Potential of the Seaweed Gracilaria Lemaneiformis for Integrated Multi-Trophic Aquaculture with Scallop Chlamys Farreri in North China
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J Appl Phycol (2009) 21:649–656 DOI 10.1007/s10811-008-9398-1 Potential of the seaweed Gracilaria lemaneiformis for integrated multi-trophic aquaculture with scallop Chlamys farreri in North China Yuze Mao & Hongsheng Yang & Yi Zhou & Naihao Ye & Jianguang Fang Received: 17 August 2008 /Revised and accepted: 16 December 2008 /Published online: 28 January 2009 # Springer Science + Business Media B.V. 2009 Abstract In this study the red alga, Gracilaria lemanei- thallus, and mortality of scallop was different between the formis, was cultivated with the scallop Chlamys farreri in IMTA treatments. The nutrient uptake rate and nutrient an integrated multi-trophic aquaculture (IMTA) system for reduction efficiency of ammonium and phosphorus changed 3 weeks at the Marine Aquaculture Laboratory of the with different cultivation density and time. The maximum Institute of Oceanology, Chinese Academy of Sciences reduction efficiency of ammonium and phosphorus was (IOCAS) in Qingdao, Shandong Province, North China. 83.7% and 70.4%, respectively. The maximum uptake rate The nutrient uptake rate and nutrient reduction efficiency of of ammonium and phosphorus was 6.3 and 3.3 µmol g−1 ammonium and phosphorus from scallop excretion were DW h−1. A bivalve/seaweed biomass ratio from 1:0.33 to determined. The experiment included four treatments each 1:0.80 (treatments 2, 3, and 4) was preferable for efficient with three replicates, and three scallop monoculture systems nutrient uptake and for maintaining lower nutrient levels. served as the control. Scallop density (407.9±2.84 g m−3) Results indicate that G. lemaneiformis can efficiently remained the same in all treatments while seaweed density absorb the ammonium and phosphorus from scallop differed. The seaweed density was set at four levels excretion and is a suitable candidate for IMTA. (treatments 1, 2, 3, 4) with thallus wet weight of 69.3± 3.21, 139.1±3.80, 263.5±6.83, and 347.6±6.30 g m−3, Keywords Gracilaria lemaneiformis . respectively. There were no significant differences in the Integrated Multi-trophic Aquaculture (IMTA) . initial nitrogen and phosphorus concentration between each Nutrient uptake rate . Nutrient reduction efficiency. Scallop treatment and the control group (ANOVA, p>0.05). The results showed that at the end of the experiment, the nitrogen concentration in the control group and treatment 1 Introduction was significantly higher than in the other treatments. There was also a significant difference in phosphorus concentra- The cultivation of filter-feeding bivalves in China has tion between the control group and the IMTA treatments developed quickly since the 1980s. In 2006, the production (ANOVA, p<0.05). Growth rate, C and N content of the was close to 11.13×106 t, which is 77.03% of total : : mariculture production in China (China Fishery Statistical Y. Mao H. Yang (*) Y. Zhou Yearbook, 2006). However, the rapid industrial growth of Institute of Oceanology, Chinese Academy of Sciences, aquaculture has raised concerns about environmental prob- Qingdao 266071, People’s Republic of China e-mail: [email protected] lems and sustainable development regarding filter-feeding, digestion and absorption, respiration, excretion, and bio- Y. Mao e-mail: [email protected] deposition (Naylor et al. 2000; Zhang 2003; Zhou et al. : : 2003; Mao et al. 2006a). Thus, ecological engineering in Y. Mao N. Ye J. Fang (*) aquaculture is sought to satisfy a complex of environmental Yellow Sea Fisheries Research Institute, and social aims rather than only being concerned with Chinese Academy of Fishery Science, Qingdao 266071, People’s Republic of China maximizing short-term profitability (Ruddle and Zong e-mail: [email protected] 1988; Primavera 1991; Hishamunda and Ridler 2004). 650 J Appl Phycol (2009) 21:649–656 Increased environmental concern about the rapid expan- with an average specific growth rate (based on wet weight) sion of intensive mariculture systems has increased research of 3.9% per day (Yang et al. 2005). We have also reported into seaweed-based integrated techniques. Seaweeds can the bioremediation potential of that species integrated with significantly absorb waste nutrients, control eutrophication fish aquaculture (Zhou et al. 2006). and, consequently, improve the health and stability of marine In this study, the nutrient (ammonium and phosphorus) ecosystems, and promote a sustainable development of uptake rates and nutrient reduction efficiency of G. aquaculture (Buschmann et al. 2001; Chopin et al. 2001; lemaneiformis was determined in an IMTA system with Troell et al. 2003;Fei2004; Neori et al. 2004;Yangetal. the scallop Chlamys farreri. The objective of this study was 2005; Mao et al. 2005). The physiological responses and the to (1) determine if G. lemaneiformis can efficiently take up biofiltering