Introduction: Positive And Negative Impacts Of The Marine Aquarium Trade On Coral Reefs, Reviewed And Revisited

In 1996 I published an article in the now defunct magazine, Marine Fish Monthly, entitled "Reef Guilt: Confessions of an Eco-Hobbyist." That article reflected a longstanding inner dilemma I had in regard to my strong beliefs in the conservation of threatened coral reefs and the conflicting practice of ornamental marine collections in the reef aquarium hobby, which I also believed in and supported. Throughout the years I have continued to strongly support industry reform in order to help bring about a more sustainable trade in marine ornamentals. While perhaps less outspoken than I have been in the past, my core beliefs have not changed and today I feel significantly more informed, realistic and involved with the issues than I was nearly a decade ago.

It has occurred to me that despite the years and despite the nearly continuous discussions among aquarists about the impact of the aquarium trade, a great deal of "lip service" is still paid to the issues. I have given lectures on the subject, conducted research and investigated many aspects of the aquarium trade and its effects on coral reefs. Many others have also provided their wisdom; John Tullock (a name belonging to a sage whom many new aquarists may not even recognize) was a pioneer in bringing ethical thoughts to the world of reef aquarists.

Ironically, a short article by Doug Robbins in Advanced Aquarist regarding trade in marine ornamentals was brought to my attention. The article was pointed out to me by Drew Weiner, the head of Reef Protection International (www.reefprotect.org), a new NGO under the umbrella of the Earth Island Institute (www.earthisland.org) whose goals include strategies to reform the aquarium trade in a tangible and positive manner by producing a, perhaps, overly simplistic "beginner's" pocket guide of fish suitable or unsuitable for captivity. I had also become a scientific board member of that organization, hoping to help effect change through their goals. After much work for them, however, I felt that their guide was too limited (and not built on solid foundations) to really make a difference in the trade of marine ornamentals. Furthermore, the very stores that needed to use the guide for new hobbyists would likely throw them into the trash since their income would be jeopardized, and so I left that group earlier this year. I will be attending a special session at the Marine Ornamentals Conference in February of 2006, and will hopefully be part of a NOAA/NMFS funded workshop on coral farming next year. Yet, as I type of other parties' and my efforts, the trade in marine ornamentals and the loss of species to reefs continues unabated and largely unchanged.

I would have imagined that those aquarists who have spent time diving and exploring coral reefs around the world would be among those most inclined to be concerned about the impact of the aquarium trade on targeted populations. Perhaps surprisingly, this is not always the case. It seems as though many aquarists who are divers see the vastness of coral reef resources and assume that the aquarium trade could not possibly amount to anything significant in terms of its impact on coral reefs. Others express concern given the observable continued deterioration of coral reefs, reductions in habitat and species populations, and the often intensive and targeted collection practices that occur in the marine ornamental trade. What most divers do not realize is that "dive sites" are intentionally designed to display the very best or most unique of islands' coral reefs and organisms. No dive shop takes divers to the highly degraded sites, the ugliest reefs on the island or to those sites where the ornamentals are harvested - at least not those who want to stay in business for long. Finally, over time a sliding baseline has occurred with new divers who view the first reefs they saw as indicative of a "pristine" condition, when in fact reefs all over the world are seriously degraded in most areas (Jackson, 1997; Bellwood et al., 2004; Baum and Myers, 2004; Pauly, 1995; Sheppard, 1995).

When I first began investigating the role of the marine aquarium trade's potential impact on coral reefs, few others had assessed the trade. As it happens, my interest apparently coincided with a number of small and large-scale investigations and efforts to better understand the effects of the aquarium trade, and over the intervening years much interest, media coverage and investigation has occurred. Unfortunately, a great deal of the information gained has appeared in sources that are not readily available to the world's aquarium hobbyists, and only some of it eventually trickles down to those who keep coral reef animals in tanks. As a result, it seems as though events are occurring to affect the aquarium hobbyists; that things are being "done unto them" without their input such as the infamous "Case Bill" that was introduced as legislation, rejected, and then reintroduced again. I have found, met and heard of scores of people making recommendations and assumptions about the reef aquarium hobby's populace often with little direct involvement, experience or understanding of what the hobby is really like.

A negative opinion of the aquarium trade commonly expressed by many groups outside the trade, largely fueled by images of cyanide caught fish and destructive collection practices for vain displays of tropical fish and corals doomed to a short lifespan in captivity, is not really a correct one (Tsuroka, 1993; Nash, 1996; Wood, 1985). Many important advances and knowledge have been gained from the reef aquarium community, most of which have gone largely unrecognized. It is not surprising that those uninvolved in the aquarium trade often see the hobby as a destructive force whose actions threaten coral reefs directly, and whose goals are seen as a vain waste of marine life that often dies quickly and senselessly within the confines of captivity, and this remains true for more than a few species. Similarly, emotion unfounded in substance dominates the arguments of aquarists angered about potential regulations of ornamental collections and conspiracy theory-like suspicions about the motivations of various conservation, governmental or management authorities.

It occurs to me that despite the fact that this is a somewhat well-worn subject, it is also important enough that it needs restating. Recently I have given several presentations that include so many data slides on trade issues that I struggle or fail to finish my talk within even unreasonably long time frames. I am always asked if I could provide the slides to the group so that they could have more time to digest them. I also think relatively few people are aware of the current state of knowledge regarding the trade in marine ornamentals. Although numbers of marine aquarists are vastly increased compared to studies done in the 1980s and early 1990s (PIJAC 1999), the survivability of many organisms in aquaria has also risen dramatically even though current literature still cites the old sources. While the improvement is encouraging, many organisms still fail to thrive or survive, and the aquarium trade overwhelmingly causes a net loss of living organisms from coral reefs. It is this loss that I hope to ameliorate through this article, my previous article in the series, and in fact in all my articles, even if indirectly. The information presented here was obtained from many sources, including published scientific literature, popular literature, various surveys and studies done by organizations monitoring the flow of live organism trade, economic trade reports, governmental agencies, phone interviews, surveys and long-term personal involvement and experience in the industry. Much of this work was jointly presented by Jonathan Lowrie and me at the 1999 meeting of the National Coral Reef Initiative in Ft. Lauderdale. Unfortunately, we missed the deadline for submission of this work. I have chosen to revisit and update the information for this article. It is important to keep in mind that the aquarium trade has grown by approximately 30% each year since much of this material was first written and the implied numbers resulting from this growth today should be taken into account.

