ICES Journal of Marine Science, 54: 998-1008. 1997
Genetic impact of escaped farmed Atlantic salmon
(Salmo salar L.) on native populations: use of DNA profiling
to assess freshwater performance of wild, farmed, and hybrid
progeny in a natural river environment
P. McGinnity, C. Stone, J. B. Taggart, D. Cooke,
D. Cotter, R. Hynes, C. McCamley, T. Cross, and
A. Ferguson
McGinnity, P., Stone, C., Taggart, J. B., Cooke, D., Cotter, D., Hynes, R.,
McCamley, C., Cross, T., and Ferguson, A. 1997. Genetic impact of escaped farmed
Atlantic salmon (Sulmo salar L.) on native populations: use of DNA profiling to assess
freshwater performance of wild, farmed, and hybrid progeny in a natural river
environment. - ICES Journal of Marine Science, 54: 998-1008.
Since Atlantic salmon (Salmo salur L.) used for farming are usually genetically
different from local wild populations, breeding of escaped farmed salmon potentially
results in genetic changes in wild populations. To determine the likelihood and impact
of such genetic change, an experiment was undertaken, in a natural spawning tributary
of the Burrishoole system in western Ireland, to compare the performance of wild,
farmed, and hybrid Atlantic salmon progeny. Juveniles were assigned to family and
group parentage by DNA profiling based on composite genotypes at seven minisatellite loci. Survival of the progeny of farmed salmon to the smolt stage was significantly
lower than that of wild salmon, with increased mortality being greatest in the period
from the eyed egg to the first summer. However, progeny of farmed salmon grew
fastest and competitively displaced the smaller native fish downstream. The offspring
of farmed salmon showed a reduced incidence of male parr maturity compared with
native fish. The latter also showed a greater tendency to migrate as autumn pre-smolts.
Growth and performance of hybrids were generally either intermediate or not
significantly different from the wild fish. The demonstration that farmed and hybrid
progeny can survive in the wild to the smolt stage, taken together with unpublished
data that show that these smolts can survive at sea and home to their river of origin,
indicates that escaped farmed salmon can produce long-term genetic changes in
natural populations. These changes affect both single-locus and high-heritability
quantitative traits, e.g. growth, sea age of maturity. While some of these changes may
be advantageous from an angling management perspective, they are likely, in specific
circumstances, to reduce population fitness and productivity. Full assessment of these
changes will require details of marine survival, homing and reproductive performance
of the adults together with information on the F, generation.
0 1997International Council for the Exploration of the Sea
Key words: Age of maturity, Atlantic salmon, DNA profiling, farmed escapes, genetic
variability, growth, local adaptation, Sulmo s&r, survival.
P. McGinnity. D. Cooke, and D. Cotter: Salmon Research Agency of Ireland, Furnace,
Newport, County Mayo, Ireland. C. Stone, R. Hynes, C. McCumley, and A. Ferguson:
School of Biology and Biochemistry, The Queen’s University, Medical Biology Centre,
97 Lisburn Road, Belfast BTP 7BL, Northern Ireland, UK. J. B. Tuggart: Department
of Biological and Molecular Sciences, University of Stirling, Stirling FK9 4LA, Scotland,
UK. T. Cross: Zoology Department, University College, Cork, Ireland. Correspondence
to McGinnity.
Introduction
Studies using protein, mitochondrial DNA, and minisatellite and microsatellite molecular markers have
shown genetic differentiation among Atlantic salmon
1054-3139/97/060998+ 11 $25,00/0/jm970286
(Sulmo salur L.) populations
(e.g. StBhl,
1987;
McConnell et al., 1995; Stone et al., 1997). Variation
among populations also occurs in various quantitative
traits, such as morphology, age of maturity, and timing
of juvenile and adult migrations (e.g. Taylor, 1991;
0 1997 International Council for the Exploration of the Sea
Escaped farmed Atlantic salmon and native populations
Heggberget et al., 1993). The genetic variation among
salmon populations is often regarded as reflecting local
adaptation although, in most cases, the evidence is
circumstantial. Alternatively, much of the genetic differentiation may result from genetic drift. The precise
homing of Atlantic salmon means that “populations”
are geographically restricted and thus genetically effective population sizes are small. Extinction and recolonization can also result in drift due to founder effects. For
quantitative traits, differences can occur among populations as a result of environmentally induced differences
in trait expression. Thus genetically identical populations may differ in such traits (e.g. age of maturity),
although this gene-environmental
interaction plasticity
may in itself be adaptive (Adkison, 1995).
It is important for management purposes to obtain
information on the extent to which Atlantic salmon
interpopulation
variation reflects local adaptation and
thus affects the fitness, productivity, and characteristics
of local populations. In particular, concern has arisen
over the extent to which deliberate or inadvertent introductions of salmon may adversely change the genetic
make-up of native populations (Hindar et al., 1991).
One major source of introductions
is the salmon
farming industry. Farming of Atlantic salmon has
increased dramatically in the past 20 years with the total
European production being in excess of 400 000 tonnes
in 1996, many times greater than that of wild salmon. As
rearing from the smolt stage is mainly in sea cages,
rather than land-based units, escapes inevitably occur
during routine handling, and losses occur, at least on a
small scale, from most sites each year (Webb et ul.,
1991). On occasions, large-scale escapes occur, as a
result of storm damage to the cages, involving tens or
even hundreds of thousands of fish (Gausen and Moen,
1991).
