Originally posted: 2009

A response to: “Crawling to Collapse: Ecologically Unsound Ornamental Invertebrate Fisheries”

By Eric Borneman

It is with some dismay that I read the responses of Watson, Moe, Wittenrich and Young regarding the article, “Crawling to Collapse: Ecologically Unsound Ornamental Invertebrate Fisheries,” by Rhyne et al. (2009).

Rhyne et al. is the most recent and comprehensive look at the marine ornamental trade from Florida in over ten years. The previous review by Adams et al. (2001) covered the period from 1990-1998, a period that represented the beginnings of the reef aquarium hobby in the United States, the phase out of Florida live rock collection, and showing Florida invertebrate landings to rise from 850,000 individual animals in 1990 to 3.3 million animals in 1998, an increase of 290%. The introduction is a basic but thorough review of the history and concerns of the global and Florida ornamental trade, including a well-stated review of the shift towards species that provide ecosystem services. This concept is insightful since the ornamental trade, besides showing demand trends over time, has indeed become more functional in terms of the species employed in the purchased diversity of modern reef aquaria. At the beginning of the previously reviewed period, marine aquarium keepers knew much less about functional species, and decorative species with poor survival were commonly available and demanded. It is also important to note that the authors also acknowledge that many of the same species used for functional roles in aquaria have similar functional roles in their natural habitat.

The methods employed were simple and effective. Data were available from the Florida Fish and Wildlife Research Institute as a requirement for the fishery, and the authors used a number of criteria to group the data to make the results more meaningful in terms of both aquaria and wild populations. They used an autocorrelation statistic to remove background noise from a time series.

The results are clearly presented and unambiguous since the data were concrete numbers that are not in dispute. The trends show an increase in numbers of organisms collected that are unsurprising and correlate well with the previous data set of Adams et al., as well as with other similar works on the global ornamental trade. The authors then discuss the results in light of the potential loss of ecosystem services from the collected species and in light of the comparatively well-managed Florida fishery. They also voice potential concern over the number of animals taken in terms of sustainability to the fishery.

The authors are all well known in their fields and Rhyne, Tlusty and Bruckner, in particular, all have extensive knowledge of the marine ornamental trade, are supportive of sustainable trade and have contributed greatly, directly and indirectly, to the marine aquarium hobby. Bruckner, in particular, has written or edited most of the seminal papers and reviews on the ornamental trades in stony corals, precious corals, cyanide fishing, and seahorses. Rhyne’s contributions to the breeding of marine species in captivity are unequivocal.

To see a reactive response by those involved in the ornamental trade to any article, lay or peer-reviewed, that lays bare the numbers and potential consequences of the aquarium trade as a threat to coral reefs is expected. Over my twenty years involved in the marine aquarium hobby, I cannot count the number of events or articles that have prompted similar responses.  The ban of live rock in Florida led to a near panic over the availability of both live rock and Ricordea florida. For years, large rocks covered in Ricordea were sold and were so common that they were not deemed exceptional, though many people had a fondness for them. As it turned out, neither R. florida nor other Ricordea species disappeared and today are among the most desirable species, commanding very high prices for colorful morphs sold as single polyps at up to 20x the cost of an entire colonial aggregate of the corallimorpharians in the not distant past. Neither did live rock disappear, with both aquacultured live rock from Florida as well as many new wild-harvested sources becoming abundantly available. At the time, collectors pointed fingers at the few “bad players” that chipped off chunks of reef substrate, and asserted themselves as conservation-minded and unjustly punished for the new regulations. In fact, live rock prices have plummeted from the prices when Florida live rock was still legal.