While many important advances in husbandry and knowledge about coral reef organisms have been gained from the aquarium hobby, many aquarists use the argument of potential benefits of advances in husbandry or in creating reef awareness to those unfamiliar with the creatures held in tanks as justifications for the hobby's existence. While perhaps noble, the fact remains that millions of animals are collected from reefs and subsequently die prematurely as a result of their collection for the trade. Whether or not the impact of the hobby is significant by comparison to other threats affecting reefs today is immaterial. It is a distinctly negative impact. Advances in husbandry which are undocumented or not carefully considered and disseminated are relatively useless bits of anecdote that do not benefit reefs, but only reef hobbyists. Any public awareness generated by those with tanks in their living rooms and bedrooms could assuredly be provided more effectively and without the huge mortality of organisms that occurs to create such awareness.

Reef tanks are fascinating, mesmerizing and educational, even if only for the reefkeeper. But I ask that readers be objective about their own involvement. I have killed far more animals than are currently alive in my tanks. I have shelves full of dead corals to prove it. Fortunately, through propagation I have probably given away three or four times more coral than I have killed, most of my fish are ten years old or older, and at the personal or aquarium hobby level, I think I have had a net positive effect. In terms of my direct impact on coral reefs as a reefkeeper, there is no question - I have caused the loss of many beautiful coral reef organisms. Hundreds by my own hands. I would estimate that my net impact is probably less than the average aquarist's impact because of my determination to seek out captive reared livestock and my very keen interest in and ability to allow the survival of animals I acquire. If we estimate that there are one million reefkeepers in the U.S., and we consider what I think is a conservative estimate of one hundred animals purchased over the average person's time as a hobbyist, it's easy to see why some people might be concerned. It is again important to keep in mind that the aquarium trade has grown by approximately 30% each year.

I hope that a more informed aquarium populace will help bring about positive change for reefs, aquarists and all those involved in the trade. I hope that in the end our skills and efforts make a difference. I will begin this part in the series with a relatively brief overview of the aquarium-based trade in marine organisms.

Collection of Marine Species

With dramatic improvements in husbandry techniques and distribution abilities, the marine aquarium trade imports thousands of species of tropical marine fish, corals and other invertebrates from coral reefs. Collection of species for the trade is predominantly from the Philippines, Fiji, Indonesia, Brazil, Vietnam, the Maldives, Sri Lanka, the Red Sea and Hawaii. While some studies exist on the impact of a few exporting nations, an assessment of the worldwide scope of such impact to natural reefs is required.

The United States is, by far, the largest consumer of reef species for aquaria (Bentley, 1998). Between 1.5 and 2 million people keep marine aquariums worldwide, with a conservatively estimated 600,000 households in the United States alone, and this old statistic probably greatly underestimates the number today. The global wholesale trade in marine species for aquaria amounts to $200-330 million, with some retail estimates today in the billions, and includes primarily fish, corals, sponges, anemones, mollusks, crustaceans and live rock. The United States has consistently been the largest importer of stony corals and live rock since the 1990s, despite prohibiting the collection or extraction of scleractinian corals and live rock in its own federal, state and territorial waters because of concerns that the species are vulnerable to overexploitation (Best, 2003). The industry that supports the trade in marine ornamentals worldwide is mostly unlicensed and unregulated (Tullock, 1998). At a time when I was trying to garner information about the trade with Jonathan Lowrie in 1998-1999, U.S. importers and wholesalers were reluctant to cooperate at all in assessing the trade or their role in it. While some retail facilities and most aquarists were helpful in compiling information about the trade, many wholesalers we contacted refused to cooperate, and one large facility even sent a "cease and desist" order upon receiving a voluntary survey in 1998. The same source had earlier provided a list of species for sale, many of which are generally deemed inappropriate for aquaria in terms of survivability. "There are only approximately 25 importers and about 100 wholesalers in the U.S., and few of them are public corporations. Thus, they have no legal requirement to divulge information" (Tullock, 1998).

A quote from the U.S. Commission on Ocean Policy (2004) reads, "As the world's largest importer of ornamental coral reef resources, the United States has a particular responsibility to help eliminate destructive harvesting practices and ensure the sustainable use of these resources. Many of these resources are harvested by methods that destroy reefs and overexploit ornamental species. A balance is needed between sustaining the legitimate trade in ornamental resources and sustaining the health and survival of the world's coral reef resources." It has been established that the number and amounts of corals (living and dead) and fishes destined for aquaria worldwide is massive, even if the qualitative effect on reefs is minimal compared to other reef degrading influences (Wheeler, 1996). Many assessments are now out of date, or significant changes and shifts in species or collection locale have occurred (Wheeler, 1996; Bentley, 1998). There is little question that the widespread use of cyanide, muro-ami and other dangerous fish collecting chemicals has negative, if not seriously damaging, effects on coral reefs (Bryant, 1998; Rubec, et al., 2001). Studies suggest that intensive collection resulting in local depletion of certain desirable species can and does occur (Wheeler, 1996; Tissot and Hallacher, 2003). Inadequate facilities for the holding and transport of species unquestionably results in a high to very high number of mortalities. Disease, unhealthy water conditions, stress, poor care, lack of education regarding the needs of marine fauna, and motivation driven by economic necessity all contribute to unacceptable levels of unnecessary losses of marine ornamental fauna (Baquero, 1999; Albaladejo, 1981; Tullock, 1998; Vallejo, 1997). Reports indicate that mortality of all marine species captured for the trade may be 50% or higher during the process of removing fish from the reef to the often primitive holding facilities prior to export. An additional 30% mortality can then occur at each step in the transport chain, culminating in what may be over 90% mortality before retail purchase (Rubec, et al., 2001). Reports of 10-40% mortality of organisms were received from export stations alone in Indonesia (Corbin and Hopkins, 2004). In more recent years, the serious findings of non-native releases by the aquarium trade into Florida and Caribbean waters have resulted in at least one species forming breeding populations (Semmens, et al., 2004). Poor or non-specific record keeping, establishment of quotas, quantification of sustainable yields, enforcement of regulations (if any) and the rapid rise in marine aquaria popularity has made investigation difficult (Shoup, 1995; Wheeler, 1996).

