© 2004 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
Conservation of genetic variation in harvested salmon populations
a NINA Tungasletta 2, N-7485 Trondheim, Norway
b Department of Mathematical Sciences, NTNU N-7491 Trondheim, Norway
c Department of Environment County Governor of Møre and Romsdal, N-6404 Molde, Norway
*Correspondence to K. Hindar: tel: +47 73 80 15 46; fax: +47 73 80 14 01. e-mail: kjetil.hindar{at}nina.no.
Management of a group of Atlantic salmon (Salmo salar) populations that are harvested together in the ocean, but separately in freshwater, is looked at from a genetic perspective. A model that estimates total effective population size from local effective population sizes and migration patterns is applied to a system of ten salmon populations in the Sognefjorden district, western Norway. This population system is dominated numerically by the River Lærdalselva population, which may act as a source of migrants into nine smaller populations in a "source–sink" metapopulation. The total effective population size of this system is to a large extent dependent on the effective population size of the Lærdalselva population, but the contribution per spawner to the total effective population size is greater for a fish from the smaller populations than for a fish from Lærdalselva. The results are discussed in light of conservation genetic theory, and empirical results on the fitness consequences of loss of genetic variation in salmonids. The genetic consequences of harvesting need to be assessed both at the levels of local populations and the metapopulation.
Keywords: Atlantic salmon, fisheries management, genetics, metapopulation, Norway, subdivided population
Received 27 January 2004; accepted 4 July 2004.
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Introduction |
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Principles for conservation of genetic variation in natural populations have been related to the population's effective size, which is defined as the size of an "ideal" population that acts in the same manner as the real population in question (Wright, 1969).1 The effective population size determines the rate of inbreeding of the population, and also the rate of loss of heterozygosity and of genetic variance in quantitative traits, such as body size, fecundity, survival, and ultimately, fitness. Empirical evidence from laboratory and domestic animals suggests that increased inbreeding and loss of genetic variation can have negative consequences for a number of fitness-related traits. Moreover, loss of genetic variation can reduce the possibility for a population to adapt to changing environments (Lande and Shannon, 1996). For short-term conservation, it has been suggested that effective population sizes of >50 per generation be maintained in order to keep the rate of inbreeding sufficiently low to avoid inbreeding depression (Frankel and Soulé, 1981). For long-term conservation, it is suggested that effective population sizes of >500–5000 be maintained to preserve typical levels of genetic variability in quantitative characters (Lynch and Lande, 1998).
Effective population size has been used as a criterion for determining the extinction risk and for setting conservation limits (CLs) of single populations (and/or species), e.g. in international guidelines for categorizing threatened species (Mace and Lande, 1991). From a fisheries management perspective, this translates into finding conservation limits that set constraints on the maximum yield that can be harvested sustainably from the populations. A major weakness, however, is that neither conservation nor optimal harvest criteria are well developed for groups of populations interconnected by gene flow and living in different environments. Such a group of populations is what population geneticists refer to as a "subdivided population" (Wright, 1969), and what ecologists have termed a "metapopulation" (Levins, 1969).
Several lines of evidence suggest that the metapopulation level needs to be considered for Atlantic salmon (Salmo salar) and other salmonids (Cooper and Mangel, 1999). First, salmon typically home to their natal river, but some fish stray to other rivers. An average straying rate of 4% has been mentioned for natural populations (Stabell, 1984). Second, genetic studies indicate that a limited number of migrants are exchanged between Atlantic salmon populations (Ståhl, 1987; Youngson et al., 2003). Estimates of FST (the fraction of total gene diversity at the molecular level attributable to between-population differences) range from 0.02 to 0.10 among natural Atlantic salmon populations (Ståhl, 1987; Bourke et al., 1997). If we assume that salmon populations are in approximate equilibrium for molecular markers (meaning that random genetic drift within populations is balanced by gene flow between them), then Wright's (1969) island model
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In Wright's (1969) island model, as well as in simple metapopulation models (Levins, 1969), it is assumed that all populations, and the habitats they occupy, are identical. Moreover, it is assumed that migration is random with respect to source and recipient populations. This is not likely to be true in the real world, where rivers differ in productivity and population size (Prévost et al., 2003), and where strays are more likely to enter nearby rivers than rivers far away (Jonsson et al., 2003). The source–sink metapopulation model of Pulliam (1988) takes some of this ecological variation into account. In this model, sink habitats are occupied by populations whose specific growth rate is negative. The sink populations cannot sustain themselves without immigration. The source, on the other hand, is self-sustainable without immigration, and produces a surplus of fish that help occupy the sink habitats (Pulliam, 1988).
