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Feeding n-3 HUFA enriched Artemia to the larvae of the pink shrimp Farfantepenaeus paulensis increases stress tolerance and subsequent growth.


It is well known that penaeid shrimp have a limited ability to perform de novo synthesis of highly unsaturated fatty acids (HUFA). This was first shown in Marsupenaeus japonicus (Kanazawa et al., 1979a), Penaeus monodon and Fenneropenaeus merguiensis (Kanazawa et al., 1979b). HUFA, particularly eicosapentaenoic acid (20:5 n-3; EPA) and docosahexaenoic acid (22:6 n-3; DHA), are vital in the maintenance of normal cell function; EPA and DHA are essential compounds required for cell membrane formation, osmoregulation, the synthesis of prostaglandin and they also appear to have an activating role in the immune system (Leger & Sorgeloos, 1992). Therefore, diets for penaeids must contain sufficient supplies of these essential nutrients.

Production of penaeid shrimp postlarvae relies heavily on the brine shrimp Artemia as the main live food organism used in commercial hatcheries (Sorgeloos et al., 1998; Wouters et al., 2009; Cobo et al., 2015). Although from a hatchery management standpoint the use of Artemia presents several advantages, the most important being easiness of storage and use (Leger & Sorgeloos, 1992), levels of n-3 HUFA in newly hatched Artemia nauplii are either low or greatly variable depending on origin (Lavens & Sorgeloos, 1996; Figueiredo et al., 2009). Since Artemia is a non-selective filter feeding organism, enhancement of n-3 HUFA levels is achieved through enrichment techniques, by which n-3 HUFA rich compounds are provided to Artemia and consequently increase their nutritional value (Sorgeloos et al., 1998; Wouters et al., 2009).

Previous studies have shown that feeding n-3 HUFA rich diets results in improved survival, growth and/or stress tolerance of several crustacean species (Tackaert et al., 1989; Rees et al., 1994; Cavalli et al., 2000; Chim et al., 2001; Martins et al., 2006; Immanuel et al., 2007; Sui et al., 2007; Jinbo et al., 2013). Nonetheless, few studies have considered the effects of the nutritional quality of larviculture diets on further shrimp performance. In this study, we assessed whether the subsequent growth of F. paulensis postlarvae during nursery rearing would be affected by previously feeding n-3 HUFA enriched Artemia during the larviculture period.


Farfantepenaeus paulensis larvae were obtained from a routine larviculture at the Marine Aquaculture Center, Universidade Federal do Rio Grande, Brazil. Upon reaching mysis I, larvae were individually counted and transferred to triplicate 200 L larviculture tanks. Aeration was provided by four air stones per tank to maintain dissolved oxygen levels above 5.0 mg [L.sup.-1]. Seawater was previously filtered by a 5 [micro]m cartridge filter, and water renewal rate was 80% per day. Temperature was maintained at 26-27[degrees]C with submerged thermostatic heaters. Photoperiod regime was natural and the diurnal cycle lasted from sunrise at 06:20 h and sunset at 19:00 h over the course of the experiment. Shrimp were reared at a density of 55 larvae [L.sup.-1]. After their transference to the tanks, larvae were fed solely Artemia according to the experimental design. For the control group (CG), larvae were fed newly hatched Artemia nauplii, whilst in the enriched group (EG) larvae were fed Artemia enriched with a commercial emulsion containing over 400 mg [g.sup.-1] n-3 HUFA on a dry weight basis (Super SELCO[R], INVE Aquaculture, USA).

Enrichment procedures were performed according to Sorgeloos et al. (1998) in 50 L cylindro-conical tanks. Density of Artemia during enrichment varied between 100-300 ind [L.sup.-1], temperature was kept between 25-28[degrees]C and strong aeration was provided to guarantee homogeneous distribution of the emulsion and dissolved oxygen levels above 5 mg [L.sup.-1]. Artemia were enriched for 24 h with two doses of 300 mg of emulsion per liter added at 12 h intervals. After enrichment, Artemia were rinsed with water over a 120 [micro]m sieve to remove any remaining emulsion.

