Nitrogen and Phosphorus Budget of a Polyculture System of Sea Cucumber (Apostichopus japonicus), Jellyfish (Rhopilema esculenta) and Shrimp (Fenneropenaeus chinensis)

LI Junwei, DONG Shuanglin, GAO Qinfeng and ZHU Changbo

1) Key Laboratory of Mariculture of Ministry of Education of China, Ocean University of China, Qingdao 266003, P. R. China

2) Key Laboratory of South China Sea Fishery Resources Exploitation & Utilization of Ministry of Agriculture of China, South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510300, P. R. China

Nitrogen and Phosphorus Budget of a Polyculture System of Sea Cucumber (Apostichopus japonicus), Jellyfish (Rhopilema esculenta) and Shrimp (Fenneropenaeus chinensis)

LI Junwei1),2), DONG Shuanglin1),*, GAO Qinfeng1), and ZHU Changbo2)

1) Key Laboratory of Mariculture of Ministry of Education of China, Ocean University of China, Qingdao 266003, P. R. China

2) Key Laboratory of South China Sea Fishery Resources Exploitation & Utilization of Ministry of Agriculture of China, South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510300, P. R. China

The nitrogen (N) and phosphorus (P) budget and the ecological efficiency of a polyculture system of sea cucumber (Apostichopus japonicus), jellyfish (Rhopilema esculenta) and shrimp (Fenneropenaeus chinensis) were studied in a cofferdam, 120.2 ha in size. The nutrients were supplied by spring tide inflow. In total, 139600 kg N yr-1and 9730 kg P yr-1input to the system; while 118900 kg N yr-1and 2840 kg P yr-1outflowed from the system concurrently, thus the outflow was 85.7% (N) and 29.2% (P) of inflow. The production of N and P was 889.5 kg yr-1and 49.28 kg yr-1(sea cucumber) and 204 kg yr-1and 18.03 kg yr-1(jellyfish and shrimp), respectively. The utilization rate of N and P by polycultured animals was 7.8‰ and 6.9‰, respectively, 21.9% and 38% higher than that of monocultured sea cucumber. Our results indicated that the polyculture system was an efficient culture system of animals and a remediation system of coastal environment as well; it scavenged 14.3% and 70.8% of N and P, respectively. Such an ecological efficiency may be improved further by increasing either the stocking density or the size of sea cucumber or both.

polyculture; nitrogen budget; phosphorus budget;Apostichopus japonicus;Rhopilema esculenta;Fenneropenaeus chinensis

1 Introduction

Sea cucumber (Apostichopus japonicusSelenka) is one of the most commercially important maricultured species in China. Its total production has reached 130000 tons in 2010 (Fisheries Department of Agriculture Ministry of China, 2011). Sea cucumber is a deposit feeder which ingests sediment, diatom, macroalgae and benthic animals (Yingst, 1982; Dame and Dankers, 1988; Inuiet al., 1991; Wu, 1995; Zhanget al., 1995; Ramofafia, 1997); thus is generally cultured in ponds with no artificial diet fed. However, the monoculture of sea cucumber cannot sufficiently utilize various natural foods due to its benthic feeding behavior.A. japonicuscannot utilize the plankton directly, and goes into aestivation while temperature is over 20℃ (Yanget al., 2005; Baoet al., 2010). It has been confirmed that the aquatic production and food utilization can be improved by polyculturing sea cucumber with other animals, and the negative influences of aquaculture on environment can be alleviated (Liet al., 2013). Binary cultures of sea cucumber with for example salmon (Ahlgren, 1998), abalone (Kanget al., 2003), scallops (Zhouet al., 2006; Renet al, 2012a), mussels (Matthew and Alexander, 2007), oysters (Paltzatet al., 2008), and shrimp (Qin, 2009) have been documented, in which sea cucumber can utilize the organic matter generated by co-cultured species, reducing the accumulation of biological sedimentation, and can grow well, playing a role in nitrogen and phosphorus reduction (Ahlgren, 1998; Kang, 2003; Zhouet al., 2006; Matthew, 2007). However, little is known about N and P budget and N and P utilization rate in these systems.

