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Pre-Publishing Version The Effect of China’s Aquaculture on Global Fish Resources

Ling Cao1, Rosamond Naylor1,2*, Patrik Henriksson3, Duncan Leadbitter4, Marc Metian5,6, Max Troell5,7, Wenbo Zhang8,9

1

Center on Food Security and the Environment, Stanford University, Stanford, CA 94035, USA.

2

Department of Environmental Earth System Science, Stanford University, Stanford, CA 94035,

USA. 3

Institute of Environmental Sciences, Leiden University Einsteinweg 2, 2333 CC Leiden, the

Netherlands. 4

Australian National Centre for Ocean Resources and Security, University of Wollongong,

Wollongong NSW 2522, Australia. 5

Stockholm Resilience Centre, Stockholm University, 106 91 Stockholm, Sweden.

6

International Atomic Energy Agency, Environment and Radioecology Laboratories, 98000

Monaco, Principality of Monaco. 7

The Beijer Institute of Ecological Economics, The Royal Swedish Academy of Sciences, 104 05

Stockholm, Sweden. 8

Institute of Aquaculture, University of Stirling, FK9 4LA, United Kingdom.

9

Key Laboratory of Aquatic Genetic Resources and Utilization (AGRU) of the Ministry of

Agriculture, Shanghai Ocean University, Huchenghuan Road 999, Shanghai 201306, PR China. *

Correspondence author. E-mail: [email protected]

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Pre-Publishing Version Abstract: The scale and complexity of China’s aquaculture sector places it in a precarious position between adding and depleting global seafood availability. China is by far the world’s largest producer and consumer of farmed fish and shellfish, and whether the sector will relieve pressure, or place increasing strain, on wild fisheries in the future depends critically on its use and sourcing of fish inputs in aquafeeds. The intersecting dynamics of China’s aquaculture and wild fisheries activities has been largely obscured to date by poor data and reporting, and by the complicated nature of fish feed production and use within the country. Here we use primary data from field surveys, and information from international and Chinese sources, to quantify and characterize China’s use of feed inputs from targeted and non-targeted (multi-species) fisheries. The latter includes over 70 species of fish captured indiscriminately in Chinese waters, up to half of which are identified to be juveniles of commercially important species. China is also the largest importer of fishmeal produced from wild fisheries, purchasing one-third or more of the global market in any given year. To explore an important remedy to the problem of overfishing for China’s aquaculture feeds, we develop a model that calculates the potential substitution of fish processing wastes for wild fish in feed production. We show that, if food safety and supply chain constraints can be overcome, extensive use of fish processing wastes in feeds could help China meet one-half or more of its current fishmeal demand, thus greatly reducing pressure on domestic and international fisheries.

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Pre-Publishing Version Main Text: China’s fisheries sector dominates the global seafood market in all dimensions, and unless the country’s consumption of fish for food and feed can be curbed, it will remain on a collision course with marine ecosystems at home and abroad. China is the world’s largest producer, consumer, processor, and exporter of finfish and shellfish (defined here as “fish”), and its fish imports are steadily rising (1-3). China produces over one-third of the global fish supply, largely from its ever-expanding aquaculture sector, as most of its domestic fisheries are overexploited (3-6). Aquaculture accounts for ~72 percent of its reported domestic fish production, and China alone contributes over 60 percent of global aquaculture volume and roughly half of global aquaculture value (1, 3). The country also operates the world’s largest international fishing fleet, with vessels in over 80 exclusive economic zones (EEZs) and foreign territories (46). Here we focus specifically on China’s aquaculture sector, with the aim of evaluating its impacts on wild fisheries and global seafood availability. How China develops its aquaculture sector—and whether such development can relieve pressure on wild fisheries—are key questions for the future state of the world’s oceans. China’s fisheries sector (farmed and capture) involves a complex web of importing, producing, processing and recycling fish for fishmeal and fish feeds, as illustrated in Figure 1. The country’s non-specific and often erroneous reporting of fish production and trade (7, 8) makes it especially difficult to assess the impact of China’s aquaculture and aquafeed use on ocean fisheries. For example, roughly 300,000 tons of marine fish “nei” (not elsewhere included or unidentified species) are cultivated annually in China’s aquaculture systems, and fish “nei” represent 31 percent of China’s marine capture, surpassing the reported catch of any individual species in its ocean fisheries (6).

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Pre-Publishing Version This paper quantifies the connections between China’s aquaculture production and wild fisheries using primary data from our field studies and evidence from Western and Chinese scientific literature. Secondary data from official Chinese and FAO sources are also used, prudently, to track trends. We estimate fishmeal demand and trade, and document, to the greatest extent possible, the species and stock status of fish used for aquafeeds from targeted fisheries, trash fish, and processing wastes. Finally, we assess the potential utilization of fish processing wastes for aquafeeds as a vehicle for reducing China’s dependence on capture fisheries while increasing net fish supplies.

Aquaculture expansion in China China’s fisheries sector has progressively moved into the international limelight, not only because of its scale, but also because of its shifting balance in global fish production, consumption, and trade (Supplemental Note 1). The country’s total production of capture and farmed fish tripled during the past two decades (2, 3). Virtually all of this increase came from aquaculture, the country’s fastest growing food sector (6 percent annual growth in volume from 2000-2012) (1, 3). China’s aquaculture output reached 40 million metric tons (mmt; including shell weight, excluding algae) in 2012, four times the production volume in 1990, while the area devoted to fish farming doubled to 8 million hectares (1). Aquaculture systems throughout the country are intensifying as producers seek higher returns on scarce land, water, and coastal zone resources (2). The process of intensification is reflected in higher stocking densities, greater reliance on commercial feeds, and more frequent water exchange and aeration (9, 10). The sector is also transitioning from low-input, multi-trophic systems (e.g., traditional carp polycultures that

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Pre-Publishing Version do not require compound feeds) to monocultures or polycultures containing high-valued species dependent on feeds (2, 11). Fish farming remains a highly diverse industry in China and benefits from a variety of government directives and policies (Supplemental Note 2). Over 100 freshwater and 60 marine fish species are raised in an assortment of habitats and infrastructures that include ponds, cages in lakes and coastal waters, and raft and bottom-sowing systems in shallow seas and mud flats (2, 3). Carps in polyculture, tilapia in monoculture and polyculture, and penaeid shrimp in monoculture are three of the largest sub-sectors, constituting over half of China’s total aquaculture production by volume (Table 1). By global standards, these systems are massive. In 2012, China produced over 90% of the world’s carp, 50% of global penaeid shrimp, and 40% of global tilapia (3). All of these species, with the exception of filter-feeding carps, rely on compound feeds. Fishmeal inclusion rates in feeds average 27% for shrimp, 6% for tilapia, and 3.2% (weighted) for carp, while fish oil inclusion is minimal (Table 1). Given the scale of carp and tilapia production in China, even small rates of fishmeal inclusion sum to a large aggregate demand for fishmeal (11). The efficiency of feeding practices and nutrient uptake by the fish, represented by the average feed conversion ratio (FCR), also determine the overall demand for fishmeal, and hence fish inputs, in aquafeeds. Based on primary survey data shown in Table 1, the average FCR for Chinese systems that use feeds is 1.7 for carps, 1.6 for tilapia, and 1.2 for penaeid shrimp. The relatively high FCR for carps reflects the use of poor quality fishmeal and the integration of various high-value fish species into carp polyculture, which often results in poor feed targeting and inefficient feed practices (11). In addition, the use of trash fish to supplement

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Pre-Publishing Version or substitute for commercial feeds via direct feeding of higher-valued species is common and contributes to poor feed efficiencies. Developments within China’s aquaculture industry are influenced heavily by the dynamics of demand, both at home and abroad. China is currently the world’s largest consumer of fish, accounting for one-quarter of global fish demand, and its fish consumption continues to rise with its burgeoning middle-income class (3). Its per capita fish intake is estimated at 12.614.2 kg/year when out-of-home consumption is included (11) and is expected to increase by 25% by 2030 (2). In China, as in other Asian countries, patterns of fish consumption and trade are determined by rising incomes, out-of-home consumption, a preference for convenience foods, and a taste for high-valued fish products (e.g., shrimp, crab, lobster, and salmon) and other luxury seafood (e.g., live reef fish and caviar) (2, 11, 12). Accordingly, China’s shrimp export volume has stagnated since 2008 (only 15 percent of its penaeid shrimp output is currently exported) while its shrimp import volume has risen by 47 percent (13). China’s farmed tilapia exports remain robust (accounting for 70 percent of production), but tilapia could follow the path of shrimp over time and become increasingly a product for its domestic consumption (11, 13). Overall, trends in domestic consumption portend a major shift in China’s trade position in fish products, from the world’s leading fish exporter to a net importer in the coming decades.