Larvae were fed the Artemia diets twice a day (10:00 and 22:00 h). Artemia used for the night feeding were stored at 4[degrees]C. Artemia were offered at an initial density of 2 [mL.sup.-1], which increased gradually to 8 [mL.sup.-1] at the end of the trial. Before daily water renewal, the number of remaining Artemia was estimated in each tank and increased as needed. These procedures were performed until PL8 (eight day-old postlarvae). At this point groups of PL8 from both groups were exposed to salinity and ammonia stress tests.

The salinity and ammonia stress tests were based on the static toxicity tests proposed by Greenberg et al. (1992). The tolerance to salinity and total ammonia were assessed separately in triplicate sets of plastic beakers containing 1 liter of water that were immersed in a water bath at 27-28[degrees]C. For the salinity stress test, thirty PL8 from each group were exposed for 24 h to a control (salinity 30 g [L.sup.-1]) and to decreasing salinity levels (24, 18, 12, 6 and 0 g [L.sup.-1]), while for the ammonia test batches of 30 PL8 from each group were transferred to the beakers and exposed during 24 h to increasing concentrations of total ammonia: 0 (control, no added ammonia), 15, 30, 45, 60 and 90 mg [L.sup.-1]. Ammonia concentrations, which were based on previous studies with F. paulensis (Ostrensky & Wasielesky, 1995; Martins et al., 2006), were added to the beakers immediately after stocking the postlarvae. During both stress tests, postlarvae were not fed and no water was exchanged. After 24 h postlarvae not responding to mechanical stimuli were considered dead and counted. Based on the mortality rates, the mean lethal salinity for 50% of the population (LSso) and the mean lethal ammonia concentration for 50% of the population ([LC.sub.50]) were estimated with the Trimmed Spearman Karber Method (Hamilton et al., 1977).

PL8 remaining in the larviculture tanks were divided into groups of 300 shrimp and further reared for 40 days. The enrichment group (EG) had three replicated groups, while the control had four replicates. Shrimp were initially reared indoors for 10 days and were gradually acclimated to the salinity 15 using the methodology proposed by Tsuzuki et al. (2000). Upon reaching PL18, they were transferred to PVC-coated polyester cages (bottom area of 1 [m.sup.2], mesh size of 1.5 mm) placed outdoors in an estuarine inlet of Patos Lagoon (32[degrees]03'55"S, 52[degrees]12'30"W), southern Brazil. During both the indoor and outdoor rearing periods and irrespective of experimental treatment, management and feeding procedures were similar among all shrimp groups. Shrimp were fed ad libitum once a day in the late afternoon with a commercial nursery diet (CR2 Camaronina, Purina[R], Brazil). At least 30 shrimp from each cage were randomly sampled for individual weight measurements on days 25 and 40. At the end of the trial shrimp remaining in each cage were hand counted to determine survival.

Temperature (mercury thermometer, precision [+ or -] 0.5[degrees]C), salinity (Atago[R] optical refractometer, Japan, [+ or -] 1.0 g [L.sup.-1]), pH (Digital pHmeter HandyLab 2BNC Schott, Germany) and dissolved oxygen (Digital oximeter Handylab OXI/SET, Schott, Germany) were recorded daily. Every morning, samples were collected to estimate the concentrations of ammonia (UNESCO, 1983) and nitrite (Bendschneider & Robinson, 1952).

Samples of newly hatched Artemia nauplii, enriched Artemia and postlarvae were washed with distilled water and frozen (-20[degrees]C) until analysis. After defrosting, samples were again washed and prepared for analysis. Crude lipids were extracted with a mixture of chloroform/methanol (2:1, v/v) as described by Folch et al. (1957). Fatty acids of the Artemia and shrimp were prepared from crude lipid by saponification with KOH (50%). Fatty acid methyl esters (FAME) were prepared by esterification with boron-trifluoride in methanol (7%) according to Metcalfe & Schmitz (1961). FAME were separated by gas-liquid chromatography on Shimadzu GC-15A (Shimadzu Corporation, Japan) equipped with a flame ionization detector (FID) and fitted with a fused silica capillary column Omegawax 320x30x0.32 mm (Supelco Inc., USA). Hydrogen was used as a carrier gas with a flow rate of 4.0 mL [min.sup.-1]. Injector and detector temperatures were programmed to 240 and 250[degrees]C, respectively. Column temperature was programmed to be isothermal (205[degrees]C). FAME were identified by means of reference standard n-3 PUFA, menhaden fish oil (4-7085-U; Supelco Inc., USA) and quantified with a Shimadzu C-R4A integrator model (Shimadzu Corporation, Japan).

