711
Timing of smolt migration in sympatric populations
of Atlantic salmon (Salmo salar), brown trout
(Salmo trutta), and Arctic char (Salvelinus alpinus)
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Arne J. Jensen, Bengt Finstad, Peder Fiske, Nils Arne Hvidsten,
Audun H. Rikardsen, and Laila Saksgård
Abstract: A study over a 22-year period of first-time migrants (smolts) of three sympatric salmonids (Atlantic salmon
(Salmo salar), brown trout (Salmo trutta), and Arctic char (Salvelinus alpinus)) in a watercourse in northern Norway demonstrated that although there was considerable overlap in smolt migration timing among the species, Atlantic salmon migrated
first, followed by Arctic char, and finally brown trout. The migration period of Arctic char had a smaller range and less annual variation than those of the two other species, possibly partly related to their more lake-dwelling habitat preference. For
all species, water flow was important in explaining day-to-day variations in smolt runs. Water flow was most important for
brown trout, change in flow for Atlantic salmon, whereas photoperiod was most important for Arctic char. These results suggest that both age and size of smolts and the timing of the smolt migration have been shaped by the different habitat preferences of these species both in fresh water and sea through local selection.
Résumé : Une étude sur une période de 22 ans des saumoneaux qui migrent pour la première fois chez trois salmonidés
sympatriques (le saumon atlantique (Salmo salar), la truite brune (Salmo trutta) et l’omble chevalier (Salvelinus alpinus))
dans un cours d’eau du nord de la Norvège démontre que, bien qu’il y ait un important chevauchement dans la migration
des saumoneaux des différentes espèces, le saumon atlantique migre le premier, suivi de l’omble chevalier et ensuite de la
truite brune. La période de migration de l’omble chevalier a une étendue plus restreinte et une variation annuelle moindre
que celles des deux autres espèces, probablement en partie à cause de sa préférence marquée pour les habitats lacustres.
Chez toutes les espèces, le débit est important pour expliquer les variations de jour en jour des migrations de saumoneaux.
Le débit est le facteur le plus important pour la truite brune, le changement de débit l’est pour le saumon atlantique, alors
que la photopériode l’est pour l’omble chevalier. Nos résultats indiquent que tant l’âge et la taille des saumoneaux que leur
calendrier de migration ont été façonnés par la sélection locale compte tenu des préférences d’habitat différentes de ces espèces, tant en eau douce qu’en mer.
[Traduit par la Rédaction]
Introduction
For diadromous fishes, habitat shifts between fresh water
and the sea can be hazardous (Bell 2009; McDowall 2010),
and for salmonids, smolt migration to the sea is a key event
during their life cycle (Klemetsen et al. 2003). It has been
suggested that the survival of smolts depends on a match–
mismatch scenario between the timing of the sea entry and
the annual variation in optimal conditions at sea (Rikardsen
and Dempson 2011), and the timing of this event is influenced clearly by species- or stock-specific genetic selection
in relation to environmental cues (Aarestrup et al. 1999).
Three anadromous salmonids are distributed naturally on
the western coasts of Europe; Atlantic salmon (Salmo salar)
is distributed in Europe and along the eastern coast of North
America, brown trout (Salmo trutta) is indigenous to Europe,
whereas Arctic char (Salvelinus alpinus) has a circumpolar
distribution (Klemetsen et al. 2003). However, sympatric
anadromous forms of all three species are found only in Iceland, in northern Norway, and in northwestern Russia. They
are all autumn spawners, and Atlantic salmon and brown
trout usually deposit their eggs in gravel in stream beds,
whereas Arctic char usually spawn in lakes when these are
available in the native watercourse. The duration of their juvenile freshwater stage (parr stage) varies from 1 to 6 years
or more, dependent on climate and latitude, where populations in colder habitats take longer to reach the smolt stage
(L’Abée-Lund et al. 1989; Metcalfe and Thorpe 1990; Klemetsen et al. 2003).
Received 25 May 2011. Accepted 3 January 2012. Published at www.nrcresearchpress.com/cjfas on 16 March 2012.
J2011-0230
Paper handled by Associate Editor Michael Bradford.
A.J. Jensen, B. Finstad, P. Fiske, N.A. Hvidsten, and L. Saksgård. Norwegian Institute for Nature Research (NINA), NO-7485
Trondheim, Norway.
A.H. Rikardsen. Department of Arctic and Marine Biology, University of Tromsø, NO-9037 Tromsø, Norway.
Corresponding author: A.J. Jensen (e-mail: [email protected]).
Can. J. Fish. Aquat. Sci. 69: 711–723 (2012)
doi:10.1139/F2012-005
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712
Atlantic salmon parr usually stay in running water, brown
trout may choose both lotic and lentic habitats during the
parr stage of their life cycle, while Arctic char usually stay
in lakes during the whole of their freshwater life (Klemetsen
et al. 2003). However, various populations of Atlantic salmon
may also use lacustrine areas (Einarsson et al. 1990; Halvorsen and Jørgensen 1996; Matthews et al. 1997), and in
northern regions some populations of Arctic char also utilize
running water (Jensen 1994; Jensen and Rikardsen 2008).
