Workpackage 3 Support the application of Integrated Multi-Trophic Aquaculture (IMTA)

Workpackage 3 Support the application of Integrated Multi-Trophic Aquaculture (IMTA) Deliverable D3.1 Case studies on successful polyculture examples in coastal Chinese seas Workpackage leader: SHOU Deliverable: D3.2 Authors: Dong Shuanglin Ocean University of China, Qingdao, China Fang Jianguang Yellow Sea Fisheries Research Institute, Qingdao, China Jansen Henrice M Wageningen University, The Netherlands Verreth Johan Wageningen University, The Netherlands Nature: Report Dissemination level: Public 1

Review on integrated mariculture in China, including case studies on successful polyculture in coastal Chinese waters Photography: Laboratory of Aquaculture & Artemia Reference Center, Ghent University, Belgium Dong Shuanglin,Ocean University of China, Qingdao, China Fang Jianguang,Yellow Sea Fisheries Research Institute, Qingdao, China Jansen Henrice M,Wageningen University, The Netherlands Verreth Johan,Wageningen University, The Netherlands 2013 2

TABLE OF CONTENTS Abstract... 4 1. Introduction... 6 2. Aquaculture development in China... 7 Status and trends in aquaculture development... 7 Constrains for development of a sustainable aquaculture sector in China... 8 Integrated aquaculture: An important route for further development of aquaculture... 8 3. Definition of integrated aquaculture (INTAQ)... 9 4. History of integrated aquaculture in China... 9 5. System classification of integrated aquaculture in China... 10 I. Complementary bio chemical functions integration... 10 II. Integration of species... 12 III. Integration of systems... 15 6. Case studies of IMTA in Chinese coastal waters... 16 Case study 1: Pond culture of shrimp, clam and seaweed... 16 Case study 2: Pond culture of shrimp and tilapia... 18 Case study 3: Pond culture of sea cucumber and shrimp... 19 Case study 4: Pond culture of sea cucumber and scallops/jelly fish... 19 Case study 5: Open water culture of abalone and kelp (suspended)... 19 Case study 6: Open water culture of abalone, kelp and sea cucumber (suspended)... 20 Case study 7: Open water culture of abalone, kelp, sea cucumber and clams (benthic)... 22 Case study 8: Open water culture of fin fish, bivalves and kelp... 24 Recent advances in tracing wastes in IMTA systems by means of biological markers... 26 Recent advances in modelling IMTA in Sanggou Bay... 27 Analyses of the environmental and economic benefits of IMTA... 28 7. Prospective... 29 Economic rationale of integrated aquaculture in China... 29 Ecological rationale of integrated aquaculture in China... 30 Policy needs... 31 Research needs... 31 References... 32 Annex 1. A short note on the opportunities for IMTA in Singapore... 38 3

ABSTRACT The current report reviews the concept, ecological and economical rationales of integrated mariculture practices in China and outlines case studies of successful polyculture applied in the Chinese coastal seas and ponds, envisioning to use this information for the development of guidelines. China is the largest aquaculture producer in the world, contributing to nearly 70% of global production of aquatic animals. It is predicted that the Chinese demand for seafood products will steadily increase, and most of the growth has to be realized by aquaculture rather than capture fishery. It is also expected this will be gained by mariculture enlargement and technological progress rather than area enlargement of inland aquaculture. At present aquaculture in China encounters several challenges and, although growth rate of aquaculture development in China is still high, the sustainability of its development has drawn much attention. The mariculture industry worldwide is searching for sustainable methods, and integrated aquaculture has been proposed as a potential tool assisting sustainable development. Definitions on integrated aquaculture are widespread but in essence relate to the polyculture of several aquatic species, or linking different productive activities. Recently Integrated Multi Trophic Aquaculture (IMTA) has become a popular term and refers to a form of integration with the explicit incorporation of species from different trophic positions, where the output (wastes) of one species are utilized by other species. Integrated aquaculture has several benefits, including enhanced carrying capacity, bioremediation, product diversification, and disease prevention. Integrated production is common practice in China (especially in inland aquaculture), and a large variety in culture types and cultured species is known. The ecological rationales behind most of these integrated systems are waste reclamation through trophic relationship, ecological balance maintenance by complementary or commensalism of farmed species or production systems, making full use of resources (time, space and natural food) of the culture systems, and ecological prevention of diseases. Integrated aquaculture in China can be classified into three groups: I. Complementary chemical functions integration; II. Integration of species including trophic, spatial, temporal integration, rotary stocking and harvesting, and multi function integration, and III. System integration including the sub groups integration of aquatic systems, and integration of aquatic and land systems. The FAO Technical Paper Integrated mariculture: a global review (Soto, 2009) reviewed the development of open water IMTA systems in several areas, however practically no information from China was included due to information unavailability (Troell, 2009). Recently, Chinese researchers have documented empirical achieved progress in integrated mariculture with sounds data and models. The current report reviewed these data, by means of specific case studies for the Shandong peninsular and recent advances in IMTA research, with the aim to show the effectiveness of IMTA in comparison to monocultures. This is essential for further development of IMTA in the coastal zones of China. Mariculture case studies were divided into coastal pond systems (case studies 1 4) and open water culture (case studies 5 8), and basically all case studies presented are based on trophic relations between the cultured species. Species cultured in these integrated systems included for example shrimp, sea cucumber, kelp, fish or bivalves. The case studies provided technological, economical and scientific information on the use, type and characteristics of each specific IMTA system. Growth and production of several species were provided and optimal co culture densities for effective bioremediation purposes were determined, showing that IMTA not simply involves the integration of different species but also the proportion between species should be taken into account in order to balance nutrients in the ecosystem. Carbon budget analysis illustrated that cultivation of shellfish and seaweed in the coastal zones can utilize a significant fraction of oceanic carbon, thereby potentially improving the capacity to absorb atmospheric CO 2. Biological tracers have been used to develop waste dispersal models for fish farms and to quantify assimilation of fish waste by shellfish and other benthic organisms. This showed that shellfish farmed close to a fish cage obtained 32 35% of their food from fish wastes and the other fraction came from ambient organic material. These better understanding of processes related to trophic interactions are also needed in development of carrying capacity models. Recently a multi species model for integrated culture of finfish, shellfish and kelp has been developed for Sanggou Bay. The model is used the estimate 4

exploitation carrying capacity, harvest potential for different seeding and harvesting scenarios, and for estimating the environmental impact of different management strategies. The evaluation approach of ecosystem services by Constanza et al. (1997) was used to evaluate for open water IMTA case studies the economic revenues on one side, and environmental bioremediation on the other side in comparison to monoculture of kelp or scallops. For all parameters included in the evaluation case study III. showed best results, demonstrating the advantages of IMTA over monoculture. 5

