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Four first records of trichodinid (Ciliophora: Peritrichia) ectoparasites from cultured molluscs and fishes in China
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Zifeng ZHAN1, 4, Hong ZENG2, Nengfeng LIN3, Kuidong XU1, 4, 5, 6, *
Acta Oceanologica Sinica | 2018, 37(10) : 91 - 97
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Acta Oceanologica Sinica | 2018, 37(10): 91-97
• Articles •
Four first records of trichodinid (Ciliophora: Peritrichia) ectoparasites from cultured molluscs and fishes in China
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Zifeng ZHAN1, 4, Hong ZENG2, Nengfeng LIN3, Kuidong XU1, 4, 5, 6, *
Affiliations
  • 1 Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
  • 2 Fujian Normal University, Fuzhou 350007, China
  • 3 Institute of Biotechnology, Fujian Academy of Agriculture Science, Fuzhou 350003, China
  • 4 Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China
  • 5 Laboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China
  • 6 University of Chinese Academy of Sciences, Beijing 100049, China
Published: 2018-10-25 doi: 10.1007/s13131-018-1305-2
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Four species of Trichodina parasitizing the gills of cultured molluscs and fishes in China are described: Trichodina pectenis Stein, 1974 from the scallop Mizuhopecten yessoensis; Trichodina jadranica Raabe, 1958 from the fishes Mugil cephalus and Anguilla bicolor bicolor; Trichodina acuta Lom, 1961 and Trichodina rostrata Kulemina, 1968 from the fish Acrossocheilus fasciatus. The description of T. pectenis presented here first includes both live characters and morphometric data obtained from specimens impregnated using the wet silver nitrate and protargol methods. The other species were revealed by the dry silver nitrate method. Intensities of infestation and comparisons with related species and populations are provided for each of the four.

taxonomy  /  Trichodina pectenis  /  Trichodina jadranica  /  Trichodina acuta  /  Trichodina rostrata  /  trichodinid ciliates
Zifeng ZHAN, Hong ZENG, Nengfeng LIN, Kuidong XU. Four first records of trichodinid (Ciliophora: Peritrichia) ectoparasites from cultured molluscs and fishes in China[J]. Acta Oceanologica Sinica, 2018 , 37 (10) : 91 -97 . DOI: 10.1007/s13131-018-1305-2
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1 Introduction
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Ciliates assigned to the genus Trichodina Ehrenberg, 1830 are parasites of a range of hosts, including fishes, molluscs, crustaceans, hydroids and amphibians (Raabe, 1959; Lom and Laird, 1969; Lom, 1970; Lom and Dykova, 1992; Xu et al., 1999a, b; Xu and Song, 2003, 2008; Xu, 2007). In recent years, trichodinid diseases of cultured marine fishes and molluscs have often been reported in China along with the development of the aquaculture industry. So far, no chemical or biological agents are really effective against these organisms without damaging their host animals. Thus, prompt identification and early treatment of trichodinids is crucial for the control of animal diseases. On the other hand, the diversity and distribution of trichodinids as well as the host-parasite relationship are still far from known. Compared to freshwater forms, marine trichodinids are still a poorly studied group (Lom and Dykova, 1992; Xu and Song, 2003).
During surveys of the parasites from culture molluscs and fishes on the coasts of the Yellow Sea and the East China Sea, four species of Trichodina were identified, and are described herein. This paper is one of a series of reports on the trichodinids of marine animals from the coastal areas off China, which aims to extend our knowledge of the diversity and distribution of these parasitic ciliates.
2 Materials and methods
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Specimens of the host mollusc Mizuhopecten yessoensis were collected from the cultured cages on the coast of Dalian, China in November 2008. All the scallop specimens were maintained in laboratory for examination. The gills were removed and washed with sterilized seawater in a Petri dish. The ciliates were isolated with a micropipette and observed by light microscopy. With the exceptions of ciliate body shape, the ratio of body width to height and contractile vacuole position, the descriptions of the trichodinids from the scallops are based on examinations of specimens impregnated with the wet silver nitrate and protargol impregnation methods, as described in Foissner (1991).
