Interactions between wild and cultured Atlantic salmon: a review of the Norwegian experience

Fisheries Research, 18 ( 1 9 9 3 ) 123-146

123

0 1 6 5 - 7 8 3 6 / 9 3 / $ 0 6 . 0 0 © 1993 - Elsevier Science Publishers B.V. All rights reserved

Atlantic salmon Interactions between wild and cultured Atlantic salmon: a review of the Norwegian experience Tor G. Heggberget*, Bjorn O. Johnsen, Kjetil Hindar, Bror Jonsson, Lars P. Hansen, Nils A. Hvidsten, Arne J. Jensen Norwegian Institute for Nature Research, N- 7005 Trondheim, Norway

Abstract

Most Norwegian salmon populations are characterized by small numbers of fish. The proportion of cultured salmon in these populations has increased together with the rapid growth of the Norwegian salmon farming industry. In several spawning populations, fish of cultured origin now exceed the number of wild fish. The cultured salmon occurring in Norwegian streams are largely dominated by escapees from fish farms, although some are released for stock enhancement and ocean ranching purposes. Life history characters in cultured salmon--for instance, age and size at spawning, time of spawning and migratory behavior--often differ from those of the local stock of wild salmon. Possible ecological effects of interactions in the freshwater stages are discussed. The most serious effects so far have been the introductions to wild populations of lethal parasites and diseases with cultured fish. In recent years, more than 30 populations of salmon have been completely wiped out by the monogean parasite Gyrodactylus salaris. High mortality of adult salmon has also been observed as a result of furunculosis in some streams. In biochemically detectable loci, small but statistically significant differences in allele frequencies exist between populations within and between rivers. Possible long-term effects of genetic interbreeding and erosion of local adaptations are discussed. Increased numbers of cultured salmon may also increase the fishing intensity on wild salmon. Suggestions to reduce negative effects of interactions from cultured fish are proposed.

Introduction About 500 Norwegian streams support Atlantic salmon (Salmo salar). Physical properties such as water temperature regime and water flow vary significan.tly for streams along the Norwegian coast ( 58-70 ° N ). Several studies have indicated the existence of both genetic (Sthhl, 1987 ) and ecological (Heggberget, 1988 ) differences among Norwegian salmon populations. This is in accordance with general ecological and genetic differences described for local salmonid populations elsewhere (Ricker, 1972; Taylor, 1991 ). Within salmonid species, a number of morphological and ecological characters differ between populations. These characters often have a genetic basis in addition to being environmentally modified (N~evdal et al., 1978; Saunders and Bai*Corresponding author.

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ley, 1980; Riddell et al., 1981; Refstie, 1987). Genetic diversity of Atlantic salmon within and among rivers in Scandinavia has been reported by Sthhl ( 1981 ), Ryman and Stgthl ( 1981 ), Heggberget et al. (1986) and Vuorinen and Berg ( 1989 ). Differences among stocks (for instance, in time of spawning and time of emergence of fry) reflect physical differences among rivers (Heggberget, 1988; Jensen et al., 1991 ). During the two last decades, the numbers of cultured salmon in rivers and in the sea have increased significantly. The sources of cultured fish in nature are alevins, parr and smolts released for general stock enhancement, smolts released for ocean ranching purposes, and escapees from fish farms. According to current Norwegian legislation, Atlantic salmon for intentional release must be of local origin. Because of the restricted number of parental fish in broodstocks used, the genetic composition of captive stocks may often differ from that of naturally produced fish in a river (Sthhl and Hindar, 1988 ). The Norwegian salmon farming industry is distributed as cage culture along most of the coast. Most farmed salmon in Norway belong to one of four selected strains which were based on parental fish collected in 40 streams at the beginning of the 1970s (Gjedrem et al., 1988, 1991 ). Until 1988, smolts for farming were imported from the Baltic, Scotland, Ireland and Iceland. As a consequence, Norwegian farmed salmon constitute groups of genetically heterogeneous fish (Sthhl and Hindar, 1988), often showing different life history characters (for instance, timing of spawning and migrations) from wild stocks of Atlantic salmon. Genetic and, to some extent, ecological interactions between different groups of animals represent long-term effects. Possible changes cannot be d o c u m e n t e d before several generations of interactions have passed. Acute effects from diseases and parasites, on the other hand, are good examples of immediate effects of interactions. Spread of diseases appears to represent an increasing problem for a n u m b e r of Atlantic salmon populations in Norway. Release from hatcheries of fish infected by the parasitic monogean Gyrodactylus have caused dramatic mortality of salmon in more than 30 Norwegian streams during the last 15 years (Johnsen and Jensen, 1986). In recent years, furunculosis has been introduced to a n u m b e r of Norwegian streams. In addition to intentionally released fish, great numbers of salmon are accidentally released from salmon farming operations, and in many spawning populations of salmon the number of farmed fish now exceeds that of native fish (Gausen and Moen, 1991 ). The present paper represents a review of recent papers and reports on interactions between wild and hatchery salmon in Norway. In addition, some new data, especially on the life history of Atlantic salmon, are included. A n u m b e r of possible types of interactions between cultured and wild fish exist (Saunders, 1991; Hindar et al., 1991 b). Based on recent data on occurrence

T.G. Heggberget et aL /Fisheries Research 18 (1993) 123-146

125

of cultured fish in Norwegian streams, we discuss both genetic and ecological effects on wild fish together with problems connected with parasites and diseases.