Among the current techniques used for collection of marine ornamental species are cyanide, prying and breakage, as well the use of nets and seines. Both short and long-term survivability are dramatically impacted by factors such as handling in transcontinental shipping procedures, wholesale holding facilities and individual retail facilities. Knowledge and expertise of the private sector consumer also play a significant role in survivability. The aquarium trade is striving toward several plans of certification and conservation to improve survivability. These plans, and some advances which already have been made, include captive breeding of fishes, propagation of corals and education about advanced husbandry techniques with the goal being to significantly lower the number of species harvested from the wild.

In reports too numerous to mention, the decline of many of the world's coral reefs is becoming all too familiar to both scientists and laypersons alike. Many forms of human impact have seriously threatened the health of coral reefs worldwide (Bryant, 1998; Richmond, 1993). Many of the most threatened areas, some of which have few protected areas, are also those areas most exploited by the marine aquarium trade. Some of the world's most extensive, diverse and threatened reefs are in the Philippines and Indonesia, and these countries supply more than 80% of the world's marine aquarium fish, and the majority of the trade in live corals also arises from Indonesia. Indonesia contains more than one third of all the world's coral reefs, and over 600 of the 800 reef-building coral species in the world. A greater variety of species exists on a single island in this region than on all the coral reefs in the Caribbean, and we counted over 50 genera of corals alone on a single 30m transect in southwest Sulawesi.

Indonesia and the Philippines together hold 77% of the region's coral reefs, including the majority of Southeast Asia's best-preserved reefs. These reefs of the Wallacea Bio-Region have been identified by the major conservation groups (The Nature Conservancy, World Wildlife Fund, World Resources Institute, Conservation International and others) as a global priority conservation area. More than 24,000 islands in Indonesia and the Philippines make up the world's largest archipelago, and they are the home to about 17% of the total number of species in the world, including 25% of the world's fish species. These countries contain over 100,000 square kilometers of coral reefs, about 25% of the world's total. Indonesia has nearly 81,000 km of coastline and includes 6 million square kilometers of ocean. All of the world's 15 families of reef-building corals are represented; a total of 80 genera and 452 species. These high diversity reefs serve as a reproductive reservoir for seeding other areas throughout the region due to circulating and seasonally changing currents. The island of Sulawesi, specifically around the Togian Islands, is the very epicenter of coral reef biodiversity (Wallace, 1997). Because of the upwelling of relatively cool waters from the south, the area is also somewhat protected from bleaching events, which have damaged so many reefs around the world.

The coastal areas of the Philippines and Indonesia are also some of the most heavily populated in the world. With rapid population growth rates, the pressure on coastal resources is exceedingly high, with families existing commonly whose every member is involved in resource extraction of some type. The pressures on coastal resources have now reached unsustainable levels in many cases. The principal threats to the region's coral reefs are destructive fishing and overfishing.

The 2002 Global Coral Reef Monitoring Network (GCRMN) report, "State of the World's Reefs," documents how destructive fishing and overfishing have led to ecological destabilization and are even pushing some high-value reef organisms, such as Beche-de-mer (sea cucumbers) to the brink of extinction, and others have been documented (Kolm and Bergland, 2003; Vegelli and Erdmann, 2002) as suffering serious declines, such as the popular aquarium fish and quasi-endemic Bangaii cardinalfish (Pterapogon kaudneri) as well as the recent listing of seahorses as a CITES Appendix II species. The most destructive techniques include: 1) blast fishing, or the use of primitive bombs for food fishing, largely for subsistence consumption and domestic markets, and 2) poison fishing, or the use of sodium cyanide, bleach or other toxins and drugs to capture marine ornamental (aquarium) fish as well as live food fish. These practices have spread from the Philippines to Indonesia, Sri Lanka and other countries, and have become more common over time, despite efforts to abate their use by training in fish catching with nets (Rubec, et al., 2001). Sadly, many corals are more damaged with nets than with chemicals. Also unfortunate is that many comparatively "reef safe" anaesthetics are available, such as clove oil, and Indonesia is the world's largest producer of cloves. The results of destructive coastal fishing have been devastating. According to the WRI's "Reefs at Risk" report, almost 90% of the coral reefs in the Philippines and Indonesia (as well as Cambodia, Singapore, Taiwan, Vietnam, Malaysia and China) are threatened. Fish larger than a few centimeters in length have become rare on many reefs, and my own diving in some of these regions confirms that although small reef fish abound and corals are diverse and healthy, larger fish are indeed a rare sight.

When coral reefs are protected, their recovery can be dramatic and rapid, as has been reported in many publications on recovery following bleaching events and other environmental catastrophes, including most recently the damage from the tsunami of 2004. If coral reefs are destroyed, siltation and sedimentation often become a problem, preventing the settlement and growth of planulae and juvenile corals. In this case, the recovery of reefs takes a very long time, and in some cases reefs never recover. It has been suggested at workshops, meetings and in publications that the best chance of reversing continuing reef degradation on a large scale is an approach that combines private sector incentives with government policy and regulation. In the Philippines, and to a lesser extent in Indonesia, the relevant policies and regulations are already in place, but a system of sustainable private sector incentives is underdeveloped, and one is needed that encourages and requires fishermen to comply with regulations for their own benefit. In the Philippines, for example, cyanide and dynamite fishing have long been illegal. However, a lack of enforcement combined with a lack of incentive to follow the law has led to a dramatic and well-documented decline in the health of the marine ecosystem, including declines in fish and coral populations. When undertaken responsibly, harvesting marine ornamentals supports sustainable livelihoods by providing one of the few potentially sustainable local industries in rural coastal villages, especially since marine ornamentals are a highly valued reef product. Data from the Maldives show that aquarium fish sell for $248 (U.S.) per pound while food fish earn only $3 (U.S.) per pound. In Indonesia, aquarium corals sell for $7,000 (U.S.) per ton, while only $60 (U.S.) per ton is paid for coral harvested for construction lime.