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Pre-Publishing Version Dependence on wild fish resources China is the world’s largest importer of fishmeal, accounting for approximately one-third of global fishmeal trade in any given year (3). During the past decade, its annual fishmeal imports have ranged from about 1.0 to 1.5 mmt (average 1.2 mmt) (3, 14-16). China’s farmed carp, tilapia, and shrimp systems alone consumed about 1 mmt of fishmeal in 2012 (Table 1), accounting for 76% of the country’s total fishmeal demand for aquaculture, and approximately 20% of global fishmeal production. The amount of fishmeal, domestically produced and imported, consumed by these three systems is equivalent to 5.1 mmt of live-weight forage fish. China’s entire aquaculture sector consumed an estimated 1.4 mmt of fishmeal in 2012 (17). This total reported volume of fishmeal is equivalent to 6.7 mmt of fish destined for reduction, which is significant in terms of China’s dependence on fish resources for aquaculture. Over one-quarter of the global fish catch (targeted and non-targeted) is comprised of reduction fisheries used for fishmeal and oil production (3, 18). Peruvian anchovy is the world’s largest targeted fishery at around 7.8 mmt per year (ranging between 4.2-10.7 mmt due to El Nino events and fishing closures in 2002-2011) (19), and China is the largest importer of Peruvian fishmeal. China also imports fishmeal reduced mainly from sardines, herring, and menhaden fisheries. Although these and other small pelagic fish reproduce rapidly, they are equally if not more vulnerable to collapse than larger predatory fish due to poor management, overfishing, and climatic fluctuations (20). All of these reduction fisheries are fully- or overexploited (Table 2). China also manufactures fishmeal domestically from targeted and non-targeted fisheries (multiple species of fish captured indiscriminately at one time, including low-valued fish and fish unfit for human consumption, a.k.a. “trash fish”) within its EEZ, and from processing wastes, as

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Pre-Publishing Version illustrated in Table 2. Domestic fishmeal production from its targeted forage fisheries has been limited by major declines in some stocks and is estimated at only 0.3 to 0.4 mmt per year (11, 21, 22). China’s main reduction fisheries, including the Japanese anchovy, Skinnycheek lanternfish, and Jack mackerel fisheries, are fully- to over-exploited, while others such as Pacific herring are moderately exploited but periodically shift to a low-productivity regime with interannual climate variation and overfishing (6, 23). Assessing the sustainability of fish inputs used for aquaculture feeds in China requires a focus well beyond targeted reduction fisheries. For example, processing wastes from wild capture fisheries—China’s domestic fisheries and its re-export industry—are used in feed production, and these fisheries are all fully exploited, over-exploited, or depleted (Table 2). In addition, large amounts of trash fish are used for fishmeal production and for direct feeding practices in China (6, 24) (Supplemental Note 3). Caught by trawl and sail stow net gears, China’s trash fish consist mainly of juveniles of commercially important fish species (~32-50%), small benthic and mesopelagic fish (e.g., sandlance, lanternfish), crustaceans, and cephalopods (25). Domestically produced fishmeal from trash fish and local processing by-products usually has a lower protein content (38-50%) and a high ash content (over 20%), and can therefore be purchased at a relatively cheap price to supplement feeds of low-valued aquaculture species (11, 26). The country’s high-valued marine aquaculture industry also uses around 3 mmt of trash fish each year for direct feeding (27, 28). Our surveys indicate that imported fishmeal from the eastern Pacific (e.g., Peru, Chile, U.S.) and Russia, which tends to be higher in protein and also in price, is commonly reserved for high-value farmed species in China. In an effort to secure future supplies of high-quality fishmeal, Chinese companies and state subsidiaries have purchased fishing rights in foreign

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Pre-Publishing Version countries, including quotas for the Peruvian anchovy fishery (Supplemental Note 3). As China commands an increasing global share of high quality fishmeal, feed companies in other parts of the world are likely to move into the lower quality fishmeal market, raising the demand for trash fish. China also sources fishmeal from other Asian countries that is derived from multispecies fisheries including trash fish (6). Given the decline in marine catches in much of China’s EEZ and its robust demand for fishmeal, the price of trash fish is expected to rise in China and elsewhere in Asia where nontargeted fisheries are common. As its value increases, so too will concerns over the impacts of multispecies fishing activities on marine resources and ocean ecosystems (6, 28). Unfortunately, the species composition of trash fish varies highly with fishing locality and season and is poorly recorded. Identifying the full range of species or species groups used for trash fish in China and in other Asian countries is thus extremely difficult. Based on our field research and an extensive literature review, we identified a total of 71 trash fish species used as feed inputs for aquaculture in China (Table S1). Relatively few trash fish species have been assessed for their stock status and, of those that have, most are classified as overfished or fully fished. Assessing the impacts of trash fish use on marine ecosystems in any systematic way will require a much broader scientific effort to identify the species composition of harvested trash fish by locality (6, 28).

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Pre-Publishing Version Potential for waste as feed The recovery of feed ingredients from fish processing wastes provides an important avenue for reducing aquaculture’s dependence on targeted and non-targeted fisheries. Between 30-70% of the volume of processed fish biomass ends up as wastes depending on the type of fish and processing level (29-31). Discards from global fish processing (i.e. trimmings, off-cut, and offal) are estimated to be around 20 mmt annually, equivalent to over a quarter of the world’s total marine catch (29). These discards, if recycled, can be further processed into niche products with a higher economic value, such as feed ingredients, human foods, pharmaceuticals, and cosmetics. Because fish processing wastes can be high in protein, minerals, and energy, their use in aquaculture feeds has gained attention (3, 30, 32). Recent estimates indicate that about 40% of China's domestically produced fishmeal (~0.25 mmt) is derived from processing wastes, with wide variation from year to year (19). Fish processing has long been a growth industry in China and is concentrated in major fish production regions such as Zhejiang and Shandong provinces. During the past decade (20032012), the country’s seafood processing industry has grown at an annual rate at 10.7%, twice that of its aquaculture sector (5.3%) (1). China is also the world’s leading re-exporter of fish (Supplemental Notes 1-2); it processes 15-20% of the global catch of cod and pollock, and large volumes of other imported whole fish such as salmon, mackerel, herring, plaice, and flatfish (33, 34). Although the re-export market is shrinking in China with rising domestic fish consumption, the volume of fish processing wastes remains large, especially when wastes from its expanding aquaculture sector are included. Utilization of the latter provides an especially important opportunity for meeting domestic fishmeal/oil demands, reducing the use of trash fish in feeds, and minimizing waste discharges and pollution from processing plants.

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Pre-Publishing Version Figure 2 displays our calculations on the expanded volume of fishmeal/oil that can potentially be derived from all finfish processing wastes in China (detailed calculations see Supplemental Note 4 and results in Table S2). Our results show that 0.65 mmt of fishmeal (0.390.92 mmt, 95% confidence interval) and 0.16 mmt of fish oil (0.09-0.22 mmt, 95% confidence interval) could be produced from China’s fish processing industry. These results suggest that fish processing wastes could be used to meet almost half (based on the average value), and potentially two-thirds (based on the upper 95% confidence limit), of China's current total demand for fishmeal in aquafeeds. A more conservative estimate, based solely on China's current fish exports (versus potential fishmeal/oil from its exports and domestically consumed fish), indicates 0.42 mmt of fishmeal and 0.1 mmt of fish oil could be produced from processing wastes (Table S3). Serious constraints exist, however, on the utilization of fish processing wastes for aquafeeds in China. First, the nutritional quality of fishmeal obtained from processing wastes tends to be inferior to conventional fishmeal produced from wild fish due to the removal of structural protein (32). Conventional fishmeal made from wild forage fish often has a crude protein content between 67% and 90%, while fishmeal derived from processing wastes usually contains between 57% and 80% crude protein depending on the raw waste used (35). Nutritional deficiencies caused by using offal-based fishmeal can be overcome with alternative feedstuffs; e.g., new plant-based products such as algae and ethanol yeast developed through the biofuels industry (36). However, alternatives to fishmeal must possess comparable nutritional values, ready availability, digestibility, and reasonable palatability at competitive cost (32). Second, the use of fish processing wastes in aquafeeds presents important food safety risks related to the bioaccumulation of contaminants, cross-species transmission of pathogens, and, possibly, prions

