Out of the 200 examined rabbits, 100 were positively infected with Eimeria spp., indicating a prevalence of 50%.
E. exigua, E. perforans, E. intestinalis, and E. irresidua were the most common species; E. flavescens and E. media were less common; and E. magna, E. coecicola, E. vejdovskyi, E. piriformis, and E. stiedae were rare (Table 1).
The morphological and morphometric characters of the recovered Eimeria species are summarized in Tables 1 and 2. The oocysts of 11 Eimeria species collected from the domestic rabbits in the present study are illustrated in Figs. 1-15.
1. E. coecicola Cheissin (1947)
Synonym: Eimeria oryctolagi Ray and Banik, 1965
Host: Domestic rabbits (Oryctolagus cuniculus) (L., 1758) (syn. Lepus cuniculus).
Locality: Qena governorate, Upper Egypt
Prevalence: 8% (8/100)
Sporulation time: 60h
Description (Tables 1 and 2, Fig. 1):
Sporulated oocysts are cylindrical and 29.75 μm (27.41–31.58 μm) in length and 17.38 μm (16.27–18.11 μm) in width, with a distinct micropyle at one end (Figs. 1B and 1D). The oocyst wall is double-layered; the outer layer is smooth, somewhat thickened, forming a small ridge at the micropyle, and the inner layer is membranous. The micropyle is well-pronounced and surrounded by a slightly thickened wall, the oocyst residuum is rounded; and the polar granule is absent (Figs. 1B and 1D). Sporocysts are elongated ovoid to spindle-shaped with a pointed end, measuring 12.04 μm (10.27–13.8 μm) in length and 7.03 μm (6.16–7.75 μm) in width, with the Stieda body and residuum (Fig. 1D). Sporozoites are elongate, lying lengthwise head to tail in the sporocysts, each with one refractile body at the wider end (Figs. 1B and 1D).
Unsporulated oocysts are cylindrical and 30.3 μm (29.52–31.22 μm) in length and 16.32 μm (15.43–16.88 μm) in width, with a conspicuous micropyle (Figs. 1A and 1C). Sporoblast (zygote) is cylindrical, measuring 22.54 μm (19.37–24.7 μm) in length and 12.07 μm (11.64–12.54 μm) in width (Figs. 1A and 1C).
2. E. exigua Yakimoff (1934)
Synonymy: Eimeria exigua Type I of Yakimoff, 1934; Eimeria exigua var. septentrionalis Madsen, 1938, pro parte; Eimeria hungarica Pelle´rdy, 1956, pro parte.
Host: Domestic rabbit, Oryctolagus cuniculus (L., 1758) (syn. Lepus cuniculus).
Locality: Qena governorate, Upper Egypt.
Prevalence: 65 (65/100)
Sporulation time: 33h
Description (Tables 1 and 2, Fig. 2):
Sporulated oocysts are spherical to subspherical, measuring 19.41 μm (17.13–24.27 μm) in length and 19.61 μm (17.56–23.37 μm) in width. The micropyle and the oocyst residuum are absent. The sporocyst is ellipsoid to elongated ovoid, measuring 11.44 μm (10.26–12.47 μm) in length and 6.75 μm (5.56–7.84 μm) in width (Figs. 2B and 2D). The sporocyst residuum is present (Figs. 2B and 2D). The Stieda body is present, and substieda and parastieda bodies are absent (Fig. 2D).
Unsporulated oocysts are spherical to subspherical, measuring 22.74 μm (20.48–25.41 μm) in length and 21.96 μm (20.61–23.88 μm) in width. The micropyle is absent (Figs. 2A and 2C). Sporoblast (zygote) is spherical to subspherical, measuring 14.58 μm (11.96–18.12 μm) in length and 13.9 μm (11.5–17.25 μm) in width (Figs. 2A and 2C).
