The specific characters of the Eimeria, with special reference to the Coccidia of the fowl

Avian Pathology ISSN: 0307-9457 (Print) 1465-3338 (Online) Journal homepage: http://www.tandfonline.com/loi/cavp20 The specific characters of the Eimeria, with special reference to the Coccidia of the fowl L.P. Joyner & P.L. Long To cite this article: L.P. Joyner & P.L. Long (1974) The specific characters of the Eimeria, with special reference to the Coccidia of the fowl, Avian Pathology, 3:3, 145-157, DOI: 10.1080/03079457409353827 To link to this article: https://doi.org/10.1080/03079457409353827 Published online: 17 Sep 2008. Submit your article to this journal Article views: 1820 View related articles Citing articles: 39 View citing articles Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalinformation?journalcode=cavp20 Download by: [46.3.192.1] Date: 30 December 2017, At: 04:33

Avian Pathology, Vol. 3, No. 3, 145 157, 1974. THE SPECIFIC CHARACTERS OF THE EIMERIA, WITH SPECIAL REFERENCE TO THE COCCIDIA OF THE FOWL L, P. JOYNER' and P. L. LONG 2 1 Central Veterinary Laboratory MAFF, Weybridge, Surrey, England 2 Houghton Poultry Research Station Houghton, Huntingdon, England SUMMARY The differentiation of species of Eimeria is discussed with special reference to those occurring in the domestic fowl. Details of the morphology of the oocysts and other developmental stages of the parasites, their location in the host and, the characteristics of the lesions produced, the timing of the patent and prepatent periods, host- and site-specificity and inimunological specificity may be used as aids for specific identification. A single criterion is usually insufficient for differentiation and depending upon the species, different characters vary in significance. Quantitative cross-immunity tests appear to be the most satisfactory means available for the differentiation of species of Eimeria affecting chickens. INTRODUCTION Nine species of Eimeria have been described from the chicken. It *s important that they should be accurately identified when they occur in the field because the diseases which they cause are different and respond differently to some of the coccidiostatic drugs. Furthermore, they are immunologically distinct and for a proper understanding of epidemiology it is necessary to distinguish the species with accuracy. At present, species of Eimeria may be differentiated by (1) the dimensions and morphology of the oocysts (2) host- and site- specificity (3) the morphology of the endogenous stages r(4) pathogenic effects (5) mmunological specificity (cross-immunity) (6) Received 22 March 1974

146 L. P. Joyner and P. L. Long the timing of the pre-patent and patent periods in experimental infections. The species of a given genus can rarely be differentiated by a single criterion. More often they are distinguished by a balance of characters which may vary in significance for particular species. The systematics of any group is constantly under review because at any time new techniques may reveal differences, the significance of which have to be assessed. It is the purpose of this paper to review the principles of the classification of the coccidiai parasites in the light of new developments and with special reference to the Eimeria of the domestic fowl. The significance of the recent new knowledge of the biology of this group in the practical diagnosis of the different forms of coccidiosis will be discussed in a further paper. Oocyst size and shape The oocyst is the most easily accessible stage of any coccidium and many species are known only by the characters of their oocysts. These include colour, size and shape, the surface texture, the presence or absence of a polar cap, the presence or absence of a micropyle and its structure, the shape of the sporocysts and the presence and nature of various ill-defined structures such as residual bodies, polar granules and Stieda bodies. In some hosts such as sheep or cattle, the species can be differentiated by such features and in these animals it is upon the identification of oocyst characters that many studies on parasite distribution and host specificity have been based. It has been known for many years that oocyst size is not necessarily constant. Fish (1931) first provided evidence for a progressive change in oocyst size as infection developed. He noted that oocysts of. tenella increased in length and breadth with time. The shape index (length/breadth) remained constant. Jones (1932) studied a number of factors likely to influence oocyst size during the patency of 'infection with E. acervulina, E. maxima and E. tenella. She concluded that oocyst size was independent of the duration and severity of infection and of the breed and age of the host. She noted however that oocysts collected from individual animals at similar times after inoculation showed appreciable variation in size. Becker et al. (1955) studied E. brunetti in chickens and concluded that small oocysts were produced early in the infection and that large ones succeeded them. These studies were later extended to oocysts of E. necatrix in which a slight though significant increase in size after the first 3 days of patency was noted. This was followed by a reduction in length towards the termination of the infection (Becker ef al., 1956). A similar phenomenon was observed by Cordero del Campillo (1959) in E. falciformis in mice. This species showed a maximum oocyst size at about mid-patency.

