Transactions nf the American Fisheries Society 126:309-315, 1997© Copyright by the American Fisheries Society 1997

Temperature Effects on Feed Utilization and Growth ofPostsettlement Stage Nassau Grouper

SIMON C. ELLIS,' WADE O. WATANABE,2 3 AND EILEEN P. ELLIS'Caribbean Marine Research Center

805 East 46th Place, Vero Beach, Florida 32963. USA

Abstract.—Feed utilization and growth of hatchery-reared, postsettlement stage Nassau grouperEpinephelus st Hants (mean weight = 3.20 g) were compared for 63 d at temperatures of 22, 25,28, and 3I°C under controlled laboratory conditions. Final weights (W/) and specific (SGR) andrelative (RGR) growth rates were significantly (P < 0.05) higher at 28 and 31°C (Wj•= 10.5-12.4

g. SGR = 1.95-2.07%/d, RGR = 246-273%) than at 22 or 25°C (Wf = 7.33-8.70 g, SGR =1.32-1.52%/d. RGR = 131-164%). Temperature unit requirements per gram of growth (range =342-234°C x d/g) also appeared to decrease with temperature within this range. Higher growthwith increasing temperature was related to feed consumption (% body weight/d), which increasedsignificantly (P < 0.05) from 1.60 at 22°C to 2.23 at 31 °C. Feed conversion ratio (weight fed/weightgained: range = 1.23-1.04) and condition factor (10-1 X weight/length-^: range = 30.6-31.7) didnot differ among treatments. Survival did not differ and remained high (range = 96.4-100%)under all treatments. The results demonstrate that sea temperature within an ecological range haspronounced and direct effects on feeding and growth of juvenile Nassau grouper. Based on in situ

sea temperature data in a known juvenile habitat, we hypothesize that liming of spawning inrelation to seasonally changing sea temperatures in these habitats may be important in determiningjuvenile growth rates, vulnerability to predation, and hence, year-class strength. A temperaturerange of 28-31°C is recommended for culture of early juveniles, although higher temperaturesmay be feasible.

The Nassau grouper Epinephelus striatus is amajor predator in Atlantic Ocean coral reef sys-tems (Shenker et al. 1993) and is an importantcommercial fishery in many areas of the Caribbeanand tropical western Atlantic (Colin 1992). Over-fishing of spawning aggregations and environ-mental degradation have resulted in steep declinesin natural populations (Colin et al. 1987), makingthe Nassau grouper a candidate for the U.S. en-dangered species list (Sadovy 1993). High con-sumer demand has stimulated research into the ear-ly life history and ecology of this species (Colinet al. 1987; Colin 1992; Shenker et al. 1993; Tuck-er et al. 1993) and into artificial propagation forcommercial cultivation or stock enhancement(Tucker et al. 1991; Watanabe et al. 1995a, 1995b,1996; Ellis et al. 1996; Head et al. 1996).

Yearly fluctuations in wild adult fish populationsare thought to be caused by recruitment variability,which is dependent on larval and juvenile mor-tality rates (May 1974; Houde 1987, 1989; Pepin

1 Present address: Sea Change Foundation, 4731North Highway Al A. Vero Beach, Florida 32963, USA.

2 Present address: Center for Marine Science Re-search, The University of North Carolina at Wilmington,7205 Wrightsville Avenue, Wilmington. North Carolina28403, USA.

3 To whom correspondence should be addressed.

1991). Although most research has emphasizedfactors that influence mortality during the earlylarval stages, there is evidence that mortality dur-ing juvenile stages can also have an important ef-fect on year-class strength (May 1974; Leggett etal. 1984; Smith 1985; Folkvord and Hunter 1986;Houde 1987; Kaeding and Osmundson 1988; Leg-gett and Deblois 1994; Malloy and Targett 1994).

Water temperature is the most potent physicalenvironmental factor controlling growth in the ear-ly life stages of fishes and is often correlated withmortality and recruitment variability in juvenileand larval temperate marine fishes (Sissenwine1974; Leggett et al. 1984; Malloy and Targett1994), although mechanisms are poorly under-stood (Buckley et al. 1990). There is evidence thatwater temperature can also have an important in-fluence on juvenile and larval marine finfish re-cruitment in tropical and subtropical areas (Bohn-sack and Talbot 1980; Walsh 1987) where subtledeclines in growth rates due to unfavorable tem-peratures can lead to large increases in mortalitythrough predation (Houde 1987).