1. INTRODUCTION China is the largest aquaculture producer in the world, both in terms of volume and its total value (Figure 1.1). In 2011 the aquaculture production of Chinese mainland was 40.2 million tonnes, contributing to nearly 70% of global production of cultured aquatic products. Seafood products contribute to approx. one third of the total animal protein consumption by the Chinese population, and make out a significant contribution in improving Chinese nutritional standard and food security. At present the aquaculture in China encounters challenges, such as epidemic outbreak, limited availability of improved varieties of farmed species, fish meal and environmental deterioration. Although the growth of aquaculture in China is still high, the sustainability of its development has drawn critical attention of the world. Figure 1.1 Global aquaculture production (source: http://www.fao.org/docrep/003/x8002e/x8002e00.htm ). The mariculture industry worldwide is searching for sustainable methods, and integrated aquaculture has been proposed as a potential tool assisting sustainable development. Integrated aquaculture has many benefits, including increment of carrying capacity, bioremediation, diversified products, and prevention of diseases (Edwards et al., 1988; Edwards, 1998; Troell et al., 2003; Neori et al., 2004; Soto, 2009). Integrated aquaculture thereby has the promise to contribute to the sustainability of aquaculture by reducing the ecological footprint, increasing economic diversification and increasing social acceptability of culturing systems. Studies on integrated systems have primarily focused on inland (freshwater) systems, and only a few have investigated the possibilities of integrated farming in marine systems. In the past two decades, integration of seaweeds with marine fish culture has been examined and studied in Canada, Japan, Chile, New Zealand, and USA (Buschmann et al., 2008; Troell et al., 2003; Chopin et al., 1999, 2001, 2008; Abreu et al., 2009). The FAO Technical Paper Integrated mariculture: a global review (Soto, 2009) reviewed integrated systems in the latter areas, but there almost no information on Chinese systems was probably due to limited availability of accurate information (in English) (Troell, 2009). In China, integration of cultures is a common practice for inland production systems, while integrated mariculture is a recent development expanding at a fast rate. It is essential for sustainable development of mariculture to define ecological rationales and draw lessons from various integrated culture techniques in inland waters. Furthermore, for further development of integrated production systems in the coastal zones of China it is important to show its effectiveness in comparison to monocultures. Such a comparison should include production and economic revenues on one side, and environmental benefits on the other side. The current report reviews the concept, ecological & economical rationales, and provides case studies of integrated mariculture practices in China in order to promote the growth of aquaculture in a way of high productivity and low carbon footprint. This report aims thereby to promote integrated aquaculture development around the world. 6

2. AQUACULTURE DEVELOPMENT IN CHINA Status and trends in aquaculture development Aquaculture in China has developed rapidly over the past decades, with a production increase from 1.8 million tonnes in 1980 to 40.2 million tonnes in 2011. Total seafood production from the mainland in 2011 was 15.5 million tonnes. It is expected that demand will reach 62 million tonnes by 2020 (Delgado et al., 2003), and grow to 73 million tonnes by 2030 (FAO, 2002). Aquaculture has already outpaced fisheries since 1988 and 2006 for mariculture and marine capture respectively (Figure 2.1), hence it is expected that the increased demand for seafood products will primarily come from the aquaculture sector because of limited fishery resources and over fishing. Figure 2.1 Fisheries Production in China (mainland, million tonnes) (source: Fisheries Department of Agriculture Ministry of China, 2012) At present, most of the Chinese aquaculture production is performed in inland ponds, lakes and reservoirs (Fisheries Department of Agriculture Ministry of China, 2012). However, it is expected that the increasing demand for seafood products will be the result of the expansion of mariculture activities and technological innovation rather than area enlargement of inland aquaculture. Total mariculture production in China was 15.5 million tonnes in 2011, and was dominated by production of molluscs (Table 2.1). With intensification of aquaculture systems and increase of the number of species farmed in China the relative quantity of high trophic level species increases rapidly. From 1999 to 2008 the production ratio of marine fed fish and crustacean to total mariculture production increased from 6.2% to 12.7%, and the production ratio of filterfeeding silver carp and bighead carp to total inland aquaculture production decreased from 35.6% to 26.4%. Therefore whether in mariculture or in inland aquaculture the production ratio of fed species is rising rapidly. Taking aquaculture as a whole in China about 41% of aquaculture production came from fed aquatic animals in 2008 (Dong, 2009). Table 2.1 Aquaculture production in China (2011) (Fisheries Department of Agriculture Ministry of China, 2012) Species Mariculture Inland aquaculture Production 10 3 t % Production 10 3 t % Fishes 964 6.2 21,854 88.4 Crustaceans 1,127 7.3 2,164 8.8 Molluscs 11,544 74.4 252 1.0 Aquatic plants 1,601 10.3 7 0.0 Others 277 1.8 441 1.8 Total 15,513 100 24,719 100 7

