GENETICS, METAPOPULATIONS, AND ECOSYSTEM MANAGEMENT OF FISHERIES
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1 S119 Ecological Applications, 8(1) Supplement, 1998, pp. S119 S by the Ecological Society of America GENETICS, METAPOPULATIONS, AND ECOSYSTEM MANAGEMENT OF FISHERIES DAVID POLICANSKY 1 AND JOHN J. MAGNUSON 2 1 Board on Environmental Studies and Toxicology, National Research Council, 2101 Constitution Avenue, NW, Washington, D.C USA 2 Center for Limnology, University of Wisconsin, 680 North Park Street, Madison, Wisconsin USA Abstract. The importance of an ecosystem approach to the management of natural resources including fisheries has been widely recognized recently. However, discussions of ecosystem management usually do not provide much detail or emphasis on genetics. Here, we discuss the anadromous salmon (Oncorhynchus spp.) of the Pacific Northwest as an illustration of how important genetic considerations can be as part of an ecosystem approach to resource management. Pacific salmon have a complex genetic and population structure, referred to as a metapopulation structure, that is strongly influenced by the spatial arrangement of the rivers in which they spawn. The many factors that have contributed to the decline of salmon populations in the Pacific Northwest have affected salmon metapopulations as well. As a result, attempts to rehabilitate salmon will need to include a focus on metapopulations as well as on improving habitat and reducing fishing and other sources of mortality. Key words: conservation; ecosystem management; fishery management; genetics; metapopulations; Oncorhynchus spp.; Pacific Northwest; salmon. INTRODUCTION The importance of an ecosystem approach to the management of natural resources including fisheries has been widely recognized recently (e.g., Naiman et al. 1995, NRC 1995, 1996a, b, Christensen et al with comments by several authors, Mangel et al with comments by several authors). Discussions of ecosystem management often mention genetics, but usually do not provide much detail or emphasis on genetics. Here, we discuss an example of a resource management problem with a major fishery component the anadromous salmon (Oncorhynchus spp.) of the Pacific Northwest as an illustration of how important genetic considerations can be as part of an ecosystem approach. The salmon problem has not been easy to resolve; many differing views, objectives, and unknowns persist. In hopes of helping to achieve resolution, in 1992 the U.S. Congress appropriated funds for the Department of Commerce to support a National Research Council (NRC) study of options for improving the long-term survival of anadromous salmonids in the Pacific Northwest. The resulting report Upstream: Salmon and Society in the Pacific Northwest (referred to herein as Upstream, NRC 1996a) is one of several recent activities intended to provide a scientific basis for a con- Manuscript received 20 February 1996; revised and accepted 15 February For reprints of this Special Issue, see footnote 1, p. S1. sensus for action (e.g., Snake River Salmon Recovery Team 1994, ISG 1996). Those reports concluded that many factors have contributed to the decline of salmon. These factors include loss of habitat, fishing, hatcheries, grazing, changes in ocean conditions, dams, and others, both natural and human-caused. The factors involve many aspects of a large ecosystem. Because of their association with humans in myriad streams across the Pacific Northwest, the declines of salmon reflect ecosystem interactions and common dependencies with humans in thousands of watersheds. Upstream (NRC 1996a) said that all of these factors need to be recognized and addressed, but it placed a large emphasis on the importance of maintaining diversity of salmon populations and their genetic structure. Many of the conclusions and recommendations were based on the underlying genetic concept of metapopulation structure. THE UNUSUAL STRUCTURE OF SALMON POPULATIONS Salmon have two important life history properties that make them unusual: they are anadromous (they spawn in freshwater and migrate to sea to grow and mature) and they home to the streams in which they hatched. Because streams have a dendritic (tree-like) structure, the salmon populations that spawn in them tend to aggregate in a similar dendritic structure, referred to as a metapopulation. Metapopulations, although incompletely understood, appear to be impor- S119
