Keynote Rebuilding depleted fish stocks: the good, the bad, and, mostly, the ugly

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1 1830 Keynote Rebuilding depleted fish stocks: the good, the bad, and, mostly, the ugly Steven A. Murawski Murawski, S. A Rebuilding depleted fish stocks: the good, the bad, and, mostly, the ugly. ICES Journal of Marine Science, 67: Recovery of depleted fish populations has become an important theme in national and international negotiations and commitments regarding sustainability. Although up to 63% of fish stocks worldwide may be in need of rebuilding, only 1% are currently classified as rebuilding, and fewer yet have been rebuilt. Recent history in stock recovery provides a rich source of examples of rebuilding plans across a spectrum of execution ( good, bad, ugly, and in progress ). Of 24 depleted stocks with formal plans that successfully reduced the fishing mortality, all but one exhibited signs of recovery. The median instantaneous annual rate of biomass recovery (0.16) was similar to the rate of depletion (20.14) experienced, but stocks with more vulnerable life histories recovered substantially slower than they had been depleted. Most successful rebuilding programmes have incorporated substantial, measurable reductions in fishing mortality at the onset, rather than relying on incremental small reductions over time. A particularly vexing issue is the differential pace of recovery among relatively productive and unproductive components of mixed-species fisheries. Rebuilding the majority of stocks classified worldwide as overfished will take a more effective, consistent, and politically supported stock-recovery paradigm, if society is eventually to meet its articulated sustainability goals for global fisheries. Keywords: fishery depletion, fishery rebuilding plans, overfishing definitions, recovery plans, stock recovery, sustainable fisheries. Received 11 February 2010; accepted 22 June 2010; advance access publication 15 October S. A. Murawski: National Marine Fisheries Service, 1315 East West Highway, SSMC , Silver Spring, MD 20910, USA; tel: ; fax: ; steve.murawski@noaa.gov Introduction Worldwide, wild fish catches are either stable or declining slightly, and the number of stocks classified as overfished or rebuilding is substantial (Garcia and Grainger, 2005; FAO, 2009). A precise account for the number of stocks in need of rebuilding is difficult, because of the skewed distribution of formal stock assessments to those fisheries and regions having adequate information and capacity for assessment, but estimates range from 28% (FAO, 2009) to as much as 63% (Worm et al., 2009). Given the tremendous worldwide focus on stock depletion and achieving sustainability, it is telling that the number of examples of successful rebuilding programmes is relatively modest globally (Caddy and Agnew, 2003, 2004; Rosenberg et al., 2006; Wiedenmann and Mangel, 2006; Wakeford et al., 2007; Mora et al., 2009; Worm et al., 2009). Explanations for the modest success in rebuilding stocks to sustainable levels include the lack of political will to make management decisions that result in substantial short-term social and economic effects to restore the long-term productivity of stocks (Rosenberg et al., 2006; Sissenwine and Symes, 2007; OECD, 2010). For some situations where recovery plans have been implemented, the slower-than-anticipated pace of recovery has been attributed variously to depensatory population dynamics at low stock sizes (Shelton and Healey, 1999), changing (poorer) environmental conditions resulting in declining survival of earlylife stages, ecological changes (including niche substitution and mixed-species effects), and science that is either lacking altogether (such as in many parts of the developing world) or scientific projections of stock rebuilding that were overly optimistic. The goals of the UNCOVER (understanding the mechanisms of stock recovery) symposium and the EC contract from which it originated were to examine carefully the record of stock recovery and lack thereof and to articulate best practices in achieving success in rebuilding, and ultimately in making fisheries sustainable. This is, of course, a wider debate than just dealing with population dynamics and ecosystem science, because many of the elements proposed for effective rebuilding programmes involve other attributes of the management system. These attributes include incentives, disincentives (i.e. enforcement), accountability measures to achieve management benchmarks, setting of risk tolerances, and long-term planning to cope with the situation once depleted stocks are rebuilt to prevent a continuing cycle of boom and bust (Caddy and Agnew, 2003, 2004; Powers, 2003; Rosenberg et al., 2006; Sissenwine and Symes, 2007; Wakeford et al., 2007). I will focus on some pivotal issues constraining wider success in stock rebuilding from a global perspective. A taxonomy Several excellent and thorough reviews of worldwide recovery plans have been conducted already (Caddy and Agnew, 2003, 2004; Wiedenmann and Mangel, 2006; Rosenberg et al., 2006; and the UNCOVER review by Wakeford et al., 2007). Additionally, summary papers evaluating the potential # United States Government, Department of Commerce, National Oceanic and Atmospheric Administration For Permissions, please journals.permissions@oxfordjournals.org

