First record of Trichodina heterodentata (Ciliophora: Trichodinidae) from channel catfish, Ictalurus punctatus cultivated in Brazil

Primeiro registro de Trichodina heterodentata (Ciliophora: Trichodinidae) em bagre-do-canal, Ictalurus punctatus cultivado no Brasil

BIOLOGY

First record ofTrichodina heterodentata(Ciliophora: Trichodinidae) from channel catfish, Ictalurus punctatus cultivated in Brazil

Primeiro registro de Trichodina heterodentata (Ciliophora: Trichodinidae) em bagre-do-canal, Ictalurus punctatus cultivado no Brasil

Martins, ML.^*; Marchiori N.; Nunes G.; Rodrigues MP.

Laboratório de Sanidade de Organismos Aquáticos - AQUOS, Departamento de Aquicultura, Universidade Federal de Santa Catarina - UFSC, Rod. Admar Gonzaga, 1346, CEP 88040-900, Florianópolis, SC, Brazil

ABSTRACT

This study characterises morphologically Trichodina heterodentata Duncan, 1977 from channel catfish, Ictalurus punctatus (Rafinesque, 1818) in the State of Santa Catarina, Brazil. Body and gill smears were air-dried at room temperature, impregnated with silver nitrate and/or stained with Giemsa. Ten characteristics were selected to compare the present material with other morphological characterisations of T. heterodentata. Prevalence rate was 100%, mean intensity 89,333.70 (3,125 to 299,100 parasites per host). Trichodina heterodentata was considered medium-sized trichodinid with mean body diameter 59.4 ± 8.5 μm, denticulate ring 38.5 ± 4.5 μm, adhesive disc 60.2 ± 6.7 μm diameter and 24.4 ± 1.6 denticles. In relation to previous reports of T. heterodentata this material resembles in 90% of the analysed characters. This work confirms the biometrical variation that exists in the different populations of T. heterodentata. A list of hosts and comparative measurements of T. heterodentata are presented and the channel catfish is considered a new host.

Keywords: channel catfish, trichodinid, Trichodina heterodentata, morphology.

RESUMO

Este estudo caracteriza morfologicamente Trichodina heterodentata Duncan, 1977 em bagre-do-canal, Ictalurus punctatus (Rafinesque, 1818) no Estado de Santa Catarina, Brasil. Esfregaços do corpo e brânquias foram secados à temperatura ambiente, impregnados com nitrato de Prata e/ou corados com Giemsa. Dez características foram selecionadas para comparar o presente material com as diferentes caracterizações morfológicas de T. heterodentata. A taxa de prevalência foi de 100%, a intensidade média foi de 89.333.75 (3.125 a 299.100 parasitos por hospedeiro). Trichodina heterodentata foi considerado um tricodinídeo de tamanho médio com a média do diâmetro do corpo de 59,4 ± 8.5 μm, anel denticulado 38,5 ± 4,5 μm, disco adesivo 60,2 ± 6,7 μm de diâmetro e 24,4 ± 1,6 dentículos. Em relação a registros prévios de T. heterodentata, 90% das características foram semelhantes. Este trabalho confirma a variação biométrica que existe em diferentes populações de T. heterodentata. Uma lista de hospedeiros e medidas comparativas de T. heterodentata são apresentadas e o bagre-do-canal considerado um novo hospedeiro.

Palavras-chave: bagre do canal, tricodinídeo, Trichodina heterodentata, morfologia.

1. Introduction

Trichodinids are among one of the most common ectoparasites in wild and cultivated fish (Basson and Van As, 1994, Martins and Ghiraldelli, 2008). This parasite occurs normally in a few numbers on mucous surface and gills. When the relationship host/parasite/environment is broken by nutritional deficiency, poor water quality, infectious and/or parasitic diseases trichodinids may proliferate being responsible for severe epidermal lesions and disease outbreaks, as reported by Madsen et al. (2000), Martins et al. (2002), Khan (2004) and Huh et al. (2005).

In pond-reared fishes, they have been found on channel catfish, Ictalurus punctatus (Rafinesque, 1818) (see Wellborn, 1967), Clarias gariepinus (Burchell, 1822) (see Basson and Van As, 1991) and Heterobranchus longifilis Valenciennes, 1840 (see Ekanen and Obiekezie, 1996); on perch, Perca fluviatilis (Linnaeus, 1758) and roach, Rutilus rutilus (Linnaeus, 1758) (see Halmetoja et al., 1992); in carp, Hypophtalmichthys molitrix (Valenciennes, 1844) (see Nikolic and Simonovic, 1998); in eel, Anguilla anguilla (Linnaeus, 1758) (see Madsen et al., 2000), and in marine cultivated fishes in Korea (Xu et al., 2001).

