Beyond ballast water: aquarium and ornamental trades as sources

Transcription

REVIEWS REVIEWS REVIEWS
Beyond ballast water: aquarium and
ornamental trades as sources of invasive
species in aquatic ecosystems
Dianna K Padilla1 and Susan L Williams2
Although ballast water has received much attention as a source of aquatic invasive species, aquariums and
trade in aquarium and ornamental species are emerging as another important source for species likely to
invade aquatic habitats. These species are spread throughout the world in a generally unregulated industry.
The recent focus on the aquarium trade as a possible mechanism for environmentally sustainable development poses an especially dangerous threat, although this has so far escaped the attention of most environmentalists, conservationists, ecologists, and policy makers.
Front Ecol Environ 2004; 2(3): 131–138
• A third of the world’s worst aquatic invasive species are aquarium or ornamental species
• The lucrative aquarium trade will never be environmentally
sustainable unless the consequences of escapees are considered
• Regulations to prevent unwanted species introductions from
aquarium and ornamental sources currently lack authority
• A white list of native or safe alternative aquarium and ornamental species will help prevent unwanted introductions
1
Department of Ecology and Evolution, Stony Brook University, Stony
Brook, NY ([email protected]); 2Bodega Marine Laboratory, University of California Davis, Bodega Bay, CA
© The Ecological Society of America
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Developed countries
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In a nutshell:
Here we make the case for increased attention to this
threat. At present we do not have all of the data on its full
environmental and economic extent, but there are
enough examples of aquarium and ornamental escapees
that are important invasive species to raise concern. We
highlight the tension between sustainable development,
intended to support the conservation of biodiversity, and
the negative impacts from invasive species. Resolution of
this conflict rapidly boils down to a need for future economic analyses. In the meantime, however, we suggest
several relatively easy steps that managers and policy makers can take immediately.
Invasive species are recognized as the second leading
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quatic invasive species are just a mouse click away from
any home in America. There are more than 11 million
hobbyists in the US alone, supporting a $25 billion-per-year
worldwide industry in aquarium and aquatic ornamental
species, most of which are available through mail order and
over the Internet (Kay and Hoyle 2001). For example,
although water hyacinth is banned in many states, and took
Florida over 100 years and considerable expense to control
(Schardt 1997), it remains available over the Internet for $4.
While aquarium release is one of the five top avenues for
introduction of non-native invasive species (Ruiz et al.
1997), it has received relatively little attention from both
scientists and policy makers. The aquarium and ornamental
species industry is growing by 14% annually worldwide, and
the majority of export dollars enter developing countries
(Figures 1 and 2). Far outstripping the per-pound value of
harvested wild fish, ornamental fish harvest and culture is
being promoted as a pathway to environmentally sustainable
development by the Fisheries Resources Office of the Food
and Agriculture Organization of the United Nations (Figure
3). However, this largely unregulated industry poses a serious
but mostly unrecognized threat to marine and freshwater
ecosystems as a source of invasive species.
Value (millions)
A
Year
Figure 1. International export value of ornamental fish. In
1996, the total export value of ornamental fish and invertebrates
was over $200 million. More than 60% ($130 million) went
into the economies of developing countries. Although organisms
caught in the wild represent only a small percentage of the trade,
it is this aspect of the industry that is most likely to directly affect
fishing communities in developing countries. Adapted from FAO
1999.
www.frontiersinecology.org
131
Sources of invasive species in aquatic ecosystems
DK Padilla and SL Williams
© Marine Aquarium Council
132
Figure 2. Major importers and exporters of marine aquarium species. The US, Western Europe, and Japan are the greatest
importers; the US alone imports more than 80% of the trade in corals.
cause of extinctions around the world (Wilcove et al.
1998). They pose severe ecological and economic threats
as well as danger to human health – for example, the
snail Biomphalaria glabrata carries schistosome parasites
(Ferrari and Hoffman 1992). To date, most attention has
focused on ballast water (Ruiz et al. 1997), including the
proposed reauthorization of the National Invasive
Species Act, which largely ignores other sources of
aquatic invasive species. Ballast water is certainly an
important and controllable vector of potential pests to
harbors and estuaries that are centers of shipping, but it
is not the only threat to aquatic habitats (Figure 4).
