Scientific Reports of the
Hokkaido Salmon Hatchery
No SO: 101-111, November 1996

Effects of Population Density and Habitat Environment onLife History Strategy and Migration of Juvenile
Sockeye (Oncorhynchus nerka) and Chum Salmon (0.keta)
Masahide Kaeriyama
Research Division, Hokkaido Salmon Hatchery, Fisheries Agency of Japan,
2-2 Nakanoshima, Toyohira-ku, Sapporo 062, Japan
Abstract. - Life hlstories of juvenile sockeye (Oncorhynchus nerku) and chum salmon (0.
keta)
show a conditional strategy which have two tactics of residence and migration. They usually remain inlakc and river if they can sufficiently obtain their resources such as food and habitat, whereas salmon
migrate seaward when they do not have enough those resources satisfying their energy metabolism.
Their migration pattern, controlled by effects of “prior residence” and “precedent migration”, may
involve a trade-off between the profitability of resource acquisition and risks such as osmoregulation,energetic demands of swimming, exposure to predators, and mobilization to non-adaptable habitat bywater current.

Introduction
The migrations of fishes are generally classed
biologically as “alimental ” for food procurement,‘2lirnatic ” for reaching a region of better climate,‘kametic” for reproduction (Harden-Jones, 1968),
and oceanographically as “mobilization” by water
current (McKeown, 1984). For diadromous fishes,
alimental and gametic migrations influence theiradaptation and differentiation through intraspecificcompetition.
McDowall (1987) estimated the total number offish species as about 20,000 and considered that 162(0.8%) of these are diadromous. Of these species, 87(54%) are anadromous, 41 (25%) catadromous, and
34 (21%) amphidromous. Baker (1978) showed thatanadromy is greatest in polar-temperate environments, and that catadromy is greatest in the tropics.
Anadromous species have evolved when foodresources in the sea exceed those in fresh water, andcatadromous species have evolved when freshwater
food resources exceed those in the sea (Gross, 1987).
Pacific salmon would have obtained the ability ofhoming migration for maximizing reproductive success in fresh water.
The purpose of this paper is to review the migration of Pacific salmon by focusing on the life history
strategy of sockeye salmon (0.nerka), which have aContribution A No. 355 from the Hokkaido Salmon Hatchery.

diverse pattern of life history, and chum salmon (0.
keta), which migrate seaward immediately after the
emergence.

Ocean Distribution and Biomass ofPacific Salmon
Figure 1 shows the known ocean distribution bya species in Pacific salmon. Masu salmon (0.rnasu)
has a limited distribution around coastal seas of the
Far East. On the other hand, pink salmon (0. gorbuscha) has the widest distribution to the North
Pacific Ocean in the 6 species. The relationshipbetween the ocean distribution and the biomass ofthem indicates that a species which ranges a wider
area can have more abundance in the North Pacific
Ocean (Fig. 2).
Figure 3 demonstrates distribution areas ofunderyearling Pacific salmon at the downstream
migration. Masu and coho (0.kisutch) salmon spend
in the river for at least one or two years before
migrating seaward as smolt. Most individuals of chinook (0. tshuwytscha) and sockeye salmon usually
rear in the freshwater for one or more years before
seaward migration. A part of them, however, enter
the sea at the underyearling stage such as ocean-type
or sea-type stocks (Wood et al., 1987; Clarke et al.,1989). Numerous fry chum salmon migrate seaward
immediately after the emergence. Only a few juvenile
spend in the river for several months (Kaeriyama,1986). All of pink salmon enter to the sea as fry

101 -2 IT . 5 TAWE scr.REP. HOKKAIDO SALMON HATCHERY, NO. 50,1996

Masu salmon

Sockeye salmon

Coho salmon

Chinook salmon

150E 160E

170E

Pink salmon

180 170W 160W 150W 140W

150E

160E

170E

180 170W 160W 150W 140W

Fig. 1. Known ocean distribution of 6 species in the genus Oncorhynchus (Kaeriyama, 1985).

