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The global trade in marine
ornamental species
Colette Wabnitz, Michelle Taylor,
Edmund Green and Tries Razak
From Ocean to Aquarium
The global trade in marine
ornamental species
Colette Wabnitz, Michelle Taylor,
Edmund Green and Tries Razak
From Ocean to Aquarium
UNEP World Conservation
Monitoring Centre
219 Huntingdon Road
Cambridge CB3 0DL, UK
Tel: +44 (0) 1223 277314
Fax: +44 (0) 1223 277136
E-mail: info@unep-wcmc.org
Website: www.unep-wcmc.org
Director: Mark Collins
THE UNEP WORLD CONSERVATION
MONITORING CENTRE is the biodiversity
assessment and policy implemen-
tation arm of the United Nations
Environment Programme (UNEP), the
world’s foremost intergovernmental
environmental organization. UNEP-
WCMC aims to help decision makers
recognize the value of biodiversity to
people everywhere, and to apply this
knowledge to all that they do. The
Centre’s challenge is to transform
complex data into policy-relevant
information, to build tools and sys-
tems for analysis and integration, and
to support the needs of nations and
the international community as they
engage in joint programmes of action.
UNEP-WCMC provides objective,
scientifically rigorous products and
services that include ecosystem
assessments, support for implemen-
tation of environmental agreements,
regional and global biodiversity
information, research on environ-
mental threats and impacts, and
development of future scenarios for
the living world.
Sponsors
Major financial support from the
David and Lucile Packard Foundation
is gratefully acknowledged, as is
some contributing support from the
Bloomberg Foundation.
PHOTOGRAPHS
Photos illustrating this report were
kindly provided by the following.
© as listed
Front cover and title page, left to right:
A. Edwards, F. Benzoni, C. Genevois,
O. Hoegh-Guldberg.
Back cover: C. Genevois.
Pages: Francesca Benzoni: p 28; Eran
Brokovich: p 16 (right); CSIRO: p 39
(both); Alasdair Edwards: pp 6, 36, 43
(both); Cédric Genevois: pp 11, 25 (left),
30, 38, 50; Edmund Green: pp 8 (lower),
25 (right), 46, 48, 53 (left), 55; Ove
Hoegh-Guldberg: pp 9 (both), 37, 45, 55;
Ofri Johan: pp 24, 34, 56 (right); Marc
Kochzius: pp 7 (lower right ), 16 (left),
17, 18, 21 (left), 33, 47 (right), 56 (left);
Ed McManus: p 26; George Mitcheson/
National Geographic Society: p 41;
Project Seahorse: pp 10 (A. Vincent),
21 (A. Vincent), 35 (D. McCorry), 52
(A. Vincent); Peter Scott: pp 7 (upper
two and lower left), 8 (top), 12, 13, 14
(both), 47 (left), 53 (right), 57, 58; Colette
Wabnitz: pp 15, 40; Zoological Survey of
India, Chennai: p 29.
ACKNOWLEDGEMENTS
This report would not have been
possible without the participation of
many colleagues from the Marine
Aquarium Council, particularly
Aquilino A. Alvarez, Paul Holthus and
Peter Scott, and all trading companies
who made data available to us for
inclusion into GMAD. The kind
assistance of Akbar, John Brandt,
John Caldwell, Lucy Conway, Emily
Corcoran, Keith Davenport, John
Dawes, MM Faugère et Gavand, Cédric
Genevois, Thomas Jung, Peter Karn,
Firoze Nathani, Manfred Menzel,
Davide di Mohtarami, Edward Molou,
Wolfgang Mueller, James O’Carroll,
Jan Olsen, Gayatri Reksodihardjo-
Lilley, Martin Selch, Claude
Schuhmacher, Craig Shuman, Derek
Thomson, Caroline Raymakers, Paul
West, and Miriam and Danny Winkels
is also very much appreciated.
The authors would like to thank Helen
Corrigan for her help with the analyses
of CITES data, and Sarah Ferriss for
assisting in assembling information
and analysing Annex D and GMAD data
on
Hippocampus
spp. We are grateful
to Neville Ash for reviewing and editing
earlier versions of the manuscript.
Thanks also for additional
comments to Katharina Fabricius,
Daphné Fautin, Bert Hoeksema, Caroline
Raymakers and Charles Veron; for
providing reprints, to Alan Friedlander,
Julie Hawkins, Sherry Larkin and Tom
Ogawa; and for providing the picture on
p41, to Yvonne Sadovy.
We are grateful to Marie-Annick
Moreau and Kristin Lunn for
information on Banggai cardinalfish
and to Craig Shuman for information
on the sea anemone fishery in the
Philippines.
© UNEP World Conservation Monitoring Centre 2003
Citation: Wabnitz, C., Taylor, M., Green, E., Razak, T. 2003.
From Ocean to Aquarium
. UNEP-WCMC,
Cambridge, UK.
URL: http://www.unep-wcmc.org/resources/publications/UNEP_WCMC_bio_series/17.htm
A Banson production Printed in the UK by Swaingrove Imaging
The contents of this report do not necessarily reflect the views or policies of UNEP or contributory
organizations. The designations employed and the presentations do not imply the expressions of any
opinion whatsoever on the part of UNEP or contributory organizations concerning the legal
status of any country, territory, city or area or its authority, or concerning the delimitation of its
frontiers or boundaries.
M
Most of us at some time or another have enjoyed the
relaxing experience of gazing into an aquarium, in
a dentist’s waiting room or during a special visit to
a public aquarium. In admiring the playfulness of clownfish
wriggling amongst the anemones’ tentacles, the grace of
angelfish swimming in open water and in our delight at
spotting reclusive shrimp and crabs crawling behind
iridescent living corals, it is all too easy to overlook the fact
that all these wonderful creatures are far from their natural
home. The great majority of animals in aquaria across
Europe and North America were collected from coral reefs
far away and flown, bagged in plastic and packed in
styrofoam boxes, thousands of miles to our hospitals and
living rooms.
This report,
From Ocean to Aquarium: The Global
Trade in Marine Ornamental Species,
takes a clear objective
look at this international industry. A potential source of
income for communities living close to coral reefs, the
aquarium trade has been heavily criticised for the use of
unsustainable collection techniques and poor husbandry
practices. Policy makers have been faced with something of
a dilemma in trying to control the environmentally
undesirable aspects of the industry without risking the
economic incentive which aquarium fishers have in caring
for the coral reefs that provide their livelihoods. Where
previously much controversy existed between opponents
and supporters of the aquarium trade, most of it based on
polarized opinion and poor information, this publication
presents sound quantitative data on the species in trade.
Through linking trade data to what is known about the life
histories of the target organisms, conservation priorities
and management recommendations are identified.
I have great pleasure in presenting this report and
wish to extend the gratitude of the authors to the long list of
collaborating organizations and companies that have made
it possible. I am confident that the information contained
here will assist efforts to promote sustainable practice
within the industry, as well as providing information to
casual admirers of marine organisms.
Mark Collins
Director
UNEP World Conservation Monitoring Centre
3
From ocean to aquarium
Foreword
5
From ocean to aquarium
Acknowledgements 2
Foreword 3
EXECUTIVE SUMMARY 6
Fish 6
Corals 7
Invertebrates 8
INTRODUCTION 9
ORGANIZATION OF THE TRADE 12
Collection 12
Airline transport 13
At destination 13
Transhipping 13
Governments 14
Associations 14
SOURCES OF TRADE DATA 15
The Global Marine Aquarium Database (GMAD) 16
ANALYSIS OF TRADE DATA 18
Fish 18
Seahorses 20
Corals 22
Stony corals 22
Soft corals and sea fans 25
Live rock 27
Invertebrates 29
Giant clams 29
CONSERVATION ISSUES 33
Destructive harvesting practices 33
Cyanide 33
Impacts on populations 35
Life histories 37
Sex-selective fisheries 42
Species suitability 43
Fishes 43
Corals 45
Post-harvesting mortality 46
Invasive species 47
User conflict 47
CONSERVATION EFFORTS 48
Marine Aquarium Council and certification 48
Mariculture 49
Corals 49
Fish 51
Invertebrates 54
Management initiatives for the trade 54
Limited access to the fishery 55
Quotas 55
Size limits 56
Marine reserves 56
Temporary closures 57
CONCLUSIONS AND RECOMMENDATIONS 58
ENDNOTES 59
REFERENCES 60
Contents
6
From ocean to aquarium
B
Between 1.5 and 2 million people worldwide are
believed to keep marine aquaria. The trade
which supplies this hobby with live marine
animals is a global multi-million dollar industry, worth
an estimated US$200-330 million annually, and oper-
ating throughout the tropics. Ornamental marine
species (corals, other invertebrates and fish) are
collected and transported mainly from Southeast Asia,
but also increasingly from several island nations in the
Indian and Pacific Oceans, to consumers in the main
destination markets: the United States, the European
Union (EU) and, to a lesser extent, Japan.
Very few of the species in trade are exploited
directly for other purposes, and there is little doubt that
aquarium animals are the highest value-added product
that can be harvested from a coral reef. If managed
sustainably, the trade could support jobs in predominantly
rural, low-income coastal communities and so provide
strong economic incentives for coral reef conservation in
regions where other options for generating revenue are
limited. However, damaging techniques occasionally used
to collect the animals, possible over-harvesting of some
species and the high levels of mortality associated with
inadequate handling and transport of sensitive living
organisms undermine this potential, and continue to pose
significant challenges to achieving sustainability. As a
result the trade has seldom been free of controversy as
traders try to generate a profit, conservationists try to
avoid further decline in coral reefs also suffering from
other pressures, and policy makers try to assemble a
legislative framework that protects coral reefs without
threatening a legitimate business activity or the incomes
of communities engaged in aquarium fishing.
In the main, this debate has taken place without
access to impartial and quantitative data on the trade and,
with so many different viewpoints, achieving consensus
on its impacts, and hence the identification of suitable
responses, has been difficult. In 2000, the United Nations
Environment Programme World Conservation Monitoring
Centre (UNEP-WCMC), the Marine Aquarium Council
(MAC) and members of various aquarium trade asso-
ciations began, in collaboration, to address this need for
better information and created the Global Marine
Aquarium Database (GMAD). Trade data have been obtained
from wholesale exporters and importers of marine
aquarium organisms, most often through copies of trade
invoices, integrated and standardized into quantitative,
species-specific information which has been placed in the
public domain: www.unep-wcmc.org/marine/GMAD. Fifty-
eight companies, approximately one-fifth of the whole-
salers in business, and four government management
authorities have provided data to GMAD. In August 2003
the dataset contained 102,928 trade records (7.7 million
imported and 9.4 million exported animals) covering a
total of 2,393 species of fish, corals and invertebrates and
spanning the years 1988 to 2003. These data have
permitted the most accurate quantitative estimates to date
of the size of the global trade in marine ornamental fish
and corals, and the first ever estimates for invertebrates
other than corals, a previously overlooked section of
the industry.
FISH
A total of 1,471 species of fish are traded worldwide with
the best estimate of annual global trade ranging between
Executive summary
Bluestreak cleaner wrasse,
Labroides dimidiatus
.
7
20 and 24 million individuals. Damselfish (Pomacentridae)
make up almost half of the trade, with species of
angelfish (Pomacanthidae), surgeonfish (Acanthuridae),
wrasses (Labridae), gobies (Gobiidae) and butterflyfish
(Chaetodontidae) accounting for approximately another
25-30 per cent. The most traded species are the blue-green
damselfish (
Chromis viridis
), the clown anemonefish
(
Amphiprion ocellaris
), the whitetail dascyllus (
Dascyllus
aruanus
), the sapphire devil (
Chrysiptera cyanea
) and the
threespot dascyllus (
Dascyllus trimaculatus
). The ten most
traded species account for about 36 per cent of all fish
traded for the years 1997 to 2002. Trade data, correlated
with aquarium suitability information, indicate that two
species known not to acclimatize well to aquarium con-
ditions are nonetheless very commonly traded. They are the
bluestreak cleaner wrasse (
Labroides dimidiatus
: GMAD
records 87,000 worldwide imports of this species from 1997
to 2002) and the mandarin fish (
Synchiropus splendidus
:
GMAD records 11,000 live individuals exported to the EU
in the same period). Data further indicate that species
characterized as ‘truly unsuitable’, mainly due to their
restricted dietary requirements, such as the foureye
butterflyfish (
Chaetodon capistratus
), the harlequin filefish
(
Oxymonacanthus longisrostris
) and the Hawaiian cleaner
wrasse (
Labroides phtirophagus
), are also commonly
traded, albeit in lower numbers.
CORALS
A total of 140 species of stony coral, nearly all
scleractinians, are traded worldwide, with the best
Executive summary
Copperhead butterflyfish,
Chelmon rostratus
: from ocean to aquarium.
8
From ocean to aquarium
estimate of annual global trade ranging between 11 and
12 million pieces. Although difficulties associated with
accurate coral identification probably make species data
less reliable for corals than for fish, it is clear that species
in seven genera (
Trachyphyllia
,
Euphyllia
,
Goniopora
,
Acropora
,
Plerogyra
,
Catalaphyllia
) are the most popular,
accounting for approximately 56 per cent of the live coral
trade between 1988 and 2002. Sixty-one species of soft
coral are also traded, amounting to close to 390,000
pieces per year.
Sarcophyton
spp. (leather/mushroom/
toadstool coral) and
Dendronephthya
spp. (carnation
coral) are two of the most commonly traded species.
However, whilst the biology of the former makes it a
hardy, fast-growing and easily propagated species under
aquarium conditions,
Dendronephthya
spp. usually die
within a few weeks, mainly due to the fact that they lack
photosynthetic symbionts and rely on filtering particles
and nutrients in the water column for food.
INVERTEBRATES
More than 500 species of invertebrates (other than corals)
are traded as marine ornamentals, though the lack of a
standard taxonomy makes it difficult to arrive at a precise
figure. The best estimate of global annual trade ranges
between 9 and 10 million animals, mostly molluscs,
shrimps and anemones. Two groups of cleaner shrimp,
Lysmata
spp. and
Stenopus
spp., and a group of
anemones,
Heteractis
spp., account for approximately 15
per cent of all invertebrates traded.
Overall, there is a pressing need for basic
information on the population dynamics and life history
characteristics of organisms targeted by the ornamental
trade. Combined with accurate trade data, such
information is essential for making more informed
decisions regarding the sustainable collection of marine
ornamentals.
Other efforts needed to achieve sustainable
management of the aquarium trade include the continued
development and wider application of third-party
certification, whereby the consumer is empowered to
assist in reducing the environmental impacts of the trade
by selectively purchasing specimens produced in an
environmentally friendly manner. At the source country
level, the implementation of measures such as quotas
and size limits, and restricted access to the ornamental
fishery through, for example, the use of permits and
the establishment of areas closed to the fishery, are
recommended where appropriate, though proper con-
sultation is essential. Further research in developing
mariculture protocols for raising commonly traded
species in source countries, to take pressure off wild
stocks and to avoid removing livelihoods from local
communities, should also be promoted. To date, only
one-fifth of giant clams are cultured, while only 1-10 per
cent of fish and fewer than 1 per cent of coral species are
capable of being captive bred. Even fewer species are
bred in commercial quantities.
Coral collected for trade.
Cleaner shrimp,
Stenopus
spp.
A
Although reefs cover less than one quarter of 1 per
cent of the marine environment, they are
considered to be amongst the most biologically rich
and productive ecosystems on Earth, often described as
the ‘rainforest of the seas’1,2. Coral reefs support over
4,000 species of fish (or a third of the world’s marine fish
species), about 800 species of reef-building corals3, and a
great number of other invertebrates and sponges.
Coral reefs provide millions of people with benefits,
both direct and indirect, including fisheries, tourism and
coastal protection2. Most coral reefs are located in develop-
ing countries, with millions depending directly on them as a
source of protein and, at least in part, for their livelihoods.
Reefs also support an important array of non-food com-
mercial fisheries including the marine ornamental fishery.
It is generally acknowledged that the collection and
export of tropical marine fish for the aquarium trade started
in Sri Lanka in the 1930s, on a very small scale4, 5. Trade
expanded during the 1950s, with an increasing number of
places (e.g. Hawaii and the Philippines) issuing permits for
the collection of species destined for the marine aquarium
tradei, 6. Although demand has fluctuated and trends vary
from year to year, the overall value of the marine fish trade,
accounting for about 10 per cent of the international orna-
mental fish trade (marine and freshwater included), has
remained fairly stable in recent years. Figures for exports
of live pieces of coral, on the other hand, showed annual
growth of 12-30 per cent from 19907until 1999, only stabi-
lizing in the last three years.
It is estimated that 1.5 to 2 million people worldwide
keep marine aquaria8, with 600,000 households in the
United States alone9. Estimates place the value of the mari-
ne ornamental trade at US$200-330 million per year10, 11
with 80 per cent of the trade in stony corals and 50 per cent
of the trade in marine fish going to the United States12.
Unlike freshwater aquaria species, where 90 per
cent of fish species are currently farmed, the great ma-
jority of marine aquaria are stocked from wild caught
species13. With nearly all tropical marine aquarium fish
and invertebrates in trade taken directly from coral reefs
and adjacent habitats, the aquarium industry has
attracted some controversy14-17, particularly regarding its
sustainability18. The high visibility of marine ornamental
products has made the trade a magnet for criticism19.
Articles in the press have tended to focus on the negative
impacts of the trade with headlines often making the
9
From ocean to aquarium
Introduction
Value of the aquarium industry
The aquarium industry as a whole is of relatively low
volume yet very high value21, 26, thus potentially
providing an incentive to conserve reef habitats17, 30 and
offering a livelihood to coastal communities often living
in low-income areas. In 2000, 1 kg of aquarium fish from
the Maldives was valued at almost US$500, whereas
1 kg of reef fish harvested for food was worth only
US$631. Similarly, the live coral trade is estimated to be
worth about US$7,000 per tonne whereas the use of
harvested coral for the production of limestone yields
only about US$60 per tonne32. In Palau, live rock is
exported for the aquarium trade at US$2.2 to US$4.4
per kilo whereas it is sold locally as construction
material for less than US$0.02 per kilo33. Sri Lanka
earns about US$5.6 million a year by exporting reef fish
to around 52 countries5and estimates indicate that
50,000 people are directly involved in the export of
marine ornamentals34. In the Philippines, about 7,000
collectors depend on the reefs for their livelihood35.
Harlequin tuskfish,
Choerodon fasciatus
. Typical retail value
can be as much as US$115 for an Australian specimen.
Species including striped thread fin,
Polydactylus plebeius
.
10
From ocean to aquarium
assumption that the trade of marine ornamentals is
incompatible with reef conservation.
Opponents to the trade emphasize:
❏the damaging techniques sometimes used to collect reef
specimens20, 21; sodium cyanide for example is a non-
selective technique used to capture fish that adversely
impacts the overall health of fish and coral and also kills
non-target organisms22,23
❏the over-harvesting of target organisms5, 13, 17, 24, and
❏the high levels of mortality associated with insensitive
shipping and poor husbandry practices along the supply
chain21, 25, 26.
Some regulation has already been established; more is
being called for17 and may follow. With more than 2.2 billion
people (39 per cent of the world’s population) living within
100 km of the coast27, coral reefs are facing an increasing
plethora of threats such as pollution, sedimentation, coral
bleaching, overfishing and tourism. Reefs of Southeast Asia,
the most important source of the majority of animals in the
marine ornamental trade, are particularly at risk, with 88
per cent of all reefs at medium to very high threat from
anthropogenic impacts28. It is therefore important that
aquarium species’ collection does not further compound
these problems29.
Supporters of the trade maintain that, if managed
properly, the aquarium industry could support long-term
conservation and sustainable use of coral reefs. Some
collection techniques have minimal impact on coral reefs.
Well-managed shipping and husbandry practices, partic-
ularly relevant in the case of fish, can also allow mortality
levels to be kept to minimal levels (as has been shown by
some operators in the industry). In addition, aquarium
animals are the highest value-added product that can be
harvested sustainably from coral reefs, so collecting and
exporting marine ornamentals in developing countries
creates jobs in rural, low-income, coastal areas26 where
resources and alternative options for generating income
can be limited. Aquarium fisheries therefore have the
potential to provide an alternative economic activity for
coastal populations, an important source of foreign
exchange for national economies5and a strong economic
incentive for the sustainable management of reefs. They
may also help foster marine conservation by providing a
strong incentive for subsistence fishers to harvest wild
populations sustainably so as to maintain fish stocks and
reef environments in good condition.
Domestic or public saltwater aquaria can provide a
unique opportunity to educate the public about coral reefs
and increase awareness and understanding of what is, for
the most part, a hidden ecosystem13, 21, 30. By allowing people
to explore the complexities and appreciate the beauty of
reefs, the need for creative solutions to environmental
problems can be illustrated. In addition, an understanding of,
and respect for, reefs can be sparked among users who are
ultimately responsible for their conservation38.
Only 1 per cent (about 25 species)36 to 10 per cent6, 37
of marine ornamental fish are captive-bred and probably
less than 1 per cent of the total trade in hard corals is
derived from cultured origins32. The development of mari-
culture facilities could in theory allow pressure to be taken
off wild populations. It should preferably be located in the
Seahorse fisherman in the Philippines at night.
mostly developing source countries, in order not to deprive
these nations of the income generated by trade. The
application of international certification schemesii may
provide an important tool for achieving this. Although still in
its infancy, the Marine Aquarium Council (MAC) certification
process has made some considerable progress (see
chapter on Conservation efforts, p 48). As more certified
organisms become available, aquarium hobbyists will be in
a position to make purchases in the knowledge that the
organisms they are buying have been collected and trans-
ported according to a set of agreed and monitored standards.
The controversy over the environmental costs and
benefits of the trade continues, largely due to a lack of
quantitative data. Global species trade data are available for
all species of hard coral and giant clams that are listed in
the Convention on International Trade in Endangered
Species of Wild Fauna and Flora (CITES)iii on Appendix II
(species vulnerable to exploitation but not yet at risk of
extinction). Shipments of corals and clams involving Parties
to the Convention must be accompanied by a CITES export
permit issued by the national CITES management authority.
Parties to CITES are then obliged to produce annual reports
specifying the quantity of trade that has taken place in
each listed species. No marine aquarium fish (although
Hippocampus
spp. will be from 15 May 2004) or
invertebrates, other than clams or corals, are listed in
CITES Appendices.
The Global Marine Aquarium Database (GMAD) was
set up in 2000 as a collaborative project between the United
Nations Environment Programme World Conservation
Monitoring Centre (UNEP-WCMC), MAC and members of
trade associations in exporting and importing countries
(e.g. the Indonesia Coral, Shell and Ornamental Fish
Association (AKKII), the Philippine Tropical Fish Exporters’
Association (PTFEA), Ornamental Fish International (OFI),
the Ornamental Aquatics Trade Association (OATA)). It
compiles accurate quantitative information on the aquarium
trade through centralizing and standardizing sales records
provided by aquarium wholesalers. Relevant information
from these records is then placed in the public domain.
This study presents an up-to-date report on the
marine aquarium trade. It first briefly describes the
organizational structure of the trade both in source coun-
tries and at destination. The next chapter then introduces
existing sources of data on the aquarium trade whilst the
chapter on Analysis of trade data presents statistics and
analyses of the trade in corals, fish and invertebrates
derived from GMAD and other sources of information (e.g.
CITES) where applicable. Conservation issues, including the
use of destructive collection practices, impacts on marine
ornamental populations, species’ suitability for aquarium
conditions, issues of invasive species and user conflict aris-
ing from the marine aquarium industry, are discussed in the
chapter of the same name. The chapter on Conservation
efforts presents steps taken by the industry and future
efforts to be made at local, regional and global levels to
ensure the marine ornamental trade develops sustainably
whilst providing local communities with livelihood oppor-
tunities, promoting reef conservation by giving local people
an incentive to maintain their reefs in a healthy state. The
final chapter concludes the report and provides some
recommendations based on its findings.
11
Introduction
Petites îles de la Sonde, a specimen collection site in Indonesia.
