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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
a r t i c l e i n f o
Article history:
Received 23 August 2013
Received in revised form 12 November 2013
Accepted 14 November 2013
Keywords:
Aquarium trade
Coral reef conservation
Coral reef sheries
Ornamental sheries
Sustainable sheries management
a b s t r a c t
Trade in ornamental coral reef wildlife supports a multi-million dollar industry but in some places threat-
ens vulnerable coral reef species and ecosystems due to unsustainable practices and lack of effective reg-
ulation. To supply this trade, shers sometimes deplete sh populations and rely on practices, such as
cyanide shing, that harm coral reef organisms and habitats. The number of countries involved, dispersed
shing localities, and the diversity of species in trade present considerable impediments to conservation
and management. For instance, traditional sheries management techniques such as stock assessments
and total catch limits may not be feasible for ornamental sheries, which are characterized by limited
data on population dynamics, stock status, and collection effort, as well as instances of illegal, underre-
ported, and unregulated shing. A number of strategies to monitor, regulate, and manage the trade have
been implemented with varying efcacy. In order to learn from previous attempts and identify promising
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 shery, 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 identied here and utilization of
data-limited methods from food sheries.
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
0006-3207/$ - see front matter 2013 The Authors. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.biocon.2013.11.025
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: thornhill.dan@gmail.com (D.J. Thornhill).
Biological Conservation 169 (2014) 225237
Contents lists available at ScienceDirect
Biological Conservation
j our nal homepage: www. el sevi er. com/ l ocat e/ bi ocon
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 236
Appendix A. Supplementary material . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 236
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 236
1. Introduction
1.1. The ornamental coral reef wildlife trade and its ecological
consequences
The trade in ornamental coral reef wildlife, which includes the
aquarium, jewelry, and curio trades, supports a multi-million dol-
lar industry (Grey et al., 2005; Wabnitz et al., 2003); however,
collection practices and a lack of effective regulation and manage-
ment may threaten vulnerable coral reef species (Thornhill,
2012;Tissot et al., 2010). Many species are targeted to supply this
trade, primarily based on their size and aesthetics. Examples in-
clude brightly-colored juvenile or male shes; stony corals with
attractive skeletons or large, colorful polyps; and mollusks with
colorful, ornate shells. The effects of the collection and trade in
ornamental wildlife are less studied than other threats to coral
reefs including climate change, ocean acidication, overshing,
and nutrient pollution in part due to the complexity of the
trade, which targets hundreds of sh and invertebrate species
(Rhyne et al., 2012;Wabnitz et al., 2003). Nevertheless, collection
has reduced certain populations, introduced invasive species, and
in rare cases caused localized extirpations (reviewed in Thornhill,
2012). For example, one of the most-studied ornamental species,
the yellow tang (Zebrasoma avescens) in West Hawaii, has de-
clined in some collection areas, but is stable or recovering within
reserves (Tissot and Hallacher, 2003; Tissot et al., 2004; Williams
et al., 2009). In the Sulawesi Archipelago of Indonesia, endemic
Banggai cardinalsh (Pterapogon kauderni) have declined in abun-
dance to the point of localized extirpations, and are now consid-
ered endangered (International Union for the Conservation of
Nature, 2012; Kolm and Berglund, 2003; Vagelli, 2008). Inverte-
brates collected for trade also exhibited population declines; for
instance, densities of symbiotic giant anemones in the Cebu re-
gion of the Philippines declined over 80% (Shuman et al., 2005).
Even stony corals (order Scleractinia), the foundation of coral reef
ecosystems, are collected. Their collection can reduce coral cover
and alter species compositions and population demographics
(Knittweis and Wolff, 2010; Ross, 1984). Yet many ornamental
sheries have continued for decades and have not collapsed. De-
spite the potential impacts of collection, the stock status and sus-
tainable harvest levels of most ornamental species remain largely
unknown and unmonitored.
Beyond the unevaluated status of targeted species and potential
population declines, destructive practices, including cyanide sh-
ing, are sometimes used to collect coral reef wildlife for trade. Cya-
nide is dispensed onto coral colonies in order to anesthetize and
easily capture sh (Rubec et al., 2001). Within minutes, these tox-
ins kill an estimated 50% or more of exposed species, with addi-
tional deaths occurring hours to days later (Hanawa et al., 1998;
Rubec et al., 2001). Non-targeted species like corals, anemones,
and other habitat forming species are also exposed and can be in-
jured or killed. In particular, cyanide blocks respiration in corals,
causing coral bleaching and mortality (Cervino et al., 2003; Jones
and Steven, 1997). The current prevalence of cyanide shing is un-
known. Cyanide shing occurs in at least 15 countries, including
major exporters like Indonesia and the Philippines, though its
use is apparently less prevalent today than 20 years ago (Bruckner
and Roberts, 2008). Other prevalent shing methods also injure
and kill both targeted and non-targeted species, including abrasive
nets, spears, and crushing of corals to capture sh (Gonzales and
Savaris, 2005; Thornhill, 2012).
The coral reef wildlife trade can also affect importing countries
through the introduction of exotic and invasive species (Semmens
et al., 2004). The most prominent example is the introduction of
lionsh (Pterois volitans and P. miles) from the Indo-Pacic into
the Caribbean and western Atlantic (Betancur et al., 2011). Since
the 1990s, lionsh spread along the U.S. east coast and throughout
the Caribbean (Betancur et al., 2011). These predators eat large
quantities of native shes resulting in reduced recruitment of
Atlantic coral reef shes, competition with native predators such
as grouper, reduction of grazers like surgeonsh and parrotsh,
and concomitant ecological changes (Albins and Hixon, 2008; Les-
ser and Slattery, 2011).
The broader ecological consequences of collection for the trade
are understudied from both sheries and ecological perspectives.
The coral reef wildlife trade targets species ranging from the foun-
dation of coral reefs (e.g., corals and live rock for aquariums and
home dcor) to top predators (e.g., sharks for teeth, jaws, and other
curio items; Grey et al., 2005; Knittweis and Wolff, 2010; Ross,
1984). One concern is that characteristics that make sh and inver-
tebrate species attractive to aquarium enthusiasts can also lead to
disproportionate impacts on the reef when these species are re-
moved. For example, hobbyists preferences for species that con-
sume algae or parasites could drive reductions of these species
on the reef, potentially with trophic effects (e.g., Edwards and
Shepherd, 1992; Rhyne et al., 2009; but see Tissot et al., 2004).
The diversity of species and complexity of interactions on coral
reefs make understanding population dynamics of coral reef wild-
life and predicting the ecosystem-level consequences of their re-
moval difcult.
1.2. Management challenges
The coral reef wildlife trade exhibits both notable similarities
and differences from other capture sheries, including characteris-
tics that can impede resource management. Organisms from nearly
every trophic level are collected, making identication and moni-
toring of collected species exceptionally challenging. The life his-
tory, demographic, and population data required for traditional
stock assessments are typically unavailable (Fujita et al., in press;
Honey et al., 2010). Even countries with higher management and
enforcement capacity, such as the U.S., generally do not conduct
stock assessments for ornamental species. In general, stock assess-
ments for many species in the trade may be difcult because rare
species are targeted. For rare species, accurate estimates of popula-
tion size are difcult to obtain because their probability of detec-
tion in surveys is quite low (e.g., see Chads et al., 2008). It is
therefore difcult for managers to monitor populations and reefs,
enforce regulations, document catches, and develop accurate pop-
ulation models.
Many locations have few (if any) regulations addressing the cor-
al reef wildlife trade. In countries where regulations exist, enforce-
ment is hindered by inaccurate reporting of landings (e.g., Walsh
et al., 2004; Rhyne et al., 2012) and illegal collection (Barber and
Pratt, 1997). Similar to issues with trans-boundary sheries
(McWhinnie, 2009), roving collectors are common in Southeast
Asian sheries and have little incentive to protect coral reef
resources in a given area, because they may never return to the
226 L.E. Dee et al. / Biological Conservation 169 (2014) 225237
same collection site (Amos and Claussen, 2009; Marine Aquarium
Market Transformation Initiative, 2006).
A complex supply-chain creates challenges for managing the
trade, especially in Southeast Asia. Similar to capture sheries,
many countries supply the trade and animals change hands
many times between collection and export with no system to
monitor this chain of custody (Amos and Claussen, 2009; Nixon
et al., 2012). At each stage of the supply chain, animals from var-
ious sources are pooled, so separating sustainably-harvested
wildlife from their unsustainable counterparts is difcult (Amos
and Claussen, 2009). This supply chain complexity complicates
reform in several ways. First, high supply-chain mortality can
lead to market inefciencies and drive overharvesting (Wabnitz
et al., 2003). Second, the complex supply chain presents chal-
lenges for reducing destructive collection practices, like cyanide
shing, since cyanide is increasingly difcult to detect with time
(Mak et al., 2005; but see Vaz et al., 2012). Third, import-docu-
mentation requirements are challenging when organisms change
hands many times. All of these challenges would benet from a
shorter and more vertically-integrated supply chain (Nixon et al.,
2012).
Despite the many similarities between ornamental sheries and
most capture sheries in coral reefs, several unique characteristics
of sheries that supply the coral reef wildlife trade demand new
management approaches and present difculties (Donaldson,
2003). Two aspects differ greatly:
(1) value is per individual rather than by biomass; and
(2) for the aquarium trade, animals must remain alive in order
to be sold.
Furthermore, collection of aquarium shes differs from harvest-
ing food shes. It often targets juveniles, affecting the populations
age structure, and brightly-colored males, potentially skewing the
sex ratios of the population.
1.3. Objective
Overcoming barriers to effective management and regulation is
daunting given that trade includes over 1800 species of sh, hun-
dreds of species of coral, over 500 species of other invertebrates,
and live rock (Rhyne et al., 2012; Wabnitz et al., 2003;). Exports
emerge from at least 45 countries while imports largely go to the
U.S. (64%), the E.U. (14%), and Japan (7%) (Tissot et al., 2010;
Wabnitz et al., 2003). Our objective is to identify successful regula-
tion and management approaches that could potentially be repli-
cated elsewhere by reviewing select management practices
around the world. For purposes of this discussion, we consider reg-
ulation to be a set of codied rules established to govern the trade,
and management to be the implementation and enforcement of
various conservation and sheries measures, including regulations.
