Are natural reproductive refugia or fisheries management the reason of the sustainability of fisheries?
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1 1 Are natural reproductive refugia or fisheries management the reason of the sustainability of fisheries? [Alternative title: Is the resilience of exploited marine populations due to natural reproductive refugia or to fisheries management? ] Juan Freire Departamento de Bioloxía Animal, Bioloxía Vexetal e Ecoloxía, Universidade da Coruña, Campus da Zapateira s/n, E A Coruña, Spain Correspondence: Juan Freire, Departamento de Bioloxía Animal, Bioloxía Vexetal e Ecoloxía, Universidade da Coruña, Campus da Zapateira s/n, E A Coruña, Spain. Ph.: , Fax: , jfreire@udc.es Running title: natural reproductive refugia and fisheries
2 2 Abstract Traditional fisheries stock assessment does not take into account the spatial component, and in the worst case only the exploited part of the stock is included in the analyses. The success or failure of management systems is usually analyzed in terms of their effectiveness to control fishing effort (over the exploited [part of the] stock) within some limits that allow the sustainability of the catches. The idea of natural reproductive refugia and their role in the sustainability of fisheries was proposed independently by Walters (1998) and Caddy (1999). Examples are presented here of governance systems using the best scientific information and technology and state-of-the-art management methods that have failed to sustain the resources, except when natural reproductive refugia are present. The hypothesis that natural refugia constitute a general mechanism of long-term resilience in exploited marine populations is presented. Natural refugia arise from the interaction of the spatial dynamics of the population, the individual behavior and the spatial pattern of fishing activity. In most cases, the refugia are constituted in deep-water habitats where low density populations occupy extensive areas. Three different types of refugia could be defined: 1) a large population with seasonal or ontogenetic (spawning) migrations between fishing grounds and reproductive refugia; 2) a metapopulation with some local populations located in fishing grounds and others in refugia (populations located in unexploited areas provide larval subsidies to the exploited populations); 3) an in situ behavioral refugia (behavior determines the seasonal unavailability of part of the stock in the fishing ground). The testing of the hypothesis of the existence of natural refugia and their role in population dynamics should be a basic objective and aspects of the present science and management should be modified to include the new reproductive refugia paradigm.
3 3 Key-words: fisheries management, metapopulations, migrations, natural reproductive refugia, marine reserves Introduction Fisheries biology has a strong component of classical population biology and relies in sophisticated statistical methods to assess key population parameters (basically abundance, age structure, growth, natural and fishing mortality) that are used to model the effects of harvesting in the dynamics of the populations (using tools as yield- and egg-per-recruit and stockrecruitment analyses) (Hilborn & Walters 1992 review the methods in use in fisheries stock assessment). These models are the basis to establish the technical regulations used in the management policy. This process is usually done assuming the unit-stock and dynamic-pool premises; in the best case the spatial component is not taken into account, and in the worst only the exploited part of the stock is included in the analyses. The success or failure of management systems is usually analyzed in terms of their effectiveness to control fishing effort (over the exploited [part of the] stock) within some limits that allow the sustainability of the catches. New trends in fisheries research and management advocate a precautionary approach, where the burden of proof has to been reversed (the recent The Third William R. and Lenore Mote International Symposium in Fisheries Ecology entitled Targets, Thresholds, and the Burden of Proof, held by the Florida State University, November 2000, debated the idea). In short, it has to be demonstrated that the fishery allows the sustainability of the population and ecosystem. But a more basic, and previous, problem, addressed in the present paper, should be to demonstrate that management has any effect in the sustainability of the exploited populations. The hypothesis of the natural reproductive refugia
4 4 Carl Walters, in the North Pacific Symposium on Invertebrate Stock Assessment and Management held in British Columbia in 1995 (Jamieson & Campbell 1998), proposed that the reason for the success of fisheries in the long term is the existence of a spatial accident that creates a large scale refuge for a substantial segment of the spawning population, and not to the effectiveness of the assessment and management in use (Orensanz & Jamieson 1998). The same idea was presented another time by Walters (1998, 2000) arguing that natural refugia provided sustainable systems. These refugia should be due to excessive economic costs and technological limitations for exploitation of these habitats, but disappeared when technological innovations allowed the exploitation of previously virgin areas. Changes in market forces could be another cause to start the exploitation of previously unprofitable natural refugia (Orensanz et al. 1998). Orensanz & Jamieson (1998) used the Walters idea to highlight the importance of an understanding of the metapopulation structure of sedentary stocks and of the use of marine protected areas as a management tool when there are no natural refugia available. In parallel, Caddy (1999) proposes the refugium paradigm (a fishery management system based in the protection of the older spawning stock) based in the existence of deep-water natural refugia for Mediterranean demersal fisheries. The importance of natural reproductive refugia in the sustainability of exploited stocks has been documented in a few case studies: Abella et al. (1997) and Caddy (1999) explain the sustainability of Mediterranean demersal trawl fisheries, which target primarily juveniles, because adults attain a deep-water refuge from fishing. The Mediterranean has a narrow shelf that drops off rapidly to slopes mostly unavailable to trawls. Orensanz et al. (1998) documented the serial depletion of crab and shrimp stocks in the Gulf of Alaska from 1960 to 1990 following a