The Atlantic salmon used for farming are generally
genetically different from local wild populations, often
being derived from geographically remote populations.
For example, many of the farmed strains used in Ireland
and Scotland are of Norwegian origin (Cross and
N T Challanain,
1991; Youngson et al., 1991). In
addition to genetic differences as a result of their origins,
farmed fish are often genetically distinct from those
of the native populations in the rivers which they enter
as a result of directional and inadvertent selection,
hybridization, and genetic drift (Skaala et al., 1990).
Clifford et al. (1997a) have demonstrated that juvenile
salmon escaping from a farm unit into a river successfully completed their life cycle and homed accurately to
breed, and interbreed with native salmon, in that river.
Similarly, studies of escaping adults have shown that
they can breed successfully, or more usually interbreed
with native fish, in the rivers which they enter, thus
altering the genetic make-up of native populations
(Crozier, 1993; Clifford et al., 1997b). This introgression
999
of foreign genes into native gene pools may have a
detrimental impact on local adaptation and thus on the
productivity and character of the native stocks. Utter
et al. (1993) contend that “interbreedings among genetically diverged salmonid populations
are generally
disadvantageous
to the natural populations”.
They
acknowledge, however, that: “The direct experimental
evidence for this contention
is admittedly sparse,
basically because - to our knowledge - appropriate
experiments to clarify this critical issue have not been
carried out”.
A direct way of determining the impact of this genetic
change on the fitness, productivity, and characteristics of
individual Atlantic salmon populations is to compare
the performance of wild, farmed, and hybrid progeny
identical
environmental
conditions.
Until
under
recently, such an experiment was not feasible as salmon
had to be reared separately, for several months, before
being large enough to tag. This separate rearing makes it
difficult to distinguish environmental and geneticallymediated differences and makes a comparison at the
early, high mortality stage impossible. DNA profiling
now enables the identification of an individual’s parentage and thus allows a direct comparison, under common
environmental conditions from the egg stage onwards,
of traits related to fitness (Ferguson et al., 1995a, b).
This paper describes such an experiment which was
undertaken in a natural spawning tributary of the
Burrishoole system, western Ireland.
Materials and methods
Experimental
stream
populations
The Burrishoole river system consists of Lough Feeagh,
a freshwater lake (410 ha) fed by a series of afferent
rivers. There are two outlets from Lough Feeagh to the
tidal Lough Furnace, both of which have permanent
upstream adult and downstream smolt trapping facilities. The experiment was undertaken on one of the rivers
entering L. Feeagh, the Srahrevagh River, and involved
an area of 7250 m2 of prime juvenile salmonid habitat. A
trap, capable of capturing all downstream and upstream
migrants from the smallest emergent fry to returning
adults, was constructed in the lower part of the river.
Natural spawners were excluded from the experimental
river in 1992 and 1993. Juvenile salmon from the 1991
natural spawning were present in the river until May
1994, with those from the 1994 natural spawning being
present from April 1995.
Parental fish for the experiment consisted of native
adult Atlantic salmon captured in the Burrishoole system during their spawning migration in December 1992
and December 1993. The 1992 Burrishoole broodstock
consisted of six wild females and eight wild males and
the 1993 broodstock of 11 wild females and 11 wild
P. McGinnity et al.
1000
Table 1. Families and groups established for the 1993 and 1994 cohorts.
Cohort
Group
No. of
families
No. of
eggs
1993
1: wild female x wild male
2: wild female x farmed male
3: farmed female x farmed male
4: farmed female x wild male
1: wild female x wild male
2: wild female x farmed male
3: farmed female x farmed male
4: farmed female x wild male
6
6
15
8
11
11
11
11
5213
5886
14 991
8659
10 531
10 531
10 537
10 531
1994
The farmed salmon were from the most commonly used strain in the Irish industry, which had been
derived from Norwegian Mowi stock by imports of eggs
between 1982 and 1986. Thereafter, the breeding system
was closed and a broodstock line maintained on the
farm. The original Mowi stock was established in the
1960s and so the farmed strain had been in culture for
some six to eight generations. The farmed broodstock
consisted of 15 females and 15 males in 1992 and 11
females and 11 males in 1993. Synchronous stripping
and fertilization was carried out to produce half-sib
families and progeny groups as listed in Table I. In
addition,
25 families and 25 975 eggs involving
Burrishoole ranched salmon parents were also produced
in 1992 but the data from these families are not considered in this paper, other than in terms of total numbers
of eggs, parr and smolts. A muscle tissue sample of each
parent was retained for DNA profiling.
The families established from the December 1992
broodstock, and which hatched in spring 1993, were
designated as the 1993 cohort. Similarly, the families
established from the December 1993 broodstock were
designated as the 1994 cohort. Fertilized eggs were
incubated in the hatchery on the Burrishoole system
until the eyed stage was reached.
For the 1993 cohort, eyed eggs (60 790) from 60
families (including those of ranched parentage) were
planted in the experimental stream on 4 March 1993.
For most families 1000 eyed eggs were counted and
placed in individual plastic mesh envelopes in wire
baskets of 16 artificial redds (design according to E.
