BULLETIN OF MARINE SCIENCE. 56(1): 33-47. 1995

REPRODUCTIVE BIOLOGY OF TWO HAWAIIAN PELAGIC CARANGID , THE BIGEYE SCAD, SELAR CRUMENOPHTHALMUS, AND THE ROUND SCAD, DECAPTURUS MACARELLUS

Thomas A. Clarke and Lisa A. Privitera

ABSTRACT Bigeye scad Selar crumenophthalmus and round scad Decapturus macarellus were sampled from commercial fishery catches in Hawaii. Size at maturity of bigeye scad is ::;200 mm standard length. Spawning season is from April through September or October. Round scad mature at about 245 mm SL, and spawning occurs from April through August. Both appear to sometime between dawn and dusk. For bigeye scad, the frequency of post- ovulatory follicles indicates that females spawn every three days; batch costs average about 3% of body weight. Postovulatory follicles were found very infrequently in round scad. Mean batch fecundities of bigeye scad and round scad were 92,000 and 136,000, respectively; relative fecundity of bigeye scad averaged about twice that of round scad. Fecundities of bigeye scad and round scad are similar to those reported for other tropical carangids. Annual reproductive output appears to be higher in bigeye scad and round scad than in the temperate Trachurus spp., but spawning frequency of the latter may have been underestimated by most previous studies.

Pelagic mackerel-like species of the family are important compo- nents of coastal pelagic ecosystems in both temperate and tropical regions. In temperate areas, particularly in eastern boundary upwelling systems, jack or horse mackerels, (Trachurus spp.), are typically second in importance only to clupei- forms in abundance and fishery yield. The counterparts of Trachurus spp. in most tropical and sub-tropical areas are species of the genera Selar and Decapturus. These genera make up important fractions of fishery yields throughout the lndo- Pacific. In Hawaii, catches of the bigeye scad or akule, S. crumenophthalmus, and the round scad or opelu, D. macarellus, were almost 500 tons in fiscal year 1990- 91, and as a group were exceeded in value only by the scombroids, deep bottom- fishes (lutjanids and serranids), and coryphaenids (Hawaii Division of Aquatic Resources statistics). Carangids, particularly tropical species, are poorly studied compared to clu- peiforms or scombroids. Studies in Hawaii by Yamaguchi (1953) and Kawamoto (1973) represent the best sources of data on the biology of round scad and bigeye scad, respectively, but neither investigated any aspect rigorously or with modern methodology. Spawning frequency has not been investigated in either genus. In this paper we present results of an investigation of reproductive biology of both species based on samples taken from fishery catches in Hawaii. Our objectives were to determine as precisely as possible the above and other reproductive vari- ables for eventual use in management of the fisheries and for comparison with available data on other carangids-particularly the temperate Trachurus spp.

MATERIALS AND METHODS

Fish Samples.-We attempted to purchase samples at approximately monthly intervals from commer- cial fishery catches. All bigeye scad and most round scad were caught off the leeward (SW) side of the island of Oahu. All results given here are based on taken between 1-2 h after sunset and 1- 2 h before dawn by surface handline used in conjunction with a night light. Fish were placed on ice immediately after capture and held iced until laboratory analyses after landing the next morning.

33 34 BULLETIN OF MARINE SCIENCE, VOL. 56, NO.1, 1995

Table 1. Linear least squares regressions of size and fecundity relationships for bigeye scad Selar crumenophthalmus and round scad Decapturus macarellus from Hawaii. Power functions are the antilog forms of linear regression using logarithms. Regressions between standard length (SL) and fork length (FL) or somatic weight (S) include data from both sexes and all seasons. For round scad the relationship between SL and the length used by Yamaguchi (1953) (YL) is also given. Regressions between batch fecundity (F) and SL, S, and between gonad weight (G) and S are based on females with separate advanced groups of oocytes.