2 S120 DAVID POLICANSKY AND JOHN J. MAGNUSON Ecological Applications Special Issue tant in the evolutionary history of salmon because the small populations (demes) that occur in individual tributaries are a product of both local adaption and incomplete isolation. Genetic differentiation among populations and local adaptation to their spawning habitats have been demonstrated in salmon (NRC 1996a), although some of the genetic differentiation is not yet explained. Locally adapted traits include homing behavior, temperature adjustments, unique local mating behavior, adjustment of smolts to feeding conditions, and timing of migration (reviewed in NRC 1996a). Straying, or failure of salmon to home, results in some genetic mixing that links the parts of the metapopulation structure together. Straying frequencies and hence the degree of isolation of salmon populations vary; in some populations, a small percentage of the population strays each year while in other populations straying is less common (Quinn et al. 1991, Pascual and Quinn 1994). Thus, the diversity and abundance of salmon populations depend to some degree on the metapopulation structure the incompletely understood balance of local adaptation of demes to individual streams and the genetic mixing between them that provides genetic and population variability for adaptation to changing conditions. The metapopulation structure itself depends on genetic variability within a population, which provides the basis for local adaptation; and variability between populations, which reflects adaptations to different conditions but also provides an occasional source of new genetic material to local populations through straying. An important feature of metapopulation structure is that strays can establish new populations if a nearby population dies out. The factors that have reduced the numbers of wild salmon have also reduced their genetic variability, both within and between populations. These factors have either been primarily selective, i.e., they affect some wild genotypes more than others, or their primary effect has been the reduction of salmon populations in a nonselective way. Both effects can result in reduced genetic variability within and between the remaining wild populations. Fishing, for example, can have selective effects that result in genetic changes in populations. However, reduction in numbers of wild salmon can occur through loss of habitat and population reduction through fishing. These effects are not necessarily selective, but they can reduce genetic variability within and between populations. Finally, the mixing of gene pools through transplantation of natural and hatchery populations from one place to another can reduce genetic variability, especially between populations. Upstream (NRC 1996a) focuses on genetic losses however they occur. SELECTIVE EFFECTS OF FISHING An early serious suggestion that fishing can cause evolution (i.e., genetically based changes in mean phenotypes) in fishes was made by Cooper (1952). He suggested that fishing selected for brown trout (Salmo trutta) and brook trout (Salvelinus fontinalis) with low growth rates. Other suggestions, especially for salmonids, include changes in the timing of spawning runs, changes in the age and size at maturity (including increases in the frequency of precocious males called jacks), and decreases in adult size. Such suggestions have been reviewed along with their management implications (e.g., Nelson and Soulé 1987, McAllister and Peterman 1992, Law and Rowell 1993, Policansky 1993a, b, Rijnsdorp 1993, Miller and Kapuscinski 1994, NRC 1996a). That such evolution occurs as a result of fishing is clear, although it is not known how widespread or significant it is. Often, the selection is complicated and varies with fish age and the place and the season of capture (Miller and Kapuscinski 1994). If selective effects of fishing are unidirectional, genetic changes in populations can occur in relatively few generations (Policansky 1993a, b). Salmon fishing probably has produced such genetic changes in many populations, for example by selectively catching larger fish or selectively catching fish at a particular time or area in the migration run (see, for example, Ricker s [1981] comments on selective effects of troll and gillnet fisheries on chinook salmon). Another kind of selection that fishing can cause is much less widely appreciated, although it is at least as important and has been discussed for 35 yr (e.g., Ricker 1958). Fishing mixed populations of different productivity has selective effects. Mixed-stock fisheries have been an important factor in the complete elimination of some populations, e.g., wild coho salmon in the lower Columbia River (Cramer et al. 1991, Flagg et al. 1995). The problems of mixed-stock fisheries are discussed extensively in Upstream (NRC 1996a) and are applicable to many fisheries. Consider, for example, a fishery on two populations that mix on the fishing grounds. Assume that population A is twice as productive as population B; in other words, there are twice as many recruits per unit of parent stock in population A. If the fish are caught at a rate that population A can just maintain, population B will be reduced and finally eliminated. The phenomenon can be particularly acute when one of the populations is supported by hatchery production, because the difference in productivity between the hatchery population and the wild population can be so large. The NRC report (1996 a) pointed out that the less productive stocks are [often] referred to as weak stocks, but that term leads to confusion. Weak cannot be equated with small, nor does it imply anything maladaptive, inferior, etc. about animals in the population. The mixed-stock (or mixed-population) fishery problem is related to differences in production rates, not the relative size of populations.
