Integrated Mariculture: Asking the Right Questions

Aquaculture 226 (2003) 69–90 www.elsevier.com/locate/aqua-online

Integrated mariculture: asking the right questions

M. Troella,b,*, C. Hallingb, A. Neoric, T. Chopind, A.H. Buschmanne, N. Kautskya,b, C. Yarishf a The Royal Swedish Academy of Sciences, Beijer International Institute of Ecological Economics, Box 50005, 104 05 Stockholm, Sweden b Department of Systems Ecology, Stockholm University, 106 91 Stockholm, Sweden c National Centre for Mariculture, Israel Oceanographic and Limnological Research Ltd., P.O. Box 1212, Eilat 88112, Israel d Centre for Coastal Studies and Aquaculture, and Centre for Environmental and Molecular Algal Research, University of New Brunswick, P.O. Box 5050, Saint John, New Brunswick, Canada E2L 4L5 e Departamento de Acuicultura, Universidad de Los Lagos, Casilla 933, Osorno, Chile f Department of Ecology and Evolutionary Biology, University of Connecticut, 1 University Place, Stamford, CT 06901-2315, USA

Abstract

Reducing negative environmental impacts from aquaculture activities is a key issue for ensuring long-term sustainability of the industry. This study examines the major findings and methodology aspects from 28 peer-reviewed studies on marine aquaculture systems integrating fed and extractive organisms. All studies include seaweeds as extractive organisms. The main objective was to analyse the degree of relevance these findings have for large-scale implementation of integrated mariculture practices, and to identify necessary research areas for a future research agenda. The following directions for future research were identified: (1) understand in detail the important biological/biochemical processes in closed recirculating and open seaweed culture systems; (2) conduct research into these advanced aquaculture technologies at scales relevant to commercial implementation or suitable for extrapolation; (3) broaden the focus to include factors affecting seaweed growth and uptake capacity; (4) improve experimental design for statistical calculations; (5) attain a detailed understanding of the temporal variability in seaweed-filtered mariculture systems; (6) define numerical design parameters critical for engineers in designing commercial recirculation systems with seaweed filters; (7) study the influences of location-specific parameters, such as latitude, climate and local seaweed strains/species, on seaweed filter performance; (8) include economic components, considering the added value of seaweeds, and

* Corresponding author. Department of Systems Ecology, Stockholm University, 106 91 Stockholm, Sweden. Tel.: +46-8-673-9532; fax: +46-8-152464. E-mail address: [email protected] (M. Troell).

0044-8486/$ - see front matter D 2003 Elsevier B.V. All rights reserved. doi:10.1016/S0044-8486(03)00469-1 70 M. Troell et al. / Aquaculture 226 (2003) 69–90 feasibility aspects; (9) analyse the role and function of integrated aquaculture practices for improved environmental, economic, and social acceptability within the broader perspective of integrated coastal management initiatives; and (10) develop educational, training and financial incentive approaches to transfer these novel and somewhat complex technologies of integrated mariculture from the scientists to the industry. D 2003 Elsevier B.V. All rights reserved.

Keywords: Mariculture; Land-based system; Open-water system

1. Introduction

Most of the world’s fishing areas have reached their maximal potential for capture fisheries production, while demand for seafood worldwide is steadily increasing (FAO, 2001). The stagnation in fisheries of commercial species has also been accompanied by a gradual shift from large, valuable, carnivorous species to smaller, less valuable species (Pauly et al., 1998; Naylor et al., 2000; Caddy and Garibaldi, 2000). On the other hand, global production from aquaculture has been increasing steadily, having more than doubled in the last decade; aquaculture now supplies one third of seafood consumed worldwide (FAO, 2001). To meet future demands for foodfish supplies, aquaculture production needs to increase by 50 million Mt by the year 2050 (Tacon and Forster, 2001). The FAO (2001) cautions that such an increase in aquaculture production will depend on new research and improved management practices. According to the FAO, major issues that need to be addressed are problems with access to proper technology and financial resources, together with environmental impacts and diseases. Some argue that further increases in aquaculture production will come mainly from further investment in biotechnology (Hardy, 1999; Hew and Fletcher, 2001; Melamed et al., 2002), including technologies ranging from protein expression and DNA vaccines (and chips) to transgenic technologies. Large programs focusing on increasing aquaculture production through such means have been running in several countries for the past few decades and new ones are being launched (Myers et al., 2001). Increased knowledge and development of new methods within marine biotechnology have resulted in important breakthroughs for the aquaculture industry and further advances within this sector will continue to be important. However, without a clear recognition of the industry’s large- scale dependency and impact on natural ecosystems and traditional societies, the aquaculture industry is unlikely to either develop to its full potential or continue to supplement ocean fisheries (Naylor et al., 2000; Chopin et al., 2001). Thus, to increase accessibility of seafood to economically depressed people, or even to maintain it at current levels, aquaculture development must be based on relevant species choices and sound technologies more relevant to developing countries (Naylor et al., 2000; Williams et al., 2000; Hambrey et al., 2001). Traditional and low technology farming approaches contain lessons learned over many generations, which should be regarded as valuable instructive bases for modern aquaculture development. Future mariculture technologies could attain sustainability by integrating waste generating (fed) and cleaning (extractive) organisms in each farm (see review in M. Troell et al. / Aquaculture 226 (2003) 69–90 71

Buschmann et al., 2001; Chopin et al., 2001). Extractive species remove nutrients from the water. Many commercial shellfish are filter feeders that remove particulate organic nutrients; algae use sunlight to extract from the water dissolved inorganic nutrients. Thus, when integrated with fed aquaculture of, e.g. fish or shrimp, extractive organisms turn wastes into productive resources (Rawson et al., 2001, 2002; McVey et al., 2002). The new integrated aquaculture systems will use multiple species from different trophic levels for reducing wastes and costs (through recycling of wastes) while increasing total productivity (in weight and in value) with respect to feed input and pollution output. Polyculture has a long history in the freshwater environment, but not in marine and brackish waters. Although poorly studied in the past, a renewed interest in integrated techniques emerged in the early 1990s, and several different systems have since been proposed. These have attempted to: reduce the negative impacts of fed aquaculture on the aquatic environment; to productively remove and recycle toxic metabolites by using recirculating systems; to increase production of specific co-cultured extractive species (e.g. shellfish and seaweeds); and to increase overall productivity of the resources of feed, water and fossil energy (see Krom et al., 2001 for review; see also Section 3 for references). On a global scale, mariculture of extractive organisms already removes a significant fraction of nutrients from the world oceans. Global aquafeed supplies for marine fish and crustaceans aquaculture for 2000 was estimated at 4.5 million Mt [FAO Review of The State of World Aquaculture data]. Up to 4% of that quantity, 180,000 Mt, is excreted to the sea as ammonia-N (using FCR of 2, feed N content of 6% and 2/3 of nitrogen excreted as ammonia-N (TAN)). Nominal nitrogen content in seaweed and in shellfish is approximately 0.5% and 1%, respectively. With present global yields of approximately 10 million Mt each [FAO Review of The State of World Aquaculture data], these harvests already extract roughly 150,000 Mt of nitrogen. However, it should be noted that extractive and fed aquaculture are very often geographically disjunctive because of the predominant monoculture approach and, consequently, rarely balance each other at the regional scale. When new culture techniques/practices are being developed, there is a need for continuous evaluation of the achieved results. Research on integrated techniques in mariculture has now reached a stage where it has become necessary for such evaluation to be conducted. The benefits generated from such evaluation is that research efforts will be directed in the right direction by identifying issues being inadequately addressed, or by identifying new important research areas. Here we examine major findings and methodological aspects from 28 peer-reviewed studies on mariculture systems that integrate fed and extractive organisms, and that have been published during the last 30 years. What these studies have in common is that they all use seaweed as an extractive organism integrated with a fed culture system. Additional publications in the ‘‘grey literature’’ have been left aside. The present paper includes a general review of conducted research on integrated mariculture. The main focus is to provide an objective analysis of the degree of relevance findings may have for large- scale implementation of integrated mariculture practices. The potential of the seaweed- involved integrated mariculture approach, and the necessary areas for further research, are identified. 72 M. Troell et al. / Aquaculture 226 (2003) 69–90

2. Importance and benefits from integrated mariculture

2.1. Integrated aquaculture—its role in aquaculture development

Traditional integrated freshwater systems primarily seek to satisfy a complex of environmental (e.g. maximizing resource use) and social aims rather than only being concerned with maximizing short-term profit (Ruddle and Zhong, 1988; Bailey, 1988; Primavera, 1991; Wilks, 1995). Although the focus of recent work on integrated techniques in modern mariculture has been on reduction of waste discharge by promoting biofiltration capacity and water recirculation, these new systems have the potential to increase overall profits through more efficient resource use (Krom et al., 2001). Commercial modern marine and brackish water aquaculture is usually practiced as large monocultures. Like intensive feedlots, these systems have the potential to generate releases of waste material to the environment from uneaten feed and excreta. Even large-scale shellfish cultures can increase dissolved inorganic nutrient concentrations by increasing remineralisation of particulate organic material. This nutrification can result in various negative local environmental effects such as eutrophication, oxygen depletion, biodiversity modifications and pollution of the surrounding waters (Gowen and Bradbury, 1987; Braaten et al., 1988; Ro¨nnberg et al., 1992; Beveridge et al., 1994; Richardson and Jørgensen, 1996; Bonsdorff et al., 1997; Mattila and Ra¨isa¨nen, 1998; Pitta et al., 1999; Ha¨nninen et al., 2000; Naylor et al., 2000). Such effects are common features of all economic activities that concentrate resources collected over vast areas and use them in a linear fashion without managing the environmental consequences. The quality and quantity of wastes from aquaculture depend mainly on culture system characteristics and the choice of cultivated species, but also on feed quality and management (Iwama, 1991). Different species release wastes of different quality and quantity, but generally most of the nutrients added through feed are released to the environment (Fig. 1). The dominant fraction being released is generally in a dissolved form, particular for nitrogen (Gowen et al., 1991; Holby and Hall, 1991; Hall et al., 1992; MacIntosh and Phillips, 1992; Briggs

Fig. 1. Range of nutrient discharge (total) from some aquaculture species. For salmon and shrimps, the percentages are for both nitrogen and phosphorus; for bivalves and abalone, the percentages are only for nitrogen. One hundred percent is the total amount of nutrients in feed (cf. Gowen et al., 1991; Holby and Hall, 1991; Hall et al., 1992; MacIntosh and Phillips, 1992; Briggs and Funge-Smith, 1994; Robertson and Phillips, 1995; Bergheim and A˚ sga˚rd, 1996; Neori et al., 2000). M. Troell et al. / Aquaculture 226 (2003) 69–90 73 and Funge-Smith, 1994; Robertson and Phillips, 1995; Bergheim and A˚ sga˚rd, 1996; Neori et al., 2000). The local impact on the environment then ultimately depends on local/regional hydrodynamic conditions, the physical, chemical and biological characteristics of the receiving ecosystem (expressed in the region’s biological assimilative capacity) and on additional release of waste products from other sources (e.g. urban and rural human settlements and sewage effluents, agricultural/industrial runoffs, precipitations, etc.). The rapid scale increase now seen in human activities in coastal areas puts further pressure on already impoverished functions of coastal ecosystems. Therefore, legislative guidelines, standards and controls regarding the discharge of nutrients from various sources (including aquaculture operations) are starting to become more stringent in many countries. Development of integrated mariculture, i.e. bioremediation via integrated concepts with a capacity to restore the quality of the discharged water to its natural state, may help the aquaculture industry avoid noncompliance, and gain both direct and indirect benefits from improving water quality and coastal ecosystem health. The aquaculture industry has, over the last decades, managed to substantially reduce its emission of wastes by intense research into feed development, better conversion efficiency and improved management (Bergheim and A˚ sga˚rd, 1996; Hardy, 1999; Chopin et al., 2001, Hardy and Tacon, 2002). Until now, this has been the only effective approach for reducing discharge of dissolved nutrients from open systems (i.e. cages). Land-based systems have some alternatives for reduction in dissolved nutrients but these have limitations (discussed below). Integration with seaweed introduces a practical and viable solution (Chopin et al., 2001). Additional arguments for integrated mariculture include possible increased income, social benefits and diversified production (Buschmann et al., 1996; Troell et al., 1997; Chopin et al., 1999b, 2001).

2.2. Existing alternative measures for waste treatment

Release of untreated water from intensive mariculture systems is more often the rule rather than the exception. Practice of ‘‘dilution–the solution’’ dominates. Adding to the mariculture cost, profit cutting approaches like water treatment are resisted by the industry, and are adopted by it only under pressure from regulating agencies or from nature itself (e.g. red tides, infectious diseases, etc.). Today, dissolved nutrients can be removed effectively from some mariculture effluents by biological and chemical filters. Biological filters are often based on bacterial oxidation of ammonia to the less toxic form of nitrogen, nitrate, by nitrification. The method, however, does not remove nutrients. Under anaerobic conditions and with the presence of proper organic matter, other bacteria can further transform nitrate waste into N2 gas that then can be removed from the system. These systems are, however, both complex and costly. Genetic engineering and selection of nitrifying and denitrifying bacteria is suggested as contributing significantly to enclosed, recirculating marine culture systems in the future (Lyndon, 1999). Different species of microalgae are also used as biological filters in outdoor tank/pond systems or in indoor tubular photo-bioreactors. Microalgae can advantageously be grown in the same pond as fish, and then be filtered out by an integrated culture of shellfish. However, 74 M. Troell et al. / Aquaculture 226 (2003) 69–90 microalgal populations are difficult to control (bloom and crash cycles) in open ponds, and limit water exchange. Too much water exchange may simply wash them out. Two main types of chemical filters are used—activated carbon filters and ion-exchange filters. Carbon filters remove dissolved nutrients by having an active carbon substance to facilitate adsorption of inorganic molecules. Carbon filters are mainly used for targeting organic molecules. Ion-exchange filters are based on ion-charged material that gets quickly inactivated in ion-rich seawater. Both these filters also get quickly biofouled. With respect to phosphorus removal, it should be possible to use chemical precipitation in a similar way as used in sewage treatment facilities. Biological phosphorus removal, by either oxic or anoxic bacteria, is also an option, but the phosphorus-saturated bacterial biomass has to be removed and disposed of to complete the process. The above discussion only applies to land-based systems; for open-water systems, no similar applicable methods for removing dissolved nutrients have been suggested in the literature. Techniques similar to those used on land could, possibly, be adapted to open systems if these farming systems are made more ‘‘closed’’ and if flow and retention time could be controlled (Bodvin et al., 1996). To our knowledge, no such integrated system exists today at any commercial scale. In summary of this issue, most biofiltration techniques in land-based systems only partially or unconsistently transform nutrients into other forms, thus not really reducing the environmental load. They also have limited abilities to function in environments with high nutrient concentrations. It can be concluded that integration with seaweed offers perhaps the most viable and attractive option to the profitable extraction of nutrients discharged from mariculture into valuable products.