Proportion of cultured fish in fisheries and spawning populations

Development of cultured salmon in wild populations The first releases of Atlantic salmon fry in Norway started about 140 years ago. Smolt releases were started about 1950 to mitigate negative effects of hydropower development in streams. In the early 1970s, salmonid pen aquaculture commenced. In the beginning, few producers were involved, but since 1980 aquaculture production has doubled every second year, reaching a production of 158 000 t in 1990. The n u m b e r of smolts produced, mainly for pen farming, was about 27 million in 1986, with a peak of more than 50 million in 1989. The total annual yield of wild salmon in Norway has varied between 1000 and 2500 t during the last 30 years, with an estimated annual production of about 6 million wild smolts (Sffthl and Hindar, 1988 ). Ocean ranching of Atlantic salmon on an experimental basis started about 1980. According to Sthhl and Hindar (1988 ), an equivalent of about 500 000 smolts of Atlantic salmon were released in 1986 in Norwegian streams for general enhancement purposes, ocean ranching or mitigation of fisheries in regulated streams. This n u m b e r increased to about 1 million smolts in 1992 and is expected to increase to about 2 million by 1994, as a consequence of a national salmon ocean ranching program. In 1986 an estimated 5% of the total n u m b e r of spawners in Norwegian streams were cultured fish (Sthhl and Hindar, 1988), mainly as a result of escapement of salmon from salmon farming operations. A monitoring program was initiated in 1986 to estimate the proportion of farmed salmon in fisheries and spawning populations (Table 1 ). The proportion of farmed salmon in fisheries and spawning populations (September-November) increased from 1986 to 1989, but not again in 1990. Because of late migration to the streams (Gausen and Moen, 1991; Okland et al., 1991 ), escapees from fish farms do not contribute significantly to the sport fishery in rivers, whereas they constitute about one-third of the spawning fish in the same rivers later in the a u t u m n (Table 1 ). Atlantic salmon escaping as smolts from freshwater tend to return to the site of escape to spawn. Straying of adults from smolts released into freshwater is generally low (0-15% ), but depends strongly on release strategy and site of release. Survival of Atlantic salmon smolts released for ocean ranching in Norway varies from 1 to 10%, and is normally within the range of 2-4%, depending on release strategy, smolt quality, origin of smolts and catch strategy. Smolts or post-smolts escaping from a marine site return to the area in the sea from which they escaped, but because of a lack of a home river, the

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7:G. Heggberget et al. / Fisheries Research 18 (1993.) 123-146

Table 1 Proportion of farmed Atlantic salmon in marine and river fisheries, and spawning populations in rivers (data from Lund et al. ( 1989, 1991 ). Moen and Gausen ( 1 9 8 9 ) a n d O k l a n d et al. ( 1991 ) Year

Group

1986

Marine fisheries Marine fisheries

1987 1988 1989 1990 1988 1989 1990 1988 1989 1990

No. of locations sampled

No. offish examined

Proportion (%) farmed fish

Variation (min.-max.)

3

963

8.5

3.6-16.5

3

746

9.8

3.9-14.7

4

899

17.2

4.8-30.2

11

2020

33.3

6.9-66.0

14

3421

36.2

6.0-64.0

41

2449

4.0

-

39

5744

7.3

0.0-26.0

39

5380

7.0

0.0-55.0

33

1251

26.5

-

16

1791

37.7

2.0-77.0

22

2004

33.0

2.0-82.0

Marine

fisheries Marine fisheries Marine fisheries River fisheries River fisheries River fisheries Spawning populations Spawning populations Spawning populations

sexually mature salmon will enter several rivers in that area to spawn late in the season (Sutterlin et al., 1982; Gunnerod et al., 1988; Hansen et al., 1989). If, however, post-smolts escape during winter, they tend to stray more and farther away than fish escaping during the rest of the year (Hansen and Jonsson, 1991 a). Adults escaping during summer seem to enter rivers at random (Hansen et al., 1987a). Post-smolts escaping in late summer, autumn and winter have poor survival to the adult stage compared with those escaping in spring (Hansen and Jonsson, 1989). Survival, however, increases with increasing fish size, and may be very high for adults. In general, the straying of returning adults released as smolts in rivers or in association with freshwater is much lower than for salmon escaping from marine sites without any connection with a home river. Furthermore, survival of salmon escaping from marine sites is higher than for salmon released in rivers. As a result of a number of accidents in marine fish farms, the numbers of migrants originating from those farms are much higher than those of migrants from ocean ranching.

T.G. Heggberget et aL / Fisheries Research 18 (1993) 123-146

127

Behavioral interactions between wild and cultured salmon

Adult salmon Experiments on migratory and spawning behavior at Ims, southwestern Norway, have shown that both wild and hatchery produced salmon released as smolts return as adults to coastal Norway at the same time of the year (Jonsson et al., 1990, 1991 ). The hatchery fish, however, seem to hesitate before entering the River Imsa, males more than females. Hatchery salmon stay in the river for a shorter period of time than wild salmon, and after spawning males descend before females. Many hatchery fish, and males in particular, leave the river without having spawned at all, whereas this rarely occurs among wild fish. Hatchery fish move within the river more than wild fish. Within the river, hatchery fish were more often injured by wounds on head, body and fins, and males more than females. These results indicate that hatchery fish may have lower spawning success than wild fish even though both groups originated from wild Atlantic salmon from the River Imsa, and both groups fed freely in the north Norwegian Sea. However, hatchery fish have no prior river experience. The observed differences may be related to differences in physical fitness, genetics a n d / o r behavior. There was no obvious difference in morphology or growth rate between the fish indicative of differences in physical fitness. However, we cannot fully rule out the possibility of differences in genetics between the groups. Large differences in behavior exist between the two groups of Atlantic salmon. These differences may be due to differences in juvenile river experience and differences in aggressiveness. Juvenile learning seems very important for homing precision, time of river ascent and probably also site recognition in the river. Late arrival at the spawning grounds and poor knowledge of the river may reduce the reproductive success of the hatchery produced fish. Hatchery fish may be more aggressive than wild fish (Riddell and Swain, 1991 ), and higher aggressiveness may result in more woundings and reduce the time the fish are able to be active in the river before returning to sea. This problem is probably greater for males than females because the males fight vigorously over females in the spawning area as the differences in woundings also show.

