Epizootiology of Eimeria ahsata coccidiosis in León (Spain)

Veterinary Parasitology, 27 (1988) 183-191 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

183

Epizootiology of E i m e r i a a h s a t a Coccidiosis in Le6n (Spain)

M.R. HIDALGO-ARG1jELLO and M. CORDERO-DEL-CAMPILLO

Departamento de Patologia Animal-Sanidad Animal, Facultad de Veterinaria, Universidad de Ldon (Spain) (Accepted for publication 23 February 1987)

ABSTRACT Hidalgo-Argtiello, M.R. and Cordero-del-Campillo, M., 1988. Epizootiology of Eimeria ahsata coccidiosis in LeSn (Spain). Vet. Parasitol., 27: 183-191. The epizootiology of ovine coccidiosis caused by Eimeria ahsata was studied in four flocks in the province of LeSn (Spain), between January 1978 and December 1979. The intensity of infection was found to be 25.5 + 1.7% and was similar in winter and spring. Eimeria ahsata was the most common species in 83.1% of the 1620 samples examined. It was also found in 86.2% of the animals examined. Only 0.3 % of the positive samples contained oocysts of a single species, and samples containing four species were the most frequent (19%). Twenty-three percent of samples contained five species and 31.3% contained six species.

INTRODUCTION

Although there is plenty of information on ovine coccidiosis in Spain ( Cordero et al., 1980 ) few articles are available on the epizootiology of this complex disease. The presence and dynamics of coccidia in animals of different ages in traditional flocks are unknown, as are the possible influences of the environment and type of animals used. Also there are only a few data on the seasonal kinetics of the parasites, the interaction between the species and other aspects of the problem. The present work is intended to determine the epizootiology of Eimeria ahsata infection in sheep under the husbandry conditions in LeSn ( Spain ).

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Locations In order to evaluate the influence of environmental factors, flocks were chosen from a mountainous area (San Emiliano, 1370 m above sea-level), a transition area (La Magdalena, 992 m ) , lower plains (Valencia de Don Juan, 703 m) and Tierra de Campos (Sahagdn de Campos, 829 m) (Fig. 1 ).

Animals Each flock was divided in groups according to age as follows: Group 1,< 1 year old; Group 2, with less than four permanent teeth, b u t > 1 year old; Group 3, with four permanent teeth and between 2-3 years old; Group 4, animals with six permanent teeth and between 3-4 years old; Group 5, with all permanent teeth a n d > 4 years old. From each flock, between 9 and 26.8% of the animals were chosen at random and examined. Within each age-group the percentages of animals studied varied between 8 and 37.5%. In all cases, faeces of at least two animals from each age-group were examined.

Farming systems In all the flocks, the grazing system was the extensive type (free-roaming). However, grazing of sheep on natural pastures in the province of Ledn is highly

185 variable with respect to the soil and the climate because the areas studied are so far apart. When the animals did not go out to graze they were fed similarly in nearly all the areas (alfalfa, barley, beet etc.). The lambing seasons also coincided in all the flocks, being between October and December, and April and June. However, a constant factor was the common practice of grouping all age-groups together in deplorable hygienic conditions.

Sampling This was always done from 9 a.m. to 10 a.m. or from 9 p.m. to 10 p.m. Faecal samples were always taken from the rectum of the females, in wide-necked plastic containers and labelled.

Laboratory techniques The oocysts were studied after flotation by a modified McMaster technique (Weybridge Laboratory, 1971). When the number of oocysts in each McMaster chamber was three or less, saturated NaC1 solution was added in the tubes containing the faecal emulsion until the meniscus was higher than the top of the tube, and then a thick cover glass was placed on top and the tube centrifuged at 1500 rpm for 3 min. The cover glass was then removed and placed on a glass slide, and all the oocysts in the preparation were counted, giving oocysts per gram of faeces. Sporulation was carried out in a 2% potassium dichromate solution at 27 ° C. The process was considered complete when sporozoites were formed in 80% of the oocysts. The morphological details of the oocysts were studied using 40 X and 100 × objectives and 8, 10 and 12.5 × eyepieces on Zeiss or Leitz microscopes. The photomicrographs were taken using an Ortholux-Leitz microscope and a Wild Photoautomat MPS 45 camera with Kodak Panatomic- X film. The keys for identification used were those of Levine (1973) and Pelldrdy (1974).

