Effect of environmental temperature on survival, growth and population structure in the mass rearing of the gilthead seabream, Sparus aurata

Aquaculture, 78 (1989) 277-284 Elsevier Science Publishers B.V., Amsterdam -

277 Printed in The Netherlands

Effect of Environmental Temperature on Survival, Growth and Population Structure in the Mass Rearing of the Gilthead Seabream, Sparus aurata A. TANDLER’, M. HAR’ELI, M. WILKS’, A. LEVINSON’, L. BRICKELLr, S. CHRISTIEI, E. AVITAL’ and Y. BARR1 INational Center for Mariculture, Israel Oceanographic and Limnological Research, P.O. Box 1212, Eilat, 88112 (Israel) 2ARDOM D.N., Eilat (Israel) (Accepted 29 November 1988)

ABSTRACT Tandler, A., Har’el, M., Wilks, N., Levinson, A., Brickell, L., Christie, S., Avital, E. and Barr, Y., 1989. Effect of environmental temperature on survival, growth and population structure in the mass rearing of the gilthead seabream, Sparus aurata. Aquaculture, 78: 277-284. This study reports the effect of temperature regime in terms of degree-days, during a period of 32 days from hatching, on growth, survival and population size structure of gilthead seabream (Sparus aurata) . We hypothesized that larger postlarvae with a higher survival potential at the nursery stage may result from an increase in the duration of exposure of larvae to higher temperatures within the tolerable range. Three culture regimes, differing in degree-day exposure, were chosen consisting of the following temperatures in four consecutive periods, 19,20.5,22.5 and 24.5” C. These were applied from the day of hatching for the following periods: (1) 13,5,5,9 days; 682.5 degree-days; (2) 8,5,5, 14 days; 710 degree-days and (3) 3,5,5,19 days; 737.5 degree-days. Survival of 32-day-old larvae decreased from 8.7 to 2.8% as number of degree-days increased from 682.5 to 737.5. Wet weights at 32 days increased from 14.0 to 16.3 mg under the same conditions. Size variation of 32-day-old larvae was positively correlated with degree-days. The presence of larger (39.1& 1.36 mg; mean & 95% CI), more aggressive larvae increased sharply from 2.8 to 18.1% as number of degree-days increased. The inverse relationship between the presence of larger larvae in the population and survival suggests that early size grading of bream larvae contributes to higher survival. The direct relationship between degree-days, growth, and size variation of 32-day-old gilthead seabream larvae and the inverse relationship with survival are discussed.

INTRODUCTION

As for many cultured species, the successful culture of gilthead seabream auratu) depends on the improvement of both larval survival and

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growth. High losses at early larval stages for the first 3 weeks (6-7 mm SL) may be attributed mainly to nutritional and environmental factors (Tandler and Sherman, 1981; Tandler and Mason, 1983; Tandler and Helps, 1985). In later larvae, reaching a standard length of 7-8 mm and an age of 25-28 days, losses could be attributed to behavioral parameters such as aggression and cannibalism. The latter phenomena are the result of changes in the size structure of the population: the larger larvae nipping the smaller ones. This phenomenon was previously observed in 32-day-old gilthead seabream (A. Tandler, unpublished data, 1986) and in red seabream (Pugrus major; Yamagishi, 1969). Amelioration of conditions for growth is paramount for reducing the duration of larval rearing. Elevation of environmental temperature within a tolerable range is one way of accelerating growth rate. Commonly, larval rearing of gilthead seabream is performed within a temperature range of 18-19 oC (Person-Le Ruyet and Verillaud, 1980; Ortega et al., 1983)) conditions approaching those prevailing in the Mediterranean in the spawning season. To accelerate growth a regime was adopted where temperatures were increased gradually from 19 to 24.5’ C (Tandler and Helps, 1985). It has been reported that conditions providing faster growth may more rapidly alter the size structure of fish larval populations (Yamagishi, 1969; A. TandIer, unpublished data, 1986)) with a possible earlier appearance of larger, more aggressive postlarvae. This behavior may affect both final survival as well as population structure. Therefore, the aim of the present study was to examine the effect of temperature regime on growth, survival and size structure of a population of gilthead seabream 32 days after hatching. MATERIALSANDMETHODS The experiment was performed in 27 conical fiberglass tanks (600 1volume) supplied with running filtered (10 FM, sandfilter) sea water. The incoming water, with a salinity of 40-41 ppt, 0.1-0.2 @U NH,-NH: and a pH of about 8.2, was pumped directly from the Gulf of Eilat (Aqaba). Before being used, the water was directed to four independent heat-exchange systems designed to supply fresh sea water continuously at the following temperatures: 19.0 + 0.5 oC, 20.5t0.5”C,22.5+0.5”C,and24.5~0.5”C. The objective of the experiment was to measure the effect of three rearing temperature regimes of varying period and degree-days (682.5,710, and 737.5 ) on growth, survival, and population structure of gilthead seabream larvae. In the first regime, larvae were reared for 13 days from hatching at 19.0 ? 0.5 ‘C, then 5 days at 20.5 -t 0.5’ C, 5 days at 22.5 t 0.5’ C, and finally for a further 9 days the larvae were maintained at 24.5 +-0.5’ C. In the next two regimes only the initial low and the final high temperatures were altered by 5 and 10 days

