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THE GROWTH AND OVARIAN DEVELOPMENT PATTERN OF POND-REARED SWIMMING CRAB PORTUNUS TRITUBERCULATUS.

INTRODUCTION

The swimming crab Portunus trituberculatus is widely distributed throughout the coastal waters of East Asia, including Korea, Japan, the Philippines, and China (Hamasaki et al. 2006) and is an important fisheries resource and mariculture crab in these countries (Kim et al. 2010, Ng'ambi et al. 2017). Because of limited wild populations and increasing market demands, pond rearing of P. trituberculatus has developed rapidly since the 1990s (Xie et al. 2002). The aquaculture production of P. trituberculatus in China reached 125,300 tons in 2016 and pond culture contributed more than 95% of total production (China Fishery Statistical Yearbook 2017); however, poor ovarian development is one of the major obstacles to the sustainable development of the P. trituberculatus farming industry because this generally leads to lower edible content and inferior reproductive performance (Wu et al. 2010, He et al. 2017). Because of the poor ovarian development of pond-cultured P. trituberculatus, broodstock crabs for commercial hatcheries are mainly dependent on the capture from wild populations, which is not beneficial to the protection of P. trituberculatus in the wild (Cheng et al. 2012).

Pond rearing of Portunus trituberculatus has been practiced for more than two decades in China (He et al. 2016); however, their growth performance and ovarian development under these conditions remain unclear. This uncertainty makes it difficult to predict and plan for proper feeding management and harvesting of P. trituberculatus. Previous studies have shown that female P. trituberculatus developed their ovaries rapidly only after their pubertal molt (Wu et al. 2007). High-quality diets are required during this period of fast ovarian development to improve their nutritional value and market price (Wu et al. 2014). Therefore, it is necessary to study the growth and ovarian development pattern of pond-reared female P. trituberculatus. In view of this, the present study was conducted to investigate the growth pattern, pubertal molt time, and monthly variation in the ovarian development pattern in pond-cultured female P. trituberculatus. The results provide valuable information for the management, feeding practices, and marketing time in the farming of P. trituberculatus.

MATERIALS AND METHODS

Crab Rearing

This experiment was conducted at the Qidong scientific research base in Shanghai Fisheries Research Institute, Jiangsu, China, between March 2016 and March 2017. Two outdoor ponds of equal sizes (length X width X height = 82.5 m X 45 m X 1.5 m) were used in this study. Tiles and stones were provided at the bottom of each pond to act as crab shelters and thus reduce cannibalism. At the beginning of March, two experimental ponds were treated with chlorinated lime. About 2 wk later, similar-sized, active, and intact juveniles were selected for this study. The crabs were then randomly stocked into two replicate ponds at the same stocking density (approximately 3-4 crabs/[m.sup.2]). The ratio of male and female was 2:8.

Culture Management

The crabs were fed twice every day and the feeding ration was approximately 3%-10% of total crab biomass, based on residual feed and water temperature during the culture period. They were fed a mixture of mysids, frozen trash fish, and wheat flour. To reduce cannibalism, feeding to satiation was adopted during the culture period. From August to October, compound microorganisms (effective microbia) were used to maintain the pond water quality every 15 days. According to the weather and dissolved oxygen (DO) of the pond water, aeration was used to increase the water DO. The water temperature, pH, DO, ammonia, and nitrite concentrations were monitored regularly. Approximately 20%-30% of the pond water was exchanged every 15-20 days depending on the water quality. The change in water temperature is shown in Figure 1.

Crab Sampling and Data Collection

A total of 20-41 crabs were randomly captured from two ponds in each month during June 2016 to March 2017. The crabs were weighed to the nearest 0.01 g after removing any excess water with a paper towel. The carapace width (CW) was measured with a digital vernier caliper (E0552; ENDURA, China, precision = 0.01 mm). Gain rate of body weight (G[R.sub.W]), gain rate of carapace width (G[R.sub.c]), specific growth rate of body weight (SG[R.sub.W]) and specific growth rate of carapace width (SG[R.sub.c]) were used as growth indices, using the following formulae,

[mathematical expression not reproducible]

where [W.sub.t] is the mean crab body weight (BW) at the sampling occasion and [W.sub.t-1] is the mean crab BW of the last sampling occasion; [C.sub.t] and [C.sub.t-1] are the average CW at the initial and final sampling, respectively; d is the number of days between two sampling occasion.

