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The Coccidian Parasites (Protozoa.
Sporozoa) of Ruminants
ORMAN D. LEVINE and VIRGINIA IVENS
44
UNIVERSITY OF ILLINOIS PRESS
ILLINOIS BIOLOGICAL MONOGRAPHS
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The Coccidian Parasites (Protozoa, Sporozoa)
of Ruminants
~>
The Coccidian Parasites (Protozoa,
Sporozoa) of Ruminants
NORMAN D. LEVINE and VIRGINIA IYENS
ILLINOIS BIOLOGICAL MONOGRAPHS 44
UNIVERSITY OF ILLINOIS PRESS URBANA, CHICAGO, AND LONDON 1970
Board of Editors-. James E. Heath, Tom L. Phillips, Willard W. Payne, Richard B. Selander,
and Philip W. Smith.
This monograph is a contribution from the College of Veterinary Medicine and the Agricul-
tural Experiment Station, University of Illinois. Issued November, 1970. Supported in part
by National Science Foundation Grants GB-5667x and GB-14096.
© 1970 by the Board of Trustees of the University of Illinois. Manufactured in the United
States of America. Library of Congress Catalog Card No. 76-630118.
252 00114 1
\
CONTENTS
INTRODUCTION 1
GENUS EIMERIA SCHNEIDER, 1875 3
GENUS ISOSPORA SCHNEIDER, 1881 136
GENUS WENYONELLA HOARE, 1933 141
DISCUSSION 143
SUMMARY 147
LITERATURE CITED 149
TABLES 165
PLATES 195
ADDENDUM 269
INDEX 273
INTRODUCTION
Coccidia are among the commonest parasites of ruminants, and
coccidiosis is an important disease of domestic sheep, cattle, and goats.
The great majority of ruminant coccidia belong to the genus Eimeria,
while a few belong to the genus Isospora. However, the literature on
these coccidia is scattered and some papers have not been carefully
evaluated. Of the two recent reviews of coccidia, Davies, Joyner and
Kendall (1963) devoted 34 pages and Pellerdy (1965) 68 pages to
those of ruminants. Kheisin (Cheissin) (1967) discussed those in
domestic ruminants briefly, and Pout (1969) reviewed coccidiosis of
sheep. Neither included all the species given in this monograph, and
none discussed them all completely.
Often in the past, authors who found coccidia in wild ruminants
have simply assigned them to species known in domestic ruminants;
this practice is not acceptable. Cross-infections experiments (Table
12) indicate that coccidia are rarely transmissible from one host genus
to another, even though they may look very much alike. An organism
that will not infect a given host is not a parasite of that host. Con-
sequently, it should not be given the same name as an organism
occurring in another host genus without proof of cross-infcctibility. This
principle has been followed wherever feasible in the present mono-
graph. The coccidia of sheep and goats {Ovis and Cnjtnt) and those
J THE COCCIDIAX PARASITES OF RUMINANTS
of cattle and water buffaloes {Bos and Bubalus) are exceptions; in
most cases the state of our knowledge does not permit clear-cut sepa-
ration, at least at this time.
The present monograph gives a critical analysis of the cocciclia of
all ruminants, both wild and domestic. The known information on
all species is assembled, so that this work should serve as a reference
point for future studies on coccidia of ruminants.
The taxonomy, life cycle, oocyst structure, criteria for separation of
coccidian species, and their general pathogenicity have been described
by Levine and Ivens (1965), and there is no need to repeat this in-
formation here.
The genera of coccidia arc taken up separately below. Within each
protozoan genus, the species are arranged according to host genus. The
ruminant classification used is primarily that of Simpson (1945), with
some of the modifications introduced by Frechkop (1955). At the
end of the monograph, the principal structural characteristics of the
oocysts of each species are tabulated.
GENUS EIMERIA SCHNEIDER, 1875
This genus is characterized by the presence of four sporocysts, each
containing two sporozoites, in each oocyst, The synonymy of this
genus has been given by Pellerdy (1963) .
Host Suborder RUMINANTIA
Host Superfamily TYLOPODA
Host Family CAMELIDAE
Eimeria cameli (Henry and Masson, 1932)
Reichenow, 1952
(Plate 1, Figs. 1 and 2; Plate 2, Figs. 5-8; Plate 3, Figs. 9-12)
Globidium cameli Henry and Masson, 1932a of Enigk, 1934.
Eimeria (Globidium) cameli (Henry and Masson, 1932a) Reiche-
now, 1952 of Abdussalam and Rauf, 1957.
Eimeria kazachstanica Tsygankov, 1950.
Eimeria casahstanica [sic] Zigankoff, 1950 of Pellerdy, 1965.
Eimeria noelleri (Henry and Masson, 1932) Pellerdy, 1956 of Dubey
and Pande, 1964.
[non] Eimeria cameli Noller, 1933 of Iwanoff-Gobzcm, 1934; of
Yakimoff and Matschoulsky, 1939; and of Tsygankov, 1950.
4 THE COCCIDIAX PARASITES OF RUMINANTS
[non] Eimeria (?) nolleri Rastegaieff, 1930.
Description. This species was described briefly by Henry and
Masson 1 1932a I and redescribed and named by the same authors
(19321), 1932c). They found it in a dromedary which died in Alfort,
France, in 1931. They first found the parasite in scrapings from the
mucosa and then in sections of the posterior ileum. Oocysts truncate
ovoid, 81-100 by 63-94 ,. t , with a wall 10.4-15.6 /<. thick. Micropyle
10-14 fx wide at the narrow end of the oocyst, covered by a clear part
of the wall which does not form a cap. Oocyst wall apparently com-
posed of 2 layers lined by a membrane. (Enigk, 1934, saw 3 layers.)
Oocyst wall colorless at first, then becoming brown and so opaque that
the development of its contents cannot be followed. Henry and Masson
saw no sporulated oocysts and were unable to produce sporulation.
The oocysts described by Tsygankov ( 1950) under the name Eimeria
kazachstanica were piriform, 75-95 by 55-70 /j. with a mean of 87.3
by 64.0 ,"., with a prominent micropyle 10-17.5 ,u in inside diameter at
the small end, with a yellow-green or dark brown, smooth, 3-layered
wall 5-9 ix thick, the outer layer being transparent, the middle one
yellow-green or dark brown, and the inner one dark green. Tsygankov
followed oocyst sporulation. Oocyst residuum absent, oocyst polar
granule present or absent, sporocysts elongate, pointed at both ends,
without Stieda body, 40-50 by 14.5-20 /* with a mean of 45 by 18 /t.
Sporocyst residuum present, composed of scattered granules and de-
scribed as containing 2 inclusion bodies. Sporozoites described as
sausage-shaped, 13-14.5 by 6-7 /x. However, we suspect that the struc-
tures which Tsygankov thought were sporozoites were actually clear
globules at one end of each sporozoite, that the structures which he de-
scribed as inclusion bodies 3.75-5 /.<. in diameter were actually the sporo-
zoite nuclei, and that he failed to see the sporozoites themselves.
Dubey and Pande (1964) found a single oocyst 67 by 57 n in a
dromedary calf in India.
Sporulation Time. According to Tsygankov (1950), sporulation of
E. kazachstanica took 10-15 days at 16-20 C.
Schizogony and Gametogony. Henry and Masson (1932b) found
spherical or ellipsoidal structures up to 350 /x in diameter in the
mucosa of the small intestine which they considered to be schizonts.
They had a simple, lamellar outer membrane which was usually very
thin, so thin that the largest schizonts were somewhat irregular in
shape; in some cases a host cell nucleus up to 50 /.«. long was present
and the membrane was thickened. The contents of these structures
were of 2 types. Most often they consisted of very fine granules whose
nature was hard to determine. In other cases there were spherules
genus Eimeria Schneider, 1875 5
(blastophores) 20-23 n in diameter distributed in the contents; these
spherules stained strongly and were surrounded by a colorless, re-
tractile zone. The second type they considered to be microgametocytes
because smears from them contained cells believed to be microgametes
which were about 6 n long and 0.5 /x wide.
Enigk (1934) found schizonts and microgametocytes up to 200 by
150 jx with a wall less than 1 /x thick. The earliest stages could not be
differentiated. Cells with 4-8 nuclei were seldom found, and cells 14 /jl
in diameter already had 12 nuclei 1.5-2.0 /x in diameter. After further
multiplication, the nuclei lay in rings or bands and formed so-called
blastophores. These blastophores coalesced in part so that there re-
mained in many cysts only a few large irregularly shaped blastophores.
At this stage the microgametocytes and schizonts could be differenti-
ated. The nuclei of each blastophore were squarish, 1 /x long, and ar-
ranged around the periphery of a central residual mass. Merozoites 2 ji
long then formed; they were elongate, with a blunt end and a pointed
one. In the microgametocytes the blastophores did not coalesce so
much; they were generally small, had uniformly staining micro-
gametes 3.0-3.5 /x long around their periphery, and had a central
residual mass. Mature microgametocytes were much more numerous
than mature schizonts.
Enigk (1934) found macrogametes in the ileum beginning 3 m be-
hind the pylorus ; their number decreased markedly near the large in-
testine; there were a few in the cecum, but none in the colon. The
youngest stages were in the epithelial cells at the base of the glands.
They were 4-5 /± in diameter, with nuclei 2 /x in diameter; a nucleolus
was present. The infected epithelial cells were markedly enlarged and
22-28 jx in diameter; their nuclei were flattened and lay against the par-
asites. As the infected cells grew, they migrated out of the epithelial
layer and finally lay beneath the epithelium in the tunica propria.
They formed a wall not more than 3 /x thick. The host cell nuclei en-
larged markedly after the cells left the epithelial layer, and 2-8 nu-
cleoli could be found in a single section. The macrogametes began to
differentiate when they reached a diameter of 12 /x. Their cytoplasm
became vacuolated and later eosinophilic, a second nucleolus formed in
the nucleus (which was now 4 /x in diameter) , spheres staining golden
yellow with iron hematoxylin formed in the outer zone, and outside
them strongly eosinophilic granules formed. The spheres coalesced, and,
when the parasite was 45 x 40 /x, formed a layer on its periphery. Enigk
found few oocysts in the mucosa, and those that he saw were not quite
as large as those seen by Henry and Masson ( 1932a) .
Prepatent Period. Unknown.
6 THE COCCIDIAX PARASITES OF RUMINANTS
Type Host. Camelus dromedarius (dromedary).
Other Hosts. Camelus bactrianus (Bactrian camel).
Location. Small intestine.
Geographic Distribution. USSR (Kazakhstan, Urals), Europe
(France — veterinary school), Pakistan, India (Rajasthan).
Pathogenicity. Henry and Masson (1932a) thought that this species
was pathogenic, producing a toxin, but Enigk ( 1934) found no evidence
of pathogenicity.
Cross-Transmission Studies. None.
Prevalence. Abdussalam and Rauf (1957) found this species in 25%
of 24 C. dromedarius in Pakistan.
Remarks. See Remarks under E. bactriani for an explanation of the
nomenclature of this species.
Eimeria dromedarii Yakimoff and Matschoulsky, 1939
(Plate 1, Figs. 3 and 4)
Eimeria cameli Noller, 1933 pro parte of Iwanoff-Gobzem, 1934
pro parte.
Eimeria cameli Iwanoff-Gobzem of Tsygankov, pro parte.
? Eimeria cameli Jakimov, 1934 of Rysavy, 1954.
Description. Oocysts ovoid; 100 oocysts measured by Yakimoff and
Matschoulsky ( 1939) were 23-33 by 20-25 ,x with a mean of 27.7 by
23.2 j±. One hundred oocysts measured by Dubey and Pancle (1964)
were 26-28 by 21-23 \x with a mode of 27 by 21 \x. Oocyst wall brown,
0.8-1.4 jx thick, "double-contoured" (2-3 \x thick, composed of 2 layers,
according to Dubey and Pande, 1964). Oocyst wall thickened to form
a kind of a "cap" 7-8 \x wide and 2-3 \x high. Yakimoff and Mat-
schoulsky (1939) said, "As the cytoplasm contracts the oocyst mem-
brane is seen to be coloured light pink or yellow." Sporocysts ovoid or
spherical, 8.5-10.5 by 6.5-8.4 /x (10-11 by 8.5 /.«. according to Dubey.
and Pande, 1964), without Stieda bodies, each containing 2 comma-
shaped sporozoites with one or 2 clear globules each. Oocyst and sporo-
cyst residua absent. Oocyst polar granule absent.
Sporulation Time. Fifteen to 17 days at 10-12 G in 2% potassium
bichromate solution.
Schizogony and Gametogony. Unknown.
Prepatent Period. Unknown.
Type Host. Camelus dromedarius (dromedary).
Other Hosts. Camelus bactrianus (Bactrian camel).
Location. Unknown.
genus Eimeria Schneider, 1875 7
Geographic Distribution. USSR (Leningrad Zoo), India (Rajas-
than) , Pakistan.
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Dubey and Pande (1964) found this species in 44%
of 45 dromedary camel calves less than 10 months old in Rajasthan,
India. Abdussalam and Rauf (1957) found it in 4 C / C of 24 C. dromc-
darius in Pakistan.
Remarks. Noller (1933), Iwanoff-Gobzem (1934) and Yakimoff
(1935a) apparently saw some E. dromedarii among the coccidia that
they called E. cameli (a synonym of E. bactriani). Yakimoff and Mat-
schoulsky (1939), however, described E. dromedarii and differentiated
it from E. bactriani. Tsygankov ( 1950) thought they were the same,
but Pellerdy (1965) reaffirmed their difference.
This is probably the species that Rysavy (1954) reported from C.
bactrianus in Czechoslovakia under the name "Eimeria cameli, Jaki-
mov 1934." Rysavy said that its oocysts were broadly ellipsoidal, 23-
32 by 18-25 fi with a mean of 27 by 20 /x, thin-walled, with a micropyle
and micropylar cap, and that its sporocysts were spherical, 8 /x in
diameter, with coarsely granular protoplasm and a small sporocyst
residuum ; its sporulation time was 64 hours.
Eimeria pellerdyi Prasad, 1960 Emend. Pellerdy, 1965
(Plate 4, Fig. 13)
Eimeria pellerdei Prasad, 1960.
Description. Oocysts oval or ellipsoidal, 22.5-24 by 12-13.5 /x with a
smooth, colorless wall composed of 2 layers, without mircopyle. Oocyst
residuum and oocyst polar granule absent. Sporocysts ovoid, 9-10.5 by
4.5-6 (i, with a small Stieda body and a sporocyst residuum. Sporo-
zoites club-shaped, 8-9.5 by 1.5-3 /x, with a central nucleus and a
globule at the large end.
Sporulation Time. According to Prasad ( 1960 ) , complete sporulation
required about 5 days, presumably at room temperature.
Schizogony and Gametogony. Unknown.
Prepatent Period. Unknown.
Type Host. Camelus bactrianus (Bactrian camel).
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. London Zoo.
THE COCCIDIAX PARASITES OF RUMINANTS
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
Eimeria rajasthani Dubey and Pande, 1963
(Plate 4, Figs. 14 and 15)
Description, Oocysts nearly ellipsoidal, 34-39 by 25-27 p with a
mode of 36 by 25 /.<,. Oocyst wall 2-3 /x thick, composed of 2 layers, the
outer one relatively thick and light yellowish green, the inner one
darker, with a shining inner contour. Micropyle not visible but appar-
ently present. Mieropylar cap present, 8-11 \x wide and 2-3 \x high.
Oocyst polar granule absent. Oocyst residuum absent. Sporocysts
almost ovoid, with Stieda body, 14-15 by 8-11 ,u with a mode of 15 by
11 n, Sporocyst residuum present. Sporozoites elongate with one end
broad and the other narrow and pointed, lying lengthwise head to tail
in sporocysts, 10-14 by 3-4 /.<., containing 2 or sometimes more globules.
Sporulation Time, According to Dubey and Pande (1963, 1964),
sporulation took about a week at room temperature.
Schizogony and Gametogony. Unknown.
Prepotent Period, Unknown.
Type Host. Camelus dromedarius (dromedary).
Other Hosts. None.
Location. Oocysts in feces.
Geographic Distribution. India.
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Dubey and Pande (1963) found this species in 62% of
45 camel calves less than 10 months old in Rajasthan, India.
Eimeria bactriani n. sp.
( Plate 4, Figs. 16-191
Eimeria cameli Noller, 1933.
Eimeria cameli Noller, 1932 emend. Yakimoff and Matschoulsky,
1939 of Pellerdy, 1965.
Eimeria cameli Iwanoff-Gobzem, 1934; Yakimoff, 1935a; Tsygan-
kov, 1950.
? Eimeria nolleri Reichenow, 1953 of Abdussalam and Rauf, 1957.
[non] Eimeria cameli (Henry and Masson, 1932a) Reichenow, 1953.
genus Eimeria Schneider, 1875 9
[rum] Eimeria noelleri (Henry and Masson, 1932a) Pellerdy, 1956.
[non] Globidium cameli Henry and Masson, 1932a.
Description. According to Noller (1933) the oocysts are spherical to
ellipsoidal, about 32 /x long and 25-27 p, wide; micropyle present, but
micropyle cap normally absent (those few oocysts with micropyle caps
which Noller saw were undoubtedly not E. bactriani) ; oocyst re-
siduum absent; oocyst wall light yellowish to yellowish brown; sporo-
cysts about 15-17 /x long and about 10 /x wide. The oocysts described
by Iwanoff-Gobzem (1934) as those of E. cameli were spherical to
short oval, with a double-contoured wall (illustrated as composed of
one layer) , 23-34 by 20-30 n with a mean of 28.3 by 25.5 /x without a
micropyle, with an oocyst polar granule, without an oocyst residuum,
with round or elongate sporocysts 8-9 by 6-9 n, with a sporocyst
residuum and with lemon-shaped sporozoites. Yakimoff (1935) de-
scribed both oval and spherical oocysts, both of which he assigned to
"E. cameli." Later, however, Yakimoff and Matschoulsky (1939) said
that only the spherical oocysts were U E. cameli," the oval ones belong-
ing to their new species E. dromedarii. The spherical oocysts seen by
Yakimoff (1935a) were 21-29 /x in diameter with a mean of 23.5 /.<,;
they were about % as common as the oval ones. Tsygankov (1950)
found oocysts measuring 22.5-30 by 20-27.5 n with a mean of 26 by
23.7 i±; these he said corresponded in structure to Iwanoff-Gobzem's
E. cameli; however, he also found oocysts which he said corresponded
to Yakimoff and Matschoulsky's E. dromedarii, and he said that the
latter was a synonym of the former.
Sporulation Time. Noller (1933) said that sporulation took 10 days
at room temperature. Yakimoff (1935a) said that the oocysts sporu-
lated in 6 clays and Tsygankov ( 1950) that they sporulated in 6-8
days at room temperature or 3 weeks at 10-12 C.
Schizogony and Gametogony. According to Enigk (1934), E. cameli
occurred in the small intestine beginning about 2 m behind the pylorus
and extending into the ileum. The epithelial cells of the villi were in-
vaded. The schizonts were surrounded by a clear zone within the host
cell. The schizonts were 16 by 10 /x and contained 20-24 merozoites each
9 by 2 /x.
The microgametocytes were also in the epithelial cells of the villi
in the small intestine. They reached a diameter of 14 /x or 12 by 19 /x.
They contained several centers of development, each with a residual
body. The mature microgametes were 4 /x long. The mature macro-
gametes were 25 by 20 /x, and were often free in the gut lumen.
Prepatent Period. Unknown.
Type Host. Camclus bactrianus (Bactrian camel).
10 THE COCCIDIAX PARASITES OF RUMINANTS
Other Hosts. Camelus dromedarius (dromedary).
Location. Small intestine, beginning about 2 m behind the pylorus
and extending into the ileum.
Geographic Distribution. USSR.
Pathogen icity . Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown. This species is apparently quite common,
but the information given by Yakimoff (1935a) and Tsygankov (1950)
is for a combination of this species and E. dromedarii.
Remarks. This species was first reported by Noller (1933) as
E. cameli in Bactrian camels from a group brought into Germany from
the Urals. Iwanoff-Gobzem (1934) , Yakimoff (1935a) and Tsygankov
( 1950) found the same species in Bactrian camels and dromedaries in
various parts of the USSR. Enigk (1934) also found it in a Bactrian
camel brought into Germany from the Urals. However, this form was
not the same as the "Globidium" cameli described by Henry and
Masson (1932a) from a dromedary in France. Since Globidium is now
accepted as a synonym of Eimeria (see Reichenow, 1952) , we are faced
with two different species of Eimeria, both assigned to the species
cameli. Pellerdy (1965) attempted to rectify the situation by calling-
Henry and Masson's (1932a) species E. noelleri; however, since these
authors used the name cameli first, their name takes precedence.
Hence, E. noelleri falls as a synonym of E. cameli (Henry and Masson,
1932a ) . The next problem is to determine the correct name for the
"#. cameli" of Noller (1933) and Iwanoff-Gobzem (1934). Pellerdy
( 1965) retained the name Eimeria cameli Noller, 1932 emend. Yaki-
moff and Matschoulsky, 1939 but this action cannot stand. We are
therefore proposing a new name, Eimeria bactriani n. sp., for it.
This is probably the species reported by Abclussalam and Rauf
( 1957) under the name ki E. nolleri Reichenow 1953" from 127c of 24
C. dromedarius in Pakistan.
\
Eimeria peruviana Yakimoff, 1934
(Plate 6, Fig. 31)
Description. Oocysts described as oval and illustrated as ellipsoidal,
28-37.5 by 18-22.5 /* with a mean of 31.8 by 19.3 S x. Micropyle absent.
Oocyst wall stated to have a double membrane but illustrated with a
single-layered wall. Oocyst polar granule absent. Oocyst residuum
present. Sporocysts illustrated as more or less ellipsoidal, without
Stiecla body, 10.5-15 by 7.5 /x. Sporocyst illustrated with granules
within the sporozoites which might or might not have been sporocyst
genus Eimeria Schneider, 1875 11
residual granules. Sporozoites elongate, illustrated as lying lengthwise
in sporocysts.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepatent Period. Unknown.
Type Host. Lama g la ma (llama).
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. USSR (presumably in a zoo) .
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Yakimoff (1934) found this species in 1 of 5 llamas.
Eimeria alpacae Guerrero, 1967
(Plate 5, Fig. 21)
Description. Oocysts ellipsoidal, rarely ovoid, 22-26 by 18-21 p. with
a mean of 24.1 by 19.6 /.<.. Oocyst wall smooth, composed of 2 layers
with a total thickness of 1.2-1.6 /x with a mean of 1.45 /.<,; outer layer
1.1 ji thick, very pale greenish to bluish; inner layer 0.4 /x thick, appear-
ing as a dark yellow line, rarely somewhat wrinkled at the micropylar
end. Micropyle present. Micropylar cap present, colorless to pale
greenish, 0.7-1.3 jx high and 4.4-7.5 p. wide with a mean of 1.0 by 5.7 jx.
Oocyst polar granule present or absent; 1-3 polar granules seen in 31%
of 55 oocysts. Oocyst residuum absent, Sporocysts ovoid, rounded
at both ends, with one end broader than the other, 10-13 by 7-8 /.<. with
a mean of 11.0 by 6.8 /<,. Stieda body very faintly perceptible. Sporo-
cyst wall about 0.2 /x thick. Sporocyst residuum present, usually con-
sisting of a few granules forming a compact mass about 1.4 \x in diam-
eter. Sporozoites elongate, with one end narrower than the other, lying
lengthwise head to tail in sporocysts. Sporozoites with 1-3 clear
globules.
Sporulation Time. Unknown.
Schizogony and Gametogony . Unknown.
Prepatent Period. Unknown.
Type Host. Lamapacos (alpaca).
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. South America (Peru).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
12 THE COCCIDIAN PARASITES OF RUMINANTS
Prevalence. Guerrero (1967) found this species in 9 of 12 alpacas
from Peru.
Eimeria lamac Guerrero, 1967
(Plate 5, Fig. 20)
Description. Oocysts ellipsoidal, occasionally ovoid, slightly flat-
tened at micropylar end, which is sometimes the smaller one. Oocyst
wall smooth, composed of 2 layers 1.4-1.8 /x in total thickness with a
mean of 1.7 \x\ outer layer 1.3 /x thick, bluish to greenish yellow; inner
layer 0.5 fi thick, brownish-yellow, sometimes somewhat wrinkled at
micropylar end. Sporulated oocysts 30-40 by 21-30 /x with a mean of
35.6 by 24.5 >x. Micropyle present. Micropylar cap prominent, dome-
shaped, colorless to light grayish, 1.5-2.2 /x high and 9-11 fi wide with
a mean of 1.8 by 9.9 /.<,. Oocyst polar granule present or absent; one
or more seen in 26% of 70 sporulated oocysts. Oocyst residuum absent.
Sporocysts elongate ovoid, rounded at both ends, with one end broader
than the other, with a Stieda body and a wall about 0.25 (i thick.
Sporocysts 13-16 by 8-10 /x with a mean of 15.2 by 8.5 /x. Sporocyst
residuum usually consisting of a few granules forming a compact mass
about 2 ix in diameter. Sporozoites elongate, with one end narrower
than the other, lying lengthwise head to tail in sporocysts. Sporozoites
with 1-3 clear globules.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Pre patent Period. Unknown.
Type Host. Lama pacos (alpaca).
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. South America (Peru).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Guerrero ( 1967) found this species in 3 out of 12 alpacas
from Peru.
Eimeria punoensis Guerrero, 1967
(Plate 5, Fig. 22)
Description. Oocysts ellipsoidal, occasionally ovoid (when ovoid,
slightly broader at microplyar end), 17-22 by 14-18 /x with a mean of
19.9 by 16.4 . wide at small end. Oocysts 26-35 by 19-25 /x
with a mean of 31 by 22 ,.l 124-31 by 15-21 p with a mean of 28 by
19 y. according to Bhatia et al. 1968). Oocyst wall smooth, homo-
geneous, yellowish to darkish brown, about 1 /i thick except at the mi-
cropylar end where it is thinner, lined by a membrane. (Two layers 1.3
/-. thick according to Bhatia et al., 1968.) A few granules composing a
"tenue body"* lie beneath the micropyle in sporulated and unsporulated
oocysts according to Bhatia et al. (1968). Oocyst residuum present
in a few oocysts as a small, irregular mass consisting of 3-4 globules
just below the micropyle. Oocyst polar granule absent. Sporocysts
lemon-shaped (i.e., broadly ovoid with one end narrower than the
other) , with a Stieda body at the smaller end, with a mean of 18 by
8 fi 1 15-18 by 7-9 ti with a mean of 17 by 7 /i according to Bhatia
et ah, 1968). Sporocyst residuum present, a distinct spherical mass
of 5-9 loosely grouped refractile granules in the center of the sporocysts
(becoming scattered and scantier with age). Sporozoites banana-
shaped, about 10 by 4 /_<., each with a refractile spherical globule about
4 /.(, in diameter at its large end and sometimes one or 2 smaller globules
1-2 /x in diameter. Nucleus central, discernible with phase contrast
microscope.
Sporidation Time. Three to 4 days in water or 2% potassium bichro-
mate solution at 29 G.
Schizogony and Gametogony. Unknown.
Pre patent Period. Unknown.
Type Host. Bubalus bubalis Ovater buffalo).
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. India (Bareilly, Izatnagar, Nagla, Uttar
Pradesh).
Pathogenicity. Gill, Chhabra and Lall (1963) observed heavy dis-
charges of oocysts without clinical symptoms. They found as many as
1.9 million oocysts per gram of feces in buffalo calves and fewer in
adult animals.
Cross-Transmission Studies. None.
Prevalence. Bhatia et al. (1968) found this species in b c /c of 305
water buffaloes in Mathura, Uttar Pradesh, India.
Remarks. It is possible that the form reported by Abdussalam and
Rauf ( 1956 ) from a water buffalo calf in Pakistan may have been
this species. They said that the oocysts were typically piriform, 29-33
* ''Tenue" means simply "small" in Portuguese; Bhatia et al. got this term from
the paper by Torres and Ramos (1939).
genus Eimeria Schneider, 1875 45
by 19-23 fi with a mean of 30 by 21 fi, with a homogeneous pinkish
brown wall, without a distinct micropyle but apparently with a nar-
row opening in some specimens, and with sporocysts 15-16 by 6-8 /j.;
the sporulation time was apparently more than 4 days. The infected
calf had dirty white offensive diarrhea, emaciation, dullness and con-
gestion of the mucous membranes; it went into a coma and died. They
thought that this form resembled E. bovis but might be a new species.
Yasin and Abdussalam (1958) used the name E. bubalis for what was
presumably this coccidium. However, they credited it to Abdussalam
and Rauf (1956), and we have been unable to find any paper in which
these latter authors used the name.
Eimeria ankarensis Sayin, 1969
(Plate 63, Figs. 282-283)
Description. Oocysts elongate ovoid, 32-43 by 25-29 /x with a mean
of 39 by 26 (i. Oocyst wall yellowish brown, composed of 2 layers
3.0-3.5 jx thick and lined by a membrane. Outer layer thick, rough,
inner layer very thick, dark brown. Micropyle 6 /x in diameter at small
end, not covered by outer layer of wall. Oocyst polar granule and
oocyst residuum absent. Sporocysts elongate, almost ellipsoidal, 18-23
by 8-10 ji with a mean of 21 by 9 /x, with Stieda body and sporocyst
residuum. Sporozoites elongate, rather comma-shaped, lying length-
wise head to tail in sporocysts, with two retractile globules each.
Sporulation Time. Three to 4 days at room temperature according
to Sayin (1969).
Prepotent Period. Unknown.
Type Host. Bubalus bubalis (water buffalo) .
Other Hosts. None.
Location. Unknown. Oocysts found in feces.
Geographic Distribution. Turkey.
Pathogenicity. Unknown.
Cross-Transmission Studies. Sayin (1969) was unable to transmit
tins species to the ox by feeding 3 week-old calves 50 sporulated
oocysts each.
Prevalence. Sayin (1969) found this species in 10% of 124 water
buffaloes in Turkey.
Remarks. Sayin (1969) said that E. ankarensis might be confused
with E. thianethi, E. bukidnonensis , E. wyomingensis and E. pcllita,
but differentiated it from them. It might also be confused with E.
46 THE COCCIDIAX PARASITES OF RUMINANTS
auburnensis, but differs in the character of its wall and micropyle; in
addition, Savin recognized E. auburnensis and distinguished between
the two forms.
Eimeria suernii (Rivolta, 1878) Martin, 1909
(Plate 11, Figs. 71-76; Plate 62, Fig. 280)
Cytospermium zurnii Rivolta, 1878.
Eimeria bovis (Ziiblin, 1908) Fiebiger, 1912 {pro parte).
Eimeria canadensis Bruce, 1921 (pro parte).
Eimeria zuerni (Rivolta, 1878) Martin, 1909 of Pellerdy, 1965.
Description. Oocysts subspherical, subovoid, ovoid or sometimes
ellipsoidal. Oocyst wall smooth, colorless, composed of a single layer
about 0.7 fjL thick (except a little thinner at the small end if there is
one) (oocyst wall in water buffalo composed of 2 layers 1.5 ju, thick
according to Bhatia et ah, 1968). Micropyle absent. Oocysts 12-29 by
10-21 ju, with means of 17-20 by 14-17 /a. Oocyst residuum absent. One
or more oocyst polar granules may or may not be present; if present,
sometimes shattered. Sporocysts elongate ovoid, with a tiny Stieda
body, 7-13 by 4-7 /x with a mean of 9-11 by 5 /x. Sporocyst residuum
present or absent; when present, composed of scattered or rather small
granules or occasionally a small, compact mass. Sporozoites elongate,
head to tail in sporocysts, with a clear globule at the large end and a
nucleus sometimes visible near the center. Free sporozoites 8-10 by
2-3 //. with a mean of 9 by 2 fi (Nyberg and Hammond, 1965) (see
figure by Christensen, 1941).
Sporulation Time. According to Marquardt, Senger and Seghetti
(I960), complete sporulation occurs in 9-10 days at 12 C, 6 days at
15 C, 3 clays at 20 C, 40 hours at 25 C and 23-24 hours at 30-32.5 C;
a few oocysts may sporulate at temperatures as low as 8 C in several
months, but sporulation is not normal above 32 C. According to Lee
and Armour (1959), complete sporulation occurs in 48-72 hours at 27
C; Svanbaev (1967a) found that it was 2-3 days at 25-28 C.
Schizogony and Gametogony. Davis and Bowman (1957) described
the endogenous stages. Schizonts are found 2-19 days after experi-
mental infection in the epithelial cells of the upper, middle and lower
small intestine, cecum and colon. When mature they are about 10 by
13 p. and contain 24-36 merozoites. They lie distal to the host cell nu-
cleus. Merozoites are first seen 7 days after infection. They are about
5 by 12 /x, have a nucleus near the tapering end and contain 2 refractile
globules. Davis and Bowman did not determine the number of asexual
genus Eimeria Schneider, 1S75 47
generations, but believed that there is more than one. The mature
schizonts late in the cycle are slightly larger than the early ones.
Macrogametes are first seen 12 days after infection. They occur in
the epithelial cells of the glands and are to a lesser extent on the sur-
face of the lower small intestine, cecum, colon and rectum, ami rarely
in the upper small intestine. They are about 11 by 14 /.<, and contain
one or 2 rows of plastic granules. Microgametocytes are first seen 15
days after infection in the same location as the macrogametes. They
are about 10 by 14 /.<. when mature. Immature oocysts are first seen
12 days after infection. According to Svanbaev (1967a), the patent
period is about 11 days.
Pre-patent Period. About 17 days (Pellerdy, 1965) or 15 days (Svan-
baev, 1967a).
Type Host. Bos taurus (ox).
Other Hosts. Bos indicus (zebu), Bubalus bubalis (water buffalo,
carabao) . Other authors have reported this species from the wisent,
white-tailed deer, roe deer and elk, but without descriptions ; they were
probably dealing with another species.
Location. Schizonts and merozoites in epithelial cells of small in-
testine, cecum and colon. Gamonts in epithelial cells of lower small
intestine, cecum, colon and rectum, rarely in upper small intestine.
Geographic Distribution. Worldwide.
Pathogenicity. E. zuernii is the most pathogenic coccidium of cattle.
In acute infections it causes a bloody diarrhea of calves. At first the
feces are streaked with blood. The diarrhea becomes more severe;
bloody fluid, clots of blood and liquid feces are passed; and straining
and coughing may cause this mixture to spurt out as much as 2-3 m.
The animal's rear quarters may look as though they had been smeared
with red paint. Anemia, weakness and emaciation accompany the
dysentery, and secondary infections, especially pneumonia, are com-
mon. This acute phase may continue for 3 or 4 days. If the calf does
not die in 7-10 days, it will probably recover.
E. zuerniim&y also be associated with a more chronic type of disease.
Diarrhea is present, but there may be little or no blood in the feces.
The animals are emaciated, dehydrated, weak and listless, with rough
hair coats, drooping ears and sunken eyes.
The lesions of coccidiosis were described by Boughton (1945) and
Davis and Bowman (1952) among others. A generalized catarrhal
enteritis involving both the small and large intestines is present. The
lower small intestine, cecum and colon may be filled with semifluid,
bloody material. Large or small areas of intestinal mucosa may be
eroded and destroyed, and the mucous membrane may be thickened,
4S THE COCCIDIAN PARASITES OF RUMINANTS
with irregular whitish ridges in the large intestine or smooth, dull gray
areas in the small intestine or cecum. Diffuse hemorrhages are present
in the intestines in acute cases, and petechial hemorrhages in mild ones.
Cross-Transmission Studies. Savin (1969) claimed to have infected
3-week-old calves {Bos taurus) with E. zuernii from the water buffalo.
Prevalence. Boughton (1945) found this species in 42% of 2,492
bovine fecal samples in the southeastern United States; Hasche and
Todd (1959a) in 26% of 355 cattle in "Wisconsin; Szanto, Mohan and
Levine (1964) in 37% of 795 beef calves in Illinois; Nyberg, Heifer
and Knapp (1967) in 23% of 86 cattle in Oregon; Jacobson and Wor-
ley ( 1969) in 6% of 486 calves and 5% of 479 adult cattle in Montana;
Torres and Ramos (1939) in 38% of 146 cattle in Brazil; Ruiz (1959)
in 1% of 100 adult cattle in Costa Rica. Ruiz and Ortiz (1961) in 2%
of 100 calves in Costa Rica; Balconi (1963) in 25% of 100 adult cattle
in Guatemala; Supperer (1952) in 11% of 130 cattle in Austria; Patyk
(1965) in 16% of 341 calves in Poland; Chroust (1964) in 83% of 77
cattle in Czechoslovakia; Joyner et al. (1966) in 64% of 110 cattle in
England; Yakimoff, Gousseff and Rastegaieff (1932a) in 13% of 126
oxen in Uzbekistan; Marchenko (1937) in 20% of 137 cattle in North
Caucasus; Yakimoff (1933a) in 18% of 41 oxen, 6% of 17 zebus and
37% of 30 water buffaloes in Azerbaidzhan; Savin (1969) in 49% of
124 water buffaloes in Turkey; Vassiliades (1969) in 38% of the cattle
he examined in Senegal; Tubangui (1931) in 11% of 28 zebus and 9%
of 11 carabaos in the Philippines; Patnaik (1965) in 36% of 136 water
buffaloes at Agra, India; and Watanabe and Iwata (1956) in 3% of
454 cattle in Japan. Svanbaev (1967a) found it in a calf as early as
15 days after birth; he found it in 30% of 781 cattle 2 months to more
than a year old in Kazakhstan. Bhatia et al. (1968) found it in 16%
of 305 water buffaloes in Mathura, Uttar Pradesh, India.
Remarks. The proper way to spell this name has been discussed by
Levine and Ivens ( 1967) .
Eimeria bovis (Ziiblin, 1908) Fiebiger, 1912
(Plate 12. Figs. 77-81; Plate 13, Figs. 82-92; Plate 14, Figs. 93-96;
Plate 15, Figs. 97-102; Plate 16, Figs. 103-106; Plate 17, Figs. 107-
108; Plate 18, Figs. 109-110; Plate 19. Figs. 111-112; Plate 20, Fig.
