Journal of Cleaner Production 32 (2012) 183e192

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Journal of Cleaner Production

journal homepage: www.elsevier.com/locate/jclepro

Review

Sustainability assessment tools to support aquaculture development

Biniam Samuel-Fitwi a, b, *, Sven Wuertz a, b, Jan P. Schroeder b, Carsten Schulz a, b
a b

Institute of Animal Breeding and Animal Husbandry, Christian-Albrechts-Universitt zu Kiel, Olsenhausenstrasse 40, 24098 Kiel, Germany Gesellschaft fr Marine Aquakultur (GMA) mbH, Hafentrn 3, D-25761 Besum, Germany

a r t i c l e i n f o
Article history: Received 28 June 2011 Received in revised form 21 March 2012 Accepted 31 March 2012 Available online 13 April 2012 Keywords: Sustainability Aquaculture Assessment Environment Life cycle assessment Ecological footprint

a b s t r a c t
Aquaculture production has doubled every decade for the past fty years, representing the fastest growing food sector. This increase reects the expansion of production areas, increased know-how in husbandry and advances in production technologies, but most importantly it entails increased use of production-inputs that lead to exploitation of natural resources and hence raising concern on environmental distress. In addition, it suggests a similar range of production-outputs apart from the actual target products that are hardly quantied but often are recognized for causing impacts on the environment as well as potential risks for human health. Although several quantitative multi-impact assessment tools have been explored to evaluate environmental impacts of industrial activities, applications in aquaculture have only recently been carried out. However, impact assessment tools applied so far do not reect the full range of aquaculture activities, and hence incorporate limitations that impair their use in aquaculture environmental assessment. Therefore, the development of tailored environmental assessment tool incorporating impacts distinctive to aquaculture is necessary. By reviewing recent methodologies used in aquaculture, their limitations are identied and future research needs are highlighted. Although large strides have been made in reaching standardized methods for environmental assessment tools such as life cycle assessment (LCA), their use in policy formulation and decision making requires relentless effort to develop the tools using fundamental problems known to aquaculture. As a prerequisite, the most signicant impacts of aquaculture are identied but need to be characterized and integrated in aquacultural assessment tool. Furthermore, social aspects of sustainability should be considered; and linkage of operational efciency with environmental performance can support in optimizing the allocation of resources while minimizing impacts. 2012 Elsevier Ltd. All rights reserved.

1. Introduction World aquaculture production has increased from 1.7 million t in 1957, to 68 million t in 2008 (FAO, 2009, 2010). Consequently, doubling every decade in the past ve decades, aquaculture production has seen a 39 fold increment, and contributes largely to global sh production for human consumption (Tacon and Metian, 2009), surpassing for the rst time the supply from capture

Abbreviations: BOD, Biological Oxygen Demand; DEA, Data Enveloping Analysis; EF, Ecological Footprint; EU, European Union; FAO, Food and Agriculture Organization; LCA, Life Cycle Assessment; IFOAM, International Federation of Organic Agriculture; OECD, Organization for Economic Co-operation and Development; SLCA, Social Life Cycle Assessment; UNEP, United Nation Environmental Programme. * Corresponding author. Gesellschaft fr Marine Aquakultur (GMA) mbH, Hafentrn 3, D-25761 Besum, Germany. Tel.: 49 (0) 4834 96539914; fax: 49 (0) 4834 96539999. E-mail address: biniam@gma-buesum.de (B. Samuel-Fitwi). 0959-6526/$ e see front matter 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.jclepro.2012.03.037

sheries (FAO, 2010). This increase reects the expansion of culture areas, increased know-how in husbandry and advances in production technologies. Most importantly it entails increased use of production-inputs such as land, water, feeds, energy, therapeutants and chemicals that lead to exploitation of natural resources and hence raising concern on environmental distress. Furthermore, the increased production-inputs suggest a similar range of production-outputs, potentially coupled with environmental impacts, comprising mainly airborne and waterborne emissions from the farms. These emissions may result in local ecosystem imbalances, particularly when carrying capacity is exceeded in the recipient water body. Recently, however, important global scale impacts that may arise during aquaculture production, such as global warming, acidication, ozone layer depletion, have gained popularity in environmental studies (Pelletier et al., 2007). Several recent studies focused on the outputs from aquaculture and quantied their release (Wu et al., 1994; Wu, 1995; Enell, 1995; Muir, 2005; Colt et al., 2008; Roque dOrbcastel et al., 2009b). However, quantication of some of the releases is difcult due to

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unavailable data and insufcient ndings of their impacts on the environment (Wu, 1995). Classical environmental studies targeted local emissions categorized into few classes of pollutants, namely nutrients and organic matter, pathogens, introduction of genetically modied organisms and escapees. Recently, global emissions, predominantly comprising greenhouse gases (carbon dioxide, methane, nitrous oxides, and uorocarbon) originating from energy consumption and their contribution to global warming and ocean acidication have been addressed. Energy use in aquaculture is linked to intensication of culture and involves an increased energy use due to a large-scale automation and complexity of workows as well as indirect energy utilization for manufacturing of feed, chemicals or material inputs as well as transportation, and is highly variable between culture systems (Colt et al., 2008; Roque dOrbcastel et al., 2009a) and management practices. Therefore, assessing aquaculture environmental impact and examining the array of multi-impact assessment tools already used in published case studies will highlight the limitations and suggest needs/ options for improvement. The objective of this work is to evaluate a set of analytical multiimpact environmental assessment tools with regard to an application for aquaculture-related studies including the identication of potentials and limitations of these tools. This study focuses on analytical assessment tools including ecological footprint (EF) and life cycle assessment (LCA) in the aquaculture context. 2. Environmental impact assessment tools

