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Aquaculture xx (2006) xxx xxx www.elsevier.com/locate/aqua-online

Polyculture of Pacific white shrimp, Litopenaeus vannamei, giant oyster, Crassostrea gigas and black clam, Chione fluctifraga in ponds in Sonora, Mexico
Luis R. Martinez-Cordova , Marcel Martinez-Porchas
Departamento de Investigaciones Cientificas y Tecnologicas de la Universidad de Sonora, Rosales y Nios Heroes, Apdo Postal 1819, Hermosillo, Sonora, 83000, Mxico Received 12 October 2005; received in revised form 13 March 2006; accepted 14 March 2006

Abstract The feasibility of a polyculture of Pacific white shrimp, Litopenaeus vannamei, giant oyster, Crassostrea gigas, and black clam, Chione fluctifraga in earthen ponds, and its effect on water quality and production parameters, was assessed in a nine-months experimental study, conducted in Sonora Northwestern Mexico. Shrimp was stocked for two crops and mollusks for a single crop during the study. Two oyster densities (10 and 16/m2), two clam densities (8 and 10/m2) and one shrimp density (30/m2) were evaluated in the experiment. Total ammonium nitrogen and chlorophyll-a were significantly lower in the ponds with the highest combined density of mollusks. During the first crop, shrimp reached 12.6 to 14.88 g in 19 weeks from postlarvae of 10 days age (around 0.002 g), with a survival ranging from 48.3% to 63.1% and a yield from 1866 to 2665 kg/ha. During the second crop, the gain in weight, survival and yield of shrimp ranged from 12.23 to 13.26 g, 61.9% to 67.3%, and 2271 to 2677 kg/ha, respectively. Oyster mean weight increased between 40.2 to 50.1 g in 6 months, with a poor survival of 10.7% to 16.2% and a yield of 746 to 1014 kg/ha. Clams grew in a range from 13.3 to 14.0 g in the same period, with a survival of 45.5% to 50.2% and a yield of 617 to 793 kg/ha. It may be concluded that polyculture of these three species seems to be feasible and that the presence of mollusks in the ponds might not have an adverse but a beneficial effect on the productive performance of shrimp. Crassostrea gigas showed not to be a good prospect for this polyculture conditions but C. fluctifraga could be a good candidate. 2006 Elsevier B.V. All rights reserved.

1. Introduction Shrimp mariculture has achieved worldwide importance in recent years. Production has increased from about 208,000 tones in 1985 (FAO, 1996) to around

Corresponding author. Dictus, Universidad de Sonora, P.O. Box 1819, Hermosillo, Sonora, 83000, Mxico. Tel.: +52 662 2 59 21 69; fax: +52 662 2 59 21 96. E-mail address: lmtz@guaymas.uson.mx (L.R. Martinez-Cordova). 0044-8486/$ - see front matter 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2006.03.026

2,000,000 tones in 2004 (Rosenberry, 2004). At present, farmed shrimp represents more than 30% of total world shrimp production (FAO, 2003). This high production has led prices of shrimp to coming down in the last years. To compete today in the international shrimp market, it is necessary to develop the most efficient culture strategies to lower the costs as much as possible. One way to make a culture system profitable, would be to polyculture two or more organisms so that additional incomes can be obtained. Polyculture have a long tradition in Asian countries as China where shrimp and fishes have been farmed in ponds for many centuries (McLarney, 1976;

Martinez-Cordova, L.R. / Martinez-Porchas, M. 2006 Polyculture of Pacific white shrimp, Litopenaeus vannamei, giant oyster, Crassostrea gigas and black clam, Chione... AQUA-627018; No of Pages 6 Aquaculture, 258 (1), p.321-326.

