Scientific Reports of theHokkaido Salmon Hatchery
No. 49: 35-40,March 1995

Occurrence of Myxobolus arcticus and M. neurobius (Myxozoa:Myxosporea) in Masu Salmon Oncorhynchus masou
from Northern Japan
Teruhiko Awakura*’, Kazuya Nagasawa*’ and Shigehiko Urawa*” #*I

Hokkaido Fish Hatchery, Kitakashiwagi 3-373. Eniwa, Hokkaido 061-14, Japan*‘National Research Instilute of Far Seas Fisheries, Fisheries Agency of Japan,
5-7-1 Orido, Shimizu, Shizuoka 424, Japan*’ Research Division, Hokkaido Salmon Hatchery, Fisheries Agency of Japan,2-2 Nakanoshima, Toyohira-ku, Sapporo 062, JapanAbstract.-Adult masu salmon (Oncorhynchus masou) from seven rivers in Hokkaido and northern
Honshu were examined for the geographical distribution of Myxobolus arcticus and M. neurobius innorthern Japan. Maturing maw salmon from Japanese coastal waters of the Okhotsk Sea, Japan Sea, andwestern North Pacific Ocean were also studied for the prevalence of these myxosporeans. Myxobolus
arcticus occurred mainly on the Japan Sea coast of Honshu, whereas M . neurobius was found in
Hokkaido along the coasts of the Okhotsk Sea and Japan Sea. Sea-caught masu salmon showed various
degrees of infections with M. arcticus and M. neurobius. This indicates that maw salmon migrating inJapanese coastal waters are a complex of mixed stocks that originate in various rivers. Prevalence data
support the recently proposed autumn migration route of maturing masu salmon from the Okhotsk Sea toJapan Sea.

Introduction
Masu salmon (Oncorhynchus masou) differ fromother species of Pacific salmon (Oncorhynchus spp.)
in that this species is geographically restricted to theJapan Sea, Okhotsk Sea, and western North Pacific
Ocean off Far East Asia (Machidori and Kato, 1984).
In northern Japan, masu salmon go to the sea after
they spend 1 or 2 years in fresh water and return totheir native rivers for spawning after they spend one
winter in the ocean (Kato, 1991). In Hokkaido andnorthern Honshu, masu salmon are of considerable
importance to the inshore fishery at sea and to thegame fishing in rivers.
Myxobolus arcticus and M. neurobius are myxosporean parasites of the brain and spinal cord of masu
salmon from Japan (Awakura et al., 1982; Nagasawa
et al., 1987; Awakura, 1989). These species are freshwater parasites: aquatic oligochaetes serve as alternate
hosts and transmission to salmonids occurs in freshwater (Kent et al., 1993; Urawa, 1994; Urawa andAwakura, 1994). Salmon become infected as juveniles and carry the infection almost throughout theirContribution A No. 350 from the Hokkaido Salmon Hatchery.
* To whom correspondenceshould be addressed.

-life (Urawa, 1994). The parasites show distinct geographical distribution and are thus used as useful natural markers for stock identification of Pacific salmon,such as maw salmon (Awakura, 1989; Urawa, 1989),
chinook salmon (0.tshawytscha)(Urawa and Nagasawa, 1991, 1995), and sockeye salmon (0. nerka)(Margolis, 1982; Moles et al., 1990).
The present study was undertaken to determine thedistribution of M. arcticus and M. neurobius in northern Japan and the occurrence of these parasites inmasu salmon caught in Japanese coastal waters to elucidate the migration and stock composition of thesesalmon.

Materials and Methods
Four hundred twenty-six masu salmon were sampled in seven rivers in Hokkaido and northem Honshufrom June to October in 1981-1989 to determine thedistribution of M. arcticus and M. neurobius (Fig. 1).
These salmon were all mature adults that had returnedto the natal streams for spawning. A total of 2,677
maturing maw salmon were also caught at 14 sites inJapanese coastal waters of the Okhotsk Sea, Japan
Sea, and western North Pacific Ocean from October toJune in 1981-1990 (Fig. 2 ) . The fish were frozen
immediately after capture and stored at -20 “c until35 -S l f . ***%

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

III

1SEAm

Nabusha R.

