Biological viability of producing white shrimp Litopenaeus vannamei in seawater floating cages

Aquaculture 259 (2006) 283 – 289 www.elsevier.com/locate/aqua-online

Biological viability of producing white shrimp Litopenaeus vannamei in seawater floating cages Martha Zarain-Herzberg a,⁎, Angel I. Campa-Córdova b , Ronaldo O. Cavalli c a Centro de Ciencias de Sinaloa, Apdo. Postal 1889, Culiacán, Sinaloa, 80010, México Unidad de Patología Marina, Centro de Investigaciones Biológicas del Noroeste, La Paz, Baja Califórnia Sur, 23000, México Laboratório de Maricultura, Departamento de Oceanografia, Fundação Universidade Federal do Rio Grande, C.P. 474, 96201-900, Rio Grande, R. S. 054545, Brazil b

c

Received 1 February 2006; received in revised form 15 May 2006; accepted 18 May 2006

Abstract In the last few years, in an attempt to foment the controlled culture of penaeid shrimp by artisanal fishermen communities, an innovative culture technology using floating cages have been developed in Brazil. In this work, we assessed the biological viability of culturing the Pacific white shrimp Litopenaeus vannamei in floating cages at different stocking densities in Santa María's Bay, México. Additionally, the influence of artificial substrates on growth performance of the shrimp was analyzed. Cages made of PVC-coated polyester mesh supported by wooden poles and PVC tubes were used for this study. Post larvae (PL) were stocked in four nursery cages at 700 PL per m2. After 30 days of nursery culture, shrimp had reached an average weight of 0.5 g and were then transferred to grow out cages at densities of 100, 150, and 200 shrimp per m2, with and without the addition of artificial substrates. Survival rate was neither affected by stocking density nor by the presence of added artificial substrates. In contrast, final shrimp weight was higher for those reared at low densities (100 shrimp per m2) and the use of artificial substrates showed a positive effect on final shrimp weight. After 2 months of culture survival rate was above 90%, the shrimp weight ranged from 6.94 ± 1.51 g to 9.33 ± 1.48 g and yields varying from 818 to 1297 g/m2 were recorded. The high shrimp production in floating cages was probably due to optimum environmental and rearing conditions provided to the shrimp. The present results confirmed the deleterious effect of high stocking density on shrimp growth, demonstrated the benefits of adding artificial food substrates to the cages, and proved the biological viability of culturing L. vannamei in seawater floating cages in México. © 2006 Elsevier B.V. All rights reserved. Keywords: Penaeid; Shrimp; Floating cages; Mariculture; Litopenaeus vannamei

1. Introduction

⁎ Corresponding author. Avenida de las Américas 2271 Norte, Culiacán Sinaloa, 80010, México. Tel.: +52 667 7599000; fax: +52 667 7599019. E-mail address: [email protected] (M. Zarain-Herzberg). 0044-8486/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2006.05.044

World production of fish for human consumption has reached its highest level ever (FAO, 2002). Nevertheless, it has been estimated that approximately 47% of the main marine species captured are now fully exploited, and their sustainability is in jeopardy (FAO, 2002), unless new sources and technologies to produce sea food are found. In the state of Sinaloa, México, near shore and