Similarly, other knee-jerk false panics have happened with the potential introduction of several house and senate bills that did not pass; notably the Case Bill  (H.R. 4928), H.B. 3330 for bag limits in Hawai’i, S.B. 953 regarding breaking or damaging coral and live rock, and more recently H.R. 669, as mentioned in Rhyne et al. and throughout the US marine aquarium hobby populace regarding potential invasive species.  Even more current is the printed responses in CORAL magazine, as well as many other Internet forums, regarding the proposed listing of 82 species of stony corals for protection under the Endangered Species Act. At the recent CoP of CITES in Qatar, the parties failed to even protect bluefin tuna or precious red and pink corals (again) – arguably among the most valuable and threatened fisheries in existence. As I have already written, even in the unlikely event that all 82 species were listed, only a handful are ones that are important to the aquarium trade, and all of those are amendable to and available by captive propagation. The logistical ramifications at many levels are beyond the scope of this response, but suffice to say that most of the responses I have seen have been very poorly informed or unaware of the actual or future impacts to the trade, even if such listings were made. The same reactions occurred with Tridacnid clams, seahorses, Caulerpa algae, ad nauseum. There have also been closures of various global ornamental fisheries, including partial or temporary bans, and the US marine hobby reaction is almost comically predictable.

Despite all the actions taken or attempted, there are more countries, more species, and more availability than at any time from the beginnings of the modern reef aquarium hobby. It is ironic that surveys and statements from marine hobbyists, aquarium clubs, aquarium events, livestock vendors (retail and wholesale), Internet forums, and even collectors all profess or make it part of their mission to be ecologically concerned over the status of corals reefs, and to only support legal sustainable trade, casually referred to as “reef-friendly.” The use of curios is met with overwhelming disdain, and reef aquarium keepers almost without exception justify their private purchases of wild collected species with rationalizations that there exists an inherent interest in keeping them alive (though the continued rates of collection demand a concomitant high rate of mortality and replacement), that they probably live longer in captivity than in the wild (with no supporting data and anecdotally an exception rather than a rule), and that keeping aquariums is educational and promotes conservation (though most do not actively use their aquariums in any meaningful educational capacity, nor does wild collection promote conservation). Captive breeding and propagation is almost universally supported as preferable to wild harvest by all but the most callous or ignorant. But, when push comes to shove, any threat – real or perceived – that could limit the availability of any species to the trade is met with wild resistance.

The most predictable response is something to the effect of, “but in comparison with all the threats facing coral reefs, the aquarium trade is insignificant.” This may be true for many species, but at this point there is substantial evidence that the marine ornamental trade is responsible for significant damage to coral reefs, significant reductions of targeted populations, and in some cases extreme overfishing that has reduced populations to critical levels or even caused extirpations (local extinctions). Because of the number of species in trade, many data gaps or lack of current data, and frequently wide-ranging abundant species, it is unlikely that the aquarium trade is a threat to many, if not most, ornamental species. However, the authors express what is a pragmatic and generally held concern that reefs, globally, are under intense pressure from many stresses and threats. Caribbean reefs, in particular, are among the most degraded and there are few signs of hope. The reference to the “slippery slope to slime” is not unjustified or overly dramatic. Coral cover has precipitously declined along with reef fish populations, and now even structural complexity is in decline. Nowhere is this more evident than the Florida Keys, where coral cover is abysmal and reefs face episodic, regular acute, and chronic stresses, both natural and anthropogenic. If there was an area where ornamental collection would potentially impact reef function, it is in the Florida Keys. Naturally depauperate in species and functional redundancy in a marginal reef environment, every stress these reefs face – or what is left of them – is one too stress too many.

A testimony to the presage of the authors is the case of Condylactis gigantea, the only species in Rhyne et al. in which the authors specifically mention the current status of the fishery. The authors suggest from their data set that this anemone likely indicates a case of overfishing. Gasparini et al. (2005) used the same anemone as a case study of overfishing.  Important ecosystem services of this species include the harboring of cleaner shrimps. They state:

“Among the ornamental invertebrates found in Arraial do Cabo, the giant anemone Condylactis gigantea provides an example of the effects of over-exploitation. Its abundance before 1990 was about 1–2 individuals per 10– 15 m2 … They have lecithotrophic planktonic larvae with a presumably short life span in the plankton, and low fecundity (Jennison 1981; Chiappone et al. 2001).