Statistical data The morphological index express the length/width relationship (L/W). A minimum of 600 oocysts of each type were measured and the average (2), standard deviation (sd), standard error (se), covariance (C) and coefficient of the linear correlation (r) of length and width were all calculated.

186

2 Fig. 2. Unsporulated (1) and sporulated (2) oocysts ofE. ahsata.

Epizootiology The seasonal variations were grouped considering 'winter' to be from 1 January to 31 March, 'spring' from 1 April to 30 June, 'summer' from 1 July to 30 September and 'autumn' from 1 October to 31 December. In view of the confusion in the bibliography concerning the use of some epizootiological terms, we follow those of J u n g m a n n et al. (1973), Catchpole et al. (1975) and Margolis et al. (1982). RESULTS The morphology of the oocysts of E. ahsata was similar to that described by other authors (Levine et al., 1962; Davies et al., 1963; Levine and Ivens, 1970; Levine, 1973; Pell~rdy, 1974; Battelli and Poglayen, 1980). Their measurements varied between 27.3-42.5 X 19.2-35.0/~m. The average was 33.9 X 22.9 pm. s d = L + 2.3, W_+ 2.1. se=L_+ 0.1, W_+ 0.1. Cxy=2.3. r=0.5. L/W=I.O-1.9 (1.5). The sporulation time was 16-32 h (Fig. 2).

Intensity of coccidiosis caused by E. ahsata The results obtained monthly from the four flocks studied show a coccidiosis incidence of 25.5 + 1.7%, with extremes of 4.2 and 88.6%. The percentage was similar in winter (30.3 ___3.3% ) and spring ( 30.3 _ 4.6% ). The incidence in the different age-groups was as follows: Group 1, 30.7 + 2.1%

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(the average of 2 year's investigation in the different areas of sampling) range 0-95.1%; Group 2, 24.4+2.3%, range 0-90%; Group 3, 26.3+2.1%, range 0-83.3%; Group 4, 22_+2.1%, range 0-85.7%; Group 5, 23.7+2.3%, range 0-94.2%. As for the incidence ofE. ahsata coccidiosis in the different age groups during different seasons of the year (Fig. 3), it may be observed that in winter this species occurs more frequently in the youngest and oldest animals (35.3 and 29.2%, respectively). In the remaining groups, the season of highest frequency was spring (30.1, 31.8 and 27%, respectively).

Predominance of E. ahsata Eimeria ahsata is one of the most predominant species, having been found in the province of LeSn (Table I), in 33.1% of the 1620 samples analysed, ranging between 28.3 (Valencia de Don Juan) and 37.7% (Sahag~n de Campos). Prevalence o[ E. ahsata Eimeria ahsata was also one of the most prevalent species in the province of LeSn (Table I), being found in 86.2% of the animals examined (1397 animals were hosts to this species). If each area is considered separately, the prevalence