Specific characters of Eimeria 147 Duszynski (1971) made a detailed study of the oocysts produced by two rats infected with E. separata. Oocysts from the two animals did not differ materially but the mean dimensions increased from 11.7M-X 10.1i* to 16.3E* x 14.3!* during the three days of patency. The shape of the oocysts remained constant. Long (1973] found that oocysts of E, mivati differed in size and shape depending upon whether they were derived from infections in embryos or chickens. With the embryo-adapted strain the oocysts were almost spherical, but with passage in chickens they assumed the dimensions and shape of those of E. acervulina. in a series of studies on the coccidia of rabbits, Kheissin has drawn attention to the variability in both size and shape of E. magna (Kheissin, 1947a) E. coecicola (Kheissin, 1947b) and E. intestinalis (Kheissin, 1957). Generally the dimensions of the oocysts increased as the infection progressed and the oocystic residual bodies diminished. The shape of the oocysts varied widely, E. intestinalis, for instance, varying from broad pear-shape to subspherical. In E. magna the margin of the micropyle was thickened to varying degrees, altering the overall shape of the oocyst. Oocysts from different animals could also vary in size at any given time. Pout (1965) and Kheissin (1947a) considered that variations in oocyst shape occurred as a result of heavy infections. Rommel (1970) associated these changes with the immune response of the host. It is clear that as specific characters, the dimensions and conformation of the oocyst are not as invariable as some authors appear to have believed. Kheissin (1947a) considered that.the range of variability is genetically controlled and the individual characteristics of oocysts cannot be used as criteria for the classification of species. For most of the species in the fowl there is considerable overlapping of dimensions and whenever oocyst size and shape are quoted as specific characters some analysis of variability should be given and careful details of their origin should be quoted. The oocysts of species in the chicken have no polar caps, no obvious micropyle, the structure and texture of the oocyst walls are all similar and the sporocysts have no peculiarities of shape or size which would enable them to be 'identified. The oocysts of E. maxima are probably the only ones in this host which can be distinguished with certainty by their large size and yellowish colour. Host specificity The host specificity of species of Eimeria is strong and it is rare for a parasite to occur naturally or to complete its life cycle in more than one host genus. Oocysts will often excyst, however, in the intestine of a host in the tissues of which they may subsequently be unable to develop. Haberkorn (1970) observed this with E. tenella from the chicken and E. falciformis from the mouse both of which excysted in the foreign host (mouse and chicken respec-

148 L - "* Joyner and P- L. Long tively) and the sporozoites invaded the intestinal epithelium and developed into trophozoites.. falciformis did not develop further in the chick but. tenella in the mouse proceeded into nuclear division. In the rat, which is more closely related to the normal host,. falciformis developed further into second-generation schizonts but gametogony did not occur. there are only very few acceptable records of the transmission of species of Eimeria from one host genus to another. Norton (1967) succeeded in infecting turkeys with. colchici from the English covert pheasant. The parasite, however, could not be maintained indefinitely in this host. Pellerdy and Dürr (1969) reported numerous attempts to break down the host specificity of. stiedai from the rabbit and. tenella from the chicken. Treatment with X-rays, hydrocortisone, ethiomine or deficient diets failed to make rats or guinea pigs susceptible to. tenella. McLoughlin (1969), (1969), however, administered daily injections of the corticosteroiid dexamethasone to chickens and succeeded in infecting them with E. meleagrimitis from the turkey. Similar treatment of turkey poults failed to make them susceptible to infection with. tenella. Vetterling (1973), also working with. tenella from the chicken, found that this parasite could not complete its development in eight other genera of gallinaceous birds but limited schizogony occurred in the partridge. Recently, Fernando and Remmler (1973 a & b) described six new coccidial species from the Ceylon Jungle Fowl solely on their oocyst characteristics. Many of the species completed their life-cycle in the domestic fowl and one of these has subsequently been identified as a vaniant of. praecox (Long, Fernando and Remmler 1974). These observations may be a reflection of the close systematic relationship of the two hosts rather than incomplete host specificity of