Regression N r Bigeye Scad FL = 5.96 + 1.054SL 450 0.98 S = 5.44E-06Sl}253 450 0.94 F = -363,347 + 2,248SL 23 0,34 F = 1.40E-04SL3.818 23 0.204 F = 12,236 + 507.5S 23 0.31 F = 459.42S1.027 23 0.30 G = 1.05 + 0.0198S 23 0.41 Round Scad FL = 7.23 + 1.027SL 738 0.99 YL = 14.96 + 0.969SL 157 0.98 S = 1.40E-05SL3OI2 738 0.98 F = -199,300 + 1,037SL 20 0.29 F = 1.01E-03SU217 20 0.25 F = -14,454 + 305S 20 0.35 F = 133.46SI.085 20 0.52 G = -1.66 + 0.0225S 20 0.47

Though we attempted to obtain fish taken just before dawn, on some dates adult-sized fish were taken only before midnight or the fishermen were unable to tell us when they were caught. Consequently, some of the samples were comprised wholly or partially of fish which had been caught before midnight and had been on ice almost 12 h between capture and preservation of the gonads. Catches from the inshore, day (net) fisheries for both species were too sporadic and unpredictable to routinely sample and are apparently comprised mainly of immature fish. Bigeye scad catches were fairly regular and predictable, but were usually restricted to the period between third and first lunar quarters. We collected samples from July 1989 to June 1991; all months were covered except March, August, and December, 1990. Because mature-sized bigeye scad proved to be sexually dichromatic, we usually selected 15-20 adult females for each sample, but for some months, mostly during the winter, there were only 5 to 10 females in the catches we examined. Samples of 10-15 adult males were collected from April, June, July, August, October, and November; other males that were occasionally misidentified as females were included. Round scad landings were not as regular or predictable as those of bigeye scad. Sixteen samples of ca. 50 unsexed fish each were purchased between January 1990 and November 1991; there were gaps >1 mo in temporal coverage between April and July, 1990; November, 1990 and February, 1991; and February and April, 1991. Even though we tried to select the largest fish from the catches, the samples frequently contained few adult females; half contained fewer than 10. Laboratory Procedures.-Standard length (SL) and fork length (FL) of each specimen were measured to the nearest rom, and total body weight was recorded to the nearest 0.1 g. Length-weigh: relationships were determined using linear least squares regression on the logarithms and expressed in antilog form as power functions (Table 1). We also give in Table 1 relationships between standard and fork length, which has been used by other studies. Because Yamaguchi (1953) used the distance "from the tip of the snout to the end of the silvery area on the caudal fin" as "standard length," we also determined the relationship between standard length and his "standard length" for a smaller series of round scad. In practice, the differences are slight and were mostly ignored for comparisons with his data. The gonads of each specimen were removed and preserved in 4% formaldehyde/seawater solution. Subsequently, gonads were blotted dry, weighed to the nearest 0.01 g, and the gonad to somatic weight ratio (G/S, as percent) calculated using gonad-free body weight. For all females, a small subsample of the ovaries was teased apart on a glass slide and examined under a compound microscope at 100X. Vitellogenesis was visually evident in oocytes >0.20-0.25 rom in diameter. Females with oocytes 050.25 mm in diameter were classed as immature, and those with oocytes >0.25 mm in diameter as mature. CLARKE AND PRIVITERA: HAWAIIAN CARANGID REPRODUCfION 35

For all mature females, the diameters of ca. 100 oocytes ;0:0.20 mm were measured to the nearest 0.01 m with an ocular micrometer. Oocytes are not perfectly spherical, and we measured the maximum "diameter" of each oocyte. Because the largest unhydrated oocyte (LMX) could be determined for all females regardless of whether or not the oocyte size-frequency distribution was bimodal, we used this value for comparison of overall oocyte size among females. If the oocyte size-frequency distri- bution was bimodal and the advanced modal group was distinctly separated from smaller oocytes, i.e., there was no overlap in size between the advanced and smaller modal groups, we determined the median size of oocytes in the advanced group (LMO). If an advanced modal group was present but not separated from smaller oocytes, i.e., if only LMX could be unequivocally determined, we estimated LMO based on differences in opacity between heavily yolked opaque oocytes apparently belonging to the left hand "tail" of the advanced group and similarly sized, more nearly translucent oocytes in the smaller, modal group. The presence of hydrating or ovulated ova was recorded, but these, which were infrequent, were not included in determining LMX. Batch fecundity was determined for females with a distinct advanced modal group of oocytes. Both ovaries were blotted dry and individually weighed to the nearest 0.01 g. A sample of at least I % of the wet gonad weight was removed from the right ovary, and all of the oocytes in the advanced group were counted under a compound microscope at 40X. For a few specimens of each species with incompletely separated advanced groups, we also estimated fecundity based on counts of the more opaque oocytes. Because of difficulty in consistently determining wet weight of small samples of the ovary, both the sample and the right ovary were placed separately into preweighed pans and dried at 60°C for 24 h. The pans were then reweighed to the nearest mg, and the dry weights of the sample and right gonad were determined by subtraction. The dry weight of the left ovary was estimated from its wet weight and the ratio of dry weight to wet weight of the right ovary. This ratio averaged about 40% for ovaries with vitellogenic, but unhydrated oocytes. Potential batch fecundity was calculated as the product of the number of advanced oocytes in the sample and the estimated dry weight of the ovaries divided by the dry weight of the sample. Relative batch fecundity was calculated as number of oocytes/g ovary-free body weight. For histological examination, ovaries were sectioned and stained with hematoxylin/eosin as de- scribed by Hunter and Goldberg (1980). The slides, identified by only a code number, were examined by each of us independently for presence of postovulatory follicles. Except for one round scad, the postovulatory follicles were readily apparent, numerous, and at roughly similar stages of degeneration for all specimens scored positive. The follicle cells were distorted in shape but still intact, and although the follicle had collapsed, the lumen was still evident. For specimens scored negative, there were either no traces of postovulatory follicles or, rarely, a few structures that were, at best, questionably postovu- latory follicles in the last stages of degeneration. We also examined the slides from females with large oocytes for coalescence of oil droplets and migration of nuclei.

