Cap 5. - Smolts and Smolting

Chapter 5
Smolts and Smolting
5.1 Organization of the Chapter
This chapter describes important elements of the parr-smolt transformation

(smolting) in Atlantic salmon and brown trout. Smolting is a preparatory physiolo
gical adaptation, which occurs in spring prior to the seaward migration. It includes
morphological transformation, and changes in salinity tolerance, visual pigments,
buoyancy, metabolism and behaviour. The changes precede the downstream
migration, and prepare the fish for marine life in pelagic waters. Smolting occurs
coincident with environmental changes such as increasing day length and tempera-
ture in spring.
The chapter commences with a description of morphological changes that occur
during smolting. In rivers, parr are primarily bottom dwellers and their cryptic
coloration allows them to blend in with the background. At smolting, the fish
acquire a silvery dress, camouflaging them in open water, when viewed from any
direction in mid-water and near the surface. The scales act as small mirrors, which
reflect incoming light. The dark back conceals them when viewed from above,
and the white belly masks it when seen from underneath. Their body form becomes
more streamlined, reflected by a decreased condition factor (weight-to-length ratio),
possibly advantageous during their long marine migrations (Webb 1984).
Then, physiological changes during smolting are briefly described. Iono
regulation is probably the most well-studied physiological change during smolting
(e.g. McCormick and Saunders 1987; Tipsmark et al. 2009). Increased gill
Na+/K+-ATPase activity and differentiation of chloride cells result in greater salt
secretory capacity, and are associated with increased salinity tolerance during
smolting. Freshwater is poor in ions, and the body fluids have higher ionic concen-
tration than the surrounding water. Hence, freshwater fish, such as parr, could
lose ions by diffusion and gain water by osmosis. Therefore, they have mecha-
nisms that retain ions and pump out excess water, and vice versa, for post-smolts
under hypo-osmotic conditions in seawater. During smolting, the ionoregulatory
capacity of the fish in fresh water diminishes temporarily. However, smolts that do
not reach seawater within a few weeks after smolting will desmolt and recoup their
B. Jonsson and N. Jonsson, Ecology of Atlantic Salmon and Brown Trout: 211
Habitat as a Template for Life Histories, Fish & Fisheries Series 33,
DOI 10.1007/978-94-007-1189-1_5, © Springer Science+Business Media B.V. 2011
212 5 Smolts and Smolting
freshwater adaptations (=desmolts). If so, they lose their seawater tolerance, often
accompanied with loss of their silvery coloration. Desmolts exhibit decreased
salinity preference and upstream instead of downstream orientation. Transferred
to seawater they will show respiratory perturbation and can die (Conte and Wagner
1965; Lundqvist and Eriksson 1985; Schmitz 1992; Morin et al. 1994). Smolting is
a seasonally recurring phenomenon, and the desmolted stage remains until the
subsequent spring, when survivors can re-smolt.
Many of the physiological and morphological changes that comprise smolting
are known to be responsive to photoperiod, and advanced by increased day length
and/or delayed by short days (Wedemeyer et al. 1980). Photoperiod is the signal
that influences the hormonal regulation of the processes. Seasonal changes in day
length provide the developing juvenile salmonids with environmental information,
entraining endogenous rhythms regulating smolting. Temperature affects the timing
of the smolting, although to a more limited degree than photoperiod. It adjusts
the start and rate of changes, through its pervasive effects on all physiological and
biochemical reactions in the body. Furthermore, low temperature limits the physio
logical response to increased day length (McCormick et al. 2000).
The endocrine system is the primary signalling pathway between external cues,
internal rhythms and seasonal physiological responses (McCormick et al. 2000).
The parr-smolt transformation occurs in association with a surge in activity of a
number of interacting endocrine systems. Hormones involved are, e.g. the thyroid
hormones, prolactin, growth hormone (GH), insulin-like growth factor I (IGF-I)
and cortisol (Björnsson 1997; Ágústsson et al. 2001; Sundell et al. 2003; McCormick
2001, 2009). The level of most of these hormones increases during smolting. They
stimulate various physiological changes which occur, but the effect of prolactin
is generally inhibitory, impeding the osmotic permeability of gill epithelia, and
thereby antagonizing the seawater adaptive effect of growth hormone (Hoar 1988;
Madsen and Bern 1992; Ebbesson et al. 2008). The prolactin level decreases during
smolting.
After considering the endocrine regulation, we describe behavioural changes
related to smolting. Parr are positively rheotactic; they face into the oncoming
current, and they avoid being swept downstream under regular flow conditions.
At smolting they lose their rheotactic response. Instead, they move away from the
bottom and swim in small schools into the current and move with it towards the sea.
The behavioural changes are described in the third part of the chapter. We discuss
relationships to water temperature and light, and mechanisms to decrease mortality
risks during the downstream movement.
At the end of the chapter, we present ecological characters such as age and size
at smolting, and how these traits vary with latitude, water temperature and growth.
Although smolting is a phenotypically plastic response to environmental cues, it
is also a genetically determined response, adapted through natural selection to
maximize fitness of organisms able to survive in both fresh and salt water. There
is genetic variation among populations in their propensity to smolt, and among
populations performing a parr-smolt transformation, there are genetic variations in
age and size at smolting.
5.2 Morphological and Physiological Changes During Smolting 213
5.2 Morphological and Physiological Changes During Smolting
Morphology and physiology of anadromous salmonids change in spring prior to

seaward migration. The transformation prepares the young fish for a migratory
way of life in pelagic salt-water. Here, we summarize the most important of these
changes associated with smolting.
5.2.1 Colour and Morphology
The most conspicuous colour-change is the development of the intense silvery,

herring-like dress masking the vertical, dark-coloured bars along the flanks
(parr marks), exhibited by the parr (cf. Figs. 1.4 and 1.5; and description in Folmar
and Dickhoff 1980). The pelvic fins lose their dark colour. The white edge, often
bordering the anal fin of brown trout parr, disappears. In Atlantic salmon smolts,
the caudal and pectoral fins darken during smolting.
The silvering is caused by deposition of guanine and hypoxanthine crystals in
the skin, two purines that are metabolic by-products of the protein synthesis.
The purines are placed in two distinct skin layers, one directly beneath the scales
and the other deep in the dermis adjacent to the body muscles. The scale and skin
layers of purines are present also in parr, but thicken and become more apparent in
smolts. The relative fraction of hypoxanthine relative to guanine also decreases
sharply during smolting.
The thyroid hormones have a direct role in the silvering of the fish (Hutchison
and Iwata 1998). Some time ago, Matty and Sheltaway (1967) demonstrated that
the incorporation of glycine (a precursor to guanine) into the skin-guanine increased
after intraperitoneal injection of thyroxin in rainbow trout. Furthermore, silvering
of parr can be achieved by adding thyroxin to food or water (Wedemeyer 1996).
The surge in plasma thyroxin, the primary secretary product of the thyroid gland,
is affected by changes in photoperiod during spring (Leatherland 1982).
The colour change is presumably adaptive for predator avoidance in pelagic
fishes, but may also be essential for water balance in a hyper-osmotic habitat (Hoar
1988). Excretion of purine nitrogen requires water, which is expensive in marine
environments. By depositing purines in the skin they conserve water.
The body form changes during the smolting. There is an increase in length
relative to mass (lower condition factor) (Gorbman et al. 1982; Beeman et al.
1995). The snout becomes more pointed and the body slimmer and more stream-
lined, probably rendering the fish more suited for a migratory way of life (Webb
1984; Hoar 1988). It is unclear to what extent the lower condition factor is part of
an adaptive change in morphology during smolting, and to what extent it is a result
of decreased lipid reserves due to energetic demands during the smolt transforma-
tion (Woo et al. 1978; McCormick et al. 1998; Jonsson and Jonsson 2005). During
smolting, there is also a reduction in skin mucus and scale attachment (O’Byrne-
Ring et al. 2003).
Changes in general body shape and coloration, however, are not sufficient by
themselves to determine the true smolt status, since parr can also have a silvery
appearance, particularly those dwelling in lakes. But, since the parr-smolt trans-
formation involves many metabolic and biochemical changes needed for sea life,
measurement of changes in the ionoregulatory capacity of the fish may be a
more objective signifier of the smolt status, than what is revealed by only a visual
inspection.
5.2.2 Physiology
The different optical and salinity properties in fresh compared to salt water, and
a pelagic instead of an epibenthic way of life, are challenges for anadromous
salmonids. They respond to these challenges by physiological alterations of vision,
buoyancy and ionoregulation mechanisms.
5.2.2.1 Visual Pigments and Ultraviolet Sensitivity
Modifications of the retina of the eyes include loss of ultraviolet-sensitive (UVS)

cone receptors, and switching of visual pigments from porphyropsin to rhodopsin
(Dann et al. 2003). Porphyropsin is most sensitive in the red spectrum, whereas
rhodopsin is maximally blue-sensitive. UVS receptors appear over the whole retina
in early life, but are lost in the metamorphic event, and do not reappear until sexual
maturation and the return to fresh waters (Allison et al. 2006). The thyroxin hormone
appears to influence both the UVS cone-loss and the change of visual pigments in
smolts (Allison et al. 2004; Raine and Hawryshyn 2009).
The change in visual pigment is probably linked to differences in the visual
properties of the two aquatic environments. Marine fishes are typically most sensi-
tive to blue and greens colours in the range of 450–550 nm, whereas freshwater
fishes often are sensitive at higher wave lengths, up to nearly 650 nm (orange-red)
(Lythgoe 1979; Levine et al. 1980). This change in absorption maxima, towards
blue wave lengths, may explain the decreased ability of smolts to maintain visual
positioning during evening-twilight in fresh water (Hasler and Scholz 1983).
5.2.2.2 Buoyancy and Metabolism
During smolting, there are increased buoyancy, lipid metabolism and protein
synthesis. The relative size of the swim bladder increases, which may be helpful
during downstream migration and subsequent feeding in pelagic seawater (Saunders
1965). Furthermore, the rate of oxygen-consumption increases, with augmented cata
bolism of carbohydrate, fat and proteins (Wedemeyer et al. 1980). The body lipids
and blood proteins change quantitatively and qualitatively. The decline in tissue
Fig. 5.1 Lipid concentration (g 100 g−1 somatic wet mass ± standard deviation) of parr and smolts of
(a) Atlantic salmon and (b) brown trout (Based on data from Jonsson and Jonsson (1998, 2003))
glycogen and fat is due not only to increased breakdown, but also to a reduced
synthesis (Hoar 1988). Also, somatic energy density decreases, and the water content
increases during smolting, probably because of energy demanding, physiological
changes concurrently with decreased external feeding. For instance, Atlantic salmon
smolts in the River Imsa exhibited 25% lower energy density than similar aged parr,
as a result of the lower lipid concentration (Jonsson and Jonsson 2003; Fig. 5.1).
In 1-year-old smolts, lipid concentration was 3.8 g 100 g wet mass−1. Lipid density
was twice as high (7.9 g wet mass−1) in corresponding parr. The energy density of
brown trout smolts was found to be lower than that of corresponding Atlantic salmon
smolts (Jonsson and Jonsson 1998, 2005), probably because of their shorter sea
sojourn and therefore lower energy needs (see Chap. 3). The changed metabolic
processes are modulated by numerous, integrated, endocrine changes involving at
least three different hormone axes, the growth hormone, thyroid hormone and
corticosteroid hormone axes.
5.2.2.3 Ionoregulation
In fresh water the body of teleosts has a higher ionic strength than the surroun
ding water, and the fish are faced with the loss of ions by diffusion and the gain
of water by osmosis. The converse is the case in seawater, where the fish must
conserve water in the cells and exclude salt. During smolting, the fish increase
their hypo-osmoregulatory ability relative to pre-migratory and non-migratory