3. E. flavescens Marotel and Guilhon (1941)
Synonymy: Eimeria pellerdyi Coudert, 1977a, b; Eimeria hakei Coudert, 1978; Eimeria irresidua Kessel and Jankiewicz, 1931 of Francalani and Manfredini, 1967.
Host: Domestic rabbit, Oryctolagus cuniculus (L., 1758) (syn. Lepus cuniculus).
Locality: Qena Governorate, Upper Egypt.
Prevalence: 30% (30/100)
Sporulation time: 45h
Description (Tables 1 and 2, Fig. 3):
Sporulated oocysts are ovoid and 29.63 μm (24.71–34.42 μm) in length and 21.08 μm (17.06–25.45 μm) in width. There are two oocyst walls; the outer wall is smooth, and the inner wall is thick. The micropyle is prominent and well-defined. There are no oocyst residuum and polar granule. The sporocyst is elongated ovoid, measuring 13.31 μm (12.08–14.07 μm) in length and 7.63 μm (6.23–8.96 μm) in width (Figs. 3B and 3C). The Stieda body is small, without substieda or parastieda bodies (Fig. 3D). The sporocyst residuum is present as a subspheroidal cluster of granules (Figs. 3B and 3D). Sporozoites are elongate, each with one clear refractile body (Figs. 3B and 3D).
Unsporulated oocysts are ovoid, measuring 27.4 μm (25.25–29.79 μm) in length and 20.25 μm (18.54–21.86 μm) in width, with a conspicuous micropyle (Figs. 3A and 3B). The sporoblast (zygote) is ovoid, measuring 18.78 μm (17.67–20.43 μm) in length and 16.6 μm (14.33–18.7 μm) in width (Figs. 3A and 3C).
4. E. irresidua Kessel and Jankiewicz (1931)
Synonymy: Eimeria elongata Marotel and Guilhon, 1941.
Host: Domestic rabbit, Oryctolagus cuniculus (L., 1758) (syn. Lepus cuniculus).
Locality: Qena Governorate, Upper Egypt.
Prevalence: 35% (35/100)
Sporulation time: 50h
Description (Tables 1 and 2, Fig. 4):
Sporulated oocysts are ellipsoid, measuring 29.69 μm (26.15–35.88 μm) in length and 19.18 μm (17.27–23.06 μm) in width. There are two oocyst walls; the outer wall is smooth, and the inner wall is thick. The micropyle is concave and conspicuous. Both the oocyst residuum and the polar granule are absent. The sporocyst is ovoidal to ellipsoidal, measuring 13.65 μm (11.98–18.9 μm) in length and 7.68 μm (6.56–9 μm) in width (Fig. 4D). The Stieda body is pointed, and substieda and parastieda bodies are absent (Figs. 4B and 4D). The sporocyst residuum is irregularly elongate, compact, and granular (Figs. 4B and 4D). Sporozoites lay end to end, each with a large refractile body at the wider end (Figs. 4B and 4D).
Unsporulated oocysts are ellipsoid, measuring 29.08 μm (28.28–29.53 μm) in length and 17.87 μm (17.53–18.11 μm) in width, with a conspicuous micropyle (Figs. 4A and 4C). The sporoblast (zygote) is ellipsoid, measuring 17.81 μm (17.75–17.87 μm) in length and 14.76 μm (14.32–15.01 μm) in width (Figs. 4A and 4C).
5. E. magna Pe´rard (1925)
Synonymy: Eimeria perforans var. magna Pe´rard, 1925.
Host: Domestic rabbit, Oryctolagus cuniculus (L., 1758) (syn. Lepus cuniculus).
Locality: Qena Governorate, Upper Egypt.