Effective population size has rarely been analysed for real-world population structures. The relationship between local effective population size and the total effective population size of subdivided populations is known for some simple situations with symmetric migration (Whitlock and Barton, 1997; Wang and Caballero, 1999). Numerical analysis seems to be needed, however, to allow estimation of the total effective population size in situations where both local population sizes and migration patterns may vary (Tufto and Hindar, 2003).
The objective of the present paper is to analyse the effective population size in a group of Atlantic salmon populations that are harvested together during one part of the life cycle (the ocean). The model developed by Tufto and Hindar (2003) is applied to a set of Atlantic salmon populations in the Sognefjorden district, western Norway. The outputs of this model should let us determine the optimal harvest strategy for the contributing populations while maintaining their total effective population size. Findings are discussed from a fisheries management perspective.
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Material and methods |
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The number of instances where estimates of Atlantic salmon spawner data for neighbouring rivers are available, and where local migration rates can be inferred from tagging data, are few. Highly transparent waters in the rivers of the Sognefjorden, a 200-km-long fjord in western Norway (Figure 1), allow for rough estimates of the number of spawners to be made by means of diver counts and bank side surveys. The River Lærdalselva (river 7) is the most renowned of these rivers, and by far the most productive in terms of salmon. In the years 1985–1994, an average of 459 multi-sea-winter (MSW) salmon were counted in autumn before spawning in the River Lærdalselva (Sættem, 1995). To this can be added a number of one-sea-winter (1SW) fish, to provide a rough total estimate of 540 anadromous spawners in the River Lærdalselva annually (Vasshaug and Løkensgard, 1987).
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Counts in six other rivers emptying into the same fjord (Sættem, 1995), and estimates based on rod catches in three additional rivers, suggest that these rivers have between 10 and 60 anadromous spawners each (Table 1). The nine rivers listed in Table 1 together have ca. 310 anadromous spawners. Therefore, the total system including the Lærdalselva has some 850 spawners annually. Count estimates of the proportion of the River Lærdalselva population in the total system (540/850 = 64%) are similar to an estimate based on mark and recapture obtained in the outer part of the fjord from returning adults, 63% of which were recaptured in the Lærdalselva (Vasshaug, 1979).
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Tagging experiments between 1949 and the 1970s suggest that 4 out of 34 (11.8%) salmon from the Lærdalselva were recaptured in other rivers (Rosseland, 1979; Lars Petter Hansen, NINA, pers. comm.). We use this estimate as the forward migration rate from the Lærdalselva and distribute the migrants among the other rivers in the Sognefjorden (Table 1). The migrants make up a high proportion of spawners in the other rivers. We further assume that this system of one big and several small populations is a source–sink system (Pulliam, 1988), such that the nine other rivers combined (the sink) produce fewer migrants to the River Lærdalselva than are contributed to the other rivers by the Lærdalselva (the source). To be precise, we assume that 64 strays are produced from the River Lærdalselva population to enter the other nine rivers, which combined produce a total of 32 strays (20 of which are assumed to enter the Lærdalselva). For this migration matrix to be amenable to population genetic analysis, it needs to be transformed into backward migration rates (Table 1).
A model for effective population size and harvesting
How much genetic variation is lost when salmon are caught in mixed-population coastal fisheries that indiscriminately harvest a number of populations that potentially differ in their productivity and genetic make-up? The scientific and management question can be formulated thus: is it possible to optimize harvest (maximum sustainable yield), while at the same time maintaining effective population size in a group of populations interconnected by migration? This problem has been addressed previously within a numerical model offered by Tufto and Hindar (2003) for the computation of total effective population size, where local population sizes are kept constant and migration rates fixed, but the pattern of migration is arbitrary. Next, the outputs of this model were combined with a simple, deterministic population dynamic model that expresses the rate at which the population is harvested as a function of local population sizes, and emigration and immigration in each subpopulation. Finally, the harvesting yield was maximized subject to constraints set by the effective population size of the total population (Tufto and Hindar, 2003).