06"NN=90

Shokanbetsu R.

$4-N

02'N

06N

3dN

36"NFig. 1. Geographical distribution of Myxobolus arcticus and M. neurobius in mature masu salmon from seven riven
in northern Japan. Pie diagrams display prevalences of single and concurrent infections with the two myxosporean species.

they were examined. Spinal cords and medulla oblongata were removed from the fish, smeared on a slide
glass individually, fixed in methyl alcohol, stainedwith Giemsa, and examined for the presence of sporesof M. arcticus and M.neurobius. Prevalence is thepercentage of fish infected in a sample (Margolis etal., 1982).

Results
Distribution ofmyxosporeans in northern Japan
There was a distinct regional difference in distribution of M. arcticus and M . neurobius in northern
Japan (Fig. 1). In Hokkaido, M. neurobius occurred inrivers flowing into the Okhotsk Sea and Japan Sea,
except for the Shokanbetsu River: 26-63% of fish- 36 -

AWAKURA ET AL. - OCCURRENCE OF MYXOBOLUS IN MASU SALMON&-SEA OFOKHOTSKRebunh u

N=31

Kamoena i~=1485

SEA OF JAPAN( (,PACIFICOCEAN
Karna i sh i

Miomote

N=39=MIarcticus (A)MI neurobius (N)
0A+N
Mega t i ve
II138'E

14GE

\I

1142E

144EFig. 2. Geographical distribution of Myxobolus arcticus and M. neurobius in maturing maw salmon from Japanese
coastal waters of the Okhotsk Sea, Japan Sea, and North Pacific Ocean. Pie diagrams display prevalence ofsingle and concurrent infections with the two myxosporean species.

from the Shari River, Nobusha River, and Mena River
were infected with M. neurobius, but concurrent infectivns with M. neurobius and M. arcticus were occasionally observed in the Nobusha River. In theShokanbetsu River, two myxosporean species werefound, although prevalence of single infection with M.
neurobius was quite low. In the Furen River on the- 37

Pacific side, two myxosporean species were present
and all fish were infected with M. arcticus andlor M.
neurobius.
In Honshu, M. arcticus was present in theMiomote River and Jinzu River flowing into the Japan
Sea, with all or nearly all of fish being infected.
Myxobolus neurobius was not found.

2If . $TW%SCI. REP. HOKKAIDO SALMON HATCHERY, NO. 49, 1995

Prevalence of myxosporeans in sea-caught salmon
Over 80% of masu salmon caught in October andNovember in the Okhotsk Sea off Abashiri and Omu
were infected with M. arcticus andor M. neurobius(Fig. 2). Similar levels of single and concurrent infections were recorded for masu salmon caught mainly inwinter in the Japan Sea off the west coast of Hokkaido
such as Rebun, Rumoi, Shakotan, and Kamoenai.
However, despite the fact that Iwanai and Suttsu wereclose to these sites, masu salmon caught in May off
Iwanai and Suttsu showed different levels of infection:
M. neurobius was common, but infection with M .
arcticus was rare.
In masu salmon caught in March-June at more
southern sites (Sado, Miornote, and Toyama) in theJapan Sea, prevalence of M . arcficus was high, but
infection of M. neurobius was usually low (Fig. 2).
Although masu salmon caught in the western
North Pacific Ocean were infected with M. arcticusand M . neurobius, there was a regional variation inprevalence of these parasites among sampling sites(Fig. 2). Masu salmon caught in May off Kamaishi
had a higher prevalence of M. arcticus and a lower
prevalence of M. neurobius than those caught off
Kushiro and Otsu.
Monthly changes in prevalence of myxosporeans
In the Shakotan area of the Japan Sea, masu
salmon were collected from December to May in
1983-1990, which enabled us to study monthly
changes in prevalence of M . arcticus andor M. neurobius. Myxobolus arcticus occurred most frequently in
December and January, but prevalence declined
steadily and reached the lowest level in March to May(Fig. 3). Contrary to this, prevalence of M. neurobius
was low in December but increased thereafter.
Prevalence of concurrent infections with M. arcticusand M. neurobius increased slightly between
December and May. These trends were almost stable
among the years.