Presmolt salmon Little information exists about interaction between offspring of cultured and wild Atlantic salmon at the parr stage. Stream-dwelling presmolt salmonids are territorial, and display aggressive behavior against individuals of both their own species (Noakes, 1980) and related species (Kalleberg, 1958). Growth rates and mortality in young salmon are controlled by both productive capacity of the habitat and the density of fish, i.e. intraspecific competi-

1 28

72G. Heggberget et ak/Fisheries Research 18 (1993) 123-146

tion (Gibson and Dickson, 1984; Gibson, 1988). Thus, density-dependent growth and mortality of salmon parr probably exist. This means that a given river, or a specific area of a river, can only support a certain number of parr. If the n u m b e r of recruits exceeds the carrying capacity, intraspecific competition will increase, resulting in increased mortality a n d / o r reduced growth rate of fry and parr. The time at which salmon become smolt is primarily dependent on size and not age (Elson, 1962). Young fish that grow quickly will become smolts at a lower age than fish that grow more slowly. Water temperature is the main factor governing growth rate in Atlantic salmon (Symons, 1979 ). Other factors, such as fish density (Le Cren, 1973) may also influence the growth rate of parr. If the smolt age in a river is increased, the number ofsmolts produced per area will be reduced. The potential sources of cultured presmolt salmon in wild populations are hatchery produced fry released for general stock enhancement, fry originating from spawning between escaped farmed salmon and presmolt escaping from smolt hatcheries situated near salmon streams (Lund and Heggberget, 1992 ). Increased intraspecific competition between different groups of Atlantic salmon at the presmolt stage will probably delay smoltification, with reduced smolt production as a consequence. However, the effects of increased competition are not known in detail and need more attention in future research.

Phenotypic and ecological variations among salmon stocks

Migratory system--a bas&for local adaptations Wright (1931) considered that mechanisms of evolutionary change, including natural selection, would be most effective in species with extensive population subdivision throughout varied environments. Salmonids have a tendency to form locally adapted populations over a range of different environments (Taylor, 1991 ). Taylor ( 1991 ) suggested that at least three conditions should be met to demonstrate local adaptation: ( 1 ) the feature or trait being investigated must have a genetic basis; (2) differential expression of the trait must be associated with differential survival or reproductive capability among individuals in a c o m m o n environment; (3) a mechanism of selection responsible for maintenance of the trait in a population should be demonstrated. In Norway, most populations of Atlantic salmon are characterized by small numbers of spawners, with some straying (4%) of fish between rivers (Stabell, 1984). It is well known that both wild and released Atlantic salmon normally return to the home river after the marine feeding migration (Harden Jones, 1968; Hansen et al., 1987a, 1989). Through this homing system, adaptation to localized environments is possible. The reproductive success of

129

72G. Heggberget et al. /Fisheries Research 18 (1993) 123-146

individuals with high survival under certain environmental conditions can be maintained and increased by the highly developed homing system in salmonids. For salmonids living under temperate and cold conditions, there appears to be a strong selection pressure on timing of some important life stage events. Offspring from individuals breeding at any time of the year other than the ideal will have limited possibilities for survival.

Life history variations between stocks of Atlantic salmon in Norwegian streams A n u m b e r of studies have shown that life history characteristics vary between salmonid stocks. Examples of varying life history characters are timing of emergence of fry (Jensen et al., 1991 ), timing of smolt migration (Hesthagen and Garnhs, 1986; Jonsson and Ruud-Hansen, 1985), timing of return migration (Hansen and Jonsson, 199 lb), timing of spawning (Heggberget, 1988), age and size at maturity (Glebe and Saunders, 1986) and smolt age (Lund et al., 1989). Age at spawning in Atlantic salmon has both genetic and environmental components (N~evdal et al., 1978; Glebe and Saunders, 1986), and shows considerable interpopulation variation (Myers et al., 1986). Smolt age is mainly determined by the water temperature regime of the natal river (Symons, 1979), but may also have a genetic component (Refstie et al., 1977). It should be noted that life history characteristics within a stock may vary between years and individuals. For instance, in the River Surna the composition of different sea-ages as returns by brood years of recaptured ocean ranched salmon vary significantly between years. A comparison of 8 years (Fig. 1 ) shows that the proportion of 1 SW salmon varies between 45 and 75%, whereas that of 2 SW salmon varies between 40 and 25%. The brood[ ] 1-Seawinter

[ ] 2-Seawinter

[ ] >3-Seawinter

100" 80"

o~ 6040-

~" 20-

i11111ili11111111 i

i

i

i

r

i

i

i

J

,

i

J

i

i

i

i

J

i

i

1965 69 71 73 76 78 83 85 87 89 1966 70 72 74 77 80 84 86 88

Year

Fig. 1. I n t e r a n n u a l v a r i a t i o n in sea-age in b r o o d year returns of Atlantic salmon of the Surna stock, released in R i v e r Surna, Norway.

130

T. G, Heggberget et al. / Fisheries Research 18 (1993) 123-146

stock has been taken from the same place each year and the production regime in the hatchery was the same each year. Variation in physical and biological marine conditions contributes to interannual stock differences in age at spawning. In addition, characters within a stock are distributed over a given range between individuals. However, despite the individual, interannual and environmentally modified variations in life history, some significant and systematic variations between Norwegian salmon stocks exist. Another example of variation between stocks is the variation in timing of smolt migration from rivers along the Norwegian coast. In the southwestern River Imsa (59 °N), smolt migration peaks around the middle of May (Jonsson and Ruud-Hansen, 1985 ), in Central Norway (64 °N) in the second half of May (Hesthagen and Garn&s, 1986 ) and in the River Alta, North Norway (70°N), in late June-early July (Fig. 2). The proximate factors triggering smolt migration varied between these streams (Fig. 2 ). In the River Imsa, the smolt migrate at low or decreasing water flow and at high (8-10 °C) water temperature. In the River Orkla, peak emigration takes place during the spring freshet, at high or increasing water flow and at low (3-6 °C) water temperaWater flow

No of smolts

R. Irnsa

-20 ~ o -15

~"

-10

~

s~ _

//

_

,"";

L.

7",

-/

~,\

R. O r k l a

k

R. Alta

/'/",,

;

20

',

F

20 15

-10 5 M

l Date

J

- ..........

Number of smolts Water flow

- -

Water temperature

Fig. 2. Simplified model o f different p r o x i m a t e triggers for Atlantic salmon smolt migration (freshwater t e m p e r a t u r e a n d water flow), correlated with seawater t e m p e r a t u r e s outside some Norwegian rivers.

