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Animal Biology, Vol. 56, No. 3, pp. 323-333 (2006) Koninklijke Brill NV, Leiden, 2006.Also available online - www.brill.nl
First record of ectoparasitic African Trichodinids(Ciliophora: Peritrichida) in a cichlid fishOreochromis mossambicus (Peters 1852) fromthe Churni river system, West Bengal, India
AMLAN KUMAR MITRA ∗, PROBIR K. BANDYOPADHYAY
Parasitology Laboratory, Department of Zoology, University of Kalyani, Kalyani 741235,West Bengal, India
Abstract—Oreochromis mossambicus (Peters 1852) and Oreochromis niloticus niloticus Linnaeus,1758 are two popular freshwater fishes introduced from Africa to India. There are many records ofdifferent species of trichodinid ectoparasites infesting wild and cultured cichlids in Africa, but nosuch study has been conducted on this parasitic group in India. The fishes Oreochromis mossambicusand Oreochromis niloticus niloticus were investigated for the occurrence of trichodinid ciliophorans.Oreochromis mossambicus was found positive for two species, viz., Trichodina centrostrigeataBasson, Van As & Paperna, 1983 and Paratrichodina africana Kazubski & El-Tantawy, 1986.Oreochromis niloticus niloticus was found not to be infested with any species of trichodinidciliophorans, although, interestingly, Paratrichodina africana was first discovered in this host fish.Comparative descriptions and prevalence of these two above-mentioned species are presented.
Keywords: cichlids; ectoparasites; India; taxonomy; trichodinids.
INTRODUCTION
One of the largest and most widely distributed ciliophoran genera is TrichodinaEhrenberg, 1838 which parasitise, or are symbionts of, aquatic invertebrate andvertebrate hosts (Van As and Basson, 1989). Work on this particular group inIndia has gained momentum since 1980, although Annandale (1912) paved theway by working on this group more than nine decades ago. In India, the mainfocus has always been on describing new species, and, as a result, 12 new speciesbelonging to the genus Trichodina have been described so far (Asmat and Haldar,
∗Corresponding author; e-mail: [email protected]
324 A.K. Mitra, P.K. Bandyopadhyay
1998; Asmat, 2000a, 2001a, b, c; 2002a, b; Mitra and Haldar, 2004, 2005).Interestingly, from India the reports on the occurrence of known trichodinid speciesare significantly less than expected. Only four previously known trichidinids,i.e., Trichodina pediculus (Annandale, 1912; Hagargi and Amoji, 1979), T. nigra(Mukherjee and Haldar, 1982; Saha et al., 1995; Asmat, 2002a), T. reticulata(Mishra and Das, 1993) and T. acuta (Asmat, 2000b), have to date been reportedfrom India. Only Asmat (2000b) reported Trichodina acuta Lom, 1961 froman exotic cichlid, Mozambique tilapia, Oreochromis mossambicus (Peters 1852)and also from a non-cichlid northern mud gudgeon, Ophiocara porocephalusValenciennes, 1846. There are only 11 species of introduced fish species in Indiawith records of only two species belonging to the family Cichlidae. These arethe Mozambique tilapia, Oreochromis mossambicus and Nile tilapia, Oreochromisniloticus niloticus Linnaeus, 1758. These species, like many other cichlids, arevery popular aquarium fish and were imported into India for this purpose. It ismost likely that they were introduced into natural waterways through accidentalor deliberate releases of aquarium fish. A study on the occurrence of trichodinidciliophorans infesting the cichlids Oreochromis mossambicus and O. niloticusniloticus inhabiting the freshwaters of the river Churni and adjacent water bodies ofWest Bengal, India, revealed the presence of two trichodinid species, i.e., Trichodinacentrostrigeata Basson, Van As & Paperna, 1983 and Paratrichodina africanaKazubski & El-Tantawy, 1986, both from Oreochromis mossambicus. This paperprovides valuable information on the biodiversity and taxonomy of Trichodinacentrostrigeata and Paratrichodina africana with new locality and prevalencerecords and the first record of these two species of trichodinid ciliophorans fromIndia.