0

so

100

1 so

200

250

Ocean Distribution Index
Fig. 2. Relationship between the ocean distribution index and the biomass in Pacific salmon. The ocean distribution index indicatesmatrix numbers of 2' X5' area where salmon were caught until 1985. The biomass shows average catch by species in 1952-1975(Kaeriyama, 1985).

- 102

KAERTYAMA-LIFE HISTORY STRATEGY OF SOCKEYE AND CHUM SALMON

FreshwaterSpecies-(River or Lake)

Sea
Estuary
Coast

Masu
Coho

Chinook
Sockeye
Chum

1

Pink

r
I
I
I I
I
I
I
I
I
I
I
I
.I
I
I
I

-

-

-

1

1

1

1

1

1

1

1

- 1

Fig. 3. Distribution areas of underyearling Pacific salmon at the downstream migration.

immediately after the emergence (Heard, 1991).
In six species of Pacific salmon (genus
Oncorhynchus), namely, a species that migrates seaward at an earlier developmental stage may havegreater abundance and a wider area of ocean distribution than later migrants (Kaeriyama, 1985).

anadromous parents. A part of them, however,remain in fresh water to mature and reproduce. The
residual population tends to have a higher growth rate
and to mature at an earlier age than the anadromous
population (Ricker 1938; Simimov, 1959). The kokanee, on the other hand, have fully adapted to freshwater life. Ricker (1940) considered the evolution of
kokanee as the following two steps: (i) the occurrence of “residual’’ offspring among the progenyof an anadromous stock; and (ii) the modification of
the progeny of residuals into the typical kokanee. In
anadromous sockeye salmon, juveniles typically rearin lakes for one or more years before the seaward
migration (lake type). Some individuals in northem
populations go to the sea immediately after theiremergence (sea type) or inhabit river channels for at

Migration and Freshwater Residence ofSockeye Salmon
Sockeye and chinook salmon exhibit the mostdiverse life histories in Pacific salmon. For instance,
adult sockeye salmon have the most number of cornmon age-groups in Pacific salmon (Table 1).
Although sockeye are primarily anadromous, there
are distinct populations called “residual” sockeye andkokanee salmon. Residual sockeye are progeny ofTable 1. The most common age-groups of genus Oncorhynchus by species based on Major et al. (1978), Healey (1986), Burgner(1991), Salo (1991), Healey (1991), and Sandercock (1991).
Species
Pink Salmon
Chum salmon
Sockeye salmon

Age-groups
0.1*
0.1*,0.2*,0.3*, 0.4*,0.5*
0.2,0.3,0.4,0.5,1.0*, 1.1*, 1.2*, 1.3*, 1.4,
2.1*,2.2*,2.3, 2.4, 3.1, 3.2, 3.3, 3.4, 4.1,4.2,4.3

Chinook salmon

0.1,0.2,0.3,0.4, 0.5. 1.1, 1.2, 1.3, 1.4, 1.5, 1.6,

Coho salmon
Masu salmon

2.1, 2.2, 2.3,2.4, 2.5
1.0, 1.1, 2.1, 3.1,4.1
1.1*, 2.1*

* Common age-groups in Japan.

103 -Numbers

3 Ij. 'd $,Lhaff%i SCI REP HOKKAIDO SALMON HATCHERY, NO. 50,1996

least one year (river type) (Wood et al., 1987).
Residual sockeye salmon are produced by an
artificial enhancement program in Lake Shikotsu.
They were originally transplanted from the residual
population in Lake Akan, Hokkaido Island, in 1893
and from an anadromous population in Lake
Urumobetsu, Iturup Island, during 1925-1940.
Although they have been geographically landlockedin Lake Shikotsu for more than 15 generations,smolts appear in this lake (Kaeriyama, 1991). Thosesmolts were released to a river flowing into the
Pacific Ocean and ascended the river as anadromous
sockeye salmon after 1-3 years. Most of the smolts, 3
years old (2+), migrated downstream between lateJune and early July. The age and season of these
Lake Shikotsu smolts during the downstream migration corresponded with the seaward migration timingof smolt sockeye salmon in Lake Urumobetsu,
although the lacustrine-limnological environment in
Lake Shikotsu differs much from that in Lake
Urumobetsu. On the other hand, progeny of sockeye
salmon derived from the Lake Shikotsu and returning
as anadromous type had several life history patterns
such as precocious, residual, and anadromous type
(Kaeriyama et al., 1992; Kaeriyama, 1994).

