Animal Biology Vol 54 No 2 pp 111-118 (2004) Koninklijke Brill NV Leiden 2004Also available online - wwwbrillnl

First Record of Chilodonella hexasticha (Kiernik 1909)Kahl 1931 (Ciliophora Chilodonellidae) infestinga freshwater fish Nandus nandus (Hamilton)from Gangetic West Bengal India

AMLAN KUMAR MITRA 12lowast DURGA P HALDAR 1

1 Protozoology Laboratory Department of Zoology University of Kalyani Kalyani 741235 WestBengal India

2 Department of Biology Kalna MSDM High School PO Kalna Dist Burdwan West BengalIndia

AbstractmdashWest Bengal situated in the eastern part of the country is one of the most beautiful andimportant states of India In a developing country like India fish is one of the cheapest sources ofprotein and West Bengal contributes a major portion of the total fish production Fishery developmentrepresents a vital sector in West Bengal The degree of success in this sector depends to a great extenton the advancement of fish parasitology research as it is evident that the increase of fish yields canonly be achieved from healthy fish stock During an investigation (July 2001 - December 2002) aprotozoan ectoparasite Chilodonella hexasticha (Kiernik 1909) Kahl 1931 was found on the gillsof a freshwater fish Nandus nandus (Hamilton) This finding is very important for the fishery sectoras this parasite causes the disease chilodonellosis which leads to mass mortality The present paperdeals with the morphology systematics seasonal incidences and prevalence of C hexasticha

Keywords Ciliophora Chilodonella hexasticha ectoparasite freshwater fish India Nandus nan-dus

INTRODUCTION

Most Chilodonella species are free living but two are considered to be seriouspathogens of fish These were described in the first decade of the 20th centuryie the cosmopolitan Chilodonella piscicola (Zacharias 1894) Jankowski 1980[syn C cyprini (Moroff 1902)] occurring on the skin and gills of carp (Cyrpinuscarpio) and the less widely distributed C hexasticha (Kiernik 1909) Kahl 1931

lowastCorresponding author e-mail amlan_mitrahotmailcom

112 AK Mitra DP Haldar

Figure 1 Courses of various rivers including the river Churni in the southern part of West BengalIndia Grey area indicates district of Nadia

from the skin and gills of tench (Tinca tinca) (Lom and Dykova 1992) Until the1970s the taxonomic status of Chilodonella species was in question as the closelyrelated C hexasticha was confused with C piscicola Prost (1952) redescribedC hexasticha and Kazubski and Migala (1974) confirmed the occurrence of twoseparate and distinct parasitic species on fish based on a morphological analysisof the two ciliophorans Chilodonella spp are found on the skin and gills of fishHeavy infestations may cause mass mortality among farmed and wild fish Causesof death involve extensive gill damage eg hyperplasia of the lamellar epitheliumand fusion of the lamellae (Hoffman et al 1979 Leibovitz 1980 Paperna and VanAs 1983 Langdon et al 1985 Urawa and Yamao 1992) Bauer and Nikolrsquoskaya(1957) found in their experimental work that the optimum temperature for themultiplication and mass infection of C piscicola was 6C while C hexasticha isknown to cause morbidity even at 26-31C (Shariff 1984) Chilodonellosis accountsfor the greatest economic losses due to a single disease in commercial tropical fishstores (Leibovitz 1980)

Until recently no work on this particular protozoan group had been conducted inIndia This paper reports on the presence of C hexasticha infesting a freshwater wildfish Nandus nandus inhabiting various beels kharis and the river Churni (23N885E) of West Bengal India for the first time

First Record of Chilodonella hexasticha (Kiernik 1909) Kahl 1931 113

Figure 2 Monthly infestation prevalence () of Chilodonella hexasticha (Kiernik 1909) Kahl1931 on Nandus nandus (Hamilton) with month wise analysis of ambient water temperature (C)and rainfall (cm) during the study period July 2001 - December 2002