Reef destruction and degradation by the marine aquarium trade result from the use of cyanide to stun and catch fish, coral breakage and the overharvesting and poor husbandry of aquarium organisms. Cyanide use causes long-term habitat devastation by killing or damaging corals and other reef animals (reviewed in Rubec, et al., 2001). Even when collected with nets, aquarium organisms often suffer from poor husbandry practices such as improper post-harvest handling, poor water quality during storage and high packing densities that result in reduced survival. The unnecessary mortality puts added pressure on coral reefs as more organisms are collected to make up for those that die, and national quota systems are often based on export levels, not collection levels, to allow for mortality without loss of income. The high levels of harvesting from limited extraction areas may then lead to overexploitation. Some marine ornamentals collectors and companies do, however, employ responsible practices, proving that it is possible to have a sustainable, environmentally sound trade that is also profitable.

Many in the industry and hobby (and other stakeholders) support a sustainable trade. Prior to the establishment of the American Marine Dealer's Association (AMDA) and then the Marine Aquarium Council (MAC), no real system had allowed consumers to choose responsible operators and sustainably-sourced products from reefs and fisheries that were well-managed, although the results of the MAC have been disappointingly slow and limited considering the resources they have expended throughout their existence. There is a need to develop options for ecosystem management of aquarium fisheries and to develop the capacity to implement the management plans through partnerships of NGOs, collectors, fishing communities, government agencies, end users and all those involved in the marine ornamental trade. I feel it is foolish to look to one organization, such as the MAC, to create change, although catalysis is a possibility.

In terms of stony corals and tridacnid clams, the U.S. Fish and Wildlife Service is empowered to enforce CITES-listed trade in this country, and consequently keeps records of all listed animals imported into the country. Unfortunately, they are understaffed and have very few inspectors to manage the huge numbers of species entering the country (Cleva, pers. comm.). CITES has proven to be a useful tool to track trade in stony corals and live rock, although it's limited for a variety of reasons (Green and Hendry, 1999); this is also a concern as no reliable tracking of non-CITES species, which comprise the majority of the trade, is currently in place (Bruckner, 2001). Correct identification is often difficult, and shipments may be only cursorily inspected to handle the volume of animals in trade (Shoup, 1995; Marquardt, pers. comm.). On the other hand, large shipments of marine organisms are sometimes unnecessarily detained or seized, resulting in mortality because of overzealous, unskilled or unaware inspectors and officials. Still, misrepresentation of livestock bills of lading, misidentification by source countries and the deplorable practice of substitutions or "box stuffing" with organisms not ordered by the customer are rampant, and such shipments certainly deserve to be confiscated despite the unfortunate mortality involved.

While many studies have focused on overexploitation of fisheries and various destructive fishing methods (Russ, 1998; Craig, 1993; Gomez, 1994), there are far fewer reports regarding the impact of the marine and reef aquarium trade on coral populations (Bruckner and Borneman, 2005; Shoup, 1995; Wheeler, 1996; Whitehead, 1986; Wood, 1992). Several studies are now underway (or recently completed) to investigate this industry's relative effect on natural populations (Bentley, 1998; Cleva & Hoover, pers. comm.).

Potential Solutions

A fundamental requirement for a successful and sustainable trade in marine ornamentals is to have an ecologically sustainable supply; for CITES-listed species, this requirement should already be met by the parties, yet rigorous studies have been performed only infrequently. Non-CITES species require no such sustainability studies unless by the law of village-based or resource nation legislation. To transform marine ornamental harvesting to sustainability, marine management areas that include reserves or no-take zones could be established where fisheries management and novel resource strategies (i.e., "farming") can be used to rebuild depleted fish and invertebrate stocks. Few, if any, coral reef management and reserve areas have been established to help maintain and restore stocks of marine aquarium organisms, and no specific programs are in place to achieve this goal. More specific to the marine aquarium trade, in most collection areas the abundance and distribution of marine aquarium resources is not known, and no methods have been available for documenting the resources. Baseline assessment and ongoing monitoring of the collection areas and target species are required to ensure that the level of harvest is sustainable and that conservation benefits are being achieved. Few efforts and little funding are available to accomplish this, in spite of the continued harvest of marine ornamentals as a significant ecological and economic use of coral reefs. The MAC has been utilizing a modified survey technique called MACTRAQ, although disputes have arisen over its utility and despite claiming success, few results have been achieved from the data collection to shape or reform the trade. The actions of village-based collectors determine the difference between sustainable reef resource use and coral reef degradation, and the collectors also contain a huge repository of knowledge of local reef conditions that is seldom exploited. Because education, finances and incentives are not anywhere near their capacity to effect change, collectors have little reason to adopt sustainable practices. As stated in a 2004 MAMTI document, "There is a shortage of funding to allow collectors to purchase the required equipment (nets, dive gear, compressor, etc.), to build holding cages, and to finance the working capital required. While these capital requirements are relatively low (typically less than $2,500 per cooperative), most poor fishing communities have not had access to appropriate sources of capital. In the absence of knowledgeable coaches and coordinators, the collectors are at the mercy of a "spot market" for their product, which often leads to monopolistic pricing, significantly/indefinitely delayed payments, and no direct contact with the international markets. As a result, collectors collect indiscriminately to assure sufficient volume." As it stands, and despite the often stated position of those in the hobby that ornamental trade is a demand-driven industry, collectors will shift from opportunistic collection to "collect on demand" - a key element of sustainable fishery - only if provided with the means and motivation to do so.

