. Early-Developing ovaries three periods during theirspawning season. Fecundi­ showed a progression of early vitellogenic oocytes ty ranged from 210,000 ova (412 mm TL) to developing from the residual stock. Well-Developed 3,220,000 ova (637 mmTL) for 18 fish capturedfrom ovaries in late April contained a mode of late April to early June (Fig. 10). Fecundity was signi­ vitellogenic oocytes cooccurring with previtellogenic ficantly correlated with both length and weight: 559 FISHERY BULLETIN: VOL. 81, NO.3

100 94 100 74 Resting, Early Developing, Stage 2 Stage 3 (March) 30 30

20 20

10 10

100 100 70 Developing, Well Developed, 52 48 Stage 3 (April) 40 Stage 4 (May) 33 30 30

20 20

10 10

u>- c ~ 100 Ripe, 100 64 Spent-Redeveloping, C" ..Q) Stage 5 (May) 42 40 Stage 5 --3 (August) LL 30 30

20 20

10 10

100 74 100 74 Well Developed, 48 Spent, 43 Stage 4 (September) Stage 6 (September)

30 30

20 20

10 10

140 280 420 560 700 840 140 280 420 560 700 840 Ova Diameter (p)

FIGum; B.-Ova diameter frequency distributions for designated ovarian developmental stages for female Caulolatilus microp.• from North Carolina.

560 ROSS and MERRINER: REPHODUCTIVE BIOLOGY OF BLUELINE TILE FISH

FII;L'HE 9.-Cross section of Well-Developed ovary from a 515 mm TL female Call/o/ati/118 microp" (21 April 1977) with lamellae composed of residual stock previtellogenic oocytes (10, early vitellogenic oocytes (IJI). and late vitellogenic oocytes (IV) (Haematoxylin and eosin X 63).

In Fecundity = 0.016 + 1.832 ( In Weight 1

45 r 2 = 0.78 In Fecundity = 8.830 + 0.00986 Total length n = 18 r' = 0.74, and o In Fecundity =0.016 + 1.832 In Weight 40 /', = 0.78.

35 o

Fecundity for 14 Ripe females captured in July x basically agreed with the above fecundity relation­ 30 ship; the estimates ranged from 196,000 (436 mm on TL) to 4,107,035 ova (736 mm TL). The estimated o fecundity of 12 Well-Developed and Ripe females >- 25 from September decreased approximately one-third I- o to one-half. The production of vitellogenic ova ap­ Z :::l 20 pears greater during the late spring-early ummel' U W spawning peak than the early fall peak. However, in­ u.. sufficient data on the frequency of spawnings by in­ 15 dividuals within age/size groups and the number of eggs released preclude further refinement of in­ x = APRIL -JUNE 10 dividual annual fecundity estimates. o =JULY o = SEPT. 5

FIGUHE IO.-Fecundity-weight relationship 1'01' ('rw/"/ati/u" mil'ro"" collecled in April to June. Fecunrlity estimates are pion cd 1'01' fish o+----,---r---,-----r----, captured in July (South Carolina) and September (North o 1,000 2.000 3,000 4.000 5.000 Carolina). TOTAL WEIGHT (g 1 561 FISHERY BULLETIN: VOL. 81, NO.3