This paper does not attempt to comprehensively review manage-
ment effectiveness in each country involved in the ornamental
coral reef wildlife trade; instead, it highlights the range of manage-
ment techniques currently used or with potential to manage the
trade. We rst examine the application of the Convention on Inter-
national Trade in Endangered Species of Wild Fauna and Flora
(CITES) to govern the coral reef wildlife trade on an interna-
tional-level (Section 3.1). Second, we review the laws, manage-
ment practices, and sheries management plans used for
ornamental sheries in exporting and importing countries (Sec-
tion 3.2). We conclude by highlighting strategies that have been
used successfully in other data-limited capture sheries that may
hold promise if they were applied to ornamental sheries
(Section 4).
2. Materials and methods
We reviewed the available peer-reviewed and grey scientic lit-
erature, as well as government websites and reports, on regula-
tions and management practices by locality for the ornamental
coral reef wildlife trade. The review focused primarily on practices
within the aquarium trade, over other ornamental trade sectors
(e.g., curios), because much of available conservation and manage-
ment literature is on this topic. Literature was compiled primarily
from online databases and search engines, including Web of Sci-
ence (thomsonreuters.com/web-of-science), Google Scholar (scho-
lar.google.com), PubMed (ncbi.nlm.nih.gov/pubmed), and Science
Direct (sciencedirect.com). Search terms included some combina-
tion of the terms wildlife trade, aquarium trade, curio trade, or or-
namental sheries with country names, management practices,
and names of the most heavily-traded species (as noted in Rhyne
et al., 2012; Wabnitz et al., 2003; Wood, 2001). These sources were
supplemented by more targeted searches for papers identied dur-
ing the search process (e.g., from the references of another paper or
report), suggestions from colleagues, and informal interviews with
management practitioners, conservationists, and academics (see
acknowledgements).
Countries that lacked source information were subsequently
excluded from this review despite their contributions to the supply
of coral reef wildlife (e.g., Mexico, Cook Islands, Solomon Islands,
and Taiwan). Additional countries were excluded because no
post-1996 source documentation was located (e.g., Samoa and
the Cook Islands). Haiti was the one exception; it was maintained
despite few sources on its practices due to its importance as an
exporting country (Rhyne et al., 2012). This resulted in a broad re-
view of existing management practices based on international
agreements, the practices of three major wildlife importers (the
U.S., European Union, and Australia), and the practices of 18 wild-
life-exporting nations, states, and territories (Australia, Bahamas,
Eritrea, Fiji, Haiti, Indonesia, Kiribati, Maldives, Philippines, Sri
Lanka, Papua New Guinea, the Kingdom of Tonga, U.S.-Florida,
U.S.-Guam, U.S.-Hawaii, U.S.-Puerto Rico, Vanuatu, and Vietnam).
Because this review examines international, national, and regio-
nal regulations and management, inevitably local and non-govern-
mental organization (NGO) efforts have been overlooked. For
example, during the Marine Aquarium Market Transformation Ini-
tiative within the Philippines, some villages developed total allow-
able catches for ornamental sh species and restricted shing
permits to villagers (D. Ochavilla, personal communication). Addi-
tionally, in both Indonesia and the Philippines, several villages
developed sheries management plans in conjunction with NGO
partnerships, though these plans were not implemented at the na-
tional level. Due to length constraints, such local initiatives are not
covered here.
3. Results and discussion
3.1. International agreements regulating the trade
Several international treaties and governing bodies set the
foundation for nations to regulate harvesting of marine species
(Table 1; Fidelman et al., 2012), yet few have been applied to the
trade in coral reef species. The primary international mechanism
regulating the coral reef wildlife trade is the Convention on Inter-
national Trade in Endangered Species of Wild Fauna and Flora
(CITES), an agreement among 175 countries (CITES, 2012). Since
1975, CITES has aimed to ensure that the international trade in
wildlife does not threaten species with extinction or endanger-
ment. The species covered by CITES are listed in three Appendices,
L.E. Dee et al. / Biological Conservation 169 (2014) 225237 227
corresponding to the level of protection (Kinch and Teitelbaum,
2008):
Appendix I provides the highest level of protection to spe-
cies threatened with extinction and vulnerable to interna-
tional trade. It strictly prohibits all international trade for
commercial purposes. For instance, the hawksbill turtle
(Eretmochelys imbricata) is listed on Appendix I, prohibiting
all international trade in this species for jewelry and luxury
items.
Appendix II lists species that are not currently in danger of
extinction but are threatened by over-exploitation. Export
permits for Appendix II specimens can be issued by the
exporting country only when (a) the Scientic Authority
has advised that export will be non-detrimental to the sur-
vival of that species or when a Management Authority reg-
ulating exports is satised that (b) the specimen was not
obtained illegally and (c) risk of injury and cruel treatment
during transport was minimized for living specimens.
Appendix II covers over 30,000 species, including the fol-
lowing coral reef wildlife species: over 2000 hard corals
(including all scleractinians), all giant clams (Tridacna and
Hippopus spp.), three species of hammerhead sharks
(Sphyrna spp.), and all seahorses (Hippocampus spp.) (CITES,
2012; Jones, 2008). Although a number of other coral reef
species have been proposed for Appendix II listing, for
instance red and pink corals (Corallium and Paracorallium
spp.) and the Banggai cardinalsh, these listing proposals
were either withdrawn or rejected (Vagelli, 2008).
Appendix III lists species that are protected by at least one
member that requests enforcement assistance from other
CITES members. In July 2008, China listed four Corallium
species in CITES Appendix III, adding permit requirements
for export of these corals from China (CITES, 2012).
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
Nature Red List of Threatened Species
Conservation Inventory on conservation status and extinction risk for species. Provides scientic advice, but
lacks regulatory authority (IUCN, 2012; Vagelli, 2008)
1973 Convention on International Trade in
Endangered Species
Trade Restricts international trade in listed species. Protects only a few species in the trade and the
process for listing additional species is cumbersome (Bruckner, 2001; Tissot et al., 2010)
1982 United Nations Convention on the Law of
the Sea
Fisheries Establishes management responsibility within Economic Exclusive Zones. Mentions responsible
shing practices within jurisdiction but is broad in scope and lacks specic guidelines.
1992 Agenda 21 and the Rio Declaration on
Sustainable Development
Fisheries Provides criteria for sustainable management of marine resources, funding mechanisms, and
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
Fisheries Provides guidelines for sustainable sheries management. Aims to reform destructive shing
practices, though lacks explicit and operational denitions for sustainable management and
overshing (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 difcult 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
and Management Act
Fisheries/
Trade
Governs sheries management within the Exclusive Economic Zone. This Act does not extend to
imports of wildlife caught by illegal shing 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 conscate 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 sh health certications for ornamental imports; assessment of countries for
suitability of imports. Established animal health and welfare requirements for imports of sh 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 shing zones
1992 Fisheries Management Regulations 1992 Fisheries Develops specic regulations for implementing the Fisheries Management Act
1994 Fisheries Act of 1994 Fisheries Provides framework and guidelines for sustainable sheries management (Ryan and Clarke,
2005)
1999 Environmental Protection and Biodiversity
Conservation Act
Fisheries/
Trade
List of acceptable species for import and only allows live sh from approved countries (Morrisey
et al., 2011)
228 L.E. Dee et al. / Biological Conservation 169 (2014) 225237
Note that when CITES listed animals are aquacultured, or born
and reared in captivity, these species move to the next Appendix
(e.g., fromAppendix I to II). This is done to reect the generally low-
er ecological impact of aquaculture compared to wild collection.
Most of the thousands of species involved in trade are not CITES
listed (CITES, 2012). The small number of listed species may not be
indicative of the status of trade species, since few species in the
coral reef wildlife trade have ever been evaluated for extinction
risk by the International Union for the Conservation of Nature or
CITES authorities (McClenachan et al., 2011), including only one
of the top-10 traded aquarium shes, Centropyge bicolor (Table 2).
For listed species, the effectiveness of CITES protection has been
questioned (Jones, 2008; Tissot et al., 2010). We illustrate these is-
sues through two examples, Banggai cardinalsh and scleractinian
corals (Supplemental Text).
3.2. Country-level regulations and management
The United Nations Convention on the Law of the Sea estab-
lished Exclusive Economic Zones (EEZs) that grant coastal coun-
tries jurisdiction over their near-shore marine resources and the
responsibility to conserve and management natural resources. Spe-
cies collected for the aquarium and ornamental trades are almost
entirely shallow water, reef-associated species that reside within
EEZs (Supplemental Table 1); therefore, countries have greater po-
tential control over the harvest of coral reef wildlife in contrast to
the many highly-migratory species targeted by food sheries. Na-
tions have implemented various measures to protect coral reef
species, including marine protected areas (MPAs), harvest regula-
tions (e.g., gear type, permits, quotas), and/or required documenta-
tion (e.g., quarantine certication) (Morrisey et al., 2011; Smith
et al., 2008; Wood, 2001). These laws and initiatives either directly
(e.g., species-specic quotas for aquarium shes) or indirectly (e.g.,
no-take reserves that protect coral reef habitats and associated
wildlife) regulate collection. The success of management regimes
and regulations varies greatly. In Sections 3.2.13.2.2 and Tables
1, 3 and 4, we highlight examples of strategies adopted by both
importing and exporting countries.
Management actions currently or potentially used for ornamen-
tal trade species (Table 3):
Gear restrictions are commonly used in both food and
ornamental sheries to either prevent negative impacts
on habitats or on non-target species (bycatch). Ornamental
sheries commonly restrict gear usage and shing meth-
ods, including cyanide shing.
Total bans prohibit collection of certain species, which
should allow for populations to recover provided that
reproductively-viable populations remain, habitat is pro-
tected, and poaching is minimized. For instance, species
listed under CITES Appendix I and the Endangered Species
Act in the U.S. are banned from trade. Similarly, the Philip-
pines banned collection of giant clams, seahorses, and black
and scleractinian corals.
Limited effort programs attempt to control total harvest
by limiting overall harvesting effort. In the aquarium trade,
effort limitation has only restricted who can sh. Although
season restrictions are common in capture sheries, to our
knowledge, they are not widely used in ornamental
sheries.