RESULTS Bigeye Scad.-Both GIS and oocyte size data indicated that bigeye scad spawn from April through October. All female bigeye scad with GIS > 1% occurred during this period, and GIS was <0.5% for all but 1 of the 71 taken during the rest of the year (Fig. 1). Less extensive data for males (not shown) also indicated that GIS values> 1% occurred only during April through October. Females judged mature on the basis of oocyte size were also restricted to April through October. During this period 82% of the 249 females taken were mature; 96% of the mature females had more developed oocytes (LMX 2::0,35 mm). All but two of the fe- males with LMX <0.35 mm were from either April or late August through Oc- tober. The spawning season appeared to end earlier in 1990 than it did in 1989 and to start earlier in 1990 than in 1991. LMX was >0.25 mm in 76% of the females from September and October, 1989, but in only 21% of those from the same months in 1990. Only one of the ten females from April, 1990, was immature, but 86% were immature in the same month of 1991. Our data are insufficient to properly estimate size at first maturity in bigeye scad. Based on both LMX and GIS values (Fig. 2), the smallest mature female was 199 mm SL and most larger females were mature during the spawning season. Females <210 rom were not, however, present in all samples during the spawning season, and only one female less than 199 rom SL was included. Bigeye scad < 190 mm 36 BULLETIN OF MARINE SCIENCE, VOL. 56. NO. I, 1995 BIGEYE SCAD 4.0

.I .: ..-.. 3.0 I ~ 0 0 • I .. I i 0 o :

CI)- I 0 •• ...•.... •• . o 2.0 o I Ii CJ • I 00. • 0 ': I ·. • • ·: 1.0 . 0 . . • • . I , · . C 60 120 180 240 300 360 CALENDAR DAY

ROUND SCAD 4.0

..-.. 3.0 ~0 CI)- ...•.... CJ 2.0

·• I • 1.0 · o '. .,I : : I . • o • . I 0.0 .. • J ••. I • 0 60 120 180 240 300 360 CALENDAR DAY

Figure 1. Gonad to somatic weight ratio (GIS) vs. calendar day for mature-sized female bigeye scad Selar crumenophthalmus (upper, N = 320) and round scad Decapturus macarellus (lower, N = 237) from Hawaii. Points are from fish> t 99 mm and >245 mm standard length, respectively.

SL taken by one of us (TAC) in other, miscellaneous collections in Hawaii were immature; thus size at first maturity is probably about 190-200 mm SL. Bigeye scad >220 mm SL were sexually dichromatic during the spawning season. The soft portion of the anal fin was dark black in males and almost pure CLARKE AND PRIVITERA: HAWAIIAN CARANGlD REPRODUCTION 37

BIGEYE SCAD 4.0 ...... ·. ..•..••. 3.0 . • .. :. .e _. ~ Ie · ••• 1 0 ....- .... :' •..- .:: ... (f)- .. -,-.-.: .....•.. ) ••• -.- ••• e (!) 2.0 . •. •••. ==...... ~~ •• :a:1 J:-..... '.. ·...'. - 1.0 · 1.:-...••••.:., • I, •• •• •'! ••• . •:: I...•••••: . . " 0.0 . 180 200 220 240 260 280 STANDARD LENGTH (mm)

