第39卷 第3期 水生生物学报 Vol. 39, No.3

2015 年 5 月 ACTA HYDROBIOLOGICA SINICA May, 2 0 1 5 doi: 10.7541/2015.74

THE FIRST RECORDS OF TRICHODINID ECTOPARASITES (CILIOPHORA, PERITRICHIA) FROM WILD MARINE FISHES IN THE SOUTH CHINA SEA

WANG Wen-Qiang, TANG Fa-Hui and ZHAO Yuan-Jun (Chongqing Key Laboratory of Animal Biology, Chongqing Normal University, Chongqing 401331, China)

Abstract: Several marine fishes were surveyed in the South China Sea, from which, four trichodind species (Ciliophora, Peritrichia) belonging to the genus Trichodina were isolated and studied. They are Trichodina puytoraci Lom, 1962, Trichodina japonica Imai, et al., 1991, Trichodina rectuncinata Raabe, 1958 and Trichodina fugu Imai, et al., 1997. This survey has revealed that Trichodina fugu Imai, et al., 1997 was the pathogen for the host Takifugu vermicularis and could cause mortality in wild condition. Taxonomic and morphometric data for these trichodinids based on dry silver nitrate-impregnated specimens are presented in the paper. To our best knowledge, this study is the first formal report on these trichodinids from the South China Sea.

Key words: Trichodina; First record; Marine fishes; South China Sea CLC number: Q959.117 Document code: A Article ID: 1000-3207(2015)03-0564-10

As part research work of investigations of fish able information of the pathogen Trichodina fugu Imai, parasitology in China, the main aquatic parasites re- et al., 1997 to the industry of mariculture and marine ported are mainly myxosporea and trichodinid groups ecology. and usually caused serious diseases in the recent find- ings[1—8]. Among them, trichodinid ciliates, as well- 1 Materials and methods known ectoparasites of fishes or mollusks, often para- The wild host fishes (Gerres filamentosus Cuvier, sitize on maricultured and freshwater animals. Up to 1829; Mugil cephalus Forskal, 1775; Leiognathus date, more than 300 nominal trichodinid species have bindus Valenciennes, 1835; Takifugu vermicularis been reported from different environments around the Temminck and Schlegel 1850) were caught in the world [6, 9—15]. South China Sea during March 2011 to June 2012 in In China, a series of research works on tricho- Sanya City, China. The fishes were adults and no ap- dinids have been carried out in the recent fifteen years from parent symptom of disease, deformity or malnutrition all kinds of freshwater and marine environments [16—24]. to be found by eye inspect except some puffer fish Although some trichodinids have been found from the (Takifugu vermicularis) in Dadonghai sea showed Bohai Bay and the Yellow Sea in China [20—24], in marine dermohemia, damaged gills, more mucus over the and brackish-water of China, trichodinid ciliophorans body and emptiness of the digestive track. Gills or still remain a poorly studied group, and these cilio- tissue smears were prepared as air dried specimens phorans from the South China Sea have been never from freshly collected fishes. These specimens were reported and need to be further studied systematically. washed with distilled water to get rid of chloride ion, In the present research work, we report four impregnated with 1% silver nitrate solution for 15min, trichodinid species collected from wild marine fishes exposed to incandescent light for 5min, examined un- from the South China Sea, and compared them with der the LEICA DM750 microscope and microphoto- previously reported population from other host fishes graphed using LEICA DM6000B. The macronucleus from other sea areas and discussed the possible rea- morphology, the micronucleus position relative to the sons for their flourish, hoping to provide some valu- macronucleus and all measurements were performed

Received date: 2014-08-27; Accepted date: 2014-11-09 Foundation item: The National Natural Science Foundation of China (No. 31101637, No. 31172068); the Project of Chongqing Science & Tech- nology Commission (No. CSTC, 2010CA1010; No. cstc2014jcyjA80008); the Science Research Foundation of the Education Committee of Chongqing (No. KJ1400530) Brief introduction of author: Wang Wen-Qiang (1986—), male, Chengdu, China; Master’s degree graduates; mainly engaged in Fish Parasitol- ogy. E-mail: [email protected] Corresponding author: Zhao Yuan-Jun, E-mail: [email protected]

