FEMS Microbiology Letters, 363, 2016, fnw028
doi: 10.1093/femsle/fnw028
Advance Access Publication Date: 5 February 2016
Research Letter
R E S E A R C H L E T T E R – Taxonomy & Systematics
Rumen ciliate protozoa of domestic sheep (Ovis aries)
and goat (Capra aegagrus hircus) in Kyrgyzstan
Gözde Gürelli1,∗ , Savaş Canbulat2 , Nurbek Aldayarov3 and Burk A. Dehority4
1
Biology Department, Faculty of Sciences and Arts, Kastamonu University, Kuzeykent/Kastamonu 37150,
Turkey, 2 Department of Environmental Engineering, Faculty of Engineering and Architecture, Kastamonu
University, Kuzeykent/Kastamonu 37150, Turkey, 3 Department of Biology, Faculty of Science,
Kyrgyzstan-Turkey Manas University, Bishkek 720042, Kyrgyzstan and 4 Department of Animal Sciences, Ohio
Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691, USA
∗
Corresponding author: Biology Department, Faculty of Sciences and Arts, Kastamonu University, Kuzeykent/Kastamonu 37150, Turkey.
Tel: +903662801906; Fax: +903662154969; E-mail: [email protected]
One sentence summary: The study is on rumen protozoa fauna of sheep and goat living in Kyrgyzstan.
Editor: Aharon Oren
ABSTRACT
Species composition and concentration of rumen ciliate protozoa were investigated in the rumen contents of 14 domestic
sheep and 1 goat living in Bishkek, Kyrgyzstan. This is the first report on rumen ciliates from ruminants living in
Kyrgyzstan. In sheep 12 genera, 28 species and 12 morphotypes were detected, whereas in goat 8 genera, 12 species and
4 morphotypes were detected. The density of ciliates in sheep was (28.1 ± 20.0) × 104 cells mL−1 and in goat was 37.0 × 104
cells mL−1 . Dasytricha ruminantium, Isotricha prostoma, Entodinium simulans and Ophryoscolex caudatus were major species
(100%) in sheep, and for the first time, Diplodinium rangiferi was detected in a domestic goat.
Keywords: Ciliate; protozoa; rumen; goat; sheep; Kyrgyzstan
INTRODUCTION
The microbial populations in the rumen consist mainly of bacteria, protozoa and fungi that involved in the digestion of feed in
the rumen. Ciliate protozoa are one of the normal microorganisms that are found in the rumen of both domestic and wild ruminants (Akbar et al. 2009). These ciliates were first observed by
Gruby and Delafond (1843) and their appearance was assumed
to be of importance in the metabolism and nutrition of the host
(Williams and Coleman 1992). Several factors seem to influence
the concentration and composition of the ciliate protozoa in the
rumen. These include the type and amount of feed consumed,
pH, turnover rate and frequency of feeding (Dehority 1978;
Franzolin and Dehority 1996). The studies on rumen ciliate composition of various domestic ruminants worldwide and the comparison of these results with those of domestic ruminants seem
to offer useful information on the relationship among the rumen
ciliates and also between the rumen ciliates and their ruminant
hosts (Ito, Imai and Ogimoto 1994; Selim et al. 1999).
Kyrgyzstan, in terms of biodiversity, is one of the richest
countries in Central Asia and there have been no studies on
the rumen ciliates of the ruminants living there. Therefore, the
aim of this study was to identify the rumen ciliates in domestic sheep (Ovis aries) and goat (Capra aegagrus hircus) living in
Bishkek, Kyrgyzstan and to compare these data with results
from other studies in different geographical locations.