ROUND SCAD 4.0

..•..••. 3.0 ~ 0 . .e '.' (f)- ' ...... •.. . . . 2.0 ...... , . (!) ,_I. ,,' . , ..~ .. .'.' .. • • •I..f/' • . .' .: : •I, . '...' .. 1.0 " .' ..' '.: ,- ... .- ." . .. . • • I. f1' : .,....-. .' -~ .... -:....•"'-1"- I' 0.0 180 200 220 240 260 280 300 320 STANDARD LENGTH (mm)

Figure 2. Gonad to somatic weight ratio (GIS) vs. standard length for female bigeye scad Selar crumenophthalmus (upper, N = 249) and round scad Decapturus macarellus (lower, N = 216) from Hawaii. Points are from all females taken during the spawning seasons: April through October and April through August, respectively. white in females. Occasionally we found females with barely visible gray patches on the anal fin. This difference was less clear (and less useful in selecting females for our sampling) for fish < about 220 mm SL and during the winter (non- spawning) months. For small fish and during the off season, the anal fins of males were often more gray than black and those of females were rarely as completely white as in large females taken during the spawning season. 38 BULLETIN OF MARINE SCIENCE, VOL. 56. NO. I. 1995 BIGEYE SCAD

4.0 · . . . : -I •• - 3.0 .-. 1-.=_ •. 1 • -~o .. . . _:1._. =.;ii:- •. - _ • I. 2.0 i := • I ••••• :.==• 1 ••••••••:::.1- .- I •••••• ' " . • . .. • 1.0 • "n····. n • • • • " 0.0 +------r--..-----...---..---~--.__-~-- 0.20 0.30 0.40 0.50 0.60 LMX(mm)

ROUND SCAD 4.0

3.0 . . -~o - .. •• 2.0 • •• • ...... I • • :.... • ·•• 11.·.....• ..I:. .. 1.0 • • • •• 1 .1...... :... " '.1 ••••• 0.0 +-.--..-----y--..----.----.....----,,...---.----, 0.20 0.30 0.40 0.50 0.60 LMX(mm) Figure 3. Gonad to somatic weight ratio (GIS) vs. diameter of the largest unhydrated oocyte (LMX) for reproductively active female bigeye scad Selar crumenophthalmus (upper, N = 221) and round scad Decapturus macarellus (lower, N = 142) from Hawaii. Points are from all femaks with LMX >0.20 mm taken during April through October and April through August, respectively.

For females with LMX >0.35 mm, both GIS (Fig. 3) and development of separate size-freqUiency modes were generally correlated with LMX, but there was considerable individual variability. In most fish with LMX 0.35-0.41 mm there was little evidence of an advanced size-frequency group of oocytes (Fig. CLARKE AND PRIVITERA: HAWAIIAN CARANGID REPRODUCTION 39

10

o 15 (b)

10

-a: 0 15 w (c) :;aCD :::::> 10 ---Z >- 0 Z 0 w :::::> 15 a (d) w a: 10 LL

0

10

OOCYTE DIAMETER (mm) Figure 4. Oocyte size-frequency plots from five bigeye scad Selar crumenophthalmus representative of different stages of oocyte development observed in Hawaiian specimens.

