Effects of salinity and temperature on survival, growth, and energy budget of juvenile Litopenaeus vannamei.

ABSTRACT A 4 x 4 factorial experiment was conducted to determine the effects of salinity (0.2 [per thousand], 11 [per thousand], 21 [per thousand], and 31 [per thousand]) and temperature (20[degrees]C, 24[degrees]C, 28[degrees]C, and 32[degrees]C) on survival, growth, and energy budget of juvenile Litopenaeus vannamei with the initial wet body weight of 0.274-0.283 g. The experiment lasted for 5 wk. The results showed that all shrimp survived at 11 [per thousand], 21 [per thousand], and 31 [per thousand], irrespective of temperature; at 0.2 [per thousand], survival decreased with increasing temperature from 20[degrees]C to 28[degrees]C, then plateaued at 32[degrees]C. At all levels of temperature with increases of salinity within the range tested, specific growth rate or food consumption gradually increased, reaching the maximum value and thereafter declined. At 0.2 [per thousand], specific growth rate, food consumption, or apparent digestibility coefficient exhibited an increasing trend from 22[degrees]C, reaching the maximum value at 28[degrees]C, then showed a decline up to 32[degrees]C with increasing temperature, whereas at salinities of 11 [per thousand], 21 [per thousand], and 31 [per thousand]; specific growth rate, food consumption, or apparent digestibility coefficient exhibited an increasing trend. By contrast, feed efficiency generally decreased in response to increasing temperature within the salinity range tested.

KEY WORDS: Litopenaeus vannamei, salinity, temperature, survival, growth, energy budget

INTRODUCTION

Shrimp farming has been developed worldwide in recent years, and also become an important industry of mariculture in China. However, the traditional aquaculture method is far from ideal that shrimp are cultured in coastal waters, which are potentially affected by adverse physical, chemical, and biological conditions (Zhang & Dong 2002). A land-based recirculating culture system, which permits efficient management by close control of the general condition, diet, and diseases circumvents all these problems (Woo & Kelly 1995).

The white shrimp Litopenaeus vannamei is the most important penaeid species for recirculating system aquaculture in China. By now, many studies have reported on the effects of different environmental factors, in particular, salinity and temperature on survival, growth, metabolism, and osmoregulation of this species (Wyban et al. 1995, Jiang et al. 2000). Equally important, but less researches are the combined effects of salinity and temperature (Ponce-Palafox et al. 1997, Diaz et al. 2001). To create an adequate condition for optimal production for the species, this study was designed to determine the effects of salinity (0.2 [per thousand], 11 [per thousand], 21 [per thousand], and 31 [per thousand]) and temperature (20[degrees]C, 24[degrees]C, 28[degrees]C, and 32[degrees]C) on survival and growth of juvenile L. vannamei, together with an analysis of the bioenergetic mechanisms involved.

MATERIALS AND METHODS

Source and Acclimation of Experimental Shrimp

The experiment was carried out at Jiangsu Key Laboratory of Marine Biotechnology, Huaihai Institute of Technology, Lianyungang, People's Republic of China. L. vannamei juveniles were obtained from Hainan Shrimp Breeding Farm, Hainan, P. R. China. The shrimp were initially held in 16 fiberglass tanks (200 x 80 x 60 cm) at 31 [per thousand] for 3 d, and were acclimated to four salinity levels (31 [per thousand], 21 [per thousand], 11 [per thousand], and 0.2 [per thousand]) by lowering the salinity at a rate of 3 [per thousand] [d.sup.-1] with adding tap water (about 0.2 [per thousand] salinity) and four temperature levels (20[degrees]C, 24[degrees]C, 28[degrees]C, and 32[degrees]C) by decreasing or increasing the temperature at a rate of 3[degrees]C x [d.sup.-1].

