Bulletin of the National Salmon
Resources Center, No. 2: 9-13
December 1999

Temporary Residence of Precocious Sockeye Salmon(Oncorhynchus nerka) in the Ocean
Shigehiko Urawa and Masahide Kaeriyama#Research Division, National Sulrnon Resources Center, Fisheries Agency of Japan,
2-2 Nakanoshima, Toyohira-ku, Sapporo 062-0922,Japan(urawa@ salmon. affrc.go,jp)
Abstract.- Ten precocious males of sockeye salmon (age 1.0, 190-220 mm in fork length) were

captured in the Bibi River of the Abira River system along the Pacific coast of Hokkaido, Japan,
during July and August 1994. Their origin was a hatchery-reared sockeye salmon stock (84-146 mm
in fork length) released in the river in the middle May of the same year. Most of precocious males
captured in the river were infected with the marine digenean parasites (Bruchyphallus crenatus
and/or Lecithaster gibbosus), indicating their ocean residence. The scale patterns suggested that theyrapidly grew in the ocean for at least 2 months. This may be the first report evidencing the seaward
migration of yearling precocious sockeye salmon and their temporary residence in the ocean environment.
Key words : sockeye salmon, precocious male, seaward migration, marine parasite, scale pattern

Introduction
Sockeye salmon (Oncorhynchus nerka) show
various life history patterns. They are typicallyanadromous fish, whose young usually remain in a
freshwater lake for at least a year before migrating tothe ocean. The length of their ocean life before
maturing varies from one to four years (Burgner1991). There are two forms that remain in fresh
water to mature and reproduce. One is kokanee, andthe other form is residual sockeye salmon. Theresidual sockeye salmon are mostly males in North
America, and they mature at the size of 16-38 cm inlength without ocean life (Ricker 1940).
In Japan, only residual sockeye salmon initially
reproduced in several lakes. Recently, however,anadromous sockeye populations are successfully
produced in several rivers on Hokkaido by artificial
enhancement using the residual form (Urawa 1991;
Kaeriyama et al. 1992). Since 1985 hatchery-reared
sockeye salmon smolts have been annually releasedin the Bibi River along the Pacific coast of Hokkai“resent address: Department of Marine Science andTechnology, Hokkaido Tokai University, Minamisawa,Minarni-ku, Sapporo 005-8601, Japan
Contribution A No. I 1 from the National Salmon
Resources Center.
0 1999 National Salmon Resources Center

do, Japan (Urawa et al. 1999). These fish originatedfrom the residual population in Lake Shikotsu.
Japanese sockeye salmon are estimated to migrate inwestern waters of the North Pacific Ocean (Ito 1972;Nagasawa and Ito 1999). They spend one or twoyears (occasionally three years) in the ocean before
returning to the natal river from late June to early
September for spawning. The spawning season isusually between October and November.
In the summer of 1994, yearling precociousmales were accidentally captured in the Bibi River 23 months after the releases from a hatchery. By
using parasites as biological indicator and scale patterns we confirmed that they migrated to the ocean,
where they stayed for several months before successfully returning to the river. In this paper, we give thefirst report evidencing the temporary residence ofyearling precocious sockeye salmon in the ocean
environment.

Materials and Methods
Study site
The Bibi River is a small stream within the AbiraRiver system, which flows into the Pacific coast ofHokkaido (Fig. I ) . There is Lake Utonai (230 ha,0.6 m in mean depth) in the lower Bibi River. It isabout 3 km from Lake Utonai to the mouth of theAbira River.

@j$k Bull. Natl. Salmon Resources Center, No. 2 , 1999

1046"NI

I

44'N

42%

1 North Pacific Ocean 1I
1 40°E

142"E

144'E

146'E

Fig. 1. Maps showing the study field (thick arrow) in the Bibi River on southwestern Hokkaido, Japan. Closed and open triangles
indicate the release and capture sites for sockeye salmon, respectively.