MATERIAL AND METHODS

Nandus nandus is a high priced wild freshwater fish inhabiting rivers canalsand beels The fish is gradually becoming extinct and currently cannot be foundin all districts of West Bengal This host fish was investigated from variousbodies of water and the river Churni (fig 1) where it was available in sufficientnumbers mainly during the rainy and winter seasons Fishermen were employedto collect fishes Live host fishes were brought to the laboratory and gill smearswere made on grease-free slides Slides containing chilodonellid ciliophorans wereseparated and impregnated using Kleinrsquos dry silver impregnation technique (Klein1958) Examinations of preparations were made under an Olympus phase contrastmicroscope at 100times magnification with an oil immersion lens and photographswere taken with an Olympus camera All measurements are in micrometers (microm)In each case minimum and maximum values are given followed in parentheses byarithmetic mean and standard deviation

RESULTS

Chilodonella hexasticha (Kiernik 1909) Kahl 1931 (figs 3-8)

Description

Measurements are based on 20 specimens The body of this ciliophoran is asymmet-rically oval and dorsoventrally flattened It measures 388-592 (483 plusmn 63) microm inlength and 357-530 (432 plusmn 50) microm wide The slightly convex dorsal side is with-out any cilia there is just a short ciliary row Cytostome is located ventrally (fig 4)

114 AK Mitra DP Haldar

Figures 3 and 4 Silver impregnated specimens of Chilodonella hexasticha (Kiernik 1909) Kahl1931 obtained from Nandus nandus (Hamilton) showing variation in appearance with divisionalphases Abbreviation C mdash cytostome in figure 4

surrounded by three short pre-oral post-oral and circum-oral kineties (figs 7 8)The posterior end of the body is without a notch (figs 4-6) The flat or slightly con-cave ventral surface has a ciliature reduced to two longitudinal belts close to themargins of the body (figs 3-5) The ventral surface has five to seven (67 plusmn 06)kineties in the right ciliary band and six to eight (69 plusmn 04) in the left band Thekineties are loosely arranged The macronucleus is oval

First Record of Chilodonella hexasticha (Kiernik 1909) Kahl 1931 115

Figures 5 and 6 Silver impregnated specimens of Chilodonella hexasticha (Kiernik 1909) Kahl1931 obtained from Nandus nandus (Hamilton) showing variation in appearance with divisionalphases

Seasonal incidence

Gill lamellae of the host fish Nandus nandus have been found to harbour ciliophoranidentified as C hexasticha This group of ectoparasites has the potential to becomedetrimental to fish health when conditions favour their proliferation Out of 360host fishes examined throughout the study period as many as 32 have beenshown to harbour the ciliophoran C hexasticha with an infestation rate of 89Peaks of prevalence were observed mainly between September and November

116 AK Mitra DP Haldar

Figures 7 and 8 Camera lucida drawings of Chilodonella hexasticha (Kiernik 1909) Kahl 1931obtained from Nandus nandus (Hamilton) Figure 7 mdash divisional phase figure 8 mdash individualspecimen Abbreviations c mdash circumoral kinety p mdash postoral kinety L mdash left straight ciliary bandR mdash right arched ciliary band

when temperatures were below 23C (fig 2) Monthly records of ambient watertemperatures (C) and rainfalls (cm) of the sampling localities have also beenincorporated in the composite graph

DISCUSSION

Confusion reigned in the taxonomy of C piscicola and C hexasticha Andreacute (1912)supported the identity of both species He observed the ciliophorans from Carassiusauratus (L) reared in an aquarium in Geneva and was the first person to give thecorrect description of the body ciliature for C piscicola Wenyon (1926) and Kahl(1931) accepted the validity of both species and Ten Kate (1931) comparing hisown material with previous descriptions also came to the conclusion that thesespecies are distinct On the other hand Schaumlperclaus (1935) expressed the viewthat these ciliates belonged to only one species and Krascheninnikow (1952 1953)expressed similar views Krascheninnikow (1952) published an extensive paper inwhich he tried to prove that only one but a very variable species C piscicolaoccurred on fishes He expressed this view in spite of the fact that he admitted tothe presence of two morphological forms of chilodonella with distinct differencesin number of kineties In a subsequent paper Krascheninnikow (1953) confirmedthe validity of the species C piscicola providing the host list of this parasiteand comparing its ciliature with other representatives of the genus especiallywith the free-living C uncinata The problem of distinguishing C piscicola andC hexasticha was also considered by Prost (1952) She found both species to beclearly different and provided descriptions and drawings Unfortunately this paperwas ignored by most authors Kazbuski and Migala (1974) clearly demonstrated thevalidity of the existence of both species viz C piscicola and C hexasticha

