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LETTER Long-term trends of coral imports into the United States indicate future opportunities for ecosystem and societal benefits Andrew L. Rhyne1,2, Michael F. Tlusty1, & Les Kaufman1,3,4 1 New England Aquarium, John H. Prescott Marine Laboratory, Boston, MA, USA 2 Roger Williams University, Department of Biology and Marine Biology, Bristol, RI, USA 3 Boston University Marine Program, Department of Biology, Boston University, Boston, MA, USA 4 Conservation International, Arlington, VA, USA Keywords Aquarium trade; coral trade; curio trade; coral triangle; marine policy. Correspondence Andrew L Rhyne, Department of Biology and Marine Biology, Roger Williams University, One Old Ferry Road, Bristol, RI 02809, USA. Tel: 401 254-5750; Fax: 401 254-3310. E-mail: arhyne@rwu.edu Received 5 March 2012 Accepted 12 June 2012 Editor Dirk Roux doi: 10.1111/j.1755-263X.2012.00265.x Abstract The international trade in corals used to be primarily a curio trade of dried skeletons, but now focuses on live corals for the marine reef aquarium trade. The trade is still rapidly evolving, creating challenges including the addition of new species that outpace effective management strategies. New species in the live coral trade initially command high prices, but as they become common the price radically decreases with feedback effects to the trade. To understand these trends, 21 years of live coral import data for the United States were assessed. Trade increased over 8% per year between 1990 until the mid-2000s, and has since decreased by 9% annually. The timing of the peak and decline varies among species, and is a result of the rising popularity of mini-reef ecosystem aquariums, the global financial crisis, and an increase in aquaculture production. The live coral trade offers opportunities for coral reef ecosystem conservation and sustainable economic benefits to coastal communities, but realization of these externalities will require effective data tracking. Introduction The marine aquarium trade is but one of many threats facing the world’s coral reefs, and despite some public opposition to the trade (reviewed in Tlusty et al. 2012), few quantitative studies of its true significance have been reported (Kolm & Berglund 2003). Species entering the market are extremely diverse and include algae, vascular plants, a wide range of invertebrate phyla and both bony and cartilaginous fishes. The trade has the potential to cause overharvesting, collateral damage to coral reef habitat and introduction of exotic species (Smith et al. 2008; Jones et al. 2009; Rhyne et al. 2009; Schofield et al. 2009). However, it is also a potential boon to conservation through elevated valuation and stewardship of wild habitats that support livelihoods based upon the collection, rearing and export of aquarium specimens (Tlusty 2002; Tlusty et al. 2008). The aquarium hobby can also benefit conservation by mobilizing public pressure to rein in other anthropogenic stressors including global climate change (Carpenter et al. 2008), unsustainable global market demand (e.g., shark fin, Napoleon wrasse, Chinese traditional medicine), and development of coastal and aquatic resources. Combined with commercial overfishing (Burke et al. 2011), these nonaquariumrelated threats are likely to be far more severe and pervasive than the direct damage done by aquarium collectors, though comparative data are lacking. Consequently, we have launched a systematic study of the marine aquarium trade and its current and potential relationship to coral reef conservation. Here we report on the changing face of the trade, in nature and magnitude, over the past 21 years with particular regard to coral biodiversity. The export of marine aquarium specimens is a global industry (Wabnitz et al. 2003). Each year, a complex trade network sells upwards of 50 million coral reef animals to an estimated 2 million hobbyists worldwide (Wood 2001; Green 2003; Wabnitz et al. 2003). The epicenter of 478 Conservation Letters 5 (2012) 478–485 Copyright and Photocopying: c 2012 Wiley Periodicals, Inc. A.L. Rhyne et al. Trade of aquarium and curio corals trade is the Coral Triangle, a region of high biodiversity that encompasses Indonesia, Malaysia, Papua New Guinea, Philippines, Solomon Islands, and Timor-Leste. The Philippines and Indonesia represent about 85% of trade volume, however, smaller island nations export unique species helping to drive high rates of overall trade biodiversity (Rhyne et al. 2012). Over 40 countries export livestock to feed the hobby and for the past three decades growth in traded volume exceeded 10% per annum (Bruckner 