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Growth and survival of pearl oyster Pinctada maxima spat reared under different environmental conditions.

ABSTRACT To understand the influences of environmental conditions on the performance of pearl oyster spat, we conducted four experiments to evaluate separately the effects of salinity (21, 24, 27, and 30), diet (Isochrysis zhanjiangensis, Platymonas subcordiformis, Chlorella; 50% I. zhanjiangensis/50% P. subcordiformis, 50% I. zhanjiangensis/50% Chlorella, and 50% P. subcordformis/50% Chlorella), diet availability (high, medium and low), and rearing site (hatchery and sea) on the growth and survival of pearl oyster Pinctada maxima spat. Results showed that environmental conditions exerted significant effects on the growth of P. maxima spat. Salinity and rearing site also had significant effects on survival, but no significant differences were observed in terms of survival between the diet and diet availability treatments. Growth declined with decrease in salinity. Spat reared at high salinities (30 and 27) showed larger shell length growth and greater survival than those at low salinities (24 and 21). Spat fed on a single diet (Chlorella) had poorer shell length growth than those fed on diets composed of more than one species. Spat reared on a medium ration (4.0 x [10.sup.4] cells/mL/day) had greater shell length growth than those reared at high (8.0 x [10.sup.4] cells/mL/day) and low (2.0 x [10.sup.4] cells/mL/day) rations. Spat held in the sea had greater shell length growth than those held in the hatchery. However, survival rate of spat was greater in the hatchery than in the sea. These results suggest that seed production of P. maxima spat could be optimized by extending the nurture period in the hatchery. Moreover, various diets should be provided to ensure balanced food intake.

KEY WORDS: Pinctada maxima, environmental conditions, spat, growth, survival, pearl oyster

INTRODUCTION

The pearl oyster Pinctada maxima exists naturally along the coast of southern China. This species is one of the most important components of molluscan mariculture in the Guangdong, Guangxi, and Hainan provinces. It is primarily cultured for high-value production of large-size pearls. Pearl production first achieved experimental success in China in 1981 (as reviewed by Jiang & He 2009). However, commercial pearl production from this species has developed slowly during recent decades because of mass mortality at early growth stages. Deng et al. (2000) reported the mortality of spat held at different cultivation sites, specifically a high mortality rate of 99.0% at age 6 mo in Qianluo Bay, Hainan. Liang et al. (2008) reported 94.1% spat mortality in Liushagang Bay, Guangdong, that lasted for 90 days. To solve this problem, a series of studies was conducted to optimize rearing conditions to improve spat survival (e.g., Luo et al. 1996, Liang et al. 1999, Liang et al. 2011).

Similar to other marine bivalves, pearl oyster spat produced in a hatchery are transferred to either a sea- or land-based nursery at approximately 2 mm in shell length for further growth. The period for successful transfer to the sea is limited by sudden changes in environmental factors (e.g., salinity and diet availability), predation, fouling and boring organisms, and so on (Monteforte & Morales 2000, Pit & Southgate 2000, Ehteshami et al. 2010). The cultivation sites for Pinctada maxima in China are generally nearshore estuarine areas, where salinity fluctuates because of heavy rains and runoff in the summer months. Food availability varies seasonally, which can influence growth and survival of pearl oyster P. maxima spat. Previous studies have reported the effects of environmental factors on the growth performance of pearl oyster P. maxima spat (Lucas 2008a, Liang et al. 2011, Xie et al. 2011).

In 2008 to 2010, we introduced breeders from Indonesia that produced 3 progeny stocks. The progeny stocks at 2 y of age had a 3.5-14.9% survival rate (Liang et al. 2011). To optimize rearing protocols for larvae and spat, we performed a series of experiments to evaluate the effects of various environmental conditions on the growth performance of this species. Our previous study evaluated the effects of environmental factors (stocking density, diet, and water exchange) on the growth performance of P. maxima larvae (Deng et al. 2013). The current study evaluated the effects of environmental factors in the hatchery on the growth performance of pearl oyster spat to improve seed production by optimizing rearing conditions.

