Migratory Behaviors in Masu Salmon ( Endocrinological Factors Oncorhynchus masou

Aqua-BioScience Monographs, Vol. 5, No. 2, pp. 29–65 (2012)
www.terrapub.co.jp/onlinemonographs/absm/
Migratory Behaviors in Masu Salmon
(Oncorhynchus masou) and the Influence of
Endocrinological Factors
Arimune Munakata
Department of Biology
Miyagi University of Education
Aoba-ku, Sendai, Miyagi 980-0845, Japan
e-mail: [email protected]
Abstract
In the freshwater phase of their lifecycle, masu salmon (Oncorhynchus masou) comprise
two different phenotypes. A portion of the juveniles (migratory form) exhibit downstream
migratory behavior after smoltification. However, some masu salmon (non-migratory form)
such as precociously mature males live continuously in their natal rivers throughout their
lifetime. The coexistence of migratory and non-migratory forms within the species indicates that this salmon can be effectively used as a model fish to illuminate both inhibitory
and stimulatory physiological control mechanisms of migratory behaviors. In masu salmon,
it was found that sex steroid hormones inhibit the occurrence of downstream swimming
behavior, the initial step in seaward migration. Moreover, after the commencement of
downstream migration, sex steroid hormones induced the upstream swimming and subsequent spawning behaviors. These findings indicate that sex steroid hormones influence
the occurrence of the downstream and upstream swimming behavior in the resulting rheotaxis fashion (negative and positive, respectively). In contrast to sex steroid hormones, it
was also found that cortisol, which is involved substantially in smoltification, stimulates
the downstream swimming behavior. These findings indicate that the occurrence of seaward migration is controlled competitively by sex steroid hormones (sexual maturation)
and smolt-inducing factors such as cortisol, in masu salmon and potentially other Pacific
salmon.
1. Introduction
Salmonids (family Salmonidae) consist of four genera, Hucho, Salvelinus, Salmo, and Oncorhynchus
(Neave 1958; Norden 1961; Murata et al. 1993). These
salmonids originally inhabited tributaries from highthrough mid-latitude areas in the northern hemisphere
(Quinn 2005). It is also known that a large part of
salmonids (in quantity: the number of species and
biomass) are anadromous, and these fish (i.e., migratory form) regularly exhibit downstream migratory
behavior from the rivers to the sea (or lakes), after the
occurrence of parr to smolt transformation (i.e.,
smoltification) (Fig. 1). However, many species capable of anadromy also have phenotypes that are fulltime residents of freshwater habitats (i.e., nonmigratory forms) and display neither smoltification nor
downstream migratory behavior to the sea (Munakata
© 2012 TERRAPUB, Tokyo. All rights reserved.
doi:10.5047/absm.2012.00502.0029
Received on
April 1, 2011
Accepted on September 22, 2011
Online published on
November 20, 2012
Keywords
• cortisol
• downstream migration
• masu salmon
• Oncorhynchus masou
• Pacific salmon
• sex steroid hormone
• spawning
• testosterone
• upstream migration
and Kobayashi 2010). Most of the non-migratory forms
will live continuously in their natal rivers throughout
their lives (Fig. 1). Regardless of these life history
types, most salmonids will spawn in freshwater environments, mainly in their natal rivers (Fig. 1) (Quinn
2005). From these phenomena, salmonids are considered to be of freshwater (fluvial) fish origin and their
migratory behaviors by and large start from the rivers
(Fig. 1).
Among the four genera of salmonids, two genera
Hucho and Salvelinus are considered evolutionally
ancient groups, based on the phylogenic analyses
(Norden 1961; Murata et al. 1993). Genus Hucho inhabit only the northern Eurasia continent and genus
Salvelinus inhabit northern Eurasia and the American
continent (Quin 2005). On the other hand, genus Salmo
(i.e., Atlantic salmon) and Oncorhynchus (i.e., Pacific
salmon), which are considered evolutionally new
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
30
River
Sea
Evolution
Pink and chum
salmon
Oncorhynchus
(Pacific salmon)
Migrants
Masu salmon
Non-migrants
-m
Salmo
(Atlantic Salmon)
Salvelinus
Hucho
Fig. 1. Schematic drawing that illustrates the diversity of
distance covered by non-migratory and migratory forms for
four salmonid genera (shown in the order of the evolutional
age). In genus Hucho, most fish live continuously in their
natal rivers. In genus Salvelinus and Salmo, some fish migrate to the sea after smoltification. In genus Oncorhynchus,
most juveniles perform long distance seaward migration for
several years. On the other hand, in masu salmon (O. masou),
a portion of the fish perform seaward migration for a year
after smoltification, while an equivalent portion of them stay
in the rivers similar to genera Hucho, Salvelinus, and Salmo.
groups, are widely distributed in the rivers and tributaries around the north Atlantic and Pacific Oceans,
respectively (Groot and Margolis 1991).
In regard to migratory behaviors, the majority of fish
in the genus Hucho and Salvelinus live continuously
in their natal river systems throughout their lifetime,
as non-migratory forms (Fig. 1). If at all existent, the
proportions of the migratory forms are much smaller,
and their temporal and spatial ranges of migratory
movements are shorter and narrower, respectively, than
those in other salmonids such as Atlantic and Pacific
salmon. On the other hand, in Pacific salmon such as
pink (O. gorbuscha) and chum (O. keta) salmon, which
are considered evolutionally the newest species, most
juveniles undergo long distance seaward migration
(e.g., from Japanese streams to the Bering Sea) which
will continue for several years (Groot and Margolis
1991). Their temporal and spatial ranges of migratory
movements are considerably longer and broader than
in other salmonid species. Based on these wide differences in migratory patterns among salmonid genera
from different evolutional time periods, it is inferred
that the proportions of migratory forms increased, and
subsequently the temporal and spatial ranges of migration became longer and broader, respectively,
through the evolutionary processes (Fig. 1).
In masu salmon (O. masou) (Fig. 2), a Pacific salmon
Fig. 2. Photographs of masu salmon (Oncorhynchus masou).
(a) precocious male non-migrants, (b) immature parr nonmigrants, (c) pseudo smolt, (d) smolt migrants, and (e) adult
smolt migrants that migrated back from the sea.
that mainly inhabits Japanese rivers (i.e., western Pacific Ocean), some yearling (1+) fish live continuously
in their natal rivers similar to the ancient salmonid
genera including genus Hucho and Salvelinus
(Machidori and Kato 1984; Kato 1991; Kiso 1995)
(Figs. 1, 3). In masu salmon, however, a portion of the
1+ juveniles exhibit downstream migratory behavior
after the occurrence of smoltification, as do other Pacific salmon such as pink and chum salmon. In masu
salmon, such differentiations in lifecycles regularly
occur within the same population from the same rivers, especially in the northern regions of their habitat
(e.g., northern Honshu through Hokkaido) (Machidori
and Kato 1984; Kato 1991; Kiso 1995).
Taking the lifecycles of masu and other salmonids
into consideration, the proportion of non-migratory and
migratory forms seem to vary, not only among different salmonid genera, but also within the same genus
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
River
Sea
Feeding
Spawning
31
Immaturre S
Immatu
Smolt
Precocious
male
Dow
D
migration
Feeding
( year)
Non-migrants
Upstream
migration
Homing
migration
Fig. 3. Lifecycles of masu salmon (Oncorhynchus masou). In masu salmon, some immature juveniles (migratory form) dis-
play the downstream migratory behavior after they have transformed from parr to smolt (smoltification). However, some
juveniles (non-migratory form) such as precociously mature males (precocious males) will live continuously in their natal
rivers throughout their lifetime. The lifecycle (migratory behavior, seaward migration) of migrants consists of downstream
migration, feeding, homing, upstream migration, and spawning. On the other hand, the lifecycle of non-migrants consists of
downstream movement within a river, stream residence, upstream movement, and spawning.
(e.g., Pacific salmon). Since both the non-migratory
and migratory forms appear within the same species,
it is hypothesized that the masu salmon possesses both
evolutionarily ancestral (i.e., fluvial) and modern (i.e.,
anadromous) characteristics of migratory behaviors. In
Japanese streams, the non-migratory form of masu
salmon is called “yamame” meaning mountain girl, and
the representative migratory form is called “sakuramasu”, meaning cherry blossoms. Why do only a portion of masu salmon juveniles exhibit the ocean-bound
migratory behaviors, whereas the rest do not?
In this monograph, an overview of the migratory
behaviors, especially the downstream and upstream migratory behaviors, and subsequent spawning behaviors
in masu salmon will be presented. Additionally, a
theory of hormonal control as a mechanism governing
downstream (negative rheotaxis) and upstream (positive rheotaxis) swimming behaviors, major components
of downstream and upstream migratory behaviors, and
subsequent spawning behaviors in masu and other Pacific and Atlantic salmon will also be presented. Since
both non-migratory and migratory forms appear within
the same population inhabiting the same river, it was
hypothesized that individual masu salmon physiologically control the inhibitory and stimulatory mechanisms
of migratory behaviors (Munakata and Kobayashi
2010).
In masu salmon, it is generally known that the nonmigratory forms are the precociously mature fish (i.e.,
precocious males) (Machidori and Kato 1984; Kiso
1995). On the other hand, most of migratory forms are
sexually immature male and female smolts, as observed
in other Pacific salmon (Quinn 2005). These phenomena thus indicated that “sexual maturation” is one of
the key physiological factors that regulate the occurrence of seaward migration. Furthermore, since most
of the downstream migrants undergo smoltification
before their seaward migration, it was hypothesized
that some physiological factors which are closely related to the smoltification stimulatory regulate the occurrence of downstream migratory behavior (Munakata
et al. 2007). Thus, previous studies investigated both
inhibitory and stimulatory control mechanisms of migratory behaviors in relation to sexual maturation (sex
hormones) and smoltification, respectively (Munakata
et al. 2000b, 2001a, 2001b, 2007, 2012a, 2012b). New
information will be used to reconsider the physiological control mechanisms, roles, and evolutionary processes of the migratory behaviors in masu salmon, and
perhaps in entire salmonids. Furthermore, this analysis incorporates not only physiological factors, but also
environmental factors that influence the migratory
behaviors. It is therefore suggested that the findings
have important implications. Especially, these data can
serve as new tools for improving our salmon stockmanagement, focusing specifically on the conservation
of their migratory behavior.
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
32
2. Roles of sex steroid hormones in the regulation
of downstream swimming behavior in masu
salmon and other salmonids
2-1. Def inition of migrator y behaviors in
salmonids
Migratory behavior of salmonids regularly consists
of downstream migratory behavior (downstream migration) from the river to the sea (or lakes), feeding
migratory behavior (feeding migration) in the sea (or
lakes), homing migratory behavior (homing migration)
from the sea (or lakes) to the mouth of their natal rivers, upstream migratory behavior (upstream migration)
from the mouth to the spawning ground in upper
reaches in the natal rivers, and spawning behaviors
(Munakata and Kobayashi 2010) (see Fig. 3). The
downstream migratory behavior, the initial step of seaward migration mainly consists of several specific
behaviors, such as schooling behavior, downstream
swimming behavior (negative rheotaxis, downstream
movement), and salinity preference (seawater adaptation) (Iwata 1995, 1996; Munakata and Kobayashi
2010). Also, the upstream migratory behavior consists
of several types of behaviors, such as upstream swimming behavior (positive rheotaxis, upstream movement), and freshwater preference. Among these phenomena, downstream and upstream swimming
behaviors, major components of downstream and upstream migratory behaviors, can be observed in an artificial raceway system (see Fig. 5) during their natural downstream and upstream migratory periods
(Munakata et al. 2000b, 2001a, 2001b, 2007, 2012a,
2012b). In this monograph, therefore, we mainly investigated the effects of endocrinological (hormonal)
factors on the occurrence of downstream and upstream
swimming behaviors in the raceway system.
2-2. Lifecycle of masu salmon
Masu salmon, a Pacific salmon, is broadly distributed in north western Pacific-rim rivers (Kamchatka
Peninsula through Kyushu Island) (Machidori and Kato
1984). In addition, several sub-species or sub-types of
masu salmon are found in this region: amago salmon
(O. masou ishilawae) inhabit streams in southwestern
Japan (e.g., southern Honshu, part of Kyushu, and the
Shikoku Islands) (Kato 1991); Biwa salmon (O. masou
rhodurus) inhabit the tributaries around Lake Biwa
(Fujioka et al. 1990); Taiwan salmon (O. masou
formosanus), an endangered sub-species, inhabit limited highland rivers of Taiwan (Oshima 1936); and a
hybrid type of the Honmasu salmon (O. masu x
rhodurus) inhabit tributaries around Lake Chuzenji
(Munakata et al. 1999, 2000a). During the spring, yearling (1+) masu salmon juveniles can be classified into
two groups, migratory and non-migratory forms. As
mentioned above, the representative migratory form
that lives in the rivers for 1.5 years regularly begins
the seaward migration following the occurrence of
smoltification (Kato 1991). On the other hand, representative non-migratory forms such as 1+ precocious
males live continuously in their natal rivers throughout their lifetime (Utoh 1976, 1977). In this section,
the lifecycles of masu salmon from hatching to the
period in which the smolt migrants exhibit downstream
migratory behavior will be summarized, with emphasis on environmental factors which induce either the
stream residency in non-migrants or smoltification in
migrants. Then, an overview of previous and recent
studies that have investigated the inhibitory roles of
sex steroid hormones, such as testosterone (T), 11ketotestosterone (11-KT), and estradiol-17 β (E2) in the
occurrence of smoltification and subsequent downstream swimming behavior in masu and other
salmonids will be outlined.
2-3. Early growth after emerging
After emerging from spawning beds (common name:
redd) which are located in the main stem or tributaries
in upper rivers, underyearling (0+) masu salmon juveniles (3 cm in standard body length) are typically found
in shallow areas (e.g., behind large stones, under fallen
trees, between roots or stems of emergent plants, etc.)
where the flow rate is moderate (Machidori and Kato
1984; Kato 1991). These 0+ juveniles then gradually
move to deeper areas, such as the edge or center of the
flow in the pools (Kiso 1995). The 0+ juveniles, after
emergence, are called “parr”, since these fish display
large black round spots (i.e., parr marks) on both sides
of their body. The parr mark is considered to allow
them to be better camouflaged against the background
of the rivers, that is, stream beds, rocks, and fallen trees.
The 0+ masu salmon parr mainly forages on drift
aquatic insects such as larval Ephemeroptera,
Trichoptera, Plecoptera, Chironomidae, and occasionally forages on fallen terrestrial insects (Machidori and
Kato 1984; Kato 1991; Kiso 1995). In upper rivers,
however, distributions of drifting aquatic and terrestrial insects are generally stratified among the different spaces. This suggests that accessibility to prey items
differs considerably among individual 0+ parr. For
these reasons, 0+ parr compete frequently with their
conspecifics as well as other species (i.e., Japanese
charr (Salvelinus fontinalis)) with the same dietary
habits for occupying focal foraging areas (i.e., territory) in which they can access substantial drifting prey
items (Nakano et al. 1990; Nakano and FurukawaTanaka 1994; Nakano 1995). Moreover, to achieve and
maintain their focal foraging areas, 0+ parr frequently
exhibit territorial aggressiveness against other individuals, and some of the territorial 0+ parr establish
themselves to be the dominant fish in each focal for-
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
33
Fig. 4. Changes in body length (BL), body weight (BW), condition factor (CF), gonad somatic index (GSI), plasma levels of
testosterone (T), 11-ketotestosterone (11-KT), estradiol-17 β (E 2), progesterone (P), 17 α -progesterone (17α -P), 17,20 βdihydroxy-4-pregnene-3-one (DHP), and pituitary hormone luteinizing hormone (LH) in male and female masu salmon. Differences in mean plasma hormone levels among experimental groups were analyzed by one-way analysis of variance (ANOVA)
followed by Scheffe’s F-test. * and *** indicates significant difference at P < 0.05 and P < 0.001, respectively. Reprinted
from Comp. Biochem. Physiol. Part B, 129, Munakata et al., The involvement of sex steroid hormones in downstream and
upstream migratory behavior of masu salmon, 661–669,  2001a, with permission from Elsevier.
aging space during autumn (Machidori and Kato 1984;
Munakata et al. 2000b). On the other hand, juveniles
that could not occupy the focal foraging areas become
the subordinates in the social order.
behavior”, result in the augmentation for distribution
of masu salmon into broader habitats within the rivers.
2-4. Differentiation in non-migratory forms
2-3A. Wintering downstream movement
During the same period (autumn through winter), a
significant proportion of 0+ masu salmon, including
non-migrants and migrants, tend to move from their
former habitat to the downstream areas (Machidori and
Kato 1984; Kato 1991), which is possibly induced by
decreased temperature (Giannico and Hinch 2003).
These movements, which are called “wintering
In juvenile masu salmon, both non-migratory (i.e.,
stream resident) and migratory (i.e., smolt) forms commonly originate from dominant and subordinate parr,
respectively, and both types can be discriminated by
their morphologic characteristics after 0+ summer
(Machidori and Kato 1984; Kiso and Matsumiya 1992;
Kiso 1995). In regard to the non-migratory forms, the
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
34
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
0+ dominant precocious males regularly become the
non-migrants that live continuously in their natal rivers. In 0+ precocious males, standard body length (BL),
body weight (BW), depth of body, and testes (gonad
weight (GW)) become larger, and the body color becomes darker than that of 0+ immature parr during
summer, and these fish subsequently attend to spawning activities in the following autumn (Kato 1991; Kiso
1995). After spawning, testes in 1+ (former 0+) precocious males regress from winter through spring
(Munakata et al. 2001a; Fig. 4). However, the size of
the testes, expressed by the gonad somatic index (GSI:
100 x GW/BW), in 1+ precocious males is still larger
than those of immature male parr (Munakata et al.
2001a; Fig. 4). The 1+ precocious males then begin
the maturation process again after spring commences,
while most of 1+ immature migrants exhibit downstream migratory behavior following smoltification.
2-5. Smoltification in subordinate juveniles
In contrast to the dominant precocious male nonmigrants, most of 0+ subordinates live as immature parr
from summer through autumn (Machidori and Kato
1984; Kiso 1990, 1995). In the following winter, some
of the 1+ immature fish initiate smoltification, which
is completed in the following spring, before the downstream migration begins.
