First Record of the Parasitic Ciliate Trichodina truttae Mueller, 1937

on Chum Salmon Fry (Oncorhynchus keta) from Japan

*1Hokkaido Salmon Hatchery , Fisheries Agency of Japan, 2-2 Nakanoshima,

Toyohira-ku, Sapporo 062, Japan
*2Maurice Lamontagne Institute , Fisheries and Oceans, P.O. Box 1000,
Mont-Joli, Quebec, Canada G5H 3Z4

(Received March 4, 1991)

The parasitic ciliate Trichodina truttae Mueller, 1937 is redescribed from silver-impregnated

specimens collected from the body surface of chum salmon fry (Oncorhynchus keta) reared in

five hatcheries of Hokkaido and northern Honshu, Japan. The description is supplemented

by scanning electron microscopic observations. The distinguishing morphological features

include its large size (body diameter 115-178 ƒÊm), high number (10-23) of radial pins per

denticle, and the presence of two markedly different lengths of cilia within the adoral ciliary

spiral. Geographical variation was observed in the body size and number of denticles. This

is the first record of T. truttae from Japan.

Ciliates belonging to the family Trichodinidae ciliates from farmed salmonids in Honshu (see
are common and occasionally pathogenic para Nagasawa et al., 1987). Recently, we also en
sites of freshwater and marine fishes (Lom and countered many cases of Trichodina infections
Hoffman, 1964; Lom and Laird, 1969; Hoffman, among hatchery-reared salmon fry. Experimen
1978). In Japan, trichodinid infections fre tally, the ciliate caused severe mortalities in
quently occur on cultured freshwater and ma chum salmon fry (Urawa, unpublished data).
rine fishes, but taxonomic and pathological The present study was conducted to clarify
studies of this group have been very few the species of trichodinid ciliate occurring on
(Egusa, 1978). Although Ariake (1929) and the skin of chum salmon fry in northern Japan,
Suzuki (1950) reported several new species of and consequently the ciliate was identified as
trichodinids from Japan, these descriptions were Trichodina truttae Mueller, 1937. This species
considered by Albaladejo and Arthur (1989) to was originally described from the gills of
be too inadequate to permit positive reidentifi hatchery-reared cutthroat trout (Oncorhynchus
cation. The only other confirmed identifications clarki) in Oregon (Mueller, 1937), and has been
of Trichodina from Japanese fishes are those of subsequently reported from various salmonids in
Ahmed (1976, 1977), who reported T. reticulata western North America and the USSR (Davis,
Hirschmann and Partsch, 1955 on goldfish (Car 1947, 1953; Bogdanova, 1963, 1967, 1977; Bog
assius auratus), crucian carp (C. auratus) and danova and Shtein, 1963; Arthur and Margolis,
color carp (Cyprinus carpio). 1984). Because this finding constitutes the first
In 1968, high mortalities occurred among record of T. truttae from Japan, the parasite
chum salmon (Oncorhynchus keta) fry reared is redescribed according to Klein's (1958) dry
in Ichani Hatchery, eastern Hokkaido, due to silver-impregnation technique and scanning el
trichodinid infections (Takeda et al., 1969). ectron microscopy (SEM), and some aspects of
Although the parasite was reported as T. do its geographical variability are noted.
merguei (Wallengren, 1897), its identification is
suspect, since it was not based on detailed
morphological studies (Nagasawa et al., 1987).
Several other papers also reported trichodinid Trichodinids were collected from the body
 (Eiko), and then observed using an Akashi
scanning electron microscope. Terminology
and methods of measurement follow the uni
form specific characteristics proposed by Lom
(1958) and Arthur and Lom (1984). All meas
urements are given in micrometers.

Trichodina truttae Mueller, 1937 (Figs. 2-9)

Host: chum salmon fry (Oncorhynchus keta).

Site of infection: Body surface.

Localities : Asahi Hatchery, Rishiri Island,

northern Hokkaido; Chitose Hatchery, western
Hokkaido; Ichani Hatchery, eastern Hokkaido;
Ohkawa Hatchery, Miyagi Prefecture, Pacific
coast of northern Honshu; Gakko Hatchery,
Yamagata Prefecture, Japan Sea coast of north
ern Honshu.