3. Research on integrated mariculture

Advances in contemporary society with integrated cultivation techniques in marine and brackish environments originate from the development of intensive methods using seaweeds (macroalgae) and bivalves for treating sewage outlets (Ryther et al., 1972, 1975; Goldman et al., 1974). Methods using seaweeds for treating effluents from enclosed land-based mariculture systems were initiated in the mid-1970s (Haines, 1975; Ryther et al., 1975; Langton et al., 1977; Harlin et al., 1978). The rapid expansion of intensive mariculture systems (i.e. fish farming and shrimp cultivation) and the concern for negative effects on the environment from such practices, have, during the 1990s, renewed and increased research into the development of seaweed-based integrated techniques (Vandermeulen and Gordin, 1990; Cohen and Neori, 1991; Neori et al., 1991, 1996; Haglund and Pederse´n, 1993; Buschmann et al., 1994, 1996, 2001; Jime´nez del Rio et al., 1996; Krom et al., 1995; Neori, 1996; Troell et al., 1997; Neori and Shpigel, 1999; Chopin et al., 1999a,b). All these studies have demonstrated that wastewater from intensive and semi-intensive mariculture is a suitable nutrient source for the intensive production of seaweed, thereby reducing the discharge of dissolved nutrients to the environment. Integrated land-based cultures have, in some cases, also developed to include additional combinations of species from different trophic levels. Examples of such systems M. Troell et al. / Aquaculture 226 (2003) 69–90 75 are: integrated bivalve-shrimp cultivations (Wang and Jacob, 1991; Jacob et al., 1993; Hopkins et al., 1993; Lin et al., 1993; Osorio et al., 1993), integrated bivalve-fish cultivations (Shpigel and Blaylock, 1991; Shpigel et al., 1993b) and integrated cultivations consisting of both algae and molluscs cultivated in effluents from fish or shrimps (Shpigel et al., 1991, 1993a; Enander and Hasselstro¨m, 1994; Neori et al., 1996, 1998, 2000; Neori and Shpigel, 1999). In open-culture systems, such as fish cage farming, only a few studies have investigated the possibilities of integrated farming. Among these some have focused on using seaweeds as biofilters (Hirata and Kohirata, 1993; Hirata et al., 1994; Troell et al., 1997; Chopin et al., 1999a), and some on the possibilities of using bivalves (Jones and Iwama, 1991; Taylor et al., 1992; Stirling and Okumus, 1995; Troell and Norberg, 1998; Buschmann et al., 2000; Mazzola and Sara`, 2001; Cheshuk, 2001). There are relatively few studies investigating the feasibility or application of integrated cultures of seaweeds and shrimps (Chandrkrachang et al., 1991; Lin et al., 1992, 1993; Primavera, 1993; Enander and Hasselstro¨m, 1994; Flores-Nava, 1995; Phang et al., 1996; Jones et al., 2001), although this approach has been regarded as promising (Primavera, 1993; Flores-Nava, 1995; Lin, 1995). There are also some studies of integrated cultures with seaweeds using mathematical models to generate data (Petrell et al., 1993; Petrell and Alie, 1996) or develop novel production technologies (Bodvin et al., 1996). Recent reviews on integrated mariculture research include a focus on seaweed utilization (Buschmann et al., 2001; Chopin et al., 2001), on bivalve utilization (Troell et al., 1999a), on shrimp farming (Troell et al., 1999b) and on integrated cultures from a coastal zone management perspective (Newkirk, 1996; Brzeski and Newkirk, 1997; Rawson et al., 2002). Conclusions from above reviews confirm the suitability of using seaweeds as biofilters. Using bivalves with the same purpose may, however, have certain limitations (Troell and Norberg, 1998; Cheshuk, 2001). With respect to shrimp farming, it is concluded that integration with seaweeds may be positive but more research is needed (Troell et al., 1999b).

4. Integrated seaweed mariculture—analysis of methods and results

The studies on integrated mariculture were divided into three groups: (1) tank cultures (mainly fish-based systems), (2) pond cultures (fish and shrimp-based systems) and (3) open-water cultures (mainly fish systems). Findings from the 28 studies included in the analysis are summarised in Table 1. From this table, we have then formulated questions under the following key issues, which we consider crucial for successful implementation of integrated mariculture on any large scale:

1. Efficiency How efficiently can seaweeds absorb nutrients from mariculture waste? How do seaweed biofilter functions change over time (diurnal and seasonal cycles)? What factors, other than light, nitrogen and phosphorus, may limit seaweed production? What nitrogen and phosphorus fractions should be analysed? 76

Table 1 Summary of important factors for integrated aquaculture systems that includes seaweeds Main culture Cultured Culture Experimental Time Optimization N uptake Uptake Qualityf Production Replicates Economic References facility species densitiesa scaleb scale aimsc removald efficiencye factorsg and calculation

controlsh 69–90 (2003) 226 Aquaculture / al. et Troell M. Tanks and ponds (fish or shrimp) Ponds/ milkfish/ fish: D; pond/aquarium: 1–3 G C – Eq T, S, pH, R(6),C no Alcantara et al., aquarium Gracilariaopsis seaweed: D B/D months L O2, G 1999 Tank salmon/ fish: D – B; fish; seaweed: 1 year G n.i. 70 – 95% Eo, Ay T, L, pH, R(3),C no Buschmann Gracilaria seaweed: B (NH4) CO2, D, et al., 1994 B, C F, G, N Tank salmon/ fish: A, B; fish; seaweed: >1 year G C up to 90% Eq, Aq T, G R (n.i.), C yes Buschmann Gracilaria seaweed: C B (NH4) et al., 1996 Tank salmon/ fish: C, D; fish; seaweed: 3–6 G C – Eo T, pH, O2, n.i. no Haglund and Gracilaria seaweed: C A months L, D, G Pederse´n, 1993 Tank salmon/ fish: C; seaweed: D >1 month G, N C, A 45%(NH4) T, S, pH, R (9 – 22ps), no Subandar et al., Laminaria seaweed: L, D, F, G C 1993 A, B Tank/ seabream/algae fish A; fish, seaweed: >1 year N C 30 – 90% T, S, O2, n.i. no Pagand et al., raceway seaweed: n.i. A (DIN) pH, G 2000 Tank seabream/Ulva fish: B; fish: B; 1 year G, N C, A 19 – 97% T, pH, L, R (3 ps), C no Jime´nez del Rio seaweed: B seaweed: C (DIN) D, F, G et al., 1996 Tank seabream/Ulva fish: FE; seaweed: C < 1 month G, N C, A 85%(NH4) T, pH, S, R(3) no Vandermeulen seaweed; F, D, G and Gordin, B, C 1990 Tank seabream/Ulva fish: FE; seaweed: C 1 year G, N C, A 39 – 96 T, L, F, R (3 ps?) no Neori et al., seaweed: (NH4) D, G 1991 A–C Tank seabream/Ulva fish: FE; seaweed: C 1 year G, N C, A – T, L, F, R (3 ps?) no Cohen and seaweed: D, G Neori, 1991 A–C Tank seabream/Ulva fish: B, C; fish: B; >1 year N, W C, A 34 – 49% T, L, S, O2, R (0 – 3), C no Neori et al., seaweed: C seaweed: C; B (DIN) Chl, G 1996 Tank seabream/Ulva fish: B, C; fish: B; >1 year N, W C, A 34 – 49% T, L, S, O2, R (0 – 3), C no Krom et al., seaweed: C seaweed: C; B (DIN) Chl, G 1995 Pond/ditches shrimp/ shrimp: FE; seaweed: B >1 month G A – N, F, G, R(3) no Nelson et al., Gracilaria seaweed: D fert 2001 Pond/canal shrimp/ shrimp: FE; shrimp comm.; 1–3 G n.i. – Eo, Aq T, pH, S, R(4),C no Phang et al., Gracilaria seaweed: C seaweed: C months O2, N, G 1996 Aquaria Fish/ fish: C; fish; seaweed: < 1 month N C 32 – 112% T, S, L, R(4),C no Harlin et al., (mollusca) Gracilaria; seaweed: A D (NH4) O2, pH 1978 Ulva Tank clams/Hypnea clam: FE; seaweed: D < 1 month N C, A – Ay T, F, G n.i. no Haines, 1975 seaweed: A .Tol ta./Auclue26(03 69–90 (2003) 226 Aquaculture / al. et Troell M. Tank abalone/ abalone: abalone; 1 year N C, A 3 – 88% Eo, F T, F, fert, n.i. (ps) no Neori et al., Gracilaria; B, C; seaweed: B (DIN)i G 1998 Ulva seaweed: B, C Tank abalone/ abalone: n.i.; abalone; 3–6 G C – F T, L, fert, R(3),C no Evans and Palmaria seaweed: A seaweed: D months (abalone), D, G Langdon, 2000 N Tank Tapes/Hypnea clams: A, B; clams; < 1 month N C 70% T, G R (ps), C no Langton et al., (polyculture) seaweed: B seaweed: D (NH4) 1977 Pond/tanks seabream/ fish/seaweed: fish: A; oyst; 1 year G, N C, A 90% T, G, pH, R(ps) no Shpigel et al., oyster; clams/ C; clams/ clams: B; (NH4) O2, cells 1993a Ulva oyster: A seaweed: C Tank fish, oyster, fish: B; fish; oyst; 6–12 G, N C 100% T, G R (3), C no Chow et al., sea urchins/ oyst: A; urchin; months (NH4) 2001 Gracilaria urchin: B; seaweed: C seaw: A Tank abalone/ abal: up to abalone; fish; 1 year G, N, W C, A 70 – 100% F T, G, pH, O2 n.i. (ps) yes Neori et al., seabream/Ulva; A; fish: B; seaweed: C (NH4) 2000 Gracilaria seaw: A, B Tank sewage/oyster/ oyster: n.i.; oyster: n.i.; 3–6 N C – G, S, pH n.i. no Ryther et al., Chondrus; seaweed: A seaweed: C months 1975 Ulva (continued on next page) 77 78

Table 1 (continued) Main culture Cultured Culture Experimental Time Optimization N uptake Uptake Qualityf Production Replicates Economic References facility species densitiesa scaleb scale aimsc removald efficiencye factorsg and calculation controlsh Lab study shrimp effluent/ shrimp: A; shrimp A; < 1 month N C 2 – 76% T, O2, R (3), C no Jones et al., oyster/ seaweed: B oyst; seaweed: (NH4) S, Chl, 2001 Gracilaria D bact, TSS .Tol ta./Auclue26(03 69–90 (2003) 226 Aquaculture / al. et Troell M. Open water (fish) Cage cultures/ salmon/ fish: FE; n.i. >1 year N A – pigment, N R no Chopin et al., nets; poles Porphyra seaweed: n.i. (3 nutrient), 1999b C Cage culture/ salmon/ fish: FE; fish: comm.; 1–3 G, N A – Eo, Ay G, depth R (10), C yes Troell et al., frames Gracilaria seaweed: C seaweed: B months 1997 Cages/net yellowtail/Ulva fish: FE; fish: comm.; 1 year G n.i. – T, G R (18) no Hirata and cages seaweed: D seaweed: C Kohirata, 1993 Cages/net seabream/Ulva fish: C; fish: comm.; < 1 month G, O2 n.i. – O2, CO2, R (n.i.), C no Hirata et al., cages seaweed: n.i. seaweed: C depth, G 1994 (mollusca) Open culture/ oyster/ oyster: n.i.; oystr; seaweed: 3–6 G C – G, T R (10), C no Qian et al., aquarium Kappaphycus seaweed: comm./C, D months 1996 A/B a Culture densities: fish, shrimp or molluscs: A= >30 kg mÀ 3 , B = 10 – 30 kg mÀ 3 ,C=1–10kgmÀ 3 ,D=<1kgmÀ 3 , FE = farm effluent; seaweeds: A= >5 kg mÀ 3 , B=2–5 kgmÀ 3 , C = 0.5 – 2 kg mÀ 3 , D = < 0.5 kg mÀ 3 , n.i. = no information. b Experimental scale: A= >10,000 l, B = 1000 – 10,000 l, C = 100 – 1000 l, D = < 100 l, comm. = commercial, n.i. = no information. c Optimization; aim: G = growth/production; N = nutrient uptake and treatment; W = water saving. d Nutrient uptake and treatment: C = measured concentration changes in water; A= measured nutrient content in algae, n.i. = no information. e Uptake efficiency: data suitable for realistic estimation of reduction of nutrient concentrations in waste water passing seaweed units. – = not measured or data not presented. f Quality of yield for : Eo = epiphytes observed; Eq = epiphytes quantifyed; F = feed; Ay = agar, alginate, carrageenan yield; Aq = agar, alginate, carrageenan quality. g Other production factors measured: T = temp, S = salinity, O2 = dissolved O2, L = light, D = stocking densities, F = flow rates, N = nutrients (in species and accum.), C = nutrient concentrations in water, Chl = chlorophyll a, bact = bacteria. h Replicates and controls: R = replicates, C = control, ps = pseudoreplication; number of replicates in brackets, n.i. = no information. i Fertilisers added. M. Troell et al. / Aquaculture 226 (2003) 69–90 79

2. Quality Does seaweed quality change in integrated cultures? Does integration with seaweed change the quality and value of the main cultured species? 3. Design and scale of experiments What is a sufficient degree of replication for obtaining statistically significant results? What controls/references should be used for comparison? How should the experiments be designed to allow for extrapolation to scaled up and commercial farming? 4. Economy Can economic benefits from integrated culture be accurately confirmed?

4.1. Efficiency

Many studies from both land-based and open-water cultures confirm that nutrients released from fish, shrimps and bivalves are suitable for seaweed growth. This is not surprising as the nitrogen released from such organisms—NH3—is often the preferred nitrogen source for seaweeds (Lobban and Harrison, 1994; Carmona et al., 2001). 3 À Dissolved release of phosphorus increases phosphate (PO4 ) concentrations in the water, which is the form of phosphorus most suitable for seaweed growth (Lobban and Harrison, 1994; Neori, 1996; Chopin and Wagey, 1999). In addition, some seaweed species in integrated cultures take up nutrients above and beyond their requirements for growth (Troell et al., 1997; Chopin et al., 1999b). Such ‘‘luxury uptake’’ of nitrogen and phosphorus has been confirmed in earlier studies on seaweed physiology (Lobban and Harrison, 1994; Harrison and Hurd, 2001). To allow nonambigous interpretations and meanings (Buschmann et al., 2001), the important concepts related to seaweed nutrient uptake should be clarified. The nutrient reduction efficiency is defined as the average reduction (%) in nutrient concentration in water. Nutrient uptake rate, on the other hand, is defined as the amount of nutrients removed per unit area of, e.g. seaweed pond per unit time. Both these concepts are important; they will vary depending on culture conditions such as depth, light, stocking density and water turnover rates (Buschmann et al., 2001). Specific properties of the seaweed species, their biology and physiology, will also play a significant role. High nutrient uptake rates are achieved by supplying the seaweed culture with high areal (per unit area) loads of nutrients, conditions that also maximise seaweed areal yield and seaweed protein content. Under these conditions, however, reduction efficiency is low, and therefore a large fraction of the dissolved nutrients remains in the water. To achieve high nutrient reduction efficiency, a seaweed culture should be ‘‘starved’’— supplied with a low areal load of nutrients, a situation that supports low seaweed areal yields with low protein content (Buschmann et al., 1994). In an integrated fish farm, it is therefore necessary to optimise the aerial nutrient load to the seaweeds, to reach acceptable levels of both nutrient uptake rate and reduction efficiency. In a recirculating system, high levels of ammonia may be acceptable (depending of the tolerance of the fed organism), allowing operation of the seaweed culture with high areal nutrient loads and achieving high nutrient uptake rates. The system will produce a high areal yield of high 80 M. Troell et al. / Aquaculture 226 (2003) 69–90 protein seaweed. If high nutrient removal (i.e. high reduction efficiency) is necessary for following environmental standards or decreasing ammonia concentrations in recirculating systems, the seaweed culture will be supplied with low areal nutrient loads, but then seaweed areal yield and protein content will be low. Under some circumstances, at some South African abalone aquaculture sites that encounter occasional harmful algal blooms (Sales and Britz, 2001), it may be important to be able to switch from a through-flow high nutrient uptake system that produces good quality seaweed, to a high nutrient reduction efficiency closed recirculating system that maintains good water quality for the abalone. The only means for optimisation between nutrient uptake rate and reduction efficiency in open-water cultures (e.g. cage cultures) may be through manipulations in seaweed densities, culture depth, species choice or harvesting frequencies (Halling et al., unpublished). However, even if the system can be manipulated to some extent, it will not be possible to achieve the same precision as in land-based cultures.