In Brazil, fish trichodinids were reported in cultivated Nile tilapia, Oreochromis niloticus (Linnaeus, 1758) (Vargas et al., 2000, Tavares-Dias et al., 2001, Ranzani-Paiva et al., 2005, Ghiraldelli et al., 2006 a, b, Martins and Ghiraldelli, 2008); in pacu Piaractus mesopotamicus (Holmberg, 1887), piauçu Leporinus macrocephalus Garavello and Britski, 1988, carp Cyprinus carpio (Linnaeus, 1758); and in mullet, Mugil platanus Günther, 1880 (Ranzani-Paiva and Silva-Souza, 2004).

However, in only a few reports are the trichodinids involved identified to species level. This includes Trichodina steini Claparede and Lachmann, 1858 from Bufo ictericus Spix, 1824 (Kattar, 1975), Trichodina acuta Lom, 1961 from Xiphophorus maculatus, Gunther, 1866, X. helleri, Heckel, 1848, Betta splendens Regan, 1910 and Carassius auratus Linnaeus, 1758 (Piazza et al., 2006), Trichodina compacta Van As and Basson, 1989 reported by Ghiraldelli et al. (2006a) and Trichodina magna Van As and Basson, 1989 by Martins and Ghiraldelli (2008) in Nile tilapia O. niloticus, Trichodina machadoi registered in gastropod Biomphalaria schrammi (Crosse, 1864) by Pinto et al. (2006) and Trichodina heterodentata found on the body and tail of the tadpole Rhinella pombali Baldissera, Caramaschi and Haddad, 2004 (Dias et al., 2009)

This study characterises morphologically Trichodina heterodentata Duncan, 1977 in pond-reared channel catfish in the State of Santa Catarina, Southern Brazil. Prevalence, mean intensity of infestation and a list of hosts and comparative measurements were also reported.

2. Material and Methods

Four specimens of channel catfish of 29.5 ± 2.3 cm total length were collected in July 2007 in a farm situated in the municipality of Porto União (26° 14' 17'' S and 51° 04' 42'' W), Santa Catarina, Brazil. Fish were maintained at 1.4 fish.m^-2 stocking density in ponds of 3,500 m² with constant flow of water. In the day of sampling the pH was 5.4 to 6.9; alkalinity 24 to 44 mg.L^-1; total ammonia 0.5 to 3.0 mg.L^-1; dissolved oxygen 6.2 to 10.8 mg.L^-1. Water temperature three days before fish sampling was 13.3 to 15.2 °C and on the day of parasitological examination, it was 9.2 to 10.8 °C.

Wet smears of skin and gills were prepared in the field and examined under the microscope. When parasites were present the smears were air-dried and impregnated with Klein's dry silver method for observation of the adhesive disc as suggested by Lom (1958). Other smears were stained with Giemsa's solution to reveal the nuclear apparatus. The span of the denticle was measured from the tip of blade to the tip of ray as described by Arthur and Lom (1984). The body diameter is the dimension of the adhesive disc plus the border membrane. Wet mounts from the specimens preserved in 5% formalin solution were studied for the observation of adoral ciliature. All measurements are in micrometres and follow the recommendations of Lom (1958) and Van As and Basson (1989). Arithmetic means ± standard deviation is followed, in parentheses, by the minimum and maximum values and number of specimens or structures measured. To compare biometrically our specimens of T. heterodentata with others from previous records, 10 characteristics were selected as the most important in a primary observation before morphological comparison, which are: body size, adhesive disc, denticle ring, number of denticles, denticle length, blade length, ray length, central part width and span.

3. Results

All fish examined were parasitised (100% prevalence) with mean intensity of 89,333.75 ± 141,583.80 varying from 3,125; 4,416; 50,694 and 299,100 parasites per host.