T.G. Heggberget et aL / Fisheries Research 18 (1993) 123-146

131

ture. In the River Alta, peak smolt migration takes place about 1 m o n t h after the high spring flow and at high or increasing water temperature ( 8-10 ° C ). The sea temperatures at the coast of Norway vary with latitude. The differing times of smolt migration are correlated with a sea temperature of 7-9 ° C, indicating that the ultimate factors for timing of smolt migration are oceanic factors, mainly dependent on temperature. Adaptation of timing of smolt migration from geographically different areas might be due to both optimal marine feeding and physiological conditions (Sigholt and Finstad, 1990). The smolts do not know the sea water temperature outside the stream. It appears that adaptations over a long period of time have developed a population-specific proximate trigger system for migration in different stocks. If this system is altered as a result of immigration of cultured fish in a wild stock, a greater proportion of the smolts will leave the river at a time other than the optimal time, and increased post-smolt mortality will probably result.

Population genetics of Atlantic salmon Genetic structure of Atlantic salmon Atlantic salmon populations are spatially organized as locally adapted, largely isolated populations, as are other salmonid species (Ryman, 1983; Sffthl, 1987 ). The a m o u n t of genetic differentiation among these populations as estimated from biochemical genetic data is large compared with that between most vertebrate populations. Atlantic salmon populations world-wide have a GST of about 0.36 (Sthhl, 1987 ); this differentiation among populations arises first from a major dichotomy between populations from either side of the North Atlantic Ocean, and second from genetic differences between European populations in Baltic and Atlantic drainages. On a more limited geographic range, for instance the Norwegian coast or northern Sweden, genetic differences between local Atlantic salmon populations result in Gsv of about 0.10 (Sthhl, 1981; St~hl and Hindar, 1988). In absolute terms, Atlantic salmon are not highly variable genetically as estimated from protein coding loci; the total gene diversity (HT) has been estimated at 0.04 (Sthhl, 1987). Studies are in progress in Norway and in many other European countries to provide a more detailed picture of the genetic structure of the species. It has been shown that a single river may contain several genetically different populations. Tagging studies suggest that homing is precise even within rivers, and early speculations on the existence of local populations within large rivers (e.g. the Tana River in Norway and the Miramichi River in Canada) have been substantiated by rearing studies (Riddell et al., 1981 ) and by biochemical genetic studies (Sthhl, 1987; Sffthl and Hindar, 1988). Whether or not this microgeographic genetic differentiation is stable over time is un-

132

TG. Heggberget et aL / Fisheries Research 18 (1993) 123-146

known, but preliminary data from the Tana River suggest that the local genetic structure is temporally stable (K. Hindar, unpublished data, 1992).

Impact of releases on natural populations The following presentation is based on a more extensive review by Hindar et al. (199 l b), drawing on evidence from both intentional and accidental releases of a n u m b e r of salmonid species from both Atlantic and Pacific drainages. Releases of cultured fish to the wild potentially threaten the species with genetic loss at the level of both the population and the individual. Genetic loss at the level of the population may be by breakdown of adapted gene complexes through interbreeding, loss of native populations as a result of displacement or eradication through disease introduction, or by homogenization of population structure through swamping a region with a c o m m o n gene pool. Furthermore, continual flooding of an area with exogenous genes prevents readaptation away from the exogenous gene pool. Loss of genetic variation at the individual level through inbreeding may be directly related to culture operations through using restricted numbers of parents. Inbreeding in wild populations may also be indirectly related to culture operations when population sizes are continually depressed as a result of mixed harvest with more abundant cultured fish.

Interbreeding Two types of empirical evidence exist regarding genetic change after introduction of cultured fish into natural environments. The first relates to changes of genotypic and allelic frequencies at loci that are identified by various biochemical and molecular techniques (Utter et al., 1987). The second relates to changes in performance traits (morphological, ecological or ethological) that have a heritable basis. A wide variety of outcomes have been observed after natural reproduction of cultured fish and their interbreeding with natural populations. At one extreme is displacement of local stocks or complete introgression between local and introduced stocks. Notable examples are the introgression between local and released stocks of brown trout in Northern Ireland and France (Taggart and Ferguson, 1986; Guyomard, 1989). At the opposite extreme are reports of no detectable introgression into native populations despite substantial introductions on non-native stocks. Presumably the non-native fish have been unable to reproduce in the new environments. For example, offspring of anadromous Atlantic salmon released into areas where only non-anadromous populations occur do not appear to have interbred with the latter (Vuorinen and Berg, 1989 ). Releases of salmonids into areas beyond their natural geographic range ap-

13 5

T.G. Heggberget et al. / Fisheries Research 18 (1993) 123-146 STO ............. INFI

Fot~ L a k .¢ Ran~ Fles.~

Bjerl Vefs Hunl

Figg Ave Qvr~

Batr Isa Tafj, Vikj~

Sval

selva

hna

Fig. 3. Map of Norway showing the 14 regions with rivers and hatcheries infected with Gyrodactylus salarisby the end of 1985, and known releases of salmon from infected hatcheries since 1975. Names of rivers which have been stocked with fish from infected hatcheries are underlined. in the 18 infected rivers show a sharp decline after 1981 and has remained very low. Gyrodactylis salaris is probably a recent introduction to Norwegian rivers. With two exceptions, the occurrence of G. salaris in Norway seems to be traced back to region 9 (Fig. 3), where it was first detected at a hatchery in July 1975. H o w the parasite first arrived in this region is unknown (Johnsen and Jensen, 1986). Malmberg ( 1 9 8 9 ) hypothesized that G. salaris originally spread to Norway from Swedish salmon hatcheries. This hypothesis was supported by Bakke et al. ( 1 9 9 0 ) , who found that susceptibility of Atlantic salmon to G. salaris was much less in a Baltic Sea drainage population than in Norwegian salmon populations. These results indicate a genetic intraspecific heterogeneity in resistance between the major salmon groups representing the Eastern Atlantic and the Baltic Sea drainages. The hypothesis that G. salaris

136

7zG. Heggberget et al. / Fisheries Research 18 (1993) 123-146

Lakselva

80

l

o

Atlantic salmon

•

Browntrout

60

40

E 20 i

i

T

I

i

T

•

r

r

r

l

r

i

r

~

i

Vefsna

80-

Atlantic salmon Browntrout

o •

d z 604020o-

1981 ' 198/3T

19'75 E 19~77 1 9 7 9

' '19'91' 1985 1987' 1989 '