20 -In Lake Shikotsu, smolts were smaller thanresidual fish (Fig. 4). Based on the allometry between
fork length and body weight (Fig. 5) and the condition factor (Fig. 6), Lake Shikotsu sockeye salmon
smolts are more slender in body shape than residuals.
Figure 7 shows a relationship between population
size and smolt rate (number of smolts / populationsize) for Lake Shikotsu sockeye salmon. In 19841986, smolts (145 -t 4 mm) were significantly smaller (P < 0.001) in fork length and smolt rate were significantly higher (P < 0.001) than those in other years(183
15 mm). A significant positive relationshipbetween population size and smolt rate was observed
except for the 1984-1986 populations (r = 0.8404, P< 0.01). These results indicate that (1) their residenceor seaward migration may be affected by both the
population density and the resource condition, whichreflects their growth, in the lake, and that (2) they
may migrate seaward when they do not fully benefit
from their resources.
These results also suggest that the life history ofsockeye salmon may be a conditional strategy which
has two tactics of residence and migration. Namely,
Lake Shkotsu sockeye salmon usually remain in thelake as a residual type if they can obtain sufficient*rn
Residual

18:

1614:

2 121

8g 101
k

8;

6:
4-

2:
1

1

20

30

40

50

60

70

80

90

100

Body weight (g)Fig. 4. Frequency distributions of body weight of residual and m o l t sockcyc salmon (age 2+) collected in Lake Shikotsu on July 15,
1987.

- 104 -

KAERIYAMA-LIFE HISTORY STRATEGY OF SOCKEYE AND CHUM SALMON

100 1
90

80
(r=0.9J6-lh * * )

n

70

E'
M
'G 60
%
m

h

g so
2.9183

W=O.O112L(1-0.9726""")

40
30

I

1s

14

"

16

I

I

I

17

18

19

I

" I '

20

21

Fig. 5. Relationships between fork length and body weight of residual and m o l t sockeye salmon (age 2+) collected in Lake Shlkotsu
on July 15, 1987.

30
25

5
0

8.0

8.5

9.0

9.5

10.0 10.5 11.0 11.5 12.0 12.5 13.0

Condition factor
Fig. 6. Frequency distributions of condition factors of residual and smolt sockeye salmon (age 2+) collected in Lake Shikotsu on July
15. 1987.

105 -

2 If

b-V248% SCI REP. HOKKAIDO SALMON HATCHERY, NO. 50,1996

90

80
n
70
0

-60

2

Q)

c,

50
40

rn

0 30

E 20
rn
10
0

0

5000

10000 15000 20000 25000 30000 35000 40000 45000 50000

Population size
Fig. 7. Relationship between population size (P) and smolt rate (S) of lacustrine sockeye salmon in Lake Shikotsu: S = 0.0000045P +0.0699 (r = 0.8404, P < 0.01). The population size shows total numbers of smolt and adult, and the smolt rate represents the num15 mm in 1978-1983 and 1987-1988
ber of smolt per population size in a population. Fork lengths of smolt population are 183(closed circles), and 145 & 4 mm in 1984-1986 (open circles). Data are obtained from Kaeriyama (1991).

*

resources such as food and habitat, whereas a part ofthe population migrates seaward as smolts after one
or two years in the lake when they do not haveenough resources to satisfy their energy metabolism.

Migration Pattern of Juvenile Chum Salmon
For juvenile chum salmon, the migration patternis controlled by effects of “prior residence” in spawning areas and “precedent migration” in rivers and atsea (Kaeriyama, 1986). Juvenile chum salmon
migrate from late winter to early summer in Japan.
Only a few fry emerging initially from spawning
redds in early spring remain in rivers for several
months with low specific growth rate (Fig. 8). Theseprior individuals tend to dominate over numerous
posterior individuals in the river (Kaeriyama, 1996).
Numerous juveniles migrate downstream immediately after the emergence. Especially, most enhanced
juveniles migrate seaward at the fry stage (FL < 50mm) less than 10 days after release because of highpopulation density (Kaeriyama and Sato, 1979;
Mayama et al., 1982). There is a significant difference (P <in fork length during the seaward
migration between wild population (54 f 7 mm)staying during long period in the Bibi River at low
density and enhanced juveniles (40 f 6 mm) migrat-

