Biological Conservation 169 (2014) 225–237
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Biological Conservation
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Review Conservation and management of ornamental coral reef wildlife: Successes, shortcomings, and future directions q ⇑ Laura E. Dee a, Stephanie S. Horii a, Daniel J. Thornhill b, a Bren School of Environmental Science & Management, University of California, Santa Barbara, 2400 Bren Hall, Santa Barbara, CA 93106, USA b Department of Conservation Science and Policy, Defenders of Wildlife, 1130 17th Street NW, Washington, DC 20036, USA article info abstract
Article history: Trade in ornamental coral reef wildlife supports a multi-million dollar industry but in some places threat- Received 23 August 2013 ens vulnerable coral reef species and ecosystems due to unsustainable practices and lack of effective reg- Received in revised form 12 November 2013 ulation. To supply this trade, fishers sometimes deplete fish populations and rely on practices, such as Accepted 14 November 2013 cyanide fishing, that harm coral reef organisms and habitats. The number of countries involved, dispersed fishing localities, and the diversity of species in trade present considerable impediments to conservation and management. For instance, traditional fisheries management techniques such as stock assessments Keywords: and total catch limits may not be feasible for ornamental fisheries, which are characterized by limited Aquarium trade data on population dynamics, stock status, and collection effort, as well as instances of illegal, underre- Coral reef conservation Coral reef fisheries ported, and unregulated fishing. A number of strategies to monitor, regulate, and manage the trade have Ornamental fisheries been implemented with varying efficacy. In order to learn from previous attempts and identify promising Sustainable fisheries management approaches, we reviewed selected management practices and regulations from diverse settings, with attention to the effectiveness of each approach. Strategies reviewed include international agreements, marine protected areas, rotational closures, banned-species lists, quotas, cyanide detection, gear restric- tions, size limits, licensing and limited entry into the fishery, and regulations on imports. Moratoriums on certain species, no-take reserves, tiered quota systems, and import and export restrictions, among others, provided examples of management successes. Further conservation and management improvements could be achieved through a wider application of successful strategies identified here and utilization of data-limited methods from food fisheries. Ó 2013 The Authors. Published by Elsevier Ltd. All rights reserved.
Contents
1. Introduction ...... 226 1.1. The ornamental coral reef wildlife trade and its ecological consequences ...... 226 1.2. Management challenges ...... 226 1.3. Objective ...... 227 2. Materials and methods ...... 227 3. Results and discussion ...... 227 3.1. International agreements regulating the trade ...... 227 3.2. Country-level regulations and management ...... 229 3.2.1. Exporting nations ...... 230 3.2.2. Importing nations ...... 232 4. Conclusions...... 235 4.1. Alternative approaches and successful practices...... 235 4.2. Catch limits ...... 235 4.3. Rights-based management ...... 235 4.4. Data-limited stock assessments ...... 235 4.5. Other promising directions...... 235 5. Conclusions...... 235
q This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. ⇑ Corresponding author. Tel.: +1 (202) 772 0227; fax: +1 (202) 682 1331. E-mail address: [email protected] (D.J. Thornhill).
0006-3207/$ - see front matter Ó 2013 The Authors. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biocon.2013.11.025 226 L.E. Dee et al. / Biological Conservation 169 (2014) 225–237
Acknowledgements ...... 236 Appendix A. Supplementary material ...... 236 References ...... 236
1. Introduction nets, spears, and crushing of corals to capture fish (Gonzales and Savaris, 2005; Thornhill, 2012). 1.1. The ornamental coral reef wildlife trade and its ecological The coral reef wildlife trade can also affect importing countries consequences through the introduction of exotic and invasive species (Semmens et al., 2004). The most prominent example is the introduction of The trade in ornamental coral reef wildlife, which includes the lionfish (Pterois volitans and P. miles) from the Indo-Pacific into aquarium, jewelry, and curio trades, supports a multi-million dol- the Caribbean and western Atlantic (Betancur et al., 2011). Since lar industry (Grey et al., 2005; Wabnitz et al., 2003); however, the 1990s, lionfish spread along the U.S. east coast and throughout collection practices and a lack of effective regulation and manage- the Caribbean (Betancur et al., 2011). These predators eat large ment may threaten vulnerable coral reef species (Thornhill, quantities of native fishes resulting in reduced recruitment of 2012;Tissot et al., 2010). Many species are targeted to supply this Atlantic coral reef fishes, competition with native predators such trade, primarily based on their size and aesthetics. Examples in- as grouper, reduction of grazers like surgeonfish and parrotfish, clude brightly-colored juvenile or male fishes; stony corals with and concomitant ecological changes (Albins and Hixon, 2008; Les- attractive skeletons or large, colorful polyps; and mollusks with ser and Slattery, 2011). colorful, ornate shells. The effects of the collection and trade in The broader ecological consequences of collection for the trade ornamental wildlife are less studied than other threats to coral are understudied from both fisheries and ecological perspectives. reefs – including climate change, ocean acidification, overfishing, The coral reef wildlife trade targets species ranging from the foun- and nutrient pollution – in part due to the complexity of the dation of coral reefs (e.g., corals and live rock for aquariums and trade, which targets hundreds of fish and invertebrate species home décor) to top predators (e.g., sharks for teeth, jaws, and other (Rhyne et al., 2012;Wabnitz et al., 2003). Nevertheless, collection curio items; Grey et al., 2005; Knittweis and Wolff, 2010; Ross, has reduced certain populations, introduced invasive species, and 1984). One concern is that characteristics that make fish and inver- in rare cases caused localized extirpations (reviewed in Thornhill, tebrate species attractive to aquarium enthusiasts can also lead to 2012). For example, one of the most-studied ornamental species, disproportionate impacts on the reef when these species are re- the yellow tang (Zebrasoma flavescens) in West Hawaii, has de- moved. For example, hobbyists’ preferences for species that con- clined in some collection areas, but is stable or recovering within sume algae or parasites could drive reductions of these species reserves (Tissot and Hallacher, 2003; Tissot et al., 2004; Williams on the reef, potentially with trophic effects (e.g., Edwards and et al., 2009). In the Sulawesi Archipelago of Indonesia, endemic Shepherd, 1992; Rhyne et al., 2009; but see Tissot et al., 2004). Banggai cardinalfish (Pterapogon kauderni) have declined in abun- The diversity of species and complexity of interactions on coral dance to the point of localized extirpations, and are now consid- reefs make understanding population dynamics of coral reef wild- ered endangered (International Union for the Conservation of life and predicting the ecosystem-level consequences of their re- Nature, 2012; Kolm and Berglund, 2003; Vagelli, 2008). Inverte- moval difficult. brates collected for trade also exhibited population declines; for instance, densities of symbiotic giant anemones in the Cebu re- 1.2. Management challenges gion of the Philippines declined over 80% (Shuman et al., 2005). Even stony corals (order Scleractinia), the foundation of coral reef The coral reef wildlife trade exhibits both notable similarities ecosystems, are collected. Their collection can reduce coral cover and differences from other capture fisheries, including characteris- and alter species compositions and population demographics tics that can impede resource management. Organisms from nearly (Knittweis and Wolff, 2010; Ross, 1984). Yet many ornamental every trophic level are collected, making identification and moni- fisheries have continued for decades and have not collapsed. De- toring of collected species exceptionally challenging. The life his- spite the potential impacts of collection, the stock status and sus- tory, demographic, and population data required for traditional tainable harvest levels of most ornamental species remain largely stock assessments are typically unavailable (Fujita et al., in press; unknown and unmonitored. Honey et al., 2010). Even countries with higher management and Beyond the unevaluated status of targeted species and potential enforcement capacity, such as the U.S., generally do not conduct population declines, destructive practices, including cyanide fish- stock assessments for ornamental species. In general, stock assess- ing, are sometimes used to collect coral reef wildlife for trade. Cya- ments for many species in the trade may be difficult because rare nide is dispensed onto coral colonies in order to