in aquaculture as well as their interlinkages (Fig. 1) impede the development of quantication tools in evaluating the complex interactions. Often, aquaculture systems reveal complex process linkages involving multiple variables that are mostly not parameterized. High input of nutrients and organic material from articial feeding results in nutrient loaded efuents leading to a substantial increase in primary production, subsequent decomposition and biochemical oxygen demand (BOD), limiting the carrying capacity of the recipient aquatic system, although this is highly dependent on the receiving ecosystem. Furthermore, the amount of nutrients and organic load from aquaculture efuents largely depend on the quantity of feed used and utilized by the target organism. The release of escaped sh or other aquatic organisms from farm sites e in addition to the risk of disease transmission e lead to the introduction of non-endemic or even invasive species, potentially outcompeting native ora and fauna (Casal, 2006; Stepien and Tumeo, 2006). Such effects are barely quantiable but may highly modify the complex ecologic interplay. Furthermore, escapees may interbreed with native stocks, entailing hybridization and introgression of native genomes, thereby inuencing the reproductive performance of individuals as well as populations in terms of allelic frequency. These dependencies are rarely understood in unaffected situations, and case-specic impact of highly variable aquaculture activities will require the incorporation of specic measuring mechanism, which is not yet available. 2.1. Impact assessment tools

Several tools have been presented in the past to facilitate the inclusion of various environmental aspects in decision making. However, the diverse and multidisciplinary nature of the environmental aspects and highly variable production processes involved

Recently, environmental case studies of aquaculture activities focused on quantiable emissions, making modeling of respective impacts easier. The most widely-used impact assessment methods

Fig. 1. Major environmental interactions supporting increased aquaculture production.

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cover climate change arising from greenhouse gas emissions, acidication from acid gas emissions, eutrophication as a result of nutrifying emissions (such as nitrate, ammoniacal nitrogen and phosphates), the release of ozone-depleting substances, and abiotic and biotic resource depletion (Pelletier et al., 2007). These multiimpact categories encompass global impacts departing from the traditional single impact assessment tools. However, it is alarming to observe that the most popular assessment focused mainly on climate change especially carbon footprint. Carbon footprint has its benet in inuencing consumer choices and decision making, as it is easy to communicate and compare between products using a single carbon dioxide emission value. However, carbon footprint is one of several impact categories and do not reect overall impact of the production for several reasons; for example, carbon dioxide emissions are mainly related to fuel-based energy use and aquaculture production systems with no energy use are selected as environmentally preferred production systems; and non-energy emissions potentially impacting the environment are completely ignored. Therefore, to meet objective evaluation in aquaculture, overall analysis is utmost essential due to the variety of alternative production systems shifting the impact from one eld to another if undetectable in the analysis (problem shifting). As a consequence, multi-impact assessment tools used in aquaculture are focused on here. Among the multi-impact tools used, EF and LCA represent methodologically the most advanced tools and are increasingly used in aquaculture studies. Both aim at providing a complete picture of a products environmental impacts and attempt to avoid problem shifting. Problem shifting involves a shift in production in order to reduce identied environmental impacts by shifting their form or location of release. For example, by taking a holistic multiimpact approach these tools consider all emission forms globally, hence avoid geographic problem shifting. Analyzing several potential impacts such as energy expenditure and emissions, impact-specic problem shifting is avoided. 2.2. Expressing assessment results Obviously, the presentation of data needs to summarize the complexity of the analysis to allow for a comparative assessment between impacts and systems and provide an overall evaluation. Ideally, this summarized presentation needs to provide an easy-tounderstand message, used to compare and further balance production parameters, environmental impacts in order to harmonize consumers as well as producers interests. Currently, comprehensive single-score units such as the footprint of a standardized units impact on a given area provide consumers a consistent measurement, and allow for integration in the purchase decision that appeals to consumers responsibility but can easily be implemented in taxation policy or the legislative framework of production and sales. However, limitations exist in applying these tools, hindering their extensive purpose as a reliable communication tool for ecological labeling. For example, organic labeling can be misleading, as available standards for organic aquaculture fail to reduce the majority of environmental impacts (Pelletier and Tyedmers, 2007). What organic labeling has achieved in the last few years is environmental awareness among consumers. The sector has grown signicantly in the last decade as a result of consumer and market reaction to concerns about poor taste and texture, contamination, animal welfare, etc. (Mente et al., 2011). However, the major organic labels (such as Naturland, EU label, KRAV) offer comparison across the various mixes of impact assessment tools which is not consistent across the various labels currently available. The disadvantage of this approach is that the information obtained from the various tools can be confusing to