MATERIALS AND METHODS
Samples of rumen contents were obtained from 14 domestic
sheep (O. aries) and one domestic goat (C. aegagrus hircus) at a
Received: 6 December 2015; Accepted: 2 February 2016
C FEMS 2016. All rights reserved. For permissions, please e-mail: [email protected]
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FEMS Microbiology Letters, 2016, Vol. 363, No. 6
slaughterhouse near Bishkek, Kyrgyzstan from March 2014 to
May 2014. The domestic sheep were 2–3 years old and the domestic goat was 2 years old. The altitude of the sheep and goat
lived was 1000–1500 m. The predominant vegetation of this altitude was mountain steppe. The mountain steppe was composed of meadows and mixed-grass steppes were characterized
by sod grass, forb species and steppe shrubs. Sheep were fed on
meadows and mixed-grass steppes and goat was fed on steppe
shrubs before slaughter. The rumen was cut open with a knife
and a sample was obtained by inserting a ladle into the rumen.
A well-mixed sample of the ruminal content was immediately
fixed with an equal volume of 18.5% formalin (Dehority 1984)
and an aliquot of each sample was stained and stored in methyl
green formalin saline (MFS) solution for total and differential
counts (Ogimoto and Imai 1981; Gürelli 2014b). MFS was used as
a nuclear stain, and Lugol’s iodine was used to indicate skeletal
plates (Gürelli and Ito 2014).
Ciliate densities were calculated with a Neubauer hemocytometer counting chamber. The Neubauer hemocytometer
counting chamber has slender grooves cut at regular intervals.
The number of cells per 1 ml of rumen contents can be calculated by the following Formula: N = 10/4 × a × d (N: number of
ciliates per 1 ml of rumen contents, a: number of ciliates in four
divisions on the Neubauer hemocytometer, d: sample dilution).
Differential counts of species were estimated from smear slides
with a total of 200–800 cells identified for each species (Gürelli
2014b).
A total of 25 cells measurements were made and specimens
were examined with a Zeiss microscope and imaging system.
Drawings were based on photomicrographs and observations of
the cells stained with MFS and Lugol’s iodine.
The identification and classification of species was based on
descriptions from studies by Dogiel (1927), Ogimoto and Imai
(1981), Öktem, Göçmen and Torun (1997) and Lynn (2008).
RESULTS
The mean number (±SD) of ciliates in the rumen contents from
14 domestic sheep and 1 goat living in Kyrgyzstan were (28.1
± 20.0) × 104 cells per mL (SE = 18.6) and 37.0 × 104 cells per
mL. Individual densities ranged from 9.5 × 104 to 88.5 × 104 for
domestic sheep. In sheep, 12 genera, 28 species and 12 morphotypes were identified, whereas in a single goat, 8 genera,
12 species and 4 morphotypes were detected. Dasytricha ruminantium, Isotricha prostoma, Entodinium simulans and Ophryoscolex
caudatus were observed in all sheep (100%), whereas E. ellipsoideum, Eudiplodinium maggii, Ostracodinium trivesiculatum and O.
gracile were detected only in one sheep (7.1%) (Table 1). For individual sheep, the total number of species ranged from 10.0 to
20.0 with an average of 14.2 ± 3.3.
Diplodinium rangiferi was detected for the first time in a domestic goat (Figs 1 and 2). Dimensions of D. rangiferi are given in
Table 2.
DISCUSSION
In the present study, 28 species and 12 morphotypes, belonging to 12 genera were found in sheep and 12 species and 4 morphotypes belonging to 8 genera were found in a single goat. Although, this is the first report on rumen ciliates of sheep and a
goat living in Kyrgyzstan, no new species were detected. Interestingly, D. rangiferi (Dogiel 1925) was found in the rumen of a
domestic goat in Kyrgyzstan, but the length and width of these
D. rangiferi specimens are smaller than that of D. rangiferi from
reindeer, red deer, sika deer, giraffe, calf and cattle. The width
of D. rangiferi was narrower than that of other specimens from
the different hosts (Table 2). Differences in width could be a result of the feeding habits of the host animal, the host species,
geographical variations or any combination of these factors
(Dehority 1974; Gürelli 2012, 2014a). Differences in width could
be a result of the interactions between ciliate species too. Differences also existed in the macronucleus shape within D. rangiferi.
For example, we observed an indent near the anterior end of the
macronucleus (Figs 1 and 2). No other researchers (Dogiel 1925;
Dehority 1997; Imai et al. 2002) observed this indent.
