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Effect of periodic light intensity change on the molting frequency and growth of Litopenaeus vannamei
Aquaculture 396–399 (2013) 66–70
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Effect of periodic light intensity change on the molting frequency and growth of Litopenaeus vannamei Biao Guo a, b, Fang Wang a,⁎, Ying Li c, Shuanglin Dong a a b c
The Key Laboratory of Mariculture, Ministry of Education, Fisheries College, Ocean University of China, Qingdao 266003, People's Republic of China Bohai Fisheries Research Institute of Tianjin, Tianjin 300000, People's Republic of China Aquatic Product Technology Promotion Department of Beijing, Beijing 100021, People's Republic of China
a r t i c l e
i n f o
Article history: Received 23 October 2012 Received in revised form 26 February 2013 Accepted 26 February 2013 Available online 6 March 2013 Keywords: Litopenaeus vannamei Periodic light intensity change Growth Molting Energy allocation
a b s t r a c t Five light intensity treatments (60 lx, “CL”; 600 lx changed to 60 lx, “FL1”; 1500 lx changed to 60 lx, “FL2”; 3000 lx changed to 60 lx, “FL3”; 6000 lx changed to 60 lx, “FL4”) were tested to determine the growth of Litopenaeus vannamei under periodic light intensity change conditions. After 45-day experiment, shrimp in FL2 treatment showed the best weight gain (WG) and specific growth rate (SGRd), which might have been caused by high food conversion efficiency (FCEd), lowest energy allocation for respiration and excretion, and highest energy allocation for growth. The molting frequency in FL4 treatment was the lowest and significantly lower than those in other treatments, but the growth was not the worst. These results suggest that periodic light intensity fluctuation from 1500 lx to 60 lx could promote growth of L. vannamei which could be used as a pattern of regulation of light intensity in the commercial shrimp culture. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Light comprises a complex of external and ecological factors, including photoperiod, color spectrum and intensity. Light characteristics are very specific in an aquatic environment, and light is extremely variable in nature (Gilles and Pierre-Yves, 1999). Many studies have focused on the effect of light intensity on the survival, molting and growth of crustaceans. Wang et al. (2004a) found that the growth of Fenneropenaeus chinensis in different photoperiods was significantly different. Van Wormhoudt and Ceccaldi (1976) have shown that different wavelengths affect the enzymatic activity in Palaemon serratus, thus affecting digestibility, assimilation and growth of the shrimp. No significant differences among shrimps F. chinensis under 0, 50, 300 and 1300 lx were observed, and the SGR of shrimps under 5500 lx was significantly lower than those under 0, 50, 300 and 1300 lx (Wang et al., 2004b). All the above studies were conducted under constant light conditions and the results laid a basis for further understanding of the effect of light on the physiological ecology of shrimps. In natural condition, different concentrations of plankton, suspended particles and dissolved organic substances in water change the spectra and induce the difference of light intensities in different water layers (Blaxter, 1968; McFarland, 1986). So the effect of light change on shrimps has attracted the attention of researchers. The significant differences of growths in Litopenaeus vannamei were also found in different rhythmic (Guo et al., 2011) or periodic light
⁎ Corresponding author. Tel./fax: +86 532 82032435. E-mail address: [email protected] (F. Wang). 0044-8486/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.aquaculture.2013.02.033
color changes (Guo et al., 2012a), and in different rhythmic light intensity changes (Guo et al., 2012b). Intensive commercial shrimp culture is becoming a major trend in China (Shen et al., 2007), which requires the efficient control of the ecological environment for providing an optimal condition for survival and growth of shrimps (Wang, 2003). The regulation and effects of temperature, salinity (Liu et al., 2008), dissolved oxygen consumption (Liu et al., 2005), nitrogen and phosphorus (Li et al., 2007), and light color (Guo et al., 2012a) in commercial shrimp culture had been extensively studied. Besides these factors, light intensity is also one of the major environmental factors influencing behavior (Zhang et al., 2006), feeding (Ricardo et al., 2008) and growth of crustaceans (Wang et al., 2004b). However, there is limited information about the regulation of light intensity in commercial shrimp culture. Guo et al. (2012b) reported that the rhythmic light intensity fluctuations affected the molting and growth of L. vannamei and the fluctuating amplitude being ±1800 lx with a mean light intensity of 2700 lx was beneficial in the growth of shrimp. In the natural environment, the pattern of light intensity changes is not only circadian rhythmic but also periodic. Considering that being cost-effective is always the key to commercial shrimp production, so the periodic light intensity change may be more feasible than the rhythmic light intensity fluctuation in commercial shrimp culture. The objective of this study is to find a suitable pattern of periodic light intensity change by measuring growth and molting of L. vannamei under one single light intensity treatment and four periodic fluctuating light intensity treatments. Our results may provide technical support for increasing the commercial indoor shrimp production.
B. Guo et al. / Aquaculture 396–399 (2013) 66–70
2. Materials and methods 2.1. Experimental shrimp and acclimation L. vannamei juveniles were obtained from Baorong Aquaculture Corporation, Qingdao, PR China. After transferring to the laboratory, the shrimps were acclimated in tanks (170 cm × 75 cm × 35 cm, water volume: 450 L) for 10 days. Seawater was pre-filtered using a sand filter. One-half to two-thirds of the water in the tank was replaced daily with fresh seawater to ensure good water quality. During acclimation period, the juveniles were fed to satiation twice daily (at 6 a.m. and 4 p.m.) with a commercial feed (crude protein, 43.39% ± 0.22%; fat, 9.74% ± 0.30%; ash, 9.91% ± 0.05% and moisture, 8.41% ± 0.06%; Mawei Fishery Feed Co., Ltd., Fujian, PR China). A salinity of 28–30 ppt, temperature of 24 °C–25 °C, and photoperiod of 14 h in lightness and 10 h in darkness were maintained. 2.2. Experimental design According to the research on shrimps by Wang et al. (2004b), one constant light intensity (60 lx, “CL”) treatment and four periodic abrupt changing light intensity treatments (600 lx changed to 60 lx, “FL1”; 1500 lx changed to 60 lx, “FL2”; 3000 lx changed to 60 lx, “FL3”; 6000 lx changed to 60 lx, “FL4”) were designed. Following the research on shrimps by Ding et al. (2008), the medium frequency of salinity fluctuation (four days high salinity then two days low salinity) was better for growth than those in high and low frequencies of fluctuation. Considering salinity affects the growth of shrimp more directly than light, the periodic abrupt changing light intensity treatments were defined as follows: a six-day strong light intensity was given firstly, a two-day weak light intensity was followed; and then a new cycle began. The duration of the experiment was 45 days. Four replicates were set up for the experiment on each regime. Twenty glass aquaria (45 cm × 25 cm × 30 cm, water volume: 35 L) were used for shrimp rearing. Each aquarium held five individuals and was covered with a 5 mm thick screen (the screen is laboratorydesigned, which is a wooden frame sandwiched with transparent plastic net) to prevent the shrimp from jumping out. The separate light treatments (shaded from each other) were held in one room where temperature was controlled using an air conditioner. The lamps were hung 60–80 cm above the aquaria. The design focused on the illumination intensity at the bottom of the aquaria. This was targeted. This was realized by adjusting the distance between the lamps and water surface as well as the number of lighting lamps. In order to achieve the changes in light intensity, some power switches were used to control the number of lighting lamps. An underwater illumination photometer (JD-1A, made in Shanghai Xuelian Instruments) was used to determine the luminance.
