Bioremediation potential of the macroalga Gracilaria lemaneiformis (Rhodophyta) integrated into fed fish culture in coastal waters of north China
Introduction
Rapid development of intensive fed aquaculture (e.g., fish and shrimp) in coastal areas throughout the world has raised increasing concerns on environmental impacts of such often mono-specific practices (e.g., Wu, 1995, Mazzola et al., 1999). Organic and inorganic inputs of food to fish culture have caused a substantial impact on organic matter and nutrient loading in coastal waters. In general, 52–95% of the nitrogen and 85% of the phosphorus input into a marine fish culture system as feed may be lost into the environment through feed wastage, fish excretion and faeces production, which may easily induce eutrophication, such as harmful algal blooms and anoxia (Wu, 1995). The negative economic and environmental features of mono-specific operations are being realized and their sustainability questioned (Chopin et al., 2001, Neori et al., 2004).
In recent years, there has been increasing emphasis on developing sustainable approaches to coastal aquacultures (Folke and Kautsky, 1989, Wurts, 2000, Frankic and Hershner, 2003, Neori et al., 2004). The cultured organisms in different trophic levels are the basis of environmentally friendly aquaculture (Chopin et al., 2001, Neori et al., 2004). It is ideal to accommodate two or more ecologically compatible species in one system; they can co-inhabit an environment with no conflict in foods and space (e.g., Neori et al., 2000, Zhou et al., in press). By integrating fed mariculture (e.g., fish and shrimp) with inorganic and organic extractive mariculture (seaweed and filter-feeding bivalve), the wastes of one resource consumer become a resource (fertilizer or food) for others in the system. Such a balanced ecosystem approach provides nutrient bioremediation capacity, mutual benefits to co-cultured organisms, and economic diversification by producing other value-added profitable products (Chopin et al., 2001). Biofiltration allows for environmentally sustainable mariculture (Schuenhoff et al., 2003, Neori et al., 2004).
The benefits of integrating the production of macroalgae (seaweeds) with the fed mariculture of fish or invertebrates to recapture waste nutrients are well known (Neori et al., 1996, Troell et al., 1997, Chopin et al., 2001). Modern integrated mariculture systems, seaweed-based in particular, are bound to play a major role in sustainable development in coastal aquaculture (Neori et al., 2004). Fish effluents produced by open-water systems are more difficult to treat than those from land-based systems (Troell et al., 1999a). Water-quality processes in open-water integrated mariculture are most comparable to natural ones (Neori et al., 2004). However, studies investigating the open-water integrated mariculture approach have been hampered by the difficulties involved with experimentation and data collection at sea (Petrell and Alie, 1996, Troell et al., 1997, Chopin et al., 2001, Neori et al., 2004). Integration with seaweeds and/or filter feeders is often proved to be the only economically feasible alternative for waste treatment in open-water systems (Troell et al., 2003). The use of seaweeds integrated with fish culture in open-sea systems has been studied in Canada, Chile, the United States, Japan, and China (Petrell et al., 1993, Petrell and Alie, 1996, Troell et al., 1997, Chopin et al., 1999, Fei et al., 2002).
The genus Gracilaria (Rhodophyta) has been demonstrated to be the most attractive candidate for intensive culture because of its ability to achieve high yields and produce commercially valuable products. Gracilaria species, being an efficient nutrient pump, offer both high bioremediation efficiency and commercial value in established markets, such as agar-agar, human consumption, and fodder for other high-valued aquaculture organisms, such as abalone (Chopin et al., 2001, Neori et al., 2004, Fei, 2004). The edible red alga Gracilaria lemaneiformis (Bory) Dawson occurs naturally in coastal areas of Shandong Peninsula, especially in Qingdao, north China. After selective breeding in the Institute of Oceanology, Chinese Academy of Sciences (IOCAS), this species has been successfully introduced to subtropical coastal waters in south China and cultivated widely due to its high productivity, good adaptability and high concentration of agar-agar (Fei et al., 1998, Fei et al., 2000).
Fish farming in coastal waters in north China boosts up greatly in the past decade. However, adverse environmental impact has been observed (Wang et al., 2001). In order to develop a sustainable aquaculture, integrated aquaculture of fish with seaweed and/or filter-feeding bivalve would be an effective measure. In coastal waters of north China, the temperate brown alga Laminaria japonica Aresch is the most important seaweed traditionally cultivated from longlines with yearly production of 3 million t. The kelp has been suggested to be potentially used for mitigation of coastal eutrophication (Fei, 2004). Unfortunately, no commercial seaweed cultivation has been undertaken in north China in the warm seasons from late spring through summer to early autumn. No high-temperature adapted macroalgae has been cultured to replace the gap after temperate seaweeds are harvested in the warm seasons.
In this study, we introduced the high-temperature adapted seaweed G. lemaneiformis from subtropical south China, for investigations on growth and bioremediation potential in a system co-cultured with fish. We also studied the feasibility of the integrated aquaculture in coastal waters of north China. This program was to develop the co-culture of G. lemaneiformis with fed fish aquaculture for eutrophication abatement, and for valuable bio-products (agar, food, fodder, etc.).
Section snippets
Experiment 1: spring–summer experiment for coculture of G. lemaneiformis and Sebastodes fuscescens in tanks
To determine whether the seaweed G. lemaneiformis from south China can be cultured in north China with the maricultured fish S. fuscescens in spring–summer, and whether the seaweed can effectively utilize dissolved nutrients from fish culture, a preliminary experiment was conducted in static systems (3 m− 3 Plexiglas tanks) at Marine Aquaculture Laboratory of IOCAS, located on the rocky seashore of Qingdao, Shandong Province, north China. The experiment was performed from 24 April to 1 June 2001
Experiment 1
During the experiment, seawater temperature increased gradually from 12.8 °C at the beginning to 22.2 °C at the end. DO in all tanks was 5.70–7.95 mg l− 1. Daily daylight irradiances ranged from 700 to 1200 μmol photon m− 2·s− 1 in a sunny day and 50–110 μmol photon m− 2·s− 1 in a cloudy day. Fig. 1 shows the variation in total dissolved inorganic nitrogen (DIN) in the five treatments. DIN in fish monoculture system (control) increased promptly with the time, from 3.23 μmol l− 1 to 64.85 μmol l− 1. In
Discussion
The importance of integrated aquaculture for marine fed organisms (e.g., fish and shrimp) with extractive organisms (e.g., seaweed and bivalve) has been re-realized since the last decade. The integrated aquaculture is proved to be potentially more sustainable than monoculture, because of the reutilization of waste products of one species by another (Petrell et al., 1993, Chopin et al., 1999, Neori et al., 2004). In China, fish aquaculture in coastal waters has been increasing since the last
Acknowledgements
We thank Chongbin Wang, Xiangbin Liu, and Huanyou Pang for their help in the field experiment at Jiaozhou Bay and Guzhen Bay. We are grateful to Qun Liu for his help in sample analysis. This work was supported by the Knowledge Innovation Key Projects of CAS (KZCX2-SW-211/3SW-214), Shandong Science and Technology Key Project (2002), Shandong Natural Science Foundation (Q2002D03), the National Natural Science Foundation of China (No. 30100139; 30170742), and the Special Funds for the Major State
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