12
From ocean to aquarium
T
The organization of the marine ornamental trade is
complex and extremely dynamic. In exporting
nations it is likely to involve a series of collectors/
fishers, wholesalers, middlemen and exporters, while in
importing nations it involves a number of importers,
wholesalers, retailers and, more recently, transhippers.
COLLECTION
Collectors tend to be small-scale fishermen from tropical
countries who work alone or in small groups, often
composed of family units, and who are either self-
employed or working for a wholesaler/exporter. They
typically work with artisanal equipment, with divers often
using wooden palms as fins39. Fish are collected using
nets (e.g. hand nets, cast nets) and fishing lines. In Sri
Lanka and the Maldives collectors catch most of their fish
using hand nets20. In Australia40, 41, the Pacific region42
and Florida43 fishers often use much larger barrier, drop
or fence nets.
Collecting fish effectively, without inflicting
damage to either fish or substrate, requires considerable
skill and experience6. At times, special techniques are
developed for collecting particular species. In Sri Lanka,
for example, fishers make use of small, tubular nets for
capturing species that live in small holes. Using a fine rod
the fish are ‘tickled’ out of their cavity into a net
strategically placed at the burrow’s entrance44 in 6. In areas
of Southeast Asia where aquarium fisheries are most
developed, fishers are assisted by a method called
‘hookah’, whereby compressors are installed on their
vessels and connected to long plastic tubes that divers
bite between their teeth or to which a regulator is
attached.
Some collection methods can be particularly
damaging to the substrate. Previously, in Sri Lanka for
example, small cast nets used to be draped over corals
and fish scared into them by hitting the coral with a stick.
This method was recently banned due to damage inflicted
upon the reef6. Branching corals, which provide shelter to
a variety of fish, are often snapped off to extract any fish
hiding in between branches20. In some countries, such as
Indonesia and the Philippines, collectors stun fish with
poison, to make their collection easier. The most common
poisons used are sodium cyanide and quinaldine. The
extent to which cyanide is used is discussed in
Conservation issues, under Destructive harvesting
practices.
Collectors harvesting corals and other immobile
invertebrates (e.g. sponge) also often use hookah and a
hammer, iron crowbar, chisel or screwdriver to remove
target colonies. Although specimens are preferably
removed with a small portion of the reef to which the
organism is attached45, minimal damage is usually
inflicted to the surrounding reef or connected corals46.
Typically, collectors tend to target small-sized colonies of
hard and soft corals that can be removed whole. However,
sometimes only fragments are taken45.
Upon collection, fish, corals and invertebrates are
placed separately in plastic containers or individual bags.
Coral pieces tend to be covered with plastic wrap to
prevent injury45. To avoid the fishes’ air bladders rupturing
due to decreasing hydrostatic pressure associated with
ascent, individuals caught on deeper parts of the reef are
often placed in a dark mesh cage and lifted to the surface
very slowly (3 m every 30-40 minutes47) to allow their
bladders to decompress. The deeper the fish have been
caught the slower they need to be brought to the surface,
ranging from hours to days depending on the species’
sensitivity48. To avoid the wait, fishers often bring the fish
to the surface immediately and pierce the inflated swim
bladder with a hypodermic needle. When performed well
and with a clean needle this method is considered safe42.
Fishermen typically bring collected fish and
invertebrates back to shore the same day. However, in
areas of the Philippines and Indonesia where collection
sites tend to be fairly isolated, fish may be on board the
boat for several days before being landed49. Once ashore,
fish and invertebrates are placed in separate holding tanks,
or immediately packaged for transport and/or export.
Collectors are usually paid for the number of
Organization
of the trade
Fish being bagged for export.
13
Organization of the trade
fish/invertebrates they have collected and prices for
individual species vary greatly depending on their
popularity on the market. However, there is a fairly large
discrepancy between the sum they earn and prices paid
by the end consumer. In Indonesia, for example, a fisher
typically receives US$0.10 for every orange clownfish
(
Amphiprion percula
)collected yet an American hobbyist
is likely to pay US$1250. The greater the number of
middlemen employed in the market chain between
collector and wholesaler, the higher this discrepancy is
likely to be. A study carried out in the Philippines showed
that, of the price paid for fish by exporters, about 85 per
cent went to middlemen whereas only 15 per cent went to
collectors51.
At their origin, fish are quarantined (this can last
from a few hours to a few months) and starved for at least
48 hours prior to shipment to ensure they do not foul their
bags. Most fish (and invertebrates) are then packed in
double polyethylene bags filled with one third water and
two thirds oxygen, sealed and placed in a cardboard box
(often reinforced with polystyrene foam for added
insulation). Aggressive species are placed in opaque bags
or have paper placed at the bottom of the bag to minimize
stress. To avoid putting the health of fish at risk, a
recommended maximum travel time of 40 hours has been
suggested for shipments (with 24 hours being considered
reasonable)47. For each consignment a licence has to be
issued allowing it to leave the exporting country. Cartons
of coral species and giant clams need to be accompanied
by the relevant CITES permits. Although practices vary
between individual countries, a health certificate issued
by the local veterinary services is usually required before
the shipment is declared for customs. Further infor-
mation on shipping practices in the ornamental industry
can be found in Cole
et al
.25.
AIRLINE TRANSPORT
International airline companies transport fish from
exporting to importing states. Shipping charges are the
main reason behind the discrepancy between marine
ornamental prices in the exporting country and final retail
price – in the case of fish, shipping charges often
correspond to approximately half to two thirds of the
landed price incurred by the importer39. Transport
associations such as the International Air Transport
Association (IATA)iv and the Animal Transportation
Association (AATA)vorganize and manage the transport of
live marine ornamentals. Fish are packaged according to
a list of criteria set out by these organizations.
AT DESTINATION
At the receiving end, importers must clear the shipment
with customs and the consignment undergoes another
veterinary check. However, criticism has been expressed
towards the latter as there is a general lack of veterinary
control and individuals performing the checks are often not
qualified to examine fish. The importer then transfers the
shipment to a wholesale facility and the boxes are opened
under dimly lit conditions to minimize stress to the fish.
Individuals are quarantined in order to acclimatize them to
life in captivity, particularly to new feeding cycles and
different water chemistry. Care is taken to keep certain
species separate and provide others with shelter to
minimize aggressive behaviour and associated stress and
thus ensure maximum survival rates. Following acclima-
tization, fish are either sold to other wholesalers or
retailers or re-exported. Invertebrate species tend to be
kept separately from fish species. Appropriate lighting, i.e.
the provision of the right colour spectrum at the appro-
priate intensity, is of crucial importance to the survival of
coral species. Unlike fish species corals do not need to be
acclimatized prior to being shipped or sold.
In recent years, wholesalers have found it more
and more difficult to remain established, mainly because
of the introduction of transhipping, but also due to the
expansion of garden centres and pet supermarkets.
These centres tend to sell fish (and to a lesser extent
invertebrates) in bulk quantities at low prices. They also
often lack qualified staff, which frequently results in a
lack of information and technical advice at the point of
sale and a lack of interest from the purchaser39.
Transhipping
Transhipping is an activity that emerged during the 1970s
and 1980s. It involves grouping the orders of several
retailers and/or wholesalers and placing them with an
exporter, collecting the shipment at the airport, clearing
customs and redistributing the boxes without opening
Bagged specimens.
14
them39. The responsibility for the entire shipment falls
onto the retailer. All transhippers require to operate is a
telephone, fax and vehicles to pick up shipments upon
arrival. Where additional services, beyond picking up the
consignment, clearing customs and transport are
required, the activity is referred to as ‘consolidating’39. In
the latter case, a more complete service is provided
whereby the transhipper takes responsibility for the fish
during a 48-hour period following delivery and offers
refunds for any animals that died during transport39.
Increasingly, particularly in Europe, transhippers
are required to hold a licence in order to operate39.
However, no skills with respect to fish handling are
necessary to obtain such a licence. Transhippers do not
need large facilities to acclimatize marine fish, and so
they can afford to sell individuals at half the price that
wholesalers would charge. Despite severe criticism about
the quality of transhipped invertebrates and non-
acclimatized fish these businesses are expanding in
Europe, unlike in the United States where increased
commercial use of the Internet has led to a decline in
the number of transhippers11. In response to criticism,
and to abide by the Marine Aquarium Council Standards
and Certificationvi, transhippers are transforming their
businesses to be able to provide increased quality and
services.
Despite the advent of transhipping and con-
solidating, established wholesalers who are able to
maintain a core set of customers as retailers are only able
to import directly through transhippers if they have both
authorization from the veterinary services and the
required and appropriate equipment/infrastructure for
acclimatization40. Moreover, the results of a survey of US
marine ornamental wholesalers revealed that firms in
states outside Florida believed there was a growing
market for small environmentally conscious companies53.
GOVERNMENTS
Governments of many exporting countries often play an
important role in the trade of marine ornamentals,
ranging from financial assistance to improved manage-
ment schemes and trade regulations21. Certain countries/
states set fishing quotas (e.g. Florida43), prohibit col-
lection from certain sites (such as designated restricted
areas in Hawaii) or prohibit certain capture methods (such
as cyanide in Indonesia). Rules and regulations naturally
vary from one country to the next. In the European Union
(EU), for example, traders must contact the appropriate
national ministry (e.g. Ministry of the Environment) and
file an application for technical certification as well as
declare all imported and exported goods to the Ministry
of Finance39.
ASSOCIATIONS
Individuals involved in the marine ornamental industry
often join forces and form associations or syndicates.
Examples include AKKII, PTFEA, the Singapore Aquarium
Fish Exporters’ Association (SAFEA), OFI, OATA and the
Pet Industry Joint Advisory Council (PIJAC). The last is
the world’s largest pet trade association, representing all
segments of the pet industry including retailers,
wholesalers/distributors, companion animal suppliers,
manufacturers, manufacturers’ representatives, hobbyist
groups and other trade organizations.
Boxes at the airport.Divers’ breathing equipment (hookahs) on deck.
From ocean to aquarium
15
From ocean to aquarium
A
All species of giant clams and stony coral are listed
in Appendix II of CITES, an international agree-
ment that protects wildlife by ensuring that
international trade is based on sustainable use and does
not threaten the survival of a species in the wild. The
treaty, established in 1973 and which entered into force
in 1975, currently has 162 Member Parties. Species
listed in Appendix II can be traded, provided an export
permit accompanies shipments and a ‘non-detriment
finding’ is made (i.e. the collection is not detrimental to
the survival of the species).
Although one of the benefits of the Appendix II
listing is that it allows for global trade to be monitored, there
are a number of difficulties associated with implementing
CITES in relation to the aquarium trade. Due to the com-
plexities of coral identification, exports of corals need only
be identified to genus level – under the provisions of the
Convention, exports usually have to be identified to species
level. Within one genus the abundance and distribution, and
thus threat of overcollection (and that of other impacts), of
individual coral species varies immensely. Hence, issuing
CITES permits at genus level may lead to certain species
being driven to extinction through overcollection7. Further
limitations include differences in traded numbers between
reported and actual exports, differences in units recorded
(e.g. specimens and kilos), and confusion arising in cases
where corals are imported and then re-exported without
appropriate reference to the country of origin54. However, an
expert group established in 2000 is to discuss and revise
listing requirements55.
The EU has been fully implementing CITES since 1
January 1984. On 9 December 1996, it adopted Council
Regulation (EC) No. 338/97 on the Protection of Species of
Wild Fauna and Flora by Regulating Trade Therein (OJ L61
of 3/3/97) which entered into force on 1 June 1997.
Commission Regulation (EC) No. 338/97 lists species on
four Annexesvii :
❏AAnnnneexx AA: All CITES Appendix I species and some CITES
Appendix II and III species, for which the EU has adop-
ted stricter domestic measures, as well as some non-
CITES species.
❏AAnnnneexx BB: All other CITES Appendix II species, some
CITES Appendix III species and some non-CITES
species.
❏ AAnnnneexx CC: CITES Appendix III species not listed in other
Annexes.
❏AAnnnneexx DD: Some CITES Appendix III species for which the
EU holds a reservation and some non-CITES species.
Seahorses are listed under Annex D. Species listed on
Annex D require an import notification, to be completed
by the importer, upon entry into the EU. In theory, all
imports of Annex D species should be recorded, but in
practice it is likely that there are some discrepancies in
the trade data.
Besides CITES, and for species not listed under the
Convention’s appendices, national governments routinely
produce statistics, through customs or other officials with
responsibility for monitoring trade, regarding the export or
import of marine ornamentals, particularly fish. Unfor-
tunately, the utility of these trade data may be limited as:
❏trade categories are rarely fully reported6, and
❏data are often aggregated so that marine fish are
categorized as ‘tropical fish’ and combined with fresh-
water fish, in some cases even including invertebrates
(e.g. starfish, sea cucumbers, marine molluscs) or other
commodities under the same category8, 26, 53.
Even in cases where trade statistics are available through
government sources, difficulties often arise because of the
use of different units. Exports and imports tend to be
registered by value (e.g. US Customs and imports to the
nations of the EU) and/or weight rather than number of
individuals. Import values are always higher than export
values as the former include the costs of livestock and
carriage as well as insurance and freight56 whereas for
exports the value of the organisms is declared without
packing, freight, tax or transport6. Trade statistics available
Sources of
trade data
Unknown species of echinoderm (sea star) in an aquarium.
16
From ocean to aquarium
as weight values include water and packaging, hence
substantially overestimating the volume of live material,
especially for fish and non-coral invertebrates. Moreover,
trade data obtained through customs’ statistics should be
treated with caution as some operators have been known to
overstate quantities on their invoices for insurance
purposes8, or on other occasions understate quantities so
as to reduce the amount of tax payable and keep annual
shipments within the individual allowable quotas57. In Hong
Kong, a study comparing information obtained from trade
statistics with data collected through market surveys
indicated that official declarations of imports are under-
reported by at least two- to three-fold24.
In very few cases will countries report trade
statistics in terms of the number of specimens exported.
Singapore and the Maldives present exceptions to this,
holding government records of the number of marine
ornamental fish exported, showing a total of 1,294,200
fish being exported in 1998 for the former, and 262,641 in
1997, 182,916 in 1998, and 167,000 in 1999 for the latter6.
Furthermore, in order to comply with governmental
guidelines for obtaining a licence, collectors in Vanuatu,
Tonga and the Solomon Islands are required to submit
records of their exports, in terms of number of each
species exported8. State governments in Australia are
unique in that they require collectors to register catch
data as opposed to export data41.
Thus, the available sources of data generally
provide, at best, qualitative information and little reliable
quantitative information on numbers, countries of origin
and destinations of the main species in trade8.
THE GLOBAL MARINE AQUARIUM DATABASE (GMAD)
Since April 2000, UNEP-WCMC and MAC have been
collaborating with members of trade associations such as
AKKII, PTFEA, SAFEA, OFI and OATA to establish GMAD as
a freely available source of information on the global
aquarium industry. The common objective of GMAD is to
gather, integrate, collect, standardize and provide fast and
easy access to data on the trade of individual species by
placing this information in the public domain, through a
web-searchable interface (http://www.unep-wcmc.org/
marine/GMAD).
For their own files, companies keep records of their
sales, either on company computer databases or, more
commonly, as paper copies of their invoices. Although the
way in which companies register their trade records varies,
all records show species name, quantity, date and usually
origin and/or destination. A number of these companies
provided UNEP-WCMC with access to their sales records.
These data have been processed, checked and formatted:
species names have been verified and electronic data from
different electronic systems placed into a single standard-
ized database. As at August 2003, GMAD contained 102,928
Royal angelfish,
Pygoplites diacanthus
(left) and a nudibranch (right).
17
Sources of trade data
records. Data records in GMAD cover 2,393 species (corals,
other invertebrates and fish) from 1988 to 2003. In order
to avoid confusion, unless otherwise stated, the term
invertebrates will be used to refer to all invertebrate
species other than corals.
Each record in GMAD is the total number of
specimens traded for a unique combination of: species
name, country of export, country of import and year.
However, for importers’ data, a large number of records
were submitted by wholesalers without information about
country of origin.
GMAD trade data are linked to two external
databases:
❏FishBase58 for photographs of fish species, and fish
distribution and taxonomy, and
❏the Species Conservation Database59 for information on
invertebrate taxonomy, distribution, relevant legislation,
conservation status and associated literature and
common names.
It is important to note that trade data cannot be pooled
because some of the contributing importers trade with
some of the contributing exporters. Hence, pooling data
would create duplications. In order to avoid such confusion,
GMAD was designed to allow for import and export data to
be queried separately.
As an example, if interested in the number of
clown anemonefish (
Amphiprion ocellaris
) traded
between Indonesia and the United States for the year 1999
one can calculate two numbers. The first, based on
importers’ data, shows that 4,223
Amphiprion ocellaris
were imported into the United States from Indonesia
between those years. The second number, based on
export data, shows that 5,565 specimens were exported
from Indonesia to the United States. As of August 2003,
GMAD contains export data from 20 Indonesian
companies (though most of the data provided pertains to
coral exports), and importers’ data from four US
wholesalers. There are, of course, other companies in
Indonesia and the United States trading in
Amphiprion
ocellaris
that have not contributed their data to GMAD,
and therefore these figures are just a quantitative total
based on data contributed to GMAD by August 2003.
As a consequence of this, GMAD cannot be used
to calculate net volumes of trade in any one species, or
between any pair of countries. Calculations of quantities of
specimens traded in a particular species will be more or
less indicative of the trade in this species depending in part
on the proportion of operational wholesale export and
import companies contributing data to GMAD. However, it
is a very useful tool as an indicator of trends and, for the
first time in the case of fish and invertebrates, it allows
estimates based on quantitative, rather than qualitative,
data to be derived.
Clown anemonefish,
Amphiprion ocellaris
.
T
The following section will describe analyses of
CITES data for trade in stony corals and giant
clams, Annex D data for seahorses and GMAD data
for fish, corals and invertebrates. Based on sales data
supplied by the 58 companies in GMAD and applying the
method described in Green8the best estimate of annual
global trade is between 20 million and 24 million for
marine ornamental fish, 11-12 million for corals and 9-
10 million for marine ornamental invertebrates.
FISH
Records within GMAD for marine ornamental fish range
from 1988 to 2003. However, the data are not uniformly
distributed and most data were collected for the years
1998 and 1999 for importers’ data and 2000 and 2001 for
exporters’ information. Data provided by importers and
exporters show that a total of 7,938,828 fish and 3,588,406
fish respectively were traded between 1991 and 2003.
(See Table 1.)
According to data held in GMAD a total of 1,471
species of fish are traded globally. Most of these species
are associated with coral reefs although a relatively high
18
From ocean to aquarium
Analysis of
trade data
Blue-green damselfish,
Chromis viridis
.
Figure 1: Global trade of fish broken down by family
a. According to exporters’ data in GMAD b. According to importers’ data in GMAD
Pomacentridae
43%
Others 17%
Callionymidae 3%
Chaetodontidae 4%
Serranidae 2%
Blenniidae 2%
Microdesmidae 2%
Pomacanthidae 8%
Acanthuridae 8%
Labridae 6%
Gobiidae 5%
Pomacentridae
47%
Others 13%
Serranidae 3%
Chaetodontidae 4%
Microdesmidae 2%
Callionymidae 2%
Blenniidae 3%
Labridae 7%
Gobiidae 7%
Acanthuridae 6%
Pomacanthidae 6%
Table 1: Total number of fish traded as
ornamentals
As derived from exporters’ and importers’ data in
GMAD.
Year Total fish traded Total fish traded
(exporters’ data) (importers’ data)
1991 – 530,612
1992 – 639,070
1993 – 541,063
1994 – 467,715
1995 – 550,028
1996 8,540 812,661
1997 5,268 629,847
1998 15,739 1,326,953
1999 642,961 1,383,106
2000 1,695,414 605,532
2001 1,122,217 434,760
2002 94,084 17,481
2003 4,183 –
Tot al 3,588,406 7,938,828
number of species are associated with other habitats
such as seagrass beds, mangroves and mudflats.
According to data provided by exporters, the
Philippines, Indonesia, the Solomon Islands, Sri Lanka,
Australia, Fiji, the Maldives and Palau, together, supplied
more than 98 per cent of the total number of fish exported
between the years 1997 and 2002. (See Table 2.)
GMAD trade records from importers for years
1997-2002 showed that the United States, the United
Kingdom, the Netherlands, France and Germany were the
most important countries of destination, comprising
99 per cent of all imports of marine ornamental fish.
Exporters’ data revealed Taiwan, Japan and Hong Kong to
be important importing areas. (See Table 3.)
Looking at the most commonly traded families,
species of Pomacentridae dominate, accounting for 43 per
cent (according to importers’ data in GMAD) of all fish
traded. They are followed by species belonging to
Pomacanthidae, Acanthuridae, Labridae, Gobiidae,
Chaetodontidae, Callionymidae, Microdesmidae, Serrani-
dae and Blenniidae. (See Figure 1.)
For the years 1997-2002, the blue-green
damselfish (
Chromis viridis
), the clown anemonefish
(
Amphiprion ocellaris
), the whitetail dascyllus (
Dascyllus
aruanus
), the sapphire devil (
Chrysiptera cyanea
) and the
threespot dascyllus (
Dascyllus trimaculatus
) are the most
commonly globally traded species. (See Table 4, overleaf.)
The top ten species together account for 36 per cent of all
fish traded from 1997 to 2002, according to data provided
by importers.
19
Analysis of trade data
Table 2: Main source countries of marine ornamental fish
Tot al number of fish traded as derived from exporters’ and importers’ data for the years 1997 to 2002 in GMAD. Percentage of
total trade for individual countries is also presented.
Origin No. of fish exported % of total no. of Origin No. of fish exported % of total no. of
(exporters’ data) fish traded (importers’ data) fish traded
Philippines 1,523,854 43 Unknown 3,556,772 81
Indonesia 943,059 26 Indonesia 316,355 7
Solomon Islands 416,262 12 Fiji 237,872 5
Sri Lanka 183,537 5 Philippines 81,294 2
Australia 173,323 5 Sri Lanka 60,220 1
Fiji 131,746 4 Solomon Islands 25,732 1
Maldives 78,018 2 Maldives 22,165 1
Palau 63,482 2
Total 3,513,281 99 Total 4,300,410 98
Table 3: Main importers of marine ornamental fish
Tot al number of fish traded as derived from exporters’ and importers’ data for the years 1997 to 2002 in GMAD. Percentage of
total trade for individual countries is also presented.
Destination No. of fish imported % of total no. of Destination No. of fish imported % of total no. of
(exporters’ data) fish traded (importers’ data) fish traded
USA 1,462,347 41 USA 3,054,273 69
Unknown 788,230 22 United Kingdom 874,557 20
Taiwan 244,454 7 Netherlands 264,976 6
Japan 223,613 6 France 103,234 2
Hong Kong 152,738 4 Germany 99,955 2
France 132,439 4
Germany 119,739 3
Netherlands 117,248 3
Italy 70,686 2
United Kingdom 48,911 1
Total 3,360,405 93 Total 4,396,995 99
For the years 1997-2002,
Amphiprion ocellaris
,
Chromis viridis
, the bluestreak cleaner wrasse (
Labroides
dimidiatus
),
Chrysiptera cyanea
, the palette surgeon-
fish (
Paracanthurus hepatus
), and the sea goldie
(
Pseudanthias squamipinnis
) are the most commonly
imported species into the EU. Together the top ten
species make up 37 per cent of all fish imported into the
EU between 1997 and 2002, according to importers’ data.
(See Table 5.)
A similar analysis for the United States showed
that the top ten species (common to both exporters’ and
importers’ datasets), including
Dascyllus aruanus,
Chrysiptera cyanea, Dascyllus trimaculatus
and
Labroides dimidiatus,
accounted for 39 per cent of all fish
species exported to the United States. (See Table 6.)
Seahorses
GMAD importers’ data showed that for all years (1988-
2002) the United States imported a total of 67,998
seahorses. The main exporters were Sri Lanka, Brazil,
Indonesia and the Philippines. Based on exporters’
information (1999-2003), the United States imported 5,638
live specimens, Japan 2,711, Taiwan 3,412 and the rest of
the world 2,688.