Sexual Maturity tured off South Carolina than those captured off North Carolina, although the biological reason for Maturity of females, defined as the size at which this is unknown. >50% of the individuals were gonadogenically ac­ Male C. microps show little gross testicular develop­ tive, occurred between 425 and450 mmTL (Table 3) ment under 500 mm TL (Table 3). Macr9scopically, which is typically a 4- or 5-yr-old fish (Ross and 50% were considered immature between 500 and Huntsman 1982). One of three age III females (387­ 525 mm TL and 100% attained maturity above 600 421 mm TL), 50% of the age IV (n = 8; 427-506 mm mm TL. No age IV (n = 4; 436-453 mm TL) and only TL), 73% ofthe age V (n = 15; 430-546 mm TL), and 12.5% of the age V males (n = 8; 485-574 mm TL) 100',{ of the age VI+ females were mature. The pat­ were considered mature, and a majority (62.5%) had tern of ovarian development corroborated the mac­ not matured until age VI (n = 8; 520-556 mm TL). roscopic maturity analysis. Relative gonad weight The initial and most pronounced increase in relative increased with total length after initial steep in­ testis size occurred in males >500 mm offNorth Car­ creases in relative gonad size between 400 and 500 olina and males >600 mm off South Carolina. His­ mm TL. Mean GSI and maximum relative gonad tological examination of testes from males 390-500 weights were consistently greater for females cap- mm TL (n = 11) revealed spermatogenesis and collections of spermatozoa in fish macroscopically TABLE 3.-Percentage ofsexually mature female and male considered immature. These testes were very small Caulolatilus microps from North Carolina and South «0.08% bodyweight) andmaroon in color. We could Carolina. not determine whether this represented precocious Total Females Males development or functional maturity. length N Percent mature N Percent mature

250-300 3 0 301-325 326·350 1 0 Sex Ratio and Sexual Transition 351·375 2 0 376·400 5 20.0 1 o 401·425 11 45.5 1 o Males outnumbered females in the combined North 426-450 8 75.0 4 o Carolina and South Carolina collections (195 to 176), 451-475 11 81.8 3 o 476-500 11 90.9 5 20.0 butthis was notsignificantly differentfrom a 1: 1ratio 501·525 24 100.0 8 50.0 (X2 = 0.97). However, sex ratios become skewed 526·550 24 100.0 9 77.8 551·575 18 100.0 9 77.8 when size (Table 4) or age (Table 5) are considered. 576-600 8 100.0 8 87.5 Females were more numerous between 300 and 500 601·825 13 100.0 7 100.0 626-650 11 100.0 13 100.0 mm TL, and in several cases there were significant 650+ 4 100.0 41 100.0 deviations from 1:1. Between 500 and 600 mm TL

TABLE 4.-Frequency of male and female Caulolatilus microps from North and South Carolina within 25 and 100 mm TL intervals, with Chi-square values assuming a 1:1 sex ratio.

Percent Percent Length Male Female female/25 mm X female/1oo mm X 101·200 25 1.0 201·300 100 301·325 326-350 1 100 88 5.4· 351·375 1 100 376·400 1 6 86 3.57 401-425 1 6 86 3.57 426·450 7 12 83 1.32 87 9.89· ;451·475 6 20 77 7.54- 476-500 14 19 58 0.75 501·525 20 23 53 0.21 526·550 15 18 55 0.27 52 0.32 551·575 19 22 54 0.22 576-600 18 16 47 0.12 601-625 19 16 46 0.26 826·650 16 6 33 2.67 30 16.9· 651-675 20 3 13 12.57· 676·700 15 2 12 9.94· 701-725 11 0 0 726·750 5 1 17 9 15.6· 751'·775 3 1 25 776·800 2 0 0 ·P5.0.05. 562 ROSS and MERRINER: REPRODUCTIVE BIOLOGY OF BLUELINE TILEFISH

TABLE 5.-Frequency of male and female oocytes (Fig. 11). The remammg three specimens Caulolotilus microps from North and South had gonads which exhibited progressive stages ofsex Carolina within age groups with Chi-square values assuming 1:1 sex ratio. reversal. The earliest stage (202 mm TL) was pre­ dominantly ovarian with an acidophilic germinal tes­ ticular mesothelium proliferating through the Age Fomales Males ovigerous lamellae from the dorsomedial connective 1.8 tissue (Fig. 12). The proliferating mesothelium con­ III 3 1 IV 16 4 7.2" tained primary spermatogonia and would be the site V 26 15 2.95 VI 16 9 1.96 ofsteroidogenesis, inducing atresia and the recycling VII 11 7 0.89 of ovarian elements (Hoar 1969). Gonads of two VIII II 16 0.93 IX 7 4 0.82 specimens (178 and 184 mm TL) in advanced stages X 4 12 4.00" of sex reversal had differentiated into the basic tes­ XI 1 3 1.0 XII a 6 6.0· ticular components with spermatogenic tubules pres­ XIII o 2 ent and spermatogenesis proceding (Figs. 13, 14). XIV o 2 3.57 XV 1 2 Both specimens revealed evidence of a previous ·PSO.05. ovarian stage in the form of atretic tructures, residual oocytes, or proliferating testicular meso­ the sex rat io was essentially 1:1. In fish> 600 mm TL, thelium along the peripheral epithelium. These males became increasingly and significantly more specimens were all captured in March and were abundant. Similarly, females outnumbered males in within the size range predicted for C. microp-, after ages III through VII while males became pre­ one year of growth (Ross and Huntsman 1982). dominant for ages X through XV. Residual oocyte were al 0 observed in 8 of 41 Histological evidence from four juvenile blueline developing testes from adult males (Fig. 15). These tilefish indicated prematurational sex reversal. The fish were 430-700 mm TL and had solid testes gonad from a 186 mm TL specimen was ovarian and which exhibited no other remnant ovarian struc­ composed of basophilic oogonia with some primary tures.

