The presence of the Pacific whiteleg shrimp (Litopenaeus vannamei, Boone, 1931) in the wild in Thailand.
KEY WORDS: Pacific whiteleg shrimp, Litopenaeus vannamei, alien species, aquaculture, population establishment, Thailand, Gulf of Thailand
During the past two decades, marine shrimp aquaculture has been important in generating export income for Thailand and other Asian countries (Briggs et al. 2004). For Thailand, this industry generates an average annual income of over 40 billion Baht (1 billion USD) (DOF 2003). Thailand's native shrimp species, Penaeus monodon, had been a major cultured species, but recent disease outbreaks, poor growth performance and declining prices for this species stalled further development of this industry. As a consequence, many shrimp farmers switched to aquaculture of the Pacific whiteleg shrimp (Litopenaeus vannamei, Boone 1931), a species native to the Pacific coasts of Central and South America (Perez Farfante & Kensley 1997), because of its fast growth, low incidence of native diseases and availability of domesticated strains. The production of L. vannamei in Thailand has rapidly increased from 10,000 metric tons in 2002 (Briggs et al. 2004) to approximately 300,000 metric tons in 2004, which comprised 80% of total marine shrimp production (Ekmaharaj 2005). This trend is also true for other Asian countries. For example, the production of L. vannamei in Mainland China comprised approximately 70% of the country's total marine shrimp production in 2003 (Briggs et al. 2004).
Rapid expansion of aquaculture and escapes of this introduced species to natural environments may pose unintended ecological and economic consequences. Many species introduced, via intentional and unintentional means, around the world have caused such problems, for example Nile tilapia (Oreochromis niloticus, De Silva 1989), the Nile perch (Lates sp.; Craig 1992) and zebra mussel (Dreissena polymorpha, O'Neill 1997). Ecological consequences may include introduction of nonnative pathogens, predation, competition and alteration of local biotic communities. Litopenaeus vannamei is already present in marine ecosystems outside ofits native range (Wenner & Knott 1991). Although no one has yet documented widespread negative ecological consequences for L. vannamei in the region, the outbreaks of Taura syndrome virus (TSV) in cultured L. vannamei have been reported in China since 1999 (Tu et al. 1999) and in Thailand since late 2002 (Nielson et al. 2005). The virus can be detected in nondiseased native shrimp species of Thailand (e.g., P. monodon and Macrobrachium resenbergii, Nielson et al. 2005; Prapasiri Barnette, Burapha University, pers. comm.). Overstreet et al. (1997) also suggested that other Penaeid shrimp species could be carriers for TSV under experimental conditions. Severity of ecological impacts at a local level depends greatly on the compatibility of the organism's physiological requirements with the new environment as well as the resiliency of local biotic communities (Moyle & Light 1996, With 2002). Ecological impacts, therefore, need to be assessed on a case-by-case basis. A prerequisite for many ecological interactions of an alien species and local biotic communities is an ability of an alien species to sustain a population.
Bangpakong River is one of the most important rivers and estuaries in eastern Thailand. It is formed by the convergence of the Nakonnayok and Prachinburi rivers at Bansang district of Prachinburi province. It runs 122 km through Bangkla, Mueang, Banpho and Bangpakong districts of Chachoengsao province (Fig. 1) before joining the Gulf of Thailand. Many people rely on the river for small-scale fishing activities, agriculture, and aquaculture. Majority of land uses along the Bangpakong watershed are urban development and agriculture (over 80%; Panutrakul et al. 2000). Aquaculture constitutes approximately 5.9% of total area of Chachoengsao province (Office of Agricultural Economics 2003). The Bangpakong watershed is one of the primary areas in eastern Thailand for shrimp aquaculture.
This paper reports the presence of subadult L. vannamei in the Bangpakong estuary. This work is a part of a larger study to understand possible factors contributing to L. vannamei's ability to establish a feral population and to assess potential ecological consequences of this introduced species to native biotic communities. The study will have larger implications for ecological risk assessment and monitoring in other countries where L. vannamei have been introduced for aquaculture.