5 5 pattern of expansion of fishing effort from inshore locations to offshore deep-water areas due to technological and market changes. Yoklavich et al. (2000) identified rock outcrops of high relief in deep canyons as natural refugia to rockfishes (genus Sebastes) in California. They acknowledge the importance of the protection of natural refuges for the adult stock due to the historical increase and spatial expansion of fishing effort. The hypothesis of the natural reproductive refugia, and not fisheries management, as a general mechanism allowing exploitation to continue until fish in refugia themselves become fished could represent a change of paradigm in fisheries, modifying the present design of research, assessment and management methods. Despite that, it has been not elaborated further. The present paper will a) present the above general hypothesis; b) elaborate a typology of natural reproductive refugia illustrated with some case studies; and c) analyze the effects that this change in paradigm could produce in fisheries research, assessment and management. Methods of study of generality of the hypothesis The existence and role of natural marine refugia are elusive topics of study due to the idiosyncrasies of fisheries research (where most attention is paid to the study of the exploited stock, and unexploited life history stages usually larvae and juveniles or the unexploited part of the adult stock are devoted less attention). In many occasions the basic data needed to test the existence and role of refugia are not available, and when the data are available they are dispersed in the literature and have not been integrated in a comprehensive analysis (although see Orensanz et al. 1998). Many fisheries scientists have overlooked the idea because their scope was directed in other directions, although they could have the needed data at hand.
6 6 This problem could be solved using two complementary approaches: comparative analyses of case studies corresponding to data-rich situations with long histories of exploitation and contrasting stock trajectories (comparing stocks that have been overfished or collapsed with others that continue to sustain commercial fisheries). the analysis of the spatial and temporal pattern of overfishing in a stock, due to serial depletion of local populations, relating local trends in population abundance with trends in spatial coverage of fleet activity (see Orensanz et al for an example of this approach). Based in the use of the above methods, and taking into consideration the different case studies cited in the present paper, the main claim for the generality of hypothesis of the importance of natural refugia should be based in the fact that if many governance systems using the best scientific information and technology and state-of-the-art management methods have failed to sustain the resources, except when natural reproductive refugia are present, systems with less information and management intervention should depend more heavily of the existence of the Walters spatial accidents. Typology of natural reproductive refugia A classification of types of natural refugia is proposed based in the mobility of the organisms (especially migrations and ontogenetic habitat shifts), the spatial dynamics of the population, and the existence of a specific behavior that could affect the catchability of the gear. Based in the combination of these three criteria we could define three different types of refugia: 1) A large population with seasonal or ontogenetic (spawning) migrations between fishing grounds and reproductive refugia. 2) A metapopulation with some local populations located in fishing grounds and others in refugia. Populations located in unexploited areas provide larval subsidies to the exploited populations.
7 7 3) In situ behavioral refugia (behavior determines the seasonal unavailability of part of the stock in the fishing ground). This type of refugia is probably the most familiar to fisheries scientists because the catchability / selectivity of the gear has been traditionally one of their key research topics. [Other form of in situ refugia, no relevant for the present paper, is dependent on the behavior of fishers. In the cases when fishers change the fishing ground when density drops below a given limit that determines a negative marginal value for the exploitation of the patch, a low-density escapement in fishing grounds is created]. I will illustrate each type of refugia comparing contrasting case studies (successes and failures in similar types of fisheries, where the main difference was the existence of natural refugia): - Type 1 (Large populations with seasonal or ontogenetic spawning migrations). Demersal fishes in continental shelf and slope areas with deepwater refugia. These fisheries are examples of the, probably, best studied marine populations with a long history of management interventions, but overfishing and collapses have been common in the last decades. Cod (Gadus morhua) fisheries in Newfoundland and Labrador (see Myers et al for a review the information). Despite the great scientific research and technological effort put in this species, these stocks collapsed in the first 90s, due to an excessive fishing effort (mediated by biased estimates of abundance and regulations that do not take into account adequately the uncertainty of the scientific data). This species have offshore-inshore spawning migrations and the distribution of fishing effort changed along the time following the decline of the local abundance until all the habitats were overfished (especially important was the appearance of large trawlers able to exploit the offshore spawning aggregations in winter). Hake (Merluccius merluccius) trawl fisheries in the Mediterranean (Abella et al. 1997, Caddy 1999). The continental shelf in the Mediterranean is narrow and the outer shelf and slope are very step and in many cases