Characterised as a medium-sized trichodinid with disc-shaped body; convex adoral surface with ciliature of 307.0° ± 12.6 (292-325, 11); aboral side with slightly concave adhesive disc; centre of adhesive disc did not show granules in silver-impregnated specimens. From the Giemsa-stained specimens the macronucleus also presents a horseshoe-shaped 43.2 ± 4.7 (32-49, 26) of external diameter and 11.0 ± 2.2 (7-17, 26) thickness. The distance between the terminations of macronucleous is 17.6 ± 8.4 (11-27, 26); micronucleus was not observed. The denticles are characterised by wide blade and sickle-shaped provided by apophysis on blade connection with the central part (Figure 1a). The blade fills the space between y and y - 1 axes. Central part robust ending rounded fitting on the next denticle filling the space between y and y - 1 axes. Ray long, robust, slightly directed anteriorly situated between the axes y and y + 1, tapering rounded provided by a relatively short apophysis (Figure 1b). Several specimens studied showed inconstant shape and length of ray.

4. Remarks

Trichodinids reproduces by binary fission and it has been the subject of study since the previous century (Kruger et al., 1995). Figure 2 shows one of the last steps of T. heterodentata's reproduction, showing blades in the process of development whilst the old ring is being resorbed. According to Kruger et al. (1995), the original denticle ring maintains its position but loses its shape. The altering of the original shape of the denticle ring is the result of the resorption process that appears to erode the denticles from the aboral side.

Comparing the measurements of the specimens herein described, 50% out of 10 characters were similar to T. magna, Trichodina claviformis Dobberstein and Palm, 2000, Trichodina mutabilis Kazubski, 1968 and Trichodina subtilihamata Tang, Zhao and Tao, 2007; 60% similar to Trichodina cancilae Asmat, 2001 and 70% similar to Trichodina wulai Basson and Van As, 1994 and Trichodina gulshae Asmat, Kibria and Naher, 2003. Nevertheless, 90% of characters were similar to T. heterodentata.

Trichodina heterodentata was originally described in three different populations from reared Tilapia zilli (Gervais, 1848), Oreochromis mossambicus (Peters, 1852) and Trichogaster trichopterus (Pallas, 1770) from the Phillipines (Duncan, 1977). Later, it was also recorded from a large number of fish species, including several Families (Table 1-4). In siluriform fish, T. siluri Lom, 1970 was reported by Bondad-Reantaso and Arthur (1989) but almost all measurements except for blade length were different.

The present specimens showed similar measurements of adhesive disc, denticulate ring and the dimensions of denticles when compared to population B and C of Duncan (1977) and those studied by Van As and Basson (1989). A lower number of denticles was reported in specimens described by Van As and Basson (1989, 1992), but a higher number was noted in two populations originally described by Duncan (1977) (Table 1). In fact, comparing the present material from channel catfish with T. heterodentata, a great number of characters measured coincided. Another point that must be commented is the position of ray and blade in relation to y axes. As demonstrated by illustrations of Van As and Basson (1989, 1992) the blade fills the space between y and y - 1 axes. The central part is robust filling the space between y and y - 1 axes. Finally, the length of ray is longer than the length of blade slightly directed anteriorly situated between the axes y and y + 1.

This species resembles the size of Trichodina vallata Wellborn, 1967 described from channel catfish (Wellborn, 1967). On the other hand, the adhesive disc and the denticulate ring diameters, as well as the number of denticles were lower than that observed in this work. In relation to Trichodina discoidea also described by Wellborn (1967) in channel catfish the number of denticles and the length of blade and ray were similar, but significant lower diameters of body, adhesive disc and denticulate ring were found. Despite the fact that it occurs in wild and cultured channel catfish, the shape of the denticle of T. discoidea and T. vallata was significantly different when compared to T. heterodentata herein characterised.

Due to the fact that the denticles may present some variability, as supported by Van As and Basson (1989) and Basson and Van As (1994), the specimens herein studied correspond to another report of T. heterodentata in Brazil and channel catfish is reported as a new host. As to confirming the variation that exists in T. heterodentata populations, the present material showed slightly higher measurements of the adhesive disc, denticulate ring, central part width and span than those found in T. heterodentata reported by Al-Rasheid et al. (2000) and Asmat (2004), and higher denticulate ring diameter when compared to Dove and O'Donoghue (2005) reports. The characterisation of T. heterodentata from tadpoles (Dias et al., 2009) showed lower measurements of denticulate ring and denticle length.