Fish releases
On May 17, 1994, a total of 107,700 sockeye
salmon (age I .O, 84-146 mm in fork length, 6.5-37.2
g in body weight) were released into the upper Bibi
River, about 4 km upstream from Lake Utonai (Fig.
1). These fish (1992 brood year stock) were reared at
the Chitose Hatchery for 15 months. About one hundred fish were randomly collected just before releasing in the river for measuring their body size andscale patterns.
Capture effish in the river
Ten precocious sockeye males were capturedwith adult sockeye salmon (ocean age 1 or 2) by anet trap in the Bibi River (about 2 km upstream fromLake Utonai) during July and August 1994 (Fig. 1).
These live fish were transported to the Chitose
Hatchery immediately after the captures.
Measurement offish
Fresh fish samples were measured for fork
length, body weight (BW in g), and gonad weight(GW in g). A gonadsomatic index (GSI in %) wascalculated by a formula: GSI = 100 x GW/BW.
Males whose GSI was over 0.05% were judged as
precocious (maturing) fish.
Parasite and scale analysis
The scales were collected from each fish, and thescale patterns were observed under a microscope.
Intervals between scale circuli were measured usinga scale analysis system (ARP, Ratoc System Engi-neer Co.). The stomach and intestine of precocious
males captured in the river were examined for parasites by a stereomicroscope. The detected parasites
were identified by morphological characteristics.
The ecological terms (prevalence and intensity) usedhere are in accordance with those of Margolis et al.
(1982).

Results
Releasedfish
Sockeye salmon released in the Abira River werecomposed of 50% female smolts, 26% male smolts,
and 24% precocious males (n=104, Table 1). The
body surface of precocious males was dark andgreenish, while smolts had slimmer and silvery body.
Precocious males
The precocious sockeye males which were captured in the river had silvery thick body (Fig. 2). The
body size was 190-220 mm in fork length and thebody weight was 92-138 g (Table 2 ) . The gonad
weight increased to 3.9-6.6 g, although it was lessthan 0.1 g when they were released in the river.
Most of their stomachs were empty.

Parasites
Two species of digenean parasites Brachyphallus
crenatus and Lecithaster gihbosus were detectedfrom the digestive tract of precocious sockeye males.
The former species was found in the stomach andoccasionally intestine, while the latter species was2 c'r . 2 $%%gBe 2 9 -6$% Bull. NatI. Salmon Resources Center, No. 2, 1999

12

Table 2. Size, scale characteristics, and burden of marine digenean parasites (Brachyphallus crenatus and Lecithnster gibbosus)
in precocious males of sockeye salmon caught in the Bibi River during July and August 1994. The fish were initiallyreleased in the river on May 14, 1994.

scalewidth ( pm)

Number ofscale

Number Of marine d%enean

circuli inzone 11B.

L.

crenalus

gibbosus

3016
59
140000I

Gonad

GSI*(g)c%u)

112.7
July 1020 157134.5
2
July 10215
57
3
July 12105.7
20359
July 12
492.2
19059
July 16563123.7
21 1
6July 24207
127.5
71138.1
July 257219728
July 25203101772
136.3
August 19922097113.4
10
August31I09217_ _ _ _ _ _ _ _ _ _ _ _ _ _ __ _ _ _ _ _ _ _ _ _ _ _ .

4.2
5.2
5.4
4.2
51
5.5
5.4
3.9
6.6
5.8

3.70
3.88
5.12
4.51
4.14
4.32
3.92
3.83
4.87
5.15

807
724
640
738
812
767
891
631
748
795

285
360
502
330
314
428
350
514
450
333

81092
1084
913
1142
8
1068
1126
910
1195
1241
9141145
I I98
10
1128
_______. 9

118.6
15.9

5.1
0.8

4.34
0.54

755
79

387
81114255

No

DateOfcaptureDays fromrelease tocapture

Forklenght(mm)Bodyweigh(g)weight1Mean
SD

72
18209
10I'One'OneI'

102parasites

Total

3016611031733
100
100
00
70
_ _ _ _ _ _ ~ _ _ _ ~_ 7~ _ _ _
7.2
6.4
0.8
1.2
6.1
5.8'GSI, gonadsomatic index.