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(8,5,5,14 days and 3,5,5,19 days, respectively). The transfer between temperatures occurred overnight, so that the change was never higher than 1°C h-l. The 27 experimental tanks were stocked randomly in 5 days so that every day five to six tanks were stocked from a given batch of eggs. Each tank was stocked with 60 000 eggs (100 1-l ) added by volume from a calibrated container. After 48 h, the number of hatched larvae in each tank was estimated by counting at least five 250-ml samples taken from different areas of the tank at a depth of ca. 80 cm. The means of these counts were subsequently used as a basis to calculate the final survivals. The following protocol was used for larval rearing. Larvae were reared in a flow-through system with a flow rate of 11 min-l (2.4 water exchanges day-l) from incubation to the end of the 19.O”C rearing period, 1.5 1 min-l (3.6 exchanges day-l) at the two intermediate temperatures and 2 1 min-l (4.8 exchanges day-l) at 24.5”C. At the initiation of larval pigmentation, 3 days after hatching, larvae were offered rotifers (BrachionuspZicatiZis) at a concentration of 10 + 2 ml-l, and algae (Isochrysis gdbana; Tahitian strain) at a concentration of 50-70 x lo3 cells ml-l. The concentrations of both rotifers and algae were maintained by continuous addition of both via a special dispensing system. However, these concentrations had to be adjusted every morning since the addition of rotifers and algae was limited to 18-20 h day-l. Fifteen days after hatching, the larvae were offered newly hatched Artemia nauplii for 3 days; subsequently they were offered nauplii enriched for 24 h with an emulsion of capelin oil. The number of Artemia offered daily increased gradually with demand, often reaching 4-5 x lo3 1-l in the 5th week of rearing. Temperature was measured daily and was always within + 0.25 oC of the preassigned temperature. Oxygen concentration was also measured daily ( ? 0.1 mg 1-l; YSI 58), after the morning adjustment of rotifer numbers, Artemiu, and algae concentration. During the course of the experiment, depending on the temperature regime, and also on the accumulation of organic matter, oxygen levels dropped gradually, but never below 75% saturation. pH was not measured in the present experiment but previous experiments with these levels of water exchange showed pH to be stable at about 7.8 units. NH,-NH,+ was measured every other day (Krom et al., 1985); it gradually increased, but was never higher than 20 ,u&l. Measurements of growth of larvae (standard length, SL; + 0.01 mm) in each tank were made every other day by examining 10 larvae randomly collected from the tank surface. Gut contents of these larvae were examined and numbers of rotifers and Artemia nauplii ingested were recorded. At the end of the rearing period 20 fish were randomly taken for measurements of SL and wet weight ( -+0.01 mg) . Final survivals were based on individual counts of all fish at the end of the 32-day rearing period. Finally, the 32-day-old larvae in individual experimental tanks were size-graded through special graders which re-