Little or no information is available on the ef-fects of temperature and other environmental fac-tors on growth of postsettlement stage Nassaugrouper. Given a potential for considerable intra-and interannual variation in sea temperatures over

309

310 ELLIS ET AL.

TABLE 1.—Mean growth, survival, and feed conversion values ± SD for juvenile Nassau grouper reared at fourdifferent temperatures for 63 d (N = 6). Means in the same row without a letter in common are significantly different(Ryan-Einot-Gabriel-Welsch multiple-range test; P < 0.05).

Variable3

Temperature (°C):22 25 28 31

Initial weight (g)CV initial weight (%)Initial length (mm)Final weight (g)

CV final weight (%)SGR (%/d)RGR (%)FC (%)FCRCondition factorSurvival (%)TU/g (°C X d/g)

3.18 ± 0.27 z31.547.17.3352.51.321311.641.1530.6100

0.80 z1.15z0.77 zl . I O z0.17z25 z0.14 z0.12 z0.76 z0.00 z

342 63 z

3.2928.147.78.7054.71.52164

1.921.2330 Q98.8

0.07 z0.20 z0.25 z1.67z1.00 z0.30 z50.9 z0.11 y0.20 z1.03z2.91 z

313 86 z

3.02 ± 0.40 z30.0 ± 0.50 z46.5 ± 1.85z1 0.5 ± 2.36 y63.8 ± l.20zl.95±0.30y246±64y

2.10 ± 0.16 yx1. 04 ± 0.09 z31.7 ± 1.34 z96.4 ± 3.91 z254 ± 7 1 z

3.29 ± 0.20 z30.7 ± 0.70 z47.8 ± 0.99 z1 2.4 ± 3.20 y63.1 ±0.80z2.07 ± 0.3 l y273 ± 74 y

2.21 ±0.18x1.04 ±0.11 z31.5 ±0.50z98.8 ±2.91 z234 ± 79 z

CV = coefficient of variation; SGR = specific growth rale; RGR = relative growth rale; FC = feed consumption; FCR = feed conversionratio; TU/g = temperature unit requirements per gram of growth.

the natural range of the Nassau grouper (20°S to32°N latitude), it is clear that understanding thethermal requirements of the early life historystages may be important in elucidating natural pat-terns of distribution and abundance. Such infor-mation can also delineate optimum rearing con-ditions for aquaculture.

Under controlled laboratory conditions, we testthe hypothesis that water temperature, within theecological ranges encountered by early life historystages of Nassau grouper in the Exuma Sound andBahama Bank, can have important effects on feedutilization, growth, and survival of juveniles andis, therefore, an important regulator of year-classstrength.

MethodsThe study was conducted at the Caribbean Ma-

rine Research Center (CMRC) on Lee StockingIsland, Exuma Cays, Bahamas, from May throughJuly 1994. Juvenile Nassau groupers (120 d post-hatching) were produced at CMRC's finfish hatch-

ery on Lee Stocking Island. Fish originated froma hormone-induced spawning of captive brood-stock (Watanabe et al. 1995b; Head et al. 1996)and were reared at an ambient temperature rangeof 21-29°C.

Growth experiments were conducted in the lab-oratory in a controlled environment. Experimentalunits consisted of 145-L aquaria (1.2 X 0.3 X 0.5m) insulated on the back, top, and both sides with19-mm-thick white polystyrene. Each tank wassupplied with aeration through a silica glass dif-fuser and with flow-through seawater (salinity, 36-38 g/L) at a rate of 0.1 L/min (one exchange per

day). Ambient room temperature was maintainedat 21°C by an air-conditioner, and water temper-ature in each tank was controlled with immersionheaters (300 W). Light was supplied from over-head fluorescent sources controlled by a timer toprovide a photoperiod of 12 h light: 12 h dark.