In relation to host specificity, the capacity of trichodinids to occur or not in a special host might be discussed and contested. For example, T. heterodentata was found in different fish families as showed in Table 5. On the other hand, Trichodina sylhetensis Asmat, Hafizuddin and Habib, 2003, Trichodina aplocheilusi Asmat, Afroz and Mohammad, 2005 and Trichodina chittagongensis Asmat, Afroz and Mohammad, 2005 were found respectively in Nandus nandus Hamilton, 1822, Aplocheilus panchax Hamilton, 1822 and Labeo bata by Hamilton, 1822 Asmat et al. (2003) and Asmat et al. (2005). In this way, the low host specificity of trichodinids can be contested according to published data. We can assume that existing variability in trichodinid host-specificity according to the environment quality in a fish farm and fish species.

5. Taxonomic Summary

• Type hosts: Oreochromis mossambicus, Tilapia zilli, Trichogaster trichopterus

• Type locality: Phillipines

• New host: channel catfish, Ictalurus punctatus

• New locality: Porto União (26° 14' 17'' S and 51° 04' 42'' W), Santa Catarina, Brazil

• Site of infection: skin and gills

• Synonyms: Trichodina equatorales Kazubski, 1986 (see Bondad-Reantaso and Arthur, 1989)

Acknowledgements - The authors thank the National Council of Scientific and Technological Development (CNPq-301072/2007-8), Macroprograma I/EMBRAPA/Technological Bases for Sustainable Aquaculture Development-AQUABRASIL and SEAP (Secretaria Especial de Aquicultura e Pesca) for financial support.