MATERIALS AND METHODS

Experimental Animal and Design

Broodstock (shell length, 15.7-17.4 cm) were introduced from Indonesia in 2009, and were transported and cultured in Beibu Bay, Zhanjiang. In April 2013, mature individuals were induced to spawn. Spawning and incubation were carried out in plastic tanks. D-shaped larvae at 48 h postfertilization were collected and reared in the tanks. Larvae were reared following the protocols of Xie et al. (2011). When eyed larvae appeared, plastic films were provided for settlement. Spat (shell length, 1.0-2.0 mm) were transferred from the plastic films and stocked into the experimental 50-L tanks.

Microalgal Diets

Three species of microalgae were used in the study: Isochrysis zhanjiangensis, Platymonas subcordiformis, and Chlorella sp. Microalgae stock cultures were obtained from the Marine Microalgae Laboratories of Guangdong Ocean University. These microalgae were cultured in 5-L and 30-L glass buckets and grown at 25.0-28.3[degrees]C in a nutrient medium developed by Chen (1995). The photoperiod was 24:0 h (light/dark), and illumination was provided by 2 daylight (40-W) fluorescent tubes. Filtered (0.45 [micro]m) and UV-treated seawater (salinity, 30.2) was used. Continuous aeration was provided to enhance growth and prevent the algae from settling. The algae were harvested during an exponential phase for feeding.

Four experiments were designed to assess the effects of salinity, diet, diet availability, and rearing site on the growth and survival of pearl oyster spat.

Experiment 1: Salinity

Four treatments consisting of salinities of 21, 24, 27, and 30 were tested. Three replicates of 1,000 spat were designed for each treatment. Spat were acclimated from a salinity of 30 using gradual salinity changes to lessen any stress caused by the new environment by conducting 50% water exchanges at 6-h intervals until the seawater reached the required salinity. Water temperature ranged from 27.6-29.2[degrees]C. All salinity treatment individuals were fed Platymonas subcordiformis, and the common feeding rate was 4.0 X [10.sup.4] cells/mL/day.

Experiment 2: Diet

Three microalgae species (Isochrysis zhanjiangensis, Platymonas subcordiformis, and Chlorella) and 3 mixed diets (50% I. zhanjiangensis/50% P. subcordiformis, 50% I. zhanjiangensis/50% Chlorella, and 50% P. subcordiformis/50% Chlorella) were selected to determine the effects of different algal diets. Triplicate tanks containing 1,000 spat were used for each treatment. Salinity was 30 and temperature ranged from 28.5-32.1[degrees]C. The seawater was renewed every other day. The algae were harvested during the exponential phase for feeding. To control the final concentration of microalgae in the experimental tanks, the feeding quantity was determined by measuring the original concentration of the different microalgal diets precisely.

All diets were fed at a concentration of 2.0 x [l0.sup.4] cells/mL in their culture media. For the mixed-diet experiments, 2 microalgal diets were adjusted to the same concentration and then mixed with a half volume of each diet before feeding to the spat. Equal cell numbers were present in the experimental tanks.

Experiment 3: Diet Availability

The microalga Platymonas subcordiformis was fed during experiment 3. Three treatments consisting of high (8.0 x [10.sup.4] cells/mL/day), medium (4.0 x [10.sup.4] cells/mL/day), or low (2.0 x [10.sup.4] cells/mL/day) rations were conducted. Spat were stocked into the plastic tanks, containing 45 L 0.45-[micro]m filtered seawater. Triplicates of 1,000 spat were used for each treatment. The common feeding rate was considered as the control (medium) feeding rate for this trial. During the rearing period, the seawater was renewed every day. Water temperature ranged from 27.8-29.9[degrees]C.