3 期 王文强等: 南中国海野生海水鱼类外寄生车轮虫新记录 565 following the uniform specific characteristic system The present host Gerres filamentosus, which is a proposed by Lom (1958)[25]. Denticle characteristics coastal inhabitant and collected from Yalong Bay of were described following the method given by Lom China, is a new host record for T. japonica. According (1958) and Van As and Basson (1989) [14, 25]. Measu- to our study, T. japonica seems more likely to infect rements were presented in mircometres (μm). coastal marine fishes in Asia, as currently it is only seen in Asia and present in nearly the smallest popula- 2 Results tion compared to other reported ones. Coincidently, it Subclass Peritrichia Stein, 1859 is also geographically distributed at the lowest latitude, Order Mobilida Kahl, 1933 which contributes to expanding its host range. Family Trichodinidae Claus, 1874 Trichodina puytoraci Lom, 1962 Genus Trichodina Ehrenberg, 1838 Host and site: Mugil cephalus (Forskal, 1775), Trichodina japonica Imai, et al., 1991 gills. Host and site: Gerres filamentosus (Cuvier, 1829), Locality: Shore of Dadonghai (109.5°E,18.2°N), gills. Sanya City, China. Locality: Yalong Bay (109.7°E, 18.2°N), Sanya Body: Medium-sized marine Tichodina speices, City, China. with diameter of 27.0—38.5 (33.76±3.18). Body: Small-sized marine Tichodina species with Adhesive disc: 23.7—34.4 (30.08±3.06) in di- diameter of 24.0—28.5 (26.0±1.75) ameter. Adhesive disc: 21.0—26.0 (23.2±1.64) in diameter. Denticle ring: 14.4—22.4 (18.78±2.45) in di- Denticle ring: 12.0—4.0 (13.1±0.85) in diameter. ameter. Border membrane: Whitish, 1.0—1.7 (1.47±0.31) Border membrane: Finely striated and 1.0—3.0 wide. (1.67±0.56) wide. Number of denticles: 18—19. Number of denticles: 20—25. Number of radial pins per denticle: 6—7. Number of radial pins per denticle: 7—9. Dimensions of denticle: Length: 2.5—3.0 (2.64± Dimensions of denticle: Length: 3.2—4.8 (3.89± 0.15), blade length: 1.5—2.0 (1.84±0.17), central part 0.47), blade length: 2.3—4.2 (3.20±0.46), central part length: 0.5—1.5 (0.99±0.15), ray: 2.5—3.0 (2.64± length: 0.7—1.9 (1.44±0.33), ray: 2.5—5.3 0.15), span: 5.5—6.5 (5.95±0.14). (3.65±0.83), span: 6.7—10.0 (8.67±0.95). Nuclear apparatus: Macronucleus horseshoe- Nuclear apparatus: Macronucleus U-shaped; mi- shaped, micronucleus not observed. cronucleus oval, usually situated in +y position. Adoral spiral: About 380°. Adoral spiral: About 380°. Denticle morphology (PlateⅠ-1): Broad blade, Denticle morphology (PlateⅠ-2): Broad blade fitting most space between Y+1 axis; round distal with slightly falcate, fitting most space between Y+1 blade surface with curve to anterior blade surface and axis; truncated or flat distal blade surface parallel to lower than tangent point; round and smooth blade border membrane when situated close to it and almost tangent point; anterior and posterior surfaces conver- at the same level with tangent point; blunt and smooth gent almost straightly and heavily to the centre; ante- tangent point; smoothly down-curved anterior surface rior surface closed to Y + 1 axis, invisible blade almost touching Y+1 axis, forming a shallow apex; apophysis and posterior projection; slender central absent anterior and posterior blade apophysis; delicate part with round point fitting loosely into preceding blade connection; slender central part with blunt point denticle and extending more than halfway to Y–1 axis; fitting tightly with preceding denticle; similar sections robust ray connection, tapering to the sharp point; ab- above and below X-axis; straight ray with throughout sent ray apophysis. same thickness, but thicker end and invisible round tip; Remarks. T. japonica was originally described visible ray apophsis. Posterior margin forms shallow, by Imai, et al. (1991) from the gills of cultured Japa- semilunar curve with deepest point lying lower than nese eel, Anguilla japonica and redescribed by Xu, et apex. al. (1999) from the gills of cultured percoids, Lateo- Remarks. T. puytoraci was originally described labrax japonicus and Chrysophrys major in Qingdao, by Lom from the gills of Mugil auratus, Mugil salieus China[20, 26]. Later, it was reported by Mitra and and Mugil cephalus from the Black Sea coast in Ru- Bandyopadhyay from the gills of Lates calcarifer in mania (PlateⅠ-3). Based on its morphology, the pre- [27] India . The population presented in our study is sent species was identified as T. puytoraci. However, it identical in morphometry and denticle shape to T. ja- [26] is comparatively smaller in size than the previously ponica originally described by Imai, et al. . reported ones from Mugil auratus, Mugil saliens, Mugil