the parasites. Site specificity In the domestic fowl where organ specificity has been most completely studied, parenteral injection of oocysts or sporozoites will be followed by the development of the parasites in the normal sites in the intestine. Davies and Joyner (1962) showed that oocysts of four species (E. acervulina, E. maxima,. necatrix and. tenella) could excyst when inoculated ntraperitoneally, intramuscularly or intravenously and that schizogony occurred in the sites normally invaded by the coccidia. Oocysts were produced after the normal prépaient period. Sharma (1964) later injected intravenously sporozoites of seven species of Eimeria of chickens and observed that infection was established in the region of the intestine characteristic of each species. Under normal circumstances the schizogony of. necatrix takes place in the intestine and subsequent gametogony occurs in the caeca. Horton-Smith and Long (1965) showed that if sporozoites

Specific characters of Eimerla 149 are introduced directly into the caeca the parasite will complete the whole life-cycle in that organ. Rose (1967a) further showed that when infection was induced in this way the subsequent immunity was not confined to the caeca. Normally, E. tenella is found in the caecum of the chicken. When however, the caeca were removed and large numbers of parasites were given Leathern (1968) found all stages of the parasite in the proximal large intestine and schizonts and gametocytes developed in the small intestine just above the caecal divert'iculum. Evidently under extreme conditions. tenella will complete its development outside its preferred site. The organ-specificity of. tenella can be reduced by the administration of corticosteroids and Long (1970) showed that schizogony of. tenella occurred in the liver of chickens treated with dexamethasone. This observation suggests that factors under the control of the host play some part in the determination of the final site of development of the parasite.? In the chick embryo some, but not all, species of Eimerla which occur in the adult bird will develop in the choriallantoic membrane (Long 1966) and, when sporozoites are injected intravenously, E. tenella wili develop to the schizogony stage in the embryonic liver. This may be regarded as a reflection of the general predisposition to parasitization of endodermal tissue. Treatment of the embryos with dexamethasone leads to enhanced gametogony and oocyst production in the liver (Long 1971). Following the work of Horton-Smith and Long (1966) it has been accepted that E. mivati may be differentiated from E. acervullna by its ability to develop in the caecum. These authors inoculated sporozoites of. acervulina, E. maxima and. mivati into the caeca of young chicks where only E. mivati developed. This distinction between. acervulina and. mivati was reduced when Joyner and Norton (1972) showed that if large numbers of sporozoites (10 é or 10 7 ) were injected,. acervulina would develop to a limited degree in the caecal epithelium. This has recently been confirmed by Long (1973) who also observed the development of. acervulina in both the small and large intestine. Although it is true that different species of Eimeria have predilections for development within different parts of the intestine this feature is not constant and may be influenced by such factors as age. For example sporozoites of. tenella normally excyst in the duodenum but Rose (1967b) found that in young chicks up to 1 week of age, they were not released until they reached the lower intestine. Similarly. necatrix develops more commonly in the lower half of the small intestine of young birds (Long unpublished observation) whereas in older birds it normally causes lesions in the mid-intestine. Extreme pressure of numbers may also disturb the site preferences of the different species. As already mentioned, when large numbers of. acervulina are administered, 'infections in the caecum can be found. Similarly in heavy or acute infections due to. te-

150 L - p - -loyner and P. L. Long nella invasion of the small intestine adjoining the caecal junctions can often be observed. Despite these exceptions, which largely have been observed under experimental conditions, the site of development is an important guide to the diagnostician. The location of the principal lesions often provides the first suggestion of the possible identity of the responsible pathogen. Endogenous stages of different species of Eimeria Detailed studies have been made on the life cycle of the different species of Eimeria including the number of schizont generations, their size and location and the number and size of the merozoites within the schizonts. This information has often been invaluable in making a final identification. For example, the large size of the 2nd generation schizonts of E. tenella and