MATERIALS AND METHODS
Several samplings were carried out to collect host fishes from the river Churni andadjoining beels and kharis passing through the district of Nadia (Lat. 23◦N, Long.88.5◦E), West Bengal, India. Live host fishes were brought to the laboratory fromwhich gill, fin and skin smears were made on grease-free slides. Slides containingtrichodinid ciliophorans were impregnated using Klein’s dry silver impregnationtechnique (Klein, 1958). Examinations of preparations were made under an Olym-pus phase contrast microscope at 1000× magnification with an oil immersion lensand photographs were taken with an Olympus camera. All measurements are givenin micrometers and follow the uniform specific characteristics proposed by Lom(1958), Wellborn (1967) and Arthur and Lom (1984). In each case minimum andmaximum values are given, followed in parentheses by arithmetic mean and stan-dard deviation. In the case of denticles and radial pins, the mode is given instead ofthe arithmetic mean. The span of the denticle is measured from the tip of the bladeto the tip of the ray. Body diameter is measured as the adhesive disc plus bordermembrane. The descriptions of denticle elements follow the guidelines proposed by
Record of African trichodinids in India 325
Van As and Basson (1989). Sequences and methods of the description of denticleelements follow the recommendations of Van As and Basson (1992).
RESULTS AND DISCUSSION
Two species of trichodinids were identified from the host fish Oreochromis mossam-bicus (Peters 1852). These were Trichodina centrostrigeata Basson, Van As & Pa-perna, 1983 and Paratrichodina africana Kazubski & El-Tantawy, 1986. No tricho-dinid ciliophorans were obtained from Oreochromis niloticus niloticus Linnaeus1758, although Paratrichodina africana was first recorded by Kazubski and El-Tantaway (1986) from this host fish in Africa. Therefore, this study establishesOreochromis mossambicus as an additional host for Paratrichodina africana. De-scriptions of these ciliophorans are provided below.
Trichodina centrostrigeata (lapsus T. centrostrigata) Basson, Van As & Paperna,1983 (figs. 1-3, 7; table 1)
Medium-sized trichodinid. Blade of ciliophoran angular in shape, truncated.Distal surface flat or slightly rounded and not parallel to border membrane, rathergradually slopes downwards. Lateral margins of the blade almost parallel. In mostcases, anterior margin makes smooth turn with no existence of a prominent apex.Anterior margin almost touches or sometimes passes beyond y + 1 axis. Tangentpoint blunt, situated lower than distal surface of blade. In few cases, tangentpoint of blade short, straight line rather than a point. Blade apophysis present.Posterior margin forms L-shaped curve with deepest point slightly lower than apex.Posterior projection not prominent. Central part conical but sometimes triangularand comparatively robust, tapering from base to sharply rounded point. Sectionabove and below x-axis similar in shape. Central part extends slightly beyondy-axes. Ray connection short. Ray apophysis not very prominent. Rays straight,of varying thickness, tapering gradually to rounded point or in some cases in blunt,flat ends. Rays directed towards y + 1 axis. Number of centre ridges varies. Widthof centre ridges corresponds with width of rays.
Taxonomic summary
Host: Oreochromis mossambicus (Peters 1852)Locality: Ranaghat, W. Bengal (Lat. 23◦N, Long. 88.5◦E)Location: GillsPrevalence: 4/144 (2.8%)Reference material: OM-2/2002 in the collection of the authors
326 A.K. Mitra, P.K. BandyopadhyayTa
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Record of African trichodinids in India 327
Figures 1-6. Photomicrographs of silver nitrate impregnated adhesive discs of trichodinid cilio-phorans. 1-3: Trichodina centrostrigeata Basson, Van As & Paperna, 1983 from O. mossambicus(Peters 1852) from India (Scale bars – 20 µm); 4-5: Paratrichodina africana Kazubski & El-Tantawy,1986 from O. mossambicus (Peters 1852) from India (Scale bars – 10 µm); 6: an enlarged view of aportion of a denticulate ring (Scale bar – 5 µm).
Remarks
Trichodina centrostrigeata was originally described by Basson et al. (1983) fromPseudocrenilabrus philander, Oreochromis mossambicus, Tilapia rendalli,T. sparrmani and Cyprinus carpio from South Africa and has since been reported
328 A.K. Mitra, P.K. Bandyopadhyay
Figures 7-8. Diagrammatic drawings of the denticles of trichodinid ciliophorans. 7: Trichodinacentrostrigeata Basson, Van As & Paperna, 1983 from Oreochromis mossambicus (Peters 1852) fromIndia. 8: Paratrichodina africana Kazubski & El-Tantawy, 1986 from O. mossambicus (Peters 1852)from India.
from O. mossambicus from Taiwan (Van As and Basson, 1986); from O. niloti-cus (El-Tantawy and Kazubski, 1986) and grass carps (Abdel-Meguid, 1995) fromEgypt; from O. niloticus from Philippines (Natividad et al., 1986; Bondad-Reantasoand Arthur, 1989); from various host fishes from the Zambesi river system, Namibia(Van As and Basson, 1992) and again from O. mossambicus from Taiwan by Bassonand Van As (1994).