I

FIGURE 1J.-Cross seclion of ovary from a juvenile j 86 mm TL COl/lola/iILls mi("l"ops collected J3 March 1961 with oogonia and primary oocyles (I) (Haemaloxylin and eosin X 200).

563 FISHERY BULLET! ': VOL. 81. NO.3

FIGURE 12.-Crnss seclion of gonad from a juvenile 202 mm TL ('(IlI/o/ati/"., mi,,/'(I".' colleclcd J;j Man:h J 961. Note OCCUITence of oogonia (00) und primary oocytes (I) along ventrolateral region (VL) with proliferating le~ticulal' I'nesolhelium (TM) originaling from dorsomedial areas (01\1) (HaemaLOxylin and eosin X 200).

FlG RE 13.- ross seclion of gonad from a juvenile 184 mm TL ('allio/a/illl., /1Ii,.,.op-, collecled \3 March 1961. Note spermatogenic tubules composing dorsomedial region (DM) and residual oocytes along luterol (L) gonadal margin (Haematoxylin and eosin X 200).

564 ROSS and MERRI ER: REPRODUCTIVE BIOLOGY OF BLUELINE TILEFISH

FIGURE J 4.-Cross section of gonad from 0 juvenile 184 mm TL Cau/o/ati/u, microps collected 13 March 1961. Note in this closeup of previous gonad the well-defined spermatogenic tubules (SPT) (Haemat­ oxylin and eosin X 400).

FIG HE 15 ..- ross seclion of Well-Developed te,les I'l'om a 562 mm TL ('au/"/ali/us ",i"m/ls caplul'ed 22 April J977, Nole extensive collection of spermalozoa ISP) and occurrence of residual previtellogenic oocyte, IRO) (Haematoxylin and eosin X 78),