4.1.1. How efficiently can seaweeds absorb nutrients from mariculture waste? To simply add additional seaweed units until satisfactory nutrient concentrations have been reached would, from a practical and economical perspective, be an unrealistic solution. Besides optimising the different separate components of the culture, also the overall performance of the culture needs to be optimised. This implies that quantitative information about seaweed culture performance needs to be available, with respect to nutrient uptake rate, reduction efficiency and secondary considerations (e.g. yield and protein content) under various culture conditions that reflect possible commercial situations. It is not only the uptake rate that we are interested in, but also the capacity to reduce nutrient concentrations below appropriate environmental standards. Table 1 shows that almost all of the investigated studies presented data that describe nitrogen removal by seaweeds, either as nutrient content in the harvested seaweeds or as changes in the water nitrogen concentration between the inflows and the outflows of the seaweed ponds. The data indicated that seaweeds efficiently remove dissolved nitrogen, ranging between 35% and 100% of nutrient input (in tanks or ponds). These results are, however, based on studies with different seaweed species and different experimental setups which make it difficult to draw nonambiguous quantitative general conclusions. Different objectives, i.e. some focusing on maximising uptake rates rather than reduction efficiency, also make it difficult to generalise. To provide valuable information and to be of practical use for integrated mariculture development, the nutrient water concentrations need to be in accordance with concentrations (and water volumes) that would be released by commercial cultures of fed species. It is, otherwise, difficult to use the data in planning for cultures on a commercial scale. Most of the investigated studies used rearing densities similar to what is found in commercial cultures of fed species. One important aspect for recirculating systems is to keep nutrient concentrations below certain limits. This parameter is affected by nutrient load (concentration and exchange rates), seaweed uptake rate and seaweed culture area. Data on reduction efficiency were presented in 68% of the studies. Open-water studies, however, do not easily permit for such measurements and, therefore, only related to uptake rates (based on the fractions of nutrients bound in seaweed protein). M. Troell et al. / Aquaculture 226 (2003) 69–90 81

Even though several seaweed species have proven able to take up nitrogen and phosphorus efficiently and at high rates, several concerns exist in relation to how effective they are on a commercial scale (Buschmann et al., 2001). These concerns are related to the areal nature of the sunlight-dependant seaweed biofilters, whereas intensive fish culture fish that is related to water volume. The extrapolation of some experimental data indicated that a large area of seaweed cultivation would be required for the removal of a significant proportion of the waste nutrients from a commercial fish farm (Troell et al., 1997). Only a very restricted number of studies have tried to address this aspect or develop solutions.

4.1.2. How do seaweed biofilter functions change over time? In most cases, intensive mariculture production proceeds year-round, and their interactions with most environments vary seasonally. Of course, the sunlight-dependent seaweed biofilter’s nutrient uptake rate and areal yield, both vary seasonally, usually being highest in summer. It is, therefore, important to capture the seasonal trends in seaweed biofilter performance over entire annual cycles. Unfortunately, only few studies were conducted long enough, and less than 40% covered even one-year production cycle.

4.1.3. What factors, other than light, nitrogen and phosphorus, may limit seaweed production? From the perspectives of seaweed growth and environmental waste load, focusing mainly on nitrogen and phosphorus is, in most cases, relevant. These nutrients are usually the main limiting factors of algal growth and also constitute a potential threat to the environment. Other nutrients may, however, also limit seaweed growth and especially in recirculating systems oxygen super-saturation, high pH or inorganic carbon limitation may occur (Craigie and Shacklock, 1995). A buildup of bacteria in the system could potentially impact negatively on seaweed growth or/and co-cultured animals. Only one of the investigated studies controlled bacterial growth. Furthermore, only 25% of the studies were designed to capture the role of seaweed stocking densities and only 30% tried to find out the importance of different light regimes. Epiphytic growth may diminish seaweed production, but only 24% of the studies mentioned anything about this (and only 7% quantified it). Few studies investigated specifically the importance of flow rate regimes (see Buschmann et al., 2001 for discussion). Water turbidity and competition with microalgae are two potentially important factors that not are addressed in any of the studies.

4.1.4. What nitrogen and phosphorus fractions should be analysed? The nitrogen fractions being analysed are mainly total ammonia nitrogen (TAN; i.e. the + + sum of NH4 and NH3), ammonium (NH4) and total nitrogen (as the sum of TAN + nitrite + nitrate + dissolve organic nitrogen, DON). As relatively few of the studies on tanks or ponds (15%) investigated the possibilities for closed recirculation systems, it is easy to understand why focus on identification of the toxic ammonia form, i.e. the concentration of un-ionic ammonia (NH3) is absent. As the equilibrium between ionised and un-ionised forms depends on temperature and pH, it should, however, be possible to calculate the concentration of the toxic form if these variables were monitored. In most cases, data on temperature were available and in 40% of the studies pH was also monitored. Phosphorus 82 M. Troell et al. / Aquaculture 226 (2003) 69–90 and its role(s) are rarely investigated as (a) phosphorus effluent discharges are generally an order of magnitude less than nitrogen effluent discharges (Chopin et al., 1999b), (b) generally considered the second limiting factor of seaweed growth, far behind nitrogen in temperate regions (but not in subtropical or tropical regions), and (c) the chemistry of the different phosphorylated fractions in seawater remains complex. Phosphorus speciation can, however, be instrumental for the energetic metabolism and energy redistribution among the different components of an integrated aquaculture system.

4.2. Quality

4.2.1. Does seaweed quality change in integrated cultures? Seaweeds produced in integrated systems may serve as nutrient scrubbers in some cultures and then be discarded. In other cultures, seaweeds either add to the overall income of the operation by possessing a value on their own (phycocolloid, pigment, food, feed, etc.) or provide an indirect value as a feed component for other co-cultured animals (e.g. abalone and sea urchins). It is, therefore, important to obtain high quality seaweeds, i.e. considering aspects dealing with both direct price-generating qualities (e.g. phycocolloid quality) as well as nutritional qualities (proteins, pigments, nutraceu- tical value, etc.). A few of the studies (22%) included detailed information about how the quality of the cultured seaweeds (e.g. phycocolloid production or protein content) is affected by the culture system. Only two of the studies on Gracilaria presented data on agar strength or melting point. In cases in which seaweeds were fed to animals, only 12% of the studies looked closer into nutritional qualities. Also related to quality is the condition of the seaweeds with respect to epiphytic growth of other algae and/or invertebrates (see Section 4.1.3).

4.2.2. Does integration with seaweed change the quality and value of the main cultured species? A very important aspect in recirculating systems is the effect that recirculated water may have upon the cultivated animal. The removal of nutrients and water re-oxygenation by seaweeds are positive for the animals, but the presence of seaweeds may also have negative implications. This may also be true for open cultures if the density of seaweed is very high or water flow rates are low. As mentioned earlier (under Section 4.1.3), no studies have looked at the pathogen transfer from the seaweed unit to the cultured animals. The influence of seaweeds on oxygen concentrations in culture waters, on a diurnal basis, has only been considered in some of the studies. The fact that only few studies focused on possibilities for closed integrated systems probably explains why most of the studies did not include effects on the co-cultivated animals.

4.3. Design and scale

There is generally a tendency for poor replication of experimental units within large- scale aquaculture studies. Many of the investigated studies also failed in this respect. To be able to use and compare findings from research on integrated cultures, it is important that experimental work is carried out with a sufficient degree of replication. This, however, is M. Troell et al. / Aquaculture 226 (2003) 69–90 83 not always easy to accomplish. When conducting studies looking at properties of culture systems, a balance is needed between he capture of temporal/spatial details and the long- term/commercial scale ‘‘real’’ culture system performance. Moreover, often scientists have only restricted access to industrial aquaculture sites, due to divergences between academic/ scientific priorities and commercial priorities or regulatory/legislative barriers.

4.3.1. What is a sufficient degree of replication for obtaining statistically significant results? It is of course impossible to give a general answer to this question as the type of experiment and experimental conditions varies, generating different amounts of variance. But it is a fact that many of the investigated studies failed, for reasons outlined in the previous section, to replicate their experimental units. Statistical analysis was therefore missing from 60% of the studies. Some studies also failed in separating true replicates from pseudo-replication.

4.3.2. What controls/references should be used for comparison? A control should reflect a 0-treatment, i.e. an experimental procedure the tested experimental treatments can be compared against. The 0-treatment is important, as it will give indications of the true effects of tested treatments. Many of the investigated studies did not use any true 0-treatment but instead discussed their results by either comparing different treatments, comparing to results from other experiments or not making any comparison at all. It may be important to be able to separate the influence of factors such as bacteria, phytoplankton, periphyton, epiphytes, etc., from the ‘‘true’’ seaweed effect. Admittedly, for open-water studies in heavily developed aquaculture regions, it may be extremely difficult to find real ‘‘control’’ sites, remote enough from any other aquaculture operation and still presenting comparable hydrodynamic, chemical, physical and biological conditions. Often regional reality forces statistical compromises with the selection of ‘‘reference’’ sites.

4.3.3. How should the experiments be designed to allow for extrapolation to scaled up and commercial farming? An important aspect, that in many cases is quite frustrating for people working within certain sectors of aquaculture research, is the conflict between obtaining results with high accuracy and obtaining results with sufficient relevance for industry. This is, of course, a problem shared with other sectors within natural science. Thus, there is a danger that precise (spatial and/or temporal) results from the laboratory cannot be extrapolated to larger-scale systems. Even though most of the investigated studies consisted of small systems, their experimental designs generated results relatively suitable for extrapolation to commercial situations.

4.4. Economy

4.4.1. Can economic benefits from integrated cultures be accurately confirmed? The ultimately essential economic aspect of integrated mariculture was missing from most of the studies investigated. Only 7% of the studies presented any economic 84 M. Troell et al. / Aquaculture 226 (2003) 69–90 calculations; moreover, they only incorporated incomes from production, i.e. omitting costs for various investments or management practices. Information about profitability is crucial when comparing different species and experimental designs. This is also important as the objective for integration may differ between users. Thus, to be able to validate the concept, there is a need to show upon feasibility both regarding technology and economy. To our knowledge, no country in the world regulates (paying for pollution) and/or enforces the treatment of aquaculture discharges/effluents, and therefore no large-scale farms treat their effluents (settling ponds in some shrimp farms makes one exception). It is, therefore, quite difficult to calculate such costs for the current industrial mariculture techniques/practices. Still, the cost of an alternative technology for restoring water quality and coastal health downstream of any commercial mariculture farm is a value added to the seaweed nutrient retention technology for the same service. This value has to be recognised and quantified. It should be added to the production cost of the principal crop culture (e.g. fed finfish or shrimp), and should constitute an income to the seaweed culture. By performing the environmental remediation service, the extractive component of an integrated aquaculture system will significantly improve and sustain the economics of the modern mariculture farm. When upcoming effluent regulations will force aquaculture companies to internalize the total environmental costs of their operations according to the ‘‘user pays’’ principle, the economic benefits of integrated aquaculture systems will become much clearer and monetary quantifiable. Moreover, by implementing better management practices, the aquaculture industry should increase its social acceptability, a variable to which it is very difficult to give a monetary value, but an imperative condition for the development of its full potential. It is important to emphasise that the yield and culturing of each species must not be evaluated and compared with a monoculture in isolation from the other species in the integrated system. It is the total ecological economic benefits of the whole integrated system that needs to be evaluated (cf. Folke and Kautsky, 1992).

5. Conclusions and suggestions for future research efforts

Most studies confirmed that nutrients from land-based and open-water mariculture operations are suitable for seaweed growth. However, an authoritative synthesis is still lacking on the many factors that can determine seaweed culture design and functioning in commercial integrated mariculture. Even though very few studies focused on closed recirculation systems, many studies report on the capacity for seaweed to dramatically reduce nutrient concentrations in effluents, to convert in the process large quantities of nutrients into useful seaweed biomass, and to improve additional water quality parameters. Many of the investigated studies also managed to capture the behaviour of integrated cultures sufficiently enough for the results to be extrapolated to larger-scale cultures. Research on land-based systems has been most successful in this respect, but more work is needed on open cultures. To be useful, such research should be made on a large commercial scale, and should address the biology, engineering, operational protocol, and economics of the technology. M. Troell et al. / Aquaculture 226 (2003) 69–90 85

Looking especially at closed recirculating systems, we found that some research groups managed to address critical issues more successfully than others. Nevertheless, there is a general need for including other factors that may limit seaweed growth, and also look at various aspects of seaweed quality. The experimental design could generally be improved, i.e. by increasing replication and using more accurate control/reference sites. This would facilitate more statistical analyses and comparisons. Moreover, temporal variations were omitted in many studies. Finally, economic considerations should get much more attention. Besides a general increase in research efforts on integrated techniques, i.e. allocation of research funds and exploration of various possible combinations, we suggest the following directions for future research:

1. Understand in detail the important biological/biochemical processes in closed recirculating and open seaweed culture systems. 2. Conduct research into these advanced aquaculture technologies at scales relevant to commercial implementation or suitable for extrapolation. 3. Broaden the focus to include factors affecting seaweed growth and uptake capacity. 4. Improve experimental design for statistical calculations. 5. Attain a detailed understanding of the temporal variability in seaweed-filtered mariculture systems. 6. Define numerical design parameters critical for engineers in designing commercial recirculation systems with seaweed filters. 7. Study the influences of location-specific parameters, such as latitude, climate and local seaweed strains/species, on seaweed filter performance. 8. Include economic components, considering the added value of seaweeds, and feasibility aspects. 9. Analyse the role and function of integrated aquaculture practices for improved environmental, economic and social acceptability within the broader perspective of integrated coastal management initiatives. 10. Develop educational, training and financial incentive approaches to transfer these novel and somewhat complex technologies of integrated mariculture from the scientists to the industry.