Outputs from the model of Tufto and Hindar (2003) suggest that:
- considerable gain can be made in total effective size in a group of populations through harvesting based on knowledge about population structure;
- in source–sink metapopulation systems, the total effective size can be increased without reducing total harvesting yield by first reducing the harvest in the smallest population(s), while keeping the harvest in the largest population;
- when populations differ in their degree of isolation, it pays to harvest relatively less in isolated populations, because these contribute more to the total effective size;
- in cases with moderate or strong directionality in the migration pattern, the total effective size can become less than the sum of the subpopulation sizes;
- strong asymmetries in subpopulation sizes can make one population dominate the other, such that the total effective size is dramatically reduced, even when there is no directionality in the migration pattern.
Relationship between census and effective size
Effective population sizes for Atlantic salmon populations are not generally available. Recently, Säisä et al. (2003) estimated the effective population size of the River Teno/Tana, northern Finland/Norway, to be at least 900 per generation, based on temporal genetic variation between 1939 and 1995. Other methods exist to find rough estimates of the effective size or of the ratio of effective to census size. In terms of a single spawning, the effective size is usually much less than the number of breeders. Deviation from a 1:1 sex ratio is common among spawning salmon, and highly skewed reproductive success is the norm rather than the exception (Jones and Hutchings, 2002). Other complications include overlapping generations and repeat spawning (iteroparity).
For species that spawn only once (semelparity), an approximate estimate of the effective size with overlapping generations is Ne = 
Nb, where is generation time, and Nb is the effective size per breeding season. A review of estimates from many species suggests that the effective size is often as low as 10–20% of the census size per breeding (Frankham, 1995); some experiments with salmonids suggest that the figure may be close to 20%. The generation time for species that spawn only once is approximately the same as the mean age of the spawners: 5 years would be a reasonable estimate for many salmon populations. Thus, with = 5, and Nb/Ncensus = 0.2, and ignoring repeat spawning, we suggest as a rule-of-thumb that the effective size of a salmon population per generation (Ne) is roughly the same as the census size per breeding season (Ncensus), or Ne/Ncensus 
1.
Some recent studies of demographic and/or genetic data from salmonid fish suggest that Ne/Ncensus is 0.5–1.0 for bull trout, Salvelinus confluentus (Rieman and Allendorf, 2001), 0.1–0.3 for steelhead trout, Oncorhynchus mykiss (Heath et al., 2002), and 0.5–0.6 for a population of chinook salmon, O. tshawytscha (from Waples, 2002). Combined, these studies indicate that our rule-of-thumb may represent a slight overestimate of Ne.
Genetically based estimate of migration rate
The number of tagged fish straying from one population to another is not necessarily a good estimate of the number of genetically effective migrants between them. For example, fish recorded as strays to another river during the angling season, often several months prior to spawning, have the possibility to "backtrack" before spawning, that is to leave the wrong river and enter the river in which they were born. Moreover, fish that spawn as strays in a non-native river may experience reduced reproductive success if they are less well adapted to local conditions than homing fish. Finally, migration rates in Wright's (1969) model refer to long-term averages and equilibrium conditions, not to a single season of migration. For these and possibly other reasons, the number of strays may represent an overestimate of gene flow (Youngson et al., 2003).
For two of the ten populations in the Sognefjorden [River Lærdalselva (number 7) and River Aurlandselva (number 8)], a preliminary allozyme analysis suggests that FST = 0.032 (K. Hindar and T. Balstad, NINA, unpublished). Using Wright's (1969) island model, this translates into Nem = 7.5 genetically effective migrants per generation. In the table of backward migration rates in the Sognefjorden (Table 1), mij among these populations have been estimated at 0.184 and 0.008, respectively (cf. the emboldened entries). If we apply the relationship Ne/Ncensus 1, then Ne for the two rivers is N7 = 540 and N8 = 35, respectively (Table 1). This leads to estimates of m78 = 7.5/540 = 0.014, and m87 = 7.5/35 = 0.214, respectively. These genetically based estimates are not far from the estimates based on the backward migration matrix in Table 1.
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Results |
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Based on the model of Tufto and Hindar (2003), the total effective population size of the system of ten rivers in the Sognefjorden can be calculated using estimates of local effective population size from counts, and by constructing a migration matrix from the results of a limited set of tagging studies (Table 1). The results are presented in terms of how sensitive the total effective population size (Ne) of the system of the ten rivers is to changes in the effective size (Ni) of each subpopulation.
