Scientific Reports of the
Hokkaido Salmon IIatcbery
No. 48: 17-21, March 1994

A Parasitological Survey of Sockeye Salmon ( Oncorhynchus nerka)
and Dolly Varden ( SaZueZinus malma) from theOzernaya River System, Kamchatka
Kazuya Nagasawa* ’, Shigehiko Urawa*’, and Vladimir A. D ~ b i n i n * ~*’ National Research Institute of Far Seas Fisheries, Fisheries Agency of Japan,
Orido, Shimizu, Shizuoka 424, Japan
Research Division, Hokkaido Salmon Hatchery, Fisheries Agency of Japan,
2-2 Nakanoshima, Toyohira-ku, Sapporo 062, Japan* 3 Kamchatka Research Institute of Fisheries and Oceanography, PetropavlovskKamchatsky, Kamchatka 683602, Russia*2

Abstract.-Adult sockeye salmon Oncorhynchus nerka from the Ozernaya River near the outlet of
Lake Kuril were infected with Myxobolus arcticus (Myxozoa) in the brain and spinal cord and with
Philonema oncorhynchi (Nematoda) in the peritoneal cavity. Some of these sockeye salmon wereaffected by light visceral adhesions. This pathological condition was found in male fish only. Myxobolus
arcticus was also found in the brain of adult Dolly Varden Salvelinus malma from a river flowing into
Lake Kuril. There was no substantial difference in spore measurement of M. arcticus from salmonids
among Kamchatka (Russia), Hokkaido (Japan), and British Columbia (Canada). The Dolly Varden
carried Salmincola carpionis (Copepoda) on the roof and floor of the buccal cavity and Anisakis
simplex (third-stage larvae) (Nematoda) on the viscera.

Introduction
Based on the 1992 program of fisheries science andtechnology cooperation between Japan and Russia, twoJapanese scientists (K.N. and S.U.) visited Kamchatka,
Russia, in August 1992. The main purpose of their visit
was to get information on various aspects of the biology ofsalmonids in Kamchatka and to discuss with Russianscientists the promotion of salmonid research in bothnations, but they also conducted with Russian scientists aparasitological survey of salmonids from the Ozernaya
River system. This survey was closely associated with theInternational North Pacific Fisheries Commission(INPFC): under the auspices of I N P F C the Japanesescientists used parasites as biological tags for determining
the ocean distribution of Asian and North Americanchinook salmon Oncorhynchus tshawytscha (Nagasawa
and Urawa, 1987; Urawa and Nagasawa, 1988,1989,1991;
Urawa et al., 1990). Furthermore, visceral adhesions, oneof parasitic diseases of salmonids, are known to be commonly present in offshore-caught sockeye salmon 0. nerka(Nagasawa, 1985, 1987), but this disease has never been
Contribution A No. 342 from the Hokkaido Salmon Hatchery- 17

studied for sockeye salmon that have returned to Kamchatka. This paper reports the preliminary results of theJapan-Russia cooperative parasitological survey in Kamchatka.

Materials and Methods
Thirty mature sockeye salmon Oncorhynchus nerka
were caught with a beach seine in the Ozernaya River near
the outlet of Lake Kuril on August 7,1992 (Fig. 1).These
fish were soon brought to the laboratory of the Lake Kurd
Field Station and were processed by recording fork length,
body weight, sex, gonad weight, infection of Philonema
oncorhynchi (Nematoda: Philometridae), and the presenceor absence of visceral adhesions. Philonema oncorhynchi isa causative agent of visceral adhesions of sockeye salmon(cf. Nagasawa, 1985,1987). The brain and anterior part ofspinal cord were removed from each fish and fixed in 10%
formalin. Two scales were also taken from the I N P F C
preferred area of the body surface of each fish for later age
determination (Major et al., 1972)
Ten adult Dolly Varden Salvelinus malma were collected in the Vychenkiya River flowing into Lake Kuril by
rod and line on August 9, 1992 (Fig. 1). These fish were
examined for nematodes in the body cavity and for parasitic

SM- %-%&H% SCI. REP IIOKKAIDO SALMON HATCHERY. NO 48, 1Y94

copepods on the body surface and in the brachial andbuccal cavities, and when parasites were present, thoseparasites were removed and fixed in 10% formalin. The
brain was also taken from each fish and fixed similarly.
The brains and spinal cords removed from the sockeye
salmon and Dolly Varden were brought to Japan andexamined for the presence of
Myxobolus arcticus(Myxozoa: Myxobolidae) by using a microscope (200400 x). For a comparison of regional variations in spore
measurement of this parasite, the spores were measured
from Kamchatkan, Japanese, and Canadian salmonids.