The smolt migration varies with temperature and latitude
and generally occurs during a few weeks between April
(south) and July (north). Before this, the individuals go
through a size- and growth-related and endocrine-controlled
smoltification process that adapts the individuals to a life in
salt water (Høgåsen 1998; Thorpe et al. 1998; Marshall and
Grosell 2006). It is generally accepted that day length triggers
the onset of smoltification, water temperature regulates the
rate and duration of this process, and once the fish are ready
to migrate, a proximate stimulus actually provokes the migration (Hoar 1976, 1988). The environmental factors that trigger downstream migration are usually level or rate of water
flow and (or) water temperature (Thorstad et al. 2011). However, these factors can stimulate the smolt migration differently in different populations and species, reflecting different
adaptations to ensure optimal conditions and high survival at
sea entry (Hvidsten et al. 1995, 1998; McCormick et al.
1998).
Differences among the species with respect to habitat
choice and duration of sea residency are expected to be important for the timing of their respective migrations from
fresh water to seawater. After smoltification, brown trout and
Arctic char usually migrate to the sea each summer, where
they feed in coastal areas close to their natal river and then
return to fresh water after a few months to spawn and (or)
overwinter (Jonsson and Jonsson 2011), although some pure
riverine populations of both species are found in the sea in
periods also during winter (Jensen and Rikardsen 2008). In
contrast, Atlantic salmon migrate to the open sea soon after
reaching the sea (Thorstad et al. 2011) and stay in the ocean
until they mature and return to fresh water 1–4 years later.
The smolt migration of Atlantic salmon has been studied
more thoroughly than the migrations of the other two species.
McCormick et al. (1998) and Thorstad et al. (2011) have reviewed comprehensively the smolt migration of Atlantic salmon and the effects of temperature, water flow, and other
environmental parameters on migration. There are a few similar studies on brown trout (Bohlin et al. 1993b; Jonsson and
Jonsson 2002; Byrne et al. 2004) and Arctic char (Berg
1995; Carlsen et al. 2004), and also some few studies on
more than one species during the same time period in the
same watercourse, like in the River Piddle, Dorset, UK (Solomon 1978), the River Imsa in southwest Norway (Jonsson
and Ruud-Hansen 1985; Jonsson and Jonsson 2002), and the
Burrishole system in Ireland (Byrne et al. 2003, 2004). However, there is little comparative knowledge about smolt migration in two or more species in the same river system in
relation to timing of migration, and we have not found any
studies comparing the effects of environmental factors and
habitat preferences on the timing of smolt migration among
species within the same river system.
In the Hals watercourse in northern Norway, Atlantic sal-
Can. J. Fish. Aquat. Sci. Vol. 69, 2012
Fig. 1. Map of the study area in northern Norway.
mon and anadromous brown trout and Arctic char live in
sympatry. The smolt migration of these species was studied
here for 22 years between 1988 and 2009. As mentioned
above, the survival of the smolts during their migration appears to depend on the precise timing of sea entry with the
most optimal conditions at sea (Rikardsen and Dempson
2011). In spite of the previous studies, it remains unknown
whether the smolts of these three species are adapted to reach
seawater at the same time or whether there is some segregation between them. Here we test the hypotheses that smolts
of these three species migrate at the same time of the year,
at the same age and body length, and that the factors most
closely associated with variation in daily counts are similar
for all three species.
Materials and methods
Study area
The Hals watercourse (70°2′N, 22°57′E) has a catchment
area of 143 km2 and drains into the Alta Fjord in northern
Norway. Approximately 20 km of the lower part of the watercourse are available for anadromous salmonids, including
Arctic char, brown trout, and Atlantic salmon. This includes
a 1.2 km2 lake that is located 2.1 km from the sea and 30 m
above sea level (Lake Storvatn, Fig. 1). The river and lake
are ice-covered from December through March–April. The
average annual water discharge is 4.3 m3·s–1. The flow is
characterized by low discharge during the period when the
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Fig. 2. (a) Annual water discharge in the River Halselva (mean value for the period 1989–2009) and (b) annual water temperatures in
the River Halselva (solid line, mean value for the period 1988–2009)
and in the sea beyond the river mouth at a depth of 3 m (dotted line,
mean value for the period 1988–2009).
river is covered with ice, a pronounced increase during the
snow-melting period in May–June, and a decrease again during July–August (Fig. 2a). The river temperature (Fig. 2b) is
close to zero during the ice-covered period, increases during
spring and summer to a maximum of approximately 13 °C in
early August, and then decreases again during autumn. The
sea temperature is at a minimum of approximately 2.5 °C in
late March and highest (approximately 11 °C) during late
July and early August (Fig. 2b).
Water temperatures in the outlet river (River Halselva)
were measured during the whole year every 4 h during
1987–1998 and every hour during 1999–2009 by use of temperature loggers, while sea temperatures were measured with
the same frequency during the same period at a depth of 3 m,
approximately 100 m from shore and 300 m north of the
river outlet.
Fish sampling
Since 1987, permanent fish traps have been situated 200 m
above the estuary of the river and catch all passing fish larger
than approximately 10 cm. Descending fish were caught in a
713
Wolf trap (Wolf 1951) (apertures 10 mm, inclination 1:10),
whereas ascending fish were captured in a fixed box trap.
