Chapter 4

Kissing Cousins: Genetic Interactions between Wild and Cultured Salmon

Fred M. Utter

The Fulton spawning channel on the Babine River (Area 4) is one of four constructed spawning channels designed to increase sockeye production. At 4 km long, Channel 2 is one of the largest spawning channels in the world, producing 67 million sockeye fry in 2001. While the sockeye catch in the Skeena region has increased since the spawning channels were constructed in the 1960s, wild runs of sockeye have declined significantly over this period. photo: Garth Traxler

119 Part Two, Chapter 4: Introduction

“...When is a chinook salmon in Puget Sound a ‘species’ ? Are Germans in Tacoma a ‘species’ of human?....Why do ‘wild’ salmon and not hatchery salmon count (under the Endangered Species Act)?”

John Carlson, Republican candidate for Governor of the State of Washington in 2000.

Introduction The above questions from a public figure reflect wide-spread public concern about the state of wild and hatchery salmon - concerns that are shared by many citizens of British Columbia. Mr. Carlson’s inquiries are not frivolous. They echo frustrations about seeming over-regulation and possible defiance of common sense and are based on understandings about genetic relationships that have been widely held for the past 50 years. When I entered the workforce in the 1950s, there were five species of the genus native to the US Pacific Northwest (chinook, coho, pink, chum, and sockeye salmon), plus the Asiatic masou salmon. In addition to being distinct from one another, the five local species were understood to have variant “races” within them such as spring-run and fall-run chinook, lake-type anadromous sockeye and non-migratory kokanee, as well as even- and odd- year pink salmon. Hatchery and ocean ranching were seen as the salvation of fisheries because, then as now, naturally-reproducing runs were declining due to habitat degradation, harvest pressures, and (in the United States at least) upstream and downstream migratory challenges imposed by dams. Like the above-noted Germans in Tacoma (presumably contrasted with those from Seattle), fall-run chinook salmon from, say, the lower Columbia River and Puget Sound were members of a common “race”. One declining segment of that race could, it was believed, readily be replenished by surpluses from the other, especially with viable hatchery returns from both groups. Of course, given the massive translocations of these two groups that have now been documented, any possible distinction that may have existed historically must have vanished through hybridization. This essay probes changes in these understandings that have occurred since I joined the work force. First, new insights into the genetic relationships among and within Oncorhynchus species are outlined. The dynamics of genetic

120 interactions among translocated and native groups are then examined. Finally, the pertinence of this knowledge to fish culture operations in British Columbia is considered.

Past and present The present era of molecular genetics began in the 1960s. The resulting understandings abundance of single-gene markers has clarified and quantified relationships of genetic within families such as the in a manner that was previously relationships impossible (Utter 1991). Among the consequences of using such molecular markers were a better understanding of the relatedness between and among different species, races and populations of Pacific salmon, and an expansion of Oncorhynchus to include of the Pacific Rim formerly included within the genus (Figure 4-1). These revised perceptions provided a better biological basis for comparisons among these salmon and species. For example, anadromous (steelhead) are now more properly grouped as biological cousins of the anadromous Pacific salmon rather than as close relatives of . The degree of divergence among the trout species is now recognized as similar to that of the North American salmon, and clear understandings have replaced formerly confusing specific and sub-specific taxonomic relationships.

Ancestral The finer genetic resolution allowed by molecular markers indicates ancestral groupings within groupings within four Pacific salmon species (Figure 4-2). These images species contrast with those of Figure 4-1 by being based primarily on frequencies of shared alleles (i.e., variant forms of single genes) rather than the more diagnostic (invariant or “fixed”) molecular genetic differences that characterize closely-related species. Nevertheless, considerable confidence can be placed in groupings such as these that reflect many variable genes (i.e., loci) as well as representative within-group sampling. The ability to project these groupings on maps is consistent with their primarily geographic character. Variable life history characteristics (e.g., run timings) provide important but secondary adaptive dimensions to geographic or ancestral group characterizations.