566 水生生物学报 39 卷 platanus and Mugil cephalus [9, 28, 29] (Tab. 1). This a lot, as the case that T. rectuncinata and T. puytoraci species can be easily distinguished from other sea- reported here from Mugil cephalus in the South water trichodinids by the presence of several thickly China Sea apparently have denticles with smaller size dotted granules in the centre of adhesive disc, and by than other populations described by Lom (1962) [9] the truncated distal blade margin, widened and swol- (Tab. 1). len tip of the ray and distinct ray apophysis. Moreover, Besides, another trichodinid species named as T. puytoraci seems to have a narrower host range, be- Trichodina chittagongesis was found to be similar to cause it was mainly found from the genus of Mugil the present species (PlateⅠ-4). T. chittagongesis Linnaeus, 1758. Thus, the identification is beyond was described from the gills of Labeo bate from doubt. This is the first report of T. puytoraci in the Karnaphuli River, India by Asmat, et al. [30]. It is South China Sea, while the difference in body size remarked by Asmat, et al. that T. chittagongesis is from other populations from different sea areas in the distinguished from T. puytoraci in the aspects such world such as the Black Sea and Samborombón Bay, as the distal margin, the tip of the ray, the ray Argentina, is considerable. Our population has the apophysis etc., and shows high morphologic simi- smallest body size and denticle numbers compared larity with the original one described by Lom [9]. with those found from areas with the lowest latitude. The relationship between T. chittagonesis and T. The different population variation within one tricho- Puytoraci maybe needs to be clarified with more dinid species from different regions or hosts can differ data (PlateⅠ-3) (Tab. 1).

Tab. 1 Morphometric comparison of different populations for Trichodina puytoraci Lom, 1962 and Trichodina chittagongensis Asmat, et al., 2005 Populations of Trichodina Trichodina Trichodina Trichodina Trichodina Trichodina Trichodina Trichodina puytoraci puytoraci puytoraci puytoraci puytoraci puytoraci chittagongensis spp. (population 1) (population 2) (population 3) (population 4) (population 5) (population 6) Host Mugil cephalus Mugil cephalus Mugil auratus Mugil saliens Liza(=Mugil) aurata Mugil platanus Labeo bata Localization gills gills gills gills gills, skin, fins gills gills the South Karnaphuli Location the Black Sea the Black Sea the Black Sea the Black Sea Argentina China Sea River 27.0—38.5 36.7—45.9 Body diameter 42—54 (45) 45—51 (48) 40—50 (43) not determined — (33.8±3.2) (40.6) Adhesive 23.5—34.5 4.8—6.4 29.6—37.7 33—42 (36) 30—42 (36) 28—41 (35) 40—52 (45.0) disc (30.1±3.1) (57.1±4.7) (33.0) Denticular 14.0—22.5 28.5—39.9 19.4—24.5 19—27 (22) 19—27 (23) 16—26 (20) 24.5—32.0 (28.5) ring (18.8±2.5) (34.1±3.4) (21.7) Border 1.0—3.0 3.0—5.1 2.5—4.1 3.3 — — 4.1—5.0 (4.5) membrane (1.7±0.6) (3.9±3.4) (3.8) Denticle 22—24 20—25 (23) 23—29 (27) 25—31 (27) 22—30 (27) 24—29 (26) 25—29 (27) number (22.9) 5—8 Radial pins per 7—9 (8) — — — 7—8 5—8 (7) (6.6) 6.5—10.0 4.9—18.4 9.7—13.3 Denticle span — — — 13.0—14.7 (13.7) (8.7±1.0) (16.4 ±1.2) (11.2) 3.0—5.0 7.6—11.2 5.1—6.1 Denticle length 7 — — — (3.9±0.5) (9.2±1.2) (5.2) 2.0—4.5 5.1—8.0 4.1—6.1 Blade length 4.5 — — 4.6—5.6 (5.1) (3.2±0.5) (6.4±0.7) (5.1) Central part 0.5—2.0 2.5—3.9 2.0—2.5 1.6 — — 2.0—3.0 (2.3) width (1.4±0.3) (3.2±0.4) (2.1) 2.5—5.5 4.9—9.0 3.1—5.2 Ray length 4.5 — — 5.8—6.7 (6.3) (3.7±0.8) (7.3±0.9) (4.0) Adoral ciliary About 380° 370°—380° — — — 390°—400° spiral Marcotegui and Asmat, Data resources Present study Lom (1962)a Lom (1962)b Lom (1962)c Özer, et al. ( 2004) Martorelli (2009) et al. (2005)