The traps operated during the ice-free period of the year
(April–October) and emptied twice every day (at 0800 and
2000 hours). The body length (natural tip length, mm) and
mass (g) of all downstream and upstream migrating fish
were recorded before they were released. All fish larger than
14 cm (since 1993, Arctic char and brown trout larger than
18 cm) were tagged individually with numbered Carlin tags.
Smaller fish were tagged by removing a flap on one or both
maxillary bones (Gjerde and Refstie 1988) in a systematic
manner to enable future identification of year of descent. As
a consequence, from 1988 and onwards, smolts (untagged individuals) could be distinguished easily from veteran migrants (tagged individuals) in the trap. The total numbers of
smolts included in this study were 22 450 Atlantic salmon,
21 044 brown trout, and 29 312 Arctic char. Each year, between 300 and 2000 (mean 1000) Atlantic salmon, 300 and
1400 (mean 950) brown trout, and 500 and 3600 (mean
1350) Arctic char smolts of wild origin descended the river.
Some individuals (usually every 30th fish) were killed routinely and analyzed for age, sex, and sexual maturation. In total, 1534 Atlantic salmon, 822 brown trout, and 1626 Arctic
char were aged, sexed, and degree of maturation determined,
after Ricker (1971).
Statistical analysis
Stepwise multiple regression models were used to examine
the relationships between daily smolt catch (dependent variable) and water flow, water temperature, changes in water
flow and water temperature, moon phase, and a proxy for
photoperiod (independent variables). At this latitude (70°N),
the sun is above the horizon continuously between 16 May
and 26 July, that is, during most of the smolt migration period, and although light intensity can change considerably
during the day, day length is 24 h throughout this period.
Hence, neither photoperiod nor day length was suitable as an
independent variable. As a consequence, we used the altitude
of the sun at solar noon at the city of Tromsø (69°39′N,
18°56′E) as a proxy variable for photoperiod (http://www.
timeanddate.com/worldclock/sunrise.html).
Only the main migration period was included in the analyses, meaning that the earliest and the latest 10% of migrating
fish were excluded. As a consequence, the periods included
in the analyses were 5 June to 29 July for Atlantic salmon,
10 June to 31 July for brown trout, and 14 June to 14 July
for Arctic char, respectively. To test the null expectation of
how many smolts would have been caught on a given date if
there was no variation in environmental factors, we used the
total number of smolts caught during the season minus the
number of smolts already caught, divided by the number of
days left in the trapping season as an offset in the model.
For a variable to be entered into the model, a probability of
≤0.05 was required, whereas for a variable to be removed, a
probability of ≥0.10 was required.
First, the expected number of fish from a null model (number of fish remaining divided by the number of days remaining) was corrected for by subtracting this expectancy from
the observed number of fish on each day. This new variable
was called the corrected number of fish. From a previous
study (Hvidsten et al. 1995), we expected social behavior
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714
generating an autoregressive structure in the number of fish
descending. A significant contribution on lag 1 from a partial
autocorrelation function was found for all three species.
Therefore, the residuals from AR1 models fitted for each
year of the corrected number of fish were used. Stepwise
multiple regression models were then performed with these
residuals as the dependent variable and environmental variables as independent variables. In this way, both the variability
caused by the fact that when few fish are remaining in the
river, few fish are expected to migrate, as well as the autocorrelations across days that may be caused by social interactions among the fish, were controlled for.
Can. J. Fish. Aquat. Sci. Vol. 69, 2012
Fig. 3. Distribution of age for smolts of (a) Atlantic salmon (n =
1534), (b) brown trout (n = 822), and (c) Arctic char (n = 1626)
caught in the trap in the River Halselva during their seaward migration over the period 1988–2009.
Results
Age and size
Atlantic salmon smolts were the youngest on average
(4.14 ± 0.69 standard deviation (SD) years), whereas brown
trout smolts were slightly younger than Arctic char on average (4.88 ± 0.97 years vs. 5.04 ± 2.05 years). However, a
considerably higher variation in age was observed for Arctic
char than for the other two species; there was a substantial
proportion of Arctic char smolts that were as young as 2–
3 years and others up to 12 years old (Fig. 3).
Atlantic salmon smolts were the smallest (142.8 ±
14.28 mm), Arctic char were intermediate in size (173.2 ±
35.91 mm), and brown trout were the largest on average
(195.2 ± 33.55 mm). In Atlantic salmon, most individuals
were between 130 and 170 mm, whereas a substantial proportion of the two other species was larger than 170 mm
(Fig. 4). In all species, smolt size increased with age (Table 1,
Table 2), with the most pronounced increase seen in brown
trout (Table 1). Some of the largest individuals may have
been residual freshwater residents that for some reason chose
to move out of the system. However, excluding all individuals larger than 250 mm did not change our results.
For all species, smolt length increased during the main migration period, but decreased again later in the summer
(Fig. 5). This seasonal variation was described best by quadratic equations (Fig. 5), which fitted the data highly significantly for all three species (P < 0.001). Also on an annual
basis, quadratic equations significantly (P < 0.05) described
the seasonal variation in smolt length in 17, 19, and 18 out
of the 22 years of data for Atlantic salmon, brown trout, and
Arctic char, respectively.