ing seaward immediately after the release at highdensity in the Tokachi River (Fig, Y).
Because the chum salmon spawn in areas of
upwelling groundwater, there may be little changesof the water temperature and a few prey around thespawning area. Prior individuals, therefore, have a
low specific growth rate (SGR < 0.006). On the other
hand, numerous juvenile migrating downstream temporarily stay at the estuary, where has much food anda rise in water temperature in the spring. They rapidly
grow in the estuary (SGR > 0.01). Namely, growth
inversion occurs between a few prior-resident andnumerous migrating juveniles (Fig. 10).
Juvenile chum salmon remain in the coastal sea
for a time and migrate offshore at post-fingerlingstage. This offshore migration is usually preceded bylarger individuals, which have higher specific growthrate, than by others in a population (Kaeriyama,1986). For instance, larger marked juveniles released
into the l t a k a m i River in the spring of 1983 began
to migrate offshore and to eat pelagic organisms earlier than others. Juveniles caught offshore preyed on
pelagic organisms such as Thernistn japonica andEuphausia pacifica. They showed much better
growth than those from neritic or inshore waters,
which fed on coastal zooplankton and terrestrial

106 -

p

KAERIYAMA-LIFE HISTORY STRATEGY OF SOCKEYE AND CHUM SALMON80 .-- E 70.

L=32 EXP(0.00 5 1t)
r=0.9861*

//

E
60.
8
bfi

/
/
/
/

2 50.

3

8 40.

k

Jan

I Feb I Mar I Apr I May I Jun
MonthFig. 8. A growth curve of wild juvenile chum salmon captured and marked around the spawning area in the ltakami River during theperiod or January to June in 1980. L = 32enws"(r = 0.9861, P < 0.001). Data are obtained from Kaeriyama (1986).

400
350

Tokachi River(n = 848)

300
h250

u

51 2 0 0

cz 150
100
50

0
30

35

40

45

SO

55

60

65

70

75

80

85

90

Fork length (mm)Fig. 9. Frequency distribution of fork length of juvenile chum salmon from Tokachi (enhanced) and Bibi (wild) rivers- 107 -

5 b j 'd -FA76$:g

SC1 REP. HOKKAIDO SALMON HATCHERY, NO 50.1996

2007

Precedent migrant

140

5 100

0

10

20

30

40

50

60

60 -

Prior resident

40Lc

L=35e 0.006t

40 -

0

20

40

60

80

100

120

140

160

180

Days after the emergence (t)Fig. 10. A model of growth invcrsion between il few prior-resident (SGR = 0.006) and numerous migrating juveniles chum salmon(SGR=0.010) in the river and at the coastal sea. The SGR shows a specific growth rate.

APR

I

MAY

I

JUN

Month
Fig. 11. Growth curves of marked juvenile chum salmon released from the Kitakami River (Kaeriyama, 1986). P ( . ), offshore migration type (food, pelagic organisms): C
neritic residence type (food, coastal zooplankton); I (a),shore residence type (food.

(o),terrestrial insects).

- 108 -

KAERIYAMA-LEE HISTORY STRATEGY OF SOCKEYE AND CHUM SALMON

Ishikari River

0

20

40

60

80

Oh River100

Days after release
Fig. 12. Multiple rcgression analysis in specific growth rate (G) of marked juveniles on days after release (t) and distance from releaseriver (k, km) in chum salmon population released from the Oh and Ishikari rivers (Modified from Kaeriyama 1986). Oh River, G =-1.450t + 1.853k + 163; Ishikari River, G = -1.010t + 0.147k +140.

insects, respectively (Fig. 11). On the other hand, asignificant multiple regression plane indicates thatthe specific growth rate of marked juvenile chumsalmon is a function of days after release and distancefrom the released river (Fig. 12). These results suggest that larger juveniles which higher growth ratemigrate more rapidly and farther away from releaserivers than those with higher population densities.
In summary, the life history strategy of chumsalmon may correspond with the conditional strategy
of sockeye salmon. The prior-resident individuals
may result from a phenotype of resident tactics in theconditional strategy. Their migration pattern indicatesthe precedent migration of larger juvenile. Because
this life history strategy is also known for m a w
salmon (0.masou) (Mayama, 1992), the conditional
strategy and the precedent migration pattern may
apply to all species of Pacific salmon.