consumers and data requirements may be extensive and costly. However, particular claims of bio-integrated systems such as aquaponics or polyculture systems need to be analyzed carefully and holistically to improve the techniques currently developed. Recent advances by researchers and growers have turned these systems into a working model of sustainable aquaculture production. However, comprehensive evaluation on the sustainability has hardly been carried out and emerging technology is mainly focused on production parameters rather than impact data. Dening standards for organic labeling is particularly important as a 240-fold increase is predicted by 2030 (El-Hage Scialabba and Hattam, 2002). The International Federation of Organic Agriculture (IFOAM) has established standards for organic agriculture production and the need for coherent EU framework and standards for aquaculture products led to the inclusion of these products within the EU regulation for organic production, although more efforts are required in terms of legislative and institutional framework (Mente et al., 2011). Moreover, inclusion of multi-impact assessment tools for evaluation of environmental impact is necessary to have accurate environmental evaluation. 3. Ecological footprint (EF) analysis In the 1990s, the concept of the EF was introduced as a measure of human demand on Earths ecosystem by comparing the amount of human appropriation with the amount of global bio-capacity to regenerate each year (Monfreda et al., 2004; Wackernagel et al., 2004). In other words, EF analyses quantify human demand on nature by assessing the biologically productive land and water area required to produce the resources consumed and to absorb corresponding waste. The human consumption of natural resources is converted into a normalized measure of land area known as global hectares (gha). The EF is adopted in aquaculture revealing enormous differences in the impacts assessed in different production systems (Larsson et al., 1994; Berg et al., 1996; Kautsky et al., 1997; Folke et al., 1998; Roth et al., 2000; Bunting, 2001). It appears that increasing intensication demands larger amount of global hectares for bio-capacity to regenerate each year, making production scale one of the most important factors affecting the environment. 3.1. EF in aquaculture production Berg et al. (1996) estimate that 1 m2 of semi-intensively managed tilapia pond requires a pond area of 0.9 m2 for phosphorus assimilation and 0.5 m2 for oxygen production. When considering tilapia production in 1 m2 intensively managed cages it is estimated that an ecosystem area of up to 115 m2 and 160 m2 is required for phosphorus assimilation and oxygen production, respectively. Moreover, the ecosystem area required for feed production was estimated to be 21,000 m2 m2. The authors concluded that from the ecological point of view, the semiintensive tilapia pond production is more sustainable as compared to the intensive cage production of tilapia. Comprehensively, sustainability needs to consider actual productive output to be able to compare in a broader economic point of view. In other words, semi-intensive farming needs to take into consideration the produced amount of sh to assure comparability with the intensive system. From an ecological perspective, each ecosystem has a carrying capacity, which is constrained by maximum impact still leading to regeneration from the impacts, independent of production units. In this context, it needs to be emphasized that the EF is not constant for a given impact, but needs to reect also the capacity of an ecosystem to regenerate. Folke et al. (1998) concluded that larger ecosystem areas are required to sustain more intensive and concentrated activities such as intensive

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monocultures of salmon and shrimp farming than less intensive systems. Thus, carrying capacity (EF) is highly dependent on ecosystem characteristics and represents a rather dynamic property, which indicates shortcomings for the EF assessment. Bunting (2001) recalculated the EF of tilapia production in semiintensive and intensive farming systems normalizing ecosystem area to the appropriated annual sh production (m2 kg1) - in contrast to the original approach referring to ecosystem area to area aquaculture facility (m2 m2), using the information from Berg et al. (1996). Consequently, the area required for excess phosphorus assimilation of intensive farming systems was lower (0.78 m2) when compared with semi-intensive tilapia farms (1.78 m2) on the basis of 1 kg of tilapia produced. Furthermore, the land required to produce the same quantities of tilapia in intensive farming is 210 times lower than the semi-intensive farm, reecting the economic constrains of semi-intensive farming of tilapia in acquiring land. On the other hand, the supply of oxygen in intensive farms is found to be higher than that of semi-intensive farms, involving additional costs (shifting the 1:210 ratio) and resources (shifting the 0.78:1.78 ratio) slightly. 3.2. Limitations of EF in aquatic environments Most importantly, EF methodology refers to a product-specic land required to regenerate impacts from a specic activity. Hereby, ecosystem properties are generalized assuming a standardized global ecosystem in terms of averaged bioproductivity. Thereby, EF is expressed as hypothetical number of global hectares, required to sustain a designated human activity. Interactions specic for a distinct ecosystem are neglected so far. This is particularly critical in isolated, vulnerable ecosystems such as coral reefs. In particular, aquatic ecosystems are characterized by a multitude of opposing biotic and abiotic factors which subsequently determine the impact of a given anthropogenic stressor. For example, the spread of emissions is highly dependent on the movement of the water and the accumulation or metabolisation is highly variable for different ecosystems based on local biotic distribution and abundance. Applying a generalized procedure for environmental assessment dangerously simplies ecological interactions, leading to a product having an identical footprint regardless of its origin (Monfreda et al., 2004; Wackernagel et al., 2004). As such, values of EF do not depict the varied quality of the physical ecosystem in use, such as a desert or forest ecosystem. In order to address this limitation, Limnios et al. (2009) used direct land area usage rather than land area derived from the volumes of outputs. However, application of direct land use measurement in seafood production is not straightforward, as the features of land and water used in seafood production are dynamic and relatively unpredictable. Furthermore, in marine ecology, assimilative capacity can also be dened in relation to specic environmental target criteria reecting dynamic ecological pathways rather than area-related measures (Roth et al., 2000). Therefore, EF needs to be adapted to specic ecosystems in the future and appropriated carrying capacity of specic ecosystems have to be dened with regard to distinctive types of impact. Intensive production systems imply the use of resources for higher short-term production-outputs with consequently environmentally damaging productivity in long-term. For example, increases in shrimp production demanded the expansion of hatcheries in many parts of the world leading to local depletion of wild broodstocks, thereby reducing long-term productivity of local sheries and biotic depletion of stocks. The short-term increase in productivity of hatcheries indicating deceptive lower values of EF, due to avoided post larval collection from the wild. However, this illusion of lower values of EF causes depletion of broodstocks in