Total allowable catch (TAC) is an aggregate annual quota
for a shery that is often set using stock assessments
complex population models that determine the status of a
shery and predict how populations will respond to har-
vest rules. Country-level export quotas, aggregate TACs on
the number of sh that can be exported in a given year,
are commonly employed by Pacic island nations.
Rights-based sheries management, sometimes called
catch shares, refers to sheries management strategies
that allocate exclusive access to a portion of the TAC to
individuals or groups of shers (Costello et al., 2008). Catch
share programs establish property rights to an otherwise
common-pool or open-access resource, and they also exist
in the form of traditional marine tenure (Hilborn et al.,
2005). In some ornamental sheries, property rights are
established through exclusive shing zones for local com-
munities or individuals called Territorial User Rights Fish-
eries (TURFs).
Spatial closures and zoning aim to protect biodiversity
and allow for the recovery of shed species by prohibiting
or zoning shing and other impactful activities in certain
areas (e.g., no-take marine reserves and MPAs). Fish
replenishment areas (FRAs) in West Hawaii specically
prohibit the collection of ornamental shes (Tissot et al.,
2004).
Size limits restrict shing or collection to a species above
or sometimes below a certain size threshold to protect a
certain portion of the breeding stock and allow the
Table 2
International Union for Conservation of Nature Red List of Threatened Species assessments for the top-10 aquarium (Wood, 2001) versus food shes (FAO, 2008).
Fishery Common name Scientic name IUCN Assessment
Aquarium Blue green damselsh Chromis viridis Not evaluated
Aquarium Sapphire devil Chrysiptera cyanea Not evaluated
Aquarium Yellow tang Zebrasoma avescens Not evaluated
Aquarium Clown anemonesh 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 angelsh 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 decient
Food Japanese anchovy Engraulis japonicus Not evaluated
Food Yellown tuna Thunnus albacares Near threatened
L.E. Dee et al. / Biological Conservation 169 (2014) 225237 229
population to grow. A 10-cm minimum size limit is often
used in seahorse sheries (Foster and Vincent, 2005).
National regulations on import/export practices can
impose requirements (e.g., documentation, permitting, or
quarantine procedures) that can regulate wildlife import,
export, and handling practices. These requirements can
help control the spread of disease and invasive species as
well as the mortality of species in the supply chain. For
instance, Australia imposes stringent import requirements
(reviewed in Morrisey et al., 2011).
Case studies highlighting the use of these strategies in both
exporting and importing countries are presented in Sections 3.2.1
and 3.2.2, respectively.
3.2.1. Exporting nations
3.2.1.1. Indonesia. At the epicenter of coral reef biodiversity, Indo-
nesia has consistently been a top exporter of coral reef wildlife for
over 30 years (Rhyne et al., 2012; Wabnitz et al., 2003). Histori-
cally Indonesian reefs were open to all extractive uses, but the
government has recently attempted to better regulate its natural
resources (Amos and Claussen, 2009; Nurhidayah, 2010). The
Ministry of Marine Affairs and Fisheries formulates national policy
for sheries management and conducts resource assessments
(Dudley and Ghofar, 2006). Management is divided into 11 sher-
ies management areas and several sheries groups (Dudley and
Ghofar, 2006; CCIF, 2013). Coral reef sh, including ornamental
and food sh species, comprise one group (Dudley and Ghofar,
2006). Since the late 1990s, local authorities have been primarily
responsible for resource utilization, conservation, and develop-
ment and implementation of management plans (Dudley and
Ghofar, 2006; Fidelman et al., 2012; Nurhidayah, 2010; Timotius
et al., 2009).
Management measures for ornamental species include busi-
ness licensing systems, a 1985 ban on destructive shing practices
including cyanide shing, harvest quotas on stony corals, and
MPAs (Dudley and Ghofar, 2006; Pet and Pet-Soede, 1999). Despite
this range of measures, effective management is stymied on many
levels, leading Indonesian sheries to be described as de facto open
access (CCIF, 2013). For example, sh and vessel licensing require-
ments are not consistently enforced, and small-scale shers are not
required to obtain licenses. The prevalence of small-scale shing
and the lack of systematic requirements limit the effectiveness of
licensing (Dudley and Ghofar, 2006; CCIF, 2013). The ban on cya-
nide shing is rarely, if ever, enforced (Pet and Pet-Soede, 1999).
Implementing management at regional and local scales is chal-
lenged by the decentralized governance structure, a lack of
enforcement and resource management capacity, and corruption
(Amos and Claussen, 2009; CCIF, 2001; Dudley and Ghofar, 2006;
Nurhidayah, 2010; Pet and Pet-Soede, 1999). This decentralized
management ineffectively supervises roving collectors a major
source of overharvesting in Indonesia who commonly travel be-
tween different jurisdictions to collect while ignoring collection
regulations (Amos and Claussen, 2009; CCIF, 2013; Marine Aquar-
ium Market Transformation Initiative, 2006).
Although there are not harvest quotas for most ornamental spe-
cies, Indonesia has established collection quotas for many sclerac-
tinian corals (Green and Shirley, 1999). Approximately 1 million
live coral pieces are permitted for export annually, including a
growing number of farmed corals (Wood et al., 2012). The quotas
efcacy is challenged by weak enforcement and a lack of popula-
tion data to set total-allowable catches (Green and Shirley, 1999).
A comparison of the quotas to population assessments indicated
that depending on the targeted genus 196% of available coral
populations could be collected thereby allowing for over-exploita-
tion of certain corals (Bruckner and Borneman, 2006). Oftentimes
there are no size restrictions on collection, allowing for the re-
moval of important demographic groups (Bruckner and Borneman,
2006).
The lack of stock assessments and quotas for the many species
leave MPAs as the most widely used measure for coral reef sh
conservation in Indonesian (Dudley and Ghofar, 2006). Indonesia
maintains a reserve system, including national parks, comprising
2% of Indonesias EEZ (World Bank, 2013). MPAs have been shown
to be a useful management tool for marine ornamental species
(e.g., Tissot et al., 2004), but the presence of MPAs alone does not
ensure effective management. For instance, a more extensive
MPA system is needed to effectively maintained connectivity in
the popular aquarium coral Heliofungia actiniformis (Knittweis
et al., 2009) Thus, although Indonesia utilizes management tools
ranging from licensing and gear restrictions to quotas and MPAs,
various studies have called for additional measures and improve-
ments (Bruckner and Borneman, 2006; Dudley and Ghofar, 2006;
Green and Shirley, 1999; Knittweis et al., 2009; Knittweis and
Wolff, 2010).
3.2.1.2. The Philippines. The Philippines is another primary export-
ing nation of ornamental coral reef wildlife, with major source
localities in Bataan, Batangas, Bohol, Cebu, Davao, Palawan, and
Zambales (Ochavillo et al., 2004; Rhyne et al., 2012). Overall the
Philippines supplies the majority approximately 55% of the
marine aquarium sh imported into the U.S. (Rhyne et al., 2012).
The Philippines conducts limited national-level sheries manage-
ment under the Philippine Fisheries Code. Similar to Indonesia,
sheries management is largely decentralized; Local Government
Code of 1991 delegated management authority primarily to
barangays or local government units (Gonzales and Savaris,
2005). In most local jurisdictions, there is little management or
enforcement capacity and poor data collection (Gonzales and Sav-
aris, 2005; Ochavillo et al., 2004).
Fishers in the Philippines are typically required to have a license
or appropriate accreditation to collect coral reef wildlife (Gonzales
and Savaris, 2005). However, there are no limits on the total num-
ber of licenses (Gonzales and Savaris, 2005), reducing their effec-
tiveness as a management tool to control shing effort (FAO,
2013). Additionally, roving collectors, who often ignore licensing
requirements, make up a sizeable portion of collection activity
(Marine Aquarium Market Transformation Initiative, 2006; S.
Green, personal communication).
Beyond licensing of collectors, the Philippines prohibits export
of species listed on Appendix II of CITES, including stony corals
and seahorses. The stony coral trade was once based primarily
on Philippine corals until collection and export was outlawed
(Ross, 1984). Commercial collection of stony corals continued for
several years, especially in the Cebu region, but the coral trade ulti-
mately dwindled (Ross, 1984). The Philippines also banned trade in
giant clams and seahorses following their listing in CITES Appendix
II in 1996 and 2002, respectively (Vincent et al., 2011; Wabnitz
et al., 2003). For seahorses, exports from the Philippines had ceased
by 2006 (Vincent et al., 2011) and recent CITES data indicate a glo-
bal reduction in the seahorse trade, possibly resulting from the
Philippine ban (Evanson et al., 2011). For most species, there are
no catch limits, species quotas, size limits, or restocking programs
(Gonzales and Savaris, 2005; Ochavillo et al., 2004). Perhaps as a
result of the few management measures in place, overshing of
coral reef species is reported (e.g., Ross, 1984; Sadovy et al.,
2001; Shuman et al., 2005).
Finally, the Philippines controls exports of coral reef wildlife
through a permitting process and limited testing for cyanide in live
sh. Although anticyanide laws exist, these bans are commonly
unenforced (Ochavillo et al., 2004). In the late 1980s and 1990s,
the government and the International Marinelife Alliance jointly
230 L.E. Dee et al. / Biological Conservation 169 (2014) 225237
established a set of Cyanide Detection Laboratories (CDL) (Barber
and Pratt, 1997; Barber, 1999; Rubec et al., 2001). However, detec-
tion of cyanide is technically difcult, and the accuracy of the CDL
tests has been questioned (Mak et al., 2005; Bruckner and Roberts,
2008). Currently, there is only one active CDL, so very few exported
shipments are tested. Despite this, the recent innovation of a new
and more reliable cyanide test, which uses optical ber technology
to detect thiocyanate, may enable the Philippines and others to
better control the trade in cyanide-caught sh (Vaz et al., 2012).
3.2.1.3. The Maldives. Since the inception of the Maldives aquarium
trade in the 1980s, the government has monitored the collection
and export of coral reef sh (Edwards and Shepherd, 1992). In
1988, concern over the trades sustainability and conicts with
the diving-tourism industry led the government to establish an
aggregate export quota of 100,000 coral reef sh and invertebrates
per year (Edwards and Shepherd, 1992). Collectors and exporters
were required to report the volume of exported coral reef sh to
customs ofcials and shing was only permitted until the quota
was reached (Edwards and Shepherd, 1992). Although this precau-
tionary measure was laudable, it insufciently protected species
from over-exploitation. A combined analysis of export data, eld
surveys of sh abundance, and rough estimates of Maximum Sus-
tainable Yield concluded that many coral reef species were poten-
tially overexploited by over-collection under this aggregate quota
system (Edwards and Shepherd, 1992).