2 Rebuilding depleted fish stocks 1831 reversibility of stock declines and specifics regarding individual fisheries provide a rich source of case histories across a spectrum of execution effectiveness (Hutchings and Myers, 1994, 1995; Mace, 1994, 2004; Powers, 1996, 2003; Myers et al., 1999; Shelton and Healey, 1999; Hutchings and Reynolds, 2004; Kell et al., 2006; Kelly et al., 2006; Shelton et al., 2006; Baker et al., 2009; OECD, 2010). Based on these evaluations and a large body of stock-assessment information available, we can generally classify rebuilding plans into those considered to have been successful in meeting their stated objectives (the good ), those that remain essentially paper plans, not achieving their stated objectives for reducing fishing mortality and biomass recovery (the bad ), and plans that have been partly to completely unsuccessful, despite major management interventions (the ugly ). Successful rebuilding plans share critical attributes of having well-defined objectives, to be reached over finite time-scales, and of being determined in an open and transparent process and contributing to support by the stakeholders and the public, as well as by political leadership (Powers, 2003; Mora et al., 2009). They also incorporate credible, consistent, and transparent scientific monitoring of progress, with simple and easily understood metrics of status and success (biomass and fishing mortality thresholds and limits; Mace, 1994). In some cases, rebuilding has been automatically triggered by science-based rules that were predefined in plans when stocks reached some reference point necessitating action (Caddy and Agnew, 2004; NOAA, 2007). Many incorporate fishers into the science process in cooperative research activities and routine monitoring surveys conducted aboard fishing vessels (NRC, 2004). Most successful rebuilding programmes incorporate substantial, measurable reductions in fishing mortality at the onset (Brodziak et al., 2008), rather than relying on incremental small reductions over time, which can be compensated for by technology creep. In contrast, bad recovery plans allow stocks to continue to decline after they have been formally implemented. Unsuccessful plans often resulted in forgoing hard choices by favouring larger reductions in fishing mortality rates later in rebuilding schedules. They are often associated with systemic underreporting of catches (Fromentin and Powers, 2005; MacKenzie et al., 2009) and excessive discarding and highgrading. In some cases, imprecise or biased science contributes to inadvertent overfishing, when managers seek to establish total allowable catches consistent with reference levels that prove wrong (Mohn, 1999). Often, there is too little precaution in the face of management implementation or stock-assessment uncertainty (Kelly et al., 2006). In extreme cases, the lack of progress in achieving stated rebuilding goals may result in calls for the use of non-fishery control statutes, such as protected-resource agreements, additional legislation, and international trade-control agreements (Gronewold, 2009). By far, the most enigmatic rebuilding programmes are those for which management interventions have happened (such as major reductions in fishing effort and which therefore would be expected to represent the good ), but for which the stocks have either not responded or are tracking up at rates much lower than projected at the onset (Caddy and Agnew, 2003, 2004). Many explanations have been offered for the delayed or non-existent recovery of these stocks, including depensatory natural mortality rates, conspiratorial climate effects, loss of evolutionary resilience, multispecies effects, and the inability to recover quickly complex life cycles determined by species co-evolution, migration patterns, and demography (Collie and Spencer, 1993; Spencer and Collie, 1997; Shelton and Healey, 1999; Bundy, 2001). The cases of rebuilding complexes of species caught in a mixed fishery (mixedspecies complexes) offer a particularly difficult management challenge when recovery is sought following systemic or sequential depletion of these resources. Rebuilding plans may be successful for more productive components of the mixed-species complex, but this poses the dilemma of allowing access to rebuilding stocks and simultaneously maintaining low fishing mortality rates on less productive ones (Brodziak et al., 2008). Rebuilding all the components of a mixed fishery should improve its overall resilience to fishing and other factors, but the transition to fully sustainable fishing may come at the cost of considerable foregone catches of the most productive component stocks. This is essentially the mirror image of sequential depletion sequential recovery. These are clearly ugly problems for fishers, managers, and scientists, requiring creative and innovative solutions involving spatial management, bycatch engineering, and, in some cases, balancing short- and long-term social and economic tradeoffs. Impediments to success Although every case of depleted stocks offers unique challenges to rebuilding, there are a number of recurring, thematic impediments to universal success (Caddy and Agnew, 2004; Beddington et al., 2007). These include those listed in the subsections below. Defining consistent reference points A basic issue to the success of any rebuilding plan is a consistent definition of what constitutes a