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open sea shrimp captures have declined dramatically in the past few years (SAGARPA, 2002), which has seriously affected the socio-economic situation of artisanal fishermen communities. Shrimp culture in floating cages is now being considered as an alternative approach to aquaculture that may prove to be a sustainable source of shrimps, as well as a valuable source of income for these communities. In México, shrimp farming in ponds is an industrial activity, mainly. This activity is performed by about 800 shrimp farms, which occupy around 15,500 m3 of water (SAGARPA, 2002). They work with external funding and they have to face the issue of land owning, which is a severe problem. The fishermen who work in the shrimp farms do not benefit fully of the activity because they are not partners or owners of the farms. On the other hand, the work model of shrimp culture in cages is designed to suit artisanal developments that are settled at concessioned waters for the fishing industry. During the last decade, experimental work has been focused to develop innovative shrimp culture technology using floating cages has been undertaken in Brazil (Wasielesky et al., 1995, 2001, 2003; Paquotte et al., 1998; Lombardi et al., 2001b; Cavalli and Wasielsky, 2003). Rearing shrimp in floating cages has several advantages over conventional pond-based shrimp culture methods, that include higher water flow rate (that removes toxic nitrogenous metabolites and provides oxygen) and an enhanced use of the natural productivity, which, compared to conventional pond culture, usually results in lower production costs (Yusufzai and Sing, 2005). Furthermore, this alternative culture system requires lower financial investment and its management is easier, allowing fishermen to maintain their original way of living (Wasielesky et al., 2003), besides it has a positive social impact. The operation of this system is ideal for studying the effect of the interaction between cultured shrimp in terms of increasing the total production per area, which will certainly improve economic returns, and expand mariculture to open sea (Lombardi et al., 2001a; Liti et al., 2005). Culture systems in open seawaters, as is the case for shrimp cage culture, discharge their nutrient rich waste (faeces and uneaten food) directly into the water and could cause increase in trophic stages. In order to avoid the adverse effects of this type of culture system, it is necessary to introduce better management practices (CBD, 2004), principally: a) proper site selection with good water circulation, b) proper feeding to decrease conversion ratios, and c) culturing together different species (polyculture) in separated culture areas, or in independent cages. (Lombardi et al., 2001a,b; Read and Fernandez, 2003; Neori et al., 2004).

For rearing activities in earth ponds, solid organics waters (faeces and unconsumed feeds) settling on the sediment accumulates with time (Boyd, 1992; Hopkins et al., 1994; Arulampalam et al., 1998; Schneider et al., 2005). In contrast, in the case of rearing cages located in running waters, solid waste does not accumulate near the cages. In addition, the process of oxygenation of the sediment due to the sea tide and currents may also be sufficient to allow a quick degradation of organic matter and to compensate either the shrimp and the plants (macrophytes, phytoplankton) respiration, so there is no significant accumulation of organic matter or drastic decrease of oxygen and the shrimps are in very good rearing conditions, since they are not in contact with organic wastes (Paquotte et al., 1998). In Brazil, successful culture of Farfantepenaeus paulensis and Litopenaeus vannamei in floating cages has been tested at different stocking densities (Wasielesky et al., 2002, 2003; Cavalli and Wasielsky, 2003; Lemos, 2003; Lombardi et al., 2003; Neves et al., 2003). It has been demonstrated the positive role of the biofilm (community of microorganisms associated with organic material) attached to submerged artificial substrates in increasing the availability of natural food items (Thompson et al., 2002; Ballester et al., 2003; Bruce et al., 2003; McNeil, 2003a,b). In this work, we assessed the biological viability of the Pacific white shrimp L. vannamei reared in seawater floating cages at different stocking densities, as well as the influence of artificial substrates placed within the cages on shrimp survival, growth and food conversion efficiency. 2. Materials and methods This study was performed in Santa María's Bay, State of Sinaloa, México (25° N, 108.3° W). This bay has an area of about 50,000 ha; an average depth of 3 m (maximum 20 m), good seawater exchange with the Gulf of California, México, it has high natural productivity and it is naturally protected from sea storms. The hydrological variables present in this bay, reported by Galindo Reyes (2000) provide ideal conditions for shrimp culture (Boyd, 2001). Water entries in to the system are about 16,509 millions m3/year, and the water exits produced by evaporation constitute 844 millions m3/year. The system presents a parameter of nitrogen fixation of 831 g/m2 and a primary production of about 1273 g C/m2/year. Cages were made of PVC (polyvinyl chloride)-coated polyester nets (Sansuy, São Paulo, Brazil) with the

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cated broodstocks, and stocked in four nursery cages at 700 PL per m2, without artificial substrate. Shrimp growth started to be recorded from day 20th, and was registered every week, 30 to 50 shrimp were randomly sampled, weighed, and returned to their cages until shrimp reached 0.5 g average weight. During the nursery phase, shrimp were supplemented with a commercial pellet from maltaCleyton Api camaron blanco 1 (40% protein) at 5% of their estimated biomass, provided in feeding trays, attached to the cages. 2.2. Grow out culture

Fig. 1. Growth curve of L. vannamei post larvae (PL 13) stocked at 700 PL/m2, reared for 65 days in floating cages. The grow out is the mean weight values of juveniles grown at densities of 100, 150 and 200 shrimp per m2.

