Life Cycle Assessment of Different Sea Cucumber (Apostichopus japonicus Selenka) Farming Systems

WANG Guodong, DONG Shuanglin, *, TIAN Xiangli, GAO Qinfeng, WANG Fang,and XU Kefeng

?

Life Cycle Assessment of Different Sea Cucumber (Selenka) Farming Systems

WANG Guodong1), DONG Shuanglin1), *, TIAN Xiangli1), GAO Qinfeng1), WANG Fang1),and XU Kefeng2)

1),,,266003,2),266071,

The life cycle assessment was employed to evaluate the environmental impacts of three farming systems (indoor intensive, semi-intensive and extensive systems) of sea cucumber living near Qingdao, China, which can effectively overcome the interference of inaccurate background parameters caused by the diversity of economic level and environment in different regions. Six indicators entailing global warming potential (1.86E+04, 3.45E+03, 2.36E+02), eutrophication potential (6.65E+01, ?1.24E+02, ?1.65E+02), acidification potential (1.93E+02, 4.33E+01, 1.30E+00), photochemical oxidant formation potential (2.35E?01, 5.46E ?02, 2.53E?03), human toxicity potential (2.47E+00, 6.08E?01, 4.91E+00) and energy use (3.36E+05, 1.27E+04, 1.48E+03) were introduced in the current study. It was found that all environmental indicators in the indoor intensive farming system were much higher than those in semi-intensive and extensive farming systems because of the dominant role of energy input, while energy input also contributed as the leading cause factor for most of the indicators in the semi-intensive farming system. Yet in the extensive farming system, infrastructure materials played a major role. Through a comprehensive comparison of the three farming systems, it was concluded that income per unit area of indoor intensive farming system was much higher than those of semi-intensive and extensive farming systems. However, the extensive farming system was the most sustainable one. Moreover, adequate measures were proposed, respectively, to improve the environmental sustainability of each farming system in the present study.

; life cycle assessment; environmental impact; sustainability evaluation

1 Introduction

China is the largest player of aquaculture in the world in terms of both volume and total economic value (FAO, 2012). The aquaculture industry in China is developing with a strong momentum of increasing number of farming species along with constant improving of trophic and intensification levels. However, intensive aquaculture is a double-edged sword with both high productivity and high energy consumption (Tacon and Forster, 2003; Dong, 2011). It is, therefore, necessary to have a more holistic understanding on the sustainability of aquaculture intensification (Dong, 2009).

Life cycle assessment (LCA) is an internationally standardized method (ISO14040-14044, 2006) for determining the environmental impact of the process of manufacturing and relevant activities. It’s an effective way of comparing the sustainability of different production systems through identifying and quantifying the energy and material inputs along with the resulting environmental waste discharge or emission to evaluate the impact on the environment. ‘Life cycle’ implies the assessment on all the phases in the process of products manufacturing, including the production of raw materials and energy, products, manufacture, transportation and use of raw materials and energy, as well as disposal and recycling use of the ultimate waste. In addition, as an important tool for environmental management, LCA is not only applied to assessing the environmental issues concerning ‘life cycle’ of products, but also providing the theoretical basis for the decision-making for sustainable development. Thus the performance of the products, the industry and even the behaviors of the industrial chain will be more in compliance with the principle of sustainable development (Guinée., 2002).

LCA has been widely applied to the packaging industry (Bonifaz, 1996), construction trade (Rivela., 2002), material manufacturing (Ibbotson and Kara, 2013), and other industries including aquaculture in recent years (Papatryphon., 2004; Aubin., 2009; Pelletier., 2009; Samuel., 2013). Aubin. (2009) investigated three kinds of finfish with LCA: rainbow trout () in France, sea-bass () in Greece, and turbot () in France. Pelletier (2009) studied one species of Atlantic salmon () that was farmed with a wide distribution of Norway, the UK, British Columbia (Canada), and Chile. LCA was used in the above cases for the purpose of comparing the environmental impacts among diverse species or different regions, which may be affected by their biological characteristics (feeding habits) or the social economic background of the aquaculture activities. Theoretically, the sustainability of different farming systems will be better illustrated if within one system the same species is focused in the same region with various intensification levels being selected.