Further management measures were added in response to such
concerns, for example a 1997 ban on destructive moxy nets (Ed-
wards and Shepherd, 1992; Saleem and Islam, 2008). Cyanide sh-
ing, although never reported in the Maldives, was also banned
(Saleem and Islam, 2008). In 1995 and 1999, twenty-ve MPAs
were established as no-take reserves (Saleem and Islam, 2008).
Still, monitoring and enforcement for these systems were lacking,
leading the government to implement a species-specic quota pro-
gram (Saleem and Islam, 2008; Wood, 2001).
This latest Maldives management system divides sh into three
categories or tiers. Category A bans export of 17 species that are
considered highly vulnerable (Saleem and Islam, 2008; see Saleem
and Adam, 2004 for lists of species in each category). Furthermore,
parrotsh, puffer sh, porcupine shes, eels, giant clams, and hard
corals other than Tubipora musica are barred from export under
this system (Saleem and Islam, 2008). Chromis viridis, a popular
aquarium species (Rhyne et al., 2012), is prohibited due to its use
as bait for tuna shing (Saleem and Islam, 2008). The second tier
(Category B) includes 66 species managed under species-specic
quotas (Saleem and Adam, 2004; Saleem and Islam, 2008). The
remaining 71 species (Category C) are managed under a 300,000
organism aggregate quota for the entire country (Saleem and Is-
lam, 2008). The efcacy of the tiered quota system is currently un-
der evaluation by the Marine Research Centre and Marine
Conservation Society.
Saleemand Islam (2008) noted the apparent effectiveness of the
new system, but also highlighted signicant challenges, including
weak enforcement, unnecessary bureaucracy, a lack of monitoring
ofcials familiar with exported species, confusion between com-
mon and scientic names for exported species, under-reporting
of value to avoid purchasing additional licenses, and roving collec-
tors. By incorporating quotas built on data from species-specic
stock estimates and export records, the tiered system is superior
to the previous open-access system. However, these data are of
uncertain reliability and have not been applied to monitor changes
in the stocks of collected species or for setting appropriate catch
limits (Saleem and Islam, 2008).
3.2.1.4. The Kingdom of Tonga. The Kingdom of Tonga is an active
exporter of sh and invertebrates for the ornamental aquarium
trade. Tonga uses a licensing system to cap the total number of
businesses collecting and exporting coral reef wildlife at ve com-
panies (Fisheries Management and Planning Section, 2008; Matoto
et al., 1996). On the reef, collectors must adhere to strict gear con-
trols that ban the use of poisons and damaging gear, only allow the
use of hand or barrier nets, and restrict the use of scuba diving to
authorized collectors (Fisheries Management and Planning Section,
2008). Limiting the spatial extent and amount of collection effort,
Tonga connes aquarium sh and invertebrate collection to certain
areas and has a blanket quota of 100,000 sh per exporting com-
pany annually (Fisheries Management and Planning Section,
2008). This aggregate volume of sh is considered to be a negligi-
ble fraction of the biomass of targeted species (Matoto et al.,
1996), suggesting that collection is largely sustainable. Neverthe-
less, no stock assessments have been conducted to determine the
status of targeted species.
Species that are susceptible to overharvesting may be insuf-
ciently protected under this system, because management is not
conducted on a species-by-species basis. Although no quotas are
placed on the harvest of invertebrates or soft corals, Tonga prohib-
its the collection of dead hard corals and live rock. Tonga also re-
quires exporters to provide detailed reports on the volume of
animals exported (Marine Aquarium Fishery Management Plan,
2008). This suite of management tools provides Tonga with a rela-
tively-comprehensive management program, particularly for
aquarium shes.
3.2.1.5. Australia. Australia exports wildlife to supply the trade, and
this collection is regulated under the national Environmental Pro-
tection and Biodiversity Conservation Act of 1999. While allowing
the export and trade in wildlife, this Act also places responsibility
on state governments to develop sheries management plans
(Department of Primary Industries and Fisheries, 2009). Approxi-
mately 60% of collection for the coral reef wildlife trade in Australia
occurs in Queensland where three aquarium sheries operate: the
Queensland Marine Aquarium Fish Fishery (MAFF), the Queensland
Coral Fishery (QCF), and the Coral Sea Fishery.
The Queensland Government regulates the MAFF and the QCF
by restricting destructive gear types and limiting entry through a
licensing system, which has not issued new commercial licenses
since 1997 (Roelofs and Silcock, 2008). Both sheries operate in
the Great Barrier Reef Marine Park that protects approximately
30% of the available habitat from shing. The MAFF (48 licenses)
employs different combinations of management techniques
including catch quotas, bans on certain species, size limits, and sea-
sonal closures (Roelofs, 2008a). For one, MAFF collection rates are
compared to sustainability benchmarks based on ecological risk
assessments (Roelofs, 2008a; Roelofs and Silcock, 2008).
The QCF (59 licenses), also state managed and regulated, is pri-
marily managed under the Policy for the Management of the Coral
Fishery (Department of Primary Industries and Fisheries, 2009).
Management under this policy includes a total allowable commer-
cial catch (TACC) of 200 tonnes, separated into 140 tonnes for orna-
mental corals (coral skeletons of acroporids and pocilloporids
collected alive and dried for ornamental purposes) and live rock.
The remaining 60 tonnes is allocated to specialty coral (hard
and soft coral and anemone species taken for live aquaria). The
smaller TACC for specialty coral recognizes that these species
may not be as highly productive as other ornamental coral species
(but see Jones, 2011). PMS and risk assessments also monitor the
status of this sheries (Roelofs, 2008b).
The adjacent Coral Sea Fishery (with 2 licenses) falls under the
jurisdiction of the Australian Fisheries Management Authority and
includes the collection of marine shes and limited collection of
live rock (Australian Fisheries Management Authority, 2011). Col-
lection is monitored and compared to tiers of precautionary catch
L.E. Dee et al. / Biological Conservation 169 (2014) 225237 231
thresholds. Management responses are initiated when the thresh-
olds are reached.
3.2.1.6. The United States: Hawaii and Florida. The U.S. states of Ha-
waii and Florida and territories of Puerto Rico and Guam supply the
coral reef wildlife trade. Each location has adopted different man-
agement measures for their sh and invertebrate sheries (Table 3).
Here, we focus on the management practices adopted in Hawaii
and Florida.
3.2.1.6.1. Spatial management in Hawaii. The Hawaiian aquar-
ium shery has grown substantially over its 50-year history into
the states second-largest inshore shery. Annually, the shery
lands over 708,800 animals, but the total catch is underestimated
due to under-reporting (Walsh et al., 2004). Collection is concen-
trated on several species, particularly yellow tang, with the top-
10 species comprising 73% of the annual aquarium-sh catch
(Walsh et al., 2004). Since 1953, the government of Hawaii has re-
stricted collection gear to small nets and traps. Today, permits are
available to anyone for a small fee. The collection of stony corals,
however, is illegal.
Since as early as 1970, collection has reduced the abundances of
target species (Tissot and Hallacher, 2003; Tissot et al., 2004). The
volume of shes taken from Hawaiian reefs has generated public
concern about the long-term sustainability of the ornamental reef
sh collection (Tissot and Hallacher, 2003; Capitini et al., 2004). In
response, in 1973 the Hawaii Division of Fish and Game required
shers to le catch reports, yet the number of permits issued and
sh caught continued to increase over time (Walsh et al., 2004).
Increasing sh collection along with growing public awareness of
population declines intensied conicts between the tourism
industry the largest economic driver in Hawaii and the aquar-
ium shery (Capitini et al., 2004), including an unsuccessful at-
tempt to ban the aquarium shery in 19971998 (Hawaii
Department of Land and Natural Resources, 2010). Efforts for a
statewide ban continue today (Miller, 2012). As an alternative
measure, Hawaii implemented Fish Replenishment Areas (FRAs)
in 2000 the rst no-take zones specically targeting aquarium
collection to protect aquarium-sh populations and reduce user
conicts (see Capitini et al., 2004 for details on FRAs establish-
ment). The FRAs, combined with existing MPAs, protect 35.2% of
the Kona coast from aquarium collection (Tissot et al., 2004; Wil-
liams et al., 2009).
From an ecological perspective, the abundance of some targeted
populations increased within FRAs, but the stock size of these spe-
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-signicant increases in abundance
(e.g., yellow tang, Hawaii Department of Land and Natural Re-
sources, 2010; Williams et al., 2009). Some adult sh have spilled
over into areas adjacent to the FRA boundaries (Williams et al.,
2009) and larval sh are dispersing from the FRAs into the collec-
tion zones (Christie et al., 2010). The effectiveness of the FRAs var-
ies among sites (see Ortiz and Tissot, 2008). Outside of the FRAs,
collection is now concentrated in the remaining open areas, collec-
tion effort remains high, and there are no catch limits (Stevenson
et al., 2011). Since FRAs were established, overall populations of
yellow tang have continued to decline (Williams et al., 2009). For
management outside of FRAs, the West Hawaii Fisheries Manage-
ment council recommended developing a white list of 25-aquar-
ium species that can be collected (Hawaii Department of Land
and Natural Resources, 2010). Ornamental sheries in Hawaii do
not employ catch limits, weakening the effectiveness of the licens-
ing and the FRAs at controlling effort.
Elsewhere in the Waikiki-Diamondhead Fisheries Management
Area of Oahu, periodic closures have been attempted to protect reef
sh from overharvesting (i.e., Williams et al., 2006). These periodic
closures temporarily increased the population of many species,
including yellow tang, but sh populations declined dramatically
when areas were open for harvesting (Williams et al., 2006).