following dimensions 3 m long × 2 m wide and 1.2 m deep; an effective volume of 9 m3 was used. A two phase (nursery and grow out) rearing system was set. Four cages 1.5 mm mesh opening, were used for nursery, while six cages (5 mm mesh) were used for grow out. Cages were supported with steel bars attached to a wooden framework suspended over 6 m long PVC tubes sealed at both ends. Each module contained two cages, which were joined to the next module by ropes. Cages were anchored in Santa María's Bay waters. 2.1. Nursery culture The experiment lasted from June to August, 2003 because of the presence of hurricane Ignacio in Mexican coasts. Shrimp (L. vannamei) post larvae (PL 13) with a mean weight of 5 ± 1.0 mg were obtained from the local hatchery Laboratorios Marinos working with domesti-

When juvenile shrimp reached an average weight of 0.5 g, they were individually counted and transferred to grow out cages at three stocking densities: 100, 150, and 200 shrimp per m2. Each condition was done in duplicate cages. In order to increase the internal cage area and hence to create favorable conditions for biofilm to grow, one set of grow out cages was supplied with two vertical polystyrene nets of 1 × 1 m, and 1 mm mesh opening, thus increasing the area of the cages by 2 m2 (total effective area of 11 m2). These nets were suspended transversally by 1-inch PVC tube joined to both ends of the cages. During the grow out experiment, shrimp were fed twice at day with commercial pellets from maltaCleyton Api camaron blanco 2 (40% protein) provided in feeding trays at a ratio of 5% shrimp biomass. Every 10 days, 30 to 50 shrimp growing in the cages were randomly sampled, weighed, and returned to their cages. At the end of the experiment, the survival rate was calculated individually by counting the total number of shrimp in each cage. Water quality parameters were recorded daily inside the cages at sunrise and sunset using the following instruments or methods: temperature with a mercury thermometer; salinity with a refractometer (Sper Scientific 300011); pH with a laboratory pH meter (Hanna HI98128); dissolved oxygen with an oxygen meter (YSI

Table 1 Weekly mean values of water quality parameters measured at sunrise and sunset within the cages during the nursery and grow out period Days

7

14

21

38

35

42

49

56

63

Mean

DO (mg/L) am DO (mg/L) pm Temperature (C) am Temperature (C) pm Salinity (ppt) pH am pH pm NH3–N(mg/L)

5.0 6.5 29.5 31.1 30 8.0 8.1 0.04

5.4 7.4 29.5 31.2 32 8.2 8.2 0.11

5.6 7.2 30.1 31.4 33 8.2 8.2 0.19

5.5 7.2 30.2 32 35 8.2 8.2 0.0

4.8 7.3 30.5 31.6 39 8.3 8.4 0.19

5.6 7.2 30.5 31.8 35 8.6 8.6 0.19

5.0 7.1 31.2 32.3 36 8.2 8.2 0.19

5.4 6.8 31.2 32.6 35 8.3 8.4 0.19

5.9 7.0 30.1 31.6 38 8.6 8.6 0.19

5.4 ± 0.35 7.1 ± 0.3 30.3 ± 0.7 31.7 ± 0.5 34.8 ± 2.8 8.3 ± 0.19 8.4 ± 0.12 0.14 ± 0.07

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Table 2 Final weight (g), food conversion rate (FCR), biomass (g/m2) and survival rate (%) of Litopenaeus vannamei reared in floating cages at different stocking densities (100, 150, 200 shrimp/m2) in presence or absence of artificial food substrates Stocking density (shrimp/m2) 100

Weight (g) FCR Biomass (g/m2) Survival (%)

150

200

100

150

200

No artificial substrate

With artificial substrate

8.71a ± 1.70 0.72 818

7.13b ± 1.38 0.72 970

7.02b,c ± 1.15 0.98 1220

9.33a ± 1.48 0.76 883

8.37a ± 1.10 0.78 1132

6.94b,c ± 1.51 0.79 1297

94

91

87

95

91

94

Data with different super scripts letters (a,b,c) are significantly different (P < 0.05).

model 55); and ammonia-nitrogen (NH3–N) with the indophenol method (Grasshoff, 1976). 2.3. Statistical analysis Results were analyzed by one-way analysis of variance (ANOVA) using the Tukey test to analyze the differences (STATISTICA software), values were considered significantly different at P < 0.05.