Sea cucumber (Selenka) farming has been developed rapidly in northeast Asia in recent years for its high commercial value (Okorie., 2008). In 2010, the total production of sea cucumber reached 130000 tons, which brought about an output value of 20 billion Yuan (RMB) in China (MOAC, 2011). At present, land-based sea cucumber farming systems mainly include indoor intensive, semi-intensive, and extensive farming systems. Many farmers prefer to adopt indoor semi-in- tensive or intensive farming systems with artificial feed to improve the yield of sea cucumber. As those patterns increase the inputs of supplemental energy and organic matter, the sustainability of such farming system has drawn more attentions of the public (Ren., 2012). The environmental impacts of indoor intensive, semi- intensive, and extensive farming systems of sea cucumber near Qingdao, China, were evaluated through comparing and quantifying the energy and material inputs, and the resulting environmental waste outputs. The study evaluated the sustainability of the farming systems with different intensification levels in order to provide a theoretical foundation for developing resource-saving and environment-friendly sea cucumber farming systems.

2 Materials and Methods

2.1 System Description

Three sea cucumber farming systems near Qingdao, Shandong Province, China, were assessed in the present study. The indoor intensive farming system was housed in a barn constructed with concrete, brick, galvanized steel, polyethylene sheets, and polyechloride pipes. Indoor sea cucumbers were reared in 20 square concrete tanks (approximately 25m2in area, 1m in water depth) in a stocking density of about 1.250kgm?2. The sea cucumbers were fed twice a day with commercial feed. Polyethylene corrugated sheets were used as a substrate for the sea cucumbers. Aeration was provided continuously to maintain adequate dissolved oxygen. Fresh seawater was pumped into the tanks from an adjacent seawater channel. Seasonal coal heating was employed to maintain optimum water temperatures of this system.

The earthen ponds of the semi-intensive farming system were mainly confined in the intertidal zone, and relied on the tides for water exchange. Wastewater was drained out of the ponds through a specially designed outlet that was constructed with concrete, brick and stain- less steel floodgate. Each earthen pond covered a water area of about 40000m2, with an average water depth of 1.5m. Polyethylene cages were used as substrates of the sea cucumbers. The producers of the semi-intensive farm- ing system relied on the tides and sediment accumulation to provide most of the food for the sea cucumbers, with formulated feed as a supplementary source of nutrition. The stocking density was about 0.050kgm?2. Aeration was used discontinuously to provide adequate oxygen for the sea cucumbers.

The extensive farming system was similar to the semi- intensive system, but was operated without artificial feeding and aerators. The stocking density of this system was about 0.046kgm?2.

2.2 Life Cycle Assessment

According to the internationally standardized method (ISO 14040-14044, 2006), LCA in the present study was divided into 4 steps: definition of the goal and scopes, analysis of the life cycle inventory, impact assessment, and interpretation of the results (Fig.1). Each step was described in details below.

Fig.1 Management of life cycle assessment procedure.

2.3 Data Collection

LCA was carried out using the data provided by workers in the three farming systems during the two-year work. The sample used for this study was a group of 4 intensive, 3 semi-intensive, and 2 extensive farming systems. For each item, raw materials input and energy production, manufacturing, transportation and emissions were evaluated from manufacture to the end use. The consumption and emission data were then aggregated into impact categories on global and regional scales using characterization factors. The life cycle impact assessment was conducted by the use of LCA software package Simapro 7.0 from PRé consultants (PRé Consultants, 2006).