Constrains for development of a sustainable aquaculture sector in China At present aquaculture in China encounters challenges related to epidemic outbreaks, limited availability of improved varieties of farmed species, and environmental deterioration. However, evaluating aquaculture in a sustainability context indicates that the main constrains for future development are environmental deterioration, increased use of energy and fishmeal. With the development of intensive marine mariculture, the impact of the industry on the ecosystem has become serious, and in turn the degraded environment has resulted in higher mortality of mariculture organisms. It was estimated by Cui et al. (2005) that waste nutrients discharged from mariculture activities along the Yellow Sea and Bohai Bay consisted of approximately 6,010 tonnes nitrogen (N) and 924 tonnes phosphorus (P). These discharges took account for 2.8% and 5.3% of total land sourced pollutants in these areas, for nitrogen and phosphors respectively. This indicates that nutrient discharges by mariculture have reached a noticeable level in certain regions of China. The intensification of aquaculture in China also leads to increased energy consumption and consequently more CO 2 discharges into the air (Xu, 2010). As a response to the global warming issue, the Chinese government has announced that by 2020 CO 2 emission per unit GNP should be reduced by 40 45% compared to 2005 (Shi, Li, Zhou et al., 2010). Therefore, the aquaculture industry should also consider this issue and develop low carbon models of development. Rising total aquaculture production combined with a rapid increase in ratio of fed species consequently has led to a fast increase in demand for fishmeal in China. Simultaneously, the global fishmeal supply has been rather stable over the past three decades, and is occasionally severely affected by the El Niño phenomenon in South America, where the major producing areas are located (FAO, 2007). The strong demand for fishmeal from China and other emerging aquaculture countries will enlarge the gap between fishmeal supply and demand, and eventually increase the cost of fed species. Fishmeal supply could become an immense obstacle for Chinese aquaculture if it pursues its present farming model and maintain its present technological level of aquafeed manufacturing. Integrated aquaculture: An important route for further development of aquaculture The mariculture industry worldwide is searching for methods to support further growth of aquaculture production in a sustainable manner. Although it is believed that modern biotechnology and modern engineering will increasingly contribute to aquaculture development, their wide application in aquaculture still needs time and effort (Losordo, 1998; Powell, 2003; Neori et al., 2004; Naylor. et al., 2005). Although aquaculture is becoming more industrialized (e.g. seen from increased ratio fed species), today mariculture production in China is still primarily based on molluscs and seaweeds (Table 2.1). Molluscs form carbonate shells and seaweeds absorb inorganic nutrients from water, and this production thereby represents a clean and carbon sequestration industry (Zhang et al., 2005; Tang, 2010). Two important routes to meet the increasing demand for aquatic products are (1) to develop an ecological approach in intensified pond farming models to achieve the goals of low carbon and high productivity, and (2) to develop an ecological approach for an industrialized open water aquaculture resulting in low carbon emission and low environmental impact. Ecosystem approach to aquaculture is a strategy for the integration of the farming activity within the wider ecosystem in such a way that it promotes sustainable development, equity and resilience of interlinked social and ecological systems (Soto et al., 2008). Integrated farming is one of the best paradigms of ecosystem approach to aquaculture with advantages of increment of carrying capacity, bioremediation, diversified products, prevention of diseases. Integrated aquaculture is probably one of the most important alternatives for China s aquaculture to develop rapidly and sustainably. 8

3. DEFINITION OF INTEGRATED AQUACULTURE (INTAQ) Definitions of integrated aquaculture are widespread (Muir, 1981; Li, 1986; Edwards et al. 1988; Edwards 1998; Tan et al. 1992; Liu and Huang, 2008; Angel and Freeman, 2009; Barrington et al., 2009) but in essence relate to an aquaculture production system where the output (waste) of one sub system is utilized by another sequential linked sub system resulting in a greater efficiency of the overall system. Sub systems can either comprise aquatic species, fisheries, agriculture, livestock or other human activities. The aim of integrated production is to create balanced systems for environmental sustainability (biomitigation), economic stability (product diversification and risk reduction) and social acceptability (better management practices). The Aquaculture Glossary of the Food and Agriculture Organization of the United Nations (FAO, 2008) described integrated aquaculture as: aquaculture system sharing resources, water, feeds, management, etc., with other activities; commonly agricultural, agro industrial, infrastructural (waste waters, power stations, etc). Soto (2009) defined integrated aquaculture as the culture of aquatic species within, or together with, the undertaking of other productive activities. Recently integrated multi trophic aquaculture (IMTA) as a very popular term for a special kind of integrated aquaculture has emerged, where multi trophic refers to the explicit incorporation of species from different trophic positions or nutritional levels in the same system (Chopin and Robinson, 2004). It is clear that integrated aquaculture has both narrowly defined and broadly defined meanings. The following parts of this paper will deal with the more broadly defined meaning, i.e. the simultaneous culture of several aquatic species or culture of aquatic species together with the undertaking of other productive activities. 4. HISTORY OF INTEGRATED AQUACULTURE IN CHINA Development of Chinese aquaculture and integrated cultures has a long history (Liu and He, 1992). China was the first country in the world to culture fish, and pond farming of carp can be traced back as far as the 11 century BC 1. The first records of integration between aquaculture and agriculture in China date back to 220 265 AD 2, when the mutual profitable relationship between grass carp and rice was reported. Evidences of polyculture of different carps originates from 1201 1204 AD 3 when the optimized ratio for stocking silver carp and grass carp was documented and trophic relationships between them were clarified. The phrase one grass carp feeds three silver carp is still popular all over China, which means grass carp is fed species, its faeces and residual feed can be filtered by silver carp or can promote the growth of phytoplankton as organic fertilizers. Records of integration of rotary stocking and harvesting came in 1573 1618 AD 4 when it was stated that stocking multiple sizes of fish fingerlings is better as it allows to sell fish at different moments in the season and the mass death of the fish due to anoxia could be avoided. In the 17 th 18 th century 5 reliable records of fish livestock agriculture integration in China appeared. In 1959 6 scientists summarized experiences of traditional freshwater fish farming into eight words, viz. water, breed, feeds, density, polyculture, rotation, (disease) prevention and management. Two of the eight experiences are about INTAQ, namely polyculture and rotation (rotary stocking and harvesting). Open water mariculture started much later than freshwater aquaculture in China. Seaweed culture (Gloiopeltis sp.) on rocky reefs started in 960 1279 AD in Fujian Province, followed by culture of Porphyra. Cultivation of oysters was systematically described in 1368 1644 AD 7. Large scale integrated mariculture started in 1975 in the Shandong and Fujian provinces with simultaneous culture of mussel and kelp along a large part of the coastline (Fu, 1979; Xie, 1981). In the beginning of the 80, polyculture of kelp, scallops and sea cucumber gained good results (Wu, 1985; Luo and Wang, 1984). Nowadays the integrated mariculture of kelp and scallops (Fang et al., 1996; Zhang et al., 2005), abalone and sea cucumber (Lin, 2005; Liu et al., 2009) are widely applied in open waters. 1 Book of Poetry (11 century BC) and The Classics on Fish Breeding (Li FAN, 473BC) 2 The Seasonal Food of WEI Wuwang (220 265AD) and The Curious in Lingbiao Region (Xun LIU, 889 904 AD) 3 Jiatai Notes (1201 1204 AD) and Complete Book on Agriculture (Guang qi XU, 1639) 4 The Classics on Fish Breeding (Xing HUANG, 1573 1618 AD) 5 Complete Book on Agriculture (1639) and The New Story of Canton (Dajun QU, about 1700 AD) 6 Chinese Editorial Committee of Cultivation Experiences of Freshwater Fishes (1961) 7 Cultivation of Oyster ( Hongtu ZHENG, 1368 1644 AD) 9