infected with Myxobolus arcticus in the brain and spinal
cord (Table 1). This parasite was also found in the brainof all Dolly Varden examined (Table 2). These findings
confirm the presence of iM. arcticus in the Ozernaya Riversystem. According to Konovalov (1971), this myxosporcan (as M. neurobius) is the most frequently occurring
parasite of Kamchatkan fishes, including various salmonids (Oncorhynchus nerka, 0. kisutch, Saloelinus spp..
Prosopium cylindraceum, and Thymallus arcticus). T h espores of M. arcticus found were pear-shaped, and there
was no substantial difference in spore measurement of M.
arcticus from salmonids from Kamchatka (Russia), Hokkaido (Japan), and British Columbia (Canada) (Table 3).
Another myxosporean species, M. neul-obius, which is a

Results and Discussion
Nine (30.0%) of the 30 sockeye salmon examined wereTable 1. Parasites, visceral adhesions, and biological features of 30 mature sockeye salmon Oncorhynchus nerka f r o m
the Ozernaya River near the outlet of L a k e Kuril on August 7, 1992 t, positive; -, negative.
I

No.
1
2
3
4
3

6
7
8

9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30

Fork
length(cml

Body
weight
(kg)

68.0
62.0
50.5
66.5
56.0
52.0
59.0
54.5
56.0
50.0

4.50
3.20
1.75
3.95
2.40
1.95
2.85
2.15
2.20
1.70
2.00
2.80
1.90
1.80
2.45
2.40
2.10
2.55
2.40
2.80
2.20
3.70
2.10
2.05
1.90
2.95
2.00
2.65
3.10
2.00

55.0
58.5
52.0
51.0
58.0
54.0
54.5

57.5
57.5
54.5
54.5
64.0
54.0
54.5
53.0
58.5
52.5
58.5
59.0
54 0

Sex

Gonad
weightAge

Mycobolus
arcticus

Philonema Visceraloncorhynchi adhesions

(d
135
89
87
67
61
99
67
105
125
79

2.3*
2.2
2.2
2.3
2.2
2.2
2.2
2.2
2.2
2.2
2.2
2.2
2.2
2.2
2.2
2.2
2.2
2.2
3.2
2.3
2.2
2.3
2.2
2.2
2.2
2.3
2.2
2.3
2.3
2.2

87
74
93
79
84
59
104
100
45
14
103
259
129
126
115
164
128
301
199
116

* Ages were recorded according to the European system

-

18

+

-

NAGASAWA E l AL.-PARASITES OF SALMONIDS OF KAMCHATKA

biological tag of Columbia River chinook salmon (Urawa
and Nagasawa, 1988,1989,1991; Urawa et al., 1990), was
not found in the Kamchatkan sockeye salmon nor Dolly
Varden.
Seven sockeye salmon (23.3%) were affected by lightvisceral adhesions (Fig. 2, Table 1). In cases of visceraladhesions of sockeye salmon caught on the high seas of theNorth Pacific Ocean, visceral organs are tightly surrounded by a thick connective tissue sheath (Nagasawa, 1985),
but such conditions were never found. Only male fish had
visceral adhesions. All sockeye salmon examined harbored
Philonema oncorhynchi (Fig. 3). Concerning the differ-

Table 2. Parasites and biological features of 10 adult
Dolly Varden Saluelinus malma from the Vychenkiya River flowing into Lake Kuril on August 9,
1992. +, positive.
Body
weight

Sex

(€9

-

1
2
3
4
5
6
7

Fork
length
(cm)
43.0
41.0
46.5
46.5
47.0
47.0
39.0

650
550

a

8

39.0

9
10

44.0
40.0

550
750
500

No.

1,000

Myxobolus Salmincola
arcticus
carpionis
5'

a
a

750
550

3

750

2

600

a
P

c9

?

e

+
+
+
+

1
2
2
12
0
0
0

Fig. 1. Map of Lake Kuril, showing locations (filled
circles) sampled for sockeye salmon (Oncorhynchus nerka) and Dolly Varden (Saluelinus
malma). Sockeye salmon were caught in the Ozernaya River (location 1) near the outlet of Lake
Kuril. Dolly Varden were sampled in the Vychenkiya River (location 2) flowing into Lake Kuril.