MATERIALS AND METHODS
During January to November 2005, we collected shrimp samples from four sites within the Bangpakong River representing the upstream to downstream portions (Fig. 1), encompassing three districts of Chachoengsao province: Bangkla (one site; 69 km from the river mouth), Mueang (one site; 45.8 km from the river mouth), Bangpakong (two sites; 10.5 and 6.5 km from the river mouth). We hired local shrimp collectors to collect wild shrimp during hours of the ebb of a major tide, using commercial shrimp nets (6 m wide x 5 m deep x 25 m long with 2.5 cm mesh), which were set for 6 h. The nets were set along the main channel of the river. We collected shrimp in three periods, January to March 2005, June 2005 and September to November 2005. The numbers of nets at each site ranged from 2-18, depending on the conditions of the river (i.e., flow rates, depth, and width). In total, 30 nets were used in January to March 2005, and 19 nets were used in each of the other two periods.
[FIGURE 1 OMITTED]
Penaeid shrimp were sorted from other crustaceans, molluscs, fish and debris at our laboratory at Burapha University, Chonburi. We identified each Penaeid shrimp specimen based on Penaeid keys for South East Asia and Australia (Grey et al. 1983, Dall et al. 1990, Leelapiyanart & Naiyanetr 1991) to the lowest possible taxon. We quantified the presence of L. vannamei in terms of the number of L. vannamei in relation to other species of Penaeid shrimp within each net (proportion per net [+ or -] SE; Hayek & Buzas 1997) and the frequencies of encounter (numbers of nets containing L. vannamei to the total number of nets collected in the sampling period). For captured L. vannamei, we measured standard length (distance between the postorbital eye socket to the end of telson) and postorbital carapace length (PO-CL; the distance between the postorbital eye socket and the posterior median edge of the cephalothorax) to the nearest 0.1 mm using calipers. We tested for changes in the means of proportions, carapace and body lengths through time using ANOVA and Turkey multiple comparison tests (SPSS v.11, SPSS Inc., USA).
To correlate L. vannemei's presence with environmental factors, we measured water chemistry parameters, namely temperature ([degrees]C), dissolved oxygen (DO, mg/1), pH and salinity (practical salinity unit; psu) at each sampling site and at the river mouth (13[degrees]28'N, 101[degrees]58'E). The water chemistry measures were taken at two depths, 0.5 m below the surface and 0.5 m off the bottom using commercial probes (Environmental Monitoring System YSI 6600, YSI incorporated, USA). We measured water quality either before or soon after each shrimp-sampling period depending on the hours of the ebb tides (night versus day).
Presence and Size Distribution of Litopenaeus vannamei
We found L. vannamei at all four sites at least once during the study (Table 1). The highest occurrence of these shrimp was found during the September-November sampling period (19 out of 19 nets). Mean relative abundance of L. vannamei ranged from 0.0003 during the June sample to 0.04 during the September-November sample. The relative abundance during the September-November sampling period was significantly higher than the prior two sampling periods (P < 0.01).
The sizes of L. vannamei caught in the Bangpakong estuary ranged from 49-138 mm for standard length and from 11.3-37.4 mm for carapace length (PO-CL) (Fig. 2; Table 1). The mean standard lengths were 85.6 [+ or -] 2.66 mm (22.4 [+ or -] 0.75 mm CL), 105.5 [+ or -] 6.13 mm (30.4 [+ or -] 1.59 mm CL), and 85.8 [+ or -] 1.04 mm (22.0 [+ or -] 0.29 mm CL) for the three consecutive sampling periods, respectively. The mean standard and carapace lengths of L. vannamei collected during the June sampling period were significantly higher than those of L. vannamei collected in the other two sampling periods.