Significant differences (P < 0.05) of survival and final weight at the end of the larviculture and nursery rearing periods were determined using the t-test. Prior to the analysis of survival, data were arcsine-square root transformed. All tests were conducted after the confirmation of homogeneity of variances (Levene's test) and normality distribution of data (KolmogorovSmirnov's test). Differences on the ammonia ([LC.sub.50]) and salinity ([LS.sub.50]) stress tests were graphically determined through the comparison of 95% confidence intervals (Greenberg et al., 1992).


Mean values of temperature, salinity, dissolved oxygen, pH ammonia and nitrite during the larviculture period were 27.0[degrees]C, 32 g [L.sup.-1], 7.7 mg [L.sup.-1], 8.0 mg [L.sup.-1], 0.24 mg TAN [L.sup.-1] and 0.01 mg N-N[O.sub.2] x [L.sup.-1], respectively. No significant differences in any of these parameters were detected between EG and CG. Final weight of PL8 was significantly higher in EG (13 [+ or -] 7 mg) than in CG (10 [+ or -] 4 mg). The [LS.sub.50] values and their 95% confidence intervals for EG and CG were 18.93 g [L.sup.-1] (18.25-19.57) and 20.53 g [L.sup.-1] (19.74-21.26), respectively. Graphical comparison indicates significant differences between groups (Fig. 1). Similarly, mean lethal concentrations of total ammonia ([LC.sub.50]) were also significantly different (Fig. 1).

Water temperature and salinity during nursery rearing in the cages were 28.5[degrees]C (range 24-32[degrees]C) and 14.7 g [L.sup.-1] (range 13-17), respectively. After the end of the nursery rearing, mean ([+ or -] SD) survival of shrimp were 82.5% ([+ or -] 14.8) and 71.5% ([+ or -] 21.5) for EG and CG, respectively, and no significant differences were detected. Differences in weight were highly significant (P = 0.00002) after 15 days of cage rearing (Fig. 2). EG shrimp weighed 0.176 g ([+ or -] 0.03), while those from CG weighed 0.109 g ([+ or -] 0.02). After 40 days, significant differences (P = 0.0001) in shrimp weight persisted, with mean final weights of 1.082 g ([+ or -] 0.118) for EG and 0.896 g ([+ or -] 0.128) for CG, respectively (Fig. 2).

The fatty acid profiles of newly hatched Artemia nauplii and enriched Artemia presented significant differences (Table I). Although no significant differences were observed for saturated, monounsaturated and n-6 PUFA, the levels of EPA and DHA, and consequently total concentration of n-3 HUFA, were significantly higher (P = 0.000012) in the enriched Artemia than in newly hatched nauplii. As a result the n-3/n-6 relation was significantly higher (P = 0.000001) in the enriched Artemia. In contrast, newly hatched nauplii had higher levels of linolenic (18:3 n3) and stearidonic (18:4 n-3) acids.

Overall, fatty acid profile of F. paulensis postlarvae (Table 2) reflected the composition of their prey. Postlarvae fed enriched Artemia (EG) presented higher levels of n-6 PUFA and n-3 HUFA than postlarvae fed newly hatched nauplii (CG). Concentrations of arachidonic acid (ARA; 20:4n-6), EPA and DHA were higher in EG, while postlarvae fed newly hatched Artemia had significantly higher levels of linolenic and stearidonic acids.


As expected, the fatty acid composition of Artemia was influenced by enrichment, which, in turn, affected the composition of the larvae that fed upon them. Accordingly, higher n-3 HUFA levels, particularly EPA and DHA, were found in the tissues of postlarvae fed enriched Artemia in comparison to those fed newly hatched Artemia. Postlarvae fed enriched Artemia also presented higher weight at the end of the larviculture period. Although this corresponds well with previous findings demonstrating the positive effect of dietary n-3 HUFA in the enhancement of larval growth and development (Leger & Sorgeloos, 1992; Rees et al., 1994; Cavalli et al., 2000; Palacios et al., 2004; Immanuel et al., 2007), it disagrees with studies where no effect of n-3 HUFA enriched Artemia were observed in the size of P. monodon (Rees et al., 1994) and F. paulensis postlarvae (Pontes & Andreatta, 2003) or where a negative relationship between dietary n-3 HUFA levels and postlarval length was observed (Martins et al., 2006). Differences between these studies may be due to various causes, including variations in experimental design, species, feed management, composition of the emulsions, postlarval size and age, or duration of the experimental period.