8 8 inaccessible to trawls. Fisheries target mainly juveniles living in the shelf, and the remaining stock attains a refugia when they migrate to deep-water for reproduction. These fisheries continue to maintain their catches showing no sings of overfishing. In contrast, in the north part of the NE Atlantic (mainly in the North Sea), where the shelf is very wide and accessible, no reproductive refugia exist and recently some stocks are experiencing declines. In this example, natural refugia appear as the key because scientific data are more abundant and management systems are more elaborated for the northern stocks (in fact, the Mediterranean lacks a formal management system). - Type 2 (metapopulation with some local populations located in natural refugia). American and European lobster fisheries in coastal areas. Both species have a long history of exploitation along all their geographical range, and the American lobster and some European lobster stocks continue to maintain high catches but other European lobster stocks have collapsed and no signs of recovery exist. Both species constitute sedentary local adult populations (although in some cases there are seasonal migrations). American lobster (Homarus americanus) (Fogarty 1998, Caddy 1999): inshore coastal fishing mortality is very high, but offshore deep-water fishing effort was historically weak or non-existent. Although the connectivity (due to adult migration and/or dispersal) among inshore and offshore stocks and offshore is a matter of debate, it has been hypothesized that the main connectivity is due to larval dispersal and that offshore reproductive effort replenish the inshore exploited stocks. European lobster (Homarus gammarus) (data have been obtained from different sources and integrated in the framework of an on-going Concerted Action funded by the European Union: European Decapod crustacean fisheries Assessment and Management, EDFAM; unpublished data). Along the coastal Atlantic waters two contrasting patterns are found. Stocks in Norway and Iberian Peninsula, where the coastal habitat is narrow and all the distribution area is accessible to the fleet, have collapsed. Sustained fisheries persist in Ireland, North Sea and
9 9 English Channel where coastal habitat is wide and the distribution of fleet effort is more restricted than the distribution of the stocks (some local populations are protected from fishing because they are located in areas distant from the coastline and/or subject to strong currents). - Type 3 (in situ behavioral refugia). Norway lobster (Nephrops norvegicus) is a mud-burrowing species in continental shelf and slopes of the NE Atlantic and Mediterranean. Individuals perform daily and seasonal cycles of activity, especially important for females that expend almost all the eggbearing period in burrows and are virtually inaccessible to trawl gears (cycles ranging from 6 months per year in the south to more than one year every two years in the north) (Chapman 1980). Despite the high fishing effort concentrated in these habitats and the absence of migrations to deepwater refugia, Nephrops maintain sustained fisheries in all the distribution area (ICES 1999). Also, this species is part of trawl multispecies fisheries where management measures are not focused directly to the conservation of the lobster stocks. Is a change needed in the paradigm of fisheries science and management? I propose that the existence of natural reproductive refugia is a basic element explaining the resilience of fishery stocks to exploitation. In fact, these refugia have a similar function to marine protected areas, and one of the main arguments to use reserves as management tools is their robustness against the uncertainty in scientific knowledge or population variability (Murray et al. 1999, Conover et al. 2000). Natural refugia arise from the interaction of the spatial dynamics of the population, the individual behavior and the spatial pattern of fishing activity. In most cases, the refugia are constituted in deep-water habitats (in relation to the depth of the exploited stock) where low-density populations occupy extensive areas (although in occasions they aggregate in restricted areas). Assuming these ideas could have dramatic consequences in the design of research,
10 10 assessment and management methods because the testing of the hypothesis of the existence of natural refugia and their role in population dynamics should be a basic objective. I propose four main aspects where the present science and management should be modified to include the new reproductive refugia paradigm: A shift in key research topics to a) understand basic aspects of habitat selection and use (see Yoklavich et al. (2000) for an example of this approach), and b) obtain data about the spatial population structure and dynamics, spatially-explicit abundance data in the complete distribution area, and the spatial distribution of fishing effort. The basic information needed for assessment should shift from quantitative estimates of global abundance to distribution maps (Orensanz & Jamieson 1998, Walters 1998). These changes in objectives could probably reduce the cost of the direct assessment surveys, although there is a need for the development of these new assessment methods. Inverse use of models of marine protected areas. An extensive theory (and experimental tests) about the effect of marine reserves in fisheries is being developed in the last decade (see i.e. a recent especial issue of Bulletin of Marine Science devoted to this topic, Conover et al. 2000). Based on basic biological, habitat and fishery data, it could be estimated the probability of overfishing of a given stock depending of the characteristics of the natural refugia (the inverse problem to the estimation of the proportion of protected habitat needed to maintain a sustainable fishery or to rebuild a stock). In the case of absence of natural refugia, the main management measures should be directed to create equivalent reserves (Orensanz & Jamieson 1998, Walters 1998, 2000). Changes in the spatial pattern of fishing activity or in the effectiveness and selectivity of gears should be closely monitored because they could have dramatic effects on the stocks, reducing or making disappear the natural refugia. Specially important could be the widespread of the use of high technology fishing gear that could make accessible the natural refugia to exploitation.