Water quality measurements at the surface and bottom of the river did not differ significantly. Therefore, we averaged the surface and bottom measures. Water temperature, dissolved oxygen (DO), and pH measures were similar across sampling sites (Fig. 2; Table 2). Over all sampling periods, water temperature ranged from 28.1[degrees]C to 34.4[degrees]C. DO concentration ranged from 2.36-5.94 mg/L. PH ranged from 6.25-7.64. In the first two sampling periods, salinity ranged from 17.45-27.90 psu with lowest salinity at Bangklah (most upstream). In the September-November sampling period, salinity approached zero at all sites.
Our study was among the first attempts in Thailand to quantify the presence of L. vannamei in natural waters. Thailand Department of Marine and Coastal Rcsources (2005) also found L. vannamei in the Bangpakong estuary. In addition, anecdotal evidence suggests that fishermen in southern Thailand caught L. vannamei off both the Andaman and Gulf of Thailand coasts after significant floods in 2003 (Briggs et al. 2004). None of these reports reflected the frequency of occurrence or quantity of L. vannamei captured. Existing evidence and our findings indicate that L. vannamei released from ponds were able to survive in Thailand's natural waters and were present in a large enough quantity to be consistently sampled. An increased encounter frequency during the study may indicate ongoing escapes from shrimp ponds or the presence of a self-sustaining population.
[FIGURE 2 OMITTED]
Water quality conditions of the Bangpakong estuary were within the normal range for both dry and rainy seasons (Table 2, Table 3) and were within the tolerance limits for L. vannamei. Litopenaeus vannamei can tolerate a wide range of salinity (0.5-45 ppt) and temperature (15[degrees]C to 33[degrees]C) (Briggs et al. 2004). Juveniles in aquaculture conditions grow well in salinity ranging from 10-15 ppt and temperature ranging from 23[degrees]C to 30[degrees]C (Briggs et al. 2004, Wyban et al. 1995). Our on-going surveys of L. vannamei abundance in the Bangpakong estuary have revealed that the mean size of L. vannamei individuais captured in January 2006 (23.9 [+ or -] 0.28 mm PO-CL) was higher than the mean size of those captured in 2005 (data shown in this paper). Our observations may indicate individual growth of escaped L. vannamei in natural environments. Even though natural reproduction generally occurs in a more marine-like environment, Parnes et al. (2004) found that inducing maturation of L. vannamei under a low-salinity condition (2-3 ppt) might be possible.
We do not have evidence that the shrimp present in the wild could reach maturation in the Bangpakong estuary or the Gulf of Thailand. The typical size of spawners in captivity is greater than 35 g (e.g., Ceballos-Vazquez et al. 2003, Palacios et al. 2000). However, there are no data on minimum size of spawners in the wild. Our L. vannamei samples include a few individuals weighing more than 25 g. We are currently comparing their gonad histology with L. vannamei of known age maintained in captivity at Burapha University (data not published).
We cannot infer from our results that there is a self-sustaining population. It is interesting to note that we caught a few small individuals (<13 mm CL). The smallest shrimp found in our preliminary survey during a spring tide in March 2005 was 11 mm CL. Small-size juveniles might be underrepresented in our data because of the limitations of our current sampling method, large mesh size, as well as sampling locations in the main channel of the river. The smaller juveniles would likely inhabit areas close to the mangroves that line the river banks. Insights obtained from extensive surveys of nursery areas for wild shrimp may indicate population establishment.