2001), with some slowing at the end of 2007 as a result of the global economic recession (Rhyne et al. 2009). The United States is a major destination of live coral reef products importing 68% of all live corals reported in CITES with the EU importing 24% (mostly split among Germany, France, the Netherlands, and Great Britain) (Jones 2008). Given the significant U.S. role in the coral trade, the United States Coral Reef Task Force identified reforms to the marine aquarium trade as a major priority in 2000 (www.coralreef.gov/international/). This resulted in efforts to increase the knowledge of this trade within the United States (Puerto Rico and Hawaii) and to help promote a sustainable global trade internationally (Tissot and Hallacher 2003; Legore et al. 2005). While there are many management challenges for ornamental fisheries at the local and the national level, global trade is the key driver (Green 2003; Olivier 2008). This is most evident in the coral trade (Bruckner 2001; Moore and Best 2001; Tissot et al. 2010), which began many decades ago with the harvest of dried “curio” specimens. The large take resulted in management measures focused on the total mass of harvested coral (Lovell 2001). With the advent of the marine home aquarium, trade emphasis shifted to the collection and transport of a much smaller volume of live colonies from remote regions (Figure 1). During the mid-1980s, scientists began to note a rapid, global degradation of coral reef habitats, an event in which the curio and aquarium trade were clearly participants. Because of the awareness of impacts to corals, “stony corals” and “live rock” have been protected by the Convention on International trade in Endangered Species of Wild Fauna and Flora (CITES code AC22 Inf. 8) since 1985, and regulated by export quotas and stringent import regulations (Department of the Interior Fish & Wildlife Service 2007). “Soft corals” and attached coral “substrata” are not covered by this convention and therefore are not highly regulated. The degradation of reefs and concern about trade of corals led to the ban of shipments from the Philippines after the CITES listing (reviewed in Green & Shirley 1999). Since the CITES listing, the harvest of corals and coral rock has seen a dramatic shift; moving away from a curio (dead) based industry to the trade of live coral for the marine reef aquarium trade. Indonesia, the largest 1980-1995 Aquarium trade -wild fishery -remote locales -increasing volumes - ornamental value Post-1995 Aquarium trade -rare species -wild fishery -remote locales -decreasing -common species -aquaculture -central production -increasing ? Future -aquaculture of curios -MPA protection of slow growing species -aquaculture production for habitat enhancement -economic benefits for remote locales Pre 1980 Curio trade -wild fishery -remote locales -large volumes -little value for rarity Figure 1 The trade in corals for the curio and live home hobby trade. The curio trade was the most important until the marine home hobby trade became popular. With the advent of ecosystem reef tanks in the mid- 1990s the trade changed again, with aquaculture of fast growing corals presently increasing. Will the future allow for aquaculture production of fast growing corals to supply the curio trade? How can the coral fisheries be managed to provide economic benefits to the remote communities dependent originally upon the fishery? supplier of stony corals, along with other south Pacific countries, claimed harvests did not significantly affect wild populations, and implemented harvest quota systems in an effort to comply with CITES (Harriott 2003). While quotas provide an important trade limitation for threatened species (Harriott 2003), questions on their effectiveness have been raised (Bentley 1998; Castello & Stewart 2010; Knittweis & Wolff 2010), and the initial large quotas may not be sufficient for slow growing stony coral species (Bruckner 2000). Bruckner (2001) reviewed the strengths and weakness of CITES for monitoring the international trade of marine aquarium species, citing the key limitation as the lack of taxonomic level information (Green & Hendry 1999). The major concern is that rare species could be overexploited under quotas set at the genus level. The illegal trade of corals is difficult to track, as it is for all wildlife, and hence significant portions of the trade enterprise can potentially be unaccounted for in formal data (Rosen & Smith 2010; Toledo et al. 2012). However, there will be an asymmetry in the illegal trade of corals. More illegal trade will likely occur in the curio side as the handling of live coral through known shipping routes