4a), but partially and, rarely, completely separated groups were found in a few cases (Fig. 4b). Advanced groups of oocytes were present in most fish with LMX >0.41 mm. Size-frequency distributions of the advanced groups were often skewed toward the larger sizes, and frequently there was a 0.01-0.06 mm long "tail" of opaque oocytes that overlapped in size with more numerous and mostly smaller oocytes that were more nearly translucent (Fig. 4c). The advanced group was rarely as distinctly separated as in Figure 4d, and was barely evident in a few fish with large oocytes (Fig. 4e). For 75 females with distinct advanced modal groups, mean LMX was 0.46 mm (range: 0.40-0.52 mm); mean LMD was 0.39 mm (range: 0.35-0.45 mm). Values were similar for 32 females with incompletely 40 BULLETIN OF MARINE SCIENCE. VOL. 56. NO. I, 1995 separated advanced groups; mean LMX was 0.45 mm (range: 0.40-0.50), and mean estimated LMD was 0.38 mm (range: 0.34-0.43). In 21 females with LMX ~0.35 mm, there were, among the ca. 100 oocytes measured for size·-frequency,one to three unhydrated oocytes 0.03-0.08 mm larg- er than the next largest oocyte, i.e., separated from the most advanced group of developing oocytes. Such oocytes, which were excluded for determination of LMX, could have been exceptionally large oocytes of the most advanced group or may have represented the residual "tails" of recently spawned batches. Post- ovulatory follicles were present in five of the twelve examined histologically; in six of the nine not examined LMX was <0.41 mm, which also indicates recent spawning (see below). LMX was 0.43-0.45 mm in the remaining three unex- amined fish. Hydrated ova were found in only 7 of the 203 mature females examined. Only one carried a large number of ovulated eggs 0.66-0.74 mm in diameter, some of which were in the oviducts and easily extruded by pressure on the abdomen. The other six females carried only a few (1-2 per subsample examined for oocyte size-frequency) unovulated, hydrated ova 0.57-0.74 mm in diameter. In the fish with ovulated eggs and five of the others, the largest unhydrated oocytes were small (LMX = 0.38-0.42 mm), and postovulatory follicles were present in his- tological preparations. In the remaining female, there was a nearly separated size- frequency group of large unhydrated oocytes (LMX = 0.52 mm), and postovu- latory follicles were absent. Ovaries from 105 females with LMX ranging from 0.35 to 0.52 mm were examined histologically. These included an initial sample of 30 fish selected to cover a wide range of LMX and development of modal groups plus all the mature females from four samples (N = 10-37) taken during the spawning season. Post- ovulatory follicles were present in 33% of the total examined. Percentages with postovulatory follicles for individual samples ranged from 20-60%; 95% confi- dence limits for estimates from all individual samples included 33%. With few exceptions, those with LMX >0.41-0.42 mm had not spawned recently and those with smaller oocytes had (Fig. 5). In fish with LMX >0.50 mm, coalescence of oil droplets appeared to be starting in some oocytes, but none were in the migra- tory nucleus stage. Among the total of 195 females with LMX ~0.35 mm, LMX was <0.42 mm in 36%--close to the percentage with postovulatory follicles among those examined histologically. Batch fecundity was estimated for 23 females (199-256 mm SL) with separate advanced modal groups .of oocytes (LMO = 0.35-0.42 mm). Histological prep- arations were done:for 15 of these; postovulatory follicles were present in none. Fecundity ranged between 48,000 and 262,000; mean relative batch fecundity was 559 oocytes/g (range: 289-1005). In about half the females used for fecundity analyses, the advanced modal group was roughly symmetrical in shape, while in the remainder there was a "tail" of small eggs on the left of the mode. The oocytes in the "ta:il" amounted to roughly less than 10% and usually less than 5% of the total oocytes in the batch, and there was no consistent difference in fecundity estimates between those with and without a "tail." Batch fecundity was not well predicted by either standard length or weight based on either linear or linear log-log regressions (Table 1). Gonad weight, like fecundity, was poorly correlated with somatic weight (Table 1). For six other females with the advanced groups incompletely separated in terms of size frequency, batch fecundities and relative fecundities estimated from counts of relatively opaque oocytes fell within the ranges observed for females with distinct advanced groups. Dry weights of five subsamples of 10 eggs each from the single female bigeye CLARKE AND PRIVITERA: HAWAIIAN CARANGID REPRODUCTION 41

25 BIGEYESCAD TOTAL ...... +..... + POF 20 >- ---0--- - POF () Z 15 W :J wa 10 a: u. 5

o 0.35 0.40 0.45 0.50 0.55 LMX (mm)