Diplodinium rangiferi was first detected from reindeer in Russia (Dogiel 1925). However, this ciliate species is not hostspecific, it is more common in cervid animals. Imai et al. (2002)
were able to successfully establish D. rangiferi in the rumen of
unfaunated calves by inoculation with sika deer rumen contents. If cervid animals and domestic goats are living in the same
place, this species could easily pass in the rumen of goat.
This species with caudal spines was first identified in Australian red deer by Dehority (1997). Imai et al. (2002) observed D.
rangiferi with distinctive caudal spines in the calves 2–3 weeks
after inoculation, and Gürelli (2014a) observed specimens of D.
rangiferi both with and without caudal spines in Turkish cattle.
In the present study, D. rangiferi did not have caudal spines. This
could be no predator species in the rumen.
When compared with ciliate surveys from other sheep living in various countries, the average ciliate density in rumen
contents of domestic sheep living in Kyrgyzstan (28.1 ± 20.0
× 104 cells mL−1 ) was less than that of sheep in Egypt (Selim
et al. 1996), sheep in Turkey (Öktem, Göçmen and Torun 1997),
sheep in Libya (Selim et al. 1999) and sheep in Northern Cyprus
(Göçmen and Gürelli 2009a). However, the average ciliate density
was the same as sheep in Egypt (Baraka 2012), and higher than
sheep in Canada (Imai et al. 1989) (Table 3).
The number of ciliate genera in sheep living in Kyrgyzstan,
was higher than from other locations from the world, but total
ciliate species was less from sheep in Turkey (Öktem, Göçmen
and Torun 1997; Göçmen, Torun and Öktem 1999) and Northern
Cyprus (Göçmen et al. 2001; Göçmen and Gürelli 2009a,b) and
higher from sheep in Canada (Imai et al. 1989), Egypt (Selim et al.
1996; Baraka 2012) and Libya (Selim et al. 1999) (Table 3).
When compared with ciliate surveys from other goats living
in various countries, the average ciliate density in the rumen
content of the domestic goat living in Kyrgyzstan (37.0 × 104
cells mL−1 ) was less than that of goats in Japan (Ito et al. 1995)
and in Turkey (Gürelli 2014b), and higher than goats in Nepal
(Gurung et al. 2002), Turkey (Göçmen et al. 2005) and Egypt
(Baraka 2012) (Table 4).
The number of rumen ciliate genera in the goat from the
present study was higher than goats from Japan (Ito et al. 1995),
Egypt (Baraka 2012) and Turkey (Gürelli 2014b), but less than
goats from Turkey (Göçmen et al. 2005), and the same in goats
in Nepal (Gurung et al. 2002). Total ciliate species was less than
goats in Turkey (Göçmen et al. 2005; Gürelli 2014b), Nepal (Gurung et al. 2002) and Egypt (Baraka 2012) and higher in goats from
Japan (Ito et al. 1995) (Table 4). These differences may be the differences the kinds and amounts of food taken, host animals or
geographical location, or a combination of these factors (Imai
et al. 1989; Ito and Imai 1990; Gürelli 2014b). Another possibility
may be the sampling (n = 1).
The rumen ciliate composition of all 14 sheep was composed
of D. ruminantium, I. prostoma, E. simulans and O. caudatus (100%).
In one goat, the dominant species were Epidinium ecaudatum
Gürelli et al.
3
Table 1. Frequency of appearance and percentage composition of rumen ciliates of sheep and a goat living in Kyrgyzstan.