conspecifics. This physiological change is associated with biochemical and
morphological changes in the gills and intestines, and increased expression of Na+/
K+-adenosine triphosphatase (ATPase) in chloride cells in the gills (Wedemeyer
et al. 1980; Hoar 1988; Franklin et al. 1992a; Uchida et al. 1996; Dickhoff et al.
1997; Ura et al. 1997). But, there is no direct relationship between the downstream
movement of the smolts and the gill Na+/K+-ATPase activity. Na+/K+-ATPase activity
increases in advance of the migration, and then, declines while the migratory urge
is increasing (Spencer et al. 2010).
The chloride cells, which are rich in mitochondria and have basolateral membranes
endowed with Na+/K+-ATPase molecules, develop during the smolt transformation
immediately prior to the seaward migration. The transport of sodium and chloride out
of the cells is driven by sodium and potassium gradients generated by Na+/K+-ATPase
with the help of the Na+ K+2Cl− cotransporter (Karnaky 1986; Boeuf 1993; Tipsmark
et al. 2002). The cotransporter is a protein that aids this transport into and out of
cells. Differences in expression of transport proteins signify differences in salinity
tolerance, but the Na+/K+-ATPase activity is an even better signifier of the ionoregu-
latory capacity of the fish (Bisbal and Specker 1991; Franklin et al. 1992b; Seidelin
et al. 1999; Mackie et al. 2007). Measurements of increasing gill Na+/K+-ATPase
can be used to predict smolting in individual fish before morphological changes are
obvious (Nielsen et al. 2004). This holds both for Atlantic salmon and brown trout.
For instance, experiments with the latter species have exhibited positive correlation
between gill Na+/K+-ATPase activity and the tendency to migrate downstream
towards the sea (Aarestrup et al. 2000).
Gill Na+/K+-ATPase occurs in several forms (Richards et al. 2003). One of these
forms, gill Na+/K+-ATPase a1a, shows high activity in fresh water, but become
nearly undetectable when the fish is in seawater. The isoform Na+/K+-ATPase a1b
is only present in small amounts in freshwater, but increases more than ten times
after seawater acclimation (McCormick et al. 2009). The different isoforms are
located in distinct chloride cells of the gills, and the different types are activated
depending on whether the fish are in fresh or salt water.
5.2.2.4 Hormonal Control
During smolting, there are increases in circulating levels of thyroxin, cortisol,

growth hormone, insulin-like growth factor I and insulin. All these hormones have
positive effects on smolt development (Hoar 1988; Dickhoff et al. 1997). For
instance, growth hormone, insulin-like growth factor I and cortisol (Franklin et al.
1992b; McCormick et al. 2000, 2002; Ágústsson et al. 2001; Pelis and McCormick
2001) stimulate the preparatory development of seawater tolerance in iono
regulatory tissues, through chloride cell proliferation and differentiation in the
gills (Nilsen et al. 2008). These hormones are also involved in the production of gill
Na+/K+-ATPase and the Na+ K+2Cl− cotransporter, allowing smolts to move rapidly
from fresh to salt water with minimum osmotic disturbance.
Growth hormone and cortisol are involved in controlling the capacity for
ionoregulation. Recent experiments by Ojima and Iwata (2010) indicated that the
growth hormone-releasing hormone and the cortico-releasing hormone also stimu-
late downstream smolt movements in rivers as well as increasing thyroxin (T4)
plasma levels. Plasma prolactin increases early during smolting and declines at the
peak (Prunet et al. 1989; Young 1988). This hormone inhibits the development of
salinity tolerance (Madsen and Bern 1992). Seawater preference of post-smolts
may be also influenced by a decreased prolactin concentration (Høgåsen 1998).
The thyroid hormones influence several behavioural changes during smolting
(Iwata 1995; Hutchison and Iwata 1998; Munakata et al. 2007). For instance,
studies show that thyroxin-treated pre-smolts of masu salmon are less aggressive
than untreated ones. Before the migratory period, juvenile chum salmon and coho
salmon yearlings prefer shaded more than open areas. However, thyroxin treatment
induced a preference for open areas. During the pre-migratory season, juvenile chum
salmon swam against the current, but thyroid hormone (T3) treatment changed their
swimming direction to downstream (with the flow of the current). Under-yearling
coho salmon showed greater preferences for seawater or undirected searching
behaviour after treatment with growth hormone, thyroid hormones (T3 and T4) and
cortisol.
5.2.2.5 Desmolting
Smolts sometimes remain in fresh water past their normal time of seawater migra-
tion. Such fish usually show signs of desmolting (Wedemeyer et al. 1980) [but some
stocks may be unable to readapt to fresh water (Boeuf 1993)]. The fish lose their
silvery coloration and exhibit reduced gill Na+/K+-ATPase activity. High water
temperature during the smolt migration may also result in loss of physiological
smolt characteristic (McCormick et al. 1999). Their experiment with wild Atlantic
salmon smolts showed that reduced gill Na+/K+-ATPase activity occurred earlier in
warm years, and was directly related to number of degree-days during spring. They
observed reduced gill Na+/K+-ATPase activity at the end of the migration period in
warm, southern rivers (Connecticut River and Penobscot River, Maine), but not in
colder northern rivers (Catamaran Brook, New Brunswick and Conne River,
Newfoundland). Both hatchery-reared and stream-reared fish, held in the labora-
tory, exhibited a more rapid loss of physiological smolt characteristics when kept
at higher temperature. Thus, delays in migration, such as those that occur at dams,
may have negative impacts on smolt survival in relatively warm rivers.
During desmolting, the tissue composition changes back towards that of parr.
Li and Yamada (1992) investigated the body composition of desmolted masu salmon,
and found that the lipid contents of muscle, liver, gut and gills of desmolts increased
compared to smolts. Furthermore, an increased proportion of triacylglycerol and
reduced proportion of phospholipids were found. Desmolting is often related to
sexual maturation, particularly in males, which have a lower size and growth threshold
for attaining maturity than females (Jonsson 1989; Fängstam et al. 1993).
How soon after smolting will smolts desmolt? Stefansson et al. (1998) found that
Atlantic salmon desmolted approximately 1 month after smolting, when maintained
at 10°C, 12°C and 14°C. Within these temperatures, the thermal exposure experi-
enced by the fish had little influence on the time to desmolting. Perhaps, desmolting
is largely influenced by photoperiod in addition to the ionic content of the water
(Soivio et al. 1988). All groups maintained good hypo-osmoregulatory ability despite
of a reduction in gill Na+/K+-ATPase activity in freshwater. Stefansson et al. (1998)
maintained that desmolting in Atlantic salmon is not a synchronised process, as
is normally observed during smolting, nor is it a parr reversion as seen among
some Pacific salmonids, at least not within the time frame of their study. According
to Mortensen and Damsgård (1998), desmolting in Atlantic salmon occurs below
15‰ salt, but the salinity threshold may be lower than this for Baltic populations
of Atlantic salmon.
Desmolts can resmolt in the subsequent year, as experimentally demonstrated for
Atlantic salmon (Eriksson 1984; Shrimpton et al. 2000). Apparently, the smolting
process proceeds faster and to a greater extent for every year it occurs (Wedemeyer
et al. 1980). Together with a more favourable surface to volume relationship of large
fish and greater ability to sustain cold seawater (Finstad et al. 1988), this might
contribute to the explanation of why larger anadromous salmonids spending the
winter in fresh water move to sea earlier in spring than younger and smaller Atlantic
salmon and brown trout (Jonsson 1985; Jonsson et al. 1990).
All in all, this shows that smolting is a recurring process occurring in spring,
prior to seaward migration, which helps the fish to survive in marine habitats.
5.2.3 Controlling Factors
Smolting happens in response to environmental cues such as photoperiod and

temperature (McCormick et al. 1998). Photoperiod is an important controller
indicating time of the year, whereas temperature appears important for the rate of
change (Zydlewski et al. 2005).
5.2.3.1 Size
Parr need to exceed a minimum size to be able to smolt. For instance, Nordgarden
et al. (2007) found a growth-hormone response indicative of smolting in Atlantic
salmon parr longer than 8 cm in length. They hypothesized that the development
of a functional light-brain-pituitary axis leading to an increase in plasma growth-
hormone levels sets the threshold developmental stage for successful smolting in
Atlantic salmon. However, minimum smolt-size varies to some extent among
populations of the same species, and in another experiment McCormick et al.
(2007) found that parr of the same age, shorter than 11 cm in January, and kept at
normal day length, did not smolt in the subsequent spring. Those larger than 12 cm
in January showed increased levels of growth hormone and cortisol in late spring
and large increases in gill Na+/K+-ATPase activity, signifying smolting. This diffe
rence in development can be directly linked to the difference in responsiveness to
photoperiod between large and small juveniles. When exposed to an advanced
photoperiod in February, large juveniles showed increased levels of plasma growth
hormone after 1 week, and increased levels of plasma cortisol after 3 weeks, and
these increases were followed by an advanced development of gill Na+/K+-ATPase
activity. In contrast, plasma growth hormone and cortisol in small juveniles were
not responsive to increased day length in February.
The relationship between smolting and size, however, is also influenced the age
of the fish, i.e. smolting is growth dependent as explained in Sect. 5.4.2.
5.2.3.2 Photoperiod
Smolting is controlled by an endogenous rhythm, itself controlled by the nervous

and endocrine systems, and is synchronized by external factors such as photoperiod
and temperature (Folmar and Dickhoff 1980; Wedemeyer et al. 1980; Hoar 1988;
Duston and Saunders 1990). Among these, photoperiod is the primary stimulus
initiating smolting. Day length is a timer, and increasing and decreasing photo
periods are major predictive, proximate factors indicating the season, as shown for
steelhead trout by Wagner (1974). The mechanism for the increase in sensitivity of
growth hormone and cortisol to day length has not been established (McCormick
2009), but one possible pathway is an increase in retinal innervation of the hypo-
thalamus in larger juvenile Atlantic salmon in early spring (Ebbesson et al. 2002).
The role of photoperiod on Atlantic salmon smolting was studied by Saunders
and Henderson (1970). They compared fish held under (a) constant day length
of 13 h light, (b) simulated natural photoperiod (increasing day length in spring),
and (c) reciprocal of natural photoperiod (decreasing day length from March and
increasing day length from June). The young salmon held under constant and
natural photoperiods exhibited no departure from the normal sequence in smolting.
The reciprocal photoperiod affected both growth and the excitability of the fish,
indicating a disturbed endocrine physiology. In contrast to the natural sequence in
smolting, fish reared under the reciprocal condition developed a high condition
factor in fresh water. Furthermore, they were less sensitive to external stimuli, than
those tested under natural or constant photoperiod. No differences between natural
and reciprocal photoperiods were noted in the degree of silvering, histology of the
thyroid gland, and plasma osmotic and chloride levels.
McCormick et al. (1987) demonstrated that continuous light from first feeding
and maintained throughout the rearing period of Atlantic salmon parr, inhibited the
ionoregulatory changes associated with parr-smolt transformation, whereas increasing
day length during winter-spring stimulated the transformation. Olsen et al. (1993)
reared yearling pre-smolts of Atlantic salmon under two different photoperiod
regimes; simulated natural photoperiod and continuous light and identical ambient
temperature conditions, from late November to late May. Gill Na+, K+-ATPase activity
increased under both photoperiod regimes from early April. But, the initial increase
and final levels in enzyme-activity were much lower in fish reared under the
continuous light regime. Fish reared under natural photoperiod exhibited lower
plasma-chloride levels in early May, which indicates better hypo-osmoregulatory
ability. Resting plasma-cortisol levels increased from March under both regimes,
but the increase was much greater in natural photoperiod regime fish.
Saunders and Henderson (1978) compared gill ATPase activity, body lipids
and moisture in fish held under different photoperiods. Under both natural and
reciprocal photoperiods, gill ATPase increased markedly during the later winter and
spring, while the levels of total body lipids declined and moisture increased. These
changes occurred earlier and were more marked in fish reared under reciprocal
photoperiod, indicating that the long nights of winter trigger pre-adaptations for the
smolt-phase of Atlantic salmon parr. Salinity resistance increases in a comparable
manner under all photoperiod regimes (Eriksson and Lundqvist 1982).
Photoperiod thus synchronizes the seasonally changing physiological processes
of smolting. In hatcheries, advanced photoperiod regimes can be used to advance
the timing of the physiological changes. The length of the photoperiod is con-
veyed through the light-brain-pituitary axis that encompasses the neural pathway
between the photoreceptor organ, brain and pituitary gland (hypophysis). The diurnal
rhythm is registered through melatonin secretion by the photosensory pineal organ
during the scotophase (Komourdjian et al. 1976), as the melatonin profile of salmo-
nids accurately reflects the dark phase throughout the annual cycle. The importance
of melatonin for smolting was demonstrated by Porter et al. (1998). They showed
that 1-year-old Atlantic salmon parr that received a melatonin implant, altered their
growth rate, seawater adaptation and seasonal time of smolting. Melatonin-feeding
of parr mimicked the effects of short photoperiod, as reported by Iigo et al. (2005)
for masu salmon. It delayed, but did not suppress, smolting. Their results indicate
that day length is transduced into changes in the duration of nocturnal elevation in
plasma melatonin levels, and that artificial modification of the plasma melatonin
pattern delays the physiological processes of smolting, induced by long-day photo-
periodic treatment.
Although the annual photoperiod cycle seems to be the primary ‘zeitgeber’ in
smolting, smolt migration is strongly dependent on water temperature. In general,
photoperiod controls the onset of the different aspects of smolting, and water
temperature is primarily a rate-controlling factor (Hoar 1988).
5.2.3.3 Temperature
Water temperature is responsible for annual variation in the time of smolting.

