Troubled Waters: The Future of Global Fisheries

Scientists debating how to assess global fisheries are now including studies of long-term ecosystem effects and options for recovery efforts. But is it possible to both conserve and farm the sea?


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Troubled Waters: The Future of Global Fisheries Virginia Gewin I t is becoming increasingly apparent that the vast blue expanse of ocean-the last frontier-is not as inexhaustible as it once seemed. While we have yet to fully explore the reaches of the sea, technology has granted humans the ability to harvest its wealth. We can now fi sh anywhere, at any depth, for any species. Like the American frontier range's bison and wolf populations brought to the brink of extinction swordfi sh and sharks are the ocean's most pursued prizes. The disadvantages associated with the depth and dimensions of this open range, however, have long obscured the real consequences of fi shing. Indeed, scientists have the formidable challenge of assessing the status of species whose home covers over 75% of the earth.
Three recent highly publicized papers-a trifecta detailing troubled waters-call attention to overfi shing's contributions to the dramatic declines in global fi sheries. Delving into the past, Jeremy Jackson and colleagues (2001) combined local historic records with current estimates to detail the ecological impacts of overfi shing, Reg Watson and Daniel Pauly (2001) drew attention to distortions of global catches, and Ransom Myers and Boris Worm (2003) highlighted the depletion of the majority of the largest ocean predators. While some have valid criticisms of the assumptions and aggregation of historic data used to assess the global situation, few disagree with the overriding conclusion that humans have drastically altered not Copyright: © 2004 Virginia Gewin. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. only fi sh biodiversity, but, increasingly, the ocean itself.
Recent reports by the United Nation's Food and Agriculture Organization (FAO) which maintains the world's most complete global fi sheries database, appear to validate the conclusions of these studies. The most recent FAO report states that 28% of global stocks are signifi cantly depleted or overexploited, and 47% are either fully exploited or meet the target maximum sustainable yield. Only 24% of global stocks are either under-or moderately exploited. As the sea is increasingly harvested, many ecologists wonder how the ecosystem will continue to function (Jackson et al. 2001). Although economic and social considerations often supercede scientifi c assessments, science will continuously be called upon to deliver management options that will straddle the needs for conservation and production, even in areas where there is only subsistence fi shing (Box 1). As scientists debate the details of global fi sheries assessment, they are also including studies of the longterm ecosystem effects and options for recovery efforts. Like was done on the open range, shall we conserve or farm the sea-or both?

Catches, Collapses, and Controversies
The FAO began keeping fi sheries records in 1950. Unfortunately, an enormous amount of data comes directly from each country's fi shing industry, which is often biased as a result of unreported discarding, illegal fi shing, and the misreporting of harvests. For example, mid-level Chinese government offi cials seeking promotions systematically enhanced China's fi sheries numbers in recent years-which infl ated and skewed international catch rates.
The FAO data show that catches, excluding a recent surge in anchoveta and China's suspect numbers, reached a peak of 80 million metric tons in the late 1980s and have since begun to decline. Regional studies validate these trends. "Most of the line fi sh around the coast of South Africa are depleted to 5%-15% of pristine levels," says George Branch, a marine biologist from the University of Cape Town (Cape Town, South Africa). Meryl Williams, Director General of WorldFish in Penang, Malaysia, notes that the Asia-specifi c database called TrawlBase (www.worldfi shcenter. org/trawl/) confi rms that the region's commercial species have been depleted to 10%-30% of what they were 30-40 years ago.
Obtaining accurate information on highly migratory species is challenging, to say the least. It is not hard to imagine that data quality is the biggest disadvantage to any scientifi c assessment. Of the 50 managed stocks in the northeast Atlantic Oceanincluding invertebrates, sport fi shes, and major commercial fi nfi sh-data are kept on only one-fi fth of the species. There are 250 fi sh species in the region, but only 55 species are of commercial interest and merit inquiry. "We know next to nothing about noncommercially fi shed species," notes Jeff Hutchings, a conservation biologist at Dalhousie University (Halifax, Nova Scotia, Canada). And that is where fi sheries have adequate access to current monitoring programs. "With the recent expansion of the Taiwanese and Chinese fl eets, we don't have the kind of sampling programs needed for those kinds of fi sheries," says Rick Deriso, a fi sheries scientist with the Inter-American Tropical Tuna Commission (IATTC) (La Jolla, California, United States).
Couple these inadequacies with previously unknown bycatch rates (i.e., the fi sh caught in addition to the target catch) and illegal catches, and it is easy to see that the task is formidable. The FAO estimates that roughly one-quarter of the marine commercial catch destined for human consumptionsome 18-40 million metric tons of fi sh-is thrown back in the sea, a harvested catch that is never utilized or counted. It is estimated that the illegal, unreported, and unregulated (IUU) fi sheries surpass allowed fi shing quotas by 300%. IUU fi shers operate in areas where fi shing is not permitted, use banned technologies or outlawed net types, or underreport catches. "The IUU fi shery for Patagonian toothfi sh expanded rapidly in the mid-1990s, likely on the order of 20-30 vessels," says Andrew Constable, an ecological modeler at the Australian Antarctic Division (Kingston, Australia), who also works with the Scientifi c Committee of the Commission for the Conservation of Antarctic Marine Living Resources (Hobart, Australia). "These rates of IUU fi shing could reduce stocks to threshold levels in some areas in two to fi ve years," he adds.
Often overlooked is the inescapable fact that even sustainable harvest rates reduce fi sh populations quickly. "If the goal is a productive fi shery, we're automatically talking about up to a 70% decline in population across the board," says Deriso. The FAO's Chief of Marine Resource Services, Jorge Csirke, states that "from a stock point of view, there is no way to preserve integrity