Prevalence: 10% (10/100)
Sporulation time: 48h
Description (Tables 1 and 2, Fig. 5):
Sporulated oocysts are ovoid, measuring 29.82 μm (28.13–32.31 μm) in length and 18.25 μm (17.82–18.97 μm) in width. The micropyle is present, with a collar-like thickening of the outer layer around the micropyle. The oocyst residuum is large (Fig. 5D); polar granule is absent. The sporocyst is ovoidal to ellipsoidal, measuring 12.72 μm (9.7–15.43 μm) in length and 7.24 μm (6.64–7.59 μm) in width (Figs. 5B and 5D). The Stieda body is small, and substieda and parastieda bodies are absent (Fig. 5B). The sporocyst residuum is coarsely granular and appears as a small cluster in the middle of sporocysts (Figs. 5B and 5D). Sporozoites lay head to tail around the sporocyst residuum, each with a central nucleus and one large refractile body at their broad end (Figs. 5B and 5D).
Unsporulated oocysts are ovoid, measuring 30.2 μm (29.74–30.87 μm) in length and 18.8 μm (17.89–19.32 μm) in width, with a conspicuous micropyle (Figs. 5A and 5C). The sporoblast (zygote) is spherical to subspherical, measuring 19.09 μm (18.72–14.07 μm) in length and 15.05 μm (13.94–16.64 μm) in width (Figs. 5A and 5C).
6. E. media Kessel and Jankiewicz (1931)
Synonymy: Eimeria media Kessel, 1929.
Host: Domestic rabbit, Oryctolagus cuniculus (L., 1758) (syn. Lepus cuniculus).
Locality: Qena Governorate, Upper Egypt.
Prevalence: 25% (25/100)
Sporulation time: 31h
Description (Tables 1 and 2, Fig. 6):
Sporulated oocysts are ellipsoid, measuring 27.44 μm (25.34–29.4 μm) in length and 18.61 μm (16.36–22.11 μm) in width. The micropyle is convex, protruding with thickening of the wall surrounding it (Figs. 6B and 6D). The oocyst residuum is spheroidal; the polar granule is absent (Figs. 6B and 6D). The sporocyst is fusiform or ovoidal to ellipsoidal, measuring 13.72 μm (11.22–15.88 μm) in length and 6.95 μm (6.5–8.01 μm) in width (Figs. 6B and 6D). The Stieda body is small and flat (Fig. 6B), and substieda and parastieda bodies are absent. The sporocyst residuum is compact and spheroidal and composed of rough granules and is generally present near the sporocyst wall. Sporozoites lay end to end (Figs. 6B and 6D).
Unsporulated oocysts are ellipsoid, measuring 26.45 μm (25.68–27.14 μm) in length and 16.94 μm (16.73–17.24 μm) in width, with an inconspicuous micropyle (Figs. 6A and 6C). The sporoblast (zygote) is spherical, measuring 18.63 μm (18.26–18.98 μm) in length and 13.78 μm (13.5–14.04 μm) in width (Figs. 6A and 6C).
7. E. perforans (Leuckart, 1879) Sluiter and Swellengrebel (1912)
Synonymy: Coccidium cuniculi Rivolta, 1878; Coccidium perforans Leuckart, 1879; Eimeria nana Marotel and Guilhon, 1941; Eimeria lugdunumensis Marotel and Guilhon, 1942.
Host: Domestic rabbit, Oryctolagus cuniculus (L., 1758) (syn. Lepus cuniculus).
Locality: Qena Governorate, Upper Egypt.
Prevalence: 63% (63/100)
Sporulation time: 30h
Description (Tables 1 and 2, Fig. 7):
Sporulated oocysts are ellipsoid, measuring 24.19 μm (16.46–26.68 μm) in length and 17.08 μm (11.73–19.76 μm) in width. The micropyle is occasionally present or absent, rarely visible in smaller oocysts. The oocyst residuum is variable, spheroidal, triangular, or composed of a chain of granules; the polar granule is absent (Figs. 7B and 7D). The sporocyst is fusiform or ovoidal to ellipsoidal, measuring 11.92 μm (8.24–13.23 μm) in length and 6.52 μm (4.26–7.88 μm) in width (Figs. 7B and 7D). The Stieda body is small (Fig. 7B), and substieda and parastieda bodies are absent. The sporocyst residuum is small and granular (Figs. 7B and 7D). Sporozoites lay end to end, each with one end being broader than the other and with one clear refractile body at the large end (Figs. 7B and 7D).