121 Part Two, Chapter 4: Ancestral groupings within species

pink salmon, O.gorbuscha

sockeye salmon, O.nerka chum salmon, O.keta

Figure 4-1 chinook salmon, O.tshawytscha

Consensus phylogenetic coho salmon, O.kisutch tree of Oncorhynchus based on a review of masu salmon, O.masou morphological and rainbow trout, O.mykiss molecular data (revised from Utter and redband trout, O.mykiss (subsp.) Allendorf 1994). Branch golden trout, O.mykiss (subsp.) lengths approximate relative divergences ……………., O. mykiss (subsp.) among taxa. The ……………., O. mykiss (subsp.) question mark reflects uncertainty about the Mexican golden trout, O.chrysogaster (?) supposed Mexican golden trout collection. , O.apache , O.gilae

westslope , O.clarki lewisi

Lahontan cutthroat trout, O.c.henshawi

coastal cutthroat trout, O.c.clarki

Yellowstone cutthroat trout, O.c.bouvieri

Colorado River cutthroat trout, O.c.pleuriticus

greenback cutthroat trout, O.c.stomias

Bonneville cutthroat trout, O.c.utah

Rio Grande cutthroat trout, O.c.virginalis

The detail and clarity provided by molecular genetic data are illustrated by the following example from sockeye salmon. In addition to purely resident kokanee, sockeye occur either as anadromous lake-type (the predominant life history) or anadromous stream-type populations (occurring as small groupings throughout the species’ range) that are not associated with a lake environment (Fig. 4-2D). Prior to the advent of molecular genetic markers, kokanee were often considered subspecies of anadromous sockeye salmon

122 O. nerka kennerlyi; (e.g., Robertson 1961), and the stream-type anadromous adaptation was more or less ignored. Molecular genetic data now indicate that • kokanee and anadromous populations within a lake system have a recent common ancestry distinct from ancestries in other lake systems; that is, sockeye and kokanee within most lakes are more closely related than either is to sockeye or kokanee, respectively, from other lakes (Foote et al. 1989), and • stream-type populations appear to be primary colonizers of vacant (e.g., post-glacial) habitats, and are thus most likely the key to the evolutionary future of the species (Wood 1995; Gustafson and Winans 1999). This example illustrates the critical role of molecular genetic data in lineage classification. Life history traits remain crucial attributes within the adaptive framework of a lineage, but their tendency to evolve independently among lineages makes them unreliable as primary ancestral markers (Utter et al. 1993).

Adaptive The distinction among subgroups within major lineages lies near or beyond divergence the threshold of detection by molecular genetic markers. Similar frequencies within major of more or less neutral marker alleles reflect recent divergence or intermittent groups gene flow among subgroups. However, these similarities may mask important directional adaptations at other loci that distinguish subgroups and enrich the genetic diversity of the lineage. For instance, no subgroup structure was apparent from a molecular genetic survey of pink salmon populations near

Juneau, Alaska (Fig. 4-3). The low index of genetic diversity (FST = .003) equated to consistently high gene flow among populations of this region, and supported a general understanding of weak regional substructure among pink salmon populations. However, genetic marking of a late upstream run in Auke Creek revealed a fine substructure (i.e., a distinct subpopulation) that persisted over at least five generations (10 years). Similar within-lineage substructures have been found in other anadromous salmonids (Hendry et al. 2000). Such revelations imply the existence of pervasive adaptive substructures within anadromous salmonid lineages. Optimizing the occupation of available or emerging habitats, these substructures apparently dissolve and re-form as habitats shift, like eddies in a stream.

123 Part Two, Chapter 4: Major population groupings

Figure 4-2 Major population grouping of four species of Pacific salmon in the Pacific Northwest (Utter 2001.)

B

Geographically diverged stream/ocean A populations are members of a common major ancestral lineage

Unclear mozaic patterns of relationships among more abundant lake populations throughout region

C D

A. Chinook salmon, contrasting major ancestral groupings putatively descended from Bering (dark groupings) or north Pacific (light groupings) refugia (Utter

et al. 1989, 1992, 1995, Teel et al. 2000). Index of genetic diversity FST = 0.123.

B. Pink salmon, odd year cycle (Shaklee et al. 1991). FST = 0.007 C. Chum salmon, contrasting early- (light groupings) and late-run (dark grouping)

lineages. (Phelps et al. 1994, Johnson et al. 1997). FST = 0.028. D. Sockeye salmon, contrasting mosaic relationships of lake-type (light grouping) and close affinities of stream-type (dark groupings) populations (Wood 1995,

Gustafson and Winans 1999). FST=0.172 (lake- type), 0.013 (stream/ocean- type).