565 FISHERY BULLETIN: VOL. 81, NO.3

DISCUSSION These are effective around the 50-100 fathom curves and could be an important means of regional reten­ The initiation of gonadogenesis in blueline tilefish tion of eggs and larvae produced by C. microps and during March and April and the termination in other shelf edge inhabitants. September-October coincide with the periods of Whether C. microps are strictly prematurationally rapidly increasing and decreasing photoperiods (Fig. or also functionally protogynous cannot as yet be 6). This is a more conservative environmental cue confirmed. Winter (between spawning periods) than temperature when considering the shelf edge collections are needed to determine whether tran­ habitat. Temperature fluctuations are not neces­ sitional adults occur. The skewed sex ratios with size sarily seasonal, but also subject to cold-water in­ and age could indicate that sex reversal occurs over trusions from outer continental shelf bottom waters an extended range of ages rather than just pre­ and meanderings of the axis of the Gulf Stream maturationally. However, skewed sex ratios with size (Stefansson and Atkinson 1967). The initiation of could be attributable to differential growth rates, gonadal development has also been correlated with which have been noted for C. microps (Ross and photoperiod for the cooccurring red porgy, Pagrus Huntsman 1982) as well asL. chameleonticeps (Tur­ pagrus, (Manooch 1976). The protractedspawningof ner et a1. 7) and other tilefishes (Dooley 1978). vermilion snapper, Rhomboplites aurorubens, was Skewed sex ratios with age could result simply by correlated with both photoperiod and water tem­ <50% ofthe juvenile females changing sex to males. perature (Grimes and Huntsman 1980); however, Furthermore, functional protogyny is questionable its occurrence over the continental shelf increases since 1) all males possessed solid testes, whereas its susceptibility to seasonal temperature varia­ secondary males generally retained remnants of the tion. hollow ovarian lumen (Smith and Young 1966; War­ Blueline tilefish ovaries seasonally undergo a pro­ ner 1975a) and 2) the existence of 400-500 mm males gressive maturation of residual stock oocytes to would have entailed their sex reversal prior to vitellogenic state with several modes generated and functioning as reproductive females. no sharp distinctions between residual and maturing Prematurational sex reversal, evidenced by his­ eggs. The multimodal size distribution ofoocytes ob­ tological examination of juvenile gonads, accounts served is characteristic of fishes that spawn several for the presence ofoocytes in de.veloping testes. The times during a protracted spawning season (Clark development of remnant ovarian gonocytes to pre­ 1934; Warner 1975a; Grimes and Huntsman 1980). vitellogenic oocytes in a testis could result from the Off North Carolina it appears that most C. microps activation of estrogens, the presence of which is im­ spawn during May-June and September-October. plicit had there been a juvenile female stage (Brusle The capture of large females (>600 mm TL) that 1969; Brusle and BrusH! 1975). The males with were Ripe in July and August might indicate more residual oocytes were captured in the spring, the frequent spawning by larger fish. The generally period ofmaximum hormonal induction for initiating larger females captured off South Carolina might gonadogenic activity (Hoar 1969). The residual spawn earlier and more frequently than those off oocytes were previtellogenic oocytes which 1) are North Carolina, although data supporting this con­ reported to be the most resistant oocytes to resorp­ clusion are incomplete. The continuous develop­ tion and atresia (Brusle and Brusle 1975) and 2) were mental pattern of male testes would certainly observed in medial connective tissue or in collecting accommodate protracted spawning by females. tubules and not interspersed within active sper­ If local spawning is directed toward the main­ matogenic tissue. tenance ofregional populations (Marshall 1966), the The occurrence of prematurational sex reversal in production of several batches of eggs during a pro­ C. microps should indicate protogyny elsewhere in its tracted spawning season should improve chances of genus or family. This is possible though not yet con­ concurrence with favorable environmental con­ firmed for several related species. Atlantic goldface ditions. Of particular relevance to C. microps spawn­ tilefish, C. chrysops, captured off North Carolina and ing are the influence and extent of transport of eggs in the Gulf ofMexico (n = 20) include 7 females 385- and larvae by the Florida Current(Gulf Stream). The ridge and trough bottom irregularity off South Car­ olina known as the Charleston Bump causes a 'Turner. S. C., C. B. Grimes, and K W. Able. Inprep. Age, growth seasonal deflection of the Gulf Stream and resulting mortality and age/size structure of the fisheries for tilefish, Lopho­ inshore southwest setting eddy currents occurringas lati/us chameleonticeps, in mid-Atlantic and southern New England waters. Department ofEnvironmental Resources, Rutgers Univer­ far north as Cape Hatteras (Brooks and Bane 1978). sity, P.O. Box 231, New Brunswick, NJ 08903. 566 ROSS and MERRINER: REPRODUCTIVE BIOLOGY OF BLUELINE TILEFISH

