Scientific Reports of theHokkaido Salmon Hatchery
No.49: 11-19,March1995

Prevalence of Myxobolus arcticus (Myxozoa: Myxosporea)
in Five Species of Pacific Salmon
in the North Pacific Ocean and Bering Sea
Shigehiko Urawa*' and Kazuya Nagasawa*'*' Research Division, Hokkaidv Salmon Hatchery, Fisheries Agency ofJapan,
2-2 Nakanoshima, Toyohira-ku, Sapporo 062, Japan*' National Research Instilute of Far Seas Fisheries, Fisheries Agency of Japan,
5-7-1 Orido, Shimizu, Shizuoka 424, JapanAbstract. - Five species of Pacific salmon (genus Oncorhynchus) captured on the high seas of theNorth Pacific Ocean and Bering Sea were examined for the freshwater brain myxosporean Myxobolus
arcticus. In the western North Pacific Ocean, the prevalence of parasite infection was relatively high inchinook (0.tshawytscha, 57.5%), sockeye (0.nerka, 30.4%),and coho (0.kisutch, 18.8%) salmon, but
low in chum (0.keta, 6.7%) and pink (0.
gorbuscha, 0%) salmon, being reflected by a mode of freshwater life of host fish before their seaward migration. Distinct regional differences in prevalence wereobserved in chinook salmon: infected fish were frequently found in the western North Pacific Ocean(especially west of 170'E), but rarely in the eastern North Pacific Ocean and Bering Sea, suggesting therestricted geographical distribution of M. arcticus in chinook salmon. The parasite may be useful as a
biological Indicator to separate the continental origin of high-seas chinook salmon.

Introduction
Myxobolus arcticus Pugachev & Khokhlov, 1979
is a freshwater protozoan parasite of salmonids OCCUTring in Asian Far East and North America facing theNorth Pacific Ocean and adjacent seas. Although its
spores are found in the nervous tissues, the parasite isharmless to host fish. The parasite survives almost
throughout the complete life cycle of host fish including their ocean migration. The freshwater oligochaetes Stylodrilus heringianus and Lumbriculus variegatus, both belonging to the family Lumbriculidae, areknown as alternate hosts of M. arcticus (Kent et al.,
1993; Urawa and Awakura, 1994). Spores are ingested by these oligochaetes following death of adultsalmon after spawning in the natal freshwater area. Inthe gut wall of the oligochaetes the parasite develops
to triactinomyxon spores. They are released into
water and then infect juvenile salmon hatched in thenext spring (Urawa and Awakura, 1994). The parasite
has a restricted geographical distribution, which specifies the parasite as an effective biological tag for stock
identification of sockeye salmon Oncorhynchus nerka(Konovalov, 1975; Margolis, 1982; Quinn et al., 1987;
Contribution A No. 347 from the Hokkaido Salmon Hatchery

Wood et al., 1987; Moles et al., 1990) and masu
salmon 0. masou (Awakura et al., 1982, 1995; Urawa,1989). However, this type of utilization was limited tolocal areas, and little information is available on theoccurrence of M. arcticus in high-seas Pacific salmon(Oncorhynchus spp.)
The present study was conducted to show theprevalence of M . arcticus in five species of Pacificsalmon collected in the North Pacific Ocean andBering Sea, and to evaluate the parasite's usefulness
as a biological tag for stock identification of high-seassalmon.

Materials and Methods
A total of 342 fishes, comprising 83 chinook
salmon (0. tshawytscha), 156 sockeye salmon, 16
coho salmon (0. kisutch), 47 chum salmon (0.keta),
and 40 pink salmon (0.gorbuscha), was caught on thehigh seas of the North Pacific Ocean and Bering Sea(41-55O N, 157°E-1410W) between May and Augustin 1982, 1983, 1986 and 1987 by seven Japanese
research vessels (Kaiun maru, Hokusei maru,
Hokushin maru, Hoyo maru, Iwaki maru, Oshoromaru, and Wakatake maru)(see Appendix). Heads orwhole bodies of the fishes were frozen after capture,
shipped to Japan, and stored under the fi-ozen condition- 11 -

%-F-Wf% SCI. REP. HOKKAIDO SALMON HATCHERY, NO. 49, 1995
Table 1. Measurements ( p m ) of the spores of Myxobolus arcticus from the brain of four species of Pacific salmon caught in the western
North Pacific Ocean.