Jellyfish (Rhopilema esculentaKishinouye) feeds on zooplankton (Fancett and Jenkins, 1988) and accelerates the settling rate of particles, for example, faeces and dead zooplankton, which are high quality food of sea cucumber (Kringelet al., 2003; Tayloret al., 2005; Renet al., 2012b). During aestivation, sea cucumber stops feeding, wasting benthic foods. However, shrimp (Fenneropenaeus chinensisOsbeck) can utilize these foods once being co-cultured withA. japonicusin summer (Changet al., 2004; Qin, 2009). Theoretically, the polyculture ofA. japonicus,R. esculentaandF. chinensiscan make a full use of foods available in farming systems (Liet al., 2013).

The present study was conducted, aiming to explore the utilization ratio of N and P of polyculturedA. japonicus,R. esculentaandF. chinensisby means of N and P budget of the system. The findings may aid to understanding theenvironmental function of farming systems, and providing a basis for the development of a productive and environment friendly farming model.

2 Materials and Methods

2.1 Studying Location

This study was carried out at a cofferdam (36°86′N, 122°13′E) locating at Homey Aquatic Development Co., LTD, Rongcheng, Shandong, China from April, 2011 to April, 2012 (Fig.1). The cofferdam was about 120.2 ha (1881 m×639 m) with an average depth of 2.5 m. Ahead of studying, the water in the cofferdam was drained out with the bottom covered with polyethylene woven cloth (Hongtai plastic spinning Co., LTD, Wenzhou, China). The seawater in the cofferdam was routinely exchanged at a rate of 12% daily during spring tides.

Fig.1 Location of the studying area in Jinghai Bay and 10 sampling sites in a cofferdam.

2.2 Stocking and Harvesting

Juvenile sea cucumber individuals, 9.0 g ± 0.8 g in weight, were stocked at a density of 105ind. ha-1from April 16 to 22, 2011, and harvested from April 10 to 20, 2012. Juvenile jellyfish individuals, 1.21 g ± 0.5 g, were stocked at a density of 1200 ind. ha-1from June 22 to 24, and harvested from September 1 to 10, 2011. Juvenile shrimp individuals, 0.098 g ± 0.01 g, were stocked at a density of 59900 ind. ha-1from June 26 to 29, and harvested from September 11 to 16, 2011. Basically, no feed was provided during the studying period.

2.3 Sample Collection and Determination of Water, Sediment and Organisms

During the studying period, water sample was collected at 10 sites, 8 in the cofferdam, 1 at water inlet and 1 at water outlet, three times per month. The water was collected at 1–1.5 m depth using a 4 L PMMA water sampler (Yuanda Nikkor Corporation, Qingdao, China). During the period of a spring tide, inflow and outflow water was collected repeatedly and pooled. The amount of inflow and outflow water was measured with a flow velocity meter (LS-1206B, Haosheng Industry and Trade Co., LTD, Nanjing, China); while temperature, salinity and DO were measured with YSI (5000-230V, YSI Incorporated, Yellow Springs, OH, USA) at 10:00–11:00 am in each sampling sites, andin situacidity was measured with an acidometer (PHS-3C, Shanghai, China). The water was taken back to a laboratory nearby for the analysis of the concentrations of TN (total nitrogen), TP (total phosphorus), NO3-N, NO2-N and NH4-N within 10 h. TN was analyzed using the potassium peroxydisulfate oxidation method described early (Grasshoffet al., 1985). TP was analyzed according to Murphy and Riley (1962). NO3-N was determined with the cadmium-copper column reduction method (Grasshoffet al., 1985). NH4-N was determined with the blue indophenol method as was modified by Mantoura and Woodward (1983). NO2-N was determined after cadmium reduction as nitriteviadiazotation (Grasshoffet al., 1985). The chlacontent was determined with fluorescence automatic analyzer (Turner Designs 7200, USA) with the fluorescence method (National Standardization Management Council of China, 2007).