04* Number of copepods foundTable 3. Spore measurements of Myxobolus arcticus from the brain of Dolly Varden (Salvelinus malma) and sockeye
salmon (Oncorhynchus nerha) from Kamchatka (Ozernaya River), Hokkaido (Chitose River), and British
Columbia (Sproat Lake).
Host(Locality)
Dolly Varden(Ozernaya River)
Sockeye salmon(Ozernaya River)
Sockeye salmon(Chitose River)
Sockeye salmon(Sproat Lake)

No. ofsporesmeasured
30

30
30

50

SL"

SW*'

14.4?0.6
10.010.4(13.3.15.6)*3 (9.4-10.9)
1 3 3 1 0 . 6 8.6f0.6(12.5-15.2) (7.6-9.8)
8.4i0.5
13.2i0.6(11.9-14.4) (7.8-9.4)

ST"

PCL*'

PCW*'

NC*'

SW/SL

7.410.3(6.8-7.8)
6.6i0.4(5.5-7.4)
6.6k0.3(5.5-7.0)

8.6-tO.6(7.0-9.4)
8.1k0.6(7.0-9.2)
8.3i0.5(7.0-9.5)

3.7k0.3(3.1-4.5)
3.2i0.2(2.8-3.9)
3.1i0.2(2.3-3.7)

8.9f0.7(8-9)
9.6f0.1(8-12)
11.Oi1.0(9-13)

0.70i0.04 0.8610.07(0.60-0.78) (0.69-0.98)
0.62i0.03 0.95i0.09(0.53-0.70) (0.75-1.11)
0.6410.04 1.0010.07(0.57-0.73) (0.86-1.11)

PCL/SW

14.2+0.7

8.6k0.5

8.1i0.5

3.4+0.2

0.61i0.04 0.96i0.07(12.9-15.6)(7.8-9.8)(7.3-9.2)(2.5-4.0)(0.50.0.69) (0.82-1 14)*'SL, spore length; SW, spore width; ST,spore thickness; PCL, polar capsule length; PCW, polar capsule width;in pm.
*' NC, number of coils per polar filament.
* 3 M e a n i S D (range).

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19 -

.

3 K tT&R% SCI REP HOKKAIDO S A L M N HATCHERY. No 48.1994

4
Figs. 2-4. Photographs of parasitized salmonids from the Ozernaya River system, Kamchatka 2. Sockeye
salmon (Oncorhmchlcr nerka. male, 50 0 cm fork length) affected by light visceral adhesions (arrows) 3,
Sockeye salmon (female. 53 0 cm fork length) infected with P h i l o n m oncorhpchi (arrow) on theviscera. 4, Dolly Varden (Saluelinus rnalma. male, 47 0 cm fork length) infected with Salmrncola carpmnrs(arrow) on the roof of the buccal cavity
enec m severity of visccraludhesions between offshore andreturned sockeye salmon, Nagasawa (1987) suggested
that visceral adhesions are transitory and disappear withfish maturation. He also noted that adhesions am morecommonly in male fish thm in female fish. Kanovalov(1971) reported the infection of P. oncorhynchi in sockeye
salmon from several Kamehalkan lakes, including Lake
Kunl.
The Dolly Varden c m c d Salrnincolo carpianis (Copepoda: Lcmaeopadidac) on the r a d and floor of the buccal
cavity (Fig. 4). Third-stage b a c of A m a h smplez(Nematoda: Amsakidae) were also found on the V I S C C ~ .
Konovalov (1971) found an id^^ sp. (pmbably A. s u mpler) larvae m “diadromous SolveLnw” fmm Lake KUnl.
The presence 01 A. smplrr mdieaks thal the Dolly Varden
have returned to Lake KUnl after suying at sea

Acknowledgments
We thank Dr. M i W M.Selifonov and Dr. Vladimir I.
Karpenka of the Kamchalka Research Insblute of Fish-eries and Oceanography for their suggestions dunng oursurvey in Kamchatka. This work could not have been done
without the ass~stznccof Mr. Vladimir S. Kuchercnko of
the Lake K d Field Shbon. Thanks are also due to Dr.
Leo Margalis of the Pacific Biological Stahon for p m v d
mg the spores of M. archfrom Canadian sockeye
salmon. and to Mr. Soto-o Ita of the Nahonal ResearchInstitute of Far Seas Fisheries for age determination of theRussian sockeye salmon.

References
Konovalov, S. M. (1971): Differenriatlon of local populations of sockeye salmon Oneorhynchus nerko (Walbum). “Nauka” Publ. House. Leningrad (translated
from Russian by L. V. Sagen, University 01Washington
Publications m Fishcnes, New Ser., Vol. 6. Universityof Washington Press, Seattle. 1975). 229 p.
Malor. R. L.. K. H. Mosher, and J. E. Mason (1972):
Idenbficabon of stocks of salmon by scale features. In
The Stock Concept m Pacific Salmon (edited by R. C.