3 Results and Discussion

3.1 Definition of the Scope

Due to different economic levels in various regions around the globe, as well as differing natural conditions such as climate and geography, the regional parameters of production and service might not be for universal use. Moreover, the comparison based on results of the assessment may vary owing to different biological features of farmed species. Ayer and Tyedmers (2009) compared the potential environmental impacts of three Atlantic salmon farming systems in western Canada, and one Arctic char () farming system in south eastern Canada. Because of the difference in geography and economic levels, the farming systems differ completely in the types of energy sources. In the present study, LCA was used to evaluate three land-based farming systems for sea cucumbers in the same region (Qingdao, China), which can reduce the interference of indeterminate regional parameters, and avoid the influence of feed and farming environment caused by species-specific differences.

The aim of the study was to seek out the differences of the environmental impacts on the three land-based farming systems of sea cucumbers in terms of energy consumption and environmental impacts. Therefore, the scope of the study was defined as the process from fingerlings to farm-gate, including constructions of farms (mainly made of concrete, steel, polyechloride, polyethylene and brick), sea cucumbers farming, energy consumption (electricity, coal and diesel) and waste emission (CO2, CO, NOX, SO2, COD, CH4, N and P),. (Fig.2). Because there was no difference in terms of the subsequent processing, wholesale and retailing, as well as preparation and disposal of the sea cucumbers, they were not quantified in this study. The functional unit of the present study was 1 ton sea cucumbers of live-weight (Brentrup., 2001). It was assumed that the same conventional sea cucumber feed (with 16% protein, 4% lipid and 36% ash, approximately) was used in this study, and that the fingerlings of sea cucumbers were reared with same hatchery procedures.

Fig.2 Life cycle flow chart for sea cucumber farming.

3.2 Analysis on the Life Cycle Inventory

The inventory analysis is a process of collecting the data for each of these processes, performing allocation steps for multifunctional processes, and completing the final calculations (Guinée., 2002). In the present study, the primary data were collected to quantify the inputs and outputs associated with each of the sea cucumber farming systems (Table 1). The indoor intensive farming system was built by materials as concretes, steels, polyechloride, polyethylene and bricks, while the semi- intensive and extensive farming systems were simply built with a small amount use of such materials as concretes, steels, polyethylene and bricks. It was supposed in the study that the depreciation periods of concrete was 10 years, steel 10 years, brick 10 years, polyechloride 4 years and polyethylene 4 years in the three farming systems.

Electric power was mainly used for pumping and aerating water in the indoor intensive farming system, which also employed the coal heaters to maintain adequate temperature in the low-temperature seasons. Diesel was mainly applied for generation of electric power in the case of power failure. Compared with the indoor intensive farming system, no polyechloride and coal were used in the semi-intensive farming system, and no polyechloride, feeds, electricity and coal were used in the extensive farming system. It was presumed that the radius for trans- portation of infrastructure materials was within 50km in all three farming systems.

Table 1 Inputs and outputs for the production of 1 ton sea cucumber from the three farming systems analyzed

3.3 Life Cycle Impact Assessment

Life cycle impact assessment is the phase in which the set of results of the inventory analysis is further processed and interpreted in terms of environmental impacts and societal preferences of the studied product system (Gui- née., 2002). To this end, suitable category indicators for the impacts were selected according to ISO guidelines. The environmental impact indicators quantified in this study were global warming potential (GWP), eutrophication potential (EP), acidification potential (AP), photochemical oxidant formation potential (POFP), human toxicity potential (HTP), and energy use (EU). According to the purpose of the present study, those essential procedures for assessment including firstly selecting impact categories, determining the indicators for each category, and identifying the characterization models; then classifying the results of life cycle inventory analysis, and finally calculating the results of the category indicators, which were all carried out step by step. Yet the selective processes like normalization, grouping, weighing and data quality analysis were not adopted. Midpoint CML baseline method was employed to analyze the impacts (Guinée., 2002).

The results of LCA of the three sea cucumber farming systems and the contribution of the different components of environmental impacts were shown in Table 2, Fig.3.

Table 2 Life cycle impacts associated with the production of 1 t sea cucumber from the three farming systems analyzed

Notes: GWP: global warming potential; EP: eutrophication potential; AP: acidification potential; POFP: photochemical oxidant formation potential; HTP: human toxicity potential; EU: energy use.