Fig. 3. Average weight of L. vannamei juvenile reared at different stocking densities (100, 150 and 200 shrimp per m2) during 35 days in floating cages with artificial substrate. For each time period, means with different letters above the bars indicate significant differences (P < 0.05).

total body weight of the shrimps in cages increased from 50% to 80%/day. Salinity, pH, temperature, dissolved oxygen, and ammonia levels did not vary significantly between the different cages during the nursery and grow out period (Table 1). Also, probably due to the high and stable temperature level (30 to 32 °C) during the experimental period, shrimp grew faster during the nursery phase. 3.2. Grow out

3. Results 3.1. Nursery After 30 days of nursery rearing, overall survival rate was 90% and mean weight was 0.51 ± 0.09 g (Fig. 1). The estimated growth rate obtained by measuring the

Fig. 2. Average weight of L. vannamei juvenile reared at different stocking densities (100, 150 and 200 shrimp per m2) during 35 days in floating cages without artificial substrate. For each time period, the mean values indicated with different letters above the bars indicate significant differences (P < 0.05).

After 35 days of grow out culture, the mean weight of shrimp reared at different densities, with and without artificial substrates, varied from 6.94 ± 1.51 g to 9.33 ± 1.48 g (Table 2), which gave shrimp yields ranging from

Fig. 4. Final average weight of L. vannamei reared during 35 days in floating cages at different stocking densities (100, 150 and 200 shrimp per m2) with and without artificial substrates. Mean values with different letters are significantly different (P < 0.05).

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818 to 1297 g/m2 of cage surface area. Survival rates varied between 87% and 94%; whereas food conversion rate (FCR) was low (1.0:1) in every experimental condition (Table 2). The different growing conditions tested had no effect on survival and FCR. Independent from the presence of artificial substrates, stocking density did not significantly affect the mean weight of shrimp (P > 0.05) during the first 10 days of grow out (Figs. 2 and 3). However, on day 20 and onwards, juvenile shrimp reared at a density of 100 shrimp per m2 showed a significantly higher weight (P < 0.05), compared to those reared at densities of 150 and 200 shrimp per m2. The results of this study, suggest a trend towards increase shrimp weight in the presence of artificial substrates (nets), although no significant (P > 0.05) effect of the addition of artificial substrates was detected among shrimp reared at stocking densities of 100 and 200 shrimp per m2. Nevertheless, for shrimp reared at 150 shrimp per m2, a significantly (P < 0.05) higher weight was observed for shrimp reared in the presence of artificial substrates (Fig. 4), suggesting a beneficial effect of an artificial substrate supplementation. 4. Discussion In this study we demonstrate that seeding density of 700 post larvae per m2 of L. vannamei on the nursing cages has a favorable outcome in shrimp growth and survival, with superior densities in 40% to the ones experimented by Paquotte et al. (1998). After 30 days of nursery, juvenile shrimp registered an average weight of 0.5 g with a survival rate close to 90%, similar to results reported by Lombardi et al. (2003). Although in the present study we used higher stocking density in the floating cages, direct comparison with other studies is difficult because of differences in initial size and stocking densities of the post larvae. Nevertheless, results obtained in our study indicates that post larvae can reach a weight of about 0.5 g at higher stocking densities, similar results are reported by Aquacop et Garen (1992), which can be directly stocked in the grow out phase. The study reveals that floating cages can be successfully utilized as nursery or grow out system for L. vannamei post larvae at densities of 700 post larvae per m2 in shrimp ponds of the state of Sinaloa, México. The survival rates during grow out were not affected by the stocking density, but final shrimp weight was significantly higher for those reared at lower densities. The present study showed the negative effect of stocking density on shrimp growth but not on survival, similar to previous studies (Pérez-Rostro et al., 1999; Yusufzai and