Host fish

Numberof sporesmeasur ed

Chinook salmon

19

Sockeye salmon

25

Coho salmon

25

Chum salmon

25

Spore

Polar capsulelengthwidth

thicknesslengthwidth

13.8+0.5*(12.9-14.8)
14.6k0.8(13.4-16.8)
14.8k0.6

8.4k0.5(7.7-9.8)
9.0k0.6(7.9-9.9)
8.9k0.5(8.0-9.8)
9.3k0.4(8.9-9.9)-

7.6k0.4(6.7-8.3)
8.1k0.5(7.1-9.1)
8.0k0.4(7.0-8.7)
8.4k0.6(7.1-9.1)

2.6k0.4(2.1-3.2)
3.1 k0.2(3.0-4.0)
3.0k 0.1(2.9-3.3)
3.2k0.2(3.0-4.0)(13.8-16.0)
14.7+0.7(13.0-15.8)-

7.2f0.3(7.0-8.0)
6.9k0.3(6.1-7.3)
6.Xk0.3(6.1-7.4)'MeankSD (range).

Table 2. Prevalence (%) of Myxobolus arcticus in five species of Pacific salmon caught in the North Pacific Ocean and Benng Sea.
North Pacific Ocean
FishBering Sea

West of 180°

East of 180"

Chinook salmon

57.5 (19/33)*'0 (0/5)50.0 (19/3X)

0 (0/45)

Sockeye salmon

30.4 (42/138)

5.6 (1/18)

27.6 (43/156)

ND*2

Coho salmon

18.8 (3/16)

ND

18.8 (3/16)

ND

Chum salmon

6 7 (3/45)

50.0 (1/2)

8.5 (4/47)

ND

Pink salmon

0 (0/37)0 (0/3)0 (0/40)

NDTotal*'Percent prevalence (number of fish infectednumber of fish examined).
"NO data

until dissected for parasite studies. The myxosporean
Myxobolus arcticus was the most detectable as sporesin the medulla oblongata of salmon (Urawa, unpublished data). Then, a slide smear was made from themedulla oblongata removed from each fish and immediately examined at X 200 magnification until thespores were identified or for approximately 5 min if noparasites were found. Throughout the test, the westernand eastern North Pacific Ocean is defined as thewaters west and east of 180' longitude, respectively.
The ecological terms in parasitology used here are inaccordance with those of Margolis et al. (1982).
Fresh spores detected from each host species weremeasured with a calibrated ocular micrometer, according
to the guidehe proposed by Lom and Arthur (1989).

Results
Description of parasite
The spore of M. arcticus is pyriform in front view
with sharp tip of valves, and has two polar capsules at
the anterior end. Spore dimensions are 12.9-16.8 p m
in length, 7.7-9.9 p m in width, and 6.1-8.0 pm inthickness. The polar capsules are cucumiform, being

6.7-9.1 pm long and 2.1-4.0 ,urn wide (Table 1).
Host range
Myxobolus arcticus was found in chinook, sockeye, coho, and chum salmon, but not in pink salmon(Table 2). Of the infected fish collected from thewestern North Pacific Ocean, the prevalence was hlghest (57.5%) in chinook salmon, and lowest (6.7%) inchum salmon.
Geographical distribution
Myxobolus arcticus was found in chinook salmon
captured in the western North Pacific Ocean between
157" 30'E and 177" 30'E, but not in the southern
Bering Sea and eastern North Pacific Ocean (Table 2,Fig. 1j. The prevalence was especially high (83%) infish from the waters west of 170" E (between 43 58"and 49O 54"). In sockeye salmon, the prevalence wasalso much hlgher in the western North Pacific Ocean(30.4%) than in the eastern waters (5.6%)(Table 2),
but there was no apparent difference in prevalence
within the western waters (Fig. 1).

- 12 -

URAWA & NAGASAWA -MYXOBOLUSARCTlCUS IN PACIFIC SALMON

150E

160E

170"E180"

170"W

160W

150"W

140"W

130'W

150E

160"E170"E

180"

170"W

160W

150"W

140"W

130"W

Fig. 1. Prevalence of Myxubolus arcticus in chinook salmon (top) and sockeye salmon (bottom) caught on the high seas of theNorth Pacific Ocean and Bering Sea by 4' X 5' area between May and August in 1982, 1983, 1986, and 1987. Closed portion of each pie shows the parasite prevalence in each area. Numeral within each area indicates number of fish examined.