This anemone seems to be unable to sustain even a very low level of exploitation due to Allee effects, i.e. individuals became too sparse to achieve significant fertilisation success. At the peak of harvesting (in the early 1990s), about 100 individuals of the giant anemone were taken a day from the Arraial do Cabo reefs. After the collapse of ornamental marine resources in Arraial do Cabo, most collectors migrated northwards to the Espırito Santo State, where about 600 individuals are currently harvested each week (Afonso Jorio, personal communication 2002). The last individual of C. gigantea in Arraial do Cabo was recorded about two years ago, despite continued, intense sampling effort (visual census sampling of approximately 6 h per week – CELF, personal observation 2000–2003). This may be the first documented case of local extinction of a relatively large marine organism due to over-exploitation by the ornamental trade in Brazil.”

The collection area for Brazil is roughly the same area as the Florida Keys, the number collected was a small fraction of the numbers coming from the Florida Keys, and they are now locally extinct. To further confirm the increasing rarity proposed by Rhyne et al., I went with a long-established Keys collector who was collecting C. gigantea for his customers. The collector made me promise not to reveal the location of the collection area because there weren’t many of these areas left. He then proceeded to wade through the area, systematically removing every anemone he came across until his order amount was met. He will return to this area the next time he needs to fill orders. This pattern of fishing is common in the ornamental trade with collectors removing every potential target organism in the area until they have enough. This type of fishing is extremely likely to result in overharvest and Allee effects, especially with species that may have patchy distributions where they occur in high densities.

In regards to the article itself, the results show a trend of increased landings and number of species over time that correlates well with the exports of other ornamental resource nations. The same concerns are voiced over and over in reports and papers from nearly every ornamental exporting source. The same trends are seen, with 10-20 species comprising the majority of collections, and numbers of collections increasing over time at a remarkably consistent rate. Valuation is similarly dynamic and in line with various management plans, quotas, demand and trends in the trade, and resource availability and condition. To me, two of the most troubling results found were the high numbers of curios still being collected, and the fact that essentially every visitor the Florida Keys can collect a personal amount of species that do not have specific restrictions against take. But, none of this is new. Previous reports and meetings have already gathered, announced, formalized, and made available the data presented in Rhyne et al. The authors have simply made it available as a concise and usable data source in a peer-reviewed publication. This is important since most of the data regarding the ornamental trades appears in the “grey” literature. This paper allows for a credible, accurate and citable current source instead of relying on speculative, out-of-date, or hard-to-obtain data in hard-to-obtain sources that are not widely read.

In commenting on the responses to Rhyne et al. published in CORAL, I was not surprised to see the predictable reaction, but was surprised by those whose comments were published and are who are well known and regarded in the industry. Moreover, the criticisms levied against Rhyne et al. are predictably hollow or were either intentional or unintentional misinterpretations of the statements made. Watson comments that many of the collected invertebrates are not from coral reefs, and then erroneously claims they have nothing at all to do with coral reefs. In fact, the shorelines, seagrass meadows, mangroves and reefs are all ecologically interconnected and are not functionally or geographically demarcated. That some of the collected invertebrates are not found on reef framework is irrelevant both in context and theory, and the authors never asserted in the paper that reefs of the Florida Keys would be directly affected; rather that loss of their ecosystem services could compromise the habitat and the sustainability of the populations. Rhyne et al. are very careful to couch their discussion points, admitting that there is insufficient data to make predictions and applauding the overall management of the areas. However, they also rightfully correlate their results and the nature of the fishery to what has been extremely well documented in similar or same fisheries elsewhere. In fact, they make no conclusions, as Watson states, except to voice a precautionary concern. Though Watson repeats his personal expertise, he offers no data and his principle complaints all seem to be misreading of the paper in light of a title that may suggest something more definitive than the paper itself. Furthermore, in the peer review process, the methods and the results are the primary components of a paper and to complain about aspects of the discussion (in this case, erroneously) is rather trivial. Any conclusions made are the interpretations of the authors. Mr. Watson could take the same data set and make his own conclusions that would be equally subject to debate. The point is, the results would still be the same.