Smoltification regularly consists of a series of morphological, physiological, and behavioral changes,
which enable 1+ (former 0+) juveniles to adapt to marine environments (Hoar 1976, 1988; Boeuf 1994;
Boeuf et al. 1994; Iwata 1995, 1996; McCormick
2001). In a short span of time, future smolts start to
display a silvery body color, and black dorsal and dorsal fin tips, which camouflage them against the colors
of the ocean waters (Quinn 2005), similar to other
marine migratory fish such as sardines (Engraulis spp.)
and saury (Cololabis spp.). The changes in the body
colors are supported fundamentally by the accumulation of granules of pigments such as guanine and
melanophores on the abdominal and dorsal skins, respectively (Hoar 1988). Masu salmon smolts also display lower condition factor (CF: 100 x BW/BL3) when
compared with those values before starting
smoltification (Aida et al. 1984; Ikuta et al. 1985, 1987;
Munakata et al. 2000b, 2001a). Their osmoregulatory
ability is modulated by hormonal factors, such as
growth hormone (GH) and cortisol (Hirano 1991;
McCormick 2001).
Physiological changes, such as an increase in gill
Na+–K+–ATPase activity allow the smolts to adapt to
salt water conditions (Boeuf et al. 1989; Iwata et al.
1990).
With regard to behavior, Iwata (1995) suggested that
1+ masu salmon smolts cease to exhibit aggressive
behaviors, which support their territorial aggressive-
ness prior to the smolting period, and these smolts subsequently exhibit a tendency to gather in open spaces
even during the daytime hours. According to Hutchison
and Iwata (1998), such behavioral changes are caused
by the increase of plasma thyroxine, which is considered to be one of the smolt-inducing factors. These
behavioral changes seemed to convert the “territorial
behavior” into “schooling behavior” in 1+ smolts, as
the peak period of their smoltification approached.
Subsequently, most 1+ smolts begin downstream swimming behavior throughout the evening (Munakata et
al. 2000b), during and after rainfall (Yamauchi et al.
1984, 1985), and snow runoff, etc. in favorable periods during the spring (Iwata 1995, 1996).
In summary, two phenotypes (forms) of masu salmon
diverge as juveniles at the age of 1+. The precocious
males retain many characteristics of parr, despite undergoing sexual maturation (Utoh 1976, 1977;
Machidori and Kato 1984). In contrast, 1+ smolts experience drastic morphological, physiological, and
behavioral changes during smoltification (Iwata 1995,
1996). Based on these observations, one might argue
that the precocious males are more similar to their fluvial ancestors than smolts. In the next section, we will
discuss how sex hormones are involved in the differentiation between the two forms and identify the likely
factors regulating these processes.
2-6. Inhibitory roles of sex steroid hormones in
the smoltification
In masu salmon, it was previously found that dissection of the testes (castration) of 0+ precocious males,
the non-migrants, during autumn induced
smoltification in the following (1+) spring, while shamoperated fish remained as precocious males (Aida et
al. 1984). Plasma androgen (T + 11-KT) levels (0.12
ng/ml) of 1+ castrated precocious males became lower
than those in sham-operated precocious males (1 ng/
ml) after surgery. If a portion of the testis was left in
the abdominal cavity, those males did not smoltify, just
as the sham-operated ones did not. Accordingly, the
findings indicate that sexual maturation, more specifically, sex steroid hormones released from the gonads
inhibited the occurrence of smoltification in the precocious males. Ikuta et al. (1985, 1987) later confirmed
that treatment (oral administration) with exogenous sex
steroid hormones, such as methyletestosterone (MT),
T, 11-KT, and E2 in 1+ masu salmon smolts in winter
through spring impaired some part of the changes associated with smoltification, such as silvery body color,
decrease in CF, seawater tolerance capacity, and plasma
rises in thyroid hormones. On the other hand, synthetic
steroid, 5 α -dihydrotestosterone (DHT) which has
stronger androgenic effects than T did not exhibit significant inhibitory effects (Ikuta et al. 1987).
The inhibitory effects of sex steroid hormones on the
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
smoltification are also confirmed in other Pacific
salmon such as amago salmon (Miwa and Inui 1986).
Therefore, it is further hypothesized that inhibitory
regulation of smoltification by sex steroid hormones
is a common phenomena in a number of Pacific salmon.
35
Current
Upper
pond
Net traps
2-7. Seasonal changes in plasma sex hormone levels
After the completion of smoltification, most masu
and other Pacific salmon smolts subsequently migrate
downstream to the sea (Quinn 2005; Munakata and
Kobayashi 2010). Therefore, by logical extension, not
only the smoltification, but also the downstream migratory behavior is repressed by some of the sex steroid hormones. To investigate which sex steroid hormones are indeed involved in the occurrence of
smoltification and downstream swimming behavior,
seasonal changes in the plasma levels of sex steroid
hormones and pituitary hormone (luteinizing hormone
(LH)) were investigated in masu salmon by
radioimmunoassays (RIAs), during the period of
smoltification and downstream migration (Munakata
et al. 2001a; Fig. 4).
2-7A. Males
In 0+ and 1+ males, precocious males (representative non-migrants) appeared and were distinguishable
from the immature males of the same age by their larger
BL, BW, CF, and GSI values and plasma sex steroid
hormone levels (Fig. 4). In 1+ precocious males, values of GSI and plasma levels of T, 11-KT, and 17,20βdihydroxy-4-pregnene-3-one (DHP) significantly increased from May through September, overlapping the
period of the smoltification and downstream migration,
while 1+ immature males (smolt and parr) did not exhibit such phenomena (Fig. 4). On the other hand,
plasma levels of progesterone (P), 17α-progesterone
(17 α-P), and LH did not show significant increases in
1+ precocious males.
In 1+ precocious males, it was noteworthy that
plasma levels of T began to increase and attained peak
levels earlier than did 11-KT and DHP (Fig. 4). Moreover, T maintained high plasma levels extensively from
March through September, overlapping the period of
their seaward migration.
2-7B. Females
In females, precocious maturation rarely occurred
among 0+ and 1+ fish in hatchery-raised strains
(Shiribetsu River strain, introduced from Hokkaido in
1980) that were used in our studies (Munakata et al.
2000b, 2001a, 2001b, 2007, 2012a). Consequently, a
major part of 1+ immature females exhibited low CF,
GSI, and plasma sex hormone levels (Fig. 4).
The females regularly commence apparent sexual
maturation at the age of 2+ during the spring through
Fishway
Lower
pond
Separated
Area
Current
Fig. 5. Schematic drawing of experimental raceway. In order to study the roles of sex steroid hormones in downstream
behavior (negative rheotaxis), the fish were transferred into
the upper pond (2 × 4 × 0.5 m) of a two-step raceway connected to the lower pond (2 × 8 × 0.5 m) through a fishway
(20 cm in diameter by 4 m in length made of a polyvinyl
chloride (PVC) half-cut pipe (Munakata et al. 2000b). Spring
water was supplied into the upper pond. Flow rate (volume)
and velocity of the water in the fishway ranged between
10–20 l/s and 70–85 cm/s, respectively. Water temperature
fluctuated between 9–10°C. At the downstream edge of the
fishway in the lower pond, a net trap (2 × 0.7 × 0.7 m) was
placed to capture fish that moved down from the upper pond.
An individual experimental fish was identified as a downstream migrant if it moved from the upper pond into the net
trap in the lower pond. In order to investigate the effects of
sex steroid hormones on the occurrence of upstream
behavior, the experimental fish and net trap were transferred
into the lower and upper pond, respectively. The frequency
of downstream or upstream migrations is expressed as a
percentage of the initial fish numbers. Reprinted with permission from Fish. Sci., 78, Munakata et al., Involvement
of sex steroids, luteinizing hormone and thyroid hormones
in upstream and downstream migratory behaviors in landlocked sockeye salmon Oncorhynchus nerka, 81–90, Fig.
1,  2012b, The Japanese Society of Fisheries Science.
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
LH
36
Fig. 7. (a) Frequency of migrants and non-migrants, plasma
levels of (b) testosterone (T), (c) pituitary contents of luteinizing hormone (LH), (d) plasma levels of LH, (e) thyroxine (T 4), and (f) triiodothyronine (T3) in control and T 500
µg-treated 1+ masu salmon smolts. Numbers above columns
in (a) indicate the number of migrants and non-migrants.
Differences in the frequency of downstream behavior from
the control group were analyzed by the χ 2 -test, using
StatView version 4.5 software (Abacus Concepts, Inc., California, USA). ** indicates a significant difference at P <
0.01 from the control group. Differences in mean plasma
and pituitary hormone levels among experimental groups
were analyzed by one-way analysis of variance (ANOVA)
followed by Fisher’s PLSD. Differing letters represent significant differences at P < 0.05 among all groups. Reprinted
with permission from Zoological Science, 17, Munakata et
al., Inhibitory effects of testosterone on downstream migratory behavior in masu salmon, Oncorhynchus masou, 863–
870, Fig. 1,  2000b, Zoological Society of Japan.
levels of (b) testosterone (T), (c) pituitary contents of luteinizing hormone (LH), (d) plasma levels of LH, (e) thyroxine (T 4), and (f) triiodothyronine (T 3) in controls, T 5 µg, T
50 µg, T 500 µg-treated smolts and precociously mature male
1+ masu salmon. Numbers above columns in (a) indicate
the number of migrants and non-migrants. Differences in
the frequency of downstream behavior from the control group
were analyzed by the χ2-test, using StatView version 4.5
software (Abacus Concepts, Inc., California, USA). * indicates a significant difference at P < 0.05 from the control
group. Differences in mean plasma and pituitary hormone
levels among experimental groups were analyzed by oneway analysis of variance (ANOVA) followed by Fisher’s
PLSD. Differing letters represent significant differences at
P < 0.05 among all groups. Reprinted with permission from
Zoological Science, 17, Munakata et al., Inhibitory effects
of testosterone on downstream migratory behavior in masu
salmon, Oncorhynchus masou, 863–870, Fig. 2,  2000b,
Zoological Society of Japan.
summer period, which coincides with the timing of
their upstream migration (Fig. 4). Their GSI and plasma
levels of T, E2, 17α-P, DHP, and LH increased in May
through October. In addition, most females used in the
investigation ovulated around October, similar to the
wild populations (Kiso 1995). In 2+ mature females,
plasma levels of T and E2 began to increase and at-
tained peak levels earlier than did 17α-P, DHP, and
LH (Fig. 4). Moreover, T maintained high plasma levels during a broader period than other sex steroid hormones.
Therefore, in males and females, it seems likely that
sex hormones, especially some of the sex steroid hormones, are important factors that regulate (inhibit) the
Fig. 6. (a) Frequency of migrants and non-migrants, plasma
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
37
display of downstream swimming behavior as well as
smoltification. Furthermore, it was indicated that the
sex steroid hormone T commonly increased earlier and
more broadly than did other sex steroid hormones in
both sexes (Fig. 4). In general, T is considered a reservoir substance for impending conversion to other sex
steroid hormones, such as 11-KT, and E2 (male), and
E2 (female) (Kagawa et al. 1982a, b). In masu salmon,
however, it was also hypothesized that T is one of the
more important sex steroid hormones that effectively
repress the occurrence of smoltification and the following downstream swimming behavior. This hypothesis was tested in the next set of studies which were
conducted in an artificial raceway system (Fig. 5). T
and other relevant sex steroid hormones were included
in these experiments.
2-8. Inhibitory roles of sex steroid hormones in
the downstream swimming behavior in masu
salmon
I investigated the effects of treatments with exogenous sex steroid hormones, such as T, 11-KT, E2, and
DHP, on the occurrence of downstream swimming
behavior, in 1+ masu salmon smolts, held in the experimental raceway system (Fig. 5).
2-8A. Roles of T in the downstream swimming
behavior
In the raceway, one experiment showed that 89.5%
(17 of 19 fish) of the control 1+ masu salmon smolts
swam from the upper pond to the lower pond through
a fishway (Munakata et al. 2000b; Fig. 6). This contrasts with the behavior of 1+ smolts into which a T
500 µg/fish via a Silastic tube capsule (Dow Corning
Corp.: outer diameter 1.95 mm, inner diameter 1.47
mm, length 20 mm) was inserted. These 1+ smolts displayed high plasma T levels (Fig. 6). Under these circumstances, the frequency of downstream swimming
behavior in the T 500 µg/fish-treated group was 31.8%
(7 of 22 fish). In the non-migrants of the T-treated fish,
plasma levels of T were higher than those in migrants,
suggesting that higher plasma T levels are important
for the suppression of downstream swimming behavior.
Since Ikuta et al. (1987) demonstrated that T inhibited
natural smoltification, it is further hypothesized that T
impairs not only downstream swimming behavior but
also seawater preference and schooling behavior in the
T-treated 1+ smolts.
2-8B. Effects of T doses on the occurrence of downstream swimming behavior
It was previously demonstrated that T-treatments significantly inhibited the occurrence of downstream
swimming behavior in 1+ smolts in a dose dependent
manner (Munakata et al. 2000b; Fig. 7). The frequency
of downstream swimming behavior in control, T5 µg,
Fig. 8. (a) Frequency of migrants and non-migrants, plasma
levels of (b) testosterone (T), (c) estradiol-17β (E2), (d) 11ketotestosterone (11-KT), (e) 17,20β-dihydroxy-4-pregnene3-one (DHP), (f) thyroxine (T4), and (g) triiodothyronine (T3)
in controls, T, E2, 11-KT, and DHP 500 µg-treated 1+ masu
salmon smolts. Numbers above columns in (a) indicate the
number of migrants and non-migrants. Differences in the
frequency of downstream behavior from the control group
were analyzed by the χ 2-test, using StatView version 4.5
software (Abacus Concepts, Inc., California, USA). * and
*** indicate significant differences at P < 0.05 and P < 0.001,
respectively, from the control group. Differences in mean
plasma and hormone levels among experimental groups were
analyzed by one-way analysis of variance (ANOVA) followed by Fisher’s PLSD. Differing letters represent significant differences at P < 0.05 among all groups. Reprinted
from Comp. Biochem. Physiol. Part B, 129, Munakata et al.,
The involvement of sex steroid hormones in downstream and
upstream migratory behavior of masu salmon, 661–669, 
2001a, with permission from Elsevier.
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
38
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
Fig. 9. (a) Frequency of migrants and non-migrants, plasma
levels of (b) testosterone (T), (c) thyroxine (T4), and (d)
triiodothyronine (T3) in control and T 500 µg-treated 1+ masu
salmon smolts. Numbers above columns in (a) indicate the
number of migrants and non-migrants. Differences in mean
plasma hormone levels among experimental groups were
analyzed by one-way analysis of variance (ANOVA) followed by Fisher’s PLSD. * indicates a significant difference
at P < 0.05 from migrants. Reprinted with permission from
Zoological Science, 17, Munakata et al., Inhibitory effects
of testosterone on downstream migratory behavior in masu
salmon, Oncorhynchus masou, 863–870, Fig. 3,  2000b,
Zoological Society of Japan.
T50 µg, T500 µ g/fish-treated 1+ smolts, and 1+ precocious male groups were 21.3, 18.2, 6.9, 4.5, and 0%,
respectively. Plasma T levels and pituitary LH contents
in the T500 µg/fish-treated smolt group were highest
among all experimental groups (Fig. 7).
In this study, on the other hand, none of the 1+ precocious males exhibited the downstream swimming
behavior in the artificial raceway, whereas their plasma
T levels were lower than those in the T500 µg/fishtreated smolt (Fig. 7). Such phenomena are consistent
with the findings that most of the 1+ precocious males
stay in their natal rivers even though their plasma T
levels are not very high.
2-8C. Roles of sex steroid hormones other than T in
the downstream swimming behavior
In maturing masu salmon, not only T but also 11-KT
(males) and E2 (females) levels increased coincident
with the period of downstream migration (Munakata
et al. 2001a; Fig. 4). On the other hand, plasma DHP
levels increased only during the spawning period in
autumn in both sexes. To test the potential roles of sex
steroid hormones other than T, the effects of treatments
of T, E2, 11-KT, and DHP (500 µg/fish) on the occurrence of downstream swimming behavior were investigated (Munakata et al. 2001a; Fig. 8).
It was found that not only T but also E 2 and 11-KT
500 µg/fish-treatments resulted in an elevation of each
sex steroid hormone and inhibited the occurrence of
downstream swimming behavior in 1+ smolts (Fig. 8).
Interestingly, DHP 500 µg/fish-treatments did not inhibit the occurrence of downstream swimming
behavior.
In the raceway system, it was also demonstrated that
all of the forty 1+ masu salmon smolts that were transferred into the upper pond performed downstream
swimming behavior within a week (Munakata et al.
2000b; Fig. 9, left columns). By comparison, 60% of
T500 µg/fish-treated smolts remained in the upper pond
during the same period (Fig. 9, right columns). These
phenomena suggest that most 1+ smolts spontaneously
exhibit negative rheophilic behavior when flowing
water is present, or that some environmental factors
are involved in the induction of downstream swimming
behavior. Since 1+ smolts seemed to swim downstream
spontaneously, it is also hypothesized that T directly
inhibits the downstream activity, or inhibits the receptiveness to some environmental factors which induce
the downstream swimming behavior.
2-8D. Effects of intra-specific interactions on the
downstream swimming behavior
In one of the previous investigations, 1+ precocious
male masu salmon, transferred into the upper pond of
the raceway, frequently displayed aggressive behaviors
towards 1+ smolts (Munakata et al. 2000b, 2012a).
Therefore, another acceptable explanation is that the
downstream swimming behavior is induced partly by
some socio-environmental factors, such as intraspecific interactions from 1+ precocious males.
2-8E. Effects of dosing period of T on the downstream swimming behavior
The dosing period was normally approximately 2
weeks before sex steroid hormone-treated 1+ masu
salmon smolts were transferred into the upper pond of
the raceway (Munakata et al. 2000b, 2001a). Consequently, some of the fish in the T500 µg/fish-treated
1+ smolts exhibited downstream swimming behavior
even when their average plasma T level (13.7 ng/ml)
was higher than those of 1+ precocious males (3.9 ng/
ml) (Fig. 7). One possible explanation is that multiple
sex steroid hormones are necessary to impede downstream swimming behavior. Evidence supporting this
supposition is that in 1+ precocious males, plasma levels of not only T but also 11-KT significantly increased
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
(Fig. 4). Moreover, it was demonstrated that treatment
with T, E2, and 11-KT 500 µg/fish significantly inhibited the occurrence of downstream swimming behavior
in 1+ smolts (Fig. 8).