anadromous migration of salmonids (Black 198 1;
Dick and Belosevic 1981; Frimeth 1987). We foundthese marine digenean parasites in eight of ten precocious sockeye salmon males captured in the Bibi
River. This is a direct evidence that maturing sockeye males migrated to the ocean, where they could
live before returning to the river.
Lake Utonai, approximately 4 km down from therelease site in the Bibi River, is not an adequate habitat for sockeye salmon, because it is a shallow lake
(only 0.6 m in mean depth) with high water temperatures during late spring and summer. Therefore,
most released sockeye salmon, including precociousmales, should have migrated down to the coastal
water after a short stay in fresh water. The inceptionof maturity was thought to inhibit the smoltification
process in salmonids (see Foote et al. 1991), but maturation had no inhibitory effect on seawater adaptability of landlocked kokanee salmon during the typical smolting period of 0. nerka from April throughJune (Foote et al. 1994). Seawater challenge tests
showed that some precocious males of sockeye
salmon reared at the Chitose Hatchery had considerable seawater adaptability in the late spring (Urawaet al. 1999). In the present case, the rate of precocious males was relatively high (24%) among sockeye salmon (n=107,700) released from a hatchery.
Thus it should be possible that some precociousmales could survive in the coastal seawater.
The scale pattern of precocious males had twozones. The first zone was apparently formed whenfish were reared at Chitose Hatchery. In addition tothe initial circuli in the first zone, 8-14 circuli withwide intervals were found in the second zone. Thereis a positive correlation between interval of circuli
and growth of sockeye salmon (Suzuki and Kaeriyama 1990). The formation of wide circuli indicatesthat precocious males rapidly grew in the coastal
seawater for a short period. It is reported that a circulus forms every 7-1 1 days under a favorable feeding
condition (Suzuki and Kaeriyama 1990). Then precocious males might stay in the ocean for at least 2months.
In North America, sockeye salmon which return
after one-year ocean life are almost males called as"jacks". These ocean age-.l mature fish are rarely
found among North American populations (Burgner1987), while they frequently appear in Japanese population (Urawa et al. 1999). In Japan, adult females
also return commonly as age-.l (jells). As far as weknow, however, there has been no record that maturing sockeye salmon migrate to sea. This may be thefirst report evidencing the seaward migration ofyearling precocious sockeye salmon and their successful residence in the ocean environment.

Acknowledgements
We thank the staffs of the Chitose Branch of theNational Salmon Resources Center for their support
to our study. We also thank William R. Heard, Auke
Bay Laboratory, Alaska Fisheries Science Center,for helpful suggestions on the manuscript.

Urawaand Kaerlyama ‑ Ocean migration 0f precocious sockeye salmon

I3tion and growthBlack, G. A. 1981. Metazoan parasites as indicators
Of anadromous
bro0k charr
Of movements(Salvelinus fontinalis) to sea. Can. J. ZO01., 59:
1892‑1896.
Burgner, R. L. 1987. Factors influencing age andgrowthOf(Oncorhynchusjuvenilenerka)tn the NOrth Pacific Ocean