J

J

Fig. 4. Mean densities (no. of fish per 100 m 2, _+95% confidence limits) of presmolt Atlantic salmon and brown trout in the infected rivers Lakselva ( 1975-1989 ) and Vefsna ( 1975-1991 ). The arrows indicate the year of the first observation of G. salaris in the river. 800 -

-

80

700 -

-

70

600 -

-

60

500 400-

200

-

I00

-

0

,

',, ,~',

300-

,

", ," " ' t - 4 - 4 - ~ - ~ "

i

,

F

,

i

1966 1968 1970 1972

,

i

~

1974

i

,

t

,

i

,

i

,

i

"~

,

i

2"" \

,

I

i

30

,

0

1976 1978 1980 1982 1984 1986 1988 1990

Fig. 5. Total river catches of Atlantic salmon in Norway ( - - - , left scale) compared with the total catches of Atlantic salmon in infected rivers ( , right scale), 1966-1990. is e x o t i c t o N o r w a y is s t r o n g l y s u p p o r t e d b y t h e s e i n v e s t i g a t i o n s ( B a k k e et al., 1 9 9 0 ) . I n v e s t i g a t i o n s ( J o h n s e n et al., 1 9 8 9 ) h a v e s h o w n t h a t r o t e n o n e t r e a t m e n t c a n b e a n e f f e c t i v e w a y o f r e m o v i n g G. salaris f r o m a w a t e r c o u r s e . I n r e c e n t

7~G. Heggberget et aL / Fisheries Research 18 (1993) 123-146

13 3

pear to be accompanied by increasing hybridization rates with closely related native species. This has occurred between released brown trout and native Atlantic salmon in Newfoundland as well as between other salmonid fishes. One study indicates that hybridization rates may increase as a result of releases of non-native stocks of one species, even though the released species itself is not new to the release site (Garcia de Lraniz and Verspoor, 1989 ). It has frequently been observed that released fish do not outperform the local wild population and only occasionally perform as well (Ricker, 1972 ). Several studies show genetic changes in adaptive traits that alone or in combination could explain the maladaptive nature of releases. One experimental study with anadromous rainbow trout Oncorhynchus mykiss indicated a direct genetic basis for survival, which was higher in wild fish than in either cultured non-native fish or in w i l d × cultured hybrids (Reisenbichler and Mclntyre, 1977). Other studies have complemented this finding by suggesting that reduced survival may be a result of reduced swimming stamina, or weakened territorial and concealment behavior shown by cultured fish. We already know that female escapees deposit fertilized eggs that survive to the alevin stage both in Scottish and Norwegian rivers (Webb et al., 1991; Lura and S~egrov, 1993). This knowledge is based on comparisons of optic isomers of astaxanthin, which differ between the eggs of cultured and wild salmon so that each group can be identified until the start of exogenous feeding. Moreover, Lura and S~egrov ( 1993 ) suggested that in one of two reproductive seasons surveyed, the spawning success of escaped females was not very much lower than that of wild females (as long as could be followed by this m e t h o d of investigation). In the following season escaped females appeared to have a very limited spawning success. It should, however, be noticed that their effect on natural populations may still be dramatic, as some escaped females excavated redds in the same place as wild fish spawning there earlier in the season (Lura and S~egrov, 1993 ). On this background, it is most likely that the large numbers of escaped Atlantic salmon now spawning in Norwegian rivers will affect natural populations genetically. Moreover, the genetic changes in natural populations will probably result in poorer adaptations to local environmental conditions and lead to lower productivity of wild stocks. Even on a short time scale, a number of populations will probably be lost as a direct result of disease introduction, or as a combined result of disease introduction and invasion of escaped fish. It seems fair to speculate that sea ranching can only add to the problems for natural populations if not carried out on the premise that it shall not result in more exogenous fish in wild populations.

Diseases-parasites Gyrodactyliasis is caused by the monogean Gyrodactylussalaris. This ectoparasite has become a serious problem for Atlantic salmon parr populations

134

T.G. Heggberget et a L / Fisheries Research 18 (1993.) 123-146

in many Norwegian rivers during the last two decades. Experiences from Norwegian rivers have also shown that wild Atlantic salmon populations can become seriously affected by furunculosis attacks. Outbreaks of the disease can cause large mortality among adult Atlantic salmon. Mortality of salmon caused by Gyrodactylus was unknown before 1975, and outbreaks of furunculosis were observed in only one river in southeastern Norway before 1970. There is, therefore, a strong correlation between the increase in gyrodactyliasis and furunculosis and the rapid expansion of the salmon farming industry with import of smolts from most areas of the Northwest Atlantic and the Baltic during the first half of the 1980s.

Gyrodactylus salaris In August 1975 the population of Atlantic salmon parr in the river Lakselva in northern Norway was found to be infected by Gyrodactylus salaris (Johnsen, 1978 ). This was the first observation of this parasite in a population of wild salmon in Norway. A catastrophic mortality of presmolt salmon was observed, and after 2 years nearly 100% of the presmolt salmon had died, although presmolt brown trout (Salmo trutta) was not affected. By the end of 1985 the n u m b e r of rivers infected with G. salaris had increased to 26, and by 1991 the parasite was found in 35 salmon rivers. Until the end of 1989 G. salaris was reported from approximately 35 hatcheries scattered throughout the country. Twenty-five of these were inland rainbow trout ( O. mykiss) farms. Rainbow trout is known to be a carrier of G. salaris. Johnsen and Jensen (1986) grouped the infected rivers into 14 regions according to their locations. A clear connection between the distribution of G. salaris in Norwegian rivers and known deliveries of stock fish from infected hatcheries was shown (Fig. 3 ). Population densities of salmon parr have been severely reduced in infected rivers. No similar trends in the densities of brown trout in infected rivers were observed in the period 1975-1989 ( P > 0 . 0 5 ; Fig. 4). Johnsen (1978), Heggberget and Johnsen (1982), Johnsen and Jensen ( 1986, 1988) and unpublished investigations in several salmon rivers have indicated that infections of G. salaris cause great reductions and near-extermination of salmon parr populations. In recent years, catches of returning salmon in the infected rivers have also declined. Official catch statistics on salmon and trout fisheries in Norwegian rivers have separated the catch of salmon from the catch of anadromous brown trout and Arctic char (Salvelinus alpinus) since 1966. In Fig. 5 we have compared the total catch of salmon in all Norwegian rivers with the total salmon catch in 18 infected rivers included in official statistics in the period 19661990. The two graphs are similar until 1981. During the last 13 years the total catch of salmon has been relatively constant, whereas the total catch of salmon

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years, 14 relatively small Norwegian rivers have been treated with rotenone in an attempt to exterminate the parasite.