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2 L.R. Martinez-Cordova, M. Martinez-Porchas / Aquaculture xx (2006) xxxxxx Table 1 Experimental design of the study Treatment Pond number Shrimp/pond Oysters/pond Clams/pond Control 2 3 4 5 1, 2, 3, 4, 5, 9, 13 7, 15 10, 12 6, 11 8, 14 12,000 12,000 12,000 12,000 12,000 0 5000 5000 8000 8000 0 4000 5000 4000 5000

Costa-Pierce et al., 1984). Polyculture of freshwater prawns and fishes is reported to be feasible in the USA (Buck et al., 1981; Malecha et al., 1981; Costa-Pierce et al., 1984). Ponds of shrimp in USA have been used to overwinter clams (Battey, 1988). Shpigel et al. (1996) cultures abalone, fish and clams in an intensive system. In Mexico shrimp and clams have been experimentally cultured with promising results (Martinez-Cordova et al., 1992). Hopkins et al. (1993) successfully polycultured oyster Crassostrea virginica and clam Mercenaria mercenaria in ponds of Litopeneaus vannamei. Lin et al. (1993) successfully farmed green mussel (Perna viridis) in waste water from an intensive shrimp pond. Bivalve filter feeders play a key role in many coastal ecosystems due to their high filtration capacity and culture density (Nunes et al., 2003). As filter feeders oysters and clams feed mostly on phytoplankton and suspended organic matter, both are normally found in high concentrations in shrimp ponds, as a result of fertilization and unconsumed feed (Chamberlain, 1988). Thus, filter feeders are able to take advantage of natural productivity and organic matter in the ponds to convert them in biomass, which represent an extra income to the farm. At the same time, they contribute to the control of the phytoplankton blooms which can be harmful in certain circumstances for the cultured organisms (Smith, 1985; Smith and Piedrahita, 1988; Shpigel and Blaylock, 1991). Mollusks also help to diminish organic matter in water column and sediment. This organic matter come mostly from unconsumed feed and at high levels may represent a serious problem in the ponds. Yokoyama et al. (2002) found that in a polyculture of the prawn Fenneropenaeus merguiensis and the mollusks Perna viridis, Nereididae sp. and Cerithideopsilla cingulata, most of the nutrients for the mollusks came from unconsumed shrimp feed. The co-production of two or more aquatic organisms may represent certain problems such as: competence for feed, oxygen and space; transmission of pathogens from one species to another, and labor costs may increase for handling and harvest of the species (Lutz, 2003). So, it is very important to select species in which these problems could be the minimum possible. In this study the shrimp L. vannamei and the mollusks C. gigas and Chione fluctifraga were farmed in combination to investigate the feasibility of their polyculture, and its effect on water quality of the ponds. 2. Materials and methods The experiment was conducted over 9 months in fifteen earthen ponds, with a water surface of 400 m2

(40 10 1 m), in the facilities of the University of Sonora at Bahia Kino, Northwestern Mexico. Before the beginning of the study, ponds were liming (40 kg CaCO3/pond) and fertilized with urea (2 kg/pond) and triple superphosphate (1 kg/pond). Fertilization regimen was repeated during the trial when water transparency was over 40 cm in the Sechi disk. A water exchange of around 5% was maintained during the trial. Each pond was stocked two times during the experiment with 12,000 postlarvae-(30 PL 15 days old/m2) of white shrimp L. vannamei, hatched in the facilities of the University of Sonora at Puerto Peasco, Sonora. Twelve of the ponds were also stocked with seeds of oysters C. gigas and clams C. fluctifraga. Oyster seeds were obtained from the laboratory of Aquaculture Institute of Sonora at Bahia Kino. Clam seeds were collected from La Cruz estuary in Bahia Kino, Sonora. Treatments consisted of four combined densities of oysters and clams with a constant density of shrimp, plus a control with only shrimp, as presented in Table 1. Treatments were randomly assigned by triplicate to the ponds . Oysters were stocked in Nestier cages (special cages for oyster culture), and clams were evenly distributed across the pond bottom. It has been previously demonstrated that C. gigas is better cultured of the bottom than on the bottom (Soletchnik et al., 2005). C. fluctifraga however, live naturally burrowed in the sediment (Martinez-Cordova, 1996). Densities of oysters and clams were decided in base to preliminary studies made by the author (unpublished). During the culture period shrimp were fed twice a day (08:00 and 14:00 h.) with Camaronina 25 (a formulated shrimp diet with 25% crude protein by Purina Mexico). Feeding rate was 10% of shrimp biomass per day for organisms from 0.5 to 1 g; 6% from 1 to 2 g and 3% for the rest of the study. Feed was supplied by hand throughout the ponds. Water quality parameters such as salinity, pH, and temperature were recorded once a day (15:00 h), and dissolved oxygen twice a day (06:00 and 15:00 Hs) in

