FOLIA PARASITOLOGICA 45: 326-328, 1998

CARP COCCIDIOSIS: LONGEVITY AND TRANSMISSION OF GOUSSIA CARPELLI (: ) IN THE POND ENVIRONMENT

Dieter Steinhagen and Katharina Hespe

School of Veterinary Medicine, Diseases Research Unit, Bünteweg 17, 30559 Hannover, Germany

Pond populations of (Cyprinus carpio L.) Antychowicz, Panczyk 1976, op. cit.). In the pond environ- and (Carassius auratus L.) often harbour infections ment, 11-day-old carp fry were already infected with the with the gut dwelling coccidian parasite Goussia carpelli parasite and released oocysts 12 days later (Zaika and Kheisin (Léger et Stankovitch, 1921) (Lom J. and Dyková I. 1992: 1959, op. cit.). How under hatchery conditions the infection is Protozoan Parasites of . Developments in Aquaculture perpetuated and the actual role of the invertebrate paratenic and Fisheries Science, Vol 26. Elsevier, Amsterdam, The host, however, remained unclear. The immediate infection of Netherlands, 315 pp.). In carp hatcheries, this parasite is carp fry with the parasite and the high prevalence of the widespread in fish from all age classes. While 2- and 3-year- infestation indicate that the rearing ponds must be old carp and spawners release very few oocysts only, the contaminated with high numbers of infective stages. In the coccidia-infection is most prevalent in carp fry from July to European carp hatcheries, fish spawn in special ponds and September. During this time, about 80 to 100% of the carp fry spawners are removed from the fry a few days after egg were infected and had high numbers of oocysts in the mucosa deposition (Barthelmes D. 1981: Hydrobiologische Grund- (Biffar M. 1990: Die Parasiten des Karpfens (Cyprinus carpio lagen der Binnenfischerei. G. Fischer Verlag, Stuttgart, L.) im Jahreszyklus unter besonderer Berücksichtigung von Germany, 252 pp). Therefore, a massive contamination of Sphaerospora renicola in einer Karpfenteichwirtschaft in brood ponds by oocysts disseminated by spawners appears to Ostniedersachsen. Dr. med. vet. thesis, Tierärztliche Hoch- be unlikely. To evaluate how the infection is maintained in schule Hannover, 123 pp.). In these fish, enteritis and intestine farm ponds, we examined whether oocysts or sporocysts can atrophy was observed, and the infection was associated with survive in the pond soils and remain infective for carp. In a high mortality rates (Ivassik V.M. and Kulakovskaya O.P. second set of experiments, we evaluated whether a paratenic 1959: Zool. Zh. 38: 1746-1750; Kocylowski B., Zelazny J., host is involved in the transmission of G. carpelli in the pond Antychowicz J., Panczyk J. 1976: Bull. Vet. Inst. Pulawy 20: environment. 12-17; Kent M.L. and Hedrick R.P. 1985: Fish Pathol. 20: 12- For infection experiments carp (Cyprinus carpio) of a 17). In the ornamental fish industry, severe losses are caused single crossing (E20 × R8, Wageningen Agricultural Univer- by G. carpelli coccidiosis due to high mortalities among brood sity, The Netherlands) were used. The fish were raised from stocks of ornamental carp (koi) and goldfish (Kent and fertilized eggs in coccidia-free conditions in laboratory in Hedrick 1985, op. cit.; Proske C. 1996: In R.W. Hofmann and aerated tap water at 20 ± 2°C and fed with pelleted carp feed E.M. Bernoth (Eds.), Tagung der Fachgruppe “Fischkrank- (Trouvit, Trouw & Co, Putten, The Netherlands). In our heiten” der DVG, Königswartha, September 24-26, 1996. experiments, carp were 2-4 months old and had a weight of Deutsche Veterinärmedizinische Gesellschaft, Giessen, pp. 5-20 g. For an infection with G. carpelli, carp were placed 201-210). into tanks with sediment or plancton samples and kept for 2 The transmission of the parasite to uninfected carp was days. The fish were then transferred to parasite free tanks with studied in laboratory experiments. Transmission of G. carpelli tap water at 20-24°C. Two weeks post initial exposure (PE), occurred by faecal contamination and by indirect transmission carp were killed and necropsied. Smears from the gut mucosa via tubificid oligochaetes (Molnár K. 1979: In “Coccidia and were prepared and examined for the presence of G. carpelli Further Prospects of their Control”, International Symposium, oocysts. November 29-30, 1979, Prague, Czech Republic, pp. 179-183; Sediment and plancton samples were collected from the Steinhagen D. and Körting W. 1990: J. Parasitol. 76: 104- ponds of a carp hatchery in the vicinity of Hannover, 107). Northwest Germany. The epizootiology of G. carpelli infections was studied in To confirm whether infective stages of G. carpelli carp hatcheries by early workers (Schäperclaus W. 1943: Z. accumulate in the pond sediment, samples of sediment Fischerei 41: 283-295; Ivassik and Kulakovskaya 1959, op. material from the surface (0-4 cm depth), 4-8 cm, and 8-10 cm cit.; Zaika V.E. and Kheisin E.M. 1959: In Bulletin of the depth were taken from drained fry ponds at moist areas from 3 State Scientific Research Institute of Lake and River Fisheries locations, pooled, and transferred to 20 l tanks filled with 49: Parasites of Freshwater Fish and the Biological Basis of aerated tap water. In these tanks 5 carp were kept for 2 weeks their Control. Leningrad, USSR, Translated from Russian by and then examined for a G. carpelli infection. Israel Program for Scientific Translations, Jerusalem, 1962, To examine the survival of infective stages in the sediment, 2nd edn., 1965, pp. 227-230; Kocylowski, Zelazny, material from the sediment surface (0-4 cm depth) of a fry