However, another acceptable explanation is that a
continuous release of a sex steroid hormone into the
plasma can obstruct the downstream swimming
behavior completely. As shown previously (see Subsection 2-4 in detail), 1+ precocious males undergo
sexual maturation during the summer of 0+ year-oldlife, a half year prior to the downstream migratory period in the river, although their GSI values and plasma
Frequency of
fish (%)
100
Migrants
Non-migrants
(a)
*
50
6
56
37
31
20
1
0
50
d
(b)
T (ng/ml)
cd
25
bc
0
Pituitary LH
(ng/pituitary)
50
ab
(c)
b
40
3
ab
20
2
a
a
a
1
0
LH (ng/ml)
10
Aside from masu salmon, we have discovered that
T500 µ g/fish-treatments significantly inhibited the
occurrence of downstream swimming behavior in 1+
land-locked sockeye salmon (O. nerka) smolts by use
of the same raceway (Munakata et al. 2012b, Fig. 10).
Furthermore, inhibitory effects of sex steroid hormones upon downstream swimming behavior were also
found in Atlantic salmon (Salmo salar) smolts
(Berglund et al. 1994). In these smolts, treatment with
11-ketoandrostendione (11-KA) via implantation of
Silastic tube capsules inhibited the downstream swimming behavioral activity occurring along the current
in the circular round tank. This suggests that inhibitory regulatory mechanisms of downstream swimming
behavior by sex steroid hormones are inhered in some
Pacific and Atlantic salmon.
3. Roles of sex hormones in the upstream swimming and spawning behaviors in masu salmon
and other salmonids
During autumn, most 2+ mature masu salmon
0
Fig. 10. (a) Frequency of migrants and non-migrants, plasma
5
b
a
20
T4 (ng/ml)
2-9. Inhibitory roles of sex steroid hormones in
the downstream swimming behavior in other
Pacific and Atlantic salmon
(d)
b
ab
ab ab
0
(e)
15
c
bc
10
5
a
b
a
a
0
20
T3 (ng/ml)
5
4
b
30
10
androgen levels largely decreased during winter (Aida
et al. 1984; Munakata et al. 2000b, 2001a). Considering these factors, it is suggested that chronic release
of sex steroid hormones into the plasma is an important factor in the inhibitory regulation of downstream
swimming behavior.
a
Pituitary LH
( g/pituitary)
a
39
(f)
15
10
5
ab
ab
ab
ab b
a
0
Control
T-treated
Fig. 10.
Precocious
male
levels of (b) testosterone (T), (c) pituitary contents of luteinizing hormone (LH), (d) plasma levels of LH, (e) thyroxine (T4), and (f) triiodothyronine (T3) in control and T 500
µg-treated smolts, and precociously mature male 1+ sockeye
salmon. In Fig. 10c, unit of Y axis in the control group was
ng/pituitary, while those of T-treated and precocious male
groups was µg/pituitary. Numbers above columns in (a) indicate the number of migrants and non-migrants. Differences
in the frequency of downstream behavior from the control
group were analyzed by the χ2-test, using StatView version
4.5 software (Abacus Concepts, Inc., California, USA).
* indicates a significant difference at P < 0.05 from the control group. Differences in mean plasma and pituitary hormone levels among experimental groups were analyzed by
one-way analysis of variance (ANOVA) followed by Fisher’s PLSD. Differing letters represent significant differences
at P < 0.05 among all groups. Reprinted with permission
from Fish. Sci., 78, Munakata et al., Involvement of sex steroids, luteinizing hormone and thyroid hormones in upstream
and downstream migratory behaviors in land-locked sockeye
salmon Oncorhynchus nerka, 81–90, Fig. 3,  2012b, The
Japanese Society of Fisheries Science.
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
40
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
sequentially migrate upstream (i.e., upstream swimming behavior) from the sea (or lakes), home to their
natal rivers and then spawn in the upper reaches of the
catchment basin (Machidori and Kato 1984; Kato 1991;
Kiso 1995). Also, during this period, nonmigratory, precocious males swim upstream from the
mid-to upper-river reaches and consequently spawn
with 2+ migrants (see Fig. 3). Since most of these fish
exhibit signs of sexual maturation while engaged in
these activities, it appears likely that sexual maturation induces or regulates these behaviors. In this section, an overview of the lifecycle of migrants and nonmigrants of masu salmon during the periods of homing and upstream migration through spawning will be
presented with regard to previous investigations of the
stimulatory effects of sex steroid hormones on the occurrence of upstream swimming and spawning
behaviors (Munakata et al. 2001a, 2001b, 2002, 2012a).
3-1. Upstream migrator y behavior in masu
salmon
The feeding migration of 1+ masu salmon smolts in
the sea occurs between March and May, after which
the major part of the run has entered into either the
Pacific Ocean or the Sea of Japan (Machidori and Kato
1984). Most of these smolts are thought to migrate into
areas between the Sea of Japan near Hokkaido Island
and the Sea of Okhotsk around June. However, it is
also thought that a small number of 1+ masu salmon
smolts migrate to coastal areas, such as off the Sanriku
coast on the Pacific Ocean side of northern Honshu
(Kiso 1995). As mentioned in Section 4, such short
distance migratory forms are considered to be “coastal
migrants” (see Subsection 5-2 in detail). The Sea of
Okhotsk is the summer-late autumn feeding ground for
most of the 1+ smolts, where they forage on fish, squid,
Amphipods, Euphausiids, Decapods, Copepods, and a
small number of terrestrial insects (Machidori and Kato
1984; Kato 1991). During this period of time, most
masu salmon reach 50 to 60 cm in BL. During winter
through spring when the smolt reach the age of 2+,
most will head southward towards their spawning
ground in natal rivers (i.e., homing migration, upstream
migration) (Machidori and Kato 1984; Kato 1991).
Values of GSI and plasma levels of sex steroid hormones start to increase in both sexes (Munakata et al.
2001a; Fig. 4). Hence, there is a correlation between
the initiation of sexual maturation and the occurrence
of homing and upstream migratory behaviors.
In general, most 2+ smolts migrate into their natal
rivers and subsequently show upstream swimming
behavior during mid spring through early summer.
According to information provided by the sports fishing industry, however, it seems that some 2+ masu
salmon called the “early run” migrate into their natal
rivers (e.g., Kitakami, Mogami, Akagawa, and Omono
Rivers) in northern Honshu during late winter through
early spring. Also, some of the 2+ smolt migrants,
members of the so-called “late run” migrate into small
rivers (i.e., Kesen, Hirose, and Natori Rivers) along
the Sanriku coast of northeastern Honshu, just before
the spawning period (Machidori and Kato 1984; Kiso
1995; Munakata et al. unpublished data). This illustrates that there are variations in timing when the 2+
smolts return to their natal rivers. Moreover, it is also
hypothesized that some masu salmon smolts can modulate their osmoregulatory ability coincident with their
entry into the natal rivers.
On reaching their natal streams, a significant proportion of masu salmon regularly inhabit deep areas
of the rivers, such as pools and the thalweg (center of
the flow), usually located downstream from their autumn spawning sites. Because 2+ migrants are now
larger (50 to 60 cm in BL), it is probable that they stay
in deep areas to hide from potential predators. Furthermore, water temperatures in deeper areas may be modulated and stabilized by spring water upwelling from
the river beds. During late summer through autumn,
most of the 2+ migrants start to move upstream again,
toward their spawning areas (Kato 1991; Kiso 1995;
Munakata and Miura, unpublished data). It is thus assumed that the upstream swimming behavior of 2+
migrants can be regularly divided into two steps: 1)
movement from the mouth of the river to the areas in
which 2+ fish spend the summer, and 2) movement
from the latter areas to their spawning areas. It seems
that the upstream migratory behavior of the “late run”,
which is generally found in small streams, coincides
with the latter upstream migratory pattern. Most 2+
migrants that reach their spawning sites exhibit high
GSI values (Munakata et al. 2001a, 2012a), and subsequently the 2+ males spermiate and 2+ females ovulate (Munakata and Kobayashi 2010).
3-2. Feeding of 2+ masu salmon migrants during
the upstream migration
As is typical for semelparous Pacific salmonids, adult
masu salmon are thought not to feed after returning to
their natal rivers. According to Sano (1947), however,
some 2+ masu salmon smolts, which are considered
the “early run”, in Nishibetsu and Shibetsu Rivers in
Hokkaido, occasionally feed. In 2010, it was also discovered that a 2+ masu salmon male migrant caught in
the Hirose River, Miyagi Prefecture, that enters Sendai
Bay near the Sanriku coast had consumed a number of
larval aquatic insects (Munakata and Miura, unpublished data). Interestingly, sport fishermen (i.e., lure,
fly, and bait fishing) consistently catch 2+ “early run”
smolts in larger rivers, such as the Kitakami, Mogami,
Akagawa, Omono Rivers in northern Honshu in late
winter through spring, while some fishermen also fish
the 2+ masu salon smolts via bait fishing nearshores
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
of Hokkaido coasts.
Thus there are conflicting reports regarding the feeding of the 2+ masu salmon migrants in the rivers. Since
most of the 2+ migrants are considered not to feed
during summer through autumn, though they seem to
feed during winter through spring in both the rivers
and offshore sea, one possible hypothesis is that the
feeding activity of 2+ migrants is determined by their
maturity, but not by the entry into the rivers.
3-3. Lifec ycle of non-migratory precocious males
Precocious male non-migrants generally maintain
their territories during 0+ winter through 1+ summer
in the upper and middle reaches of their natal rivers
(Machidori and Kato 1984; Kiso 1995). Subsequently,
the 1+ precocious males begin to become sexually competent, resulting in high plasma levels of T and 11-KT
after summer (see Fig. 4). The 1+ precocious males
then exhibit upstream movements during late summer
through autumn the same as 2+ migrants (Kiso 1995;
Munakata et al. 2001b).
In contrast to the 2+ migratory smolts, most 1+ precocious males continue to feed on insects or small fish,
prior to and during the spawning period (Munakata et
al. unpublished data), indicating that the changes in
feeding activity do not depend on the maturity of the
precocious males. After the occurrence of upstream
movements, these fish attend to spawning together with
2+ male and female migrants. The precocious male
non-migrants seem to repeat the same phenomena during the ages of 0+ through 2+ (Kiso 1995).
41
and Kobayashi 2010).
Recently, it was discovered that 2+ mature female
masu salmon release a sex pheromone, L-kynurenine,
which attracts sexually mature males (Yambe et al.
2003, 2006). The urine from 2+ mature females attracts
and elicits the male spawning behaviors, such as attending behaviors (see Figs. 17, 18). The timing of its
production in the females clearly indicates that this sex
pheromone could be a signal to non-specific males indicating sexual maturity, location of the redd, and receptiveness of 2+ females to non-specific males.
After sexually mature 2+ male migrants arrive at the
spawning grounds, these males regularly swim around
the 2+ digging females and exhibit a series of male
spawning behaviors, such as attending and quivering,
towards the digging female (Munakata and Kobayashi
2010) (see also Fig. 18). Additionally, 2+ males sometimes exhibit aggressive behaviors towards other
male(s) of the same species, to prevent the antagonistic males from showing courtship behavior to the digging female. After the redd is constructed by the female, both the female and male crouch (i.e., crouching
behavior) on the accomplished redd, and release eggs
(oviposition) and sperm (ejaculation), respectively
(Munakata and Kobayashi 2010). Thereafter, the female covers the redd (i.e., covering behavior) with
small stones and pebbles by using its caudal fin in a
similar manner to the digging behavior. Most of 2+
females and males will repeat such spawning behaviors
several times over a few weeks until most ovulated
oocytes are released (Machidori and Kato 1984).
3-4. Spawning behaviors in 2+ migrants
3-5. Spawning behaviors in 1+ precocious male
non-migrants
Spawning of masu salmon is observed in natal rivers approximately from August through October
(Machidori and Kato 1984; Kiso 1995). The peak period of spawning is generally earlier in northern regions (i.e., Hokkaido) than in southern ones (i.e.,
Honshu and Kyushu).
During the spawning period, 2+ female migrants start
to swim above specific river beds where various sizes
of stones and pebbles are located and oxygen rich water indwells, the same as coho salmon (O. kisutch)
(Sandercock 1991) (note that pink salmon spawn on
river beds where spring water upwells, Heard 1991).
Above such a river bed, a 2+ female digs up (i.e., digging behavior) the pebbles and stones to make a spawning bed (i.e., redd: 170 × 80 cm in length and width,
with a depth of 12 to 45 cm) by using her body, especially the tail (caudal fin), digging at intervals of 1 to
5 min. While digging, the 2+ female frequently checks
the redd’s shape (i.e., depth) and substrates by using
mainly the pectoral fins (i.e., probing behavior). During and after digging, most 2+ females ovulate to prepare for the oviposition (i.e., egg release) (Munakata
Spawning behaviors of precocious male nonmigrants are generally different from those in 2+ male
migrants (Munakata and Kobayashi 2010). Since the
body size of the precocious male non-migrants (10 to
30 cm in BL) is relatively smaller than that of 2+ male
migrants (Utoh 1976, 1977), most 0+, 1+, and 2+ precocious males spawn “as sneakers” (Munakata and
Kobayashi 2010). Briefly, the sneaker precocious male
does not display the specific attending and quivering
behaviors towards the nest digging 2+ female. Instead,
these males conceal their bodies behind obstacles, such
as large rocks, fallen trees, etc., while larger 2+ females and males undertake a series of spawning (pairing) behaviors (Munakata et al. unpublished data).
Also, it was observed that some precocious males swim
posteriorly to the redd, while 2+ females display digging behavior. These precocious males are called “accessory males”. During the spawning period, dominant
2+ male migrants exhibit aggressive behaviors towards
other fish including these precocious males. About the
time when the 2+ females and males release eggs and
sperm, the 0+, 1+, or 2+ precocious male sneaker(s) or
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
42
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
accessory males swim onto the redd and immediately
release their sperm on the released eggs.
3-6. Spawning behaviors in female non-migrants
Male and female non-migrant masu salmon other
than the precocious fish have been reported in some
rivers (Kiso 1995). The proportions of these types of
non-migrants generally increases towards the southern regions (i.e., Honshu and Kyushu), the same as
precocious males. These fish regularly exhibit low GSI
values compared with precocious male non-migrants,
and their sex steroid hormones remain at low levels.
However, their growth rates were relatively higher than
those of other immature fish, including the future
smolts, during the age of 0+ through 1+ (Kiso 1995).
These non-migrants regularly mature and spawn up to
twice, during the 1+ and 2+ autumn. Thus 2+ masu
salmon spawners are comprised of larger migrants,
smaller precocious males and other 2+ parr nonmigrants in the rivers. In general, the spawning
behaviors of the female and male non-migrants are
similar to those of 2+ migrants (Munakata et al. unpublished data).
3-7. Changes in plasma sex hormone levels during the upstream migratory and spawning
periods
Thus in masu salmon, the appearance of homing,
upstream migratory, and spawning behaviors is closely
related to the progress of sexual maturation and an increase in sex hormone levels. To understand which
hormonal factors control the occurrence of upstream
swimming behaviors and subsequent male and female
spawning behaviors, it is required to measure plasma
levels of sex steroid hormones and LH before, during,
and after the behavioral patterns become manifest. This
is covered in the following sections.
3-7A. Males
In 2+ males, values of GSI and plasma levels of T,
11-KT, and DHP increased during the periods of homing migration through spawning (Munakata et al.
2001a; Fig. 4). In 2+ males, moreover, it was noticed
that plasma levels of T increased earlier than did 11KT and DHP, and T retained higher plasma levels extensively during May through September.
Regarding 1+ precocious male non-migrants, such
plasma sex steroid hormone elevations coincide with
the period when these fish remain in their natal rivers,
display upstream movement toward spawning areas,
and spawning behaviors (Fig. 4).
3-7B. Females
In 2+ female masu salmon, values of GSI and plasma
levels of T, E 2, 17α-P, DHP, and LH increased during
spring through autumn, overlapping the period of their
homing, upstream migration, and spawning (Fig. 4).
Among these sex hormones, plasma T and E2 levels
began to increase after May and attained peak levels
earlier than did other sex hormones, such as 17α-P,
DHP, and LH.
3-8. Changes in sex steroid hormone levels before
and after the occurrence of upstream swimming behavior in masu salmon
3-8A. Males
We investigated the changes in the plasma levels of
sex steroid hormones (T, E2, 11-KT, and DHP) in 2+
masu salmon during the following temporal phases:
before the onset of upstream swimming behavior (initial sampling: before transfer into the lower pond of
the two-step raceway), during the migratory period
(sampled from upstream migrants), and after upstream
activity ceased (sampled from non-migrants remaining in the lower pond of the raceway) (Munakata et al.
2012a; Table 1). It was found that all of the 15 2+
males continued to spermiate before and during the
onset of upstream movements, indicating that the fish
spermiate during the upstream migratory phase. Plasma
levels of T, 11-KT, and DHP were considerably higher
during September (Table 1), comparable to the levels
displayed by hatchery raised 2+ males, as shown in
Fig. 4 (Munakata et al. 2001a). Plasma T, E2, and 11KT levels decreased significantly after the cessation
of upstream movement. Even so, plasma T, 11-KT, and
DHP maintained higher levels than those of 1+ immature males (Fig. 4).
3-8B. Females
Each of the 10 females at age 2+ that moved upstream
in the raceway ovulated while 5 non-migrants that remained in the lower pond did not (Munakata et al.
2012a; Table 1). These phenomena indicate that female masu salmon ovulate during the last phase, or
after upstream swimming behavior has ceased. Most
of the 10 females moved upstream within 1 week after
the experiment began. Interestingly, prior to the experiment, plasma levels of T and E2 in upstream migrants were significantly higher and lower, respectively, than the corresponding levels in non-migrants
(Table 1). Furthermore, plasma E2 levels significantly
decreased after the females completed their upstream
movement. Though the E2 levels decreased, the levels
of T, E2, and DHP were considerably higher than those
in the 1+ immature females (Fig. 4).
In summary, the plasma levels of sex steroid hormones increased during the upstream migratory and
spawning periods, for both 2+ males and females.
These findings are supported by the fact that patterns
in plasma elevation of sex steroid hormones during the
upstream migratory and spawning periods are consist-
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
43
Table 1. Frequency of migrants and non-migrants, and plasma levels of testosterone (T), estradiol-17β (E2), 11-ketotestosterone
(11-KT), 17,20β-dihydroxy-4-pregnene-3-one (DHP), thyroxine (T 4), and (g) triiodothyronine (T3) (mean ± SEM) in 2+ male
and female masu salmon during upstream migratory period. Differences in mean plasma hormone levels among experimental
groups were analyzed by one-way analysis of variance (ANOVA) followed by Fisher’s PLSD. Differing letters represent
significant differences at P < 0.05 among all groups. —: no sample. Reprinted from Aquaculture, 362–363, Munakata et al.,
Involvement of sex steroids and thyroid hormones in upstream and downstream behaviors in masu salmon, Oncorhynchus
masou, 158–166,  2012a, with permission from Elsevier.
ent with those detected in chum salmon, sockeye
salmon, chinook salmon (O. tshawytscha), rainbow
trout, and Arctic charr (Salvelinus alpinus) engaged in
the same activities (Lou et al. 1984; Ueda et al. 1984;
Liley et al. 1986; Truscott et al. 1986; Slater et al. 1994;
Frantzen et al. 1997).