To determine the effects of temperature ongrowth of juveniles, 24 aquaria were each stockedwith 14 fish, and growth was compared for 63 dat treatment temperatures of 22, 25, 28, and 31°C.Six replicate aquaria were maintained per treat-ment. Fish were stocked at a water temperature of27°C and acclimated to the treatment conditionsover a period of 3 d.

To begin the experiment (day 1), fish were an-aesthetized with tricaine methanesulfonate (MS-222) (75 mg/L), weighed, and measured for totallength (TL). Initial body weights (mean = 3.20g), coefficients of variation (CV = 100-SD/mean)of body weight (mean = 30.1%), and lengths(mean = 47.3 mm) were not significantly different(P > 0.05) among treatment groups (Table 1).

To monitor growth, individual fish in each tankwere weighed and measured at the beginning andat the end of the experiment, and fish in each rep-licate tank were mass-weighed weekly. Fish werehand fed to satiation twice daily (0815 and 1515hours) with a 2.2-mm formulated diet (Nippai,Dainichi Corp., Uwajima, Japan), containing 46%crude protein and 10% crude lipid, that had beenfound to produce optimum growth and feed con-version in juvenile Nassau grouper (Ellis et al.1996). The daily ration was based on a specifiedpercentage of the tank biomass determined at theprevious sampling. At each feeding, a level of feed

GROWTH OF JUVENILE NASSAU GROUPER 311

13

12

11

10

OJ 9

14 21 28 35 42 49 56 63

Time (d)

FIGURE 1.—Growth of postscttlcment stage Nassau grouper reared for 63 d at four temperatures (22°C, squares:25°C, circles: 28°C. triangles: 31°C, diamonds). Plotted symbols represent means of six replicate tanks.

was provided so that a slight excess remained after10 min. Feeding rate was adjusted by 0-0.5% oftank biomass according to this observation. Waterquality characteristics (temperature, salinity, pH,and dissolved oxygen) were monitored daily in onetank from each treatment. Feces were siphonedfollowing the afternoon feeding and deaths wererecorded daily.

Analytical procedures.—Specific growth rate(SGR; percent increase in body weight per day)was calculated as 100 X ((log^, final wet weight —\oge initial wet weight)/days). Relative growth rate(RGR; percent increase in body weight) was cal-culated as 100-(final wet weight — initial wetweight)/initial wet weight. Feed consumption (FC;percent of body weight consumed per day) during

a sampling interval was expressed as a percentageof average daily consumption to average biomassduring the interval, with consumption for the du-ration of the experimental period being the averageover all sampling intervals. Feed conversion ratio(FCR) was calculated as dry weight (g) of feedfed/wet weight gained. Condition factor (CF) wascalculated as 103 X (final weight, g)/(TL, cm)3.Average daily temperature units (TU) per gram of

fish growth (°C X d/g) were calculated as (meanexposure temperature, °C X exposure time, d) -f-(final weight, g — initial weight, g).

Treatment means were compared by one-wayanalysis of variance (ANOVA; Sokal and Rohlf1981). Following a significant (P < 0.05) ANO-VA, differences between means were further an-alyzed for significance with the Ryan-Einot-Ga-briel-Welsch multiple-range test (Day and Quinn1989). Linear regression analysis (Sokal and Rohlf1981) was used to determine the relationships be-tween SGR, FC, and temperature.

ResultsAverage daily water temperatures (±SD) during

the experimental period were 22.0 ± 0.16, 25.0 ±0.06, 28.0 ± 0.04, and 31.0 ± 0.04°C at the nom-inal treatment levels of 22, 25, 28, and 31°C, re-spectively. Average salinity (36.3 ± 0.54 g/L) andpH (8.16; range = 8.13-8.16) did not differ sig-nificantly among treatments. Average dissolvedoxygen concentrations decreased significantly (P< 0.05) with increasing temperature from 6.45mg/L at 22°C to 5.15 mg/L at 31°C.