Figure 5. Frequency vs. diameter of largest unhydrated oocyte (LMX) for female bigeye scad Selar crumenophthalmus with oocytes >0.35 mm in diameter. Dashed lines are for specimens examined histologically; "+" symbols indicate the 35 for which postovulatory folIicles (POF) were present, "0" symbols. the 70 without. Solid line is for all 195 specimens with oocytes 20.35 mm, including the 105 examined histologically. scad with hydrated, ovulated eggs indicated that mean weight per eggs was 14.9 J.Lg.Assuming that egg dry weight is not affected by hydration (Lecluse, 1979) and that drylwet weight ratio of bigeye scad is about 25-30%, a batch for a female with mean relative fecundity would represent about 3% of body weight. The relative cost per batch in terms of organic weight or energy would probably be higher since ash content of the eggs is probably lower than that of the fish. Round Scad.-Mature female round scad occurred almost exclusively from April through August; among females from the remainder of the year LMX was >0.25 mm in only four from March. GIS values >0.5% were also nearly restricted to April through August (Fig. 1). All but three of the mature females were >245 mm SL; the exceptions (231-242 mm SL) were taken during the middle of the spawning season. During the spawning season, 81% of the females >245 mm SL were mature and GIS was >0.5% (Fig. 2); in over 75% of them LMX was 2::0.35 mm. Most of the adult-sized, but immature females taken during the spawning season were from either April or late August. Data from 331 male round scad (not shown) indicated that size at maturity and breeding season were similar to that of females. With one exception all males with GIS> 0.5% were >245 mm SL, and except for a few males from a Sep- tember sample, GIS was >0.5% only during April through August. We found no evidence of sexual dichromatism in mature round scad. Among the 120 females with LMX >0.35 mm, LMX and GIS were generally positively correlated, but the latter varied greatly for given values of LMX (Fig. 3). There were only nine females with LMX between 0.35 and 0.43 mm, the range of LMX for bigeye scad that had recently spawned. The largest unhydrated oocytes found were 0.60 mm in diameter-about 15% larger that the largest found in bigeye scad. Oocyte size-frequency distributions were bimodal in some fish with LMX as low as 0.44 mm, but even in fish with larger oocytes, the advanced 42 BULLETIN OF MARINE SCIENCE, VOL. 56, NO. I, 1995

modal group was often not completely separated from smaller oocyt:es. Four fe- males carried a few hydrating, but unovulated, oocytes 0.58-0.74 mm in diameter. LMX in these was 0.49-0.60 mm; none of the unhydrated oocytes were in the migratory nucleus stage. Ovaries from all nine females with LMX of 0.35-0.43 mm and a sample of 27 others with LMX of 0.44-0.56 mm were prepared for histological examination. Postovulatory follicles were present in only three fish with LMX of 0.40-0.43 mm; in one of these the postovulatory follicles were considerably more degen- erated than in the other two or in any of the bigeye scad. Structures that could have been very degenerated postovulatory follicles were found in one other spec- imen with LMX := 0.52 rom. Estimated batch fecundity ranged from 13,000-236,000 for 20 females 248- 300 mm SL with distinct modal groups of advanced oocytes (LMD = 0.37-0.51 mm). Postovulato:ry follicles were absent in all 10 examined histologically. Only about half the variation in fecundity was accounted for by variation in fish weight (Table 1), and relative batch fecundity varied over tenfold (Table 2). Gonad weight was also poorly correlated with somatic weight (Table 1). As was the case with bigeye scad, many of the fecundity estimates were from females with a "tail" of small oocytes on the advanced group. The number of oocytes in the "tail" was, however, usually <5% of the total in the group, and inclusion of data from these fish was not the major cause of size-independent variability in batch fecundity. Estimated fecundity and relative fecundity of six other females with incompletely separated advanced groups fell within the range of values for the 20 with distinct groups.

DrscussrON The sexual dichromatism of reproductively active bigeye scad facilitated our sampling of fishery catches for this study. Sexual dichromatism has been reported previously for six carangid genera including Selar and Decapturus by Shameem and Dutt (1984) and for Caranx ignobilis by von Westemhagen (1974) and Talbot and Williams (1956). Although we did not observe dichromatism in round scad, it might be evident only in freshly caught specimens. Our estimates of spawning season of bigeye scad and round scad in Hawaii are similar to those of Kawamoto (1973) and Yamaguchi (1953), respectively. Our estimate of size at maturity in bigeye scad (:5200 mm SL) is somewhat lower than Kawamoto's (about 215 mm SL after conversion from fork length to standard length). Kawamoto's estimated growth rates indicate that bigeye scad reach ma- turity before they are a year old, i.e., that even fish hatched from eggs spawned at the end of the spawning season are likely to reach maturity during at least part of the next year's season. Our estimate of size at maturity of round scad (245 mm SL) is considerably larger than Yamaguchi's. He found mature fish as small as 175 mm and stated that all fish over 220 mm were mature during May-August. Though we found one mature female only 231 mm SL, most females <245 mm SL were clearly immature during the spawning season. Because the of the genus was unclear at the time of Yamaguchi's study, we suspect his samples, which were mostly from daytime inshore catches, may have included both D. macarellus and D. macrosoma. Tiews et al. (1970) reported that the latter matures at about 210 mm TL. The near absence of females with hydrated ova in our nighttime samples of both species indicates that they spawn sometime between dawn and dusk. Of the seven bigeye scad with hydrated ova, five had recently spawned most of their CLARKE AND PRIVITERA: HAWAIIAN CARANGID REPRODUCfION 43

e" o" '"