Considering the changing patterns of sex steroid
hormones in masu salmon, sex steroid hormones especially T, E2, 11-KT, and DHP (males), and T, E2, and
DHP (females) seem to be important factors that control the occurrence of homing, upstream swimming,
and spawning behaviors in 2+ migrants.
In 2+ non-migratory precocious males, moreover, sex
steroid hormones such as T and 11-KT seem to influence the occurrence of stream residency, upstream
movement from their territory to the spawning ground,
and spawning behaviors.
3-9. Stimulatory effects of sex steroid hormones
on the upstream swimming behavior in masu
salmon
During autumn, 1+ immature parr had low levels of
plasma sex steroid hormones and did not exhibit any
tendency to move upstream in the artificial raceway.
However, when T, E 2, and 11-KT 500 µ g/fish via
SILASCON tubing (Kaneka, Medics Corp.; outer diameter 1.5 mm, inner diameter 1.0 mm, length 30 mm)
were implanted into the abdominal cavity of 1+ immature parr, upstream swimming behavior was induced
(Munakata et al. 2001a; Fig. 11). Interestingly, it appeared that DHP 500 µ g/fish-treatment had little influence on the occurrence of upstream behavior.
In the interest of full disclosure, however, most of
the 1+ immature masu salmon used in the research
(Shiribetsu River strain) were females, because most
males from this stock mature precociously (Munakata
et al. 2000b). In this strain, the average male to female
ratio of 1+ immature parr was approximately 1:9 (for
example, Munakata et al. 2012a). In general, female
masu salmon do not have high plasma 11-KT levels
(Fig. 4, Table 1). Based on these data, it is proposed
that 11-KT is not involved in the regulation of upstream
swimming behavior in female masu salmon.
In 1+ precocious males, the control (sham-operated)
group after being transferred to the lower pond moved
upstream to the upper pond at significantly high frequencies (Munakata et al. 2001b; Fig. 12). To the contrary, castrated 1+ precocious males did not show this
tendency. However, upstream swimming behavior was
elicited from castrated 1+ precocious males treated with
T and 11-KT 500 µg/fish. In contrast, E 2 and DHP 500
µg/fish did not induce significant upstream swimming
behavior in castrated fish (Fig. 12).
To summarize these experiments, it appears that T
and E2 (females), and T and 11-KT (males) play significant roles in inducing the occurrence of upstream
swimming behavior in masu salmon. Furthermore, it
is also suggested that DHP had no significant effect on
the occurrence of the upstream swimming behaviors
in either sex (Figs. 11, 12).
3-10. Roles of T in the upstream and downstream
swimming behaviors in masu salmon
Since androgen (male sex steroid hormone) T commonly increases plasma levels in both sexes, T is regarded as one of the most important sex steroid hormones in regulating the occurrence of the upstream and
downstream swimming behaviors in salmonids, such
as masu salmon. In teleosts, however, T is also the precursor converted to other sex steroid hormones such
as estrogen E2 (males, females) and androgen 11-KT
(males) (Kagawa et al. 1982a, b). For these reasons, it
is hypothesized that T itself does not regulate the occurrence of the downstream or upstream swimming
behaviors.
3-10A. Females
In order to investigate the potential role(s) of andro-
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
44
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
Fig. 12. (a) Frequency of migrants and non-migrants, plasma
Fig. 11. (a) Frequency of migrants and non-migrants, plasma
levels of (b) testosterone (T), (c) estradiol-17β (E 2), (d) 11ketotestosterone (11-KT), (e) 17,20β-dihydroxy-4-pregnene3-one (DHP), (f) thyroxine (T4), and (g) triiodothyronine (T3)
in controls, T 500 µg, E2 500 µ g, 11-KT 500 µg, and DHP
500 µg-treated 1+ immature masu salmon parr. Numbers
above columns in (a) indicate the number of migrants and
non-migrants. Differences in the frequency of upstream
behavior from the control group were analyzed by the χ 2test, using StatView version 4.5 software (Abacus Concepts,
Inc., California, USA). *, **, and *** indicate significant
difference at P < 0.05, P < 0.01, and P < 0.001, respectively,
from the control group. Differences in mean plasma hormone
levels among experimental groups were analyzed by oneway analysis of variance (ANOVA) followed by Fisher’s
PLSD. Differing letters represent significant differences at
P < 0.05 among all groups. Reprinted from Comp. Biochem.
Physiol. Part B, 129, Munakata et al., The involvement of
sex steroid hormones in downstream and upstream migratory behavior of masu salmon, 661–669,  2001a, with permission from Elsevier.
levels of (b) testosterone (T), (c) estradiol-17β Elsevier Science (USA), with permission from Elsevier. (E 2), (d) 11ketotestosterone (11-KT), (e) 17,20β-dihydroxy-4-pregnene3-one (DHP), (f) thyroxine (T4), and (g) triiodothyronine (T3)
in castrated, castrated + T 500 µg, E 2 500 µg, 11-KT 500 µg,
and DHP 500 µg/ fish-treated groups, and sham-operated
1+ precocious male masu salmon. Numbers above columns
in (a) indicate the number of migrants and non-migrants.
Differences in the frequency of upstream behavior from the
control group were analyzed by the χ2-test, using StatView
version 4.5 software (Abacus Concepts, Inc., California,
USA). *, **, and *** indicate a significant difference at P <
0.05, P < 0.01, and P < 0.001, respectively from the control
group. Differences in mean plasma hormone levels among
experimental groups were analyzed by one-way analysis of
variance (ANOVA) followed by Fisher’s PLSD. Differing
letters represent significant differences at P < 0.05 among
all groups. Reprinted from Comp. Biochem. Physiol. Part
B, 129, Munakata et al., The involvement of sex steroid hormones in downstream and upstream migratory behavior of
masu salmon, 661–669,  2001a, with permission from
Elsevier.
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
45
Table 2. Frequency of migrants and non-migrants, and plasma levels of testosterone (T), estradiol-17β (E2), thyroxine (T4),
and (g) triiodothyronine (T 3) (mean ± SEM) in 1+ immature masu salmon implanted with T, 1,4,6-androstatriene-3,17-dion
(ATD) or tamoxifen 500 µg/fish. Differences in the frequency of upstream behavior from the control group were analyzed by
the χ2-test, using StatView version 4.5 software (Abacus Concepts, Inc., California, USA). * indicates significant difference
at P < 0.05, from the control group. Differences in mean plasma hormone levels among experimental groups were analyzed by
one-way analysis of variance (ANOVA) followed by Fisher’s PLSD. Differing letters represent significant differences at P <
0.05 among all groups. —: no sample. Reprinted from Aquaculture, 362–363, Munakata et al., Involvement of sex steroids
and thyroid hormones in upstream and downstream behaviors in masu salmon, Oncorhynchus masou, 158–166,  2012a, with
permission from Elsevier.
gen T in the regulation of upstream swimming behavior
in females, we examined the effects of implants of T,
aromatase inhibitor 1,4,6-androstatrien-3,17-dione
(ATD), and the estrogen antagonist tamoxifen 500 µg/
fish on the occurrence of upstream swimming behavior
in 1+ immature parr using the artificial raceway
(Munakata et al. 2012a; Table 2). It was assumed that
the upstream swimming behavior in the female was
regulated by aromatized E2 but not T. If this hypothesis is correct, it is inferred that administration of ATD
and tamoxifen should lower the stimulatory effects of
T treatment on the occurrence of upstream swimming
behavior. Otherwise, there is a possibility that T itself
regulates the occurrence of the upstream swimming
behavior without being converted to E2. As a result,
ATD and tamoxifen 500 µg/fish-treatment did not decrease the stimulatory effects of T on the occurrence
of upstream swimming behavior in 1+ immature female parr (Munakata et al. 2012a; Table 2, Exp 2 and
3).
3-10B. Males
In males, T and 11-KT 500 µg/fish-treatment induced
the occurrence of upstream swimming behavior in 1+
castrated precocious males (Munakata et al. 2001b; Fig.
12). Moreover, treatment with estrogen E 2 500 µg/fish
induced the occurrence of upstream swimming
behavior in 1+ intact precocious males (Munakata et
al. 2012a; Table 3, Exp 4). Hence, it is speculated that
the T, 11-KT, and E2 are potential factors involved in
the regulation of upstream swimming behavior in
males.
In order to investigate the potential role(s) of androgens, such as T and 11-KT, in the regulation of upstream swimming behavior, the effects of tamoxifen
500 µg/fish-treatment on the occurrence of upstream
swimming behavior in 1+ precocious males was investigated. As a result, it was found tamoxifen did not
decrease the stimulatory effects of T on the occurrence
of upstream swimming behavior (Table 3, Exp 4).
Therefore, it is thought that estrogens such as E2, and
androgens such as T and 11-KT may regulate the occurrence of upstream swimming behavior in males.
Thus in masu salmon, we concluded that both estrogens
such as E2 (males and females), and androgens such as
T (males and females) and 11-KT (males) are involved
in the regulation of upstream swimming behavior. Furthermore, because of the patterns of changes in the
plasma levels (Fig. 4), it is concluded that T, especially,
is one of the common sex steroid hormones that regulate the occurrence of downstream and upstream swimming behaviors.
In masu salmon, DHP did not exhibit a significant
effect on the occurrence of downstream and upstream
swimming behavior (Munakata et al. 2001a). DHP is
considered to be maturation inducing factor (MIF),
which mediate final oocyte maturation (ovulation) and
final testicular maturation (spermiation), in most
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
46
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
Table 3. Frequency of migrants and non-migrants and, plasma levels of testosterone (T), estradiol-17β (E 2), thyroxine (T4),
and (g) triiodothyronine (T3) (mean ± SEM) in castrated, castrated + E2 500 µ g/fish, sham-operated, sham-operated + E2 500
µg/fish, control, and tamoxifen 500 µ g/fish-treated 1+ precocious male masu salmon. Differences in the frequency of upstream behavior from the control group were analyzed by the χ2-test, using StatView version 4.5 software (Abacus Concepts,
Inc., California, USA). * indicates significant difference at P < 0.05, from the control group. Differences in mean plasma and
pituitary hormone levels among experimental groups were analyzed by one-way analysis of variance (ANOVA) followed by
Fisher’s PLSD. Differing letters represent significant differences at P < 0.05 among all groups. —: no sample. Reprinted from
Aquaculture, 362–363, Munakata et al., Involvement of sex steroids and thyroid hormones in upstream and downstream
behaviors in masu salmon, Oncorhynchus masou, 158–166,  2012a, with permission from Elsevier.
teleosts (Nagahama 1987a, b). Plasma DHP levels regularly increase just prior to the spawning period
(Munakata et al. 2001a; Fig. 4), while most salmonids
have already arrived at their spawning areas. As Mayer
et al. (1994) mentioned, the treatment of DHP via
Silastic tube insertion induced the occurrence of male
spawning behaviors. These findings indicate that DHP
is more important in regulating spawning behaviors
than upstream and downstream swimming behaviors.
As demonstrated previously, the frequency of downstream swimming behavior changes in accordance with
the treatment dose of T in 1+ immature masu salmon
smolts (Munakata et al. 2000b; Fig. 7). In like fashion, the induction of upstream swimming behavior in
1+ immature parr (Fig. 13) and 1+ castrated precocious males (Fig. 14) seemed to be a dose-dependent
response (Munakata et al. 2001b). These are also strong
indications that the plasma level of T is an important
factor regulating the occurrence of either downstream
or upstream swimming behaviors.
It was also detected that the dosing period may be
an important factor in initiating the upstream response.
When 1+ immature masu salmon were implanted with
T 500 µg/fish for approximately 4 months, the frequencies of upstream migrants was considerably higher
(43%) than for control individuals (19%) (Munakata
et al. 2012a; Table 2, Exp 1). On the other hand, the
frequency of upstream migrants given a dosage of T
500 µg/fish for approximately 2 months in different
trials were 17.1% (Munakata et al. 2001b; Fig. 13),
22% (Munakata et al. 2001b; Fig. 16), 36% (Munakata
et al. 2012a; Table 2, Exp 2), 52% (Munakata et al.
2001b; Fig. 11), and 57% (Munakata et al. 2012a; Table 2, Exp 3). The average frequency of upstream
swimming behavior in the later experiments (36.8%)
was lower than in the former experiment (43%)
(Munakata et al. 2012a; Table 2, Exp 1). Although the
inference is not strong, this suggests that the dosing
period (duration of plasma sex steroid hormone increase) is an important factor in this process.
In these experiments, major parts of upstream swimming behaviors occurred while there were no significant changes in plasma levels of T being administered
through Silastic or SILASCON tubing. This suggests
that the continuous release of T may play a role as a
“requirement” for the occurrence of the upstream swimming behavior (Munakata and Kobayashi 2010).
3-11. Roles of sex steroid hormones in the upstream swimming behavior in land-locked
sockeye salmon
It was determined that T 500 µg/fish treatment significantly induced the occurrence of upstream swimming behaviors in 1+ immature land-locked sockeye
salmon in the raceway (Munakata et al. 2012b; Fig.
15). In addition, precocious males of 1+ land-locked
sockeye salmon with high plasma T levels also migrated upstream at significantly high frequencies. From
this, it is inferred that stimulatory regulation of upstream migratory behavior by sex steroid hormones
might be common to multiple Pacific salmon.
3-12. Roles of sex hormones other than sex steroid
hormones in the upstream swimming
behavior in salmonids
In 2+ female masu salmon, all of the 10 upstream
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
Fig. 13. (a) Frequency of migrants and non-migrants, plasma
levels of (b) testosterone (T), (c) thyroxine (T 4), and (d)
triiodothyronine (T3) in controls, T 50 µg, T 500 µg, and T
1000 µg-treated 1+ immature masu salmon. Numbers above
columns in (a) indicate the number of migrants and nonmigrants. Differences in the frequency of upstream behavior
from the control group were analyzed by the χ2-test, respectively, using StatView version 4.5 software (Abacus Concepts, Inc., California, USA). * indicates significant difference at P < 0.05, from the control group. Differences in mean
plasma hormone levels among experimental groups were
analyzed by one-way analysis of variance (ANOVA) followed by Fisher’s PLSD. Reprinted from General and Comparative Endocrinology, 122, Munakata et al., The effects
of testosterone on upstream migratory behavior in masu
salmon, Oncorhynchus masou, 329–340,  2001b, with permission from Elsevier.
migrants ovulated, while 5 non-migrants did not
(Munakata et al. 2012a; Table 1). These results suggest that females ovulate during the last phase, or after
their upstream swimming behavior ceased. Since spermiation and ovulation are controlled physiologically
by pituitary hormones such as LH (Nagahama 1984;
Kobayashi et al. 1986, 1988), it was hypothesized that
not only sex steroid hormones but also some other sex
hormones may be involved in the occurrence of upstream swimming behavior. Investigations into masu
salmon (Amano et al. 1992, 1993), coho salmon
(Swanson 1991), and rainbow trout (Prat et al. 1996)
47
Fig. 14. (a) Frequency of migrants and non-migrants, plasma
levels of (b) testosterone (T), (c) thyroxine (T4), and (d)
triiodothyronine (T3) in castrated, cast. + T 50 µg, cast. + T
500 µ g-treated groups, and sham-operated 1+ precocious
male masu salmon. Numbers above columns in (a) indicate
the number of migrants and non-migrants. Differences in
the frequency of upstream behavior from the control group
were analyzed by the χ 2-test, using StatView version 4.5
software (Abacus Concepts, Inc., California, USA). * and
*** indicate significant difference at P < 0.05 and P < 0.001,
respectively from the control group. Differences in mean
plasma hormone levels among experimental groups were
analyzed by one-way analysis of variance (ANOVA) followed by Fisher’s PLSD. Differing letters represent significant differences at P < 0.05 among all groups. Reprinted
from General and Comparative Endocrinology, 122,
Munakata et al., The effects of testosterone on upstream
migratory behavior in masu salmon, Oncorhynchus masou,
329–340,  2001b, with permission from Elsevier.
indicate that LH levels increase with final ovarian
maturation, especially during ovulation. These studies
support the hypothesis that LH may play a role in the
regulation of upstream swimming behavior.
Implants of a gonadotropin-releasing hormone analogue (GnRHa) enhanced the occurrence of homing
behavior, the movement from the center of Lake
Shikotsu (Hokkaido) to the mouth of the natal rivers
in adult land-locked sockeye salmon (Sato et al. 1997).
Based on this, it is hypothesized that GnRH directly
influences the occurrence of upstream swimming
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
48
behavior. On the other hand, considering that the GnRH
is one important factor which stimulates the secretion
of LH from the pituitary gland into the plasma (Amano
et al. 1995), it is also inferred that GnRH plays a role
in enhancing the occurrence of homing behavior and
perhaps also upstream swimming behavior through the
release of LH into the plasma.
In masu salmon and land-locked sockeye salmon,
however, it was demonstrated that plasma LH levels
in T-treated immature fish did not exhibit clear increases over the period of downstream and upstream
(a)
18
50
13
8
2
0
(b)
c
25
b
a
0
Pituitary LH
(ng/pituitary)
50
b
a
N.S.
5
(c)
b
40
3
20
2
10
10
a
a
a
a
1
N.S.
(d)
5
a
20
ab
ab
b
b
N.S.
(e)
b
15
10
a
a
5
a
a
N.S.
0
20
(f)
b
T3 (ng/ml)
3-13A. Roles of T on the spawning behavior in males
In general, the differences in spawning behaviors
between “sneakers” (precocial males) and anadromous
males (2+ males) have been discussed. However, if a
1+ precocious male and 2+ female are transferred together into an artificial chamber, the 1+ precocious
0
Fig. 15. (a) Frequency of migrants and non-migrants, plasma
0
T4 (ng/ml)
4
30
0
LH (ng/ml)
Migrants
Non-migrants
Pituitary LH
( g/pituitary)
T (ng/ml)
50
3-13. Roles of sex steroid hormones in the spawning behavior in masu salmon
Since T was identified as one of the common sex
steroid hormones which stimulated the onset of upstream swimming behavior, T may also give rise to
spawning behaviors. In order to investigate the stimulatory role of T in the male and female spawning
behaviors, the following experiments were conducted.