Although other avenues of invasion are now receiving
attention (Naylor et al. 2001; Chapman et al. 2003), the
risks from aquarium and ornamental aquatic species
remain below the radar of most agencies responsible for
preventing and managing aquatic invasive species, and
even of concerned scientists.
For example, a recent report from the American
Association for the Advancement of Science (Best and
Bornbusch 2001) addressed habitat destruction and
overexploitation during the collection of coral reef
organisms for marine aquariums, but ignored the threat
of introduction of non-natives when these species are
transported around the world. As a step forward, the
Working Group on Introduction and Transfers of Marine
Organisms of the International Council on the
Exploration of the Sea (ICES) recently recommended
that the risk from ornamentals and aquarium species
should be evaluated (ICES 2001).
Aquarium species are important and beautiful (Figure 5);
however, like species transported in ballast, some pose
extreme threats. Because of their extraordinarily widespread
dispersal to homes and businesses after importation, they
can affect all freshwater and marine habitats. This contrasts
with ballast-transported organisms, which are only released
into ports where ballast water discharge is not regulated.
Organisms transported in ballast water are usually small,
even microscopic, and are often at very young life stages (ie
larvae and spores). Aquarium species, in contrast, are large
and usually traded as adults, which have a greater probability of surviving to reproduce. In addition, good aquarium
animals and plants are hearty, with weaker individuals
(75–85%) being weeded out during collection and trans© The Ecological Society of America
portation (Wabnitz et al. 2003). Thus,
although ballast water collects all
species, only species most likely to
survive the harsh conditions associated with collection and transport
and the broad physiological conditions needed to survive and reproduce in aquariums are used in the
aquarium and ornamental industry.
Of all the species with the potential
to establish, aquarium and ornamental species represent a subset that may
be particularly invasive.
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How large a threat?
One third of the aquatic species on
the International Union for the
Conservation of Nature (IUCN)
Invasive Species Specialist Group list
of 100 worst invasive species (Lowe et
al. 2000) are from aquarium or ornamental releases. At present, over 150
species of vertebrates, invertebrates,
plants, and microbes (including
pathogens) that have invaded natural
ecosystems have been documented to Figure 3. A juvenile lionfish (top). Lionfish are one of the many species of non-native
come from aquariums and aquatic aquarium fish that are now found in American waters.
ornamental culture (Table 1). The
vast majority of these are freshwater fish (Figure 6); other Wiedenmann et al. 2001). Aquarists prize C taxifolia for its
taxa from aquarium and ornamental releases are underesti- beauty, hardiness, and rapid growth. After being discovmated (Welcomme 1992). Released aquarium or ornamen- ered adjacent to the Monaco Aquarium in 1984, this seatal species displace native species (Ceccherelli and Cinelli weed continues to spread unchecked throughout the
1997), carry pathogens (Stewart 1991), clog waterways Mediterranean (Meinesz et al. 2001), where it displaces
(Schardt 1997), and prey on native species (Table 1), while native species (Meinesz 1999; Meinesz et al. 2001). In
others are major agricultural pests (Anderson 1993; Naylor 2000, C taxifolia was identified in California (Jousson et al.
1996), and some, like the lionfish, are a direct danger to 2000) and Sydney, Australia (Schaffelke et al. 2002).
Molecular sleuthing pinpointed the origin of the invasive
humans (Stewart 1991).
The avenues from aquariums to nature include the strain to a public aquarium in Europe, which transferred
dumping of unwanted organisms, escape from tanks and specimens to other public aquariums, including the
breeding farms (eg during storms), the drainage of water Monaco Aquarium. In virtually all invaded regions, C taxcontaining organisms from tanks, and public aquariums, ifolia shares a molecular fingerprint with strains mainand the ritualistic release of species during religious prac- tained in aquariums, and these invasive strains are genetitices (Severinghaus and Chi 1999). All of these activities cally differentiated from C taxifolia in native tropical
can also release water-borne diseases (Stewart 1991). habitats (Jousson et al. 1998; Weidenmann et al. 2001;
Often, well-meaning individuals, unaware of the problem Schaffelke et al. 2002). In southern California, over
of introducing non-native species, release unwanted pets, $4 100 000 was spent on C taxifolia management from July
believing it is more humane to release them than keep 2000 to July 2002 (B Posthumous, Southern California
them captive. Increases in the marine aquarium industry, Caulerpa Action Team, pers comm).