A great need exists for consumer awareness about the benefits of harvesting marine ornamentals using non-destructive methods from sustainably managed reefs. In numerous studies and surveys, most consumers have indicated a preference for purchasing marine ornamentals that have been harvested via non-destructive methods. Unfortunately, many local fish stores claim that their livestock were caught via sustainable practices. But, as with the species names of many of the corals they sell, neither they nor the consumers have any way of knowing if the claim is true. Such deceit may occur intentionally or inadvertently, but a lack of any clear tracking of species from collector to consumer prohibits such things from being known. The MAC has made "chain of custody" a primary function of their organization, yet in the U.S., only a handful of retail stores sell such species, and the consumer has no way to know which species present are and are not collected sustainably, nor for the store to know if its supplier has done the same, since neither is required to stock only MAC-certified stock, and no enforcement is in place to ensure compliance with the proposed certification scheme.

Trade in Marine Fish

"Only about 40 of the species currently traded can be farm raised and are commercially available. Cultured fish account for one to two percent of the global trade (Bruckner, 2005; Bronson, 2003)." Commercial trade in ornamental marine fish began in 1952 in the Philippines (Albaladejo, 1981), although earlier reports arise from Sri Lanka in the 1930s. Today, there are between 3,500 and 4,000 collectors in the Philippines, up from 1,500 in 1995, with some 60-75% of them illegally using approximately 150,000 kg of sodium cyanide per year to catch fish (Baquero, 1999). This practice has spread to other nations as 70-80% of the Philippines' reefs have been estimated as seriously threatened habitat (Bryant, 1998, et al.). While some programs now exist in the Philippines to train fisherman to use gill nets (pukot, sebay, salap), they do not exist to any degree in other exporting nations (Albaladejo, 1981; Baquero, 1999), although efforts are underway. Cyanide fishing often results in a type of sudden death syndrome, often becoming apparent only after the fish has been shipped to other countries and entered the retail channel. It has been estimated to result in nine fish killed for every one collected (Brower, 1991) and results in large amounts of collateral damage to other reef species, including corals (Bryant, 1998, et al.; Rubec, et al., 2001). Cyanide kills corals at concentrations hundreds of times lower than the concentrations used to collect fish (Dayton, 1995), and has been sprayed on approximately 10 million coral heads. Many areas that become nearly devoid of fish and coral colonies are allowed to "rest" for a few years before collectors return to harvest them again. For many reefs, and for perhaps numerous reasons, recovery does not appear to be occurring (Gomez, 1994). Juvenile fish are commonly taken for the trade because they are reported to ship better, but these juveniles have not yet had a chance to reproduce (Tullock, 1998). Collectors are seeking new locations as local reefs become depleted (Raymakers, 2002). In July 1997 the World Trade Organization announced that it recognizes ornamental fish as an important export product for 39 Least Developed Countries (LDC), and was the principal export product of one LDC.

Marine ornamental fish make up approximately 85% of the trade in live coral reef species for aquaria. Damselfish (including clownfishes) are the most traded species, but angelfish, butterflyfish, wrasses, blennies, gobies, triggerfish, hawkfish, grammas, hamlets, cardinalfish and surgeonfish (tangs) are also large portions of the estimated 1,471 total species of fish in the trade. In 1995 a survey from the American Marinelife Dealer's Association reported the sale of approximately 10 million marine specimens, generating approximately $100 million dollars in sales. An estimated 20 -24 million coral reef fishes are sold in the global trade, and this number corresponds well with estimates of the U.S. representing approximately 50-60% of the global trade in marine ornamental fishes. It is estimated that 90-99% of the trade in ornamental marine fish is provided by wild collection. An estimated 565,000 -730,000 marine aquaria in the U.S. hold between 5 and 7 million fish in captivity (Tullock, 1998; PIJAC, 1999). In 1992 the U.S. declared imports of marine ornamental fish of around 8 million fish, with an average 15-20% increase in the market during the 1990s (OATA, 1999 PIJAC, 1999). Yet worldwide estimates, based on an estimated 12-20% in marine species of a total 150-300 million ornamental fish traded, would mean world trade in marine fish is between 18-60 million fish (Wheeler, 1996; Derr, 1992). This would indicate that virtually all livestock being imported is used to replace losses in aquaria.

In fact, delayed mortality has been estimated by retailers to be on the order of up to 90% within a year (Tullock, 1998; OATA, 1999). Livestock losses are typically described to be on the order of 10-20% (for various reasons) at each level of transport and holding, with reported mortalities before export more frequently higher - perhaps 40% (Vallejo, 1997). Through the responses of some 900 surveys in 1998, we found the average length of time that aquarists kept fish alive in captivity is 2-3 years. Sixty-two percent of aquarists had kept more than 20 species of fish in their aquaria. Although captive bred-fish are available to supply up to 10% of the trade in some popular species (Wilkerson, 1998), sales figures do not indicate that this is happening, even though 23% of aquarists surveyed responded that they had captive bred fish in their aquaria. As a result of cyanide use, mortality rates of captured fish are 5% to 75% within hours of collection, with 20% to 50% of survivors dying soon thereafter. Of those that survive the collection process, another 30% on average die prior to export. Mortality statistics from cyanide use do not take into account the high incidental loss of non-target wildlife and damage to the coral reef resulting from this misguided and illegal method of fish capture. Fewer than 10% of marine aquarium species are currently captive bred and they represent less than 2% of the total trade. A list of species collected, sites and a description of some of the major fisheries in the Philippines and Indonesia can be found in Annex 14 of a MAMTI document that is available on the Internet. A thorough review of the trade in marine ornamental fish, corals and live rock is reviewed in Bruckner (2005).