One practical advantage of producing larger postlarvae is that they are knowingly more stress tolerant (Charmantier et al., 1988; Dall et al., 1990; Samocha et al., 1998; Tsuzuki et al., 2000). In other words, larger and older postlarvae are better prepared not only to deal with the stress involved in the transference to growout units, but also to cope with possible variations in environmental variables such as low salinity levels (Samocha et al., 1998; Tsuzuki et al., 2000).

A positive effect of the provision of dietary n-3 HUFA to crustaceans is that it often results in higher stress tolerance (Tackaert et al., 1989; Dhert et al., 1992; Rees et al., 1994; Cavalli et al., 2000; Chim et al., 2001; Palacios et al., 2004; Immanuel et al., 2007; Sui et al., 2007). It is therefore recognized that penaeids fed n-3 HUFA deficient diets generally express a low tolerance to stress (Chim et al., 2001; Palacios & Racotta, 2007). In the present study, comparison of the salinity ([LS.sub.50]) and ammonia tolerance ([LC.sub.50]) of 8 day-old postlarvae fed enriched or newly hatched Artemia indicated pronounced differences. The estimated [LS.sub.50] values for salinity were consistently higher for postlarvae fed enriched Artemia. Similarly, a higher tolerance to total ammonia was observed in postlarvae fed enriched Artemia. All this confirms the superior ability of the animals fed n-3 HUFA enriched Artemia to cope with adverse environmental conditions. Similar to the present findings, Tackaert et al. (1989) and Immanuel et al. (2007) verified that P. monodon postlarvae fed n-3 HUFA enriched Artemia had higher survival when exposed to a range of salinity levels in comparison to postlarvae fed unenriched Artemia, while Chim et al. (2001) demonstrated that feeding higher n-3 HUFA levels increased the cellular membrane resistance of Litopenaeus stylirostris which increased the tolerance to abrupt salinity changes. The beneficial effects of n-3 HUFA on tolerance to salinity stress may also be related to changes in the arrangement of fatty acids in the gill membrane and the consequent increase in shrimp osmosis capability (Palacios et al., 2004). Furthermore, shrimp fed n-3 HUFA rich diets have larger gill area (Palacios et al., 2004), which concurs with the more ramified gill structure reported in n-3 HUFA fed P. monodon postlarvae (Rees et al., 1994).

Although stress tests have been commonly used as a tool to compare the quality of crustacean larvae and juveniles in terms of tolerance to a number of physical and chemical parameters (Tackaert et al., 1989; Samocha et al., 1998; Cavalli et al., 2000; Chim et al., 2001; Alvarez et al., 2004; Palacios & Racotta, 2004; Martins et al., 2006; Immanuel et al., 2007; Sui et al., 2007), to date few studies have attempted to correlate the results of stress tests with the posterior growth performance of shrimp. In this regard, Bauman & Jamandre (1990) reported that batches of P. monodon postlarvae that responded positively to a salinity stress test presented a comparatively superior growout performance in ponds. Alvarez et al. (2004) found a correlation between stress testing and the survival of Litopenaeus vannamei postlarvae during simulated stocking into growout units. These authors, however, were unable to correlate the results of the stress test to growth or survival during a two-month long growout period. Palacios & Racotta (2007) hypothesized that survival of postlarvae to salinity stress tests would be a short-termed phenomenon and thus not necessarily an adequate predictive criterion for longer performance. Results from the present study, however, indicate a possible relationship between survival in the stress tests (for both salinity and ammonia) and posterior growth of shrimp during nursery.