T 500 µg/fish or T 1000 µg/fish dosages were administered to 1+ castrated precocious males or immature
females placed in an artificial stream chamber (1.5 ×
0.6 m with a water depth of 0.2 m) (Munakata et al.
2002).
42
**
48
*
Frequency of
fish (%)
100
movement when compared with corresponding values
for intact immature fish (Figs. 6, 7, 10, 15, 16). Since
one of main roles of LH is to stimulate sexual (gonadal) maturation (Nagahama 1984), there is the possibility that LH influences the upstream swimming
behavior through stimulating the synthesis and/or secretion of sex steroid hormones into the plasma. However, the critical role of LH in the regulation of migratory behaviors clearly requires further investigation.
15
10
a
a
5
a
0
Control
T-treated
a
N.S.
Precocious
male
Fig. 15.
levels of (b) testosterone (T), (c) pituitary contents of luteinizing hormone (LH), (d) plasma levels of LH, (e) thyroxine (T 4), and (f) triiodothyronine (T3) in control and T 500
µg/fish-treated 1+ immature fish, and 1+ precociously mature male sockeye salmon. In (c), unit of Y axis in the control group was ng/pituitary, while those of T-treated and precocious male groups was µg/pituitary. Numbers above columns in (a) indicate the number of migrants and non-migrants. N.S. represents no sample. Differences in the frequency of upstream behavior from the control group were
analyzed by the Fisher’s exact probability test, using
StatView version 4.5 software (Abacus Concepts, Inc., California, USA). * and ** indicate a significant difference at P
< 0.05 and P < 0.01 from the control group, respectively.
Differences in mean plasma and pituitary hormone levels
among experimental groups were analyzed by one-way
analysis of variance (ANOVA) followed by Fisher’s PLSD.
Differing letters represent significant differences at P < 0.05
among all groups. Reprinted with permission from Fish. Sci.,
78, Munakata et al., Involvement of sex steroids, luteinizing hormone and thyroid hormones in upstream and downstream migratory behaviors in land-locked sockeye salmon
Oncorhynchus nerka, 81–90, Fig. 6,  2012b, The Japanese
Society of Fisheries Science.
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
49
male exhibits male spawning behaviors typically associated with 2+ mature males (see Fig. 18). 1+ precocious males (sham-operated fish) frequently showed
attending and quivering behaviors towards the 2+ females (Munakata et al. 2002; Figs. 17, 18). 1+ castrated males did not display such behaviors (Fig. 17).
However, the full behavioral array of spawning males
(e.g., attending and quivering) can be restored by the
administration of T 500 µg/fish.
3-13B. Roles of T on the spawning behavior in females
In the artificial stream chamber, 2+ ovulated isolated
females frequently exhibited digging behaviors on the
gravel substrates (Figs. 19, 20). This behavior conforms field observations. Female Pacific salmon generally arrive at spawning sites earlier than do males
(Groot and Margolis 1991), and females, but not males,
release a pheromone L-kynurenine to attract nonspecific mature males (Yambe et al. 2003, 2006).
On the other hand, 1+ immature females did not perform digging behaviors (Fig. 19). The GSI values and
plasma sex steroid hormone levels of 1+ immature females were low (Fig. 4), and their ovaries were in the
primary growth stage (Kiso 1995). 1+ immature females, however, significantly exhibited digging
behaviors when treated with a dose of T 1000 µg/fish
(Munakata et al. 2002; Fig. 19).
3-14. Stimulatory effects of sex steroid hormones
on the spawning behavior in male rainbow
trout
It was demonstrated that treatment of DHP induced
the occurrence of quivering and attending behaviors
in castrated male rainbow trout towards sexually receptive females (Mayer et al. 1994). Interestingly, administration of 11-ketoandrostendione (11-KA) did not
induce male spawning behaviors to any significant
degree. This evidence supports the notion that male
spawning behaviors in some Pacific salmon are controlled by some sex steroid hormones, potentially T
and/or DHP, released into the plasma.
4. Roles of thyroid hormones, cortisol, growth
hormone, and environmental factors in the
regulation of downstream and upstream swimming behaviors in salmonids
During the period of smoltification and associated
downstream migration, salmonid smolts exhibit increases in various types of hormones, such as thyroxine (T4), triiodothyronine (T3), cortisol, GH, and prolactin (Ikuta et al. 1985; Young et al. 1989; Prunet et
al. 1989; Hirano 1991; Nagae et al. 1994; Dickhoff et
al. 1997; McCormick 2001). Since these hormones are
involved in both physiological and morphological
Fig. 16. (a) Frequency of migrants and non-migrants, plasma
levels of (b) testosterone (T), (c) pituitary contents of luteinizing hormone (LH), (d) plasma levels of LH, (e) thyroxine (T4), and (f) triiodothyronine (T3) in control and T 500
µg/fish-treated 1+ immature masu salmon. Numbers above
columns in (a) indicate the number of migrants and nonmigrants. N.S. represents no sample. Differences in the frequency of upstream swimming behavior from the control
group were analyzed by the Fisher’s exact probability test,
using StatView version 4.5 software (Abacus Concepts, Inc.,
California, USA). ** indicates a significant difference at P
< 0.01 from the control group. Differences in mean plasma
and pituitary hormone levels among experimental groups
were analyzed by one-way analysis of variance (ANOVA)
followed by Fisher’s PLSD. Differing letters represent significant differences at P < 0.05 among all groups. Reprinted
from General and Comparative Endocrinology, 122,
Munakata et al., The effects of testosterone on upstream
migratory behavior in masu salmon, Oncorhynchus masou,
329–340,  2001b, with permission from Elsevier.
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
50
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
Fig. 17. Frequency of quivering and attending behaviors in
the sham-operated, castrated, and castrated + testosterone
(T) 500 µg/fish-treated 1+ precocious male masu salmon.
Differences in mean frequencies of quivering and attending
behaviors among experimental groups were analyzed by oneway analysis of variance (ANOVA) followed by Fisher’s
PLSD. Differing letters represent significant differences at
P < 0.05 among all groups. Reprinted with permission from
Fish. Sci., 68, Munakata et al., Sex steroids control migration of masu salmon, 49–52, Fig. 3,  2002, The Japanese
Society of Fisheries Science.
Fig. 18. Male masu salmon showing (a) attending and (b)
quivering behaviors against 2+ mature females performing
a series of female spawning behaviors.
changes during smoltification, it is likely that these
hormones also play some roles in the regulation of
downstream swimming behavior, and perhaps in upstream swimming behavior. In previous studies, drastic increases in plasma levels of T4 (i.e., T4 surge) were
discovered during the peak periods of smoltification
in several salmonids, such as coho and masu salmon
(Grau et al. 1981; Yamauchi et al. 1984, 1985). Our
studies on masu and land-locked sockeye salmon also
demonstrated that plasma T 4 levels in 1+ smolts were
higher than those of T-treated 1+ smolts (Munakata et
al. 2000b, 2001a, 2012a, 2012b) (Figs. 6–10, Table
4). Furthermore, some 1+ mature and immature masu
salmon parr exhibited considerably high plasma T4 levels during the upstream migratory period (Munakata
et al. 2001a, 2001b, 2012a, 2012b) (Figs. 11–16, Tables 1–3). Considering these facts, thyroid hormone
T4 has been recognized as an important factor involved
in the downstream and upstream swimming behaviors.
Plasma levels of cortisol and GH continually increase
during the period of downstream migration (Prunet et
al. 1989; Nagae et al. 1994; McCormick 2001; Mizuno
et al. 2001; Zydlewski et al. 2005). The involvement
of cortisol and ovine GH (oGH) treatment on the occurrence of downstream swimming behavior in 1+ and
0+ masu salmon juveniles will be summarized in the
following sections.
Environmental factors (i.e., inorganic and organic
(e.g., biological) factors) also appear to play an indispensable role in the occurrence of downstream swimming, upstream swimming, and spawning behaviors.
In the following section, an overview of the involve-
ment of some environmental factors, such as intraspecific interaction, day-night cycle, etc., in the regulation of downstream swimming, upstream swimming,
and spawning behaviors will be presented.
4-1. Roles of thyroid hormones in the downstream
and upstream swimming behavior in masu
and land-locked sockeye salmon
Grau et al. (1981) and Yamauchi et al. (1985) discovered in coho and masu salmon smolts that plasma
T4 levels increased rapidly and significantly (T4 surge)
during the peak periods of their smoltification. In our
studies, most 1+ masu and land-locked sockeye salmon
smolts exhibited high plasma thyroid hormone levels
during the downstream migratory period. In masu and
land-locked sockeye salmon, and rainbow trout, however, plasma T4 and T 3 levels in downstream migrants
tended to be lower than those of non-migrants that remained in the upper pond of the raceway (Ewing et al.
1994; Munakata et al. 2000b, 2001a, 2012a, 2012b)
(see Figs. 6–10 and Table 4). Based on these observations, it was hypothesized that plasma T4 and T3 levels
decrease during or after the initiation of downstream
swimming behavior.
In our previous studies, however, the downstream
migratory smolts were usually sampled every morning at 09:00, over several weeks or months (Munakata
et al. 2000b, 2001a, 2012b) (Figs. 6–10). Therefore,
there is a possibility that the sampling delay (i.e., sam-
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
51
Fig. 19. Frequency of female digging behavior in the con-
trol, testosterone (T) 500 µ g/fish treated, and T 1000 µ g/
fish treated groups. Differences in mean frequency of digging behavior among experimental groups were analyzed by
one-way analysis of variance (ANOVA) followed by Fisher’s PLSD. Differing letters represent significant differences
at P < 0.05 among all groups. Reprinted with permission
from Fish. Sci., 68, Munakata et al., Sex steroids control
migration of masu salmon, 49–52, Fig. 4,  2002, The Japanese Society of Fisheries Science.
pling conducted considerably after the downstream
swimming behavior) may have influenced the decrease
in plasma T4 and T3 levels in downstream migrants.
In the previous study, therefore, the downstream
migrants from the lower pond of the three-step raceway
(Fig. 21) were sampled within 60 minutes of the occurrence of migration (Table 4). To avoid the disparity in the sampling dates between migrants and nonmigrants, six of the 1+ control smolts, T500 µg/fishtreated smolts, and precocious males were each sampled from the middle pond on May 3 during the April
29–May 11 observation period (Munakata et al. 2012a).
As a result, there were no clear differences in plasma
thyroid hormone levels between downstream migrants
and non-migrants (Table 4). Ikuta (1994) reported that
plasma T4 levels in 1+ land-locked sockeye salmon
smolts of downstream migrants differed: those that
were sampled immediately after the onset of downstream swimming behavior tended to have higher
plasma concentrations than those of non-migrants,
which were sampled simultaneously in the upper pond
of the raceway. Therefore, one possible hypothesis is
that decreases in plasma thyroid hormone levels occur
innately after the start of the downstream swimming
behavior.
4-1A. Effects of net trap on plasma thyroid changes
during the downstream migratory period in landlocked sockeye salmon
In previous studies (Munakata et al. 2000b, 2001a,
2012a) (Figs. 6–9, Table 4), we regularly used a net
trap (2 × 0.7 × 0.7 m) to catch the downstream migrating 1+ masu and land-locked sockeye salmon smolts.
Therefore, there is a possibility that captive stress in-
Fig. 20. Female masu salmon performing digging behavior.
(a) 2+ mature females and (b) 1+ immature females treated
with testosterone (T) 500 µg/fish.
duced by the net trap (Yada et al. 2007) caused a decrease in plasma T4 levels in downstream migrants.
Thus in a separate study, so as to avoid captive stress
from the net trap, we used a hand dip net to capture the
land-locked sockeye salmon downstream migrants directly from a separated area (2 × 4 × 0.5 m) in the lower
pond (Fig. 5), a few hours after the onset of downstream swimming behavior. After the downstream
swimming behavior ceased, however, plasma T4 levels of downstream migrants became lower than those
of non-migrants in the control, T 500 µg/fish-treated,
and the precocious male groups (Fig. 10). These results indicate that plasma T4 levels in downstream migrants become lower than those of nonmigrants, independent of the use of a net trap.
4-1B. Role of T4 and T3 in the upstream swimming
behavior
In ayu, Plecoglossus altivelis, an amphidromous fish,
it was found that plasma T4 levels of immature downstream migrants became lower than in the initial levels, likewise masu and land-locked sockeye salmon
smolt migrants, and that the levels of upstream migrants
became higher than in the initial plasma levels
(Tsukamoto et al. 1988). In adult chum salmon, on the
other hand, plasma levels of the thyroid hormones in
upstream migrants were lower than those of migrants
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
52
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
Table 4. Frequency of upstream and downstream swimming behaviors and, plasma levels of testosterone (T), thyroxine (T4),
and (g) triiodothyronine (T3) (mean ± SEM) in controls and T 500 µ g/fish-treated 1+ smolts and 1+ precocious male masu
salmon. Differences in the frequency of upstream and downstream swimming behavior from the control group were analyzed
by the χ2-test, using StatView version 4.5 software (Abacus Concepts, Inc., California, USA). *** indicates significant difference at P < 0.001, from the control group. Differences in mean plasma hormone levels among experimental groups were
analyzed by one-way analysis of variance (ANOVA) followed by Fisher’s PLSD. Differing letters represent significant differences at P < 0.05 among all groups. Reprinted from Aquaculture, 362–363, Munakata et al., Involvement of sex steroids and
thyroid hormones in upstream and downstream behaviors in masu salmon, Oncorhynchus masou, 158–166,  2012a, with
permission from Elsevier.
which swim in the coastal sea during their upstream
migratory period (Ueda et al. 1984). Based on these
findings, it was suggested in some Pacific salmon that
the plasma T4 and T3 levels decreased in association
with the progression of final gonadal maturation. In a
previous study, on the other hand, we used 1+ immature masu and land-locked sockeye salmon as a surrogate for 2+ maturing fish in the upstream migratory
period (Munakata et al. 2001a, b). Consequently,
plasma T 4 and T3 levels in upstream migrants tended
to be lower than those of non-migrants in 1+ masu and
land-locked sockeye salmon (Munakata et al. 2001a,
2001b, 2012a, 2012b) (Figs. 11–16, Tables 2, 3).
Hence, it is suggested that the decrease in thyroid hormones coincided with the occurrence of the upstream
swimming behavior. However, the upstream migrants
were sampled every morning at 09:00 over several
weeks or months in our previous studies (Munakata et
al. 2001a, b). Therefore, the sampling delay may have
influenced the decrease in plasma thyroid hormone
levels in upstream migrants. In a separate experiment
(Munakata et al. 2012a; Table 4), the upstream migrating T 500 µ g/fish-treated 1+ masu salmon were
sampled within 60 minutes of the occurrence of upstream swimming behavior from the upper pond of the
three-step raceway. It was found that there were no differences in plasma T4 and T3 levels between upstream
migrants and non-migrants. As a result, decreases in
plasma T4 and T3 levels may initiate a few hours after
the occurrence of the upstream swimming behavior.
To summarize these investigations, thyroid hormones, such as T4 and T3, appear to play some roles in
the regulation of downstream and upstream swimming
behavior in some anadromous salmonids. Recently, it
was demonstrated that T4-treated 0+ coho salmon parr
tended to exhibit a higher frequency of downstream
swimming behavior than the control parr (Munakata
and Schreck, unpublished data). However, it was also
previously reported that T4 itself does not induce the
occurrence of downstream swimming behavior in
salmonids (see a review by Iwata 1995). The role of
the thyroid hormones in mediating the downstream and
upstream swimming behaviors clearly requires further
investigation.
4-2. Roles of cortisol and growth hormone in the
downstream swimming behavior in masu
salmon
4-2A. Cortisol
In anadromous salmonids, cortisol and GH have been
known to regulate the hypo-osmoregulatory ability,
during the smoltification period (Hirano 1991;
McCormick 2001). In both 1+ smolts and 0+ parr of
masu salmon, on the other hand, it was found that treatment of cortisol, but not GH (oGH), caused the occurrence of downstream swimming behavior in the
raceway (Munakata et al. 2007; Figs. 22, 23). The frequency of downstream swimming behavior in the cortisol 2 mg/fish-treated group (72%) and oGH 250 µg/
fish + cortisol 2 mg/fish-treated group (82%) were significantly higher than those in the control (23%) and
oGH 250 µg/fish-treated group (18%) (Fig. 22). The
plasma cortisol levels of migrants in the cortisol 2 mg/
fish-treated 1+ smolts (Fig. 22) were similar to those
levels of naturally occurring 1+ smolts (Nagae et al.
1994; Mizuno et al. 2001).
The results indicate that the downstream swimming
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
Fig. 21. Schematic drawing of three-step raceway that consists of upper, middle, and lower ponds. This raceway enables us to quantify upstream and downstream swimming
behaviors at the same period. After the experimental fish
had been reared in tanks, they were transferred to the middle pond (4 × 2 × 0.5 m) of the raceway. The middle pond
was connected to the upper (4 × 2 × 0.5 m) and lower (4 × 2
× 0.5 m) ponds through square holes (50 × 25 cm, thickness
3 cm) which were made on wooden walls. Flow rate (volume) and velocity of the water in the raceway were 10 l/s
and 75-85 cm/s. The upstream and downstream migrants are
identified when the fish swam from the middle pond to the
net traps (2 × 0.7 × 0.7 m) that were located in the upper and
lower ponds, respectively. Reprinted from Aquaculture (in
press), Munakata et al., Involvement of sex steroids and thyroid hormones in upstream and downstream behaviors in
masu salmon, Oncorhynchus masou,  2012a, with permission from Elsevier.
behavior (negative rheotaxis) is controlled competitively by both sex steroid hormones and smolt inducing factors, such as cortisol.
In 0+ parr, frequency of downstream swimming
53
Fig. 22. Frequency of migrants and non-migrants, plasma
levels of oGH and cortisol in the control, oGH 250 µg, cortisol 2 mg, and oGH 250 µ g + cortisol 2 mg-treated 1+ masu
salmon smolts. Figures beside columns indicate the number
of migrants and non-migrants. Differences in the frequency
of downstream behavior from the control group were
analyzed by the χ2-test, using StatView version 4.5 software
(Abacus Concepts, Inc., California, USA). *** indicates a
significant difference at P < 0.001 from the control group.