Specimens of the host fishes Anguilla bicolor bicolor and Mugil cephalus were collected from the net cages in the estuary area of Fuzhou, China in May 2010. The water salinity was about 20.0 and the water temperature was about 18°C during sampling. Specimens of the host fish Acrossocheilus fasciatus were collected from a cultured pond with the water salinity of about 4.0 in Shanghai, China in May 2014. Acrossocheilus fasciatus, which has been tamed to adapt to the brackish environment, is formerly a freshwater fish. Wet smears of the skin and gills were prepared in the field using a dissecting microscope in order to detect the presence of trichodinids. The smeared slides were taken back to the laboratory for the dry silver nitrate method as described in Foissner (1991). For each host individual examined, the intensity of infestation was estimated qualitatively by assigning values ranging from + (light intensity of infestation) to +++ (heavy intensity of infestation) on one gill. Information concerning hosts collected and trichodinid infestations is provided in Table 1.
All measurements are in micrometres and follow the uniform specific characteristics proposed by Lom (1958). In each case, minimum and maximum values are given, followed in parentheses by the arithmetic mean and standard deviation. In the case of radial pins, the mode is given rather than the arithmetic mean. The span of the denticle was measured from the tip of the blade to the tip of the ray. The body diameter was measured as the adhesive disc plus the border membrane. The description of denticle elements follows the format recommended by Van As and Basson (1989).
The position of the micronucleus is given relative to the arch-shaped macronucleus, according to the format described by Lom (1958). In this system, the micronucleus is situated in one of three positions relative to the terminations of the arms of the macronucleus: (1) externally, near the right termination (+y); (2) externally, between the two terminations (–y); and (3) internally, near the right termination (–y1).
3 Results
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3.1 Trichodina pectenis Stein, 1974 (Fig. 1, Table 2)
Host and sites: Mizuhopecten yessoensis, gills.
Locality: Coast area off Dalian, China.
Voucher specimens: Four slides (ZZF-20081123-01, -02, -03, -04) with protargol and wet sliver nitrate impregnated specimens have been deposited in the Marine Biological Museum of the Chinese Academy of Sciences (MBMCAS) at Qingdao, China.
Description: Small-sized marine Trichodina. Body diameter ca. 35–45 μm in vivo, 31–42 μm in sliver–impregnated specimens. Body in vivo helmet–like, with body diameter/height ratio (1.2–1.6):1. Macronucleus horseshoe–shaped, with external diameter 28–30 μm. Micronucleus ellipsoidal, situated in +y position. Single contractile vacuole near to oral cavity. Adoral ciliary spiral 380°–400°. Haplokinety consisting of two rows of kinetosomes, polykinety with three rows. Denticles small but fill most of adhesive disc, with denticle span 9–11 μm and length 4–6 μm (Figs 1e–g). Blade acute triangular in shape, sharply pointed in almost all specimens investigated. Distal blade surface slopes downward to apex, from which anterior blade surface cannot be clearly distinguished. Tangent point located at peak of distal blade. Posterior blade surface straight to slightly curved. Apophysis of blade indistinct, while posterior projection absent. Central part of ordinary appearance, with round point fitting tightly into preceding denticle. Ray delicate and straight, tapers to sharp point. Ray apophysis distinct. Length of ray/blade ratio ca. 1.1:1. Central zone clear, with usually one, occasionally 2–5 globular granules recognizable both in vivo and in silver-impregnated specimens (Figs 1d–g).
3.2 Trichodina jadranica Raabe, 1958 (Fig. 2, Table 3)
Hosts and sites: Mugil cephalus and Anguilla bicolor bicolor, gills and skin.
Locality: Coast off Fuzhou, China.
Voucher specimens: Four slides (ZZF-20100528-01,-02, ZZF-20100531-01, -02) with dry sliver impregnated specimens have been deposited in the MBMCAS at Qingdao, China.