Verspoor, Marine Laboratory, Aberdeen, Scotland).
For 12 of the families less than 1000 ova were available
and this was counterbalanced by using more of other
families to ensure that a similar number (14 394 to
15 740) was planted out for each of the four main
groups, i.e. native (wild+ranched), farmed, and both
sets of reciprocal hybrids.
For the 1994 cohort, eyed eggs (42 148) from 44
families were planted in the experimental river on 26
February 1994. The numbers of individuals from each
family ranged from 500 to 1500, but with equal numbers
males.
(10 537) in each of the four groups. In 1994 the ova from
all families were thoroughly mixed before being apportioned to the envelopes and thus were randomly planted
out in 12 artificial redds.
Hatchery
controls
For the 1993 cohort, aliquots of 250 ova of each family
were retained in the hatchery, in separate hatching
boxes. Pre-first feeding alevins were transferred (April
1993) to a single 2 m radial flow tank and reared under
a standard farm regime. A sample of on-growing parr
was taken from this group on 25 August 1993. On 24
November 1993 the parr were sorted into small (ll%),
medium (45%) and large (44%) size grades and transferred to three separate 2 m tanks. During the grading
procedure a sample of mature male Parr, as shown by
expression of milt on handling, was collected. A sample
of fish, which showed external signs of becoming smolts,
was taken from the large and medium grade tanks in
March 1994.
For the 1994 cohort, aliquots of 200 ova from each
family were retained, reared, and sampled as for the
1993 cohort. However, prior to grading, 1500 parr were
removed at random and on-grown in a single tank from
which the March 1995 pre-smolt sample was taken.
Sampling
A sample of 230, 0+ salmon from the 1993 cohort was
obtained in August 1993 by electrofishing. Length was
measured on site and the salmon parr immediately
frozen on dry ice for transport and storage. Samples of
the 1994 cohort were obtained by electrofishing in
August 1994 (650, 0+) and in June 1995 (800, l+).
These fish were transported alive to the laboratory,
where details of weight and length were recorded and
separate aliquots of muscle tissue frozen and preserved
in 95% ethanol,
The Srahrevagh River trap started operation on 30
April 1993 and was examined on a daily basis from that
date. For the 1993 cohort, from the beginning of
Escaped farmed Atlantic salmon and native populations
trapping to 21 August 1993 all 0+ fish, salmon and
trout, were sacrificed and preserved in 95% ethanol for
species identification and genetic profiling of salmon.
From 22 August 1993 onwards only salmon were
sampled as accurate species identification could be made
visually on site. From 21 August 1993 to 26 August 1994
approximately one in every five salmon parr was killed
for analysis, with the others being adipose fin-clipped
and released downstream. From 27 August 1994 adipose
finclips were taken from the autumn and spring migrants
and the fish were released downstream. From 11
October 1994 these fish were VI tagged and Panjet
dye-marked prior to their release downstream. From 2
January 1995 to the end of the smolt migration on 20
April 1995 the fish were also coded wire tagged. The
main downstream traps at Furnace were examined on a
daily basis throughout the 1995 smelt run and all
fin-clipped smolts monitored.
All parr and smolts originating from the 1994 cohort
were sacrificed at the Srahrevagh river trap and
preserved in 95% ethanol.
Individual fish were aged by scale inspection following
standard procedures. Age designation follows standard
terminology. Thus fish in the first year of life were
denoted as 0+ and in the second year, subsequent to
winter annulus formation, as 1 +.
Parentage
identification
DNA was extracted from frozen or ethanol preserved
tissue samples (skeletal muscle or adipose fin). Parental
and progeny samples from both cohorts were screened
at minisatellite
loci Str-AS, Str-A9, Str-A22/1,
Ssa-A45/1, Ssa-A45/2/1, Ssa-A60. Minisatellite locus
Ssa-A34 was used in addition for the 1994 cohort parr
and Ssa-1OM and Ssu-11 were used instead of Ssa-A4511
and Ssa-A60 for the 1994 cohort smolts. Details of the
procedures used for minisatellite analyses at these loci
are given in Prodiihl et al. (1994) and Taggart et al.
(1995). Individual progeny were identified to family and
group parentage by comparing their composite genotypes at these loci with expected Mendelian genotypes as
described by Ferguson et al. (1995a, b). This was accomplished using a specifically-designed computer program
(Family Analysis Program; J. B. Taggart, University of
Stirling, Stirling, Scotland, unpublished). This program
also predicted the resolving power for discriminating
among groups. With the five to 12 discrete allele classes
resolved at each locus, greater than 90% of individuals
could be identified to parentage group. Any individuals
which could not be unambiguously assigned to a single
group were excluded from the data analyses. Expected
numbers in a sample were corrected for the slightly
different proportions of each group which could be
unambiguously assigned and for the differing numbers
of eggs in the case of the 1993 cohort.
Statistical
analyses
1001
of data
The null hypothesis that the farmed and hybrid groups
did not differ in their survival from the wild group was
tested by comparing observed and expected numbers
using goodness-of-fit G-tests incorporating Williams’
correction (Sokal and Rohlf, 1995). Each of three
groups was tested against the wild group and significance values corrected for multiple tests using the
sequential Bonferonni method.
