Chinese market responses to overexploitation of sharks and sea cucumbers

Biological Conservation 184 (2015) 163–173

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Review

Chinese market responses to overexploitation of sharks and sea cucumbers Hampus Eriksson a,b,⇑, Shelley Clarke c,d a

WorldFish, P.O. Box 500, Penang 10670, Malaysia Australian National Centre for Ocean Resources and Security (ANCORS), University of Wollongong, NSW 2522, Australia c Sasama Consulting, Shizuoka 428-0211, Japan d Areas Beyond National Jurisdiction Tuna Project, Western and Central Pacific Fisheries Commission, P.O. Box 2356, Kolonia, Pohnpei 96941, Federated States of Micronesia1 b

a r t i c l e

i n f o

Article history: Received 19 November 2014 Received in revised form 13 January 2015 Accepted 18 January 2015 Available online 12 February 2015 Keywords: Consumption Demand Fisheries Supply Sustainability Trade

a b s t r a c t Global exploitation of sharks and sea cucumbers to meet consumer demand in China is motivating a rising conservation concern. In order to analyze trends in resource exploitation and market dynamics, this paper reviews global production and trade data for these taxa. Sea cucumber capture production has plateaued, but overall production is still increasing because of rising aquaculture, limited public conservation concern and insufficient regulation of fishing and trade. Shark capture production has peaked and is declining, suggesting that one or more of these factors are constraining the shark fin trade. The trade networks for both commodities have been resilient to changing conditions (e.g. stock declines, closed fisheries, regulations, public opinion on conservation) and have become more widespread over the last 10 years. System resilience is evident in dynamic market attributes, such as developing new product forms and absorbing alternative target species, and presents substantial challenges for identifying conservation approaches. For shark fin, a government-led backlash against conspicuous consumption in China, combined with global conservation momentum, appears to have had some impact on traded volumes. Sea cucumbers do not enjoy the same level of attention in the global conservation discourse, despite seven species being endangered. For both taxa, the current regulatory environment is insufficient to safeguard resources and strengthened conservation strategies are required. Better resolution of trade data will improve the ability to evaluate trends and guide management and conservation. Ó 2015 Elsevier Ltd. All rights reserved.

Contents 1. 2. 3.

4.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Results and discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Global production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Sourcing network dynamics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Product substitutability. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Attitudes toward luxury and conservation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5. Regulatory environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

⇑ Corresponding author at: WorldFish, 11960 Bayan Lepas, Penang, Malaysia. Tel.: +61 (0) 2 4221 5506. 1

E-mail address: [email protected] (H. Eriksson). Present address.

http://dx.doi.org/10.1016/j.biocon.2015.01.018 0006-3207/Ó 2015 Elsevier Ltd. All rights reserved.

164 164 165 165 166 167 169 170 170 171 171

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1. Introduction Demand in China is a driving force for the exploitation and trade of endangered wildlife products (Fabinyi, 2012; GrahamRowe, 2011). Shark fin and bêche-de-mer (the dried body wall of sea cucumbers) are two of the most conspicuous products traded in China’s top-end market for dried seafood (Fig. 1) and both derive from taxa of mounting conservation concern (Clarke et al., 2013; Purcell et al., 2014a). Chinese merchants have engaged in international trade in these taxa for several hundred years leading to historical overexploitation in some areas (Payne, 2000; Schottenhammer, 2010; Schwerdtner Máñez and Ferse, 2010). With increased standards of living in China, particularly in the last two decades, the magnitude and extent of trade has rapidly expanded (Anderson et al., 2011; Clarke et al., 2006; Conand and Byrne, 1993), exacerbating depletion of low-productivity shark (Cortés, 2002) and sea cucumber (Uthicke et al., 2004) species worldwide. As a result, fishery closures for sea cucumbers due to overfishing have been recently documented in at least 24 countries (Purcell et al., 2013) and shark populations around the world are threatened by both targeted and incidental catches (Clarke et al., 2013; Dulvy et al., 2008). Although shark fin and sea cucumber may be consumed in fishing communities in some parts of the world (TRAFFIC, 1996; Purcell et al., 2013), their appeal as luxury items is mainly associated with Chinese consumers, most likely because of culturally rooted perceptions of class and health (Cheung and Chang, 2011; Clarke, 2004a; Fabinyi, 2012). Despite the similarities in history and cultural function, there are important distinctions between shark fin and sea cucumber product sourcing. In temperate regions, sea cucumbers are sometimes harvested using deep-water trawls, but most are collected by hand in shallow-water tropical multispecies fisheries (Eriksson et al., 2012a; Purcell et al., 2013; Toral-Granda et al., 2008). In addition, since the mid-2000s, a growing portion of the global sea cucumber supply has been derived from aquaculture (Eriksson et al., 2012b). In contrast, most shark fins are sourced from commercial fisheries, many of which are targeting pelagic tuna and billfishes, although artisanal fisheries catching coastal sharks undoubtedly also contribute (Gillett,