3.2.1.6.2. Effort and catch controls in Florida. The Florida Keys
supports a multi-species ornamental shery, primarily targeting
invertebrates, which has grown in size and impact since 1987
(Rhyne et al., 2009). While Hawaii implemented spatial manage-
ment through its FRAs, Florida regulates the commercial harvest
of ornamental species through licensing requirements, allowable
gear types, and harvest restrictions including quotas, closed sea-
sons or areas, size limits, and bans on certain species (Larkin
et al., 2001; Larkin and Adams, 2003). Most notably, the state con-
trols collection of ornamental invertebrates by limiting the number
of available harvest licenses for both commercial and recreational
collectors, including a 1998 moratorium on new licenses (Larkin
and Adams, 2003). By limiting entry into the shery, this cap at-
tempts to reduce collection effort and overharvesting while gener-
ating prots for permit holders. For aquarium shes, Florida
employs several management strategies to regulate collection
(e.g., daily catch limits as well as minimumand maximumsize lim-
its for buttery and angelshes) (Larkin et al., 2001; Wood, 2001).
For invertebrates, this limited-entry program restricts the num-
ber of participants, but it does not limit catch volume or collection
effort (Rhyne et al., 2009). These licenses allow shers to collect
most species unrestrictedly with the exception of long-spine
sea urchins (Diadema antillarum), Bahama starsh (Oreaster reticul-
atus), sea fans (Gorgonia abellum and G. ventalina), stony corals
(Scleractinia), and re corals (Millepora spp.) (Larkin et al., 2001).
In the absence of catch limits, the limited entry program has not
reduced shing pressure or collection effort, because the majority
of collection is done by a minority (40%) of permit holders (Larkin
and Adams, 2003; Rhyne et al., 2009). Catch landings and the num-
ber of targeted species have actually increased since the programs
implementation (Rhyne et al., 2009).
Several ornamental species also have daily bag limits that con-
trol the volume of the species (both shes or invertebrates) caught
by both commercial and recreational shers. However, these bag
limits are not set based on an overall TAC for the season or on stock
assessments. Setting TACs for this shery would be challenging for
several reasons: the shery targets multiple species, no stock
assessments exist, catch landings are underreported despite Flor-
ida law requiring reporting, and shing effort, such as the quantity
of gear and time spent collecting, is not reported or measured
(Rhyne et al., 2009).
3.2.2. Importing nations
3.2.2.1. United States. The United States accounts for the majority
(64%) of the global market for marine aquarium sh and other
coral reef wildlife (Tissot et al., 2010). The U.S. Fish and Wildlife
Service is responsible for documenting the volume and abundance
of live wildlife imports at U.S. ports of entry, but the volume and
diversity of trade makes this monitoring challenging (Rhyne
et al., 2012; Smith et al., 2008; Tissot et al., 2010). Three federal
laws the Lacey Act, the Endangered Species Act, and the Magnu-
son-Stevens Fishery Conservation and Management Act are the
primary legal protections for coral reef wildlife entering the U.S.
(Smith et al., 2008; Tissot et al., 2010).
Under the Endangered Species Act (ESA), the U.S. currently safe-
guards two coral species, Acropora palmata, and A. cervicornis, with
66 additional species under consideration for listing at the time of
this writing. The ESA requires the conservation of listed species,
including protection of critical habitat as well as prohibition of
interstate and foreign commerce. States, including Hawaii and
Florida, prohibit most collection of stony corals; however, imports
of most coral species are allowed.
232 L.E. Dee et al. / Biological Conservation 169 (2014) 225237
The Lacey Act bans the importation of organisms collected in
violation of the laws of the source country. Cyanide shing is
banned in most countries, and therefore importation of wildlife
caught with cyanide is unlawful. Nonetheless, importation of shes
captured using cyanide continues due to a lack of enforcement in
source countries and the difculty of detecting cyanide in shes
(Bruckner and Roberts, 2008). Cyanide is rapidly metabolized
meaning that detection is technically difcult and time sensitive
(reviewed in Mak et al., 2005) thereby hindering the application
of the Lacey Act. However, a recently developed cyanide detection
method may overcome these challenges (Vaz et al., 2012). The util-
ity of the Lacey act in promoting global coral wildlife conservation
is constrained by the environmental laws of the source countries.
A second provision of the Lacey Act prohibits knowingly allow-
ing any wild animal or bird to be imported under inhumane or
unhealthful conditions. Practices that cause high supply-chain
mortality appear to be prohibited under this provision; however,
the Lacey Act is not invoked because demonstrating that an impor-
ter knowingly permitted a violation to occur is difcult. Addition-
ally, the provision has not been interpreted to include imports of
sh or other coral reef wildlife species.
The Magnuson-Stevens Act in part aims to conserve and man-
age shery resources in federal waters, focusing primarily on food
sheries. Although coral reef wildlife is collected from federal
waters, domestic harvesting for ornamental uses occurs primarily
in state jurisdictions, outside of the scope of the Magnuson-Stevens
Act. The Act regulates some precious coral species. Effective Janu-
ary 30, 2012, a rule was issued for the collection of aquarium
trade species in federal waters of the Caribbean. However, this
rule has not been fully implemented and does not specify which
species are included, so its effectiveness remains to be determined.
3.2.2.2. Countries of the European Union. Countries of the European
Union (E.U.) are second only to the U.S. as importers of coral reef
wildlife (Tissot et al., 2010; Wood, 2001). The E.U. established high
regulatory standards for customs procedures, animal welfare, and
invasive species (European Commission, 2010; Wood, 2001). The
E.U. requires adherence to CITES regulations, membership in the
World Organization for Animal Health, and that exporters provide
proof of quarantine measures (European Commission, 2010). Wild-
life Trade Regulation EC 338/97 supplements CITES by allowing
importing countries to question trade sustainability from the
source country and further enables an E.U. Scientic Review Group
(SRG) to investigate (Jones, 2008; Kinch and Teitelbaum, 2008). A
negative SRG ruling can ban imports from that country (Jones,
2008).
The SRG has signicant power to protect marine aquarium
wildlife that have a high mortality rate during transport and are
unlikely to survive in captivity for a considerable proportion of
their life span (Eureopean Commission, 2010). In 1998 and
2000, the SRG temporarily suspended imports for 25 coral species
from Indonesia until data demonstrating sustainable management
were provided (Bruckner and Borneman, 2006). Since then, addi-
tional reviews have been conducted and new wildlife import sus-
pensions imposed on other species and countries (e.g., E.U.,
2011). Such suspensions enable importing countries to play a more
proactive and precautionary role in coral reef conservation. The
global benet 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. X
F
refers to management that only applies to shes. X
i
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. X
o
refers to management for which the information may be outdated (such as outdated stock assessments). NA denotes no information or
insufcient or unreliable/conicting information to score a particular category.
Producing
country or
territory
Size of
shery
Fisheries
management
plan
Fisheries: Barriers to
entry
Fisheries: Regulating commercial collection methods
Relative
size
r
Available
online
License or
permit
required
Limited
licenses
Quotas for
individual
species
Total allowable
catch
Size
limits
Fishing season or
seasonal closure by
government
Gear
restrictions
Anti-
cyanide
laws
Stock
assessments for
ornamentals
Part A
Australia
a
Large X X X X X

No X
F
X X X
Bahamas
b
Small No X No Conch only No No No X X No
Eritrea
c
NA No X No No No No NA NA NA No
Fiji
d
Large X X X X

X
F
X X X No
Haiti Medium No NA NA NA NA NA NA NA NA NA
Indonesia
e
Very
Large
No X

No X

No No X X X

Kiribati
f
NA No X No Flame
angelsh
only
X 1
species
No No No No
Maldives
g
Large NA X No X
F
X
F
No No X X No
Philippines
h
Very
Large
No X No No No No No X X No
Sri Lanka
i
Large No NA No No No NA No X NA X
o
Papua New
Guinea
j
NA NA No No X Circumstantially X No No X NA
Tonga
k
Small X X X No X
F,
No No X X No
US (Florida)
l
Large X X X X
F
X
F
X
F
X X X No
US (Hawaii)
m
Large X X No No No X
F
X X X No
US (Guam)
n
Small X X No No X

No X X No
US (Puerto
Rico)
o
Large X X X X
F
X No X X X X
o
Vanuatu
p
NA X X X 1 species 2 species No No X X X
Vietnam
q
Large No NA NA NA NA NA NA X X No
L.E. Dee et al. / Biological Conservation 169 (2014) 225237 233
major importers, particularly the U.S. and Japan, have less restric-
tive rules on imports (Tissot et al., 2010).
3.2.2.3. Australia. Australia has been one of the most successful in
regulating and managing the coral reef wildlife import trade (CCIF,
2001; Wood, 2001). Australia utilizes stringent quarantine and
anti-invasive species regulations to monitor the import and
domestic transportation of coral reef wildlife. These measures
include a list of species permitted for trade, called a whitelist,
created under the 1999 Environment Protection and Biodiversity
Property rights Species protection Ecosystem
protection
Trade standards
Territorial user
right sheries
s
Individual
transferrable
quotas
Trade Restrictions (export
inspection, quarantine laws)
Bans or laws prohibiting
catch of endangered species
OIE
member
MPAs
t
No-take
reserves
t
CITES
member
WTO
member
Part B
Australia
a
No X

X X X X X X X
Bahamas
b
NA No No X

X X No X Observer
Eritrea
c
NA No X X
,i
X No No X No
Fiji
d
X No X X X X X X X
Haiti NA NA NA NA X No No No X
Indonesia
e
X No No No X X X X X
Kiribati
f
X No No No No X X No X
Maldives
g
No No X
F,
X
F,
X X X X X
Philippines
h
X No X X

X X X X X
Sri Lanka
i
NA No X
F
X
F
X X NA X X
Papua New
Guinea
j
X No NA X X X No X X
Tonga
k
NA No X X

(and clams) No X No No X
US
(Florida)
l
No No X X X X X X X
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
Rico)
o
No No X X

(anemones) X X X X X
Vanuatu
p
X No X X

(and clams) X X X X Observer


Vietnam
q
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
Hawaii 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 = 50,000100,000 exported specimens ($150,000
USD); large = 100,000200,000 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
efcacy of any measure depends on enforcement and shers compliance.
72% have gear restrictions; 77% ban cyanide use
Marine Protected Areas represented P2% of the EEZ
a
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 sheries 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 shes
33% of the areas have spatial rights-based management
27% have size limits for >1 species with only 22% requiring size limits for shes
Of the 12 jurisdictions that prohibit collections of endangered species, these laws apply only to corals in 7 (i.e., no other invertebrates or sh)
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).