In addition to life history characters of alien species (e.g., physiological tolerance, fecundity, feeding behavior), recent literature on biological invasions suggests the number of independent releases and the number of individuals per release (i.e., propagule pressure) might facilitate the successful establishment and geographical spread of an alien species (e.g., Lockwood et al. 2005, Marchetti et al. 2004). In our case, an increased frequency of encounter of L. vannamei of similar sizes may reflect the increase in the "propagule pressure." The releases could occur during harvests, pond cleaning after disease infections or routine water exchange in ponds. The frequencies of the release could range from once to a few times per harvest cycle (2-3 cycles/year). The sizes of the shrimp escaped could range from approximately 5 mg ([PL.sub.15]) to 20 g (a typical marketable size). The Office of Agriculture Economics (2003) estimated the shrimp farming area in Chachoengsao province to be 71,098 rai (11,375 ha; 5.9% of total area of the province), with the largest concentration in Bangpakong (19,325 rai) and Bangkla (16,749 rai) districts. Most shrimp farms are located within 10 km of the Bangpakong River. The "propagule pressure" could be substantial given a stocking density of at least 100,000 PL/rai (60 individual PL/[m.sup.2]) with 80% to 90% survival (typical production is 1 mt/rai). The "propagule pressure" hypothesis might also explain our highest encounter with L. vannamei in Bangklah district (our most upstream site).
It is too early to conclude that L. vannamei is establishing a population. However, increasing trend in abundance (numbers of individuals and frequencies of encounter) raises a concern over the potential geographic spread and short-term ecological consequences (e.g., spreading of alien pathogens). Even though we need to confirm the population establishment of L. vannamei in the Bangpakong River, our findings can serve as baseline information for ecological risk assessment, as well as risk monitoring and management for introduced L. vannamei in Thailand and elsewhere.
The authors thank the Chachoengsao Provincial Fisheries Office for facilitating shrimp sampling and for shrimp farming data. Local shrimp fishermen were very helpful in collecting the shrimp samples and accommodating our research needs. The authors also acknowledge Prasarn Intacharoen, Arun Boontham, and Yuwanna Sasing at the Department of Aquatic Science, Burapha University for their technical assistance. The authors thank Dr. Acacia Alcivar-Warren and the International Marine Shrimp Environmental Genomics Initiative (IMSEGI) for the opportunity to publish in this volume, and they acknowledge anonymous reviewers for improving the quality of the manuscript. Financial support for this project came from the National Research Council of Thailand (fiscal year 2005).
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WANSUK SENANAN, (1) * NONGNUD TANGKROCK-OLAN, (1) SUWANNA PANUTRAKUL, (1) PRAPARSIRI BARNETTE, (1) CHARAN WONGWIWATANAWUTE, (2) NOPPARMARD NIPHONKIT (3) AND DAVID J. ANDERSON (4)