Discussion
Four species of the genus Myxobolus have beenrecorded from the brain or spinal cord of salmonids(Schuberg and Schroder, 1905; Yasutake and Wood,
1957; hgachev and Khokhlov, 1979; Gonzalez-Lanzaand Alvarez-Pellitero, 1984).
Pugachev andKhokhlov (1979) described two species of Myxobolusfrom the nervous system of salmonids from theKamchatka Peninsula: M. arcticus (pyriform spores)
and M . neurobius (oval spores). The latter species
was first recorded from brown trout (Sulmo trutta) in
Europe by Schuberg and Schroder (1905), but their
obscure descriptions caused subsequent taxonomicconfusion. A detailed taxonomic study is now being
carried out for the brain myxosporeans of North
American salmonids by S . Urawa and L. Margolis(Pacific Biological Station). According to theirunpublished data, the species of pyriform spores,
which has been identified as M . neurobius in North
America (Arthur et al., 1976; Margolis, 1982, 1984;
Bailey and Margolis, 1987; Quinn et al., 1987; Woodet al., 1987; Moles et al., 1990), should be treated asM. arcticus. Apparently, the pyriform myxosporean
found in high-seas salmonids is also identifiable toM. arcticus.
There were apparent differences in the prevalenceof M. arcticus among five species of Pacific salmon- 13 -2 If

5%Ab#%

SCI. REP. HOKKAIDO SALMON HATCHERY, NO. 49,1995

caught in the North Pacific Ocean. The parasite infections frequently occurred in chinook, sockeye andcoho salmon, but rarely in chum salmon. No pinksalmon were infected. The first three species usuallyspend the first 1 or 2 years of their life in fresh water
before migrating to the ocean, whereas chum and pinksalmon migrate seaward soon after emerging from thegravel beds. Then, the observed low prevalence ofinfection in chum and pink salmon is probably attributable to a lack of opportunity to gain the parasite dueto the short period of their freshwater residence.
A marked regional difference in prevalence of M.
arcticus infection was observed in chinook salmon.
The parasite was frequently encountered in the westem North Pacific Ocean (42-53ON, 157-177'E) but
not found in the southern Bering Sea (54-55" N,
175 ' W-178 E) and the Gulf of Alaska (52-55 N,141-143 W). The scale-pattern analysis has shownthat most chinook salmon in the central Bering Sea
originate in western Alaska (Major et al., 1978; Myerset al., 1987). The high prevalences of M. arcticus infish from the western North Pacific Ocean as well as
no infection in fish from the Bering Sea and Gulf ofAlaska suggest that M. arcticus frequently occurs in
Asian chinook salmon but rarely in North Americanstocks. This assumption is well corroborated byrecent intensive parasitological surveys on chinook
adults collected from major spawning rivers of Asia
and North America (Urawa, Nagasawa, Margolis andMoles, unpublished data).
Chinook salmon are the least abundant among
Pacific salmon, and a high proportion of them iscaught in fisheries at sea, often at long distance fromtheir natal rivers, causing regional and international
controversy. However, their low abundance makes
difficulty in determining the status of individual stocks
by tagging experiments (Harris, 1988). In addition,
scale pattern studies were not conclusive to determine
regional origins of chinook salmon distributed in theNorth Pacific Ocean due to discrepancies of the results(Major et al., 1978; Myers et al., 1987, 1993; Ito et al.,
1985, 1986). Most Asian chinook salmon originate inKamchatka, where M . arcticus is distributed(Pugachev and Khokhlov, 1979; Nagasawa et al.,1994). Thus, M. arcticus is expected as a biologicalindicator to determine the Asian origin of chinook
salmon migrating to offshore waters.

Acknowledgments
We thank Kenji Takagi, Jun Ito, Yukimasa Ishida,

and Kenji Shimazaki for providing samples and valuable advice. Thanks are also extended to the crews ofthe Japanese research vessels for collecting the samples. The present study was carried out under the auspices of the International North Pacific FisheriesCommissions (INPFC).