Fig.3 Comparison of the life cycle contributions to environmental impact categories for the three sea cucumber farming systems. GWP, global warming potential; EP, eutrophication potential; AP, acidification potential; POFP, photochemical oxidant formation potential; HTP, human toxicity potential; EU, energy use.

The global warming potential (GWP) was introduced to evaluate the impact of gaseous emissions including CO2, CH4and N2O, which may cause greenhouse effect through absorbing infrared radiation from the atmosphere (Houghton, 1996). It was expressed in kg CO2-equiva- lents. As demonstrated in Table 2, Figs.4–6, in the indoor intensive farming system, energy consumption was the major factor for GWP, which reached 65%, followed by infrastructure materials, 27% of GWP, and feed, 8% of GWP. The coal was the primary source for energy consumption while the others rely on electric power. The same trend was observed in the semi-intensive farming system with the energy consumption, infrastructure materials and feed contributing 90%, 8% and 2% for GWP, respectively. However, the overall GWP of the indoor intensive farming system was 5.4 times as high as that of the semi-intensive farming system judged from the values. The main reason is that no coal was used in the later system. In terms of the extensive farming system, its GWP was 78.8 times lower than that of the indoor intensive farming system, mainly because no coal, electricity or feed were used. It was also because of this that the contribution of energy consumption to GWP in the extensive farming system was reduced to only 4%, yet the infrastructure materials covered the largest proportion of 96%.

The eutrophication potential (EP) covered the potential environmental impacts of all macronutrients with nitrogen (N) and phosphorus (P) topping the list. They would lead to eutrophication of the surrounding environment. It was expressed in kg PO4-equivalents. Nutrient enrichment might cause an undesirable imbalance in the composition of species and a sharp increase of biomass production. In the aquatic ecosystems, increased biomass production might lead to decrease of dissolved oxygen levels, as the additional biomass consumed more oxygen for decomposition. It was found that feed was the major contributor (97%) to EP in the indoor intensive farming system (Table 2, Figs.4–6). On the contrary, EP demonstrated a falling momentum in both the semi-intensive and extensive farming systems. Previous studies approved that the total nitrogen and total phosphorus in the inflow water in earthen pond farming systems of sea cucumbers were greater than those in the outflow water (Zheng., 2009; Li., 2013a, 2013b). It indicated that these two systems absorbed part of the total nitrogen and total phosphorus from the inflow water. Therefore, the earthen pond farming system for sea cucumber was found to be an environment-friendly farming system, for it is not only a production system of aquatic products but also an organic matter purification system for the coast.

Fig.4 Contribution analyses for indoor intensive farming system of sea cucumber.

Fig.5 Contribution analysis for semi-intensive farming system of sea cucumber.

Fig.6 Contribution analysis for extensive farming system of sea cucumber. GWP, global warming potential; AP, acidification potential; POFP, photochemical oxidant for- mation potential; HTP, human toxicity potential; EU, energy use.

The acidification potential (AP) presented to be an indicator to measure the negative impact of acidifying pollutants on the soil, groundwater, surface waters, biological organisms and ecosystems. It was expressed in kg SO2-equivalents. The major acidifying pollutants were supposed to be SO2and NOX(Guinée., 2002). In the present study, the SO2emission was mainly caused by the inputs of concretes, polyechloride, polyethylene, coal and electricity, while the use of coal, electricity and diesel constituted the major source for the NOXemission. It was found that energy consumption presented to be major contributor to AP, with 79% and 87% in the indoor intensive farming system and the semi-intensive farming system respectively, mainly owing to the SO2emission caused by the use of coal and electricity. The AP in the extensive farming system was 34 and 9 times lower than those in the indoor intensive and semi-intensive farming systems respectively, for no coal or electricity was used in the grow-out farming cycle.