Sheep
Genus, Species, Morphotype
Charonina
ventriculi
Dasytricha
ruminantium
Diplodinium
anisacanthum
m. anisacanthum
dentatum
flabellum
m. aspinatum
m. monospinatum
rangiferi
Enoploplastron
triloricatum
Entodinium
bursa
dubardi
ellipsoideum
exiguum
longinucleatum
minimum
nanellum
ovinum
rostratum
simulans
m. dubardi
m. lobosospinosum
m. caudatum
semehatae
Epidinium
ecaudatum
m. ecaudatum
m. caudatum
m. parvicaudatum
Eudiplodinium
dilobum
maggii
Isotricha
intestinalis Stein
prostoma
Metadinium
affine
tauricum
Ostracodinium
trivesiculatum
gracile
quadrivesiculatum
Ophryoscolex
caudatus
m. bicoronatus
m. tricoronatus
m. quadricoronatus
Polyplastron
multivesiculatum
Goat
Frequency
appearance (%)
Percentage
composition (%)
Frequency
appearance (%)
Percentage
composition (%)
21.4
21.4
100
100
21.4
14.3
14.3
21.4
14.3
14.3
7.1
–
85.7
85.7
100
71.4
14.3
7.1
35.7
71.4
85.7
92.9
85.7
21.4
100
7.1
78.6
100
21.4
28.6
28.6
–
–
28.6
28.6
21.4
7.1
100
78.6
100
71.4
71.4
35.7
14.3
7.1
7.1
–
100
100
7.1
50
35.7
78.6
78.6
0.4 ± 0.9 (0–2.6)
0.4 ± 0.9 (0–2.6)
5.2 ± 1.8 (2.5–9.2)
5.2 ± 1.8 (2.5–9.2)
1.2 ± 2.4 (0–7.3)
0.2 ± 0.4 (0–1.6)
0.2 ± 0.4 (0–1.6)
0.7 ± 1.5 (0–4.3)
0.3 ± 0.9 (0–3.3)
0.3 ± 0.9 (0–3.3)
0.1 ± 0.3 (0–1.2)
–
8.2 ± 4.8 (0–16.4)
8.2 ± 4.8 (0–16.4)
55.5 ± 12.3 (34.7–69.6)
3.8 ± 3.2 (0–9.6)
0.6 ± 1.5 (0–4.7)
0.6 ± 2.2 (0–8.1)
3.5 ± 4.9 (0–11.3)
5.7 ± 4.1 (0–11.6)
5.5 ± 3.3 (0–11.4)
8.9 ± 5.1 (0–21.1)
11.0 ± 5.9 (0–18.7)
1.4 ± 2.9 (0–8.5)
11.4 ± 5.4 (2.4–23.1)
0.4 ± 1.5 (0–5.8)
3.6 ± 2.6 (0–7.9)
8.3 ± 3.0 (3.4–15.9)
0.5 ± 1.1 (0–3.7)
0.7 ± 1.4 (0–4.4)
0.7 ± 1.4 (0–4.4)
–
–
0.7 ± 1.4 (0–4.4)
2.2 ± 3.3 (0–8.7)
1.2 ± 2.3 (0–6.3)
1.2 ± 0.7 (0–2.5)
8.8 ± 3.3 (3.6–14.3)
3.3 ± 2.3 (0–7.0)
5.1 ± 2.6 (0.7–10.6)
4.6 ± 3.9 (0–13.2)
4.1 ± 3.7 (0–13.2)
0.5 ± 0.8 (0–2.5)
0.2 ± 0.6 (0–2.0)
0.1 ± 0.5 (0–2.0)
0.1 ± 0.2 (0–0.8)
–
6.2 ± 3.8 (1.2–14.2)
6.2 ± 3.8 (1.2–14.2)
0.1 ± 0.4 (0–1.7)
3.7 ± 4.9 (0–14.2)
1.9 ± 3.0 (0–9.6)
4.1 ± 4.1 (0–14.5)
4.1 ± 4.1 (0–14.5)
–
–
100
100
100
–
–
–
–
–
–
100
–
–
100
100
–
–
–
100
100
100
–
–
100
–
100
100
–
100
100
100
100
–
100
–
100
100
–
100
100
–
100
100
–
–
100
–
–
–
–
–
–
–
–
–
3.88
3.88
10.6
–
–
–
–
–
–
10.6
–
–
48.6
3.02
–
–
–
5.6
6.91
12.31
–
–
15.1
–
5.0
10.2
–
22.0
22.0
5.6
16.4
–
7.8
–
7.8
3.23
–
3.23
0.6
–
0.6
10.6
–
–
10.6
–
–
–
–
–
–
–
Total genera, species and morphotypes number in sheep: 12, 28, 12
Total genera, species and morphotypes number in goat: 8, 12, 4
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FEMS Microbiology Letters, 2016, Vol. 363, No. 6
Figure 1. Outlines of the nuclear apparatus of D. rangiferi, observed from the left sides (a, b, c, d, e, f).