2011; Shotton, 1999; Clarke et al., 2015). These differences are also reflected in the types of trade networks that bring products to market as well as the level of fishery management. For sea cucumbers, small-scale landings are commonly consolidated through local and regional dried seafood entrepôts under little or no management (e. g. Eriksson et al., 2012a). In contrast, sharks are often landed or transported through major ports handling other fishes and are influenced by international governance regimes for tuna fisheries, which catch sharks incidentally (Fischer et al., 2012). China is now fully enmeshed in the global seafood trade through distant-water fishing (Mallory, 2013), sourcing of fish meal and aquaculture production for both domestic consumption and export (Hanson et al., 2011), and a thriving re-processing trade for fish caught and consumed far beyond its borders (Clarke, 2008). This system represents a complex globalized interaction of species and habitats, and a worldwide network of seafood production, processing and marketing. Factors that shape the dynamics of this global production and trade are important to consider when evaluating the pressure on resources and formulating effective management strategies. One way to better understand this complex system is to review the major data sources for global production and trade statistics (e.g. Clarke, 2004a). In this review, we use these types of data for shark fin and sea cucumber to identify whether there are important signals for conservation. We examine five factors potentially influencing a hypothesized Chinese market: (i) global production, (ii) sourcing network dynamics, (iii) product substitutability, (iv) attitudes toward luxury and conservation, and (v) regulatory environment. 2. Methods The primary source of data for analysis of trade patterns is national import and export statistics. Empirically evaluating shark fin and sea cucumber trading networks is thus necessarily limited to the coarse scale defined by national customs data. Further limitations arise due to the lack of unique commodity codes for shark fin and sea cucumber products in many countries prior to 2012, and by under-reporting in countries that use such codes but impose tariffs (or under-report for other reasons). While China is

Fig. 1. Shark and sea cucumber supply chains. (A) Fisher’s sea cucumber catch (Actinopyga miliaris, Bohadschia subrubra, B. vitiensis, Holothuria fuscogilva, H. isuga, H. lessoni, Thelenota ananas, T. anax) in Zanzibar, Tanzania. (B) Preparation of bêche-de-mer (dried sea cucumber) smoked over mangrove wood in Zanzibar. (C) Sharks (Carcharhinus spp. and Alopius spp.) caught by artisanal vessels landing at a market in Indonesia. (D) Shark fins drying in Zanzibar. (E) Shop window displaying various species of bêche-demer and shark fins in Hong Kong (photos A, B, D, E Hampus Eriksson, C Doug Beare).

H. Eriksson, S. Clarke / Biological Conservation 184 (2015) 163–173

clearly the destination for a large proportion of shark fin and sea cucumber products, in a number of aspects such as combining frozen shark fins and shark meat under a single commodity code and documented underreporting of imported quantities of dried shark fins, its customs statistics do not provide a reliable indicator of traded quantities (Clarke, 2004a,b). For these reasons, this analysis relies heavily on trade statistics from Hong Kong, a duty-free dried seafood entrepôt that has used detailed commodity codes since 1998. Global production figures were sourced from the Food and Agriculture Organization of the United Nations (FAO) capture and aquaculture production statistics database, FishStatJ (FAO, 2013b). In the case of shark fin, all trade data were compiled from unpublished trade statistics maintained by the Hong Kong Census and Statistics Department (HKCSD). Despite their relative lack of bias, Hong Kong statistics must be adjusted to account for various states of shark fin processing. When analyzing these statistics processed fins must be removed from the analysis (or else the same fins may be double counted in unprocessed and processed forms) and frozen fin weights must be reduced (here by an assumed factor of four) to account for water content (Clarke, 2004a). Global shark production figures are assumed to be represented by chondrichthyan capture production, since many sharks have historically been, and still are, reported in unidentified chondrichthyan categories. Furthermore, in this analysis all traded products described as ‘‘shark” are understood to be derived from chondrichthyan fishes whether they be sharks, skates, rays or chimaeras. Although most are expected to be derived from true sharks, the fins of sawfishes (Pristidae), guitarfishes (Rhinobatidae), wedgefishes (Rhynchobatidae) and chimaeras (Chimaeriformes) are also utilized. When evaluating sea cucumber production and trade data, adjustments may be necessary, as weights vary considerably between the recently increasing proportions of modern non-dry product forms (e.g. blanched, salted and/or frozen; see Purcell et al., 2014b) and the traditional dry form. Total Hong Kong sea cucumber import volumes for 1986–1995 were taken from the literature (Conand, 1993; Ferdouse, 1999; Jaquemet and Conand, 1999) and compiled from HKCSD for 1996–2011. In January 2012, HKCSD implemented new codes which split the former 0307-9930 ‘‘Beche-de-mer, dried, salted or in brine” into four different codes, one of which is frozen (0308-1910; HKCSD, 2012). It is believed that until 2012 the increasing traded proportion of frozen sea cucumbers have been reported under a general frozen seafood code (0307-9940), so an adjustment to historical Hong Kong import data under the 9930 code used for this analysis does not appear necessary. FAO production data for Apostichopus japonicus is reported in fresh weight for both capture and aquaculture production, and requires adjustment using a factor of 0.04 (Purcell et al., 2013; Skewes et al., 2004). The proportions of frozen sea cucumber products imported by Hong Kong in 2012 under the new commodity code 1910 reported by Conand et al. (2014) were applied to historical FAO production data as a best estimate of product form composition for countries appearing in FAO statistics. For example, Hong Kong imports in 2012 from Canada consisted of 90% frozen products. The corresponding proportions were 37% for Mexico, 58% for the United States, and 100% for Honduras and Iceland. For Canada, Iceland and the United States the species in question (Cucumaria frondosa, Cucumaria japonica, Parastichopus californicus, Parastichopus parvimensis) have relatively thin bodywalls, so these proportions of total production were adjusted down in weight with an assumed factor of 0.1 (frozen to dry weight). For Mexico and Honduras, where a mixed species composition may be expected including species with thicker bodywalls (e.g. Isostichopus badionotus), an assumed factor of 0.2 was applied to proportion of frozen product. For all other countries the FAO production data were assumed to be dry product forms, but this is likely a positive bias – production may