Photo-oxidant formation, also known as secondary air pollution, referred to the mixing pollutants composed of both the primary pollutants such as NOXand hydrocarbons in the atmosphere, and those secondary pollutants produced after the primary pollutants were exposed to the ultraviolet light. Photochemical oxidant formation potential (POFP) was expressed in kg C2H4-equivalents. The major photo-oxidant pollutant was CH4in the present study. And the CH4emission was mainly caused by the use of polyechloride, polyethylene, diesel and electricity. In the indoor intensive and semi-intensive farming systems, energy consumption was the major contributor to POFP, accounting for 77% and 95%, respectively (Figs.4– 6). While infrastructure materials became the major contributor to POFP with 99% in the extensive farming system, because no energy was used. Among the infrastructure materials, polyethylene was the biggest contributor in the extensive farming system. Therefore, it was suggested to reduce the use of polyethylene and replace it with stones, waste concretes or tiles, and bricks to further lower the impact of POFP.

Human toxicity potential (HTP) covered the impacts of toxic substances on human health. It was expressed in kg 1, 4-Dichlorobenzene (DCB)-equivalents. The major Human Toxicity Potential pollutants were soot and CH4in the present study. The soot emission was mainly caused by the particulate matters of coal combustion and power generation. The CH4emission was mainly ascribed to the use of polyechloride, polyethylene, diesel and electricity. In the present study, the ratio of HTP among the indoor intensive, semi-intensive and extensive farming systems was 5.0:1.4:1.0.

The LCA clearly showed that Energy Use (EU), expressed in MJ, was an important factor for the impact potential–especially in the indoor intensive farming system in the present study. The major contributor to Energy Use was energy sources consumptions (85%). Infrastructure materials and feed covered about 9% and 6%, respectively (Figs.4–6). The total Energy Use of the indoor intensive farming system was 26 times and 225 times as high as that of the semi-intensive and extensive farming systems, respectively. It was mainly due to the subsequent use of a large quantity of coal and electricity. Except EP, energy consumption accounted for most of the environmental impacts in the indoor intensive farming system. It covered approximately 65% of GWP, 78% of AP, 77% of POFP, 52% of HTP and 85% of EU, much higher than the contribution of the infrastructure materials and feed.

3.4 Interpretation and Analysis

This environmental approach is often combined with economic and social cost-benefit analysis to define the best compromise for sustainable production (Orbcastela., 2009). The analysis of the annual economic profits for the three farming systems of sea cucumbers was presented in Table 3. The indoor intensive farming system was high-input (RMB 6.53E+06) and high-yield (RMB 8.00E+06), and the extensive farming system was one with low-input (RMB 1.10E+05) and low-output (RMB 1.81E+05). The output and input ratio of the extensive farming system (1.64) was higher than that of the indoor intensive farming system (1.23), with the semi-intensive farming system (1.61) in between. These findings explain why people tended to prefer the indoor intensive farming system when constrained by limited land resources. It was probably the main reason for the popularity of the semi- intensive farming systems in general.

Table 3 Annual economic accounting and analysis table for the three farming systems of sea cucumber

Economic interests triggered people to adopt the intensive farming systems. But most of them did not realize the environmental impacts caused by intensive aquaculture. LCA was used to evaluate the environmental performance of the indoor intensive, semi-intensive and extensive farming systems of sea cucumbers. It was concluded from the comparison of the three sea cucumber farming systems (Figs.3–6) that extensive and semi-in- tensive farming systems demonstrated better environmental performance than the indoor intensive farming system. Compared to the semi-intensive and extensive farming systems, the indoor intensive farming system resulted in greater environmental impact, with the largest difference of approximately 26 and 225 times respectively, mainly owing to the consumption of coal and electricity. This rising energy demand also resulted in higher contributions to other environmental impact categories, such as GWP (5 and 64 times), AP (4 and 34 times), POFP (4 and 6 times), and HTP (3 and 4 times).