234 L.E. Dee et al. / Biological Conservation 169 (2014) 225237
Conservation Act (Morrisey et al., 2011). This whitelist has several
advantages, including a clearly dened protocol for border inspec-
tions to identify permitted species. Australian regulations also re-
quire importers to provide extensive documentation, such as
permits, risk-assessments, health certicates, and identication
of shipments to the species level. Imports must be inspected and
quarantined upon entering the country. Because of these require-
ments, Australia has often served as an example of successful man-
agement of imports for the trade (CCIF, 2001; Morrisey et al.,
2011).
4. Conclusions
4.1. Alternative approaches and successful practices
Methods such as gear restrictions; entry, size, and catch limits;
shing bans; spatial management; and size limits are commonly
used, with mixed success, in this trade (Tables 3 and 4). Voluntary
certication approaches, such as the Marine Aquarium Council,
have also been attempted, but these programs were not viable
(reviewed in Amos and Claussen, 2009). Conversely, stock assess-
ments, scientically-set TACs, and rights-based sheries manage-
ment approaches (e.g., individual transferable quota systems
[ITQs] and exclusive shing zones) remain underutilized. The
limited employment of these management techniques is largely
due to data, management capacity, and resource limitations (e.g.,
nances or enforcement and monitoring personnel), as well as a
lack of attention to ornamental sheries. Furthermore, many of
these methods likely require modications in order to be made
appropriate for aquarium sheries.
4.2. Catch limits
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-
cies-specic TACs are currently used in the coral shery in Austra-
lia, whereas aggregate TACs (in the form of export quotas) are used
in several island nations including the Maldives and Tonga (Ta-
ble 3). These aggregate quotas set catch limits at different levels
for groups of species, often based on historical levels of export
(Sections 3.2.1.33.2.1.4). Oftentimes the quotas are not species-
specic and insufcient data are available to determine whether
shing effort is currently over or under sustainable levels. Though
catch limits can be benecial, they can lead to competition among
shers to sh as quickly as possible, which endangers humans, cre-
ates economic inefciencies, and can have long-term consequences
for sh populations (Hilborn et al., 2005).
4.3. Rights-based management
As a type of catch share or rights-based program, ITQs allocate a
tradable portion of the annual TAC to an individual or group, there-
by incentivizing the long-term maintenance of the shery (Costello
et al., 2008). For instance, transitioning to an ITQ program in Flor-
ida would allow the active collectors to buy out the inactive col-
lectors to gain a larger share of the total catch, making the shery
more efcient. Nevertheless, establishment of an ecologically- and
economically-successful ITQ program requires the TAC to be set
appropriately, traditionally through data-intensive stock assess-
ment models. For this reason, the rarity of ITQs and scientically-
set TACs in ornamental sheries is partially attributable to data
and management capacity limitations.
Spatial rights-based management, e.g., TURFs or exclusive com-
munity shing zones, may offer a more promising direction, espe-
cially in areas with a history of traditional marine tenure systems
(Hilborn et al., 2005). For instance, customary law in Fiji
determines access to collection areas, as well as mechanisms for
benet sharing, and enforcement of collection areas (Manoa,
2008). In exchange for access to the resource, marine aquarium
operators that collect species within the customary shing rights
areas contribute prots from sales to scholarships for the commu-
nity (J. Comley, personal communication). Such approaches can
improve the socioeconomic benets of collection to local
communities.
4.4. Data-limited stock assessments
Despite the range of management tools available, oftentimes
managers must make decisions with limited data about the sh-
erys status (Donaldson, 2003; Fujita et al., in press; Honey et al.,
2010). Methods to assess data-limited sheries are emerging to
meet this challenge (e.g., Fujita et al., in press; Honey et al.,
2010; Wilson et al., 2010). For instance, marine reserves can func-
tion as proxies for unshed conditions, thereby providing a relative
measure of stock status at local scales (Wilson et al., 2010). This ap-
proach, known as the MPA-based decision tree method, compares
catch-per-unit-effort and size structure within and outside of re-
serves as estimates of shing mortality to calibrate TAC levels.
However, the applicability of this approach and others to ornamen-
tal sheries may be limited due to insufcient information on
catch and effort trends or the biology of targeted species (Donald-
son, 2003; Fujita et al., in press). To address these problems and
improve ornamental sheries management, a tiered approach
involving biomass, productivity-susceptibility analysis, and a com-
bination of stock specic and aggregate quotas can be used (Fujita
et al., in press). To date, these data-limited methods of sheries
evaluation have not been widely applied to ornamental sheries,
but offer promising tools for future management.
4.5. Other promising directions
Other potential strategies to reform the trade include aquacul-
ture and industry reform. Although out of the scope of this review,
which focuses on state, national, and international regulations and
management, it is worth noting that aquaculture holds promise for
alleviating collection pressure on wild populations (Moorhead and
Zeng, 2010; Olivotto et al., 2011). Aquaculture has already reduced
the collection of wild shes and invertebrates, including clownsh,
seahorses, tridacnid clams, and several hard corals. These benets,
however, will depend on the extent that the supply of cultured
individuals fullls the market demand.
5. Conclusions
Despite the difculties in managing the coral reef wildlife trade,
some examples of successful management demonstrate that sus-
tainable reform of the trade is possible. Some programs in export-
ing countries, such as Floridas moratorium on corals, Hawaiis
FRAs, and the Maldives and Tongas no-take zones and tiered quo-
ta systems, represent steps towards reforming the trade. Similarly,
legislation in importing countries, such as the E.U.s Wildlife Trade
Regulation and Australias whitelist, can also improve the trades
environmental sustainability by proactively restricting and moni-
toring imports when there are concerns about the conservation
status, disease risk, or invasiveness of certain species. In contrast
to the U.S.s reactionary approach to managing the trade, the pre-
cautionary approach adopted by the E.U. and Australia allows
importing countries more control and oversight. Examples of
regulation and management in the E.U. and Australia highlight
promising ways for importing countries to proactively steer the
L.E. Dee et al. / Biological Conservation 169 (2014) 225237 235
trade towards sustainability. Different combinations of these man-
agement and regulation strategies, in conjunction with emerging
data-poor sheries management approaches, aquaculture, and
the other underutilized management tools identied here, offer
considerable promise for the future.
Acknowledgements
We thank Molly Bogeberg, James Comley, Cara Cooper, Steven
Gaines, Stuart Green, Celia Landesberg, Leah Meadvin, Steve J. Mill-
er, Domingo Ochavillo, Andrew Rhyne, Anthony Roelofs, Michael
Tlusty, Alison Schiebelhut, Todd Stevenson, Colette Wabnitz, and
Kathleen Williams for helpful comments, information, and discus-
sions that improved this review. We thank three anonymous
reviewers who provided helpful suggestions that improved this
manuscript. This work was supported by the Kingsher Founda-
tion. L. Dee was supported by a NSF GRFP and the Daniel Vapnek
Fellowship for Sustainable Fisheries at the Bren School of Environ-
mental Science & Management.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.biocon.2013.
11.025.
References
Albins, M.A., Hixon, M.A., 2008. Invasive Indo-Pacic lionsh Pterois volitans reduce
recruitment of Atlantic coral-reef shes. Mar. Ecol.-Prog. Ser. 367, 233238.
Amos, A.M., Claussen, J.D., 2009. Certication as a Conservation Tool in the Marine
Aquarium Trade: Challenges to Effectiveness. Turnstone Consulting and Starling
Resources.
Australian Fisheries Management Authority, 2011. Coral Sea Fishery, Management
Arrangements Booklet, 2011 Fishing Season. Canberra, Australia.
Barber, C.V., Pratt, V.R., 1997. Policy reform and community-based programmes to
combat cyanide shing in Philippines. SPC Live Reef Fish Informa. Bull. 3, 2635.
Barber, C.V., 1999. Recent developments in combating cyanide shing: much talk
but little action on the ground. SPC Live Reef Fish Bull. 5, 2731.
Beta, C., Bennet, G., Tairo, K., Neneuti, T., 2005. Preliminary Report on the
Ornamental Fish Survey Kiritimati Island, Kiribati. Marine Aquarium Council,
Suva.
Betancur, R.R., Hines, A., Acero, A.P., Orti, G., Wilbur, A.E., Freshwater, D.W., 2011.
Reconstructing the lionsh invasion: insights into Greater Caribbean
biogeography. J. Biogeogr. 38, 12811293.
Bruckner, A.W., 2001. Proceedings of the International Workshop on the Trade in
Stony Corals: Development of Sustainable Management Guidelines. National
Oceanic and Atmospheric Administration, Silver Spring.
Bruckner, A.W., Borneman, E.H., 2006. Developing a sustainable harvest regime for
Indonesias stony coral shery with application to other coral exporting
countries. In: Proc. 10th Int. Coral Reef Symp., vol. 1, pp. 16921697.
Bruckner, A.W., Roberts, G., 2008. Proceedings of the International Cyanide
Detection Testing Workshop. National Oceanic and Atmospheric
Administration, Silver Spring.
Capitini, C.A., Tissot, B.N., Carroll, M.S., Walsh, W.J., Peck, S., 2004. Competing
perspectives in resource protection: the case of marine protected areas in West
Hawaii. Soc. Nat. Resour. 17, 763778.
Caribbean Fishery Management Council (CFMC), 2012. Fishery Management Plan,
Final Environmental Impact Statement and Draft Regulatory Impact Review for
the Shallow Water Reef Fish Fishery of Puerto Rico and the US Virgin Islands.
CFMC, San Juan.
Cervino, J.M., Hayes, R.L., Honovich, M., Goreau, T.J., Jones, S., Rubec, P.J., 2003.
Changes in zooxanthellae density, morphology, and mitotic index in hermatypic
corals and anemones exposed to cyanide. Mar. Poll. Bull. 46, 573586.
Chads, I., McDonald-Madden, E., McCarthy, M.a, Wintle, B., Linkie, M., Possingham,
H.P.(, 2008. When to stop managing or surveying cryptic threatened species?
Proc. Natl. Acad. Sci. USA 105 (37), 1393613940.