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Pre-Publishing Version (30, 32). To avoid disease transmission, Europe Union forbids the use of farmed fish by-products in finfish feeds but allows them to be used in crustacean diets or vice versa (30). Although China currently has no such food safety regulations, there is an increasing awareness on traceability and quality in aquafeeds inputs. China is even examining a new national standard for regulating dioxins and usage of multiple species in fishmeal and oil. Finally, development may also be hindered by the predominance of small-scale processing plants with outdated equipment, and inefficient or costly collection of raw materials along the supply chain. These constraints, albeit very important, are not insurmountable, particularly in the case of aquaculture processing wastes (30). The strategic design of an aquafeed sector based on processing wastes from the aquaculture industry itself makes perfect sense for China, especially if food safety risks can be closely monitored. China’s aquaculture sector is massive and yields a steady and consistent stream of processing wastes. If processing facilities are co-located with fishmeal and feed plants, the problems of perishability, high transportation costs, and supply chain barriers can be minimized. Such a strategy of co-locating processing and feed activities would require improving facilities to meet environmental standards; co-location would then support China’s current Five-Year Plan (2011-2015), which aims to promote energy and water efficiency and to minimize waste discharges and pollution (Supplemental Note 2).

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Pre-Publishing Version Conclusions The scale and complexity of China’s aquaculture sector places it in a precarious position between adding and depleting global seafood availability. Aquaculture in China is comprised largely of low-trophic level species, including omnivorous and herbivorous finfish, shellfish, and seaweeds; however, the cultivation of marine finfish, crustaceans, and high-valued freshwater finfish is on the rise, all of which currently require diets rich in marine fish products. Feed efficiencies are sub-optimal in emerging, small-scale polyculture systems where feed targeting is by trial-and-error, and in high-valued marine systems where fish parts from non-targeted fisheries are primary feeds ingredients. The use of feeds containing fishmeal is even costeffective, and thus widely used, in low-trophic level systems in China, including carps and tilapia. The aggregate production of fish in these systems is massive, and thus the overall amount of fish demanded for aquafeeds is also immense. China is by far the largest importer of fishmeal globally. Its demand for trash fish as a feed ingredient also places considerable pressure on its domestic fisheries and the fisheries of other Asian countries where non-targeted fishing activities are common. If China is to become a net producer of fish protein globally, its aquaculture industry will need to reduce FCRs and the inclusion of fish ingredients in feeds, and improve fishmeal quality. The diversity and low-trophic level base of China’s aquaculture sector provides substantial opportunity for positive change. Our analysis shows that fish processing wastes have the potential to substitute increasingly for imported fishmeal in China’s aquaculture sector if the appropriate technology and supply chains are developed, and if food safety can be guaranteed. The availability of fish processing wastes from China’s expanding aquaculture sector could also replace the use of trash fish in feeds if the economics of such substitution were to become favorable with scale. Even if

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Pre-Publishing Version fish processing wastes are recycled as feeds, however, China’s aquaculture industry will continue to strain wild fisheries unless the country commits to stricter enforcement of regulations on targeted and non-targeted fishing within and outside of its EEZ, and to responsible sourcing of fishmeal/oil (Supplemental Note 3). Using fishmeal derived from by-catch or by-products of wild fisheries as a means of reducing pressure on wild fisheries remains controversial and should be monitored (32). Without such measures, developments within China’s aquaculture sector are destined to diminish wild fish stocks worldwide. The stakes of pursuing a sustainable seafood strategy in China are high. The world’s marine ecosystems are being degraded at an alarming rate by overfishing, coastal pollution, habitat destruction, and climate change (3, 37, 38). China’s coastal zones and continental shelf have been over-fished, and marine biodiversity in these regions has declined significantly (39). Meanwhile, China’s domestic consumption of fish continues to climb, and the country’s taste for high valued fish is expanding with growth in its middle-income population. China’s only option for meeting this rising demand without excessively exploiting the world’s wild fisheries is to expand its aquaculture industry without increasing the use of captured fish in feeds. Failing to do so will lead to irreversible damage to the world’s oceans.

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2.

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3.

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S. S. De Silva, G. M. Turchini, “Use of wild fish and other aquatic organisms as feed in aquaculture - a review of practices and implications in the Asia-Pacific” (FAO, Rome, 2009).

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Pre-Publishing Version Acknowledgements: We thank Walter Falcon, David Little, Alice Chiu, Chris Fedor, and Laura Seaman for substantive input on the manuscript. We also thank the China Fund of the Freeman Spogli Institute for International Studies at Stanford University and the Lenfest Ocean Program of the Pew Charitable Trusts for financial support leading to this manuscript, and the EU-FP7 Sustaining Ethical Aquaculture Trade (SEAT) project and the David and Lucile Packard Foundation for support of our field surveys in China.

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Pre-Publishing Version Figure 1. Connections between the Chinese aquaculture sector and global fish resources. Thick blue lines refer to main flows of fish in and out of China. Thin blue lines indicate minor flows. Hatched black lines refer to other flows with indirect connections to China’s fish industry (not included in this study). China’s aquaculture sector uses fish inputs for feeds from: i) domestic capture fisheries (marine fish nei, by-catch and poor quality/spoiled fish); ii) fishmeal and oil produced domestically or imported, which rely on capture fisheries (reduction fisheries and marine fish nei) and wild or farmed fish processing by-products; and iii) fish parts from processing wastes. The aquaculture industry provides fish for human consumption and fish processing wastes for feed production. By-products from wild and farmed processing operations are also used to manufacture various commodities such as surimi for the global market.

Figure 2. Estimated potential of fishmeal and oil production from China’s fish processing industry. The 95% confidence intervals are (0.39, 0.92) for fishmeal, and (0.09, 0.22) for fish oil. Data Source: Authors’ calculations based on 2012 data obtained from refs (1, 34). Sources of whole fish supply in China include: i) import, ii) domestic aquaculture, and iii) domestic wildcaught. A total of 36.7 mmt of whole fish was available in China in 2012, mainly from domestic aquaculture. Of these, only about one-third was processed, while the majority was sold directly at domestic market. Wastes (heads, frames etc.) generated during processing fish could be recycled and further processed into human foods or feed ingredients.

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Pre-Publishing Version Table 1. Feed efficiencies and wild fish inputs in feed for nine leading farmed species in China* Species

Total production in 2012 (mmt)

Production with feeds (mmt)

Aver. FCR†

Aver. % FM in feed‡

4.8

2.6

1.7

Forage fish equiv. (mmt)§

Aver. % FO in feed‡

Total FM used (mmt)

1.5

0

0.07

0.32

I. Carps Grass carp Silver carp



3.7

-

0

-

-

-

-



2.9

-

0

-

-

-

-

Common carp

2.9

1.6

1.7

6

0

0.16

0.77

Crucian carp

2.5

1.3

1.7

8

0

0.18

0.87

Bream

0.7

0.4

1.7

2.6

0

0.02

0.08

Black carp

0.5

0.3

1.7

2.6

0

0.01

0.06

II. Tilapia

1.6

1.3

1.6

6

0.5

0.13

0.60

III. Penaeid shrimp

1.6

1.5

1.2

27

2

0.50

2.36

Total

21

9.1

-

-

-

1.06

5.07

Bighead carp

Note: *Total production data for each species were from ref (1). Production with feeds was estimated based on ref (40). All other data were estimated from our primary field surveys. † Average economic feed conversion ratio (Aver. FCR) = total feed fed/total biomass increase. ‡ Average fishmeal (FM) and fish oil (FO) inclusion rates. § Wet weight equivalent (equiv.) of forage fish used to produce fishmeal and fish oil. An average reduction ratio of 21% for fishmeal and 5% for fish oil obtained from our field surveys were used for this estimation. ◊ Non-fed filter feeding species, graze planktons proliferated through fertilization and the leftover feeds in the polyculture system.