124 Capacity for The capacity for genetic interaction among and within Oncorhynchus species genetic defies predictions based solely on taxonomic distance. The classical interaction understanding of species as “groups of populations where gene exchange between such groups is limited by reproductive isolating mechanisms” (e.g., see discussions in Avise 1994) often breaks down in this genus. Introgressive hybridization (gene flow between genetically differentiated groups) readily occur between native and introduced trout species that have diverged for more than a million years (Leary et al. 1995). In contrast, translocations among conspecific anadromous lineages indicate strong resistances to introgression between groups separated by much shorter intervals (Figure 4-2; Utter et al. 1995). Complex co-adaptations appear to inhibit introgression among lineages of anadromous salmon through severe penalties (i.e., outbreeding depression) affecting hybridized offspring (Utter 2001). In contrast, ease of introgression within anadromous lineages suggests much weaker coadaptations and associated penalties. In response to the questions raised at the beginning of this chapter, chinook salmon of Puget Sound indeed behave as a species in the classical sense. The situation is more complex with regard to conservation issues involving hatchery and wild salmon. Critical genetic considerations include whether or not introgressive hybridization is likely to occur, and, if it does, the adverse genetic interactions between hatchery-adapted (“domesticated”) and wild populations. Also, numerous indirect effects (Figure 4-5) almost inevitably accompany large-scale culture operations and releases. Those of particular concern in the discussion below are disease transmission from cultured to wild populations and excessive harvest imposed on wild populations in mixed stock fisheries based on more abundant cultured salmon of the same species.

125 Part Two, Chapter 4: Genetic considerations

1. Sawmill Creek 2. Peterson Creek (Mainland) 3. Waydelich Creek 4. Auke Creek 5. Salmon Creek 6. Sheep Creek 7. Boulion Creek 8. Hilda Creek 9. Middle Point Creek 10. Peterson Creek (Douglas Island) 11. Fish Creek 12. Bear Creek Auke Creek Fst Nm 2 .000 Large .073 3

Before Marking All Creeks After Marking Fst Nm .003 83 3 4

5

11 Juneau 12 10 6 Douglas Island  9 7 8 Mansfield 0 510 Peninsula km

Figure 4-3

Estimate of gene diversity (FST) based on allelic variation at the sMDH-B1,2 locus before genetic marking among all creeks sampled in the vicinity of Auke Creek Alaska, and between early- and late-run fish of upper Auke Creek; between early- and late-run fish of upper Auke Creek over five generations (10 years) following genetic marking of the late even-year pink salmon run of upper Auke Creek. Based on McGregor 1982, Gharrett and Smoker 1993. From Utter 2001.

126 Genetic The range and longevity of introgression in cultured fish affects its impact considerations on wild populations. Using contrasting hypothetical examples based on in the design of Figure 4-3, consider first the case of a localized enhancement activity focused enhancement on increasing and stabilizing late returns of even-year pink salmon to upper operations: an example within Auke Creek. Straying (and thus introgression) to other temporal or geographic anadromous subgroups within or beyond Auke Creek could be minimized or prevented lineage. through design of the operation. Such an idealized operation would still have to deal with genetic concerns within the targeted subgroup. One such concern is supportive breeding where the genetically effective size of the overall subgroup is reduced by magnifying the survival of the small part of the population represented by the cultured parents and their offspring (Ryman and Laikre 1991; Waples and Do 1994). Paradoxically, this effect is increased as the enhancement becomes more successful. Thus the short-term benefits of enhancement must be weighed against the longterm loss of genetic variability affecting future adaptability of the subgroup. Harvest of the successful enhancement would also have to be controlled to prevent over-harvest of co- migrating wild fish from other subgroups. Assuming satisfactory resolution of both of these concerns, a localized enhancement program could coexist with a healthy substructure of natural reproduction (Figure 4-4). An alternative enhancement program might be a regional facility with brood fish originally obtained throughout the area, and producing a healthy surplus of returning adults free to migrate to nearby streams and interbreed with native fish. The resulting introgressions then erode largely unrecognized geographic and temporal natural substructures with a corresponding decline in natural productivity (Figure 4-4). Although hatchery production compensates for this decline in numbers of returning adults, the overall number of effective breeders is reduced by the magnified survival of cultured fish contributing to both wild and hatchery reproduction. The fitness of the increasingly homogeneous wild populations is further eroded by continued infusions of hatchery-adapted (i.e. “domesticated”) genotypes into the naturally reproducing gene pools. Although modification of the culture operation toward one without supplementation, as outlined in Figure 4-4, would permit reformation of the original regional and within-stream substructures, the regional loss of effective breeders would slow the process considerably. Though hypothetical, these alternate scenarios are based on substantial empirical observation of Oncorhynchus: • The validity of the natural substructure within a major lineage is outlined in Figure 4-3 • The effects of culture operations on pink salmon populations in Prince