stock in need of rebuilding and subsequently what constitutes a rebuilt stock, preferably before the plan is implemented. Management institutions differ greatly in how they treat situations when a stock exceeds some limit reference points (Caddy and Mahon, 1995). Triggering of a rebuilding plan is either done by consensus, prearrangement given stockstatus determination, or legislative mandate. Importantly, then, what is the basis for defining biological reference points for sustainable fisheries and how does their definition affect the stockrebuilding process? The different approaches to determining biological reference points (Mace, 1994) generally fall into three classes: (i) notional or directional advice on stock status (often called traffic light approaches); (ii) hybrid advice that uses quantitative, heuristically determined ( precautionary ) reference points for biomass (B) and fishing mortality rate (F); and (iii) maximum sustainable yield (MSY)-type advice that links F and B through surplus-production models or stock recruitment dynamics. The use of traffic light type advice (Caddy and Agnew, 2004), although requiring less scientific rigour, presents difficult challenges for managers. The boundaries between zones where categorical discrimination in directional management advice is given are often ill-defined. Therefore, one category of abundance may require directed-fishery closure vs. limited fishing of the target species, with little accompanying information on the biological or socio-economic consequences of such advice, or the ability to discern a difference. Precautionary approach (pa) reference points, such as used for advice by ICES and implemented by the European Commission and other management bodies (Cadrin and Pastoors, 2008), offer a flexible approach to status determination, as informed by time-series of spawning-stock biomass (SSB) and recruitment data (Figure 1, top panel). B lim (the SSB below which recruitment is impaired) is generally quantified by the inspection of

3 1832 S. A. Murawski Figure 1. Definitions of management reference points for North Sea cod under two management paradigms (a) as pertaining to ICES management advice (ICES, 2009): red, outside safe biological limits; yellow, remedial advice to precautionary level; green, sustainable exploitation; and (b) theoretical single-species reference points (for illustration only) as if the stock were regulated under US legislation (NOAA, 2007): red, no fishery; yellow, rebuilding plan required; green, sustainable exploitation. For further explanation, see the text. recruitment time-series for obvious points where the probability of good recruitment diminishes significantly and therefore threatens short-term stock collapse. Fishing above F lim constitutes overfishing, which means that even if the SSB is adequate, continued fishing at this level is expected to reduce the SSB below B lim (and therefore to impair recruitment) in the long term. The additional pa reference points (B pa and F pa ) are chosen to take uncertainty of both limits and the estimate of the current status into account, but the risks implied are fairly arbitrary. Importantly, B and F are independently determined; therefore, there is no specific relationship between the attainment of the specified F and the expected long-term average biomass (i.e. B and F are decoupled). In the United States, the relationship among the MSY-based F and B targets and limits are linked explicitly in a management scheme that not only prescribes the circumstances when rebuilding plans are required (i.e. when the stock falls below 0.5 B MSY ), but also the time-frames over which rebuilding must occur (Gabriel and Mace, 1999). In this case, it is critical to select the B target ( B MSY ) to define the lowest B where the stock can achieve B MSY within the prescribed time-frame (NOAA, 2007). Under the MSY reference point paradigm, the direct link between targets and limits (even when these are represented by proxies) allows forecasting of the rebuilding time-frames (Overholtz et al., 1986; Collie and Spencer, 1993; Kell et al., 2006; Brodziak et al., 2008). How would management reference points differ under the pa and MSY management systems for the same stocks? To visualize this, I plotted the pa and limit reference points, and the current F target for North Sea cod (Figure 1a, ICES, 2009). Additionally, the domain of MSY-based reference points for the same stock using the rules as implemented in the United States is given in Figure 1b. The value of F MAX is assumed to be F MSY (0.25), and the SSB MSY was calculated as the median of recruitment from 1998 to 2008 (107 million age-1 fish), multiplied by the SSB/R at F MSY (2.1 kg per recruitment or t SSB; ICES, 2009). The limit reference point for biomass was set at 1/2 SSB MSY ; the management target was set at 75% of F MSY, accounting for uncertainty. These values are for illustrative purposes only and do not constitute proposed reference points. They illustrate the potential of substantially different rebuilding reference points, depending on the paradigm, and therefore more generally emphasize that there may be confusion about what constitutes a rebuilt or recovered stock. These three management frameworks describe a hierarchy of regulatory approaches for achieving sustainable management goals and, by inference, for determining when rebuilding efforts