a long-term due to the exploited wild stocks. Limnios et al. (2009) recently have addressed the problem by accounting for both current and potential land disturbances. Categorizing current impacts is relatively well established, however assigning potential future ecological impact on biodiversity and area degradation is difcult and highly speculative. Minor deviations and inaccuracies on prediction intensely diverge from accurate results mainly because of the network of ecological relationships to be considered. Furthermore, beyond all doubt, aquatic ecosystems are by far less understood than terrestrial ones, turning ecosystem-specic approaches a major problem for EF assessments. 4. Life cycle assessment (LCA) In the past two decades, LCA has seen a tremendous amount of applications as an assessment tool in different elds for evaluating resource utilization and environmental impact assessment, thereby identifying hot spots in the production process. Therefore, based on the goal of the synopsis, extraction and processing of raw materials are carried out throughout the life cycle of the product, typically integrating manufacturing; transportation and distribution; use, reuse, and maintenance; and recycling and waste (Curran, 1993; Guine, 2002; ISO, 1997, 2006). As such, LCA in aquaculture is a departure from evaluating waste release management alternatives of environmental assessments of the 1980s that looked mainly at a single issue such as local emission from sh farms. Instead, it describes the incoming (food production, including the energy used, broodstock, water etc.) and out-coming ow (emissions, product) in order to give an overall statement based on the inclusion of all relevant activities along a life cycle. There are few published articles on LCA research in aquaculture production systems, including different salmonid feeds (Papatryphon et al., 2004), Thai shrimp products (Mungkung et al., 2006), French land based turbot production (Aubin et al., 2006), Norwegian net-cage farmed salmon (Ellingsen and Aanondsen, 2006), Finnish trout production (Grnroos et al., 2006), conventional and organic salmon feed production (Pelletier and Tyedmers, 2007, 2008), alternative salmon production technology (Ayer and Tyedmers, 2009), global salmon production impacts involving Norway, the UK, Canada and Chile (Pelletier et al., 2009) and mussel culture, consumption and reuse in Spain (Iribarren et al., 2010a). Very recently, several studies (e.g. Aubin et al., 2009; Roque dOrbcastel et al., 2009a; Pelletier et al., 2009; Pelletier and Tyedmers, 2010; Phong et al., 2011; Jerbi et al., 2012) have compared production systems, including a comparison between species, different geographical positions of production sites as well as polyculture vs. mono-species systems. Still, the majority of the studies are focused on salmonids, assessing a variety of impact categories, e.g. global warming, acidication and eutrophication potentials. Some of methodological issues related to aquacultural LCA is reviewed elsewhere (Henriksson et al., 2012) and are not detailed in this review. 4.1. LCA and its limitations Frequently, standardization is an issue since studied sites rarely vary in a single parameter. For example, there are no standardized production systems, thus evaluation at different geographical locations is consequently also a comparison of production technology inuenced by changes in regional husbandry conditions. Furthermore, such a comparison may involve background processes of economic nature on a broader scale that accordingly bias overall assessment results, if not evaluated carefully. For example, careful observation in many aquaculture LCAs indicate that cumulative emissions of energy utilization largely contribute

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to potential impacts within several impact categories. The cumulative emissions from energy dependent production are quite often dominated by direct emissions from the combustion process (Dones et al., 2007). Therefore, the delivery of the primary energy inputs causes important elementary ows to production as well as resource utilization, for example land occupation or fossil energy resources and cannot be disregarded. This implies that different energy sources (wind in one region vs. fuel in another) subsequently may result in drastically large differences in emission values even at comparable energy consumption of the selected farming sites. Environmental burdens related to natural gas production, for example, are highly dependent on the import structure, ultimately inuencing the gas transport distances (Heijungs et al., 2006). For example, Pelletier et al. (2009) analyzed the LCA of different salmonic production using regional energy supply for the different regions including Norway, UK, Canada, and Chile that the result of the assessment indicate bias. For example, Chiles main energy source is based on fuel, while in Norway natural gas is common. The impact from these different sources is drastically varying that the LCIA result, and thus LCA quantication of the aquaculture production, is mainly swayed by the different sources of energy and not on sh production itself. On a regional scale involving several countries, normalization of certain ow (e.g. input) should be considered in order to provide a comprehensive analysis. Hence, comparisons are limited by the diversity of culture species, the use of varied functional units, diverse farming systems and the inuence of farm- level management practices and consequent results of impact on environment. Despite these limitations, the LCA tool shows a potential for systemic assessment, integrating this variability. However, interpretations are usually not conclusive due to the diversity of aquaculture activities and species of culture. A main general limitation of LCA is the quantity of ows to be dened during LCI. Thus, data quality and collection, denition of the system, time boundaries, and process modeling need to be carried out carefully (de Benedetto and Klemes, 2009). Collection of data can be problematic due to the fact that quality data needed for LCA frequently involves several processes (e.g. farming, sheries, agriculture, feed manufacturing, etc) and that transparency of business data is delicate and analysis is complicated by the number of parties involved. When conducting LCA, it is important to weigh the availability of data, the time necessary to conduct the study, and the nancial resources required against the projected benets of the assessment. Ellingsen et al. (2009) described the current status of seafood environmental analyses and concluded that comparative analysis for only one or a few of the environmental impacts such as CO2 or energy consumption reduces costs but still may provide adequate environmental analysis. Consequently, the study assessed CO2 emission of farmed salmon in Norway from production to consumption and identied the farming phase as the main contributor to CO2 emission, mainly due to fuel consumption during feed production. However, limiting the choice of the impact categories to only few can underestimate the potentially severe environmental problems resulting in inaccurate assessment, ultimately diminishing the condence of using LCA as reliable assessment tool in comparing products. 4.1.1. Handling co-products Many aquaculture production systems produce more than one economic output, or co-products. Integrated farming systems or sh cultured under a polyculture system or horizontal culture system (Bunting and Shpigel, 2009) can be a good example, where the resources of the farm are used by other products produced alongside the main produce resulting in more than one products.