At present integrated mariculture has become common practice in China, especially in pond farming. However, records from mariculture in ponds are only found for the last four decades. In 1979 integrated pond mariculture of Chinese shrimp and pike was reported (Wu et al., 1980), but the rise in polyculture patterns of Chinese shrimp really won through in the 80. For example, the successful polyculture of Chinese shrimp and clam (Zhu, 1980), shrimp, pike, mullet and tilapia (Tang, 1985), shrimp, mullet and oyster (Li and Zhou, 1985), and it was also shown that polyculture of shrimp and kelp increased production of shrimp by 29% (Zhang, 1985). Later, the polyculture of Chinese shrimp and razor fish (Liu, 1991), shrimp and crab (Liang, 1992) achieved success. Nowadays the integrated mariculture of shrimp and molluscs and/or crabs and/or macro algae are popular because it helps preventing outbreaks of white spot disease (White Spot Syndrome Virus, WSSV). Additionally temporal integration, like rotary stocking and harvesting, is popular. Examples are the integrated shrimp and crab culture where shrimp are harvested first and crabs several weeks later in order to keep constant biomass in the pond (Li et al., 2010), and in rotary stocking and harvesting of five different species (Kong and Mu, 2009). Popular polyculture patterns in pond include flounder, jellyfish and razor fish (Xu, 2008), shrimp, crab and razor fish (Ding, Cui and Zhuang, 2008), sea cucumber and jellyfish (Zhang et al., 2008), shrimp and puffer fish (Li et al., 2001; Guo, 2005). 5. SYSTEM CLASSIFICATION OF INTEGRATED AQUACULTURE IN CHINA Production of traditional aquaculture (monoculture) is either limited in terms of inorganic nutrients, food, oxygen or a combination of these factors. The type of limitation has also implications for production efficiency of the system (Dong, 2011b). In practice farmers in China often implement integrated culture strategies to overcome such limitations. The degree of coupling between culture species or sub systems will affect the production and ecological efficiency of the system. Integrated aquaculture is an important category in the aquaculture activities implemented in China, and a large variety of combinations of culture types and cultured species is applied. Important ecological rationales for INTAQ are waste reclamation through trophic relationship, water quality maintenance through complementary functions between systems or species, optimizing the use of available resources through different ecological niche species, and disease prevention based on ecological priciples. The variety in types of integrated aquaculture systems can be classified based on various characteristics (Chien and Tsai, 1985; Tan et al., 1992; Liu and Huang, 2008;. Troell, 2009). In line with Troell s classification, Chinese systems are here divided into three main classes: I. Complementary chemical functions integration, II. Species integration, and III. Systems integration. The later class contains two sub classes: III 1 Integration of aquatic systems and III 2 Integration of aquatic and land systems. Within each class there are several types of integration systems I. Complementary bio chemical functions integration This type of integration is aimed at implementing two complementary bio chemical functions to improve and maintain water quality and promote the growth of cultured species. Integration of common carp and silver carp is a typical case of such integration in freshwater systems (Li, 1986). The Common carp are fed with artificial pellet, their faeces and residual feed are partially filtered by silver carp, and partially play an ecological role as organic manure. Organic manure is slow release fertilizer as it needs to be decomposed into inorganic nutrients before it can be absorbed by phytoplankton. In the process of the manure decomposition DO, ph and redox potential will go down and CO2 concentration will go up. However, after applying inorganic fertilizer the phenomenon is just opposite of that of manure and acts as a promotor of photosynthesis. Making good use of complementary bio chemical functions of pellet or manure and inorganic fertilizers helps to create an ecological balance (see Figure 5.1) and can result in enhanced production of the cultured species (Sun et al., 1990).. Table 5.1 Classification of integrated aquaculture in China Class Types Examples 10

