278
Vertical movements of “escaped” farmed Atlantic salmon (Salmo
salar L.)—a simulation study in a western Norwegian fjord
Ove T. Skilbrei, Jens Christian Holst, Lars Asplin, and Marianne Holm
Skilbrei, O. T., Holst, J. C., Asplin, L., and Holm, M. 2009. Vertical movements of “escaped” farmed Atlantic salmon (Salmo salar L.)—
a simulation study in a western Norwegian fjord. – ICES Journal of Marine Science, 66: 278 – 288.
To study the vertical distribution of fish that had been allowed to escape, farmed Atlantic salmon were tagged with acoustic tags
equipped with depth sensors, and then released on five different dates in the course of a year from two fish farms in the
Hardanger Fjord in western Norway. Release stimulated the fish to dive to deeper than 15 m during the first hours or days postrelease, often down to 50 –80 m. However, during the following 4 weeks, most of the escapees spent most of their time above the
pycnocline at depths of 0– 4 m. The fish were more widely distributed in the water column after release during winter, but still
spent most of the time in the cold surface layers. There was a wide range in the vertical distribution of individual fish, and the proportion of detections below 14-m depth ranged from 0 to 90%. There was a significant diurnal cycle in all seasons except midsummer,
when the fish were less abundant in the upper layer during daylight, especially on brighter days. The results suggest that salmon diving
activity following escape may complicate the recapture of escaped fish at the farm site but that the subsequent tendency of most fish
to stay near the surface, virtually irrespective of the time of year, may facilitate recapture.
Keywords: escaped farmed salmon, swimming depth, vertical distribution.
Received 6 June 2008; accepted 18 November 2008; advance access publication 12 January 2009.
O. T. Skilbrei, J. C. Holst, L. Asplin and M. Holm: Institute of Marine Research, PO Box 1870, Nordnes, NO-5817 Bergen, Norway. Correspondence to
O. T. Skilbrei: tel: þ47 55 236894; fax: þ47 55 238531; e-mail: [email protected].
Introduction
Farmed salmon that escape from cages are a serious problem to the
fish-farming industry, and to the management of both farmed and
wild stocks. With an annual production of .700 000 t compared
with a total catch of wild salmon of ,1000 t (ICES, 2008), the
Norwegian salmon-farming industry has become so large, compared with the size of the stocks of wild salmon, that escape
rates of even a fraction of 1% present major challenges to the management and conservation of the resource. The escapees may
spread diseases and parasites, and interfere with the genetic
make-up of wild stocks, if they manage to interbreed (Naylor
et al., 2005; Jonsson and Jonsson, 2006; Skaala et al., 2006;
Ferguson et al., 2007). There is a correlation between the incidence
of escaped farmed salmon in rivers and the intensity of salmon
farming at the county level in Norway (Fiske et al., 2006). A
global assessment carried out by Ford and Myers (2008) suggested
that salmon farming has reduced the survival rates of wild
salmon and trout populations in many countries. It is therefore
important to have a good understanding of how these fish
behave after escaping, to be able to recognize and mitigate the
environmental risks associated with escapes.
Fish farmers in Norway are required by regulation to recapture
escaped salmon (Regulation 2008-08-27 No. 984). Major escapes
have shown that efforts made close to the escape site are usually
not very successful, with a catch rate of a few per cent of the
total number of escapees (Anfinsen, 2005; Buvik, 2005). Escaped
farmed salmon are usually reported from the fishery for wild
salmon, which is seasonal and dominated by bag nets in the sea
and angling in the rivers (Fiske et al., 2001). A late autumn/
early winter sea fishery that particularly targets escaped farmed
salmonids was opened in several Norwegian counties during the
late 1990s. A positive relationship between the catch per unit
effort (cpue) of gillnetted salmon in the fishery and reported
local escape incidents indicates that a bigger proportion of the
fish can be recaptured if the fishery covers a larger geographical
area, e.g. a whole fjord (Skilbrei and Wennevik, 2006). Farmed
salmon that are not captured may find their way to the
Norwegian Sea (Hansen et al., 1999), then return as maturing
adults to the Norwegian coast and enter rivers over a broad
geographical area (Skilbrei and Holm, 1998; Hansen, 2006).
There is a need to develop effective recapture methods capable
of being employed at all times of the year.
The efficiency of fishing gears depends on the swimming
behaviour and movements of the fish that they target. There is
little information in the literature on the behaviour in the sea
of newly escaped farmed salmon, particularly concerning the
movements of fish after they escape or are released from the
cage. The behaviour of cultured smolts released from cages for
sea-ranching purposes has been monitored by underwater video
equipment (Skilbrei et al., 1994a, b), and sonic tagging has been
used to study the behaviour of simulated escapes of larger
farmed salmon. Furevik et al. (1990) followed adult salmon after
release from a farm in western Norway at different times of year.
They used a hand-held receiver to track the fish, which they
were able to follow for a couple of days. Whoriskey et al. (2006)
used stationary receiver units to locate acoustically tagged
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279
Modelling the movements of escaped salmon in a Norwegian fjord
salmon set free from a cage site in the Bay of Fundy, North
America, and were able to track some fish over longer periods of
time and longer distances. None of these studies reported on the
vertical distribution of the tracked fish.