114 AK Mitra DP Haldar

Figures 3 and 4 Silver impregnated specimens of Chilodonella hexasticha (Kiernik 1909) Kahl1931 obtained from Nandus nandus (Hamilton) showing variation in appearance with divisionalphases Abbreviation C mdash cytostome in figure 4

surrounded by three short pre-oral post-oral and circum-oral kineties (figs 7 8)The posterior end of the body is without a notch (figs 4-6) The flat or slightly con-cave ventral surface has a ciliature reduced to two longitudinal belts close to themargins of the body (figs 3-5) The ventral surface has five to seven (67 plusmn 06)kineties in the right ciliary band and six to eight (69 plusmn 04) in the left band Thekineties are loosely arranged The macronucleus is oval

First Record of Chilodonella hexasticha (Kiernik 1909) Kahl 1931 115

Figures 5 and 6 Silver impregnated specimens of Chilodonella hexasticha (Kiernik 1909) Kahl1931 obtained from Nandus nandus (Hamilton) showing variation in appearance with divisionalphases

Seasonal incidence

Gill lamellae of the host fish Nandus nandus have been found to harbour ciliophoranidentified as C hexasticha This group of ectoparasites has the potential to becomedetrimental to fish health when conditions favour their proliferation Out of 360host fishes examined throughout the study period as many as 32 have beenshown to harbour the ciliophoran C hexasticha with an infestation rate of 89Peaks of prevalence were observed mainly between September and November

116 AK Mitra DP Haldar

Figures 7 and 8 Camera lucida drawings of Chilodonella hexasticha (Kiernik 1909) Kahl 1931obtained from Nandus nandus (Hamilton) Figure 7 mdash divisional phase figure 8 mdash individualspecimen Abbreviations c mdash circumoral kinety p mdash postoral kinety L mdash left straight ciliary bandR mdash right arched ciliary band

when temperatures were below 23C (fig 2) Monthly records of ambient watertemperatures (C) and rainfalls (cm) of the sampling localities have also beenincorporated in the composite graph

DISCUSSION

Confusion reigned in the taxonomy of C piscicola and C hexasticha Andreacute (1912)supported the identity of both species He observed the ciliophorans from Carassiusauratus (L) reared in an aquarium in Geneva and was the first person to give thecorrect description of the body ciliature for C piscicola Wenyon (1926) and Kahl(1931) accepted the validity of both species and Ten Kate (1931) comparing hisown material with previous descriptions also came to the conclusion that thesespecies are distinct On the other hand Schaumlperclaus (1935) expressed the viewthat these ciliates belonged to only one species and Krascheninnikow (1952 1953)expressed similar views Krascheninnikow (1952) published an extensive paper inwhich he tried to prove that only one but a very variable species C piscicolaoccurred on fishes He expressed this view in spite of the fact that he admitted tothe presence of two morphological forms of chilodonella with distinct differencesin number of kineties In a subsequent paper Krascheninnikow (1953) confirmedthe validity of the species C piscicola providing the host list of this parasiteand comparing its ciliature with other representatives of the genus especiallywith the free-living C uncinata The problem of distinguishing C piscicola andC hexasticha was also considered by Prost (1952) She found both species to beclearly different and provided descriptions and drawings Unfortunately this paperwas ignored by most authors Kazbuski and Migala (1974) clearly demonstrated thevalidity of the existence of both species viz C piscicola and C hexasticha

First Record of Chilodonella hexasticha (Kiernik 1909) Kahl 1931 115

Figures 5 and 6 Silver impregnated specimens of Chilodonella hexasticha (Kiernik 1909) Kahl1931 obtained from Nandus nandus (Hamilton) showing variation in appearance with divisionalphases

Seasonal incidence

Gill lamellae of the host fish Nandus nandus have been found to harbour ciliophoranidentified as C hexasticha This group of ectoparasites has the potential to becomedetrimental to fish health when conditions favour their proliferation Out of 360host fishes examined throughout the study period as many as 32 have beenshown to harbour the ciliophoran C hexasticha with an infestation rate of 89Peaks of prevalence were observed mainly between September and November