There was a clear trend (Table 1; Figures 1, 2)

312 ELL1S ET AL.

2.6

2.2

1.8

1.4

2.6

2.2

1.8

1.4

19 22 25 28Temperature (°C)

31 34

FIGURK 2.—Linear regressions of mean (±SE) specific growth rate (SGR; solid line) and mean (±SE) feedconsumption (FC; dashed line) with temperature (7) for postsettlement stage Nassau grouper reared for 63 d atfour temperatures. Regression equations are FC = 0.063 T + 0.298 (r2 = 0.961, P < 0.0001, N = 24): SGR =0.089 T - 0.652 (r = 0.957, P < 0.0001, N = 24). Plotted symbols represent mean values of six replicate tanks.

toward greater growth with increasing tempera-ture, from a minimum at 22°C to a maximum at31°C. Final average body weights (Wj), SGRs, andRGRs were significantly (P < 0.05) higher at 28and 31°C (Wf = 10.5-12.4 g; SGR = 1.95-2.07%/d; RGR = 246-273%) than at 22 and 25°C(Wf= 7.33-8.70; SGR = 1.32-1.52%/d; RGR =131-164%; Table 1). There was a significant linearrelationship (P < 0.0001) between SGR and tem-perature (Figure 2).

Feed consumption increased (P < 0.05) withtemperature from 1.64 at 22°C to 2.21 at 31°C(Table 1), and there was a significant (P < 0.0001)linear relationship between FC and temperature(Figure 2). Although feed conversion ratio ap-peared to be better (lower) at 28 and 31 °C (mean

= 1.04) than at 22 and 25°C (mean = 1.19), thedifference was not significant (0.05 < P < 0.07;Table 1). Condition factor also appeared to behigher at 28 and 31°C (mean = 31.6) than at 22and 25°C (mean = 30.8), but the difference was

not significant (Table 1).Coefficient of variation of final body weights

averaged 58.3% and did not differ significantlyamong treatments (Table 1). Survival was high

(96.4-100%) for all temperature treatments anddid not differ significantly (Table 1). Temperatureunit requirements per gram of fish growth appeared

to decrease with increasing temperature from amaximum at 22°C to a minimum at 31°C (Table1), although these differences were not significant.

DiscussionA trend toward increasing growth of juvenile

Nassau grouper with increasing temperature, with-in ecological ranges, was clearly attributed to in-creased feed intake (i.e., appetite). This is similarto observations in other temperate fishes (sockeyesalmon Oncorhynchus nerka, Brett et al. 1969;hogchoker Trinectes maculatus, Peters and Boyd1972; hybrid striped bass Morone saxatilis X whitebass M. chrysops, Woiwode and Adelman 1991;summer flounder Paralichthys dentatus, Malloyand Targett 1994) and subtropical and tropical fish-es (desert pupfish Cyprinodon macularius, Kinne1960; channel catfish Ictalurus punctatus, Murray

et al. 1977; western mosquitofish Gambusia affinis,Shakuntala and Reddy 1979; sea bass Dicentrar-chus labrax, (=European bass Morone labrax), Hi-

GROWTH OF JUVENILE NASSAU GROUPER 313

dalgo et al. 1987; gilthead bream Sparus auratus,Tandier et al. 1989).

Fish fed to satiation generally show maximumgrowth and feed consumption at a similar tem-perature, indicating a physiological optimum(Brett 1979). In this study, highest growth and feedconsumption of juvenile Nassau grouper occurredat temperatures of 28-31°C, which also appearedto produce optimum feed conversion ratios. Thistemperature range may, therefore, be near a phys-iological optimum for this species, although highertemperatures should be examined. Increases infeed consumption, feed conversion, and growth astemperature increased to an optimum have alsobeen observed in hogchoker (Peters and Boyd1972), channel catfish (Murray et al. 1977), andsea bass (Hidalgo et al. 1987; Hidalgo and Alliot1988). In sea bass, improved feed conversion athigher temperatures was attributed to increasedprotein digestibility caused by a higher trypsin ac-tivity in the gut. In contrast, hybrid striped bassX white bass showed optimum feed conversion at21.2°C and maximum growth and consumption at26.8°C (Woiwode and Adelman 1991). Decreasedfeed conversion at higher temperatures was attrib-uted to higher energy maintenance requirementsusurping dietary energy that might have been usedfor growth.