Received May 27, 2009

Accepted August 6, 2009

Distributed August 31, 2010

• ALBALADEJO, JD. and ARTHUR, JR., 1989. Some trichodinids (Protozoa: Ciliophora: Peritrichida) from freshwater fishes imported into the Philippines. Asian Fisheries Science, vol. 3, p. 1-25.
• AL-RASHEID, KAS., ALI, MA., SAAKRAN, T., BAKI, AAA. and GHAFFAR, FAA., 2000. Trichodinid ectoparasites (Ciliophora: Peritrichida) of some River Nile fish, Egypt. Parasitology International, vol. 49, no. 2, p. 131-137.
• ARTHUR, JR. and LOM, J., 1984. Trichodinid protozoa (Ciliophora: Peritrichida) from freshwater fishes of Rybinsk Reservoir, USSR. Journal of Protozoology, vol. 31, no. 1, p. 82-91.
• ARTHUR, JR. and QUANG TE, B., 2006. Checklist of the parasites of fishes of Viet Nam Rome: FAO. p. 14. (Fisheries Technical Paper no. 369, part 2)
• ASMAT, GSM., HAFIZUDDIN, AKM. and HABIB, MMA., 2003. Trichodina sylhetensis sp. n. (Ciliophora: Trichodinidae) from the Mud Perch, Nandus nandus (Hamilton-Buchanan, 18822) (Nandidae) in Sylhet. Pakistan Journal of Biological Sciences, vol. 6, no. 20, p. 1774-1777.
• ASMAT, GSM., 2004. First record of Trichodina diaptomi (Dogiel, 1940) Basson and Van As, 1991, T. heterodentata Duncan, 1977 and T. oligocotti (Lom, 1970) (Ciliophora: Trichodinidae) from Indian fishes. Pakistan Journal of Biological Sciences, vol. 7, no. 12, p. 2066-2071.
• ASMAT, GSM., AFROZ, F. and MOHAMMAD, N., 2005. Four news species of Trichodina Ehrenberg, 1830 (Ciliophora: Trichodinidae) from Bangladesh fishes. Research Journal of Agriculture and Biological Sciences, vol. 1, no. 1, p. 23-29.
• BASSON, L. and VAN AS, JG., 1991. Trichodinids (Ciliophora: Peritrichia) from a calanoid copepod and catfish from South Africa with notes on host specificity. Systematic Parasitology, vol. 18, no. 2, p. 147-158.
• BASSON, L. and VAN AS, JG., 1994. Trichodinid ectoparasites (Ciliophora: Peritrichida) of wild and cultured freshwater fishes in Taiwan, with notes on their origin. Systematic Parasitology, vol. 28, no. 3, p. 197-222.
• BASSON, L., VAN AS, JG. and PAPERNA, I., 1983. Trichodinid ectoparasites of cichlid and cyprinid fishes in South Africa and Israel. Systematic Parasitology, vol. 5, no. 4, p. 245-257.
• BONDAD-REANTASO, MG. and ARTHUR, JR., 1989. Trichodinids (Protozoa: Ciliophora: Peritrichida) of Nile Tilapia (Oreochromis niloticus) in the Philippines. Asian Fisheries Sciences, vol. 3, no. 1, p. 27-44.
• DIAS, RJP., FERNANDES, NM., SARTINI, B., SILVA NETO, ID. and D'AGOSTO, M., 2009. Occurrence of Trichodina heterodentata (Ciliophora: Trichodinidae) infesting tadpoles of Rhinella pombali (Anura: Bufonidae) in the Neotropical area. Parasitology International, vol. 58, no. 4, p. 471-474.
• DOVE, ADM. and O'DONOGHUE, J., 2005. Trichodinids (Ciliophora: Trichodinidae) from native and exotic australian freshwater fishes. Acta Protozoologica, vol. 44, no. 1, p. 51-60.
• DUNCAN, BL., 1977. Urceolariid ciliates, including three new species, from cultured Phillipine fishes. Transactions of American Microscopical Society, vol. 96, no. 1, p. 76-81.
• EKANEN, DA. and OBIEKEZIE, AI., 1996. Growth reduction in African catfish fry infected with Trichodina maritinkae Basson and Van As, 1991 (Ciliophora: Peritrichida). Journal of Aquaculture in the Tropics, vol. 11, p. 91-96.
• GHIRALDELLI, L., MARTINS, ML., ADAMANTE, WB. and YAMASHITA, MM., 2006a. First record of Trichodina compacta Van As and Basson, 1989 (Protozoa: Ciliophora) from cultured Nile tilapia in the State of Santa Catarina, Brazil. International Journal of Zoological Research, vol. 2, no. 4, p. 369-375.
• GHIRALDELLI, L., MARTINS, ML., JERÔNIMO, GT., YAMASHITA, MM. and ADAMANTE, WB., 2006b. Ectoparasites communities from Oreochromis niloticus cultivated in the State of Santa Catarina, Brazil. Journal of Fisheries and Aquatic Sciences, vol. 1, no. 2, p. 181-190.
• HALMETOJA, A., VALTONEN, ET. and TASKINEN, J., 1992. Trichodinids (Protozoa) on fish from central finnish lakes of differing water quality. Aqua Fenica, vol. 22, no. 1, p. 59-70.
• HUH, MD., THOMAS, CD., UDOMKUSONSRI, P. and NOGA, EJ., 2005. Epidemic trichodinosis associated with sever epidermal hyperplasia in largemouth bass, Micropterus salmoides from North Carolina, USA. Journal of Wildlife Diseases, vol. 41, no. 3, p. 647-653.
• KATTAR, MR., 1975. Sobre Trichodina steini Claparéde and Lachmann (Protozoa, Urceolariidae) encontrada em girino de Bufo Ictericus do Brasil. Brazilian Journal of Biology, vol. 35, no. 2, p. 253-258.