Experiment 4: Rearing Sites

Two disparate environments (sea and hatchery) were evaluated during experiment 4. Spat were removed from the plastic plates and placed into 20 x 35-[cm.sup.2] nets at a density of 1,000 individuals per net. Triplicates of 1,000 spat (net) were used for each treatment. The natural groups were reared in the sea at Leizhou, Zhanjiang, and were left untouched until the experiment ended. The hatchery groups were reared separately in the 50-L tanks using ambient seawater at the same site. During the rearing period, the seawater was renewed every day and the common feeding protocol of Liang et al. (1999) was followed.

Measured Parameters

At the beginning and end of the experiments, 30 individuals were sampled randomly from each tank. The shell length of each sample was measured using digital Vernier calipers.

The relative growth rate was calculated using the formula of Walen (1963) as follows: K = (ln[SH.sub.2]- ln[SH.sub.1])/t, where [SH.sub.2] and [SH.sub.1] are the shell lengths (in millimeters) at the beginning and end of the experiment, respectively, and t is the duration of the experiment in days.

Data Analysis

Mean shell length, relative growth rate, and survival rate of spat in experiments 1-3 were analyzed using 1-way analysis of variance, followed by Tukey's test to determine significant differences between treatment means. Mean shell length, relative growth rate, and survival rate of spat in experiment 4 were analyzed using the t-test. Survival data were arcsin transformed before statistical analysis. P < 0.05 was considered statistically significant. Data are presented as mean [+ or -] SD (n = 3).

RESULTS

Experiment 1: Salinity

Shell growth of spat was affected significantly by salinity (P < 0.05). At the end of the experiment, spat cultured at salinities of 30 and 27 had significantly larger mean shell length and relative growth rate than those reared at 24 and 21 (P < 0.05). Significant differences in mean shell length and relative growth rate were observed between the latter treatments (P > 0.05). Figure 1 presents the relative growth rate among the 4 treatments. Significant differences also existed in the survival rate among the 4 treatments (P < 0.05). After a 30-day exposure to experimental conditions, survival rates of spat held at high salinities of 30 and 27 were significantly greater than those reared at salinities of 24 and 21 (P < 0.05). However, no significant differences were observed in the survival rate between the high-salinity treatments (30 and 27, P> 0.05; Table 1).

Experiment 2: Diet

Table 2 shows the mean shell length of spat fed with different microalga species during the 30-day period. Spat fed on Iso + Pla (50% Isochrysis zhanjiangensis/50% Platymonas subcordiformis) had the highest mean shell length, followed by those fed on Pla + Chl (50% P. subcordiformis/50% Chlorella) and Iso + Chl (50% L zhanjiangensis/50% Chlorella). Spat displayed poor shell length when the single-diet Chlorella was provided. Significant differences were observed in relative growth rates among the 5 treatments (P < 0.05). Spat fed on Iso + Pla had relatively higher growth rates than in the other treatments. Figure 2 shows the relative growth rate among the 5 treatments. No significant differences existed in the survival rate among the treatments fed on single diets or mixed diets (P > 0.05). Survival rate of spat ranged from 58.6-66.8%.

Experiment 3: Diet Availability

Shell length growth of spat was affected significantly by diet availability (P < 0.05). Spat fed with the medium diet quantity grew to larger sizes than individuals in the other two food treatments. A higher relative growth rate was observed when medium diet quantity was provided. No significant difference was found in survival rate among the three treatments (P > 0.05; Table 3).

Experiment 4: Rearing Sites

Significant differences existed in mean shell length between the groups cultured in the hatchery and in the sea (P < 0.05). Spat held in the sea had greater mean shell lengths than those in the hatchery. A higher relative growth rate was also observed in the sea. However, the spat reared in the hatchery had higher survival rates than those in the sea (Table 4).