Furunculosis Aeromonas salmonicida can live for a long time in fish without causing disease. Fish which survive an outbreak of the disease may be 'carriers' of the disease. Even though the 'carrier' does not develop the disease, it is well docu m e n t e d that it can transfer the disease to other fish and in that m a n n e r initiate an epidemic among previously unexposed fish (Enger, 1990). In Norway, furunculosis was found for the first time in 1964 after an import of rainbow trout from Denmark. In 1966 the disease was observed in wild Atlantic salmon in the River Numedalslhgen, the disease probably being transferred by release of rainbow trout in a tributary to that river (H~stein, 1990). In the River Numedalslhgen, furunculosis caused the most severe mortality of salmon in 1968 and 1969. In these years dead fish were observed by walking along the fiver banks. According to Gunner~d and Sigholt ( 1982 ), furunculosis has not been observed in the river after 1979. In 1985, furunculosis was found in Atlantic salmon in marine fish farms after an import of smolts from Scotland (H~tstein et al., 1989 ). At the end of 1985 the disease was verified in 16 fish farms in a region in Central Norway. In spite of establishing procedures in the infected farms in 1986 the disease still showed up in some farms in 1987 in the same region. In 1988 the disease occurred in several fish farms on the west coast of Norway, and a total of 32 farms now had the disease. At the end of 1989 the disease was found in 171 fish farms. This development continued in 1990 and by the end of that year 378 farms were infected with the disease. By the end of 1991 furunculosis had been found in 507 fish farms and most of the Norwegian west coast was affected. A similar increase was observed in salmon streams in Norway. By the end of 1989, 22 Atlantic salmon had been found infected with furunculosis. In 1990 the m i n i m u m n u m b e r of infected streams had increased to 42, and in 1991 the n u m b e r of streams with reports of dead salmon as a result of furunculosis had increased to 66. As an example of possible mortality of adult salmon caused by furunculosis, the figures from a small river (Aursunda), in Central Norway can be given. In July 1990, during a period with high water temperature, about 700 adult salmon were found dead. The mortality decreased in August, and after the beginning of September, only a few dead fish were observed. Also, presmolt brown trout and Atlantic salmon were found dead from furunculosis (Rikstad, 1991 ). There were several other examples of outbreaks of furunculosis in wild salmon populations in 1990 and 1991.

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It is shown that fish exposed to water with 10 6 A. salmonicida bacteria per millilitre quickly develop furunculosis. The bacteria has been isolated from seawater more than 20 km from a fish farm with outbreaks of furunculosis. This may explain how the disease has spread along the Norwegian coast, but it does not explain the "longest j u m p s ' the disease has made (Enger, 1990). Possible explanations are live fish transport along the Norwegian coast and escaped fish from fish farms. Both carcasses of fish which have died from furunculosis (McCarty and Roberts, 1980) and other anadromous and marine fish species may be carriers of furunculosis bacteria (McFadden, 1970; Hhstein, 1990). Allen-Austin et al. (1984) postulated that A. salmonicida may survive outside the fish, by entering a dormant phase. In the River Numedalsl~igen, which faced high mortality of salmon during the two first years, we have probably seen a development similar to that in the U K earlier in this century, i.e. from a peak in furunculosis epidemics at the beginning of the century to the low level of today. This is a characteristic pattern when a disease-developing organism meets a new and non-resistant host (Munro, 1987). The experiences from Norwegian rivers have so far shown that wild Atlantic salmon populations can be seriously affected by furunculosis attacks. The disease may appear in both large and small rivers, and it may occur during varying environmental conditions, connected with some kind of stress, such as high density of fish, high water temperature, or low volume of flow and fighting stress in the spawning season.

Minimizing the threat to natural populations A future goal is to minimize the number of cultured fish in wild salmon populations. For genetic, ecological and health reasons, migrant salmon originating from ocean ranching or cage culture represent problems when interacting with wild salmon. A n u m b e r of measures must be taken, among which are the following.

Land-based rearing The most obvious way to reduce gene flow and spread of pathogens from a closed environment is to keep escape rates at a m i n i m u m . Completely contained rearing in tanks, costly as it may seem, may be the least expensive way of reducing the impact of cultured fish on native populations. Complete containment also has some obvious positive effects on fish farming itself. Among these are (1) the economic benefit of not raising fish that escape, (2) the possibility to control incoming and outflowing water, thereby avoiding to a large extent the import and spread of pathogens and reducing inorganic contamination of the locality, (3) better quality control of the flesh of the cul-

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tured fish because of a more controlled environment with respect to temperature and salinity, and (4) reduced feed and labor costs. The increased initial cost of complete containment results partly from investment, and partly from securing rearing water. Sterilization of salmonid fishes is possible on a large scale (Chourrout, 1987 ) and constitutes a complete 'containment' with respect to direct genetic effects. However, sterilization is not preferred to better physical containment because it does not deal with the potential spread of pathogens. Also, there are unresolved questions about the ecology and behavior of sterile fish: the females and some males stay in the sea much longer than their normal life span and their ecological interaction with wild fish must be critically evaluated before large-scale releases of sterile fish can be encouraged.