anesthetize and species are targeted. For rare species, accurate estimates of popula- easily capture fish (Rubec et al., 2001). Within minutes, these tox- tion size are difficult to obtain because their probability of detec- ins kill an estimated 50% or more of exposed species, with addi- tion in surveys is quite low (e.g., see Chadès et al., 2008). It is tional deaths occurring hours to days later (Hanawa et al., 1998; therefore difficult for managers to monitor populations and reefs, Rubec et al., 2001). Non-targeted species like corals, anemones, enforce regulations, document catches, and develop accurate pop- and other habitat forming species are also exposed and can be in- ulation models. jured or killed. In particular, cyanide blocks respiration in corals, Many locations have few (if any) regulations addressing the cor- causing coral bleaching and mortality (Cervino et al., 2003; Jones al reef wildlife trade. In countries where regulations exist, enforce- and Steven, 1997). The current prevalence of cyanide fishing is un- ment is hindered by inaccurate reporting of landings (e.g., Walsh known. Cyanide fishing occurs in at least 15 countries, including et al., 2004; Rhyne et al., 2012) and illegal collection (Barber and major exporters like Indonesia and the Philippines, though its Pratt, 1997). Similar to issues with trans-boundary fisheries use is apparently less prevalent today than 20 years ago (Bruckner (McWhinnie, 2009), roving collectors are common in Southeast and Roberts, 2008). Other prevalent fishing methods also injure Asian fisheries and have little incentive to protect coral reef and kill both targeted and non-targeted species, including abrasive resources in a given area, because they may never return to the L.E. Dee et al. / Biological Conservation 169 (2014) 225–237 227 same collection site (Amos and Claussen, 2009; Marine Aquarium 2. Materials and methods Market Transformation Initiative, 2006). A complex supply-chain creates challenges for managing the We reviewed the available peer-reviewed and grey scientific lit- trade, especially in Southeast Asia. Similar to capture fisheries, erature, as well as government websites and reports, on regula- many countries supply the trade and animals change hands tions and management practices by locality for the ornamental many times between collection and export with no system to coral reef wildlife trade. The review focused primarily on practices monitor this chain of custody (Amos and Claussen, 2009; Nixon within the aquarium trade, over other ornamental trade sectors et al., 2012). At each stage of the supply chain, animals from var- (e.g., curios), because much of available conservation and manage- ious sources are pooled, so separating sustainably-harvested ment literature is on this topic. Literature was compiled primarily wildlife from their unsustainable counterparts is difficult (Amos from online databases and search engines, including Web of Sci- and Claussen, 2009). This supply chain complexity complicates ence (thomsonreuters.com/web-of-science), Google Scholar (scho- reform in several ways. First, high supply-chain mortality can lar.google.com), PubMed (ncbi.nlm.nih.gov/pubmed), and Science lead to market inefficiencies and drive overharvesting (Wabnitz Direct (sciencedirect.com). Search terms included some combina- et al., 2003). Second, the complex supply chain presents chal- tion of the terms wildlife trade, aquarium trade, curio trade, or or- lenges for reducing destructive collection practices, like cyanide namental fisheries with country names, management practices, fishing, since cyanide is increasingly difficult to detect with time and names of the most heavily-traded species (as noted in Rhyne (Mak et al., 2005; but see Vaz et al., 2012). Third, import-docu- et al., 2012; Wabnitz et al., 2003; Wood, 2001). These sources were mentation requirements are challenging when organisms change supplemented by more targeted searches for papers identified dur- hands many times. All of these challenges would benefit from a ing the search process (e.g., from the references of another paper or shorter and more vertically-integrated supply chain (Nixon et al., report), suggestions from colleagues, and informal interviews with 2012). management practitioners, conservationists, and academics (see Despite the many similarities between ornamental fisheries and acknowledgements). most capture fisheries in coral reefs, several unique characteristics Countries that lacked source information were subsequently of fisheries that supply the coral reef wildlife trade demand new excluded from this review despite their contributions to the supply management approaches and present difficulties (Donaldson, of coral reef wildlife (e.g., Mexico, Cook Islands, Solomon Islands, 2003). Two aspects differ greatly: and Taiwan). Additional countries were excluded because no post-1996 source documentation was located (e.g., Samoa and (1) value is per individual rather than by biomass; and the Cook Islands). Haiti was the one exception; it was maintained (2) for the aquarium trade, animals must remain alive in order despite few sources on its practices due to its importance as an to be sold. exporting country (Rhyne et al., 2012). This resulted in a broad re- view of existing management practices based on international Furthermore, collection of aquarium fishes differs from harvest- agreements, the practices of three major wildlife importers (the ing food fishes. It often targets juveniles, affecting the population’s U.S., European Union, and Australia), and the practices of 18 wild- age structure, and brightly-colored males, potentially skewing the life-exporting nations, states, and territories (Australia, Bahamas, sex ratios of the population. Eritrea, Fiji, Haiti, Indonesia, Kiribati, Maldives, Philippines, Sri Lanka, Papua New Guinea, the Kingdom of Tonga, U.S.-Florida, 1.3. Objective U.S.-Guam, U.S.-Hawaii, U.S.-Puerto Rico, Vanuatu, and Vietnam). Because this review examines international, national, and regio- Overcoming barriers to effective management and regulation is nal regulations and management, inevitably local and non-govern- daunting given that trade includes over 1800 species of fish, hun- mental organization (NGO) efforts have been overlooked. For dreds of species of coral, over 500 species of other invertebrates, example, during the Marine Aquarium Market Transformation Ini- and live rock (Rhyne et al., 2012; Wabnitz et al., 2003;). Exports tiative within the Philippines, some villages developed total allow- emerge from at least 45 countries while imports largely go to the able catches for ornamental fish species and restricted fishing U.S. (64%), the E.U. (14%), and Japan (7%) (Tissot et al., 2010; permits to villagers (D. Ochavilla, personal communication). Addi- Wabnitz et al., 2003). Our objective is to identify successful regula- tionally, in both Indonesia and the Philippines, several villages tion and management approaches that could potentially be repli- developed fisheries management plans in conjunction with NGO cated elsewhere by reviewing select management practices partnerships, though these plans were not implemented at the na- around the world. For purposes of this discussion, we consider reg- tional level. Due to length constraints, such local initiatives are not ulation to be a set of codified rules established to govern the trade, covered here. and management to be the implementation and enforcement of various conservation and fisheries measures, including regulations. This paper does not attempt to comprehensively review manage- 3. Results and discussion ment effectiveness in each country involved in the ornamental coral reef wildlife trade; instead, it highlights the range of manage- 3.1. International agreements regulating the trade ment techniques currently used or with potential to manage the trade. We first examine the application of the Convention on Inter- Several international treaties and governing bodies set the national Trade in Endangered Species of Wild Fauna and Flora foundation for nations to regulate harvesting of marine species (CITES) to govern the coral reef wildlife trade on an interna- (Table 1; Fidelman et al., 2012), yet few have been applied to the tional-level (Section 3.1). Second, we review the laws, manage- trade in coral reef species. The primary international mechanism ment practices, and fisheries management plans used for regulating the coral reef wildlife trade is the Convention on Inter- ornamental fisheries in exporting and importing countries (Sec- national Trade in Endangered Species of Wild Fauna and Flora tion 3.2). We conclude by highlighting strategies that have been (CITES), an agreement among 175 countries (CITES, 2012). Since used successfully in other data-limited capture fisheries that may 1975, CITES has aimed to ensure that the international trade in hold promise if they were applied to ornamental fisheries wildlife does not threaten species with extinction or endanger- (Section 4). ment. The species covered by CITES are listed in three Appendices, 228 L.E. Dee et al. / Biological Conservation 169 (2014) 225–237
Table 1 International agreements and guidelines, as well as U.S., E.U., and Australian regulations, related to the trade in coral reef wildlife.