Effect of overharvesting the source population
We first predict the genetic consequences for the whole source–sink system of reducing the population size of the source, the River Lærdalselva, by varying the census population size of the salmon in this river from 540 to 0. This scenario is motivated by the fact that the salmon parasite Gyrodactylus salaris has been observed in the River Lærdalselva, and that a dramatic reduction in the population size of this river is to be expected. In terms of harvesting, this scenario would correspond to locally overharvesting the River Lærdalselva population to extinction, for example, by a 100% effective trap on this river.
Figure 2 suggests that in this source–sink system, the total effective population size is an almost linear function of the effective population size in the Lærdalselva. The effect of increasing the population size in the Lærdalselva from 0 to 540 suggests a nearly additive increase in the total effective size from around 310 to 780 for the whole system of ten rivers.
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Effect of protecting sink populations
The small number of anadromous spawners in some of the rivers in the Sognefjorden has recently motivated local protection of spawning populations by prohibiting rod fishing in the river. Based on local counts of spawners and catch statistics, this would be equivalent to doubling the spawning population size of some of the smaller populations (Sættem, 1995).
One way of evaluating such strategies, apart from looking at the effect on each local population, is to look at how the total effective size of the system of ten rivers is affected by a change in each one of them. We have calculated the elasticity, e, of the estimate of total Ne with respect to change in the local population sizes Ni (Table 2).
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The table shows that a reduction in total effective size is least sensitive to a change in population number 7 (e = 0.78 for River Lærdalselva, the source), and most sensitive to change in some of the sink populations (e = 1.41 for population number 8, the River Aurlandselva, and e = 1.38 in population number 6, the River Utla). Why these particular sink populations have the largest incremental effect is not currently known, but it depends on the details of the (constructed) migration matrix. However, e
1 for all the sink populations in the system. |
Discussion |
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TopIntroductionMaterial and methodsResultsDiscussionReferences |
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For genetically substructured species such as salmonid fish, it is important to determine which populations or other units below the species level deserve special attention in management. Several concepts have been introduced to define and characterize such units. The most important concepts are Evolutionarily Significant Units (for long-term management and conservation; Waples, 1991) and Management Units (for short-term management; Moritz, 1994). For each population unit, general methods have been devised to assess their risk of extinction from genetic, demographic, and environmental factors (Mace and Lande, 1991; Allendorf et al., 1997), as well as to assess the potential contribution of each population unit to the species' evolutionary legacy (Waples, 1991).
One problem in applying conservation genetic guidelines to salmon management is that many existing guidelines have been designed on the basis that populations are completely isolated from each other, whereas anadromous populations have the potential to exchange migrants, and as a consequence are only partially isolated from each other. This means that the level of genetic variation is not only a function of the population size and demography of the local population, but also of the neighbouring populations, and of the level of migration (gene flow) between them. Even a few migrants between populations can provide input to reduce the risk of inbreeding and loss of genetic variation. However, these migrants may do little to reduce demographic risks to local populations (Waples, 1998).
Harvesting has a number of biological consequences for natural populations. During recent decades, several of the world's major fisheries have shown significant declines, and in 1997, the FAO estimated that 60% of major marine fisheries were either fully exploited or overexploited, some even to the point where they were considered "vulnerable" by IUCN threat categories. Other effects of harvesting include overexploitation of numerically weaker species and populations caught as by-catch in the major fisheries, and the selective regime imposed by catching specific components of the population (Ricker, 1981; Law, 2000).
The genetic diversity of most marine and anadromous fish has generally been thought to be unaffected by harvesting, because even when these populations are considered to have "collapsed", total population sizes are thought to be sufficiently numerous that changes in genetic diversity are unlikely (cf. Crow and Kimura, 1970). However, when a population is reduced from a very large to a moderate size, which would have negligible effect on heterozygosity or inbreeding, genetic variation can still be lost, because the population will harbour a lower expected number of alleles per locus (Ryman et al., 1995). This may be significant, for example in major loci/genes such as immune response genes (termed MHC, major histocompatibility complex), where adaptability seems to depend on a high number of alleles at a small number of genes. Moreover, in a recent genetic study of a marine fish, the New Zealand snapper, Pagrus auratus, Hauser et al. (2002) showed a significant decline in genetic variation (heterozygosity) during the exploitation history of the species. It was suggested that this decline took place because the effective population size of this species is five orders of magnitude smaller than its census population size, as indicated from fishery data.