Area planning, including protected areas Escaped Atlantic salmon are more rare in northernmost Norway, where aquacultural production is small. Even in areas of intense fish culture, rivers located more than 20 km from the nearest fish farm receive fewer escapees than rivers closer to a fish farm (Gausen and Moen, 1991 ). Hence, localization of culture operations may help to protect natural populations. A nationwide plan for the use of the Norwegian coast has recently been issued (Pedersen et al., 1988 ). Accompanying this plan was a list of salmon rivers worthy of protection and a preliminary establishment of protection zones around these rivers to stop new fish farms or hatcheries from being established there during a 5-year period ( 1989-1994). Do these protection zones work? In More and Romsdal county where production is large and escapees numbered more than 1 million fish during 19881989, escaped fish made up an average of 40% of the spawners in eight streams sampled during the a u t u m n of 1989, all of which are situated within a protection zone (Lund et al., 1991 ). These data show that protection zones are virtually worthless in the proximity of large numbers of escaping fish, and that only very large protection zones (e.g. all of northeastern Norway, as suggested by Sthhl and Hindar (1988 )) may offer protection from escapees. The evident conclusions are that the n u m b e r of accidentally released fish must be reduced, and that natural populations in areas of intense fish culture must be protected by moving culture operations away from these rivers and preferably onshore. An essential goal in the development of future ocean ranching is to avoid straying of salmon to neighboring rivers. Large rivers should be selected for sea ranching because straying to other rivers is reduced under such conditions (Quinn and Fresh, 1984). A perfect choice for localization of sea ranching

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operations would be the acidified rivers of southern Norway that have lost their original salmon populations and could support a sea ranching program by liming of the water. In rivers that have native populations, local stocks only should be used in sea ranching, and the release of smolts should always be compared with habitat restoration--including building fishways to increase the productive area--with respect to increasing salmon production with minimal genetic consequences (see Ryman, 1991 ). To reduce straying, the salmon smolts must be released into freshwater, and not in the marine environments outside the river.

Gene banks Extinction of local populations can be counteracted by the establishment of gene banks, i.e. natural or artificial facilities established to maintain population gene pools (Allendorf and Ryman, 1987 ) or gametes (Stoss, 1983 ). In Norway, Atlantic salmon sperm has been cryopreserved from 2800 males from 128 localities (Gausen, 1993). No m e t h o d is available at present for freezing salmonid eggs or embryos, and diploid genomes will have to be restored from cryopreserved sperm by androgenesis (Parsons and Thorgaard, 1985 ). One live gene bank has been established in Norway to secure populations that are close to extinction as a result of Gyrodactylus infection. Increased gene flow makes the management of gene banks based on wild fish difficult because of the problems associated with its timely detection (Allendorf and Phelps, 1981 ), and because all populations are potentially at risk. The establishment of gene banks in such contexts is dependent on correct identification of wild and escaped fish when collecting broodstock for the gene bank.

Reduced or selective fishing Smolt releases in an area may result in increased fishing pressure and harvest of wild salmon in that area. For instance, outside the River Oploy in Central Norway, the gear numbers in the sea increased by about 100% during the first 2 years after the start of ocean ranching (Strand et al., 1992). Many spawning populations of Norwegian Atlantic salmon are so small that it seems inevitable that the total fishing pressure on these populations must be reduced (Hindar, 1992). It is possible, however, that increased knowledge on behavioral differences between escaped and wild fish could be used to increase the fishing pressure on the former while reducing it on the latter. It is known that escaped farmed salmon and salmon released in estuaries or directly into the sea migrate into the rivers later in the season than wild fish and that they are less prone to migrate to the upper reaches of a stream (Hansen et al., 1987b, 1989; Moen and Gausen, 1989; Jonsson et al., 1990 ). Therefore,

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H~stein, T., 1990. Furunkulose som sykdom. Referat/kommunike fra mote om furunkulose 17 januar 1990, Bergen. Norges Fiskeriforskningsr~d, 5 pp. H~stein, T., Lunder, T. and Poppe, T., 1989. De viktigste sjukdommer hos oppdrettsfisk. Fiskehelse og Fiskesykdommer, 6: 389-408. Isaksson, A., 1988. Salmon ranching: a world review. Aquaculture, 75: 1-33. Jensen, A.J., Johnsen, B.O. and Heggberget, T.G., 1991. Initial feeding time of Atlantic salmon, Salmo salar, alevins compared to river flow and water temperature in Norwegian streams. Environ. Biol. Fishes, 30: 379-385. Johnsen, B.O., 1978. The effect of an attack by the parasite Gyrodactylus salaris on the population of salmon parr in the river Lakselva, Misv~er in Northern Norway. Astarte, 11: 7-9. Johnsen, B.O. and Jensen, A.J., 1985. Parasitten Gyrodactylus salaris p~ laksunger i norske vassdrag, statusrapport. Direktoratet for vilt og ferskvannsfisk, Regulerings undersokelsene, rapport 12-85, 145 pp. Johnsen, B.O. and Jensen, A.J., 1986. Infestations of Atlantic salmon, Salrno salar, by Gyrodactylus salaris in Norwegian rivers. J. Fish Biol., 29: 233-241. Johnsen, B.O. and Jensen, A.J., 1988. Introduction and establishment of Gyrodactylus salaris Malmberg, 1957, on Atlantic salmon, Salmo salar L., fry and parr in the river Vefsna, northern Norway. J. Fish Dis., 11: 35-45. Johnsen, B.O. and Jensen, A.J., 1991. The Gyrodactylus story in Norway. Aquaculture, 98: 289302. Johnsen, B.O., Jensen, A.J. and Sivertsen, B., 1989. Extermination of Gyrodactylus salaris infected Atlantic salmon Salmo salar by rotenone treatment in the river Vikja, Western Norway. Fauna Norv., Ser. A, 10: 39-43. Jonsson, B. and Ruud-Hansen, J., 1986. Water temperature as primary influence on timing of seaward migrations of Atlantic salmon (Salmo salar) smolts. Can. J. Fish. Aquat. Sci., 42: 593-595. Jonsson, B., Jonsson, N. and Hansen, L.P., 1990. Does juvenile experience affect migration and spawning of adult Atlantic salmon? Behav. Ecol. Sociobiol., 26: 225-230. Jonsson, B., Jonsson, N. and Hansen, L.P., 1991. Differences in life history and migratory behaviour between wild and hatchery-reared Atlantic salmon in nature. Aquaculture, 98: 6978. Kalleberg, H., 1958. Observations in a stream tank of territoriality and competition in juvenile salmon and trout (Salmo salar L. and Salmo trutta L.) Inst. Freshwater Res., Drottningholm, Rep. 39, pp. 55-99. Le Cren, E.D., 1973. The population dynamics of young trout (Salmo trutta) in relation to density and territorial behaviour. Rapp. P. V. Reun. Const. Int. Explor. Mer., 164:241-246. Lund, R.A. and Hansen, L.P., 1991. Identification of wild and reared Atlantic salmon (Salrno salar) using scale characters. Aquacult. Fish. Manage., 232: 499-508. Lund, R.A. and Heggberget, T.G., 1992. Migration of Atlantic salmon, Salmo salar L., parr through a Norwegian fiord: potential infection path of Gyrodactylus salaris. Aquacult. Fish. Manage., 23: 367-372. Lund, R.A., Hansen, L.P. and J~irvi, T., 1989. Identification of reared and wild salmon by external morphology, size of fins and scale characteristics. NINA Res. Rep. 1, 54 pp. (in Norwegian, English summary). Lund, R.A., Okland, F. and Hansen, L.P., 1991. Farmed Atlantic salmon (Salmo salar) in fisheries and rivers in Norway. Aquaculture, 98:143-150. Lura, H. and Saegrov, H., 1993. Documentation of successful spawning of escaped farmed female Atlantic salmon, Salmo salar, in Norwegian rivers. Aquaculture, in press. Malmberg, G., 1989. Salmonid transports, culturing and Gyrodactylus infections in Scandinavia. In: Parasites of Freshwater Fishes of North-West Europe. Materials of the International