Christie, M.R., Tissot, B.N., Albins, M.A., Beets, J.P., Jia, Y.L., Ortiz, D.M., Thompson,
S.E., Hixon, M.A., 2010. Larval connectivity in an effective network of marine
protected areas. PLoS ONE 5, e15715.
CITES, 2012. <www.unep-wcmc.org/citestrade/index.cfmS> (accessed 31.10.12).
Conservation and Community Investment Forum (CCIF), 2001. Analysis of
Destructive Reef Fishing Practices in the Indo-Pacic. Conservation and
Community Investment Forum, San Francisco.
Conservation and Community Investment Forum (CCIF), 2013. Assessment of the
Enabling Conditions for Rights-Based Management of Fisheries and Coastal
Marine Resources. Trust for Conservation Innovation, San Francisco.
Costello, C., Gaines, S.D., Lynham, J., 2008. Can catch shares prevent sheries
collapse? Science 321, 1678.
Daw, T.M., Rogers, G.C.C., Mapson, P., Kynoch, J.E., 2001. Structure and management
issues of the emerging ornamental sh trade in Eritrea. Aquarium Sci. Conserv.
3, 5364.
Department of Primary Industries and Fisheries, 2009. Policy for the Management of
the Coral Fishery. Queensland Government, Brisbane.
Dodds, F., Schneeberger, K. and Ullah, F., 2012. Review of implementation of Agenda
21 and the Rio Principles - Sustainable Development in the 21
st
century (SD21)
project. Prepared for United Nations Department of Economic and Social Affairs
Division for Sustainable Development; New York.
Donaldson, T.J., 2003. Review of the Proposed MACTRAQ Protocol in Relation to the
Marine Aquarium Market Transformation Initiative (MAMTI). Unpublished
Report.
Dudley, R.G., Ghofar, A., 2006. Marine and Fisheries Sector Strategy Sudy: Sub Sector
Strategy Review: Marine and Coastal Resources Management. Uniconsult
International Limited, Dhaka.
Edwards, A.J., Shepherd, A.D., 1992. Environmental implications of aquarium-sh
collection in the Maldives, with proposals for regulation. Environ. Conserv. 19,
6172.
Environmental Defense Fund (EDF), 2012. World Catch Share Database.
apps.edf.org/page.cfm?tagID=57622. (accessed 13.08.12).
European Commission, 2010. Wildlife Trade Regulations in the European Union: An
Introduction to CITES and its implementation in the European Union. European
Union, Luxembourg.
European Union, 2011. Commission Implementing Resulgation No 828/2011 of 17
August 2011. Suspending the introduction into the Union of specimens of
certain species of wild fauna and ora. J. Eur. Union 211, 1132.
Evanson, M., Foster, S.J., Wiswedel, S., Vincent, A.C.J., 2011. Tracking the
international trade of seahorses (Hippocampus species) the importance of
CITES. Fish. Centre Res. Rep. 19, 1104.
Fidelman, P., Evans, L., Fabinyi, M., Foale, S., Cinner, J., Rosen, F., 2012. Governing
large-scale marine commons: contextual challenges in the Coral Triangle. Mar.
Policy 36, 4253.
Fisheries Management and Planning Section, 2008. Marine Aquarium Fishery
Management Plan. Ministry of Agriculture & Food, Forestry and Fisheries,
Government of the Kingdom of Tonga.
Food and Agriculture Organization of the United Nations (FAO), 2008. Yearbook of
Fishery and Aquaculture Statistics. <http://www.fao.org/shery/soa/en>
(accessed 13.05.13).
Food and Agriculture Organization of the United Nations (FAO), 2009. National
Fishery Sector Overview, Commonwealth of the Bahamas. ftp://ftp.fao.org/Fi/
document/fcp/en/FI_CP_BS.pdf. (accessed 13.05.13).
Food and Agriculture Organization of the United Nations (FAO), 2013. Fishery and
Aquaculture Country Proles: Philippines. http://www.fao.org/shery/
countrysector/FI-CP_PH/en (accessed 13.05.13).
Foster, S.J., Vincent, A.C.J., 2005. Enhancing sustainability of the international trade
in seahorses with a single minimum size limit. Conserv. Biol. 19, 10441050.
Fujita, R., Thornhill, D.J., Karr, K., Cooper, C.H., Dee, L.H., in press. Assessing
and managing data-limited ornamental sheries in coral reefs. Fish Fish.
http://dx.doi.org/10.1111/faf.12040.
Gonzales, E., Savaris, J., 2005. International Seafood Trade: Supporting Sustainable
Livelihoods Among Poor Aquatic Resource Users in Asia (EP/R03/014). Output 2
Marine Ornamentals Trade in the Philippines and Options for its Poor
Stakeholders. Poseidon Aquatic Resource Management Ltd., Network of
Aquaculture Centres in Asia-Pacic (NACA), and the STREAM Initiative.
Green, E.P., Shirley, F., 1999. The Global Trade in Corals. World Conservation Press,
Cambridge.
Grey, M., Blais, A.M., Vincent, A.C.J., 2005. Magnitude and trends of marine sh curio
imports to the USA. Oryx 39, 413420.
Hanawa, M.L., Harris, L., Graham, M., Farrell, A.P., Bendell-Young, L.I., 1998.
Effects of cyanide exposure on Dascyllus aruanus, a tropical marine sh
species: lethality, anesthesia and physiological effects. Aquarium Sci.
Conserv. 2, 2134.
Hardin, M.P., LeGore, R.S., 2005. Development of management policy for the marine
ornamental sh and invertebrate shery in Puerto Rico: a case study. Rev. Biol.
Trop. 53, 139144.
Hawaii Department of Land and Natural Resources, 2010. Report on the ndings
and recommendations of the effectiveness of the West Hawaii regional shery
management area. State of Hawaii, Honolulu.
Hilborn, R., Orensanz, J.M.L., Parma, A.M., 2005. Institutions, incentives and the
future of sheries. Philos. Trans. Roy. Soc. B 360, 4757.
Honey, K., Moxley, J.H., Fujita, R., 2010. From rags to shes: data-poor methods for
shery managers. Managing Data-Poor Fish.: Case Stud., Models Solut. 1, 159
184.
International Union for the Conservation of Nature, 2012. Red List of Threatened
Species v2012.2. <www.iucnredlist.org> (accessed 17.06.12).
Jones, A.M., 2011. Raiding coral nurseries? Diversity 3, 466482.
Jones, R., 2008. CITES, corals and customs: a review of the international trade in
wild coral. In: Lewis, R.J., Janse, M. (Eds.), Advances in Coral Husbandry in Public
Aquariums. Burgers Zoo, Arnhem.
Jones, R.J., Steven, A.L., 1997. Effects of cyanide on corals in relation to cyanide
shing on reefs. Mar. Freshwater Res. 48, 517522.
Kinch, J., Teitelbaum, A., 2008. Proceedings of the Sub-regional Workshop on the
Marine Ornamental Trade in the Pacic. Secretariat of the Pacic Community,
Noumea.
236 L.E. Dee et al. / Biological Conservation 169 (2014) 225237
Knittweis, L., Wolff, M., 2010. Live coral trade impacts on the mushroom coral
Heliofungia actiniformis in Indonesia: potential future management approaches.
Biol. Conserv. 143, 27222729.
Knittweis, L., Kraemer, W.E., Timm, J., Kochzius, M., 2009. Genetic structure of
Heliofungia actiniformis (Scleractinia: Fungiidae) populations in the Indo-Malay
Archipelago: implications for live coral trade management efforts. Conserv.
Genet. 10, 241249.
Kolm, N., Berglund, A., 2003. Wild populations of a reef sh suffer from the
nondestructive aquarium trade shery. Conserv. Biol. 17, 910914.
Larkin, S.L., Adams, C.M., 2003. The marine life shery in Florida, 199098. Mar.
Fish. Rev. 65, 2131.
Larkin, S.L., Adams, C.M., Degner, R.L., Lee, D.J., Milon, J.W., 2001. An Economic
Prole of Floridas Marine Life Industry. University of Florida, Gainesville.
LeGore, R.S., Hardin, M.P., Ter-Ghazaryan, D., 2005. Organization and operation of
the marine ornamental sh and invertebrate export shery in Puerto Rico. Rev.
Biol. Trop. 53, 145153.
Lesser, M.P., Slattery, M., 2011. Phase shift to algal dominated communities at
mesophotic depths associated with lionsh (Pterois volitans) invasion on a
Bahamian coral reef. Biol. Invasions 13, 18551868.
Mak, K.K.W., Yanase, H., Renneberg, R., 2005. Cyanide shing and cyanide detection
in coral reef sh using chemical tests and biosensors. Biosens. Bioelectrons 20,
25812593.
Manoa, P.E., 2008. Adaptation of Fijis Legislative Framework for the Trade in
Aquarium Fish: Part 1: Assessment of the Framework. Coral Reef Initiatives for
the Pacic, Noumea Cedex.
Marine Aquarium Market Transformation Initiative, 2006. Report on Roving
Collectors: Case Studies From Indonesia and the Philippines. Marine
Aquarium Council, Makati City.
Matoto, S., Ledua, E., Mou-Tham, G., Kulbicki, M., Dalzell, P., 1996. The aquarium-
sh shery in Tongatapu, Tonga. Status and recommendations for management.
South Pacic Commission, New Caledonia.
McClenachan, L., Cooper, A.B., Carpenter, K.E., Dulvy, N.K., 2011. Extinction risk and
bottlenecks in the conservation of charismatic marine species. Conserv. Lett. 5,
7380.
McWhinnie, S.F., 2009. The tragedy of the commons in international sheries: An
empirical examination. J. Environ. Econ. Manage. 57, 321333.
Miller, E., 2012. Most residents want aquarium sh collecting banned, poll says.
Hawaii Tribune Herald. hawaiitribune-herald.com/sections/news/local-news/
most-residents-want-aquarium-sh-collecting-banned-poll-says.html.
(accessed 28.04.13).
Morrisey, D., Inglis, G., Neil, K., Bradley, A., Fitridge, I., 2011. Characterization of the
marine aquarium trade and management of associated marine pests in
Australia, a country with stringent import biosecurity regulation. Environ.
Conserv. 38, 89100.