Unsporulated oocysts are ellipsoid, measuring 19.56 μm (15.25–22.96 μm) in length and 14.08 μm (11.64–16.72 μm) in width, with an inconspicuous micropyle (Figs. 7A and 7C). Sporoblast (zygote) is ellipsoid to ovoid, measuring 13.5 μm (11.63–15.19 μm) in length and 9.56 μm (7.9–10.63 μm) in width (Figs. 7A and 7C).
8. E. intestinalis Cheissin (1948)
Synonymy: E. agnosta Pelle´rdy (1954); E. piriformis Gve´le´ssiani and Nadiradze (1945); E. piriformis Cheissin (1948) (Pelle´rdy, 1953); non-E. piriformis Kotlan and Pospesch (1934); non-E. piriformis Marotel and Guilhon (1941); non-E. piriformis Lubimov (1934).
Host: Domestic rabbit, O. cuniculus (L., 1758) (syn. Lepus cuniculus).
Locality: Qena Governorate, Upper Egypt.
Prevalence: 50% (50/100)
Sporulation time: 52 h
Description (Tables 1 and 2, Fig. 8):
Sporulated oocysts are piriform, measuring 25.19 μm (23.38–26.56 μm) in length and 18.3 μm (16.81–19.37 μm) in width. The micropyle is well-defined with a wall somewhat thickened around it. The oocyst residuum is conspicuous and granular; the polar granule is absent (Figs. 8B and 8D). The sporocyst is oblong to ovoidal, measuring 10.97 μm (9.04–13.02 μm) in length and 6.38 μm (5.74–7.77 μm) in width (Figs. 8B and 8D). The Stieda body is small (Fig. 8B), and substieda and parastieda bodies are absent. The sporocyst residuum is small or a round, compact mass (Figs. 8B and 8D). Sporozoites are elongate, lying lengthwise head to tail in sporocysts, each with one clear refractile body at the larger end (Figs. 8B and 8D).
Unsporulated oocysts are piriform, measuring 23.9 μm (20.97–25.92 μm) in length and 163.83 μm (13.71–20.34 μm) in width, with a conspicuous micropyle (Figs. 8A and 8C). The sporoblast (zygote) is spherical to subspherical, measuring 15.22 μm (14.85–15.8 μm) in length and 14.31 μm (11.87–16.57 μm) in width (Figs. 8A and 8C).
Endogenous stages (Fig. 9):
Examination of the histological section of the ileum revealed the presence of microgametes, macrogametes, and oocysts. The early microgamonts were recognized by their large number of dark small nuclei distributed throughout the entire surface of the gamont. The macrogametes were distinguishable from microgametes by their large central nucleus with a prominent nucleolus and the appearance of wall-forming bodies at their periphery. Numerous oocysts at different stages of maturation could be distinguished within parasitophorous vacuoles.
Transmission electron microscopy (Figs. 10–12):
Microgametogenesis (Fig. 10): The developing microgamonts increased in length and eventually became detached and occupied the parasitophorous vacuole. As the development of microgamonts proceeded, the microgametes began to differentiate. The fully formed microgamete had an elongated nucleus and a tubular mitochondrion, and two flagella were clearly observed. The nucleus occupied nearly all the microgamete space, and a single stretched mitochondrion was present in the nuclear depression and extended along the anterior half of the microgamete nucleus.