Length, weight, and condition factor data were tested
for normality
and equality of variance by the
Kolmogorov-Smirnov
test for goodness-of-fit, Bartlett’s
test for homogeneity of variance, and Hartley’s F-test.
As neither native nor log,, transformed data met the
requirements for parametric analyses they were subsequently analysed using the Kruskal-Wallis
nonparametric one-way ANOVA and, if this showed
significant overall heterogeneity, unplanned pairwise
comparisons were carried out using Dunn’s multiple
comparison test.
Results
Survival
and migration
Details of the samples analysed, numbers identified
to group by DNA profiling, and G-test results for
significant frequency differences relative to the wild
group, are given in Table 2. Abundance of a group in a
sample is determined by both mortality and emigration
from the experimental river and is therefore denoted as
“representation”.
Electrojished samples
Both the 1993 and 1994 August 0+ electrofished samples
of the 1993 and 1994 cohorts respectively showed
significantly lower representation of the farmed group
compared to the wild group. In the 1993 August 0+
sample there was a significant over-representation of the
wild-mother hybrid group, but significant deficits of
both hybrid groups occurred in the 1994 August 0+
sample. In the June 1995 electrofished sample of the
1994 cohort 1 + Parr, the farmed group was still significantly under-represented compared to the wild group
but the hybrid groups did not now show significant
deficits. The farmed group representation was 53%, 51%,
and 77% of the wild group in the 1993 cohort August
O+, and 1994 cohort August 0+ and June 1 + samples,
respectively.
Trap samples
Parr were first captured in the downstream trap from the
1993 cohort on 30 April 1993 and from the 1994 cohort
on 6 May 1994. In both cases parr continued to be taken
in the trap until mid-May of the following year. A
P. McGinnity et al.
1002
Table 2. Summary of G tests for pairwise comparisons of the frequencies of groups 2 (wild-mother
hybrid), 3 (farmed), and 4 (farmed-mother hybrid) against group 1 (wild) with significant differences
indicated by + (more than group 1) and - (less than group 1). Cohort indicates either the 1993 cohort
or the 1994 cohort samples.
Cohort
Sample
Sample
size
1993
1994
1994
1993
1993
1993
1993
1994
1994
1994
1994
1993
1993
1993
1994
Electrofishing Aug 1993 0+ parr
Electrofishing Aug 1994 0+ parr
Electrofishing Jun 1995 1+ parr
Trapped parr May 1993-May 1994
Trapped pre-smolts+smolts Sep 1994Apr 1995
Trapped pre-smolts Sep 1994Feb 1995
Trapped smolts Mar 1995-Apr 1995
Trapped parr May 1994May 1995
Trapped pre-smolts+smolts Sep 1995-Apr 1996
Trapped pre-smolts Sep 19955Feb 1996
Trapped smolts Mar 1996-Apr 1996
Hatchery control 0+ parr Aug 1993
Hatchery control mature 0+ parr Nov 1993
Hatchery prior to release as smolts Mar 1994
Hatchery prior to release as smolts Mar 1995
127
485
627
307
125
42
83
529
110
31
79
96
76
311
118
smaller proportion
(p<O.OOl) of migrants
occurred from the 1994 cohort, Thus, in this l-year
period, 2012 migrants were captured from the 1993
cohort (3.3% of the ova planted) but only 743 from the
1994 cohort (1.8% of the ova planted).
During the period 30 April 1993 to 17 May 1994 for
the 1993 cohort, and 6 May 1994 to 22 May 1995 for the
1994 cohort, there were significantly fewer parr of the
farmed and hybrid groups taken in the trap compared to
the wild group. Farmed parr representation was 30%
of the wild parr for the 1993 cohort and 24% of the
wild parr for the 1994 cohort. Overall, the hybrids
showed 57% representation in the trap relative to the
wild group.
Only 12 individuals of the 1993 cohort moved through
the trap in the period from 18 May to 26 August 1994,
and only four individuals were taken from the 1994
cohort from 23 May 1995 to 26 August 1995. From 27
August onwards, in both years, further migrations took
place which continued until 20 April 1995 for the 1993
cohort and 22 April 1996 for the 1994 cohort. From 27
August 1994 to 28 February 1995 this involved 143
significantly
individuals
for the 1993 cohort. This is referred to
hereafter as the autumn pre-smolt
migration.
In the
period from 1 March 1995 to 20 April 1995, 163 salmon
of the 1993 cohort were taken in the trap and, as these
fish were silvering and starting to assume the appearance
of smolts, this is denoted as the spring smolt migration.
Similar autumn and spring migrations occurred for the
1994 cohort involving 49 and 109 individuals respectively. Both autumn and spring smolts, of the 1993
cohort, tagged at the experimental river trap were recap-
Groups
significantly
different
from group 1
2+, 32-,3-,432-,3-,4None
3-,42+
2-,3-,4None
3-,4None
None
2-,3None
None
tured at the main sea entry traps downstream of Lough
Feeagh in late April and May 1995. There was no
significant difference (p=O.425) in survival between the
autumn pre-smolts and the spring smolts to the lower
traps.
The autumn pre-smolt migrants for both cohorts
showed significantly fewer individuals of the farmed and
farmed-mother hybrid groups relative to the wild group.