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L.R. Martinez-Cordova, M. Martinez-Porchas / Aquaculture xx (2006) xxxxxx Table 2 Means SD of water quality parameters in a polyculture of shrimp and mollusks during the two shrimp crops Parameter First crop Temperature C (08:00 h) Temperature C (13:00 h) Salinity (ppt) pH Morning D.O. (mg/L) Afternoon D.O. (mg/L) TAN (mg/L) Chlorophyll-a mg/m3 TSS (mg/L) Second crop Temperature C (08:00 h) Temperature C (13:00 h) Salinity (ppt) pH Morning D.O. (mg/L) Afternoon D.O. (mg/L) TAN (mg/L) Chlorophyll-a (mg/m3) TSS (mg/L) Treatment 1 24.1 2.3a 29.8 1.9a 42.5 2.1a 7.9 0.12a 3.1 1.52a 5.6 1.82a 1.12 0.22b 9.32 1.09b 87.3 4.7b Treatment 2 24.1 2.2a 29.9 2.1a 42.0 2.1a 7.9 0.13a 3.0 1.46a 5.1 1.67a 0.87 0.21ab 8.12 0.97ab 79.1 3.2ab Treatment 3 24.2 2.3a 29.7 2.0a 42.3 2.0a 7.9 0.12a 3.1 1.51a 5.2 1.79a 0.81 0.19ab 7.81 1.06ab 77.7 3.2ab Treatment 4 24.0 2.1a 29.8 1.9a 42.3 2.2a 7.8 0.13a 3.0 1.47a 5.4 1.91a 0.74 0.17a 7.71 0.85a 73.6 3.4a Treatment 5 24.2 2.3a 29.9 2.1a 42.0 2.1a 7.8 0.11a 3.0 1.50a 5.4 1.79a 0.71 0.17a 7.34 0.79a 69.9 2.9a 3

23.3 1.9a 27.8 2.8a 41.5 1.91a 8.0 0.14a 3.4 1.29a 5.8 1.67a 1.09 0.21b 9.93 1.07b 56.6 2.7b

23.1 2.0a 27.9 2.6a 41.0 1.93a 8.0 0.13a 3.2 1.31a 5.3 1.69a 0.91 0.23ab 8.81 1.17ab 51.2 2.1b

23.3 2.0a 27.7 2.7a 41.3 2.00a 8.1 0.15a 3.5 1.33a 5.5 1.59a 0.82 0.21ab 8.91 1.03ab 49.2 2.9ab

23.2 1.9a 27.8 2.8a 41.3 1.96a 7.9 0.12a 3.3 1.27a 5.6 1.61a 0.79 0.16ab 7.34 0.91ab 43.1 1.9a

23.1 2.1a 27.9 2.6a 41.0 1.91a 7.9 12a 3.2 1.25a 5.7 1.59a 0.73 0.16a 7.19 0.99a 42.0 2.2a

Means in a column with different letters were significantly different at P b 0.05. TAN = Total ammonium nitrogen.

each pond, by means of an Atago S28E salinity refractometer, an Orion 230 pH meter, and a YSI 55 D oxygen meter with sensor for temperature. Total ammonium nitrogen (TAN) and chlorophyll-a were measured by spectrophotometry using a HACH DR4000 equipment. Total suspended solids (TSS), was measured filtering a water sample through GFC fiberglass filter, which was dried in an oven at 103 to 105 C. The increase in weight of the filter represents the total suspended solids. (Clesceri et al., 1998). Twenty five shrimp from each pond were sampled weekly and weighed individually in a digital Sartorious balance. Twenty five oysters and twenty five clams were measured weekly by a digital vernier (from umbo to the most distal part of the shell). They were also weighed individually in a digital Sartorious balance. Survival and yield of shrimp and mollusks were recorded at the end of the farming period by counting and weighing the harvested organisms. Shrimp were harvested after 19 weeks; then the ponds were stocked again at the same density. Oysters and clams remained in the ponds during a second trial of shrimp. They were harvested at the end of the second trial, 9 months after stocking. An ANOVA procedure and a multiple range test were used to compare water quality and production parameters among treatments, using the STATISTICA (2000) software.