must be triggered. They do so with increasing levels of prescription and less freedom to negotiate the parameters of a rebuilding strategy. The adoption of predetermined rebuilding targets and associated time-frames in some jurisdictions (NOAA, 2007) is a direct consequence of recurrent failures of management agencies to take effective conservation-orientated decisions to avoid or mitigate stock collapses. In retrospect, because of the uncertainty in the advice (in recruitment scenarios) at the time, these agencies could not act in favour of resource conservation and stock rebuilding given social, economic, or philosophical concerns. Moving across the hierarchy, however, implies increasing degrees of certainty about stock status and in medium-term projections, and a need for greater science support. Importantly, biomass targets for chronically overfished stocks may be outside the observed range of stock sizes, which implies uncertainty regarding the capacity of the stock to attain and the ecosystem to support those targets (Brodziak et al., 2008). Although the MSY framework specifies that stocks are rebuilt when biomass targets are achieved, new information collected during a recovery programme may necessitate re-evaluation of long-term targets (either up or down). The precautionary and traffic light frameworks do not prescribe precise ending points for rebuilding plans and therefore may support a more adaptive approach, though without providing consistency between theoretically derived reference points and empirical performance. A further difficulty in all three approaches is that if even partly successful, rebuilding plans will be subject to criticism during their course when re-evaluations conclude that the goalposts should be moved up or down to be consistent with emerging information about stock productivity. As noted by Powers (2003), initial (partial) successes in stock rebuilding will be accompanied by calls to increase catches, and managers will be tempted to dissipate these early successes at the cost of completing the programme (particularly if the biomass target lies above any documented maximum). Consistency in decision-making by specifying a priori how reference points will be adaptively re-evaluated is a clear priority, if rebuilding plans are to be more generally successful. The lack of consistency in setting rebuilding targets is a particularly acute problem in the management of internationally shared

4 Rebuilding depleted fish stocks 1833 resources (Munro et al., 2004). Reconciling different domestic approaches among countries or authorities in itself requires a framework agreement that allows their blending, but any compromises may result in fishers perceiving unequal treatment under domestically imposed vs. internationally agreed restrictions. Consistent standards for defining sustainable targets, recovery goals, and triggers for adopting rebuilding plans and, in fact, criteria for when a stock has been rebuilt are needed before more universal stock rebuilding and recovery can be achieved, but this as yet remains an elusive goal (Mora et al., 2009). Using adaptive management correctly Chronically overfished stocks present a particularly difficult problem, because in some circumstances this may involve setting biomass targets that may have never been achieved within the documented history of the stock (Brodziak et al., 2008). There is usually much speculation and little credibility among managers and fishers regarding the achievability of rather theoretical rebuilding endpoints, particularly if the target lies far beyond the current stock size. In those cases, formal adaptive-management approaches embedded in the system may help to guide the achievement of feasible targets, but considering that shifting baselines may result in too narrow a view of what biomass the stocks may actually achieve (Brodziak et al., 2008). Measures might be adapted gradually based on the stochastic stock projections over the short and medium term in combination with continuing monitoring of stock development. To avoid the temptation to short-stop full stock recovery when there is a biomass increase, the advice under varying combinations of stock performance and achievement of F targets must be prespecified (i.e. which measures apply under different combinations relative to the forecast pace of rebuilding). If the advice is not pre-negotiated, the debate about constraining the fishery for a questionable long-term benefit of possibly unattainable stock sizes at the cost of certain short-term economic and social consequences will continue, particularly if rebuilding Fs are lower than the F target for rebuilt stocks. More effective use of formal adaptive-management programmes (adaptation through learning) requires simulation testing of the probability that correct decisions can be made and it certainly requires implementation of monitoring programmes with relatively high signal-to-noise characteristics. Mixed-species fishery problems The recovery of mixed-species assemblages represents one of the most persistent and widespread problems. Mixed fisheries have often through excessive harvesting depleted true admixtures of species or have sequentially depleted the more valuable components to end with the less valuable ones. Even where effective effort control has been implemented, the differential pace of stock recovery among the more and less