Acknowledgements

This work was supported by the Swedish International Development Agency (SIDA), the Natural Sciences and Engineering Research Council of Canada (AquaNet Network of Centres of Excellence in Aquaculture), the Fundacio´n Terram and the British Embassy, Chile, the Israeli Department for Energy and Infrastructure, European Union and Israeli Department of Science joint programs, and a USA–Israel BARD grant, and the State of Connecticut Critical Technology Grant Program, the Connecticut, New Hampshire and New York Sea Grant College Programs, and the Office of Oceanic and Atmospheric Research, NOAA (DOC), USA. We are grateful for Kathy Chopins help with editing and for very constructive comments by anonymous reviewers. 86 M. Troell et al. / Aquaculture 226 (2003) 69–90

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Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture

Amir Neoria,*, Thierry Chopinb, Max Troellc,d, Alejandro H. Buschmanne, George P. Kraemerf, Christina Hallingd, Muki Shpigela, Charles Yarishg

a Israel Oceanographic & Limnological Research Ltd., National Center for Mariculture, P.O. Box 1212, Eilat 88112, Israel b University of New Brunswick, Centre for Coastal Studies and Aquaculture and Centre for Environmental and Molecular Algal Research, P.O. Box 5050, Saint John, New Brunswick, Canada E2L 4L5 c Beijer International Institute of Ecological Economics, The Royal Swedish Academy of Sciences, Box 50005, 104 05 Stockholm, Sweden d Stockholm University, Department of Systems Ecology, 106 91 Stockholm, Sweden e Universidad de Los Lagos, ifmar Center—Instituto de Investigacio´n de Recursos Marinos y Ambientes Costeros, Camino Chinquihue km 6, Puerto Montt, Chile f State University of New York at Purchase, Department of Environmental Science, Purchase, NY 10577, USA g University of Connecticut, Department of Ecology and Evolutionary Biology, 1 University Place, Stamford, CT 06901, USA Received 4 August 2003; received in revised form 31 October 2003; accepted 4 November 2003

Abstract

Rising global demand for seafood and declining catches have resulted in the volume of mariculture doubling each decade, a growth expected by the FAO to persist in the decades to come. This growth should use technologies with economical and environmental sustainability. Feed accounts for about half the cost in current high-volume fed mono-species aquaculture, mainly fish net pens or shrimp/fish ponds, yet most of this feed becomes waste. The resulting environmental impact and rising feed costs therefore hamper further growth of such farms. As in certain traditional polyculture schemes, plants can drastically reduce feed use and environmental impact of industrialized mariculture and at the same time add to its income. These nutrient-assimilating photoautotrophic plants use solar energy to turn nutrient-rich effluents into profitable resources. Plants counteract the environmental effects of the heterotrophic fed fish and shrimp and restore water

* Corresponding author. Tel.: +972-8-6361445, +972-50-993-746; fax: +972-8-6375761. E-mail address: [email protected] (A. Neori).

0044-8486/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2003.11.015 362 A. Neori et al. / Aquaculture 231 (2004) 361–391 quality. Today’s integrated intensive aquaculture approaches, developed from traditional extensive polyculture, integrate the culture of fish or shrimp with vegetables, microalgae, shellfish and/or seaweeds. Integrated mariculture can take place in coastal waters or in ponds and can be highly intensified. Today’s technologies are well studied and documented. They are generic, modular and adaptable for several culture combinations of fish, shrimp, shellfish, abalone, sea urchin and several species of commercially important seaweeds and vegetables. A 1-ha land-based integrated seabream–shellfish–seaweed farm can produce 25 tons of fish, 50 tons of bivalves and 30 tons fresh weight of seaweeds annually. Another farm model can produce in 1 ha 55 tons of seabream or 92 tons of salmon, with 385 or 500 fresh weight of seaweed, respectively, without pollution. Preliminary calculations show a potential for high profitability with large integrated farms. Several freshwater integrated fish–vegetable farms and a couple of modern fish–algae–shellfish/abalone integrated mariculture farms exist today, and several additional farms are planned. Three major international R&D projects promise to soon expand the horizons of the technology further. 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. D 2004 Elsevier B.V. All rights reserved.

Keywords: Integrated aquaculture; Seaweed biofiltration; Modern mariculture

1. Introduction and rationale

While capture fisheries fall short of world demand, annual consumption of seafood has been rising, doubling in three decades (FAO, 2000). Obviously, just as we no longer depend on hunting, we can no longer depend solely on fishing. Even today, aquaculture provides over a quarter of the world’s seafood supply, a figure the FAO expects will approach 50% by the year 2030 (Tidwell and Allen, 2001). With the diminishing availability of freshwater, most of this growth will take place in seawater. Intensive fish mariculture today takes place largely in net pens while shrimp is farmed in coastal lagoons or ponds. The economic success of this approach has much to do with the fact that the nutrification of the environment involves little monetary cost to the growers, that is to say that mariculture does not yet have to internalize the cost of water treatment. However, this age is coming to a timely end in industrialized nations. Awareness by scientists, industry, the public and politicians is such that technologies with uncontrolled impact are no longer considered sustainable (Chamberlaine and Rosenthal, 1995; Costa-Pierce, 1996; Sorgeloos, 1999; Naylor et al., 2000; Chopin et al., 2001). Salmon farms in Norway are already legislated, regulated and licensed on siting, disease control, use of therapeutants, interaction with other species, waste discharges and feed quotas (Maroni, 2000). Moreover, growers themselves are coming to the realization that their own fish and shrimp live in these waters and are the first to suffer from nutrification consequences, such as harmful algal blooms, anoxia and parasites. This in itself is costly; however, growers will soon also have to pay for the remediation of the environmental impacts caused by their operations. When synthesizing the treatment of modern aquaculture waters (freshwater and marine) and the mitigation of the environmental impacts of aquaculture (Lee and Jones, 1990; Wu, A. Neori et al. / Aquaculture 231 (2004) 361–391 363

1995; Krom et al., 2001), two main practical approaches are emerging: bacterial dissimilation into gases and plant assimilation into biomass. Bacterial biofilters are dissimilative. Through a series of oxidation and reduction processes, they break the pollutants down into harmless gaseous N2 and CO2. Bacterial biofilters allow effective and significant aquaculture water recirculation (van Rijn, 1996); however, the technology is not simple (Losordo, 1998). A basic bacterial biofiltration system for fishpond water consists of devices for (i) oxygen supply, (ii) removal of particulate organic matter, (iii) oxidation (ozonation) of refractory dissolved organic matter, (iv) removal (nitrification) of ammonia, (v) alkalinity control, (vi) dissipation of excess CO2, (vii) disinfection and last but not least, (viii) a lot of water pumping through the different devices. Such systems accumulate nitrate and sludge that need to be disposed of. In the best case, using the most advanced technology, the nitrate and organic sludge are treated by an additional anoxic denitrifying bacterial biofilter arrangement. Sadly, most current ‘‘water recirculating’’ farms discharge their nitrate and organic sludge to the environment (van Rijn, 1996). Furthermore, while bacterial biofilter technologies are suitable for relatively small intensive land-based cultures of lucrative organisms (Zucker and Anderson, 1999), there is no information available as to how such technologies can be integrated into large-scale low-cost fish net pens and semi-intensive shrimp ponds. Biofiltration by plants, such as algae, is assimilative, and therefore adds to the assimilative capacity of the environment for nutrients (Krom, 1986). With solar energy and the excess nutrients (particularly C, N and P), plants photosynthesize new biomass. The operation recreates in the culture system a mini-ecosystem, wherein, if properly balanced, plant autotrophy counters fish (or shrimp) and microbial heterotrophy, not only with respect to nutrients but also with respect to oxygen, pH and CO2 (Hirata et al., 1994; Rai et al., 2000). Plant biofilters can thus, in one step, greatly reduce the overall environmental impact of fish culture and stabilize the culture environment. Algae, and in particular seaweeds, are most suitable for biofiltration because they probably have the highest productivity of all plants and can be economically cultured (Gao and McKinley, 1994). The complexity of any biofiltration comes at a significant financial cost. It is this added cost that has prevented bacterial-based intensive aquaculture technologies from producing large quantities of fish at competitive prices (Losordo and Westerman, 1994; Zucker and Anderson, 1999). To make environmentally friendly aquaculture competitive, it is necessary to raise its revenues. This can be achieved by increasing productivity per unit of feed, which, can account for about half of the production cost. The waste nutrients are considered in integrated aquaculture not a burden but a resource, for the auxiliary culture of plants (Chamberlaine and Rosenthal, 1995). The new plant biomass can nourish various shellfish, including bivalves, abalone, brine shrimp and sea urchins (Wikfors and Ohno, 2001). The additional shellfish culture is not essential, however, since algae (seaweeds, mainly) have a large market. About 8.6 million metric tons/year valued at US$6.2 billion in 1998 (FAO, 2000) are sold for human consumption, phycocolloids, feed supplements, agrichemicals, nutraceuticals and pharmaceuticals. A culture system that diversifies its products by integrating the culture of fish/shrimp with an extractive algal culture, and with organisms that grow on these algae, therefore makes much sense, not only ecologically, but also economically (Anon., 2003). 364 A. Neori et al. / Aquaculture 231 (2004) 361–391

The integrated culture of plants and herbivores side-by-side with fish and shrimp is a practical technology (Neori and Shpigel, 1999; Naylor et al., 2000). The environmental and economic consequences of this approach are better understood when the organisms are categorized into fed and extractive species (Chopin et al., 2001; Rawson et al., 2002). Fed organisms (mainly carnivorous fish and shrimp) are nourished by feed, be it commercial diets, ‘‘trash’’ fish, etc. Extractive organisms, as the name implies, extract their nourishment from the environment. The two economically important cultured groups that fall into this category are bivalve mollusks and seaweed. Bivalve mollusks (e.g., mussels, oysters and clams) build their own body while degrading suspended organic particles (uneaten feed, phytoplankton and bacteria) that they filter from the water. Algae use sunlight to build their biomass, while assimilating dissolved inorganic nutrients removed from the water. If properly cultured, the organisms of both extractive groups can turn pollutant nutrients into commercial crops and loaded effluents into clean water. The present review describes the background, the evolution and the main current practices of plant-based integrated aquaculture from polyculture and freshwater integrated aquaculture, through fish–microalgae–shellfish integrated mariculture to those systems involving fish–seaweed (macroalgae) and macroalgivores in seawater, the basics of their operation, their functioning and their economics.

2. Seaweed as a monoculture

The culture of organisms that are low in the food chain and that extract their nourishment from the sea involves relatively low input. It is therefore no surprise that the two predominant cultures in world mariculture are extractive-seaweed and filter- feeding shellfish (FAO, 2000; Muller-Feuga, 2000; Troell et al., 2003). One seaweed, Laminaria japonica, cultured on long-line ropes in the coastal waters of China, constitutes over half of the world’s aquatic plant production (Chiang, 1984; Fei et al., 1998, 2000; Tseng, 2001). Seaweeds and other aquatic plants constitute a natural resource, whose value to mankind has been extensively reviewed by Critchley and Ohno (1998). Seaweeds are eaten raw, cooked or processed. Many cosmetic and pharmaceutical products also contain seaweed polysaccharides—agars, carrageenans and alginates. The harvests of cultured seaweeds and shellfish from coastal waters also remove nearly a million tons of protein, with around 150,000 metric tons of nitrogen annually (Troell et al., 2003). The harvest of tens of thousands of metric tons of fresh seaweed and clams has economically mitigated eutrophication in the polluted Venice Lagoon (Cuomo et al., 1993). Huguenin (1976) comprehensively reviewed the early developments and the basic engineering-economic considerations in modern land-based seaweed cultivation. The traditional and modern practices of seaweed culture have been reviewed recently in a series of 19 papers, emanating from a World Aquaculture Society (WAS) workshop on the subject, in three issues of World Aquaculture Magazine (Chopin et al., 1998; 1999a,b). Most open-water seaweed monoculture has taken place in Asia, South America, South Africa and East Africa. Nevertheless, Porphyra and Laminaria cultivations are thought to have a potential for generating a viable seaweed mariculture and integrated aquaculture A. Neori et al. / Aquaculture 231 (2004) 361–391 365 industries in the USA and Canada (Chopin et al., 2001). In Atlantic Canada, successful research and development has led to the mass culture of the edible seaweed Irish Moss, Chondrus crispus, in land-based fertilized tanks and ponds (Craigie and Shacklock, 1995). In Chile, significant advances have been made towards the commercial production of Chondracanthus chamissoii and Callophyllis variegata as food products for the Japanese market (Buschmann et al., 2001a). Efficient large-scale and long-term tank cultivation of Gracilaria has been reported from Florida (Capo et al., 1999). In Israel, the various aspects involved with the commercial culture of the agarophyte Gracilaria conferta have been thoroughly developed since the 1980s (Friedlander et al., 1987, 1991).

3. The evolution from polyculture, through fish–phytoplankton–bivalve to modern seaweed-based integrated intensive mariculture

Thanks to their manageability, land-based aquaculture systems offer much promise for sustainability in tropical, subtropical and temperate mariculture. Issues such as solid waste management, nutrient recycling and feed conversion enhancement are more easily and profitably addressed on an industrial scale on land than in open-water fish farms. Pond mariculture also allows the farmer to confront and mitigate the difficult issues of ecosystem degradation, mangrove degradation, exotic species escapes, pathogen and gene transfer between cultured and wild species, harmful algal blooms (red tides), poaching, weather damage, waste and chemical discharge to the sea, and conflicts with other stakeholders of the sea. Various combinations of these benefits, intuitively sensed by aquaculturists and evidently proven profitable, have probably led to the independent development in different parts of the world of traditional aquatic polyculture, the forerunner of modern integrated mariculture. Aquatic polyculture is traditionally practiced in such parts of the world as the Pacific and Indian Ocean-bordering nations, particularly China. Rice/fish culture, popular in Europe in the 19th–early 20th centuries, has been practiced in China for millennia (Fernando, 2002). Earthen marine ponds, associated with natural or agriculture plants (such as mangroves and rice) are used on a wide scale for extensive shrimp farming in China, Indonesia, Ecuador, India, the Philippines, Taiwan, Thailand, Japan and more recently in Vietnam (Binh et al., 1997; Alongi et al., 2000). In Northern Europe, ducks, fish and crayfish have been raised together in freshwater ponds (Maki, 1982). The ducks eat the algae and small fish, and deposit manure, which promotes further growth of algae and other aquatic plants. Crayfish eat these plants, as do other herbivorous fish. In turn, predatory fish such as bass eat these. People then harvest the fish, ducks and crayfish. This type of polyculture is a managed imitation of a natural ecosystem. The culture of microalgae in wastewater from animal feedlots has also been researched and practiced in several countries for years, but will not be discussed further here. The use of seaweeds for such purposes has received only little attention (e.g., Asare, 1980; Edwards, 1998). The cohabitation of very different crops in one polyculture pond requires compromises in the farm management, leading to overall reduced yields for each organism compared with monocultures. The integration of monocultures through water transfer between the organisms alleviates this deficiency of polyculture and allows intensification. 366 A. Neori et al. / Aquaculture 231 (2004) 361–391