20
From ocean to aquarium
Table 4: The ten most traded species of ornamental fish worldwide
Tot als for number of fish are derived from exporters’ and importers’ data in GMAD for years 1997 to 2002. Species common to
both datasets are in bold.
Species No. of specimens Species No. of specimens
(exporters’ data) (importers’ data)
Amphiprion ocellaris
145,015
Chromis viridis
322,587
Chrysiptera cyanea
111,705
Zebrasoma flavescens
198,869
Dascyllus aruanus
103,948
Amphiprion ocellaris
166,119
Amphiprion percula
101,092
Dascyllus aruanus
164,094
Chromis viridis
99,451
Pomacentrus australis
161,796
Abudefduf spp.
78,945
Chrysiptera parasema
156,069
Dascyllus trimaculatus
78,536
Chrysiptera cyanea
121,657
Paracanthurus hepatus
74,557
Dascyllus spp.
116,861
Dascyllus albisella
73,726
Dascyllus trimaculatus
102,650
Chrysiptera hemicyanea
61,914
Labroides dimidiatus
86,885
Total 928,889 Total 1,597,587
Table 5: The top ten species of ornamental fish imported into the EU
Tot als for number of fish are calculated from exporters’ and importers’ data in GMAD for years 1997 to 2002. Species
common to both datasets are in bold.
Species No. of specimens Species No. of specimens
(exporters’ data) (importers’ data)
Amphiprion ocellaris
44,881
Amphiprion ocellaris
123,640
Chromis viridis
29,717
Chromis viridis
103,682
Labroides dimidiatus
21,833
Chrysiptera cyanea
43,767
Chrysiptera hemicyanea
12,111
Chrysiptera parasema
42,576
Salarias fasciatus
12,019
Zebrasoma flavescens
38,411
Chrysiptera cyanea
11,776
Dascyllus trimaculatus
33,078
Paracanthurus hepatus
11,345
Labroides dimidiatus
33,073
Synchiropus splendidus
11,168
Paracanthurus hepatus
28,674
Pseudanthias squamipinnis
10,892
Pseudanthias squamipinnis
23,134
Acanthurus leucosternon
10,290
Nemateleotris magnifica
21,897
Total 176,032 Total 491,932
EC Annex D data show that 106,662 seahorses
were reported as imported into the EU between 1997 and
2001. GMAD data for this period show a total of 20,477
seahorses reported as imported into EU countries (or
24,647 specimens between 1996 and 2002). Data from
exporters show a total of 6,138 seahorses exported to the
EU between 1999 and 2003. Annex D data show the
Netherlands, Germany, Italy, Austria and the United
Kingdom as the main importers of seahorses in the EU,
accounting for some 94 per cent of all EU imports.
Similarly GMAD data from both importers and exporters
show the Netherlands, Germany, Italy and the United
Kingdom to have been the main European importers.
The Philippines, Indonesia, Sri Lanka, Brazil and
Singapore were the main countries of export and
accounted for 96 per cent (102,074 specimens) of all
reported imports of seahorses into EU countries between
1998 and 2001 according to Annex D data. GMAD
importers’ data show Sri Lanka, Indonesia, Brazil and the
Philippines to be the most significant exporters of
seahorses. Singapore does not appear as a significant
exporter of seahorses based on GMAD data compared to
more than 7,000 exports using Annex D figures.
Trade data from both Annex D and GMAD indicate
that
Hippocampus erectus
and
Hippocampus kuda
are
the most commonly traded species and show that a large
number of individuals are being traded as
Hippocampus
spp. (35 per cent of Annex D data, 73 per cent of GMAD
importers’ data). The large number of traded individuals
recorded as
Hippocampus
spp. is undoubtedly a reflection
21
Analysis of trade data
Table 6: The top ten species of ornamental fish imported into the United States
Tot als for number of fish are derived from importers’ and exporters’ data in GMAD for years 1997 to 2002. Species common to
both datasets are in bold.
Species No. of specimens Species No. of specimens
(exporters’ data) (importers’ data)
Abudefduf spp.
78,749
Chromis viridis
218,905
Chrysiptera cyanea
73,536
Pomacentrus australis
161,740
Dascyllus aruanus
72,435
Zebrasoma flavescens
160,458
Dascyllus albisella
60,328
Dascyllus aruanus
147,525
Amphiprion percula
59,710
Dascyllus spp.
116,306
Chrysiptera hemicyanea
38,162
Chrysiptera parasema
113,493
Paracanthurus hepatus
31,636
Chrysiptera cyanea
77,890
Chromis atripectoralis
30,912
Chrysiptera hemicyanea
76,960
Dascyllus trimaculatus
30,267
Dascyllus trimaculatus
69,572
Labroides dimidiatus
28,110
Labroides dimidiatus
53,812
Total 503,845 Total 1,196,661
Seahorse,
Hippocampus erectus.
The threespot dascyllus,
Dascyllus trimaculatus
.
of the difficulties experienced in identification of
individual species. The high level of synonymy in the
Hippocampus
genus also means that there may be errors
in the trade data. For example, reports indicate that there
may be more than one species traded under the name
H.
kuda
60. Indeed, seahorse taxonomy (identification of
individual species) has undergone many changes over
recent years and a number of new species have been
described60-62.
As an interesting note, although it is strictly illegal
to import tropical species under the name of
H. kuda
into
France166, GMAD lists a total of 328 specimens from
Indonesia, Sri Lanka and the Philippines as imported into
France as
H. kuda
between the years 1997 and 2001.
CORALS
The term ‘corals’ encompasses both stony corals, defined
as ‘marine colonial polyps characterized by a calcareous
skeleton that often form reefs63, soft corals and sea fans.
However, most literature found on trade in live coral
specimens refers to the trade in stony coral species.
There has been much debate about what exactly
constitutes a ‘soft coral’. The term is most commonly
used to refer to species of the subclass Octocorallia (class
Anthozoa), which have no massive skeleton. However, the
term ‘soft coral’ often extends to contain sea fans, which
are actually supported by an internal axis64 and hence will
be addressed separately here. In this report, we will use
the term ‘soft coral’ to include all species under the order
Alcyonacea (soft coral and Stolonifera) with the exception
of
Tubipora musica
which, due to its calcified skeleton, we
have included under stony corals. Overall, according to
data held in GMAD, there are 61 species of soft corals and
140 species of stony corals in trade, although this number
is to be treated with caution due to the complexity
experienced in coral taxonomy.
Stony corals
According to CITES data, the global live coral trade rose
steadily from 1997 to 1999 with 934,463 live pieces and
1,142,242 live pieces being traded worldwide respectively
in those years. The trade decreased to 942,661 pieces in
2001. Since the late 1980s, Indonesia has become the
largest coral exporting country32. CITES figures show that
direct exports of live wild-sourced coral from Indonesia
represented 78 per cent (729,703 pieces) of the global
total for all coral species in 1997, 66 per cent (640,190
pieces) in 2000 and 71 per cent (669,192 pieces) in 2001.
(See Figure 2.) The numbers are based on data reported
by importers because values based on exporters’ infor-
mation are an indicator of the number of permits issued
rather than the actual quantity of corals exported for the
aquarium trade. To illustrate the difference, in 2001 data
from all importers showed a total of 669,192 pieces
having been exported from Indonesia, whilst information
provided by exporters indicate 1,442,413 pieces were
exported from Indonesia.
Data from 1997 to 2001 show Indonesia, Fiji, the
Solomon Islands and Tonga together supplying more than
95 per cent of live coral exports. Since the late 1990s Fiji
has been playing an increasing role as an exporter of live
coral. It is the major source country of live coral for the
aquarium trade in the Pacific Islands with smaller
contributions from Tonga, Vanuatu and the Solomon
Islands. Fiji presently receives approximately US$12
million per year in export revenue from the trade in live
coral65. Although statistics on live coral exports are
available from the Fijian Fisheries Division, values cannot
be used to assess the volume of live coral being extracted
from Fiji as they include re-exports that originated
primarily from Tonga, the Solomon Islands, Vanuatu and
Bali, and data represent maximum permitted exports
rather than actual exports. Moreover, live coral export
figures have often tended to include live rock exports,
thus artificially inflating live coral statistics. Based on
these issues, the Fijian coral industry is presently under
review by the Fisheries Division to ensure that harvest
22
From ocean to aquarium
1.5
1.4
1.3
1.2
1.1
1.0
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0.0
Millions
3.5 million
71%
Indonesia Fiji Solomon
Islands
Tonga
18%
4%
Figure 2: Major exporters of live and wild-sourced
coral (pieces)
Tot als are derived from importers’ data.
1997
1998
1999
2000
2001
Tot al
3%
levels are sustainable and to agree a system under which
export statistics reflect true imports. A recent audit at one
of the largest Fijian export companies showed that the
actual export figure was approximately 9 per cent of the
recorded declared value45. Until this case has been
resolved and the CITES Secretariat has published agreed
quotas on the CITES website, Parties to the Convention
should not accept any export permits for specimens of
CITES-listed coral species from Fiji66.
For the years 1997 to 2001, CITES statistics show
the major importers of stony corals to be the United
States, Japanviii, Germany, France, China (including Hong
Kong), Canadaix, the Netherlands and the United
Kingdom, together importing more than 95 per cent of the
total number of live corals being traded worldwide. Taking
the EU as one statistical entity, 73 per cent of total live
coral imports are accounted for by the United States, 14
per cent by the EU, 7 per cent by Japan, 2 per cent by
China (including Hong Kong), 2 per cent by Canada and 1
per cent by the Republic of Koreax. (See Figure 3.)
Commonly traded coral genera, based on CITES
export and import data 1999-2001, include
Acropora
(staghorn, cluster, bluetip, bush, cat’s paw or bottlebrush
coral),
Catalaphyllia
(elegance coral),
Euphyllia
(anchor
or hammer coral),
Galaxea
(galaxy coral),
Goniopora
(flowerpot coral),
Heliofungia
(mushroom coral),
Lobophyllia
(lobed brain coral),
Plerogyra
(bubble or
grape coral),
Trachyphyllia
(open brain coral),
Turbinaria
(cup coral) and Scleractinia. However, the last is likely to
include a large proportion of traded live rock67. These
findings are corroborated by data within GMAD showing
the same genera as the top ten species in trade from both
importers’ and exporters’ datasets, from 1988 to 2002 and
1998 to 2003 respectively. GMAD also lists
Favia
and
Porites
as common in trade. With the exception of
Acropora
, most of the genera listed are slow-growing and
23
Analysis of trade data
1.5
1.4
1.3
1.2
1.1
1.0
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0.0
Millions
3.9 million
73%
USA EU Japanviii China*Canadaix Rep of
Koreax
14%
7%
2% 2% 1%
* Including Hong Kong.
Figure 3: Major importers of live and wild-sourced
coral (pieces)
The EU is taken as one ‘entity’. Totals are derived from
importers’ data except where otherwise stated.
1997
1998
1999
2000
2001
Tot al
Table 7: The top ten most commonly traded genera of corals worldwide
Tot als for number of pieces are derived from importers’ and exporters’ data in GMAD for years 1988 to 2002 and 1998 to 2003
respectively. Genera common to both datasets are in bold.
Genera No. of pieces Genera No. of pieces
(exporters’ data) (importers’ data)
Scleractinia* 208,122
Trachyphyllia
37,082
Goniopora
192,697
Euphyllia
31,614
Euphyllia
191,670
Goniopora
27,322
Trachyphyllia
115,262
Acropora
26,451
Catalaphyllia
90,498
Plerogyra
13,878
Acropora
79,720
Lobophyllia
11,933
Heliofungia
77,924 Scleractinia* 11,035
Plerogyra
60,691
Catalaphyllia
10,907
Porites
48,889
Favia
9,531
Turbinaria
47,729
Turbinaria
8,955
Total 1,113,202 Total 188,708
* Unidentified stony corals
some generally occur at low densities, although infor-
mation on both densities in the field and growth rates is
usually limited.
For the United States, the EU and Japan (the three
main importers), according to CITES data the top ten
species imported were combinations of species of the
above listed genera. (See Table 8.)
In 1997, Indonesia established quotas for coral
export. In 1999, the CITES Scientific Review Group of the
European Commission (SRG-EC) questioned the scientific
basis for the export quotas set by the Indonesian
authorities. This resulted in a temporary suspension (still
ongoing for many) of the export of the following seven
species of stony coral from Indonesia into the 15 EU
Member Statesxi:
Blastomussa merleti
,
Catalaphyllia
jardinei
,
Cynarina lacrymalis
,
Euphyllia divisa
,
Euphyllia
glabrescens
,
Plerogyra simplex
and
Trachyphyllia
geoffroyi
. In 2000, the trade suspension was extended to
additional species: the complete genera of
Euphyllia
and
Plerogyra
,
Hydnophora exesa
,
Hydnophora microconos
and
Blastomussa wellsi
. Since then positive opinions
(temporary import suspension is lifted) have been given
for
E. ancora
,
E. glabrescens
and
H. exesa
from
Indonesia. In addition negative opinionsvii (temporary
trade suspensions) on
Goniopora lobata
,
Plerogyra
turbida
,
Scolymnia vitiensis
and
Wellsophyllia radiata
for
Indonesia and
Blastomussa wellsi
,
Scolymnia vitiensis
,
Catalaphyllia jardinei
,
Euphyllia yaeyamaensis
,
Hydno-
phora rigida
,
Plerogyra simplex
,
P. sinuosa
and
Trachyphyllia geoffroyi
for Fiji have been formed69.
The EU import restrictions for stony corals have
been put in place mainly due to a lack of information on
their population status and life history characteristics.
Understanding the biology and life history of stony corals
is essential in developing ecologically sustainable quotas,
and the need for such research should be highlighted.
24
From ocean to aquarium
Table 8: The top ten species of corals imported into
the United States, the EU and Japan
Tot als for number of pieces are derived from importers’ data
in CITES for years 1997 to 2001. Japan’s data are based on
exporters’ reports for 1997 and years 1999-2001, as Japan’s
Annual Reports for 1999-2001 are not available and they did
not report any coral imports for 1997.
Top ten imports USA
Taxon No. of pieces
Scleractinia spp. 1,838,843
Euphyllia
spp. 304,257
Goniopora
spp. 201,847
Acropora
spp. 191,475
Trachyphyllia
spp. 180,351
Catalaphyllia
spp. 159,693
Plerogyra
spp. 116,623
Heliofungia actiniformis
96,515
Lobophyllia
spp. 65,016
Turbinaria
spp. 63,508
Top ten imports EU
Taxon No. of pieces
Scleractinia spp. 153,244
Acropora
spp. 47,917
Euphyllia
spp. 40,207
Goniopora
spp. 37,356
Trachyphyllia
spp. 26,254
Plerogyra
spp. 25,035
Catalaphyllia
spp. 23,884
Goniopora lobata
19,178
Heliofungia actiniformis
18,626
Goniopora stokesi
17,353
Top ten imports Japan
Taxon No. of pieces
Scleractinia spp. 44,232
Trachyphyllia geoffroyi
28,622
Catalaphyllia jardinei
20,657
Euphyllia glabrescens
17,099
Goniopora minor
16,342
Goniopora stokesi
15,836
Goniopora lobata
15,103
Heliofungia actiniformis
14,895
Euphyllia cristata
10,010
Goniopora
spp. 9,963
Button/meat coral,
Cynarina.
Soft corals and sea fans
Most of the soft corals in trade originate from the Indo-
Pacific Ocean. Although soft coral farming is considered
to be simple and straightforward70, very few specimens
are of cultured origin. American Samoa represents an
exception52. Despite high numbers of specimens being
traded for use in aquaria, soft corals are not, unlike
stony corals, covered under CITES54. No mechanisms
other than GMAD exist to monitor quantity, origin and
destination of species in trade. GMAD data indicate that
a total of 386,849 pieces of live soft coral (according to
importers’ data) were traded between 1988 and 2002.
Based on exporters’ data, the quantity of soft corals
traded between 1998 and 2003 accounted for 7 per cent of
all coral exports (soft and stony).
The United States is the world’s largest soft coral
importer, receiving 67 per cent (according to importers’
data for years 1988-2002 and equivalent to 259,472 live
pieces) of the total trade in soft corals. Indonesia appears
as the largest exporting country of soft corals.
Based on GMAD importers’ data (1988–2002),
the most commonly traded soft coral genera worldwide
are (ordered by genera most traded):
Sarcophyton
(leather/mushroom/toadstool coral),
Sinularia
(finger
leather/soft finger/digitate leather coral),
Xenia
(pulse coral),
Cladiella
(cauliflower/finger/colt/blushing
coral),
Clavularia
(clove polyp),
Anthelia
(waving hand
polyp),
Lobophytum
(finger leather coral),
Nephthea
(broccoli coral),
Dendronephthya
(carnation/strawberry
coral) and
Cespitularia
(blue xenia).
25
Analysis of trade data
The trade in leather coral,
Sarcophyton
spp.
Sarcophyton
spp. is the most commonly traded soft
coral. This mushroom-like zooxanthellatexiii species is
hardy, fast growing and easily propagated in aquarium
conditions. Under the
Sarcophyton
genus at least
five species are known to be traded as aquarium
specimens:
S. ehrenbergi, S. glaucum, S. latum, S.
tenuispiculatum
and
S. trocheliophorum
. As reported
by importers in GMAD these five species made up 17
per cent of the total amount of soft corals traded
(importers’ data 1988-2002).
Indonesia emerged as the world’s major
exporter of
Sarcophyton
spp., supplying 85 per cent of
the total global trade in this species (exporters’ data
1998-2003). The United States was the world’s largest
importer, accounting for 64 per cent (according to
importers’ data) of the total number of soft corals
traded.
The trade in carnation coral,
Dendronephthya
spp.
Dendronephthya
spp. is among the top ten traded soft
corals. Species under this genus are extremely
difficult to maintain in aquaria as they are
azooxanthellate and hence entirely dependent on
filtering particles and absorbing dissolved nutrients
from the water column. In captivity they usually die
within a few weeks. Aquarists are strongly
encouraged not to keep
Dendronephthya
spp. Two
species in particular are known to be traded as
ornamentals:
D. klunzingeri
and
D. rubeola
.
Between 1988 and 2002 a total of 12,618 live
pieces of
Dendronephthya
spp. were traded globally.
Worldwide, the United States emerged as the largest
importer, accounting for 51 per cent of the total trade
in
Dendronephthya
spp. Indonesia emerged as the
biggest exporter of
Dendronephthya
spp. (20 per cent
of all soft coral traded according to importers’ data).
Eight genera of sea fans appear in GMAD
trade records:
Ctenocella
,
Echinogorgia
,
Ellisella
,
Euplexaura
,
Gorgonia
,
Lophogorgia
,
Pseudopterogorgia
and
Rumphella
. The genus
Gorgonia
is the most well
known and commonly traded sea fan (14 per cent or
55,375 pieces according to importers’ data 1988-2002),
with at least two species often recorded in GMAD:
G. flabellum
and
G. ventalina
. US imports accounted for
99 per cent (54,976 pieces) of all imported
Gorgonia
spp. specimens.
26
From ocean to aquarium
Fiji is the world’s primary supplier of live rock, with data
showing that in 2001 more than 800 tonnes of live rock
were harvested from its reefs73, about 95 per cent of
which were destined for the United States74. True
collection figures are likely to be greater as large
quantities of harvested live rock, subsequently
considered unsuitable for export, are often discarded and
thrown back into the sea. In Fiji, the extraction of live rock
takes place along the edges of the reef or within the
shallow lagoon. During collection villagers selectively
target rocks with a diameter of 15-35 cm45 covered with
light to dark pink coralline algae and remove them from
the reef framework using iron rods. These are then
loaded up onto a
bilibili
, or bamboo raft, and dragged onto
the beach by horses. The rocks are placed into boxes and
loaded onto a waiting truck that takes them to a
processing facility. Once at the facility, the rock is placed
under showers, which continually spray salt water for
24–72 hours before shipment. It is trimmed of all visible
green algae growth and graded according to shape,
weight and percentage of coralline algae cover.
Live rock trade constitutes an important source of
revenue for the inhabitants of Malomalo (one of the most
important live rock collection sites in Fiji). Since 1994, live
rock has been collected at Malomalo for Ocean 2000, a
local wholesaler, by the traditional male users of the reef,
both on a full time and an occasional basis. The rock is
reimbursed at a price of US$0.70 per kilo, which is
divided among the collectors (US$0.50), the custodian
(US$0.10) and the marine reserve that forms part of the
village’s traditional fishing grounds (US$0.10). As this
item is bought and sold by weight it is the highest income
earner for the villagers participating in the aquarium
trade industry. A full-time harvester extracts on average
7,500 kg a year (an average of 150 kg live rock extracted
per week) contributing US$3,750 to annual household
income.
However, after nine years of extraction, the
villagers raised concerns that live rock collection could
have detrimental long-term consequences for their
reefs. Large-scale removal of live rock, the result of
hundreds of years of accretion, can destroy reef habitat,
undermining the structure of coral reefs and leading to
increased erosion as well as reduced biodiversity. Some
fishers noticed that quantities of fish and other marine
species typically collected from areas used for collection
of live rock had been reduced45. The World Wide Fund for
Nature (WWF) and MAC joined forces to respond to the
villagers’ concerns and those expressed by the Fijian
government about the sustainability of the industry. They
worked to develop community-based processes for wise
coral harvesting and management, which also involved
helping the government structure sound policies and
legislation that would support a sustainable aquarium
trade. Moreover, the villagers of Malolomo designated
part of their traditional fishing grounds a
tabu
area, in
which extractive use was banned.
The International Coral Reef Action Network
(ICRAN) recently also developed a project with the major
objective of ensuring the sustainability of the coral trade
industry in Fiji. Should this be achieved, coastal com-
munities (mainly around Viti Levu, where returns often do
not reflect the market value of the product) will be able to
share fairly the benefits of the marine aquarium trade
industry without compromising the health of their reefs.
Source: WWF73 and ICRAN76
Live rock
Live rock
CITES defines live rock as ‘pieces of coral rock to which
are attached live specimens of invertebrate species and
coralline algae not included in the CITES Appendices and
which are transported moist, but not in water, in crates71.
Typical inhabitants of live rock are anemones, tunicates,
bryozoa, octocorals, sponges, echinoids, molluscs,
sabellarid and serpulid tubeworms, and calcareous
algae. Besides the aesthetic role live rock plays in
aquaria, the organisms which live in live rock, through
consumption of waste and production of oxygen, filter the
water and prevent the build-up of nitrate.
There are three ‘types’ of live rock in trade:
Pacific, Atlantic and aquacultured. Hobbyists tend to
prefer Pacific rock because it is very porous, light, and
usually has a nice cover of coralline algae72. Atlantic live
rock is less popular because it is fairly dense and the
rock’s shapes are less intricate than those commonly
found in Pacific rock. Due to the large amounts of coral
rock being exported from the Florida Keys in the early
1990s, the State banned the harvest of live rock from its
waters in 1997. As a result, marine ornamental
companies in the United States started to develop
aquaculture for live rock. To ‘create’ such live rock,
27
Analysis of trade data
Table 9: Main source countries of marine ornamental invertebrates
Tot al number of invertebrates traded as derived from exporters’ data (1998-2003) and importers’ data (1988-2002) in GMAD.
Percentage of total trade for individual countries is also presented.
Origin No. of invertebrates % of total no. Origin No. of invertebrates % of total no.
imported traded imported traded
(exporters’ data) (importers’ data)
Indonesia 561,506 44 Unknown 2,441,742 80
Philippines 460,817 36 Mexico 246,485 8
Sri Lanka 100,309 8 Indonesia 104,282 3
Solomon Islands 75,305 6 Singapore 68,190 2
Fiji 53,823 4 Fiji 48,358 2
Palau 10,315 1 Sri Lanka 33,782 1
Philippines 29,440 1
Vanuatu 15,904 1
Total 1,262,075 99 Total 2,988,183 98
Table 10: Main importing countries of marine ornamental invertebrates
Tot al number of invertebrates traded as derived from exporters’ data (1998-2003) and importers’ data (1988-2002) in GMAD.