165

include an unknown proportion of salted or frozen products that weigh up to ten times more than dry product forms. Pearson’s correlation coefficient r was calculated for each country’s annual shark fin and sea cucumber production data in 1996– 2011 as an indicator of trends in exports over time. The coefficient of variation was also calculated to add an indication of variability to the correlation coefficient. An analysis using Gini concentration indices was undertaken to explore how the degree of dispersion (or inequality) has changed between countries over time in response to development of trading and logistical networks. Africa was chosen as the case study region for this analysis because of the role Chinese demand is playing there in driving resource development and trade relations (Alden, 2005). The index used the generalized formula:

G¼1

37 X pj f ðr j Þ j¼1

where j = represents the 37 African countries from which Hong Kong imported shark fins from 1998 to 2011 ranked in descending order of proportion of supply, pj is the cumulative proportion of trade represented by countries 1 to j, and f(rj) is the cumulative expected proportion of trade represented by countries 1 to j if each country is assumed to have an equal share in the supply (i.e. 1/37th). The products of pj and f(rj) were summed over j countries for each year from 1998 to 2011 to give an annual measure of inequality (G) such that 0 represents perfect equality and 1 represents perfect inequality (Rodrigue, 2013). 3. Results and discussion 3.1. Global production Given the striking economic growth in China over the past two decades our initial hypothesis is that luxury seafoods such as shark fin and sea cucumber would exhibit similar trends. In fact, global shark and sea cucumber production trends show divergent trajectories, and the traded quantities in Hong Kong relative to production also differ (Fig. 2). Adjusted Hong Kong shark fin imports rose at a faster rate than global chondrichthyan capture production in 1998–2003, but then fluctuated in parallel and declined at the same rate as chondrichthyan capture production through 2011 (Fig. 2a). Further comparisons between chondrichthyan and total fish capture production quantities reveal that chondrichthyan production fell after 2003 even as total fish production remained relatively constant. This emphasizes that a factor particular to chondrichthyans, perhaps their vulnerability to overfishing (Arrizabalaga et al., 2011; Cortés et al., 2010; Costello et al., 2012), is responsible for the decline in their capture production, rather than a factor affecting all fisheries, such as fishing effort. The decline in the shark fin trade since 2003 is contrary to expectations that there would have been an increase in demand with the continued expansion of the Chinese economy. The pattern of trade decline closely matches the pattern in chondrichthyan capture production and thus suggests a strong link between the quantity harvested and the quantity traded. However, an alternative explanation for the declining quantities of shark fin traded through Hong Kong since 2003 could be trade liberalization in China. In particular, China’s accession to the World Trade Organization in December 2001 and concomitant trade regulation changes have been identified by some analysts as a possible cause of changes in Hong Kong-China trade patterns (Cheung and Chang, 2011). Despite this potential influence on the cross-border trade, the flow of shark fin into Hong Kong does not appear to have responded directly to this particular stimulus. Hong Kong’s shark fin imports increased in both 2002 and 2003 relative to 2001,

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1000

A Shark fins

10

30

B Sea cucumbers

8

600

6

4

400

200

FAO Total capture production (10 5 tonnes) FAO Chondrichtyan capture production (10 3 tonnes) Hong Kong shark fin imports (right axis)

1950

1960

1970

1980

1990

2000

2

2010

Year

Weight (103 t)

800

Weight (103 t)

Weight (103 t / 105 t)

FAO Sea cucumber capture production

25

FAO Sea cucumber aquaculture production Hong Kong sea cucumber imports

20 15 10 5

1950

1960

1970

1980

1990

2000

2010

Year

Fig. 2. Production and trade with shark fin and sea cucumber. (A) Shark fins. Comparison of total global capture production and total global chondrichthyan capture production in 1950–2011 (data: FAO, 2013b) with imports of unprocessed shark fins by Hong Kong (dried and frozen (adjusted for water content)) in 1998–2011 (data: HKCSD). (B) Sea cucumbers. Comparison of global capture and aquaculture production (data: FAO, 2013b) and Hong Kong imports (data: Conand, 1993; Ferdouse, 1999; Jaquemet and Conand, 1999 for 1986–1995 and HKCSD for 1996–2011). Missing data on Hong Kong imports in 1989–1991 is indicated with a thin dotted line.

and also showed year-on-year increases in 2007 and 2011, two years in which global chondrichthyan capture production figures also showed sharp increases (Fig. 2a). Global production of sea cucumber increased rapidly in the mid-1980s and, unlike the trends for shark fin, production has not experienced the same drop in production (Fig. 2b). Capture production has plateaued but overall production is bolstered by aquaculture, which contributed <1% of production in 2002 but 25% in 2011 (Fig. 2b). Sea cucumber aquaculture production consists mostly of A. japonicus, (94% in 2011) predominantly cultured in China. Technology transfer to tropical species Holothuria scabra and Holothuria lessoni has been partially successful (Eriksson et al., 2012b), but tropical species still played a small role (6%) in total aquaculture production in 2011. Sea cucumber imports into Hong Kong have remained relatively stable since 1986 and have not mirrored the increase in global production (Fig. 2b). For example, in 1988, 64% of global capture production was imported into Hong Kong, but by 2011 this had fallen to 33%. Shifts in traded product forms with concomitant reporting issues and weight biases in data could possibly influence the trend. For example, it is plausible that frozen sea cucumber imports have been reported under a general frozen seafood code in the absence of a distinct code, which would underestimate volumes imported to Hong Kong (see Section 2. Methods). The pattern is likely also influenced by altered trade routes directly into China. Re-export data from Hong Kong indicate that since 2004, Vietnam has replaced China as the primary recipient for products reexported from Hong Kong (To and Shea, 2012; Fig. 3), however, it