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day (at 6 a.m. and 4 p.m.). The uneaten feed and feces were collected into cups by siphon, settled, and dried 2.5 h after feeding. The molted shells were also collected. The collected uneaten feed, feces and shells were dried at 65 °C, and kept for further analysis. After a 45-day experiment, all the experimental shrimps were sampled and dried at 65 °C for 48 h. The final dry body, final wet body and initial wet body of the shrimp were weighted by AL204 Mettler Toledo Balance. The dry initial wet body was calculated as follows: W1 ¼ W0 Rd= w Rd= w ¼ Wd =Ww where, W1 and W0 are the initial dry and wet body weights of the shrimp, respectively; Rd/w is the rate of initial dry body and wet body of the shrimps; Wd and Ww are the dry and the wet body total weight of thirty randomly sampled shrimps, respectively. 2.5. Estimation of energy budget The energy contents of the shrimp carcasses, feed, feces and molted shells were measured by Parr 1281 Oxygen Bomb Calorimeter. The energy budget was calculated using the following equation (Petrusewicz and Macfadyen, 1970): C¼GþFþUþEþR where C is the energy consumed in food; G, the energy deposited for growth; F, the energy lost in feces; U, the energy in excretion; E, the energy spent for exuviation; and R, the energy for respiration. The estimation of U was based on the nitrogen budget equation (Levine and Sulkin, 1979; Lemos and Phan, 2001): U ¼ ðCN −GN −FN −EN Þ 24; 830 where CN is the nitrogen consumed from food; GN, the nitrogen deposited in shrimp body; FN, the nitrogen lost in feces; EN, the nitrogen lost in molting; 24,830, the energy content in excreted nitrogen per gram (J g−1). The nitrogen contents in the formulated feed, shrimp, feces and molting shell were determined by Kjeldahl method. The value of R was calculated based on the energy budget equation above. 2.6. Calculation of data and statistical analysis The relative weight gain rate (WG, %), molting frequency (MF, %d−1), specific growth rate (SGRd), feed intake (FId) and food conversion efficiency (FCEd) in terms of the dry weight were calculated as follows:
2.3. Rearing condition
WG ¼ 100% ðWt −W0 Þ=W0
During the experiment period, dissolved oxygen in tanks was maintained above 6.0 mg L − 1, pH around 7.8, ammonia less than 0.24 mg L − 1, seawater temperature at 25 ± 0.5 °C and salinity within 28 to 30 ppt. Photoperiod and water exchange rates were the same as those in the acclimation condition.
MF ¼ 100% ðNm =Ns Þ=T −1 ¼ 100% ð lnW2 − lnW1 Þ=T SGRd % day −1 ¼ 100% F=½T ðW2 þ W1 Þ=2 FId % B:W: day
2.4. Experimental procedure and sample collection FCEd ð% Þ ¼ 100% ðW2 −W1 Þ=F After 24 h feed deprivation, 130 size-selected shrimps (with initial wet body weight of 2.73 ± 0.02 g, mean ± S.E.) were pooled into a large fiberglass tank. Among the pooled shrimps, 30 were randomly sampled for later analysis (including initial dry weight, amount of energy and protein in shrimp). The remainder were randomly selected, individually weighed and stocked into 20 aquaria with each aquarium holding five individuals. During the experiment, the shrimps were fed twice a
where, Wt and W0 are the final and the initial wet body weight of the shrimp, respectively; Nm, the total times of molting per aquarium during the experiment; Ns, the number of shrimps per aquarium; W2 and W1, the final and the initial dry body weight of the shrimp, respectively; T, the duration (days) of the experiment; F, the total food consumed in dry weight.
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B. Guo et al. / Aquaculture 396–399 (2013) 66–70
Table 1 Survival rate, molting frequency, final wet body weight, weight gain and specific growth rate of L. vannamei in constant and periodic abrupt changing light intensity regimes.1 Treatments
Survival rate (%)
Molting frequency (%d−1)
CL FL1 FL2 FL3 FL4
100.00 100.00 100.00 100.00 100.00
6.28 6.22 6.77 7.40 4.56
1 2 3
± ± ± ± ±
0.00 0.00 0.00 0.00 0.00
± ± ± ± ±
0.74b 0.26b 0.49b 0.28b 0.21a
Final wet body weight (g) 5.14 5.33 5.60 5.46 5.16
± ± ± ± ±
0.02a 0.04b 0.03d 0.05c 0.05a
Weight gain2 (%) 88.16 95.00 105.12 99.75 88.48
± ± ± ± ±
0.83a 0.96b 1.45d 1.91c 1.58a
SGRd3 (%d−1) 1.38 1.45 1.67 1.61 1.53
± ± ± ± ±
0.04a 0.02a 0.02c 0.03c 0.01b
Values (expressed as mean ± S. E., n = 4) with different letters in the same column are significantly different from each other (P b 0.05). Weight gain are expressed and calculated by wet weight. SGRd is expressed and calculated by dry weight.
Experimental data were analyzed using SPSS 11.0 (SPSS Inc., Richmond, CA, USA), with possible differences among treatments tested by ANOVA. Duncan's multiple range post hoc tests were used to compare the differences between treatments. P b 0.05 was accepted as the level of statistical significance.
3. Results 3.1. Growth and molting No significant difference in survival rate was observed among treatments. The MF in FL4 treatment was the lowest and significantly lower than those in other treatments (P b 0.05). No significant MF difference was observed in treatments CL, FL1, FL2 and FL3 (P > 0.05). The FL2 treatment had the highest WG and SGRd, in which the WG was significantly higher than those in other treatments, whereas SGRd was significantly higher than that in CL, FL1 or FL4 treatment (P b 0.05). The WG of the shrimp in the CL treatment was the lowest and was significantly lower than those in other treatments except than that in FL4 (P b 0.05). The SGRd of the shrimp in the CL and FL1 treatments was significantly lower than those in treatments FL2–4 (P b 0.05) (Table 1).
3.2. Feed intake and food conversion efficiency There was no significant difference in FId of the shrimps in different light regimes (P > 0.05) (Fig. 1). The FCEd of the shrimps in the FL2 and FL3 treatments was significantly higher than that in CL, FL1 or FL4 treatment (P b 0.05). The FCEd of the shrimps in the CL treatment was lowest and significantly lower than those in FL2, FL3 and FL4 treatments (P b 0.05) (Fig. 2).
Fig. 1. Food intake (FId) of L. vannamei in constant and periodic fluctuating light intensity regimes.