Percentage of total trade for individual countries is also presented.
Destination No. of invertebrates % of total no. Destination No. of invertebrates % of total no.
imported traded imported traded
(exporters’ data) (importers’ data)
USA 445,085 35 USA 2,454,350 80
Taiwan 275,024 22 United Kingdom 453,430 15
France 140,032 11 Netherlands 61,525 2
Unknown 127,342 10 France 51,768 2
Germany 69,840 5 Germany 49,359 1
Japan 50,456 4
Netherlands 37,253 3
Italy 33,667 3
United Kingdom 22,545 2
Hong Kong 18,190 1
Total 1,219,434 96 Total 3,070,432 100
regular dry rock is placed in the ocean and harvested
one to several years later.
Live rock can be purchased either ‘cured’ or
‘uncured’. On collection from the ocean the rocks harbour
a large variety of sea life some of which, such as certain
species of anemones and mantis shrimp, are common
pests on live rock. ‘Uncured’ rock is rock that has been
collected and directly exported. ‘Cured’ rock, on the other
hand, is material that has been placed under a fine spray
of high salinity water for several hours or days prior to
export. The objective is to keep the coralline algae alive
but kill and wash out less hardy, unwanted organisms,
which would foul the tank water.
According to CITES importers’ data (1990-2001)
the United States, the EU, the Republic of Korea, Hong
Kong and Canada, together, imported a total of 3,897,654
pieces of live Scleractinia spp. of which one can assume a
large component to be live rock67. The same data also
show the United States, the EU and Canada importing
2,048,630 kg of Scleractinia spp. Based on importers’ data
(1990-2001) Fiji, the Marshall Islands, Tonga, Samoa, the
Solomon Islands, the ex-Trust Territories (Northern
Mariana Islands, the Republic of Palau, the Federated
States of Micronesia), Vanuatu, Haiti, Indonesia and the
Dominican Republic emerged as the top ten exporters of
live wild-sourced Scleractinia spp. supplying 2,047,785 kg
28
From ocean to aquarium
Topshell or snail
Tectus
spp.,
Trochus
spp. (pictured) and
Turbo
spp. are
gastropod molluscs found on shallow tropical reefs
throughout the Indo-Pacific. These species are mainly
herbivorous, feeding on fleshy algae and algal films
that typically develop on live rock, although they are
also known to forage on organic detritus77. They do
well in aquarium conditions when provided with ample
hiding places and room to forage, since overcrowded
conditions may cause stress and disease. Although
trochus farms are now well established in many of the
Pacific Island states, they are mainly cultured to craft
buttons and jewellery and for food consumption. Thus
most specimens in trade as marine ornamentals were
probably collected in the wild78.
Table 11: The ten most traded species of marine
ornamental invertebrates worldwide
Tot als for number of invertebrates are derived from
exporters’ and importers’ data in GMAD for years 1998 to
2003 and 1988 to 2002 respectively. Species common to
both datasets are in bold.
Species Common No. of
name specimens
(exps’ data)
Trochus
spp. Topshell or 272,203
trochus shell
Unspecified 247,038
invertebrates
Lysmata
spp. Cleaner shrimp 107,452
Heteractis
spp. Sea anemone 54,369
Stenopus
spp. Banded coral shrimp 42,802
Tridacna
spp. Giant clam 37,521
Linckia
spp. Blue sea star 32,509
Rhynchocinetes
spp. Camel shrimp 30,846
Stichodactyla
spp. Carpet anemone 27,341
Strigopagurus
spp. Hermit crab 24,512
Total 876,593
Species Common No. of
name specimens
(imps’ data)
Turbo
spp. Turbo snail 328,778
Lysmata
spp. Cleaner shrimp 288,484
Condylactis
spp. Condy/Atlantic/ 229,925
Haitian anemone
Heteractis
spp. Sea anemone 149,025
Dardanus
spp. Hermit crab 147,006
Tectus
spp. Mollusc 143,448
Paguristes
spp. Hermit crab 136,280
Sabellidae
spp. Feather worm 128,248
Actinodiscus
spp. Disc/Mushroom 123,357
anemone
Stenopus
spp. Banded coral 93,449
shrimp
Total 1,768,000
to the trade (probably mostly aquarium). CITES data
based on importers’ information showed Indonesia, Fiji,
Tonga, Solomon Islands, Samoa, the Marshall Islands,
Haiti, the ex-Trust Territories, Singapore and Vanuatu to
also supply the trade with 3,892,169 pieces.
As with live coral export statistics, government
statistics for Fijian live rock exports cannot be used to
assess the volume of live rock being extracted from Fiji.
From January to July 1999, the largest Fijian
exporter shipped 291,837 kg of live rock, 48 per cent
of the permitted quota of 606,000 kg. Despite this fact,
and the fact that the shipment included live rock from
Tonga, 606,000 kg is the figure recorded in Fiji export
data45.
INVERTEBRATES
Many invertebrates other than corals are popular in the
aquarium trade. According to data held in GMAD, 516
species of invertebrates are being traded for the
aquarium trade. However, this figure needs to be treated
with some caution due to the lack of a standard taxonomy
for marine invertebrates.
Based on GMAD a total of 1,271,547 invertebrates
were traded between 1998 and 2003, according to
exporters’ information (or 3,071,385 according to
records from importers between 1988 and 2002). Mexico,
Indonesia, Singapore, Fiji, Sri Lanka, the Philippines and
Vanuatu emerged as the main exporters (according to
importers’ data for the years 1988-2002), accounting for
close to 17 per cent of the trade. Exporters’ data for the
years 1998-2003 also showed the Solomon Islands and
Palau to be significant source countries of marine
ornamental invertebrates. (See Table 9, p 27.)
Based on importers’ data the main destination
countries were: the United States, the United Kingdom,
the Netherlands, France, Germany, Italy and Canada,
constituting close to 100 per cent of all marine
invertebrates imported for the marine aquarium
trade between 1988 and 2002. Looking at exporters’
data for the years 1998-2003 Taiwan, Japan and Hong
Kong also emerged as important importers. (See Table
10, p 27.)
The main species in trade and common to both
exporters’ and importers’ datasets within GMAD are
Lysmata
spp.,
Heteractis
spp. and
Stenopus
spp. (See
Table 11, p 28.) Other species, which occur in only one
dataset’s top ten, include
Turbo
spp.,
Tridacna
spp. and
Trochus
spp. All top ten species together account for 67
per cent of all invertebrates traded between 1998 and
2003 (according to exporters’ data).
The ten most traded invertebrates are mainly
comprised of species that feed on algae (e.g.
Tectus
spp.,
Trochus
spp. and
Turbo
spp.), parasites or dead tissue
(e.g. cleaner shrimp) and dead animals (e.g. hermit crabs).
These species are particularly important in controlling
algae growth and parasites that may find a host in fish kept
in aquaria. However, removal of cleaner species from their
natural habitats may lead to a reduction in diversity on
harvested reefs as their function is then absent (see box on
Cleaner fish in Conservation issues, page 36).
Giant clams
Giant clams represent an increasingly large proportion
of the exports of live invertebrates destined as aquarium
specimens. Although additional lighting is often
required in order to maintain giant clams, they play an
important role in removing nitrates, nitrites and
ammonia from aquaria water, elements considered as
29
Analysis of trade data
Blue starfish,
Linckia laevigata
The most commonly imported sea star in the aquarium
trade is
Linckia laevigata
. According to exporters’ data
within GMAD this species accounted for 3 per cent
(32,509 pieces) of the total trade in invertebrates.
Experienced hobbyists warn that they are very difficult
to maintain in aquarium conditions79. Their poor
survival rate in aquaria may be due to their dietary
needs of organically enriched films (or detritus) that
typically cover live rock77. They should therefore not be
placed in a newly set up tank (less than six months), or
one in which there is not enough live rock to explore.
Furthermore, they are known to often refuse artificial
aquarium food. As common predators of sea stars in
captivity are dog-faced puffers (
Arothron nigropunct-
atus
), these two species should not be allowed to co-
exist in an aquarium. Small parasitic snails (
Thyca
crystallina
) are also known to prey on
L. laevigata
79.
30
From ocean to aquarium
The nine giant clams (tridacnids) common in trade
❏
Tridacna maxima
: the rugose or small giant clam is the
most wide-ranging of all giant clam species, being found
from the east coast of Africa, through the Indian Ocean and
across the Pacific to Polynesia and Pitcairn83. It is still
relatively abundant throughout its range although its status
in the Indian Ocean is poorly known. It has a distinct brightly
coloured mantle (blue, green and brown), which makes it
particularly attractive for the aquarium trade. GMAD data
show a total of 15,172 specimens as exported from Viet Nam,
Fiji, the Solomon Islands, Tonga, Vanuatu, the United States
and unknown countries between 1991 and 2001 (importers’
data) (or a total of 8,215 from Fiji and the Solomon Islands
between 2000 and 2001 based on exporters’ data).
❏
T. squamosa
: the fluted or scaly giant clam has a generally
speckled mantle in blue, brown and green. Like
T. maxima
, it
is fairly abundant throughout its range although little is
known of its status in the Indian Ocean. GMAD data show a
total of 6,711
T. squamosa
as exported from Fiji, Indonesia,
the Solomon Islands, Vanuatu, Viet Nam and unknown source
countries between 1991 and 2001 (importers’ data) (or a total
of 2,339 from Fiji, Indonesia and the Solomon Islands
between 1999 and 2001 based on exporters’ data).
❏
T. crocea
:the crocus or boring giant clam, although
smaller, is similar to
T. maxima
in that it has a brightly
coloured mantle. It is assumed to be generally widespread
throughout its distribution area, from the west coast of the
Malaysian peninsula, the South China Sea, the Coral Sea,
southern Japan to southern Australia, to Micronesia and east
to Palau83. Like
T. maxima
it is a popular species in the
aquarium trade. GMAD data show a total of 11,685
T. crocea
as exported from the Solomon Islands, Vanuatu, Viet Nam
and unknown source countries between 1991 and 2001
(importers’ data) (or a total of 17,881 from Fiji, Indonesia and
the Solomon Islands between 2000 and 2001 based on
exporters’ data).
❏
T. gigas
:is considered to be the true giant clam as it can
reach dimensions of more than 1.4 m in shell length. The
mantle is brown-green with blue or green spots. This species
is particularly sought after for food. It has suffered extensive
reductions throughout its range due to overexploitation and
is extinct in Fiji, Guam, New Caledonia, most areas of the
Philippines and the Northern Marianas. Population levels
have been dangerously reduced in most of Japan, Taiwan,
Tuvalu, the Federated States of Micronesia and Vanuatu.
GMAD data show a total of 1,808
T. gigas
as exported from the
Solomon Islands, Vanuatu and unknown source countries
between 1991 and 2000 (importers’ data) (or a total of 149
from Palau, Indonesia and the Solomon Islands between
2000 and 2001 based on exporters’ data).
❏
T. derasa
: the smooth or southern giant clam is the second
largest species with its shell reaching lengths of up to 60 cm.
Its mantle has elongate brown, green and blue patterns. It is
known to be fairly abundant in Palau, northern Papua New
Guinea, Australia, the Solomon Islands, New Caledonia, Fiji
and Tonga. Although it has been reintroduced in a number
of locations outside its natural range, wild stocks have
only become established in Yap. GMAD data show a total
of 24,960
T. derasa
exported from the Solomon Islands,
Vanuatu and unknown source countries between 1988 and
2001 (importers’ data) (or a total of 8,937 from Fiji, Palau,
Indonesia and the Solomon Islands between 2000 and 2001
based on exporters’ data).
❏
T. tevoroa
: the deep water devil clam is a rare species that
only lives at depths greater than 20 m in the northern Tonga
Islands and eastern Fiji Islands. No data in GMAD.
❏
T. rosewateri
:is a newly described species similar to
T.
squamosa
. It has a very restricted range, only occurring on
the Saya de Malha Bank, Mauritius, in the Indian Ocean. No
data in GMAD.
❏
Hippopus hippopus
:the bear paw, horse’s hoof or
strawberry giant clam has a heavy and thick shell with a dull
yellow-brown mantle. Its distributional range is similar to
that of
T. crocea
but population numbers are lower and local
extinctions have occurred. GMAD data show a total of 58
H.
hippopus
as exported from the Solomon Islands and
unknown source countries between 1999 and 2000
(importers’ data) (or a total of 551 from Palau and the
Solomon Islands between 2000 and 2001 based on
exporters’ data).
❏
H. porcellanus
:the china clam, has a very limited range
in the region of Indonesia, the Philippines and Palau. Its
appearance is similar to that of
H. hippopus
. No data in
GMAD.
Source: Wells
80
, Ellis
81
, Raymakers et al
82
and data from GMAD.
poisonous in high quantities for other living animals in
the tank.
Belonging to the family Tridacnidae and composed
of two genera,
Tridacna
(seven species) and
Hippopus
(two species), giant clams are the largest bivalves in the
world. Their range stretches across the Indo-Pacific
region from the eastern coast of Africa in the west to the
south Pacific in the east80.
All species of giant clams have traditionally been
harvested as a subsistence food source throughout their
range. Clam shells have also been used as ornaments in
the curio trade and as troughs for holding water or
feeding livestock80. More recently, their meat has been
served as a delicacy, even considered as an aphrodisiac
in some Asian and Pacific countries. The more brightly
coloured (
T. maxima, T. crocea
and
T. derasa
) species
have been popular organisms in the marine ornamental
trade81, with
T. squamosa
and
T. gigas
also being traded
but in smaller numbers. Unsustainable exploitation
ranging from legal commercial and subsistence use to
illegal poaching activities of giant clam species has led to
the local extinctions of some species such as
T. gigas
in
at least four of the 20 countries and territories where it is
known to have occurred84. As a result of overexploitation,
all species of giant clams are listed in CITES Appendix II.
However, CITES annual report data do not include trade
by non-CITES signatories, which include all South Pacific
countries except Papua New Guinea and Vanuatu and
large importers such as Taiwan85. According to the IUCN
Red List 2000, four species of Tridacnidae are classified
as vulnerable (
T. derasa, T. gigas, T. rosewateri
and
T. tevoroa
) and the five others are considered to be
at lower risk. Import suspensions into the EU exist for
all wild specimens of the following country-species
combinations:
H. hippopus
from New Caledonia,
T.
crocea
from Viet Nam,
T. derasa
from Tonga,
T. gigas
from Guam, Federated States of Micronesia, Fiji,
Indonesia, Marshall Islands, Palau, Papua New Guinea
and Vanuatu, and
T. squamosa
from Tonga, Viet Nam and
New Caledonia86. Negative opinions were also formed for
Hippopus hippopus
from Tonga, Vanuatu and Viet Nam,
T. crocea
from Fiji, Tonga and Vanuatu,
T. derasa
from
Fiji, New Caledonia and Vanuatu,
T. gigas
from Tonga
and Viet Nam,
T. maxima
from the Federated States of
Micronesia, Fiji, the Marshall Islands, Mozambique, New
Caledonia, Tonga, Vanuatu and Viet Nam,
T. rosewateri
from Mozambique,
T. squamosa
from Fiji, Mozambique
and Vanuatu and
T. tevoroa
from Tonga69.
31
Analysis of trade data
Table 12: Number of giant clams wild sourced, captive bred and from other origins traded worldwide
Tot als for number of clams are derived from CITES data for years 1993 to 2001. Percentage of total trade for each source
category is also presented.
Source 1993 % 1994 % 1995 % 1996 % 1997 % 1998 % 1999 % 2000 % 2001 % Total
Wild 9,485 20 15,739 26 55,830 62 60,449 85 47,394 61 92,671 82 93,198 74 94,159 82 96,662 76 565,587
Captive bred 7,402 15 5,731 10 6,913 8 9,303 13 28,989 37 19,783 18 32,789 26 20,695 18 27,318 22 158,923
Other 31,546 65 38,249 64 27,721 30 1,153 2 1,256 2 157 0 319 0 531 0 2,735 2 103,876
Grand total 48,433 100 59,719 100 90,464 100 70,905 100 77,639 100 112,611 100 126,306 100 115,385 100 126,715 100 828,386
Other: unspecified, no reported source, pre-convention, ranched, Illegal/seizure
0
10
20
30
40
50
60
1993 94 95 96 97 98 99 00 2001
Philippines
Tonga
Solomon Is.
Fiji
Micronesia
Vanuatu
Viet NamMarshall Is.
No. of clams (000)
Figure 4: Major exporters of live and wild-sourced
clams
Tot als are derived from importers’ data as Viet Nam,
Philippines, Fiji and Vanuatu report on the basis of
permits issued and not on actual trade, and not all
exporters are Party to CITES.
Several source countries have also implemented
legislation to better manage and protect their giant clam
stocks. In 1996, the Philippines, previously dominating
exports for the international shell trade and one of the
main suppliers of live clams for the international
aquarium trade, adopted a total prohibition on all exports
of giant clam82. The Solomon Islands reported that only
exports of cultured giant clams were allowed, while with
help from the International Marinelife Alliance, the
government of Vanuatu recently banned collection and
exports of wild specimens of
T. crocea
for the aquarium
trade and proposed the establishment of quotas for
collection of other giant clam species on outer islands87.
Wild stocks of giant clams (especially of the
largest species
T. gigas, T. derasa
and
T. tevoroa
) have
experienced drastic declines over the last 20-30 years as
a result of high levels of exploitation for subsistence
purposes, and probably to a greater extent due to
commercial harvesting for their meat and shells.
However, the demand for live giant clams for aquaria has
also grown considerably in recent years. Figures for the
extent of the trade are patchy and fluctuate considerably
between years (see Table 12, p 31), but CITES data show
that total exports of giant clams (all species included)
have significantly increased from a total of 48,642
individuals in 1993 to 126,715 individuals in 2001. In 1993,
wild-caught giant clams represented 20 per cent of all live
specimens, versus 15 per cent originating from
mariculture facilities. In 2001, 76 per cent of all giant
clams in trade as marine ornamentals had been caught in
the wild, whereas 22 per cent had been reared.
Although maricultured clams sold for the
aquarium trade command the highest prices, hobbyists
often prefer wild-caught specimens, as farmed individuals
tend to have less highly coloured mantles45. However,
advances in selective breeding techniques have meant that
clams can now be bred for brighter mantle colours. Pacific
island nations such as (ranked in order of importance) the
Solomon Islands, Marshall Islands, Fiji and Tonga are the
main exporters of live captive-bred giant clams.
Based on CITES data from 1993 to 2001, the major
source countries of live wild-sourced giant clams for the
aquarium trade are Viet Nam, the Philippines, the
Solomon Islands, Tonga, Fiji, Vanuatu, the Marshall
Islands and Micronesia. However, the role of individual
countries changed considerably over those years. With
exports from the Philippines being banned in 1996,
exports from other source countries increased slightly
(with the exception of the Solomon Islands whose trade
has decreased) allowing Viet Nam to dominate exports as
early as 1998 (see Figure 4, p 31).
The main importers of giant clams are the United
States, the EU and Hong Kong (using CITES data from
1999 onwards). Although the United States used to
dominate imports of live giant clams, the total number of
specimens imported into the EU has been greater than
numbers imported into the United States since 1999 (see
Figure 5).
32
From ocean to aquarium
0
10000
20000
30000
40000
50000
60000
70000
80000
0
10
20
30
40
50
60
70
80
1993 94 95 96 97 98 99 00 2001
EU USA Hong Kong
No. of clams (000)
Figure 5: Top three importers of live and wild-
sourced clams
Tot als are derived from importers’ data.
A
Accounts of destructive collection practices, the
introduction of alien species, over-harvesting,
the lack of scientific information for many species
collected and the threat of extinction of target species
have raised concern about the marine aquarium trade
among politicians and conservation organizations alike.
A number of policy regulations have already been put
in place; more are being called for17 and may follow.
The US government, for example, is considering ‘taking
appropriate action to ensure that international trade in
coral reef species for use in US aquariums does not
threaten the sustainability of coral reef species’12.
DESTRUCTIVE HARVESTING PRACTICES
Destructive fishing techniques include the use of sodium
cyanide and other chemicals to stun and catch fish.
Cyanide usually only stuns fish (although high mortality
rates are often recorded post-capture), but it may destroy
coral reef habitat by poisoning and killing non-target
animals, including corals88, 89. Other chemicals, including
quinaldine and plant toxins, are also used to capture reef
fish alive. Field data are difficult to obtain due to the often
clandestine nature of these practices.
During the collection of coral pieces for the coral
trade, many more colonies may be damaged or broken
than are actually harvested19. The breaking of corals to
ease access to fish for capture is also not unusual in many
collection areas. This tends to be more common with
branching species in which small fish, such as a number
of species of the genera
Dascyllus
and
Chromis
,often find
refuge90. However, there are a number of collection areas
that support many species for the aquarium trade that are
rocky or ‘rubbly’ in nature, thus reducing damage to coral
reefs. In soft bottom habitats for example, where corals
are not attached to the substrate, the use of tools to
remove colonies is unnecessary46.
Collection of live rock has been considered as
potentially destructive as it may lead to increased erosion
and loss of important fisheries habitat91. Some harvesting
areas in Fiji, for example, have been converted into
unconsolidated rubble, possibly preventing areas from
recovering over the long term19. A study looking at the
impact of the collection of coral and other marine
organisms for the aquarium trade showed that areas fully
utilized for the collection of live rock had experienced
severe disruption of the reef flat, leading to algal
predominance and potential declines in fisheries45. By
contrast other collection sites showed that harvest of live
rock had little effect on the relatively sparse coral growth
and probably also on the three-dimensional structure of
the reef as the entire reef flat had little topographic
variability45. Overall, this relatively new trade, and its
impacts, have not been well studied and more research
should look into the potential impact of live rock removal
on surrounding reef habitat and associated fauna.
Monitoring of extraction activities and of trade in live rock
is also recommended.
Fishing on coral reefs with dynamite and
explosives is not part of the marine aquarium trade: this
is a common misconception. Dynamite is a method
commonly used for food fishing. It causes terrible damage
not only to fish populations but also to the reef habitat
itself and may be an issue worthy of more concern than
the use of cyanide92.
Cyanide
Cyanide fishing involves crushing cyanide pellets into
makeshift squirt bottles filled with seawater. The fishers
then dive down to coral formations and squirt cyanide into
crevices where fish often hide. The poison stuns fish, thus
making them easier to catch. Large percentages of fish
captured through this method die in transit due to their
weakened state93, resulting in more fish being collected
than would otherwise need to be, to allow for a fatality
margin94. Reports indicate that between as few as 5 per
cent95 in 6 and as many as 75 per cent96 of fish collected
using narcotics die within hours of collection, and 20 per
cent95 to 50 per cent die soon after that97. About another
30 per cent on average96 die prior to export and it is not
unusual for retail outlets in importing countries to
33
From ocean to aquarium
Conservation
issues
Imperator angelfish,
Pomacanthus imperator.
register mortalities of 30 per cent or more50. A 1997
survey of US retailers98 found that between one third and
more than half of the aquarium fish imported from
Southeast Asia died shortly after arrival, most probably
due to poisons used in capture and/or the stress of
handling and transport.
Cyanide fishing is not without risks to the divers
themselves, who often go to considerable depths
for extended periods of time and may suffer from
decompression sickness, ‘the bends’, upon return to the
surface.
The use of cyanide to capture reef fish originated
in Taiwan and/or the Philippines in the 1960s and was
specifically targeted at fish destined for the aquarium
market94, 102, 103. Estimates suggest that in the mid-1980s
more than 80 per cent of all fish harvested in the
Philippines and destined for the aquarium trade were
collected using cyanide94. More recent studies in the
country indicate that 70 per cent of marine ornamental
reef fish are caught with cyanide102, 104. Its use then spread
to Indonesia (in about 1985105) where, in the mid-1990s, it
was estimated that about 90 per cent of vessels
transporting live fish in the eastern islands of Indonesia
had cyanide on board106. Reports also indicate its use in
Thailand6, Papua New Guinea105, 107, Malaysia, Viet Nam,
the Maldives108 and Yemen109. There are unconfirmed
reports that its use may have spread to the Red Sea,
Palau, Tanzania, the Seychelles, Sri Lanka, the Marshall
Islands, the Solomon Islands, Fiji and Haiti108.