7

Weight (103 t)

6

Total Hong Kong import Hong Kong re-export to China Hong Kong re-export to Vietnam

5 4 3 2 1 0 2000

2005

2010

Year Fig. 3. Total Hong Kong imports and shifting trends in re-export of sea cucumber to China and Vietnam (data: HKCSD).

is expected that re-exported products are still destined for consumers in China. The altered trade route could potentially be a response to circumvent new tariffs that made direct importation unattractive for traders. Vietnam has become a regional entrepôt for wildlife trafficking (Ngoc and Wyatt, 2013) and it is possible that sea cucumbers may be caught up in this dynamic. It is believed that products still flow through traders in Hong Kong (i.e. rather than being shipped directly to Vietnam) for the sake of maintaining long-established trading networks. From this analysis we conclude that there are no clear similarities between global production quantities and the China trade as represented by Hong Kong statistics and global production data. While the quantity of shark fins in trade has declined 20% since 2003 in parallel with capture production figures, sea cucumber trade has been steady and supported by increased aquaculture production. Despite adjustments, it cannot be ruled out that the sea cucumber data are overestimating global production quantities due to the progressive increase in new non-dry sea cucumber product forms which are not recorded in distinct categories. 3.2. Sourcing network dynamics We next examined sourcing networks for both products for evidence of shifts or diversification. Such changes might be expected as a means of maintaining supplies in the face of local or regional overfishing. The top-10 suppliers of shark fin and the top-10 suppliers of sea cucumber for the Hong Kong market account for 68% and 76% of the total average annual production, respectively. Notably, four locations are on the list of top-10 suppliers of both commodities; namely, Indonesia, Japan, Singapore and Yemen (Fig. 4a and b). In the shark fin trade, it would be expected that sea-based collection networks channeling shark fins through major centres of tuna fishing (e.g. Taiwan, Japan, Spain) would show stable patterns over time, as would long-standing regional collection centres for dried fins, such as the United Arab Emirates and Singapore (Clarke and Mosqueira, 2002; Gilman et al., 2007). This expectation is confirmed in the Hong Kong trade data, with relatively consistent correlation coefficients and low variance in imported quantities from these key trading centres over time (Fig. 4a). In contrast to this pattern, the four largest sea cucumber–producing nations during 1996–2011 (i.e. Indonesia, Philippines, Papua New Guinea and Fiji) showed negative or near-level correlation coefficients (Fig. 4b), indicating that national production peaks have been reached and supplies are diminishing. Combined, the

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A Shark fins

B Sea cucumbers Morocco Cuba Mauritania Russian Djibouti Vanuatu Haiti FSM & Palau Vietnam S. Korea Kenya South Africa U A Emirates Mainland China Mauritius Egypt Seychelles Mozambique Mexico Peru Maldives Kiribati Canada Tonga Thailand Malaysia Sri Lanka Taiwan Tanzania Australia Yemen Solomon Island USA Singapore Madagascar Japan Fiji Papua New Guinea Philippines Indonesia

El Salvador Morocco Madagascar Trini Tobago New Zealand Venezuela Thailand Togo Canada Guyana Chile Philippines Australia Pakistan Uruguay Korea Sri Lanka Oman Guinea Mauritania Argentina Fiji Panama South Africa Mainland China Senegal Ecuador Peru Costa Rica USA India Yemen Brazil Japan Mexico Singapore U A Emirates Indonesia Taiwan Spain 0

400

800

Average annual export (t)

-0.5

0

0.5

Pearson’s r

0.5

1.0

Coefficient of variance

0

400

800

Average annual export (t)

-0.5 0 0.5

0.5 1.5 2.5

Pearson’s r

Coefficient of variance

Fig. 4. Top-40 shark fin (A) and sea cucumber (B) countries supplying Hong Kong listed based on quantity of average annual import by Hong Kong, 1996–2011. Pearson’s r is the correlation coefficient ranging from 1 to 1 as an indicator of trend in export over time. The coefficient of variation is the standard deviation divided by the mean, with a higher value indicating higher export variability (data: HKCSD).

Hong Kong sea cucumber imports from these countries declined by 56%, from ca. 3400 tonnes to ca. 1500 tonnes. Overall Hong Kong imports have not mirrored this downward trend because sea cucumber products were sourced from 48 additional countries in 2011 compared to 1996 (Eriksson et al., Unpublished results). Volumes from individual countries and actual routes in trade networks can be obscured by consolidation centres, such as those in East Africa (Eriksson et al., 2012a) or large resource-rich countries like the Philippines, which camouflage local depletions. In contrast, small sea cucumber–producing countries that do not use such consolidation centres, but which experience boom–bust–ban cycles, e. g. Tonga (Friedman et al., 2011), are more likely to show extreme variation in exports and thus perhaps a less clear trend in production (Fig. 4b). In fact, many of the smaller sea cucumber producers show occasional export peaks with high variability—higher than smaller shark fin-producing countries do. Businesses built and operated by expatriate Chinese since the great diaspora of the 19th century have shaped international trading networks in many different sectors. Regardless of changes in communication and transportation technologies, and the modernization of international banking, some sources claim that many Chinese businesses, including those in the shark fin trade, are still defined primarily on the basis of long-standing family or ethnic networks (Cheung and Chang, 2011). Other researchers have found that trust, or a similar kind of social cohesion arising from close association and a history of positive interactions regardless of