Differences in mean plasma hormone levels among experimental groups were analyzed by one-way analysis of variance (ANOVA) followed by Fisher’s PLSD. Differing letters represent significant differences at P < 0.05 among all
groups. Reprinted from General and Comparative
Endocrinology, 150, Munakata et al., Effects of growth hormone and cortisol on the downstream migratory behavior in
masu salmon, Oncorhynchus masou, 12–17,  2007, with
permission from Elsevier.
behavior in the cortisol 2 mg/fish-treated group (82%)
and oGH 250 µg/fish + cortisol 2 mg/fish-treated group
(90%) were higher than those in the control (18%) and
oGH 250 µg/fish-treated group (0%) (Fig. 23). Based
on these findings, it can also be hypothesized that cortisol induces the occurrence of downstream swimming
behavior not only in 1+ smolts but also in 0+ parr in
masu salmon.
A causal mechanism for how the increases of plasma
cortisol levels induce the downstream swimming
behavior in 1+ smolts and 0+ parr remains unclear.
Since only portions of 1+ masu salmon undergo the
smoltification, one possible explanation is that the
plasma cortisol levels increase innately as the
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
54
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
smoltification process advances. Alternatively, since
various types of acute and chronic environmental
stimuli, such as inter-and intra-specific interactions
(Iwata 1996; Kagawa and Mugiya 2000; Kelsey et al.
2002), fasting (Varnavsky et al. 1995), exposure to low
water (Pankhurst and Kraak 2000), fright responses
from being chased by a netter (Nichols and Weisbart
1984; Yada et al. 2007), and water quality (Barton et
al. 1987; Redding et al. 1987), increased circulating
plasma cortisol levels within a few hours in teleosts,
another explanation is that some environmental cues
directly or indirectly enhance the additional secretion
of cortisol into the plasma, and subsequently downstream swimming behavior is induced. Some studies
indicated that inter-and intra-specific interactions,
among larger and smaller individuals, may be an important factor that not only increased plasma cortisol
levels in small subordinates (Kelsey et al. 2002), but
also induced movement of smaller salmonid juveniles
out of their focal foraging areas (Nakano et al. 1990;
Nakano 1995).
Alternatively, as mentioned in Subsection 2-6, it was
found that all of the 40 1+ masu salmon smolts transferred into the upper pond of the raceway migrated
down within a week (Munakata et al. 2000b; Fig. 9).
Based on this, it was hypothesized some other environmental factors induce the plasma cortisol elevations
and subsequent downstream swimming behavior. Either downstream or upstream swimming behavior occurs mainly during the evening, through the night, and
when it rains (Yamauchi et al. 1985; Munakata et al.
2000b; Munakata et al. unpublished data; Fig. 24). Accordingly, environmental factors, such as photoperiod,
temperature, flow rate, and water quality (e.g., turbidity), which exhibit diurnal fluctuations, affect the occurrence of downstream swimming behavior through
increases in plasma cortisol.
4-2B. GH
In anadromous salmonids, GH is considered to be
an important factor which regulates the hypoosmoregulatory ability during smoltification (Hirano
1991; McCormick 2001). Previous studies also demonstrated that treatment of oGH as well as native GH
influenced the physiological processes of smoltification
and several types of behaviors such as salinity preference, foraging, and anti-predator behaviors (Iwata et
al. 1990; Boeuf et al. 1994; Johnsson et al. 1996;
Jönsson et al. 1996; Yada et al. 1999). In our previous
study, however, most oGH-treated 1+ smolt and 0+ parr
did not exhibit downstream swimming behavior during the downstream migratory period (Figs. 22, 23).
One possible explanation is that the treatment dose of
oGH may have been insufficient, or the treatment period may have been too short to affect the downstream
behavior. On the other hand, it is also possible that GH,
including oGH, is not involved in the occurrence of
Fig. 23. Frequency of migrants and non-migrants, plasma
levels of oGH and cortisol in the control, oGH 250 µg, cortisol 2 mg, and oGH 250 µg + cortisol 2 mg-treated 0+ masu
salmon parr. Figures beside columns indicate the number of
migrants and non-migrants. Differences in the frequency of
downstream swimming behavior from the control group were
analyzed by the χ2-test, using StatView version 4.5 software
(Abacus Concepts, Inc., California, USA). *** indicates a
significant difference at P < 0.001 from the control group.
Differences in mean plasma hormone levels among experimental groups were analyzed by one-way analysis of variance (ANOVA) followed by Fisher’s PLSD. Differing letters represent significant differences at P < 0.05 among all
groups. Reprinted from General and Comparative
Endocrinology, 150, Munakata et al., Effects of growth hormone and cortisol on the downstream migratory behavior in
masu salmon, Oncorhynchus masou, 12–17,  2007, with
permission from Elsevier.
downstream swimming behavior in masu salmon.
Recently, Ojima et al. (2009) reported that
hypothalamic hormone growth hormone-releasing hormone (GHRH) caused the downstream swimming
behavior in 0+ chum salmon fry. The findings thus indicate that GHRH directory modulates the occurrence
of downstream movements in chum salmon fry. Furthermore, this also indicates that GH which is stimulated by GHRH plays a role in the downstream swimming behavior. Therefore, it is necessary to investigate the effects of treatment dose and period of both
oGH and native GH on downstream swimming
behavior.
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
55
including phenotypes that will become smolts (Nakano
1995; Kiso 1995; Hutchison and Iwata 1998; Munakata
et al. 2000b). In 1+ masu salmon, moreover, the BL
and BW of non-migrants, especially the 1+ precocious
males, tended to be larger than those of downstream
migrants such as 1+ smolts (Munakata et al. 2000b;
Table 5). Similarly, BL, BW, and CF in downstream
migrants were smaller than those in non-migrants
among T500 µ g/fish-treated immature smolts
(Munakata et al. 2000b; Table 6). Although further investigation is needed, an acceptable rationale is that
intra-specific interactions, which depend partly on their
body size (growth), play roles in stimulating the downstream behavior in smaller fish.
(a)
(b)
Fig. 24. (a) Number of fish that exhibited the downstream
migratory behavior in the 1+ masu salmon smolts (white
column) and the T 500 µg/fish-treated smolts (dark column).
(b) date of rainfall during experimental period in May.
4-3. Roles of external factors in the downstream
swimming, upstream swimming, and spawning behaviors
4-3A. Roles of external factors in downstream swimming behavior
A significant portion of 1+ masu salmon smolts exhibit the downstream movement during favorable periods in the spring. Furthermore, it is believed that the
downstream migratory period in the southern regions
tends to be earlier than that in the northern regions
(Machidori and Kato 1984; Kato 1991; Kiso 1995).
This trend clearly indicates that some external (environmental) factors such as photoperiod and temperature, which show seasonal fluctuations and regional
differences, may be involved in the occurrence of
downstream swimming behavior. As mentioned previously, it is further indicated that some environmental
stimulations such as photoperiod and temperature,
which exhibit diurnal patterns, may play roles in stimulating this behavior.
According to Yamauchi et al. (1985), 1+ masu salmon
smolts exhibited downstream swimming behavior after precipitation occurred. Our previous study also suggested that the number of downstream migrants in the
1+ masu salmon smolts increased when it rained (Fig.
24). Accordingly, it is indicated that rain, snow, and
the concomitant increase in flow may trigger the occurrence of downstream swimming behavior
(Munakata et al. unpublished data).
As mentioned repeatedly, dominant precocious male
parr frequently initiate aggressive behaviors (e.g., attacking, nipping, chasing) towards subordinate fish
4-3B. Roles of external factors in the upstream swimming behavior
During the upstream migratory period, a significant
portion of the sex steroid hormone-treated 1+ immature masu salmon, and 2+ masu and land-locked
sockeye salmon moved upstream during and after dusk
(Munakata et al. 2001a, 2001b, 2012a, 2012b) (Fig.
25). Thus, we must consider that upstream swimming
behavior is triggered or regulated by some environmental factors such as photoperiodicity.
Because plasma sex steroid hormone levels of sex
steroid-treated immature fish did not show apparent
changes during the upstream migratory period
(Munakata et al. 2001a, b; Figs. 11–16, Tables 2–4),
sex steroid hormones may play roles in the regulation
of upstream behavior as a “requirement” (Munakata
and Kobayashi 2010) and sex steroid hormones may
modulate receptivity of fish from some environmental
stimulations. However, additional research will be required to validate this linkage between the physiological response and the environmental change.
4-3C. Roles of external factors in the spawning
behavior
When 2+ ovulated female masu salmon are reared
continuously in artificial environments such as in
hatchery fiber-reinforced plastic (FRP) tanks, these fish
seldom display spawning behavior, including the digging of redds. On the other hand, we discovered that
the 2+ ovulated and T 1000 µg/fish-treated 1+ immature females that were transferred into the previously
mentioned artificial stream chamber frequently displayed digging behaviors (Fig. 18). The chamber contained both gravel and flowing water, indicating that
physical environmental cues may be necessary before
a particular spawning behavior is elicited. Satou et al.
(1984) demonstrated that spawning behavior in male
land-locked sockeye salmon adults was elicited by
decoy fish which exhibit movements and oscillations
resembling a mature female in spawning condition.
This example shows that visual stimulation or oscillation from females can induce spawning behavior in
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
56
Table 5. Body length (BL), body weight (BW), and condition factor (CF) in the control, T5 µg/fish-, T 50 µ g/fish-, and T 500
µg/fish-treated 1+ smolts and 1+ precocious male masu salmon. Differences in mean BL, BW, and CF among experimental
groups were analyzed by one-way analysis of variance (ANOVA) followed by Fisher’s PLSD. Differing letters represent
significant differences at P < 0.05 among all groups. Reprinted with permission from Zoological Science, 17, Munakata et al.,
Inhibitory effects of testosterone on downstream migratory behavior in masu salmon, Oncorhynchus masou, 863–870, Table
2,  2000b, Zoological Society of Japan.
males in the same manner as pheromones, such as Lkynurenine (Yambe et al. 2003, 2006).
5. Conclusion and discussion
5-1. Roles of sex steroid hormones in the occurrence of migratory behaviors in masu salmon
In masu salmon, it was demonstrated that sex steroid hormones, such as T inhibited the occurrence of
smoltification and downstream swimming behavior
(negative rheotaxis), the initial phase in seaward migration (Aida et al. 1984; Ikuta et al. 1985, 1987;
Munakata et al. 2000b, 2001a). On the other hand,
treatment with T induced the occurrence of upstream
swimming behavior (positive rheotaxis), a component
of upstream migration in 1+ immature parr and castrated precocious males (Munakata et al. 2001a, b).
Furthermore, T commonly induced spawning behavior
in both sexes (Munakata et al. 2002). Therefore, it is
concluded that sex steroid hormones, such as T, regulate the occurrence of downstream and upstream swimming behavior, in negative and positive rheotaxis fashions, and that sex steroid hormones negatively control
the occurrence of the seaward migration.
Based on these phenomena, we now understand why
mature masu salmon that have high levels of plasma
sex steroid hormones live continuously in their natal
rivers as non-migratory forms (Figs. 3, 26). On the
other hand, delay of sexual maturation in the rivers
results from low levels of plasma sex steroid hormones
in some juveniles, and these fish regularly exhibit
downstream swimming behavior along with the river
currents, in association with the smoltification (Figs.
3, 26). In comparison, masu salmon that begin to sexually mature and consequently have high plasma sex
steroid hormone levels in the sea (or lakes) tend to
move against the river current (positive rheotaxis), and
home upstream to their natal reach. This behavior is
homologous with the upstream movement of precocious non-migrants that live continuously in their natal rivers (Figs. 3, 26). Finally, masu salmon with high
levels of plasma sex steroid hormones initiate the display of spawning behavior after they arrive at a potential spawning habitat.
Because sex steroid hormones commonly regulate
the occurrence of downstream swimming, upstream
swimming, and spawning behaviors, can it be considered that downstream (negative rheotaxis) and upstream migratory behavior (positive rheotaxis) are involved as an obligatory phase before the spawning
takes place? More specifically, these migratory
behaviors are involved as part of the spawning activities, which take place in the upper river. Because masu
salmon use different habitats (rivers and sea) during
their lifecycle, it may be that the inhibition of downstream swimming behavior and the stimulation of upstream swimming behavior by the sex steroid hormones
are “biological endorsements” that orient sexually
mature masu salmon to natal spawning areas, before
the initiation of spawning behaviors.
While masu salmon non-migrants such as 1+ preco-
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
57
Table 6. Body length (BL), body weight (BW), and condition factor (CF) in the control (Raceway 1) and T500 µg/fish-treated
smolts (Raceway 2) in masu salmon (Oncorhynchus masou). Differences in mean BL, BW, and CF among experimental
groups were analyzed by one-way analysis of variance (ANOVA) followed by Fisher’s PLSD. Differing letters represent
significant differences at P < 0.05 among all groups. Reprinted with permission from Zoological Science, 17, Munakata et al.,
Inhibitory effects of testosterone on downstream migratory behavior in masu salmon, Oncorhynchus masou, 863–870, Table
3,  2000b, Zoological Society of Japan.
cious males exhibit high plasma sex steroid hormone
levels and stay in their natal rivers, representative
downstream migratory forms, such as 1+ smolts regularly exhibit increases in plasma T4, T3, cortisol, GH,
and prolactin levels during the period of smoltification
and through downstream migration (e.g., Dickhoff et
al. 1997). Among these hormones, cortisol significantly
induced the occurrence of downstream swimming
behavior in 1+ smolts (Munakata et al. 2007; Fig. 22).
Based on these results, the initiation of seaward (downstream) migration in masu salmon seems to be controlled competitively by sex steroid hormones (sexual
maturation in rivers) and cortisol (metamorphosis of
smoltification: preparation of marine life).
Since cortisol is an smoltification-inducing factor
(Hirano 1991; McCormick 2001), it has been suggested
that the levels innately increase with the progression
of smoltification. On the other hand, it was inferred
that socio-environmental factors, such as intra-, or
inter-specific interactions acting as stressors, cause
acute and/or chronic plasma cortisol elevations in some
teleosts (e.g., salmonids) (Schreck 2000). Previous investigations also discovered that plasma cortisol levels in 1+ masu salmon smolts exhibited considerable
fluctuations within one day and among different sampling dates in the Kesen River, in northern Honshu
(Munakata et al. unpublished data). These facts suggest that some environmental factors, such as temperature, cause or regulate the occurrence of smoltification
and subsequent downstream swimming behavior via
elevations of plasma cortisol levels.
If smoltification and downstream swimming behavior
in 1+ masu salmon migrants are caused or regulated
partly by some environmental factors via plasma cortisol elevations, it is further hypothesized that the dif-
ferentiation from parr (non-migrants) to smolts (migrants) is influenced by the percipiency of environmental factors and concomitant cortisol elevations.
According to Machidori and Kato (1984) and Kiso
(1995), it is clear that 0+ precocious males grow faster
than immature parr (e.g., smolt migrants) of the same
age during 0+ summer, a half year prior to the
smoltification period. Because growth and the following sexual maturation of non-migrants appear to be
supported partly by their active foraging behaviors and
territorial aggressiveness (e.g., Nakano 1995), it is
hypothesized that intra-specific interactions, such as
territorial aggressiveness and other concomitant phenomena (e.g., hunger, delay of growth, etc.), play key
roles in regulating the transformation from nonmigrants (parr) to migrants (smolts). As a result, nonmigratory forms, such as 1+ precocious males, and
migrants, such as 1+ smolts, are eventually reciprocally balanced in some rivers (see Fig. 27).
5-2. Sub-types of non-migratory and migratory
forms
In masu salmon, it has been noted that non-migrants
such as precocious male parr and migrants such as 1+
smolts appear in most rivers, and the two forms can be
distinguished by their diagnostic characteristics, such
as appearance and increasing plasma sex steroid hormone levels (Fig. 4). In masu salmon, however, it has
also been recognized that there are phenotypes, which
exhibit intermediate migratory patterns between representative non-migrants and migrants (Kiso 1995)
(Fig. 26, Table 7). For example, in a significant numbers of rivers, there are so-called “immature parr nonmigrants”—some females and a small number of males
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
58
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
Fig. 25. Eight-day running average of the number of upstream migrants in 2+ male and female sockeye salmon in the raceway.
Dark and white bars indicate light dark-periods. This graph shows that the majority of 2+ land-locked sockeye salmon exhibit
upstream migratory behavior before, during, and after dusk between 16:00 and 22:00. There was no clear difference between
sexes. Reprinted with permission from Fish. Sci., 78, Munakata et al., Involvement of sex steroids, luteinizing hormone and
thyroid hormones in upstream and downstream migratory behaviors in land-locked sockeye salmon Oncorhynchus nerka, 81–
90, Fig. 4,  2012b, The Japanese Society of Fisheries Science.
(Kiso 1995), that live continuously in their natal rivers as do 1+ precocious males (Fig. 26, Table 7). Most
of these 1+ non-migrants are considered to be immature parr, based on their appearance (Kiso 1995) and
plasma sex steroid hormone levels (Munakata et al.
unpublished data).
In masu salmon, moreover, there are some 1+ downstream migrants, which are identified as smolts by their
appearance, but do not travel along migratory routes
to the offshore seas, likewise the representative smolt
migrants (Machidori and Kato 1984; Kiso 1995) (Fig.
26). For instance, some of these migrants migrate further downstream than the 1+ precocious males and nonmigratory 1+ parr. However, the majority of these fish
do not enter the sea and instead stay in the mid through
lower part of their natal rivers from spring onward,
then move upward in the rivers through summer and
autumn (Fig. 26). These fish exhibit a silvery body
color and low plasma sex steroid hormone levels as do
representative smolt migrants, but their body size and
CF values tend to be high (Kiso 1995). Therefore, these
sub-types of migratory forms are referred to as “pseudo
smolts” and “regressive smolts” (Kiso 1995). Although
there is no clear difference in the appearance between
the “pseudo smolts” and “regressive smolts” during the
downstream migratory period, “pseudo smolts” are
more likely to reside in the middle to upper reaches of
rivers as do the precocious males and the immature
parr non-migrants, whereas “regressive smolts” display
more distinct downstream migration and will reach the
lower part of their natal rivers (Kiso 1995).
Besides such sub-types of migratory forms, there are
also other migratory forms considered to be “coastal
smolt migrants” that will migrate near the coastal seas
between their natal rivers and the Sea of Okhotsk
(Machidori and Kato 1984; Kiso 1995). There is also
no clear difference in the appearance between the “regressive smolts” and “coastal smolt migrants” (Kiso
1995). Regularly, however, body size (25 to 40 cm in
BL) of the “coastal migrants” during the upstream migratory period is larger and smaller than those of “regressive smolts” and “representative smolt migrants”,
respectively, mainly because of the short migration
(less than a year) period in the sea (Kiso 1995).