Knowledge of the swimming depth of escaped fish is a key to
target recapture. We studied the swimming behaviour and movements of escaped, farmed salmon by releasing fish tagged with
depth-sensitive, acoustic transmitters at different times of the
year from a commercial farm in a large Norwegian fjord. Here,
we report on their vertical distribution. Our goals were to
monitor: (i) the immediate reaction of the fish to being released,
(ii) the swimming depth of the fish during the following four
weeks, (iii) their diurnal activity, and (iv) to determine whether
the depth preferences of the “escapees” changed with the season
of the year.
Material and methods
Study area
The Hardanger Fjord was selected as the study area (Figure 1). The
hydrographic conditions in the middle of the fjord, the area
around Varaldsøy, are typical of fjords. There are major freshwater sources in the near and inner region which tend
to produce a distinct upper brackish water layer at a depth of
5 –10 m and a surface salinity of ,15 –20 from spring until late
autumn. Water flow in this layer is out of the fjord on both
sides of Varaldsøy. The temperature of the brackish layer
depends on the temperature of the discharged fresh water, how
well it is mixed on its way out of the fjord, and solar heating.
The surface temperature rises to 158C during summer.
In winter, when the upper brackish layer is normally absent,
surface-layer temperatures are similar to or colder than those of
the deeper water. Below 20 –30 m, the variability in salinity and
temperature throughout the year is less, with typical values
ranging between 34 and 35, and 7.58C and 8.58C, respectively.
There is a large salmon-farming industry in the fjord. The total
production of salmon from 50 locations was close to 40 000 t in
2003, and a fishery targeting escaped salmon is prosecuted during
autumn and winter (Skilbrei and Wennevik, 2006). There is a
reason for concern about the negative effects of escaped farmed
salmon on the genetic make-up of several wild salmon stocks
that inhabit rivers that drain to the fjord (Skaala et al., 2006).
Tagging and release
In all, 132 farmed salmon were tagged with V13P-1L-S256 coded
pingers carrying a depth sensor (45-mm long, weight in water
6 g, min/max of time 40/120 s; Vemco Ltd, Shad Bay, Nova
Scotia) at two commercial salmon farms located close to the
island of Varaldsøy in the middle of the Hardanger Fjord in
western Norway (Figure 1), and released on five dates in the
course of a year in groups of 19 –30 fish (releases 1, 2, 3, 4, and
5; Table 1). The fish that were tagged showed no external signs
of maturity. The mean fork lengths of the released groups
ranged from 54 to 70 cm (Table 1).
The fish were anaesthetized with a mix of benzocaine
and metomidate. The tags were sterilized and treated with
Terramycinwvet and inserted surgically in the abdomen of the
fish. The wounds were closed with three stitches, and the
gills were irrigated occasionally during the surgery. After surgery
Figure 1. The locations of the acoustic receivers (black stars), the two cage sites (arrows and numbers) close to the island of Varaldsøy, from
which farmed salmon were tagged and released in the Hardanger Fjord, and the location of the three weather stations in Bergen, Kvam, and
Ullensvang.
280
O. T. Skilbrei et al.
Table 1. Description of releases 1, 2, 3, 4, and 5: dates of tagging and release of the fish at release site 1 or 2, mean size of fish, numbers
tagged and recorded at receivers for the four weeks post-release.
Description
Date tagged
Date released
Release site
Mean length (cm; s.d.)
Mean weight, (kg; s.d.)
Number released
Number of fish detected
Days 2 –8
Days 9 –15
Days 16– 22
Days 23– 29
Duration (h:min)
Day of days 2, 29
Night of days 2, 29
1—July
24 June 2005
1 July 2005
1
63.7 (3.5)
–
19
2—August/September
23 August 2005
28 August 2005
1
72.4 (5.6)
–
24
3—December/January
8 December 2005
15 December 2005
2
54.0 (3.1)
2.8 (0.5)
30
4—March/April
8 March 2006
15 March 2006
2
60.5 (3.3)
3.0 (0.5)
30
5—June
1 June 2006
8 June 2006
2
70.4 (3.9)
4.3 (0.8)
29
18
11
8
4
24
21
13
10
16
10
10
10
29
20
11
11
29
22
14
8
18:42, 17:01
2:04, 4:56
14:21, 11:54
6:11, 9:06
5:51, 6:34
14:19, 13:48
11:44, 14:25
9:11, 5:59
18:45, 18:34
1:52, 2:25
The calculated duration of day and night are shown for days 2 and 29 post-release.
(2– 3 min per tag), the fish were placed in a small tank until they
recovered from the anaesthesia, then transferred to a cage
4 –5 m deep and 8 m in diameter. They were fed by hand for
the next 5 –7 d, until release. This recovery period was chosen
because it has been documented that salmonids show stress
responses that last for several days at least (Olsen et al., 2002,
2005). All but one of the tags functioned satisfactorily. The
experiment and the tagging procedure were approved by the
Norwegian committee for the use of animals in scientific
experiments (FDU).
Acoustic receivers
In all, 24 VR2 receiver units (Vemco Ltd) were moored at 24 different sites in the fjord, covering a total range of 74 km from the
innermost to the outermost location (Figure 1). Release site 1
was between, and within the range of, the two receivers moored
northeast of Varaldsøy (Figure 1). One receiver was located
directly at release site 2, and an additional receiver was added to
this site in May 2006. The depth below the fish farm at release
site 1 increased from 180 to 350 m from the inner to the outer
part of the structure, with a depth of 200 m below the cage used
for the releases. At release site 2, the depth increased rapidly
from 60 to 210 m beneath the fish farm; the depth directly
below the cage was 200 m. The receivers were moored to a
weight at the bottom, which was also moored to land, and held
at a depth of 10– 15 m with a float, except for the two fastened
to the floating structure of the cages at release site 2. The water
depth at the receiver sites ranged from 25 to 110 m. Within a
circular detection area with a horizontal radius of up to 300 m,
depths typically ranged from 0 to 200 –500 m, owing to the
steep slope of the bottom in this area.
