さけ・ます資源管理センター
研究報告 第 5 号 7-12頁
2002年12月

Bulletin of the National Salmon
Resources Center, No. 5: 7-12
December 2002

Infection of Salmincola californiensis (Copepoda: Lernaeopodidae)
on Juvenile Masu Salmon (Oncorhynchus masou)from a Stream in Hokkaido
Kazuya Nagasawa*1 and Shigehiko Urawa*2*1

Nikko Branch, National Research Institute of Aquaculture,2482-3 Chugushi, Nikko, Tochigi 321-1661, Japan(ornatus@fra.affrc.go.jp)*2Research Division, National Salmon Resources Center,
2-2 Nakanoshima, Toyohira-ku, Sapporo 062-0922, Japan

Abstract. − The parasitic copepod Salmincola californiensis infected 18 (94.7%) of 19 masu salmon
juveniles collected from the Bekanbe-ushi River in eastern Hokkaido in the springs of 1982 and1983, while the parasite was not found on white-spotted charr nor Sakhalin taimen from the river.
The mean intensity of the parasite on masu salmon was 10.3 (intensity range, 1-26). There was asignificant increase in intensity of infection as the size of the host fish increased. Most of the copepods found were mature adult females, followed by chalimus larvae and young adult females. Themature adult females were attached almost exclusively to the gills and the inner surface of the operculum. The chalimus larvae were found on the gills. The distal ends of the gill filaments attachedby adult females were damaged, but there were no significant correlations between condition factor
and intensity of infection. This paper is the first confirmed record of S. californiensis from Hokkaido.
Key words : parasitic Copepoda, Salmincola californiensis, host range, masu salmon, prevalence,infection site, Hokkaido

Introduction
The lernaeopodid copepod Salmincola californiensis (Dana, 1852) is an ectoparasite of freshwater salmonids in the North Pacific rim countries(Kabata 1969). In Japan, the hitherto known hosts ofthis copepod are masu salmon (Oncorhynchusmasou), Japanese charr (Salvelinus leucomaenis pluvius) and possibly also amago salmon (O. masou
ishikawae [previously as O. rhodurus]) (Nagasawa etal. 1987). Since S. californiensis has been reported
from both wild and farmed fish in Japan (Hoshinaand Suenaga 1954; Hoshina and Nishimura 1976;
Nishimura and Hoshina 1977), it is generallybelieved to frequently occur on Japanese salmonids.
However, there is actually no information about theoccurrence of the species on salmonids from Japan.
During a parasitological survey of salmonids collectContribution A No. 28 from the National Salmon
Resources Center.
© 2002 National Salmon Resources Centered in the Bekanbe-ushi River, eastern Hokkaido, we
found that juvenile masu salmon were infected withS. californiensis. The known localities of the copepod in Japan are limited to the central area of Honshu (Nagano and Gunma prefectures), and this finding is the first record from outside Honshu in thiscountry. As a preliminary study to understand thebiology of S. californiensis in Japan, we examined
the occurrence of the parasite on juvenile masu
salmon from the river.

Materials and Methods
Juvenile masu salmon (Oncorhynchus masou)
were collected at two brooks (Toraibetsu and Chiraikaribetsu) in the Bekanbe-ushi River (Fig. 1) by
rod and line in April of 1982 (n=10) and 1983 (n=4).
Some additional fish were taken in June 1982 (n=5).
In addition, six white-spotted charr (Salvelinus leucomaenis) and three Sakhalin taimen (Hucho perryi)
were caught in a brook (Toraibetsu) in April andJune 1982. All fish were fixed in 10% formalin andbrought to the laboratory, where they were measured

8

さけ・ます資源管理センター研報 Bull. Natl. Salmon Resources Center, No. 5, 2002

Fig. 1. Maps showing the Bekanbe-ushi River where masu salmon juveniles were collected for the present study (closed circles).