113; Plate 21, Fig. 114; Plate 22, Fig. 115; Plate 23, Figs. 116-117;
Plate 24, Fig. 118; Plate 25, Fig. 119; Plate 26, Fig. 120; Plate 27,
Fig. 121; Plate 28, Fig. 122; Plate 29, Figs. 123-126; Plate 62, Fig.
276i
genus Eimeria Schneider, 1875 49
Coccidium bovis Ziiblin, 1908.
Eimeria canadensis Bruce, 1921 (pro parte) .
Eimeria smithi Yakimoff and Galouzo, 1927.
Eimeria (Globidium) bovis (Ziiblin, 1908) Reichenow, 1953.
Eimeria aareyi Rao and Bhatavdekar, 1959.
? Globidium fusiformis Hassan, 1935.
Description. Oocysts ovoid (described by Christensen, 1941, as
typically stoutly ovoid and somewhat blunted across the narrow end,
but varying considerably in shape, especially in heavy infections;
subellipsoidal, asymmetrical and elongated, tapering oocysts also
occur), 23-34 by 17-23 p with a mean of about 27-29 by 20-21 ,x
(oocysts in water buffalo 23-43 by 15-26 \x with a mean of 28 by 21 ,u
according to Bhatia et al., 1968). Oocyst wall smooth (rarely rough-
ened), composed of 2 layers, the outer one colorless and about 1.3 \x
thick and the inner one brownish yellow and about 0.4 /x thick (Levine
and Ivens, 1967). Micropyle present at small end, inconspicuous.
Oocyst polar granule absent. Oocyst residuum absent. Sporocysts
elongate ovoid, 13-18 by 5-8 fx with a mean of 15-16 by 7 /x (10-14 by
7-9 jx with a mean of 12 by 8 /x according to Svanbaev, 1967a). Stieda
body present, inconspicuous. Sporocyst residuum present. Sporozoites
elongate, with one end smaller than the other, lying lengthwise head to
tail in sporocysts, usually with one pale globule at each end and often
with the nucleus visible near the center. (See figures by Hammond,
1964 and Nyberg and Hammond, 1965) .
Sporulation Time. Two to 3 days in water or 2.5% potassium bichro-
mate solution at room temperature.
Schizogony and Gametogony. There are 2 asexual and 1 sexual
endogenous stages in the life cycle of E. bovis. Hammond et al. (1946)
described the first asexual stage in detail. The sporozoites invade the
endothelial cells of the lacteals in the villi of the posterior half of the
small intestine. These cells become detached from the lacteal lining
and lie free and greatly swollen in the lumen of the lacteals. The schi-
zonts are first found 5 days after infection. They grow to giant size,
becoming mature 14-18 days after infection. A few may still be found
as long as 30 days after inoculation, but most of these are degenerate.
The mature schizonts are 207-435 by 134-267 /x with a mean of 281 by
303 /x and contain 55,000-170,000 (mean, 120,000) merozoites. They
are easily visible to the naked eye as whitish balls, and their presence
was first pointed out by Boughton ( 1942) as a macroscopic lesion which
could be used in diagnosing coccidiosis. Sheffield and Hammond 1 1966)
found that the cyst (host cell) has microvilli on its outer surface.
50 THE COCCIDIAN PARASITES OF RUMINANTS
The first generation merozoites have been studied in detail by Ham-
mond and Ernst (1964) and Hammond, Ernst and Goldman (1965)
after staining by conventional methods. Living merozoites are 11-16
by 1-2 /i with a mean of 13.5 by 1.4 /x. They move by flexing or gliding.
Tn protargol preparations they have a cap-like covering with a terminal
pore at the anterior end and a median rodlike structure extending
back into the body. They also have prominent granules in the posterior
2 :'; of the body, with one characteristically at the posterior end; similar
granules have not been seen in the merozoites of other species of
Eimeria. The nucleus is in the posterior third of the body. Its chroma-
tin is arranged in about 3-5 coarse clumps around the periphery of the
nucleus. There are numerous small glycogen granules in the posterior
% of the body, but no sudanophilic lipids. The merozoites have a
strongly argyrophilic anterior ring, long fibrils and a rodlike structure
extending posteriorly from the region of the ring, and a strongly
argyrophilic posterior granule.
Sheffield and Hammond (1966) studied the fine structure of the
first generation merozoites. Approximately 22 subpellicular fibrils ex-
tend back from the polar ring. Within the polar ring is a conoid con-
sisting of one or more fibrils wound in a tight helix. Two rhoptries (a
term introduced by Senaud, 1964, for the paired organelles) extend
backward through the conoid from the anterior end; each is club-
shaped, with a narrow neck in the conoid region and a wider posterior
part. A median rod parallels the necks of the rhoptries. Numerous
ovoid glycogen bodies about 0.4 by 0.2 /x are concentrated in the cen-
tral third of the merozoite. The region between them and the conoid
is tightly packed with many tortuous structures with indistinct bor-
ders (i.e., micronemes, a term introduced by Jacobs, 1967). Scattered
among them are numerous ribosomes and one or 2 mitochondria. There
may also be a dense, membrane-enclosed body, possibly a lysosome,
near the mitochondria. The Golgi apparatus lies next to the flattened
anterior end of the nucleus. There may be a micropore at the level of
the Golgi apparatus. There are several cisternae of rough-surfaced
endoplasmic reticulum anterior and posterior to the nucleus.
Sheffield and Hammond (1967) studied the fine structure of the
development of the first generation merozoites. At first, the schizont
cytoplasm is subdivided into many lobes or spheroidal blastophores.
Their peripheries are lined by many nuclei resulting from repeated di-
visions. A complex of structures which later comprise the merozoite
anterior end is then formed in the cytoplasm of each future merozoite.
A thickened layer forms under the plasma membrane; it eventually
becomes the inner membrane of the merozoite. There is a central open-
genus Eimeria Schneider, 1875 51
ing in this layer, and adjacent to it lies a conoid. Subpellicular fibrils
radiate from the opening; they are closely applied to the inner mem-
brane. The blastophore membrane is then elevated into a cone-shaped
projection which later elongates into a finger-like bud, which is the
developing merozoite. This bud contains the primordia of the rhoptries,
a nucleus, Golgi apparatus near the nucleus, and other cytoplasmic
structures derived from the blastophore. As the merozoite grows
further, the outer and inner membranes are extended posteriorly, and
the membranes are folded into the blastophore. Later the merozoites
are completely formed but are still attached to the blastophore by their
posterior ends. This attachment is then broken, and free merozoites and
residual bodies are produced.
It was not realized until the work of Hammond, Andersen and
Miner (1963) that there is a second asexual generation in E. bovis. It
occurs in the epithelial cells of the cecum and colon. The mature
schizonts average 9 by 10 /<, in tissue sections and contain 30-36 mero-
zoites averaging 3.5 by 1.2 /a. Living second generation merozoites are
6-7 \x long with a mean of 6.2 \x.
The sexual stages were studied in detail by Hammond et al. (1946).
They generally occur only in the cecum and colon, but in heavy infec-
tions may be found in the terminal 1-1.3 m of the small intestine. They
are found in the epithelial cells of the intestinal glands. The cells at
the base of the glands are invaded first, and later the rest of the gland
becomes involved. The first sexual stages appear 17 days after inocula-
tion. The macrogametes contain plastic granules in their cytoplasm,
there being one layer of small granules near the surface and a less
distinct layer of larger granules beneath it. Hammond et al. (19461
did not see fertilization, but they saw 2 stages in the union of nuclei
before formation of the oocyst wall.
Scholtyseck, Hammond and Ernst (1966) described the fine struc-
ture of the macrogametes. They contain numerous spheroidal to ellip-
soidal or ovoid glycogen inclusions 0.3-1.3 \x in diameter, lipoid bodies,
broadly ellipsoidal dark bodies close to the cell membrane and 0.4-1.6
\x long, and wall-forming bodies about 1.8 /<. long. These last occur
singly or in groups in vacuoles. Typical endoplasmic reticulum is well
developed in young macrogametes but not present in any appreciable
amount in mature ones. The cell boundary consists of 2 membranes,
the inner one considerably thicker than the outer. There arc numerous
fine invaginations or micropores along the entire periphery of the
macrogametes; they are about 500 A in diameter and 1000 A deep,
normally appearing as blind pouches but sometimes opening into
vacuoles. The nucleus has a relatively large nucleolus, with prominent
52 THE COCCIDIAN PARASITES OF RUMINANTS
granules in the karyoplasm. The nuclear membrane is double, with
numerous pores.
Hammond, Scholtyseck and Miner (1967) described the fine struc-
ture of the microgametocytes. In the early microgametocytes there is
widely distributed endoplasmic reticulum, with canals containing elec-
tron-dense material, a number of thick-walled vesicles, glycogen gran-
ules, and many mitochondria. At the time the microgametes are formed
the microgametocytes are 12-18 jx in diameter. The parasitophorous
vacuole is narrow, and the microgamont has many microvilli along its
free outer surface. These protrusions interdigitate with processes
from the host cell cytoplasm; each of the latter processes contains a
mitochondrion. Micropores about 1100 A wide and 1100 A deep are
occasionally present on the microgamont surface.
Hammond, Ernst and Chobotar (1967) and Hammond, Chobotar
and Ernst (1968) described the sporozoites of E. bovis. They are 14-17
by 3-4 /t with a mean of 15.6 by 3.3 /x and move by gliding and flexion.
They have a relatively large refractile body at the posterior end and
one or more smaller refractile bodies anterior to the nucleus. The nu-
cleus is vesicular near the center of the body and has a somewhat
eccentric nucleolus and peripheral chromatin. There is a nipple-like
projection at the anterior end, some indication of peripheral fibrils and
occasionally median rodlike bodies interpreted as rhoptries. There are
numerous glycogen granules, mostly in the middle of the sporozoites.
According to Walton (1959), the haploid number of chromosomes in
E. bovis is 2.
Prepatent Period. Oocysts appear 16-21 days after experimental in-
fection (Hammond, Davis and Bowman, 1944), and most often 18-20
days after infection (Hammond et ah, 1946). Large numbers are dis-
charged for 5-7 days, and smaller numbers for 2-3 weeks. In 28 calves
studied by Senger et al. (1959), oocysts were discharged for 7-15 days
with a mean of 11.5 days. Svanbaev (1967a) found that the prepatent
period was 17-18 days and the patent period no more than 10 days.
Patnaik and Pande (1965) and Bhatia and Pande (1967b) described
the endogenous stages of a coccidium that they tentatively identified
as E. bovis in the small intestine of the water buffalo. However, they
were dealing with mixed infections, and it is uncertain that this is the
species that they actually saw. Pande et al. (1968) described several
endogenous stages in the water buffalo intestine but did not attempt to
assign them to species.
Type Host. Bos taunts (ox).
Other Hosts. Bos indicus (zebu). In addition, Tubangui (1931)
and Yakimoff (1933a) reported this species from the carabao and
genus Eimeria Schneider, 1S75 53
water buffalo (both Bubalus bubalis) , Patnaik (1965) and Bhatia
et al. (1968) from the water buffalo, and Yakimoff (1935b) in the
wisent or European bison Bison bonasus and the banteng Bibos
banteng.
Location. The first stage schizonts are in the endothelial cells of the
lacteals in the villi of the posterior half of the small intestine. The
second generation schizonts are in the epithelial cells of the cecum and
colon. The gamonts are generally in the epithelial cells of the glands
of the cecum and colon, but may extend up into the terminal 1-1.3 m
of the small intestine in heavy infections.
Geographic Distribution. Worldwide.
Pathogenicity. E. bovis is one of the 2 most pathogenic of the bovine
coccidia. Hammond, Davis and Bowman (1944) studied its effects in
experimentally infected calves. An infective dose of 125,000 oocysts
or more was generally needed to cause marked signs. These appeared
about 18 days after infection, and consisted of diarrhea and/or dysen-
tery, tenesmus, and temperatures as high as 106.6 F. One of 4 calves
given 125,000 oocysts became moribund due to coccidiosis, while in-
dividual calves given 250,000-1 million oocysts all died or became
moribund 24-27 days after infection.
The most severe pathologic changes occur in the cecum, colon and
terminal 0.3 m of the ileum. They are due to the gamonts. At first the
mucosa is congested, edematous and thickened, with petechiae or
diffuse hemorrhages. Its lumen may contain a large amount of blood.
Later, the mucosa is destroyed and sloughed, and a patchy or con-
tinuous membrane forms over its surface. The submucosa may also be
destroyed. If the animal survives, both mucosa and submucosa are
later replaced.
Senger et al. (1959) found that infection of calves with E. bovis
produced partial immunity against subsequent exposure.
Cross-Transmission Studies. Wilson (1931) was unable to infect
pigs or goats with E. bovis from the ox. Savin (1969) claimed to have
infected 3 week-old calves {Bos taurus) with E. bovis from the water
buffalo.
Prevalence. This is one of the commonest coccidia of cattle.
Boughton (1945) found it in 41% of 2,492 bovine fecal samples in
southeastern U.S. Hasche and Todd (1959a) found it in 41% of 355
cattle in Wisconsin; Szanto, Mohan and Levine (1964) in 52% of
795 beef calves from 35 farms in Illinois; Nyberg, Heifer and Knapp
(1967) in 62% of 86 cattle in Oregon; and Jacobson and Worley
(1969) in 61% of 486 calves and 30% of 479 adult cattle in Montana.
Fitzgerald (1962) reported that it was the most prevalent species in a
54 THE COCCIDIAX PARASITES OF RUMINANTS
large herd of beef cattle in Utah. Supperer (1952) found it in 66%
of 130 cattle in Austria; Joyner et al. (1966) in 75% of 110 bovine
fecal samples in England; Chroust (1964) in 69% of 184 calves in
Czechoslovakia; Patyk (1965) in 23% of 341 calves in Poland; Torres
and Ramos (1939) in 49% of 146 cattle in Brazil; Balconi (1963) in
41% of 100 adult slaughter cattle in Guatemala; Ruiz (1959) in 7%
of 100 adult cattle in the San Jose, Costa Rica abattoir; Ruiz and Ortiz
(1961) in 31% of 100 calves in Costa Rica; Vassiliades (1969) in 21%
of the cattle he examined in Senegal; Watanabe and Twata (1956) in
4% of 454 healthy cattle in Japan; Yakimoff, Gousseff and Rastegaieff
(1932a) in 40% of 126 cattle in Uzbekistan; Yakimoff (1933a) in 47%
of 17 zebus, 39% of 44 cattle and 23% of 30 water buffaloes in Azer-
baidzhan; Marchenko (1937) in 54% of 137 cattle in the North
Caucasus, and Patnaik (1965) in 52% of 136 water buffaloes at Agra,
India. Rao and Hiregaudar ( 1954a) said that it is common in Bombay
State, India. Svanbaev (1967a) found it in a calf as early as 20 days
after birth; he found it in 26% of 781 cattle 2 months to more than a
year old in Kazakhstan. Bhatia et al. (1968) found it in 31% of 305
water buffaloes in Mathura, Uttar Pradesh, India, and Savin (1969)
in 34% of 124 water buffaloes in Turkey.
Cultivation. Fayer and Hammond (1967) inoculated E. bovis into
embryonic bovine kidney, spleen, intestine, testis and thymus cells.
The sporozoites developed only in primary kidney and intestinal cell
cultures and in secondary cultures of all these tissues. Schizonts con-
taining merozoites developed only in the kidney, spleen and thymus
cells. Fayer and Hammond (1967) added ovine embryonic kidney
cells to the list of host cells for this species.
Hammond and Fayer (1967, 1968) cultivated E. bovis in monolayer
cell line cultures of bovine kidney, bovine trachea, human intestine
and mouse fibroblasts (L cells). They obtained mature first genera-
tion schizonts in all tissue cultures except the mouse fibroblasts; in
these, the sporozoites entered the cells but did not develop beyond a
trinucleate stage. Development was especially fast in the bovine
trachea cultures; mature schizonts were first seen 8 days after inocula-
tion, and some reached 292 by 118 /». 18 days after inoculation; an
early second generation schizont was present 18-19 days after inocula-
tion. The schizonts developed more slowly in bovine kidney cells than
in bovine trachea cells; the first mature schizonts were seen only after
14 days, and the largest one, seen 21 days after inoculation, was 55 by
38 //.. Relatively few schizonts developed in the human intestinal cells,
but their rate of development was about the same as in bovine kidney
genus Eimeria Schneider, 1S75 55
cells. The largest mature schizont, seen 13 days after inoculation,
was 109 by 55 ;x.
Remarks. Hassan (1935) described the sporozoites and schizonts
of an organism which he named Globidium fusiformis from 5 zebus
with dysentery and rinderpest in India. The schizonts were found in
the abomasum, duodenum and ileum ; they often occurred anterior to
the ileocecal valve, but were not found in the large intestine. They
were whitish and measured 0.4-1.0 by 0.8 mm. The merozoites were 13
by 2.0-2.5 jx, elongate, spindle-shaped, slightly curved, with one end
bluntly rounded and the other finely pointed. This form may possibly
be E. bovis. However, the fact that schizonts were found in the
abomasum as well as in the small intestine made Hammond et al.
(1946) hesitate to assign it to this species, since they never found
schizonts of E. bonis in the abomasum.
Abdussalam and Rauf (1956) described acute primary coccidiosis
in a buffalo {Bubalus bubalis) calf in Pakistan with diarrhea, emacia-
tion, dullness, congestion of the visible mucous membranes, coma, and
death. The unsporulated oocysts in the feces were 29-33 by 19-23 /<,
with a mean of 30 by 21 i±, pinkish brown, typically piriform with the
narrow end drawn out, without a distinct micropyle. At 28-30 C they
began to sporulate in 4 days and continued up to 8 clays ; the sporocysts
were 15-16 by 6-8 /_<,. They thought that this form resembled E. bovis
but that it might be a new species. It is possible that it was E. bareillyi
(see below).
Rao and Bhatavdekar (1959! described a new species of Eimeria,
E. aareyi, in zebus at the Aarey Milk Colony, Bombay State, India.
Its oocysts were ovoid, 21-40 by 14-20 /<. with a mean of 29 by 20 i±.
Its oocyst wall was thin and homogeneous and its micropyle a sharp,
dark line continuous with the oocyst wall but thinner and darger, ap-
pearing like a lid and about 7.2 /x wide. These authors gave no further
structural information except for 2 photomicrographs which revealed
little except that the sporocysts were elongate as in most other bovine
coccidia. This species resembles E. bovis, and Patnaik (1965) con-
sidered it a synonym thereof. It is possible that it is a valid species,
but in the absence of more information, Patnaik's view seems proper.
Eimeria canadensis Bruce, 1921
(Plate 30, Figs. 129-131 ; Plate 62, Fig. 275)
Eimeria zurnabadensis Yakimoff, 1931.
56 THE COCCIDIAN PARASITES OF RUMINANTS
Description. Oocysts slightly ovoid or ellipsoidal, usually with a
smooth wall but sometimes with a roughened wall. Oocyst wall com-
posed of 2 layers, the outer one colorless to yellowish, about 0.5 /x
thick (but thicker over the micropyle), and the inner one clear, yellow
and 1.3 /i thick (except somewhat thinner over the micropyle). (Levine
and Ivens, 1967, found that, while the outer layer looked light and
the inner one dark in intact oocysts, the outer layer looked dark and
the inner one light in a crushed oocyst.) Oocyst wall at the micro-
pylar end gives the appearance of being almost detached at some focal
levels. Oocyst wall lined by a thin membrane. Micropyle at small
end of oocyst, inconspicuous, but somewhat collapsed after standing
in Sheather's sugar solution. Oocysts 28-38 by 20-29 /x with a mean
of 33 by 23-24 A c (oocysts in the water buffalo 25-37 by 18-28 i± with
a mean of 31 by 22 /x according to Bhatia et al., 1968). Oocyst resid-
uum and single polar granule generally absent, but a number of
splintered polar granules present in some oocysts, and a small amount
of amphorous material present at micropylar end of others; Levine
and Ivens (1967) saw a single polar granule in one oocyst. Sporocysts
elongate ovoid, with one end somewhat broader than the other, 15-22
by 6-9 ix with a mean of 18 by 8 /.<. (sporocysts in water buffalo 13-17
by 7-8 ix with a mean of 16 by 7.5 /x according to Bhatia et al., 1968*.
Stieda body present, but merely an inconspicuous thickening of the
wall of the small end of the sporocyst. Sporocyst residuum composed
of a small number of scattered granules in some sporocysts, a larger
number of granules in others, and a compact ball in still others.
Sporozoites elongate, lying lengthwise head to tail in sporocysts.
Sporozoites with 2-3 clear globules each.
Sporulation Time. Christensen (1941) found that the sporulation
time was 3-4 days in tap water, presumably at room temperature; Lee
and Armour ( 1959 ) found that it was 3-5 days at 27 C.
Schizogony and Gamctogony. Unknown.
Patnaik and Pande (1965) described the endogenous stages of a
coccidium that they tentatively identified as E. canadensis in the water
buffalo. However, they were dealing with mixed infections, and it is
uncertain that this is the species that they actually saw.
Prepatent Period. Unknown.
Type Host. Bos taurus (ox).
Other Hosts. Bos indicus (zebu). In addition, Yakimoff (1935a)
reported this species from the wisent or European bison Bison bonasus
and the banteng Bibos banteng, and Patnaik (1965) and Sayin (1969)
from the water buffalo Bubalus bubalis.
Location. Oocvsts found in feces.
genus Eimeria schxeider, 1875 57
Geographic Distribution. North America (British Columbia, Ala-
bama, Illinois, Utah, Wisconsin), Central America (Guatemala),
Europe (England, East Germany), Africa (Nigeria), Asia (Turkey,
India), USSR (Azerbaiclzhan).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Hasche and Todd (1959a) found this species in 35%
of 355 cattle in Wisconsin; Szanto, Mohan and Levine (1964) in
35% of 795 beef calves in Illinois; Jacobson and Worley (1969) in 5%
of 486 calves and 3% of 479 adult cattle in Montana; Balconi (1963)
in 39% of 100 adult cattle in Guatemala; and Joyner et al. (1966) in
13% of 110 cattle in England. Bhatia et al. (1968) found it in 9%
of 305 water buffaloes in Mathura, Uttar Pradesh, India; and Savin
(1969) in 20% of 134 water buffaloes in Turkey.
Remarks. Patnaik ( 1965) considered that E. bombayansis was a
synonym of E. canadensis, but we prefer to list the former as a
separate species (see below) , at least for the present.
Eimeria ellipsoidalis Becker and Frye, 1929
(Plate 30, Figs. 132-134; Plate 31, Figs. 135-137; Plate 62, Fig. 277 )
Description. Oocysts ellipsoidal to very slightly ovoid. Oocyst wall
smooth, colorless, composed of a single layer (2 layers according to
Nyberg and Hammond, 1965 and Bhatia et al., 1968) about 0.8 /x
thick, sometimes apparently lined by a membrane which is often
wrinkled at the small end. Micropyle absent, but wall slightly thinner
at one end than the other; this is the small end if there is one. Oocysts
measured by various authors varied from 12-32 by 10-29 /x; those seen
by Becker and Frye (1929) were 20-26 by 13-17 p with a mean of 23
by 16 (i; those seen by Christensen (1941) were 12-27 by 10-18 /x with
a mean of 17 by 13 /.<.; those seen by Nyberg and Hammond (1965)
were 18-26 by 13-18 /x with a mean of 21 by 15 /x; those seen by Levine
and Ivens (1967) were 20-25 by 14-20 /x with a mean of 23 by 16 /x.
Oocyst residuum absent. Oocyst polar granule ordinarily absent,
occasionally represented by some small shattered granules. Sporocysts
elongate ovoid with almost flat sides, and with an inconspicuous, small,
flat Stieda body or none at small end. Sporocysts 11-16 by 5-6 ti with
a mean of 13-14 by 5 /x (Nyberg and Hammond, 1965; Levine and
Ivens, 1967). Sporocyst residuum present, composed of compact or
scattered granules. Sporozoites elongate, lying head to tail in sporo-
cysts, with a clear globule at the large end and another near the middle.
5S THE COCCTDIAX PARASITES OF RUMINANTS
Sporozoitcs larger at one end than the other, 11-14 by 2-3 n with a
mean of 13 by 3 fi at the large end and 13 by 2 /i at the small end
(Nyberg and Hammond, 1965).
Sporulation Time. Three days according to Grafner and Weichelt
(1966).
Schizogony and Gametogony. Boughton (1945) said that the endog-
enous stages were in the epithelial cells of the small intestine mucosa.
Hammond, Savin and Miner (1962, 1963) found merozoites in scrap-
ings from the middle of the small intestine of a calf killed 11 days after
inoculation. The mature schizonts were 9-16 by 7.5-15 ;± with a mean
of 11 by 9 ix and contained 24-36 merozoites 8-11 fi long and 1-2 fi
wide, usually lying parallel to each other. They found gamonts and
oocysts in the posterior 1 ^> or % of the small intestine, the greatest
concentration being in the lower ileum. They found immature gamonts
8 days after inoculation and mature ones 10 days after inoculation
in epithelial cells near the bottom of the crypts. They were generally
distal to the host cell nucleus. They found oocysts, mature macro-
gametes, microgamonts and microgametes in similar locations in a calf
killed 14 days after inoculation. Mature microgamonts were 12-16.5
by 11-16.5 /i with a mean of 15 by 13 /.<.. The microgametes were 2-3
[i long. Oocysts were discharged continuously for 4-10 and then in-
termittently for 3-12 days.
Patnaik and Pande (1965) described what they considered to be
the endogenous stages of E. ellipsoidalis in the water buffalo. However,
they were dealing with mixed infections, and it is uncertain that this
is the species they were actually describing.
Prepotent Period. Hammond, Savin and Miner (1962, 1963) found
that the prepatent period in 31 calves was 8-13 (mean 10) days.
Type Host. Bos taurus (ox).
Other Hosts. Bos indicus (zebu) ; Bubalus bubalis (water buffalo).
In addition, Yakimoff ( 1935b) reported it from the wisent or European
bison Bison bonasus, the banteng Bibos banteng and the gayal Bibos
gaurus (syn., Bos jrontalis) .
Location. Small intestine (Boughton, 1945; Hammond, Savin and
Miner, 1962) .
Geographic Distribution. North America (Alabama and other south-
eastern states, Illinios, Iowa, Montana, Oregon, Utah, Wisconsin),
Central America (Costa Rica, Guatemala), South America (Colom-
bia), Europe (Austria, Czechoslovakia, East Germany, England,
Rumania, Yugoslavia, Spain), USSR (Azerbaidzhan, Georgia, North
Caucasus, Uzbekistan), Asia (Japan, Turkey, India), Africa (Nigeria,
Senegal I .
genus Eimeria Schneider, 1S75 59
Pathogenicity. According to Boughton (1945), this species often
caused nonbloody diarrhea in calves 1-3 months old. Hammond,
Sayin and Miner (1962, 1963) observed diarrhea, usually lasting only
a few days, in 26 of 31 2-4-week-old Holstein-Friesian calves inocu-
lated with 50,000 to 1 million oocysts. The diarrhea was severe in 14
calves, moderate in 4 and slight in 9. Mucus was present in the feces
at this time in most of the calves. The severe symptoms lasted only
one day in 10 calves, and 2, 3, 6 and 8 days, respectively, in the others.
Of 11 calves subsequently challenged by Hammond, Sayin and
Miner (1962, 1963) with 500,000 oocysts 52 days after the first inocu-
lation, none had any clinical signs of coccidiosis; all but 4 (which had
received only 50,000 oocysts initially) discharged markedly fewer
oocysts than in the original infection, suggesting that some degree of
immunity had developed.
Hammond, Sayin and Miner (1962, 1963) found serous inflamma-
tion of the ileum and jejunum of 4 calves killed 8-13 days after
inoculation.
Hammond, Sayin and Miner (1963) found that the host cells of the
endogenous stages were only slightly changed.
Cross-Transmission Studies. Sayin (1969) claimed to have infected
3 week-old calves (Bos taurus) with E. ellipsoidalis from the water
buffalo.
Prevalence. Boughton (1945) found this species in 45% of 2,492
bovine fecal specimens in the southeastern U.S., Hasche and Todd
(1959a) in 43% of 355 cattle in Wisconsin; Szanto, Mohan and Levine
(1964) in 40% of 795 beef calves in Illinois; Nyberg, Heifer and
Knapp (1967) in 33% of 86 cattle in Oregon; Jacobson and Worley
(1969) in 14% of 486 calves and 3% of 479 adult cattle in Montana;
Ruiz (1959) in 3% of 100 adult cattle and Ruiz and Ortiz (1961) in
4% of 100 calves in Costa Rica; Balconi (1963) in 47% of 100 adult
cattle in Guatemala; Supperer (1952) in 15% of 130 cattle in Austria;
Chroust (1964) in 34% of 184 calves in Czechoslovakia; Patyk (1965)
in 13% of 341 calves in Poland; Joyner et al. (1966) in 26% of 110
cattle in England; Vassiliades (1969) in 12% of the cattle he examined
in Senegal; Yakimoff, Gousseff and Rastegaieff (1932a) in 23% of
126 oxen in Uzbekistan; Yakimoff (1933a) in 27% of 41 oxen, 6%
of 17 zebus and 52% of 21 water buffaloes in Azerbaidzhan; Mar-
chenko (1937) in 16% of 137 cattle in North Caucasus; and Watanabe
and Iwata (1956) in 0.4% of 454 cattle in Japan. Patnaik (1965)
found it in 21% of 136 water buffaloes at Agra, India; Bhatia et al.
(19681 in 20% of 305 water buffaloes at Mathura, Uttar Pradesh.
India; and Sayin (1969) in 53% of 124 water buffaloes in Turkey.
60 THE COCCIDIAN PARASITES OF RUMINANTS
Eimeria cylindrica Wilson, 1931
i Plate 31, Figs. 138-140; Plate 62, Fig. 281)
[non] Eimeria cylindrica Ray and Das Gupta, 1936 (synonym of
E. flfwpti Bhatia, 1938).
Description. Oocysts elongate ellipsoidal, with relatively straight
sides. Oocyst wall colorless, smooth, composed of a single layer about
1.2 //. thick at the sides and bottom and about 0.7 /x thick at one end.
(Bhatia et ah, 1968. said that the oocyst wall was composed of 2 layers
1.3 i-i thick in the water buffalo.) Alicropyle inapparent. Oocysts 16-
30 by 12-17 // with a mean of 21-25 by 13-15 /i (oocysts in water
buffalo 20-34 by 12-17 ,u with a mean of 26 by 14 jx according to
Bhatia et ah, 1968). Oocyst residuum absent. Oocyst polar granule
shattered into many small fragments. Sporocysts elongate ellipsoidal,
with a thin to somewhat thick wall, with one end narrower than the
other and truncate, but without a Stieda body. Sporocysts 12-16 by
4-6 /'. with a mean of 14 by 5 /.<. (Levine and Ivens, 1967). (Sporocysts
in water buffalo elongate ovoid. 9-13 by 4-6 /<. with a mean of 10 by
5 /.i, and with an inconspicuous Stieda body according to Bhatia et ah,
1968.) Sporocyst residuum present in most sporocysts, composed of a
ball of granules at one end of sporocyst. Sporozoites lie lengthwise
head to tail in sporocysts. Sporozoites with one or more rather in-
distinct clear globules and a central vesicle which may be a nucleus.
Sporulation Time. According to Christensen (1941), sporulation
took 2 days in water. Supperer (1952) found that it was 2-3 days.
Schizogony and Gametogony. Unknown.
Patnaik and Pande ( 1965) described what they considered to be
the endogenous stages of E. cylindrica in the water buffalo. However,
they were dealing with mixed infections, and it is uncertain that this
is the species they were actually describing.
Prepatent Period. Wilson (1931) found oocysts in a calf from the
11th to 20th days after experimental inoculation.
Type Host. Bos taurus (ox).
Other Hosts. Bos indicus (zebu). Bubalus bubalis (water buffalo).
Location. Oocysts found in feces.
Geographic Distribution. North America (Alabama. Illinois, Mon-
tana, Oregon, Utah, Virginia, Wisconsin), Central America (Costa
Rica. Guatemala), Europe (Austria, Czechoslovakia, England, Poland,
Rumania, Yugoslavia), Asia (India), Africa (Nigeria, Senegal I.
Pathogenicity. This species appears to be somewhat pathogenic.
Wilson (1931) observed blood in the feces of an experimentally in-
genus Eimeria Schneider, 1S75 61
fected calf 6 days after infection. Rao and Hiregaudar (1954a) con-
sidered this species pathogenic in zebu calves.
Cross-Transmission Studies. Wilson (1931) was unable to infect
pigs or goats with this species.
Prevalence. Hasche and Todd (1959a) found this species in 20% of
355 cattle in Wisconsin; Szanto, Mohan and Levine ( 1964 1 in 12 r r
of 795 beef calves in Illinois; Nyberg, Heifer and Knapp ( 1967 ) in
10% of 86 cattle in Oregon; Jacobson and Worley (1969) in 2% of
486 calves and none of 486 adult cattle in Montana; Ruiz (1959) in
1% of 100 adult cattle in Costa Rica; Balconi (1963) in 19% of 100
adult cattle in Guatemala; Supperer (1952) in 4% of 130 cattle in
Austria; Chroust (1964) in 8% of 184 calves in Czechoslovakia;
Patyk (1965) in 3% of 341 calves in Poland; Joyner et al. (1966)
in 13% of 110 cattle in England; and Vassiliades (1969) in 6% of the
cattle he examined in Senegal. Patnaik (1965) reported it in 7%
of 136 water buffaloes in Agra, India; and Savin (1969) in 5% of 124
water buffaloes in Turkey.
Remarks. It is possible that the form in water buffaloes is a dif-
ferent species since its oocysts and sporocysts differ to some extent in
structure (Bhatia et ah, 1968).
Eimeria auburnensis Christensen and Porter, 1939
(Plate 32, Figs. 141-143; Plate 33, Figs. 144-147; Plate 34, Figs.
148-154; Plate 35. Figs. 155-160; Plate 36, Figs. 161-167; Plate 37,
Fig. 168; Plate 38, Figs. 169-170; Plate 39, Fig. 171; Plate 40, Fig.
172; Plate 41. Fig. 173; Plate 42. Fig. 174; Plate 43. Fig. 175; Plate
63. Fig. 284)
Eimeria ildefonsoi Torres and Ramos, 1939.
Eimeria khurodensis Rao and Hiregaudar, 1954.
Eimeria sp. Pop-Cenitch and Bordjochki, 1959.
Description. Oocysts elongate ovoid (varying between almost
ellipsoidal and markedly tapered), somewhat flattened at small end.
Micropyle present at small end. Oocyst wall smooth, rarely rough or
heavily mammillated, 1.0-1.8 /-, thick, becoming thinner at micropylar
end. Oocyst wall composed of one layer lined by a thin membrane
which is slightly wrinkled at the micropylar end I Levine and Evens,
1967) or composed of 2 layers lined by a thin membrane (Nyberg and
Hammond, 1965); outer part or layer of oocyst wall yellowish orange
(Levine and Evens, 1967 1 or colorless to pink-orange or lavender (Ny-
62 THE COCCIDIAN PARASITES OF RUMINANTS
berg and Hammond, 1965) ; inner part or layer greenish (Levine and
Ivens, 1967) or orange-green (Nyberg and Hammond, 1965). (Chris-
tensen and Porter, 1939 described the wall as typically smooth,
homogeneous, transparent, noticeably brownish-yellow.) Oocysts
32-46 by 19-28 /«. with means given by various authors ranging from
36-41 by 22-26 /.<.. Oocyst polar granule present, composed of one large
and many small, shattered fragments. Oocyst residuum absent. Sporo-
cysts elongate, almost ellipsoidal, but with one end smaller than the
other. Stieda body present, not prominent. Sporocyst wall about 0.2
/t thick. Sporocyst residuum present. Sporocysts 16-23 by 7-11 /.t with
means given by different authors ranging from 18-19 by 8-9 jx. (Svan-
baev, 1967a gave a range of 15-17 by 6-7.5 n with a mean of 16 by
6 fi.) Sporozoites elongate, rather comma-shaped, lying lengthwise
head to tail in sporocysts, with one large clear globule in the large end
and sometimes one or 2 smaller globules elsewhere. Sporozoites 15-18
by 3-5 it, with a mean of 16 /.i long, 5 /.<. wide at the large end and 4 /<.
wide at the small end (Nyberg and Hammond, 1965).
Christensen and Porter ( 1939) said that the typical oocysts were
smooth, but that some were heavily mammillated and others were in-
termediate between the 2 types. In an infection experiment, they pro-
duced both smooth and mammillated oocysts by feeding the latter to
a calf; the smooth oocysts predominated.
Sporulation Time. Christensen and Porter (1939) found that the
sporulation time in tap water at room temperature was 2-3 days;
Supperer (1952) reported the same sporulation time; Lee and Armour
( 1959) reported the same time at 27 C.
Schizogony and Gametogony. Hammond, Clark and Miner (1961)
and Davis and Bowman (1962) were the first to describe the endoge-
nous stages in the life cycle of E. auburnensis. The latter found giant
schizonts in the middle and lower third of the small intestine of 2
calves killed 12 and 14 days after experimental infection. (Chobotar
and Hammond, 1967, found them throughout the small intestine but
mostly 6-12 m anterior to the ileocecal valve.) They were 78-250 by
48-150 /i with a mean of 140 by 92 fi. They were usually located in
cells of the reticular connective tissue deep in the lamina propria near
the muscularis mucosae. Chobotar and Hammond ( 1967) found them
in the epithelial cells lining the crypts of Lieberkuehn, usually at or
near the base of the crypt. (In contrast, the giant schizonts of E. bovis
are found in the endothelial cells lining the lacteals of the villi.) They
matured 10 days after inoculation (Chobotar, Hammond and Miner,
1969), being 134-338 by 95-172 ,i with a mean of 178 by 114 fi at
that time, containing thousands of merozoites and occupying the
genus Eimeria Schneider, 1875 63
whole width of the crypt. The host cell nucleus enlarged. Each
schizont lay in a parasitophorous vacuole in the host cell. The mature
merozoites within the schizonts were about 11 jx long (they measured
4-11 [x with a mean of 8 /x, but Davis and Bowman said that they
were unable to measure their full length because of their position
in the sections) . They had a compact nucleus at one end.