makes it more difficult to hide this trade compared to the bulk cargo shipping of curio products. The aquarium trade is a rapidly evolving industry (Larkin 2008; Olivier 2008; Rhyne et al. 2009). Species Conservation Letters 5 (2012) 478–485 Copyright and Photocopying: c 2012 Wiley Periodicals, Inc. 479 Trade of aquarium and curio corals A.L. Rhyne et al. can enter the trade and quickly become heavily traded (e.g., Banggai Cardinalfish, Pterapogon kauderni) (Lunn & Moreau 2004). Also, species that have been traded at a low level for decades can suddenly become a new fad and experience a sharp increase in exploitation (e.g., Ricordea mushrooms, Ricordea florida) (Torres-Pratts et al. 2011). As new products move into the market, retail prices are initially high until supply increases, at which point prices dramatically drop (Larkin 2008). Because of the low price, there is typically an influx of low quality supply as the species becomes popular and more consumers can afford the cheaper product. This rapidly changing nature of the aquarium trade creates numerous management challenges relevant to the trade of live coral. For example, the rapid shift in markets might allow for the over exploitation of slow growing corals harvested under management systems designed for faster growing corals (Jones 2011). Here, we analyze trade data for live corals for two decades from 1990 to 2010. The purpose of this is to understand the overall trends over time as coral species enter the trade and become commercially popular. We also assess the impact increased aquaculture production of corals (Parks et al. 2008) has on the trade, and forecast how changes in the trade of live corals may impact coral reef ecosystems. Methods While the focus of the aquarium trade has historically been on fishes, the advent of live reef and mini-reef aquarium set-ups has greatly increased demand for marine invertebrate taxa (Rhyne et al. 2009). Arthopoda, Mollusca, and Cnidaria are the most heavily traded tropical marine invertebrates (Wabnitz et al. 2003). The most popular cnidarians (approximately 5% of the total trade) are corals and anemones with a few species of jellyfishes (Wabnitz et al. 2003). Corals within the aquarium trade can be loosely defined as polyps (corallimorphs, and zoanthids), gorgonians, and both soft and hard corals. They are categorized arbitrarily based upon the presence or absence of a hard skeleton rather than on the basis of actual phylogenetic relationships. For example, species of Alcyonacea, Corallimorpharia, Gorgonacea, and Zoantharia are often lumped into the general term “soft corals,” while the anthozoan orders Scleractinia and Helioporacea and hydrozoan order Anthoathecata are traded as “hard corals.” In the same vein, some species of the Alcyonacea, namely Tubipora spp., are traded as hard corals. To better understand the recent changes in the stony coral trade and assess market trends we queried CITES trade data for a 21-year period (1990–2010) utilizing the World Conservation Monitoring Center trade database (United Nations Environment Programme–World Conservation Monitoring Centre 2010). Because the United States is the world’s largest importer of stony corals (Jones 2008) and numerous authors have noted discrepancies between import and export data in CITES (Bruckner 2001; Blundell & Mascia 2005; Jones 2008; Phelps et al. 2010), we limited our queries to imports of corals reported by the United States to CITES for all countries. To compare the long-term trends in the commercial curio and live trade of stony corals we analyzed “purpose code” trade data for trends in both “live” and raw or worked corals. We limited the possibility of taxonomic misidentification by sorting all records to genus level and only analyzed the aquarium corals in the reports that listed “live” items and not kilograms. Live corals traded in kilograms are likely to be biologically active “live rock,” and not coral species of interest to the hobbyists. For example, the more than 300,000 kg of “live” Acropora exported from Tonga in 2003 is almost certainly a live rock product sold under the terms “Tonga branch” or “shelf rock.” However, it is not live Acropora, it is likely dead, encrusted fragments of branching coral skeleton. The CITES data were used to designate corals by common trade designations (small polyp, SPS, or large polyp, LPS), life history traits (free-living or stationary) and method of production (wild or cultured) as indicated by CITES source codes. In an effort to understand how retail price was related to the volume traded, price data were gathered for all genera imported into the United States by collection price data