Macrogametogenesis (Fig. 11): The electron microscopic study revealed that a mature macrogamete was characterized by a large central nucleus with a prominent nucleolus. The most significant structure was the appearance of the so-called wall-forming bodies (WFB). Two types of WFBs (WFBI and WFBII) were detected. These stages were abundantly supplied with backup nutrients, amylopectin granules, and lipid droplets that were clearly visible within this stage.
Oocyst development (Fig. 12): The dissociation and progressive disappearance of WFBs were related to the onset of the appearance of the inner wall and the outer wall of the oocyst. After the completion of the formation of the oocyte wall, the WFBs were no longer observed (Fig. 12B).
9. Eimeria stiedae (Lindemann, 1865) Kisskalt and Hartmann, 1907
Synonymy: Monocystis stiedae Lindemann, 1865; Psorospermium cuniculi Rivolta, 1878; Coccidium oviforme Leuckart, 1879; Coccidium cuniculi (Rivolta, 1878) Labbe´, 1899; Eimeria cuniculi (Rivolta, 1878) Wasielewski, 1904; Eimeria oviformis (Leuckart, 1879) Fantham, 1911; Eimeria stiedae var. cuniculi Graham, 1933.
Host: Domestic rabbit, Oryctolagus cuniculus (L., 1758) (syn. Lepus cuniculus).
Locality: Qena Governorate, Upper Egypt.
Prevalence: 2% (2/100)
Sporulation time: 58h
Description (Tables 1 and 2, Fig. 13):
Sporulated oocysts are ovoid, measuring 28.13 μm (27.65 - 28.44 μm) in length and 16.99 μm (16.55 - 17.66 μm) in width. The micropyle is smooth at the narrow end of the oocyst, sometimes inapparent (Figs. 13B and 13D). The oocyst residuum and the polar granule are absent (Figs. 13B and 13D). The sporocyst is elongate ovoidal, measuring 11.01 μm (10.82 -11.18 μm) in length and 5.89 μm (5.67 - 6.03 μm) in width (Figs. 13B and 13D). The Stieda body is present (Fig. 13D), and substieda and parastieda bodies are absent. The sporocyst residuum is granular (Figs. 13B and 13D). Sporozoites are elongate (Figs. 13B and 13D).
Unsporulated oocysts are ovoid, measuring 27.31 μm (26.58 - 27.74 μm) in length, 17.37 μm (16.74 - 17.86 μm) in width, with an inconspicuous micropyle (Figs. 13A and 13C). The sporoblast (zygote) is spherical, measuring 17.05 μm (16.55 - 17.38 μm) in length and 15.24 μm (14.88 - 15.46 μm) in width (Figs. 13A and 13C).
10. Eimeria vejdovskyi Pakandl, 1988
Synonymy: Eimeria media Kessel, 1929
Host: Domestic rabbit, Oryctolagus cuniculus (L., 1758) (syn. Lepus cuniculus).
Locality: Qena Governorate, Upper Egypt.
Prevalence: 5% (5/100)
Sporulation time: 48h
Description (Tables 1 and 2, Fig. 14):
Sporulated oocysts are ovoid, measuring 28.64 μm (27.27 - 30.44 μm) in length, 18.97 μm (18.08 - 20.27 μm) in width. There are two oocyst walls; the outer wall is smooth and interrupted by the micropyle, while the inner wall is flattened or slightly concave. The micropyle is present. The oocyst residuum is spheroidal and composed of many granules, and the polar granule is absent (Figs. 14B and 14D). The sporocyst is fusiform, measuring 13.55 μm (12.68 - 14.48 μm) in length and 7.32 μm (7.07 - 7.79 μm) in width (Figs. 14B and 14D). The Stieda body is small and flat (Fig. 14B) and substieda and parastieda bodies are absent. The sporocyst residuum is compact and composed of rough granules near the sporocyst wall (Figs. 14B and 14D). Sporozoites lay end-to-end, each with a large refractile body at the more rounded end (Figs. 14B and 14D).