Over both cohorts, autumn migrants accounted for 58%
of the total smolt output for the wild group, compared
with 14% for the farmed group and 36% and 15% for
wild-mother and farmed-mother hybrid groups respectively. For the 1993 cohort, there was a significantly
greater number of the wild-mother hybrid spring smolts
compared to the wild spring smolts but no significant
differences, relative to the wild group, were present in
the 1994 cohort. Taking the overall autumn and spring
smolt output together there were no significant differences from the wild group in either cohort. The actual
number of farmed smolts in the 1993 cohort was 83% of
the wild smolts compared with a corresponding value of
81% for the 1994 cohort, although, as noted, these
frequencies were not significantly different on the basis
of goodness-of-fit G tests. However, in all three electrofished samples and total smolt outputs for both
cohorts, the pure farmed group ranked 4th. The exact
probability of this occurring is 0.001, indicating significantly poorer survival of this group throughout. For the
1993 cohort in the August 0+ electrofished sample and
in the total smolt output, wild-mother and farmedmother hybrid groups ranked 1st and 2nd respectively.
In the 1994 cohort, these hybrid groups ranked 2nd and
Escaped farmed Atlantic salmon and native populations
3rd, but with the rank position being inconsistent among
samples. Overall, the hybrids produced 88% of smolt
output relative to the wild, although the difference is not
statistically significant using either G or exact tests.
Eighty-seven adipose fin clipped, but otherwise
unmarked, smolts (22% of the total output) were
observed at the main seaward traps downstream of
Lough Feeagh in April and May 1995. Most of these fish
must have left the experimental stream as parr prior
to 27 August 1994 as only 10 autumn pre-smolts
passed through the trap between 27 August 1994 and
11 October 1994 when VI tagging and dye-marking
commenced.
The farmed group was significantly
under-represented in this sample of smolts.
Smolt age was examined in both cohorts and was
found to be almost exclusively 2 + . Age was determined
for a sample of smolts taken at the main sea entry traps
downstream of L. Feeagh (n=45) in 1995 and all were
found to be 2+ and thus derived from the 1993 cohort
only. In the June 1995 electrofishing (n = 797), age determination was carried out for 23 fish from the upper tail
of the length frequency distribution (i.e. individuals
most likely to be older). One definite 2+ individual was
found, with the remainder being l+. A further 100
individuals taken at random from this sample were all
found to be 1 +. Age determination was undertaken for
64 autumn and spring migrants from the 1994 cohort
and 60 of these were found to be either 1 + (i.e. autumn
migrants which would become 2 + smolts) or 2 + (spring
migrants). Age determination was not possible with
certainty for the remaining four fish.
Hatchery controls
No significant differences in survival were found among
the four groups in the August 1993 0+ sample of the
1993 cohort or in the pre-smolt samples taken in March
1994 and March 1995 of the fish destined to become 1+
smolts in the 1993 and 1994 cohorts respectively. In the
1993 cohort large and medium grade tanks, 99% of the
parr became l+ smolts. In the 1994 cohort ungraded
tank, 91% of the parr became l+ smolts. In the latter
situation, there were significantly (p=O.O03) more wild
fish in the remainder which were too small to become 1 +
smolts and were thus not included in the pre-smolt
sample.
Growth
Results of Kruskal-Wallis
one-way ANOVA and
unplanned Dunn’s Multiple Comparison analyses of
length, weight, and condition factor are given in Table 3.
1003
showed the wild-mother hybrid and farmed fish to be
significantly longer than wild fish.
In the August 1994 electrofished sample of the 1994
cohort, significant heterogeneities were found in overall
group comparisons for length, weight, and condition
factor. As in the 1993 cohort, the farmed group was the
smallest of the groups. However, wild progeny, despite
being the smallest, had the highest condition factor.
Weight and length differences among groups seen
in the August 1994 electrofishing sample were still
present in the June 1995 sample. The rank order of the
groups with respect to length was the same in both
samples (farmed>farmed-mother
hybrid>wild-mother
hybrid>wild). However, contrary to the August 1994
sample there was no longer significant heterogeneity in
condition factor among the groups.
The length of all groups combined was significantly
greater (p=O.Ol) in the August 1993 0+ electrofished
sample compared to those taken in the trap in the
following 17 days, i.e. the migrants were significantly
smaller than the parr remaining in the river.
Hatchery controls
In the August 1993 sample of the 1993 cohort there was
significant heterogeneity among groups in length and
weight, with fish in the wild-mother hybrid and farmed
groups being larger than fish in the wild group. No
differences in condition factor were found in this sample.
Heterogeneity among groups for length and weight was
found in the March 1+ smolt samples of both cohorts
with farmed smolts being larger than wild smolts.
Heterogeneity was present for condition factor in the
1993 cohort March l+ smolt sample with wild smolts
having a significantly higher condition factor than
farmed smolts.
Parr maturity
In the autumn pre-smolt migrants, 76% of individuals of
the 1993 cohort and 87% of the 1994 cohort were
sexually mature males. In both cohorts, a significantly
greater proportion of the mature male parr belonged to
the wild group (48%) and a significantly lower proportion to the farmed group (7%). The hybrids showed
intermediate values (30% and 15% for the wild-mother
and farmed-mother groups respectively).
There was a significantly lower frequency of wildmother hybrid and farmed fish relative to wild fish in the
sample of mature male parr taken from the 1993 cohort
hatchery control in November 1993.