productive components of the species mix creates the potential for relatively minor stock components to control the access of the fishery to the larger and more productive stocks (Vinther et al., 2004; Rätz et al., 2007; Brodziak et al., 2008; Mackinson et al., 2009). Applying recovery plans to let the less productive components rebuild may leave already recovered components underexploited. Hence, the functional recovery time for a mix of species exploited in a mixed fishery may be much longer than for some of the individual species. In the best of cases, this issue is transitional; in the worst case, a depleted unproductive stock may restrict access for a very long period, or even an indeterminate period, if a fishery-induced regime change has happened. Under such circumstances, the effect may be to undermine the validity of the recovery programme in the eyes of the stakeholders. Two major approaches to mitigation of these problems are gear restrictions to change the relative catchability of the different species and using time/area restrictions to take advantage of seasonal separation of stocks. Catch-share programmes, coupled with information sharing among harvesters, can create an incentive for fishers to make these two approaches work in practice. Greater acknowledgement of fishery-associated issues, as well as stock-related issues in recovery planning, is essential, and more attention should be paid to potential mitigation strategies at the outset. Lack of capacity for sustainable management Even in the developed world, the capacity to produce routine stock assessments and to evaluate the success of management measures remains limited (Worm et al., 2009). This has resulted in the call for more support for research, as well as for greater use of proxy reference points to help manage data-poor stocks. These issues are even more acute in the developing world. Garcia and Grainger (2005) believe the financial and technical capacity to achieve sustainable fisheries has actually declined in the past one or two decades, because of a lack of donor support. For stock recovery plans to be successful, there must be transparent and effective monitoring, outreach, and meaningful dialogue with stakeholders on plan design and frequent reporting on the pace of recovery. All of these activities are data-intensive, and they require trained professionals in resource management, stock assessment, and outreach activities. Where large-scale closures are part of the plan, effective enforcement is needed, including input and output controls. Scientific and technical impediments When the science is ambiguous through high sampling variability or retrospective bias in assessment, it is difficult to link incremental rebuilding progress to the measures taken, which can erode the credibility of the entire plan. Stakeholders have come to expect a virtually instantaneous positive feedback in stock rebuilding, often encouraged by optimistic scientific projections that do not consider appropriate time-lags. Retrospective bias in stock assessments is a difficult issue to detect and resolve and has the ability to unravel effective cooperation with fishers (Mohn, 1999). Severe restrictions on fishing may eliminate or curtail the ability to measure the effects of the measures taken through fishery-dependent monitoring. However, the need for monitoring should not be an excuse to retain small-scale fishing when it may compromise stock recovery (Shelton et al., 2006). Multispecies issues can be particularly important when prerecruit survival is low, and interspecific predation may be retarding the recovery of a prey species (Collie and Spencer, 1993; Bundy, 2001; NRC, 2006). Detecting depensatory mortality has been and continues to be problematic, but multispecies modelling can help to reconcile the desire to recover all stocks within an area to their historically observed maxima with the notion that trophic interactions may not allow universal and simultaneous rebuilding of all predators and prey. Much more work on the multispecies implications of stock rebuilding is sorely needed. Last, habitat loss and effects on resource productivity associated with climate change (changes in distributions, phenology, acidification, loss of sea ice, productivity of ocean ecosystems, sea level rise, and changing precipitation patterns) may alter the stationarity

5 1834 S. A. Murawski assumptions regarding the population dynamics supporting the ability of stocks to be rebuilt to or exceeding historical levels. Hence, the use of historical stock and recruitment data to project recovery targets and rates may prove insufficient to aid recovery planners, if environmental change affects ecosystem productivity and structure. There is a critical need for climate scientists and resource-management scientists to collaborate on recovery planning scenarios under the added threats of climate change. Are reductions in fishing mortality effective? One of the most pervasive recommendations to meet target and avoid limit reference points is the development and implementation of effective fishing mortality controls (Powers, 1996, 2003; Caddy and Agnew, 2003, 2004; Rosenberg et al., 2006; Worm et al., 2009). Begging the question, then, how have stocks that have historically been exploited well in excess of accepted limit reference points responded to substantial and sustained reductions in fishing