10080

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DEC100 IFEBJAN
11-MAR

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1M arcficus (A)Y neurobius (M)

0A+N" DECJANFEEMARAPR

Mega f i ve

MAYFig. 3. Monthly changes in percentage prevalence of single and concurrent infections with Myxobolus arcticus andM. neurobius in maturing maw salmon caught in the Japan Sea off Shakotan in 1983-1990.

-38-AWAKURA ET AL.- 0 C C m N C E OF MYXOBOLUS IN MASU SALMON

Discussion
The present study shows that sea-migrating,maturing maw salmon included those fish with various degrees of infections with M. arcticus andlor M.
neurobius, whereas the majority of adult masu salmon
from spawning rivers were infected with either M.
arcticus or M. neurobius. This indicates that masu
salmon migrating in Japanese coastal waters are acomplex of mixed individuals that originate in variousrivers.
Myxobolus arcticus and M. neurobius have theirrespective distribution patterns in northern Japan(Awakura, 1989; present study). Only M. arcticus isdistributed in rivers on the Japan Sea coast of Honshu.
Thus, the reason why maw salmon caught in springoff Sado, Miomote, and Toyama had a high prevalence of M . arcticus infection is probably because
these fish mostly originated in nearby rivers (e.g., theMiomote River and Jinzu River). A similar explanation is adopted for masu salmon caught in spring off
Iwanai and Suttsu which had a high prevalence of M.
neurobius infection. It is possible that these fish
included individuals that ascend rivers near Iwanai
and Suttsu (e.g., the Mena River where only M. neurobius occurs). In addition, although we did not
examine the distribution of the myxosporeans on thePacific coast of northern Honshu, there is a possibility
that M . arcticus only occurs in this region, because
this species was prevalent in m a w salmon caught inspring off Kamaishi.
Prevalences of M. arcticus and/or M.neurobius inmasu salmon caught off Shakotan in the Japan Seachanged in winter to spring. This is caused bychanges in stock composition of masu salmon.
Because prevalence of M . arcticus was high in
December and January, it appears that masu salmoncaught in these months included fish originating inrivers on the Japan Sea coast of Honshu. Moreover, itis possible that maw salmon with a high prevalence ofM. neurobius caught in February to May were fromrivers of Hokkaido where this parasite occurs commonly.
Based on information from tagging experiments
and biological features, Machidori and Kato (1 984)
suggested that masu salmon of Japanese origin
migrate to the Okhotsk Sea in spring as juveniles andreturn to the Japan Sea and western North Pacific inautumn as maturing fish for overwintering. Our study
demonstrates that there was no marked difference inprevalence of M. arcticus and M. neurobius in maturing masu salmon caught in the Okhotsk Sea in autumn
and in the Japan Sea in winter, indicating that masu
salmon move from the Okhotsk Sea through the Soya
Strait to the Japan Sea from autumn to winter. Thesefindings support the migration route of maturing masu
salmon, proposed by Machdori and Kato (1984), fromthe Okhotsk Sea to the Japan Sea.
A recent genetic work (Okazaki, 1986) has
demonstrated that masu salmon collected in various
rivers in northern Japan include a variety of genetically independent stocks. Furthermore, it has been suggested that masu salmon caught in Japanese coastal
waters are a mixture of such different stocks (Okazaki,1989). We examined the distribution of M. arcticusand M. neurobius in Hokkaido and northern Honshu.
However, the number of rivers surveyed was only seven and insufficient to determine the geographical distribution of these myxosporean species in northern
Japan. According to Machidori and Kato (1 984),
there are 70 rivers in Hokkaido and 32 rivers inHonshu which many masu salmon ascend. Morework is needed to establish the baseline distribution ofM . arcticus and M. neurobius in order to differentiate
stocks of sea-caught masu salmon using these parasites as biological tags.

Acknowledgments
We thank Mr. Fumio Sasaki of the Hokkaido
Fisheries Experimental Station and Dr. Toshio Okazakiof the National Research Institute of Aquaculture for
their assistance in collecting fish samples. Thanks arealso due to Dr. Leo Margolis of the Pacific Biological
Station, Canadian Department of Fisheries andOceans, for his interest and encouragement.

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