Eight sites were sampled for settling particles, which were along and about 200 m apart from the cofferdam. Three straight-sided cylindrical traps (110 mm in diameter; 550 mm in height) were used to collect settling particles at about 1.8 m depth each site. The trap was covered with a net, 0.5 cm in mesh size, to filter out large nekton and fish. Trap was set for 7 d and then taken back to laboratory. The water in trap was removed with a siphon after settling for 8 h. The particles was desalted with distilled water, and dried at 60℃ to a constant weight. Synchronically, the surface layer of sediment, 1 cm in thickness, was monthly collected with a cylindrical metal corer, 8 cm in diameter.

During the study period, the particles, sediment and cultured organisms collected from the system were dried at 60℃ to a constant weight, smashed and sieved with sample sifter. TN content of particles, sediment and organisms was determined with PE-24 CHN analyzer (Heraecus, Banau, Germany). TP content of the sediment was determined with the method of the blue indophenol method (Hu, 1999). TP content of the cultured animals was determined with the method of molybdenum yellow spectrophotometer (National Standardization Management Council of China, 2002).

2.4 Statistical Analysis

Data were analyzed using SPSS 13.0 for Windows. Difference in TN and TP content was tested through one-way ANOVA. Difference was significant ifP＜0.05.

3 Results

3.1 Quantity and Composition of TN and TP in Inflow and Outflow

The water temperature in the cof

ferdam fluctuated seasonally between -1.2℃ ± 0.05℃ in February and 29℃± 0.06℃ in August. Salinity varied between 26.5 ± 0.1 and 29.5 ± 0.2, and pH between 8.0 ± 0.1 and 8.4 ± 0.1. DOcontent was above 6.0 ± 0.05 mg L-1year round. Chlacontent varied between 0.69 ± 0.04 and 14.35 ± 0.06 μg L-1.

During the studying period, TN in inflow and outflow of the system was 138800 kg yr-1and 118900 kg yr-1, respectively; while TP was 9710 kg yr-1and 2840 kg yr-1, respectively. Outflow was cleaner than inflow; 14.3% of N and 70.8% of P was scavenged. The TN of inflow ranged from 3275 kg month-1in November and December to 29010 kg month-1in July (Table 1). Dissolved organic nitrogen (DON) was the main form of TN in the first 5 months of the study, and then either dissolved inorganic nitrogen (DIN) or the particle nitrogen (PN) evolved as the main form of TN (Fig.2a). The TN of outflow ranged from 2650 kg month-1in Dec. to 26450 kg month-1in July. DON was the main form in outflow in the first 6 months of study. TN of outflow was lower than that of inflow during the studying period (P＜0.05). The TP of inflow ranged from 110 kg month-1in Dec. to 2600 kg month-1in May (Fig.2b). The TP of outflow was less than that of inflow year round (Fig.2b). The difference varied between 86 kg month-1and 1685 kg month-1.

During the studying period, TN of the system varied between 1.39 and 2.62 mg L-1with an annual average of 2.12 mg L-1. TN in summer and autumn was higher than that in other months (Fig.2c). DIN increased gradually with NO3-N as the main form. NH4-N content was below 50.5 μg L-1all over the year, and NO2-N content was below 10 μg L-1. TP of the system varied between 0.025 and 0.064 mg L-1(Fig.2c) with an annual average of 0.04 mg L-1.

Table 1 TN, TP budgets of the integrated aquaculture system?

Fig.2 The amounts and/or contents of TN and TP in inflow, outflow and the water column. The values have been pooled each month. Values were given as mean ± SD (n=8). a: Inflow and outflow N in the cofferdam. DIN-inflow, DIN in inflow through spring tide; DON-inflow, DON in inflow. PN-inflow, particle nitrogen in inflow; DIN-outflow, DIN in outflow; DON-outflow, DON in outflow; PN-outflow, particle nitrogen in outflow. b: Inflow and outflow P in the cofferdam. TPi, phosphorus in inflow; TPo: phosphorus in outflow. c: TN and TP of water column in the sea cucumber culturing cofferdam.