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tained only the largest seabream larvae of 39 + 1.36 mg (95% CI) wet weight. These were counted and their relative presence in the population was calculated. Data were analysed using parametric tests (ANOVA, Regression, ANCOVA) following data transformation and a test for homogeneity of variances (Hartley’s F-max test; Fryer, 1966). Differences among means were tested using the Student-Neuman-Keuls (SNK) test (Sokal and Rohlf, 1969). In the ANOVA test temperature regimes and stocking days were used as sources of variation. Other sources of variation in the analysis were wet weights and their standard deviations of 32-day-old larvae. To homogenize variances, prior to analysis, percentage survival ( + 0.5)) wet weights of 32-day-old larvae and the relative abundance of large larvae in the population were log transformed. Growth analyses of length were made on the slopes of the regressions of the daily changes in the logarithms of SL. Daily measurements of gut contents, in terms of number of rotifers and Artemia were converted to biomass in terms of dry weight (Bruchionus plicatilis - 0.190 ,ug; Tandler and Mason, 1983; Artemiu nauplius - 1.63 ,ug; Vanhaecke and Sorgeloos, 1980). The effect of temperature regime on size structure of the population was measured as an effect on the standard deviation of the wet weights of 32-day-old larvae. In addition, the abundance of 39 i 1.36 mg larvae in 32-day populations of larvae was correlated with the temperature regimes. RESULTS

Larval survival declined as degree-days of the rearing regime increased. As degree-days increased from 682.5 to 737.5 there was a significant (P 0.05) the final 32-day wet weight. A direct relationship was found between growth rate (length) and degreedays of the rearing regime. Analysis of the slopes of the regressions between the logarithm of SL and age showed that as degree-days in the rearing regime increased from 682.5 to 737.5, the slopes of the regressions increased (PC 0.001) from3.73~1.46X10-3t04.15~1.59X10-3mmday-1 (Tablel).Asignificant effect of the increase in degree-days from 682.5 to 710 on growth rate in SL could not be demonstrated (P > 0.05 ) . Daily counts of gut-filling in terms of rotifers and Artemia were summed in terms of their dry biomass. A log-log relationship was established (PcO.05) between the calculated gut-filling (pup) and age in days. Analysis of the slopes

281 TABLE 1 The effect of different temperature regimes and degree-days on 32&y survival ( % ) , weight (mg, wet), standard deviation of wet weight, the proportion of 39 k 1.36 mg in the population of 32day-old larvae, the slopes of the regressions of standard length (SL, mm) and the level of gutfilling (GF, pg ) with age (days), in the larvae of Sparus auratu Rearing temp. (“C)

Temperature regime Duration (days) Regime 1

19.0 20.5 22.5 24.5 Degree-days Survival ( % ) ‘8’ Weight (mg, wet) SD weight 39-mglarvae (%)3 SL=aebA”, bE4 GF = aAgeb, b = 4

13 5 5 9 682.5 8.68 + 13.96 f 8.72 + 2.79 + 3.73f 2.99 f

Regime 2

8 5 5 14 710 3.22” 2.72” 1.92b 1.45” 1.46x1O-3” 0.175”

5.87 zk3.99s 16.97 + 2.57b 7.50 f 0.84”b 8.60 ~b4.33~ 3.81+ 1.76x 10-3” 2.78+0.310”

Regime 3 3 5 5 19 737.5 2.77 + 2.32” 16.26 ?I 2.20b 6.21f2.10” 18.10+3.55” 4.15f1.59x10-3s 3.49 f 0.414b

‘Means-t 95% confidence interval. ‘All means bearing the same superscript are not significantly different from each other (P> 0.05). 339 k 1.36 mg larvae as a proportion of the total surviving population of 32-day-old larvae. ‘b in the equation.

of these regressions showed that as degree-days increased from 682.5 to 737.5, the slope of the regression increased (P < 0.003 ) from 2.99 k 0.175 to 3.49 + 0.414 ,ugfood larva-l day-l (Table 1). An intermediate increase in degree-days from 682.5 to 710 did not have a significant effect (P> 0.05) on gut-filling rate. Finally, an inverse relationship was found between degree-days and variation in wet weight of 32-day-old larvae. There was a decrease (PC 0.025; Table 1) in the magnitude of the standard deviation (SD) from 6.2122.10 to 8.72 + 1.92, as degree-days decreased from 737.5 to 682.5. The size distribution of the final population of survivors of 32-day-old larvae was further investigated by studying the abundance of the largest larvae (39 +- 1.36 mg) in the population (Table 1) . A direct relationship was found between degree-days of the rearing regime and the presence of large larvae. As degree-days increased from 682.5 to 710 the relative presence of big larvae tripled (P
282 DISCUSSION