ofsockeye salmon (Oncorhynchus nerka) produced

Re 仕renceS

sockeyesalmonfn lakes. In SOckeye

salmon (Oncorhynchus nerka) populationbiology
and future management(edited by H. D. Smith, L.
Margolis, and C. C. WO0d). Can. Spec. Pub1. Fish.
Aquat. Sci., 96. Pp. 129‑142.
Burgner, R. L. 1991. Life history 0f sockeye salmon(Oncorhynchusnerka). In Pacific salmon life his‑tory (edited by C. Gro0t and L. Margolis). UBC
Press, Vancouver, pp. 1‑117.
Dick, T. A., and M. Belosevic. 1981. Parasites ofArctic charr Salvelinus alpinus (Linnaeus) andtheir use tn separating sea‑run and non‑migratingcharr. J. Fish Bio1., L8: 339‑347.
FO0te, C. J., W. C. Clarke, and J. Blackburn. 1991.
1nhibition Of smolting tn precocious male chino0ksalmon, Oncorhynchustshawytscha. Can. J. ZO01.,
69: 1848‑1852.
FO0te, C. J., 1. Mayer, C. C. WO0d, W. Craig, and J.
Blackburn. 1994. On the development pathway tononanadromy ;n sockeye salmon, Oncorhynchus
nerka. Can. J. ZO01., 72: 397‑405.
Frimeth, J. P. 1987. POtential use 0f certain parasites
Of bro0k chair (Salvelinusfontinalis) as biologicalRiver, New
indicators fn the Tabusintac
Brunswick, Canada. Can. J. ZO01., 65: 1989‑1995.
1t0, S. 1972. NOtes On the offshore distribution ofsockeye salmon with a large freshwater zone onscale. Bul1. Far Seas Fish. Res. Lab., 7: 125‑135.

(InJapanese with Englishsummary.)
Kaeriyama,M., S. Urawa, and T. Suzuki. 1992.
Anadromous
sockeye salmon (Oncorhynchusner‑ka) derived from nonanadromous
kokanees: life
history tn Lake TOr0. Sci Rep HOkkaido Salmon
Hatchery, 46: 157‑174.
Margolis, L., G. W. Esch, J. C. HOlmes, A. M. Kuris,and G. A. Schad. 1982. The use Of ecologicalterms tn parasitology. J. Parasito1., 68: 131‑133.
Nagasawa, K., and S. It0. 1999. Distribution, migra‑from the lacustrine form. In Stock enhancement
and sea ranching (edited by B. R. HOwel1, B.

MOksness, and T. Svasand).FishingNews BO0ks,0xford, PP. 168‑181.
Ricker, W. E. 1940. On the origin Of kokanee, afreshwater type Of sockeye salmon. Proc. Trans.
R. SOc. Can. Ser. 3, 34: 121‑135.
Suzuki, T., and M. Kaeriyama. 1990. Scale forma‑tion of juvenile sockeye salmon reared under thedifferent feeding levels. Sci. Rep. HOkkaidoSalmon Hatchery, 44: 23‑28. (In Japanese withEnglishsummary.)
Urawa, S. 1989. Parasites as biological indicators
contributingto salmonid
biology. Sci. Rep.
HOkkaido Salmon Hatchery, 43: 53‑74. (In Japan‑
ese with English summary.)
Urawa, S. 1991. A review Or sockeye salmon pr0‑
duction fn the Nishibetsu River ;n eastern HOkkai‑d0, Japan. Tech. Rep. HOkkaido Salmon Hatchery,
160: 3‑10. (In Japanese with English summary.)
Urawa, S., M. Ban, M. Fukuwaka, T. Suzuki, and M.

Kaeriyama. 1999. Progressive technologies for
artificial production of anadromoussockeye
salmon fn Japan. Bul1. TOhoku Nat1. Fish. Res.

Inst.,
62. (Inpress.)
早熟べ二ヴケの―時的 店海洋生活
浦和 茂彦 ・帰山雅秀1994 年の 7‑8 月に，北海道太平洋沿岸の 安平Ul水系
尾叉長 l90‑が 10 個体採集された ． これらの起源は 2 ，220mm)
美々 川でべ二ザケの 早熟 雄 (年齢 I． I，3 ヵ月前の 5 月中旬に同河川 lに放流された 岬化場産

べ二ザケ (放流時の 尾叉長84‑146 mm) であ った．
再 捕された早熟雄の 大部分に海洋起源の 吸虫 2 種
池 boMJ) が寄巾 rdChM ぬ lfMJCwWrM$ とぬ而肋 MH生．していたことから・ 早熟雄は降悔したことが 示された． 鱗 相解析により ， これらは沿岸に 少なくとも 2 ヵ月間滞在し 急激に成長したと 推定された ．
これは，べ二ザケの早熟 雄 l 年 奄 が降悔して海洋環境に順応して 生活したことを 示す初めての 報告
であ る ．