21

Pre-Publishing Version Table 2. Sourcing wild fish for fish feeds in China Source category Directed fisheries§

Main species

Scientific name

Stock status*

Japanese anchovy

Engraulis japonicus

Overexploited

Skinnycheek lanternfish

Benthosema pterotum

Fully exploited

Jack mackerel

Trachurus japonicus

Fully exploited

Clupea pallasii

Moderately exploited

Largehead hairtail

Trichiurus lepturus

Overexploited

Pacific sandlance

Ammodytes personatus

Moderately exploited

Japanese scad

Decapterus maruadsi

Overexploited

Slender lizardfish

Saurida elongate

Overexploited

Indian anchovy

Stolephorus indicus

Overexploited

Chub mackerel

Scomer japonicus

Fully exploited

Peruvian Anchovy

Engraulis ringens

Overexploited

Chilean jack mackerel

Trachurus Murphyi

Overexploited

Chub mackerel

Scomer japonicus

Fully exploited

Gulf Menhaden

Brevoortia patronus

Fully exploited

Atlantic Menhaden

Brevoortia tyrannus

Fully exploited

Atlantic herring

Clupea harengus

Fully exploited

Capelin

Mallotus villosus

Fully exploited

Blue Whiting

Micromesistius poutassou

Fully exploited

Alaska Pollock

Theragra chalcogramma

Fully exploited

Atlantic cod

Gadus morhua

Fully exploited

Skipjack tuna

Katsuwonus pelamis

Fully exploited

Pacific herring Domestic: Non directed fisheries

Directed fisheries Imports:

Fish processing by-productsǂ



*

Note: Stock status information was from refs (3, 18, 23, 25, 39). Moderately exploited: operated at a lower level than optimal yield, with potential for expansion in total production; Fully exploited: operated at or close to its optimum yield level, with no potential for further expansion; Overexploited: exploited at a higher level than the maximum sustainable yield, with high risk of stock depletion; Depleted: catches are far below historical levels. † Pacific herring (Yellow Sea stock) is a species with apparent regime shifts in productivity, that is, long-term change in abundance. High abundances appeared in 1970s and it is now in low-productivity regime. § Directed and targeted fisheries can be used interchangeably, which refer to the retention on board a fishing vessel of a quantity of any groundfish species or species group in an amount equal to or greater than specified percentages of the total amount of fish. ǂ Fish processing by-products are not imported directly, but derived from processing imported wild-caught whole groundfish such as pollock. Domestic fish by-products are not included in the table since they are mainly from farmed fish such as tilapia.

22

in ’s fish dustry ina Ch

Global Import 1.97 mmt

Domestic Aquaculture 24.4 mmt

Domestic Fisheries 10.4 mmt

33.8% Whole Fish 36.7 mmt

Processing 12.4 mmt

Domestic Consumption 25 mmt

Export 3.05 mmt

2% Loss

By-products 5.4 mmt (Heads, Frames etc.)

Processed Fish 3.72 mmt

Further Processing

Human Foods

(Mineral supplements, Pharmaceuticals etc.)

Feed Ingredients

0.65 mmt of fishmeal 0.16 mmt of fish oil

Industrial Use (Fuels, Cosmetics etc.)

Fertilizers

(Compost, Soil conditioners etc.)

Supplementary Materials for The Effect of China’s Aquaculture on Global Fish Resources Ling Cao, Rosamond Naylor, Patrik Henriksson, Duncan Leadbitter, Marc Metian, Max Troell, Wenbo Zhang

This file includes: Methods Supplemental Notes 1-4 Figs. S1 to S9 Tables S1 to S4 References (41-61)

1

METHODS Data collection. Primary data for this study were obtained from interviews with fish farmers, fishmeal and feed manufacturers in China’s major aquaculture producing regions− Guangdong, Shandong, Zhejiang, and Hainan. The data were based on in-depth field surveys conducted by the

Center

on

Food

Security

and

the

Environment

at

Stanford

University

(http://foodsecurity.stanford.edu) and the EU-FP7 Sustaining Ethical Aquaculture Trade (SEAT) project (www.seatglobal.eu) in 2010-2012. The surveys focused on carp, tilapia, and shrimp systems, which represent three of the largest aquaculture sub-sectors in China along a spectrum of low- to high-valued species and account for over 50 percent of the country’s aquaculture output by volume. These systems span a suite of target markets, including species produced mainly for domestic consumption (carps), species in transition from export-oriented to domestic market (shrimp), and species still primarily destined for export markets (tilapia).

Structured systematic questionnaires for two separate surveys of fish production, and fishmeal and feed manufacturing were tested in the field and then improved in response to feedback before the start of general surveys. The fish production survey mainly collected information on farm characteristics such as farm area, pond size, labor and feed use; farming techniques such as stocking density and water quality control; production costs; disease outbreak; main concerns during fish farming; as well as consumer preference for whole fish. The survey of fishmeal and feed manufacturing mainly covered topics of feeds produced, feed ingredients (raw materials) used and their origin and substitutions, utilization of fish processing wastes, annual production quantities, sales and marketing, price fluctuations, and challenges faced. Total sample size was determined according to resource availability. A total of 238 carp farms (Zhejiang 118,

2

Shandong 120), 300 shrimp farms (Guangdong 200, Hainan 100), 320 tilapia farms (Guangdong 135, Hainan 185), 21 feed and 4 fishmeal companies were surveyed. For each survey site, farm owners or head managers were interviewed. Facility records were used for verification to reduce possible errors.

A careful review of papers from the Chinese literature (and international literature) on China’s aquaculture practices, use of diverse fish inputs, including processing by-products, in feeds, multi-species fisheries, and by-catch categories was performed in order to filter out the top scholarly work and most accurate numbers/trends. References to articles written in Mandarin have been translated into English in the citations of this manuscript.

Data management and analysis. Primary data obtained from these surveys were compiled and analyzed using Microsoft Excel 2010 and R (version 3.1.0, www.r-project.org). The data were scanned for outliers in R; these outliers were then evaluated using a number of possible triangulations from our original questionnaires, and any physically or economically impossible data points were removed from further analyses. From the remaining values, FCRs and fishmeal inclusion rates in feeds were defined by arithmetic means. The fishmeal inclusion in feeds was calculated as a percentage of the total feed production for each species, thus capturing juvenile, grow-out and finisher feeds.

Monte Carlo modeling. A Monte Carlo analysis was undertaken to estimate the aggregate impact of data uncertainty on fishmeal and oil yield from fish processing waste in China (here fish is limited to finfish and crustaceans; mussels are excluded because their waste is rarely used

3

in feed production). The uncertainty parameters represented variations in the yield of fish waste during processing and its market allocation for fishmeal and oil production (Table S4). The parameter estimates for the model were obtained from our interviews with fishmeal and feed companies and from personal communication with experts in the field, and then triangulated with values taken from the literature. Uncertainty results were calculated from 50,000 simulations using the Monte Carlo sampling method.

4

Supplemental Note 1: Trends in China’s fish production, consumption and trade Production China’s total fish production (via aquaculture and capture fisheries) increased six-fold between 1986 and 2012 (Fig. S1). The country’s per capita fish supply reached 43.6 kg in 2012—almost twice the global average—and is expected to climb to 50 kg by 2030 (1, 2). Virtually all of the growth is from the aquaculture sector. Freshwater fish species accounted for 58 percent of total aquaculture production (excluding seaweeds) in China in 2012, with the rapidly growing mariculture industry (mollusks, crustaceans, and marine fishes) contributing the balance.

Consumption Growth in aquaculture production and rising per capita incomes in China have resulted in steady increases in domestic seafood consumption. These trends are expected to continue, with especially strong growth in rural consumption (41). Of all fish consumed in China, fresh whole fish account for 88%, indicating a strong preference for live and fresh fish by Chinese consumers. The demand for convenience seafood (i.e. processed fish and fishery products) is also growing in China (2). As its population and per capita incomes continue to grow, China’s reliance on finfish and shellfish, wild or farmed, is expected to continue to increase. In particular, China’s upper and burgeoning middle classes will demand more high-valued fish products (such as shrimp, crab, lobster, salmon, and scallop) and other luxury seafood such as live reef food fish (11, 12).

Per capita seafood consumption in China has doubled over the last two decades (Fig. S2). China’s average seafood consumption was 10.5 kg/capita in 2012 according to National Bureau

5

of Statistics of China (NBSC). Official Chinese statistics do not account for out-of-home consumption, however, and thus underestimate per capita seafood consumption by 20-35% in both rural and urban areas (11).

Estimates for China’s per capita seafood consumption vary by source (11). FAO statistics on per capita seafood consumption in China are substantially higher than the national averages recorded by NBSC (Fig. S3). This difference arises because FAO statistics refer to per capita seafood supply (physical availability), which are very close to the availability numbers reported in the China Fisheries Yearbook.