From the mid-September to the mid-March of next year, sampling was performed every month for observation of gonadal development. After sampling, the crabs were measured for the CW and BW. Among these, live females were dissected to obtain the hepatopancreas and ovary, which were weighed for calculating the hepatosomatic index (HSI = 100 X hepatopancreas wet weight/crab body wet weight) and gonadosomatic index (GSI = 100 X gonad wet weight/crab body wet weight), respectively. A small portion of the ovary was fixed in Bouin's solution for histological analysis. The CW at which 50% (C[W.sub.50]) of females were sexually mature was estimated by fitting a logistic regression curve to the percentage of mature Portunus trituberculatus for each size class of 5 mm CW, as described by Johnson et al. (2010).

A small number of female crabs started their pubertal molt in early August 2016. Therefore, the proportion of females that completed their pubertal molts was recorded each month after August. Approximately 20-41 crabs were randomly sampled monthly from two ponds to calculate the percentage of females that completed their pubertal molts. Identification of the pubertal molt was based on the abdominal shape of female Portunus trituberculatus (Xuan et al. 2014). Briefly, for juvenile/preadult females (uncompleted pubertal molt), the shape of the pleonal flap was triangular, whereas the shape of pleonal flap for adult females (completed pubertal molt) was oval.

After 24 h of fixation, the ovaries were taken out for histological section and hematoxylin-eosin staining (Meeratana & Sobhon 2007). The histological observations and measurements were made under a light microscope (Leica DM2500; Leica Microsystems, Inc., Bannockburn, IL). Based on the studies of Okumura and Aida (2000) and Zhu et al. (2005), the gametocytes of Portunus trituberculatus were classified into six categories: oogonia (OG), previtellogenic oocyte (PRO), endogenous vitellogenic oocyte (EN), exogenous vitellogenic oocyte (EX), near-mature oocyte (NO), and mature oocyte (MO). The OG were small and nearly round and it had a large nucleus, which occupied most of the cell volume, the PRO had an ellipsed shape with strongly basophilic cytoplasm, the EN was irregular and located on the periphery of the PRO and its cytoplasm was also strongly basophilic, the EX was nearly round or oval in shape with eosinophilic cytoplasm, the NO was nearly round and yolk granules (YG) became apparent in the entire cytoplasm, the MO was round, and the YG were distributed evenly in the entire cytoplasm of MO; however, the nucleus was located peripherally and was not easily recognized (Okumura & Aida 2000, Zhu et al. 2005). According to the GSI and ovarian histology, the ovarian staging of monthly samples was grouped, and the percentage of each ovarian stage was calculated for all samples at each month. Between eight and 10 ovaries were histologically examined for ovarian stage and for calculating GSI and HSI. In addition, the mean GSI and oocyte diameters of mature wild female P. trituberculatus were also obtained from a previous report (Wu et al. 2007) and were used to compare the differences in ovarian development between pond-reared and wild crabs.

Statistical Analysis

The data are presented as mean [+ or -] SE. Homogeneity of variance of the data was tested with Levene's test. When necessary, an arcsine square root or logarithmic transformation was performed before analysis. Differences at P < 0.05 were considered statistically significant. When the data were homogeneous and normally distributed, a one-way analysis of variance was used to determine if significant differences existed among months or ovarian stages for the various parameters; if any significant difference was detected, Tukey's multiple range test was used as the means separation procedure. When the data were not normally distributed or the variances were not homogeneous, data from different months or ovarian stages were subjected to the Kruskal-Wallis H nonparametric test, followed by the Games-Howell nonparametric multiple comparison test. The Pearson chi-square test was used to determine the statistical significance of the relationship between months/ovarian stages and different biological parameters measured. Student's t-test was used to examine the differences between pond-cultured females and wild-caught females. All statistics were performed using an SPSS statistic package (version 18.0).

RESULTS

Growth Performance

The increase of BW and CW of pond-reared Portunus trituberculatus mainly occurred during June to October (Table 1). The highest G[R.sub.W] reached nearly 318.96% during June to July, whereas the lowest G[R.sub.W] 16.63% was found during September to October (Fig. 2A). In general, changes to female G[R.sub.c] each month were similar to that of G[R.sub.W]; however, the increase of G[R.sub.c] was much lower than that of G[R.sub.W] (Fig. 2B). Furthermore, the specific growth rate pattern was also similar to that of the growth rate; it reached the highest and lowest values in June to July and September to October, respectively (Fig. 3). The overall average of SG[R.sub.W] was 2.53; nevertheless, the overall SG[R.sub.c] average was 0.98 during the pond culture period of P. trituberculatus. The CW at which 50% of females were mature (C[W.sub.50]) was estimated to be 110.2 mm (Fig. 4).