188 TABLE I Predominance and prevalence of E. ahsata Areas

Total

La Magdalena

San Emiliano

Sahagdn de Campos

Valencia de Don Juan

312

360

528

420

Samples with predominance of E. ahsata Number 110 Percentage 35.2

117 32.5

199 37.7

119 28.3

545 33.6

Animals infected with E. ahsata Number 269 Percentage 86.2

314 87.2

453 85.7

361 85.9

1397 86.2

No. of samples examined

1620

is similar in all of them, being between 85.7 ( Sahagdn de Campos) and 87.2% ( San Emiliano ). Pure- and mixed-infections From the data on prevalence already seen, 79% of the samples were studied in order to find out the different a~sociations of E. ahsata. Only 0.3% of the said samples contained pure infections. Four percent had infections caused by two species; the greatest percentage being the combination of E. ahsata-E. ovinoidalis (1.6%) etc. In 7% of the samples three species were found, and the most frequent combination was E. ahsata-E, bakuensis Musaev, 1970 (Norton, 1986) -E. ovinoidalis ( 2.5% ) etc. Four species were observed in 19% of the samples, the most numerous association being of E. ahsata-E. [aurei-E. bakuensis-E, ovinoidalis (10%) etc. Twenty-three percent contained infections with five species: E. ahsata-E, crandaUis-E, faurei-E, bakuensis-E, ovinoidalis (10.3%) etc. Six species were seen in 31.3% of the samples: E. ahsata-E, crandallis-E, faurei-E, bakuensis-E, ovinoidalis-E, parva ( 22% ) etc. In 13.2% there were seven species, mainly E. ahsata-E, crandallis-E, faurei-E, granulosa-E. bakuensis-E, ovinoidalis-E, parva (6%) etc. Eight species were only found in 2.4% of the samples: E. ahsata-E, crandaUis-E, faurei-E, granulosa-E, intricata-E, bakuensis-E, ovinoidalis-E, parva (0.8%). On the other hand, we observed that E. ahsata was present with E. ovinoidalis in 93.2% of the samples (1026 samples contained both species); with E. bakuensis in 89.6%, with E. faurei in 80.3%, with E. crandaUis in 64.6%, with E. parva in 55.3%, with E. granulosa in 19.1%, with E. intricata in 9.3% and with E. paUida in 3.3%.

189 DISCUSSION It appears that the average size is similar to that found by Honess (1942, cir. Levine and Ivens, 1970) and Pell~rdy (1974), but varies greatly from that found by Levine et al. (1962), Wiesenhtitter (1965), Levine and Ivens (1970), Golemanski and Yuzev (1977) and McDougald (1979). The sporulation period observed was shorter than that recorded by the few authors who have studied it. From our results, it can be seen that the intensity decreases from the youngest animals to the oldest. The role of age must not be forgotten when considering the receptivity of the animals to the coccidia, since it has been proved that a relationship exists between the age and an increasing resistance to infection through the immune mechanisms, although no complete protection is obtained (Levine, 1960). Our results, as far as percentages of intensity in the different age groups are concerned, differ greatly from those found by Jungmann et al. (1973) who found a lower intensity of E. ahsata for all age-groups. As for the intensity ofE. ahsata in the different age-groups, according to the different seasons of the year, our results are very different from that found by Stras~ikov~i et al. (1972) who found this species in different seasons and with much lower percentages. If we observe this seasonal variation in the different age-groups, in the different flocks and in the 2 years of sampling we can see differences in the behaviour of the flocks, especially noticeable in the flock in Sahagfin de Campos. The four areas being far apart within the province, the climate would play an important role, since, on studying the different climatological factors significant differences are found between the four areas. However, such factors may not be the only ones responsible for the seasonal variations observed. The variations could also be influenced by the farming systems, the composition of the flock in different age groups and the lambing season etc. Therefore, we believe that all these factors taken together explain this difference in behaviour and, furthermore, as Cordero (1961) showed, especially intense outbreaks can occur, coinciding with the special conditions in each area. These conditions may have occurred in the area. Similarly, Orlov (1970) pointed out that occasionally the degree of infection depended on the geographical area, a fact also observed by Glebezdin (1976). There are few references to predominance in published works, and the data obtained in the present study are higher, than those quoted in the literature reviewed (Joyner et al., 1966; Michael and Probert, 1970; Catchpole et al., 1975). The prevalence of E. ahsata found in this study was similar to that obtained by Mahrt (1969) in Alberta (Canada) and differed considerably from results obtained by other authors in different countries.

190

As for the data of pure- and mixed-infections, our results differ from those found by Shah (1963), the only data available in the literature.