Trade China is the world’s largest fish exporter, processer, and re-exporter, and its imports are rising rapidly as domestic fish consumption grows. The country’s trade volume in fish products more than doubled between 2000 and 2013, from 4 million metric tons (mmt) to 8.1 mmt, while its value of fish trade increased five-fold (1) (Fig. S4). China’s trade surplus (i.e. net trade balance) has increased about 6-fold from US$1.98 billion in 2000 to US$11.7 billion in 2013 (1).

China has dominated the fish export market since 2002, contributing over 12 percent of the global total (worth over $19 billion) in 2013 (3). Despite the slow recovery in the global economy, increasing non-tariff trade barriers among its trade partners, and rising production and transportation costs, China’s fish exports have been rising steadily during the past decade. Export value increased 5-fold between 2000 and 2013, from US$3.8 billion to US$20.3 billion, while the volume of fish exports rose from 1.5 mmt to 3.9 mmt (16). Such strong growth in exports

6

was due mainly to the disproportionate increase in aquaculture exports (8), which now account for more than half of the total. The leading export species have been shrimp, followed by tilapia, molluscs, eels, crawfish, and croakers (16). Fish fillets remains the largest export category over the last decade, accounting for 25% of total fish exports by value, and exports of value-added products, such as surimi and caviar, have also grown substantially. The main destinations for China’s fish exports include Japan, U.S., ASEAN, Europe, and South Korea with a collective market share of 68% in 2013 (16). China’s re-exports of fish, consisting of domestically processed products from imported raw fish (e.g. fish fillets and value-added products such as surimi and caviar), have also continued to grow.

Given these trends, it is not surprising that China’s import value of fish also increased five-fold between 2000 and 2013. China is now the third largest fish importer in the global market (3). The value of its fish imports increased five-fold between 2000 and 2013, reaching US$8.6 billion at the end of the period, while the volume of fish imports reached 4.2 mmt (16). Russia and U.S. remain China’s main suppliers of fish, accounting for 32% (US$2.7 billion) of total imports by value in 2013 (16). Over half of fish imports are frozen whole fish, including mainly cod, salmon, herrings, squid, largehead hairtail, plaice, and flatfish (Fig. S5). The majority, about 6075%, of the imported frozen raw fish is processed and then re-exported (2). In addition, China has become the world’s largest importer of fishmeal (Fig. S6 & S7). The country imports around 1.2 mmt of fishmeal annually (mainly from Peru, the U.S. and Chile), accounting for approximately 30 percent of global fishmeal imports (3).

7

Supplemental Note 2: Government Directives and Policies Government policies and directives designed to boost production in both distant water fisheries and aquaculture reflect the underlying goal of enhancing employment, incomes, and export revenues in the face of its declining domestic fisheries. China has historically had the world’s largest labor force employed in the fishing sector and among the highest rates of capture fishing subsidies (3, 42). The government also supports aquaculture through investments in a variety of genetic improvements (e.g., selective breeding for fish growth and pathogen resistance), and through subsidies to help producers replace outdated equipment, adopt new technologies, and insure themselves against extreme weather events and other risks (2).

In addition to supporting fish production, the Chinese government has used policy to enhance fish trade. An export tax rebate policy has been in place since 1985 to eliminate double taxation on exported goods and therefore promote export trade (43). The export tax rebate allows refunds or exemption of value-added tax (VAT) and consumption tax levied during production, distribution, and sales of exported goods. In the case of fish, the VAT rate is 0% if imports are targeted for re-exports.

There are five key aspects of China’s central planning strategy that currently shape developments in its aquaculture and capture fisheries sector toward people-centred, unified and harmonious development of economy and environment. China’s 12th Five Year Plan acts as the central guideline to all other national policies. It suggests that the seafood industry still has room for growth and must take on a much greater role in

8

meeting the country’s evolving nutritional demand. Although China has achieved remarkable progress in achieving food security during the past half-century, many people in the country still face serious nutritional deficits. It is thus in the interest of the Chinese government to promote food security in terms of protein and micronutrient consumption, and aquaculture and marine fisheries will play a crucial role in this process. Due to the constraints on land and freshwater, the intensification of the aquaculture industry will need to be more environmentally friendly. Given its scale, China’s aquaculture sector will also have to curtail the demand for fishmeal to relieve pressure on global wild fisheries. Supported by China’s “Circular Economic Promotion Law”, one promising solution would be extensive recycling of fish processing wastes.

1. China’s 12th Five-Year Plan (2011-2015) for Fisheries The Ministry of Agriculture of China released its 12th Five-Year Development Plan for the Fisheries sector. The main development goals include: a goal for increasing seafood production from 53.7 mmt in 2010 to over 60 mmt by 2015, with 75% contributed by aquaculture; a goal of raising the seafood processing rate from 35% in 2010 to 40% by 2015; a green development initiative with an emphasis on balancing growth in seafood production with improved environmental protection; and the achievement of food safety targets for 98% of its seafood products. For further details about China’s 12th Five-Year Plan for fisheries sector, see: http://www.moa.gov.cn/zwllm/ghjh/201110/t20111017_2357716.htm

2. China’s 2014 “No. 1 Central Document”

9

Food security was listed as the top priority of China’s 2014 “No. 1 Central Document”, the main policy strategy document issued each year by the Central Committee of the Communist Party of China and the State Council. Enhancing fish production is an important aspect of China’s food security in terms of increasing protein supplies and supporting rural incomes. For further information on China’s No. 1 Central Document, see: http://www.moa.gov.cn/ztzl/yhwj2014/ For English translation: http://english.peopledaily.com.cn/90785/8516743.html

3. Land Management Law To ensure the nation’s food security, China’s central government requires a minimum threshold of 120 million hectares of arable land for agricultural uses, and digging new ponds for the expansion of aquaculture in staple farmland regions is strictly prohibited (http://www.gov.cn/banshi/2005-05/26/content_989_2.htm).

This

law

reflects

the

country’s land scarcity in the face of rising population and food demand. In 2012 China’s population reached 1.35 billion—roughly one-fifth of the global population—yet the country contains only 9 percent of the world’s arable land and 6.5 percent of the world’s freshwater resources.

4. Water Policy Similar to land (above), the allocation of freshwater resources for terrestrial pond aquaculture is limited in many areas of the country, and in recent years most mediumsized reservoirs and lakes have been reserved for drinking water for nearby cities and

10

crop production. Most aquaculture cage and pen systems have been removed or highly restricted in these reservoirs and lakes due to health and sanitation reasons. Mariculture is being promoted in China due to rising constraints on freshwater quantity and quality in many parts of the country (2). For further details about China’s water policy, see: http://blogs.ei.columbia.edu/2011/10/24/chinas-decade-plan-for-water/ and http://chinawaterrisk.org/regulations/water-policy/12th-five-year-plan/

5. Circular Economy Promotion Law The use of fish processing wastes for aquafeeds is aligned with China’s “Circular Economic Promotion Law”. According to this 2009 law, the Chinese government offers tax preferences to industrial activities promoting the development of the circular economy—the recycling of energy, water, and waste products—and uses tax measures to encourage the import of water-saving technologies. Specific policy measures are formulated by the public finance department and the tax department under the State Council. See more at: http://chinawaterrisk.org/regulations/water-regulation/#sthash.oxAcX94e.dpuf

11

Supplemental Note 3: Dependence on marine resources One measure of aquaculture’s dependence on fish resources is the ratio of fish-in to fish-out (FIFO); FIFO provides a rough gauge of fish inputs used in fish feeds, but it does not identify the source of fish for feeds (i.e., targeted forage fisheries, non-targeted multispecies fisheries, bycatch, or fish processing wastes). In the case of China’s main aquaculture systems, FIFO is estimated to be 0.18 for non-filter feeding carps, 0.39 for tilapia, and 1.5 for penaeid shrimp. These values are comparable to the global estimates for FIFO for these species reported by Tacon and Metian (40) and significantly lower than earlier estimates dating back ten to fifteen years (44, 45), indicating improved feed efficiencies over time. It is likely that these FIFO ratios will decline in the future with improved feeding practices and feed efficiencies, but the aggregate use of fish for aquaculture feeds in China is still expected to grow as the culture of high-valued species reliant on feeds expands.

To secure fishmeal supply to China’s ever-growing market, Chinese companies have increasingly purchased fishing rights in foreign countries. For examples please see http://www.undercurrentnews.com/2014/01/14/china-fishery-could-buy-more-in-peru-asdiamante-owners-still-looking-for-exit/; http://www.marketwatch.com/story/china-fishery-bids556m-for-copeinca-2013-02-26;

http://sbr.com.sg/shipping-marine/more-news/china-fishery-

becomes-perus-sixth-largest-fishmeal-company; http://www.4-traders.com/news/China-Fisheryacquires-a-fishmeal-plant-and-further-increases-fishing-quota-in-Peru--13881959/.