DISCUSSION

Salinity is an important environmental factor in the hatchery, and it affects the growth of bivalve spat. Several studies have evaluated the effect of salinity on the growth performance of pearl oyster spat (e.g., Numaguchi & Tanaka 1986, Taylor et al. 1997a, O'Connor & Lawler 2004, Taylor et al. 2004, Kvingedal et al. 2008, Lucas, 2008a). For the pearl oyster Pinctada fucata martensii, for example, Numaguchi and Tanaka (1986) reported better growth rates of spat at lower salinities of 26.5 and 18.9 compared with other salinities tested over a 25-day period (15.1, 30.3, and 34.1, and an ambient salinity of 37.9). For the pearl oyster Pinctada maxima, Taylor et al. (2004) found that spat reared at a salinity of 30 for 2 days exhibited significantly faster growth compared with those spat reared at salinities of 25, 34, 40, and 45. The results of this study confirmed that salinity change can affect significantly the growth of P. maxima spat. Growth rate in terms of shell length increase was greater when spat were raised at high salinities (30 and 27). A reduction in salinity to 24 and 21 resulted in reduced shell length growth (Table 1). The most appropriate salinity range for P. maxima spat growth is between 30 and 34 (Taylor et al. 2004). Salinity reduction beyond the optimal range can clearly affect the growth of P. maxima spat.

The spat of Pinctada maxima can tolerate a broad range of salinities (25-45) without a significant effect on survival (Taylor et al. 2004). This study showed that salinity influenced the survival of P. maxima spat significantly. The mortality of P. maxima spat at salinities of 21 and 24, which was slightly lower than those tested by Taylor et al. (2004), was higher than those at salinities of 27 and 30. In China, pearl oyster spat are commonly reared inshore or in estuaries, and salinity reductions at cultivation sites may occur because of water runoff and heavy rainfalls during the summer months. This phenomenon may contribute to the mass mortality of P. maxima spat in the sea.

Diet availability is also an important environmental factor in the hatchery that affects growth performance of bivalve spat. Growth studies under different food concentrations show that, in general, growth rate declines with the increase in food densities, as detected in several bivalve species (Bayne et al. 1989, Cahalan et al. 1989, Martinez et al. 1995, Laing, 2000, Schneider et al. 2010). In this study, we also observed that shell length growth decreased with increase in food quantity. High particle concentrations increase the production of feces and pseudofeces (Widdows et al. 1979, Lucas 2008b), which may result in a significant loss of nutrients (Cahalan et al. 1989). A decline in absorption efficiency is commonly observed with bivalve molluscs in laboratory experiments with an increasing ratio of microalgae (Navarro et al. 1991), and this is also true with pearl oysters (Lucas 2008b). Excess food causes deterioration of water in the tanks and consequently decreases growth. However, this explanation was not proved as the cause of the slower growth observed in P. maxima spat because critical water-quality parameters such as ammonia among food availability treatments were not measured during the experiment.

Previous studies have evaluated the effects of various diets on the growth and survival of pearl oyster spat (e.g., Taylor et al. 1997b, Numaguchi 2000, Martinez-Fernandez et al. 2004, Zhou et al. 2007, Li et al. 2008). Taylor et al. (1997b) assessed the nutritional value of 5 species of microalgae for 75-day-old Pinctada maxima spat. They reported a relatively poor nutritional value of Chaetoceros calcitrans and Pavlova lutheri, but a relatively high nutritional value of Chaetoceros muelleri, Tetraselmis suecica, and Isochrysis. The current study observed significant differences in the growth rates among diet treatments when spat were fed on single diets or mixed diets. The spat of P. maxima showed the best growth (increase in shell length) when fed a mixture of Isochrysis zhanjiangensis and Platymonas subcordiformis. Spat fed mixed diets of I. zhanjiangensis and Chlorella, and P. subcordiformis and Chlorella also showed good growth performance. The spat performed poorly when single-diet Chlorella was fed. In general, mixed-species diets can produce greater oyster growth than monospecific diets. This phenomenon is attributed to these diets providing a balanced mix of essential nutrients (Knauer & Southgate 1999). The nutritional value of the microalgae species tested in the experiment was assessed previously in single- or mixed-species diets in the hatchery (Liang et al. 1999, Li et al. 2008). Microalgae I. zhanjiangensis and P. subcordiformis have high nutritional values when fed as either single or multispecies diets for P. maxima larvae and spat. The microalga Chlorella is a poor single-species diet for this species because the solid cell wall of the species may hamper ingestion and digestion.