Year Law or regulation Target Mechanisms and limitations International 1948 International Union for Conservation of Conservation Inventory on conservation status and extinction risk for species. Provides scientific advice, but Nature Red List of Threatened Species lacks regulatory authority (IUCN, 2012; Vagelli, 2008) 1973 Convention on International Trade in Trade Restricts international trade in listed species. Protects only a few species in the trade and the Endangered Species process for listing additional species is cumbersome (Bruckner, 2001; Tissot et al., 2010) 1982 United Nations Convention on the Law of Fisheries Establishes management responsibility within Economic Exclusive Zones. Mentions responsible the Sea fishing practices within jurisdiction but is broad in scope and lacks specific guidelines. 1992 Agenda 21 and the Rio Declaration on Fisheries Provides criteria for sustainable management of marine resources, funding mechanisms, and Sustainable Development technology transfer to developing countries, but funding arrangements and technology transfers have not been widely implemented to facilitate sustainability (Dodds et al., 2012) 1993 Convention on Biological Diversity Fisheries International collaborative agreement to promote biodiversity conservation and sustainable resource use. The US, the largest consumer of coral reef wildlife, is not a member (Smith et al., 2008). 1995 FAO Code of Conduct for Responsible Fisheries Provides guidelines for sustainable fisheries management. Aims to reform destructive fishing Fisheries practices, though lacks explicit and operational definitions for sustainable management and overfishing (Bruckner and Roberts, 2008; Syarif, 2009) 1995 World Trade Organization regulations Trade Restrictions on international trade among member nations. There is little enforcement on imports for the aquarium trade and inaccurate identifying/labeling/recording of ornamental species imported into the US (Rhyne et al., 2012; Smith et al., 2008) U.S. 1900 Lacey Act Trade Bans import of illegally collected wildlife. Develops list of ‘‘injurious’’ animals that are illegal to trade. Enforcement of this act is difficult and requires substantial evidence (Morrisey et al., 2011; Tissot et al., 2010) 1973 Endangered Species Act Conservation Framework for protecting endangered species and developing recovery plans. Few vulnerable marine species are listed (Tissot et al., 2010) 1976 Magnuson-Stevens Fishery Conservation Fisheries/ Governs fisheries management within the Exclusive Economic Zone. This Act does not extend to and Management Act Trade imports of wildlife caught by illegal fishing in other countries and most ornamental species do not have a management plan (Thorson and Wold, 2010) 2000 Civil Asset Forfeiture Reform Act Trade Government authority to confiscate illegal assets. Dependent on the Lacey Act; burden of proof shifted to government (Thorson and Wold, 2010) E.U. 1997 European Community Veterinary Controls Trade Requirements for species-level information and veterinary inspection of imports. Requires proof of quarantine and animal welfare measures as well as adherence to CITES. It requires no additional administrative burden for traders but possibly duplicates efforts of the Annex D of the WTR 1997 Wildlife Trade Regulation EC 338/97 Trade Acts as supplement to CITES, with importing countries held partly responsible for reporting violations. Creates dataset of CITES-listed species entering the EU (Annex D). More stringent than CITES, but lacks standardized protocols for collecting and managing information. The implementation of this regulation and its integration with CITES requirements varies across countries (Jones, 2008). 2006 Commission Decision 2006/656/EC Trade Requirements for fish health certifications for ornamental imports; assessment of countries for suitability of imports. Established animal health and welfare requirements for imports of fish for ornamental purpose; reinforced quarantine measures (Kinch and Teitelbaum, (2008) Australia 1991 Fisheries Management Act of 1991 Fisheries Established the Australian Fisheries Management Authority to oversee fishing zones 1992 Fisheries Management Regulations 1992 Fisheries Develops specific regulations for implementing the Fisheries Management Act 1994 Fisheries Act of 1994 Fisheries Provides framework and guidelines for sustainable fisheries management (Ryan and Clarke, 2005) 1999 Environmental Protection and Biodiversity Fisheries/ List of acceptable species for import and only allows live fish from approved countries (Morrisey Conservation Act Trade et al., 2011)
corresponding to the level of protection (Kinch and Teitelbaum, obtained illegally and (c) risk of injury and cruel treatment 2008): during transport was minimized for living specimens. Appendix II covers over 30,000 species, including the fol- Appendix I provides the highest level of protection to spe- lowing coral reef wildlife species: over 2000 hard corals cies threatened with extinction and vulnerable to interna- (including all scleractinians), all giant clams (Tridacna and tional trade. It strictly prohibits all international trade for Hippopus spp.), three species of hammerhead sharks commercial purposes. For instance, the hawksbill turtle (Sphyrna spp.), and all seahorses (Hippocampus spp.) (CITES, (Eretmochelys imbricata) is listed on Appendix I, prohibiting 2012; Jones, 2008). Although a number of other coral reef all international trade in this species for jewelry and luxury species have been proposed for Appendix II listing, for items. instance red and pink corals (Corallium and Paracorallium Appendix II lists species that are not currently in danger of spp.) and the Banggai cardinalfish, these listing proposals extinction but are threatened by over-exploitation. Export were either withdrawn or rejected (Vagelli, 2008). permits for Appendix II specimens can be issued by the Appendix III lists species that are protected by at least one exporting country only when (a) the Scientific Authority member that requests enforcement assistance from other has advised that export will be non-detrimental to the sur- CITES members. In July 2008, China listed four Corallium vival of that species or when a Management Authority reg- species in CITES Appendix III, adding permit requirements ulating exports is satisfied that (b) the specimen was not for export of these corals from China (CITES, 2012). L.E. Dee et al. / Biological Conservation 169 (2014) 225–237 229
Table 2 International Union for Conservation of Nature Red List of Threatened Species assessments for the top-10 aquarium (Wood, 2001) versus food fishes (FAO, 2008).
Fishery Common name Scientific name IUCN Assessment Aquarium Blue green damselfish Chromis viridis Not evaluated Aquarium Sapphire devil Chrysiptera cyanea Not evaluated Aquarium Yellow tang Zebrasoma flavescens Not evaluated Aquarium Clown anemonefish Amphiprion ocellaris Not evaluated Aquarium Azure demoiselle Chrysiptera hemicyanea Not evaluated Aquarium Threespot dascyllus Dascyllus trimaculatus Not evaluated Aquarium Blacktail humbug Dascyllus melanurus Not evaluated Aquarium Australian damsel Pomacentrus australis Not evaluated Aquarium Goldtail demoiselle Chrysiptera parasema Not evaluated Aquarium Bicolor angelfish Centropyge bicolor Least Concern Food Anchoveta Engraulis ringens Least Concern Food Alaska pollock Theragra chalcogramma Not evaluated Food Atlantic herring Clupea harengus Least Concern Food Skipjack tuna Katsuwonus pelamis Least Concern Food Chub mackerel Scomber japonicus Least Concern Food Largehead hairtail Trichiurus lepturus Not evaluated Food Blue whiting Micromesistius poutassou Not evaluated Food Chilean jack mackerel Trachurus murphyi Data deficient Food Japanese anchovy Engraulis japonicus Not evaluated Food Yellowfin tuna Thunnus albacares Near threatened