Virtually all of the fish hauled out of the ocean by Chinese vessels are put to economic use, first for human consumption, and then for feeds and other purposes. Discards in China’s fisheries are

12

negligible (0.5% of total catch vs. ~8% for global fish catch) (46). “Trash fish” in China thus refer only to fish of low-economic value used in fish/livestock feeds (unfit for direct human consumption), while “low value fish” generally indicates fish consumed directly by humans (27). Converting trash fish to a quality suitable for human consumption would increase the total costs due to value-adding process and extra transportation and preservation needs (28). Although the price of trash fish increased from less than $0.2 per kg before 2005 to $0.3~0.4 per kg in 2013, it is still relatively inexpensive compared to other protein sources (27). Direct and indirect use of perishable trash fish as feeds is therefore still economically viable in China. In addition, common forms of trash fish, such as that derived from Pacific sandlance, are often used to improve the appearance and meat quality of farmed carnivorous species (28). Table S1 lists some of the fish species found in China’s trash fish and their stock status. This list was compiled from information gathered by the authors of this paper (especially Leadbitter), and from other reviews and studies in the literature.

China’s aquaculture sector does not consistently follow international mandates on responsible fishmeal/oil sourcing. These guidelines were developed jointly by the Aquaculture Stewardship Council (www.asc-aqua.org), the Global Aquaculture Alliance (www.gaalliance.org), and GlobalGAP (Global Good Agricultural Practices, www.globalgap.org) in 2013. The mandates include traceability of fishmeal/oil inputs to species and country of origin; banning the use of endangered species and fish sourced from illegal, unreported, and unregulated fishing for feeds; and preference for compound feed manufactures that source fishmeal/oil from certified “sustainable” aquaculture and capture fisheries operations, including products derived from fish processing wastes.

13

Overall, China has a relatively low ranking in ocean health, and the demands that aquaculture places on the marine environment contribute to its poor performance. An ocean health index tool was developed recently to evaluate the condition of marine ecosystems from biological, physical, economic, and social dimensions, and to assess how sustainably each country/region is using the ocean (47). China received an overall index score of 58 out of 100 on its ocean health within EEZ boundaries in 2013 (ranking 161 out of 220 countries) (http://www.oceanhealthindex.org), which is below the global average (index = 65), indicating poor management of the index’s public goals and substantial room for improvement in the future.

14

Supplemental Note 4: Potential for wastes as feed Numerous papers have indicated the nutritional quality of waste derived fishmeal depends on the source of raw materials and processing technology used (32, 35, 48-51). Some fisheries by-catch or by-product (e.g. Alaskan Pollock by-product) meals may have equal nutritional quality as that of the highest-graded fishmeal. However, due to the removal of structural protein to produce fish fillets, fishmeal derived from processing wastes usually has a lower protein content and higher ash (bone) content than conventional whole-fish meal (32). In addition, key fatty acids might be low in fishmeal derived from wastes of freshwater species. Though de-boning technology has been investigated as a way to reduce ash content in raw materials (52), the nutritional quality of fishmeal obtained from processing wastes still tends to be inferior to conventional fishmeal.

Fish processing has long been a growth industry in China and has been fueled by its fish export and re-export industry. In the past, the industry has been supported by the availability of cheap labor and a rapidly growing aquaculture industry. The number of aquatic processing facilities increased from 6,900 in 2000 to over 9,700 in 2012 (1). During the same period, the country’s total processing capacity increased from 9 to 26 mmt (1). The future of the processing industry is less certain, however, due to rising wage rates in China and increasing competition in the fish reexport market by other Southeast Asian countries.

Given the traditional preference for fresh whole fish by Chinese consumers, the majority of processed fish products are destined for export (or re-export), but there is a growing domestic demand for convenience fish products. Currently, one-third of fish output available for

15

consumption in China is processed, and the portion is estimated to reach 40 percent by 2015 according to China’s 12th Five-Year Plan.

We estimate that in 2012, 12.4 mmt of finfish were used as raw materials for processing. We assume a median production yield for whole raw fish of 40% and a 2% flesh loss due to spoilage and other technical reasons. Because there is wide uncertainty in the waste ratio (percentage of waste derived from whole fish, ranging from 30 to 70 percent) and the market allocation of fish processing waste (the share of processing by-products used in fishmeal and fish oil production, ranging from 50 to 80 percent), a Monte Carlo analysis is used to determine the distribution potential of fish feed from wastes.

Calculation: potential for fish processing waste as feed in China (in year 2012) i.

Total seafood available in China (1): = imports + domestic farmed + domestic wild caught = 4,123,800 + 42,883,600 + 16,193,200 = 63,200,600 (metric tons)

ii.

Proportion used for processing (1): = total raw seafood for processing/total seafood available = 21,358,082/63,200,600 = 33.8%

iii.

Total whole fish available: = whole fish imports + domestic farmed + domestic capture fisheries

16

iv.

Whole fish used for processing: = total whole fish available × proportion used for processing

v.

Processed fish = whole fish used for processing × fish processing yield rate

vi.

Fish waste = whole fish used for processing in China × waste ratio

vii.

Potential fishmeal yield from fish waste = fish waste × fishmeal reduction ratio Potential fish oil yield from fish waste = fish waste × fish oil reduction ratio

Scenarios Two scenarios were developed to assess China’s potential in recycling fish processing wastes for feeds. Scenario 1, which examines processing wastes from finfish only, is considered as the most likely scenario since finfish processing wastes are used mainly for producing fishmeal while crustaceans wastes are used for producing a wide range of feed and (mostly) non-feed products. Scenario 2, which includes all processing wastes from both finfish and crustaceans, reported here for comparison purposes. Some crustacean processing wastes are used as aquafeed supplements or attractants.

Scenario 1: waste from processing finfish only Our results indicated that averagely about 0.65 mmt of fishmeal (95% confidence interval: 0.390.92 mmt) and 0.21 mmt of fish oil (95% confidence interval: 0.09-0.22 mmt) could be gained from China’s finfish processing (Table S3; Fig. S8). 17

Scenario 2: waste from processing both finfish and crustaceans Our results indicated that averagely about 0.9 mmt of fishmeal (95% confidence interval: 0.681.15 mmt) and 0.22 mmt of fish oil (95% confidence interval: 0.16-0.27 mmt) could be gained from processing both finfish and crustaceans (Table S3; Fig. S9).

18

50 40

Freshwater aquaculture

30

Mariculture Domestic marine fishery

2012

2010

2008

2006

2004

2002

2000

1998

1996

0

1994

Distant-water fishery

1992

10 1990

Freshwater fishery

1988

20

1986

Million metric tons

60

Figure S1. China’s total aquatic production (1)

40 35 kg per capita

30

Pork, Poultry, Beef and Mutton (Urban)

25

Aquatic Products (Urban)

20 15

Pork, Poultry, Beef and Mutton (Rural)

10

Aquatic Products (Rural)

2012

2011

2010

2009

2008

2007

2006

2005

2004

2003

2000

1995

0

1990

5

Figure S2. Per capita aquatic consumption trends compared to other meat consumption in China (53)

19

50

National Average Seafood Consumption (in-home consumption)

45

kg per capita

40

National Average Seafood Consumption (in-home plus out-ofhome consumption) Per Capita Seafood Supply - China Fisheries Yearbook

35 30 25 20 15

Per Capita Seafood Supply - FAOSTAT

10 5 0

Figure S3. Estimates for China’s per capita seafood consumption versus supply (1, 53, 54)

20

35

US$ billion

30 25 20 15 10 5 0

Export

Import

Figure S4. China’s fish trade by value from 2000-2013 (1, 16)

21

2,500,000

tons

2,000,000 1,500,000 1,000,000 500,000 -

Frozen whole fish

Salmon

Cod

Figure S5. China’s imports of frozen whole fish (34)

22

Herrings

Figure S6. The balance of global fishmeal trade in 2012 (unit: metric tons, MT) (55)

23

1.8

million metric tons

1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0

Figure S7. China’s fishmeal imports (56)

24

Figure S8. Simulated potential yield of fishmeal and oil (scenario 1)

25

Figure S9. Simulated potential yield of fishmeal and oil (scenario 2)