Feeds chemical fertilizers (Li, 1986; Sun et al., ⅠComplementary chemical functions integration 1990); manure chemical fertilizers (Boyd and Tucker, 1998; Yang et al., 1998) Ⅱ 1 Trophic integration or Integrated multi tropic aquaculture Grass carp and silver carp (Liu and He, 1992);80% fed species and 20% filter feeders (Xi and Liu, 2002); shrimp and razor fish (Wang and Cui, 2009); Sanggou Bay (Fang et al., 1996) Ⅱ 2 Spatial integration Fish culture in ponds (Liu & Huang, 2008), in reservoirs (Shi, 1991), or mariculture (Luo & Wang, 1984) ⅡSpecies integration Ⅱ 3 Rotary stocking and harvesting Several carps (Liu and He, 1992); Shrimp and crab (Li et al., 2010) Ⅱ 4 Temporal integration Two species of shrimps (Zheng, 1989);shrimp and fish (Shen and Zhang, 2004) Ⅱ 5 Multi function integration Integration of sea cucumber, jellyfish, scallop and shrimp Ⅱ 6 Disease prevention Puffer fish and shrimp for disease prevention (Liu et al., 2007) Ⅱ 7 Other integration Mmandarin fish and bait fish (Yang et al.,2006) Ⅲ 1 1 Partitioned aquaculture systems Tilapia + shrimp + oyster + Gracilaria (Shen et al., 2007) Ⅲ 1 2 Aquaculture and agriculture integration Fish rice (Liu and Cai, 1998; Liu and Huang, 2008) Ⅲ 1 3 Aquaponics Aquaponics (Ding et al., 2010); fish lotus root Ⅲ 1 (Yang, 2001) Integration of Ⅲ 1 4 Aquaculture and Fish and duck (Luo et al., 2002) aquatic waterfowl integration systems Ⅲ 1 5 Fish and amphibian Fish and turtle (Sun, 2004); fish and frog (Zheng et integration al., 2004) Ⅲ System Ⅲ 1 6 Aquasilviculture She et al. (2005) integration Ⅲ 1 7 Others Net isolated polyculture of tilapia and shrimp (Jie, 2008), cage culture of loach (Misgurnus anguillicaudatus) in carp farming pond (Zhu, 2008) Ⅲ 2 1 Integration of pond and livestock or poultry Pond sheep (Dai and Yan, 1999), pond pig (Chun, Wang and Yang, 2009), pond chicken (Li and Yu, Ⅲ 2 breeding 2000) Integration of aquatic and land systems Ⅲ 2 2 Integration of pond and plantation Pond grain (Zheng, Sun and Shi, 2006), pond grass (Tang, Jiang, Sun and Yang, 2010), pond fruit tree (Liu and Huang, 2008) Ⅲ 2 3 Other integration Shrimp culture with Cooling water from power plant (Wang, 2003) 11

CO 2 O 2 ph eh Balance CO 2 O 2 ph eh Pellet/manure Integration Inorganic fertilizers (Decomposition) (Photosynthesis) Figure 5.1 Biochemical effects by integration of two technical measures: pellet feeding and application of chemical fertilizer Similar principles have been applied to culture tilapia based on the integrated use of manure and chemical fertilizers (Boyd and Tucker, 1998; Yang, Li, Dong and Wang, 1998). II. Integration of species Integration of species includes the polyculture of two or more aquatic species occupying different trophic levels, inhabiting different water layers, or possessing dissimilar optimal temperature for growth. II 1 Trophic integration Trophic integration refers to polyculture of aquatic species from different trophic or nutritional positions in the same system, and is based on the principle that by products (wastes) from one species are recycled to become inputs (fertilizers, food and energy) for another species. These systems aim to maximize resource utilization and simultaneously reduce adverse environmental impacts (Troell, 2009). Often the term integrated multi trophic aquaculture (IMTA) is used instead of trophic integration to express this type of integrated cultures (Chopin, 2006; Barrington et al., 2009). IMTA systems can include various combinations such as shellfish/shrimp, fish/seaweed/shellfish, fish/shrimp, seaweed/shrimp (Troell et al., 2003) as well as aquasilviculture (Troell, 2009), all of which have the function of waste utilization or circulation. Within the IMTA context Chopin (2006) presented a conceptual model of the culture of fed species, such as finfish, integrated with inorganic extractive species such as seaweeds, and organic extractive species such as suspension feeding bivalves (Figure 5.2). A well known example of integration based on trophic relationships in freshwater pond farming in China is the culture of grass carp (feeding on grass) and silver carp (filtering plankton) (Xi and Liu, 2002). In mariculture trophic integration of shrimp and filtering mollusc (Wang and Cui, 2009), scallop and kelp (Fang et al., 1996), flounder, jellyfish and razor fish (Xu, 2008) are nowadays popular in China. Positive interactions are not only the bioremediation properties but enhanced water quality may also stimulate culture performance. It is for example shown that Ulva sp. in polyculture with red sea bream can positively affect the level of DO, ph and CO 2 in the water (Hirata et al., 1994). There is no information available as to how bacterial biofilters can be integrated into large scale low cost fish net pens, therefore, modern integrated systems in general, and seaweed based systems in particular, are bound to play a major role in the sustainable expansion of world aquaculture (Neori et al., 2004). 12