Edwards et al. (1988) crystallized the general definition of integrated farming as occurring when ‘‘an output from one subsystem in an integrated farming system, which otherwise may have been wasted, becomes an input to another subsystem resulting in a greater efficiency of output of desired products from the land/water area under a farmer’s control.’’ It is a prerequisite, however, that a successful sustainable integrated farming system mimics, as much as possible, the way the natural ecosystem functions (Folke and Kautsky, 1992). Kautsky and Folke (1991) introduced the concept of ‘‘integrated open sea aquaculture’’, in which coastal waters, made eutrophic by fish net pens, agricultural runoff and sewage, are used to supply cultured seaweed with dissolved nutrients and shellfish with plankton. The concept of integrated aquaculture constitutes an essential element in Coastal Zone Management, aimed at reducing, in an economically and socially beneficial manner, the adverse environmental impacts of aquaculture (freshwater, saline or marine) on the coastal environment (Chow et al., 2001; Brzeski and Newkirk, 1997; McVey et al., 2002). One solution does not, however, fit all. Integrated farming, particularly aquaculture systems are dynamic, changing according to such variables as location, season, species and social environment (Edwards, 1998; Little and Muir, 1987). Traditional integrated mariculture has been located principally in China, Japan and South Korea where farms of fish net pens, shellfish and seaweed have been placed next to each other in bays and lagoons. Through trial and error, optimal integration has been achieved, but the information for quantification and design has seldom been published (e.g., Fang et al., 1996; Sohn, 1996). Such mariculturists may not even be aware that what they do amounts to extensive integrated mariculture, and that to succeed, the fed and extractive components of their region’s mariculture should work in harmony. Western countries have been latecomers to modern integrated aquaculture. Only toward the end of the 20th century, when the assimilative capacity of natural ecosystems was being overloaded by monocultures of shrimp and fish (Primavera, 1993; Rajendran and Kathiresan, 1997), did the interest in using algae as nutrient scrubbers in integrated aquaculture of finfish, shellfish and crustaceans become renewed (Gordin et al., 1981; Chopin and Yarish, 1998). It was then realized that the recycling of waste nutrients by algae and filter-feeding shellfish is the most likely way to economically improve world mariculture sustainability (e.g., Cuomo et al., 1997; Blancheton, 2000). In modern coastal integrated mariculture, shellfish and seaweed are cultured in proximity to net pen fish culture (Troell et al., 1997; Troell and Norberg, 1998; Chopin and Bastarache, 2002). These studies have shown the potential of open-water integrated mariculture, once conditions are right (see in Troell et al., 2003). It should be noted, however, that the biofiltration of effluents by shellfish converts ‘‘nutrient packs,’’ in the form of microorganisms, into dissolved nutrients, which, may negatively impact the environment (Kaiser et al., 1998; Troell and Norberg, 1998). In land-based integrated culture (Neori et al., 1993; Shpigel et al., 1993b; Shpigel and Neori, 1996), the fed organisms, fish or shrimp, the extractive algae and the algivores are each cultured in their own pond or tank at medium to high levels of intensity. The water recycles between them. This allows taking care of the secondary mineralization of nutrients from the algae consumed ‘‘in farm.’’ A Saudi Arabian shrimp farm on the coast of the Red A. Neori et al. / Aquaculture 231 (2004) 361–391 367

Sea, perhaps the largest and most innovative of its kind, passes the effluents from over a hundred 1-ha shrimp ponds into an additional area of 100 ha of treatment ponds/lagoons, rich with algae, bacteria and shellfish (New, 1999). According to this paper, the farm has greatly raised the assimilative capacity of the coastal desert oligotrophic ecosystem and has eliminated most of the environmental problems associated with the more traditional shrimp farms. The inception of modern integrated intensive mariculture on land has been the work of Ryther et al. (Goldman et al., 1974; Ryther et al., 1975) who approached, both scientifically and quantitatively, the integrated use of extractive organisms—shellfish, microalgae and seaweeds—in the treatment of household effluent. They described the concept and provided quantitative experimental results of integrated waste-recycling marine aquaculture systems. A domestic wastewater effluent, mixed with seawater, was the source of nutrients for phytoplankton culture, which in turn was fed to oysters and clams. Other organisms were cultured in a separate food chain, based on the organic sludge of the farm. Dissolved remnants of nutrients in the final effluent were filtered by seaweed (mainly Gracilaria and Ulva) biofilters. The weakness of this approach was the questionable value of organisms grown on human waste effluents. Adaptations of this principle to the treatment of intensive aquaculture effluents in both inland and coastal areas was proposed (Huguenin, 1976) and quickly followed by the integration to their system of carnivorous fish and of the macroalgivore abalone (e.g., Tenore, 1976). The environmental and economic sense behind the integrated mariculture concept has instigated similar systems to independently be studied, or at least modeled, in Australia (Jones et al., 2001), Canada (Jones and Iwama, 1991), China (Shan and Wang, 1985; Lu et al., 1997; Qian et al., 1999b; Rawson et al., 2002), France (Hussenot et al., 1998; Lefebvre et al., 2000; Pagand et al., 2000), Japan (Inui et al., 1991), Thailand (Enander and Hasselstrom, 1994; Kwei Lin et al., 1993) and the USA (McDonald, 1987; Wang, 1990; Hopkins et al., 1993; Jacob et al., 1993; Sandifer and Hopkins, 1996; Kinne et al., 2001). Common to these approaches were dense phytoplankton populations, which were allowed to grow in fish/shrimp ponds or their effluents. The phytoplankton-laden water then passed over or through filter feeding shellfish, which harvested the phytoplankton. Most of these studies have, however, been either qualitative or at too small a scale to allow extrapolation for the industry. Perhaps the first practical and quantitative integrated land-based cultures of marine fish and shellfish, with phytoplankton as the biofilter and shellfish food, were described by Hughes-Games (1977) and Gordin et al. (1981). A semi-intensive (1 kg fish mÀ3) ‘‘green-water’’ seabream and grey mullet pond system on the coast of the Gulf of Aqaba (Eilat)–Red Sea, supported dense populations of diatoms, excellent for feeding oysters (Krom et al., 1989; Erez et al., 1990). Hundreds of kilograms of fish and oysters cultured in this experiment were actually sold. Neori et al. (1989) and Krom and Neori (1989) quantified the water quality parameters and the nutrient budgets in more intensive (5 kg fish mÀ3) green water seabream ponds. For the most part, the phytoplankton in their ponds maintained a reasonable water quality and converted on average over half the waste nitrogen into algal biomass. The development of a practical intensive culture of bivalves in these phytoplankton-rich effluents, and the extremely fast bivalve growth rates achieved under these conditions, were described in a series of articles (Shpigel and 368 A. Neori et al. / Aquaculture 231 (2004) 361–391

Fridman, 1990; Shpigel and Blaylock, 1991; Shpigel et al., 1993a,b, 2001a; Neori and Shpigel, 1999). This technology has formed the basis for a small farm (PGP 1994) in southern Israel. Today, a significant amount of quantitative information has been gathered on the design, dimensions, performance, yields, pollution and even the expected income (as volatile as seafood prices can be) of the integrated mariculture of finfish–phytoplankton– shellfish. The conceptual understanding that has emerged from the data applies not only to Israel, but also with the necessary modifications to tropical, subtropical and temperate regions of the world. Similar systems are now studied in Southern (France, Spain and Portugal) and Northern (Scotland) Europe. Shpigel et al. (1993b) presented the first quantitative performance assessment of a hypothetical family-scale fish/microalgae/bivalves/seaweed farm, based on actual pilot- scale culture data. They showed that at least 60% of the nutrient input to the farm could reach commercial products, nearly three times more than in modern fish net pen farms. Expected average annual yields of the system (recalculated for a hypothetical 1-ha farm) were 35 tons of seabream, 100 tons of bivalves and 125 tons of fresh seaweed. The most conservative figures for the yields of such a farm would be 25 tons of seabream, 50 tons of bivalves and 30 tons of fresh seaweed (Neori, unpublished). This would, of course, be a technically demanding farm, requiring experienced hands to control changes in water quality and in suitability for bivalve nutrition, related to the inherently unstable phytoplankton populations (Krom et al., 1985; Krom and Neori, 1989; Shpigel et al., 1993a). Seaweed-based integrated farms, described in the next section, alleviate the obstacles involved with microalgal-based biofiltration.

4. Seaweed-based integrated mariculture

A primary role of biofiltration in finfish/shrimp aquaculture is the treatment by uptake and conversion of toxic metabolites and pollutants. Bacterial biofilters oxidize ammonia to the much less toxic but equally polluting nitrate (e.g., Touchette and Burkholder, 2000), while microalgae photosynthetically convert the dissolved inorganic nutrients into particulate ‘‘nutrient packs’’ (Kaiser et al., 1998; Troell and Norberg, 1998) that are still suspended in the water. Macroalgae (seaweed), in contrast, sequester the nutrients out of the water. The clean and oxygen-rich effluent of a seaweed biofilter can therefore be readily recirculated back to the fishponds or discharged. Hirata et al. (1994; Hirata, personal communication) calculated that in addition to all other benefits, in a recirculation system, each kilogram of Ulva stock produces enough oxygen daily to supply the entire demand of 2 kg of fish stock. Nighttime oxygen consumption by seaweed is much lower than its daytime oxygen production. For example, gross photosynthetic O2 production by Porphyra amplissima is up to 12 times higher than is its respiratory O2 consumption (Kraemer et al., unpublished data). Integrated over a 12-h-light/12-h-dark day, a Porphyra culture could generate an O2 À1 À1 surplus of 1.8 mmol O2 gFW day . By feeding fish (and maximizing their respiration) in the day, the efficacy of algal produced O2 for fish respiration can be maximized, (Schuenhoff et al., 2003). A. Neori et al. / Aquaculture 231 (2004) 361–391 369

Marketable biofilter organisms are essential to the commercial viability of integrated mariculture farms (Neori et al., 2001a,b). The seaweed genera most common in mariculture biofiltration (Ulva and Gracilaria) are safe and have been used for consumption by humans (B. Scharfstein, personal communication), by secondary cultured macroalgivores (such as abalone and sea urchins) and by other fish (Shpigel, Kissil and Neori, unpublished).

4.1. Coastal open-water-based systems

The water quality processes in open-water integrated mariculture are closest to the natural ones. To function well, seaweed culture and/or shellfish culture take place near the fish net pens and as much as possible in the same waters. Kelp (brown algae; Subandar et al., 1993; Ahn et al., 1998; Chopin, unpublished) and red algae (Buschmann et al., 1996; Chopin and Yarish, 1998) efficiently take up dissolved inorganic nitrogen present in fish net pen effluents (Troell et al., 1999), and seaweed production and quality are therefore often higher in areas surrounding fish net pens than elsewhere (Ruokolahti, 1988; Ro¨nnberg et al., 1992; Troell et al., 1997; Chopin et al., 1999c; Fei, 2001; Fei et al., 2002; Chung et al., 2002; Chopin, unpublished). Seaweed growth on mariculture effluents has been also shown to be superior to that on fertilizer-enriched clean seawater (Harlin et al., 1978; Lewis et al., 1978; Vandermeulen and Gordin, 1990; Neori et al., 1991; Neori, unpublished; Shpigel and Scharfstein, personal communication). Agar yield and gel strength in the agarophytic red alga Gracilaria have been shown to improve when it is cultivated in salmon culture effluents (Martinez and Buschmann, 1996). The phycocolloid content of red algae usually drops under nutrient enrichment, but the increased seaweed yield more than compensates for it and results in higher total phycocolloid yield (Troell et al., 1997; Chopin and Yarish, 1998). It was also demonstrated that the abundance of phytoplankton and organic particles and the growth of filter feeders often increase in waters that surround fish net pens (Buschmann et al., 2001b; Robinson, MacDonald and Chopin, personal communication). All these observations combine to make open-water fish–seaweed–shellfish integrated mariculture an attractive approach (Rawson et al., 2002). Integration with seaweeds and/or filter feeders is often the only economically feasible alternative for waste treatment in open-water systems (Troell et al., 2003). Indeed, a hybrid open-water/onshore integrated mariculture of seaweed, fish and shellfish has formed an integral part of the mariculture operations planned for the nutrient-rich upwelled water for generation of electricity by OTEC (Ocean Thermal Energy Conversion) in Hawaii (Mencher et al., 1983; OTEC web site http://www.nrel.gov/otec/what.html and references therein). More recent work in China by Fei et al. (2000, 2002) reported the rope culture of the economically important agarophyte, Gracilaria lemaneiformis near fish net pens. Growing over 5 km of culture ropes on rafts in Guangdong Province, the seaweed increased in density from 11.16 to 2025 g mÀ1 in a 3-month growing period. After these initial studies, they enlarged the culture area over the following 4 months to 80 km of rope. They reported that there was an increase in culture density on the culture ropes to 4250 g mÀ1. They estimated an increase in the biomass of Gracilaria (in the culture area) to 340 metric tons fresh weight due to its culture in close proximity to fish net pens. Different work along similar principles has 370 A. Neori et al. / Aquaculture 231 (2004) 361–391 taken place elsewhere (Hirata and Kohirata, 1993; Matsuda et al., 1996; Yamasaki et al., 1997; Yamauchi et al., 1994). Several groups have developed, particularly, the integrated cultivation of salmonids with kelps (Fujita et al., 1989; Subandar et al., 1993; Chopin et al., 2001) or with red algae (Buschmann, 1996; Buschmann et al., 1994, 1995, 1996, 2001b; Troell et al., 1997; Chopin et al., 1999c). Another interesting complementary integrated approach for the reduction of the environmental impact on the sea bottom by the net pen sludge has been the culture underneath them of scavengers (gray mullets—Katz et al., 1996; sea cucumbers—Ahlgren, 1998), or worms in the pond sludge (Honda and Kikuchi, 2002) as secondary crops. In open mariculture systems, nutrient uptake efficiency by seaweeds has been low in some systems due to the 3-D hydrographic nature of the water flow (Petrell et al., 1993; Troell et al., 1997; Troell et al., 2003); this technology therefore requires further R&D and modeling (such as on the potential of several harvests of several crops; Chopin, unpublished). Furthermore, studies investigating the open-water integrated mariculture approach have been hampered by the difficulties involved with experimentation and data collection at sea (Petrell et al., 1993; Petrell and Alie, 1996; Troell et al., 1997, Chopin et al., 1999c, 2001). The approach may generate a heightened commercial interest once high value seaweeds such as Porphyra, Laminaria or Macrocystis can be cultured as biofilters that produce novel human food products (Fei, 2001; Gutierrez et al., in press). It seems that coastal open-water integrated mariculture farms have not yet spread through the salmonid culture industry, not so much because of technical or biological obstacles, but rather due to ignorance and disbelief (Chopin, unpublished; Yarish, unpublished). A recent interdisciplinary project supported by AquaNet, the Network of Centres of Excellence for Aquaculture in Canada, is intended to set up several preindus- trial-scale demonstrations of integrated farms, to help the net pen farm owners become familiar with the approach of integrated salmon, mussels and kelp (Laminaria) culture (Chopin and Bastarache, 2002).