mortality? Available reviews have addressed this issue from different perspectives. Earliest hints came from the large-scale reductions in fishing mortality on all stocks in the North Sea associated with World Wars I and II (Margetts and Holt, 1948; Pope and Macer, 1996), where population responses were generally positive and virtually immediate. Hutchings (2000) noted that for large numbers of stocks that had exhibited a 45 99% reduction in reproductive population size at some point in time, recovery 5, 10, and 15 years hence was limited. Mace (2004) countered that such meta-analyses were not conditioned upon whether a particular stock had been subjected to a formal rebuilding plan, and if so, whether the adopted measures had been effective in reducing F to or below the target levels. She noted that in a selection of 31 fish stocks worldwide, reductions in pre-plan F by factors of 1 92 were associated with post-plan increases in biomass by factors of She also noted the exception of the northern cod stock, which had not exhibited signs of recovery by the early 2000s, despite the imposition of a partial moratorium on commercial fishing (Brattey et al., 2009). I undertook a partial meta-analysis similar to that of Mace (2004) to ascertain the rates of stock decline and rebuilding (positive and potentially negative) associated with stocks under explicit formal rebuilding plans. Criteria for selection were: (i) the stock was formally identified in a rebuilding plan in response to documented biomass declines; (ii) stock assessment documented a decline of 50% (no time constraints) in spawning biomass (or suitable proxy); and (iii) a documented, sustained (i.e. several consecutive years) reduction of 25% in F following the biomass decline. The case of North Sea herring (Figure 2) illustrates an example. SSB plummeted between 1963 and 1977, whereas F on adults increased from 0.5 to more than 2.0 a familiar ratchet response to declining biomass. The moratorium on directed fishing on the stock was associated with a relatively rapid increase in SSB between 1978 and Under these criteria, 24 stocks were selected that comprise 25 cases (Georges Bank haddock has displayed two episodes of decline and rebuilding in its 70-year stock-assessment history). To select these cases, I screened hundreds of candidate stocks contained in electronic stock-assessment reports by ICES, ICCAT, NAFO, FAO, and in domestic assessment arenas of Canada and the United States. As Mace (2004) noted, there are relatively modest (though increasing) numbers of stocks where sustained reductions in F on stocks previously subject to chronic overfishing are well-documented. Figure 2. SSB (bars) and mean fishing mortality rate (F, ages 2 6, line with circles) for North Sea herring, (ICES, 2009). Striped and open bars represent the years used for calculating the instantaneous rates of depletion (r D ) and recovery (r R ), respectively (Table A1). The 25 cases analysed (Appendix) illustrate a wide variety of exploitation histories (persistence and degree of overexploitation; rate of decline), life-history types (short- or long-lived), and rebuilding scenarios (degree of F reduction). The linear pattern of log biomass proxies (two examples are given in Figure 3) allows estimation of the instantaneous rates of population change over the periods of decline and recovery for the various stocks (Appendix). Obvious questions to answer include: are the instantaneous rates of decline (r D ) and concomitant rates of recovery associated with reductions in F (r R ) similar; and are there lags in rebuilding indicative of depensation at low stock sizes? Although it is difficult to establish firmly cause and effect relationships between F reduction and subsequent biomass change (because of confounding effects of variable recruitment survival and natural mortality), the instantaneous rates of biomass change during the presumed recovery phase were positive in 24 of the 25 cases (Figure 4; Appendix). The one exception is for the Atlantic cod stock in the southern Gulf of St Lawrence, Canada (Swain et al., 2009). By 2009, even the northern cod stock had demonstrated a positive, though slow, rate of recovery (Brattey et al., 2009). Individual decline and recovery trajectories illustrate a set of distinctive typologies. For North Sea herring (Figure 3a), decline and recovery rates and periods were nearly symmetrical, resulting in a distinctive X-shaped pattern. For Bristol Bay red king crab and other relatively unproductive stocks, rapid declines were followed by relatively slow rates of recovery (Figure 3b), resulting in an L-shaped pattern. For stocks with an incomplete rebuilding history, the pattern can resemble l. The maximum and the minimum instantaneous annual rates of decline were documented for northern cod (r D ¼ 21.1) and Chillipepper rockfish (r D ¼ 0.05), respectively. Rates of recovery ranged from r R ¼ 0.08 (continuing decline) for southern Gulf of St Lawrence cod to r R ¼ 0.4 for California sardine. The assumptions forced an exponential growth model through time-series of arbitrarily censored data. In some cases, this resulted in trended residuals, particularly at the tails, reflecting lags in rebuilding, possibly reflecting demographic factors at the lower end and density-dependent population regulation at the upper end. Nevertheless, all fits to data were significant at p, 0.05.