f. necatrix is considered to be diagnostic. However, some caution is needed 'in the use of these criteria since it has now been shown that in a chick embryo-adapted strain of E. tenella the large 2nd generation schizonts, which normally occur 'in the lamina propiia of the caecal wall, are replaced by schizonts about one fifth of their size which are restricted to the epithelium. This strain of E. tenella is similar to the normal chicken strain in the structure and location of the other endogenous stages and oocyst size. It also produces a cross-immunity against the chicken-maintained strain (Long, 1972). The endogenous stages of some species (e. g. E. acervulina or E. acervulina var mivati) can be modified by host factors. Thus Long and Rose (1970) were able to demonstrate extended oocyst production in chickens treated with the corticosteroid betamethasone suggesting that additional generations of scbizonts may be formed when the host environment is changed by hormonal treatment. These studies show that the coccidial life cycle is not as rigid as formerly believed and that some caution is needed in the use of the morphology, location and timing of schizont generations for the identification of species of Eimeria. Tyzzer (1929) in describing the various species of Eimeria occurring in chickens mentioned the differences in the position in the epithelium in which the parasites develop. Thus E. maxima develops beneath the host epithelial cell nucleus in contrast to E. acervulina which develops in a position superficial to the host cell nucleus. Edgar and Siebold (1964) considered that E. mivati differed from E. acervulina in this respect and stated that the former species frequently penetrated the deeper regions of the host cells. In our experience this is not a distinctive feature because several species of Eimeria which normally occur in superficial sites are found in heavy infections, progressively to invade the deeper regions of the host cells.

Specific characters of Eimeria 151 Pathogenicity The processes by which coccidial parasites affect their host have not been completely determined, although there have been a number of studies on the effects of parasitism on intestinal physiology in relation to host metabolism. These have largely been concerned with E.acervulina and E. necatn'x. It is difficult to establish absolute standards for comparisons of pathogenicity but it is generally accepted that inoculations of about 300,000 to 1x10 6 oocysts of. acervulina/mivati group will regularly produce intestinal lesions with anorexia and weight loss from which the majority of birds recover, so that mortality is not a characteristic feature of these infections in young birds (Hein, 1968). With. praecox, Long (1967) reported that doses of up to 2 m'illion oocysts failed to produce either morbidity or mortality, E. brunetti and f. maxima on the other hand are often associated with mortality in the field and experimental infections with 10,000 oocysts or less with either species regularly produce severe mortality. Both E. necatrix and. tenelia can produce fatal haemorrhage in the gut but with the latter it is confined to the caecum and may be exacerbated by low vitamin K levels in the diet (Davies and Joyner, 1963). Deficiency of Vitamin A may also adversely affect the host's reaction to coccidiosis (Randall, 1964; Coles et al., 1970). Concurrent infection with Marek's disease may also exacerbate the severity of coccidiosis (Biggs et al., 1968). Under experimental conditions Long (1972) was able to show that serial passage in chick embryos caused a reduction in the pathogenicity of. tenelia. Resistance to caecal coccidiosis may be genetically controlled (Champion, 1954) and Long (1968) found that five different strains or breeds of chickens varied in their susceptibility to infection with E. acervulina, E. brunetti, E. maxima and. acervulina. Despite these reservations the pattern of disease coupled with observations on the types of lesions with which it is associated is often a useful guide to the identity of the infection. Immunological specificity It is generally accepted that resistance to reinfection with a given species of Eimeria will not protect against another. Tyzzer (1929) noted that, on feeding a mixture of species to chickens which had been immunized to only one of them, the immunity was selective and specific. The specificity of immunity has often been used to differentiate species of Eimeria in the same host. Levine (1938), for example, used this method to establish E. hagani as a new species in chickens. Birds immunized against E. praecox, E. acervulina, E. mitis, and E. maxima developed infections with E. hagani which was thus judged to be a different species. Moore and Brown (1951) also used the method to establish the distinction between E. adenceides and. meleagrimitis in turkeys.