(1) Department of Aquatic Science, Faculty of Science, Burapha University, Bangsaen, Chonburi 20131 Thailand; (2) Chachoengsao Coastal Fisheries and Development Bureau Bangpakong, Chachoengsao 24130 Thailand; (3) Chachoengsao Provincial Fisheries Office, Chachoengsao City Hall Muang, Chachoengsao 24000 Thailand; (4) IEP Program "Piboonbumpen" Demonstration School, Burapha University Bangsaen, Chonburi 20131 Thailand
* Corresponding author. E-mail: firstname.lastname@example.org
TABLE 1. Frequency of encounter (the number of nets containing Litopeneaus vannamei to the total number of nets), average relative abundance (the numbers of L. vannamei to the total number of captured Penaeid shrimps per net [+ or -] SE), and average sizes ([+ or -] SE) of L. vannamei found in the Bangpakong estuary, Thailand, during January to November 2005. Superscript letters indicate statistical differences of means at 95% confidence level. Sampling Periods Frequency of (number of nets, individuals) Encounter Jan. to Mar. 2005 (30 nets, 30 individuals from 4 sites) 10/30 June 2005 (19 nets, 4 individuals from 3 sites) 3/19 Sept. to Nov. 2005 (19 nets, 193 individuals from 3 sites) 19/19 Sampling Periods Average Relative (number of nets, individuals) Abundance Jan. to Mar. 2005 (30 nets, 30 individuals from 4 sites) 0.004 [+ or -] 0.0016 (a) June 2005 (19 nets, 4 individuals from 3 sites) 0.0003 [+ or -] 0.0002 (a) Sept. to Nov. 2005 (19 nets, 193 individuals from 3 sites) 0.04 [+ or -] 0.0035 (b) Sampling Periods Average PO Carapace (number of nets, individuals) Length (1) (mm) Jan. to Mar. 2005 (30 nets, 30 individuals from 4 sites) 22.4 [+ or -] 0.75 (a) June 2005 (19 nets, 4 individuals from 3 sites) 25.1 [+ or -] 0.07 (b) Sept. to Nov. 2005 (19 nets, 193 individuals from 3 sites) 22.0 [+ or -] 0.29 (a) Sampling Periods Average Standard (number of nets, individuals) Length (2) (mm) Jan. to Mar. 2005 (30 nets, 30 individuals from 4 sites) 85.6 [+ or -] 2.66 (a) June 2005 (19 nets, 4 individuals from 3 sites) 105.5 [+ or -] 6.13 (b) Sept. to Nov. 2005 (19 nets, 193 individuals from 3 sites) 85.8 [+ or -] 1.04 (a) (1) Postorbital carapace length is the distance between the postorbital eye socket and the posterior median edge of the cephalothorax. (2) Standard length is the distance between the postorbital eye socket and the end of telson. TABLE 2. Average water quality parameters ([+ or 1] SE) at sampling sites in the Bangpakong estuary during January 2005 to November 2005. Sampling Periods Water Quality Sites (distance from the Parameters river mouth, km) Jan. to Mar. 05 Temperature All Sites 29.00 [+ or -] 0.370 ([degrees]C) 1. Bangkla (69) 30.45 [+ or -] 0.730 2. Mueang (45.8) 29.00 [+ or -] 0.00 3. Bangpakong 1 (10.5) 28.45 [+ or -] 0.255 4. Bangpakong 2 (6.5) 28.11 [+ or -] 0.240 River mouth N/A Salinity (psu) All sites 23.17 [+ or -] 1.304 1. Bangkla (69) 19.01 [+ or -] 0.110 2. Mueang (45.8) 19.30 [+ or -] 0.150 3. Bangpakong 1 (10.5) 26.39 [+ or -] O.120 4. Bangpakong 2 (6.5) 25.84 [+ or -] 0.310 River mouth N/A Dissolved All sites 5.16 [+ or -] 0.287 oxygen (mg/l) 1. Bangkla (69) 4.38 [+ or -] 0.480 2. Mueang (45.8) 5.70 [+ or -] 0.200 3. Bangpakong 1 (10.5) 4.80 [+ or -] 0.340 4. Bangpakong 2 (6.5) 5.94 [+ or -] 0.040 River mouth N/A pH All sites 7.166 [+ or -] 0.069 1. Bangkla (69) 7.27 [+ or -] 0.040 