         Summary of Fish for Sale at a Large Los Angeles Wholesaler:

Fish "groups"

Unspecified Genera*

Named Genera

Total

47 groups

109

586

695

*This category includes the unusual, although commonly used, assignment of "assorted" species. A grab bag of species, these categories are frequently used as "box stuffers."

These fish were listed as coming from 21 separate countries or regions around the world. Sri Lanka's industry has increased rapidly over a period of twenty years, with between 200-300 species collected there for the aquarium trade. The industry is considered unsustainable and is a major industry. Overexploitation exists partly because no monitoring or management of the trade exists. Moxy nets, cyanide and other poisonous chemicals which damage reefs are used to capture fish, despite such practices' illegality. Fortunately, efforts are underway to try to remedy this problem industry (Monagurusamy and Dhanasiri, 2001).

The Philippines supplies an estimated 75-80% of the global trade in marine ornamental fish, including some 386 species in 79 families (Vallejo, 1997). Half of all collections are bound for U.S. markets. An additional 20% of the Philippine industry is composed of other invertebrates, but does not include corals whose harvest was banned in 1985. The industry employs about 2500 fish collectors with widespread use of cyanide. Training in net collection has been ongoing by several NGOs, and some measure of success has been accomplished in this regard. The major groups collected are damselfishes, butterflyfishes, wrasses and angelfishes. The industry is valued at 6.75 million U.S. dollars, with fish export prices between $3.00-$30.00. Exporters and middlemen control pricing, and export values are 100-400% higher than the prices paid to the collectors. Fish are generally exported within three days of their arrival at an exporter or holding facility after incurring 30-40% mortality at those facilities.

Despite the claimed widespread availability of U.S. tank-raised fish, few were available to aquarists surveyed, and yet 60,000 - 100,000 wild clownfish are thought to enter the U.S. each month (Wheeler, 1996). Rarer and unusual fish are becoming more commonly encountered in the trade (Delbeek, 1998), including deepwater species for which little ecological and less husbandry information is data available (Pyle, 2004). The tentative accuracy of identification, coupled with unidentified genera (possibly representing multiple species), completely unlisted scientific classifications for some fish, species in trade in other countries, those offered at different facilities, and the loose category of "assorted" makes the number of fish species probably well greater than current estimates. The Ornamental Fish Industry in the U.K. reports that over 1,000 tropical marine fish and invertebrate species enter the trade annually (OATA, 1999). Livestock lists we obtained from numerous wholesalers and transshippers there indicate that the estimates of over 1,000 fish species alone for trade in the United States are accurate.

Most facilities do not divulge actual numbers in their inventory lists; rather a three star rating system designating vague amounts of inventory is more commonly applied. A single large transshipper, of which there are dozens (and hundreds of smaller ones), showed a single week's inventory totaling 17,795 fish from Bali, only one of five countries they represented, and 45 countries now export marine fish (Bruckner, 2005; Bernardi and Vagelli, 2004; Lunn and Moreau, 2004). A retailer we spoke with claimed that most, if not nearly all, of these fish will be sold within a week. Among the fish listed were 2,000 Banggai cardinalfish, Pterapogon kaudneri, which are endemic to areas near the Island of Banggai that is off the eastern coast of Sulawesi in Indonesia. The range of this species is larger than originally estimated, but it is still not a widespread species. We learned that most large wholesalers and transshippers regularly show from 1,000-5,000 of these fish on their weekly inventory lists at a price of $4-5 each, with box lots of 120 cardinalfish selling for $2 each. This species, only recently discovered, is also one that has been shown to breed readily in captivity, even by beginners, and its wild populations are declining. For a complete list of references regarding this popular fish, see: http://www.pewmarine.org/pewFellowsDirectoryTemplate.php?PEWSerialInt=9935.

Trade in Corals

The global trade in live coral has increased by more than 500% over the last 10 years, with over 1.2 million wild-harvested stony corals in trade during 2002, as well as undocumented numbers of soft corals, zoanthids, actinians and corallimorpharians. Most of these corals originate in southeast Asia and the South Pacific. Indonesia emerged as the largest source of stony corals in the late 1980s and currently supplies 70-80% of the global trade in live corals (Bruckner, 2003). The trade in corals is more cryptic than the fish trade. Older studies showed that approximately 85% of corals in trade were dead skeletons, although it is known that these numbers have shifted (Shoup, 1995). Fortunately, there is a markedly decreased interest in using dead coral skeletons for marine aquaria, with the increased popularity of reef aquaria. Ninety-three percent of hobbyists we surveyed reported having never purchased dead coral skeletons for their marine aquaria. Rather, there is a rapidly increasing interest in live corals that can potentially be maintained in captivity with a high degree of success (Bentley, 1998; Shoup, 1995). Not only is the size of live aquarium specimens generally much smaller than with dead corals, but there is a vested personal and economic interest in keeping living corals alive.

In the 1990s, numerous reports indicated that Indonesia provided about 92-95% of the world trade in live corals and that the U.S. was purchasing 80-98% of them. For 1999, the Indonesian Scientific Authority for CITES recommended a quota of over 1,000,000 pieces of live coral, up from 1998 (see Table 1) (Lilley, 1999). It is estimated that pre-export coral mortality (as part of this quota) is many times higher. One problem with assessing the trade's impact on reefs is that the name of coral species from the collector to the aquarist is typically assigned from vague descriptions based on appearance (Shoup, 1995). Correct species level identification is rare, and even genus names are often omitted. Many errors in even broader classification exist, made all the more difficult by the inability to determine species in living corals and the concurrent requirement to do so. Some corals listed by genus only are known to have dozens of species imported. Studies have concentrated on those species listed in CITES appendix II, primarily the stony corals. Among the non-Scleractinia, classification is still largely unknown or in need of revision, and little is known of the range or numbers of many imported species. This problem is compounded in that virtually all persons involved from their collection to retail sale, including official inspectors, lack the very specialized expertise needed, or are simply unable to correctly identify various corals (Shoup, 1995; Wheeler, 1996).

Indonesia exports each year nearly 1 million pieces of stony corals to the United States (Bentley, 1998).