Significant effects existed between sea and hatchery environments on Pinctada maxima spat. Higher growth rates were observed when the spat were transferred from the hatchery to the sea. Similar results have been reported in other marine bivalve spat. For example, Martinez et al. (1992) found that early spat of Argopecten purpuratus held in the ocean for 40 days had larger sizes than a group of individuals of the same brood held in the hatchery. Pit and Southgate (2000) reported that pearl oyster Pinctada margaritifera spat (3 wk after settlement) transferred to the ocean achieved higher growth rates than those transferred at 6 wk and 9 wk after settlement. For P. maxima, Kvingedal et al. (2008) reported that spat from families reared in the ocean grew significantly faster than those in the hatchery. The current study also observed that spat reared in natural environments had higher growth rates than those in the hatchery. This result is likely a consequence of access to a more complete nutritional diet. By contrast, spat held in the hatchery had higher survival rates than those in the sea, which demonstrates the environmental stability in the hatchery compared with that in the sea.

Mass mortality of spat transferred from hatcheries to the sea is a problem in pearl oyster (Pinctada maxima) farming in China. The mortality may be caused in part by several environmental factors. As shown in the current study, environmental factors including salinity change and diet availability, which generally occur at shallow depths in coastal waters, exert significant effects on the growth performance of P. maxima spat. In commercial hatcheries, some strategies may involve the extension of the nurture period in the hatchery until the spat reach shell lengths of 5-8 mm. Moreover, various diets should be provided to ensure balanced food intake for pearl oyster spat.

ACKNOWLEDGMENTS

The study was supported by both grants from Shellfish Modern Agro-industry Technology Research System (No.nycytx-47) and the Guangdong Marine and Fishery Bureau (No. A200900A07).

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YUEWEN DENG, (1) SHAO FU, (2) FEILONG LIANG, (2) XIAODONG DU (1,2) AND SHAOHE XIE (2).

(1) Fishery College, Guangdong Ocean University, Zhanjiang, 524025; (2) Pearl Research Institute, Guangdong Ocean University, Zhanjiang, 524025

* Corresponding author. E-mail: xsh5760288@126.com

DOI: 10.2983/035.032.0308

TABLE 1.
Mean shell length and survival rate of pearl oyster Pinctada
maxima spat reared at salinities of 21, 24, 27, and 30.

Salinity       [SH.sub.1] (mm)            [SH.sub.2] (mm)

21          1.54 [+ or -] 0.16 (a)    4.42 [+ or -] 0.42 (c)
24          1.57 [+ or -] 0.17 (a)    7.03 [+ or -] 0.59 (b)
27          1.51 [+ or -] 0.14 (a)    9.17 [+ or -] 0.48 (a)
30          1.47 [+ or -] 0.18 (a)   10.82 [+ or -] 0.63 (a)

Salinity      Survival rate (%)

21          33.2 [+ or -] 3.7 (c)
24          45.4 [+ or -] 2.8 (b)
27          59.4 [+ or -] 3.2 (a)
30          61.2 [+ or -] 3.5 (a)

[SH.sub.1] and [SH.sub.2] are shell length (in millimeters)
at the beginning and end of the experiment, respectively.
Means with the same superscript letters are not significantly
different (P > 0.05).

TABLE 2.
Mean shell length and survival rate of pearl oyster Pinctada
maxima spat fed on single and mixed diets.