REFERENCES Battelli, G. and Poglayen, G., 1980. Eimeria ahsata Honess from domestic sheep (Ovis aries) in Italy. J. Protozool., 27: 151-152. Catchpole, J., Norton, C.C. and Joyner, L.P., 1975. The occurrence of Eimeria weybridgensis and other species of coccidia in lambs in England and Wales. B. Vet. J., 131: 392-401. Cordero, M., 1961. ContribuciSn al conocimiento de la epizootiologia de las coccidiosis en Espafia. An. Fac. Vet. LeSn, 7: 53-87. Cordero, M., et al., 1980. Indice Cat,logo de Zoopar~isitos Ib~ricos. Serv. Publ. Minist. San. Seg. Soc. Madrid, pp. 26-32. Davies, S.F.M., Joyner, L.P. and Kendall, S.B., 1963. Coccidiosis. Oliver and Boyd, Edinburgh and London, pp. 69-80. Glebezdin, V.S., 1976. (Prevalence of coccidiosis in sheep in the Turkmen SSR). En: Mater. II vses. S'ezda Protozool. Chast' 3 Vet. Protozool. Kiev, USSR; "Naukova Dumka": 31-32. Golemanski, V. and Yuzev, P., 1977. Coccidia (Eimeriidae) of mouflon, Ovis musimon, in Bulgaria. Acta Zool. Bulg., 8: 54-64. Joyner, L.P., Norton, C.C., Davies, S.F.M. and Watkins, C.V., 1966. The species of coccidia occurring in cattle and sheep in the South-West of England. Parasitology, 56:531-541. Jungmann, R., Ribbeck, R., Hiepe, T., Punke, G., Krishnamurthy, R., Weygandt, B. and Neuer, T., 1973. Untersuchungen ~iber Vorkommen und Bek~impfung von Kokzidien und Ektoparasiten in einer industriem~ssigen L~immermastanlage. I. Kokzidienfauna. Mh. Vet.-Med., 28: 492-497. Levine, N.D., 1960. Protozoan Parasites of Domestic Animals and of Man. Burgess Publishing Company, Minneapolis, MN, pp. 179-190. Levine, N.D., 1973. Protozoan Parasites of Domestic Animals and of Man. 2nd edn. Burgess Publishing Company, Minneapolis, MN, p. 175-186. Levine, N.D. and Ivens, V., 1970. The coccidian parasites (Protozoa, Sporozoa) of ruminants. Illinois Biological Monographs 44. University of Illinois Press, Urbana, Chicago and London, pp. 93-135. Levine, N.D., Ivens, V., Smith, W.N. and Davies, L.R., 1962. A redescription of the oocysts of Eimeria ahsata Honess, 1942, from the domestic sheep. Proc. Helminth Soc. Wash., 29: 87-90. Mahrt, J.J., 1969. Prevalence of coccidia in domestic sheep in Central Alberta. Can. Vet. J., 10: 176-178. Margolis, J., Esch, G.W., Holmes, J.C., Kuris, A.M. and Schad, G.A., 1982. The use of ecological terms in parasitOlogy (report of an ad hoc committee of the American Society of Parasitologists). J. Parasitol., 68: 131-133. McDougald, L.R., 1979. Attempted cross-transmission of coccidia between sheep and goats and description of Eimeria ovinoidalis sp. n. J. Protozool., 26: 109-113. Michael, E. and Probert, J.A., 1970. The prevalence of coccidia in faecal samples from sheep in North Wales. Res. Vet. Sci., 11: 402-403. Norton, C.C., 1986. Coccidia of the domestic goat Capra hircus, with notes on Eimeria ovinoidalis and E. bakuensis (syn. E. ovina) from the domestic sheep Ovis aries. Parasitology, 92: 279-289. Orlov, N.P., 1970. Coccidiosis of farm animals. Translated from Russian. Publ. U.S. Depart. Agric. Nat. Sci. Found., Washington, DC, Israel Programme of Scientific Translation, pp. 88-107. Pell~rdy, L.P., 1974. Coccidia and Coccidiosis. 2nd edn. Paul Parey, Berlin, Hamburg and Akad~miai KiadS, Budapest, pp. 771-805.

191 Shah, H.L., 1963.,Coccidia (Protozoa: Eimeriidae) of domestic sheep in the United States, with descriptions of the sporulated oocysts of six species. J. Parasitol., 49: 799-807. Stras~ikov~i, I., Vondrkova, D. and Chroust, K., 1972. Originators and dynamics of sheep coccidiosis in South-Moravian region. Acta Vet., (Brno), 41: 107-118. Weybridge Laboratory, 1971. Manual of Veterinary Parasitological Laboratory Techniques. Ministry of Agriculture, Fisheries and Food, Tech. Bull. No. 18, HMSO, London. Wiesenhtitter, E., 1965. Das Vorkommen yon Kokzidien und Piroplasmen bei Schafen und Ziegen in Syrien. Tier~irztl. Wschr., 78: 247-249.