kinship, is fundamental (Fong and Anderson, 2000; Menkhoff, 1994). Despite their hierarchical nature these networks are dynamic in that although the dominant shark fin suppliers appear to maintain their role in the trading network, possibly through a portfolio effect (Anderson et al., 2013), sourcing patterns can change rapidly at the distal end of the scale. Applying the Gini concentration index to 37 African countries producing shark fins for the Hong Kong market revealed a significant decrease in the index (slope = 0.006, p = 0.004) signifying a clear trend of decreasing inequality (increasing entropy) in the sourcing network in 1998– 2011 (Fig. 5). This suggests that the influence of past major regional suppliers Guinea, Mauritania, Senegal and South Africa is lessening, while the influence of other countries, notably Gambia, Morocco and Namibia, is strengthening. Our analysis suggests that trade networks for both commodities have become more widespread overtime. In some cases, ‘‘boom– bust–ban” cycles in smaller production countries are mirrored in trade statistics while in other cases regional entrepôts obscure these signals. 3.3. Product substitutability Market theory suggests scarcity can lead to product substitution (Stiff et al., 1975). Having identified the potential for scarcity in the preceding supply-side analyzes, we next examine the evidence for substitution in Chinese dried seafoods.

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0.80

14

0.78

0.76

0.74

0.72 1998

2000

2002

2004

2006

2008

2010

Year Fig. 5. Annual Gini concentration indices for adjusted shark fin imports by Hong Kong calculated for 37 African countries, 1998–2011. The line represents a linear model (slope = 0.006, r2 = 0.505, p = 0.004) showing decreasing inequality (increasing entropy) in the sourcing network. (data: HKCSD).

The popularity of shark fin and sea cucumber products is thought to be linked to a variety of cultural factors, including a belief in their medicinal (or tonic) properties, traditional use at wedding banquets and other celebrations and rites, and as a symbol of social and economic status (Clarke et al., 2007; Fabinyi, 2012; Fabinyi and Liu, 2014). While these influences would seem to combine to entrench usage of the products in Chinese society, there are potential substitutes in each case. For example, there are a number of products that are believed to provide similar healthstrengthening benefits, including (among other things) seahorse and ginseng. While use of shark fin and sea cucumber at weddings and banquets remains the norm, it was reported as of 2013 that both bird’s nest and fish maw soups have been gaining in popularity, and those consumers wishing to purchase premium seafood as luxury items can turn to abalone, lobster and scallops as alternatives (Fabinyi and Liu, 2014; Rabobank, 2012; Wang, 2013a). In addition to this substitutability between products within the same set of culturally based preference attributes, there is also substitutability among shark fin and sea cucumber products themselves. This can occur in two ways: either species can be swapped as supplies wax and wane, or artificial products can be substituted or mixed. In the case of artificial shark fin, greater use could ease pressure on depleted shark resources, but some consumers are expected to continue to demand real shark fin for cultural, social or health reasons. Specialist shark fin traders are able to make minute distinctions based on the length, thickness and texture of the ceratotrichia produced, but substitution between species can be easily accomplished at the retail level since there is often no species information provided at the point of sale (S. Clarke, pers. obs.). In contrast, sea cucumber dealers and consumers are easily able to distinguish species, and regional consumer preferences are well documented (Akamine, 2009, 2012). Furthermore, unlike shark fins (at least at present), some species of sea cucumber can be cultured and thus hold the potential to ameliorate unsustainable harvesting of wild populations. However, the rapidly burgeoning aquaculture of A. japonicus in China, the ‘spiky and bite-sized’ Japanese sea cucumber favoured in Cantonese cuisine, will only serve a portion of the market, and some consumers are expected to continue to prefer wild and foreign-produced sea cucumber due to concerns about contamination in local production and a desire for exclusivity (Fabinyi and Liu, 2014; SeafoodSource, 2013; Xu et al., 2012). To examine the potential for substitution, as well as the influence of resource depletion on the species composition in trade, global catch records for two species of sharks commonly

Proportion of total production (%)

Gini concentration index

16

12

Blue shark Mako shark

10 8 6 4 2 0 1998

2000

2002

2004

2006

2008

2010

Year Fig. 6. Proportion of total chondrichthyan capture production comprising blue shark (Prionace glauca) and mako sharks (Isurus spp.), showing the significantly greater rate of increase in the proportion of blue shark in catches during 1998–2011 (data: FAO, 2013b).