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Symposium within the Program of the Soviet-Finnish Cooperation, 10-14 January 1988, pp. 88-104. McCarty, D.H. and Roberts, R.J., 1980. Furunculosis of fish--the present state of our knowledge. Adv. Aquat. Microbiol., 2" 293-341. McFadden, T.W., 1970. Furunculosis in nonsalmonids. J. Fish. Res. Board Can., 27" 23652370. Moen, V. and Gausen, D., 1989. Romt oppdrettslaks i norske vassdrag 1988. Directorate for Nature Management Trondheim Report 3, pp. 1-26. Munro, A.L.S., 1987. Scottish experience of the occurrence and control of furunculosis. AquaNor 87, Conference 3: Fish Diseases, A Threat to the International Fish Farming Industry, pp. 59-70. Myers, R.A., Hutchings, J.A. and Gibson, R.J., 1986. Variation in male parr maturation within and among populations of Atlantic salmon, Salmo salar. Can. J. Fish. Aquat. Sci., 43:12421248. Naevdal, G., 1981. Fish rearing in Norway with special reference to genetic problems. Ecol. Bull. Stockholm, 85-93. Naevdal, G., Holm, M., Ingebrigtsen, O. and Moller, D., 1978. Variation in age at first spawning in Atlantic salmon (Salmo salar). J. Fish. Res. Board Can., 35:145-147. Noakes, D.L.G., 1980. Social behaviour in young charrs. In: E.K. Balon (Editor), Charrs: Salmonid Fishes of the Genus Salvelinus. W. Junk, The Hague, pp. 683-703. Parsons, J.E. and Thorgaard, G.H., 1985. Production of androgenetic diploid rainbow trout. J. Hered., 76: 177-181. Pedersen, T.N., Aure, J., Berthelsen, B., Elvestad, S., Ervik, A.S. and Kryvi, H., 1988. A nationwide analysis of the suitability of the Norwegian coast and watercourses for aquaculture. A coastal zone management programme. Int. Counc. Explor. Sea, C.M. 1988/F: 11, Copenhagen, 15 pp. Quinn, T.P. and Fresh, K., 1984. Homing and straying in chinook salmon (Oncorhynchus tshawytscha) from Cowlitz River Hatchery, Washington. Can. J. Fish. Aquat. Sci., 41:10781082. Refstie, T., 1987. Selective breeding and intraspecific hybridization of cold water finfish. In: K. Tiews (Editor), Proceedings of the World Symposium on Selection, Hybridization and Genetic Engineering in Aquaculture, 27-30 June 1986, Bordeaux, Vol. I. Heeneman, Berlin, pp. 293-302. Refstie, T., Steine, T. and Gjedrem, T., 1977. Selection experiments with salmon. II. Proportion of Atlantic salmon smoltifying at 1 year of age. Aquaculture, 10: 231-242. Reisenbichler, R.R. and McIntyre, J.D., 1977. Genetic differences in growth and survival of juvenile hatchery and wild steelhead trout. J. Fish. Res. Board Can., 34:123-128. Ricker, W.E., 1972. Hereditary and environmental factors affecting certain salmonid populations. In: R.C. Simon and P.A. Larkin (Editors), The Stock Concept of Pacific Salmon. H.R. MacMillan Lectures in Fisheries, University of British Columbia, Vancouver, B.C., pp. 19160. Riddell, B.E. and Swain, D.P., 199 I. Competition between hatchery and wild coho salmon (Oncorhynchus kisutch)" genetic variation for agonostic behaviour in newly-emerged wild fry. Aquaculture, 98" 16 l - 172. Riddell, B.E., Leggett, W.C. and Saunders, R.L., 1981. Evidence of adaptive polygenic variation between two populations of Atlantic salmon (Salmo salar) native to tributaries of the S.W. Miramichi River, N.B. Can. J. Fish. Aquat. Sci., 38" 321-333. Rikstad, A., 1991. Erfaringer fra furunkuloseutbruddene i Namdalen i 1990. Direktoratet for Naturfolvaltning, Rapport fra fagseminar- Gyrodactylus/Sykdom/Romt risk 15-17 april 1990, pp. 91-93. Ritter, J.A., 1975. Lower ocean survival rates for hatchery-reared Atlantic salmon (Salmo sa-

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a coastal fishery in the period from September to November would probably be more efficient for capturing escaped fish and less so for wild fish than the present fishing season from June to August.

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