In masu salmon, there is an additional type of nonmigrants in which BL and BW are considerably lower
than those of other non-migrants and migrants. According to Kiso (1995), such small sized non-migratory
masu salmon can be considered to be a “poor growth
fish”, which do not differentiate into either precocious
parr or smolt migrants during the age of 1+, indicating
that not only non-migrants but also smolts migrants
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
Hatching
(1) Precocious parr
Upper river
(2) Immature parr
non-migrants
(7) Poor growth fish
(1)
Parr
1+ year
59
2+ year
3+ year
Growth Maturation
(2)
Growth
(3)
Less growth
Maturation
Growth
Maturation
Upstream
migration
type II
(7)
Diversity
Less growth
Mid–lower river
(3) Pseudo smolts
(4) Regressive smolts
4+ year
Smoltification
f at
Downstream
e
migration
Growth
Maturation
at
(4)
4)
Rare?
tu
Growthh Maturation
Sea
(5)
5)
(5) Coastal smolt
migrants
Feeding
migration
(6) Smolt migrants
Rare?
Rare?
Maturation
Growth
(6)
Upstream
migration
type I
Homing
Fig. 26. Diagrammatic representation of the lifecycle of masu salmon (Oncorhynchus masou) (modified the figure by Kiso
1995). There seems to be a sequential diversity in migratory patterns among representative non-migratory (precocious parr)
and migratory (smolt) forms. In masu salmon, 1+ parr that occupy focal foraging areas (territory), exhibit precociously sexual
maturation, and have high plasma sex steroid levels become representative non-migrants, precocious parr. In contrast, some
of the 1+ immature fish that could not gain focal territories become representative migrants, smolt migrants. Their migratory
patterns seem to be modulated in an inhibitory fashion by their maturity and/or growth performance (see text for details).
Note that the “poor growth fish” which does not differentiate into either precocious parr or smolt migrants during the age of
1+ appears to differentiate into non-migratory parr or migratory smolts in another year, mainly during the age of 2+.
need to grow before they initiate the smoltification.
Generally, the “poor growth fish” seems to differentiate into non-migratory parr or migratory smolts in another year, mainly at age 2+ (Kiso 1995) (Fig. 26).
Such variations, especially among migratory
behaviors, may be influenced heavily by environmental and physiological factors. In Japanese streams, the
proportions of “1+ immature parr non-migrants” tend
to increase in the southern regions when compared to
the northern regions, which is also a trend observed
for 1+ precocious males (Fig. 27). In Japan, therefore,
these two types of masu salmon are commonly called
“yamame” in Japanese. Although the GSI values and
plasma sex steroid hormone levels in 1+ immature parr
non-migrants are considerably lower than those of the
precocious males during spring (Kiso 1995; Munakata
et al. unpublished data), the ovarian development stage
in 1+ immature female non-migrants is the “yolk vesicle stage”, while most 1+ immature female smolt migrants are in the “early peri-nucleolus stage” (Kiso
1995) (Table 7). It is thus indicated that some of the
immature non-migrants progress gonadal maturation
in rivers, though their sex steroid hormone levels are
low.
The existence of such non-migrants indicates that
stream residency of non-migrants is regulated not only
by high plasma sex steroid hormone levels, but also
by other physiological factors. In general, most
salmonids exhibit increases in hypothalamic and pi-
tuitary hormones such as GnRH, follicle stimulating
hormone (FSH), and LH, prior to the elevation in
plasma sex steroid hormones to stimulate gonadal
maturation after the spring (e.g., Amano et al. 1998;
Munakata et al. 2000b). In masu salmon “pseudo
smolts” and “regressive smolts”, it is also important to
note that the GSI values and/or ovarian development
stages were slightly higher than those in the 1+ smolt
migrants (Table 7). To account for these phenomena,
it is hypothesized that some sex hormones other than
the sex steroid hormones also play some roles in inhibiting the occurrence of downstream swimming
behavior in immature non-migratory forms.
It is generally thought that salmonids initiate gonadal
maturation after they have attained sufficient growth
(Nordeng 1983; Kiso 1995). Therefore, it appears likely
that not only sex hormones but also other hormones
such as GH modulate the occurrence of downstream
swimming behavior and smoltification, depending on
their growth phase. Until now, however, such a hypothesis is far from being established, and which physiological factors are actually involved in the occurrence
of downstream swimming behaviors is not fully understood. This topic clearly needs further investigation.
5-3. Variation of migratory behavior in salmonids
In masu salmon, it becomes apparent that some
strains exhibit varieties of lifecycle between the rep-
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
60
(a)
(b)
Late
Downstream migratory period
Early
Early
Honshu
Latitude
Amphidromy
Spawning period
Anadromy
Sea
Late
River
Sea
Hokkaido
High
River
Low
Kyushu
Catadromy
Fig. 27. Diagrammatic representations of (a) life histories of anadromous, amphidromous, and catadromous fish (modified
from Gross 1987) and (b) differences in lifecycle of masu salmon (Oncorhynchus masou) among different regions. In (a) (e.g.,
northern hemisphere), anadromy and catadromy exceed in northern temperate and southern tropic areas, respectively, while
amphidromy are frequent between these areas. In (b), proportion of non-migratory and migratory (e.g., smolts) forms increased in southern (e.g., Kyushu) and northern (e.g., Hokkaido) Japanese streams, respectively, maybe by the differences in
productivity among different areas. Also, spawning and downstream migratory period in masu salmon become later in southern and northern Japan, respectively (Machidori and Kato 1984).
resentative non-migratory and migratory forms. Also,
it is speculated that these varieties of non-migratory
and migratory patterns are sequentially regulated by
some physiological factors depending on the gonadal
maturation and/or growth stages, prior to and during
the downstream migratory period (Table 7).
Among the four salmonid genera, there also are varieties of non-migratory and migratory forms that resemble those lifecycles observed in masu salmon
(Groot and Margolis 1991; Thorpe 1994; Quinn 2005)
(Fig. 1). Considering the hypothesis that salmonids are
of a freshwater origin, it is acceptable to think that the
evolutionally-ancient genera such as the genus Hucho
and Salvelinus remain to show tendency depending on
freshwater life, and spawn in the rivers as do the masu
salmon non-migrants, whereas evolutionally new genera, such as the genus Salmo and Oncorhynchus
evolved to rely more heavily on ocean life (seaward
migration), as do the masu salmon migrants (Figs. 3,
26). If the migratory patterns of masu salmon can be
considered as an “epitomization” of the variations of
salmon migration, it may be hypothesized that the occurrence of migratory behavior for a major part of the
salmonids is also controlled by their gonadal maturation and/or growing stages in the rivers, which will
require further investigations for validation.
5-4. Driving force of migration from rivers to the
sea—Why do salmonids migrate?—
According to Gross (1987), it is thought that the
migration (anadromy) of salmonids evolved in relation to the availability of food (or productivity) between the rivers and the sea (Gross 1987) (Fig. 27).
Concisely, it is thought that productivity in the sea is
higher than that in the rivers in the northern hemisphere
regions, whereas contrasting patterns are found in the
southern tropic regions. This also indicates that there
are gradual variations in the productivities of the rivers and the sea along the latitude gradient within each
of the hemispheres.
Actually, in masu salmon, proportions of “precocious
male non-migrants” and “immature non-migratory
parr” are typically higher in the southern streams (i.e.,
Kyushu) than those in northern regions (i.e., Hokkaido)
(Machidori and Kato 1984) (Fig. 27). On the other
hand, the proportion of representative downstream
migratory smolts is higher in northern streams than in
the southern ones (Machidori and Kato 1984) (Fig. 27).
Considering a research hypothesis that the occurrence
of non-migrants and migrants (smolts) are modulated
by their gonadal maturation and/or growth stages,
which are influenced by the productivity of the rivers,
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
61
Table 7. Appearance of frequency and migratory pattern (area) of non-migratory and migratory forms of masu salmon
(Oncorhynchus masou) that inhabit streams along Sanriku coast in northern Honshu and its plasma sex steroid hormone
levels, gonad somatic index (GSI), and gonadal development and growth stages prior to and during the period of downstream
migration, based on Kiso (1995). Shades indicate the potential physiological factors that inhibit or modulate the occurrence of
downstream migratory behavior.
Male
Group
Precociou parr
Immature parr non-migrants
Pseudo smolts
Regressive smolts
Coastal smolt migrants
Representative smolt migrants
Poor growth fish
Migratory status
Non-migratory
—
Migratory?
Migratory
—
—
Non-migratory
Appearance freq.
High
Rare
—
—
—
Moderate
Rare
Migratory areas
Upper- middle river
—
—
Middle- lower river
Coastal sea
Sea of Okhotsk
Upper- middle river
Sex steroid hormone
High
Low
—
—
—
—
—
GSI
Gonadal development
Growth
High
Sperm-formation stage Very good
Moderate Late multiplication stage
—
Low
—
Good
—
—
—
—
Early multiplication stage Moderate
—
—
—
—
—
Poor
Migratory status
Non-migratory
—
Migratory?
Migratory
—
—
Non-migratory
Appearance freq.
Rare
Moderate
Rare
—
—
High
Rare
Migratory areas
Upper- middle river
—
—
Middle- lower river
Coastal sea
Sea of Okhotsk
Upper- middle river
Sex steroid hormone
Moderate
Low
—
—
—
—
—
GSI
Gonadal development
Growth
High
Oil drop stage
Very good
Moderate
Yolk vesicle stage
—
—
—
Good
—
—
—
Low
Late peri- nucleolus stage Moderate
—
—
—
Poor
—
Early peri- nucleolus stage
Female
Group
Precociou parr
Immature parr non-migrants
Pseudo smolts
Regressive smolts
Coastal smolt migrants
Representative smolt migrants
Poor growth fish
such differences in the proportions of non-migrants and
migrants seem to be shaped by the gradual changes of
productiveness in the rivers throughout different regions.
Again, Gross (1987) has indicated that the seaward
migration of salmonids is induced evolutionally by the
differences in productivity between the rivers and the
sea in high latitude areas of the northern hemisphere.
At the mouth of the rivers, however, there is a clear
boundary between the fresh and salt (sea) waters, and
it is still unclear as to why the ancestral form of
salmonids (freshwater origin) crossed over the osmotic
boundary and discovered the favorable feeding environments (higher productivity) in the sea.
In this monograph, it was shown that the dominant
non-migratory forms of masu salmon regularly occupy
focal foraging areas (see Subsection 2-3). Accordingly,
it is suggested that most of the downstream migratory
behavior in migrants is caused by a reduction in food
availability in the natal rivers, as shown by Gross
(1987), but more specifically, one of the important and
direct factors that cause the downstream migration from
the favorable habitat is the intra-specific interactions
between the dominant non-migrants and subordinate
migrants, depending on their stock density, or other
environmental stressors, such as changes in temperature, flow, water quality, and photoperiodicity.
If that is the case, it is easier to understand why some
of the migratory forms that could not stay in their focal territories ultimately crossed the boundary between
the rivers and the sea. Based on these phenomena, the
high productivity of the sea is considered to be less of
a causal factor of the migration than a “refuge” for the
immature salmonids that perform the downstream migratory behavior.
5-5. Evolution of migratory behavior in salmonids
Most of the juveniles of pink and chum salmon,
which are considered evolutionarily new species, exhibit long distance migration, about six months after
their hatching (see Fig. 1). Therefore, it is suggested
that evolutionarily new species are more likely to depend on marine life when compared to the older
salmonid species (Gross 1987). Based on the variations
of migratory behavior in salmonids, and the physiological control mechanisms of masu salmon and some other
species, however, these patterns in migratory behavior
are an extension of the variations of the salmon migrations. Considering these phenomena, it is acceptable
to think that the majority of the maturing salmon continue to aspire to spawn in their natal rivers, at the end
of their lifecycle. That is, the seaward migration may
be undertaken as a subsidiary choice in the lifecycle
of most salmonids. Previously, non-migratory forms
of masu salmon had been considered to be a “landlocked population”, and worse still the precocious male
parr within the entire salmonid species were generally
considered as a “biological mistake”, according to
Gross (1987). Based on the migratory patterns and
physiological control mechanism of migratory
behaviors in masu salmon, however, it is apparent that
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
62
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
these types of fish are so-called “reversions” and they
represent the ancestral forms of salmonids that matured
and spawned in their natal rivers.
5-6. Conservation implications for masu salmon
and their habitats
1) Numbers (biomass) of wild masu salmon—both
“Yamame” and “Sakura masu” are continuously decreasing in a number of rivers (e.g., Kato 1991).
2) Because the non-migrants and migrants diverge
depending on their sexual maturity and growth stages,
which are supported by the productivity in their natal
rivers, both non-migrant (yamame) and migratory
(sakura masu) forms can be increased by improving
the productivity of the rivers. In northern streams, carcasses of salmonids which migrate back from the sea
are considered to be an important resource which plays
a primary role in the increase of productivity in rivers
(JoAnna and Richard 2006). Without consideration of
such implications, the stock management program of
masu salmon would become an insufficient exercise.
3) Migratory behaviors seem to be regulated by both
physiological and environmental factors. As a result,
it is important to prevent artificial physiological and
environmental disruptions that potentially become
stressors and influence the migratory behaviors. For
example, we need to focus our attentions not only on
the direct impacts of dam constructions, but also on
the concomitant modifications in flow, temperature,
and turbidity, which all have a natural cycle critical to
fish.
4) Since most of the 2+ masu salmon migrant smolts
that migrate from the sea will stay in the deeper areas
of the mid reaches in their natal rivers throughout the
summer, where they can avoid predation and sudden
changes in water flow and temperature, the conservation of habitat diversity not only in upper reaches
(spawning ground), but also in entire rivers is essential.
Acknowledgments
This study was supported partly by research fellowships
from the Japan Society for the Promotion of Science and the
Saito Houonkai Research Grant. I am grateful to Prof.
Katsumi Aida, for providing the opportunity to write this
monograph. I thank Dr. Shoji Kitamura, Dr. Kazumasa Ikuta,
Dr. Masafumi Amano, Dr. Makito Kobayashi, Dr. Takashi
Yada, Dr. Hidenobu Yambe, Dr. Carl Schreck, Dr. Hiram Li,
and Dr. David Noakes for their input and for their open discussion of many of these investigations. Mr. Toshio Shikama
and Mr. Hidefumi Nakamura helped in part of experiments.
I am also grateful to Dr. Hiram Li, Mr. Ralph Lampman,
and Mr. Aalon Brock for reading the manuscript and providing useful advice, and Dr. Tsukasa Fukushi, Dr. Nobuharu
Goto, Dr. Kimiharu Ishizawa, Dr. Ryusaku Deguchi and Mr.
Hiroki Suzuki for their conceptual support during the research. I would also like to thank Mr. Akira Shishido for
teaching and helping with the masu salmon sampling in the
Kesen River from 2004 through 2009.
References
Aida K, Kato T, Awaji M. Effects of castration on the
smoltification of precocious male masu salmon
Oncorhynchus masou. Nippon Suisan Gakkaishi 1984; 50:
565–571.
Amano M, Aida K, Okumoto N, Hasegawa Y. Changes in
salmon GnRH and chicken GnRH-II contents in the brain
and pituitary, and GTH II contents in the pituitary in female masu salmon, Oncorhynchus masou, from hatching
through ovulation. Zool. Sci. 1992; 9: 375–386.
Amano M, Aida K, Okumoto N, Hasegawa Y. Changes in
levels of GnRH in the brain and pituitary and GTH in the
pituitary in female masu salmon, Oncorhynchus masou,
from hatching to maturation. Fish. Physiol. Biochem. 1993;
11: 233–240.
Amano M, Hyodo S, Kitamura S, Ikuta K, Suzuki Y, Urano
A, Aida K. Salmon GnRH synthesis in the preoptic area
and the ventral telencephalon is activated during gonadal
maturation in female masu salmon. Gen. Comp.
Endocrinol. 1995; 99: 13–21.
Barton BA, Schreck CB. Influence of acclimation temperature on internal and carbohydrate stress responses in juvenile chinook salmon (Oncorhynchus tshawytscha).
Aquaculture 1987; 62: 299–310.
Berglund I, Lundqvist H, Fangstan H. Downstream migration of immature salmon (Salmo salar) smolts blocked by
implantation of the androgen 11-ketoandrostendione.
Aquaculture 1994; 121: 269–276.
Boeuf G. Salmonid smolting: a pre-adaptation to the oceanic environment. In: Rankin GC and Jenson GB (eds.).
Fish Ecophysiology. Chapman and Hall. 1994.
Boeuf G, LeBail PY, Prunet P. Growth hormone and thyroid
hormones during Atlantic salmon, Salmo salar L.,
smolting, and after transfer to seawater. Aquaculture 1989;
82: 257–268.
Boeuf G, Marc AM, Prunet P, Bail PYL, Smal J. Stimulation of parr-smolt transformation by hormonal treatment
in Atlantic salmon (Salmo salar L.). Aquaculture 1994;
121: 195–208.
Dickhoff WW, Beckman BR, Larsen DA, Duan C, Moriyama
S. The role of growth in endocrine regulation of salmon
smoltification. Fish Physiol. Biochem. 1997; 17: 231–236.
Ewing RD, Barratt D, Garlock D. Physiological changes related to migration tendency in rainbow trout
(Oncorhynchus mykiss). Aquaculture 1994; 121: 277–287.
Frantzen M, Johnsen HK, Mayer I. Gonadal development
and sex steroids in a female Arctic charr brood stock. J.
Fish Biol. 1997; 51: 697–709.
Fujioka Y, Fushiki S, Tagawa M, Ogasawara T, Hirano T.
Downstream migratory behavior and plasma thyroxine
levels of Biwa salmon, Oncorhynchus rhodurus. Nippon
Suisan Gakkaishi 1990; 56: 1773–1779.
Giannico RG, Hinch SG. The effect of wood and temperature on juvenile coho salmon winter movement, growth,
density and survival in side-channels. River Res. Applic.
2003; 19: 219–231.
Grau EG, Dickhoff WW, Nishioka RS, Bern HA, Folmar LC.
Lunar phasing of the thyroxine surge preparatory to seaward migration of salmonid Fish. Sci. 1981; 211: 607–
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
609.
Groot C, Margolis L (eds.). Pacific Salmon Life Histories.
UBC Press, British Columbia, Vancouver. 1991.
Gross M. Evolution of diadromy in fishes. Am. Fish. Soc.
Symp. 1987; 1: 14–25.
Heard RH. Life history of pink salmon (Oncorhynchus
Gorbuscha). In: Groot C, Margolis L (eds.). Pacific
Salmon Life Histories. UBC Press, British Columbia, Vancouver. 1991; 119–230.