to the nearest millimeter (fork length) and weighedto the nearest gram. Based on the body size and coloration, masu salmon were thought to be age-1 fishand consisted of 18 parrs and one smolt. The
branchial cavity, body surface, fins, and fin bases
were examined for the presence of S. californiensis
using a dissecting microscope. When found, thecopepods were removed and preserved in 70%
ethanol. For the distribution of S. californiensis on
the host fish, attachment sites were recorded fromthe fish (n=14) collected in April of 1982 and 1983.
Based on morphological characters of S. californiensis given by Kabata and Cousens (1973), the copepods were designated into one of the following three
categories: chalimus larvae (with frontal filaments),
young adult females, and mature adult females. To
assess the effect of S. californiensis on juvenile masu
salmon, the condition factor (CF) of the fish (n=17,one heavily damaged fish and one smolt wereexcluded) was calculated as follows: CF = 10 5×

BW/FL3, where BW is body weight (g) and FL isfork length (mm).

Results
Eighteen (94.7%) of the 19 juvenile masu
salmon examined were infected with S. californiensis (Table 1). The parasite was not found on whitespotted charr (n=6) nor Sakhalin taimen (n=3),
although a young adult female of S. carpionis infected the gill arch of the former species. The mean
intensity of S. californiensis on masu salmon was10.3, and the largest number of copepods found on asingle host was 26 (Appendix). The fish ranged from95 to 195 (mean 137) mm in fork length, and there
was a significant increase in intensity of infection as
the size of the host fish increased (r=0.82,p<0.001)(Fig. 2).
A total of 185 copepods of S. californiensis wasfound (Appendix). Most of the copepods wereTable 1. Prevalence and mean intensity of Salmincola californiensis on salmonids caught in the Bekanbe-ushi River in thesprings of 1982 and 1983.
BrookSalmincola californiensis

FishSpecies

Fork length (mm)* Number of samples

Prevalence (%)

Intensity*

Chiraikaribetsu

masu salmon

157±53100

12.3±4.7Toraibetsu

masu salmon

133±291693.89.9±8.4

white-spotted charr

147±30600

Sakhalin taimen

225±63300* Mean±SD.

Nagasawa and Urawa − Salmincola californiensis on masu salmon in Hokkaido

9increase in intensity of infection (Fig. 3), but there
were no significant correlations between condition
factor and intensity of infection (r= -0.46, p>0.05).

Discussion

Fig. 2. Relationship between juvenile masu salmon lengthand intensity of infection with Salmincola californiensis.

Fig. 3. Scatterplot of intensity of infection with Salmincola
californiensis versus condition factor of juvenile masu
salmon.

mature adult females (82.7%), followed by chalimus
larvae (12.4%) and young adult females (4.9%). The
majority (74.1%) of the mature adult females carriedegg sacs, but some (8.6%) had no egg sacs. Of the158 copepods examined for attachment sites, mature
adult females (n=130) were the most common on thegills (49.1%) and the inner surface of the operculum(43.1%). Some mature adults were found on thepectoral and pelvic fins (5.4%) and near the bases ofthe fins (2.3%). Young adult females (n=5) also
occurred on the same sites. Chalimus larvae (n=23)
were found on the gills. There was a difference ininfection site on the gills between developmental
stages: the adult females were attached to distal endsof the gill filaments, whereas the chalimus larvae
were found on basal and middle regions of the gill
filaments.
The distal ends of the gill filaments of juvenile
masu salmon attached by adult females were damaged, and such gill portions were lost. The condition
factor showed a slight decreasing trend with an