Box 1. Fisheries Management in Developing Countries
While industrial-scale fi shing is a growing concern to fi sheries biologists, the management of subsistence fi shing in developing countries is equally complex. Indonesia alone has 1.3 million fi shers. Given the lack of alternative economic options for subsistence fi shers, it is much more diffi cult to reduce fi shing because it meets immediate food and resource needs. Local scientists, often lacking in resources, have a much more diffi cult time assessing the effects and offering advice to governmental fi sheries regulators, who have limited political infl uence. Kenyan researcher Tim McClanahan notes that a main problem is a lack of coordination and respect between traditional and national programs of management. Therefore, he focuses on the fi shing gear used. By reconciling the impact of certain fi shing gear with traditional knowledge, McClanahan has developed a basis for suggested restrictions deemed acceptable to the local community.
Bottom trawling not only removes [targeted] fi sh from seafl oor habitats, but compromises the ability of other fi sh to survive. of wild stocks and exploit them at the same time." Indeed, the United States' National Marine Fisheries Service (NMFS) considers optimal harvest rates to be between 40%-60% of virgin levels. But once fi sh populations dip below the 10%-20% mark, declines are of serious concern.
Atlantic cod in Canadian waters suffered a total population collapse and are now on Canada's endangered species list (Figure 1). From 2 billion breeding individuals in the 1960s, Atlantic cod populations have declined by almost 90%, according to Hutchings. While advisors called attention to declining cod stocks, Constable notes that by the time a signifi cant declining trend has been detected by traditional catch assessments, stocks are likely to be in poor shape, if not already depleted.
Given the task of compiling data on only the economically important species, fi sheries biologists developed a single-species management approach in the 1960s, which assumed that fi sheries affect each species in isolation. This approach, although now rife with problems, served the community and the politicians well during the decades of abundant resources. "They brought the approach of single-species management to near-perfection," says Boris Worm, a marine ecologist at the Institute for Marine Science in Kiel, Germany. A growing discontent with the model, in addition to greater awareness of ecological interactions, however, prompted Worm and his Dalhousie University colleague Ransom Myers to question the sustainability of the single-species approach. Attempting a comprehensive assessment, their widely cited recent paper (Myers and Worm 2003) indicated that the global ocean has lost more than 90% of large predatory fi shes, such as marlin, sharks, and rays.
However, this new approach to assess fi sh stocks is not without its critics. Fisheries biologists point out that the nuances of management contained in fi sheries data-such as altered fi sher behavior, the variable "catchability" of individual species, and altered gear use-were discounted in the Myers and Worm (2003) assessment and led to misinterpretations for some species, notably tropical tunas ( Figure  2). A number of tuna biologists have expressed concern that these omissions have left the mistaken impression that all tuna species are among the list of declining predators (Hampton et al 2003). Worm acknowledges that his approach can be improved, but says, "The whole point of our paper was to aggregate species to communities to see what the overall ecosystem is doing."