Experimental Design

A two-factor factorial experimental design (4 x 4) with three replications per treatment was followed. A static-water system consisting of 48 aquaria (45 x 30 x 30 cm, water volume 35L) with aeration was used. After 24 h feed deprivation, 30 shrimp with wet weight range from 0.260-0.300 g were selected from the acclimating fiberglass tanks. From the 30 shrimp, three groups of 5 individuals each were randomly sampled for analysis of initial energy content and nitrogen content of the shrimp at the corresponding salinity and temperature level. The remaining 15 shrimp were randomly stocked into 3 aquaria with each aquarium holding five individuals. The experiment lasted for 5 wk.

Shrimp were hand-fed at excess ration twice daily (at 06:00 and 18:00h) for each group with formulated pellets (29.13 [+ or -] 40.22% crude protein, 9.55 [+ or -] 0.35% crude lipid, 11.23 [+ or -] 0.22% ash, 5.46 [+ or -] 0.20% moisture, and 16.65 [+ or -] 0.01 kJ x [g.sup.-1] gross energy) manufactured by Fuzhou Haima Feed Co., Ltd., Fuzhou, P. R. China. Each meal lasted approximately 2.5 h and any uneaten food was collected and dried at 70[degrees]C. Twice a day intact feces and molts were collected from each aquarium then freeze-dried immediately and held at 20[degrees]C until analyzed. For each aquarium, two thirds of water was replaced daily to ensure high-water quality. The corresponding salinity and temperature were maintained at 0.2 [+ or -] 0.1 [per thousand], 11 [+ or -] 0.1 [per thousand], 21 [+ or -] 0.1 [per thousand], 31 [+ or -] 0.1 [per thousand] and 20 [+ or -] 0.1[degrees]C, 24 [+ or -] 0.1[degrees]C, 28 [+ or -] 0.1[degrees]C, 32 [+ or -] 0.1[degrees]C, respectively. During the experiment, dissolved oxygen was maintained >6.0 mg x [L.sup.-1], pH from 7.7-8.2, ammonia <0.24 mg x [L.sup.-1] and in photoperiod of 14L: 10D with light period from 06:00-20:00.

Calculation of Data

Specific growth rate (SG[R.sub.d]), feed efficiency in dry weight (F[E.sub.fd]), feed efficiency in energy (F[E.sub.e]), and apparent digestibility coefficient (AD[C.sub.d]) were calculated as follows:

SG[R.sub.d] = 100 x (ln[W.sub.2] - ln[W.sub.1])/t

F[E.sub.fd] = 100 x ([W.sub.d2] - [W.sub.d1])/[C.sub.d]

F[E.sub.e] = 100 x ([E.sub.2] - [E.sub.1])/[C.sub.e]

AD[C.sub.d] = 100 x ([C.sub.d] - [F.sub.d])/[C.sub.d]

where [W.sub.2] and [W.sub.1] are final and initial wet weight of the shrimp (g); [W.sub.d2] and [W.sub.d1] are final and initial dry weight of the shrimp (g); [E.sub.2] and [E.sub.1], final and initial energy contents of the shrimp (kJ x [g.sup.-1]); [C.sub.d], food consumption in dry weight; [C.sub.e], intake energy; [F.sub.d], fecal production in dry weight (g); t, duration of the experiment (d).

The energy budget equation of L. vannamei juveniles can be defined through the construction of a budget in which the intake energy (C) is partitioned between growth (G), respiration (R), excretion (U), feces (F), and exuviae (E) (i.e., C = G + R + U + F + E). The gross energy contents of diet, shrimp, feces, and molt were measured with a 1281 Oxygen Bomb Calorimeter (Parr Instrument Company, Illinois, USA). The initial energy contents of the shrimp were assumed to be equal to the average energy value of the shrimp sacrificed at the beginning of the experiment.