Trichodina rectuncinata Raabe, 1958 hizhou Island (109.8°E,18.3°N), Sanya City, China. Host and site: Gerres filamentosus (Cuvier, 1829), The following descriptions are based on the gills. Leiognathus bindus (Valenciennes, 1835), gills. specimens from L. bindus. Locality: G. filamentosus from Yalong Bay Body: Small-sized marine Tichodina species, (109.7°E, 18.2°N), and L. bindus from reefs of Wuz- with diameter of 18.9—24.9 (22.50±1.54).

3 期 王文强等: 南中国海野生海水鱼类外寄生车轮虫新记录 567

Adhesive disc: 16.5—21.9 (19.79±1.48) in diameter. clearly visible in all specimens and the ray shape and Denticle ring: 8.5—12.80 (10.82±1.35) in diameter. width of the centre part differ a lot from other popula- Border membrane: 0.9—1.7 (1.25±0.20) wide. tions from other hosts or regions in the world. The Number of denticles: 19—22. hosts, G. filamentosus and L. bindus, are new records Number of radial pins per denticle: 5—7. for T. rectuncinata, which expands the host range of Dimensions of denticle: Length: 1.6—3.1 (2.37± this parasite (PlateⅡ). 0.44), blade: 2.0—4.0 (3.17±0.56), central part: 0.7— Trichodina fugu Imai, et al., 1977 1.9 (1.04±0.28), ray: 0.4—0.9 (0.76±0.15), span: Based on the collection way, host fishes can be 4.0—6.6 (5.45±0.73). divided into two groups: Group A, fishes fishing in the Nuclear apparatus: Macronucleus C-shaped; mi- sea, and Group B, dead or dying fishes on the shore, cronucleus oval, usually situated in +y position. which were heavily infected with T. fugu. The follow- Adoral spiral: About 400°. ing descriptions are based on the specimens from Denticle morphology (Plate Ⅱ). Straight, tri- Group B, as there were more valid specimens in the angular-shaped blade with round outline, fitting a group. small proportion between Y+1 axis; smooth, round Host and site: Takifugu vermicularis (Temminck distal blade surface higher than tangent point; round, and Schlegel 1850), gills, body surface, fins, urogeni- bulbous and indistinct tangent point; almost straight tal sinus. anterior and posterior surfaces; posterior surface Locality: Haitang Bay (109.5°E, 18.2°N) and nearly on the Y axis; hardly determined blade apex Dadonghai Bay (109.8°E, 18.4°N), Sanya, China. and deepest curve point; absent anterior and posterior Body: Medium-sized, hat-shaped trichodinid with blade apophysis; wide blade connection; robust central diameter of 33.0—53.7 (45.64±4.66). part with blunt point fitting tightly with preceding Adhesive disc: 29.1—49.0 (41.30±5.08) in diameter. denticle; flat and short ray, tapering directly back- Denticle ring: 20.2—34.1 (28.82±3.50) in diameter. wards at the ends. Border membrane: Finely striated and, 0.9—2.8 Remarks. T. rectuncinata is a worldwide marine (1.59±0.45) wide. trichodinid. It was originally described by Raabe from Number of denticles: 24—30. four species of Adriatic fishes and later reported by Number of radial pins per denticle: 7—9. Lom on Gaidropsis mediterranaeus and Crenilabrus Dimensions of denticle: Length: 2.7—5.8 (4.51± griseus from the Romanian coast off Black Sea and 0.75), blade length: 3.6—5.5 (4.78± 0.45), central part Hippocampus guttulatus and Blennius pholis from length: 1.4—2.9 (2.21±0.42), ray: 3.3—6.6 (5.35±0.88), Dinard and Brittany coast of France [31]. Grupcheva, et span: 9.6—14.8 (13.09±1.37). al. studied T. rectuncinata from the gills of C. ocella- Nuclear apparatus: Macronucleus horseshoe-shaped tus, B. sanguinolentus, B. tentacularis, B. sphinx, B. and micronucleus not observed. gattorugine, Gobius guadrimaculatus, Syngnathus Adoral spiral: about 400°. typhle argentatus, S. nigrolineatus, H. hippocampus Denticle morphology (Plate Ⅲ ). Bar-shaped, microcoronatus from the Bulgarian Sea coast of the narrow blades, filling a small portion between Y axes; Black Sea and the Banyuls-sur-Mer coast of the smooth, round distal blade surface slightly higher than Mediterranean Sea [32]. Later, Loubser, et al. described tangent point; round, bulbous and indistinct tangent two populations from the Bay of Dakar, Senegal [33]. In point; straight anterior and posterior surfaces, nearly China, only two different populations of this species parallel to each other, making blade apex and deepest were reported by Xu, et al. (2001) from the gills of curve point difficult to determine; anterior surface far Lateolabrax japonicus and Agrammus agrammus in away from Y+1 axis; absent blade apophysis and the Yellow Sea and the Bohai Sea [22]. In our present prosterior projection; comparably robust, cylinder- research, another two populations of T. rectuncinata shaped,central part fitting tightly into preceding denti- were isolated from the gills of Gerres filamentosus and cle and extending to Y-1 axis; broad and short ray Leiognathus bindus, respectively, and their morpho- connection; not clearly visible ray apophysis; straight logical and morphometric data fit well within the ray slanted more or less distinctively forward and with range of original population of T. rectuncinata (Raabe, equal thickness to round points; ratio of denticle above 1958) [31]. axis to denticle below axis is about one (PlateⅢ- 9, T. rectuncinata showed a wide variation range in 10). denticle morphology. However, it can be easily recog- Division. Several development stages of T. fugu nized by the triangular blade with cavity in the adhe- were observed in silver-impregnated specimens. Dur- sive disc centre although the blade cavity was not ing binary fission, the cell split into two daughter-cells