• KHAN, RA., 2004. Disease outbreaks and mass mortality in cultured Atlantic cod, Gadus morrhua L., associated with Trichodina murmanica (Ciliophora). Journal of Fish Diseases, vol. 27, no. 3, p. 181-184.
• KRUGER, J., VAN AS, JG. and BASSON, L., 1995. Observations on the Adhesive disc of Trichodina xenopodos Fantham, 1924 and T. heterodentata Duncan, 1977 (Ciliophora: Peritrichida) during binary fission. Acta Protozooogica, vol. 34, no. 3, p. 203-209.
• LOM, J., 1958. A contribution to the systematics and morphology of endoparasitic trichodinids from amphibians, with a proposal of uniform specific characteristics. Journal of Protozoology, vol. 5, no. 4, p. 251-263.
• MADSEN, HCK., BUCHMANN, K. and MELLERGAARD, S., 2000. Trichodina sp. (Ciliophora: Peritrichida) in eel Anguilla anguilla in recirculation systems in Denmark: host-parasite relations. Disease of Aquatic Organisms vol. 42, no. 2, p. 149-152.
• MARTINS, ML. and GHIRALDELLI, L., 2008. Trichodina magna Van As and Basson, 1989 (Ciliophora: Peritrichia) from cultured Nile tilapia in the State of Santa Catarina, Brazil. Brazilian Journal of Biology, vol. 68, no. 1, p. 169-172.
• MARTINS, ML., ONAKA, EM., MORAES, FR., BOZZO, FR., PAIVA, AMFC. and GONÇALVES, A., 2002. Recent studies on parasitic infections of freshwater cultivated fish in the State of São Paulo, Brazil. Acta Scientiarum Biological Sciences, vol. 24, no. 4, p. 981-985.
• MITRA, AK. and HALDAR, DP., 2005. Descriptions of two new species of the genus Trichodina Ehrenberg, 1838 (Protozoa: Ciliophora: Peritrichida) from Indian fresh water fishes. Acta Protozoologica, vol. 44, n. 2, p. 159-165.
• NIKOLIC, VP. and SIMONOVIC, PD., 1998. Seasonal dynamics of carp infestation by Trichodina nobilis Chen. 1963 (Peritrichida, Ciliata) in two fish-ponds in Banat. Tiscia, vol. 31, p. 59-61.
• PIAZZA, RS., MARTINS, ML., GUIRALDELLI, L. and YAMASHITA, M., 2006. Parasitic diseases of freshwater ornamental fishes commercialized in Florianópolis, Santa Catarina, Brazil. Boletim do Instituto de Pesca, vol. 32, no. 1, p. 51-57.
• PINTO, HA., WIELOCH, AH. and MELO, AL., 2006. Uma nova espécie de Trichodina Ehrenberg, 1838 (Ciliophora: Trichodinidae) em Biomphalaria schrammi (Crosse, 1864) (Mollusca: Planorbidae). Lundiana, vol. 7, no. 2, p. 121-124.
• RANZANI-PAIVA, MJT. and SILVA SOUZA, AT., 2004. Co-infestation of gills by different parasite groups in the mullet, Mugil platanus Günther, 1880 (Osteichthyes, Mugilidae): effects on relative condition factor. Brazilian Journal of Biology, vol. 64, no. 3b, p. 677-682.
• RANZANI-PAIVA, MJT., FELIZARDO, NN. and LUQUE, JL., 2005. Parasitological and hematological analysis on Nile tilapia Oreochromis niloticus Linnaeus, 1757 from Guarapiranga reservoir, São Paulo State, Brazil. Acta Scientiarum Biological Sciences, vol. 27, no. 3, p. 231-237.
• TAVARES-DIAS, M., MARTINS, ML. and MORAES, FR., 2001. Fauna parasitária de peixes oriundos de "pesque-pague" do município de Franca, São Paulo, Brasil. I Protozoários. Revista Brasileira de Zoologia, vol. 18, no. 1, p. 67-79.
• VAN AS, JG. and BASSON, L., 1986. Trichodinids (Ciliophora: Peritricha) ectoparasites of cultured cichlids from Taiwan. Bulletin of the Institute of Zoology, Academia Sinica, vol. 25, no. 2, p. 135-139.
• VAN AS, JG. and BASSON, L., 1989. A further contribution to the taxonomy of the Trichodinidae (Ciliophora: Peritrichia) and a review of the taxonomic status of some fish ectoparasitic trichodinids. Systematic Parasitology, vol. 14, no. 3, p. 157-179.
• VAN AS, JG. and BASSON, L., 1992. Trichodinid ectoparasites (Ciliophora: Peritrichida) of freshwater fishes of the Zambesi River System, with a reappraisal of host specificity. Systematic Parasitology, vol. 22, no. 2, p. 81-109.
• VARGAS, L., POVH, JA., RIBEIRO, RP. and MOREIRA, HLM., 2000. Prevalência de ectoparasitos en tilapia del Nilo (Oreochromis niloticus) de origen tailandesa de Maringá, Paraná. Arquivos de Ciências Veterinárias e Zoologia da UNIPAR, vol. 3, no. 1, p. 32-37.
• XU, K., SONG, W., WARREN, A. and CHOI, JK., 2001. Trichodinid ectoparasites (Ciliophora: Peritrichida) of some marine fishes from coastal regions of the Yellow Sea and Bohai Sea. Systematic Parasitology, vol. 50, no. 1, p. 69-79.
• WELLBORN, TL., 1967. Trichodina (Ciliata: Urceolariidae) of freshwater fishes of the Southeastern United States. Journal of Protozoology, vol. 14, no. 3, p. 399-412.

Publication Dates

• Publication in this collection
  16 Aug 2010
• Date of issue
  Aug 2010

History

• Received
  27 May 2009
• Accepted
  06 Aug 2009