Migration time
In general, smolts of Atlantic salmon migrated first, followed by Arctic char and then brown trout, with pronounced
peaks and median dates of descending 22 June, 25 June, and
4 July, respectively (Table 3), although some smolts of all
three salmonids left the river throughout most of the ice-free
period of the year (Fig. 6). The median date was significantly
different between the three species (paired-samples t tests:
t = –8.12, P < 0.001, df = 21 for Atlantic salmon – brown
trout; t = –2.26, P = 0.034, df = 21 for Atlantic salmon –
Arctic char; t = 8.73, P < 0.001, df = 21 for brown trout –
Arctic char). The main migration period (i.e., the number of
days from 25% to 75% of the smolts had left the river) of
Arctic char lasted for 13.45 ± 5.02 days, which was significantly shorter than that for Atlantic salmon (25.14 ±
13.11 days) and brown trout (27.91 ± 8.53 days) (pairedsamples t tests: t = 4.49, P < 0.001, df = 21 for Atlantic salmon – Arctic char; t = 9.39, P < 0.001, df = 21 for brown
trout – Arctic char; t = –1.12, P = 0.276, df = 21 for Atlantic salmon – brown trout). However, there was substantial annual variation, with ranges of 28, 15, and 30 days between
the earliest and latest median date for the three species, respectively. Hence, the median date for Arctic char was more
stable from year to year than those of the two other species.
Different from the other species, Atlantic salmon had a second small peak of migration in October–November (Fig. 6).
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Fig. 4. Distribution of length for (a) Atlantic salmon, (b) brown
trout, and (c) Arctic char smolts descending from the River Halselva
during the period 1988–2009.
Interannual variation in median migration time was signficantly positively correlated among the three species (Fig. 7).
Hence, in years with early descent of Atlantic salmon, Arctic
char and brown trout also migrated early. There was no significant trend with time in migration date over the course of
the study (1988–2009) for any of the species (Table 4). As
well, there was no trend through time in mean river temperature in June (y = –85.1 + 0.045x, r2 = 0.039, P = 0.406).
Both river and sea temperatures at the median date of
smolt migration varied considerably among the years of the
study (Table 5). In general, both temperatures were lowest
for Atlantic salmon, which migrated first, followed by Arctic
char and brown trout, which left the river at later dates. River
and sea temperature at the median date of smolt migration for
Atlantic salmon and brown trout were significantly different
(Bonferroni post hoc tests, P < 0.001 and P = 0.012, respectively). Also, river temperatures at the median date of migration for brown trout and Arctic char were significantly
different (Bonferroni post hoc test, P = 0.011), while other
temperatures were not significantly different (P > 0.05).
715
The seaward migration was negatively correlated with
mean river temperature in June for all three species, although
this was not significant for brown trout (Fig. 8); that is, descent was delayed in years with lower June temperatures.
Values of r2 from the AR1 models varied among years for
all species, with mean values across years of 0.31, 0.22, and
0.26 and ranges of 0.001–0.63, 0.002–0.51, and 0.00–0.60
for Atlantic salmon, brown trout, and Arctic char, respectively. Further, multiple regression models explained 12%,
13%, and 6% of the residual variation in downstream migration of Atlantic salmon, brown trout, and Arctic char, respectively (Table 6). Thus, the models combined accounted for
32%–43% of the variation in downstream movements. For all
species, water flow was included in the multiple regression
model as a proximate factor explaining day-to-day variation
in smolt runs (Table 6). The rank of the different parameters
included in the model differed between the three species.
Change in water flow was the most important factor for Atlantic salmon, water flow was most important for brown
trout, and altitude of the sun at solar noon (i.e., photoperiod)
was most important for Arctic char (Table 6). Moon phase
was not included for any species. The residuals from the regression models did not differ significantly among years for
any of the three species (analysis of variance (ANOVA), Atlantic salmon: F[1,19] = 0.52, P = 0.95; brown trout: F[1,19] =
0.86, P = 0.63; Arctic char: F[1,19] = 0.20, P = 1). Hence,
among year variation in smolt migration patterns was accounted for by using the residuals from the AR1 model as
the dependent variable in the regressions.
Sex and sexual maturation
An equal proportion of females and males were detected in
the smolt runs of both Atlantic salmon (c2 = 0.709, df = 1,
n = 1 355, P > 0.05) and Arctic char (c2 = 0.006, df = 1,
n = 1 585, P > 0.05), with 51.1% and 49.9% females for Atlantic salmon and Arctic char, respectively. Among brown
trout, females predominated and constituted 63.1% of the
smolts (c2 = 40.8, df = 1, n = 589, P < 0.001). There were
no age difference between the sexes of Atlantic salmon
(Mann–Whitney U test, P = 0.809) and brown trout (Mann–
Whitney U test, P = 0.059), but Arctic char females dominated among the older individuals and males among the
younger ones (Mann–Whitney U test, males mean smolt
age = 4.74, females mean smolt age = 5.29, P < 0.001).