Address for correspondence: D. Steinhagen, School of Veterinary Medicine, Fish Disease Research Unit, Bünteweg 17, D-30559 Hannover, Germany. Phone: ++49 511 953 8560; Fax:. ++49 511 953 8587; E-mail: [email protected]

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pond was placed into a 20 l glass tank with tap water. Groups Table 1. Dispersal of Goussia carpelli in the sediment of carp of 5 carp were placed into this tank for 2 days, then ponds. transferred to clean 20 l glass tanks with tap water for another Number of Source of sediment Number of carp infected 10 days and examined for the presence of G. carpelli oocysts. carp used Carp were exposed to the pond sediment at bimonthly Surface-4 cm depth 5 5 4-8 cm depth 5 5 intervals over a period of 18 months. 8-10 cm depth 5 0 In a second experiment, sterilized washed sand was placed into a tank filled with tap water. This tank was contaminated Table 2. Longevity of Goussia carpelli in the sediment from a with G. carpelli oocysts by transferring 5 infected carp and carp pond. keeping the fish for 2 weeks. Groups of 5 carp were exposed Number Number Infections to the contaminated sand for 2 days, then transferred to clean Source of sediment of carp of carp occurred over a tanks with tap water and examined for a G. carpelli infection used infected period of 2 weeks later. Experiments were continued in monthly Moist pond sediment 45 43 18 months intervals over a period of 4 months. Air dried pond sediment 5 0 Contaminated sterile 20 13 3 months To examine whether infective stages of G. carpelli tolerate washed sand desiccation, pond sediment was air dried for 2 weeks and then rehydrated again in a 20 l tank with tap water. Carp kept in Table 3. Transmission of Goussia carpelli by paratenic hosts. these tanks for 2 weeks were subsequently examined for a Number of Number of carp Invertebrate coccidia infection. carp used infected To examine whether planctonic organisms from the pond Pond plancton 80 0 environment might serve as paratenic host of G. carpelli, Tubificid oligochaetes 10 9 plancton samples were collected from a carp pond with a Chironomid larvae 12 1 history in G. carpelli coccidiosis by passing 300-400 l water through a series of sieves with 600, 300, 212, 125, and 45 µm mesh in diameter. Organisms trapped on the sieves were of 3 months. Carp exposed after 4 months remained unin- separately resuspended in tap water, transferred to 20 l glass fected (Table 2). tanks, and 5 carp were placed into these tanks and allowed to Carp fed on planctonic organisms from ponds with a feed on the pond plancton. The carp were examined for G. history in G. carpelli coccidiosis did not acquire an infection carpelli infections 2 weeks later. Plancton sampling was done with this parasite (Table 3). Tubificid oligochaetes from the 4 times in weekly intervals from mid June to mid August pond sediment, however, were able to serve as paratenic hosts 1995. of G. carpelli. In 3 experiments, 9 out of 10 carp fed with To study the role of benthic organisms as paratenic hosts of tubificids acquired the parasite and 1 carp out of 12 fed with G. carpelli, tubificid oligochaetes ( spp., Limnodrilus chironomids was infected. spp.) and chironomid larvae were collected from sediment The results of our experiments confirmed that the pond samples, washed in tap water to remove detritus material from sediment is the main source of infective G. carpelli oocysts the body surface and then fed to individual carp. Each carp and sporocysts. In the sediment, oocysts survive for several received 5 to 10 tubificids or chiromonids and was examined months and are able to induce infections in parasite naive for coccidian oocysts 2 weeks later. carp. The oocysts, however, were found to be sensitive to The results of the infection experiments are presented in desiccation. Zaika and Kheisin (1959, op. cit.) reported that Tables 1-3. Infective oocysts were found in sediment samples oocysts deform within 15 to 20 min when dried out, and they from the surface and from 4-8 cm depth. All 10 fish exposed suggested draining carp ponds during summer as a to these sediments acquired an infection with the parasite, prophylactic measure against G. carpelli coccidiosis. This is while carp from tanks with sediment samples from 8-10 cm substantiated by the outcome of our infection experiments depth remained uninfected (Table 1). In samples taken from using resuspended dried pond sediment. In these experiments the surface of the pond sediment, infective G. carpelli stages all carp used remained uninfected. The importance of pond were found over a period of 18 months. From the carp hygiene and drying of the sediment as a preventive measure exposed to moist sediment at bimonthly intervals over this against carp coccidiosis was underlined by Kocylowski et al. period 43 out of 45 acquired an infection with the parasite. (1976, op. cit.) in their study on Polish carp ponds. The Sediment samples from the same location, which were air authors observed high prevalences of G. carpelli infection in dried and rehydrated again, were not able to induce a G. carp populations from ponds which had not been dried, and carpelli infection. Carp kept in this tank did not acquire an thus assumed that coccidian stages remained viable in the infection with the parasite (Table 2). In sterilized washed pond sediment and were a continuous source of infection for sand, infective stages of G. carpelli were found up to 3 carp fry. In our experiments, all sediment samples were taken months post contamination with oocysts. Carp exposed to the from ponds drained during spring for about 8 to 10 weeks. sand at monthly intervals acquired the infection over a period During this time, however, the sediment remained moist and