Comparisons between vertical distribution and light
conditions
Solar-radiation data from Bergen were provided by the University
of Bergen (Olseth et al., 2006, 2007), and data from the stations at
Kvam and Ullensvang close to the Hardanger Fjord were extracted
from the AgroMetBase web service of the Norwegian Institute for
Agricultural and Environmental Research (http://lmt.bioforsk.
no/agrometbase/getweatherdata.php; see locations in Figure 1).
The daily sums of solar radiation were available from all
three stations. The daily weather was categorized according to
the duration of sunshine recorded at the stations in Bergen and
Ullensvang. If the sunshine totalled ,6 min in the course of a
day, it was denoted “cloudy”, whereas days with a minimum 6 h
of sunshine were defined as “bright”. Some 70% of the days
classified into these two categories satisfied the criteria at both
stations. Owing to variability in weather within the region,
minor deviations from the criteria were accepted at one of the
two stations. It was also confirmed that the daily sum of radiation
recorded at the station in Kvam agreed with the expected range
for “cloudy” and “bright” weather.
The mean swimming depth during daylight for specific days
was calculated if there were data from at least five salmon and a
minimum of five recordings per fish, except for release 3
(December), where three salmon per day was taken as acceptable.
Four dives to .50 m were regarded as statistical outliers in
relation to the intention of studying the finer scaled patterns
close to surface, so these were not included in the comparisons
between cloudy and bright days. For each release group of fish, a
two-tailed Student’s t-test (Statsoft, Inc., 2008) was used to
investigate whether the mean swimming depth during daylight
differed between bright and cloudy days.
The diurnal cycle was divided into daylight and night as
follows: daylight, the period from sunrise to sunset; night, the
period from the onset of nautical twilight in the evening to the
end of nautical twilight in the morning. Civil twilight was used
in June and July because it is too bright then for nautical twilight
at this latitude (608100 ) in midsummer. The computations of
sunrise, sunset, and twilight times were made by the
Online-Photoperiod Calculator V 1.94 L (http://www.sci.fi/
~benefon/sol.html). Only salmon with .15 detections were
included in the calculation of depth-frequency distributions by
day or night.
To compare fine-scale differences in the vertical distribution of
salmon close to the surface between day and night, we employed
two-way analysis of variance [general linear model (GLM) procedure; Statsoft, Inc., 2008]; it used individual depth data from
depths of 0– 15 m. The two-way analysis of variance tested the
effects of both time of day (day and night) and the variability
between fish. The assumptions for the GLM were checked by
inspecting the values of homogeneity of variance (Levene’s test
281
Modelling the movements of escaped salmon in a Norwegian fjord
for homogeneity of variances), normal p-plots, and plots of means
against standard deviations (Statsoft, Inc., 2008). To comply
with the assumptions, the data were arcsine-transformed. This
was because the surface (0 m) is a boundary for vertical movements of the fish, and an arcsine transformation moves very low
values towards the centre, giving them more theoretical freedom
to vary (Sokal and Rohlf, 1981).
Spearman0 s rank order correlation (Statsoft, Inc., 2008) was
applied to test whether differences in size could explain individual
variability in the deep-diving activity. For each release, the
Spearman0 s R-statistic was calculated to determine whether the
proportional time spent below 14 m was correlated with the size
of the fish.
Hydrography
The mean temperature and salinity conditions during the four
weeks following each of the five releases were constructed based
on records from a combination of sources. First, the Institute of
Marine Research (IMR) has conducted regular hydrographic
surveys along fixed transects in the Hardanger Fjord, and these
provide reasonable temporal and spatial coverage, with profiles
of high vertical resolution from the surface down to 50 m. A
CTD-profiler (SAIV SD204) was used. Second, salinity and temperature measurements were made weekly at depths of 1, 3, and 8 m
at a number of fish farms in the Hardanger Fjord. These observations are provided by Hardanger Fiskehelsenettverk (http://
www.fom-as.no/), a cooperative of farmers established to synchronize the delousing of salmon farms. The equipment used is
not known, but the data have been validated against IMR data,
and no systematic deviations attributable to faulty instruments
or sampling methods have been found. The oceanographic conditions may vary spatially within the study area and in time
within the study period of each release. The stratifications presented were compiled as the mean values in time and space
during the first four weeks after each release date.
Results
Hydrographic conditions
Physical conditions .30 m were stable during the whole experimental period, from July 2005 to late June 2006, with a water
temperature of 8 –98C and a salinity of 33 –35 (Figure 2).
During the first release, in July 2005, a typical summer situation
was present, with a brackish, warm, upper layer 10 m deep.
Surface temperature was 168C and salinity ,15. At the second
release, in September 2005, the mean conditions were much the
same as during the release in July, but with a slight cooling of
the surface water and a rise in salinity; temperatures were still
.148C in the upper 5 m. At the beginning of winter when the
third group was released (in December), the water had become
homogeneous in temperature, at 88C. The salinity still created
a relatively weak stratification, with salinity .25 down to 10 –
15 m. During the fourth release at the end of winter (March),
the water had become homogeneous in salinity (surface value
.30), and a further cooling of the upper layer had taken place.
The upper 20 m was ,68C and the surface value was ,48C.