Ecosystem Sustainability
Despite the controversy, most agree that the large predators, particularly sharks, skates, rays, and marlin, are in the most dire straits. Unlike other lower-trophic order species, the wholesale removal of top predators has enormous effects on the rest of the ecosystem. One consequence is that overall reproduction rates can potentially suffer. Fish size, gender, and age at maturity have a substantial impact on individual species' reproduction rates. Since larger fi sh are the most susceptible to fi shing, the population's age structure can shift as individuals, particularly females, are fi shed out. For example, a 23-inch (59-cm) female vermilion rockfi sh can produce 17 times the young of a 14inch (36-cm) fi sh. Given uncertainties with population dynamics, the fact that basic biological data are missing makes the job even harder. While knowledge of these components is still quite spotty, tuna inventories, for example, have started collecting gender data on catches.
Daniel Pauly, a fi sheries biologist at the University of Vancouver (Vancouver, British Columbia, Canada), has shown that increased fi shing has caused the industry to "fi sh down the food web," or systematically move to lower trophic levels over time as higher ones were depleted (Pauly et al. 1998). The impact to ecosystems is only beginning to be uncovered. "If you fi sh out an abundant predator, the species that it was eating or competing with will increase," says Worm. "The problem is that the ecosystem may change in such a way that recovery is inhibited because a species niche space is taken or altered." Fisheries science has taken steps to increase the quality of data in recent years. "Traditional fi shery models assumed that a fi shery was a homogenous thing-like bacteria in a bottle-rather than a spatially diverse system," says Pierre Kleiber, a fi sheries biologist with the Pacifi c Islands Fisheries Science Center of the NMFS (Honolulu, Hawaii, United States). He adds that recent work accounts for spatial diversity. In addition, fi sheries are now dealing with the inherent uncertainty of their work and are factoring that into models and decisionmaking. "Uncertainty didn't used to be dealt with at all in formulating fi shery management advice," confi rms Keith Sainsbury, a marine ecologist with the Commonwealth Scientifi c and Industrial Research Organisation (CSIRO) (Clayton, South Victoria, Australia), adding that its absence gave rise to an awful lot of troubles. "Traditional models tended to assume perfect data with no holes in it," says DOI: 10.1371/journal.pbio.0020113.g001 "The big mistake is suggesting that you can manage fi sh stocks.… We can only manage human activity." Kleiber. "Now we've tried to craft a model to fi t the realities of missing data." As well as incorporating spatial diversity and uncertainty, researchers are beginning to comprehend the ecological damage caused by different types of fi shing gear. Indeed, trawling the bottom of the seafl oor for groundfi sh can destroy a half-acre footprint of habitat ( Figure 3). Detailed reports document that, depending on the habitat's stability, bottom trawling can not only remove fi sh from seafl oor habitats, but alter bottom relief such that it compromises the ability of other fi sh to survive (NRC, 1002). In Australia, for example, lingcod rely on undisturbed bottom relief to lay their eggs, while other groundfi sh species depend on complex seafl oor habitats for the majority of their food.
"Science is getting more realistic, but it is getting more diffi cult," says Branch. Ecological models are far more complex than traditional fi sheries models, says Csirke, adding that more model variables make it more diffi cult to apply to fi sheries, an industry whose focus is, understandably, not conservation. Despite its incorporation into national fi sheries policies, ecosystem-based management remains a loosely defi ned term. It is not a well-defi ned concept because it is not possible to optimize every species, says Deriso.
An additional concern to scientists is that of biomass resilience in the face of environmental changes. Francisco Chavez, a biologist with the Monterey Bay Aquarium Research Institute (Moss Landing, California, United States), recently demonstrated that over a 25year period, warmer and cooler Pacifi c waters tilt the distribution of anchoveta versus sardines, both open-ocean dwellers (Chavez et al. 2003). Indeed, El Niño infl uenced the crash of the heavily fi shed Peruvian anchoveta industry in the late 1970s. These examples illustrate how susceptible fi sheries are to environmental fl uctuations. When the biomass of a population is reduced, it is much more sensitive to environmental change. We do not know how environmental fl uctuations like these will affect the natural production of young fi sh, says Kleiber, expressing the concern that without a better understanding of climate, fi sheries scientists end up trying to estimate moving targets.
In the end, many scientists have their doubts about the infl uence of science on decision-making. "My personal view is that it's naïve to think that modifying and improving models will necessarily lead to improved natural resource management," says Simon Jennings, a fi sheries biologist with the United Kingdom's Centre for Environment, Fisheries and Aquaculture Science in Lowestoft. Indeed, the International Council for the Exploration of the Seas (Copenhagen, Denmark) recently recommended a total ban on North Sea and Irish Sea cod stocks, based on single-species assessment. Although the more intensive ecosystem-based models could not have produced a more stringent recommendation, politicians allowed harvests at roughly half of last year's catch.