- 20 -

ぬ ． "PMGAsWAET

側

slLS

OF

Simon, and P. A. Larkin). H. R. MacMillan lectures infisheries. University 0f British COlumbia, Vancouver.
pp. 209‑231.
Nagasawa, K. (1985): Prevalence of visceraladhesions insockeye salmon, Oncorhynchus nerha, in the central

S几肌 MDS

Shimizu.)
Urawa, S., K. Nagasawa, Y. Ishida,and M. Kato (1990):
A baseline 0f the prevalences of brain myxosporeanparasites for the stock identification 0f chino0k salmon
Oncorhynchus tshawytscha ;n high seas fisheries. DOcu‑
mentsubmitted t0 the Annual Meeting 0f the Interna‑
tional NOrth Pacific Fisheries COmmission, Vancouver,
Canada, October 1990. I0 p. (Available from the
National Research Institute 0f Far Seas Fisheries,

243‑253.

Nagasawa, K., and S. Urawa (1987): Preliminary report of
the use0f parasites

asbiological

tags

。MM

and NOrth American chino0k salmon (OncoThynchus
tshawytscha) in the NOrth Pacific Ocean and Bering Sea
between 1988 and 1990 estimated by the tag parasites.
DOcument
submitted t0 the Annual Meeting 0f theInternational NOrth Pacific Fisheries COmmission,
TOky0, Japan, October 1991. 20 p. (Available from the
National Research Institute 0f Far Seas Fisheries,

fn the NOrth

Pacific Ocean and Bering Sea. f% SOckeye Salmon((Oncorhynchus nerka) POpulation Biology and FutureManagement (edited by H. D. Smith, L. Margolis, andC. C. WO0d). Can. Spec. Pub1. Fish. Aquat. Sci.,96,

柵Urawa, S.,and K. Nagasawa (1991): Distribution 0f Asian

NOrth Pacific Ocean. Fish PathoL, 20, 313‑321.
Nagasawa, K. (1987): Prevalence 0f visceraladhesions insockeye salmon (Oncorhynchus nerka)OF

for the stock

identification Of ocean‑caught chino0k salmon, Onc0‑
rhynchus tshawytscha. DOcument
submitted [o theAnnual Meeting 0f the International NOrth PacificShimizu.)

Fisheries COmmission, Vancouver, Canada, October1987. 8 p. (Available from the National Research Insti‑
tute of Far Seas Fisheries, Shimizu.)
Urawa, S., and K. Nagasawa(1988): Prevalence 0f two
species 0f Myxobolus (Protozoa: Myxozoa) in chino0k

オゼルナヤ 川水系のべ二ザケとオショロ コマの寄生虫調査
長津和 也 ・浦和茂彦

・V ． A ． ズ ピーニン

salmon, Oncorhynchus tshawytscha, collectedfrom the

漁業分野におげる日本と口シアとの科学技術協カ計画

NOrth Pacific Ocean and the northwest coast 0f NOrthAmerica in 1987, with special reference t0 the stock
identification 0f ocean‑caught chino0k salmon by tag
parasites. DOcument
submitted to the Annual Meeting of
the International NOrth Pacific Fisheries COmmission,の―環として、1992@E8 月に日本人研究者がカムチャツ

TOky0, Japan, October 1988. I2 p. (Available from the
National

Research Instituteof FarSeas

Fisheries,

は軽い内臓癒着症を呈した個体があり、 それ低雄魚だげに認められた。
M r.nhnluf@ 仰血。u¥ の寄生は、クリル湖に

Shimizu.)ノ・Urawa, S.,and K. Nagasawa (1989): Ocean distribution of
Asian and NOrth American chino0k salmon (Onc0‑
rhynchus tshawytscha) determined by the tag parasites,
Myxobolus arcticus and M. neurobius (Protozoa:

Myxozoa). DOcument submitted

ヵを訪問した際、 オゼルナヤ川水系でべ二ザケとオショ
ロ コマの寄生虫調査を実施した。クリル湖の流出口に近いオゼルナヤ川で採集したべ二ザケ成熟魚は、 脳と脊髄に粘液胞子虫類のMyxobolusarc 血卯、 腔
腹内に線虫類のPhilonemfioncor
竹"chi の寄生を受げていた。
べ二ザケに

to the Annual Meeting

Of the International NOrth Pacific Fisheries COmmis‑
sion, Seattle,U.S.A., October 1989. I9 p. (Available
from the National Research Institute 0f Far Seas Fisheries, Shimizu.)― 21

流入するビ チェリキア川で採集したオショp コマの脳にも認められた。 べ二ザケ とオショ p コマ から得た
Myxx"&。 応 narc.
ぬc.us の胞子の計測
値は、 北海道 (日本) やブリティツシュ・コロリビア
州 (.カナダ) のべ二ザケから得たMyxobolusarcti。M の胞子の計測値とほほ同じであった。
オショロ コマは、口腔壁にヵイアシ類のSalm 血 colaea 叩iom た 、 腹腔内に線虫類のA れた林 ぬ simplex 悌 3 期幼虫) の寄生を受げていた。

―