Conclusion
Expanding the habitat area, therefore, species ofOncorhynchus are able to get more resources. In contrast, they incur many risks such as osrnoregulation,energetic demands of swimming, exposure to predators, mobilization to non-adaptable habitat by water
current with the expansion of distribution area.
Therefore, the benefits of their migration may
involve a trade-off between the profitability ofresource acquisition and risks associated with migration. The life history strategy and migration pattern ofthe genus Oncorhynchus evidently reflect an evolu-- 109

tion of anadromous fish that have acquired anadromy
for obtaining food resources in the sea and homing
ability for reproduction in the freshwater.

Acknowledgments
I especially thank Katherine W. Myers andKazuya Nagasawa edited the manuscript, and Mart R.
Gross and Masa-aki Fukuwaka for discussions on life
history evolution.

References
Baker, R. R. (1978): The evolutionary ecology of animal migration. Hodder and Stoughton, London.
1012 p.
Burgner, R. L. (1991): Life history of sockeye
salmon (Oncorhynchus nerka). In Pacific SalmonLife Histories (edited by C. Groot and L.
Margolis). UBC Press, Vancouver. pp. 1-118.
Clarke, W. C., J. E. Shelbourn, T. Ogasawara, and T.
Hirano (1989): Effects of initial daylength on
growth, seawater adaptability and plasma growth
hormone levels in underyearling coho, chinook
and chum salmon. Aquaculture, 82, 51-62.
Gross, M. R. (1987): Evolution of diadromy in fishes.
Am. Fish. Soc. Symp., 1, 14-25.
Harden-Jones, F. R. (1968): Fish migration. Edward
Arnold (Publishers) Ltd., London. 325 p.
Healey, M. C. (1986): Optimum size and age atmaturity in Pacific salmon and effects of sizeselective fisheries. Can. Spec. Publ. Fish. Aquat.
Sci., 89, 39-52.

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Healey, M. C. (1991): Life history of chinook salmon(Oncorhynchus tshawytscha). In Pacific SalmonLife Histories (edited by C. Groot and L.
Margolis). UBC Press, Vancouver. pp. 311-393.
Heard, W. R. (1991): Life history of pink salmon(Oncorhynchus gorbuscha). In Pacific SalmonLife Histories (edited by C. Groot and L.
Margolis). UBC Press, Vancouver. pp. 121-230.
Kaeriyama, M. (1985): Adaptation and differentiationof Oncorhynchus. Aquabiology, 7, 426-432. (InJapanese with English summary.)
Kaeriyama, M. (1986): Ecological study on early lifeof the chum salmon, Oncorhynchus keta
(Walbaum). Sci. Rep. Hokkaido Salmon Hatchery,(40), 31-92. (In Japanese with English summary.)
Kaeriyama, M. (1991): Dynamics of the lacustrine
sockeye salmon population in Lake Shikotsu,
Hokkaido. Sci. Rep. Hokkaido Salmon Hutchely,(45), 1-24. (In Japanese with English summary.)
Kaeriyama, M. (1994): Life history strategy of sockeye salmon. In Freshwater Fishes Migrating
between River and Sea (edited by A.Goto, K.
Tsukamoto, and K. Maekawa). Tokai Univ. Press,
Tokyo. pp. 101-113. (In Japanese.)
Kaeriyama, M. (1996): Population dynamics andstock management of hatchery-reared salmons inJapan. Bull. Natl. Res. Inst. Aquacult., Suppl. 2,
11-15.
Kaeriyama, M., and S. Sato (1979): Studies on a
growth and feeding habit of the chum salmon fry
during seaward migration in the Tokachi River
System -111. Relationship between migration timeand growth or the feeding behavior of the fry during 1977. Sci. Rep. Hokkaido Salmon Hatchery,(33), 47-73. (In Japanese with English summary.)
Kaeriyama, M., S. Urawa, and T. Suzuki (1992):
Anadromous sockeye salmon (Oncorhynchus
nerka) derived from nonanadromous kokanee: life
history in Lake Toro. Sci. Rep. Hokkaido Salmon
Hatchery, (46), 157-174.
Major, R. L., J. Ito, S. Ito, and H. Godfrey (1978):
Distribution and origin of chinook salmon(Oncorhynchus tshawytschu) in offshore waters of
the North Pacific Ocean. INPFC Bull., (38), 1-54.
Mayama, H. (1992): Studies on the freshwater lifeand propagation technology of masu salmon,- 110