j 52 L. P. Joyner and P. L Long The principle of immunological species-specificity was first seriously questioned by Rose (1967c) who apparently showed that birds made solidly resistant to E. maxima were almost completely immune to E. brunetti. immunity to. maxima in birds resistant to. brunetti was not so strong. These results were not confirmed by Hein (1971) who used a range of immunizing and challenge infections and concluded that birds which were resistant to E. maxima were fully susceptible to E. brunetti. Some cross-protection was demonstrated when chicks immunized by caecal infections of E. necatrix were challenged with E. tenet I a. However, birds immunized with E. tenella were not protected against E. necatrix. Other work has shown that these parasites have several common antigens (Rose and Long, 1962). Heterogeneity of immunogenicity within a species was demonstrated by Joyner (1969) who worked with two strains of E. acervulina and showed that when birds were made solidly immune to one strain,,so that they produced no further oocysts, they still could be infected with the other strain. It is clear that experiments of this type which are presented as evidence of species differentiation should be accepted with caution especially if they do not include quantitative data. This work with E. acervulina was taken a stage further by Long (1973) who showed that considerable cross-protection occurred between E. acervulina and E.mivati )n the chicken. When however the same strain of E. mivati was passaged in chick embryos this cross-protection was lost. This suggssts that some antigens are changed during the embryo passage of this species and that the distinction between E. acervulina and E.mivati is not immunological ly complete. Long (1973) has suggested that E. mivati may be more correctly referred to as E. acervulina var: mivati. When cross-immunity experiments are cited in the differentiation of species of coccidia, it is important that the conditions should be precisely defined. Details of the number and origin of strains should be given with sufficient details of the challenge infections and the response of the infected immunized birds to permit a full assessment of the ( degree of cross-protection, which is rarely absolute. An example of data from cross-protection experiments is given in Table i, whence it will be seen that birds previously infected with E. acervulina and subsequently challenged with either the same strain, or E. acervulina var mivati, were almost completely protected; less than 1 per cent of the normal oocyst output occurred. Challenge with E. praecox resulted in full oocyst production and infection with E. brunetti was followed by a nearly normal oocyst output. Patent and pre-patent periods The time of the first appearance of oocysts in the faeces of experimentally infected hosts has been used for many years as a means of identification of species of Eimeria and has been retained in a recent diagnostic chart for the domestic fowl (Reid, 1973). However

Table 1. Cross-immunity Oocysts inoculated E. acervulina none E. acervulina none. acervulina none E. acervulina none between E. acervulina and other Eimeria from the chicken Immunising infections Number of oocysts produced from 1st infection @ (in millions per bird) 86.46 0 86.46 0 Number of oocysts produced from 2nd infection 0 (in millions per bird) Oocysts inoculated 86.46 11.07. acervulina var: mivati 86.46 0 11.07 0 11.07 0 11.07 0 = 10,000 oocysts at 2 weeks of age 0 = 100,000 oocysts at 4 weeks of age + = 1,000 oocysts 10 days after 2nd inoculation * = number of oocysts produced per oocyst fed. acervulina E. praecox E. acervulina var: mivati Challenge infection* Number of oocysts produced (in millions per bird) 0.68 140.76 221.29 170.81 0.28 88.74 E. brunetti 38.07 45.14 Reproduction Index* 680 140760 221290 170810 280 88740 38070 45140 protection 99.52 0 99.68 15.66 CO a on o 3" fi) S n S en o a en CO