3 S121 (However, larger populations attract fishers. Thus, if the more productive population is also larger, fishing mortality probably will continue to reduce the less productive population.) Mixed-population fishing has a selective effect if the differences in productivity among the different populations have a genetic basis, and variations in components of productivity such as fecundity, fertility, mating behavior, growth rates, and maximum size are influenced by genetic variations (Policansky 1993a). Most fisheries take fish from more than one population, often deliberately but often through by-catch of nontarget populations. For example, protecting a population of low productivity can be difficult when it occurs in a mixture with a more productive population. Such protection would require people to stop catching fish from a population that is not in danger. As pointed out in the NRC (1996a) report, mixed-population fisheries are particularly problematic when some populations are supported by hatcheries, but they also are important in the salmonid metapopulation structure, and may be important for other fisheries. The selection is for production rates at the expense of other phenotypes. Although the increased productivity of hatchery populations results from the hatchery, the result of mixed-population fishing still has a genetic component. Any genetically based phenotypic character that the wild population does not share with the hatchery population will be selected against. Genetic structure and genetic variability of fish populations is very much an aspect of marine ecosystems, and this problem deserves more attention from managers and researchers. OTHER SELECTIVE EFFECTS Other human activities can have selective effects on fish populations. They include hatchery operations (e.g., domestication selection), habitat alteration (e.g., selection for tolerance of higher water temperatures), and almost any human activity that changes fishes environments. Selective and other adverse genetic effects of hatcheries have been widely discussed (e.g., Allendorf and Ryman 1987, Hindar et al. 1991, Waples 1991b, Bowles 1995, Busack and Currens 1995, Campton 1995, Doyle et al. 1995, Leary et al. 1995, NRC 1996a); they are significant, especially on fish like salmon that are anadromous and home. Hatchery and other nonfishing activities probably have fewer and smaller selective effects in most fish species that spend their entire lives in the ocean than in freshwater or anadromous species, because metapopulations of such marine species, especially those with pelagic eggs, are probably less structured spatially than those of salmon. Nonetheless, even widely distributed marine species such as walleye pollock (Theragra chalcogramma) have distinct populations that appear to have considerable genetic differentiation (Bakkala 1993, Dawson 1994). Perhaps genetically based metapopulation structures in such species are more important than is commonly recognized, although they almost surely are not as finely structured as those of salmon. Thus, the potential problems caused by mixed-stock fisheries should be considered in any ecosystem approach to marine fishery management. OTHER GENETIC EFFECTS Human activities have caused a significant loss of salmon metapopulation structure by reducing or eliminating demes, i.e., parts of the structure. For example, in Washington, Oregon, California, Idaho, and Montana, salmon have been eliminated from 40% of their breeding habitat over the past century; dams have eliminated about one-third of their habitat in the Columbia River watershed by blocking passage or flooding (NRC 1996a). The remaining genetic diversity has been further reduced by hatchery practices such as outplanting, which have resulted in hybridization between hatchery and wild populations (Busack and Currens 1995) and sometimes even outright replacement of wild populations (Flagg et al. 1995). Introduction of non-native fishes can result in loss of genetic variability, either through hybridization (Leary et al. 1995) or displacement or predation (Courtenay and Stauffer 1984, Etnier and Starnes 1993). These effects are less likely to be significant for marine species, however, because of their wider distribution in a more connected ecosystem and their exposure to occasional migrants from other marine areas. Habitat degradation also has reduced populations. Mechanisms of these effects are described in Upstream (NRC 1996a). The important matter here is that the resulting population declines have included losses of genetic diversity. GENETICS AND CONSERVATION The importance of genetics in conservation has often been