Moe’s comments also express concern over the conclusions drawn by Rhyne et al. He writes that the authors implicate ornamental invertebrate fisheries to phase shifts on coral reefs. This was not a conclusion, but rather background information from the introduction. “Disturbingly, Caribbean reefs are among the most degraded worldwide [10], and collection of species on Caribbean reefs may lead to a further decline of reef health, and perhaps accelerate phase shift transitions from coral dominated to algal dominated reefs. This process has been termed ‘the slippery slope to slime’ and reversal has yet to be demonstrated on a large geographic scale [11,12]” Collection of species does not mean collection of the many invertebrates from Florida’s ornamental invertebrate fishery. It is well established that removal of herbivores and urchins by fishing or collection can and does have an effect in phase shifts, and there is a strong correlation between grazer abundance and the control of algae in maintaining coral dominated reefs. It is not a conclusion of the authors, but a well-established fact. His other comments are valid in light of limited data, but Rhyne et al. repeatedly make statements that assert that there is too little information to make predictions. Even the quote used by Moe is misinterpreted. The authors state that reduced landings MAY signal lower abundance rather than lessening demand. Not only are they not making a conclusion, but the potential they propose is supported by the data and from other literature. Furthermore, they were referring here explicitly to the C. gigantea fishery, not the total of invertebrate ornamental fisheries. Moe goes on to state, “What they should have said is “Hey, the fishery for ornamental invertebrates has recently greatly expanded in Florida, we (fishery managers) should take a good look at what’s happening and where it’s happening.” And in fact, that is precisely what they are stating; i.e. a precautionary approach and the need for more data given the numbers and nature of the fishery to make predictions. Again, the primary complaint stems back to the title and the literature is rife with catchy titles for scientific works.

Wittenrich’s comments are equally perplexing.  Claiming it offers little more than speculation, Rhyne et al. provides undisputed numbers as results from recorded data. These are not numbers that the authors arbitrarily concocted, so why he chooses to use “hardcore” in quotes to mock the paper’s data is a mystery. It is exactly that – hardcore data. He also wrongfully states that virtually all fisheries historically show increasing catch over time. This is patently untrue, and neglects completely a central tenet of fisheries, the CPUE. The declining catch numbers or size of global fisheries is so well documented as to be overwhelming. Wittenrich rightfully points out the nature of boom and bust populations, and suggests that the collected invertebrates have life-history traits that imply resilience in recruitment. Unfortunately, little is known of the life history traits of most marine ornamental invertebrates, and for at least some of those in the cited work, those traits work against the notion of sustainability. Snails in this fishery, in particular, can be very long-lived. Regardless of the ecological facts of real boom and bust species, it is also a fact that stressed ecosystems in general, may not be replenished by otherwise normal recruitment events. As “evidence” to counter the real data in the paper, Wittenrich offers anecdotal photos of Ken and Pete Kehoe. He goes on to state, “This should be the take home message of the paper: that the collection of such organisms should be cautioned in the absence of such data.” Again, this is precisely what the authors state, even if the title does not. Finally, Wittentich asks, “…how can you say harvest rates are too high?”  I don’t know, since the authors do not make this statement. Nor can it be stated that harvest rates are sustainable, as the commentors have claimed. If claims of sustainable collections are true more thorough data would confirm what they already claim to know or show that they are collecting well below the Maximum Sustainable Yield (MSY) be making more money while still maintaining a sustainable fishery. On the other hand, it could also show that the fishery is unsustainable. If users are certain that the latter is not the case and are committed to responsible collection as they claim to be, it is hard to justify such vehement resistance to Rhyne et al’s proposal to collect more data and institute management accordingly – in other words, implement the precautionary principle both the authors and the commentors suggest.