3.3. Energy allocation Energy allocation for growth (G/C) in FL2 was significantly higher than in other treatments except in FL3, but allocations for respiration (R/C) and excretion (U/C) were significantly lower than those in the CL and FL1 treatments (P b 0.05). In contrast, the G/C in the CL treatment was significantly lower than those in the FL2 and FL3 treatments (P b 0.05), and the R/C and U/C were significantly higher than those in treatments FL2–4. The lowest and the highest energy allocation for feces (F/C) of the shrimp appeared in CL and FL4, respectively. A significant difference was observed in energy allocation for molting (E/C) under different light intensity treatments (P b 0.05), and the trend is similar to the MF (Table 2). 4. Discussion Light is extremely variable and can change over a tremendous range, often very rapidly (Gilles and Pierre-Yves, 1999). For a long time, the influence of constant light on crustaceans has been studied in respect to their effects on growth (Wang et al., 2004a), maturation, reproduction (Chamberlain and Lawrence, 1981; Hoang et al., 2002a, 2002b, 2002c, 2002d), survival, metamorphosis and development of larvae (Tang, 1999; Caleb and Greg, 1998). However, light changes are also involved in the control of growth and physiological functions. The suitable rhythmic (Guo et al., 2011) or periodic light color changes (Guo et al., 2012b), or rhythmic light intensity changes (Guo et al., 2012a) could promote the growth of L. vannamei. Guo et al. (2012a) found that SGRd of shrimps in the rhythmic light intensity fluctuating treatment (the amplitude was ± 1800 lx with a mean light intensity of 2700 lx) increased approximately nineteen percent above that in constant light (2700 lx). In this study, the SGRd of the shrimps in the FL2 treatment was higher than that in the CL
Fig. 2. Food conversion efficiency (FCEd) of L. vannamei in constant and periodic fluctuating light intensity regimes. Means (n = 4) with different letters indicate significant difference (P b 0.05).
B. Guo et al. / Aquaculture 396–399 (2013) 66–70
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Table 2 Estimated energy allocation for growth, respiration, excretion, and exuviation in L. vannamei subjected to fluctuating light intensities.1 Treatments
G/C2 (%)
CL FL1 FL2 FL3 FL4
15.89 16.78 19.76 19.47 17.86
1 2 3 4 5 6
± ± ± ± ±
R/C3 (%) 0.71a 0.01a 0.16c 0.11c 0.14b
61.23 59.17 55.40 55.61 56.53
± ± ± ± ±
U/C4 (%) 0.81b 0.49b 0.81a 0.53a 0.47a
5.43 5.24 4.88 4.89 4.97
± ± ± ± ±
0.11b 0.03b 0.05a 0.11a 0.03a
F/C5 (%) 16.71 18.05 19.21 19.32 20.16
± ± ± ± ±
E/C6 (%) 0.49a 0.53ab 0.78bc 0.78bc 0.53c
0.74 0.76 0.75 0.71 0.48
± ± ± ± ±
0.03b 0.01b 0.01b 0.01b 0.01a
Values (expressed as mean ± S.E., n = 4) with different letters in the same column are significantly different from each other (P b 0.05). G/C (%) = energy for growth/energy consumed in food. R/C (%) = energy for respiration/energy consumed in food. U/C (%) = energy for excretion/energy consumed in food. F/C (%) = energy for feces/energy consumed in food. E/C (%) = energy for exuviate/energy consumed in food.
treatment by a factor of about 1.21. This result suggested that periodic light intensity changes also can promote the growth of L. vannamei. Further, the periodic light intensity change may be more useful than the rhythmic light change for being more cost-effective in commercial shrimp culture. Ricardo et al. (2008) suggested that the ability of shrimp larva to catch their prey in light was stronger than that in dark. The rate of feeding in spp. Rosenbergii larva was accelerated with the increasing light intensities from 0 lx to 100 lx, but did not significantly vary when the light intensity was above 100 lx (Lin, 1998). Wang et al. (2004b) suggested that no significant difference in FId in F. chinensis was observed in different single light intensity conditions. In our study, there is no significant difference in FId for all regimes. Therefore, it seems that feed intake in relation to light intensity could be species specific and relevant to the development of crustaceans. Li et al. (2011) found that light intensity (from 14 lx to 1252 lx) had no significant effect on trypsin and pancreatic lipase activities of Eriocheir sinensis. However, Wang et al. (2006) suggested that digestive enzyme (protease, amylase and lipase enzymes) activities of F. chinensis in 5500 lx were significantly higher than that in 300 lx. The different conclusions may be caused by the different ranges of light intensities. The activity of hormones involved in metabolism increased when shrimps were under strong light (Hoang et al., 2003), so we conjectured that digestive enzymes of shrimps under strong light might be higher than those under low light. The results that the FCEd of the shrimps in treatments FL2, FL3 and FL4 were significantly higher than CL and FL1 treatments in our experiment might meet our conjecture. The reasons that the FCEd of the shrimps in treatment FL4 were significantly lower than that in FL2 and FL3 may be the following: First, the increase in hormone activity may accelerate the process of conversion of food to body tissue, but on the other hand, may increase energy expenditure. Second, lots of energy were consumed to meet the greatly abrupt change of light intensity in FL4. Anyhow, the difference of growth of L. vannamei under different light intensity treatments was related to FCEd of shrimp. Previous studies have also shown that the metabolic energy had the largest share in the energy distribution of decapoda crustaceans. Therefore, the change of metabolic energy could determine the energy accumulation for growth (Wang et al., 2005; Paul and Akira, 1989). In this experiment, the test shrimp in CL and FL1 treatments spent much more energy in respiration and excretion, while depositing less energy for growth than those in other treatments. While the shrimp in FL2 and FL3 treatments deposited more energy for growth and spent less energy in respiration and excretion, juvenile of L. vannamei in FL2 and FL3 treatments used more energy for growth contributing to a higher SGRd. Wang et al. (2004b) reported that the energy allocation for respiration, excretion and exuviation of F. chinensis under 5500 lx light treatment was higher than those under lower light treatment, which led to low energy allocation for growth and poorer quality of shrimp. Though the shrimp in the FL4 treatment in this experiment also experience high light intensity, the energy allocation for growth of the shrimp was higher