The environmental impact during the production process of such systems can generally be allocated between its co-products and is often based on mass or economic values of the co-products (Ayer et al., 2007) and may be highly inuenced by the temporal uctuation common to the food market. However, co-product allocation in inputs of raw materials, such as in feed input production, demands allocation in co-product outputs that are not represented with economic or mass values. For example, Pelletier et al. (2009) used the gross chemical energy content of co-products to allocate the resource use and emission of each co-product, consequently reecting the ow of material, energy utilization and associated emission, attributable to the functioning of the product system and is consistent with the ISO recommendation that the allocation criterion be based on the function of the co-products. However, according to ISO standard (ISO, 2006) the rst option with regards to dealing with co-products is system expansion to avoid coproduct allocation (ISO, 2006). The main concern is that coproduct allocation determines system boundaries normatively, instead of system boundary delimitation based on causality or consequences which is reective of the real-world behavior based on market signals. For example, Schmidt (2007, 2010) has successfully implemented the system expansion on all stages of agricultural production for studying LCA of vegetable oil. Detailed explanation of system expansion delimitation is given by Weidema (2003). System expansion, however, has rarely been applied in LCAs of aquaculture until recently (Iribarren et al., 2010a). However, Pelletier and Tyedmers (2011) argue that the current market signals are largely devoid of environmentally relevant contents for managing the environmental dimensions of our activities that LCA results utilizing the current economic system are inadequate. Consequently, the authors suggested basing allocation criteria on causality (e.g. physical) relational properties that link system inputs and co-product outputs in a logical manner. Thus, allocation procedures should approximate as much as possible the fundamental inputeoutput relationships and characteristics (ISO, 2006) dened in biophysical terms rather than economic terms. 4.1.2. Functional unit One of the important characteristics of agricultural LCA is the use of multiple functional units (de Boer, 2003). Such multiple functional units help in the interpretation and better understanding of the environmental burden, productivity and farm income, as different impact categories represent different effects on the environment. However, several case studies in aquaculture relate environmental impact to the mass of the product (e.g. per kg sh produced) and other representation of the function of the products such as economic value (per US$), area of production (per ha), etc. are hardly studied and therefore cannot be used interchangeably. This is mainly due to the fact that mass representation of the functional unit considers both production efciency and environmental impact. Nevertheless, we support the simultaneous use of an economic-based (US$), product related (kg) as well as protein- or energy-based (kJ) unit, to allow for fast conversion of gures and assure fast comparison between studies. Furthermore, comparison of different species of sh and livestock products without considering the qualitative dimension of the functional unit is misleading, as there is a danger that reality is not reected well (Reap et al., 2008). For example, the study by Aubin et al. (2009) assessed impacts of aquaculture involving different species and production systems in different countries using the functional unit of sh weight. However, it failed to consider the qualitative differences of the different sh species with different value functions, such as the function of providing protein and energy (Haard, 1992). Similarly, the study by Papatryphon et al. (2004), comparing environmental impact of feed based on

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different animals (pigs, poultry and sh) produced at different culture environments, cannot reect the accurate impact to support decision in selecting feed. 4.1.3. Choice of impact categories Appropriate impact categories are essential to arrive at comprehensive evaluations of the environmental impacts from aquaculture. Global warming, acidication, eutrophication, photochemical oxidant formation, aquatic/terrestrial ecotoxicity, human toxicity, energy use, abiotic resource use, biotic resource use and ozone depletion are impact categories that have frequently been used in studies on seafood production (Ellingsen et al., 2009; Pelletier et al., 2007). Still, clear prioritizations can be identied such as impacts are chosen as appropriate to the practitioner, for example, water use and land use can be excluded, and some impacts may be restricted to specic production systems. On the other hand, impact categories specic to aquaculture such as spread of disease, overexploitation of wild sh, escape, by-catch, use of antibiotics and aquatic medicines, etc. are currently not considered in LCA (Table 1), but have been major issues in the debate on sustainability and environmental risks of aquaculture (Arthur, 2008). This indicates that the scope and scale of aquaculture impact needs to be dened specically. At the same time, former categories allow for a broader comparison, i.e. between food sectors. Clearly parallel analysis of specic and generalized criteria should preferentially be carried out. Most of the aquaculture-related environmental impacts are not incorporated in appropriate impact categories in LCA. Several reasons have to be mentioned here. First, it is not easy to distinguish between the impacts and their impact categories, it is difcult to assign impact categories to an impact, or difcult to attribute impacts to the functioning of the products. Selecting impact categories in aquaculture requires careful denition of the environmental impacts, and description of the link between the impacts and the appropriate impact categories, either quantitatively or qualitatively. This is crucial in making comprehensive assessment, especially for decision making process, and needs to be addressed in the future. 5. Broadening sustainability assessment in aquaculture