3. Results No differences in temperature, salinity, pH and DO levels were observed among ponds, in any of the two shrimp crops as shown in Table 2. In both, total ammonium nitrogen (TAN) was significantly lower in treatment 5 as compared with treatment 1. The same pattern was shown by chlorophyll-a, and total suspended solids. In the first crop, differences in shrimp production parameters were observed among treatments (Table 3). Weight gain recorded the lowest value, 12.61 g in treatment control (without mollusks), similar to the
Table 3 Production parameters of white shrimp, Litopenaeus vannamei in the two crops and the five polyculture treatments Treatment First crop Growth Survival Yield (g) (%) (kg/h) Control 2 3 4 5 12.88a 12.61a 13.45ab 13.69ab 14.88b 48.3a 63.5b 61.2b 63.1b 59.7ab 1866a 2402ab 2469ab 2592ab 2665b Second crop Growth Survival Yield (g) (%) (kg/ha) 12.34a 12.23a 12.97a 13.26a 13.11a 63.2a 61.9a 66.7a 67.3a 65.2a 2356a 2271a 2595a 2677a 2564a

Means in a column with different letters were significantly different at P b 0.05.

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4 L.R. Martinez-Cordova, M. Martinez-Porchas / Aquaculture xx (2006) xxxxxx Table 4 Production parameters of oyster, Crassostrea gigas and clam, Chione fluctifraga in the polyculture treatments Treatment Oyster Growth Survival Yield (g) (%) (kg/h) 2 3 4 5 50.1b 48.5ab 43.4ab 40.2a 16.2b 12.3a 11.6a 10.7a 1014b 746a 1007b 860a Clam Growth (g) 13.3ab 12.9a 14.0b 12.1a Survival Yield (%) (kg/ha) 46.4ab 49.2ab 45.5a 50.2b 617a 793b 637a 759b

Means in a column with different letters, were significantly different at P b 0.05.

obtained in treatments 2 and 3. The highest weight gain was 14.88 g, recorded in treatment 5 (with the greatest combined density of mollusks), but no significant differences were observed with respect to treatments 4 and 3. The lowest survival was observed in the control (48.3%) and the greatest in treatment 2 (63.9%). The lowest yield was obtained in treatment control (1866 kg/ ha) similar to those obtained in treatments 2, 3 and 4. The highest yield was recorded in treatment 5 (2665 kg/ha). For the second crop, no differences in any of the production parameters were observed between treatments as shown in Table 2. In general in this trial, slightly lower growth, little higher survival and similar yield were observed as compared to the first trial. Production parameters of oysters and clams are shown in Table 4. Oysters weight gain in the nine months of the experiment, was the lowest in treatment 5 (40.2 g), and the highest in treatment 2 (50.1 g). Survival in general was very poor for all the treatments, with the minimum value (10.7%), observed in treatment 5 and the maximum (16.2%), recorded in treatment 2. Yield was significantly lower in treatment 3 (746 kg/ha) than in treatments 2 (1014 kg/ha) and 4 (1007 kg/ha). Clams grew between a minimum value of 12.1 g in treatment 5 and a maximum of 14.0 g in treatment 4. Significant differences were observed among treatments. Survival ranged from the lowest value of 45.5% in treatment 4 to the greatest of 50.2% in treatment 5. Yield of clam was lower in treatments 2 (617 kg/ha) and 4 (637 kg/ha) as compared to treatments 3 (793 kg/ha) and 5 (759 kg/ha). 4. Discussion The decrease in TAN in ponds with the highest density of mollusks seems to be contrary to the expectative. One can expect that at higher mollusk density, lower phytoplankton (due to harvest), and consequently lower TAN uptake. However it is plausible to think that