used in the shark fin trade were examined. A previous study found that two of the most distinctive and common species, blue (Prionace glauca) and mako (Isurus spp.) sharks, comprised 17.3% (confidence interval (CI) 15.5–19.1%) and 2.7% (CI 2.3–3.1%) of the Hong Kong trade in 2000, respectively (Clarke et al., 2006). Although both species are commonly caught in temperate tuna longline fisheries, the blue shark is one of the most productive pelagic sharks, whereas makos are some of the least productive (Cortés et al., 2010). It might thus be expected that the differences in their ability to respond to fishing pressure would lead to contrasting trends in the proportions of the total chondrichthyan catch comprising these two species. According to FAO capture production data for 1998– 2011, blue sharks’ proportion of total chondrichthyan catches grew from 4% to 14% due to a steady increase in reported catches of blue sharks (Fig. 6). Over the same period, the proportion of makos similarly rose from 0.5% to 1.5%. A significantly higher annual rate of increase in blue catches (7.5%, from 33.5 to 104.7 tonnes) was found in comparison to makos (5.5%; from 5.7 to 11.5 tonnes), using exponential models with r2 values of 0.85 and 0.80, respectively, and an ANCOVA contrasts test (p < 0.001). It thus appears that the relative abundance of mako sharks, while equally distinctive and more valuable and therefore perhaps more likely to be reported at the species level, is falling in comparison to a more productive species. Substitution by low-value species as high-value species are depleted is a well-documented phenomenon in sea cucumber fisheries (e.g. Purcell et al., 2013). The process can be illustrated by catch patterns in Australia’s Great Barrier Reef Marine Park (GBRMP): when harvests for high-value species declined, effort was transferred to a range of less valuable species (Roelofs, 2004). To increase the value of these low-to-medium-value species, processing improvements were made, such as individual quick-frozen (IQF) techniques to supply Chinese food service areas and restaurants, and vacuum-packed products with preparation directions and recipes on the pack destined for supermarkets (Purcell et al., 2014b; Tasmanian Seafoods Pty Ltd, 2014). The entrepreneurial skill in the processing companies, combined with flexibility in the market to accommodate new products, may have served to dampen signals of unsustainable exploitation of the sea cucumber resource as a whole, even in a highly managed area like the GBRMP (Eriksson and Byrne, 2013).

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A critical point to make in the context of substitutability is that the trend toward targeting lower-value species subsidizes the continued catch of rare, high-value species which would otherwise not be profitable to harvest—this opportunistic exploitation has been dubbed a pathway to extinction (Branch et al., 2013). Institutions are usually poorly equipped to limit such expansion. For example, the fishery and customs officers in the Indian Ocean often cannot identify live sea cucumbers and their products at a species level, so species-specific regulations or a short list of permissible species are impractical management strategies without training (FAO, 2013a). The modern broadening of product ranges for sea cucumber beyond the traditional dried form may facilitate new and unforeseen exploitation. With the wave of contemporary depletions sweeping across the tropical world, prices for lower-value species are rising, drawing attention to the potential for harvesting species that have previously not been profitable to harvest in some fisheries, e.g. Bohadschia argus, Bohadschia vitiensis and Stichopus chloronotus in Australia’s GBRMP (H. Eriksson, pers. obs.). In summary, for both sea cucumber and shark fin we found evidence of apparent market shifts either to species that are more resilient to exploitation or that have as yet remained under-utilized. These shifts can maintain an appearance of stability in markets and serve to camouflage overexploitation. 3.4. Attitudes toward luxury and conservation Recent media reports have suggested that changing attitudes toward luxury and growing conservation awareness among Chinese consumers have been responsible for a downturn in the luxury seafood market. Our fourth analysis critically examines the evidence, particularly in terms of shark fin, for the effects of these social forces. China’s to-get-rich-is-glorious awakening in the 1980s sparked the rapid expansion of the shark fin and sea cucumber trade (Fig. 2), and part of this original desire to enjoy the fruits of prosperity is still a major factor guiding consumer sentiment in China today (Gerth, 2010). Seafood is strongly associated with consumer expectations in preparing business and high-end banquets, as seafood products are expensive and associated with high social stature (Fabinyi and Liu, 2014). With increasing affluence, however, has come increasing concern about corruption and, in particular, a backlash against government officials seen to be enjoying a luxury lifestyle at public expense. Dried seafood has been caught up in this dynamic, and is also subject to the influences of international conservation campaigns and overarching trends in supplies driven by the exploitation patterns described above. Some international environmental organizations have reported a precipitous (70%) decline in shark fin imports into Hong Kong in 2012 and attributed this to conservation concerns (Tsui, 2013). While a decline of ca. 50% is supported by the official trade statistics for shark fin products per se (Table 1), there are several factors

other than conservation concerns that may have complementary or much larger impacts on these trade figures. First, the influence of the worldwide change in customs commodity codes for shark fin that took effect in 2012 cannot be dismissed. Although this change has led to the implementation of shark fin-specific commodity codes in countries around the world for the first time, its effect on the Hong Kong statistics has resulted in frozen shark fin being reported as frozen shark meat (FAO, 2014). Using this information to recalculate trade volumes for 2012 shows that imports have dropped by only 29% from the 2011 level and only 22% from the average of 2008–2010. Second, the observed decrease in trade volumes in 2012 may have been a result of the Chinese government’s ongoing campaign against conspicuous consumption. This campaign, which appears to be aimed both at stamping out corruption by government officials, as well as preserving social harmony in general, is reportedly affecting a wide range of luxury seafood product sales (Wang, 2013a,b). As the campaign began several years ago, it would not necessarily explain a sudden decline in 2012, but it could help explain a general dampening of trade. Third, recent media coverage of incidents of artificial shark fin being marketed as real shark fin has reportedly heightened public concerns about false marketing and resulted in a decrease in consumption (Fabinyi and Liu, 2014). Last, it cannot be ruled out that diminishing supplies of shark fin (e.g. in line with the continuing decline in chondrichthyan capture production reported to FAO, see Fig. 2a) may also serve to depress trade figures. Although it is difficult to confirm the role of each of these potential explanations in the observed trends, it is likely that several of them have combined to influence the Hong Kong trade figures. Therefore, on the basis of existing evidence, it cannot validly be concluded that the decrease in shark fin imports into Hong Kong in 2012 was due to rising conservation concerns per se. In addition to better understanding what factors are shaping the trade, it will be important to formulate a new methodology for tracking trade quantities given the revised commodity coding system implemented in 2012 by Hong Kong as well as by other major shark fin–trading countries. When attempting to identify trends in sea cucumber consumption and conservation, it is important to recognize the influence of the diverse Chinese cuisines and the associated broad range of species and product quality on offer, which cater to several geographical regions and levels of society (Akamine, 2009, 2012). If the only reason for declining trends in shark fin consumption was the crackdown on official banquets and lavish consumption among Chinese officials, then sea cucumber species associated with these banquets would also be expected to mirror that trend. Indeed, there are indications that consumption of sea cucumber at banquets in Beijing has also experienced a decline for this reason (Wang, 2013a). However, on the contrary, Fabinyi and Liu (2014) indicate that sea cucumber is increasingly consumed at banquets in China