One of the problems with assessing numbers in the stony coral trade is the categorization of live rock as Scleractinia (Antozzi, 1997; Shoup, 1995). Nonetheless, some widely variant numbers are reported. Throughout the 1990s, with some reports of over 1.5 million pieces for some years, it appears that increasing numbers of live corals are being traded (Shoup, 1995; Bentley, 1998; Cleva, pers. comm.; Curry, 1998). As with fish, the actual numbers of live corals are probably underreported, especially given that there are no reporting requirements for soft corals, zoanthids, gorgonians (except Gorgonia spp. in U.S. waters), or corallimorpharians. A 1995 report showed world exports of the coral Caulastrea sp. (an easily recognized genus) to be zero in 1992, and a total of 23 individual corals of this genus from 1989-1993 -all in 1993 (Shoup, 1995). Yet we had observed many more than 23 Caulastrea sp. specimens in a single retail store over the course of any one year during this time. According to this report, the author may have been personally responsible for 50% of the total world trade in Scolymia sp. (quantity= 2) and knew the location of the other one during this time period! Montipora sp., especially M. digitata, was also widely available, despite showing only 74 total imports worldwide.

Summary of Corals for Trade at a Large Los Angeles Wholesaler in 1998:

A disproportionate number of corals are of the large-polyped varieties, such as Euphyllia spp., Plerogyra sp., Fungia spp. and Catalaphyllia sp. (Shoup, 1995; Bentley, 1998). These corals have long been mainstays of the retail aquarium coral trade, despite many being much less common in the wild (Carlson, 1989). Species in the families Faviidae and Mussidae are also extremely common in aquarium retail stores, despite a fairly low report of trade in these genera. Additionally, some species, such as Nemenzophyllia sp., are almost unreported in the literature (Veron, 1986), yet they have appeared in large retail quantities for well over a decade. Other corals very commonly imported are Goniopora spp. and Dendronephthya spp., both of which are well known to have remarkably poor records of survival in captivity (Borneman, 1996, 1997). In terms of the aquarium hobby, approximately 25% of those surveyed had corals that had survived from six months - one year, and another 25% from 1-2 years. Nearly a third had corals 2-3 years old. Sixty-seven percent kept 10 or more species of coral in their aquaria. Eighty-four percent of those surveyed had captive-bred corals in their aquaria, although only 4% of the total purchase of corals was from captive-bred sources.

Very few studies have investigated the nature and potential loss of non-CITES listed marine species, specifically various invertebrates and non-scleractinian corals. The group of octocorals and zoanthids, along with still largely unclassified Indo-Pacific corallimorpharians has, in fact, long been the standard coral types stocked in retail stores. They are very hardy, and many stores and wholesalers do not stock as many stony corals (especially small-polyped varieties) because of their more demanding requirements. According to our survey, they make up 68% of the stock of typical U.S. retailers, with many reports of over 90% of retail coral livestock composed of non-scleractinian corals. This number does not reflect the statement by Bentley (1998) that, "there is no evidence that the large group commonly known as soft corals (subclass Alyconaria) are exploited in significant quantities in Indonesia." Perhaps the vast numbers of non-scleractinian corals are indeed coming from other regions, but this would entail a major discrepancy in trade percentage figures in terms of what is known about aquarium supply sources. In light of the immense number of discoveries of novel and potentially beneficial secondary metabolites being produced by these taxa, and also because of the limited knowledge of their biogeography, taxonomy and biology, this number may represent an area that should be investigated. A staff member at a large Los Angeles wholesaler stated that they often discover 1-2 shipments of unusual corallimorphs they have never seen before, and then they are never seen again.

Live Rock Trade

"The harvest of naturally-occurring live rock in Florida waters (state and federal) was prohibited in the late 1990s. During the peak, roughly 300 tons of live rock valued at an estimated $10 million were harvested annually. Former live rock harvesters have established nearly 50 submerged land leases in state and federal waters. They have deposited rock on these leases to provide a substrate for the recruitment of encrusting species. Their success has been mixed, with location and luck playing a large role. Rock placed too shallow becomes an attachment site for undesirable algae and all sites have experienced damage and loss due to algae blooms and tropical weather systems. Farm gate sales for 2001 were reported around $500,000" (Bronson, 2003). Prior to enacting a ban on live rock collection, Florida waters provided for the harvest of 250-300 tons of live rock each year (Derr, 1992). Despite a ban enacted on live rock (classified as Scleractinia, CITES appendix II designation), rock from this area continues to enter the trade illegally, despite the efforts of those now involved in the licensed aquaculture of live rock. Ricordea florida, for example, is a corallimorph that is still commonly seen in many retail shops attached to large pieces of live rock. Six years after live rock harvest became illegal, I tried to contact or visit several local facilities advertising such live rock in hobby periodicals and local newspapers. I found that our calls were not returned, and physical addresses were only P.O. boxes. Over four million pounds of rock are now on the sea bottom in Florida-based aquaculture ventures (Antozzi, 1997). Unfortunately, the massive increases in the harvest of Pacific live rock resulting from the Florida ban have dropped retail prices from around U.S. $10/pound to around U.S. $2-3/pound. Wholesale prices hover around U.S. $1.50/pound, making it very difficult for aquaculture facilities of live rock to compete in the marketplace. We found that aquarists purchased an average of 205 pounds of live rock for their aquaria. Live rock extraction leads to increased erosion and loss of important fisheries habitat. However, coral and reef rock mining is a similar industry. In Sri Lanka alone, thousands of tons of reef corals and substrate are mined each year for construction (Monagurusamy and Dhanasiri, 2001). Reports on the total amount of live rock, mainly originating in Fiji, Indonesia and, to a lesser degree, other Pacific Islands, has increased greatly and is discussed in Bruckner (2005).