503 mm TL and 13 males 503-562 mm TL (Ross un­ equipment. Robert Karl Johnson (Field Museum of publ. data). The sex ratio for anchor tilefish, C. Natural History) and Frank Schwartz (Institute of intermedius, offTexas is 66 females: 5 males between Marine Science, University ofNorthCarolina) kindly 100 and 270 mm TL, and 0 females: 8 males >270 provided juvenile specimens. Finally Gene Hunts­ mm TL (Ross, Pavela, and Chittenden unpubl. data). man, George Sedberry, and John Olney contributed Dooley (1978) reported anomalous sex ratios for L. much in their review of this and earlier versions of chameleonticeps,B. wardi, andB. serratus. Clark and the manuscript. Ben-Tuvia (1973) reported pairs of Malacanthus hoedtii outside burrows including a large male and a smaller female. Prematurational sex reversal is also LITERATURE CITED suspected of the tilefish, L. chameleonticeps, based BROOKS, D. A., AND J. M. BANE, JR. on juvenile gonadal histology and adult sex ratio data 1978. Gulf Stream deflection by a bottom feature off (Grimes footnote 4). Charleston, South Carolina. Science (Wash., D. C.) Prematurational sex reversal in C. microps is likely a 201:1225-1226. regression from monandric protogyny to functional BRUSLE,J. 1969. Hermaphroditism potential ches les males de trois gonochorism. The size-advantage model, which at­ especes d'Asteroides. Ann. Embryo!. Morphog. 2:445­ tributes protogyny to cases where an individual re­ 450. produces most efficiently as a female when young BRUSLE, J., AND S. BRUSLE. and a male when it gets older (Ghiselin 1969) is 1975. Ovarian and testicular intersexuality in two pro­ generally applicable when such things as inexper­ togynous Mediterranean groupers, Epinephelus aenous andE. gauza. In R. Reinboth (editor), Intersexuality in the ience, male dominance, mate selection, or terri­ animal kingdom, p. 222-227. Springer-Verlag, N.Y. toriality lead to a differential in male reproductive CHOAT, J. H., .\ND D. R. ROBERTSON. success at older ages (Warner 1975b). Caulolatilids 1975. Protogynous hermaphroditism in fishes of the family presumably evolved in the Caribbean and are often Scaridae. In R. Reinboth (editor), Intersexuality in the animal kingdom, p. 263-283. Springer-Verlag, N.Y. associated with reef-type habitat (Dooley 1978) CLARK,F.N. where protogyny is widespread (Choat and 1934. Maturity of the California sardine (Sardina caerulea), Robertson 1975; Smith 1975; Warner 1975a, b). A determined by ova diameter mesurements. Calif. Fish radiation of C. microps (or ancestor) in the Game, Fish Bull. 42, 49 p. evolutionary past from a reef-type environment to CLARKE, E., AND A. BEN.TuVIA. 1973. Red Sea fishes of the family Branchiostegidae with a more extensive outer continental shelf and upper description of a new genus and species Assvmeturus slope habitats may have reduced the selection pres­ oreni. Israel Bull. Sea Fish. Res. Stn. 60:63-74. Sure favoring protogyny. The increase in utilizable DOOLEY, J. K. habitat and more continuous distribution would 1978. Systematics and biology of tilefishes (Perciformes: Branchiostegidae and Malacanthidae), with descriptions allow more frequent opportunities for smaller males of two new species. U.S. Dep. Commer., NOAA Tech. to engage in spawning, hence favoring sex reversal at Rep. NMFS Circ. 411, 78 p. an earlier age and ultimately tending toward second­ DOOLEY, J. K., AND J. R. PAXTON. ary gonochorism. 1975. A new species of tilefish (Family Branchiostegidae) from eastern Australia. Proc. Linn. Soc. N.S.W. 99:151­ 156. ACKNOWLEDGMENTS FITCH, J. E., AND R. J. LAVENBERG. 1971. Marine food and game fishes of California. Univ. We wish to thank Gene Huntsman and the staff at Calif. Press, Berkeley, 179 p. the Southeast Fisheries Center Beaufort Labora­ FREEMAN, B. L., AND S. C. TuRNER. 1977. Biological and fisheries data on tilefish, LopllOlatilus tory, National Marine Fisheries Service (NMFS), ehameleonticeps (Goode and Dean). U.S. Dep. Cammer., Beaufort, N.C., for allowing access to their facilities NOAA, Tech. Ser. Rep. 5, 41 p. and data, and particularly Robert Dixon, Charles GHISELIN, M. T. Manooch, Pete Parker, Doug Willis (NMFS), 1969.. The evolution of hermaphroditism among animals. Q. Churchill Grimes (Rutgers University), and Robert Rev. Bio!. 44:189-208. GRIMES, C. B. Matheson (Duke University) for theirassistance with 1976. Certain aspects of the life history of the vermilion field collections and enlightening discussions. We snapper, R1lOmboplites aumrubens (Cuvier) from North also thank the late Patricia Berry (Virginia Institute and South Carolina waters. Ph.D. Thesis, Univ. North of Marine Science (VIMS)) for histological pre­ Carolina, Chapel Hill, 251 p. GRIMES, C. 8., AND G. R. HUNTSMAN. parations, Ken Thornberry and Bill Jenkins (VIMS) 1980. Reproductive biology of vermilion snapper, Rhombo­ for photographic assistance, and Joe Scott (College pUtes aurorubens, from North Carolina and South Car· of William and Mary) for use of photomicroscopic olina. Fish. Bull., U.S. 78:137-146.