Note that when CITES listed animals are ‘‘aquacultured,’’ or born fisheries commonly restrict gear usage and fishing meth- and reared in captivity, these species move to the next Appendix ods, including cyanide fishing. (e.g., from Appendix I to II). This is done to reflect the generally low- Total bans prohibit collection of certain species, which er ecological impact of aquaculture compared to wild collection. should allow for populations to recover provided that Most of the thousands of species involved in trade are not CITES reproductively-viable populations remain, habitat is pro- listed (CITES, 2012). The small number of listed species may not be tected, and poaching is minimized. For instance, species indicative of the status of trade species, since few species in the listed under CITES Appendix I and the Endangered Species coral reef wildlife trade have ever been evaluated for extinction Act in the U.S. are banned from trade. Similarly, the Philip- risk by the International Union for the Conservation of Nature or pines banned collection of giant clams, seahorses, and black CITES authorities (McClenachan et al., 2011), including only one and scleractinian corals. of the top-10 traded aquarium fishes, Centropyge bicolor (Table 2). Limited effort programs attempt to control total harvest For listed species, the effectiveness of CITES protection has been by limiting overall harvesting effort. In the aquarium trade, questioned (Jones, 2008; Tissot et al., 2010). We illustrate these is- effort limitation has only restricted who can fish. Although sues through two examples, Banggai cardinalfish and scleractinian season restrictions are common in capture fisheries, to our corals (Supplemental Text). knowledge, they are not widely used in ornamental fisheries. 3.2. Country-level regulations and management Total allowable catch (TAC) is an aggregate annual quota for a fishery that is often set using stock assessments – The United Nations Convention on the Law of the Sea estab- complex population models that determine the status of a lished Exclusive Economic Zones (EEZs) that grant coastal coun- fishery and predict how populations will respond to har- tries jurisdiction over their near-shore marine resources and the vest rules. Country-level export quotas, aggregate TACs on responsibility to conserve and management natural resources. Spe- the number of fish that can be exported in a given year, cies collected for the aquarium and ornamental trades are almost are commonly employed by Pacific island nations. entirely shallow water, reef-associated species that reside within Rights-based fisheries management, sometimes called EEZs (Supplemental Table 1); therefore, countries have greater po- ‘‘catch shares,’’ refers to fisheries management strategies tential control over the harvest of coral reef wildlife in contrast to that allocate exclusive access to a portion of the TAC to the many highly-migratory species targeted by food fisheries. Na- individuals or groups of fishers (Costello et al., 2008). Catch tions have implemented various measures to protect coral reef share programs establish property rights to an otherwise species, including marine protected areas (MPAs), harvest regula- common-pool or open-access resource, and they also exist tions (e.g., gear type, permits, quotas), and/or required documenta- in the form of traditional marine tenure (Hilborn et al., tion (e.g., quarantine certification) (Morrisey et al., 2011; Smith 2005). In some ornamental fisheries, property rights are et al., 2008; Wood, 2001). These laws and initiatives either directly established through exclusive fishing zones for local com- (e.g., species-specific quotas for aquarium fishes) or indirectly (e.g., munities or individuals called Territorial User Rights Fish- no-take reserves that protect coral reef habitats and associated eries (TURFs). wildlife) regulate collection. The success of management regimes Spatial closures and zoning aim to protect biodiversity and regulations varies greatly. In Sections 3.2.1–3.2.2 and Tables and allow for the recovery of fished species by prohibiting 1, 3 and 4, we highlight examples of strategies adopted by both or zoning fishing and other impactful activities in certain importing and exporting countries. areas (e.g., no-take marine reserves and MPAs). Fish Management actions currently or potentially used for ornamen- replenishment areas (FRAs) in West Hawai’i specifically tal trade species (Table 3): prohibit the collection of ornamental fishes (Tissot et al., 2004). Gear restrictions are commonly used in both food and Size limits restrict fishing or collection to a species above ornamental fisheries to either prevent negative impacts or sometimes below a certain size threshold to protect a on habitats or on non-target species (bycatch). Ornamental certain portion of the breeding stock and allow the 230 L.E. Dee et al. / Biological Conservation 169 (2014) 225–237
population to grow. A 10-cm minimum size limit is often there are no size restrictions on collection, allowing for the re- used in seahorse fisheries (Foster and Vincent, 2005). moval of important demographic groups (Bruckner and Borneman, National regulations on import/export practices can 2006). impose requirements (e.g., documentation, permitting, or The lack of stock assessments and quotas for the many species quarantine procedures) that can regulate wildlife import, leave MPAs as the most widely used measure for coral reef fish export, and handling practices. These requirements can conservation in Indonesian (Dudley and Ghofar, 2006). Indonesia help control the spread of disease and invasive species as maintains a reserve system, including national parks, comprising well as the mortality of species in the supply chain. For 2% of Indonesia’s EEZ (World Bank, 2013). MPAs have been shown instance, Australia imposes stringent import requirements to be a useful management tool for marine ornamental species (reviewed in Morrisey et al., 2011). (e.g., Tissot et al., 2004), but the presence of MPAs alone does not ensure effective management. For instance, a more extensive Case studies highlighting the use of these strategies in both MPA system is needed to effectively maintained connectivity in exporting and importing countries are presented in Sections 3.2.1 the popular aquarium coral Heliofungia actiniformis (Knittweis and 3.2.2, respectively. et al., 2009) Thus, although Indonesia utilizes management tools ranging from licensing and gear restrictions to quotas and MPAs, 3.2.1. Exporting nations various studies have called for additional measures and improve- 3.2.1.1. Indonesia. At the epicenter of coral reef biodiversity, Indo- ments (Bruckner and Borneman, 2006; Dudley and Ghofar, 2006; nesia has consistently been a top exporter of coral reef wildlife for Green and Shirley, 1999; Knittweis et al., 2009; Knittweis and over 30 years (Rhyne et al., 2012; Wabnitz et al., 2003). Histori- Wolff, 2010). cally Indonesian reefs were open to all extractive uses, but the government has recently attempted to better regulate its natural 3.2.1.2. The Philippines. The Philippines is another primary export- resources (Amos and Claussen, 2009; Nurhidayah, 2010). The ing nation of ornamental coral reef wildlife, with major source Ministry of Marine Affairs and Fisheries formulates national policy localities in Bataan, Batangas, Bohol, Cebu, Davao, Palawan, and for fisheries management and conducts resource assessments Zambales (Ochavillo et al., 2004; Rhyne et al., 2012). Overall the (Dudley and Ghofar, 2006). Management is divided into 11 fisher- Philippines supplies the majority – approximately 55% – of the ies management areas and several fisheries groups (Dudley and marine aquarium fish imported into the U.S. (Rhyne et al., 2012). Ghofar, 2006; CCIF, 2013). Coral reef fish, including ornamental The Philippines conducts limited national-level fisheries manage- and food fish species, comprise one group (Dudley and Ghofar, ment under the Philippine Fisheries Code. Similar to Indonesia, 2006). Since the late 1990s, local authorities have been primarily fisheries management is largely decentralized; Local Government responsible for resource utilization, conservation, and develop- Code of 1991 delegated management authority primarily to ment and implementation of management plans (Dudley and barangays or local government units (Gonzales and Savaris, Ghofar, 2006; Fidelman et al., 2012; Nurhidayah, 2010; Timotius 2005). In most local jurisdictions, there is little management or et al., 2009). enforcement capacity and poor data collection (Gonzales and Sav- Management measures for ornamental species include ‘busi- aris, 2005; Ochavillo et al., 2004). ness’ licensing systems, a 1985 ban on destructive fishing practices Fishers in the Philippines are typically required to have a license including cyanide fishing, harvest quotas on stony corals, and or appropriate accreditation to collect coral reef wildlife (Gonzales MPAs (Dudley and Ghofar, 2006; Pet and Pet-Soede, 1999). Despite and Savaris, 2005). However, there are no limits on the total num- this range of measures, effective management is stymied on many ber of licenses (Gonzales and Savaris, 2005), reducing their effec- levels, leading Indonesian fisheries to be described as de facto open tiveness as a management tool to control fishing effort (FAO, access (CCIF, 2013). For example, fish and vessel licensing require- 2013). Additionally, roving collectors, who often ignore licensing ments are not consistently enforced, and small-scale fishers are not requirements, make up a sizeable portion of collection activity required to obtain licenses. The prevalence of small-scale fishing (Marine Aquarium Market Transformation Initiative, 2006;S. and the lack of systematic requirements limit the effectiveness of Green, personal communication). licensing (Dudley and Ghofar, 2006; CCIF, 2013). The ban on cya- Beyond licensing of collectors, the Philippines prohibits export nide fishing is rarely, if ever, enforced (Pet and Pet-Soede, 1999). of species listed on Appendix II of CITES, including stony corals Implementing management at regional and local scales is chal- and seahorses. The stony coral trade was once based primarily lenged by the decentralized governance structure, a