Marked temperature-related differences ingrowth rates of juvenile Nassau grouper have im-portant ecological implications. In the southernand central Bahamas, Nassau grouper spawn pri-marily during the full-moon periods of Decemberand January (Colin 1992; Shenker et al. 1993), andpostlarvae settle into shallow benthic habitats fromJanuary to March, 35-50 d (mean = 42.6 d) afterspawning (D. Eggleston, North Carolina State Uni-versity, personal communication).

Because Nassau grouper spawn on a lunar cycle,newly settled postlarvae are subjected to signifi-cant interannual variations in water temperature.Water temperature data collected from 1989-1994in a shallow seagrass habitat in the southern Ba-hamas (Wicklund et al. 1993; Dennis et al. 1994)where juvenile Nassau grouper have been ob-served (S. C. Ellis, personal observation) showseasonal changes that range from an average min-imum of 24.3°C in February to an average maxi-mum of 29.8°C in August. Newly settled juveniles,originating from a spawn early in December wouldbe subjected to a mean temperature of 24.9°C forthree months (February-April) following settle-ment. In contrast, juveniles originating from aspawn al the end of January would encounter a

mean water temperature of 27.2°C for three months(April-June) following settlement. Hence, tem-poral variability in timing of spawning in relationto seasonal changes in sea temperatures may resultin average exposure temperatures during thepostsettlement period that differ by as much as2.3°C. This difference in temperature may resultin significant interannual differences in growth.Assuming that growth in nature is not limited byfood, data from the present study shows that therewould be an 8.7% difference in food consumptionrate and a 12.9% difference in SGR for fishspawned early in December compared with fishspawned late in January (Figure 2). Because mor-tality due to predation, which is an important cause

of mortality among juvenile marine finfish, is oftensize-specific (Folkvord and Hunter 1986), watertemperatures may alter vulnerability to predationand, therefore, year-class strength (Malloy andTargett 1994).

Timing of spawning in relation to seasonalchanges in sea temperatures may also produce con-siderable, albeit smaller, intraannual differences infeeding, growth rates, and survival. Assuming adifference in spawning timing of 1 month, newlysettled juveniles originating from spawnings earlyin December and January would encounter averagewater temperatures that differ by 1.00°C (Febru-ary-April versus March-May), while those orig-inating from spawnings late in December and Jan-uary would encounter water temperatures that dif-fer by 1.30°C (March-May versus April-June).Hence, seasonal changes in water temperaturewould produce smaller differences in growth ratesof juveniles spawned in the same year becausetemperature differences between postsettlementperiods are relatively small.

In this study, maximum growth as well asgrowth efficiency (i.e., minimum TU requirements

per gram of growth) were observed at the highesttemperature tested (31°C). Growth of fishes in-creases rapidly before going into gradual declinewhen their upper lethal limit is approached (Kinne1960; Woiwode and Adelman 1991). The trendsof increasing feed intake, specific growth rate, andthe apparent trend of decreasing TU requirementsper gram of fish growth with increasing temper-ature in this study showed only a slight attenuationat 31°C, suggesting that growth may be increasedat even higher temperatures.

This study demonstrates that sea temperature,within an ecological range, has pronounced anddirect effects on feeding and growth in juvenileNassau grouper and suggests that timing and rel-

314 ELLIS ET AL.

ative intensity of spawning during full-moon pe-riods in December and January may produce sig-nificant interannual differences in juvenile growthrates. These results support the hypothesis thattiming of spawning may be an important regulatorof year-class strength. Growth rates recorded inthis study can be used to estimate origin andgrowth of juveniles observed in the field. The re-sults further suggest that rearing temperatures of28-31°C are optimal for aquaculture, althougheven higher temperatures may be feasible.

AcknowledgmentsWe thank Robert Wicklund for helpful advice.

This study was supported by a grant from the Na-tional Undersea Research Program of the NationalOceanic and Atmospheric Administration and bythe Perry Foundation, Inc.

ReferencesBohnsack, J. A., and F. H. Talbot. 1980. Species-pack-

ing by reef fishes on Australian and Caribbean reefs:an experimental approach. Bulletin of Marine Sci-ence 30:710-723.

Brett, J. R. 1979. Environmental factors and growth.Pages 599-675 in W. S. Hoar, D. J. Randall, and J.R. Brett, editors. Fish physiology, volume 8. Aca-demic Press, New York.