discussed (e.g., NRC 1995) and the importance of genetics in fishery management has received thoughtful discussion (e.g., Nelson and Soulé 1987, Ryman 1991, Riddell 1993, Allendorf and Waples 1996, NRC 1996a). However, we believe that genetic considerations have not generally been accorded enough priority in the practice of fishery management. Because of their anadromy and homing behavior, salmon provide a good system for developing concepts and practices of genetic conservation. For example, Waples (1991a, 1995) described how genetic considerations led to the development of a practical approach to protecting salmon populations based on the concept of an evolutionary significant unit. The NRC (1995) used a similar approach and recommended that it be used for other species, as well as for salmon. The approach provides objective criteria for distinctiveness of a population, a term used in the Endangered Species Act of 1973 (16 U.S. Code Sections [1988]). The criteria are based on the degree to which a population
4 S122 DAVID POLICANSKY AND JOHN J. MAGNUSON Ecological Applications Special Issue is separated genetically and spatially from other populations and, thus, the degree to which it is likely to have a unique potential for evolution. (As discussed by Waples [1995] and NRC [1995], the decision on where to place the threshold, i.e., how distinct a population must be before it is worthy of protection, is a policy judgment as well as a science judgment.) The genetically based analyses of Riddell (1993) helped clarify thinking about salmon population structure and conservation. We hope that Upstream (NRC 1996a), by emphasizing the importance of genetics in an ecosystem context and by basing many of its conclusions and recommendations on that importance, can provide a model for incorporating genetic considerations more generally into ecosystem approaches to fishery management. ACKNOWLEDGMENTS We thank H. Regier, R. Waples, and an anonymous reviewer for helpful reviews. F. Allendorf, H. Carson, D. Chapman, M. Clegg, W. Fink, A. Kapuscinski, T. Quinn, B. Riddell, and B. Simpson provided much insight into the problems we have discussed in this paper. LITERATURE CITED Allendorf, F., and N. Ryman Genetic management of hatchery stocks. Pages in N. Ryman and F. Utter, editors Population genetics and fishery management. University of Washington Press, Seattle, Washington, Allendorf, F., and R. Waples Conservation genetics of salmonid fishes. Pages in J. Avise and J. Hamrick, editors. Conservation genetics: case histories from nature. Chapman and Hall, New York, New York, Bakkala, R Structure and historical changes in the groundfish complex of the eastern Bering Sea. National Oceanic and Atmospheric Administration Technical Report NMFS 114, U.S. Department of Commerce, Washington, D.C., Bowles, E. C Supplementation: panacea or curse for the recovery of declining fish stocks? Pages in H. Schramm and R. Piper, editors. Uses and effects of cultured fishes in aquatic ecosystems. American Fisheries Society, Bethesda, Maryland, Busack, C., and K. Currens Genetic risks and hazards in hatchery operations: fundamental concepts and issues. Pages in H. Schramm and R. Piper, editors. Uses and effects of cultured fishes in aquatic ecosystems. American Fisheries Society, Bethesda, Maryland, Campton, D. E Genetic effects of hatchery fish on wild populations of Pacific salmon and steelhead: What do we really know? Pages in H. Schramm and R. Piper, editors. Uses and effects of cultured fishes in aquatic ecosystems. American Fisheries Society, Bethesda, Maryland, Christensen, N., et al Report of the committee on ecosystem management. Ecological Applications 6: Cooper, E Growth of brook trout (Salvelinus fontinalis) and brown trout (Salmo trutta) in the Pigeon River, Otsego County, Michigan. Papers of the Michigan Academy of Sciences, Arts, and Letters 37: Courtenay, W. Jr., and J. Stauffer, Jr., editors Distribution, biology, and management of exotic fishes. Johns Hopkins University Press, Baltimore, Maryland, Cramer, S., A. Maule., and D. Chapman The status of coho salmon in the lower Columbia River. Report by Don Chapman Consultants to Pacific Northwest Utilities Conference Committee, Portland, Oregon, Dawson, P The stock structure of Bering Sea pollock. Thesis, School of Fisheries, University of Washington, Seattle, Washington, Etnier, D., and W. Starnes The fishes of Tennessee. University of Tennessee Press, Knoxville, Tennessee, Flagg, T., F. Waknitz, D. Maynard, G. Milner, and C. Mahnken The effect of hatcheries on native coho salmon populations in the lower Columbia River. Pages in H. Schramm and R. Piper, editors. Uses