6 Rebuilding depleted fish stocks 1835 Figure 3. Plots of ln(biomass) and estimated regression lines as a measure of instantaneous rates of population change for periods of decline (r D ) and periods of increase (r R ) for (a) North Sea herring (SSB in million tonnes); and (b) Bristol Bay red king crab (female biomass in thousand tonnes, B Female ). For the rates of change and correlation coefficients, see Table A1. Figure 4. CDFs of the instantaneous rates of population change (r) during the periods of decline and the period of increase for the 24 stocks selected (Appendix). The median instantaneous rate of decline for the 25 cases (r D ¼ 0.14) was similar to the median rate of recovery (r R ¼ 0.16), and their cumulative distribution functions (CDFs) were roughly symmetrical (Figure 4). Furthermore, the median periods of decline and recovery documented are identical (12 years). However, the median recovery period is probably biased low, because of the continuing slow recovery by some unproductive populations that are yet to be rebuilt fully as per plan reference points (Bristol Bay red king crab, northern cod). Nevertheless, these results are similar to the CDFs of recovery times provided by Caddy and Agnew (2003, 2004) and in specific examples provided by others. Consistent with the variation in recovery rates, recovery times vary by an order of magnitude across all recovery factors (a multiple of the current biomass to which the stock may recover; Table A2). One should be cautious about generalizing the results in the Appendix because predictions about the rates of decline or recovery in any particular situation. Each fishery had unique exploitation histories and differing absolute F-values pre- and post-management plan implementation, and these exploitation histories vary widely even within the same taxonomic group. Importantly, these results reinforce the conclusions of Powers (1996, 2003), Mace (2004), and others that stock depletion is, in almost all cases, reversible if fishing mortality is effectively controlled (noting the potential exception of one or more of the Canadian cod stocks to date). In addition, the roughly similar rates of decline and recovery (noting the exceptions for a few unproductive stocks; Baker et al., 2009) underscore the fact that there is little basis to conclude that depensation limits stock rebuilding for the majority of cases (Myers et al., 1999; Shelton and Healey, 1999; Caddy and Agnew, 2004). For those stocks experiencing substantial overfishing, there are two paths to increased biomass: improvements in biomass-per-recruit happening when growth rates are relatively high and natural mortality is low (Atlantic sea scallop; Murawski et al., 2000), and the coincidence of good recruitment and a major reduction in F (striped bass Richards and Rago, 1999; NEFSC, 2008; North Sea herring ICES, 2009). Improvements in biomass-per-recruit may provide early and obvious signs that stock rebuilding works (Powers, 2003); in combination with good recruitment early in the rebuilding programme, this constitutes a perfect storm (i.e. larger fish and rapidly increasing biomass) that helps to legitimize the rebuilding enterprise. Conversely, the lack of good recruitment and/or demographic response early in the process represents a much more challenging situation where patience is required and even small-scale fisheries may retard recovery substantially (Rice et al., 2003; Shelton et al., 2006). Biomass recovery should not be confused with rebuilding the full age and demographic complexity of a stock, which can only happen over a more protracted time-interval. Some of the stocks considered exhibited reductions from fishing up the accumulated biomass of a demographically diverse metapopulation, whereas others had been fished for decades to centuries before their more recent declines. If older, larger fish contribute disproportionately to the stability of the stock, the recovery plan may have to be extended to facilitate rebuilding of evolutionary mechanisms contributing to resilience (Murawski et al., 2001; Grift et al., 2003). Future developments The UNCOVER symposium has focused primarily on understanding the ecological, social, and management dynamics bearing on the recovery of depleted fish stocks through case-history analyses. The growing number of examples offers a hopeful vision

7 1836 S. A. Murawski of where the end states of stock recovery lie. Well-managed fisheries (Mora et al., 2009) are almost invariably the products of episodic overexploitation at an earlier stage. The decisions to rebuild stocks reflect the desire of fishers and managers to avoid recurrent cycles of depletion and rebuilding. In many of these fisheries, effective partnerships among fishers, managers, scientists, and politicians have been forged, resulting in a more collegial and transparent environment for decision-making. The measures taken in successful, more-proactive fishery management regimes are less risk-prone, timelier, more effective, and generally better supported by stakeholders than are many of the measures taken to end overfishing and to rebuild stocks in less successful plans. Are these sustainably managed fisheries a model for those currently requiring stock recovery? Only if in the process the transition to sustainable fishing is laid. Many of the fisheries mentioned above have adopted property-rights schemes to contract excess capacity and capture greater per capita resource rents (Costello et al., 2008; Essington, 2010). Most catch-share schemes have been put in place after overfishing was eliminated often several to many years hence. However, using catchshare programmes as a component of a recovery plan remains challenging, because two societal goals are being conflated rebuilding stocks to sustainable levels and creating economic efficiency through reducing (usually) the number of harvesters. It is easy for stakeholders to confuse the two goals and the requirements for each, further exacerbating the communication gulf that already may exist between managers and fishers. Given the impediments outlined above and the rebuilding time-frames required once effective control over fishing mortality has been attained, the rebuilding goals of the World Summit on Sustainable Development for global fisheries (FAO, 2003) will surely not be met by Nevertheless, experiences over the past decade offer important insights into the process of recovery planning and implementation that will be helpful in eventually attaining those goals. Clearly, the