Temperature affects the time of the beginning of smolting and the rate of develop-
ment (McCormick et al. 2002). Low water temperature, such as 2°C, limits the
response of Atlantic salmon parr to increased day length (McCormick et al. 2000).
5.3 Behavioural Change 221
Furthermore, since day length is similar on the same date and place every year,
photoperiod does not cause annual population variation in smolting time.
McCormick et al. (2000) examined the interaction of photoperiod and tempera-
ture in regulating the parr-smolt transformation and its endocrine control. Atlantic
salmon juveniles were reared at a constant temperature of 10°C or ambient tempe
rature (2° from January to April followed by seasonal increase) under simulated
natural day length. The results provided evidence that low temperature limits the
physiological response to increased day length and that plasma growth hormones,
insulin-like growth factor I, cortisol and thyroid hormones mediate the environmental
control of the parr-smolt transformation. In a subsequent experiment where Atlantic
salmon smolts were reared under simulated conditions of normal photoperiod
or short days (LD 9:15) and ambient temperature (normal temperature increase
in April) or an advanced temperature cycle (temperature increase in February),
McCormick et al. (2002) concluded that temperature does not provide support for
the role as a zeitgeber, but that temperature has a role in the timing of smolting by
affecting the rate of development and interacting with the photoperiod.
There is a strong relationship between the cumulative temperature experience by
fish (degree-days) and smolt development (Sigholt et al. 1998). As with many other
physiological processes, temperature controls the rate of development. To smolt
successfully, the fish need a certain amount of thermal exposure, which can be
measured as number of degree-days [number of days × mean temperature (°C)].
Zydlewski et al. (2005) showed that the temperature experienced over time
determines the behavioural and physiological changes associated with smolting, as
well as the onset and termination of the smolt migration in Atlantic salmon. Smolt
migration starts earlier and takes place over a shorter period in mild compared
to cold years. For instance, Atlantic salmon reared at 12°C exhibited maximum gill
NA+/K+-ATPase activity, an indicator of the time of smolting, in late April com-
pared with late May in a comparable group reared at 8.9°C (Handeland et al. 2004).
Similarly, temperature is found to influence time of smolting in other salmonids
such as Chinook salmon (Negus 2003), steelhead trout (Wagner 1974), Arctic charr
(Jørgensen and Arnesen 2002) and others (Hoar 1988). Increased temperature results
in earlier smolt development. This is suggested by a number of studies (e.g. Adams
et al. 1973; Johnston and Saunders 1981; Solbakken et al. 1994). However, this
general correlation does not hold for temperatures above 15°C. At such high
temperatures smolting is inhibited.
5.3 Behavioural Change
While parr are territorial and can form dominance hierarchies, do smolts migrate in
small schools to the ocean. Instead of facing upstream and holding their positions
against the current, they rise from the bottom and move downstream with the
current, at least during a part of the day. At the same time the smolting process
changes the water quality preference of the fish.
5.3.1 Gathering in Schools
While parr are chiefly epibenhtic and territorial, the smolts become restless, reduce
feeding, eliminate territoriality, decrease aggressiveness, and move away from the
bottom and up into the higher strata of the water column (Hoar 1988). Smolts in
lakes gather in schools and move around in near surface water in an exploratory
manner, before eventually heading for the outlet and swimming downstream with
the current. This searching behaviour may be specific for populations adapted to
pass through lakes on their way downstream. Stream-living populations may have
difficulty in locating the outlet when the current velocity is low, and smolts can be
delayed if transplanted from a river to a lake (Thorpe et al. 1981; Hansen and
Jonsson 1985). Findings of Aarestrup et al. (1999) indicated that there are inherited
differences among populations in their ability pass through lakes, and locate lake
outlets on their way downstream.
5.3.2 Downstream Movement
Smolts move controlled with the current downstream rivers, they move actively
out of sloughs and backwaters into the water current and are transported down-
stream. Part of the way they are transported head first with the water current. In
rapids they can turn and swim against the current, but slower than the water
velocity. Often, they only move a few hundred meters at the time before holding.
When approaching small waterfalls, they can swim several times to where the
rapid begins before letting go, as if they are testing the strength of the current.
Some descend tail first, others head first. When releasing smolts at about 1 km
above the trap in the River Imsa, the fastest group of smolts moved downstream
with a speed of between one-third and one-fourth of the current velocity in near-
surface water, tested by simultaneously releasing a cage of oranges in the river
(Hansen and Jonsson 1985). Factors influencing the downstream smolt migration
are given in Chap. 6.
How is the social structure in smolt schools? Olsén et al. (2004) tested the
hypothesis that Atlantic salmon smolt siblings migrate closer in time to each
other, than do unrelated fish during downstream migration, leading to aggrega-
tion and shoal formation with kin. Atlantic salmon embryos from three families
were reared in two tanks to create familiar and unfamiliar sibling smolts. Of the
juveniles monitored by the PIT antenna, 85% showed downstream migration at
night hours, and siblings migrated significantly closer in time than to unrelated
fish. This result suggests that there is a genetic component in the migratory
behaviour of smolts, and supports the hypothesis that smolts migrate in kin-
structured groups.
5.3 Behavioural Change 223
5.3.3 Time of Day
At low water temperature the smolts move downstream at night, and moon or
artificial light shining directly on the river can decrease the downstream movement
of the fish (Hansen and Jonsson 1985). In the River Imsa, most of the smolt activity
lasts for 5–7 h from 8–9 p.m. to 1–3 a.m., or less than 30% of the day. However, the
smolts gradually become more day-active as water temperature increases, and they
are chiefly day-active at temperatures above ca. 13°C (Thorpe et al. 1994). Also, the
downstream migration speed increases from early to late migrating fish, prossibly
as a consequence of higher water temperature.
One of the best studies on the diurnal activity of Atlantic salmon smolts is from
the River Frome, England (Fig. 5.2). There, the smolts moved to sea in the evening
and at night early in the migration period. Later they became increasingly more
diurnal until rates became approximately equal at day and night. Migration patterns
were related to water temperature, such that when mean daily temperatures were
below 12°C, hourly rates of migration were significantly lower during the day than
at night. When mean daily temperatures exceeded 12°C, there was no significant
difference between diurnal and nocturnal migration rates. Migration patterns showed
a distinct suppression of migration at dawn and dusk throughout the migration
period. They hypothesised that this behaviour is an active decision and/or an adap-
tive strategy, either to take advantage of increased food in the form of invertebrate
drift, or to reduce predation risk from actively feeding piscivores, or both.
5.3.4 Seawater Preference
Salinity preference changes with the size and physiological state of the fish. The
resistance to, and preference for, saltwater increase as salmonids grow, due to
increased mass relative to the size of the surface area (McInerney 1964; Hoar
1988). For Atlantic salmon this was demonstrated by Huntsman and Hoar (1939).
More recently, Finstad and Ugedal (1998) demonstrated that the same holds for
anadromous brown trout. Furthermore, experiments with coho salmon showed that
in midsummer, juveniles in a salt gradient exhibited a bimodal response. Zones of
preference corresponded to fresh water and to a salinity of 4–5 psu (Otto and
McInerney 1970). As the time of smolting approached, the fish lost their preference
for fresh water, and the preferred salinity increased to 6–7 psu. Concurrently, their
tolerance for seawater increased (Otto 1971).
Davidsen et al. (2009) monitored the migratory behaviour of Atlantic salmon
during the first phase of the marine migration from the River Eio, Norway. There
was no overall preference for a specific salinity concentration, but post-smolts
migrated to a large extent in brackish water (<20 psu) during the first day of sea
migration. The fish swam in the warmest depth layer, and possibly water temperature
Fig. 5.2 Hourly migration of Atlantic salmon smolts in the River Frome for 8 years combined
data for each of four 2-week periods during April and May (arrows represents sunrise and sunsets)
(From Ibbotson et al. (2006). Reproduced with permission of Wiley-Blackwell)
5.4 Ecological Characters 225
was more important than salinity for their habitat choice. In nature, the fish has to
integrate a number of environmental cues, and often habitat choice is determined
by several variables in concert, possibly to decrease discomfort.
5.4 Ecological Characters
Time at smolting is influenced by the age, size and growth rate of the fish. However,
the relationship between these variables is not constant, but varies among popu-
lations in association with differences in their habitat. This seems partly due to
genetic differences among populations, partly to be a response to environmental
conditions encountered by the fish. The tendency to smolt varies between sexes,
and there appears to be a physiological link between hormones influencing smolting
and maturation.
5.4.1 Smolt Age
Wild Atlantic salmon usually smolt at ages between 1 and 8 years, with population
means from less than 2 years to more than 4 years (Power 1969; Kuzmin and
Smirnov 1982; Jensen and Johnsen 1986; Metcalfe and Thorpe 1990; Metcalfe
et al. 1990; Englund et al. 1999). The variation in smolt-age among rivers is only
slightly greater than the within river variation in the largest Atlantic salmon rivers
such as the River Tana (~70°N) along the border between northern Norway and
Finland. There, smolt ages vary between 2 and 7 years with a mean age of more
than 4 years (Englund et al. 1999).
In brown trout smolt age varies between 1 and 9 years, with mean smolt ages
among rivers from less than 2 to almost 5 years (L’Abée-Lund et al. 1989; Jonsson
and L’Abée-Lund 1993; Jonsson et al. 2001). The most common smolt ages are 2
and 3 years over large parts of the distribution area, and typically 2–4 year classes
undertake the smolt migration each year, although greater variation is sometimes
observed (Jonsson 1985; L’Abée-Lund et al. 1989). Pre-smolt brown trout can enter
brackish water even during the first summer (0+), as observed in the Baltic Sea
(Titus and Mosegaard 1989, 1992; Järvi et al. 1996; Landergren 2001). However,
their seawater survival may be poor if the salinity exceeds 6–7 psu (Landergren and
Vallin 1998).
Smolt age increases with latitude (Dahl 1910; Allen 1941; Jones 1959; Symons
1979; Power 1981). L’Abée-Lund et al. (1989) reviewed the clinal variation in
smolt age of anadromous brown trout from 34 Norwegian rivers at latitudes
between 58° and 70° N (Fig. 5.3a), and the analysis was extended to 102 European
rivers by Jonsson and L’Abée-Lund (1993) (Fig. 5.4a). L’Abée-Lund et al. (1989)
also reported that smolt age correlated negatively with increasing water temperature
in both fresh (Fig. 5.3b), and marine waters (Fig. 5.3c) as well as with the length of
the growth season (Fig. 5.3d).
Fig. 5.4 Relationships between latitude (L °N) and (a) smolt age (A years) (Regression line:
A = −5.94 + 0.15 L; r2 = 0.694, P < 0.001); (b) smolt size (cm) in European rivers 54°N–70°N (From
Jonsson and L’Abée-Lund (1993). Reproduced with permission of Wiley-Blackwell)
In Atlantic salmon, however, the relationship between smolt age and latitude is
weaker than in European brown trout. Metcalfe and Thorpe (1990) tested data from
182 populations over a 40° latitudinal range in both Europe and North America, and
found that only 6% of the total variance in smolt age was explained by latitude, and
more independent variables had to be included to explain a larger part of the variance.
Earlier, Symons (1979) had shown that the length of the growth season influenced
smolt age. He used number of days per year warmer than 7°C as a proxy for the
length of the growing season. A reason for choosing 7°C is that growth rate during
summer commences at a water temperature of 6–7°C (Fig. 4.7; see also Saunders
and Henderson 1969; Elliott and Hurley 1997; Jonsson et al. 2001). Furthermore,
at any given temperature, food intake and turnover rates are higher at increasing
than decreasing day lengths (Higgins and Talbot 1985). Thus, by constructing an
index of growth opportunity including both temperature and photoperiod records,
Metcalfe and Thorpe (1990) could report that as much as 82% of the variance in
smolt age of North American and European Atlantic salmon was explain by this
new variable. Thus, other environmental factors than those represented by latitude,
Fig. 5.3 Relationships between mean smolt age (A years) and (a) latitude (L°N) (Regression line:
A = 0.195 L – 8.950, r2 = 0.686); (b) sea temperature (t degree-days) within the growth season
(Regression line: A = 5.561 – 0.00148 t, r2 = 0.606); (c) river temperature (t degree-days) within the
growth season (Regression line: A = 5.289 – 0.00114 t, r2 = 0.447); (d) length of the growth season
(number of days D exceeding 4°C) (Regression line: A = 5.637 – 0.0131D, r2 = 0.387); (e) passable
river length (RL km) (Regression line: A = 3.222 + 0.00298RL, r2 = 0.209); (f) yearly mean water dis-
charge (m3 s−1) (P > 0.05); and relationship between mean smolt size (S mm) and (g) latitude (L°N)
(Regression line: S = 3.812 L – 79.815, r2 = 0.394); (h) sea temperature (t degree-days) within the
growth season (Regression line: S = 202.586 – 0.0275 t, r2 = 0.328); (i) river temperature (t degree-
days) within growth season (P>0.05); (j) length of growth season (number of days >4°C) (P>0.05);
(k) passable river length (RL km) (Regression line: S = 156.729 + 0.0873RL, r2 = 0.269); (l) yearly mean
water discharge (Q m3 s−1) (Regression line: S = 154.724 + 0.1497Q, r2 = 0.152). All regression lines are
significant (P < 0.05) (From L’Abée-Lund et al. (1989). Reproduced with permission of JStor)
appeared to govern the smolt age of Atlantic salmon over such a large geographical
area. A similar approach did not improve the smolt-age prediction for European
brown trout over that of latitude alone (Jonsson and L’Abée-Lund 1993). A climatic
difference between North America and West Europe is probably the main reason
why the index of growth opportunity fitted the Atlantic salmon data better than
those of European brown trout.
Within rivers, there are annual differences in smolt age. Climatic conditions
encountered during embryonic development influence the subsequent growth rate
and thereby smolt age. Correlation studies in the River Imsa indicated that
the warmer and wetter the winter before hatching, the better the offspring grew in the
subsequent first year of life, and the higher the proportion of the cohort smolted as
1-year-olds (Jonsson et al. 2005). Strothotte et al. (2005) reported a similar associa-
tion between first year’s growth and smolt age in Canadian Atlantic salmon. Owing
to high water temperature during embryonic development, the embryos hatch early,
extending the first growth season, as e.g. found in brown trout (Elliott et al. 2000).
Furthermore, feeding opportunities may be good after mild, wet winters with high
flow and large water-covered areas. Thus, the parr may become large at the end of
the first growth season resulting in relatively more 1-year-old smolts.
5.4.2 Size and Growth
The decision to undergo smolting and migration to the sea is associated with fish
size and growth trajectories. Elson (1957) assumed that Atlantic salmon had to
reach a minimum length of 10 cm in the preceding autumn to smolt in the subse-
quent spring. Fahy (1985) also maintained that parr smolted as quickly as possible
after having passed this threshold length. This rule of thumb has been shown useful
for hatchery managers, but is too simple when applied to wild populations (Økland
et al. 1993). The main reason is that wild fish are often more variable in size than
hatchery fish, and typically, they smolt over a longer size and age span than those
from hatcheries. Fast-growing parr tend to smolt younger and smaller than slower-
growing parr (Jonsson 1985). This holds for brown trout, and often also for Atlantic
salmon, although results vary among rivers (Figs. 5.5 and 5.6) Very fast-growing
parr can smolt before reaching 10 cm, whereas slow-growing parr can pass 10 cm
more than a year before they smolt. This illustrates that growth rate also influences
smolt size. Based on this, Økland et al. (1993) hypothesized a functional relationship
between growth rate and smolt size of Atlantic salmon and brown trout where fitness
is maximized (Fig. 5.7).
Populations that consist of fast-growing parr often have large smolts (Jonsson and
L’Abée-Lund 1993). Furthermore, there is tendency for smolt size to increase with
increasing latitude and decreasing water temperature in the sea entered by the smolts
(L’Abée-Lund et al. 1989). This among population regression holds for limited geo-
graphical areas such as the Norwegian coastline (58–71°N) (Fig. 5.3e), but not for
much larger regions such as Norway, the British Isles and the Baltic Sea area
(Fig. 5.4b). The reason may be that the ocean is not uniformly warmer from the British
Isles to Norway, and the Atlantic Ocean has higher salinity than the Baltic Sea.
Fig. 5.5 Annual body length increment (mm) of Atlantic salmon parr grouped according to smolt
age (years). The end of the lines gives mean age and length at smolting. The horizontal dotted line
gives the mean length of the shortest smolt age group in the Norwegian rivers (a) Beiarelva, (b)
Saltdalselva, (c) Lærdalselva and (d) Sandvikselva (From Økland et al. (1993). Reproduced with
permission of Wiley-Blackwell)
Among rivers, mean smolt sizes of Atlantic salmon populations vary from about
12 cm to 22 cm (Power 1969; Jensen and Johnsen 1986). Individual fish, however,
can vary from ca. 8 cm to more than 30 cm (Jonsson et al. 1998a). In brown trout,
population means in smolt size are between 7 and 25 cm (Jonsson 1985; Jonsson and
L’Abée-Lund 1993; Jonsson et al. 2001), and the within-population variation is typi-
cally greater than that of Atlantic salmon. When these two species occur in the same
river, smolts of Atlantic salmon are usually smaller than those of brown trout. For
instance, in the River Imsa, most Atlantic salmon smolts weigh between 30 and 60 g,
while brown trout smolts are approximately twice this heavy (Jonsson and Jonsson
2009). The size difference may be associated with the fact that Atlantic salmon has
better ionoregulatory capacity in seawater than brown trout (Hoar 1988). In addition,
pre-smolts of brown trout can enter brackish water early in life. For instance, in the
Baltic Sea, brown trout not longer than 30 mm (0.3 g wet mass) have been observed
Fig. 5.6 Annual body length increment (mm) of anadromous brown trout parr grouped according
to smolt age (years). The end of the lines gives mean age and length at smolting. The horizontal
dotted line gives the mean length of the shortest smolt age group in the Norwegian rivers (a)
Beiarelva, (b) Saltdalselva, (c) Lærdalselva and (d) Sandvikselva (From Økland et al. (1993).
Reproduced with permission of Wiley-Blackwell)
entering brackish water from the small stream Arån on the Swedish island, Gotland.
The brown trout emigrated in summer, from about 3 months after hatching
(Landergren 2001). Brown trout may even spawn in brackish water and leave viable
offspring in areas with salinity below 4 psu (Landergren and Vallin 1998; Limburg
et al. 2001). We know of no similar observation from Atlantic salmon.
Some of the smallest Atlantic salmon smolts have been found in cold, glacier-fed
rivers where the fish are slow-growing, and they enter relatively warm seawater with
good growth opportunities (Jensen and Johnsen 1985, 1986). The largest Atlantic
salmon smolts, on the other hand, occur in high latitudes rivers such as the Koksoak
River, where the smolts enter the very cold Ungava Bay, Canada (Power 1958, 1969;
Dempson et al. 2010). There, they migrate into extremely cold seawater, only warm
enough for Atlantic salmon to survive during a few weeks in the summer.
Fig. 5.7 A hypothetical cost/benefit model of smolting at different sizes. It is assumed that the
net benefit of smolting decreases with increasing distance to an optimal smolt size. Smolting when
body size is too small increases post-smolt mortality, smolting when too old and large results in
decreased post-smolt growth and higher accumulated mortality before smolting. Fast-growing
parr are probably constrained earlier by limited food resources in the river due to their higher
metabolic requirements, and therefore have a smaller optimal smolt size than slower-growing parr
(From Økland et al. (1993). Reproduced with permission of Wiley-Blackwell)
Also in brown trout, the largest smolts are reported from rivers as far north such
as the sub-Arctic River Tana. Those that enter a cold sea area are larger than those
migrating into a warmer sea (Fig. 5.3h). There is no similar significant correlation
between smolt size and river temperature or the length of the growth season
(Fig. 5.3i, j). Large smolt size in populations that migrate into particularly cold
seawater probably reflects that ionoregulation in cold seawater is energetically
expensive for the fish.
Growth opportunities and temperature at sea are both important factors influen
cing smolt size. Inter-population variation in smolt size appears both to reflect a
phenotypic plasticity response to variation in growth rate (Jonsson 1985), and
inherited among population variation adapted to local growth and survival oppor
tunities (cf. Refstie et al. 1977).
5.4.3 Habitat Constraints
In small streams, mean smolt size and age (the two are significantly correlated) of
brown trout increase with increasing mean annual water discharge, but the trend
levels off at mean annual water flows of approximately 0.1 m3 s−1 (Fig. 5.8)
(Jonsson et al. 2001). Furthermore, the variation in smolt length (CV) correlates
negatively with mean annual water discharge of the streams. The greater heteroge-
neity in small streams may reflect more variable success of large smolts in these
Fig. 5.8 Relationships between mean annual water discharge of the nursery stream (Q m3 s−1) and
(a) mean smolt length (S mm) (Regression line: S = 180.9 – 3.87/Q, r2 = 0.633, P = 0.001); (b) coef-
ficient of variation in smolt length (CVs) (Regression line: ln CVs = −0.395 ln Q – 2.1, r2 = 0.61,
P = 0.001); (c) mean smolt age (A years) (Regression line: A = 2.54 – 0.0377/Q, r2 = 0.492,
P = 0.002); (d) coefficient of variation in smolt age (CVa) (Regression line: ln CVa = −0.23 ln Q – 1.736,
r2 = 0.46, P = 0.003) of anadromous brown trout from Norway (From Jonsson et al. (2001).
Reproduced with permission of Wiley-Blackwell)
streams. The small streams included in the study by Jonsson et al. (2001) some-
times dry out during summer, except for some scattered pools. To survive, the fish
often leave early. The significant correlation between smolt size and water flow is
weak for streams with mean annual water discharge above 1 m3 s−1 (Fig. 5.3m).
Large streams probably have enough water to sustain even large parr, reducing the
importance of flow variation for size at seaward migration. Thus, stream size can
restrict smolt size in small streams, whereas the effect is minute (if any) in large
streams and rivers.
In streams with mean annual water discharge above 1 m3 s−1, brown trout smolt
size correlates positively with river length, and the correlation is stronger than that
between water flow and smolt size (Fig. 5.3e). This may reflect a cost of migration
which increases with the distance from the sea. We know of no similar study for
Atlantic salmon.
5.4.4 Sex Ratio
Females are more abundant than males among downstream migrating smolts. This
is general for Atlantic salmon (Dahl 1910; Österdahl 1969; Jonsson et al. 1998a)
and brown trout (Jonsson 1985; Dellefors and Faremo 1988). Approximately 60%
females and 40% males are common among populations of anadromous brown
trout and Atlantic salmon, although some variation is observed (Jonsson and
Jonsson 1993). This is partly due to an inherited difference in life history tactics
between the sexes. Given the same growth rate, females have a higher tendency to
smolt than males, whereas males have a higher tendency to attain parr maturity. In
males, mortality can increase as a cost of reproduction, and the fish can re-mature
instead of smolting and migrating to sea (Hansen et al. 1989; Jonsson 1989). The
higher proportion of migratory females than males is partly because the mortality
of mature parr is higher than that of similar aged juveniles as a cost of reproduction,
partly because male parr can remature in the subsequent year instead of migrating
to sea. The latter is common in brown trout (Jonsson 1985; Dellefors and Faremo
1988), but can also occur in Atlantic salmon (Hansen et al. 1989). Thus, smolting
and sexual maturation can be alternative tactics in partly migratory populations.
5.4.5 Smolting Versus Sexual Maturation
Are smolting and sexual maturation competing processes? Landgrebe (1941)