Figure 5.2 Conceptual diagram of an integrated multitrophic aquaculture (IMTA) operation including fish, shellfish and seaweeds (Source: Chopin, 2006) II 2 Spatial integration Making full use of space in culture systems can be achieved by stocking species that inhabit different water layers. Spatial preference of each species is related to the food resources available in the subsequent water layers, and if stocking partial or all these species most of the natural resources available in a culture system can be utilized. The vertical mariculture model for example integrates cultures of Undaria which is cultured in upper water layer to receive light, scallop and mussel cultured at middle upper layer to filter phytoplankton and detritus, sea cucumber and abalone are cultured at the bottom to feed on detritus and benthos (Luo and Wang, 1984). This example shows that by stocking species which occupy different spatial niches not only space and natural food resources are utilized most efficient, but the trophic relationship among them can also be exploited. II 3 Rotary stocking and harvesting In China Rotary stocking and harvesting is based on two culture principles: One principle is based on the harvest of bigger fish immediately followed by stocking smaller fingerlings of the same species multiple times a year. The other principle is basically similar but is based on the culture of different species (Liu and He, 1992). The theoretical basis for Rotary stocking and harvesting lies in utilizing space and natural food resources most efficiently. This method originated in freshwater fish farming 400 years ago, and nowadays mariculture of shrimp and crab is often based on this principle (Li et al., 2010). Shrimp and crab larvae are stocked into ponds during late spring, and with the growth of both species the total biomass in the pond increases. In summer the total biomass is too high to enhance further growth and the shrimp which by then have reached commercial size are harvested. Following shrimp harvest the crab are able to grow again due to enhanced food availability as a result of reduced total culture biomass. Through rotary stocking and harvesting high biomass can be sustained in the culture pond (Figure 5.3). II 4 Temporal integration Temporal integration aims to make full use of time and can be achieved by the culture of various aquatic species in different seasons according to the optimal temperature of each cultured species. More than 200 species are now commercially cultured in China. Although most are temperate eurythermic species, some such as tilapia and the Pacific white shrimp belong to tropical species and only survive in the warm season of temperate zones. Others belong to boreal species, such as kelp, abalone and sea cucumber, and cannot survive the summer season of temperate zones. Combining cultures of tropical and boreal species in temperate regions makes full use of time and resources. Examples are known from integrated cultures of two types of shrimps (Zheng, 1989) and subsequent cultures of Pacific white shrimp (May Oct) and mandarin fish (Oct May) (Shen and Zhang, 2004). Temporal integration can fully make use of time resources and may yield in higher total production of a system. 13

ng Figure 5.4 Multi function integration of sea cucumber, and harvesting of shrimp and crab in pond systems jellyfish, scallop and shrimp Figure 5.3 Bioma ss develo pment during Rotar y stocki II 5 Multi function integration In Section II 2 (Spatial integration) it was already shown that by stocking species based on their spatial niche also the trophic relationship among them can be exploited. By means of integration based on multiple assets the complementary of farmed species and the resources (time, space and natural food) of the culture system are fully utilized. Zhang et al. (2008) reported the integrated culture of sea cucumber and jellyfish, in which the differences of trophic levels and habitat between both species were utilized. Nowadays multi functional integration of sea cucumber, jellyfish, scallop and shrimp is developed in the Shandong Province (Figure 5.4). Sea cucumbers (deposit feeder) are stocked and harvested multiple times a year; Jellyfish (zooplankton feeder) are cultured from May to October; Scallops (phytoplankton feeder) are cultured from October to next May; Shrimp (benthos feeder) are cultured in summer when sea cucumber goes to aestivation. The jellyfish and scallop utilize plankton that the sea cucumber and shrimp do not use, and the biodeposits of the former two are food source for sea cucumber. This is a typical example of multi functional integration with trophic, spatial and temporal integration, resulting in high economic and ecological efficiencies (Ren, 2012). II 6 Disease prevention integration Integrated mariculture of shrimps and molluscs and/or crabs and/or macro algae are popular because of white spot disease (White Spot Syndrome Virus, WSSV). The co culture of puffer fish and shrimp (Liu et al., 2007) is an example of integration based on disease control as the fish prey on ailing shrimp. Fish will not get infected by the WSSV virus, while if healthy shrimp preying on ailing shrimp would get infected. II 7 Other integrations Besides above mentioned types of species integration there are also other types which are based on other considerations, such as co culture of broodstock from the Chinese carps with carnivorous fish, such as mandarin fish. The mandarin fish predates on small fishes which compete for feed with the broodstock fish resulting in higher food availability for the broodstock (Yang et al.,2006). 14

III. Integration of systems III 1 System integration: aquatic systems By system integration we refer to the integration of aquaculture with other activities, in this case other aquatic production activities. Integration may take place in the same water body or through sequentially linked sub systems. Integration of aquatic sub systems through sequential linkage of systems with different species is based on the flow of waste streams in order to utilize the trophic relationship between all cultured species (III 1 1 partitioned systems). For example, integration of tilapia, shrimp, oysters and seaweed (Shen et al., 2007), where shrimp feeds on pellets, tilapia removes zooplankton, the oyster filter phytoplankton, and seaweed absorb the inorganic nutrients. It is also possible to link the culture of aquatic species to agriculture activities, making use of the same water body (III 1 2). Fish rice integration is a typical and the most popular example of this type of integration (Liu and Huang, 2008). When culture of aquatic animals is integrated with production of aquatic vegetables it is called Aquaponics (III 1 3). Aquatic vegetables absorb inorganic nutrients from water and thereby reduce nutrient loading from the aquaculture system. Integration of aquaculture with waterfowl rearing is popular all over China (III 1 4). The faeces of the duck or goose is either feed for the fish or become manure that simulates primary production (Luo et al., 2002). It is also popular to integrate fish culture with culture of soft shell turtle (Sun, 2004), and also examples of integrated fish and frog cultures are known (Sun, 2004; Zheng et al., 2004) (III 1 5). In Aquasilviculture (III 1 5) mangrove plantation is integrated with aquaculture (shrimp, oyster or fish). It has been shown that by combining fish culture with mangrove forest both growth rates of the fishes and water quality were improved significantly (Yu et al., 2005). Fish cage culture can also be applied in ponds (III 1 7) where for example tilapia kept in cages still control water quality but feed competition between tilapia and shrimp is avoided (Sun et al., 2010). III 2 System integration: aquatic & land systems Aquaculture can also be integrated with other productive activities on nearby land. The pond sub system is then connected to the sub system on land, thereby promoting production efficiency and ecological efficiency of the whole area. Pond aquaculture can be integrated with livestock and/or poultry farming (III 2 1) (Dai and Yan, 1999; Chun et al., 2009; Li and Yu, 2000). The faeces of livestock and chicken is then used as manure to fertilize the fish pond, and some of the faeces can be fed to the fish directly. Recently food hygiene issue of this type of integration has drawn much attention of the public (Cai, 2009), however, after fermentation the faeces can be used safely. When aquaculture is combined with plantation (III 2 2) the integrated system includes a series of dike pond systems, in which aquatic animals are cultured in the pond and grain (Zheng, Sun and Shi, 2006), grass (Tang, Jiang, Sun and Yang, 2010), vegetables and fruit trees (Liu and Huang, 2008) are planted on the pond dike. The sediment in the pond can be used as fertilizer for the plants on the dike, and the pond water can also serve as irrigating water for the plants. Finally, there are still other forms of integrated land aquatic systems in China, for example, integrated power plant aquaculture systems (Lin and Ji, 1993; Wang, 2003; Liu, 2005), and waste fed species aquaculture (Huang, 1992). However, the latter is not popular due to the hygiene issue of its products. 15