Brett, J. R., J. E. Shelbourn, and C. T. Shoop. 1969.Growth rate and body composition of fingerlingsockeye salmon, Oncorhynchus nerka, in relation totemperature and ration size. Journal of the FisheriesResearch Board of Canada 26:2363-2394.

Buckley, L. J., A. S. Smigielski, T. A. Halavik, and G.C. Laurence. 1990. Effects of water temperature

on size and biochemical composition of winterflounder Pseudopleuronectes americanus at hatchingand feeding initiation. U.S. National Marine Fish-eries Service Fishery Bulletin 88:419-428.

Colin, P. L. 1992. Reproduction of the Nassau grouper,Epinephelus striatus (Pisces: Serranidae) and its re-lationship to environmental conditions. Environ-mental Biology of Fishes 34:357-377.

Colin, P. L., D. Y. Shapiro, and D. Weiler. 1987. Aspectsof the reproduction of two groupers, Epinephelusguttatus and E. striatus in the West Indies. Bulletinof Marine Science 40:220-230.

Day, R. W., and G. P. Quinn. 1989. Comparisons oftreatments after an analysis of variance in ecology.Ecological Monographs 59:433-463.

Dennis, G. D., H. M. Proft, and R. I. Wicklund. 1994.Summary of data from the temperature monitoringnetwork: Lee Stocking Island, Bahamas, 1992-1993. Caribbean Marine Research Center, TechnicalReport 94-5. Lee Stocking Island, Bahamas.

Ellis, S. C., G. Viala, and W. O. Watanabe. 1996.Growth and feed utilization of hatchery-reared, ju-venile Nassau grouper fed four practical diets. Pro-gressive Fish-Culturist 58:167-172.

Folkvord, A., and J. R. Hunter. 1986. Size-specific vul-nerability of northern anchovy, Engraulis mordax,larvae to predation by fishes. U.S. National MarineFisheries Service Fishery Bulletin 84:850-869.

Head, W. D., W. O. Watanabe, S. C. Ellis, and E. P. Ellis.1996. Hormone-induced multiple spawning of cap-tive Nassau grouper (Epinephelus striatus) brood-stock. Progressive Fish Culturist 58(l):65-69.

Hidalgo, F, and E. Alliot. 1988. Influence of watertemperature on protein requirement and protein uti-lization in juvenile sea bass, Dicentrarchus labrax.Aquacullure 72:115-129.

Hidalgo, F, E. Alliot, and H. Thebault. 1987. Influenceof water temperature on food intake, food efficiencyand gross composition of juvenile sea bass, Dicen-trarchus labrax. Aquaculture 64:199-207.

Houde, E. D. 1987. Fish early life dynamics and re-cruitment variability. Pages 17-29 in R. D. Hoyt,editor. 10th annual American larval fish conference.American Fisheries Society, Symposium 2, Bethes-

da. Maryland.Houde, E. D. 1989. Subtleties and episodes in the early

life of fishes. Journal of Fish Biology 35(Supple-ment A):29-38.

Kaeding, L. R., and D. B. Osmundson. 1988. Interactionof slow growth and increased early-life mortality:an hypothesis on the decline of Colorado squawfishin the upstream regions of its historic range. En-vironmental Biology of Fishes 22:287-298.

Kinne, O. 1960. Growth, food intake, and food con-version in a euryplastic fish exposed to differenttemperatures and salinities. Physiological Zoology33:288-317.

Leggett, W. C., and E. Deblois. 1994. Recruitment inmarine fishes: is it regulated by starvation and pre-dation in the egg and larval stages? NetherlandsJournal of Sea Research 32:119-134.

Leggett, W. C., K. T. Frank, and J. E. Carscadden. 1984.Meteorological and hydrographic regulation ofyear-class strength in capelin (Mallotus villosus).Canadian Journal of Fisheries and Aquatic Sciences41:1193-1201.

Malloy, K. D., and T. E. Targett. 1994. Effects of rationlimitation and low temperature on growth, bio-chemical condition, and survival of juvenile sum-

mer flounder from two Atlantic Coast nurseries.Transactions of the American Fisheries Society 123:182-193.