Unsporulated oocysts are ovoid, measuring 29.97 μm (29.56 - 30.58 μm) in length and 18.14 μm (17.93 - 18.45 μm) in width, with a conspicuous micropyle (Figs. 14A and 14C). The sporoblast (zygote) is spherical, measuring 15.14 μm (15.04 - 15.36 μm) in length and 16.2 2 μm (15.99 - 16.61 μm) in width (Figs. 14A and 14C).
11. Eimeria piriformis Kotla´n and Pospesch, 1934
Synonymy: Eimeria pyriformis Kotla´n and Pospesch, 1934 lapsus calami; non Eimeria piriforsmis Lubimov, 1934; Eimeria piriformis Marotel and Guilhon, 1941; non Eimeria pellerdyi Prasad, 1960; non Eimeria pellerdyi Coudert, 1977a, b.
Host: Domestic rabbit, Oryctolagus cuniculus (L., 1758) (syn. Lepus cuniculus).
Locality: Qena Governorate, Upper Egypt.
Prevalence: 3% (3/100)
Sporulation time: 40h
Description (Tables 1 and 2, Fig. 15):
Sporulated oocysts are piriform, measuring 23.98 μm (22.2 - 25.12 μm) in length and 18.25 μm (17.93 -18.51 μm) in width. There are two smooth oocyst walls and the outer wall is thickened around the micropyle. The micropyle is prominent, located at the narrow end of the oocyst and surrounded by the thickened outer wall. The oocyst residuum and polar granule are absent (Figs. 15B and 15D). Sporocysts are ovoidal to spindle-shaped, measuring 10.54 μm (10.4 - 10.71 μm) in length and 6.42 μm (6.15 - 6.66 μm) in width (Figs. 15B and 15D). The Stieda body is apparently present at the pointed end of the sporocyst (Fig. 15B) and substieda and parastied bodies are absent. The sporocyst residuum is granular and usually located in the center of the sporocyst (Figs. 15B and 15D). Sporozoites are elongate, lay head-to-tail in the sporocyst, each with one end being wider than the other and with one clear refractile body at the wider end (Figs. 15B and 15D).
Unsporulated oocysts are piriform, measuring 25.68 μm (24.35 - 26.83 μm) in length and 20.12 μm (18.58 - 21.13 μm) in width, with a conspicuous micropyle (Figs. 15A and 15C). The sporoblast (zygote) is spherical, measuring 15.44 μm (14.32 - 16.14 μm) in length and 13.87 μm (13.05 - 14.53 μm) in width (Figs. 15A and 15C).
A Key to Eimeria spp. infecting domestic rabbits:
1- Oocysts piriform …………………………………………….….…………… 2
Oocysts ovoid or ellipsoid .…………………….………................................. 3
Oocysts spherical or cylindrical ……………………………..………………... 7
2- Oocyst residuum present.................................................................. E. intestinalis
Oocyst residuum absent……..……………………………………. E. piriformis
3- Oocysts ovoid ………………………………………………………………… 4
Oocysts ellipsoid ………………………………………………...................... 6
4- With micropyle and oocyst residuum; collar-like thickening of outer wall layer around micropyle…………………...…………………..…………… E. magna
With normal micropyle and oocyst residuum……………………… E. vejdovesky
With micropyle and without oocyst residuum ………..………………………. 5
5- With prominent micropyle ……………..………………………….. E. flavescens
With smooth micropyle, sometimes inapparent................................ E. stiedae
6- No apparent micropyle; with variable oocyst residuum, spherical, triangular or composed of a chain of granules..............................................……E.perforans
With micropyle and spherical oocyst residuum ……………. …….. E. media
With conspicuous micropyle and without oocyst residuum………. E. irresidua
7- Oocyst spherical, micropyle and oocyst residuum absent …………………………………………..………………………… E. exigua
Oocyst cylindrical, well-pronounced micropyle and rounded oocyst residuum ………………………………………………………………………… E. coecicola