economy. For example, about 70% of global aquaculture is assigned to China and Chinese aquaculture mainly comprises small production units (FAO, 2009), which support local economies and markets. Thus, one could argue that aquaculture needs to be evaluated with regard to social impact, particularly for local communities. Although environmental aspects of sustainability have gained increasing importance, the social aspects are mainly ignored in the discussion of sustainability. Recent publications (Dreyer et al., 2006; Hauschild et al., 2008; Kruse et al., 2009; UNEP, 2009) in the LCA tool development have consequently focused on the development of the economic and social counterparts of LCA, namely, life cycle costing (LCC) and social life cycle assessment (SLCA), respectively. The economic LCA is well established, but beyond the scope of this review. Here, use of SLCA in aquaculture will focus on the identication social impact categories and use of qualitative data. Still, SLCA needs to be explored further as it is undoubtedly important in sustainable aquaculture development. Kruse et al. (2009) have attempted to apply SLCA in salmon production to compare the relative socio-economic impacts of comparable products coming from different production systems. The authors described the socio-economic impact with two impact indicators selected, an additive indicator and a descriptive (general and specic) indicator. At present the methods used in SLCA are largely inconsistent with one another and efforts in developing a standard SLCA is underway. For example, in an effort to complement environmental LCA, UNEP (2009) developed a guideline for social LCA of products by following the general guideline established in environmental LCA. Such efforts are fundamental for further development and renement of methods to assess the results of social indicators using a life cycle perspective in the future. Areas of future development efforts should focus on the development of impact indicators and on the methodological developments particularly dening system boundaries, on populating databases and identifying trade-offs between stakeholders and pillars of sustainability (Kruse et al., 2009). LCAs applied in aquaculture have not yet integrated SLCA in the assessment and future research needs to develop and integrate SLCA based on social indicators specic to the sector. 5.2. Towards environmental efciency

It is important to broaden the inclusion of the different facets of sustainability to include economic, social, and environmental aspects, as well as increasing the scope for inclusion of impact categories crucial for accurate decision making, for example, impact categories related to aquaculture. Diana (2009) made similar observation in identifying the critical environmental impacts of aquaculture on biodiversity conservation indicating that an expanded LCA methodology holds much promise in providing quantitative sustainability comparisons among aquaculture, capture sheries, and agriculture systems. Moreover, other aspects of sustainability, such as social aspects, incorporated in the assessment could improve the suitability of the tool for decision making. Furthermore, resource use efciency through an optimized use of inputs at maximized outputs obtained reects operational efciency stipulating a link between operational efciency analysis method and LCA. Similar research efforts may lead to a new level of rening the technique for direct use in managerial decision making process. 5.1. Social life cycle assessment (SLCA) In the context of aquaculture production, the environmental, social and economic facets are often listed as the main pillars of sustainability. Up to now, aquaculture supports rather local

The linkage between operational efciency and environmental performance shows that the way the operational efciencies are carried out greatly inuences the environmental impact of the processes (Zhou et al., 2007), reducing impact with increasing efciency. Furthermore, benchmarking of operations is possible with the aim of identifying operational inefciencies that allow reduction of input consumption and increase of production. Some studies (Bunting, 2001; Bunting and Shpigel, 2009) suggested an integration of seaweeds and lter feeders as lter units in aquaculture systems. Other studies have demonstrated how effectively commercial scale intensive ow-through trout culture efuents are treated with constructed wetlands (Schulz et al., 2003, 2004; Sindilariu et al., 2009). In such an integrated horizontal system, LCA represents a tool to describe environmental quality, in contrast to intensive mono-species aquaculture. Consequently, culture systems combining species from different trophic levels, apply horizontal integration and generate multiple services and outputs, which is benecial from an environmental as well as economic (e.g. co-product diversication) point of view. 5.2.1. LCA for environmental efciency Current LCA research can be used to indicate biophysical sustainability (Pelletier et al., 2007) and can be used to identify

Table 1 Overview of impacts specic to aquaculture. Impacts specic to aquaculture Nutrient impact Description Related to release of efuents from sh farms and is strongly associated with feed coefcient, feed composition, and metabolic process. Effect on the environment Potential eutrophication of recipient waters Inclusion in LCA or EF Included under Eutrophication potential in LCA. Also included in the area needed to bioassimilate the nutrient release in EF. Not included