568 水生生物学报 39 卷 containing half the number of denticles compared with discovered from Takifugu rubripes from Qingdao (the the mature individuals (Plate Ⅲ-11, 12). On the pe- Yellow sea, China) by Xu, et al. (2007) and showed [24] riphery, the new denticles are generated, gradually very high similarity with our population . However, forming the blade, the central part, and the ray. The the denticle dimensions and number of our population specimens also display the adhesive disc with a dark are comparatively smaller than those of the popula- centre and no visible radical pins, and has a body di- tions from Nagasaki and Shizuoka by Imai, et al. ameter approximately half of that of the mature ones (1997). Although Imai, et al. (1997) used forma- (Plate Ⅲ-12) lin-fixed cells for silver impregnation [34], which made Remarks. The present described population of T. the adhesive disc of the species was not well impreg- fugu found from Takifugu vermicularis in Sanya (the nated, the number of the denticles was clear. The den- South China Sea, China) has coincident morphometric ticle number was 24—30 (27) (Sanya) and 23—30 (27) data of that originally from Takifugu rubripes from (Qingdao), smaller than those of 26—33 (29) (Na- Japan described by Imai, et al. [34]. T. fugu was also gasaki) and 29—35 (31) (Shizuoka) (Tab. 2).

Tab. 2 Morphometric comparison (in micrometers) of different populations on Trichodina fugu Imai et al., 1997 Populations of Populations 1 Populations 2 Populations 3 Populations 4 Trichodina fugu Host Takifugu vermicularis Takifugu rubripes Takifugu rubripes Takifugu rubripes Localization gills, body surface, urogenital sinus gills gills gills Location Sanya, China Qingdao, China Nagasaki, Japan Shizuoka, Japan Body diameter 33.0—54.0 (45.6±4.7) 33—44 (38.9±2.9) 36—60 (46) 50—64 (57.3) Adhesive disc 29.0—49.0 (41.3±5.1) 29—39 (34.1±2.8) 28—48 (36.0) 39—54 (47.4) Denticular ring 20.0—34.1 (28.8±3.5) 18—24 (21.3±1.8) 19—31 (24,0) 30—39 (32.6) Border membrane 0.9—2.8 (1.6±0.5) 2—3 (2.5±0.4) 1.0 1—3 (2.0) Denticle number 24—30 (27) 23—30 (27.3±1.7) 26—33 (29.0) 29—35 (31.6) Radial pins per 7—9 6—8 6—7 8 Denticle span 9.5—15.0 (13.1±1.4) 7.5—9.5 (8.4±0.6) — — Denticle length 2.5—6.0 (4.5±0.8) 3—4 (3.5±0.4) 3—4 4—5 (4.3) Blade length 3.5—5.5 (4. 8 ±0.5) 3—4 (3.5±0.4) 3—4 3.5—6 (4.5) Central part width 1.5—3.0 (2.2±0.4) 1.5—2 (1.8±0.2) 1.5—2 2—4 (3.0) Ray length 3.0—6.5 (5.4±0.9) 2.5—3.5(3.0±0.2) 3—4.5 4—5.5 (4.5) Adoral ciliary spiral About 400° 380°— 390° 380° 380° Data resources Present study Xu (2007) Imai, et al. (1997) Imai, et al. (1997)