The present paper is the first confirmed record ofS. californiensis from Hokkaido. Prior to this report,
there was a record of S. falculata from this region.
Yamaguti (1939) described this species from kokakee (Oncorhynchus nerka) taken in Lake Penke,
eastern Hokkaido. Subsequently, in his review
paper on the genus Salmincola, Kabata (1969) synonymized S. falculata with S. californiensis, andthus the latter species had been believed to be distributed in Hokkaido (cf. Hoshina and Nishimura
1976; Nishimura and Hoshina 1977). However,
Nagasawa et al. (1995) noted that the copepods
reported by Yamaguti (1939) were not S. californiensis but S. carpionis, and this view has been
currently accepted. Salmincola californiensis is thethird species of the genus found in Hokkaido, and S.
stellatus has been reported to occur in this region(Kabata 1986, Nagasawa and Urawa 1991, Nagasawa et al. 1994).
Salmincola californiensis was recorded from
salmon belonging to the genus Oncorhynchus inwestern North America (Kabata 1969). The present
survey confirmed that white-spotted charr andSakhalin taimen, cohabited with juvenile masu
salmon, were not infected, although Nishimura andHoshina (1977) reported S. californiensis fromJapanese charr reared at a hatchery along the Shinano River System in Nagano. It may be necessary
to reconfirm the presence of the parasite on Japanesecharr in that area, because Japanese charr is commonly infected with S. carpionis (Nagasawa et al.
1995).
The intensity of S. californiensis increased withincreasing body length of masu salmon. Similar
results have been reported for other species of thegenus Salmincola (Bowen and Stedman 1990 for S.
corpulentus; Nagasawa et al. 1995, 1998 for S. carpionis). In a laboratory study, Poulin et al. (1991)
demonstrated that larger brook trout (Salvelinus
fontinalis) acquired more infections with Salmincola
edwardsii. This is because larger fish have a greatersurface for attachment of infective larvae and are
exposed to parasites for a longer period .
Most of the adult females found were attached to10

さけ・ます資源管理センター研報 Bull. Natl. Salmon Resources Center, No. 5, 2002

the gills and the inner surface of the operculum.
This result is consistent with the finding by Kabata
and Cousens (1977), who reported that adult S. californiensis were the most common in the branchialcavity of juvenile sockeye salmon (O. nerka) underlaboratory conditions. However, these authors foundthat S. californiensis were the most abundant in theregion of the pectoral and pelvic fins in case of sockeye salmon fry, and it has been suggested that, withan increase in fish length, the gills become a major
attachment site for adult copepods (Kabata andCousens 1977; Sutherland and Wittrock 1985). In
the present study, the chalimus larvae were found on
the basal and middle regions of the gill filaments,suggesting that larval attachments occur in theseregions and preadult females move to distal ends ofthe gill filaments and the inner surface of the operculum for the final attachment (Kabata and Cousens
1977; Sutherland and Wittrock 1985).
Gill tissue destruction caused by adult S. californiensis has been reported (Hoshina and Suenaga
1954; Kabata and Cousens 1977; Sutherland andWittrock 1985). Up to 25% loss of the gill surface
due to this parasite is known (Kabata and Cousens
1977). Although we did not measure the missing
surface areas of infected gills, we recognized similar
damaged conditions reported by Kabata and Cousens(1977, Fig. 8) and Sutherland and Wittrock (1985,Fig. 5). Some histopathological studies on infectedgill tissues have been made (Hoshina and Suenaga
1954; Kabata and Cousens 1977; Sutherland andWittrock 1985), but little information is available on
the effect of the parasite on the body condition ofinfected fish. We did not find a significant decreasein condition factor for the infected fish, but since S.
californiensis has been documented to reduce theegg production of hatchery-reared rainbow trout (O.
mykiss) (Gall et al. 1972), it is desirable to assess theimpact of this parasite on the growth, maturation,and physiology of the host fish.

Acknowledgements
We thank Motohiro Sakurai, Jun Nakata, andChiaki Fujisawa for their help with fish sampling.