116 AK Mitra DP Haldar

Figures 7 and 8 Camera lucida drawings of Chilodonella hexasticha (Kiernik 1909) Kahl 1931obtained from Nandus nandus (Hamilton) Figure 7 mdash divisional phase figure 8 mdash individualspecimen Abbreviations c mdash circumoral kinety p mdash postoral kinety L mdash left straight ciliary bandR mdash right arched ciliary band

when temperatures were below 23C (fig 2) Monthly records of ambient watertemperatures (C) and rainfalls (cm) of the sampling localities have also beenincorporated in the composite graph

DISCUSSION

Confusion reigned in the taxonomy of C piscicola and C hexasticha Andreacute (1912)supported the identity of both species He observed the ciliophorans from Carassiusauratus (L) reared in an aquarium in Geneva and was the first person to give thecorrect description of the body ciliature for C piscicola Wenyon (1926) and Kahl(1931) accepted the validity of both species and Ten Kate (1931) comparing hisown material with previous descriptions also came to the conclusion that thesespecies are distinct On the other hand Schaumlperclaus (1935) expressed the viewthat these ciliates belonged to only one species and Krascheninnikow (1952 1953)expressed similar views Krascheninnikow (1952) published an extensive paper inwhich he tried to prove that only one but a very variable species C piscicolaoccurred on fishes He expressed this view in spite of the fact that he admitted tothe presence of two morphological forms of chilodonella with distinct differencesin number of kineties In a subsequent paper Krascheninnikow (1953) confirmedthe validity of the species C piscicola providing the host list of this parasiteand comparing its ciliature with other representatives of the genus especiallywith the free-living C uncinata The problem of distinguishing C piscicola andC hexasticha was also considered by Prost (1952) She found both species to beclearly different and provided descriptions and drawings Unfortunately this paperwas ignored by most authors Kazbuski and Migala (1974) clearly demonstrated thevalidity of the existence of both species viz C piscicola and C hexasticha

116 AK Mitra DP Haldar

Figures 7 and 8 Camera lucida drawings of Chilodonella hexasticha (Kiernik 1909) Kahl 1931obtained from Nandus nandus (Hamilton) Figure 7 mdash divisional phase figure 8 mdash individualspecimen Abbreviations c mdash circumoral kinety p mdash postoral kinety L mdash left straight ciliary bandR mdash right arched ciliary band

when temperatures were below 23C (fig 2) Monthly records of ambient watertemperatures (C) and rainfalls (cm) of the sampling localities have also beenincorporated in the composite graph

DISCUSSION

Confusion reigned in the taxonomy of C piscicola and C hexasticha Andreacute (1912)supported the identity of both species He observed the ciliophorans from Carassiusauratus (L) reared in an aquarium in Geneva and was the first person to give thecorrect description of the body ciliature for C piscicola Wenyon (1926) and Kahl(1931) accepted the validity of both species and Ten Kate (1931) comparing hisown material with previous descriptions also came to the conclusion that thesespecies are distinct On the other hand Schaumlperclaus (1935) expressed the viewthat these ciliates belonged to only one species and Krascheninnikow (1952 1953)expressed similar views Krascheninnikow (1952) published an extensive paper inwhich he tried to prove that only one but a very variable species C piscicolaoccurred on fishes He expressed this view in spite of the fact that he admitted tothe presence of two morphological forms of chilodonella with distinct differencesin number of kineties In a subsequent paper Krascheninnikow (1953) confirmedthe validity of the species C piscicola providing the host list of this parasiteand comparing its ciliature with other representatives of the genus especiallywith the free-living C uncinata The problem of distinguishing C piscicola andC hexasticha was also considered by Prost (1952) She found both species to beclearly different and provided descriptions and drawings Unfortunately this paperwas ignored by most authors Kazbuski and Migala (1974) clearly demonstrated thevalidity of the existence of both species viz C piscicola and C hexasticha

First Record of Chilodonella hexasticha (Kiernik 1909) Kahl 1931 117

These two species can be distinguished from one another by the followingmorphological features C piscicola has an asymmetrically oval body with aclear notch in the posterior margin There are usually more kineties in the right(range 7-15) and left (range 12-13) ciliary bands compared to C hexasticha whichhas five to seven kineties in the right and seven to nine in the left band The latterspecies also lacks a clear notch A further difference between these two species isthat it appears that C piscicola tends to infect fingerlings while C hexasticha isfound on older fish (Lom and Dykova 1992)