Chobotar (1968) found mature second generation schizonts 12-14
days after inoculation in cells of the lamina propria under the villar
epithelium of the small intestine. They were 6-12 by 5-9 /x with a mean
of 8.5 by 6 (i and contained 4-11 (mean 7) merozoites each. The second
generation merozoites were spindle-shaped, 7-9 by 1-2 /i with a mean
of 8 by 1.5 jx, and contained a vesicular nucleus in the broader posterior
end of the body. Their host cells were only slightly altered.
The gamonts occur in the subcpithelium in mesenchymal-mesoder-
mal cells of the small intestine (Hammond, Clark and Miner, 1961,
Chobotar, 1968). Davis and Bowman (1962) found many more micro-
gamonts near the muscularis mucosae than in the villi; 16 out of 20
randomly selected ones were in the basal half of the mucosa. Ham-
mond, Clark and Miner (1961) found gamonts of both sexes 14-18
days after infection, and Davis and Bowman (1962) found micro-
gamonts 12-14 days after infection. They were very large. Hammond,
Clark and Miner (1961) reported that the mature microgamonts were
67-103 by 48-83 /x with a mean of 85 by 65 /x and that each contained
thousands of microgametes. Davis and Bowman (1962) found that
the mature microgamonts were 36-288 by 27-150 /x with a mean of
125.5 by 79.5 /x. Chobotar (1968) said that mature microgamonts at
18-19 days were 61-151 by 42-109 /x with a mean of 103 by 70 fi.
According to Hammond, Clark and Miner ( 1961 ) , the microgametes
were 4-8 /x long with a mean of 5.5 /x, 0.5-0.75 /x wide, and had 2
posteriorly directed flagella about 10-12 /x long.
According to Hammond, Clark and Miner ( 1961 ) , the macrogametes
were about 18 /x long at 18 days, being considerably smaller than the
microgamonts.
Scholtyseck, Hammond and Ernst (1966) described the fine struc-
ture of the macrogametes. They contain closely spaced glycogen
granules 0.3-1.0 /x in diameter, mostly joined at the margins with one
or more adjacent granules. The dark bodies are larger than those of
E. bouis, averaging 1.5 fx in greater diameter. The wall-forming bodies
arc slightly larger than the dark bodies, averaging 1.7 /<. in diameter.
This species is distinguished by having groups of microtubules, usually
several layers deep in some places and few or none in others. The
parasitophorous vacuole is relatively large and is filled with amorphous
<>4 THE COCCIDIAN PARASITES OF RUMINANTS
electron-dense material. There arc numerous mitochondria in the host
near the vacuole. Scholtyseck, Hammond and Chobotar (1967) de-
scribed pinocytosis in E. auburnensis macrogametes.
Hammond, Scholtyseck and Miner (1967) described the fine struc-
ture of the microgamonts. They contain thousands of irregularly
distributed nuclei which never become arranged at the surface. They
do not contain typical endoplasmic reticulum or glycogen granules, but
do contain large and small vacuoles, mostly with thick walls, and either
empty or containing electron-dense material. The parasitophorous
vacuole is well developed around growing microgamonts, but narrow
or nonexistent around mature ones; it contains parasite mitochondria
enclosed in a thin layer of parasite cytoplasm. The interior of the
microgamonts contains furrows which become confluent in later stages,
separating the cytoplasm into many small masses with relatively large
interstitial spaces. As the microgamete flagella developed, they were
seen in these spaces.
Hammond, Ernst and Chobotar (1967) and Hammond, Chobotar
and Ernst (1968) described the sporozoites of E. auburnensis. They
are broadly lanceolate. 16-21 by 3.5-5 //. with a mean of 18.7 by 4.5 \x
and move by gliding and flexion. They have a relatively large retractile
body at the posterior end and one or more smaller retractile bodies
anterior to the nucleus. The nucleus is vesicular, near the center of the
body, and has a somewhat eccentric nucleolus and peripheral chroma-
tin. There is a nipple-like projection at the anterior end, some indica-
tion of peripheral fibrils and occasionally median rodlike bodies
interpreted as paired organelles (rhoptries). There is a small spherical
structure resembling a retractile body at the extreme posterior end.
There are numerous glycogen granules, mostly in the middle of the
sporozoite.
Hammond, Clark and Miner (1961) found oocysts in the lamina
propria of calves killed 18-19 days after inoculation.
Chobotar and Hammond (1967) found schizonts as early as 6 days
after inoculation.
Patnaik and Pande (1965) and Bhatia and Pande (1967a) described
what they considered to be the endogenous stages of E. auburnensis in
the small intestine of the water buffalo. However, they were dealing
with mixed infections, and it is uncertain that this is the species that
they were actually describing.
Prepatent Period. Christensen and Porter (1939) reported that the
prepatent period in one calf was 24 days; it discharged large numbers
of oocysts for 3 days and small numbers for the next few weeks. Ham-
mond, Clark and Miner (1961) found that the prepatent period in 22
genus Eimeria Schneider, 1875 65
calves was 18-20 clays, being 18 days in the great majority. The patent
period was 2-7 days. Svanbaev (1967a) found that the prepatent
period was 18-19 days and the patent period 8 days in 2 calves. Chobo-
tar (1968) found that the prepatent period was 16-17 days and the
patent period 2-4 clays.
Type Host. Bos taunts (ox).
Other Hosts. Bos indicus (zebu); Bubalus bubalis (water buffalo).
Location. Middle and lower third of small intestine.
Geographic Distribution. USA (Alabama, southeastern states. Illi-
nois, Missouri, Oregon, Texas, Utah, Wisconsin, Wyoming), Central
America (Costa Rica, Guatemala), South America (Brazil, Colombia),
Europe (Austria, Czechoslovakia, England, Rumania, Spain, Yugo-
slavia), Asia (India, Japan, Turkey), USSR (Kazakhstan), Africa
(Nigeria, Senegal).
Pathogenicity. This species apparently has a moderate degree of
pathogenicity. Christensen and Porter (1939) produced a profuse,
watery green diarrhea accompanied by slight apathy in a 2-week-old
calf by administering 8,000 sporulated oocysts. The signs appeared 9
days after infection (i.e., 15 days before the first oocysts appeared in
the feces) and continued for 5 days. According to Davis and Bowman
(1952), infections with E. auburnensis are usually accompanied by
straining and the passage of visible blood and mucus, especially follow-
ing experimental inoculation with large numbers of oocysts or in
natural outbreaks where contamination is heavy. Hammond, (lark
and Miner (1961) reported that 4 calves 1-6 weeks old inoculated
with 100,000-750,000 oocysts discharged moderate to high numbers of
oocysts (about 14,000-200,000 per gram of feces); one had severe
diarrhea 18-20 days after inoculation, 2 had mild diarrhea 18-19 days
after inoculation, and one showed no signs of coccidiosis. Davis and
Bowman (1962) reported that a month-old calf had diarrhea 6-12
days after inoculation; at autopsy on the 12th day, its small intestine
was edematous 7 m anterior to the ileocecal valve.
Cross-Transmission Studies. Sayin (1969) claimed to have infected
3 week-old calves {Bos taurus) with E. auburnensis from the water
buffalo.
Prevalence. E. auburnensis is one of (he commonest coccidia of
cattle in North America. Davis and Bowman (19521 found it in all
of 20 calves in Alabama; Hasche and Todd ( 1959a i in 45 r r of 355
cattle in Wisconsin; Szanto, Mohan and Levine (1964) in MV f of
795 beef calves in Illinois (originating from Illinois, Missouri, Texas
and Wyoming); Nyberg, Heifer and Knapp (1967) in 1-Ur of 86
cattle in Oregon; Jacobson and Worley (1969) in 32 r r of 486 calves
66 THE COCCIDIAX PARASITES OF RUMINANTS
and 12% of 479 adult cattle in Montana; Torres and Ramos (1939) in
32% of 146 cattle in Brazil; Supperer (1952) in 3% of 130 cattle in
Austria; Watkins (according to Lapage, 1956) in 91% of the calves he
examined in Devonshire, England; Joyner et al. (1966) in 34% of 110
cattle in England; Marinkelle (1964) in 32% of 100 calves in Colom-
bia; Ruiz and Ortiz (1961) in 1% of 100 calves in Costa Rica; Balconi
( 1963) in 43% of 100 adult cattle in Guatemala; Watanabe, and Iwata
(1956) in 2% of 454 cattle in Japan; Chroust (1964) in 18% of 184
calves in Czechoslovakia; Patyk (1965) in 15% of 341 calves in
Poland; and Vassiliades (1969) in 12% of the cattle he examined in
Senegal. Svanbaev (1967a) found it in a calf as early as 30 days after
birth; he found it in 5% of 781 cattle 2 months to more than a year
old in Kazakhstan. Lee and Armour (1959) said that it was very
common at Vom, Nigeria. Patnaik (1965) reported E. auburnensis in
19% of 136 water buffaloes at Agra, India, Bhatia et al. ( 1968) in 32%
of 305 water buffaloes at Mathura, Uttar Pradesh, India; and Savin
1 1969) in 44% of 124 water buffaloes in Turkey.
Remarks. The name Eimeria ildefonsoi Torres and Ramos (1939)
is now accepted as a synonym of E. auburnensis. (See Levine, 1961;
Pellerdy, 1965.) Patnaik (1965) thought that E. khurodensis Rao and
Hiregaudar (1954a) was a synonym of E. thianethi, but Levine and
Ivens (1967) showed that it was a synonym of E. auburnensis. Hire-
gaudar and Rao ( 1966) insisted that E. khurodensis was different from
E. bukidnonensis, but there was nothing in their description that could
be used to differentiate it from the mammillated form of E. auburnensis
except that they gave its sporulation time as 10-15 days as opposed to
2-3 days for E. auburnensis. However, sporulation times are subject to
wide variation depending on the circumstances of sporulation. If this
species is indeed distinct from E. auburnensis, a far better description
than has heretofore been provided must be given. Pellerdy (1965) and
Bhatia et al. (1968) stated that E. bombayansis Rao and Hiregaudar
( 1954a) is a synonym of E. auburnensis ; this may well be true, but the
size given for the sporocysts of E. bombayansis is smaller than that of
E. auburnensis.
Pop-Cenitch and Bordjochki (1959) described an Eimeria sp. from
cattle in Serbia which Pellerdy ( 1965) considered to be E. auburnensis;
we agree.
Eimeria brasiliensis Torres and Ramos, 1939
(Plate 44, Figs. 176-178; Plate 45, Figs. 179-180; Plate 61, Figs.
269-270; Plate 63, Fig. 285)
genus Eimeria Schneider, 1875 67
Eimeria boehmi Supperer, 1952.
Eimeria orlovi Basanova, 1952.
Eimeria helenae Donciu, 1961.
Description. Oocysts ellipsoidal, 31-49 by 21-33 \x with means of
36-38 by 25-27 /x (31 to 44 by 20-29 /* with a mean of 39 by 27 /x in
the water buffalo according to Bhatia et al., 1968). Micropyle present,
covered by a mound-shaped or flat cap about 1.5-4 fx high and 7-12 //.
wide. Oocyst wall generally smooth, brownish yellow, generally com-
posed of a single layer 1.8 fx thick at the sides and 1 \x thick at the
end opposite the micropyle. (Two layers 1.3 jx thick in the water
buffalo according to Bhatia et al., 1968.) Oocyst wall lined by a
brownish membrane. Surface of oocyst occasionally covered by round,
partially coalescent yellowish plaques about 5 /x in diameter (each
presumably originating from a flattened plastic granule) which form
an incomplete additional layer on the surface, giving it a rough ap-
pearance; some of these plaques may be partially scaled off of the
oocysts. Oocyst residuum and polar granule generally absent, but tiny
scattered granules present in some oocysts and some amorphous ma-
terial in others. Polar granules present according to Torres and Ramos
(1939). "Tenue body" (i.e., polar granule) just beneath micropyle in
sporulated and unsporulated oocysts in the water buffalo according to
Bhatia et al. (1968). Sporocysts elongate ellipsoidal, with relatively
narrow ends, 16-22 by 7-10 \x. Definite Stieda body absent, but repre-
sented by a dark, thickened wall at one end of sporocyst. Sporocyst
residuum composed of more or less scattered granules. Sporozoites
elongate, lying head to tail in sporocysts, with one large clear globule
at each end. (See figures by Marquardt, 1959, and Levine and Ivens,
1967.)
Sporulation Time. The sporulation time is 6-7 days at 27 C accord-
ing to Lee and Armour (1958), 12-14 days at 20 C according to Sup-
perer (1952), or 7-8 days at 25-28 C in 2 C / C potassium bichromate
solution according to Svanbaev ( 1967a) .
Schizogoni/ and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Bos taurus (ox).
Other Hosts. Bos indicus (zebu); Bubalus bubalis I water buffalo i.
Location. Oocysts found in feces. Svanbaev (1967a) said that this
species occurs in the anterior ileum.
Geographic Distribution. North America (Alabama, Illinois. Mon-
tana, Wisconsin), Central America (Guatemala), South America
(Brazil), Europe (Austria, England, Hungary, Rumania. Yugoslavia),
Africa (Nigeria, Senegal), Asia (India), USSR (Kazakhstan I .
(> s THE COCCIDIAN PARASITES OF RUMINANTS
Pathogenicity . Unknown.
Cross-Transmission Studii s. None.
Pr, valence. Hasche and Todd (1959a, hi found this species in 3% of
355 cattle in Wisconsin; Szanto. Mohan and Levine ( 1964 1 in 4 r r
of 795 beef calves in Illinois. Jacobson and Worley (19691 in none of
486 calves and 0.2 r r of 479 adult cattle in Montana; Torres and
Ramos 1 1939 1 in 3% of 146 cattle in Brazil; Balconi (1963) in 3%
of 100 adult cattle in Guatemala; Joyner et al. (1966) in 7% of
110 cat lie in England; Supperer (1952) in l ( f of 130 cattle in
Austria; Donciu 1 1961 I in 0.4 r r of 2,183 cattle in Rumania; and
Vassiliades (1969i in 2' 7 of the cattle he examined in Senegal.
Svanbaev ( 1967a I found it in a calf as early as 30 days after
birth; he found it in 4 r r of 781 cattle 2 months to more than
a year old in Kazakhstan. Bhatia et al. (19681 found this species in
2 ( f of 305 water buffaloes in Mathura, Uttar Pradesh, India; and
Savin ( 1969 1 in 1.6% of 124 water buffaloes in Turkey.
Remarks. Bhatia et al. (1968) considered that E. gokaki was a
synonym of E. brasiliensis, but it is smaller and we prefer to leave it
as a separate species, at least for the present.
Eimeria alabamensis Christensen, 1941
i Plate 45, Figs. 181-184; Plate 62, Fig. 278)
Description. Oocysts ovoid, but with sides rather tapering toward
small end. Micropyle absent. Oocyst wall smooth, very pale yellow,
composed of a single layer about 0.6-0.7 i>. thick, lined by a thin mem-
brane which may collapse at the small end after standing in Sheather's
sugar solution (2 layers 1.3 ». thick in the water buffalo according
to Bhatia et ah, 1968). Oocysts 13-25 by 11-17 /±. Oocysts polar granule
and oocyst residuum absent, except for some tiny scattered fragments
which might or might not be polar granule fragments. Sporocysts
elongate, with one end bullet-like and bearing a tiny Stieda body,
without sporocyst residuum. Sporocysts 11-16 by 4-5 /<. with a mean
of 11.9 by 4.6 fi. (8-11.5 by 5-6 /<, with a mean of 9 by 5 /.t according to
Svanbaev, 1967a.) Sporozoites lie lengthwise, head to tail, in sporo-
cyst-. Sporozoites with 2-3 clear globules. (See figure by Levine and
Ivens, 1967.)
Sporulation Time. Christensen (1941) and Lee and Armour (1959)
reported that the sporulation time was 4-5 days in water at room
temperature and 27 C, respectively; Svanbaev 1 1967a) found that
it was 4-5 days at 25-28 C in 2 r r potassium bichromate solution.
genus Eimeria Schneider, 1875 69
Schizogony and Gametogony. Davis, Bowman and Boughton (1957)
described the endogenous life cycle of E. alabamensis. It took place in
the nucleus of the intestinal cells. The sporulatcd oocysts excysted
in the rumen, omasum and small intestine. The sporozoites entered the
epithelial cells of the villi of the small intestine, where they rounded
up and became schizonts; they were generally in the distal end of the
host cell but then entered the nucleus, where they were found 2 days
after infection. At first the sporozoites were spindle-shaped and 3-7
by 1.5-3 /<.; when they rounded up they were 2.8-3.5 /x in diameter
with a mean of 3.1 fi. The young schizonts were in the apical cells of
the tips of the villi, and were almost always surrounded by a clear.
halo-like area.
The schizonts then grew, becoming mature at 3 days. Mature schi-
zonts containing merozoites were found 3-8 days after infection. At
4 days they were found only in the lowest third of the small intestine.
They were numerous at this time, but became fairly sparse by the 8th
day. One to several schizonts were present in each host cell nucleus.
The mature schizonts were 7-12 by 6-10 /i at 3 days, 8-15 by 7-12 n
at 4 days, 10-15 by 7-13 r , at 6 days, and 8-18 by 5-14 r at 8 days.
They contained 16-32 merozoites; occasionally a host cell nucleus
contained 48 merozoites, but these were apparently derived from
more than one schizont.
It is probable that there is more than one asexual generation; Davis,
Bowman and Boughton (19571 found merozoites penetrating host cell
nuclei in the lower small intestine as early as 4 days after infection
and said that "they probably developed into other schizonts or initi-
ated gametogenesis."
Gamonts were formed in the nuclei of the epithelial cells of the
villi of the small intestine; in heavy infections they also occurred in
the cecum and upper colon. They could be recognized as early as 6
days after infection. The ratio of niacrogametes to microgamonts was
78:22. Two or 3 microgamonts and 3-5 niacrogametes or oocysts per
host cell nucleus were not uncommon. The microgamonts were 8-25
by 7-21 jj, with a mean of 15.6 by 11.5 /<.. The niacrogametes were 7-20
by 7-12 /<, with a mean of 12 by 9.1 << and contained peripheral plastic
granules.
Oocysts were present beginning days after infection in the lower
7 in of the ileum.
Prepatent Period. According to Oavis, Boughton and Bowman
(1955), the prepatent period in 21 low-grade infections ranged from
6-11 days with a mean of 8.6 days. The patent period was 1-10 days
with a mean of 4.6 days. The period of high oocyst discharge was
70 THE COCCIDIAN PARASITES OF RUMINANTS
1-9 clays with a mean of 3.9 days. Smith and Davis (1965) found that
the prepatent period was 7-9 days whether the oocysts were given to
calves in dry feed or liquid. The patent period was 5-13 days in the
former and only 1-8 days in the latter. Svanbaev (1967a) found that
the prepatent period was 7-8 days and the patent period 9 days in
2 calves.
Type Host. Bos taunts (ox I.
Other Hosts. Bos indicus (zebu); Bubalus bubalis (water buffalo).
Location. Primarily small intestine, but also cecum and upper
colon in heavy infections.
Geographic Distribution. USA (Alabama, southeastern states, Illi-
nois, Oregon, Missouri, Montana, Texas, Utah, Wisconsin, Wyoming),
Central America (Costa Rica, Guatemala), Europe (England, Poland),
Asia (Turkey), USSR (Kazakhstan), Africa (Nigeria, Senegal).
Pathogenicity. According to Davis, Boughton and Bowman (1955),
E. alabamensis is essentially nonpathogenic under field conditions.
However, it may or may not cause symptoms in the laboratory.
Boughton ( 1943) found that it was pathogenic and even caused the
death of 2 out of 5 calves 8 and 14 days after infection when large
numbers (many millions) of oocysts were given. Davis, Boughton and
Bowman (1955) found that it also caused severe nonfatal infections
in 2 previously unexposed 14-month-old cattle and in a 2-year-old cow.
(The above were mixed infections with other unspecified species of
Eimeria.) According to Davis, Bowman and Boughton (1957), there
was general enteritis in the lower half of the small intestine of one of
the 2 calves that died and in the last meter of the ileum of the other.
There was also massive destruction of the epithelium, with leucocytic
infiltration and villar edema. Clusters of swollen villi formed macro-
scopically visible tufts, and in severe infections nearly all villi in a
7 meter length of small intestine were infected.
Cross-Transmission Studies. None.
Prevalence. Davis, Boughton and Bowman ( 1955) found this species
in 93% of 102 dairy calves in 6 herds in southeastern United States
in a weekly fecal survey; they found it in 24% of 135 animals from
which only a single fecal sample was taken; it was present in all of
26 herds from which at least 5 animals were examined. Hasche and
Todd (1959a) found it in 42% of 355 cattle in Wisconsin; Szanto,
Mohan and Levine (1964) in 17% of 795 cattle from Illinois, Missouri,
Texas and Wyoming; Nyberg, Heifer and Knapp (1967) in 1% of 86
cattle in Oregon; Jacobson and Worley (1969) in 0.4% of 486 calves
and none of 479 adult cattle in Montana, Joyner et al. (1966) in 14%
of 110 cattle in England; Patyk (1965) in 9% of 341 calves in Poland;
genus Eimeria Schneider, 1875 71
Ruiz and Ortiz (1961) in 20% of 100 calves in Costa Rica. Balconi
(1963) in 43% of 100 cattle in Guatemala, and Vassiliades (1969) in
2% of the cattle he examined in Senegal. Patnaik (1965) reported it in
1% of 136 water buffoles in Agra, India; Bhatia et al. (1968) in 3%
of 305 water buffaloes at Mathura, Uttar Pradesh, India, and Sayin
(1969) in 10% of 124 water buffaloes in Turkey. Svanbaev (1967a)
found it in a calf as early as 10 days after birth; he found it in 8%
of 781 calves 2 months to more than a year old in Kazakhstan.
Davis, Boughton and Bowman (1955) found that under farm con-
ditions E. alabamensis was relatively rare in calves 3-9 weeks old
and relatively common in those 3-9 months old.
Eimeria subspherica Christensen, 1941
(Plate 46, Figs. 186-189; Plate 62, Fig. 279)
Description. Oocysts spherical to subspherical. Oocyst wall smooth,
pale yellowish, composed of a single layer about 0.5-0.6 /<. thick. (Two
layers 0.7-1.0 /x thick in the water buffalo according to Bhatia et ah,
1968.) Micropyle absent. Oocysts 9-14 by 8-13 /x with a mean of
11-13 by 10-12 jx (Christensen, 1941; Lee and Armour, 1959; Levine
and Ivens, 1967) . Oocyst residuum and oocyst polar granule absent.
Sporocysts elongate ovoid, often with rather flat sides, with small
Stieda body, 7-10 by 3-4 \x with a mean of 8 by 3.5 jx (Levine and
Ivens, 1967) . Sporocyst residuum absent or occasionally composed
of a few granules. Sporozoites wider at one end than the other, lying
lengthwise head to tail in sporocysts. Sporozoites with a clear globule
at the large end.
Sporulation Time. Four to 5 days in water at room temperature
according to Christensen ( 1941 ) .
Schizogony and Gametogony. Unknown.
Patnaik and Pande (1965) described the endogenous stages of a
coccidium that they tentatively identified as E. subspherica in the
water buffalo. However, they were dealing with mixed infections,
and it is uncertain that this is the species that they actually saw.
Prepatent Period. Unknown.
Type Host. Bos taurus (ox).
Other Hosts. Bos indicus (zebu); Bubalus bubalis (water buffalo).
Location. Oocysts found in feces.
Geographic Distribution. North America (Alabama, Illinois, Oregon.
LTah, Wisconsin), Central America I Costa Rica, Guatemala), South
i _ THE COCCIDIAN PARASITES OF RUMINANTS
America I Colombia ) . Europe (England, East Germany), Asia (Tur-
key. India) , Africa (Nigeria, Senegal) .
Pathogenicity. Unknown.
( 'ross-Transmission Studies. None.
Prevalence. Hasche and Todd (1959a) found this species in 11%
of 355 cattle in Wisconsin; Szanto, Mohan and Levine (1964) in 8% of
795 beef calves in Illinois; Nyberg, Heifer and Knapp (1967) in 8%
of 86 cattle in Oregon; Ruiz and Ortiz (1961) in 3% of 100 calves in
Oosta Rica; Balconi (1963) in 12 r r of 100 adult cattle in Guate-
mala; Joyner et al. (1966) in 28% of 110 cattle in England, and
Vassiliades (1969) in 6 r r of the cattle he examined in Senegal. Pat-
naik (1965) reported this species in 21% of 136 water buffaloes in
Agra. India; Bhatia et al. (1968) in 16 r /r of 305 water buffaloes in
Mathura, Uttar Pradesh. India; and Savin (1969) in 15% of 124
water buffaloes in Turkey.
Eimeria wyomingensis Huizinga and Winger, 1942
(Plate 48, Fig. 198; Plate 49, Figs. 199-200; Plate 62, Fig. 274)
? E. bukidnonensis Tubangui, 1931 of Christensen, 1938a.
[non] E. bukidnonensis Tubangui, 1931.
Description. Oocysts ovoid. Oocyst wall yellowish brown to brown-
ish yellow, speckled and somewhat rough, composed of a single layer
about 2.0-3.5 /<, thick, lined by a membrane. Micropyle present, about
5 ji in inside diameter, at small end of oocyst, generally sunken.
Oocysts 36-46 by 26-32 j± with a mean of 40 by 28 /.<, (Huizinga and
Winger, 1942; Lee and Armour, 1959). Oocyst residuum and polar
granule absent. Sporocysts ellipsoidal, with somewhat narrow ends,
with a tiny flat Stieda body at one end. Sporocysts about 18 by 9 /x
(sporocysts in the water buffalo 21-24 by 8-9 /_/. with a mean of 22
by 9 ,» according to Bhatia et ah. 1968). Sporocyst residuum generally
absent ; sometimes present in form of granules. Sporozoites with one
end wider than the other, lying lengthwise head to tail in sporocysts.
Sporozoites with a large, clear globule about 7-8 ». long by 5 /x at
broader end.
Sporulation Time. Five to 7 days at room temperature in shallow,
dilute potassium bichromate solution, according to Huizinga and
Winger (1942); 3-5 days at 27 O in water, according to Lee and
Armour 1 1959 ) .
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
genus Eimeria Schneider, 1875 73
Type Host. Bos taurus (ox).
Other Hosts. Bos indicus (zebu), Bubalus bubalis (water buffalo).
Location. Oocysts found in feces.
Geographic Distribution. North America (Alabama?, Illinois, Texas,
Wyoming), Europe (England, Poland), Africa (Nigeria, Senegal),
Asia (India).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Szanto, Mohan and Levine (1964) found this species
in 6% of 795 beef calves in Illinois; these animals had originated in
Illinois, Texas and Wyoming. Joyner et ah (1966) found it in 14% of
110 rattle in England; Patyk (1965) in 1% of 341 calves in Poland,
and Vassiliades (1969) in 1% of the cattle he examined in Senegal.
Bhatia et ah (1968) found it in 5% of 305 water buffaloes in Mathura,
Uttar Pradesh, India, and Savin (1969) in 0.7% of 124 water buffaloes
in Turkey.
Remarks. This species has been confused with E. bukidnonensis, but
Levine and Ivens (1967) clarified the difference. E. Wyoming ensis
differs from E. bukidnonensis in that it lias smaller oocysts that are
ovoid rather than piriform, and in that its wall, although brownish and
rough, is not radially striated.
Eimeria pellita Supperer, 1952
(Plate 48, Figs. 194 and 195)
Description. Oocysts ovoid with a flattened small end, 36-41 by
26-30 jx. Alicropyle at small end. Oocyst wall relatively thick and dark
brown, bearing numerous small, uniformly distributed protuberances
on its surface in the form of small, blunt points which give the wall a
velvety appearance. Oocyst polar granule and oocyst residuum absent.
Sporocysts elongate ovoid, 14-18 by 6-8 /<., without a Stieda body.
Sporocyst residuum present, usually compact. Sporozoites lie length-
wise head to tail in sporocysts. Sporozoites with 2 refractile globules
(Supperer, 1952) .
Sporulation Time. Ten to 12 days according to Supperer (19521.
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Bos taurus (ox I.
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. Europe (Austria, England).
THE COCCIDIAX PARASITES OF RUMINANTS
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Supperer (1952) found this species in 5% of 130 cattle
in Austria, and Joyner et al. 1 19661 in 4.59c of 110 cattle in England.
Remarks. Bhatia et al. ( 1968) considered E. pcllita a synonym of
E. bukidnonensis. However, the structure of its oocyst wall and shape
of its oocyst differentiate it (See Joyner et al., 1966).
Eimeria illinoisensis Levine and Ivens, 1967
(Plate 49, Fig. 201)
Description. Oocysts ellipsoidal or slightly ovoid. Oocyst wall
smooth, colorless, composed of a single layer about 1.3 /x thick, with
a pale tan inner surface which looks like a membrane in the intact
oocyst. Definite micropyle absent, but one end of oocyst wall slightly
thinner and flatter, with darker boundaries, than the other. Oocysts
24-29 by 19-22 /x with a mean of 26 by 21 /x. Oocysts residuum and
oocyst polar granule absent. Sporocysts elongate ovoid, with one end
slightly tapered and slightly smaller than the other, with a small, flat
to knoblike (in isolated sporocyst) Stieda body. Sporocysts 13-16 by
6-7 ix with a mean of 15 by 6.5 jx. Sporocyst residuum generally a
compact, granular ball plus some scattered granules. Sporozoites with
one end larger than the other, lying lengthwise head to tail in sporo-
cysts. Sporozoites with 2 or more clear globules.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Pre patent Period. Unknown.
Type Host. Bos taurus (ox).
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. North America (Illinois).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
Eimeria bukidnonensis Tubangui, 1931
( Plate 46. Fig. 185; Plate 47, Figs. 190-193)
Description. Oocysts piriform. Micropyle about 3-5 ,u in diameter
at small end of oocyst, more or less sunken in sporulated oocysts but
genus Eimeria Schneider, 1S75 75
not in unsporulated ones. Oocyst wall yellowish brown, punctate,
radially striated, composed of a single layer about 3-4 fx thick, lined
by a rather thick membrane which may be slightly wrinkled at the
small end. Oocysts 43-54 by 29-39 /x. (Svanbaev, 1967a, gave dimen-
sions of 34-50 by 26-34 /x with a mean of 39 by 30 fx; he may have
been dealing with a mixture of E. bukidnonensis and E. Wyoming ensis.)
(Oocysts in water buffalo 38-46 by 25-35 fx with a mean of 42 by 31 /x
according to Bhatia et al., 1968.) Oocyst residuum and polar granule
absent. Sporocysts elongate, somewhat pointed at both ends, with
inconspicuous flat Stieda body, about 20 by 10 /x. (12-20 by 9-12 /x
according to Svanbaev, 1967.) (Sporocysts in water buffalo 15-19 by
8-11 ix with a mean of 17 by 9 p. according to Bhatia et al., 1968.)
Sporocyst residuum absent or perhaps represented by a few tiny,
scattered granules. (According to Hiregaudar and Rao, 1966 and
Bhatia et al., 1968, there is a large amount of sporocyst residual ma-
terial.) Sporozoites with one end wider than the other, lying length-
wise head to tail in sporocysts. Sporozoites with a clear globule at
each end. (See figure by Levine and Ivens, 1967.)
Sporulation Time. According to Baker (1939), the sporulation time
is 24-27 days; according to Lee (1954) it is 17 days at room tempera-
ture, and according to Lee and Armour (1959) it is 5-7 days at 27 C;
it is 4-8 days according to Hiregaudar and Rao (1966). Svanbaev
( 1967a) said that it was 5-9 days at 25-28 C in 2% potassium bi-
chromate solution.
Schizogony and Gametogony. Unknown. Davis and Bowman ( 1964)
found many merozoites 9-13 fx long throughout the small intestine of
a calf 13 days after oral infection at one week of age with 1 million
oocysts. They found oocysts in the small intestine 0.3 m anterior to
the ileocecal valve in another calf 25 days after infection at 3 months
of age with 60,000 oocysts. They were beneath the epithelium about
half-way down to the muscularis mucosae.
Prepotent Period. Baker (1939) found that oocysts first appeared
in an experimentally infected calf 10 days after inoculation. Davis
and Bowman (1964) found that the prepatent period was 15-17 days
in 7 calves. Svanbaev (1967a) found that it was 24-25 days in 2
calves.
Type Host. Bos indicus (zebu).
Other Hosts. Bos taurus (ox). In addition, Yakimoff (1935b) re-
ported finding a single oocyst (which he called E. bukidnonensis) in
a banteng Bibos banteng; it was 39 by 27 /x. Patnaik (1965) and
Bhatia et al. (1968) found it in water buffaloes (Bubalus bubalis) in
India.
76 THE COCCIDIAN PARASITES OF RUMINAXTS
Location. Oocysts found in feces. Svanbaev (1967a) said that it
occurred in the middle and posterior ileum.
Geographic Distribution. North America (New York. Illinois, Mon-
tana i. Europe (England, East Germany, Poland). Asia (Philippines,
India. Japan. Turkey i. South America I Brazil I, Africa ( Nigeria I.
USSR (Azerbaidzhan, Kazakhstan. Turkestan, Uzbekistan).
Pathogi nicity. Baker ( 1939 » observed a tendency toward a diarrheic
condition from the 7th to 15th days after experimental inoculation of
a 70-day-old calf with oo oocysts.
( 'r oss-Transmission Studies. None.
Pr< valence. Since earlier authors failed to differentiate between
E. bukidnonensis and E. wyomingensis, little can be said about tie
prevalence of either species. Szanto, Mohan and Levine 11964) found
it in \ c ( of 795 beef calves in Illinois; Jacobson and Worley (1969)
in 9 r r of 486 calves and 4 c 'c of 479 adult cattle in Montana; Joyner
et ah (1966) in 2 r ( of 110 cattle in England; and Patyk (1965) in 39r
of 341 calves in Poland. Patnaik (1965) reported it from 3% of 136
water bnffaloes in Agra. India, and Bhatia et ah (1968) in o c /c of
305 water buffaloes in Mathura, Uttar Pradesh, India. Svanbaev
(1967a) found it in a calf as early as 40 days after birth; he found it
in 9 r r of 781 cattle 2 months to more than a year old in Kazakhstan.
Remarks. The oocysts that Patnaik (1965) found in the water
buffalo were said to be considerably smaller than the minimum range
given by other authors, but Patnaik gave no measurements. Whether
he was dealing with a different species remains to be determined.
Bhatia et ah (1968) considered E. pellita, E. thianethi, E. mundaragi
and E. khurodensis to be synonyms of E. bukidnonensis. We consider
the first three to be presumably valid species, and E. khurodensis to
be a synonym of E. auburnensis.
Eimeria bombayansis Rao and Hiregaudar, 1954
Description. Oocysts ellipsoidal, tending toward the cylindrical,
sometimes with one side relatively flat and the other convex. Oocysts
32-40 by 20-25 ... with a mean of 37 by 22 .... Micropyle distinct.
2-4 fjL wide at base. Oocyst wall thickened around micropyle. Oocyst
wall smooth, transparent, homogeneous, pale yellowish brown. 1.0-
1.5 fx thick. Oocyst residuum absent. Presence or absence of oocyst
polar granule not mentioned. Sporocysts 12-15 /.<. long, ovoid. Sporo-
cyst residuum present. Sporozoites 4-6 /x long, rounded.
Sporulation Tunc. Two to 3 days according to Rao and Hiregaudar
(1954).
genus Eimeria Schneider, 1S75 77
Schizogony and Gametogony. Unknown.
Prepatent Period. Unknown.
Type Host. Bos indicus (zebu).
Other Hosts. None.
Locution. Oocysts found in feces.
Geographic Distribution. Asia (India).
Pa thoge n icity . Unknown .
Cross-Transmission Studies. None.
Prevalence. Unknown. Rao and Hiregaudar (1954) stated that its
prevalence was great in calves in a dairy herd near Bombay.
Remarks. Pellerdy (1965) considered this name a synonym of E.
auburnensis, saying that it is apparently identical and differs from it
in no essential characteristic. Bhatia et ah (1968) agreed. Patnaik
(1965) considered it a synonym of E. canadensis. However, its sporo-
cysts are smaller than those of E. auburnensis or E. canadensis. While
we suspect that Pellerdy or Patnaik is probably correct, we prefer to
list this name separately in case future research confirms that a dif-
ference exists.
Eimeria mundaragi Hiregaudar, 1956
Description. Oocysts ovoid, 36-38 by 25-28 /x, with a smooth, trans-
parent, pale yellow or yellow wall 0.3 thick (slightly thicker at micro-
pylar end). Micropyle distinct, 0.5 /x in diameter. Oocyst residuum
and oocyst polar granule absent. Sporocysts ovoid, 15 by 9 /x, thinning
at the pointed end. Sporocyst residuum present. Sporozoites 4-6 by
1-3 /'., finely granular (Hiregaudar, 1956).
Sporulation Time. One to 2 days during the summer according to
Hiregaudar 1 1956).
Schizogony and Gametogony. Unknown.
Prepatent Period. Unknown.
Type Host. Bos indicus (zebu).
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. India ( Bombay ) .
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Pre valen ce . Unknown .
Remarks. Levine (1961) remarked that the extremely (liin wall and
tiny, distinct micropyle might differentiate this form from other bovine
coccidia, but that the possibility must not be overlooked that these
oocysts might be those df another species from which the thick, brittle
7S THE COCCTDIAX PARASITES OF RUMINANTS
outer wall had cracked. Patnaik (1965) considered this name to be a
synonym of E. auburncnsis, but E. mundaragi's thin oocyst wall and
lack of a polar granule appear to differentiate it. Bhatia et al. (1968)
considered E. mundaragi to be a synonym of E. bukidnotiensis ; this
is possible.