In the present study, according to the percentage of inputs in each system, energy consumption was regarded as the decisive factor for the indoor intensive farming system. The same trend was observed in turbot in an inland re-circulating system close to the seashore in France (Aubin., 2009). In the semi-intensive farming system, energy consumption was a major contributor to most of the environmental performance. Because less energy was consumed, the infrastructure materials, polyethylene in particular, were the dominant factor of the environmental impact in the extensive farming system.

Feed was an important environmental impact in most aquaculture systems. Conventional fish or shrimp feeds typically contained high levels of protein and lipid, which were mainly from ?sh meal or oil, various wheat meals, and the by-products of animal products (Tyedmers, 2000). The sea cucumber was a deposit-feeder, and its optimum dietary protein and lipid requirements were as low as 18% and 5%, respectively (Zhu., 2005). Therefore, the sea mud, a mixture of microalgae and decaying organic matter, was provided as the main component of formulated feeds, which could also be replaced by the yellow soil that can easily be obtained from cultivated farm land (Liu., 2009).

In terms of the life cycle environmental impact categories adopted in the study, the extensive farming system had better environmental performance than the semi-in- tensive farming system. The advantages of the extensive farming system mainly lay in decreased consumption of feed and energy. Correspondingly, GWP, EP, AP, POFP, HTP and EU of the extensive farming system were decreased by 93%, 33%, 97%, 95%, 28% and 88% respectively, in comparison to the semi-intensive farming system. The extensive farming system had therefore better sustainable development from an ecological perspective.

4 Conclusions and Suggestions

In conclusion, the results of the present study revealed that the increased use of indoor intensive system in sea cucumber farming might lead to growing environmental impacts of global concern. When compared to the indoor intensive farming system, the semi-intensive and extensive farming systems had the advantages of reducing the above mentioned environmental impacts significantly.

The decisive factor of the indoor intensive and semi- intensive farming systems was energy consumption. Infrastructure materials were the major contributors to the environmental impacts of the extensive farming systems.

In terms of the indoor intensive and semi-intensive farming systems, the sustainability might be improved if the consumptions of coal and electricity were replaced with renewable and clean energy. Furthermore, the environmental impacts of the semi-intensive and the extensive farming systems could be further reduced by better use of infrastructure materials.

Acknowledgements

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

Aubin, J., Papatryphon, E., Werf, H. M. G., and Chatzifotis, S., 2009. Assessment of the environmental impact of carnivorous finfish production systems using life cycle assessment., 17: 354361.

Ayer, N. W., and Tyedmers, P. H., 2009. Assessing alternative aquaculture technologies: Life cycle assessment of salmonid culture systems in Canada., 17 (3): 362373.

Bonifaz, O., Hansj?rg, N., and Walter, K., 1996. LCAHow it came about: An early systems analysis of packaging for liquids., 1 (2): 6265.

Brentrup, F., Küsters, J., Kuhlmann, H., and Lammel, J., 2001. Application of the life cycle assessment methodology to agricultural production: An example of sugar beet production with different forms of nitrogen fertilisers. E, 14: 221233.

Dong, S. L., 2009. On sustainable development of aquaculture: A functional perspective., 16 (5): 798805.

Dong, S. L., 2011. High efficiency with low carbon: The only way for China aquaculture to develop., 35 (10): 179184.

FAO, 2012.. FAO, Rome, 125-128.

Guinée, J. B., Gorrée, M., Heijungs, R., Huppes, G., Kleijn, R., Koning, A., Oers, L., Wegener, S. A., Suh, S., Udode, H. A., Bruijn, H., Duin, R., and Huijbregts, M. A. J., 2002.. Kluwer Academic Publishers, Dordrecht, 322-350.

Houghton, J. T., Meira, L. G., Callander, B. A., Harris, N., Kattenberg, A., and Maskell, K., 1996.. Cambridge University Press, Cambridge, United Kingdom, 89-92.

Ibbotson, S., and Kara, S., 2014. LCA case study. Part 2: Environmental footprint and carbon tax of cradle-to-gate for com- posite and stainless steel I-beams., 19 (2): 272-284.