26

Table S1. Numerous trash fish species found in China and their stock status (23, 25, 28, 57) Fish species Scientific name Stock status Region Ambassis Bald glassy Unkown South China Sea gymnocephalus Beka squid Loligo beka Unkown East China Sea Belenger's croaker Johnius belengerii Unkown East China Sea Bladder moon snail Polinices didyma Unkown East China Sea Bluespotted Xenocephalus elongat Unkown East China Sea stargazer us Moderately-fully Bombay-duck Harpadon nehereus East China Sea exploited Brownback Carangoides Unkown South China Sea Trevally praeustus Butterfly Bobtail Sepiola birostrata Unkown East China Sea Squid Chinese ditch Palaemon gravieri Unkown East China Sea prawn Commerson's Stolephorus commers Overexploited East China Sea anchovy onnii Common frog shell Bufonaria rana Unkown East China Sea Common hairfin Yellow and Bohai Seas; Setipinna tenuifilis Unkown anchovy East China Sea Common octopus Octopus vulgare Depleted East China Sea Crocodile flathead Cociella crocodila Unkown East China Sea Deep pugnose Secutor ruconius Unkown South China Sea ponyfish Dotted gizzard shad Konosirus punctatus Unkown South China Sea Fat greenling Hexagrammos otakii Unkown East China Sea Chaeturichthys Finespot goby Unkown East China Sea stigmatias Firefly lanternfish Hygophum proximum Unkown East China Sea Forksnout searobin Lepidotrigla alata Unkown East China Sea Gaper Tresus Keenae Unkown East China Sea Gray stingfish Minous monodactylus Unkown East China Sea Gunther's lizard Synodus kaianus Unkown South China Sea fish Hardyhead Atherinomorus lacuno Unkown South China Sea silverside sus Indian anchovy Stolephorus indicus Overexploited East China Sea Apogonichthys Indian perch Unkown East China Sea lineatus Japanese bonnet Phalium bisulcatum Unkown East China Sea Japanese scad Decapterus maruadsi Overexploited South China Sea Japanese silver Gerres equulus Unkown South China Sea 27

biddy Japanese stone crab Javelin goby Kammal thryssa Keeled mullet Kobi cuttlefish Largehead hairtail Largescale lizardfish Longtail silver biddy Macclelland's codlet Mackerel scad Mantis shrimp Mimika bobtail squid Moonfish Offshore Ponyfish Orangefin ponyfish Oriental flying gurnard Osbeck's grenadier anchovy Pacific mackerel Pacific sandlance Pinkgray goby Red eelgoby Robust tonguefish Sand crab Scaly hairfin anchovy Shortheaded tonguesole Shortnose ponyfish Silver jewfish Skinnycheek lanternfish

Charybdis Japonica Synechogobius hasta Thrissa kammalensis Liza carinata Sepia kobiensis Hoyle Trichiurus lepturus

Unkown Unkown Unkown Unkown Unkown Overexploited

East China Sea East China Sea South China Sea South China Sea East China Sea South China Sea

Saurida brasiliensis

Overexploited

East China Sea

Gerres longirostris

Unkown

South China Sea

Unkown

East China Sea

Unkown

East China Sea

Unkown

East China Sea

Euprymna morsei

Unkown

East China Sea

Mene maculata Equulites rivulatus Photopectoralis bindus Dactylopterus orientalis

Unkown Unkown

South China Sea East and South China Seas

Unkown

South China Sea

Unkown

East China Sea

Coilia mystus

Unkown

East China Sea

Scomber japonicus Ammodytes personatus Amblychaeturichthys hexanema Caragobius rubristria tus Cynoglossus robustus Ovalipes punctatus

Unkown

South China Sea

Unkown

East China Sea

Unkown

East China Sea

Unkown

East China Sea

Unkown Unkown

East China Sea East China Sea

Setiponna taty

Unkown

East China Sea

Cynoglossus kopsii

Unkown

East China Sea

Unkown

South China Sea

Overexploited

East and South China Seas

Unkown

East China Sea

Bregmaceros mcclella ndi Decapterus macasellus Oratosquilla oratoria

Leiognathus brevirostris Argyrosomus argentatus Benthosema pterotum

28

Slender lizardfish Small yellow croaker

Spotted velvetfish Striated frogfish

Saurida elongate Larimichthys polyactis Callionymus huguenin i Collichthys lucidus Apogonichthys carinatus Erisphex pottii Antennarius striatus

Swordtip squid

Loligo edulis

Toothpony Veined rapa whelk Wart perch Whipfin silver biddy White croaker Whitespotted conger

Gazza minuta Rapana venosa Psenopsis anomala

Unkown Unkown Moderately exploited Unkown Unkown Unkown

Gerres filamentosus

Unkown

South China Sea

Genyonemus lineatus

Unkown

East China Sea

Conger myriaster

Unkown

East China Sea

Spear dragonet Spinyhead croaker Spotfin cardinalfish

Overexploited

East China Sea

Unkown

East China Sea

Unkown

East China Sea

Unkown

East China Sea

Unkown

East China Sea East China Sea East China Sea

29

East and South China Seas South China Sea East China Sea East China Sea

Table S2. China’s potential in recycling fish processing wastes for feeds Potential fishmeal yield Potential fish oil yield Statistics (tons) (tons) * Base case 793,821 189,005 Meanǂ

652,557

155,371

648,340

154,367

139,442 278,971 1,049,655 624 970,845

33,200 66,422 249,918 148 231,153

901,487

214,640

898,381

213,900

131,570 591,750 1,273,511 588

31,326 140,893 162,324 140

Medianǂ Scenario 1

ǂ

Standard deviation Minimumǂ Maximumǂ Mean standard errorǂ Base case* Meanǂ Median

Scenario 2

ǂ ǂ

Standard deviation Minimumǂ Maximumǂ Mean standard errorǂ

Note: *Base case: modeling results without uncertainty analysis. ǂ Modeling results are calculated from 50,000 Monte Carlo simulations.

30

Table S3. Fishmeal and fish oil potential derived from processing wastes in China's finfish export sector (year 2011) Product

Group

Product types

Conversion factor*

Waste ratio*

Export (tons)ǂ

Fish, frozen, nei Sardines, sardinellas, brisling or sprats, frozen Mackerels nei, frozen Tilapias, frozen

fish

frozen whole

1.00

0.00

354939

0

fish

frozen whole

0.00

126926

0

fish fish

0.00 0.00

126452 107600

0 0

Fish live, nei

fish

0.00

72665

0

Herrings nei, frozen Skipjack tuna, frozen Croakers, frozen

fish fish fish

0.00 0.00 0.00

72492 40257 39975

0 0 0

Fish, fresh or chilled, nei

fish

frozen whole frozen whole live, fresh or chilled frozen whole frozen whole frozen whole live, fresh or chilled

0.00

27643

0

0.00

19799

0

0.00 0.00 0.00

17164 15375 11642

0 0 0

0.00

10539

0

0.00

9494

0

0.00

6577

0

0.00

6194

0

0.00

5638

0

0.00

5023

0

0.00

3496

0

0.00

3279

0

0.00

3049

0

0.00

2965

0

0.00

2649

0

0.00

2302

0

0.00

2019

0

0.00

2018

0

Miscellaneous pelagic fishes, nei, frozen Plaices, frozen, nei Hairtails, frozen Cods nei, frozen Octopus, live, fresh or chilled Fish waste, nei Yellowfin tuna, frozen, nei Caviar and caviar substitutes

fish

frozen whole

fish fish fish

fish

frozen whole frozen whole frozen whole live, fresh or chilled waste

fish

frozen whole

fish

caviar

fish

Eels and elvers live

fish

Bigeye tuna, frozen, nei Croakers, fresh or chilled Greenland halibut, frozen Pacific salmon, frozen, nei Fish for culture incl. ova, fingerlings etc. Tunas nei, frozen

fish

Carps live

fish

Albacore (=Longfin tuna), frozen, nei Livers, roes, milt, frozen

fish

live, fresh or chilled frozen whole live, fresh or chilled frozen whole

fish

frozen whole

fish

1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00

fish

fish

1.00 1.00 1.00

live, fresh or chilled frozen whole live, fresh or chilled

fish

frozen whole

fish

livers/roes

31

1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00

Waste (tons)