Eimeria sp. Rastegaieff, 1929
Eimeria smithi Yakimoff and Galouzo, 1927 of Rastegaieff, 1929b.
Rastegaieff (1929b, 1930) reported finding this species in 2 bison
(Bison bison) in the Leningrad zoo. She called it "Eimeria smithi
Yakimoff and Galouzo, 1927," but it is very unlikely that it actually
belonged to this species (a synonym of E. bovis). The oocysts were
ovoid, 16-29 by 14-21 /.<,, with a clearly visible micropyle 6 /.*. in
diameter and an oocyst wall 1.8 /x thick. The sporocysts were piri-
form, 13.5 by 7 ix. Neither oocyst nor sporocyst residua were present.
No oocyst polar granule was illustrated. The sporozoites were illus-
trated as lying lengthwise in the sporocysts.
Host Suborder RUMINANTIA
Host Superfamily BOVOIDEA
Host Family BOVIDAE
Host Subfamily HIPPOTRAGINAE
Host Tribe REDUNCINI
Eimeria macieli Yakimoff and Matchulski, 1938
(Plate 10, Fig. 59)
Description. Oocysts ovoid, yellow, with a micropyle, flattened at
the micropylar end, with a double-contoured, radially striated wall
(illustrated as composed of a single layer) 1.5 p. thick. Oocysts 24-
34 by 20-24 ,u with a mean of 29.7 by 21.2 /x. Oocyst polar granule
and residuum absent. Sporocysts described as ovoid, 10-14 by 4-6 /<.,
with a sporocyst residuum. Sporozoites elongate, lying lengthwise head
to tail in sporocysts.
Sporidation Time. Ten days in 1% potassium bichromate solution
at 15 C according to Yakimoff and jNIatchulski ( 1938) .
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Kobus (syn., Cob us) ellipsiprymnus (waterbuck).
Other Hosts. None.
genus Eimeria Schneider, 1875 79
Location. Oocysts found in feces.
Geographic Distribution. Leningrad zoo.
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
Host Suborder RUMINANTIA
Host Superfamily BOVOIDEA
Host Family BOVIDAE
Host Subfamily HIPPOTRAGINAE
Host Tribe ALCELAPHINI
Eimeria talboti Prasad and Narayan, 1963
(Plate 48, Fig. 196)
Description. Oocysts ovoid and asymmetrical, one side being
slightly more convex than the other, 35-38 by 22-28 /<. with a mean of
36 by 25 jx. Oocyst wall smooth, described as double-layered but
illustrated with a single layer, yellowish. Micropyle absent. Oocyst
residuum and polar granule absent. Sporocysts generally piriform,
without Stieda body, 12.5-15 by 9-10 jx with a mean of 14 by 10 //..
Sporocyst residuum absent. Sporozoites spindle-shaped, lying length-
wise in sporocysts with both broad ends at the large end of the sporo-
cyst, each with a large retractile globule at the rounded end.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepatent Period. Unknown.
Type Host. Alcelaphus cokei (syn., .4. cockei) (hartebeest, kongoni).
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. Africa (Kenya).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
Eimeria sp. Prasad and Narayan, 1963
Description. Oocysts ellipsoidal, 22-28 by 19-20 fi with a mean of
25 by 19 fi. Micropyle absent. Oocyst wall colorless, double-layered,
with the outer layer slightly thicker than the inner one. Oocysl polar
granule present. Oocyst residuum absent. Sporocysts lemon-shaped,
SO THE COCCIDIAN PARASITES OF RUMINANTS
with a prominent Stieda body and a very thick wall, 11-12.5 by 6-7 /x
with a mean of 11 by 6 /.<.. Sporocyst residuum not mentioned. Sporo-
zoites with one end broadly rounded and the other sharply pointed.
Sporulation Time. Unknown.
Schizogony ami Gametogony. Unknown.
Pre patent Period. Unknown.
Type Host. Alcelaphus cokei (syn., .4. cockei) (hartebeest, kongoni).
Other Hosts. None.
Location. Oocysts in feces.
Geographic Distribution. Africa (Kenya).
Pathogenicity. Unknown.
Cross-Transm ission Studies. None.
Prevalence. Unknown.
Remarks. Prasad and Narayan (1963) found only a few oocysts of
the species and therefore hesitated to name it.
Eimeria connochaetei N. Sp.
(Plate 48, Fig. 197)
Eimeria ellipsoidalis Becker and Frye, 1929 of Prasad, 1960.
[non] Eimeria ellipsoidalis Becker and Frye, 1929.
Description. Oocysts roughly ellipsoidal, 20-27 by 13-15 /<, with a
mean of 22.1 by 14.0 /.<.. Oocyst wall smooth, pale yellow, with double
membrane. Micropyle absent. Oocyst polar granule absent. Oocyst
residuum absent. Sporocysts ovoid, with small (? not illustrated)
Stieda body and sporocyst residuum. According to Prasad's text, the
sporocysts were 4.5-5 by 2.5-3 ,», ; however, either the oocysts were 22.1
by 14.5 /I. and contained sporocysts 7.6-8.4 by 3.8-4.6 n (oocyst di-
mensions from his text, and sporocyst dimensions calculated in relation
to them from the figure) or the oocyst was 34 by 22 /x and contained
sporocysts 12-13 by 6-7 \x (both oocyst and sporocyst dimensions cal-
culated from his figure). Sporozoites 4.5-5 by 1.5 /x, lying lengthwise in
sporocysts, with a clear globule at the large end.
Sporulation Time. According to Prasad (1960), complete sporula-
tion took 48 hours at room temperature in 2.5 r r potassium bichromate
solution.
Schizogony and Gametogony . Unknown.
Prepotent Period. Unknown.
Type Host. Connochaetes gnu (gnu, black wildebeest).
other Hosts. None.
genus Eimeria Schneider, 1S75 SI
Location. Oocysts found in feces.
Geographic Distribution. Tanganyika.
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
Remarks. Prasad (1960) called this species E. ellipsoidalis, pre-
sumably because it resembled that species (from the ox). However,
its sporocysts are smaller than those of E. ellipsoidalis, and the phy-
logenetic distance between the two hosts {Bos in the subfamily
Bovinae and Connochaetes in the subfamily Hippotraginae) also
suggests that it is a separate species.
Eimeria gorgonis Prasad, 1960
(Plate 50, Fig. 203)
Description. Oocysts ellipsoidal, 20.5-26 by 15-18 ,», with a mean
of 22.7 by 16.5 /<,. Micropyle absent. Oocyst wall smooth, composed
of 2 layers of which the outer is pale yellow and slightly thicker than
the colorless inner layer. Oocyst polar granule very small; oocyst
residuum absent. Sporocysts 12-15 by 4.5-6 /<., lemon-shaped with a
distinct neck, a prominent Stieda body, a retractile vacuole at the
narrow end, and a double membrane. Sporocyst residuum present.
Sporozoites club-shaped, lying head to tail lengthwise in sporocysts,
10-13 by 3 /i, with a clear globule at the large end.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Gorgon taurinus (brindled gnu, blue wildebeest I .
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. London zoo I from East Africa).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
Host Suborder RUMINANTIA
Host Superfamily BOV( >I I )EA
Host Family BOVIDAE
Host Subfamily ANTILOITNAE
Host Tribe ANTILOPI XI
82 THE COCCIDIAN PARASITES OF RUMINANTS
Eimeria antilocervi Rav and Mandal, 1960 emend.
Eimeria antelocerviHay and Mandal, 1960.
Description. Oocysts cylindrical, 28-34 by 12-16 /.<.. Oocyst wall
1.5-2.0 [x thick, light brown, presumably composed of a single layer.
Micropyle present, 1.5 fi wide. Oocyst polar granule not mentioned.
Oocyst residuum absent. Sporocysts piriform, 11 by 7 /'.. Sporocyst
residuum present.
Sporulation Time. According to Ray and Mandal (1960), sporula-
tion took 40-72 hours at 31 C in 2.59f potassium bichromate solution.
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Presumably Antilope cervicopra (antelope) (Ray and
Mandal, 1960, called the host "Antelopecervi caprae.")
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. India (Calcutta Zoo) .
Pathogenicity. Unknown.
Cross-Transmission Studies. Ray and Mandal (1960) were unable
to transmit this species to a young calf (presumably a zebu calf).
Prevalence. Unknown.
Eimeria impalae Prasad, and Narayan, 1963
( Plate 50, Figs. 205 and 206)
Description. Oocysts ellipsoidal, 30-36 by 20-24 ,u with a mean of
33 by 22 fi. Oocyst wall described as double-layered but illustrated as
composed of a single layer, smooth, yellowish green, with the inner
layer slightly thicker than the outer one. Micropyle 6 y. wide, covered
with ''a thickening of the outer wall like that of Eimeria stiedae of
the rabbit." Oocyst residuum and polar granules absent. Sporocysts
ovoid, with one end broadly rounded 8-14 by 7-9 /t with a mean of 11
by 8 ix. Stieda body described as not prominent but not illustrated.
Sporocyst residuum absent. Sporozoites spindle-shaped, 8-11 by 2-4 /.<.
with a mean of 10 by 3 fi, with a retractile globule at the broader,
rounded end.
Bigalke ( 1964 ) described a coccidium from the impala in South
Africa which he said was E. impalae. Since there is a question whether
lie was dealing with this species, it is described separately here. Oocysts
relatively robust, 33-45 by 22.5-31 /x with a mean of 39 by 27 /.i.
Oocysts ellipsoidal with the micropylar end slightly flattened and more
genus Eimeria Schneider, 1875 83
tapered than the opposite end. Micropyle formed by a thinning of the
oocyst wall, about 6 \x in diameter. Oocyst wall yellowish brown, about
2 \x thick; number of layers not stated but illustrated with a single
layer having a heavy inner line. Oocyst residuum and oocyst polar
granule absent. Sporocysts elongate ovoid, with inconspicuous Stieda
body, 18-21 by 7.5-9 /x. Sporocyst residuum composed of rather loosely
scattered granules which obscured the sporozoites. Sporozoites elongate,
presumably lying lengthwise in sporocysts, presumably with one large
clear globule at one end and 1 or 2 smaller ones elsewhere (Bigalke
could not distinguish the sporozoites with certainty).
Sportdation Time. Unknown.
Schizogony and Gametogony. Prasad and Narayan (1963) did not
describe the endogenous stages. Bigalke ( 1964 ) saw no structures
identifiable as schizonts, but found numerous gamonts, microgametes
and oocysts in the small intestine and rarely the cecum and colon.
The macrogametes were 9-10 \x in diameter when immature and grew
to about 21 by 17 /<, when mature. They had a layer of eosinophilic
granules around their periphery. Their host cells were virtually oblit-
erated, with only a compressed crescentic nucleus remaining; the para-
sites appeared to be distal to the nucleus. Both epithelial cells and
histiocytes appeared to be parasitized. The microgamonts were present
in the same location as the macrogametes. They were about 9 \x in
diameter when young and grew to 30-48 by 17.5-37.5 \x with a mean of
37 by 28 /.<.. The microgametes developed in a number of nuclear whorls
within the microgamonts, and became crescentic or filamentous and
about 3-4 jx long when mature.
Prepotent Period. Unknown.
Type Host. Aepyceros melampus (impala).
Other Hosts. None.
Location. Oocysts found by Prasad and Narayan (1963) in feces.
Endogenous stages found by Bigalke (1964) and Pienaar et al. (1964)
in the small intestine (posterior third of jejunum and ileum) and rarely
in the cecum and colon.
Geographic Distribution. Africa (Kenya, South Africa).
Pathogenicity. Prasad and Narayan (1963) found no evidence of
pathogenicity, but Pienaar et al. (1964) and Bigalke (1966) considered
this species highly pathogenic when young impala were brought to-
gether in small paddocks. Pienaar et al. described 3 outbreaks under
these conditions in South Africa; in the first, 26 animals died, in the
second 17 out of 27 animals, and in the third a single animal. The
most prominent sign was diarrhea; there was no dysentery. Dehydra-
84 THE COCCIDIAN PARASITES OF RUMINANTS
tion was also present. The intestine was virtually empty, and the
mucosa of the posterior third of the jejunum and ileum was thickened
and dull grayish-red, with numerous pinpoint- to pinhead-sized gray-
ish foci scattered throughout. There were numerous intense red, ir-
regular patchy areas from 1 cm in diameter to 7 cm long and involving
the whole width of the gut. There was also a small number of subendo-
and subepicardial petechiae. There was marked hyperemia of all layers
of the intestine, due lamina propria and submucosa were slightly
edematous. There did not appear to be definite cellular infiltration,
although there may have been a slight increase in numbers of plasma
cells and eosinophils in the propria.
The endogenous stages of the parasites (macrogametes, mieroga-
monts, microgametes and oocysts) were mainly in the epithelial cells
lining the crypts of Lieberkuehn. The infected glands were greatly
enlarged, and the blood vessels in the heavily infected part of the
intestine were markedly congested. Occasionally small groups of
organisms (mostly oocysts) were found in the lymph nodes in the
submucosa just below the muscularis mucosae; they were presumed to
he in macrophages, but some were extracellular.
The lumina of many crypts contained erythrocytes and desquamated
cellular debris.
( ' ros.s - Tra n s m iss io n St u dies . None .
Prevalence. Unknown.
Remarks. It is possible, as mentioned above, that the forms de-
scribed by Prasad and Narayan (1963) and Bigalke (1964) may have
belonged to different species, but for the present the evidence is not
considered sufficient to justify their separation.
Eimeria walleri Prasad, 1960
(Plate 50, Fig. 204)
Description. Oocysts roughly oval, 27-30 by 22-25 /i with a mean
of 28.5 by 23.5 <<.. Micropyle distinct, about 3 », wide. Oocyst wall
smooth, colorless, with a triple membrane. Oocyst polar granule and
oocyst residuum absent. Sporocysts broadly ovoid with a wall com-
posed of a double membrane, 8-11 by 5-6 /t (as stated by Prasad, 1960)
or either 10-11 by 6.5 or 12-13 by 7.6 // las determined by measuring
his drawing). Stieda body present, very small. Sporocyst residuum
present. Sporozoites roughly club-shaped, lying lengthwise head to tail
in sporocysts, with a clear globule at the large end.
Sporulation Time. According to Prasad (19601, a few sporulated
genus Eimeria Schneider, 1S75 S5
oocysts were present at the end of the 5th day at room temperature
in 2.5% potassium bichromate solution.
Schizogony and Gametogony. Unknown.
Preyatent Period. Unknown.
Type Host. Litocranius walleri (gerenuk).
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. London Zoo.
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
Eimeria elegans Yakimoff, and GoussefF
and Rastegaieff, 1932
(Plate 50, Fig. 2071
Description. Oocysts elongate ovoid, almost cylindrical, with one
end rounded and the other flattened, with a micropyle 3.6 ,u wide.
Oocyst wall composed of 2 layers. (Oocyst wall smooth, double con-
toured, yellow-green or yellow brown, and 1.1-1.8 n thick according
to Svanbaev, 1958.) Oocysts 23-45 by 18-23 /t with a mean of 34.2
by 19.8 /-. (37 by 20 ,x according to Yakimoff and Machul'skii, 1937b)
(32-39 by 16-25 /x with a mean of 35.1 by 21.7 /x according to Svan-
baev, 1958). Oocyst polar granule and residuum absent. (Polar gran-
ule sometimes present according to Svanbaev, 1958.) Sporocysts 10-14
by 6-9 i>, (9-13 by 7-11.5 /i with a mean of 10.7 by 8.8 \x according to
Svanbaev, 1958). Sporocyst residuum present. Sporocysts ovoid, short-
ovoid or spherical according to Svanbaev (1958). Sporozoites bean-
shaped, comma-shaped or piriform, 6-9 by 4-6 \x with a mean of 8 by
4.5 jx according to Svanbaev (1958). (5-11 by 2-4 /i according to
Yakimoff and Machul'skii, 1937b.)
Sporulation Time. Three to 5 days in 2 c /c potassium bichromate
solution at 25-28 C according to Svanbaev (1958) ; 7-8 days at 15 C
according to Yakimoff and Machul'skiT ( 1937b) .
Schizogony and Gametogony. Unknown.
Prepatent Period. Unknown.
Type Host. Gazella subguttarosa (goffered gazelle, zheiran,
dscheiran).
Other Hosts. Svanbaev (1956) described E. elegans from the saiga
Saiga tatarica in Kazakhstan. Oocysts ellipsoidal, 29-47 by 17-26 //
with a mean of 37 by 20.5 y.. colorless to greenish, yellow or lilac.
S6 THE COCCTDIAX PARASITES OF RUMINANTS
Oocyst wall smooth, double-contoured, 1.4-2.1 /x thick, with a micro-
pyle at one end. Oocyst polar granule present, sometimes absent.
Oocyst residuum absent. Sporocysts ovoid or spherical, 11-13 by 6.5-
11 n with a mean of 12 by 8 /<.. Stieda body not mentioned. Sporocyst
residuum present. Sporozoites bean-shaped, 7-8 by 5-6 /a, with a mean
of 7 by 5 ix. Despite its resemblance to E. elegans, the fact that Saiga
is in a different subfamily from Gazella makes us doubt whether the
form described by Svanbaev is actually E. elegans.
Location. Oocysts found in feces.
Geographic Distribution. USSR (Turkestan, Kazakhstan I.
Pathogen icit y. Unknown .
Cross-Transtnission Studies. None.
Prevalence. Svanbaev (1958) found this species in 12<^ of 17 G.
subgutturosa in Kazakhstan.
Eimeria spp. Rysavy, 1954
Eimcria arloingi Marotel, 1905 of Rysavy, 1954 in Gazella sub-
gutturosa.
Eimeria crandallis Honess, 1942 of Rysavy, 1954 in Gazella sub-
gutturosa.
Eimeria faurei Moussu and Marotel, 1901 of Rysavy. 1954 in Ga-
zella subgutturosa.
Eimeria ninae-kohl-yakimovi Yakimoff and Rastegaieva, 1930 of
Rysavy, 1954 in Gazella subgutturosa.
Description. None.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Gazella subgutturosa (goitered gazelle).
Other Hosts. See Remarks.
Location. Oocysts found in feces.
Geographic Distribution. Czechoslovakia.
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
Remarks. Rysavy (1954) reported the above 4 species of Eimcria
as occurring in Gazella subgutturosa in Czechoslovakia. The natural
host of E. arloingi and E. ninakohlyakimovae is the domestic goat, and
that of the others is the domestic sheep. Since Rysavy did not describe
any of them from the goitered gazelle, and since he attempted no cross-
transmission experiments, it is impossible to give them names; it is
genus Eimeria Schneider, 1S75 87
extremely doubtful that they actually belonged to the species to which
he assigned them.
Eimeria sp. Svanbaev, 1958
Eimeria ninae kohl-jakimov Jakimoff and Rastegaieff, 1930 of
Svanbaev, 1958.
Svanbaev (1958) gave the following information about "E. ninae
kohl-jakimov" that he found in 41% of 17 gazelles Gazella subguttu-
rosa in Kazakhstan: Oocysts oval, short-oval or spherical, 17-25 by
20-28 n with a mean of 19.8 by 24.2 /x. Oocyst wall smooth, double
contoured, greenish yellow green or brown, 1.2-1.7 /.i thick. Micropyle
absent. Sporocysts oval or short-oval, 5-8 by 6.5-11 fi with a mean of
8.7 by 6.4 fi. Sporozoites comma-shaped, 2-4 by 4-8 /x with a mean of
5.8 by 2.9 /i. Oocyst residuum absent. Sporocyst residuum present.
Sporulation time 2-3 days in 2% potassium bichromate solution at
25-28 C.
Host Suborder RUMINANTIA
Host Superfamily BOVOIDEA
Host Family BOVIDAE
Host Subfamily CAPRINAE
Host Tribe SAIGINI
Eimeria sajanica Machul'skif 1947
Description. Since Machul'skii's (1947) paper is not available to us,
we are using the information given by Svanbaev (1958) . Oocysts ovoid
or spherical, colorless, with a double-contoured wall up to 1.0 //. thick.
Oocysts 18-23 by 16.5-20 //. with a mean of 20.7 by 18.3 jx. Oocyst polar
granule and oocyst residuum absent, Sporocysts ovoid, 5-10 by 3-5 ».,
with a sporocyst residuum.
Sporulatio?i Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Saiga tatarica (saiga).
Other Hosts. None.
Location. Oocysts found in feces (?).
Geographic Distribution, USSR (Buryat-Mongolian ASSR).
Pathogenicity. Unknown.
Cross-Transm ission St udies. None.
Prevalence. Unknown.
SS THE COCCIDIAN PARASITES OF RUMINANTS
Eimeria saiga Svanbaev, 1958
(Plate 50, Fig. 208)
Description. Oocysts spherical, rarely short ovoid, 27-32 by 28-34
ji, with a mean of 29.5 by 30.5 () THE COCCIDIAN PARASITES OF RUMINANTS
Sporulation Time. Four to 6 days according to Supperer and Kutzer
(1961).
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Rupicapra rupicapra (chamois).
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. Europe (Austria, Germany, Italy, Lenin-
grad Zoo I .
Pathogenicity. Unknown.
Cross-Transmission Studies. Restani (1968) was unable to transmit
this species to a goat, a lamb or a calf.
Prevalence. Unknown.
Eimeria yakimoffmatschoulskyi Supperer
and Kutzer, 1961 emend.
( Plate 50. Fig. 212 ; Plate 61, Fig. 273 1
Eimeria yakinioff-matschoulskyi Supperer and Kutzer, 1961.
Eimeria arloingi Marotel, 1905 of Yakimoff and Matschoulsky,
1940.
Eimeria bohmi Supperer, 1952 of Bohm and Supperer, 1956.
Description. Oocysts ellipsoidal or ovoid, with a wall 1.0-1.5 [x
thick, yellowish, with a more or less distinct micropyle and colorless
micropylar cap which is easily lost. Oocyst wall illustrated as com-
posed of a single layer. Oocysts 24-32.5 by 18-22.5 /x ( 19.5-34 /x long-
according to Boch and Lucke, 1961; 23-31 by 17-23 \i with a mean
of 27.2 by 20.4 /-. according to Yakimoff and Matschoulsky, 1940).
Oocyst residuum absent. Oocyst polar granule absent. Sporocysts
ovoid, 9.5-12.5 by 7-9 ,u (8-12.5 by 6-8 \x according to Yakimoff and
Matschoulsky, 1940) , with sporocyst residuum. Sporocyst Stieda body
not mentioned. The oocysts measured by Restani (1968) were 27-
36.5 by 18-26 \x with a mean of 34 by 23.5 /.<.; the sporocysts averaged
13 by 7 ix.
Sporulation Time. Three to 5 days according to Supperer and
Kutzer ( 1961 1 .
Prepotent Period. Unknown.
Type Host. Rupicapra rupicapra (chamois).
Other Hosts. None.
Location. Oocysts found in feces.
genus Eimeria Schneider, 1S75 91
Geographic Distribution. Europe (Austria, Germany, Italy, Lenin-
grad Zoo).
Pathogenicity. Unknown.
Cross-Transmission Studies. Supperer and Kutzer (1961) were un-
able to transmit this species to the sheep or goat, Kutzer (1964) was
unable to transmit it to 2 sheep. Restani (1968) said that he infected
a goat and a lamb but not a calf with this species. The goat and lamb
became positive 8 days after exposure. However, he gave no informa-
tion on number of oocysts, and apparently made no pre-exposure
examinations.
Prevalence. Unknown.
Remarks. Supperer and Kutzer (1961) said that this was the species
previously reported from the chamois by Yakimoff and Matschoulsky
(1940) as E. arloingi and by Bohm and Supperer (1956) as E. bohmi.
Eimeria alpina Supperer and Kutzer, 1961
(Plate 52, Fig. 217)
Description. The following description is based on Supperer and
Kutzer (1961) and Kutzer (1964). Oocysts almost always spherical,
10-14 jx in diameter. Oocyst wall composed of one layer, very thin,
colorless, smooth, without micropyle. Oocyst residuum and polar
granule absent. Sporocysts subspherical, 5-6 by 4-5.5 //,, without sporo-
cyst residuum. Sporozoites illustrated as elongate, lying head to tail
in sporocysts.
Sporulation Time. Unknown.
Prepatent Period. Unknown.
Type Host. Rupicapra rupicapra (chamois).
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. Europe (Austria).
Pathogenicity. Unknown.
Cross-Transmission- Studies. Kutzer (1964) was unable to transmit
this species to 2 sheep.
Prevalence. Unknown.
Eimeria suppereri Kutzer, 1964
(Plate 52, Fig. 215)
Description. Oocysts ellipsoidal, generally 43-49 by 32-37 /i with a
92 THE COCCIDIAX PARASITES OF RUMINANTS
mean of 45 by 34 /t. Oocyst wall composed of 2 layers, the outer one
1.5-2.0 p. thick, rough, brown, with a micropyle, and relatively difficult
to separate from the inner layer, which is colorless to yellowish and
about 1 (i thick. One or 2 oocyst polar granules present ; oocyst resid-
uum absent. Sporocysts drop-shaped, 16-19 by 9-11 fi, with sporocyst
residuum.
Sporulation Time. Generally 12-14 days at 25 C in 1.5% potassium
bichromate solution according to Kutzer (1964 ) .
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Rupicapra rupicapra (chamois).
Other Hosts. None.
Location. Oocysts in feces.
Geographic Distribution. Europe (Austria).
Pathogenicity. Unknown.
Cross-Transmission Studies. Kutzer (19641 was unable to transmit
this species to 2 sheep.
Prevalence. Unknown.
Eimeria spp. of Rysavy, 1954 and of Delic
and Cankovic, 1961
Eimeria arloingi Marotel, 1905 of Rysavy, 1954 and of Delic and
Cankovic, 1961 in Rupicapra rupicapra.
Eimeria crandallis Honess, 1942 of Rysavy, 1954 in Rupicapra
rupicapra.
Eimeria ninae-kohl-yakimovi Yakimoff and Rastegaieva. 1930 of
Rysavy, 1954 and of Delic and Cankovic, 1961 in Rupicapra rupicapra.
Eimeria parva Kotlan, Moczy and Vajda. 1929 of Rysavy, 1954 in
Rupicapra rupicapra.
Description. Xone.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Rupicapra rupicapra (chamois).
Other Hosts. See Remarks.
Location. Oocysts in feces.
Geographic Distribution. Czechoslovakia, Yugoslavia.
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
genus Eimeria Schneider, 1S75 93
Remarks. Rysavy (1954) reported the above 4 species of Eimeria
as occurring in Rupicapra rupicapra in Czechoslovakia and Delic and
Cankovic (1961) reported E. arloingi and E. ninakohlyakimovae from
the same host in Yugoslavia. The natural host of E. arloingi and E.
ninakohlyakimovae is the domestic goat and that of the others is the
domestic sheep. Since Rysavy did not describe any of them from the
chamois, and since he attempted no cross-transmission experiments, it
is impossible to give them names; it is extremely doubtful that they
actually belonged to the species to which he assigned them.
Eimeria longispora Rudovsky, 1922
Description. Rudovsky (1922) reported finding this species in cham-
ois feces in Austria. His complete description was, "Die eine Form
wird wegen der Sporozoitengestalt Eimeria longispora benannt und ist
neu." Obviously, this description is so incomplete that the form can
never be recognized, and the name Eimeria longispora must be con-
sidered a nomen nudum.
Host. Rupicapra rupicapra (chamois).
Other Hosts. Pellerdy (1963, 1965) gave the domestic goat and
domestic sheep as hosts, but we have not seen this species reported from
these hosts.
Remarks. Pellerdy (1965) said that he had never read the original
description of this species, but thought it advisable to invalidate it
because "the few references in the literature to that description show
it to be rather imperfect."
Eimeria oreamni Shah and Levine, 1964
(Plate 52, Fig. 216)
Description. Oocysts elongate ovoid, slightly piriform, 26-34 by
17-20 ji with a mean of 29 by 19 /.<.. Oocyst wall composed of 2 layers,
the outer smooth, pale greenish-yellow to yellowish-brown, about 1 /t
thick, the inner layer brownish-yellow, about 0.4 ^ thick. Oocyst lined
by a membrane apparently formed by the inner layer and usually
slightly wrinkled at the micropylar end. Micropyle at small end of
oocyst, about 2 /x wide. Micropylar cap absent. Oocyst polar granules
present, fragmented. Oocyst residuum absent. Sporocysts broadly
ovoid, with tiny Stieda body, 10-12 by 7-9 fx with a mean of 11 by 8 /.<..
Sporocyst residuum present, usually consisting of granules scattered
9-i THE COCCIDIAX PARASITES OF RUMINANTS
loosely in sporocyst. Sporozoites elongate, one end narrower than the
other, lying lengthwise head to tail in sporocysts. A single large, clear
globule at one end of sporozoite; sometimes one or more additional
smaller clear globules present in each sporozoite.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Oreamnos americanus (Rocky Mountain goat).
Other Hosts. None.
Location. Unknown. Oocysts found in feces.
Geographic Distribution. North America (Montana).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
Remarks. Todd and O'Gara ( 1968) also found this species in an 0.
americanus from Montana.
Eimeria ernsti Todd and O Gara, 1968
(Plate 51, Fig. 213)
Eimeria ernesti Todd and O'Gara (1968). Lapsus calami.
Description. Oocysts ellipsoidal, sometimes with nearly flat sides,
28-37 by 19-25 /x with a mean of 33 by 23 /i. Oocyst wall smooth, com-
posed of 2 layers and an inner membrane, 1.8-2.3 [i thick. Outer layer
light brown, about % of total wall thickness; inner layer dark brown.
Inner membrane wrinkled in micropylar area. Micropyle present.
Micropylar cap present, 7-11 ». wide and 2-4 /x high with a mean of
9 by 3 ji. Oocyst residuum absent. Oocyst polar granule present in
freshly sporulated oocysts, rare in older oocysts. Sporocysts elongate
ovoid, 14-20 by 6-9 /.<, with a mean of 17 by 7 /a. Stieda body distinct.
Sporocyst residuum present. Sporozoites located at an angle near each
end of sporocyst. Sporozoites with single large retractile wrinkled
globule.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Oreamnos americanus (Rocky Mountain goat).
Other Hosts. None.
Location. Unknown. Oocysts found in feces.
Geographic Distribution. North America (Montana).
Pathogenicity. Unknown.
genus Eimeria Schneider, 1875 95
Cross-Transmission Studies. None.
Prevalence. Unknown.
Eimeria montanaensis Todd and O Gara, 1968
(Plate 51, Fig. 214)
Description. Oocysts subspherical to ellipsoidal, flattened at micro-
pylar end, 15-23 by 13-19 /x with a mean of 19 by 15 p.. Oocyst wall
smooth, composed of 2 layers about 1.5-2.0 /i thick; outer layer light
blue, about % of total wall thickness; inner layer light brown. Micro-
pyle present, 2-3.5 i± wide. Small micropylar cap on 6% of oocysts.
Oocyst residuum absent. Oocyst polar granule present, sometimes
fragmented into as many as 5 pieces. Sporocysts broadly to elongate
ovoid, 8-12 by 4-7 /x with a mean of 10 by 5 /i. Sporocyst residuum
composed of a few fine granules between sporozoites. Stieda body
small. Sporozoites blunt, located at an angle near each end of the
sporocyst. A large and a small retractile globule present in each
sporozoite.
Spondation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepatent Period. Unknown.
Type Host. Oreamnos americanus (Rocky Mountain goat).
Other Hosts. None.
Location. Unknown. Oocysts found in feces.
Geographic Distribution. North America (Montana).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
Host Suborder RUMINANTIA
Host Superfamily BOVOIDEA
Host Family BOVIDAE
Host Subfamily CAPRINAE
Host Tribe CAPRINI
Eimeria arloingi (Marotel, 1905) Martin, 1909
(Plate 52, Figs. 218-221; Plate 53, Figs. 222-223; Plate 54. Figs.
224-225)
Coccidium arloingi Marotel, 1905.
96 THE COCCIDIAN PARASITES OF RUMINANTS
Eimeria ahsata Honess, 1942 of Chevalier (1966) from the goat,
non E. ahsata Honess, 1942 of Chevalier (1965) from the sheep.
Eimeria crandallis Honess, 1942 of Chevalier (1966) from the goat.
Eimeria faurei (Moussu and Marotel, 1902) of Tsygankov, Palclmk
and Balbaeva (1963) and of some other Russian authors.
Description, The following description is based on Levine, Ivens
and Fritz (1962), Shah and Joshi (1963), Chevalier (1966) and Savin
(1965). Oocysts ellipsoidal or slightly ovoid, slightly flattened at the
micropylar end, 22-36 by 16-26 p with a mean of 28 by 19-21 ,x.
Oocyst wall composed of 2 layers, the outer one smooth, colorless, 1.0
/x thick, and the inner one brownish yellow, 0.4-0.5 /x thick. The inner
layer forms a membrane which is often slightly wrinkled at the micro-
pylar end. Micropyle present at small end of oocyst. Micropylar cap
prominent, colorless, mound-shaped, 0.4-3.0 /x high and 4-9 /x wide
with a mean of 2 by 6-7 jx. One or more oocyst polar granules ordi-
narily present; they sometimes appear to be shattered into many
rather fine particles. Oocyst residuum absent. Sporocysts elongate
ovoid, with a rather truncate small end. Stieda body absent or vestig-
ial. Sporocysts 11-17 by 6-10 /.<, with a mean of 13-15 by 7-8 /.<. (10
by 5 jx according to Singh, 1964). Sporocyst residuum present. Sporo-
zoites elongate, lying lengthwise, head to tail, in sporocysts. Sporo-
zoites usually contain a large, clear globule at the large end and a
small one at the small end.
Sporulation Time. Two to 4 days according to Chevalier (1966),
60 hours at 20 C according to Savin (1965), or 1-2 days at room tem-
perature in India (Singh, 1964).
Schizogony and Gametogony. Uncertain. Levine, Ivens and Fritz
1 1962) found 2 types of schizont in a kid infected with E. arloingi,
E. christenseni and E. crandallis. It is possible (but not proven) that
they may have been those of E. arloingi. Giant schizonts up to 280 by
150 jx were present in endothelial cells of lacteals in the jejunum. They
were surrounded by 2 layers of eosinophilic material. They saw dif-
ferent developmental stages of these schizonts. Some contained a
number of groups of nuclei arranged in circles, others contained nuclei
quite evenly distributed through the whole schizont, and still others
contained fully developed merozoites. These last were straight, with
one end rounded, and tapered to a point at the other end. They were
about 10-12 by 0.8-1.2 /x, with vesicular, ellipsoidal to spherical nuclei
without an endosome, about 1.3-1.5 /x in diameter, and lay at the wider
end of the merozoite with no cytoplasm discernible between them and
the end of the cell. The merozoites lay side by side in clusters like
bundles of sticks within the schizonts, with the nuclei of each cluster
genus Eimeria Schneider, 1S75 97
all at the same end. Each giant schizont contained approximately
100,000 merozoites.
One collapsed giant schizont, which had released the great majority
of its merozoites, was found in a lacteal. Most of the epithelial cells
of the villi and glands in its vicinity contained merozoites which had
apparently penetrated them only recently and which were in the pro-
cess of rounding up. These merozoites lay above the host cell nuclei
and were surrounded by a clear area about 3-5 /x in diameter. The
rounded-up merozoites were about 3 /x in diameter and contained vesic-
ular nuclei about 1 /.<, in diameter with a small, central endosome.
A second type of schizont was present in some glands of the jejunum.
Large numbers of these small schizonts and of single merozoites lay
rather deep in the glands of Lieberkuehn, where they occurred in
groups. The mature small schizonts lay above the host cell nuclei of
the epithelial cells, enlarging the host cell somewhat. They were about
10-14 by 9-10 n with a mean of 12 by 9 /x and appeared to contain
16-22 merozoites each. The merozoites lay parallel to each other like
a bundle of sticks. They were straight, elongate lanceolate, with one
end rather bluntly rounded and the other drawn out more. They were
about 9 by 0.8 /x and had a vesicular nucleus without a central endo-
some, about 2.2 by 1.0 \x which was about 1 \x or less from the large
end of the merozoites.
There were numerous diffusely scattered pale yellow to white focal
plaques about 0.5 cm in diameter in the mucosa of the duodenum, jeju-
num and ileum; a few were present in the first third of the colon. The
plaques consisted essentially of masses of macrogametes, microgamonts
and young oocysts in the epithelial cells of the tips and sides of the villi
and also in the crypts. The parasites ordinarily lay above the host
cell nuclei, and multiple infections of the same host cell were the
rule. The mature macrogametes were 12-24 by 8-15 \x with a mean of
16 by 12 fi in stained sections. The mature microgamonts were 11-26
by 8-16 fx with a mean of 16 by 11.5 /i and contained crescentic or
comma-shaped microgametes about 3.5 jx long and 0.4 /l wide. The
young oocysts were 19-26 by 12-18 /x with a mean of 24 by 15 /<.. and
often had discernible micropylar caps.
Levine, Ivens and Fritz (1962) concluded that the giant schizonts
which they described were probably those of E. arloingi and that the
small schizonts and sexual stages were those of either E. arloingi, E.
crandallis, E. christenseni or a fourth species which had not yet begun
to produce oocysts in the feces. Savin (19651 found giant schizonts
up to 141 by 100 jx in endothelial cells of the lacteals in the villi of the
ileum in Angora goats. He found no other schizonts. lie found
98 THE COCCIDIAX PARASITES OF RUMINANTS
gamonts and oocysts in the epithelial cells of the tips and sides of the
villi and also in the crypts in the small intestine, where they formed
pale yellow to white plaques 0.3-0.4 mm in diameter.
P. P. Singh and Pande (1967) and Pande et al. 1 1967) found en-
dogenous stages in the small intestine of goats in India that they
thought were those of E. arloingi. However, they were dealing with
mixed infections.
Prepotent Period. Unknown.
Type Host. Capra hircus (domestic goat).
Other Hosts. Capra aegagrus, C. falconeri (see Rysavy, 1954), C.
ibex (see Couturier, 1962; Pellerdy, 1965), C. sibirica (called E. faurei
by Svanbaev, 1958). See Remarks for reports from additional hosts.