During the fifth release (June 2006), summer conditions had
been re-established with a distinct 5 –10 m upper layer of warm,
fresher water. The temperatures were .168C, but the salinity
was still relatively high, at .25 (Figure 2).
Figure 2. Mean temperature (top) and salinity (bottom) conditions
in the study area during the four weeks following the releases in July,
August, December, March, and June (releases 1, 2, 3, 4, and 5).
Vertical swimming behaviour
Days 0 –1
Many fish dived immediately on release. Diving activity was more
intense in autumn and winter than in summer (Figures 3 and 4).
Six of the 19 “escapees” dived deeper than 30 m immediately following their summer release in July 2005 (release 1; five of them
are shown in Figure 3), and some reached depths of 60 –80 m.
The mean percentage of detections .14 m deep during the first
2 d after release summed to just more than 10% of the total, a
level comparable with the release in June 2006 (7%; release 5;
Figure 4). The diving response was more extensive on 28 August
and 15 December (releases 2 and 3), when many of the fish
moved deeper than 10 m during the first hours after release, and
several repeated their diving to .20 m until the next day
(shown for the 28 August release in Figure 3). More than 40 and
20% of the time, respectively, was spent at 15 m or deeper
during the first 2 d after the releases in late August and
mid-December (releases 2 and 3; Figure 4). Diving peaked
following the release on 15 March (release 4, Figure 3). The fish
then spent some 50% of their time .14 m deep during the first
2 d (Figure 4), and almost 25% of the time during the next 28 d
(Figure 4). Following release 5 in midsummer, on 8 June 2006,
fish did not dive immediately. Instead they moved closer to the
surface on day 0 than the other release groups. Only one of the
65 detections received during the first 4 h post-release was made
from .14 m, and 7% of the time was spent .14 m during
the first 2 d post-release (Figure 4).
282
O. T. Skilbrei et al.
Figure 3. Swimming depth of ten individually tagged salmon from (a) release 1 on 1 July, (b) release 2 on 28 August, and (c) release 4 on 15
March, during days 0 – 1 post-release. The fish with the most post-release detections during days 0 and 1 were selected for depiction. Values
with the same symbols are records for the same individual at different detection times. The time of release is shown by the arrow.
Days 2 –29
During the next four weeks the salmon spent most of their time
close to the surface, notably in the upper 4 m (Figure 4). This
general distribution was evident throughout the year, but was
less pronounced during daylight in winter, when the fish were
more widely spread throughout the water column.
A significant diurnal cycle could be observed after all releases
except the midsummer releases (releases from July to April;
releases 1, 2, 3, and 4), from which fish were more abundant in
the upper layers at night (Figures 4 and 5, Table 2). Differences
observed between mean swimming depth by day and by night
ranged from fish staying 6 m closer to the surface at night to
some that displayed the reverse relationship between day and
night (Figure 5). The latter alternative was observed most
frequently after the midsummer release in June (Release 5),
when about half the fish stayed either lower or deeper at night
(Figure 5), and there was no significant effect of time of day
(Table 2). Generally speaking, the effect of the diurnal cycle was
most evident after the July, August/September, and March/April
releases (releases 1, 2, and 4), when most of the fish remained
closer to surface at night, but not so clear for the December/
January release in midwinter (Figure 5). These relationships are
also reflected in higher F-values for the diurnal effect following
the July, August/September, and March/April releases (Table 2).
Modelling the movements of escaped salmon in a Norwegian fjord
283
Figure 4. Mean proportion of detections of individual fish at 1-m depth intervals from each of the five releases. The first period from release
until the next day (days 0 –1), and the following four weeks (days 2 – 29) are presented separately. The second period is split further into two
vertical columns according to the time of day: day and night. See text for the description of the duration and calculation of the periods
defined as day and night.
284
O. T. Skilbrei et al.
Figure 5. Mean fish swimming depth (m) by day (white squares) and night (black squares) from days 2 to 29 following all five releases within
the upper 15-m depth range. The fish are arranged according to decreasing difference between day and night measurements, with fish
ascending to the surface at night to the left and fish descending at night to the right of each panel. Lines are drawn only for visualization
purposes, and 95% confidence intervals are shown.
Table 2. Results from a two-way analysis of variance (GLM, see text for details) test of the effect of day and night (diurnal) and individual
variability on swimming depths from 0 to 15 m from days 2 to 29 following releases 1, 2, 3, 4, and 5.
Whole model
Release
1—July
2—August/September
3—December/January
4—March/April
5—June
R2
0.17
0.37
0.35
0.25
0.28
F
77
286
54
44
68
Diurnal
p
*
*
*
*
*
F
155
360
51
387
1
Individual 3 Diurnal
Individuals
p
*
*
*
*
n.s.
Data are arcsine-transformed.
R 2, squared correlation; F, F-value; p, significance level, where *¼p , 0.001 and n.s.¼not significant.
F
74
382
37
53
45
p
*
*
*
*
*
F
8
63
26
37
12
p
*
*
*
*
*
285
Modelling the movements of escaped salmon in a Norwegian fjord
Discussion
Figure 6. The proportion of time spent .14 m deep during days
2 –29 following all five releases plotted against fork length at tagging
for individual salmon. Fish with fewer than 20 detections have been
excluded. See Table 1 for specific dates.
Deep diving (.15 m) was occasional for all groups. The frequency of detections .14 m deep was lower for the first two
releases in July and August/September (0 –7%) than for the
other three releases, December/January, March/April, and June
(releases 3, 4, and 5; 10 –25%; Figure 4). Time spent deeper than
14 m also varied widely among fish, from 0 to 90% (Figure 6).