127 Part Two, Chapter 4: Genetic interactions

William Sound described in Seeb et al. (1999) provide the basis for proposing different effects of local and regional hatchery programs • An example of regional homogenization induced by extended hatchery management is provided by “tule” fall-run chinook salmon of the lower Columbia River (Utter et al. 1989) • Evidence exists for reduced effective population numbers arising from Pacific salmon hatchery operations (Waples and Teel 1990), and the inescapable reality of culture-induced domestication was reviewed by Waples (1999) • Considerable evidence has also accumulated for the reduced fitness of hybridized cultured-wild anadromous salmonids contrasted with native-wild The Snootli Hatchery raises populations (e.g., Reisenbichler and McIntyre 1977, Campton et al. 1991, coho and chinook that are Hindar et al. 1991, Reisenbichler and Rubin 1999) released into streams in the • The ability of anadromous salmonid substructures to re-form following stress Bella Coola Region (Area 8). or in vacated habitats has repeatedly been demonstrated (e.g., Withler 1984, The short term gain in fish production must be weighed Quinn et al. 1996, Kinnison et al. 1998, Hendry et al. 2000). against the long term loss in In addition to introgressive hybridization, other genetic interactions may occur genetic variability. between native and cultured salmonids. For example, another direct genetic photo: Terry Brown effect is altered selection regimes imposed on native as a consequence of releases (e.g., Waples 1995). Also, the above-noted indirect genetic effects com- monly accompany large-scale culture operations and releases (Figure 4-5).

Genetic The above background provides a useful basis for examining the genetic effects interactions of culture operations on wild salmon populations in British Columbia. The between wild and arguments that follow may be summarized thus: cultured salmon in British Columbia: • Distinct ancestries minimize concerns about introgressive hybridizations levels of concern between Atlantic salmon and Pacific salmon and trout • However, poorly predicts genetic interactions within Oncorhynchus where • gene flow is strongly inhibited among subspecific anadromous lineages, but • gene flow occurs freely within subspecific anadromous lineages • In addition, important within-lineage adaptive substructure lies near or beyond the threshold of molecular genetic detection where • enhancement can unwittingly erode this substructure by stimulating over- harvest, reduction of the overall effective population size, and infusion of non-nadaptive genotypes

128 WITHOUT SUPPLEMENTATION (Overall Productivity = x) A complex and dynamic set of subgroups constantly adjusting to shifting natural habitats, Figure 4-4 and affected by such variables as times of migration and spawning, locations of migration Contrasting A culture operation with and spawning, duration of freshwater and isolated reproduction and subgroup marine residence, and microhabitat distinctions harvest is not excluded as a (e.g., temperature, stream flow) structure with subunit and without supplementation within an anadromous salmonid lineage. Regeneration of natural complexity following discontinuation of supplementation

WITH SUPPLEMENTATION (Overall Productivity < x) A reduced set of subgroups homogenized by gene flow imposed by persistent releases, straying, and outplanting of cultured fish.

These conclusions, when viewed in the context of the principles for salmon conservation outlined in the Wild Salmon Policy (Fisheries and Oceans Canada 2000) point to increasing concern as the potential for gene flow between cultured and wild fish increases (Table 4-1). For this reason, Atlantic salmon escaping from netpen operations actually represent the lowest level of concern. Despite some experimental evidence for Oncorhynchus spp. x Salmo salar hybridization (e.g., Gross 1999) up to the first generation, the possibility for introgressive hybridization appears to be virtually non-existent (see discussions in Chevassus et al. 1983, Galbreath and Thorgaard 1994). Nevertheless, current evidence for successful colonization by escaped Atlantic salmon in BC indicates a potentially serious problem, namely competition with already threatened native salmon populations (Volpe et al. 2000, Volpe 2001). Although numerous failures at intentional colonization minimized this concern in the past (Alverson and Ruggerone 1997), recent evidence warrants greater monitoring and, where necessary, remedial action. Gene flow among Oncorhynchus species is a greater worry. Though not recorded among salmon species, introgressive hybridization between steelhead and coastal cutthroat trout has been documented in Washington State with higher incidences related to cultural releases (Campton and Utter 1985, Hawkins