Regulation to prevent Caulerpa entry into the US (its
particularly the trade in “live rock” (whole communities
of animals and plants encrusting rocks), heighten these listing in 1999 under the Noxious Weed Act of 1974) and
into California (Assembly Bill 1334 of 2001, California
threats (Figure 7) .
Fish and Game Code Section 2300) has been ineffective in
controlling the import, possession, or trade of this alga.
Case histories
Shipped with corals and live rocks from the southeastern
The “killer alga” Caulerpa taxifolia is a good example of an Pacific, Caulerpa continues to be distributed in aquarium
aquarium species turned invasive (Jousson et al. 1998; stores from Los Angeles and San Francisco (S Ellis,
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introduced to Florida waterways
after the World’s Industrial and
Biocontrol
Cotton Centennial Exposition in
Unknown
New Orleans in 1884 (Tabita and
Mix
Woods 1962), when a visitor
brought a souvenir back home to
Conservation
Florida and released it. Water
Aquarium release
hyacinth has been called “the
Bait release
world’s most troublesome weed”
Stocked
(Gopal and Sharma 1981). Able to
double the size of its dense floating
mats in about a week, it covered
US
Florida
51 000 ha by the late 1950s
Figure 4. Comparison of alternative pathways for the introduction of fish in Florida and (Schmitz et al. 1993). Due to its
the US as a whole. Aquarium release is the largest source of introduced fish in Florida and explosive growth, this invader
the second largest source in the country, rivaled only by deliberate stocking for sport and interferes with navigation in
release of bait species.
Florida waterways, requiring legislative appropriations of millions
California Department Fish and Game, pers comm), which of state and federal dollars for limited control. Water
sell over a dozen varieties of Caulerpa, including C taxifolia hyacinth has established itself from Florida to Texas and
(Withgott 2002). Worse still, the Californian legislation is up into Virginia, as well as in California and Hawaii
effectively unenforceable due to amendments added in (Gopal and Sharma 1981; Staples and Cowie 2001).
response to vociferous objections from the aquarium trade Indeed, it has become established on all continents except
and hobbyists. The original bill banned the genus Caulerpa Antarctica.
because other Caulerpa species present a risk (Davis et al.
Water hyacinth invasions have had even more devas1997; Piazzi and Ceccherelli 2002), and identification to tating effects in Africa, where it is still spreading a
the species level is difficult, even for experts. The century after its initial introduction (Navarro and
amended, chaptered legislation bans only C taxifolia, a few Phir 2000). Water hyacinth “draws down” scarce water
Caribbean look-alikes, and other documented invasives.
reserves through its exceptional rate of evapotranspiraIt is generally agreed that the beautiful water hyacinth tion. Before control was implemented in the Nile
(Eichhornia crassipes), native to the Amazon basin, was region, one tenth of the average available water
(7 billion m3 of water per year)
was lost from the river (de
Groot 1993). Navigation and
water supply systems are
clogged and biodiversity has
been impacted. Even worse
to contemplate is the disruption to fishing and associated
increases in mosquito-borne
diseases (Gopal and Sharma
1981). The sums being invested to control this weed
necessarily precipitate tradeoffs with other pressing socioeconomic needs.
At present, this popular ornamental is still used widely, and
is available to anyone over the
Internet. Although each of four
different Internet vendors we
sampled indicated that water
hyacinth cannot be shipped to
states that prohibit it, each site
listed a different set of prohibited states. There are no general
Figure 5. The beauty of reef species makes them popular for home aquarium hobbyists.
regulatory mechanisms in place
Courtesy of P Fuller, USGS
Ballast water
to ensure that this dangerous
invader is not sent to states
where it is prohibited.
135
The challenge of
preventing introductions
It is widely accepted that prevention is the most effective
means of reducing the future
costs of invasive species. The
California experience with
Caulerpa shows that prevention through regulation of the
aquarium hobby and trade will
be difficult. In general, regulation of the introduction and
transfer of invasive species is
hindered by the lack of overarching federal and binding
international instruments that
regulate the intentional introductions and transfers of nonnative species (Shine et al.