lack of on Philippine corals until collection and export was outlawed enforcement and resource management capacity, and corruption (Ross, 1984). Commercial collection of stony corals continued for (Amos and Claussen, 2009; CCIF, 2001; Dudley and Ghofar, 2006; several years, especially in the Cebu region, but the coral trade ulti- Nurhidayah, 2010; Pet and Pet-Soede, 1999). This decentralized mately dwindled (Ross, 1984). The Philippines also banned trade in management ineffectively supervises ‘‘roving’’ collectors – a major giant clams and seahorses following their listing in CITES Appendix source of overharvesting in Indonesia – who commonly travel be- II in 1996 and 2002, respectively (Vincent et al., 2011; Wabnitz tween different jurisdictions to collect while ignoring collection et al., 2003). For seahorses, exports from the Philippines had ceased regulations (Amos and Claussen, 2009; CCIF, 2013; Marine Aquar- by 2006 (Vincent et al., 2011) and recent CITES data indicate a glo- ium Market Transformation Initiative, 2006). bal reduction in the seahorse trade, possibly resulting from the Although there are not harvest quotas for most ornamental spe- Philippine ban (Evanson et al., 2011). For most species, there are cies, Indonesia has established collection quotas for many sclerac- no catch limits, species quotas, size limits, or restocking programs tinian corals (Green and Shirley, 1999). Approximately 1 million (Gonzales and Savaris, 2005; Ochavillo et al., 2004). Perhaps as a live coral pieces are permitted for export annually, including a result of the few management measures in place, overfishing of growing number of farmed corals (Wood et al., 2012). The quotas’ coral reef species is reported (e.g., Ross, 1984; Sadovy et al., efficacy is challenged by weak enforcement and a lack of popula- 2001; Shuman et al., 2005). tion data to set total-allowable catches (Green and Shirley, 1999). Finally, the Philippines controls exports of coral reef wildlife A comparison of the quotas to population assessments indicated through a permitting process and limited testing for cyanide in live that – depending on the targeted genus – 1–96% of available coral fish. Although anticyanide laws exist, these bans are commonly populations could be collected thereby allowing for over-exploita- unenforced (Ochavillo et al., 2004). In the late 1980s and 1990s, tion of certain corals (Bruckner and Borneman, 2006). Oftentimes the government and the International Marinelife Alliance jointly L.E. Dee et al. / Biological Conservation 169 (2014) 225–237 231 established a set of Cyanide Detection Laboratories (CDL) (Barber trade. Tonga uses a licensing system to cap the total number of and Pratt, 1997; Barber, 1999; Rubec et al., 2001). However, detec- businesses collecting and exporting coral reef wildlife at five com- tion of cyanide is technically difficult, and the accuracy of the CDL panies (Fisheries Management and Planning Section, 2008; Matoto tests has been questioned (Mak et al., 2005; Bruckner and Roberts, et al., 1996). On the reef, collectors must adhere to strict gear con- 2008). Currently, there is only one active CDL, so very few exported trols that ban the use of poisons and damaging gear, only allow the shipments are tested. Despite this, the recent innovation of a new use of hand or barrier nets, and restrict the use of scuba diving to and more reliable cyanide test, which uses optical fiber technology authorized collectors (Fisheries Management and Planning Section, to detect thiocyanate, may enable the Philippines and others to 2008). Limiting the spatial extent and amount of collection effort, better control the trade in cyanide-caught fish (Vaz et al., 2012). Tonga confines aquarium fish and invertebrate collection to certain areas and has a blanket quota of 100,000 fish per exporting com- 3.2.1.3. The Maldives. Since the inception of the Maldives’ aquarium pany annually (Fisheries Management and Planning Section, trade in the 1980s, the government has monitored the collection 2008). This aggregate volume of fish is considered to be a ‘‘negligi- and export of coral reef fish (Edwards and Shepherd, 1992). In ble fraction’’ of the biomass of targeted species (Matoto et al., 1988, concern over the trade’s sustainability and conflicts with 1996), suggesting that collection is largely sustainable. Neverthe- the diving-tourism industry led the government to establish an less, no stock assessments have been conducted to determine the aggregate export quota of 100,000 coral reef fish and invertebrates status of targeted species. per year (Edwards and Shepherd, 1992). Collectors and exporters Species that are susceptible to overharvesting may be insuffi- were required to report the volume of exported coral reef fish to ciently protected under this system, because management is not customs officials and fishing was only permitted until the quota conducted on a species-by-species basis. Although no quotas are was reached (Edwards and Shepherd, 1992). Although this precau- placed on the harvest of invertebrates or soft corals, Tonga prohib- tionary measure was laudable, it insufficiently protected species its the collection of dead hard corals and live rock. Tonga also re- from over-exploitation. A combined analysis of export data, field quires exporters to provide detailed reports on the volume of surveys of fish abundance, and rough estimates of Maximum Sus- animals exported (Marine Aquarium Fishery Management Plan, tainable Yield concluded that many coral reef species were poten- 2008). This suite of management tools provides Tonga with a rela- tially overexploited by over-collection under this aggregate quota tively-comprehensive management program, particularly for system (Edwards and Shepherd, 1992). aquarium fishes. Further management measures were added in response to such concerns, for example a 1997 ban on destructive moxy nets (Ed- 3.2.1.5. Australia. Australia exports wildlife to supply the trade, and wards and Shepherd, 1992; Saleem and Islam, 2008). Cyanide fish- this collection is regulated under the national Environmental Pro- ing, although never reported in the Maldives, was also banned tection and Biodiversity Conservation Act of 1999. While allowing (Saleem and Islam, 2008). In 1995 and 1999, twenty-five MPAs the export and trade in wildlife, this Act also places responsibility were established as no-take reserves (Saleem and Islam, 2008). on state governments to develop fisheries management plans Still, monitoring and enforcement for these systems were lacking, (Department of Primary Industries and Fisheries, 2009). Approxi- leading the government to implement a species-specific quota pro- mately 60% of collection for the coral reef wildlife trade in Australia gram (Saleem and Islam, 2008; Wood, 2001). occurs in Queensland where three aquarium fisheries operate: the This latest Maldives management system divides fish into three Queensland Marine Aquarium Fish Fishery (MAFF), the Queensland categories or tiers. Category A bans export of 17 species that are Coral Fishery (QCF), and the Coral Sea Fishery. considered highly vulnerable (Saleem and Islam, 2008; see Saleem The Queensland Government regulates the MAFF and the QCF and Adam, 2004 for lists of species in each category). Furthermore, by restricting destructive gear types and limiting entry through a parrotfish, puffer fish, porcupine fishes, eels, giant clams, and hard licensing system, which has not issued new commercial licenses corals other than Tubipora musica are barred from export under since 1997 (Roelofs and Silcock, 2008). Both fisheries operate in this system (Saleem and Islam, 2008). Chromis viridis, a popular the Great Barrier Reef Marine Park that protects approximately aquarium species (Rhyne et al., 2012), is prohibited due to its use 30% of the available habitat from fishing. The MAFF (48 licenses) as bait for tuna fishing (Saleem and Islam, 2008). The second tier employs different combinations of management techniques (Category B) includes 66 species managed under species-specific including catch quotas, bans on certain species, size limits, and sea- quotas (Saleem and Adam, 2004; Saleem and Islam, 2008). The sonal closures (Roelofs, 2008a). For one, MAFF collection rates are remaining 71 species (Category C) are managed under a 300,000 compared to sustainability benchmarks based on ecological risk organism aggregate quota for the entire country (Saleem and Is- assessments (Roelofs, 2008a; Roelofs and Silcock, 2008). lam, 2008). The efficacy of the tiered quota system is currently un- The QCF (59 licenses), also state managed and regulated, is pri- der evaluation by the Marine Research Centre and Marine marily managed under the Policy for the Management of the Coral Conservation Society. Fishery (Department of Primary Industries and Fisheries, 2009). Saleem and Islam (2008) noted the apparent effectiveness of the Management under this policy includes a total allowable commer- new system, but also highlighted significant challenges, including cial catch (TACC) of 200 tonnes, separated into 