Trichodina centrostrigeata has been found to be a common parasite of thewild and cultured tilapia from the Churni river system. Trichodina centrostrigeatacan be distinguished from any other species based on body dimensions, denticlemorphology, presence and structure of centre ridges. Although presence of centreridges alone is not the most important distinguishing character, as a few other ecto-parasitic trichodinids also contain centre ridges, i.e., Trichodina miranda Stein,1979; T. frenata Van As & Basson, 1992.
The present paper confirms the existence of Trichodina centrostrigeata for thefirst time in India from a cichlid fish Oreochromis mossambicus. The ciliophoranobtained from the gills of Oreochromis mossambiocus agree well with the descrip-tions of Basson et al. (1983), Van As and Basson (1986), Van As and Basson (1992)and Basson and Van As (1994).
The body dimension of this species in the present study falls in the same rangeas reported by Basson et al. (1983), as well as Basson and Van As (1994) differingslightly in the number of centre ridges (7-14 in the present study vs. 12-14, 13-16in those of previous authors) and the number of the denticles (20-25 in the presentstudy vs. 26-30, 24-29 in those of previous authors).
Record of African trichodinids in India 329
Trichodina centrostrigeata appears to be highly specific to cichlid fishes. Thereare only two reports of this species of trichodinid ciliophorans from non-cichlids,i.e., by Basson et al. (1983) and Abdel-Meguid (1995) from common carp and grasscarp, respectively.
A comparison of Trichodina centrostrigeata morphometrics found in the presentstudy with those of other authors is presented in table 1.
Paratrichodina africana Kazubski & El-Tantawy, 1986 (figs. 4-6, 8; table 2)
Small sized trichodinid. Denticles have pronounced centrifugal blades. Shapeof blade similar to equilateral triangle with top directed towards adhesive centre.Posterior margin of blade slightly concave and anterior margin convex when seenfrom adhesive disc centre. Distal surface of blade rounded, which give it a semilunarshape, running parallel with border membrane. Tangent point is a small line ratherthan point and situated at same level or just below distal point of distal surface.Anterior margin makes slightly angular turn to form inconspicuous apex. Anteriormargin never touches y-axes. Prominent blade apophysis present. Posterior marginof blade with moderately deep semilunar curve. Blade connection thin and long.Posterior projection not visible. Central part delicate. In most cases tip of centralpart extends halfway towards y-1 axis. Ray connection short. Centripetal raysstraight, narrow, finger shaped and with same thickness along their length. Tip of rayrounded. Ray apophysis absent. Rays directed towards geometric centre of adhesivedisc.
Taxonomic summary
Host: Oreochromis mossambicus (Peters 1852)Locality: Ranaghat, W. Bengal (Lat.23◦N, Long. 88.5◦E)Location: GillsPrevalence: 2/144 (1.4%)Reference material: OM-1/ 2002 in the collection of the authors
Remarks
Paratrichodina africana was obtained for the first time from Nile tilapia in 1984and mentioned as belonging to the genus Tripartiella Lom, 1959 in a shortcommunication at the VIIth International Congress of Protozoology in Nairobi(Kazubski, 1985; El-Tantawy and Kazubski, 1985). The taxonomic position ofthis species was reviewed by Kazubski and El-Tantawy in 1986. The presenceof two important characters, i.e., the straight blade in line with the radius of theadhesive disc and no incision at the base of the blade into which the central partof the neighbouring denticle could enter, helped them to allocate this trichodinidciliophoran to the genus Paratrichodina. Mainly due to the uniqueness of theshape of the denticle, presence of the spine-like outer fragment of the central
330 A.K. Mitra, P.K. Bandyopadhyay
Table 2.Morphometric comparison of Paratrichodina africana Kazubski & El-Tantawy, 1986, obtained in thepresent study, with those of other authors.