than that in CL treatment. Maybe the light intensity fluctuation affected the energy distribution of shrimps, which was beneficial to the growth of L. vannamei. Wang et al. (2004a) suggested that the growth of shrimps may be related to feed, digestion and absorption of food, and the molting is related to the secretion of hormone. So there may be separate environmental regulations (e.g. light intensity) present for molting and growth in shrimp. So the MF and energy allocation for molting of shrimps did not appear significantly different between the treatments with best and poorest growth, but the MF and energy allocation for molting of shrimps in FL4 were significantly lower than those in other treatments. Compared to the rhythmic light intensity fluctuation reported by Guo et al. (2012b), the changes from 1500 lx to 60 lx were also beneficial to the growth of L. vannamei and more cost-effective in commercial shrimp culture, so this periodic light intensity change could be implemented in L. vannamei commercial culture to improve the FCR and growth of shrimp. Acknowledgment This research was supported by the projects under Major State Basic Research of China (grant no. 2009CB118706) and the Ministry of Science & Technology of China (grant no. 2011BAD13B03). References Blaxter, J.H.S., 1968. Visual thresholds and spectral sensitivity of herring larvae. Journal of Experimental Biology 48, 39–53. Caleb, G., Greg, B.M., 1998. Effect of photoperiod and light intensity on survival, development and cannibalism of larvae of the Australian giant crab Pseudocarcinus gigas (Lamarck). Aquaculture 165, 51–63. Chamberlain, G.W., Lawrence, A.L., 1981. Effects of light intensity and male and female eyestalk ablation on reproduction of Penaeus styirostris and P. vannamei. Journal of the World Aquaculture Society 12, 357–372. Ding, S., Wang, F., Guo, B., Li, X.S., 2008. Effects of salinity fluctuation on the molt, growth, and energy budget of juvenile Fenneropenaeus chinensis. Chinese Journal of Applied Ecology 19, 419–423 (in Chinese with English abstract). Gilles, B., Pierre-Yves, L.B., 1999. Does light have an influence on fish growth? Aquaculture 177, 129–152. Guo, B., Wang, F., Dong, S.L., Gao, Q.F., 2011. The effect of rhythmic light color fluctuation on the molting and growth of Litopenaeus vannamei. Aquaculture 314, 210–214. Guo, B., Mu, Y.C., Wang, F., Dong, S.L., 2012a. Effect of periodic light color change on the molting frequency and growth of Litopenaeus vannamei. Aquaculture 362–363, 67–71. Guo, B., Wang, F., Dong, S.L., Zhong, D.S., 2012b. Effect of fluctuating light intensity on molting frequency and growth of Litopenaeus vannamei. Aquaculture 330–333, 106–110. Hoang, T., Lee, S.Y., Keenan, C.P., Marsden, G.E., 2002a. Maturation and spawning performance of pond-reared Penaeus merguiensis in different combinations of temperature, light intensity and photoperiod. Aquaculture Research 33, 1243–1252. Hoang, T., Lee, S.Y., Keenan, C.P., Marsden, G.E., 2002b. Ovarian maturation of the banana prawn, Penaeus merguiensis de Man under different light intensities. Aquaculture 208, 159–168. Hoang, T., Lee, S.Y., Keenan, C.P., Marsden, G.E., 2002c. Effects of light intensity on maturation and spawning of ablated female Penaeus merguiensis. Aquaculture 209, 347–358. Hoang, T., Lee, S.Y., Keenan, C.P., Marsden, G.E., 2002d. Spawning behaviour of Penaeus merguiensis de Man and the effect of light intensity on spawning. Aquaculture Research 33, 351–357. Hoang, T., Barchiesis, M., Lee, S.Y., Keenan, C.P., Marsden, G.E., 2003. Influences of light intensity and photoperiod on moulting and growth of Penaeus merguiensis under laboratory condition. Aquaculture 216, 343–354.
70
B. Guo et al. / Aquaculture 396–399 (2013) 66–70
Lemos, D., Phan, V.N., 2001. Energy partitioning into growth, respiration, excretion and exuvia during larval development of the shrimp Farfantepenaeus paulensis. Aquaculture 199, 131–143. Levine, D.M., Sulkin, S.D., 1979. Partitioning and utilization of energy during the larval development of the xanthid crab, Rhithropanopeus harrisii (Gould). Journal of Experimental Marine Biology and Ecology 40, 247–257. Li, Y.Q., Li, J., Wang, Q.Y., Zhang, H.Y., 2007. Effect of stocking density on input and output of nitrogen and phosphorus in super-intensive shrimp farming pond. Journal of Fishery Sciences of China 14 (6), 926–931 (in Chinese with English abstract). Li, X.W., Li, Z.J., Liu, J.S., Zhang, T.L., Zhang, C.W., 2011. Effects of light intensity on molting, growth, precocity, digestive enzyme activity, and chemical composition of juvenile Chinese mitten crab Eriocheir sinensis. Aquaculture International 19, 301–311. Lin, X.T., 1998. The light conditions in the process of seed rearing about Macrobrachium rosenbergii. Freshwater fisheries 28, 39–40 (in Chinese). Liu, H.Y., Qu, K.M., Zhang, Q.Q., Li, J., 2005. Study on dissolved oxygen consumption both in industrial and pond cultures of shrimps. Marine Fisheries Research 26 (5), 52–56 (in Chinese with English abstract). Liu, J., Qu, K.M., Liu, H.Y., Zhu, J.X., Li, J., Ma, D.L., 2008. Studies on features of water environment in industrialized shrimp culture system. Marine Fisheries Research 29 (6), 1–8 (in Chinese with English abstract). McFarland, W.N., 1986. Light in the sea-correlations with behaviours of fishes and invertebrates. American Zoologist 26, 389–401. Paul, A.J., Akira, F., 1989. Bioenergetics of the Alaskan crab Chionoecetes bairdi (Decapoda: Majidae). Journal of Crustacean Biology 9, 25–36. Petrusewicz, K., Macfadyen, A., 1970. Productivity of Terrestrial Animals: Principles and Methods. IBP Handbook No.13.Blackwell, Oxford (190 pp.). Ricardo, C., Gisela, D., Cátia, B., Cristovão, N., Antonina, S., Maria, T.D., 2008. Importance of light and larval morphology in starvation resistance and feeding ability of newly
hatched marine ornamental shrimps Lysmata spp. (Decapoda: Hippolytidae). Aquaculture 283, 56–63. Shen, N.N., Li, C.H., Jia, X.P., Li, Z.J., Yu, M.C., Wang, X.W., Cao, Y.C., 2007. Application of three microbiological preparations to control of water quality in industrialized shrimp culture. South China Fisheries Science 3 (3), 20–25 (in Chinese with English abstract). Tang, J.C., 1999. The effect of light intensity and temperature on larval development and survival rate of Macrobrachium rosenbergii. Changchun Fisheries 1, 5–11 (in Chinese). Van Wormhoudt, A., Ceccaldi, J.H., 1976. Influence de la qualite' de la lumie're en e'levage intensif de Palaemon seratus Pennant. In: Persoone, G., Jaspers, G. (Eds.), Proc. 10th Eur. Symp. Mar. Biol., vol. 1. Universal Press, Belgium, pp. 505–521 (Mariculture). Wang, K.X., 2003. The industrialized culture technology of Litopenaeus vannamei. Shandong Fisheries 20 (1), 47–48. Wang, F., Dong, S.L., Dong, S.S., Huang, G.Q., 2004a. Effects of photoperiod on the molting and growth of juvenile Chinese shrimp Fenneropenaeus chinensis. Journal of Fishery Sciences of China 11, 354–359 (in Chinese with English abstract). Wang, F., Dong, S.L., Huang, G.Q., Zhu, C.B., Mu, Y.C., 2004b. The effect of light intensity on the growth of Chinese shrimp Fenneropenaeus chinensis. Aquaculture 234, 475–483. Wang, F., Zhang, J.D., Dong, S.L., Mu, Y.C., 2005. The effects of light intensity and photoperiod on the growth of juvenile Fenneropenaeus chinensis. Periodical of Ocean University of China 35, 768–772 (in Chinese with English abstract). Wang, F., Song, C.M., Ding, S., Dong, S.L., 2006. Effects of light on specific activities of three digestive enzymes in juvenile Chinese shrimp Fenneropenaeus chinensis. Journal of Fishery Sciences of China 13, 1028–1032 (in Chinese with English abstract). Zhang, P.D., Zhang, X.M., Li, J., Huang, G.Q., 2006. The effects of body weight, temperature, salinity, pH, light intensity and feeding condition on lethal DO levels of whiteleg shrimp, Litopenaeus vannamei (Boone, 1931). Aquaculture 256, 579–587.