Preliminary experiment indicated that nitrogen in L. vannamei juveniles was mainly excreted as ammonia, with only negligible amounts of urea and uric acid. The excretory nitrogen is converted into energy using the equivalent of 24,830 J x [g.sup.-1] N for nitrogen excreted (Elliott 1976). Hence, the energy lost as U can be calculated using the equation:

U = ([C.sub.N] - [G.sub.N] - [F.sub.N] - [E.sub.N]) x 24,830

where [C.sub.N], [G.sub.N], [F.sub.N], [E.sub.N] represent the nitrogen contents of diet, shrimp, feces, and molt, respectively. The nitrogen contents of diet, shrimp, feces and molt were measured with a PE-240 element analyzer (Beijing NCS Analytical Instrument Company, Beijing, P. R. China). The initial nitrogen contents of the shrimp were assumed to be equal to the average nitrogen value of the shrimp sacrificed at the beginning of the experiment.

The energy lost as R can be calculated using the equation:

R = C - G - F - E - U

Statistical Analysis

Data from each treatment were subject to a two-way ANOVA. When overall differences were significant at less than 5% level, Tukey test was used to compare the mean values between individual treatments. The square-root transformation of the sine-arc before analyzing the values given in percentages was used. Statistical analysis was performed using SPSS (Statistic package for social science) 10.0.

RESULTS

Survival

All shrimp survived at 11 [per thousand], 21 [per thousand], and 31 [per thousand] irrespective of temperature; at 0.2 [per thousand], survival decreased with increasing temperature from 20[degrees]C to 28[degrees]C, then plateaued at 32[degrees]C (Fig. 1). ANOVA showed that survival was only affected by salinity and the interaction between salinity and temperature. Survival in shrimp maintained at 0.2 [per thousand] and 28[degrees]C to 32[degrees]C was not significantly different from those maintained at 0.2 [per thousand] and 24[degrees]C, but it was significantly lower as compared with other treatments.

[FIGURE 1 OMITTED]

Growth

The results showed that at all levels of temperature with increases of salinity within the range tested, specific growth rate, and food consumption gradually increased, reaching the maximum value and thereafter declined. At 0.2 [per thousand], specific growth rate, food consumption, or apparent digestibility coefficient exhibited an increasing trend from 22[degrees]C, reaching the maximum value at 28[degrees]C, then showed a decline up to 32[degrees]C with increasing temperature, whereas at salinities of 11 [per thousand], 21 [per thousand], and 31 [per thousand], specific growth rate, and food consumption or apparent digestibility coefficient exhibited an increasing trend. By contrast, feed efficiency generally decreased in response to increasing temperature within the salinity range tested (Fig. 1).

ANOVA showed that specific growth rate, food consumption, and feed efficiency were significantly affected by salinity, temperature, and the interaction between salinity and temperature, whereas apparent digestibility coefficient was only affected by temperature. The relationship between specific growth, food consumption, feed efficiency or apparent digestibility coefficient, salinity, and temperature was shown in Table 1.

The shrimp maintained at 21 [per thousand] and 32[degrees]C had significantly higher specific growth rate, whereas those maintained at 0.2 [per thousand] and at 20[degrees]C had significantly lower value. The relationships between specific growth rate or feed efficiency and salinity or temperature were shown in Table 2.

Energy Budget

The pattern of energy allocation varied with salinity and temperature, in which 63.60% to 78.49% of consumed energy lost through respiration, 10.38% to 21.17% invested in growth, 4.17% to 10.74% for feces, 3.62% to 5.37% for excretion, and only 0.90% to 1.45% for exuviae (Fig. 2). At all salinities with increases in temperature, the percentage of intake energy lost in respiration or excretion (the energy value expressed as the percentage of intake energy, %C) exhibited an increasing trend, whereas that invested in growth (%C) exhibited a decreasing trend. At each temperature level with increasing salinity within the range tested, the percentage of intake energy invested in growth (%C) gradually increased, reaching the maximum value, and thereafter declined, whereas that lost in respiration or excretion (%C) exhibited an inversed trend.