References
Bowen, C. A., II, and R. M. Stedman. 1990. Hostparasite relationships and geographic distributionof Salmincola corpulentus (Copepoda: Lernaeopodidae) on bloater (Coregonus hoyi) stocks in Lake
Huron. Can. J. Zool., 68: 1988-1994.
Gall, G. A. E., McClendon, E. L., and W. E. Schafer.
1972. Evidence on the influence of the copepod(Salmincola californiensis) on the reproductive
performance of a domesticated strain of rainbow
trout (Salmo gairdneri). Trans. Am. Fish. Soc.,
101: 345-346.
Hoshina, T., and G. Suenaga. 1954. On a newspecies of parasitic copepods from yamame(salmonoid fish) of Japan. J. Tokyo Univ. Fish.,41: 75-78, 1 pl.
Hoshina, T., and T. Nishimura. 1976. On a parasitic
Copepoda, Salmincola californiensis found on asalmonid fish, yamame, Oncorhynchus masou.
Fish Pathol., 11: 153-157. (In Japanese with English summary.)
Kabata, Z. 1969. Revision of the genus Salmincola
Wilson, 1915 (Copepoda: Lernaeopodidae). J.
Fish. Res. Board Can., 26: 2987-3041.
Kabata, Z. 1986. Redescriptions of and comments onfour little-known Lernaeopodidae (Copepoda).
Can. J. Zool., 64: 1852-1859.
Kabata, Z., and B. Cousens. 1973. Life cycle ofSalmincola californiensis (Dana 1852) (Copepoda: Lernaeopodidae). J. Fish. Res. Board Can., 30:
881-903.
Kabata, Z., and B. Cousens. 1977. Host-parasite relationships between sockeye salmon, Oncorhynchus
nerka, and Salmincola californiensis (Copepoda:Lernaeopodidae). J. Fish. Res. Board Can., 34:
191-202.
Nagasawa, K. and S. Urawa. 1991. New records ofthe parasitic copepod Salmincola stellatus fromSakhalin taimen (Hucho perryi) in Hokkaido, witha note on its attachment site. Sci. Rep. Hokkaido
Salmon Hatchery, 45: 57-59.
Nagasawa, K., S. Urawa, and T. Awakura. 1987. A
checklist and bibliography of parasites ofsalmonids in Japan. Sci. Rep. Hokkaido Salmon
Hatchery, 41: 1-75.
Nagasawa, K., J. R. Watanabe, S. Kimura, and A.
Hara. 1994. Infection of Salmincola stellatus(Copepoda: Lernaeopodidae) on Sakhalin taimen
Hucho perryi reared in Hokkaido. Bull. Fac. Fish.
Hokkaido Univ., 45: 109-112.
Nagasawa, K., M. Yamamoto, Y. Sakurai, and A.
Kumagai. 1995. Rediscovery in Japan and hostassociation of Salmincola carpionis (Copepoda:

Nagasawa and Urawa − Salmincola californiensis on masu salmon in Hokkaido

Lernaeopodidae), a parasite of wild and reared
freshwater salmonids. Can. J. Fish. Aquat. Sci., 52(suppl. 1): 178-185.
Nagasawa, K., K. Ikuta, H. Nakamura, T. Shikama,and S. Kitamura. 1998. Occurrence and effects ofthe parasitic copepod Salmincola carpionis onsalmonids in the Nikko District, central Japan. J.
Mar. Systems, 15: 269-272.
Nishimura, T., and T. Hoshina. 1977. On a parasitic
Copepoda, Salmincola californiensis found on asalmonid fish, Salvelinus leucomaenis pluvius. J.
Tokyo Univ. Fish., 63: 67-70. (In Japanese withEnglish summary.)
Poulin, R., M. A. Curtis. And M. E. Rau. 1991. Size,behaviour, and acquisition of ectoparasitic copepods by brook trout, Salvelinus fontinalis. Oikos,
61: 169-174.
Sutherland, D. R., and D. D. Wittrock. 1985. The
effects of Salmincola californiensis (Copepoda:Lernaeopodidae) on the gills of farm-raised rainbow trout, Salmo gairdneri. Can. J. Zool., 63:2893-2901.
Yamaguti, S. 1939. Parasitic copepods from fishes ofJapan. Part 6. Lernaeopodida, I. Vol. Jubil. pro
Prof. Sadao Yoshida, 2: 529-578.