T. fugu is similar to Trichodina urinaria Dogiel, are responsible for the death of puffer fish. As men- 1940, Trichodina oviduct Poljansky, 1955 and tioned by Xu (2007), T. fugu seems to have rather Trichodina nephritica Lom, 1958, all of which are narrow host range and has only been found from the members of endozoic trichodinids. As noted by Kos- tiger puffer Takifugu rubripes. In Takifugu rubripes tenko and Karaev, the narrow denticle shape and (by Xu), the intensity of T. fugu is lower than other higher denticle number are typical for endocommensal Trichodina species [24]. However, in our study, T. fugu members of the genus, such as T. oviduct and T. is the only parasite and has extremely high intensity nephritica. As expected, we found the species was (more than 20 individual trichodinids could be found parasitic on urogenital sinus. However, endohabitat is per slide) in diseased fish Takifugu vermicularis, not the only choice for the species. Besides, the denti- which proved that Takifugu vermicularis is more vul- cle number is apparently smaller than that of T. ovi- nerable to T. fugu. Furthermore, T. vermicularis was duct and T. nephritica. Last, it is not a commensal heavily infected with T. fugu, leading to the host mor- species but a pathogen for purple puffer. tality in wild environment. Mortality of other fishes In general, the outbreak of trichodinids in aqua- caused by trichodinds have also been observed under culture is due to high host population density, controlled experiments in some study [35, 36], in which eutrophication or poor water quality. We speculate that most of them are ectocommensal on fish while both high host population density and water condition feed on suspended bacteria.

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Parasitic specificity could control the population et al. (1989) and Loubser, et al. (1995) suggested that of a species not being too large. It is well-known that T. rectuncinata requires comprehensive revision [32, 33]. the dynamic of infectious diseases are related to the As is vividly depicted in the chart (Fig. 1, 2), the density of host populations. In Sanya, however, the overall trend shows that the size of trichodinid and the population of Takifugu vermicularis can not be that denticle number increase with the latitude. However, high, because many fisheries are fully or over-exploi- regularity is not clear possibly due to the following ted and the mariculture is not corelated in the region. reasons. On the one hand, the latitude is only one of Thus, the number of both the puffer fish and its prey several factors influencing the body size of trichodinid, are reduced recently. In spite of this, it is still possible as marine environment is very complex and the change that there are other cultured fishes that share the para- of the environment and faunas are not strictly followed sites of T. fugu, but are not as vulnerable as the puffer by the increase of latitude. On the other hand, some fish, Tiger puffer, such as Takifugu rubripes, a breed- populations reported previously are from cultured ing object in some Asia fiery. On the other hand, fishes imported from other places, and the trichodinid unlike other microparasites such as viruses and bacte- can translocate via the introduction of their fish hosts. ria, which do not have free-living stage in their life Last, trichodinid in the present study are more related cycle, the trichodinids can spread more than by host- to the cultured fish or experimental condition. Thus, to-host contact, as previously proved by other authors more research and data are needed to reveal a clearer that the trichodinids only can temporarily leave the trend for supporting our hypothesis. host to find new individual host. Moreover, aquatic micro-parasites may also be transported by water movement[37, 38]. In other parts of the coastal South China Sea, such as Wanning City, which is 120 kilo- meters away from Sanya, the number of farmed ma- rine fish increases rapidly with aquaculture growth. Marine aquaculture facilities are typically open to the surrounding ecosystem and, therefore, wild and farmed populations are connected by their shared parasite. Furthermore, protististic parasites have al- ready caused serious problems in marine aquaculture Fig. 1 The relationship between denticle number and geographi- in Wanning. If this is true, the influence of aquaculture cal distribution (with the increase of latitude) on the marine ecosystems may be more serious. Trichodina japonica: (18.2°N, 18.2) (present study), (21.5°N, 18) (Mitra & Bandyopadhyay, 2005), (33.1°N, 20.7) (Imai, et al., 1991), Because trichodinids are not fed on their hosts, so (36,0°N, 19.2) (Xu, et al., 1999). the flourish of the parasite may not always in accor- Trichodina puytoraci: (18.2°N, 23) (present study), (22.3°N, 22.9) dance with the population density of the hosts. In (Asmat, et al., 2005), (34.6°S, 27) (Marcotegui & Martorelli, 2009), eutrophic water, the high concentration of bacteria and (41.5°N, 26) (Özer, et al., 2004). Trichodina fugu: (18.2°N, 27) (present study), (32.6°N, 29) (Imai, et al. suspended particles in the water flourished the para- 1997), (35.1°N, 31) (Imai, et al., 1997), (36.0°N, 27.3) (Xu, 2007). sites, and the parasites infected hosts. Incidentally, the dead puffer fish (with seriously infected with tricho- dinids) was found in Dadonghai where the on-board- restaurants dumped food scrap directly to the sea in the present research, therefore, the water condition should be taken into consideration. 3 Discussion