A large proportion of the fish released during summer in June
and July (releases 1 and 5) was never recorded .14 m, whereas
most of the fish released during winter (releases 3 and 4; the
December/January and March/April releases) spent at least 10%
of their time .14 m. There were no significant correlations
between the tendency to dive deep and fish size (Spearman0 s
R-statistic; not significant).
The effect of weather conditions on vertical swimming
behaviour
There was a tendency for fish to double their mean distance to the
surface on bright days compared with cloudy days. This was
significant for two of the releases, and close to significance for
two others (Table 3). There were no bright days during the
observation period of the December/January release (release 3).
This may have contributed to the slightly smaller differences
between day and night swimming depth for this release group
than for the August/September and March/April releases
(described above; Table 2, Figure 5).
Our study has demonstrated that the immediate response of adult
salmon escaping from cages is most probably a dive to depths of
20 –80 m. Subsequently, however, the escapees stayed close to
the surface most of the time for the next four weeks. This observation was almost independent of season and the high annual
variability in temperature above the pycnocline of the fjord.
There was a clear diurnal cycle that affected the abundance of
fish within the upper layers, fish tending to move deeper by day,
especially in bright weather.
Farmed fish kept in cages have not had the opportunity to swim
into the full range of depths available in the fjords before they
escape. Therefore, it is a dramatic environmental change for a
salmon that has escaped from a fish farm, where it was held in an
enclosure under crowded conditions, to be able to move freely in
all directions outside the cage. Our observations suggest that
there is a great probability that this change may stimulate immediate diving. Fish habituated to a cage environment will experience a
sudden loss of such physical stimuli as the presence of a cage floor
and interaction with other fish in the cage. The reason for diving
may simply be the sudden absence of physical obstructions, or it
may be a genetically based behavioural response of wild salmon.
Four hypotheses have been advanced to explain wild-salmon
diving behaviour: (i) an orientation during homing migration,
(ii) a need to feed in deeper layers, (iii) to control body temperature, and (iv) predator avoidance (Wada and Ueno, 1999; Reddin
et al., 2004). For our escapees, diving during the first hours and
days of freedom may be a way of mapping the new environment,
perhaps like orientation diving during migration. Moreover,
if salmon dive to escape predators and potentially harmful
conditions, another possibility would be that immediate deep
diving is an escape response triggered by being released into an
unknown environment. If diving is related to avoidance of
danger, then the darkness of the depths may be sensed as a protecting environment compared with the brighter surface layers. It is
less likely that fish migrate to deep water to feed so soon after
release, because they have become habituated to surface feeding
in culture and do not have any experience of feeding in a new,
perhaps deeper, environment.
The fact that diving was observed under quite different oceanographic conditions throughout the year and that the rate declined a
few days post-release suggests that temperature regulation was not
its main reason. However, because farmed salmon seem to prefer
higher temperatures at this latitude (Oppedal et al., 2007), the
extent and the duration of diving following release at different
times of the year may have been influenced by temperature stratification. Pre-release diving activity was least obvious in June and
July, when surface waters are warmer than the underlying water
Table 3. Mean depth (m) and (s.d.) of fish during daylight under bright and cloudy weather conditions (see text for detail), and the
significance levels of a t-test comparing the differences between cloudy and bright days.
Cloudy
Release
1
2
3
4
5
Period
6 –22 July 2005
31 August–13 September 2005
23 December –11 January 2006
23 March–9 April 2006
14 June –5 July 2006
Depth (s.d.)
2.9 (0.9)
2.2 (0.9)
5.6 (3.9)
4.8 (0.7)
3.2 (1.4)
Bright
Days
4
5
5
6
5
Depth (s.d.)
4.3 (1.0)
5.1 (2.8)
–
10.6 (4.7)
7.4 (3.9)
Days
6
5
0
6
9
t-test (p-value)
0.07
0.06
–
,0.05
,0.05
286
masses, and most pronounced in March/April, when the fish
dived from cold surface temperature through the thermocline to
warmer water below.
Despite the annual surface-temperature range of almost 158C,
similar to the natural temperature range of Atlantic salmon, fish
released at various times of the year spent most of their first
four weeks of freedom close to the surface. Temperature would
therefore seem to be of minor importance in stimulating vertical
migration of newly escaped salmon. On the other hand, temperature gradients may be one reason for attracting salmon to the
mixed surface layer. The depth of travel of adult sockeye salmon
(Oncorhynchus nerka) is apparently controlled by a general
preference for the surface, avoidance of warm (also low salinity)
water, and orientation to the thermocline (Quinn et al., 1989).
Westerberg (1982) observed Atlantic salmon making vertical
excursions of 5 –15 m and concluded that they tended to follow
fine-structure gradient layers in the quasi-mixed surface layer or
in the thermocline, possibly for orientation during their homing
migration.
The pycnocline in the Hardanger Fjord at a depth of 5 –10 m is
a strong barrier to vertical water mixing, perhaps isolating surface
water from deep water. Johansson et al. (2007) showed in a study
of the swimming behaviour of cultured salmon in cages that the
occurrence of a pycnocline influenced both the distribution of
the fish and the oxygen depth profile. The water above the pycnocline was characterized by low salinity and varying temperature,
with high levels of oxygen, whereas the salinity and the temperature of the water below the pycnocline were more stable, with
lower concentrations of oxygen. In the present study, the fish
spent most of their time in the water above the pycnocline at
depths of 0 –5 m. Perhaps the salmon preferred the physical parameter(s) typical of this water, such as the greater oxygen content.