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Sing, 2005). Although the present study is limited by the use of a small amount of cages (10 cages), the results obtained are very similar in yield and survival rate values, compared to a productivity study done by our group during the period March to July 2005, using 4420 floating cages in nine different estuaries of the state of Sinaloa (Zarain-Herzberg, 2006). The present results suggest that the inclusion of artificial substrates within cages had a positive effect on shrimp growth, particularly for those reared at 150 shrimp per m2. Recent results obtained by our group in a large scale study under progress, that is financed by the Mexican government confirmed these observations (data not shown). A positive effect of artificial substrates on shrimp growth was observed during the nursery rearing of Farfantepenaeus paulensis in indoor systems (Thompson et al., 2002) and in cages (Ballester et al., 2003). These authors also concluded that shrimp may benefit from feeding on the microorganisms present in the biofilm attached to these substrates, which is in accordance with the relatively low food conversion rates observed in the present study. This parameter is probably showing that primary productivity has a significant contribution in shrimp growth when shrimp population is daily fed with balanced food in a proportion equal to 5% of shrimp biomass. It is also important to note that the food has always administrated ad libitum. However, for higher densities it is possible that a more aggressive food program regime supplemented with artificial substrates is needed. Shrimp survival seems to be only affected by artificial substrates at highest density (200 shrimp per m2), because the artificial substrate reduced the effective density of shrimp by distributing them more evenly throughout the cages, as the stocking density increases, so does the effect of the artificial substrate (Lopez, 1997). Although overall growth rates during the first 20 days of the grow out phase were approximately 0.2 ± 0.04 g/ day, during the final 15 days of culture shrimp increased 0.3 ± 0.03 g/day. The late growth rate is 50% higher than the early growth rate, estimated for shrimp reared in earth ponds at similar stocking densities (Aquacop, 1987; Sandifer et al., 1991). For instance, shrimp reared in floating cages may take advantage of higher availability of organic particles, which have been associated with rapid growth of L. vannamei (Moss and Pruder, 1995; Schneider et al., 2005), or natural live food items (e.g. microalgae and zooplankton) rich in essential nutrients, such as omega-3 highly unsaturated fatty acids, which are known to play an important role on shrimp growth (D'Abramo, 1997; Tidwell et al., 1997), especially under intensive culture conditions. Otoshi et al. (2001) demonstrated that L. vannamei is able to compensate

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for nutritional deficiencies when reared in organically rich waters. Additionally, a comparatively higher water flow rate and a low presence of potential predators in floating cages may also explain these differences. Under the conditions of the present study, the high production of L. vannamei observed in floating cages in Santa María's Bay, Sinaloa, is probably due to the sum of optimum environmental and rearing conditions provided to the shrimp, which involves four parameters:1) substrate surface per shrimp, 2) stocking density, 3) natural sea water food (productivity) and 4) dry feed. In this study all these parameters affected weight gain and FCR more rather than survival rate. The present study also shows the deleterious effect of stocking density on shrimp growth, the benefit of adding artificial substrates, and the biological viability of culturing L. vannamei in seawater floating cages. Finally, from the socio economic point of view, shrimp culture in seawater floating cages may prove to be a sustainable activity that can provide work to Mexican fishermen and help to decrease the damage on the ecosystem done by the traditional fisheries. Acknowledgements Funds for this study were provided by a grant from SIMAC (CONACyT) 20020107501. R.O. Cavalli is a research fellow of CNPq (Proc. 302688/2003-0). Special thanks to Dr. Fausto Burgueño-Lomelí for providing experimental facilities and technical support. We express our appreciation to Dr. Angel Zarain-Herzberg for the critical reading of the manuscript. Thanks to CIBNOR editing staff. References Aquacop et Garen, 1992. Elevage intensif de crevettes peneids. Le point des techniques au COP. Rap.Interne COP.DRV/Aq/Tah. 92018,18p. Arulampalam, P., Yusoff, F.M., Shariff, M., Law, A.T., Rao, P.S.S., 1998. Water quality and bacterial population in a tropical marine cage culture farm. Aquac. Res. 29, 617–624. Ballester, E.L.C., Wasielesky Jr., W., Cavalli, R.O., Santos, M.H.S., Abreu, P.C., 2003. Influence of the biofilm on the growth of the pink shrimp Farfantepenaeus paulensis in nursery system. Atlantica 25 (2), 37–42. Boyd, C.E., 1992. Shrimp pond bottom soil and sediment management. In: Wyban, J. (Ed.), Proceedings of the Special Session on Shrimp Farming. World Aquaculture Society, Baton Rouge, LA, pp. 166–181. Boyd, C.E., 2001. Métodos para mejorar la camaronicultura en Centroamérica/tr. Emilio Ochoa Moreno, Primera edición. Editorial-Imprenta UCA, Managua, Nicaragua. 304 pp. Bruce, C., Bratvold, D., Browdy, C., 2003. Preliminary assessment of factors that may change shrimp production with AquaMats. Book

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