Species P. africana P. lizae P. incissa
Host Oreochromis mossambicus Liza parsia Pooled data fromall hosts
Locality West Bengal, India River Matla, India Urasia
Location gills gills gills
Reference(s) present study Asmat Lom and Haldar(2002a) (1977)
Diameter ofbody 15.4-24.8 (20.1 ± 1.3, 29) 17.2-24.4 (22.1 ± 1.7) 18-45.5adhesive disc 12.2-18.3 (14.2 ± 1.3, 29) 13.2-20.4 (17.5 ± 1.6) 16-31
Dimension of bodydenticulate ring 5.7-11.3 (9.2 ± 0.7, 29) 8.7-11.2 (10.2 ± 1.1) 9-30central area – 4.1-8.1 (5.8 ± 1.3) –
Width of border 1.5-2.1 (1.8 ± 1.1, 29) 2.0-3.1 (2.3 ± 0.4) 16-24membrane
Number of denticles 17-22 (20, 29) 18-21 (19.6 ± 0.9) 19-30radial pins/denticle 3-6 (4, 29) 3-5 (4.2 ± 0.6) 4-8
Dimension of denticlespan 2.9-5.1 (3.7 ± 0.6, 29) 3.6-6.1 (5.3 ± 0.7) –length 3.1-4.4 (3.7 ± 0.4, 29) 2.0-2.5 (2.1 ± 0.1) –
Dimension of denticlecomponentslength of the ray 0.5-2.1 (1.1 ± 0.5, 29) 1.2-2.0 (1.8 ± 0.3) 1.2-4.3length of the blade 2.0-3.8 (2.8 ± 1.1, 29) 1.9-3.6 (2.9 ± 0.4) 2.3-4.8width of the central part 0.5-0.9 (0.6 ± 0.1, 29) 0.5-1.0 (0.8 ± 0.2) 0.6-2.2
Adoral ciliary spiral 260-270◦ 240◦ 150-210◦
part, Kazubski and El-Tantawy (1986) proposed this ciliophoran as a new speciesinfesting gills and skins of tilapia from Kenya and Egypt.
The present paper reports on the occurrence of this species for the secondtime, but not from the same host (Oreochromis niloticus niloticus) as reported byKazubski and El-Tantawy. We found this Paratrichodina species from Oreochromismossambicus, establishing an additional host for this ciliophoran and also low hostspecificity of the species. Paratrichodina africana is reported for the first timefrom India with a much smaller body dimension range, i.e., 15.4-24.8 µm in theIndian population vs. 24-45 µm as described by Kazubski and El-Tantawy (1986),although detailed dimensions of denticle components have not been provided bythese authors. Variation in body dimensions between African and Indian populations
Record of African trichodinids in India 331
of Paratrichodina africana might be due to different environmental parameters ofthe habitat of both host and parasite.
Paratrichodina africana obtained from Oreochromis mossambicus in India re-sembles Paratrichodina lizae Asmat, 2002; the only other Paratrichodina speciesreported from India, in having almost the same biometric data (table 2), but themorphology of the denticular components differs significantly. The central area ofthe adhesive disc of Paratrichodina lizae contains one to eight non-impregnable,bright, marble-like round particles, which are completely absent in Paratrichodinaafricana. The shape of the blade is also different between the two species. Theblades of Paratrichodina lizae are rectangular and do not have prominent distinctnotches (anterior projection of the blade) in the anterior margin, whereas the shapeof the blade of Paratrichodina africana is semilunar and has a significantly extendedblade apophysis which is completely absent in Paratrichodina lizae. The morphol-ogy of Paratrichodina africana also resembles to some extent Paratrichodina in-cissa, although the biometric data vary significantly (table 2). The main differencesbetween these two species are the structure of the blade and blade apophysis. Theblade apophysis of Paratrichodina incissa is not as elongated as that of Paratrichod-ina africana. The distal surface of the blade of Paratrichodina africana is rounded,whereas it is straight in Paratrichodina incissa. The anterior tip of the blade apoph-ysis in Paratrichodina incissa is sharply pointed, but in Paratrichodina africana isbluntly rounded.
Since its first description from Egypt and Kenya by Kazubski and El-Tantawy(1986), Paratrichodina africana has never been reported from any corner of theworld. The first report of Paratrichodina africana from India and comparisons withclosely related species provide a new locality and host records for this species.
Acknowledgements
The authors wish to acknowledge Dr. Stanislaw L. Kazubski of the Museum andInstitute of Zoology, Polish Academy of Science, Warszawa, Poland for his kindopinion on our manuscript, especially on Paratrichodina africana which, along withDr. E. L. Tantawy, he described.
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Abdel-Meguid, M. (1995) Ectoparasitic fauna of grass carp Ctenopharyngodon idella in DeltaBreeding Station (D.B.S.) in Egypt. Vet. Med. J., 43, 53-63.
Arthur, J.R. & Lom, J. (1984) Some trichodinid ciliates (Protozoa: Peritrichida) from Cuban fishes,with a description of Trichodina cubanensis n.sp. from the skin of Cichlasoma tetracantha. Trans.Am. Microsc. Soc., 103, 172-184.
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332 A.K. Mitra, P.K. Bandyopadhyay
Asmat, G.S.M. (2000b) First record of Trichodina acuta Lom, 1961 (Ciliophora: Trichodinidae) fromIndia. Chittagong Univ. J. Sci., 24, 63-70.
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