A recent review of inbreeding in salmonids suggests that a 10% increase in inbreeding results in a reduction in fitness from about 3–15% in instances of rapid inbreeding to 1–5% in instances of slow inbreeding (Wang et al., 2002). It has, however, proven difficult to measure the impact of inbreeding and the loss of genetic variation in the wild. For example, Wang et al. (2002) found only one study of inbreeding depression in salmonids that was carried out in a near-natural situation. In that study, Ryman (1970) showed inbred Atlantic salmon to be recaptured at a lower rate than outbred individuals after release into Swedish streams.
If homing was perfect, anadromous populations would be entirely isolated from one another, and a clear relationship between population size and level of neutral genetic variation would be expected (cf. Crow and Kimura, 1970). For small populations, markedly less genetic variation would be expected after a few generations in isolation, and none at all during the time elapsed since the last deglaciation (ca. 1000 generations ago). If we apply the relationship 
H = 1/(2Ne) between effective population size (Ne) and the per-generation change in heterozygosity (H; and similarly in inbreeding, F), it is clear that the smaller populations in the Sognefjorden district would soon run into problems of inbreeding and loss of overall genetic variation. This is, however, not the case. Presumably, gene flow among Atlantic salmon populations, even if limited, is sufficient to counteract local variation in overall variability of neutral genes.
In the Sognefjorden district, one river dominates the others with respect to local population size and productivity, and has the potential to act as a major source of migrants into the other nine rivers. When the population size of this river was varied from 0 to 540, the total effective population size of the entire system varied from 310 to 780 in response. These figures amount to rates of inbreeding (and losses of heterozygosity) per generation for the entire system of 0.16 and 0.06%, respectively. With respect to the conservation genetic rules-of-thumb cited above, this system does not seem in danger with respect to immediate inbreeding depression, but on the other hand, will not be considered secure from a long-term evolutionary perspective (if it existed alone).
For one particular asymmetrical scenario (the Sognefjorden river complex) with potentially high migration rates between rivers (Table 1), we have exemplified a system where the local adjustment of harvesting has little incremental effect on the total effective population size in comparison with the harvesting being uniformly distributed across populations (Tufto and Hindar, 2003). In other words, a mixed fishery on these populations in the fjord would have approximately the same effect on the total effective size as an optimal, river fishery, so long as the total number of spawners can be controlled. The results might have been different with other local population sizes and a different migration matrix, for example, if migration rates were typically lower or less dominated by a single river. Even so, the current example suggests that the setting of conservation limits on a river-by-river basis or for an aggregate of several rivers may have only minor genetic consequences if assessed in terms of their effect on total effective population size, Ne. In such cases, where Ne seems not to discriminate among varying options for choosing the best level for setting CLs, the choice needs to be grounded on other considerations (e.g. population dynamics). For example, stock-recruitment relationships developed for European rivers including the River Lærdalselva (Prévost et al., 2003) seem to suggest that many more spawners are required in this river than the number observed since the mid-1980s, a number that cannot be deduced from considerations of Ne alone.
The total effective size of a subdivided population may be a too simplistic criterion for selecting among contrasting management options. It can be argued that other factors, such as local number of spawners, local inbreeding depression (Lynch, 1991), local demographic and environmental stochasticity (Lande et al., 1999), and local adaptations (Taylor, 1991; Merilä and Crnokrak, 2001) need to be included. In particular, adaptations in timing of return to a particular river or tributary (Stewart et al., 2002) would make different populations differentially vulnerable to harvesting. The relationship between absolute numbers of spawners and effective population size can also change as a population is harvested. It is possible to incorporate a number of different processes into the modelling framework of Tufto and Hindar (2003). However, a fundamental difficulty is how to evaluate effective population size against harvesting yield or losses arising from other processes. This would require more precise knowledge of how reductions in local effective population size translate into reduction in population viability and productivity.
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Acknowledgements |
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This paper developed from the work accomplished within the EU concerted action project SALMODEL. We thank our co-workers in this project for fruitful discussion, and two anonymous referees for helpful comments on the manuscript.
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Footnotes |
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1 The ideal population assumes no selection, random mating, and random chance of each offspring having a particular parent
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