Changes in Ovarian Histology, GSI, and HSI during Ovarian Development

Based on changes in ovarian histology, ovarian development of pond-reared Portunus trituberculatus was divided into five stages. The main characteristics of each stage were as follows. In stage I, the cytoplasm was strongly basophilic for all types of gametocytes (Fig. 5A) and the GSI ranged from 0.14 to 0.54. The dominant types of gametocytes in the early-stage-I ovary were OG with a mean length of 9.70 [+ or -] 0.17 [micro]m. A large amount of PRO but small amounts of EN were present in the ovaries at the end of stage I (Fig. 5B). In stage II, the cytoplasm was also strongly basophilic for all gametocyte types (Fig. 5C) and the GSI ranged from 0.41 to 1.17. The dominant gametocyte types in the stage-II ovary were EN with a mean length of 49.19 [+ or -] 0.68 [micro]m and PRO with a mean length of 28.47 [+ or -] 0.44 [micro]m (Fig. 5C). In stage III, the dominant gametocyte type was EX and the GSI ranged from 0.92 to 4.91. Yolk granules were present in the EX and the cytoplasm in the oocytes transformed from basophilic to eosinophilic. Furthermore, only a small amount of irregularly shaped EN was visible in the middle zone of the ovarian lobules (Fig. 5D). The mean length of EX was 113.54 [+ or -] 1.52 [micro]m. In stage IV, many YG were present in the NO and the cytoplasm was still eosinophilic (Fig. 5E). The mean length of NO was 245.32 [+ or -] 2.05 urn and the GSI at this stage ranged from 3.38 to 7.80. In stage V, the dominant gametocyte type was MO (Fig. 5F) and the YG were distributed evenly in the entire cytoplasm; however, the nucleus was located peripherally and it was not easily recognized. The mean length of MO was 324.88 [+ or -] 2.97 [micro]m and the GSI ranged from 6.20 to 8.94.

Figure 6 shows that the GSI increased significantly during ovarian maturation and increased up to 7.94% in ovarian stage V. It was noteworthy that the GSI increased by 5.7 times (570%) from ovarian stage I to III during the early development period; however, the GSI increased only by 2.6 times (260%) from ovarian stage IV to V. Hepatosomatic index showed a slow decrease trend during ovarian maturation. The highest HSI was found at ovarian stage I, whereas HSI of ovarian stage V had the lowest values among the five stages.

Monthly Variation of Pubertal Molt, Ovarian Stages, and GSI

Figure 7 showed that only 13% of pond-reared females finished their pubertal molt in mid-August. A total of 78.05% females finished pubertal molt in mid-September. All sampled crabs finished their pubertal molt in mid-October. As shown in Table 2, the ovaries of pond-reared female Portunus trituberculatus were mainly at stage I and only 13.33% of females were at ovarian stage II in mid-August. At this time, most crabs had not finished their pubertal molt. By the end of September, the ovarian development of females was mainly in ovarian stage II. Subsequently, the females entered rapidly developed, with 43.24% being in ovarian stage III by the end of October. At the end of November, the ovarian development was mainly in ovarian stage III (82.86%) and the mean GSI increased significantly to 2.57%. From December to late January, the crabs were mainly in ovarian stage III and IV and the mean GSI increased significantly to 2.72%. A small number of crabs (3.85%) developed their ovaries to stage V in December. By the end of February, the percentage of female ovaries at stage III was significantly reduced to 15% compared with that in January and the percentage of females at ovarian stage IV increased to 85%. At this time, the GSI increased significantly to 5.25%. The crabs were mainly in ovarian stage IV (52.17%) and ovarian stage V (26.09%) and the GSI was further increased by the end of March sampling. Moreover, a small percentage of berried crabs were found in the pond at mid-March sampling. During the ovarian development cycle of Portunus trituberculatus, the HSI showed a slightly decreasing trend.

DISCUSSION

The Growth Pattern of Pond-Cultured Portunus trituberculatus The growth of Portunus trituberculatus depends on molting frequency and associated size increments at each molt (Gao et al. 2016). Previous studies have reported the growth of P. trituberculatus in earthen ponds and cement tanks, but possible gender differences were not considered (Sun et al. 1984, Wang et al. 2014). Female P. trituberculatus with fully developed ovaries have a high edible yield, and current aquaculture practices generally have high percentage of females. Their growth pattern in ponds, however, remained unclear. In the present study, the results indicated that the G[R.sub.W] of pondreared females was greater than 100% during each monthly interval from June to September and the G[R.sub.W] peaked at 318.96% during June and July. This indicates that these crabs grow faster from June through September. The lowest G[R.sub.W] was found during September and October. Possibly, when the females completed their pubertal molt, nutrients and energy were mainly used for the ovarian development. The G[R.sub.W] during the early ovarian stage (June to September) was significantly greater than that of the later stage (September to November), similarly to other crustaceans (Wu et al. 2012). A shorter molt interval during the early stage rather than the late stage may have led to faster growth (Gao et al. 2016).