2000; Naylor et al. 2001).
Although invasive aquarium
species and ornamentals are a
concern of the IUCN and the
ICES, their position statements, policies, and guidelines Figure 6. Freshwater fishes
currently lack teeth (Sandlund prominent invaders.
et al. 1999). The Convention
on International Trade in Endangered Species falls short
of protecting aquatic habitats from invasions because it
deals only with the trade in listed endangered and threatened species. This issue is further complicated because
governments are loathe to restrict trade. The provisions to
from the aquarium trade such as this discus fish are especially
protect the environment within trade agreements such as
the General Agreement on Tariffs and Trade and the
North American Free Trade Agreement must be
expanded to include preventing the introduction and
spread of invasive species (Jenkins 1996; McNeely 2002).
A major problem is that every
Table 1. Aquatic invasive species introduced through the aquarium and
aquatic plant listed as a federal or
ornamental trade
state noxious weed in the US can
be purchased over the Internet
Habitat
Phylum or division
Class
Families
Species
(Kay and Holye 2001). Most of the
global trade probably takes place
Freshwater
Chordata
Osteichthyes
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115
via this route, thereby creating new
Amphibia
1
2
difficulties in the enforcement of
Reptilia
1
1
Mollusca
Gastropoda
4
10
regulations. US governmental
Arthropoda
Crustacea
1
1
agencies are making some headway
Magnoliophyta
Magnoliopsida
7
8
in dealing with the illicit Internet
Liliopsida
7
10
trade. An Internet surveillance
Pterophyta
Polypodiopsida
1
1
application has been developed to
Marine
Chordata
Osteichthyes
1
1
monitor and deter the sale of invaChlorophyta
Bryopsidophyceae
1
1
sive species and is now in use by
USDA-APHIS (R Stinner, pers
Total
50
150
comm).
Only those species with primary literature documentation of successful introduction through the
In stark contrast to the threat of
aquarium or ornamental trade or associated activities are included. See web-only version for full list of
releases
as a result of unregulated
families and species with references.
growth in the trade of aquarium and
136
2003). This example highlights
the importance of economic
analyses in setting trade policies
that avoid unwelcome economic and ecological outcomes.
The total elimination of the
trade in potential invaders is
unlikely to occur. Economic
models will become very useful
tools for minimizing the risks of
invasions during trade. For
example, listings on a speciesby-species basis require prohibitively costly information on the
consequences of releases, and
are therefore viewed as tradeunfriendly as well as difficult
and costly for governmental
agencies to enforce. Thus,
there is an economic incentive
for regulation to move away
from these “black lists” of proFigure 7. Entire communities of animals and plants are sold as “live rock” in aquarium stores. hibited species.
Pieces of live rock such as this one may contain dozens of species.
A more trade-friendly alternative to blacklisting would be
aquatic ornamental species, this industry is promoted as a to allow trade, but to require the posting of bonds equal to
method of environmentally sustainable development. the estimated cost of repairing any future damage that
International organizations committed to the environment could occur in the worst-case scenario, and only to allow
and protecting biodiversity support cultivation and “envi- trade in species that, if they were to escape, could be comronmentally friendly” collection, with little recognition of pletely removed from the wild (a revocable outcome).
the threat these species pose when they are introduced or Thomas and Randall (2000) developed an economic
escape into natural habitats (Bunting and Meyers 2002). model to address the issues associated with the risk of
Conservation biologists have promoted the aquarium trade invasion for introductions through agriculture and the
in the Amazonian floodplain as a means of saving the rain- release of genetically modified organisms. They found
forest, while ignoring the risks to other aquatic ecosystems that the most sustainable strategy was balanced both to
(Norris and Chao 2002).
the advantage of society and business. The strategy
Resolving the tensions between the positive benefits of involved businesses posting bonds on the future potential
an environmentally sustainable aquarium trade and the cost of reversing an invasion (or other worst-case negapotential negative effects of escaped species that become tive outcome), the use of non-native or genetically modiinvasive will require good economic data to evaluate the fied organisms (and their presence in the environment)
relative costs (environmental as well as economic) and that were revocable, and introductions made initially at
benefits of alternative strategies, and the mutual coopera- low levels.