6. CASE STUDIES OF IMTA IN CHINESE COASTAL WATERS The previous sections have shown that China has a rich experience in integrated cultures, and out of the various types of integration (Table 5.1) trophic integration or Integrated Multi Trophic Aquaculture (IMTA) is one of the most important ones. However, relatively little information is available on IMTA system performance in the coastal Chinese waters (Troell, 2009). According to the prevailing conditions at the culture site there are many different possibilities of IMTA combinations. Given the vast number of cultured species around the world there are combinations that can be used in all situations from tidal flats to tropical estuaries and sandy beaches, regarding that species from different trophic levels that have appropriate interactions are selected. The following chapter describes a number of co culture possibilities that are currently in use for integrated aquatic production occurring in marine pond systems (case studies 1 3) and in open water cultures along the Shandong peninsular in China (case studies 4 7). These case studies provide technological and scientific information on the use, type and characteristics of each IMTA practice. Specific information on the use of biological tracers and modelling tools in research are also provided. The last section of this chapter focuses on environmental benefits and economic revenues of IMTA systems in comparison to monocultures. Case study 1: Pond culture of shrimp, clam and seaweed Shrimp cultures rely on the external input of feed. However, residual feed and faecal products from shrimp may serve as a food source for clams in integrated culture systems, while the excretory products generated by both shrimp and clams are taken up by the macro algae and converted into plant biomass through photosynthesis (Figure 6.1). Shrimp Pellets DO Metabolic wastes (NH 4, Inorganic nutrients Faeces Particulate matter (organic nutrients) Residues Absorption Absorption Seaweed Phytoplankton DO Metabolic wastes (NH 4, CO 2) Consumption by bivalves Clam Figure 6.1 Case study 1: Schematic representation of nutrient fluxes within an IMTA pond system including shrimp, clam and seaweed cultures 16

Table 6.1 Energy budget and conversion efficiency in shrimp monoculture (P) and different levels of integrated shrimp, clam and seaweed culture (PCS1 PCS4) Level of integration P PCS1 PCS2 PCS3 PCS4 P stocking rate (ind m 2 ) 30 30 30 30 30 C stocking rate (ind m 2 ) 0 7 15 30 45 S stocking rate (g m 2 ) 0 360 280 200 120 P net production (g m 2 ) 115 119 117 137 107 P yield size (g ind) 5.5 6.1 5.3 5.5 5.3 P survival rate (%) 68 70 68 78 63 C net production (g m 2 ) 5 16 33 25 S net production (g m 2 ) 938 743 780 390 Photosynthetic conversion 0.1 0.7 0.6 0.8 0.5 efficiency (%) Total energy conversion 43 91 83 92 61 efficiency (%) N utilization rate (%) 25 38 35 36 26 P utilization rate (%) 7 14 14 17 10 Ratio of output and input 1.2 1.9 1.7 1.7 1.3 P=Shrimp (L. vannamei), C=Clam (C. sinesis), S=Seaweed (G. lichevoides). Integration of shrimp (L. vannamei), clam (Cyclina sinesis) and macro algae (Gracilaria lichevoides) pond culture is conducted at Tanggu, Tianjin, where energy budget and conversion efficiency of different culture systems, in which shrimp were either cultured in monoculture or as part of integrated cultures, have been studied. The results (Table 6.1) indicated that integration of shrimp with bivalve and seaweed can raise culture efficiencies, ecological efficiencies and economic efficiencies (Bao et al., 2006; Chang et al., 2006; Wang et al., 2006; Dong et al., 2007). Nutrient utilization is improved in integrated systems (Table 6.1). Wang et al (2006) showed that discharge rates could be reduced by 110% and 250% for N and P respectively compared to monoculture systems. Integrated systems with shrimp and clams, thus excluding seaweed, reduced nutrient discharges by 18 25%. During the past decade 9 kinds of integrated shrimp culture structures in ponds have been optimized (Table 6.2). This shows that optimal culture densities of the species co cultured with shrimp in marine pond systems varies between species and integration type. In general it can be concluded that a three species integration structure is ecological more efficient than two species integration systems. Table 6.2 Optimal co culture densities of integrated shrimp culture in marine pond systems Integration Gross production ratios Reference F. chinensis + tilapia 1: 1 Wang et al., 1998 F. chinensis + razor clam 1: 3 Wang et al., 1999a F. chinensis + oyster 1: 6 Su et al., 2003 F. chinensis + bay scallop 1: 1 Wang et al., 1999b F. chinensis + tilapia + razor clam 1: 0.3: 2 Tian et al., 2000 L. vannamei + Cyclina 1: 0.8 Wang et al., 2006 L. vannamei + Gracilaria 1: 5 Niu et al., 2006 L. vannamei + Cyclina + Gracilaria 1: 1.3: 8.3 Wang, 2006 L. vannamei + Scapharca + Gracilaria 1: 1: 5.9 Niu, 2006 17