11 11 Acknowledgements I thank the information and ideas provided by people participating in the Concerted Action EDFAM and the opportunity to discuss about this topic with Francisco Sardá (Institut de Ciènces del Mar, Barcelona, CSIC) that were basic for the development of this paper. This study was partially funded by the European Union (Concerted Action EDFAM "European Decapod crustacean Fisheries: Assessment and Management options ) and the Spanish Ministerio de Ciencia y Tecnología (grant REN ). References Abella, A.J., Caddy, J.F. and Serena, F. (1997). Do natural mortality and availability decline with age? An alternative yield paradigm for juveniles fisheries, illustrated by the hake Merluccius merluccius fishery in the Mediterranean. Aquatic Living Resources 10, Caddy, J.F. (1999). Fisheries management in the twenty-first century: will new paradigms apply?. Reviews in Fish Biology and Fisheries 9, Chapman, C.J. (1980). Ecology of juvenile and adult Nephrops. In: The biology and management of lobsters. Vol. II: Ecology and management (eds J.S. Cobb and B.F. Phillips). Academic Press, London, pp Conover, D.O., Travis, J. and Coleman, F.C. (2000). Essential fish habitat and marine reserves: an introduction to the Second Mote Symposium in Fisheries Ecology. Bulletin of Marine Science 66, Fogarty, M. (1998). Implications of migration and larval interchange in American lobster (Homarus americanus) stocks: spatial structure and resilience. In: Proceedings of the North Pacific Symposium on Invertebrate Stock Assessment and Management. G.S. Jamieson and A. Campbell, eds. Canadian Special Publication of Fisheries and Aquatic Sciences 125, ICES (1999). Report of the Working Group on Nephrops stocks. ICES CM 1999/ACFM:13.
12 12 Jamieson, G.S. and Campbell, A. (eds.). Proceedings of the North Pacific Symposium on Invertebrate Stock Assessment and Management. Canadian Special Publication of Fisheries and Aquatic Sciences 125. Myers, R.A., Hutchings, J.A. and Barrowman, N.J. (1997). Why do fish stocks collapse? The example of cod in Atlantic Canada. Ecological Applications 7, Murray, S.N., Ambrose, R.F., Bohnsack, J.A., Botsford, L.W., Carr, M.H., Davis, G.E., Dayton, P.K., Gosthall, D., Gunderson, D.R., Hixon, M.A., Lubchenco, J., Mangel, M., MacCall, A., McArdle, D.A., Ogden, J.C., Roughgarden, J., Starr, R.M., Tegner, M.J. and Yoklavich, M.M. (1999). No-take marine reserves: sustaining fishery populations and marine ecosystems. Fisheries 24, Orensanz, J.M. and Jamieson, G.S. (1998). The assessment and management of spatially structured stocks: an overview of the North Pacific Symposium on Invertebrate Stock Assessment and Management. In: Proceedings of the North Pacific Symposium on Invertebrate Stock Assessment and Management. G.S. Jamieson and A. Campbell, eds. Canadian Special Publication of Fisheries and Aquatic Sciences 125, Orensanz, J.M., Armstrong, J., Armstrong, D. and Hilborn, R. (1998). Crustacean resources are vulnerable to serial depletion - the multifaceted decline of crab and shrimp fisheries in the Greater Gulf of Alaska. Reviews in Fish Biology and Fisheries 8, Hilborn, R. and Walters, C.J. (1992). Quantitative fisheries stock assessment. Choice, dynamics and uncertainty. Chapman & Hall, New York. Walters, C. (1998). Designing fisheries management systems that do not depend on accurate stock assessment. In: Reinventing fisheries management (eds T.J. Pitcher, P.J.B. Hart and D. Pauly). Chapman & Hall, London, pp Walters, C. (2000). Impacts of dispersal, ecological interactions, and fishing effort dynamics on efficacy of marine protected areas: How large should protected areas be? Bulletin of Marine Science 66,
13 13 Yoklavich, M.M., Greene, H.G., Caillet, G.M., Sullivan, D.E., Lea, R.N. and Love, M.S. (2000). Habitat associations of deep-water rockfishes in a submarine canyon: an example of a natural refuge. Fisheries Bulletin 98,
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