Cyanide fishing is illegal in most countries. In
Indonesia, for example, legislation from 1985 includes
specific prohibition of the use of destructive fishing
practices, such as the use of poison, with penalties up to
ten years in prison and/or a fine of 100 million rupiahs110
(equivalent to US$12,000). The marine police and navy, in
collaboration with the fisheries service, are in charge of
enforcing the law110. However, the high premium paid
(often allowing for large bribes), the ease with which a
great number of fish can be caught in a short time period,
the often poor law enforcement capacities and high levels
of corruption have allowed the use of poison to spread
rapidly throughout the Asia-Pacific region102 and have
made the eradication of this illegal and highly destructive
fishing technique nearly impossible.
In 1989, the Haribon Foundation in collaboration
with Ocean Voice implemented, in the Philippines, the
Alternative to Cyanide Fishing project in order to train
aquarium collectors in the use of nets as an alternative to
sodium cyanide. Results showed that 29 per cent of the
trainees monitored were fully converted net users whilst
the majority of fishers persisted in using sodium cyanide,
though at a greatly reduced rate111. Subsequently, the
Philippines government and the International Marinelife
Alliance implemented a second, more aggressive
programme to retrain fishers in alternatives to
cyanide51, 112. Public campaigns in the media and schools
are also helping to raise awareness about the values of the
reefs of the Philippines and the negative impacts of cyanide
fishing113. Five cyanide-detection facilities, capable of
detecting low levels of cyanide in fish tissues as well as
organs, have also been established. After five years of
intensive efforts, live reef fish that test positive for cyanide
declined from 80 per cent in 1993 to 20 per cent in 199851, 98.
A similar programme initiated in Indonesia for
fishers in northern Sulawesi showed that barrier nets did
34
From ocean to aquarium
Cyanide use and corals
One of the greatest threats posed by cyanide fishing is
to reef ecosystems99, 100. Cyanide kills non-target
organisms, such as other invertebrates and fish,
although only relatively limited scientific data are
available on this. Reports have demonstrated that
exposure of corals to cyanide causes bleachingxiv, 88, 89.
Results from a recent study101 demonstrated that
exposure of colonies of the commonly traded species
Acropora millepora
,
Goniopora
spp
., Favites abdita,
Trachyphyllia geoffroyi, Plerogyra
spp
.
(grape coral,
pictured),
Heliofungia actiniformis, Euphyllia divisa
and
Sarcophyton
spp. to varying concentrations of
cyanide over different time periods caused mortality in
all corals (through, for example, bleaching and
progressive tissue detachment from the skeleton).
Acropora
, the genus most likely to be specifically
targeted by fishers for the collection of fish, as these
tend to hide amongst its branches, was most
vulnerable to cyanide exposure, showing rapid signs of
stress and bleaching101.
not prove to be an effective collection method and many
collectors have been slow to switch to nets or have
reverted to cyanide after the net training programme102.
Although considerable demand for ‘green’ marine
products exists in overseas specialty markets, and
possibly even locally, the markets have failed to convey
this to producers in an explicit way.
Consequently, an ever-increasing percentage of
fishes are caught in Australia, Hawaii, Florida, the Greater
Caribbean6, 102 and the Pacific Islands such as Fiji, where
collectors are often the exporters (90 per cent in
Australia40) and are known to use more sustainable capture
techniques, such as nets. As a result, survivorship post-
capture is higher and mortality for the target species
following shipping and handling often negligible.
There is hope that the use of cyanide can be
curtailed. However, in order to accomplish this a number of
major steps are required. The first, and probably the most
difficult one, requires governments of source countries to
face up to this problem by reforming their policies and
strengthening their institutions (e.g. mount public
awareness campaigns in the media and schools; regulate
the importation, distribution and use of cyanide). Secondly,
governments of importing countries must take steps to
reinforce measures adopted by the source countries (e.g.
monitor imports of live fish and provide data to exporting
countries; raise awareness of the impacts of cyanide
fishing)102. A reduction in the number of middlemen often
involved would help ensure that a greater percentage of the
price paid by exporters for ornamental fish goes to
collectors. Consumers also have an important role to play:
if sufficient numbers of informed consumers demand fish
that have been caught using sustainable techniques it is
likely that this will have important positive repercussions
on fishing methods in Southeast Asia.
IMPACTS ON POPULATIONS
Most traders argue that the collection of marine
ornamentals for the aquarium trade has no negative
impact on reef fish populations. This is likely to be true for
fisheries that are fairly small in comparison to the
available resource base (fish population). A study in the
Cook Islands showed that the total catch per unit effort
remained constant between 1990 and 1994114, an indicator
that fish populations on these islands were probably being
harvested sustainably. In Australia, through the use of
permits, the aquarium trade fishery is such that current
levels of exploitation are sustainable41. However, Australia
is an unusual case, as the Great Barrier Reef is the
largest reef system in the world. The available habitat and
the interconnectivity of fish populations provide resilience
to adverse effects from a comparatively small marine
ornamental fishery41. Nevertheless, no matter how large
a fishery is, not all fish are equally available or equally
attractive to the industry and the most common fish are
not necessarily those most favoured by hobbyists.
Consequently, the effects of collecting for the aquarium
fish trade should be measured with respect to their
potential to deplete particular species or locations rather
than viewed in terms of their global impact41.
Several countries in Asia and South America, for
example, have begun to implement collection restrictions
of certain ornamental fish species due to fears of
reduction beyond recovery of population numbers115 and
possible restructuring of reef communities due to
sustained collection pressures on favoured species18, 47.
Although no marine species collected for the aquarium
trade is known to have been driven to global extinction,
studies carried out in Sri Lanka116, Kenya116, the
Philippines117, 118, Indonesia119 and Hawaii120 and anecdotal
information from Australia41 all reported localized
depletion of a number of target aquarium species of fish
(e.g. butterflyfish, angelfish), due to heavy collecting
pressure. However, there is a need for improved infor-
mation on fishing effort121, catch and location, as well as
more research on the effects of collection of fish for the
aquarium trade. To date, most evaluations of direct
impacts of the aquarium trade on reef fish (coral and
invertebrates) populations come from visual censuses of
fish densities, calculations of potential yield from
35
Conservation issues
A typical collector’s boat, called
bancas
, in the Philippines.
modelling, estimated exports from custom records, or
observations by experienced biologists and commercial
fishers, often without quantitative validation37. The most
thorough attempt at quantifying the impact of coral
harvesting on species distribution and abundance was
carried out in the Philippines. Results of the study, which
compared coral community parameters at two sites, one
where no collection occurred, the other heavily harvested,
showed that coral collection had resulted in a reduction of
coral cover (31 per cent) and coral density (64 per cent)122.
Six commonly collected corals experienced declines in
abundance, by more than 70 per cent122. Although coral
exports have since been banned from the Philippines, it is
possible that similar impacts would be observed at
heavily exploited sites in Indonesia. No comparable study
to date has been carried out for Indonesia.
The only systematic study assessing the effects of
harvesting fish for the aquarium trade on resource
populations was carried out in Hawaii120, 123. The study
reported that eight of the ten species most targeted by
collectors showed declines in abundance at harvesting
sites relative to control sites (i.e. where no collection of
organisms was taking place). The magnitude of the overall
decline was highest for Achilles tang (
Acanthurus achilles
)
(57 per cent) and lowest for pebbled butterflyfish
(
Chaetodon multicinctus
) (38 per cent). However, temporal
effects such as yearly fluctuations in recruitmentxv of
common species (e.g. yellow tang (
Zebrasoma flavescens
))
36
From ocean to aquarium
Cleaner fish,
Labroides dimidiatus
Cleaner fish and shrimp have stimulated discussion
regarding the impact of marine ornamental fisheries on
ecological processes. The two main groups of cleaner fish,
which remove parasites and other material such as mucus
and dead tissue125 from other reef organisms, are gobies
and wrasses, but juvenile species of angelfish have also
been observed feeding this way6. Many of these species are
popular marine ornamental species (e.g. the French
angelfish
Pomacanthus paru
, grey angelfish
Pomacanthus
arcuatus
) with reports of the bluestreak cleaner wrasse,
Labroides dimidiatus
, being traded in large numbers – at
least 20,000 a year from Sri Lanka44. GMAD importers’ data
(exporters’ data from 1996-2003 in parenthesis where
applicable) for the years 1988-2002 showed 33 individuals
(173) exported from Fiji, 7,258 (23,597) from Indonesia, 62
from Kenya, 3,164 (3,707) from the Maldives, 30 from the
Netherlands (re-export), 831 (23,159) from the Philippines,
97 from Singapore (re-export), 5,347 (11,100) from Sri
Lanka and 132,092 from an unknown origin. Exporters’
records also showed 43 individuals exported from the
Marshall Islands, 51 from Palau, 78 from Saudi Arabia and
412 from the Solomon Islands.
Labroides dimidiatus
tend to be more abundant at
sites with greater numbers of sedentary fish, fewer
predators, fewer fish aggregating in large schools and
where the species richness of the fish community is
higher125. Due to their role in maintaining the health and
diversity of their ‘clients’, concerns have been raised
about the impact on population levels of the species and
reef health in general of removing large quantities of
Labroides dimidiatus
for the aquarium trade57. Most
experimental removals of cleaner fish have failed to show
significant effects126-128, although parasite load was
shown to increase four-fold on selected clients within 12
hours of being deprived of access to cleaner fish129.
A recent study which analysed the causal link
between cleaner fish presence/absence and reef fish
diversity at Ras Mohammed, Egypt, demonstrated that
Labroides dimidiatus
has a significant effect on local reef
fish diversity with a more rapid increase in diversity being
recorded when cleaner fish are added to individual reef
patches130. Indeed, the removal of
Labroides dimidiatus
had no effect on fish abundance within the first few weeks,
but a significant decline in fish diversity was recorded after
a 4-20 month time period. On the other hand, the
immigration or addition of
Labroides dimidiatus
indivi-
duals to reef patches led to an immediate, i.e. within 2-4
weeks, significant increase in fish diversity.
In addition to playing a key role in reef health – the
removal of
Labroides dimidiatus
in large quantities for
the aquarium trade is likely to have negative impacts on
reef diversity – this species tends to fare poorly in
aquarium conditions unless kept with a large community
of fishes, and is not likely to accept substitute foods, so
aquarists are advised to avoid it131.
might be substantial for the time frame of such a study and
thus results need to be evaluated with care. The study also
showed that, although the three most heavily collected
species were herbivorous (
Zebrasoma flavescens,
spotted
surgeonfish (
Ctenochaetus strigosus
)and
Acanthurus
achilles
), and suffered significant reductions in abundance
at collection sites, no increases in algae abundance were
recorded when compared with control sites120.
Life histories
While a huge diversity of species is demanded for the
aquarium trade, a large part of the trade tends to be
centred on individual species. These species’ vulnerability
to collection will depend on a number of life history
parameters, in particular growth, reproduction and
recruitment54.
Stony corals
Overall, there is very little information available on the life
history characteristics, growth rate or reproduction mode
of most coral genera in trade. Environmental conditions
influencing individual corals tend to be responsible for
great variations in life history characteristics. The same
species of coral sampled in two different locations may
display a different mode of reproduction and great
variation in growth rate. For example, coral specimens at
shallower depth tend to grow faster than specimens
found in deeper water135.
Corals show various sexual characteristics,
including two different types of sex, gonochoric (separate
male and female colonies) and hermaphroditic (single
individual is both male and female). In a hermaphroditic
coral (e.g. most corals in the genera
Acropora
and
Cynarina
), a single individual is capable of producing both
eggs and sperm. Examples of gonochoric corals include
Catalaphyllia
,
Euphyllia
,
Goniopora
and
Heliofungia
.
Corals also exhibit two distinct modes of reproduction:
brooding and spawning. In brooding corals, eggs are
fertilized inside the coral polyp and are released as fully
formed planula larvae that are ready to settle onto reef
substrate. Spawning corals, on the other hand, release
their gametes into the water column, where fertilization
and larval development takes place externally. Spawning
in hermaphroditic species is usually restricted to one
or a few nights each year, and occurs synchronously
throughout each population. Gonochoric spawners, on the
other hand, tend to have longer breeding periods and less
tightly synchronized spawning episodes136. Significant
reductions in population densities of corals due to
collection of colonies for the aquarium trade could have
implications on their reproductive success, and thus long-
term reef stability and health.
37
Conservation issues
Sea anemones
Of all 100 species of sea anemones occurring
throughout the world’s oceans, only ten are hosts to
anemonefish132. Anemonefish, on the other hand,
with the exception of
Dascyllus trimaculatus
,are
always associated with anemones and can only
be found in parts of the Indian Ocean, Red Sea
and Pacific Ocean (pictured are Barrier Reef
anenomefish,
Amphiprion akindynos
). Anemones and
their obligate symbiontsxvi are very popular with
marine aquarists due to their colourful displays, ease
of care and longevity in captivity. In the Florida Keys,
collectors with the appropriate licence may harvest
400 giant sea anemones (
Condylactis gigantean
) per
vessel per day. Estimates show that an annual
average of approximately 11.8 million anemones
were landed between 1997 and 1999, with more than
90 per cent of these collected in the Florida Keys133.
Data from collectors’ logbooks in the Olango region,
Philippines, revealed that fishers in the region landed
510 sea anemones (equivalent to 1.7 per cent of all
collected organisms) and 17,160 anemonefish
between January and April 2002134.
In an analysis of the marine ornamental fish
trade undertaken in the Maldives in 1992, the authors
voiced concern over the potential local overexploitation
of sea anemones and the possible negative impacts a
lack of suitable habitat (i.e. anemones) may have on
local clownfish populations90. Indeed, anemonefish
strictly depend on anemones, recruiting to them as
larvae and utilizing them as adults. Results of the only
study to date addressing the population-level impacts
of collecting marine ornamentals (in this case sea
anemones) show that close to 60 per cent of the catch
of collectors in the Philippines consisted of anemone-
fish and anemones, and that both these resources
exhibited significantly lower densities at exploited
sites134. Moreover, the low abundance of sea anemones
explained 80 per cent of the reduced density of
anemonefish recorded in collection areas134.
Stony corals are known to reproduce both sexually
and asexually. A variety of environmental factors are
known to regulate reproduction in corals. These include
sea temperature, day length, lunar phases, tidal cycles,
daily light/dark cycles, water quality, salinity and food
availability. Variations of these factors in aquaria have
allowed public aquaria and a few dedicated hobbyists to
witness sexual reproduction of corals in a closed system.
Sexual reproduction requires the fertilization of eggs by
sperm and results in small planula larvae, which disperse
into the plankton and may eventually settle on their reef
of origin or on distant reefs. Rates of recruitment (the
process whereby newly formed individuals become part
of the reef community137) differ greatly between coral
species, with species of
Acropora
and
Pocillopora
charac-
terized by high recruitment rates, and individual reefs
vary markedly in the number of coral recruits they
receive. Hence, replacement rates of harvested corals for
these two species tend to be relatively high. In contrast
other species, particularly in areas experiencing lower
recruitment rates, may have a lower capacity to recover
from collection pressures138.
Asexual reproduction is a common process for a
large number of coral species, particularly in branching
corals. Fragmentation, an important means of asexual
reproduction139, is the most common method used by
aquarium hobbyists for propagating corals. It is a
straightforward process that involves carefully breaking off
branches or pieces from the parent colony and placing
them elsewhere in the tank. Fragmentation can be applied
to most species of stony coral. The Waikiki aquarium, for
example, distributed 780 fragments in 199732. Fragments of
various species are frequently traded between individual
hobbyists, thus providing an alternative supply source
(although a minor one), at least for some species, to corals
harvested from the wild.
To date little more information is available at a
species-specific level than the general descriptive
reproduction biology described above. Acquiring more
information and detailed species- and country-specific
data on these basic aspects of coral biology, and how
collection for the aquarium trade may impact populations,
is important and necessary when attempting to derive
management strategies based on sustainable yields for
the aquarium trade.
Coral growth rate is another important factor to
take into consideration when developing a sustainable
coral harvest management plan. Although different
environmental conditions such as light, temperature and
depth can have a tremendous impact on variation in growth
rates, massive corals (with dense skeletons) are said to
exhibit average annual growth rates of 10-12 mm140 and
branching species (with more porous structures) 30-40
mm, with some
Acropora
species growing up to 100-200
mm per year141. Hence, fast-growing corals will tend to
suffer less from collection pressure whereas slow-growing
species will take longer to recover.
However, overall, it is important to put the
potential impacts of harvesting coral species for the
ornamental trade in perspective. Results from a study
looking at the amount of corals gathered from reef areas
for the production of lime show that in West Lombok 60
families produce an annual total of 900 tonnes of lime per
year142, necessitating the collection of approximately
1,600 tonnes of coral. Considering that in the mid-1990s
Indonesian exports never exceeded an annual total of
2,000 tonnes, it is clear that practices such as coral
mining for the production of lime rock have a much more
significant impact on the alteration of coral populations
and community structure than the collection of corals for
the ornamental trade.
Soft corals and sea fans
Similarly to stony corals, soft corals reproduce sexually
(spawning and brooding) and asexually. Most soft coral
and sea fan species are gonochoric; however some
species such as
Xenia
are hermaphroditic. Many
gonochoric species, such as the genus
Clavularia
, the
family Xeniidae and many gorgonians, are brooders.
Alcyoniid soft corals (e.g.
Cespitularia
,
Sinularia
,
Sarcophyton
,
Lobophytum
) are spawners, where mass
spawning is synchronized by lunar phase and/or water
temperature. Asexual propagation, for example through
38
From ocean to aquarium
Cauliflower/alabaster coral,
Pocillopora
spp.
fission, is very common in soft coral reproduction. Most
soft corals, both in the wild and in captivity, propagate
themselves this way.
Fish
Although coral reef fish exhibit a wide variety of mating
strategies, ranging from mass spawning events to
established nests and incubating eggs in a special pouch
on the abdomen, most fish larvae distribute widely
through wave and wind-driven ocean currentsxvii 143-145.
This makes replenishment of reefs with new fish larvae
highly dependent on these currents, and by extension the
number of fish available for sustainable aquarium
collection is highly variable.
Just as mating systems differ widely between
species, fish display unusual plasticity in their sexuality.
Some species are gonochoristic, with individual fish being
permanently male or female. However, for many species
sex is not fixed and is determined through social
interactions. In anemonefish, for example, the largest
individual is a female. New recruits start their life as
male. Should the female be removed from the colony, the
largest male changes sex and becomes the dominant
female41, 132. The effects of fishing are significantly
different for species that are hermaphroditic compared
with species that do not change sex. A fishery selectively
removing larger animals first will mean that animals will
have to start changing sex at smaller sizes, possibly
reducing the fitness of individuals, and thus making
hermaphroditic stocks more vulnerable to overfishing.
Greater fishing pressure, together with the biological and
ecological characteristics of some of these species, may
make them more vulnerable to exploitation than other
fish species41. Life history traits of fish are associated with
their vulnerability to exploitation146, 147, their rarity148 and
their risk of extinction149-151.
Trade in ornamental marine fishes tends to be
characterized by extreme selective harvesting. For all
species, with the possible exception of smaller species
such as gobies, blennies and dottybacks, juveniles are
preferentially targeted by aquarium fish collectors due to
their distinctive coloration, ease of maintenance and size-
ratio with respect to tank size37. A study carried out in
Hong Kong showed that 56 per cent of 12,652 fishes ready
for retail sale were juveniles24. Such preferences may
potentially reduce the risk of over-harvesting by leaving
39
Conservation issues
Anecdotal information has suggested that some
populations of the scribbled angelfish (
Chaetodontoplus
duboulayi
, pictured) may be depleted. Although this
information has not as yet been validated by scientific
surveys, local fishers in Queensland, Australia, have
observed significant fluctuations in population densities
over the years and thus have raised concerns. Population
estimates between the Keppel Island group and the
southern extent of the species in Hervey Bay, Australia,
show lower population numbers than in the past.
Scribbled angelfish are an important species in the
aquarium trade because they are ‘endemic’ to Australia and
Papua New Guinea, hence rare and therefore in high
demand. According to GMAD data 3,544 (total) of this
species were exported from Australiaxviii between 1988
and 2001.
Individuals of this species tend to be found relatively
close to shore, in soft reef and sponge reef habitats, in the
turbid waters that stretch from Hervey Bay north to Papua
New Guinea. In the Cairns region, anthropogenic influences
have severely impacted this habitat and may have indirectly
led to declines in scribbled angelfish populations. Although
fishing pressure is thought to be one of a number of
impacts to have affected numbers, biological and other
characteristics, such as annual recruitment patterns
dependent on seasonal temperature or rainfall, habitat
alteration due to trawling, and sedimentation and pollution
may have contributed to their decline.
Baseline information and general life history data are
needed on this species to help make more informed
decisions regarding its collection for the aquarium trade.
Establishing areas closed to the fishery of this species,
as well as limiting commercial effort in the fishery, have
been suggested as recommendations to prevent further
depletion of these fish stocks.
Source: QFMA41
The scribbled angelfish,
Chaetodontoplus duboulayi
Scribbled angelfish,
Chaetodontoplus duboulayi
: female (left)
and male (right).
breeding adults on the reefs. However, should juveniles
consistently be heavily harvested, adult populations will
suffer as only a limited number of young will grow to
reach adult size and replenish the adult stock.
Most coral reef fishes have broad distributions152.
Some species such as the Moorish idol,
Zanclus cornutus,
are distributed throughout most of the Pacific and Indian
Oceans. A small number of species, on the other hand,
are known only from restricted waters and/or are known
as endemics. In assessing the conservation value of these
endemic species, distribution and abundance must be
distinguished. Some species are naturally rare, occurring
only in very restricted locations, or naturally occur in
lower numbers, even though they may be widely
distributed6. Other species may be abundant at different
sites, but their distribution is limited to specific habitats41.
The more widespread and/or abundant a species is, the
less vulnerable it is to exploitation.
Increased rarity often implies higher prices6.
Individuals of two rare species, the yellow-faced
angelfish,
Pomacanthus xanthometapon
, and the blue-
girdled angelfish,
Pomacanthus navarchus
, fetch prices
in the range of hundreds of dollars in the United States37.
The peppermint angelfish
Centropyge boylei
may
command a price as high as US$10,00037. Officially
protected species may artificially drive prices up for the
few licensed to trade in them (e.g. seadragons,
Phycodurus eques
and
Phyllopteryx taeniolatus
)37.
However, high prices are not necessarily an indication
that a species is rare and therefore vulnerable to
overcollection6. The deep reef species, Tinker’s
butterflyfish,
Chaetodon tinkeri
, can sell for up to
US$1,000 per pair and has a restricted range, occurring
only in the Marshall, Johnston and Hawaiian Islands.
However, the high price is probably driven by the difficulty
in collecting the fish as it lives at depths of 27 to 135 m153.
Furthermore, due to the depth at which this species
occurs it is possible that it is more abundantly distributed
than at first appears.
Caution should be exercised when examining the
rarity of individual species. For example the raccoon
butterflyfish,
Chaetodon lunula
, the blackwedged
butterflyfish,
Chaetodon falcula
, the dwarf angelfish,
Centropyge multispinis
, and the regal angelfish,
Pygoplites diacanthus
, are rare off Sri Lanka, making
collection inadvisable, but abundant in the Maldives
where populations could maintain sustainable collection6.
Hence, in order to encourage protection and conservation
of these species in Sri Lanka’s waters, hobbyists should
try to purchase specimens originating from the Maldives
(and/or Mozambique in the case of the dwarf angelfish)6.
Information relating to
Pterapogon kauderni
and
Hippocampus
spp. will be presented and used as exam-
ples to demonstrate species vulnerability to collection for
the marine ornamental trade.