Discussion
River samples
An overall Kruskal-Wallis test indicated significant heterogeneity in the length of juvenile parr among groups in
the 1993 cohort August sample. Multiple comparisons
Experimental
design
Fleming et al. (1996) showed that, in some situations
at least, farmed salmon are likely to be relatively
P. McGinnity et al.
Table 3. Summary of Kruskal-Wallis one way ANOVA among groups for length, weight, and
condition factor. (See Table 1 for designation of groups.) Where a significant overall heterogeneity
value was obtained, Dunn’s Multiple Comparison Test was used for pairwise comparison of groups
within the sample. Groups which are significantly different at the 95% confidence level are noted, with
the larger group in the comparison preceding the smaller, e.g. Gpl>GpZ.
Cohort
1993
1994
1994
1993
1993
1993
1994
1993
1994
1994
1993
1993
1993
1994
1993
1994
1994
1993
1993
1993
1994
Parameter and sample
Length
Electrofishing Aug 1993 0+ parr
Electrofishing Aug 1994 0+ parr
Electrofishing Jun 1995 I + parr
Hatchery control 0+ parr Aug 1993
Hatchery mature 0+ parr Nov 1993
Hatchery presmolts Mar 1994
Hatchery presmolts Mar 1995
Weight
Electrofishing Aug 1993 0+ parr
Electrofishing Aug 1994 0+ parr
Electrofishing Jun 1995 1+ parr
Hatchery control 0+ parr Aug 1993
Hatchery mature 0+ parr Nov 1993
Hatchery presmolts Mar 1994
Hatchery presmolts Mar 1995
Condition factor
Electrofishing Aug 1993 0+ parr
Electrofishing Aug 1994 0+ parr
Electrofishing Jun 1995 1+ parr
Hatchery control 0+ parr Aug 1993
Hatchery mature 0+ parr Nov 1993
Hatchery presmolts Mar 1994
Hatchery presmolts Mar 1995
unsuccessful in the wild due to competitive and reproductive inferiority. The Burrishoole experiment was
designed to eliminate behavioural differences among
spawning adults and determine genetic aspects of performance, assuming successful reproduction. Throughout the experiment every effort was made to eliminate
environmental variables and thus to provide a true test
of genetic differences contributing to variation in freshwater survival, migration and smolting of juvenile
Atlantic salmon of wild, farmed and hybrid parentage.
The experimental families were established by stripping
gametes and fertilizing eggs synchronously. Eggs were
then placed in a common hatchery environment which
uses water from the Burrishoole system. Before the eyed
egg stage it is difficult to distinguish between fertilized
and unfertilized salmon eggs. In addition, it is potentially damaging to handle and count fertilized eggs until
the eyed stage. By introducing eyed eggs to the stream it
was possible to ensure that only viable eggs were
used and that these could be counted accurately.
While it is possible that rearing to the eyed stage in
culture could have affected subsequent survival this
is unlikely given the uniform performance of all groups
in the hatchery controls. In the second cohort, all
eggs were mixed before being introduced to the exper-
Overall
heterogeneity
(P)
Yes (0.0007)
Yes (0.0000)
Yes (0.0000)
Yes (0.0003)
No (0.1911)
Yes (0.0016)
Yes (0.0000)
No data
Yes (0.0001)
Yes (0.0000)
Yes (0.0004)
No data
Yes (0.0016)
Yes (0.0000)
No data
Yes (0.0014)
No (0.6204)
No (0.2935)
No data
Yes (0.0111)
No (0.3466)
Multiple
comparions tests
Gps 2,3>Gp 1
Gps 2,3,4>Gp 1 and Gp 3>Gp 2
Gps 2, 3,4>Gp 1
Gps 2,3>Gp 1
Gps 3,4>Gp 1
Gps 2,3>Gp 1 and Gp 3>Gp 4
Gps 3,4>Gp 1
Gps 3,4>Gp 1
Gps 2,3=-Gp 1
Gps 3>Gp 1
Gps 2,3>Gp 1 and Gp 3>Gp 4
Gpl>Gps2and3
Gp l>Gp 3
imental river in order to minimize the impact of
redd location on survival. The experiment was carried
out in two successive years with some variations in
the protocol. The concordance of the results in the
two cohorts considerably increases confidence in the
findings.
A novel and unique part of the experiment was the use
of single locus minisatellite DNA profiling for identification of parentage. As far as is known, this is the first
time that this approach has been used to identify fish
families on this scale and under natural conditions.
Blind testing of replicates suggested that the accuracy of
identification exceeded 98% for individuals which could
be unambiguously matched to a single family. In practice, however, the approach was very time-consuming
and expensive. Current developments in microsatellite
technology and automation are enabling DNA profiling
to be carried out more quickly and cheaply (Jarne and
Lagoda, 1996; O’Reilly et al., 1996). Several authors
(e.g. Hard, 1995) have argued that quantitative genetic
variation in life history, physiological, and behavioural
traits is more relevant than single locus molecular variation to adaptation and thus to fisheries management
and conservation. DNA profiling enables, for the first
time, relative fitness of quantitative life history traits to
Escaped farmed Atlantic salmon and native populations
be investigated in natural populations
(Ferguson et al., 1995a, b).