concluded that there is a genetic basis for when Atlantic salmon smolt, and that
smolting and sexual maturation are not competing processes. Also, there is a large
literature demonstrating that in Atlantic salmon, mature parr often go through a
smolting process subsequent to maturation (e.g. Österdahl 1969; Hansen et al.
1989; Berglund et al. 1991). For instance, with some annual variation, about 50%
of the male smolts in the River Imsa are previously mature parr. This was demon-
strated by colour marking of mature and immature parr in the autumn and monitoring
of the downstream migration during the subsequent spring (Bohlin et al. 1986), and
by inspecting the gonads of every tenth smolt descending to sea in the Rive Imsa
since the early 1980s (Jonsson et al. 1998b). However, some mature parr re-mature,
and this seems influenced by the hormonal status of the fish. The fraction of mature
male parr that smolted was increased when the testes were stripped for spermatozoa
in the autumn (Hansen et al. 1989), and when they were kept in relatively warm
water over winter (>4°C) (Berglund et al. 1991), probably decreasing the level of
steroid hormones in the fish.
Do Atlantic salmon or brown trout attain maturity the same year as they smolt?
In Atlantic salmon post-smolts can mature the first autumn after smolting, but usually
smolted fish postpone maturation one or more years (Jonsson et al. 1993). Brown
trout, on the other hand, mature regularly in the first autumn subsequent to smolting
(Jonsson 1985; Jonsson et al. 2001). The ultimate reason for the species difference
is probably that the fitness advantage by feeding at sea and/or the cost of maturation
and returning to fresh water for spawning is higher in Atlantic salmon than brown
trout. For instance, the mass of Atlantic salmon increases about 30 times during the
first year at sea, from about 50 g to 1.5 kg. The corresponding figures for brown
trout staying at sea a similar length of time are approximately eight times, from
about 75 g to 600 g (Jonsson 1985; Jonsson et al. 1991, 2001). The increase in mass
reflects the increase in reproductive effort and success for the fish (Fleming et al.
1996; Wootton 1998). As parr in fresh water, brown trout grow faster than Atlantic
salmon. The relative difference in sea survival between Atlantic salmon and brown
trout is smaller than that in growth. In the River Imsa, where most Atlantic salmon
and brown trout return to the river after only 1 year at sea, sea survival of Atlantic
salmon was estimated at 8.9% between 1976 and 1994 (Jonsson et al. 1998b). The
corresponding figure for brown trout from 1976 to 2003 was 11.4% (Jonsson and
Jonsson 2009). For parr in fresh water, survival, if different, may be higher for
brown trout than Atlantic salmon due to higher growth rate and more sheltered
habitat use. Thus, the fitness advantage of feeding at sea (c.f. Eq. 7.1) is higher for
Atlantic salmon than brown trout, particularly thanks to the large difference in
growth rate at sea. Due to the longer sea migration in Atlantic salmon than brown
trout, the cost of returning to freshwater for spawning is also higher selecting
against an early maturation and return in this species.
Also, in other salmonids, such as Arctic charr and sockeye salmon, sexual matu-
ration in parr typically precludes subsequent smolting. As with brown trout, sexually
mature parr do not smolt, but become freshwater resident. In sockeye salmon, the
fastest growing individuals may smolt at the youngest age (Ricker 1938). Slower
growing individuals mature sexually as parr, whereas even slower-growing indi-
viduals smolt the year thereafter. A similar difference in growth between resident
and anadromous brown trout was reported for brown trout females from Vangsvatnet
Lake, Norway (Fig. 5.9). The fastest-growing fish should be able to acquire enough
resources to mature and spawn, but still they smolt and move to sea. Possibly, matu-
ration is postponed according to their genetic program because the expected life-
time fitness increases if they stay immature and go to sea. This observation is in
apparent contrast to Thorpe and co-worker’s (e.g. Thorpe 1994, 2007; Thorpe and
Metcalfe 1998; Thorpe et al. 1998) view that smolts are individuals that fail to reach
the required energy threshold for maturation while in freshwater. However, the rela-
tive lipid deposits of the migrants may be lower than that of residents as reported
for anadromous Arctic charr by Rikardsen et al. (2004). The fish deplete their lipid
deposits during smolting, and in this species, migrants also have lower energetic
density in the autumn than corresponding residents which attain maturity in the
subsequent summer and autumn. Thus, regulatory mechanisms for the energy allo-
cation for individuals choosing different life history patterns probably exists, but
are as yet poorly understood (Matty and Lone 1985; Post and Parkinson 2001;
Jonsson and Jonsson 2003; Claireaux and Lefrançois 2007).
Individuals from freshwater resident salmonid populations can show signs of
smolting in spring. For instance, Arctic charr from a freshwater resident popula-
tion in the River Imsa can move to sea in spring like regular smolts. However, none
(a)
20
15
10
5
Length increments
0
(b)
20
15
10
0
1 2 3 4
Age
Fig. 5.9 Estimated mean length increment (cm) of (a) female parr smolting at age-2 and ³3 years
(solid lines) and those attaining maturity at age ³3 years (broken line) and become freshwater
resident; (b) male parr smolting at ages 2, 3 and 4 years (solid lines) and those attaining maturity
at age 2 and ³3 years (broken lines) and becoming freshwater resident in Vangsvatnet Lake,
Norway (Based on data from Jonsson (1981))
of them returns to the river, but some have been captured in other rivers, which they
cannot reach without moving through full seawater (35‰ salt) (Jonsson et al. 1989).
This behaviour disperse freshwater resident fish among water courses. Kiiskinen
et al. (2002) showed that non-anadromous Atlantic salmon in Lake Saimaa, Finland,
go through a smolting process in the spring, similar to anadromous populations.
These fish attain maturity without having been to sea. This supports the view that
smolting in Atlantic salmon is a seasonal phenomenon independent of sexual matu-
ration. On the other hand, landlocked Atlantic salmon from other systems, such as
Lake Byglandsfjord, Norway, do not exhibit increased levels in the growth hormone
and cortisol axes similarly to anadromous salmon (Nilsen et al. 2008), illustrating
that in this trait, there are genetic differences among populations.
There are also genetic differences among conspecific populations in the tendency
to migrate (Jonsson 1982; Svärdson and Fagerström 1982). Probably the hormonal
status of parr in spring must exceed a minimum level for the fish to smolt and go
to sea. This level may be determined through natural selection, and the hormonal
level appears to depend on the age and size of the fish. Young fish show increased
gill Na+/K+-ATPase activity and cortisol each spring, and the process proceeds
faster and to a greater extent every year the young fish remain in fresh water
(Wedemeyer et al. 1980). As a consequence, large smolts migrate to sea earlier in
spring and in colder water than smaller smolts (Jonsson et al. 1990; Bohlin et al.
1993), in line with their improved ability of ionoregulation in cold seawater.
5.5 Is Smolt-Age Inherited?
There is heritability for age at smolting, as experimentally documented from both