DOI: 10.3856/vol45-issue1-fulltext-2

Received: 25 April 2016; Accepted: 28 August 2016


This study was partially funded by the Brazilian Council for Scientific and Technological Development (CNPq) through a study grant to the first author. E.L.C. Ballester, W. Wasielesky Jr. and R.0. Cavalli are research fellows of this agency.


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Diana W. Mutti (1), Eduardo L.C. Ballester (2), Ricardo C. Martino (3) Wilson Wasielesky Jr. (1) & Ronaldo O. Cavalli (4)

(1) Universidade Federal do Rio Grande-FURG, Instituto de Oceanografia, Rio Grande, RS, Brazil

(2) Universidade Federal do Parana-UFPR, Campus Palotina, Palotina, PR, Brazil

(3) Fundacao Instituto de Pesca do Estado do Rio de Janeiro-FIPERJ Unidade de Tecnologia do Pescado, Rio de Janeiro, RJ, Brazil

(4) Universidade Federal Rural de Pernambuco-UFRPE

Departamento de Pesca e Aquicultura, Recife, PE, Brazil

Corresponding author; Ronaldo Cavalli (

Corresponding editor: Fernando Vega

Caption: Figure 1. Mean ([+ or -] 95% confidence interval) lethal salinities ([LS.sub.50] - left) and lethal concentrations of total ammonia ([LC.sub.50] right) for 50% of the population of Farfantepenaeus paulensis postlarvae (PL8) fed Artemia enriched with a commercial emulsion containing over 400 mg [g.sup.-1] of n-3 highly unsaturated fatty acids (EG) or newly hatched Artemia (CG). Superscript letters indicate significant differences.

Caption: Figure 2. Mean (PSD) weight (g) of the pink shrimp Farfantepenaeus paulensis reared for 30 days in cages and that were originally fed either Artemia enriched with a commercial emulsion containing over 400 mg [g.sup.-1] n-3 highly unsaturated fatty acids (dark) or newly hatched Artemia nauplii (light) during the larviculture period. Superscript letters indicate significant differences.
Table 1. Mean values ([+ or -] SE) of the main fatty acids
(% area) in Artemia enriched with a commercial emulsion
containing over 400 mg g-1 of n-3 highly unsaturated
fatty acids (EG) and newly hatched Artemia nauplii (CG).
(1) n-6 PUFA [greater than or equal to] 18:2 n-6, (2) n-3
HUFA [greater than or equal to] 20:3 n-3. EG:
enriched group, CG: control group. For each fatty acid,
values with different superscripts were significantly
different (P < 0.05).

Fatty acid                  EG                         CG

14:0              2.44 ([+ or -] 1.47)        4.67 ([+ or -] 6.13)
15:0              0.56 ([+ or -] 0.21) (b)    0.98 ([+ or -] 0.28) (a)
16:0             10.65 ([+ or -] 2.93)        9.06 ([+ or -] 2.02)
17:0              1.26 ([+ or -] 1.44)        1.39 ([+ or -] 1.09)
18:0              3.98 ([+ or -] 1.26)        3.27 ([+ or -] 1.45)
20:0              0.41 ([+ or -] 0.17) (a)    0.12 ([+ or -] 0.07) (b)
22:0              0.26 ([+ or -] 0.15) (a)    0.02 ([+ or -] 0.05) (b)
14:1              1.33 ([+ or -] 0.66) (a)    0.47 ([+ or -] 0.55) (b)
16:1n-7           4.08 ([+ or -] 0.93)        3.32 ([+ or -] 0.41)
18:1n-9          18.57 ([+ or -] 4.42)       13.62 ([+ or -] 5.77)
18:1n-7           3.32 ([+ or -] 2.82)        4.48 ([+ or -] 1.82)
20:1n-7+9+11      1.25 ([+ or -] 1.02)        0.75 ([+ or -] 0.25)
22:1              0.68 ([+ or -] 0.60) (a)    0.02 ([+ or -] 0.84) (b)
18:2n-6           5.53 ([+ or -] 0.43)        5.39 ([+ or -] 1.25)
18:3n-6           0.38 ([+ or -] 0.16) (b)    0.71 ([+ or -] 0.20) (a)
18:4n-6           0.52 ([+ or -] 0.11) (a)    0.17 ([+ or -] 0.20) (b)
20:2n-6           0.18 ([+ or -] 0.12)        0.16 ([+ or -] 0.13)