Table 1 Imports of dried and frozen shark fins into Hong Kong, 2008–2012 (data: Hong Kong Census and Statistics Department). Product category (code)

Dried shark fins with cartilage (0305-5950 until January 2012, then 0305-7111) Adjusted frozen shark fins with cartilage (0305-5960 until January 2012, then 0305-7112) Shark fins NESOIa (0305-7190)b Total adjusted shark fins with cartilage Frozen shark meat (0303-7500 until January 2012, then 0303-8100)c Sum of total adjusted shark fins with cartilage and adjusted frozen shark meat a b c

Not elsewhere specified or indicated. Code implemented in 2012. No data for 2008–2011. Weight adjusted with a factor of four to account for water content (see Section 2. Methods).

Amount per year (t) 2008

2009

2010

2011

2012

4131 1405 – 5536 0 5536

4328 1231 – 5559 0 5559

4522 1237 – 5759 0 5759

4907 1268 – 6175 0 6175

3177 47 0 3164 4934 4398

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and the FAO statistics do not suggest any dampening effect on global production (Fig. 2b). The larger impact of anti-corruption actions on total trade is difficult to discern for the reasons given above and it would not be expected that the same level of public attention would accompany any such trends, as sea cucumbers are not as high as sharks on the agenda of conservation organisations. Considering that there is limited information available on sea cucumber consumption, the global production trend is increasing, and a large proportion of the consumption takes place outside of formal banquets, a realistic interpretation of the situation is that total consumption of sea cucumber in China is at least stable or more likely following the global production increase. We conclude that social forces are acting differently on shark fin and sea cucumber trade. While several factors appear to be jointly dampening trade and consumption of shark fins, there is little evidence that conservation concerns or lifestyle changes are impacting on trade and consumption of sea cucumbers. 3.5. Regulatory environment One action in response to overexploitation of marine resources is to adopt fishery management and trade regulations. As some regulations that apply to sharks and sea cucumbers have been in place for several years, this analysis explores whether there is any evidence for regulatory constraints on trade. The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) has long-standing trade controls for basking shark (Cetorhinus maximus), whale shark (Rhincodon typus), great white shark (Carcharodon carcharias) and the sawfishes (Pristidae), as well as more recently implemented controls for oceanic whitetip (Carcharhinus longimanus), scalloped hammerhead (Sphyrna lewini and look-alikes great (Sphyrna mokarran) and smooth (Sphyrna zygaena) hammerheads), porbeagle (Lamna nasus) sharks, and the manta rays (Manta spp.). The only sea cucumber currently listed in CITES is Isostichopus fuscus (brown sea cucumber), which was listed by Ecuador on Appendix III, meaning that export from Ecuador requires an Ecuadorian export permit (ToralGranda et al., 2008). This relatively limited use of international trade restrictions for sea cucumbers does not reflect the precarious state of global sea cucumber stocks, exemplified by seven species being listed on the International Union for Conservation of Nature (IUCN) Red List as endangered, and nine species listed as vulnerable (Purcell et al., 2014a). The disproportionate conservation attention and research effort can at least partially be explained by the public’s embrace of the emblematic status of sharks versus the uncharismatic nature of sea cucumbers (McClenachan et al., 2012). Another form of regulation and management specific to sharks is controls on finning. Between 2004 and 2008, all of the tuna regional fishery management organizations (RFMOs) implemented requirements that the weight of shark fins on board fishing vessels up until the point of landing can be no more than 5% the weight of the shark carcasses on board. Nevertheless, there are several reasons why the effects of finning controls may not be readily apparent. First, finning controls generally do not prevent use of shark fins; they only govern whether the fins are separated and the carcass disposed of at sea. Second, enforcement of finning controls is lacking in many cases. For example, a recent analysis of observer data from the Western and Central Pacific Fisheries Commission (WCPFC) suggests that although finning controls have been in place since 2008, the proportion of sharks finned is still 20–40% (Fig. 7; Clarke, 2013). A final form of regulation that may have an influence on the quantity of shark fins being traded is no-retention or no-possession measures. In recent years, several countries have implemented national bans on the retention of sharks by commercial fisheries. These self-described shark ‘sanctuaries’ (Eilperin, 2012), if robustly

100

Proportion finned (%)

170

Purse seine Longline

80 60 40 20 0 2005

2006

2007

2008

2009

2010

2011

Year Fig. 7. Proportion of sharks finned in WCPFC longline and purse seine fisheries based on observer data, 2005–2011. (Source: Clarke, 2013).