140 tonnes for orna- weak enforcement, unnecessary bureaucracy, a lack of monitoring mental corals (coral skeletons of acroporids and pocilloporids officials familiar with exported species, confusion between com- collected alive and dried for ornamental purposes) and live rock. mon and scientific names for exported species, under-reporting The remaining 60 tonnes is allocated to ‘‘specialty coral’’ (hard of value to avoid purchasing additional licenses, and roving collec- and soft coral and anemone species taken for live aquaria). The tors. By incorporating quotas built on data from species-specific smaller TACC for specialty coral recognizes that these species stock estimates and export records, the tiered system is superior may not be as highly productive as other ornamental coral species to the previous open-access system. However, these data are of (but see Jones, 2011). PMS and risk assessments also monitor the uncertain reliability and have not been applied to monitor changes status of this fisheries (Roelofs, 2008b). in the stocks of collected species or for setting appropriate catch The adjacent Coral Sea Fishery (with 2 licenses) falls under the limits (Saleem and Islam, 2008). jurisdiction of the Australian Fisheries Management Authority and includes the collection of marine fishes and limited collection of 3.2.1.4. The Kingdom of Tonga. The Kingdom of Tonga is an active live rock (Australian Fisheries Management Authority, 2011). Col- exporter of fish and invertebrates for the ornamental aquarium lection is monitored and compared to tiers of precautionary catch 232 L.E. Dee et al. / Biological Conservation 169 (2014) 225–237 thresholds. Management responses are initiated when the thresh- closures temporarily increased the population of many species, olds are reached. including yellow tang, but fish populations declined dramatically when areas were open for harvesting (Williams et al., 2006). 3.2.1.6. The United States: Hawaii and Florida. The U.S. states of Ha- 3.2.1.6.2. Effort and catch controls in Florida. The Florida Keys waii and Florida and territories of Puerto Rico and Guam supply the supports a multi-species ornamental fishery, primarily targeting coral reef wildlife trade. Each location has adopted different man- invertebrates, which has grown in size and impact since 1987 agement measures for their fish and invertebrate fisheries (Table 3). (Rhyne et al., 2009). While Hawaii implemented spatial manage- Here, we focus on the management practices adopted in Hawaii ment through its FRAs, Florida regulates the commercial harvest and Florida. of ornamental species through licensing requirements, allowable 3.2.1.6.1. Spatial management in Hawaii. The Hawaiian aquar- gear types, and harvest restrictions including quotas, closed sea- ium fishery has grown substantially over its 50-year history into sons or areas, size limits, and bans on certain species (Larkin the state’s second-largest inshore fishery. Annually, the fishery et al., 2001; Larkin and Adams, 2003). Most notably, the state con- lands over 708,800 animals, but the total catch is underestimated trols collection of ornamental invertebrates by limiting the number due to under-reporting (Walsh et al., 2004). Collection is concen- of available harvest licenses for both commercial and recreational trated on several species, particularly yellow tang, with the top- collectors, including a 1998 moratorium on new licenses (Larkin 10 species comprising 73% of the annual aquarium-fish catch and Adams, 2003). By limiting entry into the fishery, this cap at- (Walsh et al., 2004). Since 1953, the government of Hawaii has re- tempts to reduce collection effort and overharvesting while gener- stricted collection gear to small nets and traps. Today, permits are ating profits for permit holders. For aquarium fishes, Florida available to anyone for a small fee. The collection of stony corals, employs several management strategies to regulate collection however, is illegal. (e.g., daily catch limits as well as minimum and maximum size lim- Since as early as 1970, collection has reduced the abundances of its for butterfly and angelfishes) (Larkin et al., 2001; Wood, 2001). target species (Tissot and Hallacher, 2003; Tissot et al., 2004). The For invertebrates, this limited-entry program restricts the num- volume of fishes taken from Hawaiian reefs has generated public ber of participants, but it does not limit catch volume or collection concern about the long-term sustainability of the ornamental reef effort (Rhyne et al., 2009). These licenses allow fishers to collect fish collection (Tissot and Hallacher, 2003; Capitini et al., 2004). In most species unrestrictedly – with the exception of long-spine response, in 1973 the Hawaii Division of Fish and Game required sea urchins (Diadema antillarum), Bahama starfish (Oreaster reticul- fishers to file catch reports, yet the number of permits issued and atus), sea fans (Gorgonia flabellum and G. ventalina), stony corals fish caught continued to increase over time (Walsh et al., 2004). (Scleractinia), and fire corals (Millepora spp.) (Larkin et al., 2001). Increasing fish collection along with growing public awareness of In the absence of catch limits, the limited entry program has not population declines intensified conflicts between the tourism reduced fishing pressure or collection effort, because the majority industry – the largest economic driver in Hawaii – and the aquar- of collection is done by a minority (40%) of permit holders (Larkin ium fishery (Capitini et al., 2004), including an unsuccessful at- and Adams, 2003; Rhyne et al., 2009). Catch landings and the num- tempt to ban the aquarium fishery in 1997–1998 (Hawai’i ber of targeted species have actually increased since the program’s Department of Land and Natural Resources, 2010). Efforts for a implementation (Rhyne et al., 2009). statewide ban continue today (Miller, 2012). As an alternative Several ornamental species also have daily bag limits that con- measure, Hawaii implemented Fish Replenishment Areas (FRAs) trol the volume of the species (both fishes or invertebrates) caught in 2000 – the first no-take zones specifically targeting aquarium by both commercial and recreational fishers. However, these bag collection – to protect aquarium-fish populations and reduce user limits are not set based on an overall TAC for the season or on stock conflicts (see Capitini et al., 2004 for details on FRAs establish- assessments. Setting TACs for this fishery would be challenging for ment). The FRAs, combined with existing MPAs, protect 35.2% of several reasons: the fishery targets multiple species, no stock the Kona coast from aquarium collection (Tissot et al., 2004; Wil- assessments exist, catch landings are underreported despite Flor- liams et al., 2009). ida law requiring reporting, and fishing effort, such as the quantity From an ecological perspective, the abundance of some targeted of gear and time spent collecting, is not reported or measured populations increased within FRAs, but the stock size of these spe- (Rhyne et al., 2009). cies may not have increased overall. Within the FRAs, 8 out of the top-10 targeted populations appear to be recovering, with 4 spe- cies exhibiting statistically-significant increases in abundance 3.2.2. Importing nations (e.g., yellow tang, Hawai’i Department of Land and Natural Re- 3.2.2.1. United States. The United States accounts for the majority sources, 2010; Williams et al., 2009). Some adult fish have spilled (64%) of the global market for marine aquarium fish and other over into areas adjacent to the FRA boundaries (Williams et al., coral reef wildlife (Tissot et al., 2010). The U.S. Fish and Wildlife 2009) and larval fish are dispersing from the FRAs into the collec- Service is responsible for documenting the volume and abundance tion zones (Christie et al., 2010). The effectiveness of the FRAs var- of live wildlife imports at U.S. ports of entry, but the volume and ies among sites (see Ortiz and Tissot, 2008). Outside of the FRAs, diversity of trade makes this monitoring challenging (Rhyne collection is now concentrated in the remaining open areas, collec- et al., 2012; Smith et al., 2008; Tissot et al., 2010). Three federal tion effort remains high, and there are no catch limits (Stevenson laws – the Lacey Act, the Endangered Species Act, and the Magnu- et al., 2011). Since FRAs were established, overall populations of son-Stevens Fishery Conservation and Management Act – are the yellow tang have continued to decline (Williams et al., 2009). For primary legal protections for coral reef wildlife entering the U.S. management outside of FRAs, the West Hawai’i Fisheries Manage- (Smith et al., 2008; Tissot et al., 2010). ment council recommended developing a ‘white list’ of 25-aquar- Under the Endangered Species Act (ESA), the U.S. currently safe- ium species that can be collected (Hawai’i Department of Land guards two coral species, Acropora palmata, and A. cervicornis, with and Natural Resources, 2010). Ornamental fisheries in Hawaii do 66 additional species under consideration for listing at the time of not employ catch limits, weakening the effectiveness of the licens- this writing. The ESA requires the conservation of listed species, ing and the FRAs at controlling effort. including protection of critical habitat as well as prohibition of Elsewhere in the Waikiki-Diamondhead Fisheries Management interstate and foreign commerce. States, including Hawaii and Area of Oahu, periodic closures have been attempted to protect reef Florida, prohibit most collection of stony corals; however, imports fish from overharvesting (i.e., Williams et al., 2006). These periodic of most coral species are allowed. L.E. Dee et al. / Biological Conservation 169 (2014) 225–237 233