Atlantic salmon and Chinook salmon (Refstie et al. 1977; Clarke et al. 1992, 1994).
However, the genes involved have not been identified (Ferguson 2006). Inheritance
studies also suggest that both timing of and propensity for smolting are under
genetic control. On the other hand, a change in gene expression does not mean that
the process of smolting is entirely under genetic control (Ferguson 2006). The fact
that juveniles leave the nursery area, when there are poor feeding opportunities or
hostile environmental conditions (Forseth et al. 1999; Juanes et al. 2004; Jonsson
and Jonsson 2009), illustrates that phenotypic plasticity may be also important for
the emigration from rivers.
In Chinook salmon, crosses between life-history variants have indicated that
smolting in the first year of life was dominant and probably controlled by few loci
(Clarke et al. 1992, 1994). These authors used body morphology and coloration to
discriminate between fish smolting at age 1 and 2 years. In sockeye salmon and
rainbow trout, crosses between resident and anadromous forms, also suggest that
there is a genetic basis for the propensity to undergo smolting (Foote et al. 1992).
In these species, hybrids were intermediate between freshwater and migratory forms
in their ability to hypo-osmoregulate in seawater, suggesting that the propensity for
smolting is under additive rather than dominant genetic control. This is further
supported by the observation that transplanted offspring of anadromous brown trout
retained their ability to smolt and migrate to sea when released among non-anadromous
conspecifics above an upstream passable waterfall, contrary to the non-anadromous
offspring that held their position in the river instead of migrating to sea when
released among migratory fish downstream of the waterfall (Jonsson 1982).
But, phenotypically plastic aspects of the trait are suggested by the observation
that releases of offspring of non-migratory brown trout have given rise to anadromous
populations where environmental conditions at sea are suitable (McDowall 1988).
On the other hand, the tendency to smolt and migration to sea can be retained in
populations even when migrants are unable to return to their river of origin for
spawning. Furthermore, it has been shown that non-anadromous populations can
5.6 Summary 237
bring about the physiological changes necessary to adjust to marine conditions after
having been in fresh water for more than 1,000 generations (Staurnes et al. 1992;
Jonsson et al. 1989; Kiiskinen et al. 2002), and offspring of non-anadromous popu-
lations of brown trout survive and grow equally well in the ocean as conspecific
offspring from anadromous populations (Jonsson et al. 1994a, b, 1995).
The fact that growth rate influences age and size at smolting signifies that there
are also environmental influences on the expression of the trait. However, it is
difficult to determine whether environment influences the gene expression, operates
through the neuroendocrine system, or whether it is an endogenous gene control by
other genes, or both. But the observation that different populations differ in ability
to survive in seawater lends support to the hypothesis that smolting is under genetic
control (Burton and Idler 1984; Nilsen et al. 2003). Thus, there is evidence for that
the tendency to smolt is inherited, but that the expression of the trait can be modified
by environmental influences.
5.6 Summary
1. The parr-smolt transformation (smolting) is characterized by changes in

morphology, physiology and behaviour. Smolts are silvery due to crystals of two
purines, guanine and hypoxanthine. Improved hypo-osmotic capacity is caused
by increased expression of Na+-K+adenosine triphosphatase (ATPase) in chloride
cells of the gills. Smolts lose the positive rheotaxis characteristics of parr.
2. Smolting is controlled by an endogenous rhythm, itself controlled by the nervous
and endocrine systems, and synchronized by external factors such as photoperiod
and temperature. Increasing and decreasing photoperiods are major predictive,
proximate factors indicating the season. Water temperature influences develop-
mental rate, and is responsible for variation in seasonal time of smolting.
3. Smolts are restless, exhibit reduced feeding, cease territoriality, exhibit decreased
aggressiveness and move away from the bottom and up into the higher strata of
the water column. Smolts move downstream in small schools. The migration is
active, but the smolts use the water current when moving downstream.
4. In European brown trout, latitude is a good predictor for smolt age, at least from
the British Isles to northernmost Norway. In Atlantic salmon, an index based on
temperature and photoperiod is a good predictor of smolt age.
5. Size at smolting depends on growth rate and age. Smolt length tends to increase
with increasing age and decreasing growth rate within and among populations of
brown trout and Atlantic salmon. Smolt size of brown trout increases along the
Norwegian coast, but this trend does not hold when populations from the British
Isles and Baltic region are included. Within populations, large fish smolt and
move to sea earlier in spring than smaller ones, probably because they are better
able to ionoregulate in cold seawater.
6. In streams with annual mean annual flow below 0.1 m3 s−1, smolt size of brown
trout increases with increasing water discharge. Parr can escape from small
streams into brackish water during drought or poor feeding conditions.
7. There is a larger proportion of female than male smolts in both brown trout and
Atlantic salmon due to an inherited difference in life history tactics between the
sexes. Many males attain maturity instead of smolting. In Atlantic salmon, but
not in brown trout, a large proportion of previously mature male parr can smolt
after having spawned.
8. There is an inherited tendency for the propensity to smolt, but the genes involved
are not identified. However, the smolting process is not entirely under genetic
control. Juveniles also exhibit phenotypic plasticity for the trait.
9. Smolts desmolt if retained in freshwater past their normal time of seawater
migration. They lose their silvery colour and exhibit reduced gill Na+, K+-ATPase
activity. Also, their tissue composition changes back towards that of parr. Desmol
ting is often related to sexual maturation, indicating a link between hormones
influencing de-smolting and sexual maturation.
References
Aarestrup K, Jepsen N, Rasmussen G et al (1999) Movements of two strains of radiotagged