To Conserve or to Farm?
While lowering fi sheries' effort seems the most logical approach to the recovery of depleted fi sheries, social DOI: 10.1371/journal.pbio.0020113.g002

Box 2. The Establishment of High Profi le MPAs
While MPAs are heavily touted as one of the best management tools to address both conservation and fi sheries management, few have been enacted. In 2001, following a strong mandate by the Australian Minister to the Environment and overwhelming political will, the Great Barrier Reef Marine Park Authority (GBRMPA) in Australia established a network of marine protected, or no-take, areas as an ecosystem-based management approach.
In setting up the reserve networks, scientists determined the most effective areas to protect biodiversity with little impact to productivity. "We tried to avoid peak use areas, while protecting at least one-third of each bioregion and minimizing the impact to users of the Great Barrier Reef Park," says Phil Cadwallader, Director of Fisheries at the GBRMPA.
Off the coast of California, the Channel Islands network of marine reserves, established in April 2003, consists of 13 areas designed to protect biodiversity and critical habitat for breeding fi sh and to maintain biodiversity. The area has suffered serious declines of red snapper, angel sharks, and abalone, once plentiful off the California coast, over the past decade. Scientists designed the network to protect those productive habitats that would help ensure that larval dispersal was maintained between the individual reserves. Totaling 132 nautical square miles (342 nautical square kilometers), 11 of the areas are no-take reservesallowing no fi shing or harvest of any kind. and economic concerns often stymie political action. Yet demand for seafood continues. Therefore, scientists also are investigating both conservation and alternative production options.
Given the social, economic, and political problems associated with that, managers have often used closures to help a hard-hit species recover. In many cases, however, the recovery time for exploited species is longer than once thought (Hutchings 2000). "Based on the available information, it is not unusual for fi sh populations to show no or little recovery even after 15 years," says Hutchings. "All else being equal, we predict the earlier the age of maturity, the faster the rate of recovery," he adds. And that depends on environmental conditions as well. "In the case of Antarctic species, some overexploited populations remain at less than 5% pre-exploitation abundance after 30 years," says Constable.
One management strategy to recover species is to create marine protected areas (MPAs), zones that restrict all removal of marine life (Box 2). A number of marine ecologists are staunch supporters of MPAs for both conservation and fi shery's recovery. What looked like sustainability in the past were fi sheries out of our reach-naturally protected areas-says Pauly, adding that our increasing ability to harvest fi sheries necessitates the creation of MPAs now. In theory, these areas are refugia for fi shes to reproduce, spilling over not only healthy adults but also potentially transporting thousands of viable young-seeding surrounding waters. To date, less than 1% of the ocean's area is protected, which hinders the ability to conclusively determine if spillover rates have the predicted impact on fi shery's recovery.
A review of 89 studies of MPAs by Ben Halpern, a student at the University of California, Santa Barbara (Santa Barbara, California, United States), demonstrated that the average number of fi sh inside a reserve increases between 60%-and 150% (Halpern 2003). In addition, 59% of the sites had increased diversity. While the numbers inside the reserves look good, the crucial condition of larval spillover has yet to be proven. Most scientists involved in the debate agree that MPAs should be one component in an overall management scheme, but worry that until the crucial element of fi shing effort is resolved, MPAs may just displace the vast industrial fl eets.
In terms of simply producing fi sh for global food needs, aquaculture (also known as fi sh farming) is another, increasingly popular, option. In 2001, the European Union produced 17% of total fi shery's production via aquaculture. These numbers are projected to steadily increase, but some question whether aquaculture would be suffi cient to supply what has been lost by overexploited fi sheries.
Concentrated in coastal areas, aquaculture has aroused numerous concerns. Indeed, in developed countries, most operations grow carnivorous fi sh, which necessitates growing fi sh to feed fi sh. While the process has become more effi cient in recent years, due in part to a growing reliance on vegetarian diets, it still takes about 3 pounds (1.36 kg) of fi sh to create 2.2 pounds (1 kg) of desirable meat (Aldhous 2004). Yet, the total catch of food fi sh continues to grow, as do concerns about nutrient runoff and estuary pollution resulting from aquaculture. Increasingly, coastal residents often complain about the aesthetics of such activities, and there is also new research that indicates that farm-raised fi sh harbor more cancercausing pollutants than wild species (Hites et al. 2004).
To alleviate many of these concerns, open-ocean aquaculture is now being considered. Indeed, the NMFS is set to propose a Code of Conduct for Offshore Aquaculture, which would open up the 200-mile (322-km) United States Exclusive Economic Zone to net pens seaward of coastal state boundaries and authorities. The Sea Grant program in conjunction with interested business, is also currently assessing the carrying capacity of openwater pens as well as their potential environmental impact. Given increased industrial interest and unchanging demand for seafood, many think farming the sea may be around the corner.
Undoubtedly, scientifi c effort will continue to inform both conservationists and industry about fi sheries' capacity and potential recovery options. As attitudes towards fi sheries continue to change, increased understanding of the ecological underpinnings should help strike a more informed balance between fi sheries' conservation and production. "The big mistake is suggesting that you can manage fi sh stocks," says Niels Daan, a biologist with the Netherlands Institute for Fisheries Research (IJmuiden, The Netherlands). "In my opinion, we can only manage human activity."