The vertical distribution of the released adult salmon appeared
to be similar to those observed for wild Atlantic salmon during
migration in the sea. According to a study by Sturlaugsson
(1995) in Iceland, most homing Atlantic salmon spend most of
their time in the upper 3 m. Similar results were observed in
another Icelandic study, with as much as 91% of the period of
migration spent in the upper 2 m (Sturlaugsson and Thorisson,
1997). In a study in the Baltic Sea, almost all the salmon remained
close to the surface, with a median swimming depth of 2 m
(Karlsson et al., 1996). Diving was rapid in all three of these
studies. Occasional dives of wild salmon similar to those observed
for our “escaped” farmed fish were made down through the
thermocline to depths of 20– 40 m (Karlsson et al., 1996), and
even down to .100 m (Sturlaugsson, 1995; Sturlaugsson and
Thorisson, 1997).
Our escaped fish moved closer to the surface at night or, alternatively, tended to move away from the upper layer by day. The
fact that the fish were closer to the surface in cloudy than in
bright weather supports the notion that light intensity is a factor
that influences the depth preference of escaped salmon. Salmon
in cages apparently follow a similar diel migration by descending
at dawn and moving closer to the surface at dusk (Juell and
Westerberg, 1993; Oppedal et al., 2001; Juell and Fosseidengen,
2004; Johansson et al., 2006). By adjusting the levels of artificial
light, Oppedal et al. (2007) concluded that farmed salmon positioned themselves vertically in a cage according to a behavioural
trade-off between a preference for the highest temperature available and an attraction to a preferred light intensity. The data on
wild salmon are not conclusive. Reddin et al. (2004) found
O. T. Skilbrei et al.
evidence in two of three Newfoundland stocks that kelts spend
more time in warm water close to the surface at night. Similar
observations have been made during post-smolt seaward
migrations, and it has been suggested that post-smolts avoid
bird predators during the hours of daylight by locating themselves
deeper in the water column (Reddin et al., 2006). However,
Sturlaugsson and Thorisson (1997) observed that spawning
migrants along the coast of Iceland were closest to the surface
around noon, and Karlsson et al. (1996) failed to find any
diurnal pattern in the mean depth preference of salmon during
the spawning migration in the Baltic Sea. It is an open question
whether the small-scale, vertical diurnal cycle of our simulated
escapees is a behaviour learned during their life in cages or
whether it resembles the behaviour of wild salmon.
Post-release diving behaviour is disadvantageous to fish
farming for several reasons. If farmed salmon are accidentally
lost from a cage, there may be no sudden surface activity by the
fish in the water around the cages to notify the farmer of an
escape. It may also be a difficult task to estimate the number of
fish that have escaped, especially if few fish escape from large production units holding tens of thousands. Moreover, the recapture
of the escaped salmon will be difficult, and only marginally effective. There seems to be a great risk that the fish will disperse downwards in the water column, so avoiding many types of fishing gear.
If the fish are distributed widely in the water column, they will
occupy a larger volume, requiring much larger and more costly
fishing effort to recapture them.
The fact that escaped salmon seem to have a preference for
remaining close to the surface during at least their first four
weeks at liberty, almost irrespective of the time of the year,
makes it highly likely that their catchability will be enhanced,
with traditional salmon-fishing gear such as the gillnets and bag
nets deployed by anglers the most efficient at catching them.
This behaviour may explain the observations of Skilbrei and
Wennevik (2006) that escape incidents were followed by a regional
increase in the cpue of gillnetted, escaped farmed salmon, of
duration 4 – 5 weeks. However, the pronounced variability in the
depth distribution of the salmon we observed suggests that catchability will vary substantially at an individual level, especially
during winter, when the fish appear to be more widely distributed
in the water column. If some fish prefer to stay in deeper water,
then the likelihood of their recapture will be less.
The clear tendency of the fish to remain close to the surface
at night may affect the capture efficiency of the different types of
fishing gear. Such behaviour should favour the use of floating
gillnets, because it will increase the abundance of the fish at
the setting depth of those nets. The proportion of the catch of
juvenile coho salmon (Oncorhynchus kisutch) caught at depths
of 0 –2 m in stratified gillnet sets fell from 52.5 to 12.1% from
the darker to the brighter portion of the day (Pearcy and
Fisher, 1988). However, several authors have noted that successful catches of post-smolt coho and Atlantic salmon with pelagic
or surface trawls are made almost exclusively by day (Shelton
et al., 1997; Holm et al., 2000; Krutzikowsky and Emmet,
2005). Krutzikowsky and Emmet (2005) suggested that the fish
missed the surface trawl because the headrope passed below
them during night trawling, usually at depths between 0.8 and
1.6 m. The greater abundance of simulated escaped salmon in
the top metre of the water column at night, as observed here,
therefore suggests that surface trawls will be less efficient at
recovering “escapees” by night.
Modelling the movements of escaped salmon in a Norwegian fjord
In summary, we have presented an analysis of vertical movements of Atlantic salmon released from cages in the sea. The
results seemingly show that any fishing effort to recapture
escaped farmed salmon should be concentrated in the surface
layers. The associated data on horizontal movements from these
experiments are currently being analysed and will be documented
in a forthcoming paper, which will include a broader discussion
that includes consideration of the distribution of the fish in
space and time, as well as the effects of these distributions on,
for instance, recapture practices.
Acknowledgements
We thank Marine Harvest AS for their cooperation in the project.