Atlantic salmon (Salmo salar L.) smolts through a reservoir. Fish Manage Ecol 6:97–107
Aarestrup K, Nielsen C, Madsen SS (2000) Relationship between gill NA+, K + -ATPase activity
and downstream movement in domesticated and first generation offspring of wild anadromous
brown trout (Salmo trutta). Can J Fish Aquat Sci 57:2086–2095
Adams BL, Zaugg WS, McLain LR (1973) Temperature effect on parr-smolt transformation in
steelhead trout (Salmo gairdneri) as measured by gill sodium-potassium stimulated ATPase.
Comp Biochem Physiol 44A:1333–1339
Ágústsson T, Sundell K, Sakamoto T et al (2001) Growth hormone endocrinology of Atlantic
salmon (Salmo salar): pituitary gene expression, hormone storage, secretion and plasma levels
during parr-smolt transformation. J Endocrinol 170:167–234
Allen KR (1941) Studies on the biology of the early stages of the salmon (Salmo salar). III.
Growth in the Thurso River System, Caithness. J Anim Ecol 10:273–295
Allison WT, Haimberger TJ, Hawryshyn CW et al (2004) Visual pigment composition in
zebrafish: evidence for a rhodopsin-porphyropsin interchange system. Vis Neurosci
21:945–952
Allison WT, Dann SG, Veldhoen KM et al (2006) Degeneration and regeneration of ultraviolet
cone photoreceptors during development in rainbow trout. J Comp Neurol 499:702–715
Beeman JW, Rondorf DW, Tilson ME et al (1995) A nonlethal measure of smolt status of juvenile
steelhead based on body morphology. Trans Am Fish Soc 124:764–769
Berglund I, Hansen LP, Lundqvist H et al (1991) Effects of elevated winter temperature on seawater
adaptability, sexual rematuration and downstream migratory behaviour in mature male Atlantic
salmon parr (Salmo salar). Can J Fish Aquat Sci 48:1041–1047
Bisbal GA, Specker JL (1991) Cortisol stimulates hypoosmoregulatory ability in Atlantic salmon
Salmo salar L. J Fish Biol 39:421–432
Björnsson BT (1997) The biology of salmon growth hormone: from daylight to dominance. Fish
Physiol Biochem 17:9–24
Boeuf G (1993) Salmon smolting: a pre-adaptation to the oceanic environment. In: Rankin JC,
Jensen FB (eds) Fish ecophysiology. Chapman & Hall, London
Bohlin T, Dellefors C, Faremo U (1986) Early sexual maturation of male sea trout and salmon – an
evolutionary model and some practical implications. Rep Inst Freshw Res Drottningholm
66:17–25
References 239
Bohlin T, Dellefors C, Faremo U (1993) Date of smolt migration depends on body-size but not
age in wild sea-run brown trout. J Fish Biol 49:157–164
Burton MP, Idler DR (1984) Can Newfoundland landlocked salmon, Salmo salar L. adapt to sea
water? J Fish Biol 24:59–64
Claireaux G, Lefrançois C (2007) Linking environmental variability and fish performance: inte-
gration through the concept of scope for activity. Philos Trans R Soc Lond B 362:2031–2041
Clarke WC, Withler RE, Shelbourn JE (1992) Genetic control of juvenile life history pattern in
Chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 49:2300–2306
Clarke WC, Withler RE, Shelbourn JE (1994) Inheritance of smolting phenotypes in backcrosses
of hybrid stream-type X ocean-type chinook salmon (Oncorhynchus tshawytscha). Estuaries
1A:13–25
Conte FP, Wagner HH (1965) The development of osmotic and ionic regulation in juvenile steel-
head trout Salmo gairdneri. Comp Biochem Physiol 14:603–620
Dahl K (1910) The age and growth of salmon and trout in Norway as shown by their scales.
Salmon and Trout Association, London
Dann SG, Allison WT, Levin DB et al (2003) Identification of a unique transcript down-regulated
in the retina of rainbow trout (Oncorhynchus mykiss) at smoltification. Comp Biochem Physiol
136B:849–860
Davidsen JG, Plantalech Manella N, Thorstad EB et al (2009) Vertical movements of Atlantic
salmon postsmolts relative to measures of salinity and water temperature during the first phase
of the marine migration. Fish Manage Ecol 16:147–154
Dellefors C, Faremo U (1988) Early sexual maturation in males of wild sea trout, Salmo trutta L.,
inhibits smoltification. J Fish Biol 33:741–749
Dempson JB, Braithwaite VA, Doherty D et al (2010) Stable isotope analysis of marine feeding
signatures of Atlantic salmon in the North Atlantic. ICES J Mar Sci 67:52–61
Dickhoff WW, Beckman BR, Larsen DA et al (1997) The role of growth in endocrine regulation
of salmon smoltification. Fish Physiol Biochem 17:231–236
Duston J, Saunders RL (1990) The entrainment role of photoperiod on hypo-osmoregulatory and
growth-related aspects of smolting in Atlantic salmon (Salmo salar). Can J Zool 68:707–715
Ebbesson LOE, Ekström P, Ebberson SOE et al (2002) Neural circuits and their structural and
chemical reorganization in the light-brain-pituitary axis during parr-smolt transformation in
salmon. Aquaculture 222:59–70
Ebbesson LOE, Björnsson BT, Ekström P et al (2008) Daily endocrine profiles in parr and smolt
Atlantic salmon. Comp Biochem Physiol A 151:698–704
Elliott JM, Hurley MA (1997) A functional model for maximum growth of Atlantic salmon parr,
Salmo salar, from two populations in Northwest England. Funct Ecol 11:592–603
Elliott JM, Hurley MA, Maberley SC (2000) The emergence period of sea trout fry in a Lake
District stream correlates with the North Atlantic Oscillation. J Fish Biol 56:208–210
Elson PF (1957) The importance of size in the change from parr to smolt in Atlantic salmon. Can
Fish Culturist 21:1–6
Englund V, Niemelä E, Länsman M et al (1999) Variations in Atlantic salmon, Salmo salar L.,
smolt age in tributaries of the River Teno, Finland. Fish Manage Ecol 6:83–86
Eriksson T (1984) Adjustments in annual cycles of swimming behaviour in juvenile Baltic salmon
in fresh and brackish water. Trans Am Fish Soc 113:467–471
Eriksson LO, Lundqvist H (1982) Circannual rhythms and photoperiod regulation of growth and
smolting in Baltic salmon (Salmo salar L.). Aquaculture 28:113–121
Fahy E (1985) Cyclic fluctuations in the abundance of trout (Salmo trutta L.). Arch Hydrobiol
Suppl 3:404–428
Fängstam H, Berglund I, Sjöberg M et al (1993) Effects of size and early sexual maturity on down-
stream migration during smolting in Baltic salmon (Salmo salar). J Fish Biol 43:517–529
Ferguson A (2006) Genetics of sea trout, with particular reference to Britain and Ireland. In: Harris
G, Milner N (eds) Sea trout: biology, conservation and management. Blackwell, Oxford
Finstad B, Ugedal O (1998) Smolting of sea trout (Salmo trutta L.) in northern Norway.
Aquaculture 168:341–349
Finstad B, Staurnes M, Reite OB (1988) Effect of low temperature on sea water tolerance in rainbow
trout, Salmo gairdneri. Aquaculture 72:319–328
Fleming IA, Jonsson B, Gross MR et al (1996) Experimental tests of the reproductive impact of
farmed on wild Atlantic salmon (Salmo salar). J Appl Ecol 33:893–905
Folmar LC, Dickhoff WW (1980) The parr-smolt transformation (smoltification) and seawater
adaptations in salmonids. Aquaculture 21:1–37
Foote CJ, Wood CC, Clarke WC et al (1992) Circannual cycle of seawater adaptability in
Oncorhynchus nerka: genetic differences in smoltification of sympatric sockeye salmon and
kokanee. Can J Fish Aquat Sci 49:99–109
Forseth T, Næsje TF, Jonsson B et al (1999) Juvenile migration in brown trout: a consequence of
energetic state. J Anim Ecol 68:783–793
Franklin CE, Davison W, Forster ME (1992a) Seawater adaptability of New Zealand’s sockeye
(Oncorhynchus nerka) and chinook salmon (O. tshawytscha): physiological correlates of
smoltification and seawater survival. Aquaculture 102:127–142
Franklin CE, Forster ME, Davison W (1992b) Plasma cortisol and osmoregulatory changes in
sockeye salmon transferred to sea water: comparison between successful and unsuccessful
adaptation. J Fish Biol 41:113–122
Gorbman A, Dickhoff WW, Mighell JL et al (1982) Morphological indices of developmental
progress in parr-smolt coho salmon, Oncorhynchus kisutch. Aquaculture 28:1–19
Handeland SO, Wilkinson E, Sveinsbø B et al (2004) Temperature influence on the development
and loss of seawater tolerance in two fast-growing strains of Atlantic salmon. Aquaculture
233:513–529
Hansen LP, Jonsson B (1985) Downstream migration of reared smolts of Atlantic salmon (Salmo
salar L.) in the River Imsa. Aquaculture 45:237–248
Hansen LP, Jonsson B, Morgan RIG et al (1989) Influence of parr maturity on emigration of
smolts of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 46:410–415
Hasler AD, Scholz AT (1983) Olfactory imprinting and homing in salmon. Springer, Berlin
Higgins PJ, Talbot C (1985) Growth and feeding in juvenile Atlantic salmon (Salmo salar L.). In:
Cowey CB, Mackie AM, Bell JG (eds) Nutrition and feeding in fish. Academic, London
Hoar WS (1988) The physiology of smolting salmonids. In: Hoar WS, Randall D (eds) Fish physio
logy, vol XIB. Academic, New York
Høgåsen HR (1998) Physiological changes associated with the diadromous migration of salmo-
nids, Canadian Special Publication of Fisheries and Aquatic Sciences 127. National Research
Council, Ottawa
Huntsman AG, Hoar WS (1939) Resistance of Atlantic salmon to sea water. J Fish Res Board Can
4:409–411
Hutchison MJ, Iwata M (1998) Effect of thyroxine on the decrease of aggressive behaviour of four
salmonids during the parr-smolt transformation. Aquaculture 168:169–175
Ibbotson AT, Beaumont WRC, Pinder A et al (2006) Diel migration patterns of Atlantic salmon
smolts with particular reference to the absence of crepuscular migration. Ecol Freshw Fish
15:544–551
Iigo M, Ikuta K, Kitamura S et al (2005) Effects of melatonin feeding on smoltification in masu
salmon (Oncorhynchus masou). Zool Sci 22:1191–1196
Iwata M (1995) Downstream migratory behavior of salmonids and its relationship with cortisol
and thyroid hormones: a review. Aquaculture 135:131–139
Järvi T, Holmgren K, Rubin RF et al (1996) Newly-emerged Salmo trutta fry that migrate to the
sea – an alternative choice of feeding habitat? Nord J Freshw Res 72:52–62
Jensen AJ, Johnsen BO (1985) Growth and smolt age of Atlantic salmon (Salmo salar L.) in
the glacier river Beiarelva, Northern Norway. Rep Inst Freshw Res Drottningholm
62:86–90
Jensen AJ, Johnsen BO (1986) Different adaptation strategies of Atlantic salmon (Salmo salar L.)
populations to extreme climates with special reference to some cold Norwegian rivers. Can J
Fish Aquat Sci 43:980–984
Johnston CE, Saunders RL (1981) Parr-smolt transformation of yearling Atlantic salmon (Salmo
salar) at several rearing temperatures. Can J Fish Aquat Sci 38:1189–1198
References 241
Jones JW (1959) The salmon. Collins, London