Based on the morphometric data and geographi- Fig. 2 The relationship between adhesive disc and geographical cal distribution of each population for T. japonica, T. distribution (with the increase of latitude) puytoraci and T. fugu, we found an interesting phe- Trichodina japonica: (18.2°N, 23.9) (present study), (21.5°N, 22.4) (Mitra & Bandyopadhyay, 2005), (33.1°N, 33.6) (Imai, et al., 1991), nomenon that the body size and denticle number seem (36,0°N, 24.3) (Xu, et al., 1999). to be enlarged with the increase of latitude. The rela- Trichodina puytoraci: (18.2°N,30.1) (present study), (22.3°N, 33.0) tionship between size and latitude is harder to show by (Asmat, et al., 2005), (34.6°S, 57.1) (Marcotegui & Martorelli, the data of T. rectuncinata, as previous studies re- 2009), (41.5°N, 45.0) (Özer, et al., 2004). Trichodina fugu: (18.2°N, 39.3) (present study), (32.6°N, 36.0) vealed considerable variations in morphometric data (Imai, et al., 1997), (35.1°N, 47.4) (Imai, et al., 1997), (36.0°N, and in denticle morphology of the species. Grupcheva, 34.1) (Xu, 2007).

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[23] Xu K D, Song W B, Warren A. Taxonomy of trichodinids Trichodina Ehrenberg, 1830 (Ciliophora: Trichodinidae) from the gills of marine fishes in coastal regions of the from Bangladeshi fishes [J]. Research Journal of Agriculture Yellow Sea, with descriptions of two new species of and Biological Sciences, 2005, 1(1): 23—29 Trichodina Ehrenberg, 1830 (Protozoa: Ciliophora: [31] Raabe Z. On some species of Trichodina (Cialiata–Peritricha) Peritrichia) [J]. Systematic Parasitology, 2002, 51: 107—120 of gills of Adriatic fishes [J]. Acta Parasitologica Polonica, [24] Xu K D. Trichodinid ectoparasites (Ciliophora, Peritrichia) 1958, 6: 355—362 from the tiger puffer Takifugu rubripes in the Yellow Sea, [32] Grupcheva G, Lom J, Dykova I. Trichodinids (Ciliate: with revision of Trichodina jadranica Raabe, 1958 [J]. Acta Urceolaridae) from gills of some marine fishes with the Protozoology, 2007, 46(4): 311—324 description of Trichodina zaikai sp. n [J]. Folia [25] Lom J. A contribution to the systematics and morphology of Parasitologica, 1989, 36(3): 193—207 endoparasitic trichodinids from amphibians, with a proposal [33] Loubser G J. Trichodinid ectoparasites (Ciliophora: of uniform specific characters [J]. Journal of Protozoology, Peritrichida) of some fishes from the Bay of Dakar, Senegal 1958, 5(4): 251—263 (West Africa) [J]. Acta Protozoology, 1995, 34(3): 211—216 [26] Imai S, Miyazaki H, Nomura K. Trichodinid species from [34] Imai S, Inouye K, Kotani T, et al. Two trichodinid species the gills of cultured Japanese eel, Anguilla japonica, with the from the gills of cultured tiger puffer, Takifugu rubripes, in description of a new species based on light and scanning Japan, with the description of new species [J]. Fish electron microscopy [J]. European Journal of Protistology, Pathology, 1997, 32(1): 1—6 1991, 27(1): 79—84 [35] Subasinghe R P. Effects of controlled