Case study 2: Pond culture of shrimp and tilapia Integration of shrimp and filter feeder fish, such as tilapia, is popular in China, especially in brackish water ponds. In theory, the shrimp are fed with pellets and tilapia feeds on natural resources. However, there are some problems involved in the integration as tilapia may feed on the high protein food that are provided to shrimp. In addition tilapia can suppress zooplankton (Zhang et al., 1999), that in turn may cause a decline of primary production rates in pond and subsequently affect fish growth (Tian et al., 1997). Net isolated polyculture system of shrimp and tilapia (Figure 6.2) can solve these problems (Jie, 2008). Sun et al. (2010, 2011) reported that the areas without tilapia played a role as refuges for zooplankton. The refuge significantly increased the rotifer biomass and phytoplankton diversity, and decreased the phytoplankton biomass. However, the copepod biomass was not affected by the refuge. Shrimp Tilapia Shrimp Figure 6.2 Case study 2: A net isolated polyculture of shrimp and tilapia A comparison was made between production efficiencies of shrimp monoculture and net isolated polyculture of shrimp and tilapia, for a pond system in Dongying, Shandong Province. At start nine ponds were stocked with Pacific white shrimp juveniles (0.01 ± 0.01 g m 2 ), and six of them contained cages with tilapia (51.7 ± 19.6 g m 2 ) which were placed in the centre of the pond. Three of the polyculture ponds received feed (0.5% fish body weight feeds every day), while the others did not receive any external input. After 95 days survival rates and net production rates of shrimp in polyculture were higher compared to shrimp monoculture (Table 6.3). Table 6.3 Production data for shrimp monoculture and net isolated polyculture of shrimp and tilapia after a culture period of 95 days. Different letters indicate statistical significant differences Treatment Net production (g m 2 ) Shrimp Body weight (g) Survival rate (%) Tilapia Net production (g m 2 ) Shrimp monoculture 256 ± 2 a 11 ± 2 a 50 ± 4 a Shrimp tilapia culture 290 ± 9 b 9 ± 2 b 74 ± 15 b 112 ± 3 a without feed Shrimp tilapia culture with feed 288 ± 3 b 10 ± 3 ab 62 ± 5 ab 131 ± 2 b 18

Case study 3: Pond culture of sea cucumber and shrimp Sea cucumber integrated with shrimp pond farming utilizes wastes, such as residual food and faecal material, originating from the latter species. The effect of stocking density on growth and survival of integrated of sea cucumber (A. japonicus) and Chinese shrimp (F. chinensis) pond culture was studied by Qin (2009). The results indicated that the body weights and survival rates of sea cucumber were not significantly affected by shrimp nor sea cucumber stocking density. Shrimp growth, on the other hand, showed that with increase of shrimp stocking density growth was significantly reduced, with 40% lower growth at high densities (8 ind m 2 ) compared to low densities (2 ind m 2 ). Survival rates showed a similar pattern, with decreasing shrimp survival at higher stocking densities. Although the total shrimp production (210 kg hm 2 ) at high densities was higher than that at low densities (178 kg hm 2 ), the profit of the latter was higher due to significant difference of yield sizes and values. This study showed that integration of sea cucumber with shrimp is viable in pond systems, and thereby can provide additional profit from shrimp production without affecting the growth of the sea cucumber. Case study 4: Pond culture of sea cucumber and scallops/jelly fish Integration of scallops with sea cucumber culture accelerates biological sedimentation, through faecal deposition of the scallops, which serves as a food source to the detrivorous feeding sea cucumbers. It was indeed shown that sea cucumber (A. japonicus) growth was 50% higher when cultured together with scallops (Chlamys farreri) compared to sea cucumbers produced in monoculture systems (Ren et al. 2012). Conversely, sea cucumbers are not expected to enhance scallop growth and indeed no difference was observed for scallop growth in integrated systems compared to scallop monoculture systems, yet, adding sea cucumbers to scallop cultures will alleviate organic matter accumulation in the pond and thereby benefit the sustainability of the integrated system. Integration of jellyfish with sea cucumber is in principle similar to that with scallops. Jellyfish (Rhopilema esculenta) feeds on zooplankton and enhance the sedimentation rate of total particulate matter in ponds (Ren & Dong 2012). The same study also showed that the sea cucumber actively fed on the deposited material, and thereby reduced the organic accumulation in the pond. Integrated mariculture of sea cucumber with jellyfish can utilize both plankton in water column and organic matter in the sediment, resulting in improvement of economic products and reduction of the accumulation of organic matter in the ponds (Zheng et al., 2009; Ren & Dong, 2012). Carbon budgets of an integrated sea cucumber, jellyfish and shrimp culture at Homey Company showed that total organic carbon utilization was 9.3, which is higher compared to the 7.4 for sea cucumber monoculture (Li et al., 2013a; b). Additionally, the outflow from the pond contained lower nutrient concentrations compared to the input, therefore, this system was not only a production system of aquatic products but can also be considered as an organic matter purification system for the coast. Case study 5: Open water culture of abalone and kelp (suspended) In an IMTA system based on culture of abalone (Haliotis discus) and kelp (L. japonica), the excretory and waste products (NH 4, CO 2 ) generated by the abalone are taken up by the kelp and converted into plant biomass through photosynthesis. Kelp plants can in turn be used as a source of nutrition for herbivores, e.g. abalone (see upper part Figure 6.3). Abalone and kelp are co cultured on a large scale from suspended longlines in the coastal waters of North China. A demonstration area (1600 m 2 ) for polyculture of abalone and kelp was developed at Xunshan Fishery Company, located in north coast of Sanggou Bay. Each cultivation unit consisted of four rafts with longlines containing in total 12,000 kelp Laminaria japonica plants and 33,600 abalone individuals. Kelp was cultivated from November to June. When the plants reached 1m length they were removed from the culture rope and placed into the net cage for feeding the abalones. When feeding the abalones once a week, market size (8 10cm) could be reached within 2 years. The aim of the project was to determine the optimal co culture proportion of abalone and seaweed. In these production systems ammonia is considered as an important factor to assess the impacts of abalone farming on the environment. Ammonia excretion rates of abalone should not exceed uptake rates by kelp in 19