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Effect of periodic light intensity change on the molting frequency and growth of Litopenaeus vannamei Biao Guo a, b, Fang Wang a,⁎, Ying Li c, Shuanglin Dong a a b c
The Key Laboratory of Mariculture, Ministry of Education, Fisheries College, Ocean University of China, Qingdao 266003, People's Republic of China Bohai Fisheries Research Institute of Tianjin, Tianjin 300000, People's Republic of China Aquatic Product Technology Promotion Department of Beijing, Beijing 100021, People's Republic of China
a r t i c l e
i n f o
Article history: Received 23 October 2012 Received in revised form 26 February 2013 Accepted 26 February 2013 Available online 6 March 2013 Keywords: Litopenaeus vannamei Periodic light intensity change Growth Molting Energy allocation
a b s t r a c t Five light intensity treatments (60 lx, “CL”; 600 lx changed to 60 lx, “FL1”; 1500 lx changed to 60 lx, “FL2”; 3000 lx changed to 60 lx, “FL3”; 6000 lx changed to 60 lx, “FL4”) were tested to determine the growth of Litopenaeus vannamei under periodic light intensity change conditions. After 45-day experiment, shrimp in FL2 treatment showed the best weight gain (WG) and specific growth rate (SGRd), which might have been caused by high food conversion efficiency (FCEd), lowest energy allocation for respiration and excretion, and highest energy allocation for growth. The molting frequency in FL4 treatment was the lowest and significantly lower than those in other treatments, but the growth was not the worst. These results suggest that periodic light intensity fluctuation from 1500 lx to 60 lx could promote growth of L. vannamei which could be used as a pattern of regulation of light intensity in the commercial shrimp culture. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Light comprises a complex of external and ecological factors, including photoperiod, color spectrum and intensity. Light characteristics are very specific in an aquatic environment, and light is extremely variable in nature (Gilles and Pierre-Yves, 1999). Many studies have focused on the effect of light intensity on the survival, molting and growth of crustaceans. Wang et al. (2004a) found that the growth of Fenneropenaeus chinensis in different photoperiods was significantly different. Van Wormhoudt and Ceccaldi (1976) have shown that different wavelengths affect the enzymatic activity in Palaemon serratus, thus affecting digestibility, assimilation and growth of the shrimp. No significant differences among shrimps F. chinensis under 0, 50, 300 and 1300 lx were observed, and the SGR of shrimps under 5500 lx was significantly lower than those under 0, 50, 300 and 1300 lx (Wang et al., 2004b). All the above studies were conducted under constant light conditions and the results laid a basis for further understanding of the effect of light on the physiological ecology of shrimps. In natural condition, different concentrations of plankton, suspended particles and dissolved organic substances in water change the spectra and induce the difference of light intensities in different water layers (Blaxter, 1968; McFarland, 1986). So the effect of light change on shrimps has attracted the attention of researchers. The significant differences of growths in Litopenaeus vannamei were also found in different rhythmic (Guo et al., 2011) or periodic light
⁎ Corresponding author. Tel./fax: +86 532 82032435. E-mail address: [email protected] (F. Wang). 0044-8486/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.aquaculture.2013.02.033
color changes (Guo et al., 2012a), and in different rhythmic light intensity changes (Guo et al., 2012b). Intensive commercial shrimp culture is becoming a major trend in China (Shen et al., 2007), which requires the efficient control of the ecological environment for providing an optimal condition for survival and growth of shrimps (Wang, 2003). The regulation and effects of temperature, salinity (Liu et al., 2008), dissolved oxygen consumption (Liu et al., 2005), nitrogen and phosphorus (Li et al., 2007), and light color (Guo et al., 2012a) in commercial shrimp culture had been extensively studied. Besides these factors, light intensity is also one of the major environmental factors influencing behavior (Zhang et al., 2006), feeding (Ricardo et al., 2008) and growth of crustaceans (Wang et al., 2004b). However, there is limited information about the regulation of light intensity in commercial shrimp culture. Guo et al. (2012b) reported that the rhythmic light intensity fluctuations affected the molting and growth of L. vannamei and the fluctuating amplitude being ±1800 lx with a mean light intensity of 2700 lx was beneficial in the growth of shrimp. In the natural environment, the pattern of light intensity changes is not only circadian rhythmic but also periodic. Considering that being cost-effective is always the key to commercial shrimp production, so the periodic light intensity change may be more feasible than the rhythmic light intensity fluctuation in commercial shrimp culture. The objective of this study is to find a suitable pattern of periodic light intensity change by measuring growth and molting of L. vannamei under one single light intensity treatment and four periodic fluctuating light intensity treatments. Our results may provide technical support for increasing the commercial indoor shrimp production.
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2. Materials and methods 2.1. Experimental shrimp and acclimation L. vannamei juveniles were obtained from Baorong Aquaculture Corporation, Qingdao, PR China. After transferring to the laboratory, the shrimps were acclimated in tanks (170 cm × 75 cm × 35 cm, water volume: 450 L) for 10 days. Seawater was pre-filtered using a sand filter. One-half to two-thirds of the water in the tank was replaced daily with fresh seawater to ensure good water quality. During acclimation period, the juveniles were fed to satiation twice daily (at 6 a.m. and 4 p.m.) with a commercial feed (crude protein, 43.39% ± 0.22%; fat, 9.74% ± 0.30%; ash, 9.91% ± 0.05% and moisture, 8.41% ± 0.06%; Mawei Fishery Feed Co., Ltd., Fujian, PR China). A salinity of 28–30 ppt, temperature of 24 °C–25 °C, and photoperiod of 14 h in lightness and 10 h in darkness were maintained. 2.2. Experimental design According to the research on shrimps by Wang et al. (2004b), one constant light intensity (60 lx, “CL”) treatment and four periodic abrupt changing light intensity treatments (600 lx changed to 60 lx, “FL1”; 1500 lx changed to 60 lx, “FL2”; 3000 lx changed to 60 lx, “FL3”; 6000 lx changed to 60 lx, “FL4”) were designed. Following the research on shrimps by Ding et al. (2008), the medium frequency of salinity fluctuation (four days high salinity then two days low salinity) was better for growth than those in high and low frequencies of fluctuation. Considering salinity affects the growth of shrimp more directly than light, the periodic abrupt changing light intensity treatments were defined as follows: a six-day strong light intensity was given firstly, a two-day weak light intensity was followed; and then a new cycle began. The duration of the experiment was 45 days. Four replicates were set up for the experiment on each regime. Twenty glass aquaria (45 cm × 25 cm × 30 cm, water volume: 35 L) were used for shrimp rearing. Each aquarium held five individuals and was covered with a 5 mm thick screen (the screen is laboratorydesigned, which is a wooden frame sandwiched with transparent plastic net) to prevent the shrimp from jumping out. The separate light treatments (shaded from each other) were held in one room where temperature was controlled using an air conditioner. The lamps were hung 60–80 cm above the aquaria. The design focused on the illumination intensity at the bottom of the aquaria. This was targeted. This was realized by adjusting the distance between the lamps and water surface as well as the number of lighting lamps. In order to achieve the changes in light intensity, some power switches were used to control the number of lighting lamps. An underwater illumination photometer (JD-1A, made in Shanghai Xuelian Instruments) was used to determine the luminance.