All females of Atlantic salmon and brown trout were immature. Among Arctic char, 0.5% of the females were mature
(out of 791 examined). Mature males were observed only
among Atlantic salmon, all of them during autumn, and constituted 1% of the males.
Among the Atlantic salmon smolts that descended during
the second, small peak in October–November (Fig. 6), 89%
(n = 106) were males, whereas 92% of these were mature
(some of them with running milt). All autumn migrating females were immature. The age and size of the mature autumn
migrating males (3.77 ± 0.55 years, 137.9 ± 10.7 mm, n =
86) did not differ significantly from the corresponding immature fish in the same period (3.73 ± 0.67 years, 142.9 ±
17.3 mm, n = 20, P > 0.05), but both groups were significantly younger (P < 0.001), but not smaller (P > 0.05), than
the smolts that migrated earlier. None of the 242 CarlinPublished by NRC Research Press
716
Can. J. Fish. Aquat. Sci. Vol. 69, 2012
Table 1. Average length (mm) of Atlantic salmon, brown trout, and Arctic char smolts of different ages caught
in the downstream trap in the River Halselva during 1988–2009.
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Atlantic salmon
Smolt age
(years)
2
3
4
5
6
7
8
9
10
11
12
Length
117.67
133.78
142.94
152.14
158.78
149.0
SD
13.65
11.61
12.64
15.91
14.15
14.14
Brown trout
n
3
226
893
379
32
2
Length
116.67
149.79
178.64
193.36
203.47
215.68
216.00
Arctic char
SD
10.97
25.35
22.11
19.04
19.25
25.83
32.41
n
3
48
221
335
159
31
4
Length
127.75
145.09
166.62
184.54
191.88
193.46
192.66
195.77
196.85
197.00
183.00
SD
11.13
18.54
22.99
24.12
28.63
26.05
26.16
25.50
19.10
42.48
—
n
83
453
213
233
229
194
134
62
26
5
1
Note: SD, standard deviation; n, sample size.
Table 2. Relationship between smolt length and smolt age for Atlantic salmon, brown trout, and Arctic
char descending from the River Halselva during the period 1988–2009.
Species
Atlantic salmon
Brown trout
Arctic char
Parameter estimates
Model summary
b0
107.4
117.5
122.0
F
319.4
364.0
1056
b1
8.87
14.7
9.88
df1
1
1
1
df2
1533
799
1631
r2
0.172
0.313
0.393
P
<0.001
<0.001
<0.001
Note: b0, intercept in the regression line; b1, slope of the regression line; F, F value in the statistical test; df1
and df2, degrees of freedom; r2, coefficient of determination; P, level of significance.
tagged individuals of autumn migrating Atlantic salmon
smolts have been reported recaptured.
Discussion
The present study reports a considerable overlap in smolt
migration among the three species of salmonids in the River
Halselva, although Atlantic salmon migrated first, followed
by Arctic char, and finally brown trout. The migration period
of Arctic char had a smaller range and less annual variation
than those of the two other species, possibly partly related to
their more lake-dwelling habitat preference. For all species,
water flow was included in the model explaining day-to-day
variations in smolt runs. Water flow was most important for
brown trout, changes in water flow most important for Atlantic salmon, whereas photoperiod was most important for Arctic char.
The general ability of anadromous salmonids to survive in
seawater increases with body size (McCormick and Naiman
1984; McCormick 1994; Finstad and Ugedal 1998). Larger
individuals are less vulnerable to predation than smaller individuals (Dill 1983) and are also more tolerant to the osmotic
pressure that is associated with low seawater temperatures
(Sigholt and Finstad 1990). Based on several studies, as referred to in McCormick (1994), there is a strong correlation
between the age at migration and fish size for the migratory
behaviour and seawater tolerance. Rounsefell (1958) stated
that the salmonid genera Oncorhynchus had the earliest development of salinity tolerance, followed by Salmo and then
Salvelinus. The parr–smolt transformation of Atlantic salmon,
Arctic char, and brown trout follows a similar pattern with
respect to the development of the hypo-osmoregulatory ability and regulatory (endocrine) mechanisms (Finstad and Ugedal 1998; Jørgensen et al. 2007). After sea entry, Atlantic
salmon postsmolts, as the smallest and youngest of the three
species, commonly use only a few days to leave fjord and
coast to the assumed safer open sea where they feed for 1–
4 years (Thorstad et al. 2011). In contrast, the larger sized
postsmolts of brown trout and the intermediate sized Arctic
char remain in coastal areas not far from their natal river before they return to fresh water (Klemetsen et al. 2003). Normally, the sea sojourn of Arctic char postsmolts is shorter
than that of brown trout, and in the present study their first
sea sojourn in average lasted for 1 and 2 months, respectively
(A.J. Jensen, unpublished data). Hence, the different smolt
size of the three sympatric species might reflect an unequal
selection pressure for optimal size for the three species in relation to a trade-off among size-selective mortality at sea, the
time that they stay in predation and parasite risky coastal
areas, and the increased mortality by staying one extra year
in fresh water.
In contrast with some other studies on Arctic char (Rikardsen et al. 1997; Rikardsen and Elliott 2000), the age and
length distribution of smolts of this species in the present
study were asymmetrical and skewed to the right and hence
also deviated from those of Atlantic salmon and brown trout.