ecological functions of seaweeds has been the dissolved ammonium and phosphorus from C. farreri studied in different culture systems, e.g., in filter-feeding excretion; and (2) evaluate the optimum ratio of seaweed to bivalve culture systems (Fang et al. 1996a), in fish cage scallop for IMTA systems. farms (Troell et al. 1997;Zhouetal.2006; Hayashi et al. 2008), in shrimp culture ponds (Jones et al. 2001;Nelsonet al. 2001;Xuetal.2007), and in IMTA systems containing Materials and methods finfish, shellfish, and seaweed (Shpigel and Neori 1996; Neori et al. 2000;Chowetal.2001;Shenetal.2007). To determine whether the seaweed can effectively utilize IMTA has been proposed as a means of developing dissolved nutrients from scallop culture, a laboratory environmentally sound aquaculture practices and resource experiment was conducted in static systems at the Marine management through a balanced coastal ecosystem approach Aquaculture Laboratory of Institute of Oceanology, Chinese (Chopin et al. 2001; Troell et al. 2003; Neori et al. 2004). Academy of Science, located in Qingdao, Shandong IMTA is potentially more sustainable than monoculture, Province, North China. The experiment was performed for because of the reutilization of waste products from one 3 weeks in October 2002. species by another (Petrell et al. 1993; Neori et al. 2007). Both the seaweed G. lemaneiformis and scallop C. farreri Most studies have focused on seaweeds integrated with fish were collected form Sanggou Bay, Northern China. They cultures (Petrell et al. 1993; Hirata and Kohirata 1993; were carried to the laboratory in temperature preservation Buschmann et al. 1994; Troell et al. 1997, 2003;Chopinet cases with ice. After being disinfected and cleaned of any al. 2001; Neori et al. 2004;Zhouetal.2006). Only few visible fouling organisms by washing with filtered seawater, studies have investigated the possibilities of IMTA systems they were acclimatized in separate tanks for one week. of bivalves and seaweeds (Qian et al. 1996; Evans and During acclimatization, seawater was changed once per day, Langdon 2001; Langdon et al. 2004). and the scallops were fed with 5 g dry algal powder China has a long history of IMTA of filter-feeding bivalves (Spirulina sp.) twice a day (at 9:00 and 16:00). and seaweeds (Zhang and Wang 1985;Wangetal.1993; G. lemaneiformis and C. farreri were cultivated in 15 Fang et al. 1996b; Hawkins et al. 2002;Yangetal.2000, cylindrical Plexiglas tanks (3 m3, 1.8 m diameter, 1.2 m 2005; Nunes et al. 2003; Mao et al. 2006b;Zhouetal. height, 1.1 m water depth), as shown in Fig. 1. The scallops 2006). The temperate kelp species, Laminaria japonica,has were cultured in a lantern polyethylene net cage, which was been widely used for IMTA with scallops and oysters to tied to a bamboo bar over the bank. The cage was separated mitigate the coastal eutrophication in Northern China (Fei 2004). But during summer and early autumn, the kelp is Water harvested, and no high-temperature-adapted seaweed has Bamboo bar been cultured to replace the L. japonica during the warm seasons. Water The high-temperature-adapted red alga Gracilaria lema- neiformis grows naturally on the coast of Shandong Macroalgae rhodophyte Peninsula, Northern China. After selective breeding at the IOCAS (Fei et al. 1998), this species has been successfully Scallop introduced in Fujian coast in the South China Sea (Tang et Scallop cage al. 2005), and cultivated widely due to its high growth rate, good adaptability, and higher concentration of agar. Weights Previous experiments showed that the seaweed also grows Air stone well in Sanggou Bay, in Shandong Province, North China. 18 cm After 116 days of cultivation, the average wet weight of the − − algae increased 89 times from 0.1 kg rope 1 to 8.9 kg rope 1, Fig. 1 IMTA system for seaweed and scallop J Appl Phycol (2009) 21:649–656 651 into five chambers by plastic discs 30 cm in diameter, The nutrient uptake rate and nutrient reduction efficiency 18 cm apart, with some round holes on them. Each chamber of ammonium and phosphorus were calculated as follows: contained ten scallops. The seaweed thalli (15 cm length) NUR ¼ ðÞC À M V=DW=t were nipped at 8–10 cm intervals in 1.5-m long ropes, t t which were tied to the bamboo bar and positioned vertically around the scallop cage in the tanks. Two air stones were NRE ¼ ðÞCt À Mt =Ct  100 placed in the bottom of each tank. The experiment was −1 −1 conducted in outdoor conditions with plastic shade cloth where NUR (µ mol g DW h ) is the nutrient (ammonium (light transmittance 80%). All tanks were aerated, and no or phosphorus) uptake rate, NRE (%) is the nutrient water was exchanged except for the supplement of (ammonium or phosphorus) reduction efficiency, Ct and Mt evaporated water with fresh seawater. (µM) is the nutrient concentration of control (no seaweed) The experiment included four treatments each with three and treatment tanks at time t since the beginning, respec- replicates. Three scallop tanks served as control.