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day (at 6 a.m. and 4 p.m.). The uneaten feed and feces were collected into cups by siphon, settled, and dried 2.5 h after feeding. The molted shells were also collected. The collected uneaten feed, feces and shells were dried at 65 °C, and kept for further analysis. After a 45-day experiment, all the experimental shrimps were sampled and dried at 65 °C for 48 h. The final dry body, final wet body and initial wet body of the shrimp were weighted by AL204 Mettler Toledo Balance. The dry initial wet body was calculated as follows: W1 ¼ W0 Rd= w Rd= w ¼ Wd =Ww where, W1 and W0 are the initial dry and wet body weights of the shrimp, respectively; Rd/w is the rate of initial dry body and wet body of the shrimps; Wd and Ww are the dry and the wet body total weight of thirty randomly sampled shrimps, respectively. 2.5. Estimation of energy budget The energy contents of the shrimp carcasses, feed, feces and molted shells were measured by Parr 1281 Oxygen Bomb Calorimeter. The energy budget was calculated using the following equation (Petrusewicz and Macfadyen, 1970): C¼GþFþUþEþR where C is the energy consumed in food; G, the energy deposited for growth; F, the energy lost in feces; U, the energy in excretion; E, the energy spent for exuviation; and R, the energy for respiration. The estimation of U was based on the nitrogen budget equation (Levine and Sulkin, 1979; Lemos and Phan, 2001): U ¼ ðCN −GN −FN −EN Þ 24; 830 where CN is the nitrogen consumed from food; GN, the nitrogen deposited in shrimp body; FN, the nitrogen lost in feces; EN, the nitrogen lost in molting; 24,830, the energy content in excreted nitrogen per gram (J g−1). The nitrogen contents in the formulated feed, shrimp, feces and molting shell were determined by Kjeldahl method. The value of R was calculated based on the energy budget equation above. 2.6. Calculation of data and statistical analysis The relative weight gain rate (WG, %), molting frequency (MF, %d−1), specific growth rate (SGRd), feed intake (FId) and food conversion efficiency (FCEd) in terms of the dry weight were calculated as follows:
2.3. Rearing condition
WG ¼ 100% ðWt −W0 Þ=W0
During the experiment period, dissolved oxygen in tanks was maintained above 6.0 mg L − 1, pH around 7.8, ammonia less than 0.24 mg L − 1, seawater temperature at 25 ± 0.5 °C and salinity within 28 to 30 ppt. Photoperiod and water exchange rates were the same as those in the acclimation condition.
MF ¼ 100% ðNm =Ns Þ=T −1 ¼ 100% ð lnW2 − lnW1 Þ=T SGRd % day −1 ¼ 100% F=½T ðW2 þ W1 Þ=2 FId % B:W: day
2.4. Experimental procedure and sample collection FCEd ð% Þ ¼ 100% ðW2 −W1 Þ=F After 24 h feed deprivation, 130 size-selected shrimps (with initial wet body weight of 2.73 ± 0.02 g, mean ± S.E.) were pooled into a large fiberglass tank. Among the pooled shrimps, 30 were randomly sampled for later analysis (including initial dry weight, amount of energy and protein in shrimp). The remainder were randomly selected, individually weighed and stocked into 20 aquaria with each aquarium holding five individuals. During the experiment, the shrimps were fed twice a
where, Wt and W0 are the final and the initial wet body weight of the shrimp, respectively; Nm, the total times of molting per aquarium during the experiment; Ns, the number of shrimps per aquarium; W2 and W1, the final and the initial dry body weight of the shrimp, respectively; T, the duration (days) of the experiment; F, the total food consumed in dry weight.
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Table 1 Survival rate, molting frequency, final wet body weight, weight gain and specific growth rate of L. vannamei in constant and periodic abrupt changing light intensity regimes.1 Treatments
Survival rate (%)
Molting frequency (%d−1)
CL FL1 FL2 FL3 FL4
100.00 100.00 100.00 100.00 100.00
6.28 6.22 6.77 7.40 4.56
1 2 3
± ± ± ± ±
0.00 0.00 0.00 0.00 0.00
± ± ± ± ±
0.74b 0.26b 0.49b 0.28b 0.21a
Final wet body weight (g) 5.14 5.33 5.60 5.46 5.16
± ± ± ± ±
0.02a 0.04b 0.03d 0.05c 0.05a
Weight gain2 (%) 88.16 95.00 105.12 99.75 88.48
± ± ± ± ±
0.83a 0.96b 1.45d 1.91c 1.58a
SGRd3 (%d−1) 1.38 1.45 1.67 1.61 1.53
± ± ± ± ±
0.04a 0.02a 0.02c 0.03c 0.01b
Values (expressed as mean ± S. E., n = 4) with different letters in the same column are significantly different from each other (P b 0.05). Weight gain are expressed and calculated by wet weight. SGRd is expressed and calculated by dry weight.
Experimental data were analyzed using SPSS 11.0 (SPSS Inc., Richmond, CA, USA), with possible differences among treatments tested by ANOVA. Duncan's multiple range post hoc tests were used to compare the differences between treatments. P b 0.05 was accepted as the level of statistical significance.
3. Results 3.1. Growth and molting No significant difference in survival rate was observed among treatments. The MF in FL4 treatment was the lowest and significantly lower than those in other treatments (P b 0.05). No significant MF difference was observed in treatments CL, FL1, FL2 and FL3 (P > 0.05). The FL2 treatment had the highest WG and SGRd, in which the WG was significantly higher than those in other treatments, whereas SGRd was significantly higher than that in CL, FL1 or FL4 treatment (P b 0.05). The WG of the shrimp in the CL treatment was the lowest and was significantly lower than those in other treatments except than that in FL4 (P b 0.05). The SGRd of the shrimp in the CL and FL1 treatments was significantly lower than those in treatments FL2–4 (P b 0.05) (Table 1).
3.2. Feed intake and food conversion efficiency There was no significant difference in FId of the shrimps in different light regimes (P > 0.05) (Fig. 1). The FCEd of the shrimps in the FL2 and FL3 treatments was significantly higher than that in CL, FL1 or FL4 treatment (P b 0.05). The FCEd of the shrimps in the CL treatment was lowest and significantly lower than those in FL2, FL3 and FL4 treatments (P b 0.05) (Fig. 2).
Fig. 1. Food intake (FId) of L. vannamei in constant and periodic fluctuating light intensity regimes.