tion of scientists, conservationists, and the aquarium and
Introductions would not be allowed to increase until
ornamental industry. Economic data compiled by the there were no demonstrated negative outcomes for some
United Nations Environmental Programme (Wabnitz et period of time, and would then increase in a cautious and
al. 2003) are now available for global trade in marine stepwise manner, with bond continuing to be posted. If the
ornamental fish and invertebrates, but not freshwater bond is too small relative to the real costs of worst-case
species, and data on the economic costs of such invasive negative outcomes, society must absorb the cost. If an
species are lacking.
escaped species cannot be eliminated once it has escaped,
Economists have just begun to develop models that can then the outcome is irreversible. If the business is too small
guide the development of trade policy that incorporates relative to the worst-case cost, but the profit is very high,
the costs of invasive species (Perrings et al. 2000). The then the business will gamble for the profit and underinresult of one recent model for the impact of invasive sure against losses. Thus, the success of this strategy
species on agriculture was counterintuitive: freer trade was depends on setting the appropriate bond level and balancpredicted to result in reduced, not increased, total damage ing the true cost of dealing with worst-case disasters when
from invasive species, because lower crop-related damage they arise, as well as the profit level of the proposed busioffset higher ecological damage (Costello and McAusland ness and the ability of a business enterprise to absorb the
costs and risks of negative outcomes. A similar analysis
could be done to examine the applicability for trade in
non-native aquarium and ornamental species. Limited
trade in an aquarium commodity might be permitted,
backed by bonds, monitored for escapes into the wild, and
followed by incremental increases in the trade if warranted.
The aquarium trade industry is well organized, while
those concerned about its environmental soundness are
not. Thus, collaboration with the industry is essential for
educating buyers, sellers, and the public, certifying stock,
and preventing species from being released. Groups concerned with the protection of coral reefs have had success
working with aquarists through the Marine Aquarium
Council to develop an international certification system
for the quality and sustainability of marine aquarium
species. This system of certification and best-practice
guidelines must be expanded to include guarantees that
wholesalers and retailers market “invasives-free” products
and avoid close relatives of invasive species. In addition,
certification that aquatic ornamental cultivators and
large-scale aquariums sterilize their outflows and take
active steps to prevent the accidental release of species is
essential. Educating both retailers and hobbyists about
invasive species and steps they can take to reduce the risk
will have an immediate impact (USGS 2003). One step
could be as easy as attaching a warning statement to the
package of every non-native species sold which says: “Do
Not Dump into Natural Waters!”.
In some cases, public aquariums acquire their specimens from the aquarium and ornamental trade, and have
been implicated in the release of invasive species
(Meinesz 1999; Komatsu et al. 2003). Yet public aquariums can also assist in the prevention of new introductions. Educational displays on how to eliminate escapes
from aquariums reach a very wide audience. Providing
lists of environmentally acceptable substitutes for known
invasive species would benefit both the industry and the
consumers (McNee 2002). These proactive steps could go
a long way to avoid the need for increased regulation, but
they will not be sufficient until the industry, organizations committed to the protection of biodiversity, and
policy-making bodies recognize that aquarium and ornamental species represent a potential and realized threat to
aquatic communities.
Acknowledgments
We thank Paul Bourdeau for helping with literature
research, figures, and Table 1, Mike Doall and the
Functional Ecology Research and Training Lab (SBU)
for assistance with figures, Don Strong and Roz Naylor
for comments, the Aldo Leopold Leadership Program of
the Ecological Society of America, and the
Distinguished Research Fellow program at BML (DKP).
This report is published in part by Grant NA16RG1044,
Project R/ES-54, from the National Oceanic and
Atmospheric Administration to Washington Sea Grant
Program, University of Washington, and Award R/CE18 to the Research Foundation of State University of
New York for New York Sea Grant (to DKP). The views
expressed are those of the authors and do not necessarily
reflect the views of those organizations. This is
Contribution 2194, Bodega Marine Laboratory,
University of California at Davis.
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Beyond ballast water: aquarium and ornamental trades as sources

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