off the internet available on retailer web pages as well as eBay. Listing on eBay was of specific interest because of the number of rare or unique corals being offered for sale. Retail prices (price per individual) were analyzed against trade volume, life history traits (free, fixed) and trade designations (SPS, LPS) and variation (more than 10%) from mean retail prices were further scrutinized for likely causes for this deviation. Results and discussion Trade The total number of stony corals imported into the United States from the Coral Triangle and South Pacific grew at a yearly rate of 8.75% from 1990 until the mid-2000s. After a brief level period it dramatically declined by 8.98% annually (Figure 2). During this period, the proportion of corals originating from the Coral Triangle decreased from >90% in the 1990s to a low of 65% in 2010 as Australia expanded its exports. The life history traits (free, fixed) and trade designations (SPS, LPS) of coral species imported into the United States can be combined into three 480 Conservation Letters 5 (2012) 478–485 Copyright and Photocopying: c 2012 Wiley Periodicals, Inc. A.L. Rhyne et al. Trade of aquarium and curio corals Figure 2 Number (individual items unless otherwise indicated) of corals imported into the United States over the past 21 years by trade type (top) for live species grouping (middle) and by% composition (bottom). LPS and SPS are trade terms for Large Polyp Stony corals and Small Polyp Stony corals. LPS species are grouped into Fixed, those species that attached to substrata or Free those species that are free living and not attached to the substrata. Raw and worked (curio trade) corals (top) are shown in both kilograms and pieces. Note the large increase in kilograms imported in 2003 is a result of live rock (Tonga Branch Rock) imports mislabeled as raw Acropora sp. from Tonga. groups (Figure 2), each exhibiting a different historical trend. The percent of SPS-fixed corals in the trade tracks the total import numbers, increasing from <10% in 1992 up to 38% in 2006, then decreasing to 27% in 2009. The LPS-fixed corals trend in the opposite direction, decreasing between 1992 (>50% of the trade) and 2006 (34%) before rising again to 43% in 2009. The percent of LPSfree corals in the trade decreased between 1992 and 2009 beginning at just over 38% and ending at just under 30% of the trade (Figure 2). This pattern is repeated in the annualized import records of the top six species of stony corals (Figure 3). Acropora spp. imports decline sharply post 2006 while the Figure 3 Top six genera of stony corals imported as “live,” in individual units, for trade into the United States over the past 21 years. remaining five species (all SPS) peak earlier and decrease slightly if at all. The increase in the number of species imported is a result of the switch in the marine aquarium hobby to the keeping of “mini-reef” ecosystems (Rhyne et al. 2009). This trend in the hobby also explains the change in the proportion of the different types (positive trend of SPS and negative of LPS), as SPS are more desirable for the smaller mini-reef aquariums. The dramatic decrease post-2006 was likely a result of two factors. The first was the economic downturn (Mittelman 2009), in which spending on “luxury items” was curtailed. Probably more important, however, was a change in coral sourcing. While the majority of corals are collected from the wild, there is a small but growing fraction of corals from aquaculture production (Figure 4). Nearly all-wild corals imported into the United States for the aquarium trade originate from Pacific sources, with a majority originating from the Coral Triangle, although Fiji and Australia are shipping greater proportions of the total amount. Currently, only a small number of coral genera can be commercially produced in aquaculture with a majority belonging to the genus Acropora (Figure 4b). The significant decline in Acropora spp. imports to the United States (Figures 3 and 4b) is a result of the switch in production from wild capture to aquaculture. Hidden in this decline is a growing importance of ex situ production through fragmentation (“fragging”), which has been successfully used for commercial production of SPS and some branching LPS corals. Much of this type of production can occur within the United States and import records do not account for domestic production, which began in the early 1990s (Perrin 1993). Currently, the statistical tracking of coral production inside the United States is lacking. Thus, the U.S. domestic production Conservation Letters 5 (2012) 478–485 Copyright and Photocopying: c 2012 Wiley Periodicals, Inc. 