In addition, the age distribution was bimodal with maxima at
smolt ages of 3 and 5–6 years. These skewed distributions
indicate selection for larger and older than average individuals of Arctic char in the present watercourse, but not for the
two other species. There are, however, at least two other exPublished by NRC Research Press
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Fig. 5. Seasonal variation in length (mm) of smolts descending
through the fish trap in the River Halselva over the period 1988–
2009: (a) Atlantic salmon (r2 = 0.126, y = –0.0031x2 + 1.36x +
1.377, F[2,19301] = 1388, P < 0.001); (b) brown trout (r2 = 0.046,
y = –0.0051x2 + 1.87x + 25.3, F[2,16941] = 408, P < 0.001); and
(c) Arctic char (r2 = 0.072, y = –0.0067x2 + 2.72x – 95.8,
F[2,28172] = 1 097, P < 0.001).
planations to this. First, resident char may transform into
anadromous char after spawning one to three times, as described from the Salangen River system (Nordeng 1961,
1983), and such individuals will be larger and older than
maiden first-time migrants. Second, in the Halselva watercourse growth rates of young Arctic char differ considerably
717
Table 3. Median date for descent and range in median date
among years of descent for Atlantic salmon, brown trout, and
Arctic char smolts caught in the fish trap in the River Halselva during the period 1988–2009.
Species
Atlantic salmon
Brown trout
Arctic char
Median date
22 June
4 July
25 June
Range
7 June – 5 July
19 June – 18 July
17 June – 2 July
between the different habitats, with considerably higher
growth rates in the rivers than in the lake (Strand and Heggberget 1994; Jensen 1995). Arctic char parr are numerous in
the tributary to Lake Storvatn and are also present in lower
densities in the main river downstream of the lake (Strand
and Heggberget 1994; Jensen 1995), and they are also numerous in the profundal part of the lake (Strand and Heggberget 1994). River-dwelling Arctic char grow considerably
faster than Atlantic salmon and brown trout parr found at the
same localities in the watercourse (A.J. Jensen, unpublished
data) and hence smoltify at a younger age than the two other
species. Similar results have been observed for Arctic char in
other watercourses (Jensen 1994), and this is contrary to Atlantic salmon parr living in lakes, where they grow faster
than experienced by fluvial counterparts (Hutchings 1986;
Halvorsen and Svenning 2000). The main reason for the fast
growth of river-dwelling char is probably that despite the
very similar thermal performances of the three species, the
growth efficiency (per unit food) of Arctic char is twice that
of the two other species (Jonsson et al. 2001; Forseth et al.
2009; Finstad et al. 2011). Lake-dwelling Arctic char, however, experience conditions with fewer nutrients and lower
water temperature than river-dwelling individuals, because
young char in lakes that live sympatric with brown trout usually select benthic and deep-pelagic habitats (Johnson 1980;
Klemetsen et al. 2003). Hence, the parr population of Arctic
char consists of two groups, river-dwelling individuals with
smolt ages of 2–4 years and lake-dwelling individuals with
smolt ages of 3–12 years, making the smolt age distribution
bimodal.
For all three species, smolt size increased with age. The
transformation from parr to smolt has been shown to be related to factors such as body size, growth rate, developmental
rate, and physiological state of the fish (Klemetsen et al.
2003), and the developmental rates (growth, smolting, maturation) in salmonids are heritable, but operate under environmental instruction (Thorpe et al. 1998). Rikardsen and Elliott
(2000) showed that the seasonal growth pattern of the individual determins its age and size at smoltification. The fastgrowing individuals with high metabolic rates were the first
to become constrained by the food limitations in fresh water
and therefore smoltified at a younger age and smaller size
than the intermediate and slower-growing individuals, possibly corresponding to the youngest, but also smallest, smolts
of all the studied species in the present study.
The mean size of smolts of all three species increased during the main migration period and decreased again later in
summer. The finding that smaller smolts tend to migrate later
in the season than bigger ones has been reported for several
other locations (Ewing et al. 1984; Bohlin et al. 1993a),
while the observation that the earliest migrants were also
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718
Can. J. Fish. Aquat. Sci. Vol. 69, 2012
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Fig. 6. The time of seaward migration of smolts of Atlantic salmon (solid line), brown trout (dash-dotted line), and Arctic char (dashed line)
from the River Halselva during the period 1988–2009 (5-day moving average).
Table 4. Relationship between median descending day (day of the
year) and calendar year for smolts of Atlantic salmon, brown trout,
and Arctic char during the period 1988–2009.
Species
Atlantic salmon
Brown trout
Arctic char
Parameter estimates
Model summary
b0
308
200
127
F[1,20]
0.063
0.001
0.901
b1
–0.068
–0.007
0.152
r2
0.003
0.001
0.043
Table 5. Mean river and sea temperatures (°C) at the median date
for descent of Atlantic salmon, brown trout, and Arctic char from
the River Halselva during the period 1988–2009.