154 L. p - Joyner and P. L. Long the pre-patent periods of most species occurring in a given host overlap so that this criterion is rarely of value. In the chicken only E. praecox could be separated from the other species by this means because it appears to produce 'its first oocysts some 9 hours before those of other species. The patent period or duration of oocyst production is sometimes characteristic of a species. For example, the oocyst production in infections due to E. maxima is generally shorter than that due to E. acervulina. However, this distinction is markedly affected by the severity of infection and may be confused when other species are present. Conclusions From the foregoing account it is clear that most of the characters by which the species of Eimeria are distinguished are more variably than is often recognized. In some cases this variability is sufficient to bring into doubt the validity of previously acceptable species. Of the criteria discussed in this paper, host specificity is the first guide to the identity of species of Eimeria. In general it is unusual for a given species to develop in other than closely related hosts and rarely in different genera except perhaps in certain experimental situations. This certainly applies to the coccidia of the domestic fowl. Site specificity is also a useful diagnostic guide in natural infections especially where endogenous stages can be recognized such as the large 2nd generation schizonts of E. tenella or E. necatrix, the macrogametes of E. maxima or the large rmcrogametocytes of E. brunetti. The period of patency may sometimes be distinctive, as for example in E. maxima and E. praecox where it is short or in. acervulina or E. necatrix where it tends to be extended. The prepatent periods of most of the species of Eimeria occurring in the fowl however are too close for differentiation. For this group of parasites, oocyst size and morphology are of little systematic value with the single exception of E. maxima. Immunological specificity is probably of greatest value and cross-protection tests, especially when carried out quantitatively, are most likely to provide a definitive guide to identity. It is in the E. acervulina/mivati complex that immunological specificity fails to give clear-cut distinctions. The other available criteria a!so fail to provide distinctions which are of diagnostic value. E. mivati was established on the grounds that it could be distinguished from E. acervulina by the region parasitized, the location of the parasite in relation to the host cell nucleus, the size of the oocysts, the prepatent period and immunological differences. Later it was found that the parasite develops in the caecum of the fowl or the chorioallantois of the chick embryo. All of these features have been found to fall within the range of variation of E. acervulina. Similarly the descriptions of E. mitis given by Tyzzer (1929) and Joyner (1958) are not sufficient to distinguish it from the now recognised wide range of variation of E. acervulina. The status of

Specific characters of Eimeria - 55 E. mitis must remain in doubt until it can be examined in further detail. The bearing these considerations have on the practical diagnosis of coccidiosis in the domestic fowl and the techniques available for the isolation and identification of the different species will be the subject of a further paper. REFERENCES Becker, E. R., Jessen, R. J. Pattillo, W. H. and Van Doominck, W. H. (1956). A biometrical study of the oocyst of Eimeria necatrix, a parasite of the common fowl. Journal of Protozoology, 3: 126-131. Becker, E. R., Zimmermann, W. J. and Pattillo, W. H. (1955). A biometrical study of the oocyst of Eimeria brunetti, a parasite of the common fowl. Journal of Protozoology, 2: 145-150. Biggs, P. M., Long, p. L, Kenzy, S. G. and Rootes, D. G. (1968). Relationship between Marek's disease and coccidiosis II. The effect of Marek's disease on the susceptibility of chickens to coccidial infection. Veterinary Record, 33: 284-289. Champion, L. R. (1954). The inheritance of resistance to cecal coccidiosis in the domestic fowl. Poultry Science, 33: 670-681. Coles, Barbara, Biely, J. and March, B. E. (1970). Vitamin A deficiency and Eimeria acervulina infection in the chick. Poultry Science, 49: 1295-1301. Cordero