[FIGURE 2 OMITTED]

Two-way ANOVA showed that growth, respiration, or excretion (%C) was significantly affected by salinity, temperature, and the interaction between salinity and temperature, whereas the feces (%C) was only affected by temperature. The relationship between growth, respiration, excretion or feces (%C), salinity, and temperature was shown in Table 1.

At 11 [per thousand] to 31 [per thousand] and 20[degrees]C, the percentage of intake energy deposited in growth (%C) was significantly higher, whereas at 0.2 [per thousand] and 32[degrees]C, the percentage of intake energy deposited in growth (%C) was significantly lower compared with other treatments.

Discussion

The Interaction of Salinity and Temperature on Survival and Growth of L. vannamei Juveniles

It has long been recognized that the interactions between two or more ecological factors can modify the effect of factors acting individually (Linton et al. 1994, Vernberg & Piyatiratitivorakul 1998). For example, Hall and Burns (2002) reported that elevated temperatures decreased the salinity tolerance level of Daphnia carinata adults. Currently, the significantly decreased survival in shrimp maintained at 0.2 [per thousand] and 28[degrees]C to 32[degrees]C implicates that high temperature may become a contributing factor to mortality when acting together with tap water stressful conditions. Consistent with our study, Kumlu et al. (2000) also suggested that elevated temperature might be suitable for growth of aquatic animals, but it had an inverse effect on survival.

Regression analyses indicated that the optimal salinity corresponding to maximum specific growth rate was about 21.03 [per thousand], 21.05 [per thousand], 25.00 [per thousand], and 21.01 [per thousand] at temperatures of 20[degrees]C, 24[degrees]C, 28[degrees]C, and 32[degrees]C, respectively (Table 2). Because a significant interaction between salinity and temperature was detected for specific growth rate, the optimal salinity for L. vannamei juveniles may be dependent on temperature. Similarly, the effects of temperature on growth of aquatic animals were also modified by salinity. Imsland et al. (2001) found that the optimal temperature for growth ([Max.sub.T]) of juvenile turbot Scophthalmus maximus varied with salinity: [Max.sub.T] at 33.5 [per thousand] was 19.6 [+ or -] 0.3[degrees]C, whereas [Max.sub.T] at 15 [per thousand] was 22.9 [+ or -] 1.0[degrees]C and at 25 [per thousand] was 24.7 [+ or -] 2.1[degrees]C. Likongwe et al. (1996) found that at salinities of 0 [per thousand], 8 [per thousand], and 16 [per thousand], final mean weights of juvenile Nile tilapia Oreochromis niloticus were significantly higher at 32[degrees]C, whereas at salinity 12 [per thousand] final mean weights were significantly higher at 28[degrees]C. In the current study, the optimal temperature corresponding to maximum specific growth rate was above 32[degrees]C at salinities of 11 [per thousand] to 31 [per thousand], whereas at salinities of 0.2 [per thousand], the optimal temperature was close to 28.65[degrees]C (Table 2).

Salinity Effect on Growth of L. vannamei Juveniles

The isosmotic point for penaeids ranged from 23-30 ppt (Castille & Lawrence 1981, Dill 1981). Early work on Penaeus chinensis demonstrated the highest proportion of intake energy to growth in isosmotic salinity, because the animal would expend the minimal proportion of energy in osmoregulation (Zhang & Dong 2002). A similar energy allocation pattern was observed in this study (i.e., specific growth rate, food consumption, and the proportion of intake energy invested in growth (%C) gradually increased, reaching the maximum value and thereafter declined with increases of salinity within the range tested, whereas the proportion of energy losses (respiration and excretion, %C) exhibited an inversed trend with salinity (Fig. 2). Therefore, from a bioenergetic perspective, the growth differences between salinities are primarily the consequence of variations in food consumption and energy allocation.