327 in these samples we still found infective G. carpelli stages. however, indicated that chironomids were able to transfer the Infective stages were present up to a depth of 4-8 cm. This infection, which probably occurred by passive transfer with underlines that coccidian stages may survive even in deeper the intestinal contents. In laboratory experiments, carp were layers of sediment material. Therefore, draining or liming of resistant to a secondary infection via direct transmission, but a ponds as a control measure of carp coccidiosis appears only to secondary infection could be induced when the fish were fed be effective when it is done for a sufficient time. on contaminated tubificids (Steinhagen and Körting 1990, op. In laboratory experiments, parasite naive carp acquired the cit.). In nature, tubificids are the major food organism of carp infection by ingestion of oocysts from the contaminated in their 2nd and 3rd year (Barthelmes 1981, op. cit.) and thus environment and by feeding on infected tubificids acting as may represent a significant source of infection for these fish. paratenic hosts (Steinhagen and Körting 1990, op. cit.). Our finding that tubificids from pond sediments were able to induce G. carpelli infections indicates a wide distribution of Acknowledgements. Many thanks are due to K. Böttcher and G. carpelli stages in tubificids from pond sediments and S. Bunnajirakul, Hannover for skillful technical help. S.H. suggests that transmission of G. carpelli by a paratenic host Leenstra and Dr. G. Wiegertjes, Wageningen, The Nether- plays a significant role in nature. Organisms from the pond lands generously provided fertilized carp eggs. The study was plancton and chironomids appeared not to be of major financially supported by a grant from the Niedersächsische importance for the transfer of the infection. Our observations, Minister für Wissenschaft und Kultur.

Received 15 September 1997 Acceped 19 March 1998

FOLIA PARASITOLOGICA 45: 328, 1998

HYSTEROTHYLACIUM NIPPONENSE NOM. N. (NEMATODA: ANISAKIDAE) FOR H. JAPONICUM MORAVEC ET NAGASAWA, 1998 PREOCCUPIED BY HYSTEROTHYLACIUM JAPONICUM RAJYALAKSHMI, 1996

František Moravec1 and Kazuya Nagasawa2

1Institute of Parasitology, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic; 2National Research Institute of Far Seas Fisheries, Fisheries Agency of Japan, 5-7-1 Orido, Shimizu, Shizuoka 424-8633, Japan

Since Hysterothylacium japonicum Moravec et Nagasawa, 1998 (Acta Parasitol. 43: 39-42) was found to be a homonym of H. japonicum Rajyalakshmi, 1996 (Riv. Parassitol. 13: 53-60) described from India, a new name, H. nipponense nom. n., is now proposed for the former, Japanese species.

Received 19 October 1998 Accepted 19 October 1998

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