Table 2. Comparison of D. rangiferi dimensions from different hosts in various locations (a Mean, b SD, c Range not reported).
References
Dogiel (1925)
Sládeček (1946)
Lubinsky (1958)
Westerling (1970)
Kleyhans and Van Hoven (1976)
Imai et al. (1993)
Dehority(1997)
Imai et al. (2002)
Gürelli (2014b)
Present study
Host
Country
Length
Width
L/W
Reindeer
Red deer
Reindeer
Reindeer
Giraffe
Sika deer
Red deer
Calve
Cattle
Goat
Russia
Czechoslovakia
Canada
Finland
South Africa
Japan
Australia
Japan
Turkey
Kyrgyzstan
166b (128–210)
a,b
(77–142)
a,b
(147–258)
196.0b,c
171.6 b (154.1–190)
110.2 ± 15.6 (80–150)
115 ± 17.6 (80–167)
106.1 ± 10.4 (95–130)
113.8 ± 9.4 (91.7–118.8)
104.0 ± 7.4 (93.7–120.4)
136b (110–165)
a,b
(58–110)
a,b
(113–204)
157.5b,c
102.6 b (87.7–116.5)
74.7 ± 7.5 (65–0)
85.3 ± 11.5 (65–122)
89.8 ± 18.8 (65–80)
78.2 ± 7.6 (66.4–97.6)
64.7 ± 4.7 (55.3–74.1)
1.2b
1.3b
1.1–1.5b
1. 2b
1.7b
1.5 ± 2.1
1.4 ± 0.1
1.5 ± 0.1
1.5 ± 0.1
1.6 ± 0.1
(22%) and E. simulans (15%). The ratio of species is affected by the
diet of the host (Hungate 1966).
Entodinium semehatae was first detected from sheep living in
the vicinity of Izmir, Turkey (Öktem, Göçmen and Torun 1997),
and later, the same species was observed from goats living in
the same area (Gürelli 2014b). Until the present study, there was
no record of E. semehatae from other locations of the world.
In a number of previous investigations, rumen ciliate populations have been divided into four main types: A, B, K and
O (Eadie 1957, 1962; Imai, Katsuno and Ogimoto 1978, 1979;
Ogimoto and Imai 1981; Williams and Coleman 1992; Göçmen
et al. 2001; Gürelli 2014b). Four groups have the genera Isotricha,
Dasytricha and Entodinium. However, Type A population is designated including Polyplastron multivesiculatum and usually, but
not always, Metadinium affine. Type B population has Epidinium
sp., E. maggii, or both. Type K populations are observed in cattle populations specifically including Elytroplastron bubali. Type
O populations contain only Isotricha, Dasytricha and Entodinium,
because of the predatory activity of P. multivesiculatum, Type B
population, containing Epidinium and Eudiplodinium, can not be
maintained in a host with the type A because P. multivesiculatum can eliminate Epidinium sp. and E. maggii. In sheep living in
Kyrgyzstan Type A population was dominant. However, P. multivesiculatum and E. ecaudatum m. parvicaudatum were found in
two sheep (sheep 6 and 11). Additionally, in sheep 6, P. multivesculatum was also with E. maggii. Since Epidium ecaudatum can have
caudal spines, protecting it from predators, this may help to explain was it could exist with P. multivesiculatum. Moreover, the
presence of E. caudatum, E. maggii or P. multivesiculatum in the
same sheep indicates this animals was recently cross-infected
by other sheep, since rumen ciliates are orally transmitted
(Hungate 1966; Ogimoto and Imai 1981). Goat sample has Type B
population.