Temperature Effect on Growth of L. vannamei Juveniles

Temperature is one of the most important modifiers of energy flow, and hence growth of shrimp (Dong et al. 1994a, Zhang et al. 1998), and an increase in temperature over the range of 20[degrees]C to 32[degrees]C resulting in an increase of growth of L. vannamei juveniles had been reported (Ponce-Palafox et al. 1997, Jiang et al. 2000). In this study, specific growth rate, food consumption, feed efficiency, apparent digestibility coefficient, and energy allocation pattern of L. vannamei juveniles were significantly affected by temperature (Fig. 1 and Fig. 2), which were similar to that of Macrocrachium nipponense and Penaeus chinensis (Dong et al. 1994b, Zhang et al. 1998). By contrast, previous investigations on Phoxinus phoxinus, Ctenopharyngodon idellus, and Lateolabrax japonicus suggested that temperature had no significant effects on the energy allocation pattern (Cui & Wootton 1990, Cui et al. 1995, Dai et al. 1998), indicating the different bioenergetic mechanisms across species.

In land-based recirculating culture systems, a higher temperature may markedly shorten the culture period of shrimp. However, Zhang et al. (1998) believed that increasing water temperature might increase the energy expenditure for maintenance, leaving less consumed energy available for growth. This was partly in line with the results of the present study (i.e., the proportion of intake energy invested in growth (%C) appeared to decrease with increases of temperature from 20[degrees]C to 32[degrees]C, whereas total metabolic expenditure (respiration and excretion, %C) displayed inverse trends with temperature (Fig. 2); this suggests that it is energetically expedient to grow L. vannamei juveniles at relatively lower temperatures.

ACKNOWLEDGMENTS

This study were funded by Chinese National Agricultural Development Project (Grant no. K2002-15), Jiangsu Provincial Science Foundation for Talent Youths (Grant no. 2006548) and Open Fund of Jiangsu Key Laboratory of Marine Biotechnology (Grant no. 2006HS017).

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TABLE 1.

The relationship between specific growth rate, food consumption,
feed efficiency, apparent digestibility coefficient or the percentage
of intake energy allocated to growth, respiration, excretion or
faces (C%), salinity, and temperature.

                                                              [R.sup.2]

SG[R.sub.d] = -16.350 + 0.09268S + 1.353T -
              0.003251[S.sup.2] - 0.02138[T.sup.2]
              + 0.001799S x T                                   0.923
F[C.sub.d] = -1.892 + 0.003635S + 0.03945T
             -0.002281[S.sup.2] + 0.003336[T.sup.2]             0.902
             + 0.003342S x T
F[E.sub.fd] = 32.379 + 0.204S - 0.694T - 0.003322[S.sup.2]
              - 0.0002942S x T                                  0.975
AD[C.sub.d] = -15.984 + 6.466T - 0.108[T.sup.2]                 0.878
                                                              [R.sup.2]
G/C = 33.389 + 0.116E - 0.701T - 0.005216[S.sup.2]
      + 0.00507S x T                                            0.984
R/C = 45.318 - 0.139S + 1.045T + 0.004664[S.sup.2]
      - 0.003108S x T                                           0.982
U/C = 0.996 + 0.01948S + 0.138T + 0.0005022[S.sup.2]
      - 0.001678S x T                                           0.982
F/C = 54.998 - 3.301T + 0.05376[T.sup.2]                        0.968

S, salinity; T, temperature; SGRd, specific growth rate (dry weight);
F[C.sub.d], food consumption (dry weight); FEfd, feed efficiency (dry
weight), AD[C.sub.d], apparent digestibility coefficient (dry weight);
G/C, the percentages of intake energy allocated to growth (i.e., feed
efficiency in energy [F[E.sub.e]]); R/C, the percentages of intake
energy allocated to respiration; U/C, the percentages of intake energy
allocated to excretion; F/C, the percentages of intake energy allocated
to feces (%).

TABLE 2.

The relationship between specific growth rate or feed efficiency
and salinity or temperature.