Location. Small intestine.
Geographic Distribution. Worldwide.
Pathogenicity. Uncertain. Deiana and Delitala (1953b) reported
that E. arloingi gamonts and gametocytes had caused hyperplasia of
the small intestine with pseudo-adenomatous metaplasia of the villi,
atrophy of the crypts of Lieberkuehn and cellular infiltration of the
mucosa in kids. Gill and Katiyar (1961) described an outbreak of
enteritis associated with lesions in the ileum in 12 kids 1-2 months old
in India which they considered due to E. arloingi. Sharma Deorani
(1966) also described lesions in the small intestine of 4 naturally in-
fected goats in India which he considered due to E. arloingi; he did
not describe the oocysts. The lesions in the small intestine seen by
Levine, Ivens and Fritz ( 1962) in a kid in Illinois have been described
above. However, in both cases it is uncertain whether the enteritis
was caused by E. arloingi or by another coccidium. Savin (1965)
found white to pale yellow plaques 0.3-0.4 mm in diameter, with ir-
regular edges in the small intestine of Angora goats in Turkey. The
feces of one kid were watery.
Cross-Transmission Studies. Deiana and Delitala (1953a) at-
tempted to transmit "Eimeria arloingi" (probably a mixture of several
species of Eimeria with capped micropyles) from the goat to two 1-
month-old lambs, two 1 -month-old rabbits and two 40-day-old guinea
pigs. They found a few oocysts in the lambs 4-10 days after exposure,
but none in the rabbits and guinea pigs; they did not describe the
oocysts they found, nor did they establish that the lambs were coccidia-
free to begin with. Krylov ( 1961 ) was unable to transmit this species
from the goat to 3 lambs 1.5 months old. Tsygankov, Palchuk and
Balbaeva (1963) were unable to transmit E. arloingi (which they
called E. faurei) from the goat to one saiga and one lamb, although
they produced a patent infection in a kid. No other valid cross-
transmission attempts have apparently been made.
genus Eimeria Schneider, 1875 99
Prevalence. Balozet (1932a) found this species in 56% of 41 goats
in Tunisia. Jacob (1943) found it in 18% of 11 goats in Germany and
Chevalier (1966) in at least 39% of 40 goats in the same country.
Svanbaev (1957) found it in 52% of 48 goats in Kazakhstan. Sayin
( 1965, 1966) found this species in 77% of 900 Angora goats in Turkey.
Wiesenhiitter (1965) found it in 95% of 413 goats in Syria. Shah and
Joshi (1963) found it in 31% of 300 goats in Madhya Pradesh, India.
Singh (1964) found it in 84% of 214 goats, and Jha and Subramanian
(1966) in 69% of 243 goats in Uttar Pradesh, India. Fernando (1957)
found it in 43% of 62 goats in Ceylon.
Remarks. As stated under E. ovina below, the evidence indicates
that the li E. arloingi" of sheep will not develop completely in the goat.
In addition, Krylov (1961) and Tsygankov, Paichuk and Balbaeva
( 1963) were unable to transmit E. arloingi from the goat to sheep.
Furthermore, there are certain structural differences between the
oocysts of the 2 forms; the goat form is ellipsoidal while the sheep
one generally has rather straight sides. For these reasons we think it
best to consider the forms from these hosts to be different species, and
to use the name E. arloingi for the goat form only.
Until it is proven otherwise, we feel it best not to consider as E.
arloingi those coccidia reported by various authors from ruminants of
genera other than Capra. These include Oris aries, O. canadensis, O.
ammon, O. musimon, the tahr Hcmitragus jemlahicus, the chamois
Rupicapra rupicapra, the red deer Cervus elaphus, the fallow deer
Dama dama, the roe deer Capreolus capreolus and the gazelle Gazella
subgutturosa (Jacob, 1943; Rysavy, 1954; Svanbaev, 1958; Delic and
Cankovic, 1961; Pellerdy, 1965).
Chevalier (1966) reported as E. ahsata, E. arloingi, and E. cran-
dallis forms which he found in the goat in Germany and which differed
only in oocyst and sporocyst dimensions. These differences were not
great, however; although they were statistically significant, the work
of Becker et al. ( 1956) on E. necatrix of the chicken proved that statis-
tically significant size differences occurred at different periods after an
infection became patent. Hence, such variations in size cannot be
justified as a basis for differentiating species. Consequently we con-
sider that the above 3 "species" of Chevalier were actually E. arloingi.
Eimeria ninakohlyakimovac Yakimoff
and Rastegaieff, 1930 emend. Levine, 1961
l Plate 55, Figs. 226-230)
Eimeria nina-kohl-yakimovi Yakimoff and Rastegaieff. 1930.
100 THE COCCIDIAX PARASITES OF RUMINANTS
Eimeria galouzoi Yakimoff and Rastegaieff, 1930 pro parte.
Description. E. ninakohlyakimovac was first described by Yaki-
moff and Rastegaieff (1930) from the goat. The following description
is based on those of the above authors and of Shah and Joshi (1963),
Singh (1964), Savin (1964) and Chevalier (1966) from the goat.
Oocysts ellipsoidal or subspherical to somewhat ovoid, slightly narrow
at the micropylar end, 19-28 by 14-23 /.<.. Oocyst wall composed of 2
layers, the outer one smooth, colorless to slightly yellowish and 1 /x
thick, and the inner one yellowish-brown, 0.4 /x, thick. Micropyle
present at small end of oocyst (not reported by Yakimoff and Raste-
gaieff, 1930). Micropylar cap absent. Oocyst polar granule or gran-
ules present (Savin, 1965, said that there was none). Oocyst residuum
absent. Sporocysts elongate ovoid, 9-14 by 4-10 /x. Stieda body pres-
ent. Sporocyst residuum present. Sporozoites elongate, lying length-
wise head to tail in sporocyst, with one or 2 clear globules.
The following description is based on those of Christensen (1938b),
Shah (1963), Jackson (1964) and Chevalier (1965) from the sheep.
Oocysts usually ellipsoidal or subspherical to somewhat ovoid, 16-30
by 13-22 [x with a mean of 23 by 18 /x (Christensen) or 26 by 20 /x
(Shah; Jackson). Oocyst wall composed of 2 layers, the outer one
smooth, colorless to slightly greenish yellow, 1 /x thick, the inner one
yellowish brown, 0.4 /x thick; oocyst lined by a membrane often
wrinkled at the micropylar end. Micropyle present at small end of
oocyst. Micropylar cap absent. Two or more oocyst polar granules
ordinarily present (Chevalier and Christensen saw none). Oocyst
residuum absent. Sporocysts elongate ovoid, 10-14 by 4-8 /x with a
mean of 12 by 7 p. (Shah) or 13 by 8 /x (Jackson). Stieda body present.
Sporocyst residuum present. Sporozoites elongate, lying lengthwise
head to tail in sporocysts. Sporozoites with one large and one small
clear globule.
Sporulation Time. One-2 days according to Christensen (1938b),
3-4 days according to Balozet (1932a), 60 hours at 20 C according to
Savin (1964) or 1-3 days according to Singh (1964) and Chevalier
(1965).
Schizogony and Gametogony. Balozet (1932a) and Savin (1965)
described the endogenous stages in the goat, and Lotze (1954) de-
scribed them briefly from the sheep. Since their accounts differed,
they are given separately below.
Balozet (1932b, c) found in a kid killed 39 days after infection that
the schizonts were 15-35 /x in diameter and contained 40-200 mero-
zoites 1.5-2 /x in diameter. The schizonts were in the epithelial cells
of the glands of Lieberkuehn in the duodenum 3-4.5 meters from its
genus Eimeria Schneider, 1875 101
anterior end. The microgamonts were 45-50 /x in diameter, apparently
in the same type of host cell. The microgametes were 3-4 [x long and
had a flagellum 1-2 /x long. The macrogametes were apparently in
the same type of host cell ; Balozet did not give their size.
Sayin (1964) found one type of schizont in Angora goats. The
schizonts were ellipsoidal or round, 31-43 by 22-31 \x with a mean of
37 by 26.5 \x\ they were in the epithelial cells of the ileum, cecum and
upper part of the large intestine. Gamonts and oocysts were present
in the same location. The mature macrogametes were 9-18 by 7-13 \x
with a mean of 13.5 by 10 \x. The microgamonts were 20-25 by 15-18
ji with a mean of 22.5 by 16.5 /<. and had whorls of microgametes on
their surface and some residual material in the center.
Lotze (1954) found in sheep that the sporozoites entered the epithe-
lial cells at the base of the glands of Lieberkuehn in the small intestine,
where they formed schizonts about 300 /x in diameter containing thou-
sands of merozoites. The macrogametes and microgamonts occurred
in the epithelial cells of the ileum, cecum and upper part of the large
intestine, appearing 15 or more days after infection.
Svanbaev (1967a) found that the patent period in 4 lambs was
8-10 days.
It is possible that Balozet, Sayin and Lotze were dealing with dif-
ferent species, or that Balozet and Sayin may have seen second genera-
tion merozoites not mentioned by Lotze.
N. Singh and Pande (1967) found endogenous stages in the small
intestine of sheep in India that they thought were those of E. nina-
kohlyakimovae. However, they were dealing with mixed infections.
Prepatent Period. Balozet (1932b, c) found that the prepatent
period was 10-13 days in goats; Shumard (1957a) found that it was
15 days in lambs, Krylov (1961) that it was 14 days in one lamb,
Svanbaev (1967a) that it was 11-13 days in 4 lambs, and Hammond,
Kuta and Miner (1967) that it was 9-10 days in most of 75 2.5-3.5-
month-old lambs following inoculation of oocysts in dry or pelleted
feed. The patent period was 10-28 days and peak oocyst production
occurred 9-16 days after inoculation.
Type Host. Capra hircus (domestic goat).
Other Hosts. Capra aegagrus (wild goat), (Rysavy, 1954); C. sibi-
rica (Siberian wild goat) (Rysavy, 1954; Svanbaev, 1958); C. ibex
(Alpine ibex) (Couturier, 1962); Oris aries (domestic sheep) (many
authors); O. canadensis (bighorn sheep) (Honess, 1942); O. musimon
(mouflon) (Yakimoff, Gousseff and Rastegaieff, 1932b; Rysavy. 1954 I :
O. amnion (argali) (Rysavy, 1954; Svanbaev, 1958). In addition.
Yakimoff and Matikaschwili (1933) reported this species from a
102 THE COCCIDIAN PARASITES OF RUMINANTS
Gazella subgutturosa from Transcaucasia; Rysavy (1954) reported it
from Capreolus capreolus, Cervus elaphus, Duma da ma, Rupicapra
rupicapra and Gazella subgutturosa; Svanbaev (1958) reported it from
G. subgutturosa and Saiga tartarica and Delic and Cankovic (1961)
from R. rupicapra. "Whether this species actually occurs in hosts other
than Capra and Oris is doubtful.
Location. Small intestine, especially the posterior part, and also
cecum and colon.
Geographic Distribution. Worldwide.
Pathogenicity. Balozet (1932a) observed a case of mucosanguinous
diarrhea followed by death in a naturally affected adult goat, and pro-
duced the disease experimentally in 2 newborn kids. A mucous diar-
rhea appeared 22 days after infection, became bloody, and persisted
until about the 39th day. Savin (1964) found numerous round, smooth
white plaques about 0.2-0.3 mm in diameter in the mucosa of the small
intestine, cecum and colon. There was slight to moderate enteritis.
The cellular reaction consisted of lymphocytes and polymorphonuclear
leucocytes.
This is one of the most pathogenic of sheep coccidia. Svanbaev
( 1967b) observed clinical effects in 3 of 4 40-day-old lambs fed about
10,000 oocysts. Diarrhea, sometimes dysentery, fever, depression, in-
appetance, anemia, loss of weight, and loose wool were among the
symptoms. Lotze ( 1954) found that as few as 50,000 oocysts caused
diarrhea in a 3-month-old lamb; as few as 500,000 oocysts caused
death. He produced dysentery in a 2-year-old sheep by inoculation
with as few as 1 million oocysts. Smith and Davis (1965) found that
only 20,000 oocysts caused death and only 10,000 caused clinical signs
in lambs if the oocysts were given in dry feed rather than in liquid.
Lotze (1954) found that the feces of experimentally infected lambs
became soft in 12-17 days. They became watery a day or two later
and remained so for a week or more. The feces of the more heavily
infected lambs contained blood-stained mucus beginning 15 days after
infection or soon thereafter. The feces of those animals which re-
covered remained soft for some weeks.
Hammond, Kuta and Miner (1967) found in lambs 2.5-3.5 months
old given oocysts in dry feed that 48,500 oocysts produced diarrhea
lasting 3-11 (mean 7) days and dysentery lasting 3-10 (mean 6) days;
2 of 11 lambs died 16-21 days after inoculation. In lambs given 58,200
oocysts, the diarrhea lasted 5-9 (mean 6.6) days and the dysentery 0-4
(mean 1.4) days; no lambs died. In lambs given 97,000 oocysts, the
diarrhea lasted 4-12 (mean 7) days and the dysentery 4-8 (mean 5.5)
days; 6 of 10 lambs died 14-22 days after inoculation. In all groups
genus Eimeria Schneider, 1S75 103
diarrhea began 10-11 days and dysentery 11-12 days after inoculation.
At necropsy, Lotze (1954) found petechial hemorrhages in the small
intestine 3-7 days after infection. The small intestine then became
thickened and inflamed. There was extensive hemorrhage in the pos-
terior small intestine of severely affected lambs by the 15th day. The
cecum and upper part of the large intestine became thickened and
edematous, and were hemorrhagic by the 19th day. Vast areas of the
posterior small intestine of heavily infected lambs were denuded.
Svanbaev (1967a) noted similar lesions in the small intestine, and
also saw white pinhead nodules in the jejunum and ileum.
Shumarcl (1957b) studied a less pathogenic strain. He observed
lowered feed consumption, lassitude, generalized incoordination and
slight diarrhea with some bleeding in 50-day-old lambs experimentally
inoculated with 7 million oocysts of E. ninakohlyakimovae plus 100,000
oocysts of E. faurei. Clinical signs appeared 9 days after inoculation
and ended about the 22nd day. One out of 4 lambs died on the
15th day.
Cross-Transmission Studies. Balozet (1932a) was unable to infect
a recently weaned lamb with E. ninakohlyakimovae from a goat, al-
though he did infect 2 newborn kids; he thought that the lamb was
too old. Krylov (1961) failed to infect 2 yearling goats with E. nina-
kohlyakimovae from sheep, although lie did infect a 2-month-old lamb.
Lotze et al. (1961) failed to infect 6-month-old goats with E. nina-
kohlyakimovae from sheep or 4-month-old sheep with this species
from the goat; at any rate, they found no oocysts in the feces. Lotze
et al. (1964) found schizonts of an unknown coccidial species in the
mesenteric lymph nodes of 2- and 7-month-old goats fed a mixture
of 70% E. arloingi, 25 c /c E. ninakohlyakimovae and 5% E. faurei
oocysts from the sheep. Tsygankov, Paichuk and Balbaeva (19631
were unable to transmit E. ninakohlyakimovae from the slice]) to one
saiga and 4 kids, although they produced a patent infection in a lamb.
They were unable to transmit E. ninakohlyakimovae from the goat to
one saiga and one lamb although they produced a patent infection with
it in a kid. Fitzsimmons (1964) infected 2 coccidia-free kids aged 50
and 58 days with E. ninakohlyakimovae from sheep; oocyst production
was lower than in a control lamb. In an uncontrolled experiment.
Subramanian and Jha (1966) said that they transmitted E. nina-
kohlyakimovae from the goat to a lamb by feeding it 50,000 oocysts.
In the absence of Fitzsimmons' and Subramanian and , Ilia's findings,
it would be safe to say that the form in the sheep belongs to a different
species from that in the goat. However, under the present circum-
stances, it appears that they may be different strains or denies of (lie
104 THE COCCIDIAN PARASITES OF RUMINANTS
same species. Further work should be done to resolve this question.
Prevalence. Balozet 1 1932a) found this species in 34% of 41 do-
mestic goats in Tunisia; Svanbaev (1957) in 31% of 48 goats in
Kazakhstan; Chevalier (1966) in 12 c c of 40 goats in Germany; Mer-
divenci (1959) in 36% of the goats he examined in Turkey; and Savin
( 1964. 1966 ) in 23% or 25% of 900 Angora goats in Turkey. Wiesen-
hiitter ( 1965) found it in 56% of 642 sheep and 60% of 413 goats in
Syria; Shah and Joshi ( 1963) in 12% of 300 goats in Madhya Pradesh,
India; Singh (1964) in 23% of 214 goats and Jha and Subramanian
( 1966) in 53% of 243 goats in Uttar Pradesh, India.
Christensen (1938b) found it in 3% of 100 sheep from Maryland
and Idaho; Hammond and Hamilton (1940, 1941) in 4% of 50 sheep
in northern Utah; Shah (1963) in 1% of 153 sheep from Illinois and
other states; Joyner et al. (1966) in 88% of 198 sheep in England;
Jacob (1943) in 5% of 100 sheep in Germany; Chevalier (1965) in
26% of 200 sheep in Germany; Patyk (1965) in 26% of 222 lambs
aged 1-8 months in Poland; Delic (1955) in 14% of the sheep and
lambs he examined in Yugoslavia; Merdivenei (1959) in 13% of the
sheep he examined in Turkey; Balozet (1932a) in 35% of 63 sheep
in Tunisia; and Svanbaev (1957) in 52% of 302 sheep in Kazakh-
stan, USSR.
Remarks. The results of cross-transmission experiments described
above bring into question whether sheep and goats both have E. nina-
kohlyakimovae. The oocysts reported under this name from hosts of
other genera are probably not E. ninakohlyakimovae.
Eimeria christenseni Levine, Ivens and Fritz, 1962
(Plate 55. Fig. 234)
Description. The following description is based on Levine, Ivens
and Fritz (1962). Shah and Joshi (1963), Shah (1965) and Chevalier
( 1966l Oocysts ovoid, sometimes ellipsoidal, slightly flattened at
micropylar end, 32-44 by 22-30 /.«. with a mean of 38-39 by 25-26 ,x.
Oocyst wall composed of 2 layers, the outer one smooth, colorless to
very pale yellowish, about 1.0 » thick, and the inner one brownish
yellow. 0.4 /i thick. The inner layer forms a membrane which is usu-
ally wrinkled at the micropylar end. Micropyle present, at small end
of oocyst. Micropylar cap prominent, colorless, mound-shaped, 1-4 /./.
high and 2-10 /j. wide with a mean of 2-3 by 7-8 (jl. One or more oocyst
polar granules present, sometimes partly shattered into many rather
fine particles. Oocyst residuum absent. Sporocysts broadly ovoid,
genus Eimeria Schneider, 1875 105
14-18 by 8-11 ju with a mean of 15-16 by 9-10 fi. Stieda body absent
or vestigial. Sporocyst residuum present. Sporozoites lie lengthwise,
head to tail, in sporocysts. Sporozoites contain a large, clear globule
at one end and sometimes one or more additional smaller, clear
globules.
Sporulation Time. Six days according to Chevalier ( 1966) .
Schizogony and Gametogony. Unknown. See the discussion of E.
arloingi.
Prepatent Period. Unknown.
Type Host. Capra hircus (domestic goat) .
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. United States (Illinois) , Europe (Ger-
many), India (Madhya Pradesh, Uttar Pradesh), Africa (Senegal).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Shah and Joshi (1963) and Shah (1965) found this
species in 5% of 300 goats in Madhya Pradesh and Jha and Subra-
manian (1966) in 1% of 243 goats in Uttar Pradesh, India. Chevalier
(1966) found it in 9% of 40 goats in Germany.
Remarks. This species has undoubtedly been confused with E.
ahsata and E. arloingi in the past.
Eimeria maroteli Anon.
Eimeria maroteli Anonymous; see Gill and Katiyar, 1961.
Description. No description was given.
Type Host. Capra hircus (domestic goat) .
Geographic Distribution. India (Mukteswar).
Remarks. Gill and Katiyar (1961) said that a new species of coccid-
ium which was named E. maroteli was found in the feces of a goat at
Mukteswar, India, but that no description was given. This name was
apparently given in the annual report of the Indian Veterinary Re-
search Institute, Mukteswar, for 1949-50, and is obviously a nomen
nudum.
Eimeria ibicis Colombo, 1958
? Eimeria faurei Auctores in Capra ibex.
Description. Oocysts ovoid, bright rose, apparently smooth, with a
106 THE COCCIDIAN PARASITES OF RUMINANTS
micropyle 5-6 p wide, without micropylar cap, 27 by 18 fi , without
oocyst residuum. No other information given.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Pre patent Period. Unknown.
Type Host. Capra ibex ibex (ibex).
Other Hosts. None.
Location. Oocysts found in feces.
Geographic Distribution. Italy.
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
Remarks. Colombo (1958) found this species in the ibex in Gran
Paradiso National Park, Italy. It is smaller than E. faurei, with
which it might be confused, and has a broader micropyle.
Eimeria faurei (Moussu and Marotel, 1902) Martin, 1909
(Plate 55, Figs. 231-233)
Coccidium faurei Moussu and Marotel, 1902.
Coccidium ovis Jaeger, 1921 (according to Pellerdy, 1963).
? Coccidium caprae Jaeger, 1921 (according to Pellerdy, 1963).
Eimeria aemula Yakimoff, 1931.
Description. The following description of E. faurei from sheep is
based on Balozet (1932a), Christensen (1938b), Kamalapur (1961)
and Jackson (1964). Oocysts ovoid, with micropylar. narrow end
slightly flattened. Oocysts 25-36 by 19-28 p. (25-33 by 18-24 /x with
a mean of 29 by 21 <> according to Christensen, 1938a; 27-35 by 20-23 fi
with a mean of 31.5 by 22 ,u according to Balozet. 1932c; 27-30 by
18-28 fi with a mean of 28 by 23 j± according to Kamalapur, 1961;
28-37 by 21-27 /.<, with a mean of 32 by 23 /.<. according to Jackson,
1964). Oocyst wall smooth, composed of a single layer, faint green,
greenish yellow, pale yellowish brown, delicate salmon pink, or pale
yellowish pink, 1.3-1.8 /x thick, lined by a membrane. Micropyle
conspicuous, 2-3 ,u in diameter, described by Kamalapur (1961) as
having a small internal plug. Micropylar cap absent. A small knob
1 /(, high and 1-3 /<. wide sometimes projects beyond the micropyle ac-
cording to Kamalapur (1961). According to Jackson (1964), the
micropyle is a prominent clear zone with a retractile cup-shaped in-
ward projection. Oocysts polar granule present. Oocyst residuum
absent. Sporocysts broadly ovoid, ovoid or piriform, 11-17 by 7-9 \x
genus Eimeria Schneider, 1S75 107
with a mean of 14-15 by 8 /a. Stieda body absent or inconspicuous.
Sporocyst residuum present, composed of many or scattered granules.
Sporozoites lie lengthwise head to tail in sporocysts. One or two large
globules present in each sporozoite.
The following description of E. faurei from the domestic goat is
based on Shah and Joshi (1963) and Singh (1964). Oocysts ovoid,
slightly flattened at narrower, micropylar end, 24-34 by 19-25 /a with
a mean of 29-30 by 22 /.<.. Oocyst wall smooth, composed of a single
layer, 1.4 /i thick, faint green to greenish yellow brown. Micropyle
present, with a small internal plug. Micropylar cap absent. Oocyst
polar granule present. Oocyst residuum absent. Sporocysts piriform,
with one end pointed. Stieda body absent or vestigial. Sporocysts 11-
17 by 8-11 ix with a mean of 13 by 9 [i. Sporocyst residuum present.
Sporozoites lie lengthwise, head to tail, in sporocysts. Sporozoites
usually with one or 2 large clear globules.
Svanbaev (1967a) said that the patent period was 9-10 days.
Sporulation Time. One to 2 days according to Christensen (1938b)
and Singh (1964) ; 3-4 days according to Balozet (1932a).
Schizogony and Gametogony. The life cycle of E. faurei does not
appear to have been worked out. According to Lotze (1953) its
schizonts are about 100 jx in diameter and contain thousands of mero-
zoites. N. Singh and Pande ( 1967) found endogenous stages in the
large intestine of sheep and P. P. Singh and Pande (1967) in the large
intestine of goats in India that they thought were those of E. faurei.
However, they were dealing with mixed infections.
Prepatent Period. Twelve to 14 days according to Svanbaev ( 1967a i .
Type Host. Ovis aries (domestic sheep) .
Other Hosts. Ovis canadensis (bighorn sheep), O. ammon polii
(argali), O. a. sewerzewi, O. musimon (moufion), O. orientalis (Asia
Minor moufion), Ammotragus lervia (audad, Barbary sheep), Capra
hircus (domestic goat), C. ibex (ibex), C. sibirica (wild goat), Rupi-
capra rupicapra (chamois) ,Capreohts capreolus (roe deer) ,Dama dama
(fallow deer) (Honess, 1942; Rysavy, 1954; Donciu, 1961; Pellerdy,
1965). Whether this species actually occurs in hosts other than Ovis
and Capra is dubious (see below).
Location, Small intestine.
Geographic Distribution. Worldwide.
Pathogenicity. E. faurei is only mildly pathogenic. Lotze (19541
found that single infections of 3-month-old lambs with 5 million
oocysts produced only a temporary softening of the feces without
significantly affecting the health or physical condition of the animals.
Infections with 50 million oocysts failed to cause death. Svanbaev
10S THE COCCIDIAX PARASITES OF RUMINANTS
(1967a) reported symptoms in 2 out of 4 40-day-old lambs given
10,000 oocysts each. They had diarrhea, inappetance, depression,
anemia, conjunctivitis and gained weight poorly. Inflammation, hy-
peremia and gray-white nodules were present in the duodenum and
rarely the jejunum and ileum.
Cross-Transmission Studies. Krylov (1961) was unable to transmit
E. faurei from the sheep to the goat or from the goat to the sheep.
Lotze et al. (1961) were unable to infect goats with E. faurei from
sheep. Tsygankov, Paichuk and Balbaeva (1963) were unable to
transmit E. faurei (which they called E. aemala) from the sheep to
one saiga and 4 kids, although they produced a patent infection in a
lamb. They were unable to transmit E. faurei (which they called E.
aemula) from the goat to one saiga and one lamb although they pro-
duced a patent infection with it in a kid. Fitzsimmons (1964), how-
ever, infected 2 coccidia-free kids 50 and 58 days old with E. faurei
from sheep, but said that coccidia from sheep developed much better
in sheep than in goats. In an uncontrolled experiment, Subramanian
and Jha ( 1966) said that they transmitted E. faurei from the goat to
a lamb by feeding it 160,000 sporulated oocysts.
Prevalence. Christensen (1938b) found E. faurei in 11% of 100
sheep from Idaho, Maryland, New York, and Wyoming; Hammond
and Hamilton (1940, 1941) found it in 10% of 50 sheep in northern
Utah; Shah (1963) in 6% of 153 sheep from Illinois and other states;
Joyner et al. (1966) in 72% of 198 sheep in England; Jacob (1943)
in 40% of 100 sheep in Germany; Chevalier (1965) in 4% of 183
sheep in Germany; Patyk 1 1965) in 33% of 222 lambs aged 1-8 months
in Poland; Delic (1955) in 12% of the sheep and lambs he examined
in Yugoslavia; Merdivenci (1959) in 13% of the sheep he examined in
Turkey; Wiesenhutter (1965) in 23% of 642 sheep and 28% of 413
goats in Syria; Svanbaev (1957) in 43% of 302 sheep in Kazakhstan,
USSR; Balozet (1932a) in 21% of 63 sheep in Tunisia and Deom
and Mortelmans (1956) in 6% of 230 sheep in the Belgian Congo.
E. faurei has apparently not been found in goats in the United States.
However, Jacob (1943) found it in 18% of 11 goats in Germany;
Merdivenci (1959) in 17% of the goats he examined in Turkey; Svan-
baev ( 1957) in 40% of 48 goats in Kazakhstan, USSR; Balozet (1932a)
in 2% of 41 goats in Tunisia; Sayin (1966) in 5% of 900 Angora goats
in Turkey; Shah and Joshi (1963) in 1% of 300 goats in Madhya
Pradesh, India; Singh (1964) in 11% of 214 goats and Jha and
Subramanian (1966) in 34% of 243 goats in Uttar Pradesh, India; and
Fernando (1957) in 8% of 62 goats in Ceylon.
Remai-ks. Moussu and Marotel (1901) were the first to recognize
genus Eimeria Schneider, 1S75 109
sheep coccidia as different from rabbit coccidia. They (1902) described
them and named them Coccidium faurei. Martin ( 1909a) later trans-
ferred this species to the genus Eimeria. Later writers thought that
sheep had one species of coccidium, which they called E. faurei, and
and that goats had another, which they called E. arloingi. Balozet
(1932a), however, said that both species occurred in both sheep and
goats, and Christensen ( 1938b) concurred. Subsequent authors have
accepted their view. However, Orlov (1956), working in Kazakhstan
(and also referring to the work of Melikyan, 1953, in Armenia)
considered E. arloingi a synonym of E. faurei. He apparently based his
opinion on work by Yakimoff (1931a) who held to the old view that
all capped oocysts in sheep were those of E. faurei. Because of this
view, Yakimoff (1931) had to give a new name, E. aemula, to the E.
faurei that he saw in sheep. We now know that both sheep and goats
have capped oocysts; their names are discussed elsewhere [E. ahsata,
E. arloingi, E. erandallis, E. christenseni, E. ovina, E. intricata).
Whether both sheep and goats have E. faurei is open to question.
Although the oocysts referred to this species from both hosts are ap-
parently structurally identical, the fact that Krylov ( 1961 ) , Tsygan-
kov, Paichuk and Balbaeva (1963) and Lotze et al. (1961) failed
to transmit them from one host to the other (although Fitzsimmons,
1964, did so) raises the question whether the forms from the 2 hosts
may not be different strains or demes at the very least. Certainly,
reports of E. faurei from hosts other than Ovis and Capra must be
considered of dubious validity.
Eimeria intricata Spiegl, 1925
(Plate 56, Figs. 235-238; Plate 61, Fig. 271 )
Description. This species was described by Spiegl (1925), Balozet
( 1932a) , Christensen ( 1938b I , Ray ( 1961 ) , Shah ( 1963 ) , and Jackson
(1964), among others. Oocysts ellipsoidal or slightly ovoid, 39-54 by
27-36 ii with a mean of 47 by 32 /x (Christensen), 46 by 33 jjl (Spiegl)
or 47-59 by 34-47 /x with a mean of 51 by 39 fi (Shah). Oocyst wall
composed of 2 layers, the outer irregular, granular, brownish yellow
to dark brown, 2-3 \x thick, transversely striated and appearing di-
vided into 2 sublayers by a faint line; the inner layer dark brown,
0.4-0.8 jx thick; oocyst wall lined by a membrane which is often
wrinkled at the micropylar end. Micropyle present, 6-10 /x in diameter
and not extending to the inner layer. Micropylar cap prominent, dome-
shaped, colorless to greenish yellow, 1-4 /<, high and 6-18 ». wide;
110 THE COCCTDIAN PARASITES OF RUMINANTS
micropylar cap detachable; Shah ( 1963) found none on 8 of 50 oocysts.
One or more oocyst polar granules generally present. Oocyst residuum
absent. Sporocysts elongate ovoid, with one end bluntly pointed, 17-
22 by 9-14 /t with a mean of 20 by 11 p (Shah) or 20 by 14 ,x (Jack-
son). Stieda body absent or extremely tiny. Sporocyst residuum
present. Sporozoites elongate, with one end narrower than the other,
lying lengthwise head to tail in sporocysts, with 2-3 clear globules.
Sporulation Time. Three to 5 days at room temperature (Christen-
sen, 1938b) ; 9-12 days at 21-23 C (Ray, 1961) or 4-6 days at room
temperature (Singh, 1964).
Schizogony and Gametogony. Davis and Bowman (1965) and
Pande, Bhatia and Chauhan ( 1966) studied the endogenous stages of
this species. According to Davis and Bowman, the schizonts occur in
the lower small intestine, mostly in the cells lining the intestinal crypts.
The largest they found were only 65 by 45 /x and contained large mero-
zoites up to 19.5 by 4 /.«.; the size of the merozoites gave the schizonts
a granular appearance. In one lamb killed 23 days after infection,
gamonts and oocysts were found from midway in the small intestine
posteriorly to the rectum, with most in the cecum. These forms, too,
were in the cells lining the intestinal crypts. Pande, Bhatia and Chau-
han (1966) found 4 mature schizonts in epithelial cells of the crypts;
they were 32-37 by 21-25 [x with a mean of 34.4 by 22.7 /x and con-
tained 25-40 spindle-shaped merozoites 7-9 by "2.5-2" /x. They found
gamonts and oocysts in the epithelial cells of the crypts of the small
intestine from the jejunum to the ileum. The oocysts in sections were j
36-46 by 25-37 \x with a mean of 41 by 30 /.<.; the macrogametes were
36-54 by 25-36 \x with a mean of 42 by 30 /_/. ; the fully developed micro-
gamonts were 61-250 by 36-71 jx with a mean of 113 by 52 fx. The
slender flagellated microgametes were 4.6-6 /.<, long. According to
Davis and Bowman (1965) the patent period is 6-11 days; according
to Svanbaev ( 1967 ) it is 5-6 clays.
Prepotent Period. Twenty to 27 days according to Davis and Bow-
man (1965) ; 23 days according to Krylov (1961) ; 22-23 days accord-
ing to Svanbaev ( 1967a) .
Type Host. Oris ones (domestic sheep).
Other Hosts. Ovis canadensis (Rocky Mountain bighorn sheep)
(Honess, 1942); O. musimon (mouflon) (Yakimoff, Gousseff and
Rastegaieff, 1932a; Rysavy, 1954); O. amnion (argali) (Svanbaev,
19581; Capra hircus (domestic goat) (Yakimoff, 1933a; Ray, 1961;
Jha and Subramanian, 1966). In addition, Wetzel and Enigk (1936)
reported it from the roe deer Capreolus capreolus, and Rysavy (1954)
genus Eimeria Schneider, 1S75 111
from this host and Dama dama; whether this species actually occurs in
deer is doubtful.
Location. Davis and Bowman (1965) found the schizonts in the
lower small intestine. They found gamonts and oocysts from midway
in the small intestine posteriorly to the rectum, with most in the cecum.
Pande, Bhatia and Chauhan (1966) found gamonts and oocysts in the
jejunum and ileum. Both schizonts, gamonts and oocysts were in
epithelial cells lining the crypts.
Geographic Distribution, Worldwide.
Pathogenicity. These oocysts are rarely found in large numbers.
Svanbaev (1967a), who produced infections with 10,000 oocysts in
3 out of 4 40-day-old lambs that he exposed, observed clinical signs in
2 of them. These consisted of soft, mucoid feces, anemia, poor ap-
petites, disinclination to move, a slight temperature and decreased
weight gains. In one lamb which he killed 30 days after inoculation,
he saw petechiae and an edematous mucosa in the jejunum and ileum
(and slightly in the cecum) ; the lamb was no longer shedding oocysts
at this time.
Cross-Transmission Studies. Krylov (1961) failed to transmit
E. intricata from the sheep to 7 goats 3 months to 2 years old, but did
succeed in infecting 2 lambs 1.5-2 months old. Lotze et al. (1961) failed
to infect 6-month-old goats with E. intricata from sheep. Tsygankov,
Paichuk and Balbaeva (1963) were unable to transmit E. intricata
from the sheep to one saiga and 4 kids, although they produced a patent
infection in a lamb.
Prevalence. Christensen (1938a) found this species in 14% of 100
sheep from Maryland, New York, and Wyoming; Hammond and
Hamilton (1940, 1941) found it in 28% of 50 sheep in northern Utah;
Shah (1963) found it in 7% of 153 sheep from Illinois and other states;
Jacob (1943) in 13% of 100 sheep in Germany; Chevalier (1965) in
0.4% of 200 sheep in Germany; Joyner et al. (1966) in 29% of 198
sheep in England; Delic (1955) in 8% of the sheep and lambs lie
examined in Yugoslavia; Patyk (1965) in 7% of 222 lambs aged 1-8
months in Poland; Merdivenci (1959) in 5% of the sheep he examined
in Turkey; Wiesenhtitter (1965) in 19% of 642 slice]) and none of 413
goats in Syria; Balozet (1932a) in 3% of 63 sheep in Tunisia; Svan-
baev (1957) in 4% of 302 sheep in Kazakhstan, USSR; Singh (1964)
in 1% of 214 goats; and Jha and Subramanian (19661 in 0.7 r r of 243
goats in Uttar Pradesh, India.
Remarks. The failure of Krylov (19611, Lotze et al. (1961) and
Tsygankov, Paichuk and Balbaeva (1963) to infect goats with E.
112 THE COCCTDIAN PARASITES OF RUMINANTS
intricata from sheep raises the question whether the same species
occurs in both hosts. However, until careful comparative morphologic
and life cycle studies are done, we are leaving the two forms as a single
species.
Eimeria parva Kotlan, Mocsy and Vajda, 1929
(Plate 56, Figs. 239-241 ; Plate 57, Figs. 242-244)
Eimeria nana Yakimoff, 1933.
Eimeria galouzoi Yakimoff and Rastegaieff, 1930, pro parte.
Description. The forms in the sheep and goat are described sep-
arately. That in the sheep is based on Kotlan, Mocsy and Vajda
(1929), Balozet (1932a), Svanbaev (1957), Christensen (1938b),
Kamalapur (1961), Jackson (1964), and Chevalier (1965). That in
the goat is based on Shah and Joshi (1963), Singh (1964) and Cheva-
lier (1966).