The Ovarian Development Pattern of Pond-Cultured Portunus trituberculatus

It is generally believed that the pubertal molt is the start of ovarian development in crabs, and that subsequently, females begin to develop their ovaries rapidly (Liu et al. 2014). In this study, the pubertal molt of pond-cultured female Portunus trituberculatus mainly occurred from mid-August to early September, which was earlier than wild crabs. Moreover, the rapid ovarian development of pond-cultured females occurred during October to February of the following year and matured females were found at the end of February. Therefore, the entire ovarian development process lasted around 6 mo. Rapid ovarian development period of wild females, however, occurs from November to March of the next year and the period of the entire ovarian development process was 7 mo (Wu et al. 2007). Possible reasons for the earlier pubertal molt and faster ovarian development in pond-cultured crabs could include higher water temperatures and more abundant food than sea regions. This has also been observed in pond-cultured shrimp Penaeus kerathurus (Medina et al. 1996). In addition, ovarian development started before the pubertal molt in pond-cultured females and the highest GSI reached 1.09%. This is inconsistent with a previous view that "the female P. trituberculatus do not develop their ovaries before pubertal molt (Wu et al. 1996)," which indicates that this prior view was not accurate.

The present study showed that ovigerous crabs were found in mid-March. In one study, however, crabs began from mid-late April under natural temperature conditions (Hamasaki et al. 2004). Therefore, appropriate times for broodstock selection of pond-cultured Portunus trituberculatus should be before the end of February. Furthermore, the GSI and the oocyte diameter of pond-cultured females were much lower than that of wild females (Fig. 8). Precocity of pond-cultured P. trituberculatus has been observed and suggested to be related to higher temperatures and food abundance (Liu et al. 1999). Therefore, the nutritional requirements of females need to be further studied during the ovarian development period; high-quality food should be fed to crabs during their early ovarian development to mature ovarian stage for female P. trituberculatus, which could promote ovarian development and enhance the reproductive performance of pond-cultured broodstock.

Application of Growth and Ovarian Development Pattern

The present study showed a peak of growth, and pubertal molts in pond-cultured females mainly occurred during June to July and mid-late August to early September. If appropriate and sufficient shelters are provided in the pond, this could reduce cannibalism and thus improve crab survival during the pubertal molts (He et al. 2016). Previous studies have shown large differences regarding the nutritional requirements between the growth and ovarian developmental stage of Portunus trituberculatus. Generally, juvenile P. trituberculatus require high dietary protein levels and low dietary lipids contents (Jin et al. 2015), whereas females during ovarian development need high dietary lipids but moderate amounts of dietary protein (Ding et al. 2017). Therefore, during the rapid growth period of pond-cultured female P. trituberculatus from June to September, the females should be fed on high-protein-formulated diets (Jin et al. 2015, Wang et al. 2016), whereas the diets with high lipids may promote ovarian development of this species (Ding et al. 2017).

The ovary and hepatopancreas are the two main edible parts of females; therefore, the status of their gonadal development directly affects their food values and market price (Jiang et al. 2014). Generally, female Portunus trituberculatus with GSI values of more than 4% could be sold as high-value products (Xie et al. 2002). The results of this study showed that 23% of the females developed their ovaries to stage IV by the end of December, which could be sold at market. By the end of February, most of the females developed into the ovarian stage IV, which had the highest GSI and edible yields. After that, the females started to spawn, which decreases their edible value.

In conclusion, the growth of pond-cultured Portunus trituberculatus females mainly occurred during June to October and fast ovarian maturation was found during October to February in the following year. Pond-reared P. trituberculatus females developed their ovaries to become mature at the end of February. Both the pubertal molt and ovarian maturation time of pond-cultured female P. trituberculatus were earlier than that of the wild crabs. These results provide valuable information for the culture management, feeding practice, and marketing time of P. trituberculatus.