enforced, would be expected to reduce the amount of shark products entering trade, but would not necessarily result in a sufficient reduction in shark mortality rates (i.e. some proportion of sharks will not survive their encounter with the fishery even if they are not retained). Similar no-retention measures, which prohibit retaining any part or whole carcass of the designated shark species, have been adopted by most of the tuna RFMOs for some species shown to be under threat from fishing pressure (Clarke, 2013; WCPFC, 2014). In addition to these shark-oriented fisheries regulations, a number of state jurisdictions in the United States of America have adopted bans on the possession of shark fins. The proponents of these bans believe that they will decrease mortality rates for sharks, but there may be issues to overcome regarding banning trade in shark fins which are otherwise legally obtained (Guilford, 2013). A range of regulatory measures for management of sea cucumber fisheries at the national level has been recommended by Purcell (2010), including size limits, gear restrictions, catch quotas and licensing, temporal closures and area-based measures. While the reasons why certain measures are implemented may reflect fishery types or institutional design, they do not appear to be sufficient to limit overfishing. For example, fisheries in 10 out of 14 Indian Ocean countries are considered overfished or depleted (FAO, 2013a). In addition, in most fisheries, the capacity to monitor and enforce rules is insufficient (Purcell et al., 2013). This limitation is coupled with the dire economic circumstances that confront fishers in the tropics, which cause them to respond to declines in ways that expand and reinforce unsustainable rates of harvest (Cinner, 2012; Eriksson et al., 2012a). Encouragingly, the past decade has seen an increase in research and management attention to this fishery in recognition of its importance as a source of income in poor communities. Sea cucumber fisheries now also have a high priority on the regional fisheries policy agenda in the Pacific, predominantly due to the precarious state of stocks in the region and in recognition of their importance for livelihood among coastal communities (HoF, 2013; IUCN, 2014). It is clear that the expansion of fishing and trade for both sharks and sea cucumbers has outpaced national and international management. The exploitation of sharks has recently been the subject of a number of strong regulatory actions, however these have been implemented too recently to be able to observe responses in shark fin trade volumes. It may be possible in the future to conduct a more conclusive analysis of the effects of regulations for both sharks and sea cucumbers. 4. Conclusions The production and trade systems included in this analysis are complex, and the data available to describe and quantify them are

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incomplete. As a result, an analysis of this kind may raise more questions than it is able to answer, but it represents an important step toward using trade data as a valuable and complementary source of insight for seafood products that are sourced and traded globally. This analysis has shown that shark fin and sea cucumber trading networks have proved resilient to changing conditions (e.g. stock declines, closed fisheries, regulations, public opinion on conservation). It has also shown that the networks are expanding in the face of overfishing to meet demand for dried seafood products by Chinese consumers. Given the resilient dynamics of the sourcing and trade system, it can be difficult to definitively identify which drivers are most strongly influencing trade and what conservation measures will have the greatest impact. Hypotheses presented in this paper thus represent a platform for further analysis to inform management and conservation. Given the strong cultural tradition embodied in the two products, and the assumption that growth in China drives increasing production, it would be expected that the production patterns of both shark fin and sea cucumber would have increased under the prosperous economic conditions in China during the past decade. However, this is not the case. Global sea cucumber production has not fallen because there are still available supplies, aquaculture production, limited public conservation awareness and an insufficient regulatory environment. In contrast, shark fin production appears to have declined, either due to resource constraints, changing consumer attitudes and/or regulatory curbs on trade. The expanding globalization of commerce and trade is not unique to the Chinese dried seafood market. Similar features are evident for other markets and seafood commodities (Berkes et al., 2006; Swartz et al., 2010a,b) and this should caution against perceptions of stereotypic Chinese exploitation. Therefore, while it is appropriate to target conservation awareness messages at the largest consumer markets for shark fin and sea cucumbers in China, it is also important to emphazise that action is required in sourcing and trading countries as well. Furthermore, there may be inertia in the sourcing systems, such as economic dependency of coastal communities on sea cucumber harvests or non-target catches of sharks in commercial fisheries, which will perpetuate resource depletion even if market demand wanes. It is unlikely that the current global sourcing and trade systems for shark fin and sea cucumber are sustainable under the current regulatory environment. While management systems are evolving as a response to fishery expansion, they are in many cases not yet sufficiently comprehensive or well implemented to reverse population declines over time. For both taxa, but particularly for coastal and sedentary sea cucumber species, resource conservation will rely primarily on the ability of national management policies to effectively control exploitation and exports. For sharks, and to support and complement national measures for sea cucumbers, trans-national cooperative management approaches are required to regulate sourcing, to reinforce national policies across regions including the high seas, and to implement rigorous monitoring. At present, despite interpretive difficulties in some cases, trade statistics provide an important information source for assessing trends in exploitation and evaluating conservation strategies. In the future, it is expected that improved trade monitoring systems (e.g. universally implemented product-specific and species-level commodity codes, effective border inspection systems, catch documentation and other traceability schemes) will greatly assist in guiding appropriate management responses. Acknowledgements This study was supported by Mistra (the Swedish Foundation for Strategic Environmental Research) through a core grant to the

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Stockholm Resilience Centre, the Nereus Program at the Stockholm Resilience Centre, a collaborative Nippon Foundation initiative, the Australian Centre for International Agricultural Research (ACIAR) Project FIS/2012/074 and the CGIAR Research Program on Aquatic Agricultural Systems. We thank S.W. Purcell and three anonymous reviewers for their constructive evaluation of the manuscript. We thank Henrik Österblom, Max Troell, Beatrice Crona, Andrew Merrie and Marc Metian for valuable discussions in the preparation of this study, Allen To at the World Wide Fund for Nature (WWF) Hong Kong for providing data and Neil Andrew for comments on the manuscript. HE also thanks his previous employer, the Department of Ecology, Environment and Plant Sciences at Stockholm University.

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