We also gratefully acknowledge Per Arne Åkre for helping to
organize the tagging and releases at the fish farms, Håkon
R. Sæbø for his skills in fish surgery, Hugh Allen for comments
on the paper, Fred Whoriskey and Frode Oppedal for improving
the work through comments and suggestions during the final
stages of drafting of the paper, and Ole Torrissen for playing
such a significant role during the initiation of the project. The
Norwegian Ministry of Fisheries and Coastal Affairs provided
the financial support for the study.
References
Anfinsen, A. R. 2005. Oppsummeringsrapport etter havari av
fiskeoppdrettsanlegg i Storvikja i Tustna kommune i Møre
og Romsdal. Etter arbeid i referansegruppen i tilknytting
Aquastructures AS sin tekniske rapport (in Norwegian). 11 pp.
Buvik, P. 2005. Gjenfangstfond for rømt oppdrettslaks—oppsummering
etter drift fra 20.06-04.08.05. Rapport fra Alta Utviklingsselskap
(in Norwegian). 7 pp.
Ferguson, A., Fleming, I., Hindar, K., Skaala, Ø., McGinnity, P., Cross,
T. F., and Prodöhl, P. 2007. Farm escapes. In The Atlantic Salmon:
Genetics, Conservation and Management, pp. 357– 398. Ed. by E.
Verspoor, L. Stradmeyer, and J. L. Nielsen. Blackwell Publishing,
Oxford.
Fiske, P., Lund, R. A., and Hansen, L. P. 2001. Rømt oppdrettslaks i
sjø- og elvefiskeriet i årene 1989– 2000. NINA Oppdragsmelding,
704 (in Norwegian). 26 pp.
Fiske, P., Lund, R. A., and Hansen, L. P. 2006. Relationships between
the frequency of farmed Atlantic salmon, Salmo salar L., in wild
salmon populations and fish farming activity in Norway, 1989–
2004. ICES Journal of Marine Science, 63: 1182 – 1189.
Ford, J. S., and Myers, R. A. 2008. A global assessment of salmon
aquaculture impacts on wild salmonids. Public Library of Science
Biology, 6: e33. doi:10.1371/journal.pbio.0060033.
Furevik, D., Rabben, H., Mikkelsen, K. O., and Fosseidengen, J. E.
1990. Migratory patterns of escaped farm-raised Atlantic salmon.
ICES Document CM 1990/F: 55. 19 pp.
Hansen, L. P. 2006. Migration and survival of farmed Atlantic salmon
(Salmo salar L.) released from two Norwegian fish farms. ICES
Journal of Marine Science, 63: 1211 – 1217.
Hansen, L. P., Jacobsen, J. A., and Lund, R. A. 1999. The incidence of
escaped farmed Atlantic salmon, Salmo salar L., in the Faroese
fishery and estimates of catches of wild salmon. ICES Journal of
Marine Science, 56: 200– 206.
Holm, M., Holst, J. C., and Hansen, L. P. 2000. Spatial and temporal
distribution of post-smolts of Atlantic salmon (Salmo salar L.) in
the Norwegian Sea and adjacent areas. ICES Journal of Marine
Science, 57: 955– 964.
ICES. 2008. Report of the Working Group on North Atlantic Salmon
(WGNAS), 1 – 10 April 2008, Galway, Ireland. ICES Document CM
2008/ACOM: 18. 233 pp.
287
Johansson, D., Juell, J-E., Oppedal, F., Stiansen, J-E., and Ruohonen,
K. 2007. The influence of the pycnocline and cage resistance on
current flow, oxygen flux and swimming behaviour of Atlantic
salmon (Salmo salar L.) in production cages. Aquaculture, 265:
271– 287.
Johansson, D., Ruohonen, K., Kiessling, A., Oppedal, F., Stiansen, J-E.,
Kelly, M., and Juell, E. 2006. Effect of environmental factors on
swimming depth preferences of Atlantic salmon (Salmo salar L.)
and temporal and spatial variations in oxygen levels in sea-cages
at a fjord site. Aquaculture, 254: 594– 605.
Jonsson, B., and Jonsson, N. 2006. Cultured Atlantic salmon in nature:
a review of their ecology and interaction with wild fish. ICES
Journal of Marine Science, 63: 1162 – 1181.
Juell, J-E., and Fosseidengen, J. E. 2004. Use of artificial light to control
swimming depth and fish density of Atlantic salmon (Salmo salar)
in production cages. Aquaculture, 233: 269 – 282.
Juell, J-E., and Westerberg, H. 1993. An ultrasonic telemetric system
for automatic positioning of individual fish used to track
Atlantic salmon (Salmo salar L.) in a sea cage. Aquacultural
Engineering, 12: 1 – 18.
Karlsson, L., Ikonen, E., Westerberg, H., and Sturlaugsson, J. 1996. Use
of data storage tags to study the spawning migration of Baltic
salmon (Salmo salar L.) in the Gulf of Bothnia. ICES Document
CM 1996/M: 9. 16 pp.
Krutzikowsky, G. K., and Emmet, R. L. 2005. Diel differences in
surface trawl fish catches of Oregon and Washington. Fisheries
Research, 71: 365– 371.
Naylor, R., Hindar, K., Fleming, I. A., Goldburg, R., Williams, S.,
Volpe, J., Whoriskey, F., et al. 2005. Fugitive salmon: assessing
the risks of escaped fish from net-pen aquaculture. BioScience,
55: 427– 437.