mollusks harvest controls phytoplankton excess and maintains an active and vigorous algal community (in the log phase), which needs higher amounts of nitrogen (De la Lanza, 1999). TAN is probably the form of nitrogen most rapidly taken by phytoplankton (Bufford and Lorenzen, 2004). Stolzemburg (1992) reports that mussels can decrease dramatically the concentration of ammonium nitrogen in downstream. Total ammonium nitrogen in treatment without mollusks was little higher than the limit of 1 mg/L that has been recommended for some authors as non-lethal for shrimp farming (Alcaraz et al., 1999). Other authors, however consider that TAN must be in the range of 0.2 to 2 mg/L and the unionized ammonia lower than 0.2 mg/L (Boyd and Gautier, 2000). The higher concentration of chlorophyll-a, and total suspended solids in treatment control (without mollusks), compared to treatment 5, (with the highest combined density of mollusks), and the other 3 treatments (also containing mollusks), is related to the consumption of organic matter and phytoplankton from water column, by these filter feeder organisms. This probably had an effect on the concentration of total ammonium nitrogen, because a lower amount of organic matter was available for bacterial decomposition. Similar results have been previously reported by Jones (1999), Jones and Preston (1999) and Jones et al. (2001). Shpigel et al. (1993), found that bivalves in an integrated system can assimilate 10.5% of the original N. An additional 33% of the original nitrogen in particulate form would be metabolized by the mollusks. Weight gain and yield of shrimp obtained in this study are comparable to those reported in successful semiintensive commercial farms (Clifford, 1994). The better growth and yield in the first trial were obtained in ponds with higher combined mollusk density. This was probably due to the improvement of water quality produced by the mollusks, agreeing with the report by Smith (1985), Smith and Piedrahita (1988), Hopkins et al. (1993) and Yokoyama et al. (2002). Hu et al. (1995) reported on the improvement of shrimp and oyster production in a mixed-culture system. Oyster production parameters were better in treatment with the lowest combined density of mollusks, which suggest that its development is affected by high densities. Oyster weight gain in this study was similar to that obtained in commercial farming in natural environments (Islas-Olivares, 1982). However, oyster survival was very poor and commercially unsuitable. The high mortalities are associated to the temperatures over 30 C recorded in some periods of the second shrimp crop, specially at afternoon. Summer temperatures in Norwest

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Mexico reach more than 40 C and rapidly warm up water column of shallow ponds. C. gigas is an organism from temperate regions and high mortalities may occur in summer months in tropical and subtropical regions (Soletchnik et al., 2005). The growth recorded by clam was similar to that observed in natural ecosystems (Martinez-Cordova, 1996), and survival and yield can be considered acceptable for commercial purposes. Production parameters of clam were not related to mollusks combined density. Differences in survival between oysters and clams could be also related to adaptation, as Chione seeds came from a nearby area while oysters seed came from a hatchery. According to the results of this investigation, it can be concluded that polyculture of shrimp and mollusks in ponds is technically feasible and that the presence of mollusks (even in the highest combined density used in this study), did not affect growth, survival and yield of shrimp, at contrary they improve some variables of water quality such as concentration of ammonium nitrogen and total suspended solids. However it is clear that the density of mollusks must have a limit, related with the carry capacity of the system. It is necessary in future research to investigate this limit not only in these semiintensive ponds but also in intensive (aerated) ponds. C. gigas showed not to be a good species for polyculture in this region, and conditions. Probably in other regions without extreme temperature, it can be suitable for combined culture with shrimp. C. fluctifraga could be considered as a good prospect for polyculture with shrimp in Northwest Mexico and other tropical, subtropical and inclusively temperate regions. A further economic analysis of the polyculture is necessary to know if the benefits are higher than the labor costs for maintaining the bivalves, although ecologic benefits are difficult to evaluate. Acknowledgements We want to thank CONACYT (The National Science and Research Council in Mexico) for the financial support to this research. References
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