481 Trade of aquarium and curio corals A.L. Rhyne et al. Figure 4 (Top) Total number of individual corals imported into the United States. (Bottom) Acropora sp. imported into the United States. White bars are from wild harvests,while black bars indicate those corals from captive culture (CITES source codes F, R, C). of SPS corals is a likely factor in causing the negative trend in both the percent imports of SPS-fixed species, as well as the total number of corals imported. Increasing aquaculture production also occurs in source nations. For example, 26% of Acropora imported into to the United States from Indonesia in 2009 were listed under CITES codes (F-farm, C-captive bred, and R-ranch) indicating aquaculture production. Aquaculture will likely continue to gain traction with the vast majority of SPS corals being aquacultured within the next decade. Not all species lend themselves to culture, however. Large polyp species of corals in the sessile genera Catalaphyllia, Nemenzophyllia and all free living LPS corals are more challenging to produce and therefore wild production is likely to dictate supply for the time being. Free living species, which can be fragmented commercially, e.g., Fungia spp. are difficult to certify as aquacultured according to existing standards (Pasaribu 2008) and cultured species may be imported under existing wild harvest quotas. % Australian Figure 5 (Top) Relationship of price and volume (total number imported) for corals imported into the United States. (Bottom) Relationship (r2 = 0.55) of mean price and composition of coral imported from Australia. Markets Retail prices of all corals averaged US$56.29 per piece ranging from US$5.00 to US$499.99. No relationship was observed (y = –9E−05x + 57.56, r2 < 0.01) between volume imported and average price (Figure 5 top). However, SPS-fixed corals were more likely to be devalued than the two LPS designations, as the residuals from the above mentioned relationship for the SPS corals were significantly less than 0, and lower than the residuals for the LPS corals (Figure 6). The Australian corals had a major influence on this relationship as the more prevalent these corals became, the greater the price (Figure 5 bottom). The higher-priced corals are sold with key words of “rare,” “limited edition,” “unique” or sold under producer’s name or strain name (e.g., Green Warpaint 482 Conservation Letters 5 (2012) 478–485 Copyright and Photocopying: c 2012 Wiley Periodicals, Inc. A.L. Rhyne et al. Trade of aquarium and curio corals Figure 6 The average price range (US$) and the average residual from the price-volume (total number traded) relationship (Figure 4 top) for the three different coral categories. Scolymia) which appears to have increased their mean price due to limited number of highly priced individuals. Therefore, prices appeared more dependent on perceived market abundance and not the actual supply as indicated from CITES records. While true abundance will affect price (Courchamp et al. 2006), here it is postulated that perceived rarity will also affect price, as often unusual colors command greater prices than common colors. This rarity price premium will also muddle a comparison of the cost of wild and aquacultured species. Corals that are sold as “aquacultured” are often much smaller than wild corals with many domestic producers selling “frags” or small cuttings of corals whereas wild corals are often sold as “large” “x-large” or “show” sizes. Currently many cultured corals are imported as wild product, since it is simpler to identify aquaculture products as wild than it is to provide all of the appropriate documentation of the aquacultured product (D. Palmer, personal communication). These confounding variables will make it difficult to accurately determine the resource economics of the coral trade. Sustainability considerations While these data are used to assess trade chains and the value of the home hobby industry, they can also be used to highlight where conservation programs can focus their attention for maximum impact. The surge of aquaculture amongst SPS corals indicates that these fast growing corals would be ideal candidates for localized habitat restoration programs (Edwards & Gomez 2007), or even curio products. Typically, aquaculture concentrates production near central distribution gateways, and not in remote villages. Efforts need to be made to understand the impact of this centralized production on small rural communities in exporting countries, and to promote the small communities that have been the historically important harvest locales. This localized production along with restocking would help to maintain coral