Hirano T. Endocrine control of osmoregulation in migratory
fishes. In: Mauchline J, Nemoto T (eds.). Marine Biology: Its Accomplishment and Future Prospect. Hokusensha, Japan. 1991, 3–14.
Hoar WS. Smolt transformation: evolution, behavior, and
physiology. J. Fish. Res. Bd. Canada. 1976; 33: 1233–
1252.
Hoar WS. The physiology of smolting salmonids. In: Hoar
WS, Randall DJ (eds.). Fish Physiology, Vol. II B. Academic Press, New York. 1988; 275–343.
Hutchison MJ, Iwata M. Effect of thyroxine on the decrease
of aggressive behaviour of four salmonids during the parrsmolt transformation. Aquaculture 1998; 168: 169–175.
Ikuta K. Effects of steroid hormones on migration of
salmonid fishes. Bull. Natl. Inst. Aquacult. Suppl. 1994;
2: 23–27.
Ikuta K, Aida K, Okumoto N, Hanyu I. Effects of thyroxine
and methyletestosterone on smoltification of masu salmon
(Oncorhynchus masou). Aquaculture 1985; 45: 289–303.
Ikuta K, Aida K, Okumoto N, Hanyu I. Effects of sex steroids on the smoltification of masu salmon, Oncorhynchus
masou. Gen. Comp. Endocrinol. 1987; 65: 99–110.
Iwata M. Downstream migratory behavior of salmonids and
its relationship with cortisol and thyroid hormones: A review. Aquaculture 1995; 135: 131–139.
Iwata M. Downstream migratory behaviors and endocrine
control of salmonid fishes. Bull. Natl. Res. Inst. Aquacult.
1996; Suppl. 2: 17–21.
Iwata M, Yamauchi K, Nishioka RS, Lin R, Bern HA. Effects of thyroxine, growth hormone and cortisol on salinity preference of juvenile coho salmon (Oncorhynchus
kisutch). Mar. Behav. Physiol. 1990; 17: 191–201.
JoAnna LL, Richard WM. Influence of marine-derived nutrients from spawning salmon on aquatic insect communities in southeast Alaskan streams. Oikos 2006; 113(2):
334–343.
Johnsson JI, Petersson E, Jönsson E, Björnsson BTh, Järvi
T. Domestication and growth hormone alter anti-predator
behavior and growth patterns in juvenile brown trout,
Salmo trutta. Can. J. Fish. Aquat. Sci. 1996; 53(7): 1546–
1554.
Jönsson E, Johnsson JI, Björnsson BTh. Growth hormone
increases predation exposure of rainbow trout. Proc. Roy.
Soc. Lond. Ser. B. 1996; 263: 647–651.
Kagawa H, Young G, Nagahama Y. Estradio-17 β production in isolated amago salmon (Oncorhynchus rhodurus)
ovarian follicles and its stimulation by gonadotropins. Gen.
Comp. Endocrinol. 1982a; 47: 361–365.
Kagawa H, Young G, Adachi S, Nagahama Y. Estradiol-17β
production in amago salmon (Oncorhynchus rhodurus)
ovarian follicles: role of the thecal and granulosa cells.
Gen. Comp. Endocrinol. 1982b; 47: 440–448.
Kagawa N, Mugiya Y. Exposure of goldfish (Carassius
63
auratus) to bluegills (Lepomis macrochirus) enhances
expression of stress protein 70 mRNA in the brains and
increases plasma cortisol levels. Zool. Sci. 2000; 17: 1061–
1066.
Kato F. Life histories of masu and amago salmon
(Oncorhynchus masou and Oncorhynchus rhodurus). In:
Groot C, Margolis L (eds.). Pacific Salmon Life Histories. UBC Press, British Columbia, Vancouver. 1991; 448–
520.
Kelsey DA, Schreck CB, Congleton JL, Davis LE. Effects
of juvenile steelhead on juvenile chinook salmon behavior
and physiology. Transactions of the American Fisheries
Society 2002; 131: 676–689.
Kiso K. Polymorphism of life form in masu salmon
(Oncorhynchus masou) in the rivers of southern Sanriku
District, Honshu, Japan. Bull. Inst. Zool. Academia Sinica
1990; 29(3): 27–39.
Kiso K. The life history of masu salmon Oncorhynchus
masou originated from rivers of the Pacific coast of northern Honshu, Japan. Bull. Natl. Res. Inst. Fish. Sci. 1995;
7: 1–188 (in Japanese with English abstract).
Kiso K, Matsumiya Y. Growth of the fluviatile form masu
salmon Oncorhynchus masou in rivers of southern Sanriku
District, Honshu, Japan. Nippon Suisan Gakkaishi 1992;
58: 9–13.
Kobayashi M, Aida K, Hanyu I. Gonadotropin surge during
spawning in male goldfish. Gen. Comp. Endocrinol. 1986;
62: 70–79.
Kobayashi M, Aida K, Hanyu I. Hormone changes during
the ovulatory cycle in goldfish. Gen. Comp. Endocrinol.
1988; 69: 301–307.
Liley NR, Fostier A, Breton B, Tan ES. Endocrine changes
associated with spawning behavior and social stimuli in a
wild population of rainbow trout (Salmo gaidneri). Gen.
Comp. Endocrinol. 1986; 62: 157–167.
Lou SW, Aida K, Hanyu I, Sakai K, Nomura M, Tanaka M,
Tazaki S. Endocrine profiles in the female of a twiceannually spawning strain of rainbow trout. Aquaculture
1984; 43: 13–22.
Machidori S, Kato F. Spawning populations and marine life
of masu salmon Oncorhynchus masou. Int. North Pacific
Fisheries Commission 1984; 43: 1–138.
Mayer I, Liley N, Borg B. Stimulation of spawning behavior
in castrated rainbow trout (Oncorhynchus mykiss) by
17 α ,20 β -dihydroxy-4-pregnene-3-one, but not by 11ketoandrostendione. Hormones and Behavior 1994; 28:
181–190.
McCormick SD. Endocrine control of osmoregulation in
teleost fish. American Zool. 2001; 41: 781–794.
Miwa S, Inui Y. Inhibitory effects of of 17 α-methyle testosterone and estradiol-17β on smoltification of sterilized
amago salmon (Oncorhynchus rhodurus). Aquaculture
1986; 53: 21–39.
Mizuno S, Ura K, Onodera Y, Fukada H, Misaka N, Hara A,
Adachi S, Yamauchi K. Changes in transcript levels of
gill cortisol receptor during smoltification in wild masu
salmon, Oncorhynchus masou. Zool. Sci. 2001; 18: 853–
860.
Munakata A, Kobayashi M. Endocrine control of sexual
behavior in teleost fish. Gen. Com. Endocrinol. 2010; 165:
456–468.
Munakata A, Amano M, Ikuta K, Kitamura S, Aida K. Growth
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
64
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
of wild honmasu salmon parr in a tributary of Lake
ChuzenjiGrowth masu salmon, Oncorhynchus masou.
Fish. Sci. 1999; 65(6): 965–966.
Munakata A, Björnsson BTh, Jönsson E, Amano M, Ikuta
K, Kitamura S, Kurokawa T, Aida K. Post-release adaptation processes of hatchery-reared honmasu salmon parr.
J. Fish Biol. 2000a; 56: 163–172.
Munakata A, Amano M, Ikuta K, Kitamura S, Aida K. Inhibitory effects of testosterone on downstream migratory
behavior in masu salmon, Oncorhynchus masou. Zool. Sci.
2000b; 17: 863–870.
Munakata A, Amano M, Ikuta K, Kitamura S, Aida K. The
involvement of sex steroid hormones in downstream and
upstream migratory behavior of masu salmon. Comp.
Biochem. Physiol. Part B 2001a; 129: 661–669.
Munakata A, Amano M, Ikuta K, Kitamura S, Aida K. The
effects of testosterone on upstream migratory behavior in
masu salmon, Oncorhynchus masou. Gen. Comp.
Endocrinol. 2001b; 122: 329–340.
Munakata A, Amano M, Ikuta K, Kitamura S, Aida K. Sex
steroids control migration of masu salmon. Fish. Sci. 2002;
68 Suppl. 1: 49–52.
Munakata A, Amano M, Ikuta K, Kitamura S, Aida K. Effects of growth hormone and cortisol on the downstream
migratory behavior in masu salmon, Oncorhynchus masou.
Gen. Comp. Endocrinol. 2007; 150: 12–17.
Munakata A, Amano M, Ikuta K, Kitamura S, Aida K. Involvement of sex steroids and thyroid hormones in upstream and downstream behaviors in masu salmon,
Oncorhynchus masou. Aquaculture 2012a; 362–363: 158–
166.
Munakata A, Amano M, Ikuta K, Kitamura S, Aida K. Involvement of sex steroids, luteinizing hormone and thyroid hormones in upstream and downstream migratory
behaviors in land-locked sockeye salmon Oncorhynchus
nerka. Fish. Sci. 2012b; 78: 81–90.
Murata S, Takasaki N, Saitoh M, Okada N. Determination
of the phylogenic relationships among Pacific salmonids
by using short interspersed elements (SINEs) as temporal
landmarks of evolution. Proc. Nat. Acad. Sci. USA. 1993;
90: 6995–6999.
Nagae M, Fuda H, Hara A, Saneyoshi M, Yamauchi K.
Changes in serum concentrations of immunoglobulin M
(IgM), cortisol and thyroxine (T4) during smoltification
in the masu salmon Oncorhynchus masou. Fish. Sci. 1994;
60(2): 241–242.
Nagahama Y. Mechanism of gonadotropin control of steroidogenesis in teleost gonads. In: Gunma Symp.
Endocrinol. Center for Academic Publication, Tokyo, Japan. 1984; 21: 167–182.
Nagahama Y. Gonadotropin action on gametogenesis and
steroidogenesis in teleost gonads. Zool. Sci. 1987a; 4(2):
209–222.
Nagahama Y. 17α ,20β-Dihydroxy-4-pregnen-3-on a teleost
maturation-inducing hormone. Develop. Growth and Differ. 1987b; 29(1): 1–12.
Nakano S. Individual differences in resource use, growth
and emigration under the influence of a dominance hierarchy in fluvial red-spotted masu salmon in a natural habitat. J. Animal Ecol. 1995; 64: 75–84.
Nakano S, Furukawa-Tanaka T. Intra- and interspecific dominance hyerarchy and variation in foraging tactics of two
species of stream-dwelling chars. Ecol. Res. 1994, 9: 9–
20.
Nakano S, Kachi T, Nagoshi M. Restricted movement of the
fluvial form of red-spotted masu salmon, Oncorhynchus
masou rhodurus, in a mountain stream, central Japan.
Japanese J. Ichthyol. 1990; 37(2): 158–163.
Neave F. The origin and speciation of Oncorhynchus. Trans.
Roy. Soc. Canada 1958; 551: 25–39.
Nichols DJ, Weisbart M. Plasma cortisol concentrations in
Atlantic salmon, Salmo salar: Episodic variations, diurnal changes, and short term response to adrenocorticotrophic hormone. Gen. Comp. Endocrinol. 1984; 56: 169–
176.
Norden CR. Comparative osteology of representative
salmonid fishes, with particular reference to the grayling
(Thymallusus arcticus) and its phylogeny. J. Fish. Res.
Bd. Can. 1961, 18: 679–791.
Nordeng H. Solution to the “char problem” based on Arctic
char (Salvelinus alpinus) in Norway. Can. J. Aquat. Sci.
1983; 40: 1372–1387.
Ojima D, Iwata M. Central administration of growth
hormone-releasing hormone triggers downstream movement and schooling behavior of chum salmon
(Oncorhynchus keta) fry in an artificial stream. Comp.
Biochem. Physiol. Part A. 2009; 152: 293–298.
Oshima M. Ecological study on the masu of the Taiko River.
Botany and Zoology 1936; 4: 1–13.
Pankhurst NW, Kraak GVD. Evidence that acute stress inhibits ovarian steroidogenesis in rainbow trout in vivo,
through the action of cortisol. Gen. Comp. Endocrinol.
2000; 117: 225–237.
Prat F, Sumpter JP, Tyler CR. Validation of radioimmunoassay for two salmon gonadotropins (GTH I and GTH
II) and their plasma concentrations throughout the reproductive cycle in male and female rainbow trout
(Oncorhynchus mykiss). Biol. Reproduction. 1996; 54:
1375–1382.
Prunet P, Boeuf G, Bolton JP, Young G. Smoltification and
seawater adaptation in Atlantic salmon (Salmo salar):
Plasma prolactin, growth hormone, and thyroid hormones.
Gen. Comp. Endocrinol. 1989; 74: 355–364.
Quinn, TP. The Behavior and Ecology of Pacific Salmon and
Trout. University of Washington Press, Seattle. 2005. 378
pp.
Redding JM, Schreck CB, Everest FH. Physiological effects
on coho salmon and steelhead of exposure to suspended
solids. Transactions American Fisheries Society 1987; 116:
737–744.
Sandercock FK. Life history of coho salmon (Oncorhynchus
kisutch). In: Groot C, Margolis L (eds.). Pacific Salmon
Life Histories. UBC Press, British Columbia, Vancouver.
1991; 396–445.
Sano S. Changes in masu salmon during the no-feeding season. Salmon J. 1947; 44: 9–14.
Sato A, Ueda H, Fukaya M, Kaeriyama M, Zohar Y, Urano
A, Yamauchi K. Sexual differences in homing profiles and
shortening of homing duration by gonadotropin-releasing
hormone analog implantation in lacustrine sockeye salmon
(Oncorhynchus nerka) in Lake Shikotsu. Zool. Sci. 1997;
14: 1009–1014.
Satou M, Oka Y, Kusunoki M, Matsushima T, Kato M, Fujita
I, Ueda K. Telencephalic and preoptic areas integrate
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.
A. Munakata / Aqua-BioSci. Monogr. 5: 29–65, 2012
sexual behavior in hime salmon (landlocked red salmon,
Oncorhynchus nerka): results of electrical brain stimulation experiments. Physiol. Behav. 1984; 33: 441–447.
Schreck CB. Accumulation and long-term effects of stress
in fish. In: Moberg G, Mench J (eds.). The Biology of Animal Stress. C.A.B. International Press, Wallingford, U.K.
2000; 147–158.
Slater CH, Schreck CB, Swanson P. Plasma profiles of the
sex steroids and gonadotropins in maturing female spring
chinook salmon (Oncorhynchus tshawytscha). Comp.
Biochem. Physiol. 1994; 109A: 167–175.
Swanson P. Salmon gonadotropins: Reconciling old and new
ideas. In: Scott et al. (eds.). Proc. Fourth Int. Symp Reproductive Physiology of Fish. University of East Anglia,
Norwich. 1991; 2–7.
Thorpe JE. An alternative view of smolting in salmonid.
Aquaculture 1994; 121: 105–113.
Truscott B, Idler DR, So YP, Walsh JM. Maturation steroids
and gonadotropin in upstream migratory sockeye salmon.
Gen. Comp. Endocrinol. 1986; 62: 99–110.
Tsukamoto K, Aida K, Otake T. Plasma thyroxine concentration and upstream migratory behavior of juvenile ayu.
Nippon Suisan Gakkaishi 1988; 54(10): 1687–1693.
Ueda H, Hiroi O, Hara A, Yamauchi K, Nagahama Y.
Changes in serum concentrations of steroid hormones,
thyroxine, and vitellogenine during spawning migration
of the chum salmon, Oncorhynchus keta. Gen. Comp.
Endocrinol. 1984; 53: 203–211.
Utoh H. Study of the mechanism of differentiation between
the stream resident form and the seaward migratory form
in masu salmon, Oncorhynchus masou Brevoort, I. Growth
and gonadal maturity of precocious masu salmon parr. Bull.
Fac. Fish. Hokkaido Univ. 1976; 26: 321–326 (in Japanese).
Utoh H. Study of the mechanism of differentiation between
the stream resident form and the seaward migratory form
in masu salmon, Oncorhynchus masou Brevoort, II.
Growth and sexual maturity of precocious masu salmon
parr (2). Bull. Fac. Fish. Hokkaido Univ. 1977; 28: 66–73
(in Japanese).
Varnavsky VS, Sakamoto T, Hirano T. Effects of premature
65
seawater transfer and fasting on plasma growth hormone
levels of yearling coho salmon (Oncorhynchus kisutch)
parr. Aquaculture 1995; 135: 141–145.
Yada T, Nagae M, Moriyama S, Azuma T. Effects of prolactin and growth hormone on plasma immunoglobulin M
levels of hypophysectomized rainbow trout, Oncorhynchus
mykiss. Gen. Comp. Endocrinol. 1999; 115: 46–52.
Yada T, Azuma T, Hyodo S, Hirano T, Grau EG, Schreck
CB. Differential expression of corticosteroid receptor
genes in rainbow trout (Oncorhynchus mykiss) immune
system in response to acute stress. Can. J. Fish Aqua Sci.
2007; 64(10): 1382–1389.
Yamauchi K, Koide N, Adachi S, Nagahama Y. Changes in
seawater adaptability and blood thyroxine concentrations
during smoltification of the masu salmon, Oncorhynchus
masou, and the amago salmon, Oncorhynchus rhodurus.
Aquaculture 1984; 42: 247–256.
Yamauchi K, Ban M, Kasahara N, Izumi T, Kojima H, Harako
T. Physiological and behavioral changes occurring during
smoltification in the masu salmon, Oncorhynchus masou.
Aquaculture 1985; 45: 227–235.
Yambe H, Munakata A, Kitamura S, Aida K, Fusetani N.
Methyltestosterone induces male sensitivity to both primer
and releaser pheromones in the urine of ovulated female
masu salmon. Fish Physiol. Biochem. 2003; 28: 279–280.
Yambe H, Kitamura S, Kamio M, Yamada M, Matsunaga S,
Fusetani N. L-Kynurenine, and amino acid identified as a
sex pheromone in the urine of ovulated female masu
salmon. Proc. Natl. Acad. Sci. USA 2006; 103: 15370–
15374.
Young G, Björnsson BTh, Prunet, P, Lin, RJ, Bern, HA.
Smoltification and seawater adaptation in coho salmon
(Oncorhynchus kisutch): Plasma prolactin, growth hormone, thyroid hormones, and cortisol. Gen. Comp.
Endocrinol. 1989; 74: 335–345.
Zydlewski GB, Haro A, McCormick D. Evidence for cumulative temperature as an initiation and terminating factor
in downstream migratory behavior of Atlantic salmon
(Salmo salar) smolts. Can. J. Fish. Aquat. Sci. 2005; 62:
68–78.
doi:10.5047/absm.2012.00502.0029 © 2012 TERRAPUB, Tokyo. All rights reserved.