Forrest Young also weighed in with his response in CORAL in which he repeatedly misstates the authors, makes inaccurate statements about the paper and in other general statements, and uses typical arguments of fishers and collectors. Like the others, he offers no data to refute Rhyne et al. because it can’t be done. The results are never in question. What is in question is the actual impact of the removal of almost 9,000,000 organisms in one year from  chronically and acutely stressed ecosystems (that includes functionally interrelated habitats as well as the local habitat individually). The authors state,

“For most invertebrates, the reproductive age, growth rate, population density/distribution, and population connectivity remain elusive. Furthermore, it remains unknown whether cryptic populations or species exist, or whether these invertebrates have the ability to withstand rapid changes in fishery pressure. Despite a general trend of a minority of licenses reporting landings on any given species, frequently fished invertebrates have experienced 10-fold increases in landings since data have become available. Without these invertebrates, are important reef ecosystems crawling to their eventual collapse?…A growing body of evidence supports the idea that removing grazers decreases the resilience of a reef ecosystem, thereby reducing its ability to withstand a phase-shift from a coral to an algal-dominated state as well as decreasing the potential for subsequent phase-shift reversals…. To date, the data collected on imported aquarium ornamentals is sparse and only includes abundance and country of origin [33]. While there is taxonomic and life history stage data available at the time of import, there is no database information available for fisheries use. This data gap on international ornamental imports prevents predictable forecasting; in other words, the inevitable increased pressure on Florida fisheries is not quantifiable at this time…. Management challenges arise from ecosystem complexity and a paucity of baseline data, resources and support. Often, small fisheries grow beyond their intended capacity. In Florida, the once small ornamental fishery is now an invertebrate-dominated industry supplying five continents. As a result, the FLML may be positioned for collapse…. Considering ornamental invertebrates outside of the food industry is vital whether they swim or crawl, as collapse may be on the horizon for many of these overlooked species.”

I’m not sure how, where or why the responses to this article somehow miss the very obvious statements by Rhyne et al. (i.e the conclusions that seem to be at the heart of the critiques) that clearly show that the data available do not allow for predictions, that the potential for overharvest and resultant effects are possible and of concern (based on similar fisheries and papers too numerous to mention), that data gaps exist and should be filled to better make predictions, and caution is advised because such information is vital to prevent potential collapse.

Respondents also laud the management of the Florida Keys fishery and how collectors want more management. In a 2004 newspaper article, columnist David Flesher writes,

“About three miles off the coast of Islamorada, Ken Nedimyer glides along the ocean floor, trailing bubbles from his scuba gear and carrying two nets. Two yellow jawfish emerge from their sandy holes. He squirts them with an anesthetic called quinaldine and scoops them up…”This fishery is largely pursued in sensitive areas, particularly coral reef areas,” said Lee Schlesinger, spokesman for (the Florida Fish and Wildlife Conservation Commission)…

While no one knows whether the aquarium trade has caused any species to decline, divers and government officials say there appear to be fewer of these fish in Florida waters.

“My gut feeling is that some of these species numbers are down,” said Billy Causey, superintendent of the Florida Keys National Marine Sanctuary, who himself used to catch fish for the aquarium trade…

Formal stock assessments have not been done for any species captured for aquariums, which means that no one knows whether the current level of fishing is sustainable. This lack of information is precisely why many fishermen are pressing for restrictions.

“There’s no science on this fishery,” said Nedimyer, chairman of the Florida Marine Life Association, which represents people who catch the fish. “Nobody really has a clue how many fish are out there. There’s a handful of us trying to be managers, trying to help the state do the right thing.”