3.2 Stocking and Harvesting of Cultured Animals

The stocking biomass ofA. japonicus,R.esculentaandF.chinensiswas 650, 1.5 and 5.85 kg ha-1, and their TN input was 2.62, 0.002 and 0.14 kg ha-1, respectively, whereas, their TP input was 0.156, 0.0001 and 0.01 kg ha-1, respectively. During the studying period, the harvest of sea cucumber was 125 kg ha-1, and the TN production was7.40 kg ha-1. The harvest of jellyfish was 1033 kg ha-1, and the TN accumulation was 1.70 kg ha-1. The harvest of the shrimp was 4.2 kg ha-1, and the TN accumulation was 0.09 kg ha-1. In addition, 6 kg of TN and 2 kg of TP of some non-stocked fishes were yielded. The TP production ofA. japonicus,R. esculentaandF. chinensiswere 0.42, 0.13 and 0.02 kg ha-1, respectively.

3.3 Settling Matter and Sediment Characteristics

The TN settling rate of sinking matter ranged from 26.75 to 408.2 mg m-2d-1with an annual average of 62.13 mg m-2d-1. The maximum occurred in September (Fig.3a), whereas the minimum was recorded in winter, which was different from the maximum significantly (P＜0.05). The TP settling rate ranged from 5.65 to 82.95 mg m-2d-1with an annual average of 37.33 mg m-2d-1and a maximum in autumn (Fig.3a). TN in the settling matter ranged from 1.83 to 3.91 mg g-1and the maximum occurred in September (Fig.3b). TP in the settling matter ranged from 0.58 to 0.79 mg g-1and the maximum occurred in September (Fig.3c). TN in the sediment ranged from 0.48 to 3.78 mg g-1, varing significantly among months (P＜0.05) (Fig.3b). TP in the sediment ranged from 0.5 to 0.68 mg g-1(Fig.3c) with an annual average of 0.57 mg g-1. It was noticed that TN in the settling matter was higher than that in the sediment during the studying period (P＜0.05). The ratio of TN/TP of the settling matter and sediment showed a rising trend, ranging from 3.2 to 6.9 and from 0.9 to 7.4, respectively (Fig.3d). In general, TN/TP in settling matter was higher than that in sediment (P＜0.05).

Fig.3 The characteristics of TN and TP in the settling matter and sediment in the cofferdam system. The values have been pooled each month. Value was expressed as mean ± SD (n=8). a: TN and TP settling velocity of the settling matter in the cofferdam. b: TN of the settling matter and sediment in the cofferdam. c: TP of the settling matter and sediment in the cofferdam. d: Ratio of TN/TP of the settling matter and sediment in the cofferdam.

4 Discussion

As a deposit feeder, sea cucumber can utilize the organic matter in sediment (Yingst, 1982; Inuiet al., 1991; Wu, 1995) and grow well only relying on the foods from tidal inflow (Qinet al., 2009; Renet al., 2010). However, the foods in water column and on the bottom of pond in summer will be wasted when sea cucumber was monocultured (Yanget al., 2005; Baoet al., 2010). In contrast, polyculturing sea cucumber with other species may solve the problem, improving the utilization rate of N and P. Our findings showed that TN and TP in outflow were 118900 kg yr-1and 2840 kg yr-1, respectively, accounting for 85.7% and 29.2% of TN and TP in inflow, respectively (Table 1). These findings indicated that polyculturing sea cucumber with jellyfish and shrimp is an efficient system and a remediating system as well for the coastal environment; it eliminated 14.3% of N and 70.8% of P.

The input and output of N and P in an aquaculture system consist of several components (Qiet al., 1998). Biological nitrogen fixation (BNF) was the important source of the input N when there are abundant blue-green algae (Howathet al., 1988; Qiet al., 1999a). In addition, the denitrification function is important to the output N when the water is under the anoxic condition (Briggs and Funge-Smith, 1994; Qiet al., 1999b). In the present study, the function of BNF and denitrification could be ignored;the water was under well-oxygenated condition with less blue-green algae. Qiet al. (1998) reported that the N and P loss through seepage accounted for 5% of the total output TN and 0.4% of the total output TP in a shrimp farming pond, 3000 m2in area. Because of the large cofferdam with muddy bottom, the N and P loss through seepage can be ignored in this study. The rainfall in the studying area was about 800 mm in 2011, and TN of the rain was about 0.48 mg L-1. Therefore TN from rainfall was about 468 kg, accounting for only 0.3% of the inflow TN and thus can be ignored. Regardless of the function of BNF, the input of N and P was mainly from the inflow, which was about 139600 kg N yr-1and 9730 kg P yr-1, respectively. The N and P production of sea cucumber in the system was 889.5 kg and 49.28 kg, and the TN and TP production of the jellyfish and shrimp were 204 kg and 18.03 kg. The N and P utilization rate of the input TN and TP in the polyculture system were 7.8‰ and 6.9‰, which were 21.9% and 38% higher than that of sea cucumber monoculture. The increase tendency of N and P utilization rate was similar to that of other study (Renet al., 2012b). The change of TN and TP in the sediment agreed with that of TN and TP in the settling matter (Figs.3b, c and d), indicating that the TN and TP in the sediment were affected by the settling matter directly.