3.3. Energy allocation Energy allocation for growth (G/C) in FL2 was significantly higher than in other treatments except in FL3, but allocations for respiration (R/C) and excretion (U/C) were significantly lower than those in the CL and FL1 treatments (P b 0.05). In contrast, the G/C in the CL treatment was significantly lower than those in the FL2 and FL3 treatments (P b 0.05), and the R/C and U/C were significantly higher than those in treatments FL2–4. The lowest and the highest energy allocation for feces (F/C) of the shrimp appeared in CL and FL4, respectively. A significant difference was observed in energy allocation for molting (E/C) under different light intensity treatments (P b 0.05), and the trend is similar to the MF (Table 2). 4. Discussion Light is extremely variable and can change over a tremendous range, often very rapidly (Gilles and Pierre-Yves, 1999). For a long time, the influence of constant light on crustaceans has been studied in respect to their effects on growth (Wang et al., 2004a), maturation, reproduction (Chamberlain and Lawrence, 1981; Hoang et al., 2002a, 2002b, 2002c, 2002d), survival, metamorphosis and development of larvae (Tang, 1999; Caleb and Greg, 1998). However, light changes are also involved in the control of growth and physiological functions. The suitable rhythmic (Guo et al., 2011) or periodic light color changes (Guo et al., 2012b), or rhythmic light intensity changes (Guo et al., 2012a) could promote the growth of L. vannamei. Guo et al. (2012a) found that SGRd of shrimps in the rhythmic light intensity fluctuating treatment (the amplitude was ± 1800 lx with a mean light intensity of 2700 lx) increased approximately nineteen percent above that in constant light (2700 lx). In this study, the SGRd of the shrimps in the FL2 treatment was higher than that in the CL
Fig. 2. Food conversion efficiency (FCEd) of L. vannamei in constant and periodic fluctuating light intensity regimes. Means (n = 4) with different letters indicate significant difference (P b 0.05).
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Table 2 Estimated energy allocation for growth, respiration, excretion, and exuviation in L. vannamei subjected to fluctuating light intensities.1 Treatments
G/C2 (%)
CL FL1 FL2 FL3 FL4
15.89 16.78 19.76 19.47 17.86
1 2 3 4 5 6
± ± ± ± ±
R/C3 (%) 0.71a 0.01a 0.16c 0.11c 0.14b
61.23 59.17 55.40 55.61 56.53
± ± ± ± ±
U/C4 (%) 0.81b 0.49b 0.81a 0.53a 0.47a
5.43 5.24 4.88 4.89 4.97
± ± ± ± ±
0.11b 0.03b 0.05a 0.11a 0.03a
F/C5 (%) 16.71 18.05 19.21 19.32 20.16
± ± ± ± ±
E/C6 (%) 0.49a 0.53ab 0.78bc 0.78bc 0.53c
0.74 0.76 0.75 0.71 0.48
± ± ± ± ±
0.03b 0.01b 0.01b 0.01b 0.01a
Values (expressed as mean ± S.E., n = 4) with different letters in the same column are significantly different from each other (P b 0.05). G/C (%) = energy for growth/energy consumed in food. R/C (%) = energy for respiration/energy consumed in food. U/C (%) = energy for excretion/energy consumed in food. F/C (%) = energy for feces/energy consumed in food. E/C (%) = energy for exuviate/energy consumed in food.
treatment by a factor of about 1.21. This result suggested that periodic light intensity changes also can promote the growth of L. vannamei. Further, the periodic light intensity change may be more useful than the rhythmic light change for being more cost-effective in commercial shrimp culture. Ricardo et al. (2008) suggested that the ability of shrimp larva to catch their prey in light was stronger than that in dark. The rate of feeding in spp. Rosenbergii larva was accelerated with the increasing light intensities from 0 lx to 100 lx, but did not significantly vary when the light intensity was above 100 lx (Lin, 1998). Wang et al. (2004b) suggested that no significant difference in FId in F. chinensis was observed in different single light intensity conditions. In our study, there is no significant difference in FId for all regimes. Therefore, it seems that feed intake in relation to light intensity could be species specific and relevant to the development of crustaceans. Li et al. (2011) found that light intensity (from 14 lx to 1252 lx) had no significant effect on trypsin and pancreatic lipase activities of Eriocheir sinensis. However, Wang et al. (2006) suggested that digestive enzyme (protease, amylase and lipase enzymes) activities of F. chinensis in 5500 lx were significantly higher than that in 300 lx. The different conclusions may be caused by the different ranges of light intensities. The activity of hormones involved in metabolism increased when shrimps were under strong light (Hoang et al., 2003), so we conjectured that digestive enzymes of shrimps under strong light might be higher than those under low light. The results that the FCEd of the shrimps in treatments FL2, FL3 and FL4 were significantly higher than CL and FL1 treatments in our experiment might meet our conjecture. The reasons that the FCEd of the shrimps in treatment FL4 were significantly lower than that in FL2 and FL3 may be the following: First, the increase in hormone activity may accelerate the process of conversion of food to body tissue, but on the other hand, may increase energy expenditure. Second, lots of energy were consumed to meet the greatly abrupt change of light intensity in FL4. Anyhow, the difference of growth of L. vannamei under different light intensity treatments was related to FCEd of shrimp. Previous studies have also shown that the metabolic energy had the largest share in the energy distribution of decapoda crustaceans. Therefore, the change of metabolic energy could determine the energy accumulation for growth (Wang et al., 2005; Paul and Akira, 1989). In this experiment, the test shrimp in CL and FL1 treatments spent much more energy in respiration and excretion, while depositing less energy for growth than those in other treatments. While the shrimp in FL2 and FL3 treatments deposited more energy for growth and spent less energy in respiration and excretion, juvenile of L. vannamei in FL2 and FL3 treatments used more energy for growth contributing to a higher SGRd. Wang et al. (2004b) reported that the energy allocation for respiration, excretion and exuviation of F. chinensis under 5500 lx light treatment was higher than those under lower light treatment, which led to low energy allocation for growth and poorer quality of shrimp. Though the shrimp in the FL4 treatment in this experiment also experience high light intensity, the energy allocation for growth of the shrimp was higher