Oocysts in the sheep subspherical, ovoid, ellipsoidal or spherical,
slightly narrow at micropylar end, 12-23 by 10-19 /x with a mean
of 16.5 by 14 fi (Christensen), 17 by 13.5 (i (Balozet), 18 by 15 ji
(Kamalapur, Jackson) or 15 by 14.5 /x (Svanbaev). Micropyle incon-
spicuous. Micropylar cap absent. Oocyst wall smooth, pale yellow
to yellowish green, brownish yellow or faint pinky mauve, composed
of 2 layers, the outer 0.8-1.2 /x thick and thinning at the micropylar
end, and the inner layer a dark, thin membrane. Oocyst polar granule
generally present. Oocyst residuum absent. Sporocysts ovoid to elon-
gate ovoid, 6-13 by 5-8 p. with a mean of 10 by 6 /x (Kamalapur) or
9 by 5 ft (Jackson). Stieda body absent or small. Sporocyst residuum
present as a few fine granules. Sporozoites with one clear globule.
Oocysts in the Rocky Mountain bighorn sheep similar to those in
the sheep but larger, 17.5-23.5 by 17-22 jx with a mean of 20 by 19 /x
(Honess, 1942).
Oocysts in the goat 16-23 by 13-22 /x with a mean of 20 by 19 p.
(Shah and Joshi), 14-19 by 12-15 /x with a mean of 16 by 13 /x (Singh),
or 17 by 14.5 /x (Chevalier). Oocysts subspherical, ovoid to ellipsoidal
or spherical. Oocyst wall smooth, pale yellow to yellowish brown or
bright brown, composed of 2 layers, the outer 0.8 /x thick and the inner
a dark thin membrane. Micropyle inconspicuous. Micropylar cap
absent. Oocyst polar granule present (absent according to Chevalier).
Oocyst residuum absent. Sporocysts broadly ovoid, 7-13 by 5-9 /x
with a mean of 10 by 7 /x (Shah and Joshi) or 9 by 6 /x (Chevalier).
Stieda body absent (present according to Singh). Sporocyst residuum
genus Eimeria Schneider, 1S75 113
present (a small residuum present in only a very small number of
sporocysts according to Chevalier) . Sporozoites lie head to tail in
sporocysts; each contains 2 clear globules.
Sporulation Time. One to 2 days (Christensen, 1938b; Singh, 1964),
7-8 days (Balozet, 1932a), 3-5 days in the sheep (Chevalier, 1965)
or 2-5 days in the goat (Chevalier, 1966) .
Schizogony and Gametogony. Kotlan, Pellerdy and Versenyi (1951a,
1951b) described the endogenous stages in sheep. However, since
Pellerdy (1965) considered E. pallida a synonym of E. parva, since
at least one of their lambs was also infected with E. ovina and E. in-
tricata, and since they found two types of schizont, it is not certain
whether they were actually dealing with E. parva alone. They found
schizonts throughout the small intestine that were up to 185-256 by
128-179 /x and easily visible to the naked eye as whitish bodies. They
lay in the mucosa, usually near the surface but sometimes as far down
as the muscularis mucosae. They invaded endothelial cells and en-
larged both the host cell and its nucleus enormously. They were sur-
rounded by a rather thick layer of connective tissue which became
thinner as they increased in size. Each schizont produced thousands
of straight merozoites 10-12 /.<, long.
A second, much smaller, type of schizont was also present in the
small intestine. It occurred in the superficial epithelial cells, was 10-
12 jx in diameter, and contained about 10-20 merozoites 2.5-3.0 /x long.
Kotlan, Pellerdy and Versenyi were not sure whether these were part
of the life cycle of E. parva.
The sexual stages occurred mostly in the cecum and colon, and to
a lesser extent in the small intestine. They were present in epithelial
cells and were 15-19 by 10-16 /x.
N. Singh and Pande (1967) found endogenous stages in the large
intestine of sheep in India that they thought were those of E. parva.
However, they were dealing with mixed infections.
In 4 kids that died 11-15 days after inoculation with 25,000-
250,000 sporulated oocysts, Savin (1966) found gamonts and oocysts
in mucosal scrapings from the colon, cecum and posterior small in-
testine, and schizonts in the epithelial cells of the villi of the middle
part of the small intestine. The schizonts were up to 260 by 180 /x
and could be easily seen with the naked eye as whitish bodies. He
also saw much smaller schizonts 15-18 by 9-12 /<, in the epithelial cells
of the crypts of Lieberkuehn in one kid. The gamonts and oocysts were
in the epithelial cells of the mucosa. The macrogametes were 14-18 by
9-14 n and the microgamonts were 22-25 by 15-20 /<..
114 THE COCCIDIAN PARASITES OF RUMINANTS
If the above accounts are accurate, then the forms known as E.
parva in the sheep and goat are different species.
Svanbaev (1967a) found that the patent period in sheep was 6-8
days.
Prepotent Period. Fifteen days according to Krylov (1961), 11-13
days according to Svanbaev (1967a). 10-13 days according to Sayin
(1966).
Type Host. Ovis aries (domestic sheep).
Other Hosts. Oris orientalis (mouflon), 0. ommon (argali), 0.
musimon (mouflon), 0. canadensis (bighorn sheep), Capra hircus
(domestic goat), C. sibirica (Asian wild goat), C. ibex (Alpine ibex)
(See Couturier, 1962). In addition, Yakimoff (1933b) reported this
species from Ammotragus lervia (syn., Oris tragelaphus) (aoudad),
Jacob (1943) from a roe deer and Rysavy 1 1954) from Cervus elaphus
(red deer), Capreolus capreolus (roe deer), Dama dama (fallow deer)
and Rupicapra rupicapra (chamois) ; however, these reports are
erroneous (Pellerdy, 1965) or dubious. Indeed, it is uncertain whether
this same species occurs in both Oris and Capra.
Location. The schizonts occur in the small intestine, and the sexual
stages mostly in the cecum and colon, and to a lesser extent in the small
intestine. Svanbaev (1967a) said that E. parva is located in the
duodenum and jejunum.
Geographic Distribution. Worldwide.
Pathogenicity. E. parva is apparently not very pathogenic in sheep.
Most of the damage is caused by the sexual stages in the large and
small intestines. In a lamb killed by Kotlan, Pellerdy and Versenyi
(1951b) 16 days after experimental inoculation, the contents of the
cecum and colon were semifluid, dark and mixed with blood in places.
The wall was thickened and its surface uneven and denuded of
epithelium in places. On histologic examination, the cecal mucosa
was found to have been stripped from the glandular layer in places,
and the tissue had become necrotic and infiltrated with lymphocytes
and neutrophils but no eosinophils. Sharply separated from these ne-
crotic areas were other areas in which most of the epithelial cells con-
tained microgamonts, macrogametes or young oocysts. Svanbaev
(1967a) infected 3 out of 4 40-day-old lambs by feeding them 10,000
oocysts each. The coccidia produced no symptoms.
According to Sayin (1966), E. parva may be markedly pathogenic
for the goat. Nine of 12 Angora goats 6-10 weeks old given 25,000-1
million oocysts developed diarrhea, and 4 of them died 11-15 days
after inoculation. Four of the survivors were challenged 6 weeks
genus Eimeria Schneider, 1S75 115
after inoculation with 5 or 10 million oocysts; none had clinical signs,
and all discharged markedly fewer oocysts than after the original
infection.
Cross-Transmission Studies. Krylov (1961) was unable to transmit
E. parva from the sheep to 8 goats aged 3 months to 2 years, although
he did infect 2 young lambs. Tsygankov, PaTchuk and Balbaeva ( 1963 )
were unable to transmit E. parva (which they called E. galouzoi)
from the sheep to one saiga and 4 kids, although they produced a
patent infection in a lamb. They were unable to transmit E. parva
(which they called E. galouzoi) from the goat to one saiga and one
lamb although they produced a patent infection with it in a kid. Fitz-
simmons (1964) was unable to infect two coccidia-free kids 50 and
58 days old with "Eimeria pallida /Eimeria parvu^ and other species
from sheep. He did infect a control, coccidia-free lamb with these
species, although they constituted only 1% of the coccidia passed by it.
Prevalence. Christensen (1938b) found this species in 50% of 100
sheep from Idaho, Maryland, and Wyoming; Hammond and Hamilton
(1940, 1941) in 34% of 50 sheep in northern Utah; Shah (1963) in
5% of 153 sheep from Illinois and other states; Joyner et al. (1966)
in 56% of 198 sheep in England; Jacob (1943) in 52% of 100 sheep in
Germany; Chevalier (1965) in 7% of 200 sheep in Germany; Patyk
(1965) in 52% of 222 lambs aged 1-8 months in Poland; Merdivcnci
(1959) in 31% of the sheep he examined in Turkey; Svanbaev (1957)
in 9% of 302 sheep in Kazakhstan; Balozet (1932a) in 21% of 63 sheep
in Tunisia; and Deom and Mortelmans (1956) in 41% of 230 sheep in
the Belgian Congo.
Jacob (1943) found it in 9% of 11 goats in Germany; Chevalier
(1966) in 2 c /c of 40 goats in Germany; Merdivenci (1959) in 45%
of the goats he examined in Turkey; Wiesenhiitter (1965) in 38% of
642 sheep and 31% of 413 goats in Syria; Balozet (1932a) in 22% of
41 goats in Tunisia; Savin (1966) in 26% of 900 Angora goats in
Turkey; Deom and Mortelmans (1956) in 50% of 6 goats in the
Belgian Congo; Shah and Joshi ( 1963) in 1.3% of 300 goats in Madhya
Pradesh, India; Singh (1964) in 16% of 214 goats and Jha and Su-
bramanian (1966) in 58% of 243 goats in Uttar Pradesh, India; and
Fernando ( 1957) in 54% of 62 goats in Ceylon.
Remarks. In view of the failure of cross-transmission attempts
of this species between sheep and goats, it is quite likely that the
forms from these hosts actually belong to different species. However, in
the absence of careful comparative structural and life cycle studies.
we are retaining the name E. parva for both forms for the present.
116 THE COCCIDIAN PARASITES OF RUMINANTS
Eimeria gilruthi (Chatton, 1910) Reichenow
and Carini, 1937
Gastrocystis gilruthi Chatton, 1910.
Globidium gilruthi (Chatton. 1910) Noller, 1920.
Description. The oocysts of this species are unknown, only the
schizonts and merozoites having been seen (see below) .
Sporulation Time. Unknown.
Schizogony and Gametogony. The schizonts occur in the connective
tissue and mucous membranes of the abomasal wall. They are easily
visible to the naked eye as whitish nodules, and are 300-900 /x in di-
ameter. The cyst wall is up to 40 /./. thick. The host cell nucleus is
flattened and greatly enlarged. The mature schizonts contain thou-
sands of crescent- to sickle-shaped merozoites about 4.5-7.5 /.i long
and 1.2-2.0 fi wide.
Gilruth (1910) said that the cyst in sheep was somewhat oval,
500 by 300 /i, and contained spindle-shaped merozoites, "with extremi-
ties tapering to a fine point," 4-6 by 0.5 /*, and with a central nu-
cleus. Triffitt (1925) said that the cyst in sheep was rounded or ovoid,
300-900 \x in diameter, with a wall the inner layer of which was 36 \x
thick in young cysts and 7.5 fi thick in almost mature cysts. This
layer was dark grayish and composed of delicate, circumferentially
arranged fibers in a very finely granular matrix. It composed about
J 4 of the whole thickness of the young cysts and about % of that of
the mature cysts. Outside it was a lighter layer, coarsely granular on
its inner surface and with a hyaline outer surface thrown up into
slight folds and ridges so that it had a peculiar brushlike structure. In
young cysts, the brushlike portion consisted of short, hairlike processes
about 18 /.i long; in old cysts it was markedly thinner, appearing only
as a fine line. According to Triffitt (1925), the merozoites were
elongate, slightly curved, rounded at one end and slightly tapering
at the other, about 12 /x long and 2.5 \x wide, with a nucleus near the
rounded end. Sarwar ( 1951 ) found it commonly in sheep and goats in
Lahore, Pakistan. Bhatia and Pande (1966a) said that the mature
schizonts in sheep were 677-878 by 584-830 /.<. and contained "millions"
of merozoites of differing size and structure. They described 3 types.
The largest were 13-15 by 1.6-1.8 /-. with a mean of 14.0 by 1.7 /x;
they were somewhat sickle-shaped, with pointed ends and a vesicular
or oval nucleus quite near one end. The intermediate-sized merozoites
were 8-12 by 1.3-1.6 /x with a mean of 10.0 by 1.4 /_/.; they were slightly
slender, with one end blunt and the other tapering, and with an ovoid
nucleus somewhat nearer the blunt than the tapering end. The smallest
genus Eimeria Schneider, 1S75 117
merozoites were 7-8 by 1.3-1.7 ti with a mean of 7.0 by 1.5 //,; they
were spindle-shaped, with one end more pointed than the other, and
with a vesicular nucleus near the center. Matta and Pande (1966)
confirmed these findings.
Pande and Bhatia ( 1966) said that mature cysts in the goat were
580-966 by 500-830 p, while developing ones were 200-780 by 180-670
p.. The cyst wall was composed of 2 layers and up to 40 xt thick. They
found 3 sizes of merozoites. The largest were 9-12 by 1.2-1.5 /<.,
straight or slightly curved, with one end tapered and the other some-
what blunt, and an oval or ellipsoidal nucleus about % of the body
length from the blunt end. The intermediate-sized merozoites were
6-8.5 by 1.0-1.3 p., slender, slightly curved, with tapering ends and
subcentral nearly oval or spherical nucleus. The smallest merozoites
were 5-8 by 1.5-1.7 /x, with a comparatively robust and stumpy form,
"abruptly ending extremities," and a somewhat central nucleus.
These dimensions are for smears from the schizonts fixed in alcohol
and stained with hematoxylin and eosin. Sarwar (1951) found
merozoites measuring 10.0 by 1.5 fi, and Soliman (1960) said that they
were 6-9 by 1.2-1.8 /<.. Pande et al. (1967) also found giant schizonts
in the abomasum of two kids.
Triffitt (1928) described uninucleate schizonts 6-8 /x in diameter
in epithelial cells of the abomasum of the goat, and 12-nucleate Plas-
modia (without distinct merozoites) about 16 \i long and 9.5 \x wide in
a roughly spherical host cell about 28 /x in diameter. She also found
mature schizonts containing merozoites similar to those she had seen in
the sheep.
According to Soliman ( 1960) , the schizonts from sheep and goats
(he did not differentiate between the parasites in the 2 hosts) rested
on the muscularis mucosae with their upper borders 215 p. below the
intestinal lumen, while some mature cysts with diameters of 380-559
jx were only a few microns from the intestinal lumen. The cyst wall
had 2 clear zones, an inner one 3-4 /x thick and an outer one 3-7 /x thick,
with perpendicular striatums. The merozoites ("spores") were sickle-
shaped, with a nucleus at the blunt end and the other end sharp and
hyaline with a distinct granule between it and the cell nucleus; the
unfixed merozoites were 6-9 p long and 1.2-1.8 p wide.
Various authors have described giant schizonts (globidia) from the
small intestine of sheep and goats (and even from the cecum of the
sheep — Bhatia and Pande, 1966b). Whether they belong to the
same species as the abomasal schizonts is unknown.
Pre-patent Period. Unknown.
IIS THE COCCIDIAN PARASITES OF RUMINANTS
Type Host. Ovis aries (domestic sheep).
Other Hosts. Capra hircus (domestic goat) ; Capra sibirica (Siberian
wild goat). In addition, Abdussalam (1953) found this species in a
wild sheep Pseudois nahoor (Ovis nahura) which died in the Zoological
Gardens at Lahore, Pakistan.
Actually, it is uncertain whether this species occurs in both sheep
and goats even though it has been reported from them. Further study
may reveal that these hosts have different species which are at present
assigned to "E. g Unit hi."
Location. Abomasum.
Geographic Distribution. Worldwide.
Pathogenicity. Unknown .
Cross-Transmission Studies. None.
Prevalence. This form is very common in some parts of the world,
but not in others. Gilruth (1910) found it in Australia. Chatton
( 1910a, 1)1 found it in the abomasa of almost all the sheep he examined
in France. Triffitt (1925) found it in 92% of 138 sheep slaughtered in
London. Alicata (1930) found it in 9% of 78 sheep in Indiana, 11%
of 101 from West Virginia and 8% of 72 from Idaho. Marsh and Tun-
nicliff (1941) found it in Montana, and Morgan and Hawkins (1952)
said that it had also been seen in Wyoming and Michigan. We have
seen it in a very small percentage of sheep at the Illinois State Veterinary
Diagnostic Laboratory. Sarwar (1951) found it in 34% of the sheep
and goats slaughtered at Lahore, Pakistan, and found it in as many
as 94% in other parts of East Pakistan. Soliman (1958) found it
in 18% of 250 sheep slaughtered in Egypt and in 32% of 425 sheep in
the Sudan. Gilruth (1910) and Rac and Willson (1959) found it in
sheep in Australia. Canham ( 1931 ) found it in sheep in Natal. Bhatia
and Pande (1966a) and Matta and Pande (1966) found it commonly
in sheep in India.
Triffitt ( 1928) found it in the goat in England. Ferguson and Goldsby
(1961) found it in all of 15 goats in Missouri and Arkansas. Sarwar
(1951) found it in 34% of the goats slaughtered at Lahore, Pakistan;
Soliman (1958) in 28% of 150 goats slaughtered in Egypt; Soliman
(1960) in 40% of 240 goats in the Sudan; and Pande and Bhatia
(1966) in 9% of 100 goats in Mathura, LTttar Pradesh, India. Mugera
and Bitakaramire (1968) found it in the goat in Kenya. Hilgenfeld
(1966) reported giant schizonts which he assigned to this species in
the submucosa of the large and small intestines of the Siberian wild
goat Capra sibirica.
Remarks. k 'E. gilruthi" is undoubtedly the schizont of one or more
species of coccidia of the sheep and goat already known from the
genus Eimeria Schneider, 1875 119
oocysts. However, we do not know what species it or they may be.
Reichenow (1929) said that it was very probably E. intricata. Becker
(1956) agreed and, since the name E. gilruthi has priority, synony-
mized E. intricata with it. However, Davis and Bowman (1965) found
that E. intricata does not have giant schizonts, so this species cannot
be E. gilruthi.
Eimeria granulosa Christensen, 1938
(Plate 57, Figs. 246-247)
Description. The following description is based on those of Chris-
tensen (1938b), Shah (1963) and Jackson (1964) for E. granulosa from
the domestic sheep. Oocysts piriform, ellipsoidal or shaped like a
stout, broad-shouldered urn, with a micropyle and micropylar cap at
the broad end. Oocysts 22-35 by 17-25 /x with a mean of 29.4 by
20.9 ,l (Christensen, 1938b), 30-35 by 21-22 M with a mean of 31 by
22 S x (Shah, 1963) or 28-37 by 21-26 /x with a mean of 32.5 by 24.0 /-.
(Jackson, 1964). Oocyst wall composed of 2 layers, the outer one
smooth, pale yellow to yellowish green, 0.4-0.6 /x thick, and the inner
one brownish yellow and 0.8 /x thick. Oocyst wall lined by a mem-
brane often slightly wrinkled at micropylar end. Micropylar cap
prominent, faintly brownish, shaped like a truncate cone with a
slightly convex top, easily dislodged, 1-3 /x high and 5-12 /x wide.
Two or more oocyst polar granules ordinarily present (Shah, 1963)
or absent (Christensen, 1938b). Oocyst residuum absent. Sporocysts
ovoid or elongate ovoid, rounded at both ends. Stieda body faintly
perceptible (Shah, 1963). Sporocysts 13-16 by 8-9 /x with a mean of
15 by 8 p. (Shah, 1963; Jackson, 1964). Sporocyst residuum present,
usually consisting of granules scattered loosely in sporocyst but form-
ing a compact mass in a few sporocysts. Sporozoites elongate, with
one end narrower than the other, lying lengthwise, head to tail, in
sporocysts, with 1-3 clear globules.
According to Honess (1942), E. granulosa in the bighorn sheep was
identical in all respects except size with Christensen 's (1938b) descrip-
tion. The oocysts he found in this host were 33-39 by 24-25 /x with a
mean of 36.2 by 24.7 /x; their micropylar caps were 2-4 /x high and
8-12 /x wide, with a mean of 3.1 by 9.8 /x.
According to Shah and Joshi (1963), the oocysts in the domestic
goat were ellipsoidal or piriform, slightly flattened at the micropylar
end, 30-34 by 20-26 /x with a mean of 32 by 23 /i. Oocyst wall com-
posed of 2 layers, the outer one smooth, pale yellow to yellowish brown
120 THE COCCIDIAN PARASITES OF RUMINANTS
and 1 n thick, the inner one brownish yellow, 0.6 fx thick. Micropylar
cap prominent, faintly brownish, cone-shaped, easily dislodged, 2-3 fx
high and 8-10 ,u wide with a mean of 3 by 9 /x. Three or more oocyst
polar grannies present. Oocyst residuum absent. Sporocysts elongate
ovoid, with faintly perceptible Stieda body, 13-15 by 8-9 /a. Sporocyst
residuum present. Sporozoites elongate, lying lengthwise head to tail
in sporocysts, with 1-2 clear globules in each sporozoite.
Sporulation Time. Three to 4 days according to Christensen
(1938b).
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Ovisories (domestic sheep).
Other Hosts. Ovis canadensis (Rocky mountain bighorn sheep),
Capra hircus (domestic goat).
Location. Unknown. Oocysts found in feces.
Geographic Distribution. Worldwide.
Pathogenicity. Unknown.
Cross-Transmission Studies. Krylov (1961) failed to transmit E.
granulosa from the sheep to a 3-month-old kid or a 2-month-old
lamb.
Prevalence. Christensen (1938b) found this species in 10% of 100
sheep from Maryland and New York; Hammond and Hamilton (1940,
1941) found it in 16% of 50 sheep in northern Utah; Shah (1963) in
4% of 153 sheep from Illinois and other states; Joyner et al. (1966)
in 9% of 198 sheep in England; Jacob (1943) in 1% of 100 sheep in
Germany; Patyk (1965) in 3% of 222 lambs aged 1-8 months in Po-
land; Merdivenci (1959) in 6% of the sheep he examined in Turkey;
and Wiesenhiitter (1965) in 13% of 642 sheep and none of 413 goats
in Syria. Honess (1942) remarked that E. granulosa was more fre-
quent and numerous in bighorn sheep than in domestic sheep in
Wyoming. Merdivenci (1959) found it in 6% of the goats he examined
in Turkey, and Sayin (1966) in 3% of 900 Angora goats in Turkey.
Shah and Joshi ( 1963) found it in 1% of 300 goats in Madhya Pradesh,
India, and Jha and Subramanian (1966) in 10% of 243 goats in Uttar
Pradesh, India.
Eimeria pallida Christensen, 1938
(Plate 57, Fig. 248-249)
Description. The forms in the sheep and goat are described sepa-
rately. That in the sheep is based on Christensen ( 1938b) , Shah (1963)
genus Eimeria Schneider, 1875 121
and Jackson (1964). That in the goat is based on Shah and Joshi
(1963).
Oocysts in the sheep ellipsoidal, 12-20 by 8-15 /x with a mean of 14
by 10 [i (Christensen) 15 by 11 n (Shah) or 14 by 11 /x (Jackson).
Oocyst wall smooth, colorless to very pale yellow or yellowish green,
composed of 2 layers 0.5 /.<, in total thickness; outer layer accounts for
almost the whole thickness of the wall; inner layer appears simply as
a dark line on inner surface of wall. Micropyle imperceptible, perhaps
absent. Micropylar cap absent. Oocyst polar granule present (absent
according to Christensen) . Oocyst residuum absent. Sporocysts elon-
gate ovoid, 6-9 by 4-6 tt with a mean of 7 by 4 /x (Shah) or 8 by 4 /±
(Jackson). Stieda body absent. Sporocyst residuum present. Sporo-
zoites elongate, usually lying lengthwise head to tail in sporocysts, but
often with a tendency to lie crosswise in them. Sporozoites with a
single clear globule.
Oocysts in the goat ellipsoidal or slightly ovoid, 13-18 by 10-14 tt
with a mean of 16 by 12 p.. Oocyst wall smooth, colorless to very pale
yellow, composed of 2 layers of which the outer is 0.6 /<. thick and the
inner one is merely a dark line on the inner surface of the wall. Micro-
pyle imperceptible. Micropylar cap absent. Oocyst polar granule
present. Oocyst residuum absent. Sporocysts elongate ovoid, 6-9 by
4-5 ji with a mean of 7 by 5 p.. Stieda body absent. Sporocyst resid-
uum present. Sporozoites elongate, lying lengthwise head to tail in
sporocysts, with a single clear globule.
Sporulation Time. One day according to Christensen (1938b); 2-3
days at 21-23 C according to Ray (1961) .
Schizogony and Gametogoriy. Unknown.
Pre-patent Period. Unknown.
Type Host. Ovis aries (domestic sheep).
Other Hosts. Capra hircus (domestic goat), C. ibex (Alpine ibex)
(See Couturier, 19621.
Location. Unknown. Oocysts found in feces.
Geographic Distribution. Presumably worldwide.
Pathogenicity. Unknown.
Cross-Transmission Studies. Fitzsimmons ( 1964) failed to infect
2 coccidia-free kids 50 and 58 days old with "Eimeria pallida /Eimeria
parva" and other coccidia from a sheep, although he did succeed in
infecting a control, coccidia-free lamb; however, Eimeria pallida, par va
constituted only 1% of the coccidia passed by the lamb.
Prevalence. Christensen (1938b) found this species in 10% of 100
sheep from Maryland and Wyoming; Hammond and Hamilton (1940,
1941) found it in 4% of 50 sheep in northern Utah; Shah (1963) in
122 THE COCCIDIAN PARASITES OF RUMINANTS
6 r r of 153 sheep from Illinois and other states; Joyner et al. (1966)
in 37 r r of 198 sheep in England; Patyk (1965) in 3% of 222 lambs
aged 1-8 months in Poland; Merdivenci (1959) in 4% of the sheep and
3% of the goats he examined in Turkey; Savin (1966) in 2% of 900
Angora goats in Turkey; Wiesenhiitter (1965) in 1% of 642 sheep and
none of 413 goats in Syria; Shah and Joshi (1963) in 0.37c of 300
goats in Madhya Pradesh, India; Jha and Subramanian (1966) in 6%
of 243 goats in Uttar Pradesh, India; and Fernando (1957) in 6% of
62 goats in Ceylon.
Remarks. Kotlan, Pellerdy and Versenyi (1951a) and Pellerdy
(1965) considered E. pallida a synonym of E. parva, but Shah (1963)
and Jackson (1964) verified that the two are different.
Eimeria hawkinsi Ray, 1952
(Plate 57, Fig. 250)
Description. According to Ray (1952, 1961), the oocysts are spheri-
cal to subspherical. Although he said that the wall "had a single con-
tour." he described 2 walls; the ''endocystic" wall was darker and more
prominent than the "eetocystic" wall; the general color of the oocyst
was light grayish pink in daylight. Oocysts 20-25 by 15-22.5 /.<. with
a mean of 22.4 by 18.4 ,u. Micropyle present. There is apparently no true \
polar cap although Ray said that there was one. He said (1952), ''The
polar cap seemed to be a protruberance [sic] of the endocystic wall and
its protruded portion had just come out of the endocystic wall in the
form of a triangle, the base of which was embedded in the endocystic
wall. The micropyle was a very minute gap between the base of the tri-
angle and the endocystic wall." In his later (1961) paper, Ray illus-
trated a triangular protrusion through the micropyle; his drawing
looked like either a membrane containing the oocyst contents pro-
truding through a single-layered wall and coining to a point, or a dou-
ble-layered wall with the inner border of the inner layer protruding
through the oocyst wall and coming to a point outside it. Whatever it
was, it was not a true polar cap. Oocyst polar granules apparently
absent. Oocyst residuum absent. Sporocysts piriform, 10-15 by 7.5-10
jj. with a mean of 11 by 8 /i. Sporocyst residuum present.
Sporulation Time. Five to 6 clays at 21-23 C according to Ray
(1961) ; 10 hours at 37 C according to Ray ( 1952 ) .
Schizogony and Gametogony. Unknown.
Prepatent Period. Unknown.
Type Host. Oris aries (domestic sheep).
genus Eimeria Schneider, 1S75 123
Other Hosts. Copra hircus (domestic goat).
Location. Oocysts found in feces.
Geographic Distribution. India. Ray (1961) reported this species
from sheep in Madhya Pradesh, Uttar Pradesh, Madras, and Orissa.
He reported it from goats in Uttar Pradesh, Bengal, and Kashmir.
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Jha and Subramanian (1966) reported this species from
18% of 243 goats in Uttar Pradesh, India.
Remarks. While Ray (1952, 1961) considered that this form was
different from any previously reported from sheep or goats because of
its peculiar "polar cap," Pellerdy (1965) said that it was a synonym
of E. arloingi (i.e., E. ovina) . Shah and Joshi (1963) said that, except
for the shape of the micropylar cap and slightly larger sporocyst size,
E. hawkinsi closely resembles E. crandalUs, and they thought that it
might not be a valid species. Acceptance as a separate species will
depend upon further study by other investigators. Jha and Subrama-
nian ( 1966) said that they would report on the validity and structure
of this species in a later communication, but we have not seen it if it
has appeared.
Eimeria punctata Landers, 1955
(Plate 58, Figs. 251-253)
Eimeria honessi Landers, 1952.
[non] E. honessi Alderson, 1951 nomen nudum.
[non] E. media var. honessi Carvalho, 1943.
Description. The following description of E. punctata from sheep
is based on Landers (1952) and Shah (1963). Oocysts ellipsoidal or
subspherical to ovoid, slightly flattened at micropylar end, 18-28 by
16-21 jx with a mean of 21 by 18 /<, (Landers) or 26 by 19 /.i (Shah).
Oocyst wall with conspicuous, uniform, cone-shaped pits about 0.4-0.5
jx in diameter, composed of 2 layers, the outer layer 1.4 /x thick, color-
less to yellowish, and the inner layer 0.4 /.<, thick, greenish to brownish
yellow. Micropyle at small end of oocyst. Micropylar cap impercep-
tible to prominent, colorless, cone-shaped, generally 5-7 /i wide and
1-2 fi high with a mean of 6 by 2 /.<,. Oocyst polar granule ordinarily
present (absent according to Landers). Oocyst residuum usually pres-
ent (absent according to Landers). Sporocysts elongate ovoid (Landers
said that they were spherical or ellipsoidal, but illustrated them as piri-
form). Stieda body faintly perceptible. Sporocysts 12-15 by 7-9 /x
124 THE COCCIDIAX PARASITES OF RUMINANTS
with a mean of 13 by 8 fi (Shah) or 8 /<. in diameter or 10 by 7 fi (Lan-
ders) . Sporocyst residuum present. Sporozoites elongate, lying head to
tail in sporocysts, with a single clear globule at one end.
Chevalier (1966) described the oocysts in the goat. They were
ovoid to ellipsoidal, 21-31 by 15-23 (i with a mean of 26 by 19.5 /.<,, with
a broad micropyle and a high, transparent micropylar cap, a greenish
yellow to brownish green wall, composed of several layers and pitted
like a thimble; the sporocysts were slender but could not be measured
because of the thickness of the oocyst wall. For the same reason he
could not determine whether polar granule, oocyst residuum, or sporo-
cyst residuum were present.
Sporulation Time. According to Landers (1952) the sporulation
time of E. punctata from the sheep is 36-48 hours at room temperature.
According to Chevalier (1966), the sporulation time of E. punctata in
the goat is 2-5 days.
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Ovis aries (domestic sheep) .
Other Hosts. Capra hircus (domestic goat) (Chevalier, 1966).
Location. L T nknown. Oocysts found in feces.
Geographic Distribution. North America (Wyoming, Illinois) , Eu-
rope (Germany).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Landers (1952) found this species in 2 of 9 sheep in
Wyoming, Shah (1963) in 1% of 153 sheep in Illinois, Chevalier
(1966) in V/c of 40 goats in Germany, and Savin (1966) in 0.1% of
900 Angora goats in Turkey.
Remarks. The descriptions of Landers (1952) and Shah (1963) of
E. punctata from sheep and of Chevalier (1966) of E. punctata from
the goat differ in some respects. Further study is needed to determine
whether they were all referring to the same species.
Alderson (1951) named E. honessi from the elk Cervus canadensis
nelsoni in Wyoming, but did not describe it. His name is therefore a
nomen nudum besides being a homonym of E. media var. honessi
Carvalho, 1943.
Eimeria ovina n. sp.
(Plate 58, Figs. 254-256)
Eimeria arloingi forma ovina Krylov, 1961.
Eimeria arloingi Auctores from sheep.
genus Eimeria Schneider, 1875 125
Eimeria faurei (Moussu and Marotel, 1902) of Yakimoff, 1931a,
of Tsygankov, Paichuk and Balbaeva, 1963, and of some other Russian
authors.
[non] Eimeria arloingi (Marotel, 1905) Martin, 1909.
[non] Eimeria faurei (Moussu and Marotel, 1902) Martin, 1909.
Description. The following description is based on those of Honess
(1942), Kamalapur (1961), Jackson (1964), and Chevalier (1965).
who described this species from sheep and separated it from E.
crandallis and E. ahsata. Other descriptions cannot be used because
they were deficient in one of these 2 points. Oocysts ellipsoidal to
ovoid, generally with rather straight sides, slightly flattened at the
micropylar end, 23-36 by 16-24 /x with a mean of 27 by 20 /x (Honess,
1942), 29 by 21 P . (Kamalapur, 1961) 30 by 20 fi (Jackson, 1964)
(Jackson's measurements did not include the height of the cap).
Oocyst wall composed of 2 layers; outer one smooth (occasionally
roughened by regular circular pits in the surface according to Jackson,
1964), greenish (Kamalapur, 1961) or yellow-brown to orange (Jack-
son, 1964), about 1.3 jx thick; inner layer a brownish-yellow membrane
0.5 [i thick (Kamalapur, 1961) or a dark brown to black line (Jack-
son, 1964) . Micropyle present. Micropylar cap present, dome- to
mound-shaped, colorless, 1-3 n high and 4.5-10 /x wide with a mean of
2 by 7 /x (Kamalapur, 1961) or 2 by 8 /x (Jackson, 1964). One or more
oocyst polar granules present, sometimes as small shattered particles.
Oocyst residuum absent. Sporocysts elongate ovoid, with one end
narrow but blunt. Stieda body absent (Kamalapur, 1961) or incon-
spicuous (Jackson, 1964). Sporocysts 11-17 by 6-9 /x with a mean of
14 by 7.5 /x (Kamalapur, 1961) or 15 by 7 /x (Jackson, 1964). Sporo-
cyst residuum present as small granules arranged in rows, groups, or
rosettes. Sporozoites elongate, lying head to tail in sporocysts. Sporo-
zoites with a large clear globule at one end and a smaller one at the
other end.
Honess (1942) said that the oocysts of E. ovina (syn., E. arloingi)
from Ovis canadensis were 24-30 /x long and had mean dimensions of
27.5 by 22.0 /x.
Sporulation Time. Two to 4 days according to Chevalier (1965).
Schizogony and Gametogony. Lotze (1953) studied the life cycle of
E. ovina (syn., E. arloingi) in experimentally infected lambs. The
sporozoites emerge from the oocysts in the small intestine, enter tin 1
crypts of Lieberkiihn, and penetrate through the tunica propria into
the interior of the villi. Here they enter the endothelial cells lining
the central lacteals and grow. The host cell also grows, and its nucleus
becomes very large. There is apparently only one generation of
126 THE COCCIDIAX PARASITES OF RUMINANTS
schizonts and mcrozoitcs. The schizonts become mature 13-21 days
after infection. At this time they are about 122-146 n in diameter and
contain a large number (perhaps hundreds of thousands) of merozoites
about 9 /x long and 2 i± wide.
The merozoites break out of the schizonts and enter the epithelial
cells of the small intestine. Sometimes only a small group of cells at
the bottom of the crypts is parasitized, but in heavy infections
practically all the epithelial cells of the villi are invaded. The infected
villi are enlarged and grayish. Some of these merozoites become micro-
gamonts; these form many microgametes, leaving a large mass of
residual material. Most of the merozoites become macrogametes,
which contain large plastic granules when mature.
Following fertilization, the macrogametes turn into oocysts, which
break out of the host cells and are first seen in the feces 20 days after
infection. Their numbers increase for about 5 days and then decrease
at about the same rate for the next 5 days. Thus the patent period is
about 10 days following a single exposure.
N. Singh and Pande (1967) found endogenous stages in the small
intestine of sheep in India that they thought were those of E. ovina.
However, they were dealing with mixed infections.
Pre-patent Period. Nineteen days according to Lotze (1953).
Type Host. Ovis aries (domestic sheep).
Other Hosts. Ovis canadensis (Rocky Mountain bighorn sheep), 0.
ammon ( argali) , 0. musimon (mouflon).
Location. Small intestine.
Geographic Distribution . Worldwide.
Pathogenicity. Lotze (1952) studied the pathogenicity of E. ovina
(syn., E. arloingi) in 3-month-old lambs experimentally inoculated
with 200,000 to 60 million oocysts. No visible signs were produced by
infections with 1 million oocysts or less. In lambs inoculated with
3 or 5 million oocysts, the feces became soft on the 13th day and then
returned to normal during the next 6 days. The health, general condi-
tion and weight gains of these animals were not affected.
Severe diarrhea was produced with higher doses, but none of the
animals died although one was killed in extremis. In general, the ex-
perimentally infected lambs appeared normal up to the 13th day after
inoculation, when their feces became soft. In the more heavily infected
lambs the feces then became watery, and diarrhea was severe begin-
ning on the 15th day. Blood-tinged mucus was passed by affected
lambs only occasionally. The feces began to return to normal on the
17th day and were usually nearly normal by the 20th day. Lambs
with marked diarrhea became weak and refused feed.
genus Eimeria Schneider, 1875 127
At autopsy, only a few small, slightly hemorrhagic areas scattered
throughout the lining of the small intestine were seen up to the 13th
day. From the 13th to 19th days the small intestine was more or less
thickened and edematous, and thick, white opaque patches made up of
groups of heavily parasitized villi were present.