Pterapogon kauderni
The Banggai cardinalfish, originally described by
Koumans in 1933 and ‘rediscovered’ in 1991121, is a
popular fish amongst hobbyists and public aquarists due
to its attractive appearance and the ease with which most
individuals readily acclimatize to aquarium confines131. A
paternal mouth brooder (males incubate the female’s
eggs in their mouths until after hatching of the young), the
Banggai cardinalfish is a small (maximum 55 mm58)
species of fish that is relatively common, but whose
distribution is restricted to the shallow waters (reef and
seagrass habitat) of the Banggai Islands, an area of
approximately 10,000 km2off the east coast of central
Sulawesi, Indonesia. It usually lives in groups of 20 to 200
individuals that hover above long-spined sea urchins,
Diadema setosum
, or branched corals that the species
uses as a refuge if threatened154, 155. Juveniles are also
known to associate and take shelter in the fungiid coral
Heliofungia actiniformis
and anemones156, 157.
Biologists and conservationists have expressed
concern about the potential impact of collecting this
species for the aquarium trade155 due to:
❏the high and increasing fishing levels recorded over the
species’ entire distributional range156, e.g. 180,000 fish
per month being sold in the Banggai region75
❏its restricted habitat158
❏its low fecundity (lowest recorded fecundity rate of all
apogonids) and increased energy invested in parental
care
❏its low dispersal rate due to the lack of planktonic
dispersal of its eggs121
40
From ocean to aquarium
Banggai cardinalfish,
Pterapogon kauderni.
❏the fact that very little is known about existing
populations
❏the degraded and deteriorating state of its habitats,
mainly due to destructive fishing practices159, and
❏its popularity amongst hobbyists.
A recent study showed that, despite the use of non-
destructive fishing methods, the fishery had a negative
effect on fish density when sites with high fishing pressure
were compared to sites with low fishing levels155. Fishing
also had a significant effect on group size (halving of
average group size where sites with high and low fishing
pressure were compared), which may lead to strong nega-
tive impacts on individual fitness in the future (referred to
as the Allee effect in the scientific literature)155, 160, 161.
As a precautionary measure the species has been
informally proposed for listing on the IUCN Red List of
Threatened Species as ‘Critically Endangered’157. Should
such a listing be made official it would merely draw
attention to the threats facing this species without
imposing any trade restrictions.
Soon after the Banggai cardinalfish appeared in
the aquarium trade, a breeding programme was
developed at the New Jersey State Aquarium162. As this
fish can be reared through its entire life cycle in
captivity162, it is strongly recommended that efforts be
developed to raise this species in captivity and in the field
(preferably in Indonesia to avoid removing livelihoods
from local communities). This would reduce the need to
capture wild specimens to supply the trade. It is further
recommended that a trade monitoring system be
established through direct collaboration with aquarium
fish exporters. Targeting and inputting trade volumes of
the Banggai cardinalfish into GMAD could help spearhead
such a monitoring initiative and allow better estimates of
traded numbers to be derived. Improvements in the
sustainability of the current trade through directed
training programmes on holding, packing and shipping,
to reduce mortality rates of the species, are also
recommended75. The development of environmental
education material and programmes to promote public
awareness are strongly encouraged and the potential
41
Conservation issues
Extremely limited scientific information, particularly on its
biology and fishery, is available for the small, benthic dragonet
of the Western Pacific. All individuals traded for the aquarium
industry are taken from the wild and the impact of heavy
collection (21,458 individuals based on importers’ data or
11,168 individuals based on exporters’ data in GMAD, traded
within the EU only) on fish populations is unknown. It is subject
to a sex-selective fishery (up to 70 per cent of fish caught are
male) as larger males are most attractive to hobbyists. This
has the potential to disrupt exploited populations, both by
direct removals and through the indirect effects of removing
larger adult males in a mating system where females prefer to
spawn with large males.
In the Philippines, Batasan Island fishers heavily
targeted mandarinfish between 1987 and 1995. In 1998,
average size was recorded at 30 mm total length compared
with 60 mm in the 1980s, and reduced numbers were
recorded at capture sites. After the mid-1990s, prices fetched
by mandarinfish on the aquarium market dropped and the
fishery declined. Though species size has recovered
somewhat since 1995, abundances are still low – 1,000 fish in
three hours of fishing when fish were common, versus 23 fish
in two hours in 2001.
In addition to being vulnerable to collection in the wild,
this species is difficult to maintain in captivity as it needs to be
provided with large amounts of live prey and must be kept in a
well established aquarium with live substrate and plenty of
hiding places
131
.
It is recommended that continuous efforts be made to
rear this species in captivity to lessen sex-selective pressure
on wild populations. However, due to its aquarium
‘unsuitability’ (see below, p 43) overall imports of this species
should be closely monitored and restricted. Individual
specimens should only be considered for sale to experienced
aquarists.
Source: Sadovy
170
The mandarinfish,
Synchiropus splendidus
implementation of marine protected areas should be
investigated75.
Hippocampus spp.
Seahorses are distinctive, bony fishes, which belong to
the family Syngnathidae, a family that also includes
seadragons, pipefishes and pipehorses. All seahorses
are included in one genus,
Hippocampus
. There are
approximately 40 recognized species of seahorse, with
a few more likely to be described in the future163. New
species of seahorses recently described include
Hippocampus denise
61 and
H. queenslandicus
164.
Seahorses have a global distribution, with the
highest diversity occurring in the Indo-Pacific. They
typically inhabit marine or brackish water and occur at
depths of 1-15 m, among seagrasses, kelp beds, algal and
rocky reefs, mangrove prop roots and coral reefs, with a
few species preferring open sand or muddy bottoms165.
Very little is known about the basic life history parameters
of most seahorse species. For species where data are
available individuals mature between the age of six and
twelve months166. In all species of seahorses it is the male
who becomes pregnant and broods the developing
embryos for ten days to six weeks depending on species
and water temperature. Seahorses form faithful long-
term pair bonds and a male will mate exclusively with a
female partner. Once the young are born, they are fully
independent and receive no care from either parent.
Seahorses are particularly vulnerable to overcollection as
they have a limited reproductive rate (due to lengthy
brooding) and their social structure can easily be
disrupted (due to faithful pair bonding) further reducing
the reproductive rate166. To compound the problem their
habitat range is under threat from anthropogenic
activities, which are quickly destroying ecosystems of the
coastal zone. A number of reports167 have expressed
concern over overexploitation in the wild and consequent
declines in populations of seahorses.
All seahorses are listed as ‘Vulnerable’ or ‘Data
Deficient’ on the IUCN Red List of Threatened Species,
except for
H. capensis
, which is listed as ‘Endangered’. In
November 2002,
Hippocampus
spp. was listed in
Appendix II of CITES, to become effective on 15 May 2004,
meaning that permits will be required to import and
export species of this genus (32 species as recognized by
CITES Appendix II). Six species were listed on the basis
that harvest for trade exceeds sustainable levels that can
be continued in perpetuity, and the remaining 26 were
listed to bring trade in specimens of the other species
under effective control, as individual
Hippocampus
species can be extremely difficult to differentiate. The
European Regulation, which entered into force in 1997,
lists
Hippocampus
spp. on Annex D. Until their inclusion
in CITES Appendix II and thus corresponding up-listing to
Annex B on 15 May 2004168,
Hippocampus
spp. will remain
listed in Annex D.
In Australia, seahorses have been protected since 1
January 1998169 as their populations are considered to be
rare/and or threatened with overexploitation6. Export per-
mits will be granted only for specimens that have been
reared in approved captive breeding programmes, or taken
from the wild during an approved harvesting operation.
It is also important to remember that once caught
and placed in an aquarium seahorses are notoriously
difficult to keep, requiring a steady supply of varied live
foods. Moreover, they are highly vulnerable to a number of
fungal, parasitic and bacterial infections. Even public
aquaria, with access to vast resources and often highly
competent and trained staff, admit that these are among
the most difficult fishes to maintain in captivity.
Invertebrates
Giant clams, popular invertebrates in the aquarium trade,
occur in association with coral reefs throughout the
tropical Indo-Pacific region. These bivalve molluscs
obtain food in two ways: by filtering phytoplankton (small
algae) from the surrounding water and through
zooxanthellae embedded in their mantle that are able,
through photosynthesis, to produce nutrients, using
sunlight. Giant clams are susceptible to over-harvesting
due to the ease with which they can be collected (they are
sessile, live in shallow water to maximize use of sunlight
and can easily be spotted due to their colourful
appearance), their late sexual maturity (with size and age
at maturity varying with species and geographical
location), slow growth, sporadic reproduction patterns
and low natural recruitment rates. Insufficient life history
information exists to identify conservation issues for the
vast majority of more than 500 invertebrate species in
trade.
Sex-selective fisheries
Males of many coral reef fish species tend to be preferred
due to their distinctive coloration. Male mandarinfish,
Synchiropus splendidus
, for example, bear attractive dorsal
fins and displays170. Male wrasses, such as the bird wrasse
Gomphosus varius
, and the sapphire devil
Chrysiptera
cyanea
, are also often preferred to plain-looking females37.
Such brightly coloured specimens are also likely to fetch
higher prices on the market. Selectively harvesting for
males of particular populations on a regular basis may lead
to reproductive failure and ultimately population collapse
due to heavily biased sex ratios in remaining schools (i.e.
reduced male biomass)171, 172.
42
From ocean to aquarium
SPECIES SUITABILITY
Fishes
Michael131 gives each species of fish an aquarium
suitability index rating from 1 to 5 (see box) giving an
indication of that species’ durability, hardiness, and/or
adaptability to captive conditions and food. Factors such
as readiness to feed, dietary breadth, competitiveness,
tolerance of sudden changes and ability to withstand
less-than-ideal water conditions have been taken into
account when applying a rating. For example, a species
typically loses one rating point on this scale if live food
is required.
Two of the most traded fish species (see Tables 4-
6, pp 20-21), the mandarin fish and the bluestreak
cleaner wrasse, have an aquarium suitability ranking of
2, indicating that they do not acclimatize well to
aquarium conditions. Two others, the powder blue tang
(
Acanthurus leucosternon
) and the palette surgeonfish
(
Paracanthurus hepatus
), have an aquarium suitability
ranking of 3 indicating that they are relatively sensitive to
aquarium conditions. All other of the most frequently
43
Conservation issues
Table 13: Top ten species of ornamental fish
according to datasets derived for the United
States, the EU and worldwide, and their suitability
for aquaria according to criteria defined by Scott
Michael and John Brandt
Where labelled ‘na’, no suitability code is assigned for
this marine ornamental fish species according to Scott
Michael and/or John Brandt. See box and text for
explanation of codes.
Species Suitability Suitability
code code
(Michael) (Brandt)
Abudefduf
spp. na na
Acanthurus leucosternon
3na
Amphiprion ocellaris
4na
Amphiprion percula
4na
Chromis viridis
4na
Chrysiptera cyanea
5na
Chrysiptera hemicyanea
na na
Chrysiptera parasema
5na
Dascyllus albisella
na na
Dascyllus aruanus
5na
Dascyllus trimaculatus
5na
Labroides dimidiatus
2B
Nemateleotris magnifica
5na
Paracanthurus hepatus
3na
Pomacentrus australis
na na
Pseudanthias squamipinnis
4na
Salarias fasciatus
4na
Synchiropus splendidus
2B
Zebrasoma flavescens
4na
Male sea goldie,
Pseudanthias squamipinnis
. Female sea goldie,
Pseudanthias squamipinnis
.
MMiicchhaaeell’’ss aaqquuaarriiuumm ssuuiittaabbiilliittyy iinnddeexx113311
1. These species are almost impossible to keep and
should be left on the reef.
2. Most individuals of these species do not acclimatize
to the home aquarium, often refusing to feed, and
waste away in captivity.
3. These species are moderately hardy, with most
individuals acclimatizing to the home aquarium if
species care is provided.
4. These species are generally durable and hardy, with
most individuals acclimatizing to the home aquarium.
5. These species are very hardy with almost all
individuals readily acclimatizing to aquarium confines.
traded fish species have been allocated suitability ratings
of either 4 or 5. (See Table 13 on the previous page.)
John Brandt, an experienced aquarium hobbyist,
categorizes fish species according to two lists, which
are dynamic and continually open to revisitation and
revisionxii.
LLiisstt AA:: These species have the most disappointing record
of captive care. They are the truly unsuitable species,
dominated primarily by obligatory feeders such as coral-
eating butterflyfishes. In most cases aquarists regard
these species as impossible to maintain in captivity and
many feel that they should not be collected for the
aquarium trade. In general, relatively few of these
animals are collected, as demand is much lower than with
other species. There should be almost universal
agreement among aquarists that these species do belong
in this category, and not on List B.
An analysis including all species in GMAD and
listed with a suitability code of 1 according to Michael131 or
classed in list A by Brandt showed that the following
species were traded the most: the harlequin filefish
(
Oxymonacanthus longirostris
), Hawaiian cleaner wrasse
(
Labroides phthirophagus
), foureye butterflyfish
(
Chaetodon capistratus)
, harlequin snake-eel (
Myrichthys
colubrinus
), blueblotch butterflyfish (
Chaetodon
plebeius
), eastern triangular butterflyfish (
Chaetodon
baronessa
), melon butterflyfish (
Chaetodon trifasciatus
),
bluelashed butterflyfish (
Chaetodon bennetti
), nurse
shark (
Ginglymostoma cirratum
), eightband butterflyfish
(
Chaetodon octofasciatus
) (see Table 14). All these
species with the exception of
Ginglymostoma cirratum
are difficult to keep in captivity due to their restricted
diets. Nurse sharks are common in the aquarium trade
although, with a growth rate of approximately 19 cm a
year in captivity, they will almost certainly outgrow all
home aquaria131. Furthermore, they are highly predatory,
often eating other organisms kept in the same tank131.
Myrichthys colubrinus
is a very selective eater whilst the
remaining species are obligate corrallivores, meaning
44
From ocean to aquarium
Table 14: Species classified as most unsuitable for maintenance in aquaria by Scott Michael and John Brandt
Species’ names, quantity traded and most frequent country of origin according to exporters’ and importers’ data in GMAD.
Species Suitability code Common name Quantity traded Most frequent country of origin
(Brandt) (Michael) (exps’ data) (imps’ data) (exps’ data) (imps’ data)
Holacanthus arcuatus
* A na Black-banded angel – 131 – Unknown
Chaetodon austriacus
A1Blacktail butterflyfish 2 48 Sri Lanka Saudi Arabia
Chaetodon baronessa
A1Eastern triangular 450 1,318 Indonesia Indian Ocean
butterflyfish
Chaetodon bennetti
A1Bluelashed butterflyfish 603 811 Indonesia Indian Ocean
Chaetodon capistratus
na 1 Foureye butterflyfish – 5,280 – Caribbean
Chaetodon larvatus
A1Hooded butterflyfish 504 191 Saudi Arabia Yemen
Chaetodon lunulatus
A1Redfin butterflyfish 50 – Saudi Arabia –
Chaetodon melapterus
Ana Arabian butterflyfish 14 – Bahrain –
Chaetodon meyeri
A1Scrawled butterflyfish 421 123 Indonesia Indian Ocean
Chaetodon octofasciatus
A1Eightband butterflyfish 2,025 421 Solomon Islands Indian Ocean
Chaetodon ornatissimus
A1Ornate butterflyfish 648 149 Philippines Indonesia
Chaetodon plebeius
A1Blueblotch butterflyfish 233 1,712 Fiji Fiji
Chaetodon reticulatus
AnaMailed butterflyfish 232 45 Philippines Indian Ocean
Chaetodon speculum
A1Mirror butterflyfish 939 236 Philippines Indian Ocean
Chaetodon triangulum
AnaTriangle butterflyfish 85 130 Indonesia Indonesia
Chaetodon trifasciatus
AnaMelon butterflyfish 863 874 Sri Lanka Fiji
Ginglymostoma cirratum
na 1 Nurse shark – 632 – South America
Labroides phthirophagus
A1Hawaiian cleaner wrasse – 5,338 – USA
All
Labropsis
species A na Tubelips 94 33 Indonesia Indonesia
(about 6 species)
Myrichthys colubrinus
na 1 Harlequin snake-eel 294 2,532 Philippines Indian Ocean
Orectolobus maculatus
na 1 Spotted wobbegong – 23 – Unknown
Oxymonacanthus
A1Harlequin filefish 1,393 15,731 Philippines Fiji
longirostris
* Also known as
Apolemichthys arcuatus
or
Desmoholocanthus arcuatus
. See box p 43 and text for explanation of codes.
they feed exclusively on live coral polyps, a diet that
cannot be duplicated in normal aquarium conditions.
LLiisstt BB:: These species have a disappointing record of
captive care. Very few individuals acclimatize to captivity
or thrive over time. When individuals can be maintained,
the lifespan is usually reduced. Feeding and nutrition are
the primary cause of difficulties. Experienced aquarists or
those using special techniques may have limited success
with these species. Overall, much more research should
be conducted on these species to determine the best
methods for proper husbandry, or if any of these should
be included on List A.
In general, there is a reduced demand for these
animals and so fewer are collected compared with the
more hardy species. Some aquarists would argue that a
number of species on this list should not be included.
These aquarists feel that there are enough documented
cases of success to regard the species as being suitable.
List B includes (as too extensive for full inclusion in this
report): all seahorse and pipefish species, bicolour
angelfish C
entropyge bicolour
, keyhole angelfish
Centropyge tibicen,
scribbled angelfish
Chaetodontoplus
duboulayi,
bluespotted ribbontail ray
Taeniura lymma,
bluestreak cleaner wrasse
Labroides dimidiatus,
Moorish
idol
Zanclus cornutus
, all dragonets and all parrotfish
species.
Corals
Although no authoritative lists similar to the ones
produced for fish by John Brandt and Scott Michael are
available for corals, general aquarium suitability, toxicity
(i.e. how strongly one coral species is likely to react to
toxins from another) and sensitivity parameters are
available from
The Modern Coral Reef Aquarium
180.
Corals such as
Acropora elseyi
,
Cynarina lacrimalis
and
Lobophyllia hemprichii
rank highest in ease of
maintenance. Species of the genera
Heliopora
and
Goniopora
, on the other hand, do not survive well in
aquarium conditions.
Goniopora
is one of the most
45
Conservation issues
The harlequin filefish,
Oxymonacanthus longirostris
In 1998 an extensive bleaching event was observed in reef
areas worldwide. This event severely impacted the fringing
reefs of Bise, off the northwest coast of Okinawa, Japan,
with most of the living coral dying and filamentous algae
quickly covering the dead corals. Of all species, acroporid
corals seemed the most susceptible to bleaching174, 175.
Among coral-reef fishes, the species that are most likely
to be affected by coral disturbances are obligate coral-
dwelling or coral-feeding species, including butterflyfishes
(Chaetodontidae)176. In response to the bleaching event,
Chaetodon trifasciatus
and
Chaetodon trifascialis
showed
significant declines in abundance. The small (maximum 9
cm) harlequin filefish,
Oxymonacanthus longirostris
,
typically inhabits shallow coral reefs in the Indo-West Pacific
and spends most of the day feeding almost entirely on the
polyps of corals of the genus
Acropora
177. It lives in an
exclusive and heterosexual pair, with the male and female
sharing the same territory to feed.
Growth rates of adult
Oxymonacanthus longirostris
during coral bleaching were significantly lower, and tagged
harlequin filefish were found to disappear at rates
significantly higher than in previous years. In March 1999, no
juvenile, young or adult fish of this species were observed
at the site. This species is known to exhibit high site
fidelity178, and abundance of
Oxymonacanthus longirostris
on surrounding reefs where the bleaching event was less
severe was low, so the fish inhabiting this site seem to have
died as a result of bleaching. Considering this species’ diet,
the study clearly indicates that the occurrence of healthy
acroporid corals is essential to the survival of this species in
the wild. High collection rates of this fish for the aquarium
trade in addition to the higher frequency of natural disaster
events such as bleaching observed in recent years may
genuinely put at risk local populations and drive stocks
below their critical recovery level.
Source: Kokita and Nakazono179
abundant corals in trade, partly because these species
survive poorly in captivity and so must be regularly
replaced. Aquarists have reported that, in aquaria, these
species usually deteriorate and eventually die within a
period of three to six months. A regular feature of
aquarium specimens is unexplained stunted growth.
Corals are also easily damaged during collection and are
susceptible to disease74.
Heliofungia
is one of the oldest
species in the history of the coral trade181. Like
Goniopora
,
Heliofungia
has a poor survival record in aquarium
conditions as it is very sensitive, can easily be infected by
bacteria, and colonies can quickly die due to changing
ultraviolet (UV) light conditions181.
Overall, mortality rates of coral pieces in home
aquaria are fairly high, with one study concluding that
complete mortality occurs after 18 months182 and others
registering up to 76 per cent mortality in hard corals kept
in aquaria for more than 18 months183.
Plerogyra
spp. and
Catalaphyllia
spp. registered lowest mortality rates, 54
per cent and 60 per cent respectively, whilst
Heliofungia
spp. (100 per cent),
Goniopora
spp. (95 per cent) and
Tubastrea
spp. (100 per cent) registered the highest
mortalities183. Nonetheless, species in these genera are
commonly traded. (See Tables 7 and 8, pp 23-24.)
Recent advances in the maintenance of corals
in aquaria, through improved and more affordable
technologies, may lead to an increase in coral longevity in
aquaria. Further improvements in coral husbandry
techniques and the wider dissemination of information on
how to keep and maintain coral species (especially as more
information is available over the internet) should also
minimize coral mortality.
Soft corals and sea fans
Most of the common traded species of soft corals such
as
Cladiella, Clavularia, Cespitularia, Lobophytum,
Nephthea, Sarcophyton, Sinularia
and
Xenia
possess
zooxanthellae. They generally do not require plankton or
special foods and thus are fairly easy to keep in aquaria.
Described as hardy species, they are able to survive
stress during collecting and shipping and to heal wounds
as well as regenerate tissue relatively fast. Once
established they tend to grow quickly and are regularly
observed to propagate asexually. Cutting off their
branches may even be necessary to prevent overgrowth in
aquarium conditions. Their suitability as aquarium
specimens may be related to the fact that they are more
tolerant to fluctuations in water quality (although many
soft coral species will not tolerate salinity levels of less
than 30‰181) than other species of corals64. Notable
exceptions to this are the more sensitive species
Anthelia
spp.,
Cespitularia
spp. and
Xenia
spp., which do not fare
well after fragmentation, are vulnerable to transport and
sudden changes in aquarium conditions181, 184. Never-
theless, they grow fast once established.
Unfortunately, most of the more colourful and
beautiful soft corals do not contain zooxanthellae (i.e. they
are non-photosynthetic). Azooxanthellate soft corals, for
example
Dendronephthya
spp. (one of the ten most traded
soft corals, see box p 25) and
Studeriotes
spp., cannot
easily be propagated and are extremely difficult
to maintain in aquaria as they are entirely dependent
on filtering particles and absorbing dissolved nutrients
from the water column64, 181, 184. Due to these dietary
requirements, these species usually die within a few weeks
under aquarium conditions. Scientists and experts in the
aquarium industry strongly recommend that people do not
collect or keep azooxanthellate soft corals in captivity,
unless they are the subject of scientific research185.
Azooxanthellate sea fans such as
Ctenocella
spp.,
Echinogorgia
spp.,
Ellisella
spp.,
Euplexaura
spp. and
Lophogorgia
spp. are just as difficult to maintain. They
attract aquarists’ interest due to their bright red or yellow
colour, but show poor survival rates in captivity. On the
other hand, zooxanthellate species such as
Gorgonia
spp.,
Pseudopterogorgia
spp. and
Rumphella
spp., often
brown to yellowish brown, are fast growing, their
maintenance in aquaria is fairly straightforward and they
can be easily fragmented for propagation purposes.
POST-HARVESTING MORTALITY
There are many factors that lead to post-harvesting
mortality, such as physical damage and use of chemicals
during collection, poor handling practice and disease.