The Lacey Act bans the importation of organisms collected in rule has not been fully implemented and does not specify which violation of the laws of the source country. Cyanide fishing is species are included, so its effectiveness remains to be determined. banned in most countries, and therefore importation of wildlife caught with cyanide is unlawful. Nonetheless, importation of fishes 3.2.2.2. Countries of the European Union. Countries of the European captured using cyanide continues due to a lack of enforcement in Union (E.U.) are second only to the U.S. as importers of coral reef source countries and the difficulty of detecting cyanide in fishes wildlife (Tissot et al., 2010; Wood, 2001). The E.U. established high (Bruckner and Roberts, 2008). Cyanide is rapidly metabolized – regulatory standards for customs procedures, animal welfare, and meaning that detection is technically difficult and time sensitive invasive species (European Commission, 2010; Wood, 2001). The (reviewed in Mak et al., 2005) – thereby hindering the application E.U. requires adherence to CITES regulations, membership in the of the Lacey Act. However, a recently developed cyanide detection World Organization for Animal Health, and that exporters provide method may overcome these challenges (Vaz et al., 2012). The util- proof of quarantine measures (European Commission, 2010). Wild- ity of the Lacey act in promoting global coral wildlife conservation life Trade Regulation EC 338/97 supplements CITES by allowing is constrained by the environmental laws of the source countries. importing countries to question trade sustainability from the A second provision of the Lacey Act prohibits knowingly allow- source country and further enables an E.U. Scientific Review Group ing any wild animal or bird to be imported under inhumane or (SRG) to investigate (Jones, 2008; Kinch and Teitelbaum, 2008). A unhealthful conditions. Practices that cause high supply-chain negative SRG ruling can ban imports from that country (Jones, mortality appear to be prohibited under this provision; however, 2008). the Lacey Act is not invoked because demonstrating that an impor- The SRG has significant power to protect marine aquarium ter knowingly permitted a violation to occur is difficult. Addition- wildlife that ‘‘have a high mortality rate during transport and are ally, the provision has not been interpreted to include imports of unlikely to survive in captivity for a considerable proportion of fish or other coral reef wildlife species. their life span’’ (Eureopean Commission, 2010). In 1998 and The Magnuson-Stevens Act in part aims to conserve and man- 2000, the SRG temporarily suspended imports for 25 coral species age fishery resources in federal waters, focusing primarily on food from Indonesia until data demonstrating sustainable management fisheries. Although coral reef wildlife is collected from federal were provided (Bruckner and Borneman, 2006). Since then, addi- waters, domestic harvesting for ornamental uses occurs primarily tional reviews have been conducted and new wildlife import sus- in state jurisdictions, outside of the scope of the Magnuson-Stevens pensions imposed on other species and countries (e.g., E.U., Act. The Act regulates some precious coral species. Effective Janu- 2011). Such suspensions enable importing countries to play a more ary 30, 2012, a rule was issued for the collection of ‘‘aquarium proactive and precautionary role in coral reef conservation. The trade species’’ in federal waters of the Caribbean. However, this global benefit of this legislation is limited, however, because other
Table 3 The presence and absence of various management strategies in 18 exporting countries, states, and territories. ‘‘X’’ denotes a management strategy that has been implemented in a location for multiple groups of species. ‘‘No’’ indicates no record of the management strategy being planned or implemented in these countries in the literature reviewed here. Given the wide diversity of species targeted by the trade, management often differs across groups of species within a country or territory. ‘‘X⁄’’ refers to management that only applies to corals and live rock. ‘‘XF’’ refers to management that only applies to fishes. ‘‘Xi’’ refers to management that only applies to ornamental invertebrates other than corals. In other places, management actions were only applied to 1 species, which was noted when the information was available. The quality, quantity, and availability of information differed dramatically across regions. ‘‘Xo’’ refers to management for which the information may be outdated (such as outdated stock assessments). ‘‘NA’’ denotes no information or insufficient or unreliable/conflicting information to score a particular category.
Producing Size of Fisheries Fisheries: Barriers to Fisheries: Regulating commercial collection methods country or fishery management entry territory plan Relative Available License or Limited Quotas for Total allowable Size Fishing season or Gear Anti- Stock sizer online permit licenses individual catch limits seasonal closure by restrictions cyanide assessments for required species government laws ornamentals Part A Australiaa Large X X X X X⁄ No XF XXX Bahamasb Small No X No Conch only No No No X X No Eritreac NA No X No No No No NA NA NA No Fijid Large X X X X⁄ X⁄ XF XXXNo Haiti Medium No NA NA NA NA NA NA NA NA NA Indonesiae Very No X⁄ No X⁄ X⁄ No No X X X⁄ Large Kiribatif NA No X No Flame X1No No No No angelfish species only Maldivesg Large NA X No XF XF No No X X No Philippinesh Very No X No No No No No X X No Large Sri Lankai Large No NA No No No NA No X NA Xo Papua New NA NA No No X Circumstantially X No No X NA Guineaj Tongak Small X X X No XF,⁄ No No X X No US (Florida)l Large X X X XF XF XF XXXNo US (Hawaii)m Large X X No No No XF XXXNo US (Guam)n Small X X No No X⁄ X⁄ No X X No US (Puerto Large X X X XF XNoXXXXo Rico)o Vanuatup NA X X X 1 species 2 species No No X X X Vietnamq Large No NA NA NA NA NA NA X X No 234 L.E. Dee et al. / Biological Conservation 169 (2014) 225–237
Property rights Species protection Ecosystem Trade standards protection Territorial user Individual Trade Restrictions (export Bans or laws prohibiting OIE MPAst No-take CITES WTO right fisheriess transferrable inspection, quarantine laws) catch of endangered species member reservest member member quotas Part B Australiaa No X⁄ XXXXXXX Bahamasb NA No No X⁄ X X No X Observer Eritreac NA No X X⁄,i XNoNoXNo Fijid XNoX X XXXXX Haiti NA NA NA NA X No No No X Indonesiae XNoNoNoXXXXX Kiribatif XNoNoNoNoXXNoX Maldivesg No No XF,⁄ XF,⁄ XXXXX Philippinesh XNoX X⁄ XXXXX Sri Lankai NA No XF XF XXNAXX Papua New XNoNAX XXNoXX Guineaj Tongak NA No X X⁄ (and clams) No X No No X US No No X X X X X X X (Florida)l US (Hawaii)m No No X X X X X X X US (Guam)n No No X Gold coral only X X X X X US (Puerto No No X X⁄ (anemones) X X X X X Rico)o Vanuatup XNoX X⁄ (and clams) X X X X Observer Vietnamq NA No X⁄ NA X X No X X
a A. Roelofs (2008a, 2008b), personal communication and Australian Fisheries Management Authority (2011). b FAO (2009). c Daw et al. (2001). d J. Comley, personal communication, Manoa (2008) and Teh et al. (2009). e Dudley and Ghofar (2006), Green and Shirley (1999), Knittweis and Wolff (2010), Pet and Pet-Soede (1999) and Wood (2001). f Beta et al. (2005). g Saleem and Adam (2004) and Saleem and Islam (2008). h Bruckner and Roberts (2008), Gonzales and Savaris (2005), Ochavillo et al. (2004) and S. Green, personal communication. i Wihelmsson et al. (2002), Wijesekara and Yakupitiyage (2000) and Wood (2001). j Papua New Guinea Fisheries Act of (1998). k Marine Aquarium Fishery Management Plan (2008). l Larkin et al. (2001) and Larkin and Adam (2003). m Hawai’i Department of Land and Natural Resources (2010) and Walsh et al. (2004). n D. Ochavilla, personal communication and WPRFMC (2005). o Hardin and LeGore (2005), LeGore et al. (2005), CFMC (2012), USCRTF (2001) and Wood (2001). p Kinch and Teitelbaum (2008), SPC (2009) and Vanuatu Fisheries Management Plan of 2009. q Bruckner and Roberts (2008). r Rhyne et al. (2012) and Wood (2001); Small 650,000 specimens exported annually (value <$100 000 USD); medium = 50,000–100,000 exported specimens ($150,000 USD); large = 100,000–200,000 exported specimens ($300,000 USD); very large P200 000 specimens exported (>$300 000 USD). s EDF (2012). t Wood (2007).