11

別寒辺牛川のサクラマス幼魚におけるヤマメナガクビムシ（新称）Salmincola californiensis の寄生状況
長澤和也・浦和茂彦
北海道東部の別寒辺牛川で1982年と1983年の春季に採集したサケ科魚類におけるヤマメナガクビムシ
Salmincola californiensisの寄生状況を調べた．検査したサクラマス幼魚19個体中，18個体（94.7%）が寄生を受け，1個体当たりの平均寄生数は10.3虫体であった．アメマスとイトウには本虫の寄生がみられなかった．寄生数は，サクラマス幼魚の体長の増加とともに有意に増加した．採集されたヤマメナガクビムシは成熟雌，未成熟雌，カリムス幼生から成り，成熟雌の多くは鰓や鰓蓋内面に寄生していた．
カリムス幼生は鰓のみに見られた．成熟雌が鰓先端部に寄生した場合には，寄生部位は欠損していた．
寄生数の増加に伴ってサクラマス幼魚の肥満度は有意に減少しなかった．わが国におけるヤマメナガク
ビムシの記録はこれまで長野県と群馬県に限られ，本報告が北海道からの初記録となる．なお，
Salmincola属とこの属に含まれる種に対して和名がないことから，本属に対してヤマメナガクビムシ属，S. carpionisにイワナナガクビムシ，S. stellatusにイトウナガクビムシ，S. edwardsiiにオショロコマナガク
ビムシの和名を提案する．

195
127

masu salmon
masu salmon
masu salmon
masu salmon
masu salmon
masu salmon*1
white-spotted charr*2
white-spotted charr
white-spotted charr
white-spotted charr
white-spotted charr
white-spotted charr
Sakhalin taimen
Sakhalin taimen
Sakhalin taimen

April 29, 1982

April 29, 1982

April 29, 1982

April 29, 1982

April 29, 1982

April 29, 1982

April 29, 1982

April 29, 1982

June 27, 1982

June 27, 1982

June 27, 1982

June 27, 1982

June 27, 1982

April 23, 1983

April 23, 1983

April 23, 1983

April 23, 1983

April 29, 1982

June 27, 1982

June 27, 1982

June 27, 1982

June 27, 1982

June 27, 1982

April 23, 1983

June 27, 1982

June 27, 1982

Chiraikaribetsu

Toraibetsu

ToraibetsuToraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu

Toraibetsu*1 Smolt. Other masu salmon were parrs.
*2 One preadult of Salmincola carpionis infected the gill arch.

masu salmon

masu salmon

masu salmon

masu salmon

masu salmon

masu salmon

masu salmon

masu salmon

masu salmon

masu salmon

masu salmon

287

227162150125120120185181168

175

115

132

135

122

139

106

105

95

103

114

149

155

160

160

152

April 29, 1982

masu salmon

masu salmon

Fork length(mm)April 29, 1982

SpeciesFish

Chiraikaribetsu

Date of catch

Chiraikaribetsu

Brook

318.2

170.2

42.9

47.6

26.2

28.9

24.9

85.6

63.4

22.1

93.0

58.0

54.2

24.8

35.4

38.6

30.7

38.6

12.2

14.5

11.2

13.6

19.7

44.9

46.2

51.0

58.7

45.1

Weight (g)Appendix. A record of Salmincola californiensis on salmonids caught in the Bekanbe-ushi River.

00000000000000000000035100005Chalimus
larvae0000000000103002020000000100

Young adultfemales

000000000024131801219412131116616

90000000000

1002242010

100

30000

Adult females Adult femaleswith egg sacs with no egg sacs

Number of parasites

000000000026132123831151348241671614Total12さけ・ます資源管理センター研報 Bull. Natl. Salmon Resources Center, No. 5, 2002