River temperature
P
0.804
0.975
0.354
Note: b0, intercept in the regression line; b1, slope of the regression line;
F, F value (with degrees of freedom) in the statistical test; r2, coefficient of
determination; P, level of significance.
smaller than average has not been reported before. The earlymigrating fish might be individuals with the highest metabolic requirements and growth rates (Rikardsen and Elliott
2000), possibly selecting for an early migration to a habitat
with higher food availability (i.e., the sea). One explanation
that some small individuals migrated to the sea in late
summer is that these individuals were too small to smoltify
in spring, but reached a length suitable for smoltification later
in the summer and hence migrated to the sea at a later date.
However, the survival of fish that leave the river outside the
most profitable “smolt window” is expected to be poor (Rikardsen and Dempson 2011).
The annual median time of migration in the River Halselva
correlated significantly among the three species, which indicated that similar environmental factors regulate the parr–
smolt transformation in these species. The observation that
migration was delayed in years with low water temperatures
in June (not significant for brown trout) confirms that in addition to photoperiod, water temperature is the main factor
that regulates the parr–smolt transformation (McCormick et
al. 1998). On the other hand, day-to-day variations in smolt
migration was best explained by a model that for Atlantic salmon only included changes in water flow and water flow. For
brown trout, water temperature measures (both change in
temperature and temperature) were included in the model in
Species
Atlantic salmon
Brown trout
Arctic char
Mean
6.78
8.79
7.42
SD
1.52
1.58
1.29
Sea temperature
Range
5.0–10.2
6.5–11.7
5.5–10.2
Mean
8.22
9.54
8.63
SD
1.65
1.25
1.34
Range
5.6–11.3
7.1–11.3
6.0–11.1
Note: SD, standard deviation; range, range among years.
addition to water flow and changes in water flow. This, in
combination with a more dispersed and longer migration period for brown trout, provides evidence that the parr–smolt
transformation of this species occurs in a less punctual manner than that in Atlantic salmon.
In contrast with the other two species, the altitude of the
sun at solar noon, which was used as a proxy variable for
photoperiod, was the environmental parameter that correlated
best with the smolt run of Arctic char during a period of 24 h
of sunlight at these latitudes. As discussed earlier, most of
the presmolts of Arctic char live in Lake Storvatn, and many
of these are in the profundal habitat. Hence, these do not that
easily sense increased water flow or water temperature, in
contrast with individuals that live in the river. Thus, water
flow and temperature are not suitable cues to initiate the
smolt run for most Arctic char. Photoperiod and day length
are related more closely to a specific calendar date than water
flow and temperature, and this is expected to be one main
reason why Arctic char smolts migrated more synchronously
and at a more fixed time of the year than the two other species.
Flow, temperature, and light have been cited as key environmental stimuli triggering seaward migration of Atlantic
salmon, which is the most studied of the three species (Klemetsen et al. 2003). However, the relative importance of
these factors likely varies among populations, locations, and
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Jensen et al.
719
Fig. 8. Relationships between mean water temperature in June (°C)
in the River Halselva and the median date (day of the year) for smolt
descent for (a) Atlantic salmon (y = –3.26x + 192, r2 = 0.305, P <
0.05), (b) brown trout (y = –1.68x + 195, r2 = 0.117, P = 0.140),
and (c) Arctic char (y = –2.50x + 191, r2 = 0.563, P < 0.001).
years (Ruggles 1980; McCormick et al. 1998; Klemetsen et
al. 2003). In rivers where high spring floods are common, as
in River Halselva, water flow may often be the most important factor (Hvidsten et al. 1995). For brown trout, water temperature (Jonsson and Jonsson 2002) or a combination of
water temperature and water flow (Bohlin et al. 1993a,
1993b; Hembre et al. 2001) have been reported to be the
main cues to initiate emigration of smolts, while such data
for Arctic char are lacking.
As for the variation in size and age among the three species, the differences in the timing of smolt descent among
the species are also expected to reflect different adaptation
strategies to life at sea. Several studies have been conducted
on the marine habitat use and feeding of Arctic char and
brown trout originating from the Hals watercourse. Both
brown trout and Arctic char feed commonly in shallow, nearshore areas in the fjord and partly on different food items
(Rikardsen et al. 2007a), and they partly utilize different
depth and temperature habitats within the fjord (Rikardsen et
al. 2007b). Also, more piscivorous feeding behaviour of
brown trout indicates that this species is less dependent on
precise timing of smolt migration than Arctic char and can
enter the sea later. The earlier sea entry of Arctic char than
sea trout may therefore be an adaption to different thermal
habitat and prey preferences in the sea. For Atlantic salmon,
it may be important to reach the open sea as early as possible
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Fig. 7. Relationships between the median day for the seaward migration of smolts of the three salmonids in the River Halselva during the
period 1988–2009: (a) Atlantic salmon versus brown trout (y =
0.454x + 106.4, r2 = 0.291, P < 0.01); (b) Atlantic salmon versus
Arctic char (y = 0.277x + 128.3, r2 = 0.209, P < 0.05): and (c) Arctic
char versus brown trout (y = 0.786x + 46.5, r2 = 0.320, P < 0.01).
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720
Can. J. Fish. Aquat. Sci. Vol. 69, 2012
Table 6. Multiple regression models that describe the environmental variables,
in order of importance, that provide the best explanation of smolt migration for
the three species.