The villi containing the schizonts become thin-walled sacs and are
presumably destroyed. The sexual stages are clustered in the epithelial
cells of the villi and destroy these cells when they emerge. However,
they do not do as much damage as the asexual stages, since the condi-
tion of affected animals appeared to improve before oocysts were shed.
E. ovina is less pathogenic than E. ninakohlyakimovae or E. ahsata.
Cross-Transmission Studies. Krylov (1961) attempted to transmit
E. ovina from sheep to goats and E. arloingi from goats to sheep. He
failed to produce clearcut infections in 9 goats 3 months to 2 years of
age by feeding as many as 100,000 oocysts of E. ovina from sheep or
in 3 lambs 1.5 months old by feeding 210,000 oocysts of E. arloingi
from goats. He had no difficulty, however, in infecting 4 lambs 1.5-2.0
months old with E. ovina from sheep.
Krylov's failure to infect goats with the form from sheep and vice
versa led him to conclude that the forms in the 2 hosts are biological
races or xenodemes; he therefore gave the name E. arloingi forma
ovina to the form in the sheep. However, his work is subject to some
criticism because it is not known whether his experimental animals had
had previous natural infections or were free of coccidia at the time of
exposure.
Lotze et al. (1961) were unable to produce patent infections in goats
with E. ovina (syn., E. arloingi) from sheep or in sheep with E. arloingi
from goats. However, they (1961, 1964) found schizonts in the
mesenteric lymph nodes of both sheep and goats fed E. ovina (syn., E.
arloingi) oocysts from sheep. The schizonts in the sheep were more
numerous than in the goats; they appeared normal, were about 30-360 /t
in diameter, and contained merozoites that appeared to be approach-
ing maturity. The schizonts in the goats were about 32-100 fx in
diameter, appeared somewhat abnormal, and their merozoites were
not as mature as those in the sheep; presumably they later degenerated.
Bhatia and Pande (1967a) found giant schizonts in the mesenteric
lymph nodes of a naturally infected kid in India, but were unable to
assign them to a species.
Tsygankov, Paichuk and Balbaeva (1963) were unable to transmit
E. ovina (which they called E. jaurci) from the sheep to one saiga and
4 kids, although they produced a patent infection in a lamb. They
were unable to transmit E. arloingi (which they called E. faurei)
12S THE COCCIDIAX PARASITES OF RUMINANTS
from the goat to one saiga and one lamb although they produced a
patent infection with it in a kid.
Prevalence. This is probably the commonest coccidium of sheep.
Christensen (1938b) found it in 90% of 100 sheep from Idaho, Mary-
land. New York, and Wyoming; Hammond and Hamilton (1940,
1941) in 94^ of 50 sheep in northern Utah; Shah (1963) in 53% of
153 sheep from Illinois and other states; Balozet (1932a) in 52%
of 63 sheep in Tunisia; Jacob (1943) in 58% of 100 sheep and Chevalier
(1965) in 17% of 183 sheep in Germany; Joyner et al. (1966) in 95%
of 198 sheep in England; Svanbaev (1957) in 52% of 302 sheep in
Kazakhstan; Patyk (1965) in 45% of 222 lambs aged 1-8 months in
Poland; Merdivenei (1959) in 50% of the sheep with coccidiosis that
he examined in Turkey; Wiesenhiitter (1965) in 94% of 642 sheep in
Syria; and Deom and Mortelmans (1956) in 69% of 230 sheep in
Belgian Congo.
Remarks. There is a structural difference between the oocysts of
E. arloingi from the goat and the so-called E. arloingi from sheep.
The oocysts of the former are ellipsoidal, while those of the latter
generally have rather straight sides. This difference was noted by
Lotze (personal communication) and can also be seen by comparing
the illustrations of "E. arloingi" from the sheep given by Kamalapur
(1961) with that of E. arloingi from the goat given by Levine, Ivens
and Fritz (1962).
On the basis of the above evidence, it appears that the "E. arloingi"
of sheep and the E. arloingi of the goat are not the same. We there-
fore believe it best to use the name E. ovina n. sp. for the form from
the sheep, since E. arloingi was first described from the goat.
Eimeria gonsalezi Bazalar and Guerrero, 1970
(Plate 57, Fig. 245; Plate 65, Fig. 291)
Eimeria sp. Patyk, 1965.
Description. Oocysts ellipsoidal or ovoid, 26-38 by 18-26 /.<., slightly
flattened at the micropylar end. Oocyst wall smooth, 1-2 /_<, thick
(mean 1.8 /x), composed of 2 layers, the outer being transparent and
the inner yellowish brown. Micropylar cap 6-9 /i wide and 1-3 /.<. high
with a mean of 8 by 2 /x. Oocyst residuum absent. Oocyst polar gran-
ule present. Sporocysts ovoid, 12-15 by 6-9 j± with a mean of 14 by 8 /.<.,
with a slightly perceptible Stieda body and a residuum. Sporozoites
with 2-3 clear globules each.
Sporulation Time. Four to 6 days according to Patyk (1965).
Schizogony and Gametogony. Unknown.
genus Eimeria Schneider, 1875 129
Pre-patent Period. Unknown.
Type Host. Ovis aries (domestic sheep).
Other Hosts. None.
Location. Unknown. Oocysts found in feces.
Geographic Distribution. South America (Peru), Europe (Poland).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Bazalar and Guerrero (1970) found this species in
17% of 240 sheep in Peru. Patyk (1965) found it in 3% of 222 lambs
aged 1-8 months in Poland.
Remarks. This species resembles E. ovina but differs in that its
micropylar cap extends a little way down the sides of the oocysts and
its oocyst wall does not have straight sides. In addition, since Patyk
(1965) and Bazalar and Guerrero (1970) both reported E. ovina
(as E. arloingi) from their sheep and considered this form different, it
may well be a new species.
Eimeria sp. Mincheva, Sherkov, Monov, Kyurtov,
Bratanov, Meshkov and Donev, 1966
Description. Oocysts spherical to ellipsoidal, with a thick, smooth
colorless wall. Micropyle prominent. Spherical oocysts 10 /.<. in di-
ameter, ellipsoidal oocysts 10 by 6 jx. Sporocysts spherical. No other
information given.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepatent Period. Unknown.
Type Host. Ovis aries (domestic sheep) .
Other Hosts. None.
Location. Oocysts in feces.
Geographic Distribution. Europe (Bulgaria).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
Eimeria ahsata Honess, 1942
(Plate 58, Fig. 257; Plate 59, Figs. 258-259)
Eimeria ah-sa-ta Honess, 1942.
Description. Oocysts ellipsoidal to somewhat ovoid, slightly flat-
tened at the micropylar end, which is almost always the smaller one.
130 THE COCCTDIAX PARASITES OF RUMIXAXTS
According to Lcvinc et al. 1 1962) , the oocysts from the domestic sheep
in Illinois are 36-44 by 22-29 p. with a mean of 40 by 26 fi. Those
originally described from the domestic sheep by Honess (1942) in
Wyoming were 29-37 by 17-28 /.i with a mean of 33 by 23 /*; those
described by him from the bighorn sheep were 30-40 by 20-30 p. with
a mean of 33 by 24 //,. The oocysts described from the domestic sheep
in Illinois by Kamalapur (1961) were 23-48 by 20-28 fi with a mean
of 36 by 24 /x; those described from this host in Rumania by Donciu
(1961) were 31-39 by 22-28 M ; those described from this host in
Australia by Jackson (1964) were 34-47 by 22-29 /x with a mean of
39.4 by 25.6 )x (not counting the micropylar cap which averaged
9.9 /J. wide and 2.6 ,u high) ; those described from this host in Germany
by Chevalier (1965) were 30-39 by 18-30 /.i; those reported from
this host in Senegal by Vassiliades (1965) were 30-34 by 18-24 /<.
with a mean of 31.2 by 20.1 ,u. Oocyst wall smooth, lavender to pink-
ish yellow to light brown, composed of 2 layers 0.9-1.3 fi in total
thickness. The true outer layer accounts for almost the whole thick-
ness of the wall; in intact oocysts the inner layer appears simply
as a dark line on the inner surface of the wall and may sometimes be
somewhat wrinkled at the micropylar end; in crushed oocysts the
inner layer is a distinct membrane separate from the outer layer.
Micropyle present. Micropylar cap present, dome-shaped, 0.4-4.0 /x
high and 7-11 \x wide with a mean of 2 by 9 \x according to Levine et al.
(1962) (mean 2.6 by 9.9 \x according to Jackson, 1964). One or occa-
sionally more oocyst polar granules ordinarily present. Oocyst residuum
absent (Jackson, 1964, saw an oocyst residuum in a very small number
of oocysts). Sporocysts elongate ovoid, rounded at both ends, with one
end somewhat broader than the other. Stieda body absent (inconspicu-
ous according to Jackson, 1964). Sporocysts 18-20 by 7-10 \x with a
mean of 18 by 9 ,u in the domestic sheep according to Levine et al.
( 1962 ) ; 12-22 by 7-10 /x with a mean of 17 by 6 fi in this host accord-
ing to Kamalapur ( 1961 ) ; 10-12 by 6-8 /.<. according to Donciu ( 1961) ;
with a mean of 19 by 8 /.<, according to Jackson (1964). Sporocysts
in 3 hosts 9-11 by 5-8 \x according to Rysavy (1954) ; in bighorn
sheep with a mean of 15.4 by 7.8 \x according to Honess (1942).
Sporocyst residuum present. Sporozoites elongate, lying head to tail
in sporocysts. One to three clear globules present in each sporozoite.
Sporulation Time. According to Chevalier (1965) 36-72 hours.
Schizogony and Gametogony. According to Davis, Bowman and
Smith (1963), the schizonts occur mostly in the central portion of
the mucosa of the small intestine, most being in the jejunum; a few
occur in the lacteals of the villi and a very few in the muscularis
genus Eimeria Schneider, 1S75 131
mucosae. Ten days after experimental inoculation, the schizonts were
50 jx or less in size; at 15 days the average size was 184 by 165 jx
and the largest one was 265 by 162 /a. The host wall around the
schizonts was up to 9 /x thick, the larger the schizont the thinner the
wall. The outer wall of the host membrane around young schizonts
was fimbriated, with radially arranged fibril-like strands as long as
13 ix.
Davis, Bowman and Smith (1963) first saw gametogony 12 days
after infection. The macrogametes measured 35-45 p. and the mi-
crogamonts about 26 by 36.5 /.<.. The gamonts and oocysts were
mostly in the columnar epithelial cells lining the intestinal glands
rather than in epithelial cells covering the villi as in E. arloingi.
Smith and Davis (1965) found that the patent period was 12 days
in lambs inoculated with oocysts in dry feed and 10-11 days in lambs
inoculated with oocysts in liquid.
Precedent Period. Eighteen to 20 days according to Smith, Davis
and Bowman (1960). Smith and Davis (1965) found that the pre-
patent period was 19 days in lambs given oocysts in dry feed, and
20-21 days in lambs given oocysts in liquid.
Type Host. Oris canadensis (Rocky Mountain bighorn sheep).
Other Hosts. Oris aries (domestic sheep); O. musimon (mouflon).
In addition, Rysavy (1954) listed the Central Asian wild goat Capra
sibirica as a host in Czechoslovakia, and Krylov ( 1961 ) reported
finding it in the domestic goat in Tadzhikhistan; Jha and Subramanian
(1966) in the goat in Uttar Pradesh, India; and Wiesenhutter (1965)
in Syria. These reports from Capra may possibly have been of E.
christenseni. Chevalier (1966) reported E. ahsata from the domestic
goat in Germany, but his description resembles that of E. arloingi.
Location. Small intestine.
Geographic Distribution, United States (Alabama, Illinois, Wy-
oming), USSR (Tadzhikhistan), Europe (Czechoslovakia, Germany.
Rumania), Turkey, India (Uttar Pradesh), Australia, Africa
(Senegal).
Pathogenicity. Smith, Davis and Bowman (1960) considered this
species the most pathogenic of all sheep coccidia. They produced fatal
infections in 4 out of 9 lambs 1-3 months old by feeding them 100,000
oocysts. The intestines of the infected lambs had thickened, somewhat
edematous areas in the upper part. The Peyer's patches and the last
20-25 cm of the small intestine above the ileocecal valve were inflamed.
Smith and Davis (1965) found that as few as 31,000 oocysts
caused death in lambs when administered in dry feed, and 100,000
oocysts when given in liquid.
132 THE COCCIDIAX PARASITES OF RUMINANTS
Mahrt and Sherrick (1965) described an outbreak of coeeidiosis
in Illinois feeder lambs in which E. ahsata was the principal cause
of death. Four flocks containing 2,000 lambs imported from Texas
were crowded into feedlots; 33-40% had diarrhea, inappetence and de-
pression. Weight loss was a prominent sign, and lambs which recovered
did not gain weight well. About 4-6% of the lambs died. Of the
oocysts present in the lambs' feces, 65% were E. ahsata, 18% E. nina-
kohlyakimovae, 10% E. arloingi, 5% E. granulosa and 2% E. cran-
dallis. Endogenous stages of the coccidia were abundant in the small
intestine.
Cross-Transmission Studies. Krylov (1961) was unable to infect
a 2-year-old domestic goat with E. ahsata from the domestic sheep;
three 3-month-old goats passed a few oocysts from 2 to 24-28 days
after infection; these were probably not due to cross-transmission.
Krylov 1 1961) was unable to infect three 1.5-month-old lambs with
"E. ahsata" (possibly E. christenseni) from the domestic goat.
Prevalence. Relatively little is known about the prevalence of
E. ahsata because it had been confused with E. arloingi until Smith,
Davis and Bowman (1960) showed clearly that it was different.
Shah (1963) found it in 24 r f of 153 sheep from Illinois and other
states, Chevalier (1965) in 39% of 200 sheep in Germany, and Joyner
et al. (1966) in 62% of 198 sheep in England. Jha and Subramanian
(1966) said that they found it in 5% of 253 goats in Uttar Pradesh,
India. Wiesenhiitter 1 1965) reported it from 34% of 642 sheep and 42%
of 413 goats in Syria, and Savin 1 1966) said he found it in 63% of
900 Angora goats in Turkev.
Eimeria crandallis Honess, 1942
(Plate 59, Figs. 260-261 ; Plate 60, Figs. 264-265)
[non] E. crandallis Honess, 1942 of Chevalier (1966) from the goat.
? Eimeria hirci Chevalier, 1966.
Description. Because this species has been described from 3 dif-
ferent hosts, the descriptions are given separately for each.
E. crandallis was first found by Honess (1942) in the Rocky Moun-
tain bighorn sheep Ovis canadensis. He illustrated the oocysts as
ellipsoidal, with a micropylar cap at one end. He said that the oocysts
were 17.5-23 by 17.5-22 /x with a mean of 22 by 19 //. The polar cap
varied in height from ''the slightest indication" to 1.7 /.i, and in width
from 3.3-6.6 ,u; it averaged 0.8 by 4.9 \x. Oocyst wall colorless, faint
pink or greenish, with a distinctly demarcated outer edge. Number
genus Eimeria Schneider, 1875 133
of layers in oocyst wall not given. Oocyst polar granule and oocyst
residuum not mentioned, but polar granule shown in photomicrograph.
Sporocysts 8-11 by 5-8 fx with a mean of 10 by 6 /x. Stieda body and
sporocyst residuum not mentioned; not discernible in photomicrograph.
E. crandallis was described from the domestic sheep by Kamalapur
(1961). Jackson (1964) also described it from sheep, but, since he
may have been dealing with a mixture, we are not using his description.
According to Kamalapur (1961) the oocysts are subspherical to broadly
ellipsoidal, with a slightly narrower micropylar end, 18-28 by 15-20 [x
with a mean of 22 by 18 /x. Oocyst wall smooth, composed of 2 layers,
the outer one colorless and 0.9-1.3 i± thick with a mean of 1.1 p., and
the inner one a darkish yellow membrane lining the inner surface,
slightly wrinkled at the micropylar end. Micropyle present, distinct
to indistinct. Micropylar cap present or absent (present in 87% of
the oocysts he studied), colorless, flat to saucer-shaped, 0.2-1.3 /x
high and 2.2-5.8 fx wide with a mean of 0.8 by 4 [x. One or more oocyst
polar granules usually present, often appearing as shattered small
particles. Oocyst residuum absent. Sporocysts broadly ovoid, with
one end pointed, sometimes blunt. Stieda body absent. Sporocysts
8-13 by 6-9 \x with a mean of 11 by 7 \x. Sporocyst residuum present
as a few small granules or absent. Sporozoites at ends of sporocysts,
transverse, with one or 2 clear globules.
E. crandallis was described from the domestic goat by Levine, Ivens
and Fritz (1962), Shah and Joshi (1963) and Singh (1964). The
oocysts are ellipsoidal, slightly flattened at the micropylar (small) end,
19-27 by 14-20 ,x with a mean of 22-23 by 18-19 fx (17-24 by 17-22 fi
according to Singh, 1964). Oocyst wall composed of 2 layers, the outer
one smooth, colorless and 0.8-0.9 (x thick, and the inner one light
brownish yellow and 0.4 \x thick. Inner layer forms a membrane
which is sometimes slightly wrinkled at the micropylar end. Micropyle
present, usually indistinct, rarely invisible; oocyst wall relatively
thin at micropylar end. Micropylar cap absent or present (present
in 25% of Levine, Ivens and Fritz's material, and presumably more
often in Shah and Joshi's material), colorless, rather flat to mound-
shaped, sometimes slightly pointed, when present 0.4-2 \x high and
3-6 \x wide with a mean of 1 by 3-5 /x. One to several oocyst polar
granules present, often appearing shattered into coarse or fine particles.
Oocyst residuum absent. Sporocysts broadly ovoid, usually rather
pointed at one end, sometimes blunt. Stieda body ordinarily absent,
but occasionally present and minuscule. Sporocysts 8-12 by 6-8 /x with
a mean of 10-11 by 7 /x (14 by 4 /x according to Singh's (1964) text.
but about 10 by 4-6 (x according to his drawing). Sporocyst residuum
134 THE COCCIDIAN PARASITES OF RUMINANTS
usually present, sometimes absent or consisting of a few sparse gran-
ules. Sporozoites lie at more or less of an angle in the sporocysts, but
primarily at the ends. Sporozoites sometimes contain one or 2 clear
globules.
Descriptions given by others (Rysavy, 1954; Donciu, 1961; Ray,
1961) did not differentiate between the forms in different hosts.
Sporulation Time. One to 3 days at room temperature in India,
according to Singh 1 1964) .
Schizogony and Gametogony. Unknown. See the discussion of
E. arloingi.
Prepotent Period. Fifteen to 20 clays according to Pout (1965).
Type Host. Ovis canadensis (Rocky Mountain bighorn sheep).
Other Hosts. Ovis aries (domestic sheep), 0. musvmon, 0. amnion.
In addition, this species has been reported from the domestic goat
Capra hircus, from C. sibirica, C. aegagrus, Capreolus capreolus,
Cervus elaphus, Dania dama, Rupricapra rupricapra and Gazella
subgutturosa (all but the bighorn sheep, domestic sheep and domestic
goat by Rysavy, 1954 and Donciu, 1961). The validity of the identi-
fication of this species in goats is discussed below. It is extremely
dubious that it occurs in any other host genera.
Location. Small intestine, extending anteriorly from the ileocecal
valve (Pout, 1965).
Geographic Distribution. Form in bighorn sheep: USA (Wyoming).
Form in domestic sheep: USA (Alabama, Illinois), Europe (En-
gland, Czechoslovakia, Poland, Rumania), USSR (Tadzhikhistan),
India (Bombay, Bihar, Kashmir, Madhya Pradesh, Madras, Uttar
Pradesh) , Australia, Africa (Senegal) .
Form in domestic goat: USA (Illinois), Europe (Czechoslovakia,
Germany, Rumania), India (Bihar, Madhya Pradesh, Orissa, Uttar
Pradesh).
Pathogenicity. Smith and Davis (1961) found that inoculations of
100,000 to 3 million infective oocysts from sheep in Alabama had no
noticeable harmful effects in lambs. Pout (1965) found that 2,500
oocysts from sheep in England daily for 7 days had no noticeable
effect, whereas 250,000 oocysts daily for 7 days caused lassitude, soft,
gray feces, indications of abdominal pain, and, in one lamb, death.
The ileum was slightly thickened and the ileo-colic lymph nodes were
enlarged.
Cross-Transmission Studies. Krylov (1961) was unable to infect
two 3-month-old kids with E. crandallis from sheep, and obtained
dubious results in an attempt to infect 2 one-year-old goats.
Prevalence. Shah (1963) found E. crandallis in 24% of 153 sheep
genus Eimeria Schneider, 1S75 135
from Illinois and other states, Joyner et al. (1966) in 90% of 198 sheep
in England, Patyk (1965) in 1% of 222 lambs aged 1-8 months in
Poland, Sayin (1966) in 11% of 900 Angora goats in Turkey, and
Wiesenhutter (1965) in 25% of 642 sheep and 22% of 413 goats in
Syria. Shah and Joshi (1963) found it in 10% of 300 goats in Madhya
Pradesh, India; Singh (1964) in 29% of 214 goats; and Jha and
Subramanian (1966) in 13% of 243 goats in Uttar Pradesh, India.
Remarks. There is a question whether E. crandallis parasitizes
both sheep and goats, even though it has been reported from both hosts.
The oocysts described from the 2 hosts appear to be structurally
identical, but the fact that Krylov (1961) failed to transmit this
coccidium from sheep to goats suggests that there must at least be
host-specific strains or denies. At any rate, we do not believe that
reports of this species from host genera other than Ovis and Capra
can be accepted without proof of cross-transmissibility.
Eimeria arkhari Yakimoff and Matschoulsky, 1937
(Plate 10, Fig. 60)
Description. Oocysts ellipsoidal, often ovoid, with a double-con-
toured wall (illustrated as composed of a single layer) up to 1 /<, thick,
sometimes yellowish. Micropyle absent. Oocysts 20-24 by 18-20 /<,
with a mean of 22.4 by 17.4 jx. Oocyst polar granule and oocyst
residuum absent, Sporocysts ellipsoidal, 6-8 by 6 /x. Sporocyst resid-
uum absent, Sporozoites sausage-shaped.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Ovis vignei (urial, arkhar) (Yakimoff and Matschoul-
sky, 1937a gave the host as "Ovis vignei s. O. arkhar") .
Other Hosts. Ovis amnion polii and O. a. sewerzowi (argali)
(Yakimoff and Matschoulsky, 1940).
Location. Unknown. Oocysts found in feces.
Geographic Distribution. USSR (Tashkent zoo).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
Remarks. Pellerdy (1965) said that this species was difficult to
distinguish from E. faurei and E. ninakohlyakimovae; its one clearly
distinctive feature, he said, might be the absence of a sporocyst resid-
uum, which differentiated it from all other sheep coccidia.
GENUS ISOSPORA SCHNEIDER, 1881
In this genus, the oocyst has two sporocysts, each containing four
sporozoites. The synonymy of this genus has been given by Pellercly
(1963).
Isospora orlovi Tsygankov, 1950
(Plate 59, Fig. 262)
Description. Oocysts ellipsoidal, ovoid, piriform, cylindrical or
figure-8 shaped, dark gray. Oocyst Avail smooth, about 1 /<. thick,
described as composed of 2 layers (but illustrated with one layer),
the outer one yellow-green or light green, the inner layer rose, dark
rose, red or brown. Oocysts 27-35 by 15-20 /.<.. Micropyle absent.
Oocyst polar granule and oocyst residuum absent. Sporocysts ellip-
soidal, ovoid or spherical, 15-20 by 13-17 /x (the spherical ones 13.5-
15 jx in diameter) . Stieda body absent. Sporocyst residuum spherical
or shapeless. Sporozoites elongate ellipsoidal, 7-10 by 4-6 fi.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepatent Period. Unknown.
Type Host. Camel, species not stated.
136
GENUS IsOSTpOra SCHNEIDER, 1881 137
Location. Oocysts in feces.
Geographic Distribution. USSR (Kazakhstan)
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Unknown.
Isospora rangiferis Yakimoff, Matschoulsky
and Spartansky, 1937
(Plate 61, Fig. 272)
Isospora sp. Yakimoff, Sokoloff and Matschoulsky, 1936.
Description. Oocysts ovoid or subspherical, 26-32 by 24-30 /x with
a mean of 29 by 24.5 i±. Oocyst wall described as double-contoured,
illustrated with a single layer. Micropyle absent. Oocyst residuum
absent. Oocyst polar granule present. Sporocysts ovoid with a
"double-contoured" wall and prominent Stieda body. Sporocyst
residuum present. Sporocysts described in text as 16-19 by 8-12 ».,
listed in table as 12-16 by 8-12 /i. Sporozoites comma-shaped, illus-
trated with a clear globule at the large end.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepatent Period. Unknown.
Type Host. Rangifer tarandus (reindeer).
Location. Feces.
Geographic Distribution. USSR (Murmansk area, Kola Peninsula).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Yakimoff, Sokoloff and Matschoulsky (1936) found
this species in 4 out of 39 reindeer from the Murmansk area. Yakimoff,
Matschoulsky and Spartansky (1937) found it in 1 out of 27 reindeer
from the Kola Peninsula.
Isospora capreoli Svanbaev, 1958
(Plate 59, Fig. 263)
Description. Oocysts ovoid or piriform, 40-46 by 28-32 /x with a
mean of 43 by 31 /a. Micropyle prominent, 4-5 /x wide, occasionally
with an inconspicuous micropylar cap. Oocyst wall smooth, apparently
composed of 2 layers, 2-4 /x thick, yellowish brown or brown, with
13S THE COCCTDIAN PARASITES OF RUMINANTS
the inner layer radially striated. Oocyst residuum present. Oocyst
polar granule absent. Sporocysts piriform or ovoid, 19-25 by 11-16 fi
with a mean of 21.7 by 13.5 /i. Sporozoites piriform or comma-shaped,
8-13 by 3-4 ti with a mean of 11 by 4 /a.
Sporulation Time. Three to 4 days at 25-28 C in 2% potassium
bichromate solution according to Svanbaev (1958, 1959).
Schizogony and Gametogony. Unknown.
Pre patent Period. Unknown.
Type Host. Capreolus capreolus (roe deer).
Location. Oocysts in feces.
Geographic Distribution. USSR (Kazakhstan).
Pathogenicity. Unknown .
Cross-Transmission Studies. None.
Prevalence. Svanbaev (1958) found this species in 3 roe deer.
Isospora aksaica Bazanova, 1952
Description, Oocysts spherical, dark silver under low magnification
and light pinkish gray under high, 26 i± in diameter. Oocyst wall 1.6
fx, thick, smooth and double-contoured, with a light blue outer layer
and a greenish, dingy rose inner layer. Micropyle presumably absent.
Oocyst residuum presumably absent. Oocyst polar granules possibly
present. Sporocysts ellipsoidal or spherical, 22 by 15 /x. Sporocyst re-
siduum presumably absent. Sporozoites spherical, bean-shaped or
ellipsoidal, 15 by 11 /x.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Bos taurus (ox).
Location. Oocysts found in feces.
Geographic Distribution, USSR (Kazakhstan).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence, Unknown.
Remarks. There is a question whether this is a valid species of
bovine coccidium or a pseudoparasite. Levine and Mohan (1960),
Levinc (1961) and Pellerdy (1965) discussed this question; all were
dubious about the validity of the species.
genus Isospora Schneider, 1SS1 139
Isospora sp. Levine and Mohan, 1960
(Plate 60, Fig. 267)
? Isospora sp. Cooper and Gulati, 1926.
Description. Oocysts usually subspherical, occasionally spherical,
21-33 by 20-32 /x with a mean of 27 by 25 /.<,. Oocyst wall smooth,
colorless, pale lavender or pale yellowish, composed of a single layer
about 1 ji thick, sometimes apparently lined by a thin membrane.
Micropyle absent. Oocyst residuum absent. Several irregular, refrac-
tile polar granules present. Sporocysts lemon-shaped, quite thick-
walled, 14-20 by 10-12 jx with a mean of 17 by 11 i±. Sporocyst
Stieda body a button-shaped cap, with a dependent globular, hyaline
mass (substiedal body) protruding into the interior of the sporocyst.
Sporocyst residuum finely granular. Sporozoites appear sausage-
shaped, not arranged in any particular order in sporocyst. Sporocyst
residuum and sporozoites enclosed in a membrane, forming more or
less of a ball within the sporocyst.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Bos taunts (ox) ; Bos taurus-B. indicus hybrids.
Other Hosts. Presumably Bos indicus (zebu) (See Cooper and
Gulati, 1926, below).
Location. Oocysts found in feces.
Geographic Distribution. United States (Illinois), India (?).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Levine and Mohan (1960) found this form in 11%
of 54 cattle on 3 farms in Illinois.
Remarks. Levine and Mohan (1960) found that this form was prac-
tically indistinguishable from /. lacazci of the English sparrow, and
concluded that the oocysts they found in boAune feces might well
be those of /. lacazei. Their calculations indicated that oocysts pres-
ent in sparrow droppings might pass through a calf and be discovered
in its feces if it ate a single fecal deposit from a single sparrow in
the course of a clay.
It is possible that the Isospora sp. reported from bovine feces in
India by Cooper and Gulati (1926) might have been the same form as
this, but their description was too meager for any conclusion to be
drawn.
140 THE COCCIDIAX PARASITES OF RUMINANTS
Isospora sp. Shah, 1963
{Plate 60, Fig. 266)
Description. Oocyst usually subspherical, occasionally spherical,
20-25 by 20-24 /x with a mean of 23 by 22 /x. Oocyst wall composed of
2 layers, the outer one smooth, pale yellowish or pale yellowish brown
and 1 /x thick, the inner one brownish yellow, 0.5 \x thick, forming a thin
membrane. Micropyle and micropylar cap absent. Oocyst residuum
absent. Oocyst polar granule ordinarily present. Sporocysts lemon-
shaped, finite thick-walled. Stieda body in form of a button-shaped cap
with a dependent hyaline mass extending into the interior of the
sporocyst, 14-15 by 9-10 /t with a mean of 14 by 10 /±. Sporocyst
residuum present as fine granules. Sporozoites more or less sausage-
shaped, not arranged in any particular order in sporocyst. There
appeared to be a membrane within the sporocysts which enclosed both
the sporozoites and sporocyst residuum so that they formed more
or less of a ball.
Sporulation Time. Unknown.
Schizogony and Gametogony. Unknown.
Prepotent Period. Unknown.
Type Host. Ovis aries (domestic sheep).
Location. Unknown. Oocysts found in feces.
Geographic Distribution. North America (Illinois).
Pathogenicity. Unknown.
Cross-Transmission Studies. None.
Prevalence. Shah (1963) found this form in 1% of 153 sheep from
Illinois and other states; the infected sheep came from Illinois.
Remarks. It is uncertain, as Shah ( 1963) said, whether this form
is actually a genuine parasite of the sheep or a pseudoparasite; it
resembles I. lacazei from the English sparrow and may have been a
feed contaminant passing through the sheep.
GENUS WENYONELLA HOARE, 1933
In this genus, the oocyst has four sporocysts each containing four
sporozoites.
Wenyonella markovi Grobov and Ven-Shun', 1963
(Plate 60, Fig. 268)
Description. Oocysts shaped like a round-bottomed urn, bright
yellow or yellow gray, 31-46 by 21-31 /x with a mean of 39.4 by 25.2 fi.
Oocyst wall composed of 2 layers, 1.5-2.3 /x thick with a mean of
1.7 /.<,; outer layer thin, smooth, with fine stippling on its surface;
inner layer thick, rough. Micropyle prominent at small end of oocyst,
4-6 [x in diameter with a mean of 5.0 /x. Oocyst polar granule and
oocyst residuum absent. Sporocysts ellipsoidal, apparently without
Stieda body, 9-12 by 8-12 /x with a mean of 11 by 10 /a. Sporocyst
residuum absent. Sporozoites 5-6 by 5 /x with a mean of 5.2 by 4.7 /<.
Each sporozoite contains a "polar granule."
Sporulation Time. According to Grobov and Yen '-Shun' (1963), the
sporulation time in 2% potassium dichromate solution at room
temperature (13-20 C) was 26-30 days.
Schizogony and Gamctogony. Unknown.
141
142 THE COCCIDIAN PARASITES OF RUMINANTS
Prcpatent Period. Unknown.
Type Host. Capreolus caprcolus pygargus (Siberian roe deer)
Location. Oocysts found in feces.
Geographic Distribution. USSR (Primorskii region).
Pa thoge nic it y . Unknown .
Cross-Transmission Studies. None.
Prevalence. Unknown.
DISCUSSION
In Tables 1 through 9 are summarized the known structural char-
acters of the known species of coccidia from ruminants. Tables 1
through 8 give the characters of the species of Eimeria, arranged by
host family or subfamily, while Table 9 gives the characters of the
Isospora and Wenyonella species.
Number of Species of Ruminant Coccidia
A total of 100 named species of coccidia is included in this mono-
graph. Eimeria is by far the most common genus, with 95 named
species. In addition, 4 species of Isospora and one of Wenyonella have
been named.
While this may seem quite a large number, it is, as in the rodent
coccidia, only a small percentage of the number of species which must
actually occur in ruminants. In Table 10 are listed the numbers of
genera and species in each ruminant family together with the numbers
of species of Eimeria which have been described from them. Eimeria
has been described from only 30>
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PLATES
197
Plate 1
Fig. 1. E. cameli (Henry and Masson, 1932) Reichenow, 1952. Oocyst from
the camel (from Tsygankov, 1950 — cited as E. kazachstanica) . X 700.
Fig. 2. E. cameli (Henry and Masson, 1932) Reichenow, 1952. Oocyst from
Camelus dromedarius (from Dubev and Pande, 1964 — cited as E. noelleri).
X 1000.
Fig. 3. E. dromedarii Yakimoff and Matschoulsky, 1939. Oocyst from Camelus
dromedarius (from Yakimoff and Matschoulsky, 1939).
Fig. 4. E. dromedarii Yakimoff and Matschoulsky, 1939. Oocyst from Camc-
lus dromedarius (from Dubey and Pande, 1964). X 2100.
198
Plate 2
Fig. 5. E. cameli (Henry and Masson, 1932) Reichenow, 1952. Oocyst from
Camelus dromedarius in the mucosa (from Henry and Masson, 1932b — cited
as Globidium cameli).
Figs. 6-8. E. cameli (Henry and Masson, 1932) Reichenow, 1952, from Ca-
melus bactrianus (from Enigk, 1934 — cited as Globidium cameli). Fig. 6.
Cross section of an unsporulated oocyst. X 1050. Fig. 7. Section of an imma-
ture schizont. X 1S00. Fig. S. Section of a schizont or microgametocyte be-
fore blastophore formation. X 1900.
199
10
f ^e©
i/;
11
12
Plate 3
Figs. 9-12. Eimeria cameli (Henry and Masson, 1932) Reichenow, 1952 from
Camelus bactrianus (from Enigk, 1934 — cited as Globidium cameli). Fig. 9.
Section of a ripe schizont. X 1800. Fig. 10. Section of an immature micro-
gametocyte. X 1800. Fig. 11. Section of a mature microgametocyte. X 1800.
Fig. 12. Developing macrogamete. X 1200.
200
Plate 4
Fig. 13. E. pellerdyi Prasad, 1960 emend. Pellerdy, 1965. Oocyst from Ca-
melus bactrianus (from Prasad, 1960). X 2002.
Figs. 14-15. E. rajasthani Dubey and Pande, 1963. From Camelus dromeda-
rius (from Dubey and Pande, 1963). Fig. 14. Oocyst. X 1638. Fig. 15. Sporo-
cyst. X 163S.
Fig. 16. E. bactriani n. sp. Oocyst from the camel (from Iwanoff-Gobzem,
1934 — cited as E. cameli) .
Fig. 17. E. bactriani n. sp. Oocyst from the camel (from Yakimoff, 1935a —
cited as E. cameli) .
Figs. 18-19. E. bactriani n. sp. from Camelus bactrianus (from Enigk, 1934 —
cited as E. cameli). Fig. IS. Schizont. X 163S. Fig. 19. Immature micro-
gametocyte. X 1638.
201
Plate 5
Fig. 20. E. lamae Guerrero, 1967. Oocyst from Lama pacos (from Guerrero,
1967). X2295.
Fig. 21. E. alpacae Guerrero, 1967. Oocyst from Lama pacos (from Guerrero,
1967). X2295.
Fig. 22. E. punoensis Guerrero, 1967. Oocyst from Lama pacos (from Guer-
rero, 1967). X2295.
Fig. 23. E. austriaca Supperer and Kutzer, 1961. Oocyst from Ccrvus ela/phus
(from Supperer and Kutzer, 1961). X 1020.
Fig. 24. E. ivassilewskyi Rastegaieff, 1930. Oocyst from Axis axis (from Ras-
tegaieff, 1930).
Figs. 25-26. E. asymmetrica Supperer and Kutzer, 1961 from Cervus elaphus
(from Supperer and Kutzer, 1961). Fig. 25. Insporulated oocyst. X 1020.
Fig. 26. Sporulated oocyst. X 1020.
202
Plate 6
Figs. 27-2S. E. asymmetric a Supperer and Kutzer, 1961 from Cervus elaphus
(from Boch and Lucke, 1961). Fig. 27. Unsporulated oocyst. X 820. Fig. 28.
Sporulated oocyst. X S20.
Figs. 29-30. E. robusta Supperer and Kutzer, 1961 from Cervus elaphus (from
Boch and Lucke, 1961 — cited as E. cervi) . Fig. 29. Unsporulated oocyst.
X S20. Fig. 30. Sporulated oocyst, X 820.
Fig. 31. E. peruviana Yakimoff, 1934. Oocyst from Lama glama (from Yaki-
moff, 1934).
Figs. 32-34. E. schoenbuchi Boch, 1963. Oocysts from Cervus elaphus (from
Boch, 1963). XS20.
2o:
Plate 7
Figs. 35-36. E. robust a Supperer and Kutzcr, 1961 from Cervus elaphus (from
Supperer and Kutzer, 1961). Fig. 35. Unsporulated oocyst. X 740. Fig. 36.
Sporulated oocyst. X 740.