Trade in Other Species

"In addition to colorful and exotic marine reef fish, hobbyists are also interested in a wide variety of crustaceans and molluscs. Various ornamental shrimp (golden banded coral, fire, Caribbean anemone, clown anemone and peppermint), molluscs (queen conch, Florida fighting conch, giant clams (Tridacna spp)) and other invertebrates (feather duster worms) are prime candidates for aquarium collection. Immediate production and distribution of these species is slowed by the work needed to resolve larval survival or regulatory conflicts (Bronson, 2003)." As the number of aquarists keeping reef aquaria continue to increase, concurrent increases in the number of other invertebrate species available are likely. Reef aquarists are quickly learning the value of biodiversity in establishing more stable conditions, and some popular works have even alluded to the experimental practice of using sponges and tunicates as "biofiltration" (Tyree, 1998). Many of the invertebrate species commonly available are either inappropriate for closed systems in that they are incompatible with corals or fishes, or they are very difficult or impossible to maintain in captivity at present. This is especially true of planktivorous filter feeders. Other species, such as many of the colorful nudibranchs, crinoids and sea stars have long appeared in the aquarium trade, despite being generally acknowledged as inappropriate species for captivity. Anemones that host clownfish have been notoriously short-lived in captivity, despite exceptions (Wilkerson, 1998). Surprisingly, anemones are most frequently reported as the longest-lived invertebrates in hobbyists' aquaria, according to our survey. Nonetheless, certain anemones (especially H. malu and H. magnifica) have very poor records of survival but appear regularly in retail stores. While the husbandry of anemones is not impossible, their needs are apparently well beyond the abilities of the majority of aquarists. Whether this is a matter of education, motivation or ability does not change the fact that many thousands of actinians are failing to survive. Although the trade in tridacnid clams was officially banned in Fiji in 1988, the Secretary-approved exemptions allow export of live clams to continue (Sant, 1995). Wild-caught tridacnid clams appear regularly in the trade and also appear on availability lists. Philippine wild-caught clams also appear on availability lists, including one dated March 30, 1999.

A recent article examined the trade in ornamental crustaceans. The authors identified 128 heavily traded species: 49 species of caridean shrimp (15 from the family Hippolytidae), 32 species of anomuran crabs, 27 species of brachyuran crabs, 7 stenopodidean shrimp, 7 astacidean lobsters and 6 panulirid lobsters. Culture of the crustaceans is impeded by long and sometimes complex larval development and low commercial value of some species. Ecological impacts from the high rates of collections of hermit and Mithrax crabs from tidal areas, cleaner shrimps, and Hymenocera picta as a predator of coral eating crown-of-thorns starfish (Acanthaster planci) are seen as an area of serious concern (Calado, et al., 2003). Unfortunately, data on trade in the myriad of other invertebrate species are virtually nonexistent and/or unpublished.

Summary of Other Invertebrate Species for Trade at a large Los Angeles Wholesaler:

The Road to Change

The Indonesian Coral Reef Working Group is a multi-stakeholder organization brought together to address weaknesses or limitations in management and monitoring of the coral trade. Developed at the Technical Meeting on Controlling and Monitoring of Coral Reefs Utilization in Bali (2001), this group developed agendas shortly after the International Workshop on the Trade in Stony Corals, held in Jakarta (Bruckner, 2001). Together with other NGOs, the trade in corals may be able to utilize suggestions and sustainability data recently provided by Bruckner and Borneman (2004, 2005) and initially developed in the Jakarta workshops and subsequent protocols later tested in the Spermonde Archipelago of Sulawesi. Bruckner (2005) further suggests potential solutions to each major impediment to the attainment of a sustainable marine ornamental trade.

The Solomon Islands have experimented with light capture traps to collect and rear presettlement larval fish for the aquarium and food fish trades (Hair, et al., 2002). While successful, the authors note that their efforts alone could not supply the trades, but if coupled with multiple efforts could significantly reduce the number of fishes collected for these industries. In particular, the overcollection of rare species and food fish pose the greatest risks, along with the use of destructive fishing techniques. Similar operations have begun in other areas. One group, EcOcean, is particularly well developed and supported, and is working extensively with local communities. Its exports of larval reared fish for the aquarium trade have already begun from several operations in the Philippines. These fish are also becoming available in the U.S. (http://www.ecocean.com/).

Surveys

A number of formal and informal surveys have been conducted in the U.S. and abroad that are useful in determining some information on various aspects of the marine aquarium hobby (Greco in Reefs U.K., Borneman at 1999 NCRI and 2000 ICRS conference, Nilsen in Aquarium Frontiers magazine, unsuitable species lists by Borneman, Scott Michael, John Brandt, and Reef Protection International, From Oceans to Aquariums, etc.). While surveys may provide some anecdotal evidence of aquarist trends and practices, there seem to be some discrepancies between survey answers and actual practices.

Summary

The marine ornamental trade is plagued by a number of problems that have come to the forefront of the international reef conservation communities. While perhaps not an issue that, if properly addressed, will save coral reefs from the plight they face, as aquarists and resource users we have an intrinsic responsibility to, and stewardship of, these important ecological communities. I urge readers to consult the references in this article. Next month I will conclude this series with practical solutions for collectors, exporters, wholesalers, retailers and hobbyists to help improve the survival of marine ornamental species based on my personal experiences in this hobby over the years. In turn, this will hopefully and concomitantly produce economic incentives for positive change.

Acknowledgements

I would like to thank the following persons for their aid in obtaining documents, statistics and information in the preparation of this paper: Andrew Bruckner (NOAA/NMFS), Peter Rubec (Florida Marine Research Institute), Ferdinand Cruz (International Marinelife Alliance), Mark Erdmann (Conservation International), Gregor Hodgson (Reef Check), Caroline Rogers (TRAFFIC), Craig Hoover (TRAFFIC), Ann Hunt (MCS), Leath Muller (GBRMPA), Sandy Cleva (USF&W), Charles Delbeek (Waikiki Aquarium), Nokome Bentley (Trophia), Carl delFavero (Indoor Oceans), Morgan Lidster (Inland Aquatics) and Theresa Herndon (formerly of Sea Critters).

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