and effects of cultured fishes in aquatic ecosystems. American Fisheries Society, Bethesda, Maryland, USA Hindar, K., N. Ryman, and F. Utter Genetic effects of cultured fish on natural fish populations. Canadian Journal of Fisheries and Aquatic Sciences 38: ISG (Independent Scientific Group) Return to the river: restoration of salmonid fishes in the Columbia River ecosystem. Development of an alternative conceptual foundation and review and synthesis of science underlying the Columbia River Basin Fish and Wildlife Program of the Northwest Power Planning Council. Prepublication Copy. Northwest Power Planning Council, Portland, Oregon, Law, R., and C. Rowell Cohort-structured populations, selection responses, and exploitation of North Sea cod. Pages in T. Stokes, J. McGlade, and R. Law, editors. The exploitation of evolving resources. Lecture Notes in Biomathematics 99. Springer-Verlag, Berlin, Germany. Leary, R., F. Allendorf, and G. Sage Hybridization and introgression between introduced and native fish. Pages in H. Schramm and R. Piper, editors. Uses and effects of cultured fishes in aquatic ecosystems. American Fisheries Society, Bethesda, Maryland, Mangel, M., et al Principles for the conservation of wild living resources. Ecological Applications 6: McAllister, M., and R. Peterman Decision analysis of a large-scale fishing experiment designed to test for a genetic effect of size-selective fishing on British Columbia pink salmon (Oncorhynchus gorbuscha). Canadian Journal of Fisheries and Aquatic Sciences 49: Miller, L., and A. Kapuscinski Estimation of selection differentials from fish scales: a step towards evaluating genetic alteration of fish size in exploited populations. Canadian Journal of Fisheries and Aquatic Sciences 51: Naiman, R., J. Magnuson, D. McKnight, and J. Stanford, editors The freshwater imperative: a research agenda. Island, Washington, D.C., Nelson, K., and M. Soulé Genetical conservation of exploited fishes. Pages in N. Ryman and F. Utter, editors. Population genetics and fishery management. University of Washington Press, Seattle, Washington, NRC (National Research Council) Science and the Endangered Species Act. National Academy Press, Washington, D.C.,. 1996a. Upstream: salmon and society in the Pacific Northwest. National Academy Press, Washington, D.C.,. 1996b. The Bering Sea ecosystem. National Academy Press, Washington, D.C., Pascual, M. A., and T. P. Quinn Geographical patterns of straying of fall chinook salmon, Oncorhynchus tshawytscha (Walbaum) from Columbia River (USA) hatcheries. Aquaculture and Fisheries Management 25 (Supplement 2): Policansky, D. 1993a. Fishing as a cause of evolution in fishes. Pages 2 18 in T. Stokes, J. McGlade, and R. Law, editors. The exploitation of evolving resources. Lecture
5 S123 Notes in Biomathematics 99. Springer-Verlag, Berlin, Germany b. Evolution and management of exploited fish populations. Pages in G. Kruse, D. Eggers, R. Marasco, C. Pautzke, and T. J. Quinn, editors. Management strategies for exploited fish populations. Alaska Sea Grant, Fairbanks, Alaska, Quinn, T. P., R. S. Nemeth, and D. O. McIsaac Homing and straying patterns of fall chinook salmon in the lower Columbia River. Transactions of the American Fisheries Society 120: Ricker, W. E Maximum sustained yields from fluctuating environmental and stocks. Journal of the Fisheries Research Board of Canada 15: Changes in the average size and average age of Pacific salmon. Canadian Journal of Fisheries and Aquatic Sciences 38: Riddell, B Spatial organization of Pacific salmon: What to conserve? Pages in J. Cloud and G. Thorgaard, editors. Genetic conservation of salmonid fishes. Plenum Press, New York, New York, Rijnsdorp, A Fisheries as a large-scale experiment in life-history evolution: disentangling phenotypic and genetic effects in maturation and reproduction of North Sea plaice, Pleuronectes platessa L. Oecologia 96: Snake River Salmon Recovery Team Snake River Salmon Recovery Plan recommendations. National Marine Fisheries Service, Seattle, Washington, Waples, R. 1991a. Pacific salmon, Oncorhynchus spp., and the definition of species under the Endangered Species Act. Marine Fisheries Review 53: b. Genetic interactions between hatchery and wild salmonids: lessons from the Pacific Northwest. Canadian Journal of Fisheries and Aquatic Sciences 48(Supplement 1): Evolutionarily significant units and the conservation of biological diversity under the Endangered Species Act. Pages 8 27 in J. Nielsen and D. Powers, editors. Evolution and the aquatic ecosystem. American Fisheries Society, Bethesda, Maryland,
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