Economic losses due to Chilodonella spp have been reported by Leibovitz(1980) and Shariff (1984) According to Shariff (1984) chilodonellosis occursthroughout a wide temperature range Mass infections with C piscicola werefound at temperatures slightly above zero (4C) to slightly above 20C whileC hexasticha caused morbidity even at 26-31C Paperna and Van As (1983) gavea detailed report on pathogenesis in skin lesions due to Chilodonella infestationLangdon et al (1985) reported on massive mortalities in the native fishes ofAustralia in the winter when the temperature was 8-13C Urawa and Yamao (1992)conducted scanning electron microscopy studies on C piscicola and remarked onthe pathogenicity of this species on juvenile salmonids

The present chilodonella species obtained from a freshwater wild fish Nandusnandus has been identified as C hexasticha by its smaller body dimensions andsmoothly arranged kineties falling within the range of the species as proposed byLom and Dykova (1992) (figs 3 5) The present population also lacks any posteriornotch (figs 4 6) as seen in C piscicola Chilodonella hexasticha obtained fromour study occurs mainly in the colder months (September to December) whentemperatures range between 11-23C In summer when the temperature rises above32C no chilodonellids were found (fig 2)

REFERENCES

Andreacute E (1912) Les chilodontes parasites des cyprinides Rev Suisse Zool 20 207-212Bauer ON amp Nikolrsquoskaya NP (1957) Chilodonella cyprini (Moroff 1902) ee biologija i epizooti-

logicheskoe znachenie IZV Vsesojuzn nauchn-issled Inst Ozern i Rechn Rybn Loz 42 53-66Hoffman GL Kazubski SL Mitchel AJ amp Smith CE (1979) Chilodonella hexasticha (Kiernik

1909) (Protozoa Ciliata) from North American warmwater fish J Fish Dis 2 153-157Kahl A (1931) Urtiere oder Protozoa Die Tierwelt Deutschlands Bd 30 JenaKazubski SL amp Migala L (1974) Studies on the distinctness of Chilodonella cyprini (Moroff) and

Ch hexasticha (Kiernik) (Chlamydodontidae Gymnostomatida) ciliate parasites of fishes ActaProtozool 13 9-39

Klein BM (1958) The dry silver method and its proper use J Protozool 5 99-103Krascheninikow S (1952) The variability of Chilodonella cyprini Moroff Ann Ukr Acad Art Sci

US 2 293-304Krascheninikow S (1953) The silver line system of Chilodonella cyprini (Moroff) J Morph 92

79-114Langdon JS Gudkovs N Humphrey JD amp Saxon EC (1985) Deaths in Australian freshwater

fishes associated with Chilodonella hexasticha infection Aust Vet J 62 409-412

118 AK Mitra DP Haldar

Leibovitz L (1980) Chilodonelliasis J American Vet Med Ass 177 222-223Lom J amp Dykova I (1992) Protozoan parasites of fishes Development of Aquaculture and Fisheries

Science 26 Elsevier Science Publishers BV Amsterdam The NetherlandsPaperna I amp Van As JG (1983) The pathology of Chilodonella hexasticha (Kiernik) Infection in

cichlid fishes J Fish Biol 23 41-450Prost M (1952) Badania and pierwofniakami pasozytnymi skrzzeli ryb II Chilodonella cyprini

Moroff i Chilodonella hexasticha Kiernik Ann UMCS Sect C 8 1-13Schaumlperclaus W (1935) Chilodon cyprini Moroff and als krankheitserreger bei Forellenbrut und seine

fischpathologische Bedeutung im Allgemeinen Z F Parasitenkunde 7 447-465Sharif M (1984) Occurrence of Chilodonella hexasticha (Kiernik 1909) (Protozoa Ciliata) on big

head carp Aristichthys nobilis (Richardson) in Malaysia Trop Biomed 1 69-75Ten Kate CGB (1931) Zur kenntnis von Chilodon cyprini Moroff nebst systematischen bemer

kungen Arb Unger Biolog Forschungsinstitutes 4 64-83Urawa S amp Yamao S (1992) Scanning electron microscopy and pathogenicity of Chilodonella

piscicola (Ciliophora) on jevenile salmonids J Aquat Anim Health 4 188-197Wenyon CM (1926) Protozoology A manual for Medical Men Veterinarians Zoologists Vol I and

II Bailliegravere Tindall amp Cox (Eds) 1563 p London