Description: The specimens from the skin and gills of Mugil cephalus and Anguilla bicolor bicolor match well in morphometry and denticle morphology. Morphometric data for the two populations from the two hosts are presented in Table 3. The description given below is based on all well impregnated specimens obtained from both the gills and skin. Medium-sized marine Trichodina with an average of cell diameter 46 μm from Mugil cephalus and 55 μm from Anguilla bicolor bicolor. Blade broad, sickle–shaped, filling most of space between y–axes, in certain specimens even extending beyond y–axes (Figs 2d, f). Distal blade surfaces difficult to separate from anterior blade surfaces, which distinctly slope downwards in most impregnated specimens. Posterior blade surfaces curved, the deepest point on same level as apex. Tangent point located at peak of distal blade, sharply pointed in almost all specimens investigated. Apophysis of blade distinct in most specimens examined, while prominent posterior projection at base of blade recognizable only in well impregnated specimens (Figs 2a, b and f). Central part robust, fitting tightly into preceding denticle and extending more than half way to near y–axis. Ray short, straight to slightly curved, with rounded to bluntly pointed end; length of ray to length of blade about 1:1.3. Ray apophysis distinct. Centre of adhesive disc contains a clear circle, which is 9–20 μm in diameter and studded with several dark granules 0.5–1.0 μm across.
3.3 Trichodina acuta Lom, 1961 (Figs 3a–c, Table 4)
Host and sites: Acrossocheilus fasciatus, gills and skin.
Locality: Fish culture pond in Shanghai, China.
Voucher specimens: Four slides (ZZF-20140506-01, -02, -03, -04) with dry sliver impregnated specimens have been deposited in the MBMCAS at Qingdao, China.
Description: The specimens from the gills and skin of the fish Acrossocheilus fasciatus match well in morphometry and denticle morphology. Thus, the description is based on all well impregnated specimens obtained from both the gills and skin. Medium-sized Trichodina with an average of cell diameter 61 μm (Table 4). Blade broad, sickle-shaped, filling most of space between y–axes, with sharp tangent point. Distal blade surface may be round, parallel to border membrane or sloping downwards to sharp apex, from which anterior blade surface cannot be clearly distinguished. Anterior blade surface, extending beyond y–axes (Figs 3a–c). Posterior blade surface curved, the deepest point on same level as apex. Apophysis and posterior projection of blade distinct in most specimens examined. Central part robust, fitting tightly into preceding denticle and extending more than half way to y–axis. Ray relatively long, straight or slightly curved, tapers to sharp point. Ray apophysis present. Length of ray/blade ratio ca. 1.2:1. Central zone clear, with one bright granule.
3.4 Trichodina rostrata Kulemina, 1968 (Figs 3d–f, Table 5)
Host and sites: Acrossocheilus fasciatus, gills and skin.
Locality: Culture pond of Shanghai, China.
Voucher specimens: Four slides (ZZF-20140506-01, -02, -03, -04) with dry sliver impregnated specimens have been deposited in the MBMCAS at Qingdao, China.
Description: The specimens from the gills and skin of Acrossocheilus fasciatus match well in morphometry and denticle shape. Thus, the description is based on all well impregnated specimens obtained from both the gills and skin. Medium-sized Trichodina with an average of cell diameter 50 μm (Table 5). Blade broad, beak-shaped, filling most of space between y–axes, with round to sharp tangent point. Distal blade surface may be round, parallel to border membrane or sloping downwards to sharp apex, from which anterior blade surface cannot be clearly distinguished. Anterior blade surface, extending beyond y–axes in most impregnated specimens (Figs 3d–f). Posterior blade surface curved, the deepest point on same level as apex. Apophysis of blade indistinct, while posterior projection absent. Central part robust, fitting tightly into preceding denticle and extending more than half way to y–axis. Ray straight, tapers to sharp point (on occasions, it slants forwards slightly; Figs 3d, e). Ray apophysis present. Length of ray/blade ratio ca. 1:1. Central zone clear, without bright granules.