Jonsson B (1981) Life history strategies of brown trout. Dr philos thesis, Univ Oslo
Jonsson B (1982) Diadromous and resident trout Salmo trutta: is their difference due to genetics?
Oikos 38:297–300
Jonsson B (1985) Life history patterns of freshwater resident and sea-run migrant brown trout in
Norway. Trans Am Fish Soc 114:182–194
Jonsson B (1989) Life history and habitat use of Norwegian brown trout (Salmo trutta). Freshw
Biol 21:71–86
Jonsson B, Jonsson N (1993) Partial migration: niche shift versus sexual maturation in fishes. Rev
Fish Biol Fish 3:348–365
Jonsson N, Jonsson B (1998) Body composition and energy allocation in life history stages of
brown trout. J Fish Biol 53:1306–1316
Jonsson N, Jonsson B (2003) Energy density and content of Atlantic salmon: variation among
developmental stages and types of spawners. Can J Fish Aquat Sci 60:506–516
Jonsson B, Jonsson N (2005) Lipid energy reserves influence life history decision of salmonid
parr. Ecol Freshw Fish 14:296–301
Jonsson B, Jonsson N (2009) Migratory timing, marine survival and growth of anadromous brown
trout Salmo trutta in the River Imsa, Norway. J Fish Biol 74:621–638
Jonsson B, L’Abée-Lund JH (1993) Latitudinal clines in life history variables of anadromous
brown trout in Europe. J Fish Biol 43(Suppl A):1–16
Jonsson B, Jonsson N, Ruud-Hansen J (1989) Downstream displacement and life history
variables of Arctic charr (Salvelinus alpinus) in a Norwegian river. Physiol Ecol Jpn Spec
1:93–105
Jonsson N, Jonsson B, Hansen LP (1990) Partial segregation in the timing of migration of Atlantic
salmon of different ages. Anim Behav 40:313–321
Jonsson N, Hansen LP, Jonsson B (1991) Variation in age, size and repeat spawning of adult
Atlantic salmon in relation to river discharge. J Anim Ecol 60:937–947
Jonsson N, Hansen LP, Jonsson B (1993) Migratory behaviour and growth of hatchery-reared
post-smolt Atlantic salmon Salmo salar L. J Fish Biol 42:435–443
Jonsson N, Jonsson B, Hansen LP (1994a) Sea ranching of brown trout (Salmo trutta). Fish
Manage Ecol 1:67–76
Jonsson N, Jonsson B, Hansen LP et al (1994b) Effects of sea-water-acclimatization and release
sites on survival of hatchery-reared brown trout Salmo trutta. J Fish Biol 44:973–981
Jonsson N, Jonsson B, Aass P et al (1995) Brown trout Salmo trutta released to support recre-
ational fishing in a Norwegian fjord. J Fish Biol 46:70–84
Jonsson N, Jonsson B, Hansen LP (1998a) Long-term study of the ecology of wild Atlantic
salmon smolts in a small Norwegian river. J Fish Biol 52:638–650
Jonsson N, Jonsson B, Hansen LP (1998b) Density-dependent and density-independent relation-
ships in the life cycle of Atlantic salmon, Salmo salar. J Anim Ecol 67:751–762
Jonsson B, Jonsson N, Brodtkorb E et al (2001) Life history traits of brown trout vary with the
size of small streams. Funct Ecol 15:310–317
Jonsson N, Jonsson B, Hansen LP (2005) Does climate during embryonic development influences
parr growth and age of seaward migration in Atlantic salmon (Salmo salar) smolts? Can J Fish
Aquat Sci 62:2502–2508
Jørgensen EH, Arnesen AM (2002) Seasonal changes in osmotic and ionic regulation in Arctic
charr, Salvelinus alpinus, from a high- and a sub-arctic anadromous population. Env Biol Fish
64:185–193
Juanes F, Gephard S, Beland KF (2004) Long-term changes in migration timing of adult Atlantic
salmon (Salmo salar) at the southern edge of the species distribution. Can J Fish Aquat Sci
61:2392–2400
Karnaky KJ (1986) Structure and function of the chloride cell of Fundulus heteroclitus and other
teleosts. Am Zool 26:209–224
Kiiskinen P, Hyvärinen H, Pironen J (2002) Smolting and seasonal variation in the smolt charac-
teristics of one- and two-year-old Saimaa landlocked salmon under fish farm conditions. J Fish
Biol 60:1015–1030
Komourdjian MP, Saunders RL, Fenwick JC (1976) Evidence for the role of growth hormone as
a part of a ‘light-pituitary axis’ in growth and smoltification of Atlantic salmon (Salmo salar).
Can J Zool 54:544–551
Kuzmin OG, Smirnov YA (1982) Environmental factors and growth of young Atlantic salmon,
Salmo salar (Salmonidae), in small rivers of the Kola Peninsula. J Ichthyol 22:42–51
L’Abée-Lund JH, Jonsson B, Jensen AJ et al (1989) Latitudinal variation in life history characte
ristics of sea-run migrant brown trout Salmo trutta. J Anim Ecol 58:525–542
Landergren P (2001) Survival and growth of sea trout parr in fresh and brackish water. J Fish Biol
58:591–593
Landergren P, Vallin L (1998) Spawning of sea trout, Salmo trutta L., in brackish waters: lost
effort or successful strategy? Fish Res 35:229–236
Landgrebe FW (1941) The role of the pituitary and the thyroid in the development of teleosts.
J Exp Biol 18:162–169
Leatherland JF (1982) Environmental physiology of the teleostean thyroid gland: a review.
Environ Biol Fish 7:83–110
Levine JS, Lobel PS, MacNichol EF (1980) Visual communication in fishes. In: Ali MA (ed)
Environmental physiology of fishes. Plenum, New York
Li HO, Yamada J (1992) Changes of the fatty acid composite ion in smolts of masu salmon
(Oncorhynchus masou) associated with desmoltification and sea-water transfer. Comp
Biochem Physiol 103:221–226
Limburg KE, Landergren P, Westin L et al (2001) Flexible modes of anadromy in Baltic Sea trout:
making the most of marginal spawning streams. J Fish Biol 59:682–695
Lundqvist H, Eriksson LO (1985) Annual rhythms of swimming behaviour and seawater adapta-
tion in young Baltic salmon, Salmo salar, associated with smolting. Environ Biol Fish
14:259–267
Lythgoe JN (1979) The ecology of vision. Oxford University Press, Oxford
Mackie PM, Gharbi K, Ballantyne JS et al (2007) Na+/K+/Cl(-) cotransporter and CFTR gill expres-
sion after seaward transfer in smolts (0+) of different Atlantic salmon (Salmo salar) families.
Madsen SS, Bern HA (1992) Antagonism of prolactin and growth hormone – impact on seawater
adaptation in 2 salmonids, Salmo trutta and Oncorhynchus mykiss. Zool Sci 9:775–784
Matty AJ, Lone KP (1985) The hormonal control of metabolism and feeding. In: Tytler P, Calow
P (eds) Fish energetics new perspectives. Croom Helm, London
Matty AJ, Sheltaway MJ (1967) Thyroxine and skin purines in trout. Gen Comp Endocrinol
9:473–482
McCormick SD (2001) Endocrine control of osmoregulation in teleost fish. Am Zool 41:781–794
McCormick SD (2009) Evolution of the hormonal control of animal performance: insight from
the seaward migration of salmon. Integrat Comp Biol 49:408–422
McCormick SD, Saunders RL (1987) Preparatory physiological adaptations for marine life in
salmonids: osmoregulation, growth and metabolism. Am Fish Soc Symp 1:211–229
McCormick SD, Saunders RL, Henderson EB (1987) Photoperiod control of parr-smolt transfor-
mation in Atlantic salmon (Salmo salar): changes in salinity tolerance, gill Na+, K+-ATPase
activity, and plasma thyroid hormones. Can J Fish Aquat Sci 44:1462–1468
McCormick SD, Hansen LP, Quinn TP et al (1998) Movement, migration, and smolting of
Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 55:77–92
McCormick SD, Cunjak RA, Dempson B et al (1999) Temperature-related loss of smolt charac-
teristics in Atlantic salmon (Salmo salar) in the wild. Can J Fish Aquat Sci 56:1649–1658
McCormick SD, Moriyama S, Bjornsson BT (2000) Low temperature limits photoperiod control
of smolting in Atlantic salmon through endocrine mechanisms. Am J Physiol Regul Integr
Comp Physiol 278:1352–1361
McCormick SD, Shrimpton JM, Moriyama S et al (2002) Effects of an advanced temperature
cycle on smolt development and endocrinology indicate that temperature is not a zeitgeber for
smolting in Atlantic salmon. J Exp Biol 205:3553–3560
References 243
McCormick SD, Shrimpton JM, Moriyama S et al (2007) Differential hormonal responses of
Atlantic salmon parr and smolt to increased daylength: a possible developmental basis for
smolting. Aquaculture 273:337–344
McCormick SD, Regish AM, Christensen AK (2009) Distinct freshwater and seawater isoforms
of Na+/K+-ATPase in gill chloride cells of Atlantic salmon. J Exp Biol 212:3994–4001
McDowall RM (1988) Diadromy in fishes, migrations between freshwater and marine environ-
ments. Chapman & Hall, London
McInerney JE (1964) Salinity preference: an orientation mechanism in salmon migration. J Fish
Res Board Can 21:995–1018
Metcalfe NB, Thorpe JE (1990) Determinants of geographical variation in the age of seaward
migrating salmon, Salmo salar. J Anim Ecol 59:135–149
Metcalfe NB, Huntingford FA, Thorpe JE et al (1990) The effects of social status on life-history
variation in juvenile salmon. Can J Zool 68:2630–2636
Morin PP, Andersen O, Haug E et al (1994) Melatonin rhythms in Atlantic salmon (Salmo salar)
maintained under natural and out-of-phase photoperiods. Gen Comp Endocrinol 98:73–86
Mortensen A, Damsgård B (1998) The effect of salinity on desmoltification in Atlantic salmon.
Munakata A, Amano M, Ikuta K et al (2007) Effects of growth hormone and cortisol on the down-
stream migratory behavior in masu salmon, Oncorhynchus masou. Gen Comp Endocrinol
150:12–17
Negus MT (2003) Determination of smoltification status in juvenile migratory rainbow trout and
Chinook salmon in Minnesota. N Am J Fish Manage 23:913–927
Nielsen C, Aarestrup K, Norum U et al (2004) Future migratory behaviour predicted from premi-
gratory levels of gill Na+-K+ ATPase activity in individual wild brown trout (Salmo trutta). J
Exp Biol 207:527–533
Nilsen TO, Ebbesson LOE, Stefansson SO (2003) Smolting in anadromous and landlocked strains
of Atlantic salmon (Salmo salar). Aquaculture 222:71–82
Nilsen TO, Ebbesson LOE, Kiilerich P et al (2008) Endocrine systems in juvenile anadromous and
landlocked Atlantic salmon (Salmo salar): seasonal development and seawater acclimation.
Gen Comp Endocrinol 155:762–772
Nordgarden U, Björnsson BT, Hansen T (2007) Developmental stage of Atlantic salmon parr
regulates pituitary GH secretion and parr–smolt transformation. Aquaculture 264:441–448
O’Byrne-Ring N, Dowling K, Cotter D et al (2003) Changes in mucus cell numbers in the epider-
mis of the Atlantic salmon at the onset of smoltification. J Fish Biol 63:1625–1630
Ojima D, Iwata M (2010) Central administration of growth hormone-releasing hormone and
corticotropin-releasing hormone stimulate downstream movement and thyroxine secretion in
fall-smolting coho salmon (Oncorhynchus kisutch). Gen Comp Endocrinol 168:82–87
Økland F, Jonsson B, Jensen AJ et al (1993) Is there a threshold size regulating smolt size in
brown trout and Atlantic salmon? J Fish Biol 42:541–550
Olsen YA, Reitan LJ, Røed KH (1993) Gill Na+, K+ -ATPase activity, plasma cortisol level, and
non-specific immune response in Atlantic salmon (Salmo salar) during parr-smolt transforma-
tion. J Fish Biol 43:559–573
Olsén KH, Petersson E, Ragnarsson B et al (2004) Downstream migration in Atlantic salmon
(Salmo salar) smolt sibling groups. Can J Fish Aquat Sci 61:328–331
Österdahl L (1969) The smolt run of a small Swedish river. In: Northcote TG (ed) Salmon and
trout in streams. University of British Columbia, Vancouver
Otto RG (1971) Effects of salinity on the survival and growth of pre-smolt coho salmon
(Oncorhynchus kisutch). J Fish Res Board Can 28:343–349
Otto RE, McInerney JE (1970) Development of salinity preference in pre-smolt coho salmon
(Oncorhynchus kisutch). J Fish Res Board Can 27:793–800
Pelis RM, McCormick SD (2001) Effects of growth hormone and cortisol on Na+ K+-2Cl(-)
cotransporter localization and abundance in the gills of Atlantic salmon. Gen Comp Endocrinol
124:134–143
Porter MJR, Randall CF, Bromage NR et al (1998) The role of melatonin and the pineal gland on
development and smoltification of Atlantic salmon (Salmo salar) parr. Aquaculture
168:139–155
Post JR, Parkinson EA (2001) Energy allocation strategy in young fish: allometry and survival.
Ecology 82:1040–1051
Power G (1958) The evolution of the freshwater races of the Atlantic salmon (Salmo salar L.) in
eastern, North America. Arctic 11:86–92
Power G (1969) The salmon of Ungava Bay. Arctic Institute of North America, Technical paper
22, Montreal
Power G (1981) Stock characteristics and catches of Atlantic salmon (Salmo salar) in Quebec, and
Newfoundland and Labrador in relation to environmental variables. Can J Fish Aquat Sci
38:1601–1611
Prunet P, Boeuf G, Bolton JP, Young G (1989) Smoltification and seawater adaptation in Atlantic
salmon (Salmo salar): plasma prolactin, growth hormone, and thyroid hormones. Gen Comp
Endocrinol 74:355–364
Raine JC, Hawryshyn CW (2009) Changes in thyroid hormone reception precede SWS1 opsin
downregulation in trout retina. J Exp Biol 212:2781–2788
Refstie T, Steine TA, Gjedrem T (1977) Selection experiments with salmon. II. Proportion of
Atlantic salmon smolting at 1 year of age. Aquaculture 10:231–242
Richards JG, Semple JW, Bystriansky JS et al (2003) Na+/K+-ATPase a-isoforms switching in gills
of rainbow trout (Oncorhynchus mykiss) during salinity transfer. J Exp Biol 206:4475–4486
Ricker WE (1938) “Residual” and kokanee salmon in Cultus Lake. J Fish Res Board Can 4:192–218
Rikardsen AH, Thorpe JE, Dempson JB (2004) Modelling the life history variation of Arctic
charr. Ecol Freshw Fish 13:305–311
Saunders RL (1965) Adjustment of buoyancy in young Atlantic salmon and brook trout by
changes in swim-bladder volume. J Fish Res Board Can 22:336–352
Saunders RL, Henderson EB (1969) Growth of Atlantic salmon smolts and post-smolts in relation
to salinity, temperature and diet. Fish Res Board Can Techn Rep 149:1–20
Saunders RL, Henderson EB (1970) Influence of photoperiod on smolt development and growth
of Atlantic salmon (Salmo salar). J Fish Res Board Can 27:1295–1311
Saunders RL, Henderson EB (1978) Changes in gill ATPase activity and smolt status of Atlantic
salmon (Salmo salar). J Fish Res Board Can 35:1542–1546
Schmitz M (1992) Annual variations in rheotactic behavior and seawater adaptability in land-
locked Arctic char (Salvelinus alpinus). Can J Fish Aquat Sci 49:448–452
Seidelin M, Madsen SS, Byrialsen A et al (1999) Effects of insulin-like growth factor-I and cor-
tisol on Na+, K+-ATPase expression in osmoregulatory tissues of brown trout (Salmo trutta).
Gen Comp Endocrinol 113:331–342
Shrimpton JM, Björnsson BT, McCormick SD (2000) Can Atlantic salmon smolt twice?
Endocrine and biochemical changes during smolting. Can J Fish Aquat Sci 57:1969–1976
Sigholt T, Asgard T, Staurnes M (1998) Timing of parr-smolt transformation in Atlantic salmon
(Salmo salar): effects of changes in temperature and photoperiod. Aquaculture 160:129–144
Soivio A, Virtanen E, Mouna M (1988) Desmoltification of heat-accelerated Baltic salmon (Salmo
salar) in brackish water. Aquaculture 71:89–97
Solbakken VA, Hansen T, Stefansson SO (1994) Effects of photoperiod and temperature on
growth and parr smolt transformation in Atlantic salmon (Salmo salar L.) and subsequent
performance in seawater. Aquaculture 121:13–27
Spencer RC, Zydlewski J, Zydlewski G (2010) Migratory urge and gill Na+, K+-ATPase activity
of hatchery-reared Atlantic salmon smolts from the Dennys and Penobscot River stocks, Maine.
Trans Am Fish Soc 139:947–956
Staurnes M, Lysfjord G, Berg OK (1992) Parr-smolt transformation of a nonanadromous popula-
tion of Atlantic salmon (Salmo salar) in Norway. Can J Zool 70:197–199
Stefansson SO, Berge AI, Gunnarsson GS (1998) Changes in seawater tolerance and gill Na+, K+-
ATPase activity during desmoltification in Atlantic salmon kept in freshwater at different
temperatures. Aquaculture 168:271–277
References 245
Strothotte E, Chaput GJ, Rosenthal H (2005) Seasonal growth of wild Atlantic salmon juveniles
and implications on age at smoltification. J Fish Biol 67:1585–1602
Sundell K, Jutfelt F, Ágústsson T et al (2003) Intestinal transport mechanisms and plasma cortisol
levels during normal and out-of-season parr-smolt transformation of Atlantic salmon (Salmo
salar). Aquaculture 222:265–285
Svärdson G, Fagerström Å (1982) Adaptive differences in the long-distance migration of some
trout (Salmo trutta L.) stocks. Rep Inst Freshw Res Drottningholm 60:51–80
Symons PEK (1979) Estimated escapement of Atlantic salmon (Salmo salar) for maximum smolt
production in rivers of different productivity. J Fish Res Board Can 36:132–140
Thorpe JE (1994) An alternative view of smolting in salmonids. Aquaculture 121:105–113
Thorpe JE (2007) Maturation responses of salmonids to changing developmental opportunities.
Mar Ecol Progr Ser 335:285–288
Thorpe JE, Metcalfe NB (1998) Is smolting a positive or a negative developmental decision?
Thorpe JE, Ross LG, Struthers G et al (1981) Tracking Atlantic salmon smolts Salmo salar L.
through Loch Voil, Scotland. J Fish Biol 19:519–537
Thorpe JE, Metcalfe NB, Fraser NHC (1994) Temperature dependence of the switch between
nocturnal and diurnal smolt migration in Atlantic salmon. In: Mackinlay DD (ed) High perfor-
mance fish. Fish Physiology Association, Vancouver
Thorpe JE, Mangel M, Metcalfe NB et al (1998) Modelling the proximate basis of salmonid life-
history variation, with application to Atlantic salmon, Salmo salar L. Evol Ecol 12:581–599
Tipsmark CK, Madsen SS, Seidelin M et al (2002) Dynamics of Na+, K+, 2Cl– cotransporter and
Na+, K+ -ATPase expression in the branchial epithelium or brown trout (Salmo trutta) and
Atlantic salmon (Salmo salar). J Exp Zool 293:106–118
Tipsmark CK, Jørgensen C, Brande-Lavridsen N et al (2009) Effects of cortisol, growth hormone and
prolactin on gill claudin expression in Atlantic salmon. Gen Comp Endocrinol 163:1270–1277
Titus RG, Mosegaard H (1989) Fluctuating recruitment and variable life history of migratory
brown trout, Salmo trutta L., in a small, Baltic coast stream. J Fish Biol 35(Suppl
A):351–353
Titus RG, Mosegaard H (1992) Fluctuating recruitment and variable life history of migratory
brown trout, Salmo trutta L., in a small, unstable stream. J Fish Biol 41:239–255
Uchida K, Kaneko T, Yamauchi K et al (1996) Morphometrical analysis of chloride cell activity
in the gill filaments and lamellae and changes in Na+, K+-ATPase activity during seawater
adaptation in chum salmon fry. J Exp Zool 276:193–200
Ura K, Mizuno S, Okubo T et al (1997) Immunohistochemical study on changes in gill Na+, K+-
ATPase a-subunit during smoltification in the wild masu salmon, Oncorhynchus masou. Fish
Physiol Biochem 17:397–403
Wagner HH (1974) Photoperiod and temperature regulation of smolting in steelhead trout (Salmo
gairdneri). Can J Zool 52:219–234
Webb PW (1984) Form and function in fish swimming. Sci Am 251:58–68
Wedemeyer GA (1996) Physiology of fish in intensive culture systems. Chapman & Hall, New
York
Wedemeyer GA, Saunders RL, Clarke WC (1980) Environmental factors affecting smoltification
and early marine survival of anadromous salmonids. Mar Fish Rev 42:1–14
Woo NYS, Burns HH, Nishioka RS (1978) Changes in body composition associated with smolti-
fication and premature transfer to seawater in coho (Oncorhynchus kisutch) and king salmon
(Oncorhynchus tshawytscha). J Fish Biol 13:421–428
Wootton RJ (1998) Ecology of teleost fishes, 2nd edn. Kluwer, Dordrecht
Young G (1988) Enhanced response of the interrenal of coho salmon (Oncorhynchus kisutch) to
ACTH after growth hormone treatment in vivo and in vitro. Gen Comp Endocrinol 71:85–92
Zydlewski GB, Haro A, McCormick SD (2005) Evidence for cumulative temperature as an initiating
and terminating factor in downstream migratory behavior of Atlantic salmon (Salmo salar)
smolts. Can J Fish Aquat Sci 62:68–78