Even when collected in an environmentally sound manner,
aquarium organisms often suffer from poor handling and
transport practices resulting in stress and poor health of
marine individuals30. Accurate figures of post-harvesting
mortality are not available due to the sensitivity of such
46
From ocean to aquarium
A branching coral ready for export.
information. However, research on the marine ornamental
trade between Sri Lanka and the United Kingdom
demonstrates that in the mid-1980s about 15 per cent of
fish died during and immediately after collection, another
10 per cent died during transit and a further 5 per cent in
holding facilities20. Similar levels of mortality of 10-20 per
cent were found in a study examining the Puerto Rican
trade186. As a result of such mortality, more fish often need
to be collected than would be necessary to harvest in order
to meet market demand32. Where organisms are collected,
stored and handled by adequately trained individuals, and
transported in suitable conditions, estimated levels of fish
mortality have been as low as a few per cent.
Although post-harvest mortality levels are generally lower
for corals than they are for fish, more live rock and coral
fragments are often collected than would be needed to
satisfy trade demand as originally harvested pieces
are often considered of inadequate size, shape or colour
and discarded.
State-of-the-art equipment may help reduce
losses, but it is also expensive and thus beyond the budget
of many wholesalers in source countries. Fortunately, this
trend is reversing with an increasing number of facilities
in source nations investing in high-tech equipment,
particularly UV lighting systems and protein skimmers.
INVASIVE SPECIES
The introduction of aquarium fish species to areas where
they do not occur naturally is a problem more acute for
freshwater species than for marine species. Reports have
indicated that a number of individuals of the species
Pterois volitans
, lionfish (marine fish native to the Indo-
Pacific region), have been observed on four wrecks and
one natural hard bottom off the coast of North Carolina at
depth ranges between 40 and 45 m during 2000 and
2001187. Some individuals were also observed off the
Atlantic coast of Georgia during 2001187. Previous reports
include six lionfish accidentally released in Biscayne Bay,
Florida, from a home aquarium during Hurricane Andrew
(1992) and diver reports of lionfish off Palm Beach and
Boca Raton, Florida, in the early 1990s187. The US
Geological Survey (USGS) invasive species database lists
fish species (http://nas.er.usgs.gov/fishes/index.html)
that have been introduced into US waters through
intentional and accidental stocking, release of bait fish,
release of unwanted aquarium fish, escape from aqua-
culture facilities and discharge of ballast water188.
Examples of species introduced through the potential
release of unwanted aquarium fish include Moorish idol
(
Zanclus cornutus
)
,
sailfin tang (
Zebrasoma desjardinii
),
yellow tang (
Zebrasoma flavescens
), bursa triggerfish
(
Rhinecanthus verrucosus
), racoon butterflyfish
(
Chaetodon lunula
), orbiculate batfish (
Platax orbicu-
laris
), imperator angelfish (
Pomacanthus imperator
) in
Florida and lemonpeel angelfish (
Centropyge flavissimus
)
in Kaneohe Bay, Hawaii.
USER CONFLICT
One of the most vocal complaints against the aquarium
trade has been that it reduces fish populations in areas
where tourism is thriving and constitutes an important
source of revenue. This has been an issue of particular
concern in Australia and Hawaii30 and more recently in
Fiji35. In popular Australian tourist areas such as Cairns,
Moreton Bay and Whitsunday tourists and recreational
divers often interact with fish and coral collectors41. After
a study was carried out in Hawaii showing a significant
reduction in several species of fish due to collection
for the marine aquarium trade, fishing of marine
ornamentals was banned along 30 per cent of the west
coast of the island of Hawaii123.
In some Pacific Islands local fishers have also
expressed concern at the aquarium fishery being
unwanted competition for food fish33.
47
Conservation issues
Yellow tang,
Zebrasoma flavescens
.Bagging specimens for the ornamental trade.
48
From ocean to aquarium
M
Marine ornamental fisheries need to be managed
in such a way that they are biologically
sustainable, do not conflict with other resource
uses and keep post-harvest mortalities to a minimum.
Biologically sustainable means that harvested species
need to be replenished in their natural habitat at the
same or a greater rate than they are collected6. At the
same time, it is important to ensure that habitat damage
as well as impacts to other species are minimized.
Fisheries must also check that species unsuited to life in
aquaria are not collected. From a socio-economic point of
view, trade needs to be equitable and resource conflicts
between users (especially with members of the tourism
industry) need to be minimized.
The establishment of marine reserves where the
collection of marine ornamentals is made illegal may help
reduce this conflict, whilst at the same time removing a
section of the fish population from exploitation and
boosting recruitment to adjacent areas. Other measures
that can be taken to control collection pressure on marine
resources whilst conserving stocks of ornamental species
to ensure future sustainable harvests include the setting
of quotas and size limits, and restricting access to the
ornamental fishery through, for example, the use of
permits.
Governments and the industry itself play an
important role in supporting conservation initiatives and
promoting best practice. However, the consumer can also
encourage and promote change in the trade. Third-party
certification of the trade, whereby the consumer is em-
powered to assist in the reduction of the environmental
impacts of the trade by selectively purchasing products
produced in an environmentally friendly manner, has been
recommended by many as a possibility for improved
management and monitoring of the trade.
In conjunction with efforts at local and govern-
mental levels to develop management plans guaranteeing
the sustainable collection of marine ornamentals from
the wild, pressure can be taken off wild populations by
supplying the trade with tank-bred rather than wild-
caught specimens.
MARINE AQUARIUM COUNCIL AND CERTIFICATION
MACxix, on behalf of hobbyists, the industry and various
environmental groups, is developing a certification
scheme that will track an animal from collector to
hobbyist. Established in 1996, the goals of MAC are to
develop standards for quality products and sustainable
practices and a system to certify compliance with these
standards, and to create consumer demand for certified
products. With a network of 2,600 stakeholders in more
than 60 countries, it is recognized as the lead organization
for developing and coordinating efforts to ensure that the
international trade in ornamental marine organisms is
sustainable. MAC certification covers both practices
(industry operators, facilities and collection areas) and
products (aquarium organisms), and is often lauded as
the most effective means to ensure market demand and
support for quality products and sustainable practices in
the industry30.
Industry operators at any link in the chain of
custody (collectors, wholesalers, exporters, importers,
retailers) can be certified through an evaluation for
compliance with the appropriate MAC standard for the
Certification of Practices. For the Certification of Products,
MAC-certified marine ornamentals must be harvested
from a certified collection area and pass from one certified
operation to another, for example, from collector to
exporter to importer to retailer. MAC-certified marine
organisms bear the ‘MAC-certified’ label on the tanks and
boxes in which they are kept and shipped. To ensure that
MAC certification is credible and internationally acceptable,
MAC does not verify compliance with its own standards. It
accredits independent third-party certification companies
(Accredited Certifiers), which in turn assess compliance
with the appropriate MAC standard.
The MAC Core Standards outline the requirements
for third-party certification of quality and sustainability in
Conservation
efforts
A healthy reef off Nusa Penida, Indonesia.
49
Conservation efforts
the marine aquarium industry from reef to retail. There
are three MAC Core Standards covering the ‘reef to retail’
supply chain.
❏The Ecosystem and Fishery Management (EFM) Core
Standard: addresses
in-situ
habitat, stock and species
management and conservation by verifying that the
collection area is managed according to principles that
ensure ecosystem health and the sustainable use of
the marine aquarium fishery.
❏The Collection, Fishing and Holding (CFH) Core
Standard: addresses harvesting of fish, coral, live rock
and other coral reef organisms, handling prior to
export, holding, plus packaging and transport, to
ensure the health of the collection area, sustainable
use of the marine aquarium fishery and optimal health
of the harvested organisms.
❏The Handling, Husbandry and Transport Core
Standard: addresses the handling of marine life forms
during export, import and retail to ensure their optimal
health, their segregation from uncertified organisms
and proper documentation to show that they pass only
from one MAC-certified industry operator to another.
The Core Standards are accompanied by Best Practice
Guidance documents that provide advice to industry
operators on how they might be able to comply with the
standards.
This programme is not without cost to
participating companies, which initially will have to pay
fees to an independent certification authority as well as to
MAC. In the future, MAC certification hopes to develop into
a largely self-financed system, based on superior
economic returns from certified marine ornamentals
through the industry’s as well as the consumer’s
willingness to pay a premium for marine organisms of
demonstrable quality30. A list of companies that are
seeking to be certified or already sell certified marine
organisms is available from: www.aquariumcouncil.org
Another important aspect of this certification
programme is the establishment of a monitoring system
within collection areas to ensure early detection of any
changes to fish populations resulting from collection for
the trade. ReefCheck, a non-profit community-based
coral reef education and monitoring organization,
developed this monitoring system, entitled the Marine
Aquarium Trade Coral Reef Monitoring Protocol
(MAQTRAC), in conjunction with MAC. MAQTRAC was
tested in the field in the Philippines, Indonesia, Fiji,
Hawaii and the Maldives from summer 2001 through
spring 2002.
MARICULTURE
One way to reduce the pressure on coral reef ecosystems
brought about by an increasing demand for marine
ornamentals is to improve and further develop the ability
to culture desirable organisms for trade190.
Corals
Mariculture can be an environmentally sound way to
increase the supply of hard and soft corals, and has
proved successful for a large number of species. In light
The SMART project
The South Pacific Forum Secretariat, together with the
Marine Aquarium Council, has started a programme to
implement marine ornamentals certification within
the South Pacific Region. It will focus primarily on the
islands of Fiji, the Cook Islands and the Solomon
Islands and will address the negative impacts the
ornamentals industry presently has or may have. It will
also introduce market-driven third-party certification
for established operators to ensure sustainable
development of the industry whilst maintaining reef
ecosystem health. The programme is to be imple-
mented using a two-step process whereby national
consultations and workshops will be conducted first
and profiles of local industry partners derived. Recent
funding from the EU towards the Sustainable
Management of Aquarium Reef Trade (SMART) Project
will help build on these efforts and extend the number
of countries targeted to also include Kiribati, Vanuatu,
Federated States of Micronesia, Marshall Islands,
Palau, Tonga and Samoa.
The two-year initiative seeks to alleviate poverty
in Pacific Small Island Developing States by involving
coastal communities in the MAC-certified marine
aquarium trade, thus enabling communities to engage
in economically viable enterprises whilst sustainably
managing their coral reef resources. Furthermore, it
will disseminate tools in ecosystem management
planning, sustainable collection of aquarium products
and market linkages to communities within the
added-value context of MAC certification. These
activities will implement the Barbados Programme of
Action for Small Island Developing States, which
highlights the need for international cooperation and
partnership in efforts made by Small Island Develop-
ing States to conserve, protect and restore their
ecosystems.
Source: Lovell45 and Scott189
50
From ocean to aquarium
of this, coral aquaculture is increasingly mentioned as a
priority solution for reducing the harvest pressures on
coral reefs190. An additional advantage is that cultured
coral is acknowledged as adapting better to aquarium
conditions than wild-caught coral191.
To date, based on CITES importers’ data (1997-
2001), 99 per cent of the total global trade in live corals
originates from ‘wild’ sources and only 0.3 per cent is
captive bred/ranched, with China (42 per cent), Indonesia
(25 per cent), Taiwan (10 per cent), the Marshall Islands
(5 per cent), the Solomon Islands (4 per cent), Nicaragua
(2 per cent), Tonga, the United States and Micronesia
accounting for 99 per cent of total non-wild exports.
The aquaculture of corals, both soft and stony,
refers to coral propagation by fragmenting a large colony
(mother colony) into smaller pieces, or pruning the tips
of larger colonies, and subsequently attaching the
fragments to a new substrate using superglue or sus-
pending them in water on a nylon line. These fragments
are then left to grow in holding tanks or placed back into
the sea until they have reached a marketable size. Most
branching corals, for example, can be easily propagated
from small trimmings clipped from a parent colony and
achieve, in about a year, a five- to ten-fold increase in
biomass. Soft coral fragments can grow to a marketable
size within four to twelve months184 and stony corals (e.g.
Acropora
spp.) within four to six months192. Pacific Farms,
a company based in Los Angeles, and with stations in Fiji
and Tonga, is one of the largest in the coral mariculture
business with a team capable of fragmenting and planting
1,500 new corals a day193.
More than 75 species of coral can be captive bred,
but only fast-growing corals appear to be economically
profitable74. Hence propagation in species of stony coral
is mainly targeted at the fast growing branching
species such as
Acropora
,
Pocillopora
,
Seriatopora
and
Stylophora
194. Unfortunately, most of the popular species
in trade such as
Blastomussa
,
Plerogyra
,
Trachyphyllia
and
Goniopora
are slow growing, have little presently
known about their life histories and characteristics and so
are difficult to propagate.
Soft corals such as
Clavularia
,
Sarcophyton
,
Lobophytum
,
Sinularia
,
Alcyonium
and
Cladiella
are
suitable for aquarium propagation, due to their ability to
heal wounds and regenerate tissue rapidly. The most
commonly used practice for soft coral propagation is to
simply remove, underwater, a piece of tissue from the
parent colony using sharp scissors or a scalpel. Freshly
cut specimens should be left exposed to fresh seawater
motion or dipped in fine sand, for one or two weeks. They
can subsequently be tied or glued to appropriate
substrate and harvested within four to twelve months.
Cladiella
spp. and other azooxanthellate species that are
sensitive to fragmentation are almost impossible to
propagate64, 184.
When setting up coral farms, besides investigating
which species are most suitable for propagation, the cost
effectiveness of such enterprises needs to be explored 195.
A study of the economic viability of a community-based
coral farm situated on an Indo-Pacific Island demon-
strated that even after ten years of operation the facility
would remain in debt190. The main reasons included high
start-up costs, high operating costs and fairly low returns
in comparison with wild-caught products. This may be
true of newly set-up farming operations. On the other
hand, should established exporters develop farming as a
side activity, costs would be greatly reduced, as they
would only have to bear the expense of the equipment in
the grow-out facilities and labour costs. With time it is
then expected that cultured corals would become the
main source of exports. Non-governmental organizations
are likely to play an important role in encouraging and
securing potential initial funding (with governments and
foreign aid as the most probable source) to kick-start
farming activities and provide local community members
with the required training.
An example of a successful coral mariculture
initiative comes from the Solomon Islands where a group
of 25 women have been growing about 12 different
species of hard corals and a few species of soft corals.
Small nubbings of live coral are attached to concrete
discs, placed in trays and left to grow in carefully chosen
sites for four to six months until the fragments have
Finger leather/cabbage coral,
Lobophytum
spp.
51
Conservation efforts
reached a marketable size. By providing the country’s
main exporting company with a regular supply of cultured
pieces this small group of women is earning a regular
income192.
Fish
In recent years there has been an increased focus on
supplying aquarium fishes through closed system
culturing. Although to date virtually all marine
ornamentals are wild caught (breeding and rearing
marine species only accounts for 1 to 2 per cent of the
trade at present) and efforts to develop captive cultivation
have been limited, there is increasing pressure to develop
reliable and sustainable hatchery procedures for the
captive breeding of many reef fish species.
Although not exhaustive, Table 15 lists some of
the main species for which breeding and farming has
been mastered, some of those for which production and
marketing are presenting difficulties, and some of those
which have not yet been bred and reared but for which
research projects have been developedxx.
Aquaculture can be an environmentally sound
way to increase the supply of such organisms, by helping
reduce pressure on wild fish populations and producing
juvenile and market-size fish of a wide variety of species
year round. Furthermore, rearing aquarium fish in closed
systems is likely to lead to the production of hardier
species, which fare better in captivity and survive
longer21, 47, 196. To date it has proved successful for a few
fish species197. It is hoped that much of the market
demand for the more popular ornamentals such as
clownfish, yellow tangs and angelfish may eventually be
satisfied by cultured fish, once culture technologies have
been established successfully198. However, in reality,
most marine ornamental aquaculture remains com-
paratively problematic, both from a technical and a socio-
economic point of view199. Attempts at closing life cycles,
i.e. spawning, rearing and mating, repeatedly in closed
systems have proved technically challenging for most
species (except for species within the Pomacentridae
family200, as for example
Amphiprion
spp.) and existing
mariculture projects have been developed on a relatively
small scale37. Blennies, gobies and members of the
Pomacentridae family are relatively easy to rear in
captivity as they attach or deposit their eggs on or in
various substrates and, for species such as the clownfish,
can be conditioned to spawn voluntarily by manipulation
of day length and water temperature201. Most other fish
Amblyeleotris randalli
1
Amblygobius phalaena
1
Amblygobius rainfordi
1
Amphiprion akallopisos
1
Amphiprion akindynos
1
Amphiprion allardi
1
Amphiprion biaculeatus
1
Amphiprion clarkii
1
Amphiprion ephippium
1
Amphiprion frenatus
1
Amphiprion melanopus
1
Amphiprion ocellaris
1
Amphiprion percula
1
Amphiprion perideraion
1
Amphiprion polymnus
1
Amphiprion rubrocinctus
1
Amphiprion sandaracinos
1
Cypho purpurascens
1
Dascyllus trimaculatus
1
Doryrhamphus excisus excisus
1
Elacatinus puncticulatus
1
Gobiodon citrinus
1
Gobiodon okinawae
1
Gobiosoma evelynae
1
Gobiosoma louisae
1
Gobiosoma multifasciatum
1
Gobiosoma oceanops
1
Gobiosoma randalli
1
Lythrypnus dalli
1
Hippocampus barbouri
1
Pseudochromis aldabraensis
1
Pseudochromis dutoiti
1
Pseudochromis flavivertex
1
Pseudochromis fridmani
1
Pseudochromis sankeyi
1
Pseudochromis splendens
1
Pseudochromis steenii
1
Pterapogon kauderni
1
Amphiprion bicinctus
2
Amphiprion chrysopterus
2
Amphiprion polymnus
2
Gobiosoma xanthiprora
2
Abidefduf abdomnialis
3
Anisotremus virginicus
3
Apogon
spp. 3
Bodianus rufus
3
Calloplesiops altivelis
3
Centropyge potteri
3
Chaetodon lunula
3
Chaetodon miliaris
3
Chromis cyanea
3
Chrysiptera parasema
*3
Dascyllus albisella
3
Dascyllus aruanus
3
Diodon
spp. 3
Equetus acuminatus
3
Equetus lanceolatus
3
Equetus punctatus
3
Forcipiger flavissimus
3
Gramma loreto
3
Hippocampus erectus
3
Hypoplectrus unicolor
3
Hypsypops rubicundus
3
Microspathodon chrysurus
3
Opistognathus aurifrons
3
Pomacanthus arcuatus
3
Pomacanthus paru
3
Synchiropus splendidus
3
Zebrasoma flavescens
3
Table 15: Main species bred for the marine aquarium trade
1 = commercially available; 2 = production and marketing difficult; 3 = subject of research
*Successfully reared very recently200.Source: Oliver39; Ogawa and Brown47; Oceans, Reefs and Aquariums236; Tropical Marine
Centre237; and data taken from GMAD.
52
From ocean to aquarium
species such as angelfishes and butterflyfishes are
known as broadcast spawners, i.e. they spread their eggs
freely in the water column, and are therefore more
difficult to culture in captivity; they also usually require
hormone treatment to induce spawning. To date, the
greatest obstacle to successful tank breeding of orna-
mental reef fish is rearing larvae beyond the sixth to
eighth day of development, a time typically associated
with failure to initiate larval feeding47. This is often due to
larval feeds being too large or not meeting the nutritional
requirements of fish larvae. Once the larvae transform
into small juveniles, they are weaned onto semi-natural
diets and various prepared rations and can be transported
and sold201. Beside technical challenges, the high price
commanded by some cultured aquarium fishes compared
to those wild caught often undermines their economic
viability37.
The increasing use of mariculture to supply coral,
other invertebrates and fish to the marine ornamental
trade raises its own suite of issues. Firstly, should rearing
facilities be established mainly in developed countries, as
the trend so far seems to indicatexxi. Relations between
the different players involved in the marine ornamental
trade may be altered, possibly depriving local fishers of
employment and losing the community- and national-
level benefits the trade provided203, 204. This would be
contrary to the first article of the Convention on Biological
Diversity ratified by 170 countries205 (but not the United
States), the objectives of which are: ‘the conservation
of biological diversity, the sustainable use of its com-
ponents and the fair and equitable sharing of the benefits
arising out of the utilization of genetic resources,
including by appropriate access to genetic resources and
by appropriate transfer of relevant technologies, taking
into account all rights over these resources and to
technologies, by appropriate funding.’ Development of
facilities in source countries has the potential to raise the
standards among rural communities and provide income
opportunities for a great number of households due to its
ability to generate considerable income per unit area,
with high export earnings5. Furthermore, setting up
hatcheries in source countries would also reduce the risk
associated with escapes and, by extension, the risk of
introducing exotic species.
A relatively recent type of mariculture whereby
fish larvae are captured via means of light traps206, 207 or
crest nets (shaped like funnels and placed on the reef
edges) has been raising much interest. Not only would
it provide local communities with the benefit of such
activities and/or provide them with an alternative
Captive breeding of seahorses
In light of expressed concerns of overexploitation of
seahorse populations, the possibilities for captive breed-
ing are of great interest and a number of captive breeding
projects have been set up around the world. The Seahorse
Trust202 reports that it has bred 18 species of seahorse
with varying levels of success; for example, it has bred six
generations of
Hippocampus capensis
with a 90 per cent
success rate, compared to only two
H. comes
(pictured)
out of many broods. In addition, the Tropical Marine Centre
in the United Kingdom has captive breeding facilities and
breeds seahorses, e.g.
H. barbouri
. However, it is only if
aquaculture is developed as an alternative livelihood for
fishers in source countries that it can be highlighted as
having great potential for integrating conservation and
sustainable development objectives167. Results of a recent
protocol developed for culturing
H. kuda
, one of the most
heavily exploited species for the aquarium trade, in the
source countries are encouraging. They indicate that
H.
kuda
grows rapidly from birth to 14 weeks and showed
highest survival rates when fed
Artemia
(brine shrimp, a
commonly available feed for aquarium fish) enriched with
a locally available crustacean,
Acetes
spp.167.
53
Conservation efforts
Cleaner shrimps
In GMAD eight species under the genus
Lysmata
and
four species under the genus
Stenopus
were identified as
being traded as marine ornamentals:
L. debelius
(fire/blood/scarlet cleaner shrimp),
L. grabhami
(Atlantic
white-striped cleaner shrimp),
L. amboinensis
(Indo-
Pacific white-striped cleaner shrimp),
L. wurdemanni
(peppermint shrimp),
L. intermedia
,
L. multicissa
,
L.
rathbunae
(peppermint shrimp),
L. californica
(pepper-
mint/red rock shrimp),
S. cyanoscelis
(golden banded
shrimp),
S. hispidus
(yellow-banded coral shrimp),
S.
tenuirostris
(blue-banded coral shrimp) and
S.
zanzibaricus
(gold-banded coral shrimp). They are hardy
species and their maintenance as adults in aquaria is fairly
straightforward, although they are sensitive to sudden
changes in aquarium conditions. These species feed
mainly on parasites and diseased skin, hence their
common name ‘cleaner shrimp’, as well as any missed
food items, a beneficial function to aquaria as it relieves
pressure on filtration systems212. Although suited to
maintenance in aquarium captivity and of benefit to the
health of fish maintained in a tank, their removal from
coral reefs may lead to a reduction in reef diversity
because of their natural ecosystem role of removing
parasites from reef fishes and animals. However, in recent
years efforts have been made to develop aquaculture
protocols for marine ornamental shrimps, especially
species of
Lysmata
(cleaner shrimp) and
Stenopus
(banded coral shrimp) to reduce wild specimen
collection213. Many companies have commercially raised
the peppermint shrimp
L. wurdemanni
, and rearing
protocols for it and other related species, including
L.
debelius
, are available214-216. The largest bottleneck for
commercial production is their relatively long and variable
larval durations217. Thus, most research efforts have
focused on identifying appropriate broodstock and larval
diets to reduce larval durations and increase the
aquaculture potential for these species, which are among
the most popular invertebrates in the marine aquarium
trade217. Due to these constraints, the vast majority of
traded specimens are still being collected from the wild.
LeRoy Creswell, of the Harbor Branch Oceanographic
Institution, and Junda Lin, Florida Institute of Technology,
have set up a private company Oceans, Reefs, and Aquaria
Inc., which is commercially producing, and marketing,
peppermint shrimp as tank-reared ornamentals218. They
are also engaged in pilot production of the gold-banded
coral shrimp. In the United Kingdom, the primary producer
of captive raised invertebrates is the Tropical Marine
Centre, which is actively breeding
L. debelius, L. ambo-
inensis
and
L. californica
.