The input N of the present system was 139600 kg yr-1, and the output N was 120000 kg yr-1(outflow+cultured organisms+wild fish). There was 19600 kg yr-1inflow N retained in the polyculture system. Moreover, the input TP of the present system was 9730 kg yr-1, and the output TP was 2910 kg yr-1(outflow+cultured organisms+wild fish), indicating that 6820 kg yr-1TP retained in the system. The TN content of the sediment increased from 0.48 to 3.79 mg g-1(Fig.3b) and the change was caused by the retaining function of the system. Though the TP content of the sediment did not change obviously, the amount of the sediment increased significantly, resulting in the TP accumulation in the system. The proportion of input N, P deposited into outlet water, sediment and different animals were 85.2%:14%:0.8% and 29.2%:70.1%:0.7%, respectively. The accumulation of the TN and TP in the sediment indicates that improvement of the N and P utilization rates within the system was an important way to improve environmental purification capacity of the system.

Although the TN and TP production of the polyculture system has improved in comparison with a monoculture system, it is still lower than that of other farming systems. The TN and TP conversion efficiency of input N and P in a polyculture system of shrimp, tilapia and razor clam was 23.4% and 14.7%, respectively (Tianet al., 2001), and the TN and TP utilization rate for the input N and P in the tilapia and Philippine clam system was 15.06% and 6.8%, respectively (Yanget al., 1998). TN and TP utilization rate of the present system may be improved through increment of stocking density and/or stocking size of the sea cucumber and shrimp.

Zhenget al. (2009) found that the feeding ofA. japonicuscan reduce the accumulation of inorganic nutrients in the sediment of farming waters. Renet al. (2010) also found that the TN and TP content in the sediment of sea cucumber farming waters increased during the period of sea cucumber aestivation, and decreased during their feeding period. The TN and TP content in the sediment was affected by the settling matter mostly, but the influence ofA. japonicusfeeding on N and P content of the sediment was not observed (Figs.3b, c and d). Enhancing the stocking density and/or the stocking size ofA. japonicusmay improve the utilization rate of the input N and P of the system. The stocking density of shrimp had no significant effect on the growth ofApostichopus japonicuswhen the stocking density ranged from 0 to 8 ind. m-2. The optimal stocking density of the shrimp in terms of net production was 14.1 ind. m-2for the non-feeding supplement regime (Qinet al., 2009). The stocking density of shrimp was 6 ind. m-2in the present system, which was far below the optimal density. Thus, increasing the shrimp stocking density is a way to improve the eco-efficiency of the integrated aquaculture system.

5 Conclusions

The good survival and growth of shrimp and jellyfish co-cultured with sea cucumber in this study indicated that they were suitable species for sea cucumber polyculture systems. Results also showed that such polyculture system was efficient for aquatic production and advantageous for the remediation of coastal environment as well. The ecological efficiency of such farming system may be improved further by increasing either the stocking density or the size of sea cucumber or both. However, further studies were needed to understand the effects of shrimp and jellyfish stocking density on the TN and TP utilization of this polyculture system.

Acknowledgements

This work was supported by the National Key R & D Program (2011BAD13B03) and National Marine Public Welfare Project of China (200905020).

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(Edited by Qiu Yantao)

(Received October 19, 2012; revised December 17, 2012; accepted November 21, 2013)

? Ocean University of China, Science Press and Spring-Verlag Berlin Heidelberg 2014

* Corresponding author. Tel: 0086-532-66782799 E-mail: dongsl@ouc.edu.cn