ReferencesArthur, J. R., L. Margolis, and H. P. Arai (1976):Parasites of fishes of Aishihik and Stevens Lakes,Yukon Territory, and potential consequences of
their interlake transfer through a proposed water
diversion for hydroelectrical purpose. J. Fish. Res.
Board Can., 33,2489-2499.
Awakura, T., H. Kojima, K. Sugiwaka, and T. Ogawa(1982): Studies on parasites of masu salmon,
Oncorhynchus masou-111. Myxobolus (Protozoa:Myxosporea) found in spinal cord. Sci. Rep.
Hokkaido Fish Hatchery, (37), 37-47. (In Japanesewith English summary.)Awakura, T., K. Nagasawa, and S. Urawa (1995):
Occurrence of Myxoholus arcticus and M. neurobius (Myxozoa: Myxosporea) in masu salmon
Oncorhynchus masou from northern Japan. Sci.
Rep. Hokkaido Salmon Hatchery, (49), 35-40.
Bailey, R. E., and L. Margolis (1987): Comparison ofparasite fauna of juvenile sockeye salmon(Oncorhynchus nerka) from southern British
Columbian and Washington State lakes. Can. J.
Z ~ o l .65,420-431.
,Gonzalez-Lanza, M. C., and M. P. Alvarez-Pellitero(1984): Myxoholus farionis n. sp. and M. ibericus n.
sp. of Salmo trutta f. ,fario from the Duero basin(NW Spain). Description and population dynamics.
Angewandte Parasitologie, 25, 181-189.
Harris, C. K. (1988): Recent changes in the pattern ofcatch of North American salmonids by the Japanesehigh seas salmon fisheries. In Salmon Production,
Management, and Allocation: Biological, Economic,and Policy Issues (edited by W. M. McNeil).
Oregon State University Press, Corvallis. pp. 41-65.
Ito, J., Y. Ishida, and S. Ito (1985): Stock identification of chinook salmon in offshore waters in 1974
based on scale pattern analysis. Document submitted to the Annual Meeting of the International
North Pacific Fisheries Commission, Tokyo, Japan,October 1985. 18 p. (Available from the National
Research Institute of Far Seas Fisheries, Shimizu,Shizuoka 424, Japan.)Ito, J., Y. Ishida, and S. Ito (1986): Further analysis of- 14 -

URAWA& NAGASAWA

‑MYXO

BOLUS

ARCTICUS

stock identification 0f chino0k salmon fn offshore
waters tn 1974. DOcument

1979,

parasite 0f Pacifica myxosporeansalmon, via a triactinomyxon from the aquatic
Oligochaete Stylodrilus heringianus (Lumbriculidae).
Can. J. ZOo/., 71, 1207‑1211.
KOnovalov, S. M. (1975): Differentiation 0f local pop‑ulations 0f sockeye salmon Oncorhynchus nerka(Walbaum). University Of Washington Publicationsin Fisheries, New Series, VOlume 6. 290 p.
LOrn, J.,and J. R. Arthur (1989): A guideline for thepreparation of species descriptions tn Myxosporea.
J. Fish Diseases, 12, 151‑156.
Major, R. L., J. It0, S. It0, and H. GOdfrey (1978):
Distribution

andoriginof

chino0ktern,

the NOrth

Pacific Ocean.

Int. NOrth

Myxosporeans

Salmon0f the genus(1979):

Myxobolus

Systematic and Ecology of Fishes fn the Far East.
Quinn, T. P., C. C. WO0d, L. Margolis, B. E. Riddel1,and K. D. Hyatt (1987): HOming fn wild sockeye
salmon (Oncorhynchusnerka) populations as
inferred from differences fn parasite prevalence andallozyme allele frequencies. Can. J. Fish. Aquat.
$d., 44, 1963‑1971.
Schuberg, A., and 0. Schroder (1905): Myxosporidien

Fish.

demNervensystem
undder HautderBachforelle (Myxobolus neurobius n. sP. u. Henne‑aus‑nusslini n. sP.). Archiv fur Protistenkunde, 6,47‑60, 1 Pl.

an overview. f@ Aspects Of Parasitology (edited byE. Meerovitch). McGill University, MOntrea1.
pp.

HOkkaido

pp. 137‑139. (In Russian.)

Bul1.,38, 1‑54.

Margolis, L. (1982): Parasitology Of Pacific salmon$c;. Rep.

‑ parasites
Of the brain and spinal cord Of Salmonidae. Insalmon
Pac.

Kamchatka.

Hatchery, (48), 17‑21.
Pugachev, 0. N., and P. P. Khokhlov(Oncorhynchus tshawytscha)fn offshore waters ofCOmm.