Juvenile
survival,
migration,
in a realistic way
and maturity
Frequencies of the farmed group in the parr and smolt
samples were significantly lower compared to the wild
group. In general the hybrids, with the exception of
wild-mother hybrids in the 1993 cohort, were intermediate between the wild and farmed groups in frequency. As
the proportion of both farmed and hybrid parr taken in
the trap was lower than for the wild, the lower representation of these groups in the parr samples from the river
and in the smolt samples is thus a reflection of poorer
survival in the river rather than greater emigration from
the river. From August of the first summer to the smolt
stage, the frequencies of the farmed and hybrid groups
increased relative to the wild. This would not appear to
be the result of increased relative survival in this period
but rather of relatively fewer individuals emigrating
compared to the wild group.
Downstream emigration seems to have been induced
by density-dependent factors. Thus, in the second cohort
relative downstream dispersal was only 55% of the first
cohort. This would suggest that the ova planting density
in 1994 (5.8 m-‘) was closer to the carrying capacity of
the stream than in 1993 (8.4 m - 2). These relatively high
values of ova planting were deliberately chosen since
when escaped farmed salmon enter a river they do so in
addition to the natural fish and thus ova deposition and
subsequent competition are likely to be increased.
Although the number of parr moving downstream was
significantly different for the two cohorts, the pattern of
movement was the same in each year (wild>wild-mother
hybrid>farmed-mother
hybrid>farmed).
This is the
inverse of the rank order of the mean lengths of the
groups and would suggest that the smaller fish were less
able to compete and dispersed downstream. Further
evidence for downstream movement of smaller fish is
given by the significantly larger size of fish in the August
1993 electrofished sample compared with those taken in
the trap in the subsequent 17 days. In spite of this being
a period of rapid growth, these fish taken later in the
season were smaller than those in the river. Thus the
faster-growing farmed and hybrid offspring competitively displaced the smaller native fish, especially under
the higher density conditions of the 1993 cohort, and
thereby increased their relative frequency in the river.
This faster growth of farmed progeny is not surprising
given the selective breeding which has been undertaken
in the farmed strain for this trait and is likely to be a
characteristic of all established farm strains. Increased
growth rate of the farmed fish may also be the result of
behavioural differences with native fish being dominated
by the farmed fish (Einum and Fleming, 1997). However, although the farmed group showed the fastest
1005
growth, the condition factor of this group, in the 1994
cohort (data not available for 1993 cohort), was the
lowest of the four groups, being significantly lower than
the wild group. This difference in condition factor could
be the result either of reduced nutritional status or
difference in body shape, both of which may have
survival implications.
Given the high overall mortality which normally
occurs from eyed-egg to first summer (mean 92% in this
experiment) there is ample opportunity for differential
survival in the period from hatching to the first summer.
By contrast, in the hatchery, it is possible to minimize
this mortality, in this case to approximately 100/o, by
supplying a surplus of food and providing a protected
environment. In keeping with this, no difference in
survival was observed among the four groups of both
cohorts in the hatchery controls through to smolting.
Wild and farmed progeny showed a further difference
in migratory
behaviour in the “autumn”
period
(September to February) prior to smolting with a significantly greater proportion of the wild group emigrating in this period compared to the farmed group. As far
as survival to smolts passing through the main Furnace
traps to the sea is concerned, there was no difference in
survival between fish which passed through in the
autumn period and the spring period (March and April).
In the Girnock Burn, a tributary of the River Dee in
Scotland, a substantial part of the annual production of
migrant pre-smolt juveniles leaves the river in autumn
rather than in spring. In this river, Youngson et al.
(1994) demonstrated. by coded wire tagging of migrants,
that adult recapture rates were similar for autumn and
spring migrants. Thus autumn migration is a component
of smolt migration. As was also recorded in the Girnock
Burn, a high proportion of the autumn migrants, in this
study, were mature males. Similarly, in the hatchery
control, there was a significantly greater proportion of
mature parr in the wild group. This is contrary to the
suggestion that faster-growing individuals are more
likely to mature early (Fleming, 1996) and implies a
heritable basis to male parr maturity.
Salmon that moved downstream through the trap as
Parr, prior to the second autumn, were later recovered at
the Furnace sea-entry traps. Thus these fish must have
survived in the river downstream of the trap or in the
freshwater Lough Feeagh, which is known to provide
suitable habitat for Parr. These smolts comprised a
significantly higher proportion of the wild group and,
when this is taken into account, the overall farmed smolt
output was only 56% relative to the wild. However, in
many situations displaced parr would not be able to
survive and so it could be argued that only a comparison
with respect to the experimental stream is valid. Irrespective of whether the comparison is restricted to the
experimental stream or involves the overall smolt production from the planted eggs, there is significantly
P. McGinnity et al.
1006
lower smolt output from the farmed progeny than from
the wild, with only the extent of mortality difference
being altered.
Although the farmed fish were derived from I+
smolts they migrated as 2+ smolts from the river
indicating that age of smolting is predominantly determined by growth opportunity, as shown experimentally
by Thorpe et al. (1989).