.~'" ·E" u

~ ~I"- NID r'lN -I IN t:.e. ON IDN NID IDlI) I"-lI) I I - I I

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N e§e§e§~§e~ § r;;" e e e e e e § ~O_OOO\OOC)OO"

r'lOo\-OOll)lI)lI)OO lI)- Z NN~N...... -lN('()"""....-l""" M- 44 BULLETIN OF MARINE SCIENCE, VOL. 56, NO. I, 1995 large eggs, one was either spawning or about to spawn, and one was possibly beginning to hydrate a batch for spawning in the near future. The four round scad with hydrating eggs also appeared to be in the early stages of preparing for spawning. Because we have no data on day-caught fish, we cannot exclude the possibility that either species spawns at night but that the females with hydrated ova are infrequently captured by night fishing methods; however, the above evi- dence plus the absence of females with oocytes in the migratory nucleus stage is more consistent with daytime spawning, Most other observations of carangids indicate daytime spawning. von Western- hagen (1974) observed spawning by Alectes indicus and Caranx ignobilis during the day and suggested that interactions required visual contact. Johannes (1981) reported that several species of carangids apparently spawn during the day; he also reported daytime spawning for "Trachurus hoops" (which he lists under Scombridae, but almost certainly means Trachurops [=Selar] hoops, a congener of bigeye scad). Our unpublished data on both planktonic egg stages and adults of the omaka, Atule mate, in Hawaii clearly indicate spawning during the day. Farris's (1961) dalta on planktonic egg stages of the jack mackerel, Trachurus symmetricus indicate, however, that this temperate species spawns around mid- night. Our estimates of fecundity in bigeye scad and round scad are based on size- frequency modal groups of developing oocytes and could overestimate fecundity if not all eggs in the group are ripened and spawned. The occasional presence of unovulated, hydrated ova in fish that had recently spawned and of larger ooctyes isolated from the main group of developing oocytes indicate that in at least some individuals, a fraction of the oocytes in the advanced group are left behind and not spawned. These "stragglers" amounted to <5% of the oocytes i.n the sub- samples; thus their effect on fecundity estimates is minor--especially compared to the high variability in fecundity and relative fecundity values. The percentage of female bigeye scad with postovulatory follicles indicates that individual females spawn about every three days. This assumes that the postovula- tory follicles were all from spawning within the last 24 h before captun~.Postovu- latory follicles remain detectable for at least 2 days in species such as the northern anchovy (Hunter and Goldberg, 1980) which live at lower temperatures, but de- teriorate beyond recognition in less than 24 h in the tropical Hawaiia.n anchovy (Clarke, 1.987).The postovulatory follicles observed in preparations from bigeye scad ovaries were all readily apparent and were similar to the early stages of collapse and degeneration described by the above studies. If postovulatory folli- cles were detectable for more than 24 h after spawning, some fish would be expected to have more degenerated, completely collapsed postovulatory follicles. Our estimate of spawning frequency also assumes our samples were not biased with respect to spawners and non-spawners. Segregation of spawning females during the day may well occur, but given that bigeye scad appear to stay within a rather narrow range of depth and distance from shore (Kawamoto, 1973), it seems likely that s.pawning and non-spawning females would have remixed by the time they begin feeding at night and would be equally susceptLble to the fishery. The near absence of female round scad with postovulatory follicles indicates that spawning frequency is much lower than in bigeye scad, but our results with round scad are more equivocal. Round scad occur farther from shore than do bigeye scad, and the nighttime fishermen generally also range farther offshore. If round scad spawn during the day, the spawning areas could be sufficiently re- moved from the area where the fishery operates that spawners do not completely CLARKE AND PRIVITERA: HAWAIIAN CARANGID REPRODUCTION 45 remix with the exploited fraction of the population by nighttime. Alternatively, postovulatory follicles may deteriorate beyond recognition much more rapidly than in bigeye scad. Fishermen generally agree that flesh quality of round scad deteriorates or "goes soft" much sooner than in bigeye scad, and it is possible that round scad gonadal tissue also deteriorates more rapidly after capture. Assuming a spawning frequency of once every 3 days and the estimated av- erage cost per batch as a percentage of female weight, reproductive output in bigeye scad is about I% of body weight/day. We have no idea how long individual females spawn at this rate, but our data on oocyte size indicates that during the spawning season almost all mature-sized females