SALMON

Bul1.,52, 1‑86.
Myers, K. W., C. K. Harris, C. M. Knudsen, R. V.
Walker, N. D. Davis, and D. E. ROgers (1987):
Stock origins 0f chino0k salmon ;n the area Of theJapanese mothership salmon fishery. NOrth AW. J.
Fish. Manage., ?, 459‑474.
Nagasawa, K., S. Urawa, and V. A. Dubinin (1994): A
parasitological survey
0f sockeye salmon(Oncorhynchusnerka) andDOlly Varden(Salvelinus malma) from the Ozemaya River sys‑

submitted to the Annual

Meeting Of the International NOrth Pacific Fisheries
COmmission, Anchorage, USA, NOvember, 1986.
19 p. (Available from the National ResearchInstitute of Far Seas Fisheries, Shimizu, Shizuoka
424,Japan.)Kent, M. L., D. J. Whitaker, and L. Margolis (1993):
Transmission Of Myxobolus arcticus Pugachev andKhokhlov,

IN PACIFIC

guyaUrawa,

135‑226.

occurrence

0f Micr0‑

COlumbia.

f@ SOckeye

Salmon(Oncorhynchus

ner‑ka) POpulation Biology and Future Management(edited by H. D. Smith, L. Margolis, and C. C.
WO0d). Canadian Special Publication 0f Fisheries
and Aquatic Sciences 96. pp. 12‑24.
Yasutake, W. T., and E. M. WO0d (1957): SOme
Myxosporidia found ;n Pacific northwest salm0‑
nids. J. Parasito1., 43, 633‑642.

salmonids in this area. Int. NOrth Pac. Fish. COmm.

― l5S. (1989): Seasonal

sporidium takedai (Microsporida) infection tn masu
salmon, Oncorhynchus
masou,
from the ChitoseRiver. Physiology and Ecology Japan, Special
VOlume 1, 587‑598.
Urawa, S., and T. Awakura (1994): Protozoan diseases
Of freshwater fishes in HOkkaid0. Sci. Rep.
HOkkaido Fish Hatchery, (48), 47‑58.
WO0d, C. C., B. E. Riddel1, and D. T. Rutherford(1987): Alternative juvenile lifehistoriesofsockeye
salmon {Oncorhynchus nerka) and theircontribution
to production fn the Stikine River, northern British

Margolis, L. (1984): Preliminary report 0n identifica‑tion 0f continent Of origin Of ocean‑caughtsteelhead
trout, Salmo gairdneri, using naturally occurring
parasite"tags"
Department Of Fisheries and Oceans,
Fisheries Research Branch, Pacific Biological
Station, Nanaim0, B.C., Canada V9R 5K6.
(Unpublished report.)
Margolis, L., G. W. Esch, J. C. HOlmes, A. M. Kuris,and G. A. Schad (1982): The use of ecologicalterms fn parasitology. J. Parasito1., 68, 131‑133.
MOles, A., P. ROunds, and C. KOndzela (1990): Use of
the brain parasite Myxobolus neurobius fn separat‑ing mixed stock 0f sockeye salmon. Am. Fish. SOc.
Symp., ?, 224‑231
Myers, K. W., C. K. Hams, Y. Ishida, L. Margolis,and M. Ogura (1993): Review 0f the Japanese land‑
based driftnet salmon fishery @n the western NOrth
Pacific Ocean and the continent Of origin of―

珊報 Scl ． REP ． HOKK

さけ・ます

皿 OSMMONHATC

低 RY ， NO・49 ， l995

低く (6． ?%) ，カラフトマスには寄生がみられなかった
これらの結果は， 各魚種の降悔するまでのf水炎 生活様式

北大平洋およびベーリング 海に分布するサケ属魚類
5 種における粘液胞子虫 Myx@o0bolusarcticusの寄生率の比較

・の違いに原因しており，淡水生活期間の短いサケやカラ類に感染し延髄など 神経組織で胞子を形成して宿主のの海域で高く，北太平洋東部およびベーリング
悔では著ほぼ―生を通じて寄生する．ここでは，北太平洋およびベーリング海で 漁獲されたサケ 属 5 甘 種における M ．
什。ぬ " 胞子の寄生率を比較した．北西太平洋におけるCぬの寄生が地理的に限定されていることを示唆し本・

矛しく低かった．この結果はマスノスケにおけるM・粘液胞子虫Myxobolusarcticusは，淡水中でサケP+甘 、フトマスでは感染の機会カ 三少ないため寄生率カ砥いと推
本虫の寄生率は，海域に定された．マスノ スケにおけるより明らかな差がみられ，北太平洋の東経 170 。 より西側

浦和茂彦 長津和也

0，， ti‑

史は海洋に分布する
マスノスケの大陸起源を判別する生物標識として使える可能性が高い．

十寄生率は，マス スケ (57.5%)， べ二ザケ (30.4%) おノ

よびギンザケ (18.8%) で比較的高かったが，サケではt6