Diet            [SH.sub.1] (mm)           [SH.sub.2] (mm)

Iso          1.38 [+ or -] 0.15 (a)   10.48 [+ or -] 0.58 (a)
Pla          1.42 [+ or -] 0.12 (a)   10.23 [+ or -] 0.52 (a)
Chl          1.41 [+ or -] 0.14 (a)    7.48 [+ or -] 0.67 (b)
Iso + Pla    1.39 [+ or -] 0.18 (a)   11.77 [+ or -] 0.72 (a)
Iso + Chl    1.36 [+ or -] 0.13 (a)   10.54 [+ or -] 0.66 (a)
Pla + Chl    1.44 [+ or -] 0.16 (a)   11.22 [+ or -] 0.54 (a)

Diet           Survival rate (%)

Iso          63.4 [+ or -] 4.3 (a)
Pla          66.8 [+ or -] 3.9 (a)
Chl          64.7 [+ or -] 3.8 (a)
Iso + Pla    59.4 [+ or -] 3.2 (a)
Iso + Chl    61.6 [+ or -] 2.6 (a)
Pla + Chl    58.6 [+ or -] 2.9 (a)

Chl, Chlorella; Iso, Isochrysis zhanjiangensis;
Pla, Platymonas subcordiformis; Iso +Pla, 50% I.
zhanjiangensis/50% P. subcordiformis; Iso + Chi,
50% I. zhanjiangensis/50% Chlorella; Pla + Chl,
50% P. subcordiformis/ 50% Chlorella. [SH.sub.1]
and [SH.sub.2] are shell length (in millimeters)
at the beginning and end of the experiment,
respectively. Means with the same superscript
letters are not significantly different (P > 0.05).

TABLE 3.
Mean shell length and survival rate of pearl oyster Pinctada
maxima spat fed on different diet quantities.

Diet
availability      [SH.sub.1] (mm)           [SH.sub.2] (mm)

High           1.54 [+ or -] 0.13 (a)    8.28 [+ or -] 0.58 (b)
Medium         1.57 [+ or -] 0.10 (a)   10.43 [+ or -] 0.72 (a)
Low            1.51 [+ or -] 0.15 (a)    7.17 [+ or -] 0.67 (b)

Diet                                              Survival
availability             K value                  rate (%)

High           0.0561 [+ or -] 0.0034 (b)   61.8 [+ or -] 3.3 (a)
Medium         0.0631 [+ or -] 0.0027 (a)   64.7 [+ or -] 3.7 (a)
Low            0.0519 [+ or -] 0.0022 (b)   62.5 [+ or -] 2.8 (a)

[SH.sub.1] and [SH.sub.2] are shell length (in millimeters) at the
beginning and end of the experiment, respectively. The K value is
the relative growth rate. Means with the same superscript letters
are not significantly different (P > 0.05).

TABLE 4.
Mean shell length and survival rate of pearl oyster Pinctada
maxima spat held in the hatchery and in the sea.

Rearing site        [SH.sub.1] (mm)           [SH.sub.2] (mm)

Hatchery        1.51 [+ or -] 0.14 (a)    9.32 [+ or -] 0.42 (a)
Sea             1.62 [+ or -] 0.18 (a)   12.58 [+ or -] 0.63 (b)

                                                   Survival
Rearing site             K value                   rate (%)

Hatchery        0.0606 [+ or -] 0.0018 (b)   65.3 [+ or -] 3.6 (a)
Sea             0.0683 [+ or -] 0.0023 (a)   41.7 [+ or -] 2.4 (a)

[SH.sub.1] and [SH.sub.2] are shell length (in millimeters) at the
beginning and end of the experiment, respectively. The K value is
the relative growth rate. Means with the same superscript letters
are not significantly
different (P > 0.05).
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Article Details
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Author:Deng, Yuewen; Fu, Shao; Liang, Feilong; Du, Xiaodong; Xie, Shaohe
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:9CHIN
Date:Dec 1, 2013
Words:4844
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