infections of [27] Mitra A K, Bandyopadhyay P K. First records of Trichodina Trichodina sp. on transmission of epizootic ulcerative japonica Imai, Miyazaki et Nomura 1991 and Trichodina syndrome (EUS) to naive snakehead, Ophicephalus straitus mutabilis Kazubski et Migala 1968 (Ciliophora, [J]. Bloch Journal Fish Disease, 1997, 16(2): 161—164 Trichodinidae) from Indian fishes [J]. Protistology, 2005, [36] Obiekezie A I, Ekanem D A. Experimental infection of 4(2): 121—127 Heterobranchus longifilis with Trichodina maritinkae [28] Özer A, Öztürk T. Trichodina puytoraci Lom, 1962 and (Ciliophora: Peritrichida) [J]. Aquatic Living Resources, Trichodina lepsii Lom, 1962 (Peritrichia: Ciliophora) 1995, 8(4): 439—443 infestations on mugilids caught at the Black Sea coast of [37] Gustafson L L, et al. Hydrographics and the timing of Sinop Turkey [J]. Turkish Journal of Zoology, 2004, 28(2): infectious salmon anemia outbreaks among Atlantic salmon 179—182 (Salmo salar L.) farms in the Quoddy region of Maine, USA [29] Marcotegui P S, Martorelli S R. Trichodinids (Ciliophora: and New Brunswick, Canada [J]. Preventive Veterinary Peritrichida) of Mugil platanus (Mugiliformes: Mugilidae) Medicine, 2007, 78(1): 35—56 and Micropogonias furnieri (Perciformes: Sciaenidae) from [38] Viljugrein H, et al. Integration of hydrodynamics into a Samborombon Bay, Argentina, with the description of a new statistical model on the spread of pancreas disease (PD) in species [J]. Folia Parasitologica, 2009, 56(3): 167—172 salmon farming [J]. Diseases of Aquatic Organisms, 2009, [30] Asmat G S M, Afroz F, Mohammad N. Four new species of 88(1): 35—44

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南中国海野生海水鱼类外寄生车轮虫新记录

王文强 唐发辉 赵元莙 (重庆师范大学动物生物学重点实验室, 重庆 401331)

摘要: 研究对采自南中国海的 7 种海水鱼类进行了调查研究, 并分离获得 4 种隶属于车轮虫属的种类，分别 为浦氏车轮虫 Trichodina puytoraci Lom, 1962; 日本车轮虫 Trichodina japonica Imai, et al., 1991; 直钩车轮虫 Trichodina rectuncinata Raabe, 1958 与车轮虫鲀 Trichodina fugu Imai, et al., 1997。研究发现鲀 车轮虫 Trichodina fugu Imai, et al., 1997 为寄主鱼虫纹东方鲀 Takifugu vermicularis 的病原, 且能在野生条件下将其 致死。上述 4 种车轮虫的形态分类学数据均基于干银法标本获得。研究是对我国南中国海车轮虫的首次报道。

关键词: 车轮虫；新记录；海水鱼；南中国海

Plate Ⅰ Phtomicrographs of silver impregnated adhesive discs of trichodinid species 1. Trichodina japonica Imai, et al., 1991 from Gerres filamentosus (present study). 2. Trichodina puytoraci Lom, 1962 from Mugil oeur (present study). 3. Trichodina puytoraci from Mugil saliens (from Lom, 1962). 4. Trichodina chittagongensis from Labeo bata (from Asmat, et al., 2005) (Scale-bars: 20 μm)

3 期 王文强等: 南中国海野生海水鱼类外寄生车轮虫新记录 573

Plate Ⅱ Phtomicrographs of silver impregnated adhesive discs of different populations of Trichodina rectuncinata Raabe, 1958 5—6. Population from Leiognathus bindus. 7—8. Population from Gerres filamentosus (Scale-bars: 20 μm)

Plate Ⅲ Phtomicrographs of silver impregnated adhesive discs of Trichodina fugu Imai, et al., 1977 9. Group A. 10. Group B. 11. Trichodina fugu in the period of binary fission. 12. Daughter cell of Trichodina fugu (Scale-bars: 20 μm)