del Campillo, M. (1959). Estudios sobre Eimeria falciformis (Eimer, 1870) parásito del raton. Anales déla la Facultad de Veterinaria de Leon, 4: 55-73. Davies, S. F. M. and Joyner, L P. (1962). Infection of the fowl by the parenteral inoculation of oocysts of Eimeria. Nature, London, 194, 996-997. Davics, S. F. M. and Joyner, L. P. (1963). Design of therapy for the control of species of Eimeria in the domestic fowl. Journal of Comparative Pathology, 73: 379-390. Duszynski, D. W. (1971). Increase in size of Eimeria separata oocysts during patency. Journal of Parasitology, 57: 948-952. Edgar, S. A. and Seibold, C. T. (1964). A new coccidium of chickens, Eimeria mivati sp. n. (Protozoa; Eimeriidae) with details of its life history. Journal of Parasitology, 50: 193-204. Fernando, M. A. and Remmler, O. (1973a). Four new species of Eimeria and one of Tyzzeria from the Ceylon jungle fowl, Gallus lafayettei. Journal of Protozoology, 20: 43 45. Fernando, A. and Remmler, O. (1973b). Eimeria diminuta sp. n. from the Ceylon jungle fowl Gallus lafayettei. Journal of Protozzology, 20: 357. Fish, F. F. (1931). Quantitative and statistical analyses of infections with Eimeria tenella in chicken. American Journal of Hygiene, 14: 560-576. Haberkorn, A. (1970). Zur Empfänglichkeit nicht spezifischer Wirte für Schizogonie- Stadien verschiedener Eimeria-Arten. Zeitschrift für Parasitenkunde, 35: 156-161. Hein, Helen (1968). The pathogenic effects of Eimeria acervulina in young chicks. Experimental Parasitology, 22: 1-11. Hein, Helen (1971). Eimeria brunetti: cross infections in chickens immunized to E. maxima. Experimental Parasitology, 29: 367-374. Horton-Smith, C. and Long, P. L. (1965). The development of Eimeria necatrix Johnson 1930 and Eimeria brunetti Levine, 1942 in the caeca of the domestic fowl. (Gallus domesticus)- Parasitology, 55: 401-405. Horton-Smith, C. and Long, P. L (1966). The fate of the sporozoites of Eimeria acervulina, Eimeria maxima and Eimeria mivati in the caeca of the fowl. Parasitology, 56: 569-574. Jones, E. E. (1932). Size as a species characteristic in coccidia: Variation under diverse conditions of infection. Archiv für Protistenkünde, 76: 130-170. Joyner, L. P. (1958). Experimental Eimeria mitis infections in chickens. Parasitology, 48: 101-112.

]56 L. P. Joyner and P. L. Long Joyner, L. P. (1969). Immunological variation between two strains of Eimería acervulina. Parasitology, 59: 725 732. Joyner, L. P. and Norton, C. C. (1972). The development of Eimeria acervulina in the caeca of young fowls. Parasitology, 64: 479 483. Kheissin, E. M. (1974). Variability of the oocysts of Eimeria magna Pérad. Zoologicheskii Zhurnal, 26 (1): 17 30. Kheissin, E. M. (1974b). A new species of rabbit coccidia (Eimeria coecicola n. sp.) Comptes Rendus (Doklady) de l'académie des Sciences de l'urss., 55 (2): 177 179. Kheissin, E. M. (1957). Variability of cocysts of Eimeria intestinalis Kheissin 1948, parasite of domestic rabbits. Vestnik Leningradskogo Universiteta Leningrad, No. 9, 43 52. Leathern, W. D. (1968). Organ specificity of Eimeria tenella in caecectomized chickens. Journal of Protozoology, 15: Suppl. 1, 18. Levine, P. P. (1938). Eimeria hagani n. sp. (Protozoa: Eimeriidae) a new coccidium of the chicken. Cornell Veterinarian, 28: 263 266. Long, P. L. (1966). The growth of some species of Eimeria in avian embryos. Parasitology, 56: 575 581. Long, P. L. (1967). Studies on Eimeria praecox Johnson, 1930, in the chicken. Parasitology, 57: 351 361. Long, P. L. (1968). The effect of breed of chickens on resistance to Eimeria infections. British Poultry Science, 9: 71 78. Long, P. L. (1970). Development (schizogony) of Eimeria tenella in the liver of chickens treated with corticosteroid. Nature, London, 225: 290 291. Long, P. L. (1971). Schizogony and gametogony of Eimeria tenella in the liver of chick embryos. Journal of Protozoology, 18: 17 20. Long, P. L. (1972). Eimeria tenella: reproduction, pathogenicity and immunogenicity of a strain maintained in chick embryos by serial passage. Journal of Comparative Pathology and Experimental Therapeutics, 82: 429 