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Parameter
Atlantic salmon (r2 = 0.12)
1. Change in flow
2. Water flow
(Constant)
Brown trout (r2 = 0.13)
1. Water flow
2. Water temperature
3. Change in flow
4. Change in temperature
(Constant)
Arctic char (r2 = 0.06)
1. Altitude of the sun at solar noon
2. Water flow
3. Water temperature
(Constant)
B
t
P
1.616
0.441
–5.96
9.25
6.31
–5.20
<0.001
<0.001
<0.001
0.702
1.590
0.575
–2.083
–23.17
7.80
7.80
4.11
–2.39
–9.08
<0.001
<0.001
0.002
0.017
<0.001
12.58
0.489
2.321
–570.3
5.02
53.38
3.32
–5.09
<0.001
0.001
0.001
<0.001
Note: The data are for the period 1990–2009. B, unstandardized coefficients; t, values
in the t test; P, level of significance. The dependent variables are the residuals from the
AR1 model for each species. Only factors significant at the 0.05 level were included.
to reduce both the predation and parasite (e.g., salmon lice)
pressure that often increases during summer in the fjords
(Bjørn et al. 2007) and also to maximize the length of the
postsmolt growth period, which is considerably shorter than
that for populations further to the south (Jensen et al. 2011).
On the other hand, studies have shown that Atlantic salmon
postsmolt survival is often positively correlated with high
sea water temperatures during the spring, probably mainly related to a higher food availability at high temperatures along
the Norwegian coast (Hvidsten et al. 2009). In the present
study, the variation in sea temperature at sea entry for all
three species between years was considerable, and postsmolt
mortality is expected to be high in cold years owing to low
tolerance to salinity at low sea temperatures (Sigholt and Finstad 1990) and lower food abundance (Rikardsen and Dempson 2011). Based on all this, it is likely that the different
species will have different match–mismatch scenarios related
to their timing of sea entry to ensure the most optimal conditions for growth and survival at sea.
We found no shift in migration time over the course of the
study for Atlantic salmon, brown trout, or Arctic char. This is
consistent with 30-year studies on brown trout in Ireland
(Byrne et al. 2003) and on Atlantic salmon in northern Finland (Jutila et al. 2005). In addition, the timing of migration
of stocks into the Gulf of St. Lawrence appears to have
changed little over the past century. In contrast, in the Gulf
of Maine and the Nova Scotia area, as well as in River
Bush, Northern Ireland, the migrations of salmon smolts
have shifted to earlier dates (Friedland et al. 2003; Kennedy
and Crozier 2010).
The sex ratio in a smolt run reflects the reproductive strategy of the population and mainly that of males. Maturation
of Atlantic salmon males in fresh water before smolting (precocious males) has been reported throughout their geographi-
cal range, but its incidence varies among localities. In
contrast, females migrate to sea almost exclusively before
maturation (Hoar 1988; Fleming 1996). Only a small fraction
of the precocious males smoltify and survive; hence, the sex
ratio in populations of Atlantic salmon reflects the proportion
of precocious males. In the River Halselva, this group seems
to be rather small. Among Arctic char, males and females
were distributed evenly, whereas females predominated in
the smolt run of brown trout. However, there were significantly more females among the oldest and largest smolts of
Arctic char. This corresponds with findings of Rikardsen et
al. (1997), who hypothesized that this may result in a higher
mortality at sea for males, resulting in the common observed
dominance of females among the mature individuals of this
species found in both their and other studies (Nordeng 1983;
Dempson and Green 1985). Our results may give support to
such a theory, as females dominate the mature individuals of
both species in the Hals watercourse (A.J. Jensen, unpublished data).
Atlantic salmon that left the river during the second peak
in October–November were younger and smaller than those
that descended during the main peak in June, and there was
a predominance of mature males. The downstream migration
of Atlantic salmon parr in autumn has been reported previously on both sides of the Atlantic Ocean (Buck and Youngson 1982; Cunjak et al. 1989). The ecological drivers for
such migrations are unclear, although several mechanisms
have been proposed (Riley et al. 2009). In the River Frome
in southern England, a large part of the population is expected to migrate to the estuary during autumn, and a few
tagged fish have been recaptured as grilse. However, the
River Halselva is a small river that is covered with ice and
has a very low discharge during winter, and there is no estuary in which Atlantic salmon parr can survive during winter.
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Jensen et al.
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No tagged fish have been recaptured, and we expect that Atlantic salmon that migrate to sea from this river during autumn do not survive.
On the basis of the results from this study, the hypotheses
that smolts of Atlantic salmon, brown trout, and Arctic char
migrate to the sea at the same time of the year, and at the
same age and size, are rejected. Further, the results suggest
that both the age and size of smolts and the timing of the
smolt migration have been shaped by the different habitat
preferences of these species both in fresh water and at sea
through local selection.
Acknowledgements
This study was financed by the Directorate for Nature
Management and the Norwegian Institute for Nature Research. This work could not have progressed without the invaluable assistance of the staff at the Talvik Research Station
with the traps in the River Halselva. Ola Diserud, NINA, is
thanked for help with the statistical analyses, and two anonymous referees are thanked for valuable criticism of an earlier
version of this paper.
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