Thanks to Rhyne et al., there is now science to aid in the process of management of collection that does indeed occur on coral reef areas. There are already scores of management plans that began after, and have now surpassed, the management actions of the Florida Keys Sanctuary, including invertebrate stock assessments and even manuals to conduct marine ornamental stock assessments. In regard to Wittenrich’s comments, the ornamental biomass is known and reported in places as undeveloped as Tonga. In reading all available years of the minutes of the Florida Marine Life Workgroup Meetings, there are arguments over tiny amounts of substrate (reef) that should not be removed when collecting large bag limits of corallimorpharians, gorgonians and sponges – commonly available sponges that for 20 years are well known to never survive long term in aquaria and that are efficient water filterers for the reefs and associated habitats. These same sponges that are destined to die in aquaria, of all things, could help improve water quality of the Keys that was often blamed for decreasing numbers of collected species. At the same meeting, the group made anecdotal statements that admitted declines in C. gigantea seemed to be due to worsening environmental conditions (with no data) and not collection (for which there is data). A collector then stated that same speculation moments later as fact; “since the cause is environmental why should marine life fishers have to have more strict regulations?” The same collector was, “not impressed with current state of knowledge on CRTF (United States Coral Reef Task Force).” “They are making decisions based on ignorance,” he said regarding banning the use of quinaldine to catch fish, ignoring some evidence cited to the contrary, the exceptional credentials of the USCRTF, and that many of those same collectors state in their advertisements that they do not use chemicals to catch fish, yet hold permits for quinaldine use and collect fish with it. Butterflyfish and parrotfish are among the species collected, the former being a bioindicator of reef health, the latter a critical reef herbivore, and neither are particularly or at all suitable species for the marine ornamental trade. To paint the Florida ornamental fishers with a broad brush as being above reproach is as disingenuous as the comments about Rhyne et al.

In regards to comments in The New York Times article, I was interviewed for 45 minutes by the article’s author, Henry Fountain. He was genuinely trying to learn about – and make sense of – a very complex and foreign subject, and was making rather extraordinary efforts to speak with many knowledgeable people prior to writing the article. At no point was I aware that the article was pointed towards the findings of Rhyne et al., but rather towards acquiring a balanced view of the positive and negative aspects of the trade in marine ornamentals. Considering he had no prior knowledge of the trade, and the general nature of newspaper articles to misquote or misrepresent issues, I felt he did an exemplary job considering the subject, the nature of newspaper media, and the audience. Of course, mass media tends to be sensationalist, but it also draws attention to subjects that would otherwise leave subjects like the ornamental trade ignored and unknown to the general public. Several comments were made how articles like this will cause outcry. If it is so harmless, why wouldn’t we want the public to know all the details with transparency rather than the pervasive secrecy of this industry? If the trade is so harmless, where are the data and the peer-reviewed papers to show it? There are some reports from other source countries convincingly showing a negligible impact of some trade and, to be fair, there have been many newspaper articles extolling the accomplishments and wonder of the marine ornamental hobby. But, to pretend there is nothing harmful in the collection of animals for the marine ornamental trade is dismissive and patently untrue. It does not really matter to what degree the aquarium trade is contributing to reef decline because it is a stress to coral reefs and related habitats that acts synergistically with other stresses. I don’t believe any rational person would say that removing at least 8.8 million reported organisms, most of which provide valuable ecosystem services, many from a National Marine Sanctuary (in the US, no less) is beneficial or harmless. Unless, of course, it is the removal of the many well documented, non-native or invasive species introduced by the marine ornamental hobby, mostly in Florida waters.

A well-known and comparatively excellent wholesaler told me of a conversation he had with Marshall Meyers, the CEO of the Pet Industry Joint Advisory Council (PIJAC), where he said, “This trade is dirty. You know it and I know it and everyone knows it and its got to change or we are going to be out of business.” It’s time for the US aquarium trade and hobby to wake up to this fact, much as the EU has already done. There is significant pressure to close the trade, as well as pressure to maintain a sustainable trade. It does not help the perceptions of this trade when so many attempts to suggest positive changes or provide data to ensure sustainability and conserve coral reefs is met with revile, even moreso when the authors are friends of the trade and not enemies.

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