Sharks nei, frozen Eels, frozen Pomfrets, ocean breams, fresh or chilled Miscellaneous demersal fishes,nei, fresh or chilled Swordfish, frozen Flatfishes nei, frozen Livers, roes, milt, fresh or chilled, nei Common sole, frozen Cods, fresh or chilled, nei

fish fish

Ornamental fish nei

fish

Atlantic(Thunnus thynnus)and Pacific(Thunnus orientalis)bluefin tuna, frozen Toothfish (Dissostichus spp.), frozen

fish fish

live, fresh or chilled

fish fish

frozen whole frozen whole

fish

livers/roes

fish

frozen whole live, fresh or chilled live, fresh or chilled

fish

fish

1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00

frozen whole

0.00 0.00

1812 1755

0 0

0.00

1430

0

0.00

1029

0

0.00 0.00

912 905

0 0

0.00

870

0

0.00

853

0

0.00

734

0

0.00

571

0

0.00

249

0

0.00

223

0

0.00

142

0

0.00

114

0

0.00

84

0

0.00

27

0

0.00

25

0

0.00 0.00 0.00

24 13 12

0 0 0

0.00

5

0

0.00

5

0

0.00

1

0

0.00

0

0

0.00

0

0

0.00

0

0

1.00 fish

Saltwater fish nei, live

fish

Puffer, fresh or chilled

fish

Salmonoids, frozen

fish

Eels, fresh or chilled

fish

Atlantic salmon and Danube salmon, frozen Hake nei, frozen Trouts and chars, frozen Halibuts nei, frozen Flatfishes, fresh or chilled, nei Mackerels, nei, fresh or chilled Sardines, sardinellas, brisling or sprats, fresh or chilled Albacore (=Longfin tuna), fresh or chilled Bigeye tuna, fresh or chilled Common sole, fresh or chilled

frozen whole frozen whole live, fresh or chilled

frozen whole live, fresh or chilled live, fresh or chilled frozen whole live, fresh or chilled

fish

frozen whole

fish fish fish

frozen whole frozen whole frozen whole live, fresh or chilled live, fresh or chilled

fish fish fish fish fish fish

live, fresh or chilled

1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00

live, fresh or chilled live, fresh or chilled live, fresh or chilled

1.00 1.00 1.00

32

Haddock, fresh or chilled Haddock, frozen Halibuts, fresh or chilled, nei Herrings, fresh or chilled, nei Plaices, fresh or chilled, nei Saithe (=Pollock), fresh or chilled Saithe (=Pollock), frozen Salmonoids, fresh or chilled, nei Salmons, fresh or chilled, nei Sharks nei, fresh or chilled Skipjack tuna, fresh or chilled Sockeye salmon (red salmon)(Oncorhynchus nerka), frozen

fish fish fish fish fish fish fish fish fish fish fish fish

1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00

frozen whole

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

435

0

0.00

3

0

0.00

16

0

0.00

115

0

0.00 0.65 0.59

0 5940 864168

0 11048 1253044

0.00

12896

0

1.00

Tilapias, fresh or chilled

fish

Trouts and chars live

fish

Trouts and chars, fresh or chilled Tunas, fresh or chilled, nei Yellowfin tuna, fresh or chilled Herring, salted or in brine Anchovies, salted or in brine

live, fresh or chilled frozen whole live, fresh or chilled live, fresh or chilled live, fresh or chilled live, fresh or chilled frozen whole live, fresh or chilled live, fresh or chilled live, fresh or chilled live, fresh or chilled

fish fish fish fish fish

Herrings nei, smoked

fish

Miscellaneous demersal fishes, salted or in brine, nei

fish

Salmons, smoked

fish

Herring roes, cured Catfish fillets, frozen Fish fillets, frozen, nei Miscellaneous dried fish, whether or not salted, nei

fish fish fish fish

live, fresh or chilled live, fresh or chilled live, fresh or chilled live, fresh or chilled live, fresh or chilled dried/salted/s moked dried/salted/s moked dried/salted/s moked dried/salted/s moked dried/salted/s moked roes fillets fillets dried/salted/s moked

33

1.00 1.00 1.00 1.00 1.00 1.20 1.33 1.67 1.60 1.92 0.00 2.86 2.45 4.00

Fish fillets, dried, salted or in brine Fish fillets, fresh or chilled, nei Toothfish (Dissostichus spp.), fillets, frozen Toothfish (Dissostichus spp.), meat, frozen Fish minced nei, prepared or preserved Fish nei, prepared or preserved, not minced Fish minced nei, in airtight containers prepared or preserved Fish nei, smoked Fish nei, salted or in brine Fish meat, whether or not minced, frozen, nei Cods nei, salted or in brine Mackerel prepared or preserved, not minced, nei Tunas prepared or preserved, not minced, nei River eels, prepared or preserved, not minced, nei Sardines, sardinellas, brisling or sprats, prep. or pres., not minced, nei Salmon nei, not minced, prepared or preserved Herrings prepared or preserved, not minced, nei Miscellaneous freshwater fishes, prepared or preserved, not minced, nei Anchovies, prepared or preserved, not minced Atlantic salmon, not minced, prepared or preserved Cods nei, dried whether or not salted

fish

dried/salted/s moked

fish

fillets

fish

fillets

fish

fish meat

fish

fish minced

fish

prepared or preserved

fish

fish minced

4.00 2.45 2.45 1.94 1.44 1.44

0.59

39825

94280

0.59

3655

5283

0.59

183

265

0.00

116

0

0.00

131222

0

0.48

105597

72862

0.00

31912

0

0.00

2262

0

0.00

442

0

0.69

52442

70240

0.00

1152

0

0.49

64862

46135

0.48

52163

35992

0.63

35199

44990

0.30

12404

3991

0.35

4637

2467

0.38

1707

797

0.48

652

450

0.54

641

692

0.35

188

100

0.00

8365

0

1.44 fish fish

dried/salted/s moked dried/salted/s moked

fish

fish meat

fish

dried/salted/s moked

fish

prepared or preserved

fish fish fish

1.44 2.03

prepared or preserved

fish

prepared or preserved

fish

prepared or preserved

fish

prepared or preserved

fish

prepared or preserved

2.70 1.46

prepared or preserved

prepared or preserved

4.00 1.94

prepared or preserved

fish

1.61

1.07 1.52 1.22

1.44

fish

2.00 1.52

dried/salted/s moked

34

3.00

Tilapia fillets, frozen Tilapias prepared or preserved, not minced Livers, roes, milt, smoked, dried, salted or in brine Fish meals, nei Fish liver oils, nei Miscellaneous coastal fishes, salted or in brine, nei Fish heads, tail, maws etc., dried, salted, or in brine Freshwater fishes nei, dried, salted, or in brine Miscellaneous coastal fishes, dried, whether or not salted Miscellaneous pelagic fishes, salted or in brine, nei Fish body oils, nei Fish meal fit for human consumption, nei Shark fins, prepared or preserved Shark fins, dried, salted, etc.

fish fish fish

fillets prepared or preserved

2.70 2.03

dried/salted/s moked

fish fish

meal oil

fish

dried/salted/s moked

fish

dried/salted/s moked

fish

dried/salted/s moked

fish

dried/salted/s moked

fish

dried/salted/s moked

fish

oil

fish

meal

fish

fins

fish

fins

0.00 4.76 0.00

158112

269218

0.63

63379

80937

0.00

6862

0

0.00 0.00

441 386

0 0

0.00

1

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

0

0

0.00

22666

0

0.00

1890

0

0.00

146

0

0.00

343

0

1.39 0.00 1.50 4.00 1.39 0.00 0.00 0.00 0.00

*

0.63

Waste Sum (tons) Fishmeal potential (tons)

1,992,790 418,486

Fish oil potential (tons)

99,639

Note: Conversion factor (CF) is used to convert product weight to live weight (live weight = product weight * CF). Waste ratio: ratio of waste after processing. Refs: (58-60). ǂ Export data from ref (19).

35

Table S4. Uncertainty parameters for calculating recycling fish processing wastes for fishmeal and oil production Low High Most likely Assumed Uncertainty parameters value value value distribution ◊ Finfish processing yield rate 30% 70% 40% Triangular ǂ Crustaceans processing yield rate◊ 30% 50% 40% Triangular ǂ * Waste ratio 28% 68% 58% Triangular ǂ Market allocation† 50% 80% Uniform Note: ◊ Typical production yield for whole raw fish, from refs (31, 58, 61). *

Percentage of waste derived from whole fish = 1− fish processing yield rate – loss (assumed 2%) Percentage of fish processing waste destined for fishmeal and oil production. ǂ Triangular distribution has lower and upper limits and a midpoint value. †

36

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38