ACKNOWLEDGMENTS

This study was funded by a research and extension project (No. 2016-1-18) from Shanghai Agriculture Committee, a special research project for North Jiangsu area from Science and Technology Department of Jiangsu province (No. SZ-LYG2017019) and a project (No. 41276158) from the Natural Science Foundation of China. Infrastructure costs were partially supported by the Shanghai Universities Top Disciplines Project of Fisheries (No. 2015-0908) from Shanghai Municipal Education Committee and Collaborative Innovation Project for Mariculture industry in East China Sea from Ningbo University. The authors would like to thank Dr. Nicholas Romano from University of Arkansas at Pine Bluff, AR, for proofreading and language correction.

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JIE CHE, (1[dagger]) MEIMEI LIU, (1[dagger]) ZHIGUO DONG, (2*) WENJIE HOU, (3) GUIPING PAN (3) AND XUGAN WU (1,4,5*)

(1) Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, No. 999, Shanghai City Ring Road, Nanhui New Town, Pudong New Area, Shanghai 201306, China; (2) Key Laboratory of Marine Biotechnology of Jiangsu Province, Huaihai Institute of Technology, No. 59, Cangwu Road, Haizhou District, Lianyungang 222005, China; (3) Shanghai Fisheries Research Institute, Shanghai Fisheries Technical Extension Station, No. 265 Jiamusi Road, Yangpu District, Shanghai 200433, China; (4) Centre for Research on Environmental Ecology and Fish Nutrition of Ministry of Agriculture, Shanghai Ocean University, No. 999, Shanghai City Ring Road, Nanhui New Town, Pudong New Area, Shanghai 201306, China; (5) National Demonstration Centre for Experimental Fisheries Science Education, Shanghai Ocean University, No. 999, Shanghai City Ring Road, Nanhui New Town, Pudong New Area, Shanghai 201306, China

(*) Corresponding authors. E-mails: wuxugan@hotmail.com or dzg7712(a)yahoo.com.cn

([dagger]) These authors contributed equally to this work.

DOI: 10.2983/035.037.0308
TABLE 1. Changes in BW and CW during the adult culture stage of
pond-cultured female Portunus trituberculatus.

Month      Sample
           number           BW(g)                     CW (mm)

June       43        8.69 [+ or -] 0.59 (e)   35.57 [+ or -] 1.85 (e)
July       36       36.39 [+ or -] 1.89 (d)   66.29 [+ or -] 1.13 (d)
August     30       69.18 [+ or -] 1.38 (c)   83.05 [+ or -] 0.67 (c)
September  41      153.23 [+ or -] 3.52 (b)  109.62 [+ or -] 0.97 (b)
October    37      178.70 [+ or -] 5.04 (a)  116.91 [+ or -] 1.48 (a)
November   35      180.90 [+ or -] 4.80 (a)  117.03 [+ or -] 0.88 (a)
December   26      183.79 [+ or -] 6.39 (a)  117.15 [+ or -] 1.64 (a)

Values are presented as mean [+ or -] SE. Different superscript letters
within the same column indicate significant differences (P < 0.05).

TABLE 2. The ovarian stages, GSI, and HSI of female Portunus
trituberculatus during the different months of pond culture process.

Month      Sample number  I      II     III    IV     V

August     30             86.67  13.33  -      -      -
September  41             21.95  75.61   2.44  -      -
October    57             -      56.76  43.24  -      -
November   35             -       5.71  82.86  11.43
December   26             -      15.38  57.69  23.08   3.85
January    24             -      -      79.17  20.83  -
February   20             -      -      15.00  85.00  -
March      23             -      -      21.74  52.17  26.09

Month      GSI (%)                 HSI (%)

August     -                       -
September  0.86 [+ or -] 0.05 (c)  7.24 [+ or -] 0.35 (a)
October    1.07 [+ or -] 0.09 (c)  4.55 [+ or -] 0.38 (b)
November   2.57 [+ or -] 0.27 (b)  5.22 [+ or -] 0.39 (b)
December   2.55 [+ or -] 0.48 (b)  4.87 [+ or -] 0.32 (b)
January    2.72 [+ or -] 0.33 (b)  4.87 [+ or -] 0.27 (b)
February   5.25 [+ or -] 0.38 (a)  6.76 [+ or -] 0.17 (a)
March      5.65 [+ or -] 0.44 (a)  4.75 [+ or -] 0.29 (b)

The values of GSI and HSI are presented as mean [+ or -] SE. Different
superscript letters within the same column indicate significant
differences (P < 0.05).
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Author:Che, Jie; Liu, Meimei; Dong, Zhiguo; Hou, Wenjie; Pan, Guiping; Wu, Xugan
Publication:Journal of Shellfish Research
Article Type:Report
Date:Aug 1, 2018
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