ISO 1404014044, 2006. Environmental Management. Life Cycle Assessment Principles and Framework. International Organisation for Standardisation (ISO), 102-130.

Li, J. W., Dong, S. L., Gao, Q. F., and Zhu, C. B., 2013a. Nitrogen and phosphorus budget of integrated aquaculture system of sea cucumber, jellyfishand shrimp., 14 (3): 503-508.

Li, J. W., Dong, S. L., Gao, Q. F., Wang, F., Tian, X. L., and Zhang, S. S., 2013b. Total organic carbon budget of integrated aquaculture system of sea cucumber, jellyfishand shrimp., 45 (11): 1825- 1831.

Liu, Y., Dong, S. L., Tian, X. L., Wang, F., and Gao, Q. F., 2009. Effects of dietary sea cucumber and yellow soil on growth and energy budget of the sea cucumber(Selenka)., 286 (3): 266270.

MOAC (Ministry of Agriculture, China), 2011.. China Agriculture Publisher, Beijing, 67-69.

Okorie, O. E., Ko, S. H., Go, S., Lee, S., Bae, J. Y., Han, K., and Bal, S. C., 2008. Preliminary study of the optimum dietary ascorbic acid level in sea cucumber,(Selenka)., 39: 758- 765.

Orbcastela, E. R., Blanchetona, J. P., and Aubinb, J., 2009. Towards environmentally sustainable aquaculture: Comparison between two trout farming systems using life cycle assessment., 40 (3): 113119.

Papatryphon, E., Petit, J., Kaushik, S. J., and Werf, H. M. G., 2004. Environmental impact assessment of salmon in feeds using life cycle assessment (LCA)., 33: 316323.

Pelletier, N. L., Tyedmers, P. H., Sonesson, U., Scholz, A., Zeigler, F., Flysjo, A., Kruse, S. A., Cancino, B., and Silver- man, H., 2009. Not all salmon are created equal: Life cycle assessment (LCA) of global salmon farming systems., 43: 87308736.

PRé Consultants. Simapro 7, http://www.pre.nl/simapro/default. htm, 2006.

Ren, Y. C., Dong, S. L., Qin, C. X., Wang, F., Gao, Q. F., and Tian, X. L., 2012. Ecological effects of co-culturing sea cucumber(Selenka) with scallopin earthen ponds., 30: 7179.

Rivela, B., Hospido, A., Moreira, M. T., and Feijoo, G., 2006. Life cycle inventory of particleboard: A case study in the wood sector., 11 (2): 106-113．

Samuel, F. B., Schroeder, J. P., and Schulz, C., 2013. System delimitation in life cycle assessment (LCA) of aquaculture: Striving for valid and comprehensive environmental assessment using rainbow trout farming as a case study., 18: 577-589.

Tacon, A. G. J., and Forster, I. P., 2003. Aquafeeds and the environment: Policy implications., 226: 181-189.

Tyedmers, P. H., 2000. Salmon and sustainability: The biophysical cost of producing salmon through the commercial salmon ?shery and the intensive salmon culture industry. PhD thesis. University of British Columbia, Vancouver, 55- 89.

Zheng, Z. M., Dong, S. L., Tian, X. L., Wang, F., Gao, Q. F., and Bai, P. F., 2009. Sediment-water fluxes of nutrients and dissolved organic carbon in extensiveculture ponds., 37: 218224.

Zhu, W., Mai, K. S., Zhang, B. G., Wang, F. Z., and Xu, G. Y., 2005. Study on dietary protein and lipid requirement for sea cucumber,., 29: 54-58.

(Edited by Qiu Yantao)

DOI 10.1007/s11802-015-2640-y

ISSN 1672-5182, 2015 14 (6): 1068-1074

? Ocean University of China, Science Press and Spring-Verlag Berlin Heidelberg 2015

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

(March 31, 2014; revised November 17, 2014; accepted September 23, 2015)