                                                            [Max.sub.S]
T ([degrees]                                                   ([per
C)                                              [R.sup.2]    thousand])

  20           SG[R.sub.d] = -0.0032[S.sup.2]
                 + 0.1346S + 2.0555              0.7535        21.03
  24           SG[R.sub.d] = -0.0028[S.sup.2]
                 + 0.1179S + 3.8889              0.6916        21.05
  28           SG[R.sub.d] = -0.0014[S.sup.2]
                 + 0.07S + 5.2539                0.4819        25.00
  32           SG[R.sub.d] = -0.0056[S.sup.2]
                 + 0.2353S + 4.6021              0.8393        21.01
  20           F[E.sub.fd] = -0.0045[S.sup.2]
                 + 0.2459S + 18.242              0.9353        27.32
  24           F[E.sub.fd] = -0.0026[S.sup.2]
                 + 0.1566S + 16.216              0.8481        30.12
  28           F[E.sub.fd] = -0.0003[S.sup.2]
                 + 0.09S + 12.935                0.8167          --
  32           F[E.sub.fd] = -0.0064[S.sup.2]
                 + 0.2926S + 9.9897              0.9461        22.86
  20           F[E.sub.e] = -0.0056[S.sup.2]
                 + 0.2285S + 19.047              0.8788        20.40
  24           F[E.sub.e] = -0.004[S.sup.2]
                 + 0.2111S + 16.988              0.9533        26.39
  28           F[E.sub.e] = -0.0026[S.sup.2]
                 + 0.1649S + 14.18               0.7297          --
  32           F[E.sub.e] = -0.0091[S.sup.2]
                 + 0.4065S + 10.297              0.9819        22.34

S ([per                                                     [Max.sub.T]
thousand])                                      [R.sup.2]   ([degrees]C)

   0.2         SG[R.sub.d] = -0.0425[T.sup.2]
                 + 2.4355T - 29.759              0.9276        28.65
  11           SG[R.sub.d] = 0.2792T - 2.2016
  21           SG[R.sub.d] = 0.2919T - 2.1116    0.9687          --
  31           SG[R.sub.d] = 0.2821T - 2.1968     0.862          --
   0.2         F[E.sub.fd] = -0.0196[T.sup.2]    0.9007          --
                 + 0.3125T + 19.998              0.9915          --
  11           F[E.sub.fd] = 0.0392[T.sup.2]
                - 2.7028T + 58.852               0.9749          --
  21           F[E.sub.fd] = 0.0012[T.sup.2]
                 - 0.7815T + 36.725              0.9893          --
  31           F[E.sub.fd] = 0.0039[T.sup.2]
                 - 0.904T + 37.945               0.9957          --
   0.2         F[E.sub.e] = -0.0335[T.sup.2]
                 + 1.0312T + 11.763              0.9955        15.39
  11           F[E.sub.e] = 0.0195[T.sup.2]
                 - 1.6682T + 46.92               0.9775          --
  21           F[E.sub.e] = -0.0185[T.sup.2]
                 + 0.4298T + 19.978              0.9819          --
  31           F[E.sub.e] = -0.0176[T.sup.2]
                 + 0.3351T + 21.32                0.982          --

T, temperature; S, salinity; SG[R.sub.d], specific growth rate (dry
weight); F[E.sub.fd], feed efficiency in dry weight; F[E.sub.e], feed
efficiency in energy (i.e., the percentages of intake energy allocated
to growth [G/C]); [Max.sub.T], the optimal temperature corresponding to
maximum specific growth rate or feed efficiency; [Max.sub.S], the
optimal salinity corresponding to maximum specific growth rate or feed
efficiency.

BINLUN YAN, XINGQIANG WANG * AND MEI CAO

Jiangsu Key Laboratory of Marine Biotechnology, Huaihai Institute of Technology, Lianyungang, 222005, People's Republic of China

* Corresponding author. E-mail: [e-mail]