May, R. C. 1974. Larval mortality in marine fishes andthe critical period concept. Pages 3-19 in J. H. S.Blaxter, editor. The early life history offish. Spring-er-Verlag, New York.

Murray, M. W, J. W. Andrews and H. L. DeLoach. 1977.Effects of dietary lipids, dietary protein and envi-ronmental temperatures on growth, feed conversionand body composition of channel catfish. Journal ofNutrition 107:272-280.

Pepin, P. 1991. Effect of temperature and size on de-velopment, mortality, and survival rates of the pe-lagic early life history stages of marine fish. Ca-nadian Journal of Fisheries and Aquatic Sciences48:503-518.

GROWTH OF JUVENILE NASSAU GROUPER 315

Peters, D. S., and M. T. Boyd. 1972. The effect oftemperature, salinity and availability of food on thefeeding and growth of the hogchoker, Trinectes ma-culatus (Bloch and Schneider). Journal of Experi-mental Marine Biology and Ecology 7:201-207.

Sadovy, Y. 1993. The Nassau grouper, endangered orjust unlucky? Reef Encounter 13(JuIy):10-12.

Shakuntala, K., and R. Reddy. 1979. Influence of tem-perature-salinity combinations on the food intake,growth and conversion efficiency of Gambusia af-Jinis. Polskie Archiwum Hydrobiologii 26:173-181.

Shenker, J. M., and five coauthors. 1993. Onshore trans-port of settlement-stage Nassau grouper Epinephe-lits striatus and other fishes in Exuma Sound, Ba-hamas. Marine Ecology Progress Series 98:31-43.

Sissenwine, M. P. 1974. Variability in recruitment andequilibrium catch of the southern New England yel-lowtail flounder fishery. Journal du Conseil ConseilInternational Pour TExploration de la Mer 36:15-26.

Smith. P. E. 1985. Year-class strength and survival ofO-group clupeiods. Canadian Journal of Fisheriesand Aquatic Sciences 42(Supplement l):69-82.

Sokal, R. R.. and F. J. Rohlf. 1981. Biometry, 2nd edi-tion. Freeman, San Francisco.

Tandler, A., and seven coauthors. 1989. Effect of en-vironmental temperature on survival, growth andpopulation structure in the mass rearing of Giltheadbream, Sparus aurata. Aquaculture 78:277-284.

Tucker, J. W., Jr., P. G. Bush, and S. T. Slaybaugh. 1993.Reproductive patterns of Cayman Islands Nassaugrouper (Epinephelus striatus) populations. Bulletinof Marine Science 52:961-969.

Tucker. J. W., Jr., J. E. Parsons, G. C. Ebanks. and P. G.Bush. 1991. Induced spawning of Nassau grouperEpinephelus striatus. Journal of the World Aqua-culture Society 22:187-191.

Walsh, W. J. 1987. Patterns of recruitment and spawningin Hawaiian reef fishes. Environmental Biology ofFishes 18:257-276.

Watanabe, W. O., and five coauthors. 1996. Evaluationof first-feeding regimens for larval Nassau grouper(Epinephelus striatus) and preliminary pilot-scaleculture through metamorphosis. Journal of theWorld Aquaculture Society 27:323-331.

Watanabe, W. O., C.-S. Lee, S. C. Ellis, E. P. Ellis.I995a. Hatchery study on the effects of temperatureon eggs and yolksac larvae of the Nassau grouper(Epinephelus striatus). Aquaculture 136:141-147.

Watanabe, W. O., and seven coauthors. 1995b. Progressin controlled breeding of Nassau grouper (Epine-phelus striatus) by hormone induction. Aquaculture138:205-219.

Wicklund, R. 1., G. D. Dennis, and K. W. Mueller. 1993.Summary of data from the water temperature mon-itoring network: Lee Stocking Island, Bahamas.1988-1991. Caribbean Marine Research Center,Technical Report Series 93-1, Lee Stocking Island,Bahamas.

Woiwode, J. G.. and I. R. Adelman. 1991. Effects oftemperature, photoperiod, and ration size on growthof hybrid striped bass X white bass. Transactionsof the American Fisheries Society 120:217-229.

Received May 23, 1996Accepted September 28, 1996