This study of gilthead seabream larvae has shown an inverse relationship between increase in degree-days in rearing period and survival. It follows that for improved survival an even lower temperature regime should be tested with a possible growth retardation. This is supported by rearing procedures for gilthead seabream described by Barnabe (1976)) who recommended the use of 1618°C for the first 10 days after hatching and 18-21°C from then on. PersonLe Ruyet and Verillaud (1980)) in laboratory-scale experiments with gilthead seabream, used a 19 + 1’ C regime for the entire rearing period up to 25 days. The mean survival in these experiments was 11%) with a maximum of 67%. In another report, but dealing with the mass production of gilthead seabream, Ortega et al. (1983 ) twice used a temperature range of 17-19’ C for the first 30 days. Survival in these trials was 27-30%, but growth was retarded and larvae reached a total length of only 6-7 mm. It is interesting to note that in these latter experiments salinities of 42.5 ppt were used, as compared to the slightly lower salinities used in the present study. Wet weights of 32-day-old larvae and growth rates in the present study were positively correlated with degree-days between 682.5 and 737.5. The effect of temperature on the growth of gilthead seabream is well exemplified in Person Le-Ruyet and Verillaud’s study (1980) in which 41-44-day-old larvae had a mean weight of 16.49 mg, with a maximum of 19.9 mg wet. In the present study the mean weight of 32-day-old fish with the high temperature regime was 16.3 mg. The positive relationship between temperature and growth rate within the tolerated temperature range in fish was elaborated by Brett (1976) for sockeye salmon (Oncorhynchus nerka) . A direct relationship between growth rate and temperature between 11 and 21’ C was reported for the Pacific sardine (Sardinops caerulea; Lasker, 1964)) and by Fonds (1979) for Solea solea within a temperature range of lo-16°C. However, unlike the present study where an effect of degree-days on growth was demonstrated, those reports were based on observations of fish acclimated to unchanging experimental temperatures. The feeding rate of gilthead seabream larvae was directly correlated to degree-days. Analysis of the slopes of larval gut-filling with rotifers and Artemia with age showed a 25% increase in the magnitude of the exponent in the longer exposures to the high temperature regime (Table 1). Brett (1976), in a summary on sockeye salmon energetics, has shown, within a limited range of tolerable temperatures, that there is a direct relationship between feeding rate and temperature. In accordance with Fry’s (1971) definition of temperature as a controlling factor, this study suggests that the rate of feeding in gilthead seabream larvae is positively correlated with the duration of exposure to a high temperature rearing regime. Finally, an inverse relationship was found between degree-days and the magnitude of the variation in 32-day wet weights. Commonly, however, a direct

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relationship exists between size and variation (Weatherley and Gill, 1987)) suggesting that the 32-day population structure reflects a size-selective mortality. A size-selective mortality was also suggested by Peguin’s (1984) data for 12-day-old gilthead seabream larvae. In his study he found that conditions which supported the highest larval survival of 14.0% were associated with a mean dry weight of 23.8 pg, while conditions associated with best growth of 52.2 pugwere associated with 1.7%, E-day survival. Selective mortality was further suggested by our results which showed an inverse relationship (PC 0.002) between the 32-day proportion of the 39 t 1.36 mg fraction of larvae and survival. Therefore, we believe that within a given population of gilthead seabream, larval mortality is size dependent. At the onset of larval life the larger larvae are probably more resistant, and towards the fourth week after hatching, when larvae reach a SL of over 8 mm, aggression and cannibalism take place. We suspect (unpublished data, 1986) that the 39 & 1.36 mg group in the population is probably a portion of the population of larvae which expresses a strong aggressive behavior, a factor which may well explain the size-selective mortality that appears to exist in the later part of larval rearing. This suggests that size-grading of larvae of gilthead seabream may be paramount for improved survival. Moreover, it suggests that temperature regime has an indirect effect on survival via the change in size structure of the population; therefore, benefits associated with amelioration of conditions for growth might be obtained only if gilthead seabream larvae are size-graded. In conclusion, this study with gilthead seabream has shown that there is an inverse relationship between degree-days and survival, a direct relationship with growth rate, feeding rate, and abundance of larger, more aggressive 32day-old larvae. ACKNOWLEDGEMENTS

We wish to express our thanks to H. Gordin for his critical reading of the manuscript, and to the rest of the staff of NCM for their assistance in different aspects of this study.

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