carry oocytes that could be advanced to spawning size within 3 days. Even if individuals only spawned for a month, the output would be almost a third of body weight. Costs of reproductive output in bigeye scad are unlikely to be met by reserves accumulated during the short non-spawning season. Hunter and Leong (1981) have estimated that the northern anchovy, which spawns only about once per week, can meet only about 35% of its seasonal reproductive requirements from body reserves and must depend on feeding during the season for the rest. In tropical species such as bigeye scad, the Hawaiian· anchovy (Clarke, 1987) and skipjack tuna (Hunter et aI., 1986), which spawn much more frequently, main- tenance of continued reproductive output would require a consistent high level of food intake. As Clarke (1987) suggested for the Hawaiian anchovy, individual variation in recent feeding success could result in short term variation in energy available for oocyte development and may thus be responsible for the high size- independent variation in both gonad weight and batch fecundity observed in this study. Our data indicate several differences, besides the apparent difference in spawn- ing frequency, between bigeye scad and round scad. Round scad mature at a larger size and probably greater age. The spawning season of round scad is shorter. Maximum diameters of both unhydrated oocytes and hydrated ova in round scad are roughly 15-20% larger than those of bigeye scad and therefore about 50-70% greater in volume. Even if round scad spawn as frequently as bigeye scad, relative reproductive rate per batch is probably lower. The difference in egg size is in- sufficient to compensate for differences in relative fecundity. Although mature- sized round scad females are ca. 25% larger than bigeye scad, batch fecundities are similar, and mean relative fecundity of bigeye scad is about twice that of round scad. Comparison of our data with those from other species of Decapturus and other tropical carangids (Table 2) is limited because previous studies have often not based fecundity determination on distinct oocyte size-frequency modal groups. Most other species of Decapturus appear to mature at smaller sizes than D. ma- carel/us, but estimated "fecundities" are in the same range as observed in both species we investigated. Data from two larger Caranx spp. indicate that relative fecundities are of the same order as observed here and that individual variability in relative fecundity is likewise high. Reproductive output in bigeye scad and round scad appears to be higher than reported in temperate jack mackerels (Table 2). MacGregor's (1976) estimates of mean relative batch fecundity for Trachurus symmetricus are much lower than our means for bigeye scad and round scad. Chigirinsky's (1970) estimates of the "first batch" of eggs in T. japonicus are comparable to those for bigeye scad and round scad. Chigirinsky concluded that yolked oocytes in other, smaller "batches" might be spawned during the same season; inclusion of these provided annual fecundity estimates that would be matched by bigeye scad or round scad spawning 46 BULLETIN OF MARINE SCIENCE, VOL. 56, NO. I, 1995 only 2-3 times per year. Macer (1974) estimated annual fecundity of T. trachurus from the total of vacuolated plus yolked oocytes at the beginning of the season. His values are understandably greater than batch fecundity estimates for bigeye scad and round scad-in part because his specimens were apparently larger, but again either of the tropical species would have to spawn only a few times per season to exceed the estimates for T. trachurus. The above results may, however, underestimate seasonal output in Trachurus spp. Lisovenko and Andrianov (1991) report that T. symmetricus murphyi is an indeterminate spawner. Although they give few details or supporting data, they state that output over a spawning season can be as high as 1.2 X 106 eggs-roughly equivalent to about 12 batches in bigeye scad or round scad. Further consideration of differences in life history variables between temperate and tropical carangids will require better understand- ing of spawning frequency and duration in both groups as well as better data on other relevant variables such as age and size at maturity and reproductive lifespan.

ACKNOWLEDGMENTS

We are particularly grateful to C. and H. Aoki, B. Rice, and B. Takenaka for their assistance and cooperation in obtaining our samples. We also thank R. Famble, M. Minford, and S. Murphy-Walker for assistance in analyse:s.This study was supported by the Hawaii Division of Aquatic resources, the University of Hawaii Sea Grant Program, and by the University of Hawaii, Hawaii Institute of Marine Biology. This is UNlHl-SEAGRANT-JC-94-33 under NOAA grant NA 89AA-D-SG063.

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DATE ACCEPTED: October 6, 1993.

ADDRESS: Hawaii Institute of Marine Biology, University of Hawaii at Manoa, P.O. Box 1346, Kaneohe, Hawaii 96744.