437. Long, P. L. (1973). Studies on the relationship between Eimeria acervulina and Eimeria mivati. Parasitology, 67: 143 155. Long, P. L, Fernando, M. A. and Remmler, O. (1974). Experimental infections of the domestic fowl with a variant of Eimeria praecox from the ceylon jungle fowl. Parasitology, 69, 1 9. Long, P. L. and Rose, M. E. (1970). Extended schizogony of Eimeria mivati in betamethasone-treated chickens. Parasitology, 60: 147 155. McLoughlin, D. K. (1969). The influence of dexamethasone on attempts to transmit Eimeria meleagrimitis to chickens and E. tenella to turkeys. Journal of Protozoology, 16: 145 148. Moore. E. N., and Brown, J. A. (1951). A new coccidium pathogenic for turkeys, Eimeria adenoeides n.sp. (Protozoa: Eimeriidae). Cornell Veterinarian, 41: 124 136. Norton, C. C. f 1967J. Eimeria colchici sp. nov. (Protozoa: Eimeriidae), the cause of caecal coccidiosis in English Covert Pheasants. Journal of Protozoology, 14: 772 781. Péllerdy, L. and Dörr, U. (1969). Orale und parenterale Ubertragungsversuche von Kokzidien auf nicht spezifische Wirte. Acta Veterinaria Academlae Scientiarum Hungaricae. 19: 253 268. Pout, D. D. (1965). Coccidiosis in lambs. Veterinary Record, 77: 887 888. Randall, C. J. (1964). Vitamin A. deficiency and its relation to intestinal parasitic infections in the chick. Veterinary Bulletin, 34: 123 126. Reid, W. M. (1973). A diagnostic chart for nine species of fowl coccidia, University of Georgia, College of Agriculture Experimental Sttaion Research report, 163, pp 18. Rommel, M. (1970). Studies on the nature of the crowding effect and of the immunity to coccidiosis. Proceedings: Second International Congress of Parasitology, Journal of Parasitology, 56: No. 4 Section 2 p. 468. flose, M. E. (1967a). Immunity to Eimeria tenella and Eimeria necatrix infections in the fowl. I Influence of the site of infection and the stage of the parasite II Cross-protection. Parasitology, 57: 567 583. Rose, M. E. (1967b). The influence of age of host on infection with Eimeria tenella. Journal of Parasitology, 53: 924 929.

Specific characters of Eimeria - 57 Rose, M. E. (1967c]. Immunity to Eimeria brunetti and Eimeria maxima infections in the fowl. Parasitology, 57: 363 370. Rose, M.., and Long, P. L. (1962). Immunity to four species of Eimeria in fowls. Immunology, 5: 79 93. Sharma, N. N. (1964). Response of the fowl. (Gallus domesticus) to parenteral administration of seven coccidial species. Journal of Parasitology, 50: 509 517. Tyzzer, E. E. (1929). Coccidiosis in gallinaceous birds. American Journal of Hygiene, 10: 269 383. Vetterling, J. M. (1973). Eimeria tenella: Host specificity studies in eight species of gallinaceous birds. Journal of Protozoology, 20: 510. Résumé CARACTÈRES DES ESPÈCES D'EIMERIA, AVEC RÉFÉRENCE SPÉCIALE AUX COCCIDIES DES GALLINÉS Discussion de la differentiation des espèces d'eimeria avec référence spéciale á celles de galinés. Les détails de la morphologie des oocystes et d'autres phases de l'évolution des parasites, leur localisation chez l'hôte et les caractères des lésions produites, le temps des périodes de patente et de prépatente, la spécificité d'hôte et de localisation et la spécificité immunologique, peuvent être employés en vue de l'identification des espèces. Un ceul critère ne suffit généralement pas à la différenciation et l'importance des divers caractères varie selon l'espèce. Les tests quantitatifs d'immunité croisée semblent être le moyen le plus satisfaisant qui soit á notre disposition pour différencier les espèces d'eimeria des gallinas. Zusammenfasung DIE SPEZIFISCHEN EIGENSCHAFTEN VON EIMERIA UNTER BESONDERER BERÜCKSICHTIGUNG DER KOKZIDIEN DES GEFLÜGELS Die Differenzierung der Eimeria-Arten wird unter besonderer Berücksichtigung der Arten, die beim Haushuhn vorkommen, diskutiert. Morphologische Details der Oozysten und anderer Entwicklungsstufen, ihre Lokalisation im Wirt sowie die dort hervorgerufenen charakteristischen Veränderungen können ebenso als Hilfe für die species-ldentifikation herangezogen werden wie die Dauer der Patenz- und Präpatenzperiode. die Wirts- und Organispezifität und die Immunspezifität.