129 Part Two, Chapter 4: Case study

1997). Similar hybridizations between rainbow trout and cutthroat trout have been found in British Columbia. Some serious problems with introgressions between released hatchery rainbow and native westlope cutthroat trout have been observed in the Kootenay drainage, where hybrids beyond the first generation (identified by nuclear markers) and random mating (identified by mtDNA markers) were observed at each of 11 sites examined (Rubidge et al. 2001). A sample of presumably pure coastal cutthroat from Vancouver Island revealed high levels of hybridization in an area stocked with rainbow trout (A. Dale and D. Heath, pers. com.). Concerns about gene flow or displacement among lineages focus first on uncertainties regarding the existence and extent of those lineages (“conservation units”, Principle Two of the Wild Salmon Policy). In other words, in many cases such conservation units are not yet defined. Figure 4-2 provides valuable but preliminary approximations of such units, many of which are almost certainly subdivided into further lineages. Salmon culture operations which intentionally or potentially release fish must know the population structure of wild conspecifics with which cultured fish may interbreed, interact, and who they may even displace. Cultured fish of distinct ancestry threaten wild populations in several ways. Interbreeding promotes severe outbreeding depression, leading to wasted reproduction and potential displacement (Utter 2001). Continued and large- scale releases further threaten wild populations with excessive harvest in mixed fisheries (e.g., Utter and Ryman 1993). Management to optimize sustainable benefits and conserve wild salmon (Principle Four of the Wild Salmon Policy) cannot occur under these conditions. These concerns extend to escapes of native salmon reared in British Columbia, amounting to 10,000 tons or 20% of all farmed salmon in 1999 (Egan 2000).

Case study: The highest levels of genetic concern relate to erosion of substructures within The Babine Lake major lineages. An assessment of the Babine Lake Development Project for Development sockeye salmon (BLDP) provides a useful example of culture-wild interactions Project within a single major lineage (Wood et al. 1998). Babine sockeye represent a single ancestral grouping characterized by three distinct run timings (early, mid, late; Varnavskaya et al. 1994). Begun in the 1960s, the BLDP consists of two major spawning channels in tributaries to Babine Lake, where semi- natural rearing tempers concerns about domestication. Through its initial decades, the project was an unquestionable numerical success, averaging an almost three-fold increase (to 2.7 million) in adult returns. However, recent declines in smolt survival, attributed in part to white spot disease, appear to be

130 moderating this trend, with a forecast of pre-enhancement levels for 1998. Despite attempts to focus harvests on enhanced fish, returns to un-enhanced areas have declined, particularly those whose timing coincided with that of the enhanced fish. At the same time, sizeable surpluses (averaging 46%) have accumulated at the two enhanced areas. Therefore, despite initial numerical growth and efforts directed toward distinct management of cultured and wild segments, continuation of present trends by the BLDP will result in reductions in complexity of subgroup structure, overall productivity, and genetically The Pinkett spawning effective population size. Indirect effects of the BLDP have been particularly channel is one of 4 channels problematic for non-Babine sockeye populations of the Skeena River, most of that comprise the Babine Lake which have declined in abundance since BLDP and remain well below minimal Development Project on the sustainable yield despite efforts to reduce their harvest (C. Wood, pers. com. Upper Skeena River. The PBS). Pinkett spawning channels produced 25 million fry in A similar trend has been linked to a hatchery program for winter steelhead on 2001. photo: Garth Traxler the Stamp/Somass River where, over many years, native summer runs declined in tandem with intensive hatchery releases. The situation was remedied when hatchery releases were reduced (S. Pollard, pers. com.).

Conclusions In closing, Principle Six of the Wild Salmon Policy warrants special consideration. At each hierarchical level of genetic interaction (Table 4-1), placing top priority on conserving wild salmon populations reduces genetic concerns to zero. However, this priority inevitably conflicts with the goals of supplementation, as is evident in the BLDP (e.g., see discussion in Ryman et al. 1995). Erosion of substructure appears to be reversible if left alone; presumably, despite losses, enough genetically effective breeders are left (Figure 4-4). The threatened extinction of non-Babine sockeye through BLDP-induced mixed-stock fisheries is therefore theoretically reversible. In general, the longterm viability and productivity of wild salmon populations may best be secured by turning the focus away from supplementation and towards habitat protection and restoration. Such redirection will permit fuller operation of the natural processes that have optimized salmon abundance since long before the advent of humankind.