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HAYASHI, Y. MOE, M. A., JR. 1977. Studies on the maturity and the spawning of the re d 1969. Biology of the red grouper, Epinephelus moria tilefish in the EastChina Sea-I. Estimation ofthe spawn­ (Valenciennes) from the eastern GulfofMexico. Fla. Dep. ing season from the monthly changes of gonad index. Nat. Resour., Mar. Res. Lab., Prof. Pap. Ser. 10,95 p. BulL Jpn. Soc. Sci. Fish. 43:1273-1277. Ross, J. L., AND G. R. HUNTSMAN. HOAR, W. S. 1982. Age, growth, and mortality of blueline tilefish from 1969. Reproduction. In W. S. Hoar and D. J. Randall North Carolina and South Carolina. Trans. Am. Fish. (editors), Fish physiology, vol. III, p. 1-73. Acad. Press, Soc. 111:585-592. N.Y. SMITH, C. L. HUNTSMAN, G. R. 1965. The patterns of sexuality and the classification of 1976. Offshore headboat fishing in North Carolina and South serranid fishes. Am. Mus. Novit. 2207, 20 p. Carolina. Mar. Fish Rev. 38(3):13-23. 1975. The evolution of hermaphroditism in fishes. In R. HYDER, M. Reinboth(editor), Intersexuality in the animal kingdom, p. 1969. Histological studies on the testes of Tilapia leueo­ 295-310. Springer-Verlag, N.Y. stieta and other species of the genus Tilapia (Pisces: SMITH, C. L., AND P. YOUNG. Teleostei). Trans. Am. Microsc. Soc. 88:211-23l. 1966. Gonad structure and the reproductive cycle ofthe kelp Lons, B. bass, Paralabrax clathratus (Girard), with comments on 1968. Patterns in testicular activity. In D. J. W. Barrington the relationships ofthe serranid genus Paralabrax. Calif. and C. B. Jorgensen (editors), Perspectives in endocrinol­ Fish Game 52:283-292. ogy, p. 239-304. Acad. Press, Lond. and N.Y. STEFANSSON, U., AND L. P. ATKINSON. MANOOCH, C. S., III. 1967. Physical and chemical properties of shelf and slope 1975. A study of the taxonomy, exploitation, life history, waters off North Carolina. Duke Univ. Mar. Lab., Tech. ecology and tagging of the red porgy, Pagrus pagrus, Rep., 23 p. Linnaeus off North Carolina and South Carolina. WARNER, R. R. Ph.D. Thesis, North Carolina State Univ., Raleigh, 1975a. The reproductive biology of the protogynous herma­ 286 p. phrodite Pimelometopcm pulchrum (Pisces: Lab­ 1976. Reproductive cycle, fecundity, and sex ratios ofthe red ridae). Fish. Bull., U.S. 73:262-283. porgy, Pagrus pagrus (Pisces: Sparidae) in North Car­ 1975b. The adaptive significance of sequential hermaphro­ olina. Fish. Bull., U.S. 74:775-781. ditism in animals. Am. Nat. 109:61-82. MARSHALL, N. B. 1966. The life of fishes. Universe Books, N.Y., 402 p.

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