4 Discussion
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This is the first record of Trichodina pectenis reported and described since the original description by Stein (1974) from the scallop Mizuhopecten yessoensis and the sea urchin Echinorachnius parma in Russia. The original description was based only on impregnated specimens. Some important morphological data, such as the body diameter and height, nucleus shape and position, adoral ciliary spiral value and contractile vacuole position were not provided. Our specimens which were isolated from the same host M. yessoensis correspond well with those described by Stein (1974) in the adhesive disc size, central granule number, and denticle shape and dimensions (Table 2). Thus, conspecificity is beyond reasonable doubt. We redescribed T. pectenis in detail based on both live and silver impregnated cells and supplemented the morphological data, which are lacking in the original description. Trichodina pectenis resembles, to some extent, T. chlamydis Xu, Song and Warren, 1999, a parasite of the marine scallop Chlamys farreri. However, the shape of the blades is distinctly different (triangular in T. pectenis vs. rectangular in T. chlamydis) (Figs 1g, 2a and b; Xu et al., 1999b). It is similar to T. caecellae Xu, Song and Warren, 2003 in the denticle shape and dimensions, but differs distinctly in the structure of the central zone (with 1–5 globular granules vs. absent).
Trichodina jadranica is a trichodinid parasite widely distributed on the gills and/or skin of various host fishes worldwide since Raabe (1958) established it based on specimens from the host fish Mullus barbatus. So far, most populations of T. jadranica were reported from marine fishes and only two from freshwater fishes (Arthur and Lom, 1984; Imai et al., 1991, 1997; Loubser et al., 1995; Xu et al., 2001; Xu, 2007). The morphological identification of T. jadranica is often difficult due to the population variability and the presence of misidentification. Xu (2007) made a thorough revision on T. jadranica and showed that the species is highly variable in body size, denticle dimensions, and the number of denticles. The present trichodinid specimens match well in the morphometry and denticle shape with the other Chinese and Japanese populations, though they are slightly larger than the type specimens reported by Raabe (1958) (Table 3). These are also the first host records for T. jadranica parasitizing Mugil cephalus and Anguilla bicolor bicolor. Both the host fish Mugil cephalus and Anguilla bicolor bicolor were collected from an estuary of Fuzhou, where the perennial salinity was 15–22. This is an intermediate environment among marine and fresh waters. Our study further supports the view of Xu (2007), who indicated that T. jadranica has the ability to live in marine, brackish and fresh environments.
Trichodina acuta and T. rostrata are typically freshwater fish parasites distributed worldwide. These trichodinids are easy to distinguish by their denticle shape and dimensions (Lom, 1961; Kulemina, 1968; Tao and Zhao, 2006; Liu and Zhao, 2010). Our specimens were detected from the freshwater fish Acrossocheilus fasciatus, a species has been tamed to adapt to brackish environment with the water salinity about 4. Thus, the fish A. fasciatus from the brackish water represents new host and locality records for these two trichodininids. It is reasonable to assume that the two trichodinids adapted the saline environment with their hosts because both trichodinids have never been detected from marine host animals.
To date, more than 260 Trichodina species have been reported, but at least one-third of trichodinids are still needed to be confirmed or redescribed using modern methods (Xu et al., 2001; Gong et al., 2005). The comparative analysis of the morphometry and denticle shape is the routine way to identify Trichodina species. Many Trichodina spp. show morphological similarity to closely related species, and some similar species even concomitantly occurred in the same host. Under such circumstances, morphological identification has its limitation. There is a pressing need for molecular methods, for example the DNA barcoding, to assist in the identification as well as the phylogenetic analysis of trichodinids (Zhan et al., 2009, 2013).
Funding
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  • The National Natural Science Foundation of China under contract Nos 41406171 and 41476144.
References
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doi: 10.1007/s13131-018-1305-2
  • Receive Date：2017-08-14
  • Online Date：2026-04-14
  • Published：2018-10-25
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  • Received：2017-08-14
  • Accepted：2018-02-28
Funding
The National Natural Science Foundation of China under contract Nos 41406171 and 41476144.
Affiliations
    1 Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
    2 Fujian Normal University, Fuzhou 350007, China
    3 Institute of Biotechnology, Fujian Academy of Agriculture Science, Fuzhou 350003, China
    4 Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China
    5 Laboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China
    6 University of Chinese Academy of Sciences, Beijing 100049, China

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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