Deposition of specimens : One slide including

silver-impregnated specimens from chum salm
on fry from Asahi Hatchery has been deposited
in the National Science Museum, Tokyo (NSMT
Pr. 165).
Fig. 1. Map of collection localities for Trichodina
truttae infecting chum salmon fry in north Description
ern Japan. Numbers refer to hatcheries The following description is based mainly on
given in the legend of Fig. 10. silver-impregnated ciliates collected from Asahi
and Chitose Hatcheries (Table 1), supplemented
surface of chum salmon fry from five hatcheries by SEM observations.
in Hokkaido and northern Honshu between A relatively large trichodinid with a disc
1981 and 1990 (Fig. 1). Air-dried smears of shaped body (Fig. 6), 114.7-177.5 in diameter.
living ciliates taken from the skin were pre Adhesive disc cup-shaped, 81.1-125.0 in diame
pared for light microscopical observations. ter, surrounded by a wide border membrane,
Smears were immersed in a 2% solution of 6.5-12.0 in width. Adoral ciliary complex con
silver nitrate (AgNO3) for 10 min, and exposed sisting of three distinct ciliary bands : basal ciliary
to ultraviolet light for 15-20 min (Klein's dry ring, locomotor ciliary wreath, and marginal
silver-impregnation technique). In addition , ciliary ring (Figs. 6-8). Center of adhesive disc
some formalin preserved specimens were im dark and uniformly granular in silver-impreg
pregnated with silver according to Wellborn nated specimens. Denticulate ring 45.3-75.0 in
(1967). For SEM, ciliates were fixed by im diameter, consisting of 24-31 denticles (Figs. 2
mersion of whole living chum salmon fry in and 3). Span of denticle 24.5-35.5; length
1% glutaraldehyde in 0.1 M phosphate buffer . 12.8-20.0. Blade of denticle acutely falciform
Parasites were centrifuged and dehydrated with highly concave anterior border and sharply
through a graded alcohol series. The alcohol angled posterior margin (Fig. 4). Blade joining
was replaced with isoamyl acetone , and the central portion of denticle posterior to median
samples were dried in a Hitachi critical point axis of thorn. Length of blade 8.8-14.0. Central
drying unit, gold-coated in a sputter-coater part thick, 4.5-8.5 in width, its external portion
 85

Figs. 2-5. Photomicrographs of Trichodina truttae from chum salmon fry. 2, Adhesive disc
of silver-impregnated specimen collected from Asahi Hatchery. Bar=20ƒÊm. 3,
Adhesive disc of silver-impregnated specimen from Chitose Hatchery. Bar=25 ƒÊm .
4, Detail of adhesive disc in Fig. 3, showing radial pins, which appear as pairs in
this specimen. Bar =10 ƒÊm. 5. Oral view of fresh specimen from Chitose Hatchery,
showing adoral ciliary spiral. Bar =40 ƒÊm. LAC. long adoral cilia: SAC, short

adoral cilia.
 S.Urawa and J.R. Arthur

Figs. 6-9. SEM photomicrographs of Trichodina truttae from chum salmon fry reared in Chitose

Hatchery. 6, Oral view of entire specimen. Bar=35ƒÊm. 7, Enlargement of oral

surface showing short adoral cilia. Bar=7ƒÊm. 8, Enlargement of oral surface

showing long adoral cilia and buccal cavity. Bar=8 ƒÊm. 9, Adhesive disc showing

radial pins and denticles. Note the low number of radial pins per denticle (about

12) indicative of a recently divided specimen. Bar=5ƒÊm. ACS, adoral ciliary spiral;

BC, buccal cavity; BM, border membrane; D, denticle; LAC, long adoral cilia;

LCW, locomotor ciliary wreath; MCR, marginal ciliary ring; RP, radial pins; SAC,

short adoral cilia.