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Additives and medicaments

Antimicrobial resistance

Spread of disease

Additives to feed include: vitamins (e.g. B12 and biotin), Antimicrobial (eg. aeromycin, oxytetracycline and nitrofurazone) and pigments. Therapeutic chemicals (e.g. malachite green, formalin, copper sulfate and diterex). Used for control of antifouling and may include toxic chemicals (e.g. heavy metals and sometimes TBT). Emergence of antimicrobial resistance bacteria in treated animals and transfer of these resistant organisms to humans (or their resistance genes and human pathogens) via the food chain (Andersson and Levin, 1999; Akinbowale et al., 2006). Spread of disease from farmed sh to wild stock. Aquaculture can change the dynamics of normally occurring native parasites by providing parasites novel access to juvenile hosts (Krko sek et al., 2006; Costello, 2009) Several countries rely on introduced non-native species for aquaculture. The escapement of species from aquaculture to the wild has resulted in the introduction and establishment of these species in local ecosystems (Casal, 2006). This is especially of concern in freshwater ecosystem with relatively high endemism that may pose signicant ecological implications. Coastal habitats (e.g. mangroves) are often destroyed for marine sh farming, resulting in losses of nursery and spawning grounds for marine animals (Adeel and Pomeroy, 2002)

Effects of pigments and vitamins poorly known

Escapees

Insufcient quantitative studies on impact assessment for antimicrobial use in aquaculture Difcult to trace disease identied in one population as having been spread from another Insufcient evidence to ascertain the ecological impact of most escaped aquaculture stock

Not included

Not included

Not included

Destruction of coastal habitats

Overexploitation of wild species

Harvesting of wild seed to stock aquaculture ponds and insufcient outputs of farmed sh compared to the use of shmeal and sh oil have adverse effects on wild stocks and recruitment, which for some species is currently outside the safe biological limit.

The destruction of mangroves certainly affects the supply of wild stock replenishment. However, there is no easy way of quantifying the ecological importance of mangroves as a nursery ground and the contribution to the supply of stock replenishment in the wild. Overexploitation of wild stocks

Not included

Partly included in biotic depletion impact category in LCA, but complete picture determining its effect on overexploitation still lacks.

189

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critical processes in production (hot spots) that contribute largely to specic kinds of environmental impacts (e.g. Ayer and Tyedmers, 2009; Roque dOrbcastel et al., 2009a; Pelletier et al., 2009; Mungkung et al., 2006). This can be incorporated for formulating eco-labeling and certication criteria in aquaculture that may improve production efciency as well as identifying potential environmental trade-offs. Still, LCA reports are extremely technical, characterized by long list of environmental pollutants (Nissinen et al., 2007) that hinder consumers from making informed choices about sh products. Therefore, for the purchase decision, sustainability needs to be expressed in a simplied form with easy access to information by consumers, in a way which is comparable to the illustrative presentation of the EF with ease for visualizing the impacts. Standardization such as the development of a single index would enable furthermore the direct comparison of different case studies and broaden their practical relevance (Roy et al., 2009). Still converting the impact in a single score requires the use of validated criteria, which is seen with skepticism with respect to its scientic rigor. 5.2.2. Joint data enveloping analysis (DEA) - LCA method for environmental efciency Data enveloping analysis (DEA) is a well established methodology used to evaluate the relative efciency of a set of comparable entities called decision making units with multiple inputs and outputs by some specic mathematical programming models (Lozano et al., 2009). DEA has been recently applied to measure ecological efciency (Dyckhoff and Allen, 2001; Zhou et al., 2007; Lozano et al., 2009). However, in the context of environmental performance measurement, the assumption of radial efciency measures used by the traditional DEA models that all the outputs should be maximized is not appropriate when undesirable outputs are also generated as a by-product of the desirable outputs in the production process. Thus, using radial efciency measures often leads to the case where a lot of decision-making units have the same efciency score and hence difculty in ranking the environmental performance of these decision making units only based on their efciency scores. Since non-radial efciency measures have a higher discriminating power in evaluating the efciencies of decision making units, non-radial DEA-based models seem to be more effective in measuring environmental performance (Dyckhoff and Allen, 2001; Zhou et al., 2007). Zhou et al. (2007) have developed a non-radial DEA approach to measuring environmental performance using the case study on Organization for economic co-operation and development (OECD) countries. Although a series of non-radial DEA models have been developed in the traditional DEA framework, the development of such non-radial DEA model applicable to environmental performance is the rst. Recently, a joint application of DEA and LCA, linking both operational efciency and environmental impact has been applied in aquaculture (Lozano et al., 2009). Assuming that life cycle inventory data are available on multiple decision making units, DEA can be used to gauge their efciency and establish efciency targets. In this sense, the study compared the results of the original life cycle impact assessment (LCIA) and the computed targets life cycle impact assessment (LCIA). This results in reduced environmental impacts for the computed targets because for the same amount of output, a lower amount of inputs will be used. Lozano et al. (2009) used a case study of 62 mussel cultivation sites (rafts) in Galicia, Spain. They performed LCA for each raft and computed non-radial DEA with the aim of reducing inputs and increasing outputs in mussel cultivation (Fig. 2). The result showed that the target total environmental impact is lower than the current one for all the impact categories considered. This indicates that

Fig. 2. Simplication of data enveloping analysis (DEA) of mussel production.