The main importers of ornamental shrimps should
work together with the main exporters to adopt sustain-
able procedures and develop the necessary technology for
rearing the most important species in trade. Developing
this expertise in developing countries with optimal climate
conditions and low production costs would allow for more
effective conservation programmes to be implemented
whilst generating a valuable source of revenue219.
A banded coral shrimp,
Stenopus hispidus.
Banded coral shrimps collected for the trade
.
54
From ocean to aquarium
livelihood but it might also relieve some of the fishing
pressure on coral reefs. The two groups pioneering this
technique are researcher Vincent Dufour (under a
programme called AquaFish Technology) and his team
based in the Pacific, and members of ICLARM–The World
Fish Center, based in the Solomon Islands and the British
Virgin Islands. Considering that the vast majority of fish
larvae die after having settled onto the reef (10 per cent
survival rate), removing them prior to the high mortality
rate fish populations suffer at recruitment would
guarantee minimal fishing impact208. Species farmed this
way and exported from French Polynesia to France
showed promising growth rates, were more gregarious,
accepted a wider variety of food and were less sensitive to
stress than wild-caught individuals of the same
species209. The research group based in the eastern
Caribbean region has also developed a floating mesh cage
system in which larvae can be grown out by providing
them with a constant supply of plankton-rich water210. The
plankton pump uses a single light at night and utilizes an
airlift pump during the day. With an average price of
US$0.5 per fish, by trading 50 individuals grown out using
this system, members of fishing communities in
Southeast Asia, for example, could be provided with a
livelihood211. On the downside this larval collection
technique depends on inputs of fish larvae, which are
typically unpredictable in space and time as well as in
species composition – not all larvae caught may be
suitable for rearing, or in demand for trade.
Invertebrates
Since technical constraints regarding the spawning of
mature giant clams and raising of larvae and juveniles were
overcome in the 1980s, interest in giant clam culture and
population management has increased considerably84.
Giant clam mariculture has several advantages: the
animals require no artificial feeding, rearing techniques
are relatively simple and the setting up of facilities
requires little capital investment and can involve local
community members. Furthermore, unlike many other
forms of mariculture it does not require broodstock to be
continuously captured from the wild and hence the impact
on wild stocks is minimal.
James Cook University in Australia, the
Micronesian Mariculture Demonstration Centre (MMDC)
in Palau and the Coastal Aquaculture Centre (CAC) in the
Solomon Islands80 have developed pioneering research
activities on clam mariculture. In the 1980s, scientists
from Australia, the Philippines and a range of Pacific
Islands nations (e.g. Kiribati, Fiji, the Solomon Islands and
Palau) teamed up to further develop advanced giant clam
mariculture technologies220.
The initial interest in culturing giant clams came
from concerns related to the decline, and in some cases
extinction, of wild stocks throughout their range, due
partly to increasing pressure on coastal systems as a
result of settlement expansion, pollution and improved
harvesting efficiency. Hatcheries were initially developed
to reseed depleted reefs and with the aim of growing
clams as a food source to relieve pressure on wild
populations81, provide employment and earn foreign
exchange80. Nowadays, giant clams are also reared
specifically for sale as aquarium species with government
and commercial hatcheries in most tropical Pacific
nations and island groups where giant clams are known
to occur. These hatcheries are having commercial suc-
cess because the giant clams can be sold at smaller sizes
and thus the loss rate experienced due to predation on
cultured stocks is reduced80. In fact giant clam farms
developed for subsistence purposes showed poor
economic viability82. Any conservation efforts for
invertebrates other than clams and cleaner shrimps
would be constrained by the near uniform lack of infor-
mation on key life history characteristics.
MANAGEMENT INITIATIVES FOR THE TRADE
Marine ornamental fisheries, if managed sustainably and
integrated with other resource uses, have the potential to
provide many people in source countries with a stable
source of income and thus a livelihood. Countries like the
Solomon Islands and Vanuatu have no specific manage-
ment plans for the ornamental marine industry221. On the
other hand countries such as Fiji, Palau and Australia
have policies regulating collection of reef organisms6.
Unfortunately, these often exist only on paper, are not
enforced and were rarely implemented on the basis of
rigorous scientific baseline studies or monitoring
activities and so in most cases might not be effective at
actually conserving populations.
When addressing issues relating to the
management of ornamental fisheries, it is important to
involve all parties concerned. This includes collectors,
wholesalers, governments, hobbyists, scientists and
members of industries who might have a resource conflict
with aquarium collectors (e.g. the tourist industry)6. One
of the most promising and effective strategies is to allow
local communities to manage and control their fisheries.
A number of islands in the Pacific Ocean, where local
village communities have legal rights to particular reef
areas, are successful examples of such a system222.
Overall it is also important to highlight the need
for further research on the biology, population dynamics,
recruitment and conservation importance of species
involved in the marine ornamental trade, with a particular
55
Conservation efforts
focus on rare or endemic species and species that show
poor survival in aquarium conditions. A survey of the
distribution and abundance of target species, including an
assessment of the exploitable area, is also crucial when
attempting to set quotas or develop a management plan
for resources harvested for the aquarium trade.
In a similar manner as for many conventional
commercial food fisheries, measures such as limiting
access to the fishery, establishing reserves and setting
quotas have been suggested as direct ways for controlling
aquarium fisheries and ensuring their sustainable
development. In all of these instances, scientific data
such as the biology, population dynamics and recruitment
patterns of traded species need to be collected. However,
to date, such scientific information has been lacking.
Catch data to species level is also important when
attempting to assess the effects of collection, developing
management strategies and assessing their efficacy.
Limited access to the fishery
A licensing system, such as the one operating in
Australia, the Cook Islands, Palau and a number of other
Pacific Island countries, whereby collection effort is
regulated through a limited number of permits being
issued each year, offers a good way of monitoring the
industry6. In addition, Australia has introduced restric-
tions on net size to ensure a limited number of permits
is not offset by greater fishing effort6. The number of
permits to be issued should be based on scientific studies
estimating the resource base and sustainable harvest
quotas, be non-transferable, subject to review on a
regular basis and clearly state the conditions under which
fishing is authorized. The licensing system in Florida,
where collectors operate under state legislation, and in
Fiji, where conditions attached to operators’ licences are
severe, stands in contrast to schemes in place in
countries such as Indonesia where permits are issued but
enforcement and control is difficult6.
Quotas
Limiting the number of fish being exported from any
source country is another way of reducing or limiting
collecting pressure. Quotas are only likely to be effective if
based on rigorous scientific research and implemented at
a species-specific level6. Although relatively simple and
easily enforced, general quotas are not advisable as they
may simply encourage collectors to focus collection on the
most valuable species, hence not ensuring protection of
stocks overall and least so of vulnerable species6.
Species-specific quotas such as those stipulated for
butterflyfishes, angelfishes and giant Caribbean ane-
mones under the Florida Administrative Code43 ensure
that collection activities are maintained at sustainable
levels and that a healthy population remains on the reef.
Unfortunately, the difficulties of a species-specific quota
system lie in identifying species to which such a system
should apply, which requires detailed knowledge of their
life histories, recruitment patterns, the aereal extent of
exploitation as well as species densities on the reef90. This
is compounded by the fact that such quotas need to be
developed on a country-by-country basis6.
Although there is no specific requirement within
the text of CITES to establish quotas to limit the trade in
listed species, the use of export quotas has become an
effective tool for the regulation of international trade.
Export quotas are usually set by each member state
individually, but they can also be set by the Conference of
the Parties, and they generally relate to a calendar year (1
January to 31 December). Before any Party can issue a
permit to allow export of specimens of species in Annex II,
the scientific authority of the state must advise that the
proposed export will not be detrimental to the survival of
the species (the so-called non-detriment finding). In order
to help make sure that export quotas are not exceeded,
export permits should indicate the number of specimens
already exported in the current year and the quota for the
species concerned223.
Indonesia has implemented a quota system for the
collection of stony corals based on available information
on rates of growth, recruitment, distribution and
abundance of coral species7. The management plan for
coral harvesting also includes a system of rotational
harvests including no-take zones. However, in practice,
quotas for coral species are based on very limited data,
making it difficult to determine whether there is any
basis for regarding these quotas as sustainable. As a
result of this, the EU expressed concern at the potential
Lined butterflyfish,
Chaetodon lineolatus.
56
From ocean to aquarium
unsustainability of current export volumes and its CITES
Scientific Review Group has temporarily banned the
import of a number of coral species into the EU until
Indonesia can demonstrate that collection according to
the set quotas is indeed not contributing to reef
degradation.
Size limits
Size limits are another useful tool in managing aquarium
fisheries. The marine ornamental fish trade tends to be
highly selective in favour of juveniles due to their dis-
tinctive coloration, low transport cost for exporters and
optimal size to fit in a home aquarium. However, the young
of some popular fish species are easily stressed and hence
may suffer high mortality during holding and transport6.
Setting minimum size limits such as those encouraged by
an Ocean Voice International–Haribon Foundation project
in the Philippines118 would help ensure that stock is not
unnecessarily wasted224. Maximum size limits are equally
important to ensure that sufficient numbers of breeding
adults remain on the reef. At the recent Nineteenth Meeting
of the Animals Committee (18-21 August 2003) the decision
of ‘a universal minimum permissible size of 10 cm (height)
[…] for all seahorses in international trade, […] to allow
animals to reproduce before being caught’ was adopted.
The State of Florida has an exemplary regulation
system stipulating minimum and maximum sizes for a
number of ornamental fish species. According to the
Florida Administrative Code butterflyfishes and several
species of angelfishes (grey, French, queen and rock
beauty), for example, are subject to both a minimum and a
maximum length restriction43. Maximum length limits are
also specified for gobies, jawfish and the Spanish hogfish43.
Maximum size restrictions for the collection of
coral pieces are important to ensure that mature colonies
are not removed from the reef. Such restrictions would
be particularly useful for species of coral which tend
to develop particularly large colonies. The Indonesian
authorities have stipulated maximum size limits of 15 cm
and 25 cm for slow-growing species such as
Plerogyra
and C
atalaphyllia
and fast-growing species such as
Acropora
respectively224. Removing primarily small
specimens is also likely to reduce damage to the reef
habitat structure.
A study of
Pocillopora verrucosa
in the Philippines
showed that maximum sustainable yield could be
calculated using information on distribution and
abundance as well as growth rate and rates of mortality
and recruitment225. The minimum size that should be
allowed at harvest was calculated to be 18 cm in height,
equivalent to six years old.
Marine reserves
A potential solution to the localized depletion and habitat
degradation that may result from extensive and
unmonitored collection of marine ornamentals is the
creation of marine reserves, areas where fishing is
prohibited or controlled. Marine reserves have often been
recommended, and suggested as useful tools in managing
marine fisheries (usually food fisheries), for they have
been shown to increase fish abundance226-230 and protect
ecosystems from habitat destruction due to fishing231, 232.
Hence, they could also, if set up and managed appro-
priately, prove to be a valuable tool for managing aquarium
fisheries6, 13, 20, 224. Australia, for example, has developed an
effective management strategy whereby coral reef
Grape/bubble coral,
Plerogyra
spp.Eritrean butterflyfish,
Chaetodon paucifasciatus
.
57
Conservation efforts
habitats have been divided into zones for different uses,
which include no-take areas74. Selected collection areas,
representing less than 1 per cent of the reefs in a region,
have been established for licensed collectors to harvest
coral for the aquarium trade74. Government statistics show
that despite collectors harvesting 45-50 tonnes of coral
per year for 20 years, no noticeable impact on the resource
has been observed74.
Reef fish assemblages and patterns of distribution
of fish are influenced by the associated reef habitat, which
provides food and shelter to a large number of organisms.
The greater the complexity of the reef structure the greater
the available fish biomass and the more diverse fish
assemblages will be233. Therefore, in order to be effective at
protecting the wide range of fish species of interest to the
marine aquarium trade, marine reserves need to include a
great diversity of habitats, i.e. have structural complexity18.
The limited home range size and high level of habitat
specificity associated with marine ornamental fish seem to
indicate that marine reserves should be effective tools at
managing ornamental fish populations.
Management decisions (e.g. location for reserves)
should involve participation by all stakeholders, with
appropriate consultation with scientists and fishers at
the local and national levels, so as to minimize conflict
and optimize benefits55, 234, 235. Marine reserves are likely
to be most successful at ensuring the sustainable use of
local resources as well as increasing awareness and
understanding of conservation and management issues if
implemented by the collectors and relevant members of
the community themselves, a process often referred to as
community-based management. By giving community
members a sense of ownership of their resources, they
will more likely guard these against destructive uses17, 30.
Traditional management under customary marine
tenure (CMT) presents a unique set of conditions for the
successful implementation of marine reserves. CMT plays a
key role in the overall social, economic and cultural aspects
of societies in the Pacific Islands222. In the Pacific basin,
although CMT comes under a range of different organiz-
ational concepts, and has in part been eroded because of
colonialism, the local community is often the exclusive
owner of marine resources, managing coastal fisheries and
habitats222. The essence of CMT structures is based on the
idea that the more responsibility is left to local communities
for the control of local resources, the less governments will
have to be implicated in legal, conservation and social
issues, and the greater the sense of responsibility members
will have towards the sustainable use and conservation of
marine resources and habitats. However, their effective-
ness is likely to be dependent on how such systems adapt to
changing socio-economic conditions.
Temporary closures
Temporary closures are often cited as an alternative to the
implementation of reserves. This approach is commonly
used to protect species during reproductive phases to
ensure there is sufficient recruitment to sustain the
population. Although not in operation specifically for the
aquarium trade at present, such closed seasons could
allow juvenile fish to grow to a size unsuitable for
aquarium collection thus making sure that a healthy stock
of adult fish is maintained on the reefs6. These adults in
turn would contribute recruits and help maintain healthy
population levels despite irregular and stochastic
recruitment events. It is important to note that temporary
closures are only likely to be effective if implemented at
the right time and at the right location224.
Holding tanks at a marine aquarium wholesaler.
58
From ocean to aquarium
G
Given the wide range of threats facing coral reefs,
with reefs in Southeast Asia – the most important
source of the majority of animals in the marine
ornamental trade – particularly at risk, it is becoming
increasingly important that harvesting of marine
organisms for the aquarium trade is appropriately
managed in order not to further compound these
problems. However, to date only a relatively small
number of countries have put in place comprehensive
regulations to control the collection of marine
ornamentals. The highly selective nature of these
fisheries increases their impact on populations of
targeted species. They may also, directly through the
use of destructive fishing practices or indirectly through
the removal of key species (e.g. cleaner fish/shrimp),
impact other species and ecological processes in the
habitats where fishing for the aquarium trade occurs.
Most of the restrictions that regulate the trade to
date have been put in place despite a lack of information
on the population status and life characteristics of the
targeted species. More accurate trade data, and much
more specific information on particular life history
characteristics such as recruitment and growth rates,
should be collected to establish quotas and maximum
sustainable yields, as well as to help in the development of
frameworks to manage the collection of reef organisms
for trade on a sustainable basis. Certification schemes
and associated operational standards for the industry
need to be further developed and more widely applied
to make certain that fish are collected, handled and
transported in a manner that minimizes stress to the
animals right through the process from ‘reef to retail’.
Raising awareness through the circulation of information
materials about these standards and the steps that
consumers can take to help ensure animals are being
collected in a way that is sustainable should also be
promoted. The purchasing power that hobbyists possess is
undoubtedly the single most important market force in the
marine aquarium industry. If sufficient numbers of
informed consumers demand fish that have been caught
using sustainable techniques it is likely that this will have
important positive repercussions on fishing methods
globally. In source countries, and particularly in Southeast
Asia, steps need to be taken to reform policies, strengthen
institutions (e.g. mount public awareness campaigns in
the media and schools) and develop pro-active training
programmes to encourage collectors to use non-
destructive methods.
Species that are unsuited to life in aquaria or
exhibit low population densities, restricted ranges, or life
history traits that make them particularly vulnerable to
collection, should receive special attention to reduce the
risks of overexploitation.
The designation of marine reserves, establish-
ment of quotas and size limits in addition to measures
to limit access to the fishery are examples of ways in
which population stocks of marine ornamentals could be
both conserved and managed so as to provide sustainable
livelihoods for low-income coastal populations. It is
important that management decisions, such as the
location of reserves, involve the participation of all
stakeholders, including appropriate consultation with
scientists and fishermen at the local and national levels.
In this way, conflicts can be minimized and benefits
optimized.
Finally, further research into mariculture
technologies is needed in order to take pressure off
wild stocks and increase the cost effectiveness of
facilities. Such projects should develop as an alternative
livelihood for fishing communities in source countries,
thereby integrating conservation and sustainable
development objectives.
Conclusions and
recommendations
On the journey from ‘reef to retail’.
59
From ocean to aquarium
Endnotes
i. The marine aquarium trade is composed of: saltwater fish,
corals (stony and soft) and invertebrates (e.g. shrimps, small
clams) that can be kept in an aquarium. Fish make up about 85
per cent of the trade by value.
ii. Process by which a product is labelled, making it possible for
the consumer to choose products that are environmentally
friendly and have been collected in a sustainable way.
iii. CITES (the Convention on International Trade in Endangered
Species of Wild Fauna and Flora) is an international agreement
between governments. Its aim is to ensure that international
trade in specimens of wild animals and plants does not
threaten their survival. CITES is an international agreement to
which States (countries) adhere voluntarily. States that have
agreed to be bound by the Convention ('joined' CITES) are
known as Parties. Although CITES is legally binding on the
Parties – in other words they have to implement the Convention
– it does not take the place of national laws. Rather it provides
a framework to be respected by each Party, which has to adopt
its own domestic legislation to ensure that CITES is
implemented at the national level. Further information on
CITES and its Appendices can be found at http://www.cites.org/
iv. Further information on live animal transport can be found at
http://www.iata.org/cargooperations/liveanimals/index
v. For more information visit http://www.aata-animaltransport.org/
vi. The MAC Core Standards Interpretation Document can be
found at: http://www.aquariumcouncil.org/docs/library/1/10-
01-02_MAC_Core_Standards_Interpretation.pdf
vii. Further details on EU wildlife trade regulations can be found
at: http://europa.eu.int/comm/environment/cites/home_en.htm
or http://www.eu-wildlifetrade.org/
viii. Japan’s data are based on exporters’ reports for 1997 and
years 1999-2001 as Japan’s Annual Reports for 1999-2001 are
not available and Japan did not report any coral imports for
1997.
ix. Canada’s data are based on exporters’ reports for 1997 and
2000 – there were no coral imports reported in 1997 and
Canada’s 2000 Annual Report is unavailable.
x. Republic of Korea’s data for 2001 are based on exporters’
reports as its 2001 report is unavailable.
xi. The EU comprises Austria, Belgium, Denmark, Finland, France,
Germany, Greece, Ireland, Italy, Luxembourg, Netherlands,
Portugal, Spain, Sweden and the United Kingdom.
xii. The author, through a MAC representative, approached John
Brandt, an experienced aquarium hobbyist, for an alternative
opinion. In answer to the question, ‘What constitutes an
unsuitable species?’, and in response to a request to derive
species lists fitting that criterion, he replied:
‘The experiences of aquarium hobbyists and professional
aquarists have shown that some species of animals are
unsuitable for captivity. Though there may be a variety of
causes, the underlying factor with these animals is that they
cannot consistently be maintained in aquariums successfully.
Unsuitability is a culturally derived category. Most aquarists
agree that a failure to thrive in captivity is a fundamental
characteristic of an unsuitable species. Some aquarists regard
species that can reach a large adult size as being unsuitable.
There is also a common sentiment that truly unsuitable species
should not be collected for the aquarium trade.
‘The most frequent reason that an animal cannot
acclimatize to captive care is that its dietary needs cannot be
met. Many reef species are obligatory feeders (e.g.
Butterflyfishes42, 173), meaning that they eat only one or few
types of foods in the wild. When placed in aquariums they may
refuse to eat prepared foods or if they begin eating they may
experience malnutrition over time. Unsuitability is
characterized by high rates of mortality and greatly reduced
lifespans. Occasionally individuals can be found that have
acclimatized to captivity, but rarely can any particular factor be
attributed to their success.
‘The factors for unsuitability in lists A (highly unsuitable
species) and B (generally unsuitable species) only involve
failure to thrive in captivity; not potential size, toxicity or any
other factors that may make a species unsuitable.
‘These compiled lists and their criteria do not represent a
highly formalized approach to the issue. Much dialogue
between hobbyists, professional aquarists and scientists on
this topic should occur before any official regulations, policies
or legislation be enacted from these lists.’
xiii. Coral that has a mutualistic relationship with zooxanthellae
(small algae) and, hence, grows only in sunlit waters.
xiv. Loss of the coral’s zooxanthellae.
xv. Recruitment is an integral part of fish population dynamics,
because the survival of juveniles ultimately dictates the
abundance of adult populations. In order to survive, juveniles
must overcome competition, predation and habitat
availability124. Typically, researchers define recruitment as the
survival of individuals that settle as larvae out of the plankton
to reef habitat.
xvi. An organism that has an intimate association with one or more
organisms of a different species.
xvii. Two notable exceptions to the rule:
Acanthochromis polyacanthus
: This species of damselfish
incubates its eggs in a small crevice for two weeks. Once the
eggs hatch they do not disperse with ocean currents but
instead shoal near the bottom;
Pterapogon kauderni
: In this species the male retains the free
embryos in his oral cavity for several days and so there is a
complete lack of a planktonic phase.
xviii. Main countries of destination given by the database were the
Netherlands and the United States.
xix. This section is based on the MAC website and Holthus113.
xx. More detailed information on cultured fish and invertebrates
can be found under the breeders’ registry:
http://www.breeders-registry.gen.ca.us/
xxi. Currently, the most important farms are based in the Bahamas
(Aqualife Research), the United States (ORA Farms and Dynasty
Marine Associates in Florida and C-Quest in Puerto Rico) and
the UK (Tropical Marine Centre in London).
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From Ocean to Aquarium
The global trade in marine
ornamental species
From Ocean to Aquarium
is the product of a collaboration between UNEP-WCMC,
the Marine Aquarium Council (MAC) and the industry itself. It is the first of its
kind, examining issues surrounding the trade of live coral, fish and invertebrates
for the marine aquarium trade, and presenting a comprehensive and independent
synthesis of related information.
With the total value of the trade amounting to as much as US$330 million
a year and an estimated 2 million people worldwide keeping marine aquaria, the
industry plays a significant role in both source and destination countries.
Tropical coral reefs are the most important source of specimens for the
aquarium trade – mainly fish, including seahorses, the corals themselves, and
others such as anemones, starfish and giant clams. Almost all marine aquarium
species are taken from the wild, with few examples of captive breeding. Most
originate from Southeast Asia, particularly Indonesia.
From Ocean to Aquarium
presents a brief overview of how the trade
functions and the impacts it has on coral reefs, as well as on the human com-
munities that derive an income from trading in marine ornamental species. It
describes, for example, the effects of destructive harvesting techniques such
as the use of cyanide, and the risks certain species face of over-collection to
satisfy the demands of aquarium hobbyists. However, it also highlights the
measures that can be taken to ensure the sustainable collection of organisms,
minimizing the impacts on coral reefs while maximizing the income for coastal
communities.
It is with this in mind that organizations are working together to ensure
the future for coral reefs, their animals and the aquarium trade.
UNEP World Conservation
Monitoring Centre
219 Huntingdon Road, Cambridge
CB3 0DL, United Kingdom
Tel: +44 (0) 1223 277314
Fax: +44 (0) 1223 277136
Email: info@unep-wcmc.org
Website: www.unep-wcmc.org
UNEP-WCMC Biodiversity Series No 17
ISBN: 92-807-2363-4
www.unep.org
United Nations Environment Programme
P.O. Box 30552, Nairobi, Kenya
Tel: +254 (0) 20 621234
Fax: +254 (0) 20 623927
Email: cpiinfo@unep.org
Website: www.unep.org
October 2003