reef ecosystem services. Ornamental fishery products from many Pacific island countries are a major source of export revenue, and are important economic drivers, but it is important to continue the financial benefits of the trade to the small collector communities. Fijian communities that harvest corals for the aquarium trade have a higher median income from this harvest when compared to traditional fishery products (Wabnitz et al. 2003; Lovell & Whippy- Morris 2009). In situ aquaculture production or ranching is a means to match the various needs for ecological, economic and societal benefits. It is critical to have economic benefits of ornamental species production (fishery or aquaculture) remain in the original source communities (Tlusty 2002): this should be a priority for a responsible global trade, and will align the aquarium fishery with the Convention on Biological Diversity (Secretariat of the Convention on Biological Diversity 2005). The CITES system for overseeing the live coral trade, while imperfect as currently implemented, is a good one and it accomplishes a majority of the objectives for trade regulation (Phelps et al. 2010). Indonesia has responded to CITES and calls for a more sustainable coral trade by developing meaningful mariculture standards with traceability (Pasaribu 2008). However, in a dramatically fast moving industry, monitoring trends in the trade is not a simple matter of assessing volumes over time. For example, quotas that were derived from the curio trade data in which product is measured in tonnage and focused on fast growing species is inappropriate for slower growing aquarium species that are sold by the piece or “individual” (Jones 2011). Furthermore, price is susceptible to product rarity and perceived supply limitations. These “rare” corals do not appear in trade data, as they are unique color morphs untraceable through the CITES or any other governmental monitoring system. The additional tracking of the value of imports will also be important to determine if decreasing trends reflect supply difficulties, which could indicate significant pressure on populations from the fishery. If imports decrease, and price remains stable or declines, then demand is likely being met by domestic production. However, if imports decline, and the price increases, then supply is not meeting the demand (Courchamp et al. 2006). Conclusion In summary, the aquarium and curio trade for corals is associated with positive and negative impacts to ecosystems and societies. It is a rapidly evolving trade, and because of this, needs to be adaptively managed in a way Conservation Letters 5 (2012) 478–485 Copyright and Photocopying: c 2012 Wiley Periodicals, Inc. 483 Trade of aquarium and curio corals A.L. Rhyne et al. to support conservation efforts and maximize the benefit of the trade. The increasing importance of aquaculture will need to be integrated into both CITES rules and also sourcing decisions for retailers within the trade. Valuing in situ production of corals will help maintain historically critical locales and communities, which will in return maintain value to extant reef ecosystems. The aquarium trade needs to be a fully vested partner in such market-driven coral reef conservation initiatives. Future monitoring must accurately catalogue wild and aquacultured corals, their color morphs, and their value. It will also be important to address (1) the relative risks and benefits of ex situ or concentrated in situ production of corals for the aquarium trade; (2) how significant production increases will affect total revenue; and (3) whether there can be a return to curio corals through aquacultured eco- or fair-trade labeled products. Answers to these questions will be critical to evaluate whether coral production will continue to be part of a long-term sustainable economic solution especially for remote island communities. Acknowledgments The data and presentation of these data were prepared for the 2011 United States Department of Commerce, National Oceanic and Atmospheric Administration Coral Mariculture Workshop held in Bali, Indonesia. Rhyne is supported by a National Oceanic and Atmospheric Administration (NOAA) Coral Reef Conservation Program Grant NA09NMF4000385. The authors are grateful to Ana Malone Oliver and Elizabeth Futoma, Roger Williams University, for help in capturing the market and CITES data. Laura Dee, University of California at Santa Barbara, provided helpful comments on the market data. Kerri Warren, Roger Williams University, and two anonymous reviewers provide helpful comments on a previous draft of this manuscript. 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