Fig. 37. E. sordida Supperer and Kutzer, 1961 from Cervus da pirns (from
Supperer and Kutzer, 1961). X 902.
Fig. 38. E. elaphi Jansen and van Haaften, 1966 from Cervus elaphus (from
Jansen and van Haaften, 1906) .
Fig. 39. E. odocoilei Levine, Ivens and Senger, 1967 from Odocoileus h. hemi-
onus (from Levine, Ivens and Senger, 1967). X 1924.
Fig. 40. E. arctiea Yakimoff, Matschoulsky and Spartansky, 1939 from Rangi-
fer taraitdus (from Yakimoff, Matschoulsky and Spartansky, 1939).
204
Plate S
Fig. 41. E. wapiti Honess, 1955 from Cervus canadensis nelsoni (from Honess,
1955).
Fig. 42. E. mayeri Yakimoff, Sokoloff and Matschoulsky, 1936 from Rangifer
tarandus (from Yakimoff, Sokoloff and Matschoulsky, 1936) .
Fig. 43. E. muehlensi Yakimoff, Sokoloff and Matschoulsky, 1936 from Rangi-
fer tarandus (from Yakimoff, Sokoloff and Matschoulsky, 1936).
Fig. 44. E. tarandiha Yakimoff, Sokoloff and Matschoulsky, 1936 from Rangi-
fer tarandus (from Yakimoff, Sokoloff and Matschoulsky, 1936).
Figs. 45-46. E. ponderosa Wetzel, 1942 from Capreohis capreohis (from Boch
and Lucke, 1961). Fig. 45. Sporulatecl oocyst. X 850. Fig. 46. Sporulated
oocyst, X 820.
Fig. 47. E. panda Supperer and Kutzer, 1961 from Capreohis capreohis (from
Boch and Lucke, 1961). X 650.
Fig. 4S. E. ponderosa Wetzel, 1942 from Capreohis capreolus (from Wetzel,
1942). X 1000.
Fig. 49. E. superba Pellerdy, 1955 from Capreohis capreohis (from Boch and
Lucke, 1961). X 850.
Fig. 50. E. sp. Boch and Lucke, 1961 from Capreohis capreolus (from Boch
and Lucke, 1961). X 850.
Fig. 51. E. rotunda Pellerdy, 1955 from Capreohis capreolus (from Boch and
Lucke, 1961). X 820.
205
C\
r •
s
&
VI
43
206
54
51
Plate 9
Fig. 52. E. antilocaprae Huizinga, 1942 from Antilocapra americana (from
Todd, Hammond, and O'Gara, 1967). X 2057.
Fig. 53. E. copreoli Galli-Valerio, 1927 from Capreolus capreolus (from
Pellerdy, 1955 ) .
Fig. 54. E. rotunda Pellerdy, 1955 from Capreolus capreolus (from Pellerdy,
1955).
Fig. 55. E. ponderosa Wetzel, 1942 from Capreolus capreolus (from Pellerdy,
1955).
Fig?. 56-57. E. panda Supperer and Kutzer, 1961 from Capreolus capreolus
(from Supperer and Kutzer, 1961 j. X 1169. Fig. 56. Unsporulated oocyst.
Fig. 57. Sporulated oocyst.
Fig. 58. E. canna Trifntt, 1924 from Taurotracjus oryx (from Triffitt, 1924).
Plate 10
Fig. 59. E. macieli Yakimoff and Matchulski, 1938 from Kobus ellipsiprymnus
(from Yakimoff and Matchulski, 1938) .
Fig. 60. E. arkhari Yakimoff and Matschoulsky, 1937 from Oris rig net
(from Yakimoff and Matschoulsky, 1937a ) .
Fig. 61. E. trijfittae Yakimoff, 1934 emend, from Taurotragus oryx (from
Yakimoff, 1934).
Fig. 62. E. mccordocki Honess, 1941 from Odocoileus h. hemionus (from
Landram and Honess, 1955) .
Fig. 63. E. austriaca Supperer and Kutzer, 1961 from Cervus elaphus (from
Boch and Lucke, 1961). X 735.
Fig. 64. E. (?) polaris Yakimoff and Sokoloff, 1935 from Rangifer tarn ml us
(from Yakimoff, Sokoloff and Matschoulsky, 1936.) .
Figs. 65-66. E. bareillyi Gill, Chhabra and Fall, 1963 from Bubalm bubalis
(from Gill, Chhabra and Lall, 1963). Fig. 65. Unsporulated oocyst. Fig. 66.
Sporulated oocyst, X 1211.
20S
Plate 11
Fig. 67. E. yakimovi Rastegaieff, 1929 from Boselaphus tragocamelus (from
Rastegaieff , 1930) .
Fig. 68. E. thianethi Gwelessiany, 1935 from Bubalus bubalis (from Patnaik,
1965). X770.
Fig. 69. E. ovoidalis Ray and Mandal, 1961 from Bubalus bubalis (from
Patnaik, 1965 — cited as E. ivijomingensis) . X 770.
Fig. 70. E. gokaki Rao and Bhatavdekar, 1959 from Bubalus bubalis (from
Patnaik, 1965 — cited as E. brasiliensis) . X 770.
Figs. 71-76. E. zuernii (Rivolta, 1878) Martin, 1909 from Bos taurus. Fig. 71.
Oocyst (from Levine and Ivens, 1967). X 230S. Fig. 72. Same as Fig. 71.
Fig." 73. Oocyst (from Christensen, 1941). X 1154. Fig. 74. Oocyst (from
Nyberg and Hammond, 1965). X 2138. Fig. 75. Sporozoite (from Nyberg
and Hammond, 1965). X 2138. Fig. 76. Oocyst (from Joyner et al., 1966).
X 1389.
I'd! I
Plate 12
Figs. 77-81. E. bovis (Ziiblin, 1908) Fiebiger, 1912 from Bos taurus. Fig. 77.
Oocyst (from Levine and Ivens, 1967). X 2700. Fig. 78. Oocyst (from Joyner
et al., 1966). X 1625. Fig. 79. Oocyst (from Christensen, 1941). X 1350.
Fig. SO. Sporocyst (from Nyberg and Hammond, 1965). X 2500. Fig. 81.
Oocyst (from Nyberg and Hammond, 1965). X 2500.
210
Plate 13
Figs. S2-92. E. bovis (Ziiblm, 190S) Fiebiger, 1912 from Bos taurus (from
Hammond, Ernst and Goldman, 1965). Fig. 82. Fresh schizonts concentrated
in a petri dish. X 1.24. Fig. S3. Fresh schizonts. X 14. Fig. 84. Fresh
merozoite. Phase contrast. X 1432. Fig. 85. Fresh merozoite undergoing
flexion. Wrinkles in bent region (arrow). Phase contrast. X 1432. Fig. 86.
Merozoite, protargol preparation, showing nucleus (arrow) and cytoplasmic
granules. X 1910. Fig. 87. Merozoites, protargol preparation, showing an-
terior cap (upper arrow) and cytoplasmic granules including posterior granule
(lower arrow). X 1910. Fig. 88. Merozoite, protargol preparation, showing
anterior cap (top), cytoplasmic granules (center), nucleus (near bottom), and
posterior granule (arrow). Dark field. X 1910. Fig. 89. Merozoite, protargol
preparation, with continuous membrane over anterior end (arrow). Dark field.
X 1910. Fig. 90. Merozoite, protargol preparation showing longitudinal fibrils.
X 1910. Fig. dl. Merozoites, protargol preparation. One showing pore at
anterior end (arrow). X 1910. Fig. 92. Merozoite, protargol preparation,
showing median rodlike structure in anterior portion of body (arrow). X 1910.
211
85
83
v
i
86
87
§ %
% % #
•
*~f***
90 m **& 91 "\
92
212
Plate 14
Figs. 93-96. E. bovis (Ziiblin, 190S) Fiebiger, 1912 from Bos taunts (from
Hammond, 1964). Fig. 93. Section of villus with 2 nearly mature 1st genera-
tion schizonts, one showing the host cell nucleus (arrow) ; fixed in Zenker's
and stained with iron-hematoxylin. X 143. Fig. 94. Early 2nd generation
schizont fixed in Helly's and stained with iron-hematoxylin. X 1337. Fig. 95.
Intermediate 2nd generation schizont fixed in Helly's and stained with iron-
hematoxylin. X 1337. Fig. 96. Mature 1st generation schizont; fresh speci-
men. X 191.
213
Plate 15
Figs. 97-102. E. bovis (Ziiblin, 190S) Fiebiger, 1912 from Bos taunts (from
Hammond, 1964). Fig. 97. Mature 2nd generation sehizont containing mero-
zoites. X 1337. Fig. 98. Intermediate gamonts; microgametocyte (m) and
macrogamete (M). X 1337. Fig. 99. Second generation merozoite, fresh
specimen. X 23S8. Fig. 100. Two early gamonts in the same host cell. X 1337.
Fig. 101. Alicrogamete, fresh specimen, phase contrast. X 2S65. Fig. 102.
Oocysts and maturing gamonts with severe damage to the mucosa. X 2N7.
(Figs. 97, 98, 100 and 102 from preparations fixed in Helly's and stained with
iron-hematoxylin.)
214
Plate 16
Figs. 103-106. E. bovis (Ziiblin, 190S) Fiebiger, 1912 from Bos taunts. Fig.
103. Unsporulated oocyst (from Hammond, 1964). X 1067. Fig. 104. Sporu-
lated oocyst (from Hammond, 1964). X 1067. Fig. 105. Excysting oocyst
with a sporozoite escaping and other sporozoites still inside (from Hammond,
1964). X 1455. Fig. 106. Electron micrograph of section showing numerous
randomly oriented merozoites in host cell vacuole (from Sheffield and Ham-
mond, 1966). X 6305.
215
y
_ ®
A \
;**? -
! & H -
.;** * **:^ . . . ^
■*™ **| ,- * « f-1
■s ; " ? 9$3 vSjT *£• '- ^*k 1 SI'S
**»•..■*;
216
Plate 17
Figs. 107-108. Electron micrographs of E. bovis fZtiblin, 190S) Fiebiger, 1912
from Bos taurus (from Sheffield and Hammond, 1966). Fig. 107. Cross section
of several merozoites. Note rhoptries (paired organelle) and median rod
within the conoid, fibrils apparently attached to polar ring and the 2 mem-
branes (arrows) surrounding the cell. X 40,320. Fig. 10S. Longitudinal section
of 2 merozoites showing subpellicular fibrils in one and anterior vesicle in the
other. X 23,184.
C, conoid; F, fibril; P, polar ring; V, vesicle.
217
Plate IS
Figs. 109-110. Electron micrographs of E. bovis (Ziiblin, 190S) Fiebiger, 1912
from Bos taurus (from Sheffield and Hammond, 1966). Fig. 109. Anterior end
of a merozoite with a vesicle at the end of the rhoptries (paired organelle).
X 24,450. Fig. 110. Section of 2 conoids. Note the small circular profiles in
the lower conoid and the parallel striations in the upper conoid. X 24,450.
C, conoid; O, rhoptries; V, vesicle.
2 is
±2±
111
Plate 19
Figs. 111-112. Electron micrographs of E. bovis (Ziiblin, 190S) Fiebiger, 1912
from Bos taunts (from Sheffield and Hammond, 1966). Fig. 111. Longitudinal
section of the anterior end of a merozoite showing the median rod between the
necks of the rhoptries (paired organelle). X 72,600. Fig. 112. Section through
one member of the rhoptries. Note alveolar and dense portions of the club-
shaped part of the rhoptries. X 34,650.
C, conoid; IM, inner membrane; 0, rhoptries; OM, outer membrane; R,
median rod.
219
.$•** : s-
r:
•w '^6feC
Plate 20
Fig. 113. Electron micrograph of E. bovis (Ziiblin, 190S) Fiebiger, 1912 from
Bos taurus (from Sheffield and Hammond, 1966). Longitudinal section of
several merozoites showing the position of the cell components near the nu-
cleus. X 25,950.
ER, endoplasmic reticulum; G, Golgi zone; GL, glycogen body; L, lysosome;
M, mitochondrion; N, nucleus.
220
r*
5
Plate 26
Fig. 120. Electron micrograph of E. bovis (Ziiblin, 190S) Fiebiger, 1912 from
Bos taurus (from Hammond, Scholtyseck and Miner, 1967). Peripheral por-
tion of microgametocyte showing micropore. X 23,400.
G, glycogen granule; H, host cell; N, nucleus; MI, mitochondrion; MIP, mi-
cropore; MP, cell membrane of parasite.
226
• * .. * x»
^— MIH
«*"-<
«.
-. r X:-.*
Plate 27
Fig. 121. Electron micrograph of E. bovis (Ziiblin, 190S) Fiebiger, 1912 from
Bos taurus (from Hammond, Scholtyseck and Miner, 1967). Microgameto-
cyte; stage with nuclei completing division. X S5S0.
AH, adjacent host cell harboring macrogamete within vacuole (AV) ; MI,
mitochondrion; MIH, mitochondria of the host cell; MYE, external micro-
villi of the host cell; OR, osmiophilic ring adjacent to nuclear membrane.
227
Plate 2S
Fig. 122. Electron micrograph of £\ 6ouis (Ziiblin, 190S) Fiebigcr, 1912 from
Bos taurus (from Hammond, Scholtyseck and Miner, 1967). Microgameto-
cyte; older stage showing a close spatial relationship between parasite and
host cell. X 12,400.
MH, cytoplasmic membranes of the host cell; MIH, mitochondrion of the
host cell; MP, cell membrane of the parasite; N, nucleus; VE, different kinds
of vesicles.
228
Plate 29
Figs. 123-126. E. bovis (Ziiblin, 190S) Fiebiger, 1912 from Bos taurus. Fig.
123. Sporozoite showing location of glycogen granules. Based on PAS prepa-
rations (from Hammond, Chobotar and Ernst, 196S). X 3S00. Fig. 124.
Sporozoite, typical form, drawn from fresh specimens (from Hammond,
Chobotar and Ernst, 1968). X 3S00. Fig. 125. Nucleus of 1st generation
merozoite as seen in Feulgen preparation (from Hammond, Ernst and Gold-
man, 1965). X S000. Fig. 126. First generation merozoite showing distribu-
tion of glycogen granules as seen in PAS preparation (from Hammond, Ernst
and Goldman, 1965) . X 4000.
Fig. 127. Diagram of the ultrastructure of a young macrogamete of the genus
Eimeria (from Scholtyseck, Hammond and Ernst, 1966).
DB, dark bodies; ER, endoplasmic reticulum; G, glycogen granules; L, lipoid
inclusions; M, mitochondria; X, nucleus; NU, nucleolus; OM, osmiophilic
masses; P, pores in nuclear membrane; TL, longitudinal sections of micro-
tubules; TT, transverse sections of microtubules; V, small vesicles of the
endoplasmic reticulum; VER, large vesicles of the endoplasmic reticulum;
WB, wall-forming bodies.
Fig. 12S. Diagram of the ultrastructure of a young microgametocyte of the
genus Eimeria (from Hammond, Scholtyseck and Miner, 1967).
ER, endoplasmic reticulum; G, glycogen granule; L, lipid inclusion; MI,
mitochondrion; X, nucleus; XU, nucleolar substance; P, pore in nuclear
membrane; VE, different kinds of vesicles.
220
125
VER P OM
126
280
Plate 30
Figs. 129-131. E. canadensis Bruce, 1921 from Bos taunts. Fig. 129. Oocyst
(from Levine and Ivens, 1967). X 2592. Fig. 130. Oocyst (from Joyner et al.,
19(36). X 1560. Fig. 131. Oocyst (from Christensen, 1941). X 1296.
Figs. 132-134. E. ellipsoidaUs Becker and Frye, 1929 from Bos taurus. Fig.
132. Oocyst (from Christensen, 1941). X 1296. Fig. 133. Oocyst (from
Xyberg and Hammond, 1965). X 2400. Fig. 184. Sporocyst (from Xyberg
and Hammond, 1965). X 2400.
231
Plate 31
Figs. 135-137. E. ellipsoidalis Becker and Frye, 1929 from Bos taurus. Figs.
135 and 136. Oocysts (from Levine and Ivens, 1967). X 2700. Fig. 137.
Oocyst (from Joyner et aL, 1966). X 1625.
Figs. 138-140. E. cylindrica Wilson, 1931 from Bos taurus. Fig. 13S. Oocyst
(from Joyner et aL, 1966). X 1625. Fig. 139. Oocyst (from Christensen,
1941). X 1350. Fig. 140. Oocyst (from Levine and Ivens, 1967). X 27(H).
Plate 32
143
Figs. 141-143. E. auburnensis Christensen and Porter, 1939 from Bos taurus.
Fig. 141. Sporulated oocyst (from Levine and Ivens, 1967). X 2592. Fig. 142.
Oocyst with heavily mammillated wall with section removed to show struc-
ture of wall and portion of spherical sporont (from Christensen and Porter,
1939). X 1536. Fig. 143. Sporulated oocvst (from Christensen and Porter,
1939). X 1536.
23:
Plate 33
Figs. 144-147. E. auburnensis Christensen and Porter, 1939. Fig. 144. Specu-
lated oocyst from Bos taunts (from Nyberg and Hammond, 1965). X 2500.
Fig. 145. Sporulated oocyst from Bos taurus (from Joyncr et al., 19G6).
X 1620. Fig. 146. Sporozoite (from Nyberg and Hammond, 1965). X 2500.
Fig. 147. Sporulated oocyst from Bubalus bubalis (from Bhatia et al., 1968).
X 1500.
234
Plate 34
Figs. 148-154. Sporozoites of E. aiiburnensis Christensen and Porter, 1939
from Bos taurus (from Hammond, Chobotar and Ernst, 196S). X 3648. Fig.
148. Broadly lanceolate form. Fig. 149. Intermediate form with 2 anterior
refractile bodies. Fig. 150. Intermediate form with one anterior retractile
body. Fig. 151. Elongate form. Fig. 152. Fully flexed form showing dark
points or ridges at concave surface of bent portion. Fig. 153. Partially flexed
form also showing dark points or ridges. Fig. 154. Bluntly rounded form
showing a dark point or ridge at one side of anterior region.
All drawings made to scale from photographs of living specimens.
23.5
Plate 35
Figs. 155-160. E. auburnensis Christensen and Porter, 1939 from Bos taunts
(from Hammond, Clark and Miner, 1961). X 579. All figures are specimens
in sections of small intestine fixed in Zenker's fluid and stained with iron-
hematoxylin. Fig. 155. Early microgametocyte showing 3 nuclei with host cell
nucleus at top. Fig. 156. Early macrogamete with host cell nucleus at bottom.
Fig. 157. Early microgametocyte showing 10-15 nuclei with host cell nucleus
at top. Fig. 158. Intermediate microgametocyte showing 25-30 nuclei with
host cell nucleus at top. Fig. 159. Later microgametocyte showing arrange-
ment of nuclei at surface of spheres with host cell nucleus at upper right.
Fig. 160. Two later microgametocytes and 4 later macrogametes showing
granules arranged to outer wall.
236
Plate 36
Figs. 161-167. E. auburnensis Christensen and Porter, 1939 from Bos taurus
(from Hammond, Clark and Miner, 1961). Fig. 161. Three mierogametocytes,
the one at the top showing mierogametes arranged in whorls around residual
bodies, and the one in the center with mierogametes in random arrangement.
X 579. Figs. 162-165. Mierogametes each showing flagella. Fresh specimens,
phase contrast. X 1448. Fig. 166. Two oocysts in the lamina propria of a
villus. X 579. Fig. 167. An oocyst inside its host cell in smear of mucosa.
Fresh specimen. X 579.
Except where otherwise stated, all figures are of specimens in sections of small
intestine fixed in Zenker's fluid and stained with iron-hematoxvlin.
no'7
— /
4 '"
\ * 1
162
*3? *.'**
4$K?H
(
"\ i
1
At 7^# 166
* y 167
238
;
Plate 37
Fig. 16S. E. auburnensis Christensen and Porter, 1939 from Bos taunts (from
Scholtyseck 3 Hammond and Ernst, 1966). Electron micrograph of macro-
gamete within the host cell showing much electron-dense material in the
vacuole surrounding the parasite and many mitochondria in the adjacent host
cell cytoplasm. X 17,000.
DB, dark bodies; G, glycogen granules; H, host cell; HM, mitochondria;
HV, vacuole; TT, transverse sections of microtubules.
230
Plate 3S
Figs. 169-170. Electron micrographs of E. auburnensis Christensen and Porter,
1939 from Bos taunts (from Scholtyseck, Hammond and Ernst, 1966). X
33,000. Fig. 169. Macrogamete within the host cell showing microtubules in
longitudinal section at the surface of the macrogamete; these lie in the vacuole
surrounding the parasite. Fig. 170. The same as Fig. 169 but showing the
microtubules in cross section.
DB, dark bodies; G, glycogen granules; HV, vacuole; TL, longitudinal section
of microtubules; TT, transverse sections of microtubules.
240
Plate 39
Fig. 171. E. auburnensis Christensen and Porter, 1939 from Bos taiirus (from
Hammond, Scholtyseck and Miner, 1967). Electron micrograph showing loca-
tion of microgametocyte in host cell lying beneath the epithelial layer of a
villus. X4750.
H, host cell; LU, lumen of intestine; N, nucleus; NE, nucleus of epithelial
cell layer.
Fixation in OS0 4 , dehydration in acetone and embedding in Vestopal.
241
• - , . 9 *
3"
242
f
i
Plate 40
Fig. 172. E. auburnensis Christensen and Porter, 1939 from Bos taurus (from
Hammond, Scholtysesk and Miner, 1967). Electron micrograph of micro-
gametocyte in host cell. Stage similar to that of Figure 171 (Plate 39), show-
ing detail of area of contact between parasite and host cell. X 22,000.
H, host cell; MIV, mitochondrion of parasite in vacuole of host cell; MP, cell
membrane of parasite.
For preparation of tissue, see legend for Plate 39.
248
Plate 41
Fig. 173. E. auburnensis Christensen and Porter, 1939 from Bos taurus (from
Hammond, Scholtyseck and Miner, 1967). Electron micrograph of micro-
gametocyte in host cell, showing detail of furrows and flagella. X 12,000.
F, furrows; FL, flagella; H, host cell; L, lipid inclusion; MIV, mitochondrion
of parasite in process of being pinched off into vacuole of the host cell; MP,
cell membrane of the parasite; N, nucleus.
For preparation of tissue, see legend for Plate 39.
244
I I S
-
ml
. « -a-
•
Plate 42
Fig. 174. £\ auburnensis Christensen and Porter, 1939 from Bos taurus (from
Hammond, Scholtyseck and Miner, 1967). Electron micrograph of micro-
gametocyte in host cell. Interior portion of microgametocyte showing flagella
in spaces subdividing the protoplasm into small masses. X 17,000.
FL, flagella; N, nucleus; S, spaces.
For preparation of tissue, see legend for Plate 39.
245
Plate 43
Fig. 175. E. auburnensis Christensen and Porter, 1939 from Bos taunts (from
Hammond, Scholtyseck and Miner, 1967). Electron micrograph of micro-
gametocyte in host cell. An older stage showing relatively large spaces con-
taining flagella of microgametes. X 17,000.
FL, flagella; N, nucleus; S, spaces; VE, different kinds of vesicles.
For preparation of tissue, see legend for Plate 39.
246
Plate 44
Figs. 176-178. E. brasiliensis Torres and Ramos, 1939. Fig. 176. Sporulated
oocyst from Bos taurus (from Levine and Ivens, 1967). X 2552. Fig. 177.
Sporulated oocyst from Bubalus bubalis (from Bhatia et al., 196S). X 1370.
Fig. 17S. Sporulated oocyst from Bos taurus (from Joyner et al., 1966).
X 1531.
247
Plate 45
Figs. 179-180. E. brasiliensis Torres and Ramos, 1939 from Bos taunts. Fig.
179. Oocyst showing rough wall sloughing off (from Levinc and Ivens, 1967).
X 2592. Fig. ISO. Sporulatecl oocyst (from Supperer, 1952 — cited as E.
boehmi). X 1104.
Figs. 181-184. E. alabamensis Christensen, 1941. Fig. 181. Sporulatecl oocyst
from Bos taurus (from Joyner et al., 1966). X 1560. Fig. 182. Sporulated
oocyst from Bubalus bubalis (from Bhatia et al., 1968). X 1440. Fig. 183.
Unsporulated oocyst from Bos taunts (from Christensen, 1941). X 1296.
Fig. 1S4. Sporulated oocyst from Bos taunts (from Levinc and Ivens, 1967).
X 2592.
IMS
Plate 46
Fig. 1S5. E. bukidnonensis Tubangui, 1931 from Bos taunts (from Levine and
Ivens, 1967). X 2700.
Fig. 186-189. E. subspherica Christensen, 1941. Fig. 186. Sporulated oocyst
from Bos taurus (from Levine and Ivens, 1967). X 2700. Fig. 1S7. Sporu-
lated oocyst from Bos taurus (from Joyner et al., 1966). X 1625. Fig. 188.
Sporulated oocyst from Bubalus btibalis (from Bhatia et al., 1968). X 1500.
Fig. 189. Unsporulated oocyst from Bos taurus (from Christensen, 1941).
X 1350.
249
Plate 47
Figs. 190-193. E. bukidnonensis Tubangui, 1931. Fig. 190. Sporulated oocyst
from Bos taurus (from Joyner ct al., 196(3). X 1436. Fig. 191. Sporulated
oocyst from Bubalus bubalis (from Bhatia ct al., 196S). X 141S. Fig. 192.
Sporulated oocyst without outer wall (from Bhatia et al., 196S). X 1418.
Fig. 193. Sporulated oocyst from Bos indicus (from Tubangui, 1931 ). X 105S.
250
Plate 4S
Figs. 194-195. E. pellita Supperer, 1952 from Bos taurus. Fig. 194. Sporulated
oocyst (from Joyner et al., 1966). X 15S4. Fig. 195. Sporulated oocyst (from
Supperer, 1952)! X 1170.
Fig. 196. E. talboti Prasad and Narayan, 1963 from Alcelaphus cokei (from
Prasad and Narayan, 1963 ) . X 878.
Fig. 197. E. connochaetei n. sp. from Connochaetes gnu (from Prasad, 1960 —
cited as E. ellipsoidalis) . X 829.
Fig. 198. E. Wyoming ensis Huizinga and Winger, 1942 from Bos taurus (from
Levine and Ivens, 1967). X 2633.
251
Plate 49
Figs. 199-200. E. Wyoming ensis Huizinga and Winger, 1942. Fig. 199. Specu-
lated oocyst from Bos taurus (from Joyner et al., 1966). X 1620. Fig. 200.
Sporulated oocyst from Bubalus bubalis (from Bhatia et al., 1968). X 1 500.
Fig. 201. E. illinoisensis Levinc and Ivens, 1967 from Bos taurus (from Levine
andlvens, 1967). X 2700.
Fig. 202. E. bareillyi Gill, Chhabra and Fall, 1963 from Bubalus bubalis (from
Bhatia et al., 1968). X 1500.
Plate 50
Fig. 203. E. gorgonis Prasad, 1960 from Gorgon taurinus (from Prasad, 1960).
X 1900.
Fig. 204. E. walleri Prasad, 1960 from Litocranius walleri (from Prasad, 1960).
X850.
Figs. 205-206. E. impalae Prasad and Xarayan, 1963 from Aepyceros melam-
pus. Fig. 205. Sporulated oocyst (from Prasad and Narayan, 1963). X 900.
Fig. 206. Sporulated oocyst (from Bigalke, 1964). X 1430.
Fig. 207. E. elegans Yakimoff, Gousseff and Rastegaieff, 1932 from Gazella
subgutturosa (from Yakimoff, Gousseff and Rastegaieff, 1932b).
Fig. 208. E. saiga Svanbaev, 195S from Saiga tatarica (from Svanbaev, 195S).
X800.
Fig. 209. E. rupicaprae Galli-Valerio, 1924 from Rupicapra rupicapra (from
Yakimoff and Matschoulsky, 1940).
Figs. 210-211. E. riedmuelleri Yakimoff and Matschoulsky, 1940 emend, from
Rupicapra rupicapra (from Yakimoff and Matschoulsky, 1940).
Fig. 212. E. yakimoffmatschoulskyi Supperer and Kutzer, 1961 emend, from
Rupicapra rupicapra (from Supperer and Kutzer, 1961). X 1230.
>54
Plate 51
Fig. 213. E. ernsti Todd and O'Gara, 196S from Oreamnos americanus (from
Todd and O'Gara, 1968). X 2S00.
Fig. 214. E. montanaensis Todd and O'Gara, 196S from Oreamnos americanus
(from Todd and O'Gara, 196S). X 4200.
Plate 52
Fig. 215. E. suppereri Kutzer, 1964 from Rupicapra rupicapra (from Kutzcr,
1964). X 1166.
Fig. 216. E. oreamni Shah and Levine, 1964 from Oreamnos americanus (from
Shah and Levine, 1964). X 2405.
Fig. 217. E. alpina Supperer and Kutzer, 1961 from Rupicapra rupicapra
(from Supperer and Kutzer, 1961 ). X 1156.
Figs. 218-221. E. arloingi (Marotel, 1905) Martin, 1909 from Capra hircus.
Fig. 21S. Sporulated oocyst (from Chevalier, 1966). X 64S. Fig. 219. Sporu-
lated oocyst (from Levine, Ivens and Fritz, 1962). X 2405. Fig. 220. Sporu-
lated oocyst (from Chevalier, 1966 — cited as E. ahsata). X 64S. Fig. 221.
Sporulated oocyst (from Chevalier, 1966 — cited as E. crandallis). X 64S.
256
<*r' J \
t. if
*r SCH
• • ... iJi^T? %--^ . r w v M «
* i • . * %. • ' « * ,*- • • «.. *N
kazachstanica. See Eimeria eameli
khurodensis, 42, 76
khurodensis. See also Eimeria au-
burnensis
lamae. 12, 165,201
longispora, 93
macieli. 78, 175, 207
madisonensis, 27, 16S, 267
maroteli. 105
mayeri, 29, 168, 204
mccordocki, 25, 168, 207, 267
media var. honessi. See Eimeria
honessi
montanaensis, 95, 178, 254
muehlensi, 29, 35, 168,204
mundaragi, 76, 77, 174
nachitschevanica, 145
/mnfl. See Eimeria parva
necatriz, 99
ninae kohl-jakimov . See Eimeria
sp. (in Gazella subgutturosa)
ninae-kohl-yakimovi. See also E7-
wiena spp. (in Capreolus ca-
preolus) ; Eimeria spp. (in Cervus
elaphus); Eimeria spp. (in Dama
dama) ; Eimeria spp. (in G'a-
2e//a subgutturosa) ; Eimeria spp.
(m Hupicapra rupicapra)
ninakohlyakimovae, 14, 37, 86, 93,
99, 127, 132, 135, 145, 146, 148,
178, 188, 189, 258, 269
nina-kohl-yakimovi. See Eimeria
ninakohlyakimovae
noelleri. See Eimeria eameli
? nolleri. See Eimeria bactriani
odocoilei, 25, 168, 203, 267
oreamni, 93, 178,255
orlovi. See Eimeria brasiliensis
ovina, 99, 113, 123, 124, 129, 146,
148, ISO, 192, 193,261,269
ovoidalis. 43, 172, 187, 20S
oweni, 23
paMY/a, 113, 115, 120, ISO, 192, 260,
269
panda, 35, 169, 204, 206
pa/7s), 129, 181, 260.
See Eimeria gonzalezl
sp. (in Rangifer tarandus). See
Eimeria mayerl
sp. (in 8;'/va hortulorum) , 24, 167
(?) sp. (in Axis axis), 15
spp. (in Capreolus capreolus), 36,
169
spp. (in Cervus elaphus), 22
spp. (in Dama dama), 14, 167
spp. (in Gazella subgutturosa) , 86,
176
spp. (in Ruplcapra rupicapra) , 92,
178
spp. (in Saioa tatarlca), 177
Gastrocustls gllruthl. See Eimeria
gilruthi
Gazella d ore as, 270
Gazella subgutturosa, 85, 86, 87, 90,
102, 134, 176, 189, 190, 191, 193,
252
Gimffidae (Family), 183, 185
Giraffinae (Subfamily), 183
Globldlum cam ell. See Eimeria camell
"Globldium" camell, 10, 270
? Globldlum fuslformes. See Eimeria
bo vis
Globldium gllruthl. See Eimeria gil-
ruthi
Gorgon taurlnus, 81, 175, 252
Hemltragus jemlahicus, 99
Hippotraginae (Subfamily), 78, 79,
175, 184, 185
Hippotragini (Tribe), 184
Hydropotini (Tribe), 183
Isospora, 1, 17, 136, 143, 147, 182
aksalca, 138, 182
capreoli. 137, 182, 262
lacazel, 139, 140
orlovl, 136, 182, 262
rangiferis, 137, 182, 264
sp. (in Bos taurus; Bos taurus-B.
indicus), 139, 182,263
sp. (in Ovis arles), 140, 182, 263
sp. (in Rangifer tarandus). See
Isospora rangiferis
? sp. (in Bos Indicus). See Isospora
sp. (in Bos taurus; Bos taurus-B.
indicus)
Kobus elllpslpripnnus, 78, 175, 207
Lama glama, 11, 165, 202
Lama 'pacos, 11, 12, 13, 165, 201
Litocranius wallerl, 85, 176, 252
Moschinae (Subfamily), 183, 185
Muntiacinae (Subfamily), 1S3, 185
Muntiacus, 144
Neotragini (Tribe), 184
Odoeoileinae (Subfamily), 24, 28, 31,
168, 183, 185
Odocoileini (Tribe), 24, 183
Odocoileus //. hem/onus, 25, 26, 16S,
203, 207, 26S
27S
THE COCCTDIAN PARASITES OF RUMINANTS
Odocoileus virginianus, 26, 27, 168,
2(37
Oreamnos americanus, 94, 95, 178,
254, 255
Orias carina. See Taurotragus oryx
Ori/ctolagus ciniiculus, 1S7, 193
Ovibovini (Tribe), 184
Oris, 1, 102, 107, 114, 135, 146, 148
amnion. 99, 101, 110, 114, 126, 134,
178, 179, ISO, 188, 1S9, 190, 191,
192, 11)3
amnion polo, 107, 135
annnon sewerzewi, 107, 135
aries. 99, 101, 107, 110, 114, 118,
120, 121, 122, 124, 126, 129, 131,
134, 140, 144, 148, 17S, 179, 180,
181,182, ISO, 1S7, 188, 189, 190,
191, 192, 193, 258, 259, 260, 261,
262, 263, 264, 26S, 269
canadensis, 99, 101, 107, 110, 114,
120, 125, 126, 131, 132, 134, 178,
179, 180, 1S1
musimon, 99, 101, 107, 110, 114,
126, 131, 134, 178, 179, ISO, 181
nahura. See Pseudois nahoor
orientalis, 107, 114, 179
tragelaphus. See Ammotragus lervia
vignei, 135, 207
"vignei s. o. arkhar." See Ovis
vignei
Palaeotragimie (Subfamily), 183
Portax pixtus. See Boselaphus trago-
camelus
Pseudoaxis diibovskyi. See Sika hor-
tulorum
hortidorum. See Sika hortnlorum
Pseudois nahoor. 118, ISO
Rangifer, 144
tarandus, 28, 29, 30, 31, 137, 168,
169, 182, 203, 204, 207, 264
Rangiferini (Tribe), 28, 168, 183
Reduneini (Tribe), 78, 175, 184
Ruminantia (Suborder), 3, 13, 24, 28,
31, 37, 38, 40, 78, 79, 81, 87, 88, 95
Rupicapra rupicapra, 89, 90, 91, 92,
93, 99, 102, 107, 114, 134, 145, 177,
178, 186, 252, 255, 264, 270, 271
Rupicaprini (Tribe), 88, 177, 184
Rasa. 144
Saiga tartarica. 85, 87, 88, 102, 176,
177, 186, 187, 188, 189, 190, 191,
192, 193, 252
Saigini (Tribe), 87, 177, 184
Sika, 24
hortulorum, 15, 24
Strepsicerotini (Tribe), 38, 171, 1S4
Sus scrofa. 187
Taurotragus oryx, 39, 171, 193, 206,
207
Tragulidae (Family), 183, 1S5
Tragulus, 144
Tylopoda (Superfamily), 3, 165
Wenyonella, 141, 143, 147, 182
markovi, 141, 182, 263
A Note on the Author
Norman D. Levine is professor of veterinary parasitology, veterinary
research, and zoology, and director of the Center for Human Ecology
at the University of Illinois. He received his B.S. from Iowa State Uni-
versity in 1933 and his Ph.D. from the University of California at
Berkeley in 1937. He has served as president of the Society of Proto-
zoologists (1959-60), president of the American Society of Professional
Biologists (1967-69) , president of the Illinois State Academy of Science
(1966-67), president of the American Microscopical Society (1968-69)
and chairman of the Tropical Medicine and Parasitology study section
of the National Institutes of Health (1965-69). He has been editor of
the Journal of Protozoology since 1966. His numerous publications
include Protozoan Parasites of Domestic Animals and of Man ( 1961 ) ,
Preventive Medicine in World War II, Volume VI (co-author with
twelve others, 1963), Malaria in the Interior Valley of North America:
A Facsimile Selection from Daniel Drake's (1850) Book (1965). The
Coccidian Parasites (Protozoa, Sporozoa) of Rodents (with Virginia
Ivens, 1965), Natural Nidality of Transmissible Diseases with Special
Reference to the Landscape Epidemiology of Zooanthroponoses, by E.
N. Pavslovsky, translated by F. K. Pious, Jr. (editor, 1966) and
Nematode Parasites of Domestic Animals and of Man ( 1968) .
A 1950 graduate of the University of Illinois, Virginia Ivens is instruc-
tor at the College of Veterinary Medicine at the university. She has
co-authored numerous articles in scientific journals and has translated
several articles from Russian. She co-authored with Norman D. Levine
The Coccidian Parasites (Protozoa, Sporozoa) of Rodents (1965).
UNIVERSITY OF ILLINOIS PRESS
252 (