reduction in environmental impact is possible provided that the estimated operational inefciencies are removed. Similarly, Iribarren et al. (2010a) suggested the use of joint application of DEA and LCA to remove operational inefciencies in dispatch centers of Spanish mussel sector. The proposed approach has the advantage of detecting and removing the technical inefciencies that are the source of unnecessary environmental impact by using LCI data that are directly related to the operation of the facilities (Iribarren et al., 2010b; Vazquez-Rowe et al., 2010). In conclusion, the linkage between operational efciency and environmental performance shows that the way the operational efciencies are carried out greatly inuences the environmental impact of the processes, reducing impact with increasing efciency. Furthermore, benchmarking of operations is possible with the aim of identifying operational inefciencies that allow reduction of input consumption and increase of production. 5.3. EF and LCA as communication tool Although EF has the advantage in illustrating the environmental impacts in a visual, simple way, expressing impacts as global hectares, its application in a dynamic interacting aquatic environment is often restricted. Therefore, it can be misleading in measuring aquaculture sustainability. Roth et al. (2000) concluded that the static measurement of a footprint-based approach will not in itself explain the reason for a non-sustainable development of aquaculture. Consequently, the use of EF as a reliable tool for the support of a comprehensive decision making process in aquaculture is limited compared to other sectors (Roth et al., 2000). Consequently, Mungkung et al. (2006) advocated the use of LCA in seafood eco-labeling, certication and consumer education practices. However, Pelletier and Tyedmers (2008) identied that current LCA practices consider a range of environmental impacts that differ from the most eco-labeling, certication and consumer awareness programmes currently practiced. Similarly, Ellingsen et al. (2009) pointed out the limited use for determining the essence of an environmentallyfriendly sheries and aquaculture industry in the public environmental debate and stressed the need of scientically sound, e.g. environmental analyses to communicate the basis of eco-labeling. The growing interest on certication of aquaculture products indicates a potential in reducing production externalities and increasing efciency. However, most certication practices mainly focus on high-value species intended for export and are based on the willingness of the farmer to get such certication. Hence, a coherent regulation and framework for aquaculture products is required. European Union regulation EC No. 710/2009 addressing the issue of organic aquaculture production came into force in 2009 (EU, 2009) setting a number of guidelines and principles related to the origin of animals, husbandry practices, breeding, feeds and feeding, disease prevention and veterinary treatment. This regulation will result in major changes to sh production through certication, while at the same time inuencing the role of government regulations and institutions, in the near future. However, the regulation is not comprehensive and the progress on the development of legislative and institutional framework is slow (Mente et al., 2011). Therefore, LCA-based certication scheme

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needs to be implemented in the legislative framework to enforce sustainable aquaculture development. Undoubtedly, the growing importance of global aquaculture demands for the evaluation and adaptation of quantitative tools for the identication of hot spots for potential technical improvements with regard to economic efciency, environmental and social concerns. Thus, in addition to supporting policy making processes, future development of the aquaculture industry relies on assessment tools to evaluate prospected expansion under the dominion of sustainability. 6. Conclusions For sustainable aquaculture development, a broader range of science based decision making tools is the key to enhance awareness and policy formulation. Key global problems generated from aquaculture are water use, nutrient and organic matter releases, impacts associated with provision of feed, introduction of diseases, introduction of exotic species, escapes, changed usage of coastal areas, and climate change. Thus, application of assessment tools needs to be specically adapted. Several tools have been presented in the past, but adaptation to aquaculture is insufcient. The failure to include impacts distinctive to aquaculture is accompanied with large discrepancies in methods employed. To summarize, limitations stem out the fact that no single tool alone is capable or sufcient in itself for generating a comprehensive assessment appropriately encompassing the different aspects of sustainability. Although large strides have been made in reaching standardized methods for environmental assessment tools such as LCA, their use in policy formulation and decision making requires relentless effort to develop the tools using fundamental problems known to aquaculture. This underscores the use of these tools as only one of several tools that should be integrated to assure comparability. Furthermore, comparability is only achieved if inter-conversion of data can easily be conducted, demanding for guidelines on the functional units used and normalizations carried out in parallel. Development of a comprehensive tool integrating the various aspects of sustainability in aquaculture could potentially ease decision making. However, the development of such universal assessment tool requires more contextual understanding and broader participation that will expand the realm of choice available to decision makers. Decision making should incorporate feedback and social learning processes and reect what is continually being learned from the mutual evolution of tools and techniques, its social setting, and consequent outcomes. Efforts to improve the sustainability of aquaculture production will require efforts that must include an optimization on how to efciently allocate resources between competing users, maximizing returns (outputs) and minimizing impacts (from inputs). The new approach of linking DEA and LCA stimulates new methodological developments and presents a driving force to environmental sustainability through economic benets envisaged by increased operational efciency. Finally, sustainability includes many economic and social aspects, apart from the environmental ones. LCA or other assessment tools need to combine economic, environmental and social aspects to comprehensively support sustainable aquaculture development. New approaches in aquaculture LCA parting from the traditional LCA methodology is thus needed, including the development of appropriate impact categories, distinctive to the aquaculture system, providing the basis for coherent regulatory framework. Acknowledgment The authors would like to thank Karsten Tusche, Saskia Kroekel, and Chris van Bussel for their contribution in proof reading the

article and support during the review process and writing of the manuscript. Financial assistance is provided by Deutscher Akademischer Austauschdienst (DAAD) and Gesellschaft fr Marine Aquakultur (GMA) mbH, which the authors are grateful.

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