131 Part Two, Chapter 4: Conclusions

Figure 4-5 Some indirect and direct genetic effects of released exogenous hatchery-reared fish on native populations (modified from Utter 1998).

INDIRECT DIRECT GENETIC EFFECTS GENETIC EFFECTS

EXOGENOUS PRE-INTRODUCTION EXOGENOUS POPULATION NATURAL POPULATION POPULATION

overharvest through mixed- stock fisheries resulting from cultured releases Effects on natural disease population introduction Introgressive by means of from resistant hybridization carriers

habitat reduction and fragmentation Outbreeding through depression naturaliztion

wasted reproduction Modified growth, from non- survival, reproduction, introgressive and behavior hybridization

Reduced population size and Persisting capabilities Hybrid swarms fragmentation with resulting for migration, gene flow, replace original loss of genetic variability and adaptation populations and promote spreading Greatly increased likelihood genetic degradation of displacement and extinction

Modified selection regimes on remnant subgroups

132 Table 4-1 Matrix of potential genetic interactions of native and introduced salmonid populations at different taxonomic levels (columns), and principles of British Columbia Wild Salmon policy (rows).

0 none, * low, ** moderate, *** high, **** extreme.

POTENTIAL FOR GENETIC INTERACTION

Salmo- Among Among Within Oncorhychus Oncorhychus conspecific conspecific Wild Salmon Principle interactions species lineages lineages 1. Wild Pacific salmon will be conserved by maintaining ** ** *** **** diversity of local populations and their habitats. 2. Wild Pacific salmon will be managed and conserved as 0 * *** **** aggregates of local populations called conservation units. 3. Minimum and target levels of abundance will be determined * * *** **** for each conservation unit. 4. Fisheries will be managed to conserve wild salmon and 0 ** **** **** optimize sustainable benefits. 5. Salmon cultivation techniques may be used in strategic inter- 0 ** **** **** vention to preserve populations at greatest risk of extirpation. 6. For specified conservation units, when genetic diversity and 0 0 0 0 longterm viability may be affected, conservation of wild salmon populations will take precedence overother production objectives involving cultivated salmon.

133 Part Two, Chapter 4: References

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Volpe, J.P. 2000. Do we know what we don’t know: Atlantic salmon in British Columbia: a review, pages 28-33 in, Aquaculture and the protection of wild salmon (P. Gallaugher and C. Orr, eds) Simon Fraser University. Volpe, J.P. 2001. Super-unnatural. Report published by the David Suzuki Foundation. Vancouver, BC. Volpe, J.P., E.B. Taylor, D.W. Rimmer and B.W. Glickman. 2000. Evidence of natural reproduction of aquaculture escaped Atlantic salmon (Salmo salar) in a coastal British Columbia river. Conservation Biology 14:899-904. Waples, R.S. 1995. Genetic effects of stock transfers of fish. Pages 51-69 in, Proceedings of the World Fisheries Congress, Theme 3. Oxford and IBH, New Delhi. Waples, R.S. 1999. Dispelling some myths about hatcheries. Fisheries 24(2):12-21. Waples, R.S. and C. Do. 1994. Genetic risks associated with supplementation of Pacific salmonids: captive broodstock programs. Canadian Journal of Fisheries and Aquatic Sciences 51 (Suppl. 1):310-329. Waples, R.S. and D. Teel. 1990. Conservation genetics of Pacific salmon. I. Temporal changes in allele frequency. Conservation Biology 4:144-156. Withler, F.C. 1982. Transplanting Pacific salmon. Canadian Technical Report of Fisheries and Aquatic Sciences 1079. Wood, C.C. 1995. Life history variation and population structure in sockeye salmon. Pages 195- 216 in, Evolution and the Aquatic Ecosystem: defining unique units in population conservation (J. Nielsen, ed). American Fisheries Society Symposium 17, Bethesda, Maryland. Wood, C.C., D.T. Rutherford, D. Bailey and M. Jakubowski. 1998. Assessment of sockeye salmon production in Babine Lake, British Columbia with forecast for 1998. Canadian Techncial Report of Fisheries and Aquatic Sciences 2241. Wood, C.C. Personal communication. Pacific Biological Station. Department of Fisheries & Oceans. February, 2001.

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