Table 4 Summary of trends in management strategies and regulations employed by 18 exporting countries or territories (Table 3). Regardless of the regulations and strategies in place, the efficacy of any measure depends on enforcement and fishers’ compliance.
72% have gear restrictions; 77% ban cyanide use Marine Protected Areas represented P2% of the EEZa for 43% of these countries; however, with the exception of the FRAs in Hawaii, these MPAs were not established for the expressed purpose of conserving ornamental species Only 42% had fisheries management plans for ornamentals Only 4 areas required any form of stock evaluation or assessment. Assessments for 2 of those countries were outdated. Indonesia only requires stock evaluations for hard corals Only Australia employed data-limited stock assessments for fishes 33% of the areas have spatial rights-based management 27% have size limits for >1 species with only 22% requiring size limits for fishes Of the 12 jurisdictions that prohibit collections of endangered species, these laws apply only to corals in 7 (i.e., no other invertebrates or fish) Most areas (78%) require collection permits; less than half of those areas cap available permits Most of the reviewed countries are members of CITES (83%) and the WTO (83% members; 11% observers)
a World Bank (2013). major importers, particularly the U.S. and Japan, have less restric- 2001; Wood, 2001). Australia utilizes stringent quarantine and tive rules on imports (Tissot et al., 2010). anti-invasive species regulations to monitor the import and domestic transportation of coral reef wildlife. These measures 3.2.2.3. Australia. Australia has been one of the most successful in include a list of species permitted for trade, called a ‘‘whitelist,’’ regulating and managing the coral reef wildlife import trade (CCIF, created under the 1999 Environment Protection and Biodiversity L.E. Dee et al. / Biological Conservation 169 (2014) 225–237 235
Conservation Act (Morrisey et al., 2011). This whitelist has several (Hilborn et al., 2005). For instance, customary law in Fiji advantages, including a clearly defined protocol for border inspec- determines access to collection areas, as well as mechanisms for tions to identify permitted species. Australian regulations also re- benefit sharing, and enforcement of collection areas (Manoa, quire importers to provide extensive documentation, such as 2008). In exchange for access to the resource, marine aquarium permits, risk-assessments, health certificates, and identification operators that collect species within the customary fishing rights of shipments to the species level. Imports must be inspected and areas contribute profits from sales to scholarships for the commu- quarantined upon entering the country. Because of these require- nity (J. Comley, personal communication). Such approaches can ments, Australia has often served as an example of successful man- improve the socioeconomic benefits of collection to local agement of imports for the trade (CCIF, 2001; Morrisey et al., communities. 2011). 4.4. Data-limited stock assessments 4. Conclusions Despite the range of management tools available, oftentimes 4.1. Alternative approaches and successful practices managers must make decisions with limited data about the fish- ery’s status (Donaldson, 2003; Fujita et al., in press; Honey et al., Methods such as gear restrictions; entry, size, and catch limits; 2010). Methods to assess data-limited fisheries are emerging to fishing bans; spatial management; and size limits are commonly meet this challenge (e.g., Fujita et al., in press; Honey et al., used, with mixed success, in this trade (Tables 3 and 4). Voluntary 2010; Wilson et al., 2010). For instance, marine reserves can func- certification approaches, such as the Marine Aquarium Council, tion as proxies for unfished conditions, thereby providing a relative have also been attempted, but these programs were not viable measure of stock status at local scales (Wilson et al., 2010). This ap- (reviewed in Amos and Claussen, 2009). Conversely, stock assess- proach, known as the MPA-based decision tree method, compares ments, scientifically-set TACs, and rights-based fisheries manage- catch-per-unit-effort and size structure within and outside of re- ment approaches (e.g., individual transferable quota systems serves as estimates of fishing mortality to calibrate TAC levels. [ITQs] and exclusive fishing zones) remain underutilized. The However, the applicability of this approach and others to ornamen- limited employment of these management techniques is largely tal fisheries may be limited due to insufficient information on due to data, management capacity, and resource limitations (e.g., catch and effort trends or the biology of targeted species (Donald- finances or enforcement and monitoring personnel), as well as a son, 2003; Fujita et al., in press). To address these problems and lack of attention to ornamental fisheries. Furthermore, many of improve ornamental fisheries management, a tiered approach these methods likely require modifications in order to be made involving biomass, productivity-susceptibility analysis, and a com- appropriate for aquarium fisheries. bination of stock specific and aggregate quotas can be used (Fujita et al., in press). To date, these data-limited methods of fisheries evaluation have not been widely applied to ornamental fisheries, 4.2. Catch limits but offer promising tools for future management. TACs set limits on the overall collection of a species or group of species in a given year. Although TACs are not widely utilized, spe- 4.5. Other promising directions cies-specific TACs are currently used in the coral fishery in Austra- lia, whereas aggregate TACs (in the form of export quotas) are used Other potential strategies to reform the trade include aquacul- in several island nations including the Maldives and Tonga (Ta- ture and industry reform. Although out of the scope of this review, ble 3). These aggregate quotas set catch limits at different levels which focuses on state, national, and international regulations and for groups of species, often based on historical levels of export management, it is worth noting that aquaculture holds promise for (Sections 3.2.1.3–3.2.1.4). Oftentimes the quotas are not species- alleviating collection pressure on wild populations (Moorhead and specific and insufficient data are available to determine whether Zeng, 2010; Olivotto et al., 2011). Aquaculture has already reduced fishing effort is currently over or under sustainable levels. Though the collection of wild fishes and invertebrates, including clownfish, catch limits can be beneficial, they can lead to competition among seahorses, tridacnid clams, and several hard corals. These benefits, fishers to fish as quickly as possible, which endangers humans, cre- however, will depend on the extent that the supply of cultured ates economic inefficiencies, and can have long-term consequences individuals fulfills the market demand. for fish populations (Hilborn et al., 2005). 5. Conclusions 4.3. Rights-based management Despite the difficulties in managing the coral reef wildlife trade, As a type of catch share or rights-based program, ITQs allocate a some examples of successful management demonstrate that sus- tradable portion of the annual TAC to an individual or group, there- tainable reform of the trade is possible. Some programs in export- by incentivizing the long-term maintenance of the fishery (Costello ing countries, such as Florida’s moratorium on corals, Hawaii’s et al., 2008). For instance, transitioning to an ITQ program in Flor- FRAs, and the Maldives’ and Tonga’s no-take zones and tiered quo- ida would allow the active collectors to ‘‘buy out’’ the inactive col- ta systems, represent steps towards reforming the trade. Similarly, lectors to gain a larger share of the total catch, making the fishery legislation in importing countries, such as the E.U.’s Wildlife Trade more efficient. Nevertheless, establishment of an ecologically- and Regulation and Australia’s ‘‘whitelist,’’ can also improve the trade’s economically-successful ITQ program requires the TAC to be set environmental sustainability by proactively restricting and moni- appropriately, traditionally through data-intensive stock assess- toring imports when there are concerns about the conservation ment models. For this reason, the rarity of ITQs and scientifically- status, disease risk, or invasiveness of certain species. In contrast set TACs in ornamental fisheries is partially attributable to data to the U.S.’s reactionary approach to managing the trade, the pre- and management capacity limitations. cautionary approach adopted by the E.U. and Australia allows Spatial rights-based management, e.g., TURFs or exclusive com- importing countries more control and oversight. 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