2. Mueang (45.8) 6.97 [+ or -] 0.080 3. Bangpakong 1 (10.5) 7.07 [+ or -] 0.165 4. Bangpakong 2 (6.5) 7.34 [+ or -] 0.020 River mouth N/A Sampling Periods Water Quality Sites (distance from the Parameters river mouth, km) June 05 Temperature All Sites 32.71 [+ or -] 0.413 ([degrees]C) 1. Bangkla (69) 30.75 [+ or -] 0.150 2. Mueang (45.8) 32.15 [+ or -] 0.450 3. Bangpakong 1 (10.5) 33.40 [+ or -] 0.100 4. Bangpakong 2 (6.5) 32.95 [+ or -] 0.450 River mouth 34.30 [+ or -] 0.100 Salinity (psu) All sites 23.88 [+ or -] 1.669 1. Bangkla (69) 17.45 [+ or -] 0.450 2. Mueang (45.8) 19.95 [+ or -] 0.050 3. Bangpakong 1 (10.5) 27.90 (surface only) 4. Bangpakong 2 (6.5) 27.90 [+ or -] 0.00 River mouth 28.20 [+ or -] 0.600 Dissolved All sites 3.46 [+ or -] 0.166 oxygen (mg/l) 1. Bangkla (69) 3.28 [+ or -] 0.430 2. Mueang (45.8) 3.58 [+ or -] 0.005 3. Bangpakong 1 (10.5) 4.04 [+ or -] 0.470 4. Bangpakong 2 (6.5) 3.41 [+ or -] 0.130 River mouth 2.99 [+ or -] 0.455 pH All sites 7.35 [+ or -] 0.085 1. Bangkla (69) 7.15 [+ or -] 0.060 2. Mueang (45.8) 7.34 (surface only) 3. Bangpakong 1 (10.5) 7.32 [+ or -] 0.040 4. Bangpakong 2 (6.5) N/A River mouth 7.64 [+ or -] 0.00 Sampling Periods Water Quality Sites (distance from the Parameters river mouth, km) Sept. to Nov. 05 Temperature All Sites 29.38 [+ or -] 0.209 ([degrees]C) 1. Bangkla (69) 28.91 [+ or -] 0.005 2. Mueang (45.8) 29.01 [+ or -] 0.350 3. Bangpakong 1 (10.5) N/A 4. Bangpakong 2 (6.5) 30.24 [+ or -] 0.035 River mouth 29.54 [+ or -] 0.066 Salinity (psu) All sites 3.65 [+ or -] 2.062 1. Bangkla (69) 0.085 [+ or -] 0.005 2. Mueang (45.8) 0.18 [+ or -] 0.027 3. Bangpakong 1 (10.5) N/A 4. Bangpakong 2 (6.5) 1.60 [+ or -] 0.00 River mouth 9.07 [+ or -] 4.833 Dissolved All sites 4.25 [+ or -] 0.379 oxygen (mg/l) 1. Bangkla (69) 5.27 [+ or -] 0.120 2. Mueang (45.8) 4.16 [+ or -] 0.392 3. Bangpakong 1 (10.5) N/A 4. Bangpakong 2 (6.5) 2.53 [+ or -] 0.170 River mouth 4.38 [+ or -] 0.405 pH All sites 6.81 [+ or -] 0.148 1. Bangkla (69) 6.25 [+ or -] 0.00 2. Mueang (45.8) 6.64 [+ or -] 0.178 3. Bangpakong 1 (10.5) N/A 4. Bangpakong 2 (6.5) 6.88 [+ or -] 0.025 River mouth 7.19 [+ or -] 0.276 N/A = Data not available. TABLE 3. Historical water quality in the Bangpakong River. The values reported are for the entire length of the Bangpakong River (122 km). Sampling Periods Water Quality Parameters Mar. 00 (1) July 00 (1) Temperature ([degrees]C) 31.0 [+ or -] 0.6 32.71 [+ or -] 1.31 Salinity (psu) 8.0 [+ or -] 4.02 0.0 [+ or -] 0.0 Dissolved Oxygen (mg/L) 5.3 [+ or -] 0.3 5.3 [+ or -] 0.2 pH 7.5 [+ or -] 0.1 6.6 [+ or -] 0.1 Sampling Periods Water Quality Parameters Jan. to Apr. 04 (2) July to Oct. 04 (2) Temperature ([degrees]C) 26.0-33.6 28.4-33.3 Salinity (psu) 1.6-30.2 0.0-8.2 Dissolved Oxygen (mg/L) 0.7-13.3 2.2-6.8 pH 6.7-8.4 6.0-8.0 (1) Reported as an average [+ or -] SE (Panutrakul et al. 2001). (2) Reported as a range (Department of Marine and Coastal Resources 2005).
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|Author:||Senanan, Wansuk; Tangkrock-Olan, Nongnud; Panutrakul, Suwanna; Barnette, Praparsiri; Wongwiwatanawut|
|Publication:||Journal of Shellfish Research|
|Date:||Dec 1, 2007|
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