Oncorhynchus masou (Brevoort). Sci. R e p .
Hokkaido Salmon Hatchery, (46), 1-156. (InJapanese with English summary.)
Mayama, H., M. Kato, J. Seki, and I. Shimizu (1982):
Studies on the chum salmon released in the
Ishikari River System - I. On the seaward migration and inshore distributions of liberated fry in
1979. Sci. Rep. Hokkaido Salmon Hatchery, (36),1-17. (In Japanese with English summary.)
McDowall, R. M. (1987): Evolution and importanceof diadromy: the occurrence and distribution ofdiadromy among fishes. Am. Fish. Soc. Symp., 1,
1-13.
McKeown, B. (1984): Fish migration. Croom Timber
Press, Beaverton. 224 p.
Ricker, W. E. (1938): “Residual” and kokanee
salmon in Cultus Lake. J. Fish. Res. Bd Can., 4,192-217.
Ricker, W. E. (1940): On the origin of kokanee, afreshwater type of sockeye salmon. Proc. Trans.
R. SOC.Can., Ser. 3,34, 121- 135.
Salo, E. 0. (1991): Life history of chum salmon(Oncorhynchus keta). In Pacific Salmon Life
Histories (edited by C. Groot and L. Margolis).
UBC Press, Vancouver. pp. 231-309.
Sandercock, F. K. (1991): Life history of coho
salmon (Oncorhynchus kisutch). In Pacific SalmonLife Histories (edited by C. Groot and L.
Margolis). UBC Press, Vancouver. pp. 395-445.
Smimov, A. I. (1959): Differences in the biology of
reproduction and development of residual or dwarf
sockeye and anadromous sockeye, Oncorhynchus
nerka (Walbaum). Nauchn. Dokl. Vyssh. Shk. Biol.
Nauk., 3, 59-65. (Transl. from Russian; Fish. Res.
Board Can. Transl. Ser. 266.)
Wood, C. C., B. E. Riddell, and D. T. Rutherford(1987): Alternative juvenile life histories of sockeye salmon (Oncorhynchus nerka) and their contrbution to production in the Stikine h v e r , Northern
British Columbia, I n Sockeye Salmon(Oncorhynchus nerka) Population Biology and
Future Management (edited by H. D. Smith, L.
Margolis, and C. C. Wood). Can. Spec. Publ. Fish.
Aquat. Sci., 96. pp. 12-24.

紺

"'"

棚

LIFE HISTORYSTRATEGY

OF SOCKEYE

AND

CHUM

SALMONべ二ザケ と サケ幼稚魚の 生活史戦略と回遊に 及ときは残留するが，彼らのエネルギー
代謝を満たずだけぼす個体群密度と 生息環境の 影苦の充分な資源が得られない場合は降海する． 彼らの回遊

帰山雅秀
べ二ザケ (Oncorけnchusner 比) とサケ (0 ． keta) 幼稚
2つの戦術からなる
条件戦略
魚の生活史は，残留と移動のを示す．幼稚
魚は， 餌料や生息場などの資源が得られる

パターンは，「先住効果」と「先行移動」により制御されており，浸透圧調節
能 ， 遊泳エネルギー要求量，被食，および海流による
不適な環境への移送などのリスクと 資源獲得の好適度とのトレード・オフにより決定されるのだろ "