4.2. Land-based integrated aquaculture

Integrated aquaculture takes place in water of all salinities. A major evolution is taking place in freshwater integrated aquaculture. Lewis et al. (1978), Culley et al. (1981), Corpron and Armstrong (1983), Schwartz and Boyd (1995), Brown and Glenn (1999), and Brown et al. (1999) described the use of wetlands and floating plants in the treatment of freshwater and saline aquaculture effluents. While most wetland plants have little commercial value, the integration of fish culture with vegetable cultivation, referred to by some as ‘‘aquaculture hydroponics’’ (Seawright et al., 1998), ‘‘aquaponics’’ (Rakocy, 1999) and ‘‘partitioned aquaculture’’ (Turker et al., 2003) makes good economic sense. Effluents from an Arizona (USA) semi-intensive, low-salinity shrimp farm have recently been shown as a good nutrient source even for cereals and olive trees, with obvious economic advantages for both shrimp and crop farms (McIntosh and Fitzsimmons, 2003). The freshwater approach has culminated in the US Virgin Islands, where lettuce is cultured in the effluents of a tilapia farm in a two-crop recirculating production system (Rakocy, 1997, 1999). Future Aqua Farms, near Halifax, Nova Scotia, Canada, is also operating a hydroponics system with tilapia and spinach, lettuce, arugula, basil and watercress A. Neori et al. / Aquaculture 231 (2004) 361–391 371

(Lockett, 2003). In the USA, tilapia is cultured with phytoplankton (Turker et al., 2003). Bringing this approach back to seawater, a large shrimp-Salicornia farm has been operating in Eritrea for several years (web site http://www.cnn.com/2000/WORLD/ africa/12/25/eritrea.sea.farm/). Apparently, the farm cultures marine shrimp, whose excre- tions nourish microbial/phytoplankton-fed tilapia. From there, the water flows to Sali- cornia basins and finally to a mangrove plantation (http://www.shaebia.org/artman/ publish/article_251.html). Interesting studies on seaweed-based integrated mariculture, starting on a laboratory scale and slowly expanding to outdoors pilot scale, began appearing in the 1970s. In the earliest quantitative studies, Haines (1976), followed by Langton et al. (1977), reported on an excellent red seaweed yield when cultured in a shellfish culture effluent. Harlin et al. (1978) then reported on the integrated culture of fish and seaweed (Hypnea musciformis). The theoretical and practical principles of intensive large-scale land-based seaweed culture were studied and developed first at Woods Hole Oceanographic Institution in Massachu- setts and later at Harbor Branch Oceanographic Institution in Florida, USA, by Ryther et al. (Huguenin, 1976; Lapointe and Ryther, 1978; DeBusk et al., 1986; Hanisak, 1987; Bird, 1989) and in Halifax, Nova Scotia, Canada (Bidwell et al., 1985; Craigie and Shacklock, 1995; Craigie, 1998; Craigie et al., 1999). Seaweed-based integrated systems have since gained recognition as a most promising form of sustainable mariculture (Naylor et al., 2000), once their practicality, the quantitative aspects of their functioning and their economics are demonstrated (Vandermeulen and Gordin, 1990; Cohen and Neori, 1991; Neori et al., 1991, 1993; Shpigel et al., 1993b; Troell et al., 2003). Further developments in mariculture seaweed biofilter R&D, and the integration of fish or shrimp with seaweed culture, have taken place on land, or with results that are applicable to land-based farms, in Chile (Buschmann et al., 2001b, Gracilaria; Chow et al., 2001, Gracilaria), China (Chang and Wang, 1985; Qian et al., 1999a,b, Ulva), Israel (Neori and Shpigel, 1999, Ulva and Gracilaria), South Korea (Chung et al., 2002), the Philippines (Hurtado-Ponce, 1993, Gracilariopsis; Alcantara et al., 1999, Gracilariopsis), Spain (Grand Canaria—Jimenez del Rı´o et al., 1994, 1996, Ulva) and Sweden (Haglund and Pedersen, 1993, Gracilaria). Systems that integrate shrimp and red seaweed have been studied, the largest being in Hawaii (Nelson et al., 2001, Gracilaria), and small-scale efforts have been reported by Phang et al. (1996, Gracilaria) from Malaysia, Kinne et al. (2001, various algae) from the USA and Chang and Wang (1985), Yin (1987), Wei (1990) and Liu et al. (1997) from China, all of them with Gracilaria. Ali et al. (1994) reported on a laboratory-scale integrated culture of shrimp and green seaweed (Ulva) in Japan. There are also similar studies in the Asia Institute of Technology in Thailand (Yi et al., 2001; Kwei Lin, personal communication). Quantitative nutrient budgets and performance data from sub-commercial-scale integrated systems of fish and seaweed in warm- and cold-water regions, respectively, have been published from Israel (Krom et al., 1995; Neori et al., 1996) and Chile (Buschmann et al., 1996). In both climates, the fish assimilated only a quarter of the nitrogen in the feed, and the associated seaweed could remove most of the remaining unassimilated nitrogen. The excess nitrogen from the culture of 1 kg of fish could nourish the culture of over 5 kg of seaweed. Excess phosphorus was removed in much smaller proportions than nitrogen. 372 A. Neori et al. / Aquaculture 231 (2004) 361–391

The quantitative production estimates that exist from both warm- and cold-water regions agree with each other. Recalculated from the data in Shpigel and Neori (1996) and conservatively revised, a 1-ha seabream–Ulva farm is expected to produce 55 tons of fish and 385 tons fresh weight of seaweed annually. Calculations for a commercial-scale integrated tank system of salmonids and red seaweed (Buschmann et al., 1996) show that a 1-ha farm is expected to produce 92 tons of fish and 500 tons fresh weight of seaweed annually. The functioning and management of a co-culture of several organisms, each with its own requirements and influence on water, can get rather complicated. Harvesting strategy and marketing policy can add to the confusion. Mathematical and design models have therefore been instrumental and should be even more so in the future, in the development of modern integrated aquaculture (Huguenin, 1976; Fralick, 1979; Indergaard and Jensen, 1983; McDonald, 1987; Petrell et al., 1993; Dalsgaard et al., 1995; Ellner et al., 1996; Chung et al., 2002).

5. Principles of seaweed biofilter design and operation

Ammonia is toxic to most commercial fish at concentrations above 100 AM (1.5 mg À1 NH3–N l ) (Wajsbrot et al., 1991; Hagopian and Riley, 1998). To avoid toxicity, the capacity of any useful fishpond biofilter to remove TAN (total ammonia N, NH3+NH4) should therefore match the rate of TAN production. In seaweed-based integrated mariculture systems, TAN and the other excess nutrients from the fed finfish/shrimp culture are taken up by seaweed. Most systems studied used Ulva spp. and Gracilaria spp., whose industrial culture technologies are known and whose nutrient uptake capacities are among the highest known (e.g., Martinez-Aragon et al., 2002). The use, as biofilters, of species from the economically important seaweed genus Porphyra (nori in Japanese) is currently under study in the USA and Canada (Yarish et al., 1999, 2001). The choice of seaweed species for inclusion in an integrated aquaculture system must first depend upon meeting a number of basic criteria: high growth rate and tissue nitrogen concentration; ease of cultivation and control of life cycle; resistance to epiphytes and disease-causing organisms; and a match between the ecophysiological characteristics and the growth environment. In addition, given the ecological damage that may result from the introduction of nonnative organisms, the seaweed should be a local species. Beyond these basic criteria, the choice of seaweed will be influenced by the intended application. If, the focus is placed on the value of the biomass produced, then subsequent decisions will be based on the quality of the tissue and added value secondary compounds (e.g., r-phycoerythrin). If the principal focus is the process of bioremediation, then nutrient uptake and storage and growth are the primary determi- nants. The optimal system would include a seaweed species that incorporates both value and bioremediation. Growth rate is defined, to a large extent, by morphology (Littler and Littler, 1980); generally speaking, the higher the ratio of surface area to volume (SA/Vol), the faster the specific growth rate. Phytoplankton have higher SA/Vol than seaweeds, with correspond- A. Neori et al. / Aquaculture 231 (2004) 361–391 373 ingly higher growth rates (Table 1). Similarly, the thin sheet morphology has a higher growth rate than does the fleshy one. It is more difficult to generalize on nutrient sequestration. A biofilter seaweed species must grow very well in high nutrient concentrations, especially ammonium. Seaweed that does not show this capacity, such as Chondrus (that prefers nitrate over ammonium) has only a limited use. To take up nitrogen at a high rate, fast-growing seaweed should be able to build up a large biomass N content. The common biofilter seaweeds, when grown in eutrophic waters, accumulate a high total internal N content. When expressed on a percent dry weight basis, maximal values for Ulva, Gracilaria and Porphyra grown in the eutrophic conditions characteristic of fish farm effluent range between 5–7% as N in dw or 30–45% as protein in dw (Neori et al., 2000; Carmona et al., 2001; Schuenhoff et al., 2003). In addition to the requisites described above, the ideal choice for the seaweed biofilter also has a market value (Sahoo et al., 2002). This encompasses the sale of seaweed products for a range of markets, including human consumption as food or therapeutants (Critchley and Ohno, 1998), specialty biochemicals, or simply as feed for the algivore component of the integrated system (Neori et al., 1998, 2000). To date, only a handful of seaweeds have been thoroughly investigated for their aquaculture and/or bioremediation potential. Perhaps the most complete body of research has encompassed the genus Ulva. These flat sheet morphotypes have corre- spondingly high growth rates as well as high nitrogen contents, making them very good candidates for remediation (Cohen and Neori, 1991; Neori et al., 1991). Their life cycle and its controls are generally well known, and Ulva has been successfully integrated into mid- to large-scale animal mariculture systems (Hirata and Kohirata, 1993; Jimenez del Rı´o et al., 1996; Neori et al., 2001b; Schuenhoff et al., 2003). Possibly the only drawback is the limited after-market for harvested biomass. Porphyra not only has many of the same characteristics (e.g., maximal growth rates >25% dayÀ1) but also produces biomass with high market value, including the tissue itself (for use as nori) and specialty biochemicals. On the other hand, the life cycle of Porphyra, is not understood well enough, yet, to maintain year-round growth of a purely vegetative culture. Gracilaria

Table 1 Examples of the influence of morphology on growth rate of potential biofilter seaweeds Morphology Dimensions SA/Vol Example Representative specific growth rate (% dayÀ1) Small sphere 10 Am diameter 150,000 Tetraselmis 51a (phytoplankton) suecia Thin sheet 2Â5cmÂ80 Am thick 25,000 Porphyra 25b amplissima, Ulva spp. Fleshy 2Â5cmÂ500 Am thick 4100 Gracilaria 10c parvispora a Gonzalez Chabarri et al. (1992). b Kraemer et al. (unpublished). c Nelson et al. (2001). 374 A. Neori et al. / Aquaculture 231 (2004) 361–391 and C. crispus (Irish moss) have a history of mariculture study. Nutrient removal during growth and extraction of agar or carrageenans from the harvest are important, though maximal growth rates of these fleshy morphotypes are typically less (ca. 10% dayÀ1) than the flat sheets (Marinho-Soriano et al., 2002; Nagler et al., 2003).Kelps (Laminaria and Macrocystis) are candidates presently being investigated in Canada (Chopin and Bastarache, 2002) and Chile (Gutierrez et al., in press). Resistance to epiphytes (as well as to small herbivorous animals) is a biological requisite of a biofilter seaweed species. Epiphytes are pest seaweeds and microalgae that use the cultured seaweed or the walls of the pond as substrates and compete for nutrients and light. Once the epiphyte population becomes significant, the seaweed culture is no longer a monoculture. Epiphyte growth on the cultured seaweed itself and on the pond’s walls can be prevented, their growth rate can be slowed down or they can sometimes be selectively killed off. Fast growing opportunistic seaweeds, such as Ulva, suffer from epiphytes only when they get stressed and do not grow at their usual fast rate. The fact that it is often the main epiphyte in monocultures of other seaweed makes Ulva the preferred biofilter seaweed genus (‘if you can’t beat them—use them’). However, once a different kind of seaweed (perhaps more marketable like the rhodophytes Gracilaria, Phorphyra or Kappaphycus) is selected as the biofilter, proper management of the cultures can lessen the epiphyte problem. Prior studies are already providing promising directions for preventing, and effectively combating, epiphytes. Filtered and even UV-treated inflow water can greatly reduce the potential for epiphyte contamination of a system. Grazing invertebrates have been tested with limited success, but are probably not a solution for commercial-scale operations (Craigie and Shacklock, 1995). The control over environmental conditions allowed by tank mariculture systems may be used strategically to influence competition between maricultured seaweeds and epiphytes. The main management tools are proper harvesting frequency and water flow (Buschmann et al., 1994), changes in water level (Neori, Shpigel, Scharfstein and Ben Ezra, unpublished), pulse feeding and a high stocking density (Friedlander et al., 1987, 1991). Less opportunistic seaweed, such as Gracilaria, can be effectively maintained ‘‘clean’’ by a judicious use of pulse nutrient supply and control of light levels through stocking density. Pulse nutrition promotes the growth of fleshier Gracilaria, which can store nutrients over a longer period than can the thin bladed epiphytes, Ulva and Enteromorpha. Likewise, overstocking slower growing low-light seaweed allows it to compete for the light and nutrients with the fast-growing high-light epiphyte (Craigie and Shacklock, 1995). Over stocking and frequent slight changes in water level are particularly effective in combating epiphyte growth on the pond’s walls. Since epiphytes are generally small, they are rapidly affected by environmental stresses, a strategy that Asian mariculture operations take advantage of by periodically raising Porphyra nets out of the water and allowing the biomass to partially dry. This kills much of the epiphyte biomass without significantly harming the macro- phytes. Fleshy seaweeds are more tolerant of chemicals such as chlorine than thin seaweeds, a fact that can ultimately be of use in the eradication of a severe thin-epiphyte problem. An acute epiphyte infestation may eventually require replacement of the entire stock, cleaning of the pond and restocking with clean seaweed stock from ‘clean’ restocking ponds. These ideas offer starting points but, clearly, additional research is needed to define the best solutions (Troell et al., 2003). A. Neori et al. / Aquaculture 231 (2004) 361–391 375