Moorhead, J.A., Zeng, C.S., 2010. Development of captive breeding techniques for
marine ornamental sh: a review. Rev. Fish. Sci. 18, 315343.
Nixon, K., Cartwright, C., Horrii, S., Mazaroli, N., Nelson, A., Reynolds, A., 2012.
Saving Nemo: Solutions to Reform the Marine Ornamental Trade. University of
California, Santa Barbara.
Nurhidayah, L., 2010. Integrated coastal zone management in Indonesia: framework
assessment and comparative analysis. Division for Ocean Affairs and the Law of
the Sea, Ofce of Legal Affairs, the United Nations, New York.
Ochavillo, D., Hodgson, G., Shuman, C., Ruz, R., 2004. Status of the Philippine marine
aquarium sh trade. In: Turbulent Seas: The Status of Philippine Marine
Fisheries. Department of Agriculture-Bureau of Fisheries and Aquatic Resources,
Cebu City, pp. 6064.
Olivotto, I., Planas, M., Simoes, N., Holt, G.J., Avella, M.A., Calado, R., 2011. Advances
in breeding and rearing marine ornamentals. J. World Aquacult. Soc. 42, 135
166.
Ortiz, D.M., Tissot, B.N., 2008. Ontogenetic patterns of habitat use by reef-sh in a
Marine Protected Area network: a multi-scaled remote sensing and in situ
approach. Mar. Ecol.-Prog. Ser. 365, 217232.
Pet, J.S., Pet-Soede, L., 1999. A note on cyanide shing in Indonesia. SPC Live Reef
Fish Inform. Bull. 5, 2122.
Ryan, S., Clarke, K., 2005. Ecological assessment of the Queensland Marine
Aquarium Fish Fishery. Report prepared for the Australian Government
Department of Environment Heritage, Brisbane.
Rhyne, A., Rotjan, R., Bruckner, A., Tlusty, M., 2009. Crawling to collapse:
ecologically unsound ornamental invertebrate sheries. PLoS ONE 4, e8413.
Rhyne, A.L., Tlusty, M.F., Schoeld, P.J., Kaufman, L., Morris Jr., J.A., Bruckner, A.W.,
2012. Revealing the appetite of the marine aquarium sh trade: the volume and
biodiversity of sh imported into the United States. PLoS ONE 7, e35808.
Roelofs, A., 2008a. Ecological Risk Assessment of the Queensland Marine Aquarium
Fish Fishery. Department of Primary Industries and Fisheries, Brisbane.
Roelofs, A., 2008b. Ecological Risk Assessment of the Queensland Coral Fishery.
Department of Primary Industries and Fisheries, Brisbane.
Roelofs, A., Silcock, R., 2008. A sustainability assessment of marine sh species
collected in the Queensland marine aquarium trade. Department of Primary
Industries and Fisheries, Brisbane.
Ross, M.A., 1984. A quantitative study of the stony coral shery in Cebu, Philippines.
Mar. Ecol. 5, 7591.
Rubec, P.J., Cruz, F., Pratt, V., Oellers, R., McCullough, B., Lallo, F., 2001. Cyanide-free
net-caught sh for the marine aquarium trade. Aquarium Sci. Conserv. 3, 3751.
Sadovy, Y., Mitcheson, G., Rasotto, M.B., 2001. / Early development of the
mandarinsh, Synchiropus splendidus (Callionymidae), with notes on its
shery and potential for culture. Aquarium Sci. Conserv. 3, 253263.
Saleem, M.R., Adam, M.S., 2004. Review of the Aquarium Fish Industry in the
Maldives 2003. Marine Research Center, Mal.
Saleem, M., Islam, F., 2008. Management of the aquarium shery in the Republic of
the Maldives. In: Proc. 11th Int. Coral Reef Symp. vol. 1, pp. 10381042.
Secretariat of the Pacic Community (SPC), 2009. Vanuatu National Marine
Aquarium Trade Management Plan. SPC, Noumea.
Semmens, B.X., Buhle, E.R., Salomon, A.K., Pattengill-Semmens, C.V., 2004. A hotspot
of non-native marine shes: evidence for the aquarium trade as an invasion
pathway. Mar. Ecol.-Prog. Ser. 266, 239244.
Shuman, C.S., Hodgson, G., Ambrose, R., 2005. Population impacts of collecting sea
anemones and anemonesh for the marine aquarium trade in the Philippines.
Coral Reefs 24, 564573.
Smith, K.F., Behrens, M.D., Max, L.M., Daszak, P., 2008. U.S. drowning in unidentied
shes: scope, implications, and regulation of live sh import. Conserv. Lett. 1,
103109.
Stevenson, T.C., Tissot, B.N., Dierking, J., 2011. Fisher behaviour inuences catch
productivity and selectivity in West Hawaiis aquarium shery. ICES J. Mar. Sci.
68, 813822.
Syarif, L.M., 2009. Promotion and management of marine sheries in Indonesia. In:
Winter, G. (Ed.), Towards sustainable sheries law: a comparative analysis.
IUCN, Gland, pp. 3182.
Teh, L.C.L., Teh, L.S.L., Starkhouse, B., Sumaila, U.R., 2009. An overview of socio-
economic and ecological perspectives of Fijis inshore reef sheries. Mar. Policy
33, 807817.
Thornhill, D.J., 2012. Ecological Impacts and Practices of the Coral Reef Wildlife
Trade. Defenders of Wildlife, Washington.
Thorson, E., Wold, C., 2010. Enforcing sustainable and legal trade in corals and other
coral reef species. International Environmental Law Project, Lewis & Clark Law
School; Portland.
Timotius, S., Idris, Syahrir, M. 2009. A review on ornamental coral farming effort in
Indonesia. In: International Ocean Science, Technology and Policy Symposium:
World Ocean Conference, pp. 112.
Tissot, B.N., Hallacher, L.E., 2003. Effects of aquarium collectors on reef shes in
Kona, Hawaii. Conserv. Biol. 17, 17591768.
Tissot, B.N., Walsh, W.J., Hallacher, L.E., 2004. Evaluating effectiveness of a marine
protected area network in West Hawaii to increase productivity of an aquarium
shery. Pac. Sci. 58, 175188.
Tissot, B.N., Best, B.A., Borneman, E.H., Bruckner, A.W., Cooper, C.H., DAgnes, H.,
Fitzgerald, T.P., Leland, A., Lieberman, S., Amos, A.M., Sumaila, R., Telecky, T.M.,
McGilvray, F., Plankis, B.J., Rhyne, A.L., Roberts, G.G., Starkhouse, B., Stevenson,
T.C., 2010. How US ocean policy and market power can reform the coral reef
wildlife trade. Mar. Policy 34, 13851388.
United States Coral Reef Task Force (USCRTF), 2001. International Trade in Coral and
Coral Reef Species: The Role of the United States. USCRTF, Washington.
Vagelli, A.A., 2008. The unfortunate journey of Pterapogon kauderni: a remarkable
apogonid endangered by the international ornamental sh trade, and its case in
CITES. SPC Live Reef Fish Inform. Bull. 18, 1728.
Vaz, M.C.M., Rocha-Santos, T.A.P., Rocha, R.J.M., Lopes, I., Pereira, R., et al., 2012.
Excreted thiocyanate detects live reef shes illegally collected using cyanide: a
non-invasive and non-destructive testing approach. PLoS ONE 7, e35355.
Vincent, A.C.J., Foster, S.J., Koldewey, H.J., 2011. Conservation and management of
seahorses and other Syngnathidae. J. Fish Biol. 78, 16811724.
Wabnitz, C., Taylor, M., Green, E., Razak, T., 2003. From Ocean to Aquarium: The
Global Trade in Marine Ornamental Species. UNEP-WCMC, Cambridge.
Walsh, W.J., Cotton, S.P., Dierking, J., Williams, I.D., 2004. The commercial marine
aquarium shery in Hawaii 19762003. In: Friedlander, A.M. (Ed.), Status of
Hawaiis Coastal Fisheries in the New Millennium, Revised. American Fisheries
Society, Hawaii Chapter, Honolulu, pp. 129156.
Western Pacic Regional Fishery Management Council (WPRFMC), 2005. Fishery
Ecosystem Plan for the Mariana Archipelago. WPRFMC, Honolulu.
Wihelmsson, D., Haputhantri, S.S.K., Rajasuriya, A., Vidanage, S.P., 2002. Monitoring
the trends of marine ornamental sh collection in Sri Lanka. In: Linden, O.,
Souter, D., Wilhelmsson, D., Obura, D. (Eds.), Coral Degradation in the Indian
Ocean: Status Report 2002. University of Kalmar, Kalmar, pp. 158166.
Williams, I.D., Walsh, W.J., Miyasaka, A., Freelander, A.M., 2006. Effects of rotational
closure on coral reef shes in Waikiki-Diamond head shery management area,
Oahu, Hawaii. Mar. Ecol.-Prog. Ser. 310, 139149.
Williams, I.D., Walsh, W.J., Claisse, J.T., Tissot, B.N., Stamoulis, K.A., 2009. Impacts of
a Hawaiian marine protected area network on the abundance and shery
sustainability of the yellow tang, Zebrasoma avescens. Biol. Conserv. 142,
10661073.
Wilson, J.R., Prince, J.D., Lenihan, H.S., 2010. A management strategy for sedentary
nearshore species that uses marine protected areas as a reference. Mar. Coast.
Fish. 2, 1427.
Wijesekara, R.G.S., Yakupitiyage, A., 2000. Ornamental sh industry in Sri Lanka:
present status and future trends. Aquarium Sci. Conserv. 3, 241252.
Wood, E., 2001. Collection of Coral Reef Fish for Aquaria: Global Trade, Conservation
Issues and Management Strategies. Marine Conservation Society, Ross-on-Wye.
Wood, E.M., Malsch, K., Miller, J., 2012. International trade in hard corals: review of
management, sustainability and trends. In: Proc. 12th Int. Coral Reef Symp.,
Cairns, Australia, 913 July 2012.
Wood, L.J., 2007. MPA Global: A Database of the Worlds Marine Protected Areas.
<www.mpaglobal.org> (accessed 07.06.13).
World Bank, 2013. Indicators. <http://data.worldbank.org/indicator?display=
default>. (accessed 20.08.13).
L.E. Dee et al. / Biological Conservation 169 (2014) 225237 237