cylindrical. Thorn thickened at base, tapering (Fig. 7), only final area near buccal cavity com-
gradually to a sharp point. Length of thorn prised of long cilia (Fig. 8). Macronucleus U-
10.4-16.0. Number of radial pins per denticle shaped, about 80 in diameter.
10-23 (Figs. 4 and 9). Adoral ciliature forming
a spiral of about 450° (Fig. 5). The majority Geographical Comparison
of cilia comprising the adoral ciliary spiral short Fig. 10 compares variation in parasite size
 Table 1. Comparison of morphometrics of Trichodina truttae from salmonids in Japan
and Canada. Measurements are given in micrometers, and are based on silver
impregnated specimens

(denticulate ring) and number of denticles among the more than 100 species of Trichodina described
T. truttae populations collected from five hatch from freshwater fishes, and the number of radial
eries in northern Japan and one in Canada. The pins per denticle (14-26) is the highest number
ciliates from Asahi (location 1) and Ichani (2) reported for any member of the genus (Arthur
Hatcheries in Hokkaido are significantly larger and Margolis, 1984). In addition, their SEM
than those from other hatcheries (P<0.01). The observations, confirmed by the present study,
number of denticles appears to increase with note that the presence of two markedly different
decreasing latitude in northern Japan except for lengths of cilia within the adoral ciliary spiral
specimens from Chitose Hatchery (3) where the may also be unique to T. truttae. Morphological
denticle number is very small (24-26). features of our specimens are comparable with
those of T. truttae as given by Arthur and
Discussion Margolis (1984) (Table 1).
Many of our Japanese specimens have low
Arthur and Margolis (1984) stated that the numbers (8-12) of radial pins per denticle (Fig.
diagnostic features of T. truttae are its large 9). These individuals are smaller than ciliates
size and large number of radial pins per den with high denticle number (18-23). These
ticle. This species is the largest ciliate among smaller ciliates have recently undergone mi
 other hatcheries. Then, these differences in the
body size may be due to differences in environ
ment (e.g., water temperature) and/or differences
in the number of recently divided ciliates among
the populations. Kazubski and Pilecka-Rapacz
(1981) similarly reported seasonal and interpo
pulational variability in the body dimensions of
T. nigra Lom, 1961.
Takeda et al. (1969) recorded T. domerguei
from chum salmon fry reared in Ichani Hatchery
without providing any morphological descrip
tion. Takeda (1971) also reported a heavy in
fection of Cyclochaeta (=Trichodina) domerguei
on chum salmon alevins in Nemuro Hatchery,
eastern Hokkaido, and listed Sakhalin taimen
(Hucho perryi) and masu salmon (Oncorhynchus
masou) as experimental hosts. Although T.
domerguei has, on one occasion (see Bogdanova
and Shtein, 1963), been reported from chum
salmon fry, this species is primarily a parasite
of gasterosteid fishes (see Lom and Stein, 1966).
Our finding of only T. truttae from the same
hatcheries as those from which T. domerguei
was reported by Takeda et al. (1969) and Takeda
(1971) and the lack of supporting evidence to
validate their identifications leads us to believe
Fig. 10. Geographical variation in the diameter that these reports are probably referable to T.
of the denticulate ring and number of truttae.
denticles for Trichodina truttae. Each
open circle represents the mean, the ver
Acknowledgements
tical bar represents the range. The number
above or below each point is the sampling The authors thank Mr. Akira Kumagai of
locality. 1, Asahi Hatchery (n=25); 2,
Kesennuma Miyagi Prefectural Fisheries Exper
Ichani Hatchery (n=20); 3, Chitose Hatch
imental Station and Mr. Yutaka Kasahara of
ery (n=21); 4, Ohkawa Hatchery (n=20);
5, Gakko Hatchery (n=20); 6, Quinsam Fisheries Office, Yamagata Prefecture for pro

Hatchery (49.3'N, 124.2'W) on Vancouver viding fish samples, and Dr. Kiyokuni Muroga
Island, B. C. (n=25; from Arthur and of Hiroshima University for valuable comments
Margolis, 1984). on the manuscript.

tosis. They have completed production of a References

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