Water is the medium that transports the pollutants from the fish culture to the biofilter. In typical modern land-based integrated systems, water from fishponds recirculates through seaweed biofilter ponds, where waste organic matter is broken down and dissolved nutrients are taken up. Recirculation between the fish and the seaweed improves the performance of the integrated system, since it reduces pumping in of clean water and discharging of effluents, while at the same time maintaining in the fishpond safe ammonia and dissolved oxygen levels. Treatment of the fish culture effluents on their way to be discharged without water recirculation wastes many advantages of seaweed biofilters and cuts significantly the intensification of the fish culture unit. The rate of areal TAN uptake (grams N taken up per square meter per day) is an economically critical feature in seaweed biofilters. For a given fish culture capacity, a higher areal ammonia uptake rate is inversely proportional to the size and the cost of the biofilter systems. Another critical feature of a seaweed biofilter is the N uptake efficiency, the fraction of TAN concentration in the raw effluents removed as they pass through the biofilter. Higher ammonia uptake efficiencies reduce the rate at which the fish/shrimp pond water has to be recirculated. The dependence of TAN uptake rate and of uptake efficiency on TAN load are inversely proportional to each other. A seaweed biofilter has to be N starved to remove TAN with a high efficiency. Unfortunately, N-starved seaweed biofilters perform poorly with respect to the other three important biofiltration parameters—areal TAN uptake rate, yield and protein content. Hence, it is not possible to achieve in one-stage seaweed biofilters that are high in both TAN uptake rates and TAN uptake efficiencies (Cohen and Neori, 1991; Chopin et al., 2001; Troell et al., 2003). A novel three-stage seaweed design has solved this conflict (Schuenhoff et al., 2003; Neori et al., 2003). Ulva cultured in this biofilter design has taken up TAN at high uptake rates (3–5 g N mÀ2 dayÀ1) and at the same time also with high TAN uptake efficiencies (approaching 90%). With this performance and with 1000 metric tons fish releasing about 500 kg TAN dayÀ1, a seabream farm requires between 10 and 16 ha of Ulva sp. biofilters for each 1000 tons of fish standing stock. Ammonia (and ammonium), a chemically reduced compound, is assimilated as much as two to three times faster than the oxidized nitrate by many types of seaweed (Lobban et al., 1985; Neori, 1996; Ahn et al., 1998). The microbial oxidation of ammonia (nitrification) therefore diminishes the performance of the integrated system (Krom et al., 1995; Schuenhoff et al., 2003) and should be avoided. Maintaining the cleanliness of all wet surfaces, including those of pipes, helps prevent the development of nitrifying bacteria (Dvir et al., 1999). Piping between the fishponds and the biofilters should have the smallest possible SA/Vol ratio (i.e., wide and short), and anaerobic conditions inside them should be prevented. The performance of a seaweed biofilter of good design, construction and operation, depends on the areal TAN loading rate (concentration times the water exchange rate) by a saturation curve that approaches an asymptote at about 8 g TAN mÀ2 dayÀ1. The maximal biofiltration of any nutrient occurs, of course, in daytime, yet some TAN is also taken up at night, particularly when the TAN load to the algae is low (Cohen and Neori, 1991; Schuenhoff et al., 2003). Water recirculation between the fishponds and the seaweed ponds, or passing the effluent through a series of seaweed biofilters, can raise TAN uptake efficiency by the 376 A. Neori et al. / Aquaculture 231 (2004) 361–391 seaweed biofilters while maintaining high areal uptake rates, seaweed yield and protein content (Schuenhoff et al., 2003; Neori et al., 2003). Areal yield (kg mÀ2 dayÀ1) is the product of seaweed areal density (kg mÀ2) and growth rate (kg produced kgÀ1 dayÀ1). Optimal seaweed density maximizes yield by absorbing 99% of the incoming sunlight. For maximal yield, seaweed density is maintained at its optimum by the harvest of the biomass once it doubles, as frequently as every 2–3 days in summer. Land-based culture of seaweed in tanks, ponds and ditches has been developed in most places following the bottom-aerated pond approach developed by the group led by Ryther in the 1970s and concisely described by Huguenin (1976), Bidwell et al. (1985), DeBusk et al. (1986), Bird (1989) and Craigie and Shacklock (1995) . The basic principle of this successful technology has been the vertical movement, by bottom aeration, of seaweed suspensions in tanks and ponds, and the passage of nutrient-laden water through them. The vertical movement of an optimally stocked seaweed pond allows each algal frond to be exposed to an optimal light dose. The water turbulence generated by the aeration thins the hydro-boundary layer around the frond surface, speeding the inflow to the fronds of nutrients and outflow from the frond of excess oxygen, a feature that has been shown to minimize photorespiratory losses of production in a culture of the red alga Porphyra yezoensis (Gao et al., 1992).An alternative approach in seaweed pond and ditch culture, using stakes and ropes, has emerged from the technologies used for large-scale coastal seaweed farming of Southeast Asia, such as in Malaysia (Phang et al., 1996). This approach, however, has not provided the nutrient removal rates and the areal yields necessary for intensive mariculture, for reasons probably related to insufficient water turbulence, high turbidity and low nutrient concentrations. The by-production of high-quality seaweed in the biofilters calls for the co-culture of marine macroalgivores. Already in the 1970s, Tenore (1976) published his pioneer study on the integrated culture of seaweed and abalone. This was followed by the integrated abalone–Ulva and Gracilaria system of Neori et al. (1998) in Israel, of abalone and green algae in Japan (Sakai and Hirata, 2000), and of Palmaria–abalone in the USA (Evans and Langdon, 2000). The quantitative aspects of the three-stage integrated cultivation of fish, seaweed and abalone were assessed by Shpigel et al. (1996) and Shpigel and Neori (1996). A fish– seaweed–abalone farm has since been built and operated based on this assessment (see below). Data from a commercial pilot study and from the commercial farm conservatively suggest that for a 1-ha farm, the annual production of 50 tons of seabream, 33 tons of abalone and 333 tons fresh weight of seaweed, all of which is eaten by the abalone. Buschmann et al. (1996) and Chopin et al. (2001) described detailed economic income calculations for a fish–seaweed farm. They showed seaweed sales would profitably cover the extra cost associated with the biofilters. Internalizing the environmental benefits of nutrient removal by the seaweed (the cost a responsible society is ready to pay for the treatment of that amount of nutrients by standard technologies) can be calculated as an additional significant monetary advantage, inherent to the seaweed ‘‘self-cleaning’’ technology in comparison with fed monocultures (Chopin et al., 2001), as detailed below. A. Neori et al. / Aquaculture 231 (2004) 361–391 377

6. SeaOr Marine Enterprises—a modern seaweed-based integrated farm

SeaOr Marine Enterprises, on the Israeli Mediterranean coast, 35 km north of Tel Aviv, is a modern intensive integrated mariculture farm. It is the culmination of much of the knowledge reviewed in the present article. The farm cultures marine fish (gilthead seabream), seaweed (Ulva and Gracilaria) and Japanese abalone (Fig. 1).

Fig. 1. The SeaOr Marine Enterprises integrated mariculture farm in Mikhmoret, on the Mediterranean coast of Israel. From back to front (numbers in line diagram): (1) water reservoir, (2) abalone culture facility, (3) fishponds, (4) seaweed ponds and (5) effluent sump and seaweed harvesting facility. 378 A. Neori et al. / Aquaculture 231 (2004) 361–391

This farm best utilizes the local advantages in climate and recycles the fish-excreted nutrients into seaweed biomass, which is fed on site to the abalone. The process of nutrient recapture in the mariculture system is at the same time also an effective water purification process that allows the water to be recycled to the fishponds or to meet point-source effluent environmental regulations. The farm has received permits and support from the agencies concerned with environmental protection in Israel.

7. Economics

In the cost sheet of a modern intensive fish culture farm, the cost of fish feed proteins constitutes the largest item. However, three quarters of the proteins fed to the fish are excreted and eventually end up as dissolved ammonia. Algae recapture from the water and recycle ammonia, carbon dioxide, orthophosphate and micronutrients back into useful, protein-rich (>35% of dw) biomass (Neori et al., 1991, 1996). As predicted by Ryther et al. in the 1970s (Huguenin, 1976), seaweed farms on land can be profitable, as proven by the farm of Acadian Seaplants Limited in Nova Scotia, Canada (http://www.acadianseaplants. com/edibleseavegetables.html) which has been operating for years. It is only logical to conclude that synergism can make an integrated farm, composed of two independently profitable farms (fish or shrimp and seaweed) even more profitable particularly with the savings on seaweed fertilization and on wastewater treatment. An efficient algal-based integrated mariculture farm maintains optimal standing stocks of all the cultured organisms, considering the respective requirements of each for water and nutrients and the respective rates of excretion and uptake of the important solutes by each of them. This allows the profitable use of each of the culture modules with minimum waste.

Table 2 Integrated mariculture—seabream–Ulva: expected performance from the use of 500 metric tons feed yearÀ1a Organism Pond dimensions Yield Revenues (ha) (metric tons yearÀ1) (Â1000 Euro yearÀ1) Seabream 1 265 1050 Ulva 3.5 2215 885–1770 Total 4.5 2500 1935–2820 a The numbers in Tables 2–6 are rounded and are based on pre-commercial pilots (each about 200 m2) operated in Southern Israel. The following values have been used (results from commercial farms are not very different, but are protected from publication by proprietary rights): Seabream: Food Conversion Ratio (FCR)=1.9; feed protein content=49%; average fish stocking density=200 metric tons haÀ1; average annual fish yield=300 metric tons haÀ1; seabream farm gate price=4 Euro kgÀ1; Seaweed: ammonia uptake rate=4 g mÀ2 dayÀ1; ammonia uptake efficiency=85%; average annual Ulva yield=600 metric tons haÀ1;DWinUlva=15%; protein content in Ulva=40% in dw; seaweed farm gate price=0.4–0.8 Euro (fresh weight kg)À1; Abalone: FCR=12 metric tons Ulva 1 metric ton of production; average stocking density=25 kg mÀ2; average annual yield=10 kg mÀ2; farm gate price=35 Euro kgÀ1; added cost of production of a kilogram abalone to a seabream and Ulva farm=16 Euro kgÀ1; Sea urchin: FCR=8 metric tons Ulva 1 metric ton of production; average stocking density=20 kg mÀ2; average annual yield=10 kg mÀ2; farm gate price=20 Euro kgÀ1; added cost of production of a kilogram sea urchins to a seabream and Ulva farm=about the same as for abalone, but data are less solid. A. Neori et al. / Aquaculture 231 (2004) 361–391 379

Table 3 Integrated mariculture—seabream–Ulva–abalone/sea urchin: expected performance from the use of 500 metric tons feed yearÀ1a Organism Pond dimensions Yield Revenues (ha) (metric tons yearÀ1) (Â1000 Euro yearÀ1) Seabream 1 265 1050 Ulvab 3.5 2215 0 Abalonec 1.85 185 6500 Sea urchinsc 2.75 275 5500 Sums 6.35–7.25 450–550 6550–7550 a See footnote a in Table 2. b Used for algivore culture and neglecting nitrogen recycling. c Both herbivores can be cultured interchangeably.

Of course, sunlight is a necessary prerequisite in algal systems. The following additional factors all need to be considered in the assessment of the economic viability of a seaweed-based integrated mariculture system: cost of land, energy and labor; access to clean seawater, supplies, marketing, shipping and other services; availability of educated and/or technically oriented people; access to large markets; political, business and financial infrastructures that can support or at least understand a hi-tech agricultural project. It is therefore difficult to compare the situation in different countries. The data from Israel, presented below, may only assist readers to estimate the financial plan of hypothetical farms in other countries. Labor cost can be critical. A seabream–Ulva farm of the scale described next needs 10–12 employees (including management and marketing). In Israel, with an average salary of about 27,000 Euro a year, labor costs cut profits by approximately 40%. The pilot farms operated at the Israeli National Center for Mariculture (Neori et al., 1996; Neori and Shpigel, 1999) have generated preliminary real estimates, somewhat less conservative than our earlier estimates, of the financial costs and revenues expected from this technological approach (Tables 2–6). A seabream (Sparus aurata)–seaweed (Ulva lactuca) farm that annually uses 500 metric tons of seabream feed is expected to market 265 metric tons of fish and over 2000 metric tons of algae (Table 2). It will occupy about 4.5 ha of ponds and will generate farm gate revenue of 2–3 million Euro annually for the sale of the fish and the seaweed, according to present price ranges. A more advanced farm, based on the model implemented in Israel by SeaOr Marine Enterprises, can expect to

Table 4 Cost information for an integrated mariculture farm that uses 500 metric tons feed yearÀ1 (7–8-ha pond area) at current Israeli prices in 1000 Euro yearÀ1a Integrated system Initial investment Salaries Operationb Total annual cost (Â1000 Euros) for the farm Seabream–Ulva 1300 230 1650 1870 Seabream–Ulva–abalone ** ** ** 4810 **Proprietary data. a See footnote a in Table 2. b The initial investment is broken up and included in the operating costs over the years. 380 A. Neori et al. / Aquaculture 231 (2004) 361–391

Table 5 Investment breakdown for a seabream–Ulva–abalone farma Component % Fish culture facilities 34 Seaweed culture facilities 24 Abalone culture facilities 25 Other costs 17 a See footnote a in Table 2. convert the biofilter seaweed to 185 metric tons of the Japanese abalone (Haliotis discus hannai) or 275 metric tons of the purple sea urchin Paracentrotus lividus (Table 3). This sophisticated farm will occupy up to 7.25 ha of ponds and will generate 6.5–7.5 million Euro annually, but its expenditures will also be high. The expected investment for the two- species farm is 1.3 million Euro in Israel (Table 4); detailed figure estimates for a three- species farm of this size have not been disclosed by the company. However, an estimate for a small seabream and abalone farm, with an annual production of 20 and 11 metric tons, respectively, is an initial investment of 730,000 Euro and annual operating costs of 525,000 Euro, including the payback of the initial investment (Neori et al., 2001a,b). Based on these numbers, the estimated breakdown of investment between the species (Table 5) and our results from smaller pilots (Shpigel, Scharfstein and Neori, unpublished), the overall annual operating costs for the farm described in Table 3 will be slightly less than 5 million Euro (Table 4). When comparing these figures with those of a flowthrough pond farm with untreated effluents, or with the figures of a net pen farm, one has to consider that in the not too distant future the cost of the water treatment, on the basis of the ‘‘polluter pays’’ principle, will be added to the costs of those monoculture farms. The internalization of the waste treatment value of 12 Euro per kilogram of nitrogen waste and 2 Euro per kilogram of phosphorus waste (based on wastewater treatment cost in Sweden) (Chopin et al., 2001) can reduce the annual revenues (1,050,000 Euro, Tables 2 and 3) of net pen seabream farms (but not integrated farms) of the same fish production (265 metric tons) as described here by 225,000 Euro, or nearly a quarter. As has already been calculated for a land-based salmon and Gracilaria farm in Chile, this internalization will probably erase much of the profit of a conventional fish (or shrimp) monoculture farm in today’s highly competitive seafood markets. The overall estimated profits of the two integrated seabream farms in this admittedly simplistic calculation (Table 6) suggest a good potential for profitability. The economic data provided here should serve to illustrate that intensive seaweed-based

Table 6 Approximate profits assessed for two types of seaweed-based integrated mariculture farms that would each use 500 metric tons feed yearÀ1, in Israel, in thousands of Euros yearÀ1a Integrated system Revenues Total annual cost for Profits (Tables 2 and 3) the farm (Table 4) Seabream–Ulva 1935–2820 1880 55–940 Seabream–Ulva–abalone/sea urchins 6550–7550 4810 1740–2740 a See footnote a in Table 2. A. Neori et al. / Aquaculture 231 (2004) 361–391 381 integrated mariculture has good potential for being highly profitable, even before and, certainly, after the ‘‘polluter pays’’ principle is implemented in mariculture.