Fatty acid                  EG                         CG

20:3n-6           0.22 ([+ or -] 0.15)        0.34 ([+ or -] 0.23)
20:4n-6           1.13 ([+ or -] 0.16) (a)    0.70 ([+ or -] 0.18) (b)
16:3n-3           0.53 ([+ or -] 0.10)        1.50 ([+ or -] 1.26)
18:3n-3          15.76 ([+ or -] 6.28) (b)   31.32 ([+ or -] 1.67) (a)
18:4n-3           2.67 ([+ or -] 1.24) (b)    6.79 ([+ or -] 2.15) (a)
20:3n-3           0.43 ([+ or -] 0.12)        0.43 ([+ or -] 0.41)
20:4n-3           0.60 ([+ or -] 0.08)        0.55 ([+ or -] 0.32)
20:5n-3           6.66 ([+ or -] 0.88) (a)    1.62 ([+ or -] 0.22) (b)
22:5n-3           0.86 ([+ or -] 0.31) (a)    0.02 ([+ or -] 0.04) (b)
22:6n-3           5.52 ([+ or -] 2.27) (a)    0.08 ([+ or -] 0.11) (b)
[SIGMA]          19.56 ([+ or -] 5.36)       19.52 ([+ or -] 3.87)
[SIGMA] Mono     29.70 ([+ or -] 3.75)       22.78 ([+ or -] 6.78)
n-6 PUFA (1)      8.61 ([+ or -] 0.89)        7.47 ([+ or -] 1.62)
n-3 HUFA (2)     14.07 ([+ or -] 2.88) (a)    2.71 ([+ or -] 0.88) (b)
dha/epa           0.84 ([+ or -] 0.35) (a)    0.05 ([+ or -] 0.06) (b)
n-3/n-6           1.63 ([+ or -] 0.26) (a)    0.36 ([+ or -] 0.07) (b)

Table 2. Main fatty acids (% area) in Farfantepenaeus
paulensis postlarvae fed Artemia enriched with a commercial
emulsion containing over 400 mg [g.sup.-1] n-3 highly
unsaturated fatty acids (EG) and newly hatched Artemia
nauplii (CG). (1) [SIGMA] (n-6) [greater than or equal to]
18:2 n-6. (2) [SIGMA] (n-3) [greater than or equal to] 20:3 n-3.

Fatty acid                     EG      CG

14:0                           9.78    7.10
15:0                           0.58     0.0
16:0                          12.67   10.22
17:0                           0.76     1.3
18:0                           3.86    3.78
20:0                           0.21     0.0
22:0                           0.25     0.0
14:1                           1.25     0.0
16:1 n-7                       4.03    3.41
16:1 n-9                        0.0     0.0
18:1 n-9                      11.32   14.12
18:1 n-7                       3.83    5.21
20:1 n- 7+9+11                 1.29    1.26
22:1                           0.43     0.0
18:2 n-6                       8.77    7.56
18:3 n-6                       0.23     0.0
18:4 n-6                       0.33    1.47

Fatty acid                     EG      CG

20:2 n-6                       0.35     0.0
20:3 n-6                       0.31     0.0
20:4 n-6                       1.53     0.0
16:3 n-3                       0.55     0.0
18:3 n-3                      12.80   31.25
18:4 n-3                       1.90    5.74
20:3 n-3                       0.22     0.0
20:4 n-3                       0.56     0.0
20:5 n-3                       7.84    3.67
22:5 n-3                       0.72     0.0
22:6 n-3                       3.57    1.51
[SIGMA] Saturated             28.11   22.40
[SIGMA] Monounsaturated       22.15   24.00
[SIGMA] (n-6) PUFA (1)        12.09    9.03
[SIGMA] (n-3) HUFA (2)        12.91    5.18
dha/epa                        4.96    0.41
[SIGMA] (n-3)/[SIGMA] (n-6)    1.07    0.57
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Title Annotation:Research Article
Author:Mutti, Diana W.; Ballester, Eduardo L.C.; Martino, Ricardo C.; Wasielesky, Wilson, Jr.; Cavalli, Ron
Publication:Latin American Journal of Aquatic Research
Date:Mar 1, 2017
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