recovery of depleted stocks is a difficult societal issue requiring substantial technical, administrative, and regulatory resources, as well as political and stakeholder consensus or at least acquiescence wherever it has been successful. Usually, the fisheries and the accrual of benefits from these plans changed in substantial ways over their course. Often the reallocation of benefits had not been anticipated. Moreover, those stakeholders upon whom regulations were most severe have not necessarily shared proportionally in the benefits from recovered stocks, because of the long recovery periods required and political and economic expediencies that occur as recovery trajectories evolve. Cogent examples include the loss of traditional markets for North Sea herring after the moratorium (Dickey-Collas et al., 2010) and the relative allocation of striped bass catches to recreational and commercial sectors before and after the harvest moratorium (Richards and Rago, 1999). One of the most difficult issues confronting recovery planners is what to do with fishers and fishing effort during the rebuilding period and with the capacity thereafter. Experience has proven that allowing excess capacity to sit idle while awaiting recovery requires substantial and continuing social adjustment payments, preserving vessels that in all likelihood will not be required to exploit stocks at sustainable harvest rates once they have been rebuilt. The alternatives are: (i) to find alternative target species for the effort (either permanently or in the interim); (ii) utilize excess capacity to assist in evaluating the state of stocks in either sentinel fisheries or cooperative research (NRC, 2004; Shelton et al., 2006); or (iii) retire excess capacity permanently through government intervention or property-rights schemes. Increasingly, the first option is less likely feasible, because of the declining proportion of global fish stocks that allow increased exploitation (FAO, 2009), although the Newfoundland experience demonstrates that alternative fisheries for lower trophic-level species may develop when predators are depleted (Bundy, 2001; Worm and Myers, 2003). The second option can only solve part of the problem, because the sentinel fisheries themselves may result in non-trivial F if lethal sampling is involved. Only the third option appears to provide an end solution to the problem in the global fisheries sector, but even there management issues and societal constraints limit our ability to retire excess capacity effectively (OECD, 2010). Importantly, the choice of alternatives (or a mix of all three) to accommodate excess effort may have profound effects on the structure of the fisheries affected, and failure to make explicit choices about how society wants to restructure the fishery eventually to become sustainable may undermine the credibility of recovery programmes, puts additional pressure on the science supporting monitoring and projections, because of inherent uncertainty about future development, and may encourage managers to declare victory prematurely and go fishing (Powers, 2003). Given the high social, economic, and monitoring costs required to rebuild depleted stocks fully and develop sustainable fisheries, the basic question arises whether it is worth the effort. Of course, the alternative is the continuing loss of economic benefits without providing a solution to global food-security issues arising from the large fraction of depleted stocks. However, mobilizing a political and societal agenda to undertake the steps necessary to solve the underlying causes of overfishing remains frustratingly difficult, because fisheries are prosecuted for a wide variety of economic and social reasons. In some cases, the priority to end overfishing and rebuild stocks has been established legislatively (NOAA, 2007) or in international agreements (Munro et al., 2004) consequently the choice to rebuild has been evaluated and made. In others, particularly in the developing world, the lack of institutional and social capacity to support stock rebuilding and sustainable management reduces the question to moot unless and until such support is forthcoming (Garcia and Grainger, 2005; Mora et al., 2009). Given the globalization of fisheries, there is a real concern that countries in the developed world will meet their demand for seafood products in the medium and long term from unsustainable fisheries emanating from exports from developing economies, thereby exacerbating food-security issues in those regions (Worm et al., 2009). Certification programmes for sustainable fisheries and aquaculture products may have a role in curtailing this outcome, but fisheries remain a lucrative source of export income and enforcement of certification programmes is voluntary. The good news from UNCOVER and previous assessments is that if overfishing has been the proximal cause of stock collapse, substantial reduction in fishing mortality results in positive rates of recovery a rule proved by its exceptions (Rice et al., 2003). Can we rebuild stocks? Yes we can! Do the outcomes justify the costs? They surely do in the long term, but few programmes have predetermined the associated producer and consumer surpluses, never mind the associated non-monetized social costs. When economic evaluations are done, they may often use social discount rates reflecting opportunity costs of capital that are inconsistent with the appropriate time-frames of rebuilding periods. Mostly, supporting economic forecasts operate at

8 Rebuilding depleted fish stocks 1837 macroeconomic levels, whereas stakeholders are vitally interested in analyses at the firm and community levels. Nor have social and economic analyses reflected the societal and management changes required to effect lasting commitments to sustainability. Hence, we may never know the sum of effects of efforts to rebuild depleted populations. If we are to recover the majority of stocks classified worldwide as overfished, it will take a more holistic, adaptive, and ecosystem-based approach to stock recovery that incorporates trophodynamics, habitat restoration, and climate effects on lifehistory characteristics and stock resilience. A new, more consistent, effective and politically supported recovery paradigm that results in sustainable harvesting (Mora et al., 2009) and incorporates appropriate incentives (Hilborn et al., 2005) is necessary if society is to meet its articulated sustainability goals. 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