8. Conclusions

A large body of good-quality research has been made worldwide, on different integrated aquaculture systems that use plants to take up waste nutrient and at the same time add to the income of the farms. Today’s integrated sustainable mariculture technologies have developed from the traditional ‘‘all in one pond’’ polyculture and allow much higher intensification. R&D over three decades has brought the integrated land-based technology to a commercial reality. Through plant biofilters, integrated aquaculture recycles nutrients into profitable products, while restoring water quality. Fish–phytoplankton–shellfish systems convert the fish waste into bivalves, which have a large global market. Fish–seaweed–macroalgivore (such as abalone and sea urchin) systems have a choice of marketing either the seaweed or the macroalgivore, while they use less land than the fish–phytoplankton–shellfish systems and maintain a more stable water quality. Integrated aquaculture, in both freshwater and seawater, can be profitable, thanks to the sales of the biofilter organisms—vegetables, shellfish and seaweed. The results are higher yields and income per ton of feed and per ton of water. Furthermore, the integrated culture system fulfills, at no extra effort, practically all the requirements of organic aquaculture (NaturlandR, 2002), a feature that opens up to the aquaculturist new lucrative markets. The technologies are generic and modular, adaptable for fish/shrimp culture at any level of intensification. Several commercial freshwater farms already cultivate fish with vegetables. Two or three integrated marine farms culture fish, shrimp, seaweed, oysters, clams, abalone and sea urchins, and the interest in this approach is growing. The use of a similar approach in open-water fish culture farms has not yet reached commercial reality in the western world, even though several studies have proven its practicality and even tough it is done traditionally in coastal mariculture particularly in Southeast Asia. What slows the commercial implementation of integrated technologies is not related, in our opinion, to careful commercial considerations or to the technological/scientific unknowns delineated in Troell et al. (2003). Rather, it is related to a resistance to change and to the slow implementation of the ‘‘polluter pays’ principle. Of course, further R&D will better define the processes and interactions that operate between the cultured organisms, improve the performance of each module and of the integrated farm, improve management protocols and adapt the concept to different locations and to different organisms. Three large programmes are attempting to address this today. (A) Supported by AquaNet, the Network of Centres of Excellence for Aquaculture, an interdisciplinary project, involving the University of New Brunswick, the Canada Department of Fisheries and Oceans, the Canadian Food Inspection Agency and several industrial partners, is developing an open-water integrated mariculture system in the Bay of Fundy, Canada. Salmon (Salmo salar), mussel (Mytilus edulis) and kelp (Laminaria saccharina) are being grown together at several industrial pilot-scale sites to develop an integrated aquaculture model and to train students and professionals in this innovative 382 A. Neori et al. / Aquaculture 231 (2004) 361–391 approach to aquaculture. The productivity and role of each component (fish, shellfish and seaweed) is being analyzed so that the appropriate proportions of each of them can be defined. The data are expected to help develop a sustainable system in which metabolic processes counterbalance each other within acceptable operational limits and according to food safety guidelines and regulations. The ultimate goal of this project is to transfer this model, of environmentally and economically balanced diversification and social respon- sibility, to other sites and make it a concept transferable to other aquaculture systems. (B) Funded by the European Commission’s ‘‘Quality of Life’’ programme and coordinated by the Wadden Sea Station Sylt (AWI), the SEAPURA (species diversification and improvement of aquatic production in seaweeds purifying effluents from integrated fish farms) project intends to develop and test cultivation of high-value seaweed species not used before in poly-aquaculture with fish farms in Spain and Portugal, with accompanying research conducted in Germany and Northern Ireland. The research tackles issues such as unwanted seaweed sporulation and seasonality. The cultivated seaweed biomass will be used for the human food market mainly in France, for extraction of pharmaceutical substances, or for fish feed additives, with possible antibiotic effects of the cultivated seaweed. (C) Funded by the European Commission’s ‘‘Innovation’’ programme and coordinated by Israel Oceanographic and Limnological Research, National Center for Mariculture, Eilat, the GENESIS programme is a collaboration between Israeli, French and Scottish scientists and companies. It develops the evaluation and transfer of the generic integrated environmentally friendly mariculture approach from Eilat, Israel, to the European mariculture industry. Three prototype integrated systems for warm (Israel), temperate (Southern France) and cold (Scotland) water conditions, with a variety of valuable marine products including fish, crustaceans, mollusks and aquatic plants, are evaluated for their performances with respect to water, nutrients and waste management. Intensification and the use of nutrients, water and energy are optimized. The project also develops suitable products and services for the commercialization of the technology and establishes the financial viability and consumer acceptance of its products. It is anticipated that the results of these projects, which utilize information reviewed in the present paper, will establish the generic characteristics of the integrated aquaculture concept. They should greatly enhance the understanding and acceptance of the approach, leading to the development of integrated mariculture farms throughout Europe and the Mediterranean countries, North and South America and the Indo-Pacific regions.

Acknowledgements

This work was supported by the Israeli Ministry for National Infrastructures, the Israeli Ministry of Industry and Commerce and several grants from the European Union (A.N. and M.S.), the Ministry of Science and Technology of Israel, Binational Israeli–American Fund for R&D in Aquaculture (BARD), and the Negev-Arava R&D Network (A.N.); the Natural Sciences and Engineering Research Council of Canada, AquaNet Network of Centres of Excellence for Aquaculture (T.C.; this paper is contribution no. 73 from the Centre for Coastal Studies and Aquaculture); the Fundacio´n Terram (contribution no. 3 from i-mar) and A. Neori et al. / Aquaculture 231 (2004) 361–391 383 the British Embassy, Chile (A.H.B); the Swedish International Development Cooperation Agency—SIDA (M.T. and C.H.); the State of Connecticut Critical Technology Grant Program, the Connecticut, New Hampshire and New York Sea Grant College Programs, and the National Marine Aquaculture Initiative of the Office of Oceanic and Atmospheric Research, NOAA-DOC, USA (C.Y., G.P.K. and T.C.). We are grateful to B. Scharfstein for the photograph and the information on the Sea or Marine Enterprises form, to Kathy Chopin for her help with editing, and for the very constructive comments by several reviewers.

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Commentary Applicability of integrated coastal aquaculture systems

Max Troell! *, Nils Kautsky!, Carl Folke"

!Department of Systems Ecology, Stockholm University, S-106 91 Stockholm, Sweden "Beijer International Institute of Ecological Economics, Royal Swedish Academy of Sciences, Box 50005, S-104 05 Stockholm, Sweden

1. Introduction

Two recent papers published in Ocean and Coastal Management deal with sustainable coastal aquaculture production. The most recent by Brzeski and Newkirk [1], ‘‘Integrated coastal food production systems — a review of current literature’’, is a comprehensive overview of traditional as well as present integrated aquaculture systems. The second is by Newkirk [2] ‘‘Sustainable coastal production systems: a model for integrating aquaculture and fisheries under community management’’, a paper which takes the integrated concept a bit further and discusses it from a community level perspectives. In both papers references are given to a model of integrated coastal aquaculture, previously being presented in Folke and Kautsky [3] and Kautsky et al. [4]. This model describes a coastal polyculture system, with inter- acting biological components; fish, mussels and seaweeds, and their connection to terrestrial runoff. It is a simple and conceptual model with the main purpose to view aquaculture from an ecological perspective, and where wastes from one of the components is used as a resource input by others leading to reduced environmental impacts and increased outputs of seafood and seaweeds. From Brzeski and Newkirks presentation it is easy to get the impression that the model actually has been tested by field experiments (p. 59). Only one reference indicating its practical feasibility is given [5] and the discussion about constraints is

* Corresponding author. Tel.:#46 816 1358; fax:#46 816 1358; e-mail: [email protected].

0964-5691/99/$ — see front matter ( 1999 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 4 - 5 6 9 1 ( 9 8 ) 0 0 0 8 2 - 9 64 M. Troell et al. / Ocean & Coastal Management 42 (1999) 63—69 largely lacking. We fully agree with the authors that benefits from coastal integrated aquaculture could be substantial and that further research within this field is needed. We have in previously published papers urged that continuous development of aquaculture needs to be based on ecological engineering and ecological economic principles [4, 6]. We have since first presenting the model gained further knowledge about uncertain- ties and bottlenecks that may restrict future development of this type of integrated aquaculture. To the important discussion initiated by Brzeski and Newkirk we would like to add results from more recent experimental work conducted by others and ourselves. Thus, to be able to go forward and start the development of more ecologically sound aquaculture in large scale we need to include in the discussion all relevant information available.

2. Increased interest for ecological engineering

The practice of ecological engineering as a tool for reducing effluents from marine and brackish water aquaculture has recently gained new interest, and many suggestions of integrated systems using different combinations of seaweeds, bivalves, fish and shrimps have been proposed. Some additional papers to the review in Brzeski and Newkirk [1] aiming at increasing our understanding about the integrated concept should be mentioned [7—16]. These studies have shown that waste water from land- based fish and shrimp cultivations is suitable as a nutrient source for seaweeds and bivalves, and that such integration is beneficial from a nutrient reduction perspective. However, in open culture systems e.g. fish cage cultures, the continuous exchange of water makes waste disposal difficult to control, and so far, few studies have investigated the possibilities for such an integration [17—21]. The constraints associated with the open nature of such system is just briefly mentioned in Brzeski and Newkirk [1] and needs to be further elaborated on.

3. Suspended bivalves and ﬁsh cage culture

Though easy to visualise and intuitively promising, the integration of suspended bivalve and seaweed culture with cage culture of fin fish may have difficulties to succeed in practice. Particulate waste materials, i.e. faeces and waste feed from fish cages, as well as possible increase in phytoplankton concentration, could constitute a suitable food source for filter feeders. This assumption is strengthened by the fact that bivalves in some cases have been found to grow much better adjacent to salmon fish cages [5, 22], indicating that they are making use of an enhanced particle concentration. However, there are also findings showing no, or only minor, increase in growth from such co-cultivation [23, 24]. Differences in success may be due to different environmental conditions and cultivation design. The availability of organic food particles has been mentioned as the single most important factor determining growth rate of mussels [25]. Perhaps the existence of both temporal and spatial M. Troell et al. / Ocean & Coastal Management 42 (1999) 63—69 65 variation in food availability in natural water bodies can explain the degree of success for a combined fish—bivalve cultivation. The flow-through and open characteristics of a fish cage results in high water-flow rates that generate waste in low concentrations. Such waste is difficult to control. By modelling output of waste from a salmon cage cultivation and particle filtration by mussels, Troell and Norberg [26] were able to identify some constraints in using filter feeders for removing particles from fish cage farms: 1. Suspended solids from the fish cages will be highly diluted by the large volume of water passing through the cages. During continuous feeding (demand feeding) the concentration of released suspended solids was low (0.06—0.3 mg l\). Only when fish density in the cages was high prior to harvest and water currents were slow (0.03—0.05 m s\), the increase in released concentrations were above 0.1mg l\. 2. Addition of feed in pulses increased water particle concentration by 3—30 times, but the short duration of a pulse and saturation of mussel feeding would make long-term seston concentration more important for mussel growth. 3. The potential particle retention from a rich pulse was limited by mussel pseudofaeces threshold level. The conclusions from their model were that in a co-cultivation of mussels and salmons, the ambient seston concentration is of major importance in controlling mussel growth, and that increases in suspended solids from fish cages may contribute significantly only during periods of low plankton production or low organic particle concentration. In the study by Wallace [22], where mussel growth was higher adjacent to fish cages, it was shown that the different mussel populations had roughly the same growth rate during the summer period. However, the mussels adjacent to the cages did not experience the long winter intermission in growth, caused by low phytoplankton levels, as they could utilise particles released from the fish cages. Stirling and Okumus [24] also found that mussels farmed outside salmon cages did not deplete their reserves during the winter period, which resulted in a slight (5—12%) but significant (P(0.05) increase in shell growth compared to controls. This increase was, however, only found in one of the two experiments. Their data on monthly growth also showed that mussel growth adjacent to the cages was only facilitated during September—March when ambient seston concentration was low. This is in accordance with findings from the model by Troell and Norberg [26]. Jones and Iwama [25] found that oysters (Crassostrea gigas) co-cultivated with salmon in cages had a three times greater increase in shell heights compared to controls. Their mean POM concentration during the four month cultivation period was 7.9 mg l\ , which is above pseudofaeces production threshold value of 4.6 mg l\ for C. gigas [28]. However, over time seston concentration varied consider- ably (range 1.3—15 mg l\). This resulted in a POM concentration being under the threshold for pseudofaeces production 62% of the study time for the controls compared to 25% inside the cages. This could explain the higher growth adjacent to the cages. Another potential problem of integration could be seen in the study by Taylor et al. [23], who found no increase in growth for mussels cultivated on ropes adjacent to 66 M. Troell et al. / Ocean & Coastal Management 42 (1999) 63—69 salmon cages. They concluded that most of the released particulate waste material was instead absorbed by a dense mussel population growing directly on the net cages.

4. Suspended seaweeds and ﬁsh cage culture

Besides output of particulate wastes, fish farming also releases dissolved nutrients (mainly P and N). There is a consensus that at least 80% of the total nutrient losses from fish farming are plant available as potentially eutrophicating substances [29—31]. Generally, only about 30% of the nutrients added through feed will be removed through fish harvest [32—34]. Solutions for treating effluents from intensive fish cage aquaculture have mainly been sought in technical fixes [35], but the conceptual model by Folke and Kautsky [3] offers a more ecological approach for waste reduction. Troell et al. [21] co-cultivated Gracilaria chilensis with salmon cages, to test the viability of making use of dissolved nutrients as a resource, while at the same time reducing the risk for coastal eutrophication. They found that Gracilaria cultivated at 10 m distance from the cages had up to 40% higher growth rate (specific growth rate; 7% day\) compared to growth at 150 m and 1 km distance. The algae nutrient content was also found to be significantly higher close to the cages compared to controls. However, agar yield per unit biomass varied between 17 and 23% of dry weight and was lowest close to the farm. But due to higher growth rate, the accumu- lated agar production was still highest close to the fish cages. The degree of epiphytes and bryozoa coverage was overall low. Since the results are based on small-scale experiments, conducted only during a limited part of the year, further research is needed to understand how a full-scale integrated open cultivation functions during different parts of the year. Fish cages situated in fresh waters have been shown to increase adjacent ambient dissolved nutrient concentrations [36—39], a result also found in marine environments [40, 41]. In fresh water this hyper-nutrification can in some cases lead to an overall change in the nutrient status of the whole water body [42, 31], which for marine environments may be an exception due to rapid water exchange. However, nutrient enrichment has also been documented from cage farms placed along Swedish and Finnish coasts of the Baltic ([31], and references cited therein), and from farms placed in fjord estuaries [43]. The fact that many studies have failed to document enhanced phytoplankton production in the vicinity of marine coastal cage farms [44, 32, 45], is not surprising considering the water exchange rate in relation to the doubling time of phytoplankton. It is, however, documented that macro-algae can have significantly higher growth rates close to coastal fish farms compared to further away [46—49]. Petrell et al. [20] found that advection and diffusion parameters, in a model simulating release of dissolved nutrients from a sea cage, were invalid due to unsteady and complicated flow pattern in the vicinity of the cages. Few empirical data exist but Black and Carswell [40] and Weston [41] suggest that dilution of ammonia is greatest within 10 m of sea cages, and that significantly higher than normal background concentrations are found from 10 to 40 m away from the cages. M. Troell et al. / Ocean & Coastal Management 42 (1999) 63—69 67

These results illustrate that there is lot to be learned about temporal and spatial variations in dissolved nutrient concentrations around sea cages.

5. Conclusions

Integrated cultivation may have an important role to play in aquaculture development. It has the potential to reduce the many negative environmental impacts of salmon cage farming and may prove to be also socially and economically viable. However, the system needs to be further tested. But lack of more complete information should not be seen as a permit to expand intensive farming systems e.g. salmon cage farms. On the contrary, the environmental costs generated by already existing ﬁsh farms should be borne by those who pollute [50, 6]. Actually, paying the costs for environmental impacts, such as those caused by nutrient releases, will create incentives for the development of environmentally benign marine aquaculture technology, of which integrated open sea aquaculture may be one alternative.

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