Olsen, R. E., Sundell, K., Hansen, T., Hemre, G-E., Myklebust, R.,
Mayhew, T. M., and Ringø, E. 2002. Acute stress alters the intestinal
lining of Atlantic salmon, Salmo salar L.: an electron microscopical
study. Fish Physiology and Biochemistry, 26: 211 –221.
Olsen, R. E., Sundell, K., Mayhew, T. M., Myklebust, R., and Ringø, E.
2005. Acute stress alters intestinal function of rainbow trout,
Oncorhynchus mykiss (Walbaum). Aquaculture, 250: 480 – 495.
Olseth, J. A., Cleveland, F., and de Lange, T. 2006. The radiation observatory radiation yearbook No. 41. Radiation observations in
Bergen, Norway, 2005. Meteorological report series, University of
Bergen, Department of Geophysics. 78 pp.
Olseth, J. A., Cleveland, F., and de Lange, T. 2007. The radiation observatory radiation yearbook No. 42. Radiation observations in
Bergen, Norway, 2006. Meteorological report series, University of
Bergen, Department of Geophysics. 78 pp.
Oppedal, F., Juell, J-E., and Johansson, D. 2007. Thermo- and photoregulatory swimming behaviour of caged Atlantic salmon: implications for photoperiod management and fish welfare.
Aquaculture, 265: 70– 81.
Oppedal, F., Juell, J-E., Taranger, G. L., and Hansen, T. 2001. Artificial
light and season affect vertical distribution and swimming behaviour of post-smolt Atlantic salmon in sea cages. Journal of Fish
Biology, 58: 1570– 1584.
Pearcy, W. G., and Fisher, J. P. 1988. Migrations of coho salmon,
Oncorhynchus kisutch, during their first summer in the ocean.
Fishery Bulletin US, 86: 173– 195.
Quinn, T. P., Terhart, B. A., and Groot, C. 1989. Migratory orientation
and vertical movements of homing adult sockeye salmon,
Oncorhynchus nerka, in coastal waters. Animal Behaviour, 37:
587– 599.
Reddin, D. G., Downton, P., and Friedland, K. D. 2006. Diurnal and
nocturnal temperatures for Atlantic salmon postsmolts (Salmo
salar L.) during their early marine life. Fishery Bulletin US, 104:
415– 428.
Reddin, D. G., Friedland, K. D., Downton, P., Dempson, J. B., and
Mullins, C. C. 2004. Thermal habitat experienced by Atlantic
288
salmon (Salmo salar L.) kelts in coastal Newfoundland waters.
Fisheries Oceanography, 13: 24 – 35.
Shelton, R. G. J., Turrell, W. R., and Macdonald, A. 1997. Records of
post-smolt Atlantic salmon, Salmo salar L., in the Faroe– Shetland
Channel in June 1996. Fisheries Research, 31: 159– 162.
Skaala, Ø., Wennevik, V., and Glover, K. A. 2006. Evidence of temporal
genetic change in wild Atlantic salmon, Salmo salar L., populations
affected by farm escapees. ICES Journal of Marine Science, 63:
1224– 1233.
Skilbrei, O. T., and Holm, M. 1998. Effects of long-term exercise on
survival, homing and straying of released Atlantic salmon (Salmo
salar) smolts. Journal of Fish Biology, 52: 1083 – 1086.
Skilbrei, O. T., Holm, M., Jørstad, K., and Handeland, S. O. 1994a.
Migration motivation of cultured Atlantic salmon, Salmo salar
L., smolts in relation to size, time of release and acclimatization
period. Aquaculture and Fisheries Management, 25: 65– 77.
Skilbrei, O. T., Jørstad, K., Holm, M., Farestveit, E., Grimnes, A., and
Aardal, L. 1994b. A new release system for coastal ranching of
salmon and behavioural patterns of released smolts. Nordic
Journal of Freshwater Research, 69: 84– 94.
Skilbrei, O., and Wennevik, V. 2006. The use of catch statistics to
monitor the abundance of escaped farmed Atlantic salmon and
rainbow trout in the sea. ICES Journal of Marine Science, 63:
1190– 1200.
O. T. Skilbrei et al.
Sokal, R. R., and Rohlf, J. F. 1981. Biometry. W. H. Freeman and Co,
New York. 859 pp.
StatSoft, Inc. 2008. STATISTICA (data analysis software system),
version 8.0. www.statsoft.com.
Sturlaugsson, J. 1995. Migration studies on homing of Atlantic salmon
(Salmo salar L.) in coastal waters W-Iceland—depth movements
and sea temperatures recorded at migration routes by data
storage tags. ICES Document CM 1995/M: 17. 13 pp.
Sturlaugsson, J., and Thorisson, K. 1997. Migratory pattern of homing
Atlantic salmon (Salmo salar L.) in coastal waters W-Iceland,
recorded by data storage tags. ICES Document CM 1997/CC: 09.
23 pp.
Wada, K., and Ueno, Y. 1999. Homing behaviour of chum salmon
determined by an archival tag. NPAFC Document, 425. 29 pp.
Westerberg, H. 1982. Ultrasonic tracking of Atlantic salmon (Salmo
salar L.). 2. Swimming depth and temperature stratification.
Drottningholm, 60: 102– 115.
Whoriskey, F. G., Brooking, P., Doucette, G., Tinker, S., and Carr, J. W.
2006. Movements and survival of sonically tagged farmed Atlantic
salmon released in Cobscook Bay, Maine, USA. ICES Journal of
Marine Science, 63: 1218 – 1223.
doi:10.1093/icesjms/fsn213