Cap 5. - Smolts and Smolting

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Chapter 5

Smolts and Smolting

5.1 Organization of the Chapter

This chapter describes important elements of the parr-smolt transformation

5.2 Morphological and Physiological Changes During Smolting

Morphology and physiology of anadromous salmonids change in spring prior to

5.2.1 Colour and Morphology

The most conspicuous colour-change is the development of the intense silvery,

5.2.2.1 Visual Pigments and Ultraviolet Sensitivity

Modifications of the retina of the eyes include loss of ultraviolet-sensitive (UVS)

5.2.2.2 Buoyancy and Metabolism

their hypo-osmoregulatory ability relative to pre-migratory and non-migratory

During smolting, there are increases in circulating levels of thyroxin, cortisol,

Smolting happens in response to environmental cues such as photoperiod and

Smolting is controlled by an endogenous rhythm, itself controlled by the nervous

Water temperature is responsible for annual variation in the time of smolting.

5.3 Behavioural Change

5.4 Ecological Characters

5.4.2 Size and Growth

5.4.5 Smolting Versus Sexual Maturation

Are smolting and sexual maturation competing processes? Landgrebe (1941)

5.5 Is Smolt-Age Inherited?

There is heritability for age at smolting, as experimentally documented from both

1. The parr-smolt transformation (smolting) is characterized by changes in

Aarestrup K, Jepsen N, Rasmussen G et al (1999) Movements of two strains of radiotagged

Jones JW (1959) The salmon. Collins, London

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5.1 Organization of the Chapter

5.2 Morphological and Physiological Changes During Smolting

5.2.1 Colour and Morphology

5.2.2.1 Visual Pigments and Ultraviolet Sensitivity

5.2.2.2 Buoyancy and Metabolism

5.3 Behavioural Change

5.4 Ecological Characters

5.4.2 Size and Growth

5.4.5 Smolting Versus Sexual Maturation

5.5 Is Smolt-Age Inherited?