Impact
natural
of escaped
populations
farmed
Atlantic
salmon
on
This study has shown that farmed and hybrid progeny
can survive in the natural environment to the smolt
stage. Thus the intrusion of escaped farmed salmon into
a river, with a natural population of salmon, will have
both ecological and genetic effects. The impact that this
will have on the total smolt output of a river will depend
on the overall density of juveniles relative to the carrying
capacity. Where natural juvenile production is lower
than the carrying capacity, escaped farmed fish could
result in an increase in smolt output. Where the carrying
capacity is reached, the higher competitive ability of the
farmed and hybrid progeny will result in a reduction in
smolt output from the wild group. However, if the
farmed and hybrid fish displace an equivalent number of
wild fish, the total smolt output may not be affected. It is
possible, although there is no evidence to support the
supposition, that the faster growing farmed and hybrid
fish may require more food, and thus a larger territory,
and may displace more than an equivalent number of
wild fish.
The impact of the replacement of wild salmon by
farmed and hybrid fish on the adult return to the river
will depend on survival during the marine phase of the
life cycle, ability to home to the natal river, and on
reproductive
competence. Smolts (15 000 of 1993
cohort, 11 300 of 1994 cohort) produced from the hatchery controls in this experiment were released to sea (i.e.
ranched) in 1994 and 1995 respectively. Preliminary
analysis of returning adults (authors’ unpublished data)
has shown that salmon of farmed and hybrid parentage
can survive at sea and home to their river of origin. Wild
salmon, as expected from their grilse parentage, returned
almost exclusively as one-sea-winter-fish. Many hybrids,
especially farmed female x wild male, returned as 2SW
salmon. Few pure farmed fish have returned but as these
were of 3SW and 4SW parentage, they may yet do so in
subsequent years, although it is unlikely that the return
rate will be substantial given the normally high mortality
at sea of such age groups. The sea age of return of the
hybrids is in keeping with the high heritability of age of
maturity in Atlantic salmon. For example, in a ranching
experiment in Iceland, the estimated heritability of this
trait was 0.71 (J. Jonasson, Stofnfiskur, Reykjavik,
Iceland, pers. comm.).
A poor return of farmed salmon from the sea would
result in a reduction in the fishing productivity and
spawning escapement in a river. Thus the farmed parr
displace wild fish but their ability to complete the life
cycle is much reduced. Repeated incursions of escaped
farmed salmon, as typically occurs, will inevitably
depress the smolt productivity in a cumulative fashion,
potentially resulting in an extinction vortex.
Breeding by escaped farmed salmon is more likely to
be with native fish than with other escaped individuals as
a result of sex bias in the reproductive performance of
farmed fish and non-discriminatory
mate choice by
males (Fleming et al., 1996; Clifford et al., 1997a, b). The
performance of the hybrids, therefore, is much more
important than that of pure farmed progeny and the
impact of escaped farmed salmon on natural populations is likely to be primarily through hybridization. In
this study, the hybrids were generally intermediate
between the wild and farmed fish in survival, migration,
growth and parr maturity and often were not significantly different in these measures from the wild fish.
There was no conclusive evidence of hybrid vigour,
although the wild x farmed hybrids did show a significantly higher survival than the wild fish in the 1993
cohort only. Similarly, there was no evidence of outbreeding depression, indicating that the native and
farmed salmon examined here are not sufficiently distinct genetically for this to occur, not at least in the first
generation. However, unless genetic differences between
hybridizing populations are large, outbreeding depression may not occur until coadapted gene complexes have
been disrupted by recombination in the second or later
generations (Gharrett and Smoker, 1991; Hard, 1995).
Assuming that the returning hybrids are reproductively competent, the survival of these fish will result in
introgression of farm genes into natural populations.
This will result in changes in the genetic make-up of
native populations, both in respect of single locus and
polygenic characters. Regarding the latter, changes in
high-heritability
quantitative
traits,
for example,
growth, male parr maturity and sea age of maturity, are
likely to result. Thus it must be considered a distinct
possibility that escaped farmed salmon will result in an
increase in age of maturity in native populations. An
increase in multi-sea-winter salmon may be seen as
desirable from an angling perspective and a current goal
of salmon management. However, in spite of the higher
fecundity of these larger fish, it may have a detrimental
effect on fitness and productivity in native populations.
In some rivers, selection may be against large salmon
because low water flows make successful ascent and
breeding by larger fish more difficult (Fleming, 1996).
Before definitive statements can be made as to the effect
on fitness and productivity, further information
is
required, especially in relation to relative marine survival, fecundity and reproductive performance of F, and
Escaped
farmed
Atlantic
salmon and native populations
later generation hybrid fish. Such studies are currently
being undertaken by the authors.
As only a small number of farm strains comprise most
of the production in Europe, introgression between
farmed and wild salmon has the potential to reduce the
level of genetic heterogeneity found among natural
populations of Atlantic salmon. Since farmed strains
often show reduced genetic variation, as based on
molecular markers, the level of genetic variation in
individual populations could also be reduced. Based on
results from other organisms, this homogenization and
reduction of genetic variability is likely to be disadvantageous in the long term.
In undertaking studies on the genetic impact of
escaped farmed salmon there are many variables and
any single experiment is unlikely to give a definitive
generalized answer. Thus experiments of this type are
required on several different river systems and using
different strains of salmon before generalized statements
can be made about the genetic impact of escaped farmed
salmon on native populations.
Acknowledgements
This project was supported
contract AIRl-CT92-0719.
by European
Commission
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