than that in CL treatment. Maybe the light intensity fluctuation affected the energy distribution of shrimps, which was beneficial to the growth of L. vannamei. Wang et al. (2004a) suggested that the growth of shrimps may be related to feed, digestion and absorption of food, and the molting is related to the secretion of hormone. So there may be separate environmental regulations (e.g. light intensity) present for molting and growth in shrimp. So the MF and energy allocation for molting of shrimps did not appear significantly different between the treatments with best and poorest growth, but the MF and energy allocation for molting of shrimps in FL4 were significantly lower than those in other treatments. Compared to the rhythmic light intensity fluctuation reported by Guo et al. (2012b), the changes from 1500 lx to 60 lx were also beneficial to the growth of L. vannamei and more cost-effective in commercial shrimp culture, so this periodic light intensity change could be implemented in L. vannamei commercial culture to improve the FCR and growth of shrimp. Acknowledgment This research was supported by the projects under Major State Basic Research of China (grant no. 2009CB118706) and the Ministry of Science & Technology of China (grant no. 2011BAD13B03). References Blaxter, J.H.S., 1968. Visual thresholds and spectral sensitivity of herring larvae. Journal of Experimental Biology 48, 39–53. Caleb, G., Greg, B.M., 1998. Effect of photoperiod and light intensity on survival, development and cannibalism of larvae of the Australian giant crab Pseudocarcinus gigas (Lamarck). Aquaculture 165, 51–63. Chamberlain, G.W., Lawrence, A.L., 1981. Effects of light intensity and male and female eyestalk ablation on reproduction of Penaeus styirostris and P. vannamei. Journal of the World Aquaculture Society 12, 357–372. Ding, S., Wang, F., Guo, B., Li, X.S., 2008. Effects of salinity fluctuation on the molt, growth, and energy budget of juvenile Fenneropenaeus chinensis. Chinese Journal of Applied Ecology 19, 419–423 (in Chinese with English abstract). Gilles, B., Pierre-Yves, L.B., 1999. Does light have an influence on fish growth? Aquaculture 177, 129–152. Guo, B., Wang, F., Dong, S.L., Gao, Q.F., 2011. The effect of rhythmic light color fluctuation on the molting and growth of Litopenaeus vannamei. Aquaculture 314, 210–214. Guo, B., Mu, Y.C., Wang, F., Dong, S.L., 2012a. Effect of periodic light color change on the molting frequency and growth of Litopenaeus vannamei. Aquaculture 362–363, 67–71. Guo, B., Wang, F., Dong, S.L., Zhong, D.S., 2012b. Effect of fluctuating light intensity on molting frequency and growth of Litopenaeus vannamei. Aquaculture 330–333, 106–110. Hoang, T., Lee, S.Y., Keenan, C.P., Marsden, G.E., 2002a. Maturation and spawning performance of pond-reared Penaeus merguiensis in different combinations of temperature, light intensity and photoperiod. Aquaculture Research 33, 1243–1252. Hoang, T., Lee, S.Y., Keenan, C.P., Marsden, G.E., 2002b. Ovarian maturation of the banana prawn, Penaeus merguiensis de Man under different light intensities. Aquaculture 208, 159–168. Hoang, T., Lee, S.Y., Keenan, C.P., Marsden, G.E., 2002c. Effects of light intensity on maturation and spawning of ablated female Penaeus merguiensis. Aquaculture 209, 347–358. Hoang, T., Lee, S.Y., Keenan, C.P., Marsden, G.E., 2002d. Spawning behaviour of Penaeus merguiensis de Man and the effect of light intensity on spawning. Aquaculture Research 33, 351–357. Hoang, T., Barchiesis, M., Lee, S.Y., Keenan, C.P., Marsden, G.E., 2003. Influences of light intensity and photoperiod on moulting and growth of Penaeus merguiensis under laboratory condition. Aquaculture 216, 343–354.
70
B. Guo et al. / Aquaculture 396–399 (2013) 66–70
Lemos, D., Phan, V.N., 2001. Energy partitioning into growth, respiration, excretion and exuvia during larval development of the shrimp Farfantepenaeus paulensis. Aquaculture 199, 131–143. Levine, D.M., Sulkin, S.D., 1979. Partitioning and utilization of energy during the larval development of the xanthid crab, Rhithropanopeus harrisii (Gould). Journal of Experimental Marine Biology and Ecology 40, 247–257. Li, Y.Q., Li, J., Wang, Q.Y., Zhang, H.Y., 2007. Effect of stocking density on input and output of nitrogen and phosphorus in super-intensive shrimp farming pond. Journal of Fishery Sciences of China 14 (6), 926–931 (in Chinese with English abstract). Li, X.W., Li, Z.J., Liu, J.S., Zhang, T.L., Zhang, C.W., 2011. Effects of light intensity on molting, growth, precocity, digestive enzyme activity, and chemical composition of juvenile Chinese mitten crab Eriocheir sinensis. Aquaculture International 19, 301–311. Lin, X.T., 1998. The light conditions in the process of seed rearing about Macrobrachium rosenbergii. Freshwater fisheries 28, 39–40 (in Chinese). Liu, H.Y., Qu, K.M., Zhang, Q.Q., Li, J., 2005. Study on dissolved oxygen consumption both in industrial and pond cultures of shrimps. Marine Fisheries Research 26 (5), 52–56 (in Chinese with English abstract). Liu, J., Qu, K.M., Liu, H.Y., Zhu, J.X., Li, J., Ma, D.L., 2008. Studies on features of water environment in industrialized shrimp culture system. Marine Fisheries Research 29 (6), 1–8 (in Chinese with English abstract). McFarland, W.N., 1986. Light in the sea-correlations with behaviours of fishes and invertebrates. American Zoologist 26, 389–401. Paul, A.J., Akira, F., 1989. Bioenergetics of the Alaskan crab Chionoecetes bairdi (Decapoda: Majidae). Journal of Crustacean Biology 9, 25–36. Petrusewicz, K., Macfadyen, A., 1970. Productivity of Terrestrial Animals: Principles and Methods. IBP Handbook No.13.Blackwell, Oxford (190 pp.). Ricardo, C., Gisela, D., Cátia, B., Cristovão, N., Antonina, S., Maria, T.D., 2008. Importance of light and larval morphology in starvation resistance and feeding ability of newly
hatched marine ornamental shrimps Lysmata spp. (Decapoda: Hippolytidae). Aquaculture 283, 56–63. Shen, N.N., Li, C.H., Jia, X.P., Li, Z.J., Yu, M.C., Wang, X.W., Cao, Y.C., 2007. Application of three microbiological preparations to control of water quality in industrialized shrimp culture. South China Fisheries Science 3 (3), 20–25 (in Chinese with English abstract). Tang, J.C., 1999. The effect of light intensity and temperature on larval development and survival rate of Macrobrachium rosenbergii. Changchun Fisheries 1, 5–11 (in Chinese). Van Wormhoudt, A., Ceccaldi, J.H., 1976. Influence de la qualite' de la lumie're en e'levage intensif de Palaemon seratus Pennant. In: Persoone, G., Jaspers, G. (Eds.), Proc. 10th Eur. Symp. Mar. Biol., vol. 1. Universal Press, Belgium, pp. 505–521 (Mariculture). Wang, K.X., 2003. The industrialized culture technology of Litopenaeus vannamei. Shandong Fisheries 20 (1), 47–48. Wang, F., Dong, S.L., Dong, S.S., Huang, G.Q., 2004a. Effects of photoperiod on the molting and growth of juvenile Chinese shrimp Fenneropenaeus chinensis. Journal of Fishery Sciences of China 11, 354–359 (in Chinese with English abstract). Wang, F., Dong, S.L., Huang, G.Q., Zhu, C.B., Mu, Y.C., 2004b. The effect of light intensity on the growth of Chinese shrimp Fenneropenaeus chinensis. Aquaculture 234, 475–483. Wang, F., Zhang, J.D., Dong, S.L., Mu, Y.C., 2005. The effects of light intensity and photoperiod on the growth of juvenile Fenneropenaeus chinensis. Periodical of Ocean University of China 35, 768–772 (in Chinese with English abstract). Wang, F., Song, C.M., Ding, S., Dong, S.L., 2006. Effects of light on specific activities of three digestive enzymes in juvenile Chinese shrimp Fenneropenaeus chinensis. Journal of Fishery Sciences of China 13, 1028–1032 (in Chinese with English abstract). Zhang, P.D., Zhang, X.M., Li, J., Huang, G.Q., 2006. The effects of body weight, temperature, salinity, pH, light intensity and feeding condition on lethal DO levels of whiteleg shrimp, Litopenaeus vannamei (Boone, 1931). Aquaculture 256, 579–587.