Eadie (1967) also reported that it was not possible to establish Epidinium and Ophryoscolex in the same animal, but in the
present study we observed them in the same sheep. Since domestic ruminants can live in the same area, they have many opportunities for cross-infection to each other.
In sheep and goat living in Kyrgyzstan, the density of E. simulans morphotypes with caudal spines were higher than that
of the morphotype without caudal spines. It may be the feeding habits of animals or that the caudal spines protect against
engulfment by larger predatory ciliates such as E. bursa, and P.
multivesiculatum (Coleman 1980). According to Lubinsky (1957),
Gürelli et al.
5
Figure 2. Photomicrographs of D rangiferi, fixed and stained with MFS and Lugol’s iodine, observed from the right sides (a, b, c, d).
ciliates with well-developed caudal spines are prevalent when
the food is rich in starch.
Sheep and goats are intermediate feeders (or opportunistic feeders). Sheep are grazers, while goats are more browsers
(Burritt and Frost 2006; Cannas and Pulina 2008). Goat eats concentrate selection such as tree sprouts and leaves (Ito et al. 1995;
Gurung et al. 2002; Cannas and Pulina 2008), whereas sheep consume mostly grass dominated diets and herbaceous flowering
plants, also called forbs (Burritt and Frost 2006). Dietary sources
of sheep living in Kyrgyzstan meadows and mixed-grass steppes
including sod grasses and forb species, and goat dietary source
was steppe shrubs. In goats and sheep, the density of Entodinium
spp. are high. When the host is fed a concentrate-rich ration, Entodinium spp. rapidly grow and the ratio of Entodinium spp. and
the total ciliate density become higher (Hungate 1966). Additionally, species belonging to the genus Entodinium are normally predominant in the rumen and have a wide distribution in almost
all ruminants, worldwide (Imai 1998). According to Ito, Imai and
Ogimoto (1993), the rumen of intermediate-type feeders may
have environmental factors more advantageous for the growth
of Entodinium spp. than those of the browser or grazer.
In goat and sheep, Epidinium, Eudiplodinium, Ostracodinium,
Diplodinium, Metadinium were observed. These ciliates have been
considered to possess cellulolytic activity and ingest many fragments of plants (Hungate 1966; Imai 1988). Ophryoscolex is predominant in sheep living in Kyrgyzstan. Such ciliate species,
Eudiplodinium, Ostracodinium, Diplodinium, Epidinium, Metadinium,
Ophryoscolex would be favorable for host animals fed mainly
fresh and dried grass with low nutritive value (Rong et al. 2000).
In conclusion, the genetics and physiology of the host animal, its diet, transfaunation and antagonism among ciliate
species, and geographical distribution of the host species, are
important factors in establishing both the composition and concentration of the rumen ciliate community. More investigations
6
FEMS Microbiology Letters, 2016, Vol. 363, No. 6
Table 3. Total ciliate density and distribution of the total number of genera, species and morphotypes of ciliates from the rumen contents of
sheep from various locations around the world.
Locality
No. of
animals
Ciliate density
(x104 cells mL−1 )
Total no.
of genera
Total no.
of species
Total no.
of morphotypes
Canada
Egypt
Turkey
6
9
7
19.0
67
53.9
7
7
10
17
18
30
–
6
30
Libya
Northern Cyprus
9
10
220
37.8
5
6
14
34
5
50
Egypt
Kyrgyzstan
32
14
28.1
28.1
6
2
14
28
–
12
References
Imai et al. (1989)
Selim et al. (1996)
Öktem, Göçmen
and Torun (1997),
Göçmen et al.
(1999)
Selim et al. (1999)
Göçmen et al.
(2001), Göçmen
and Gürelli
(2009a,b)
Baraka (2012)
Present study
Table 4. Total ciliate density and distribution of the total number of genera, species and morphotypes of ciliates from the rumen contents of
goats from various locations around the world.
Locality
Japan
Nepal
Turkey
Egypt
Turkey
Kyrgyzstan
No. of
animals
Ciliate density
(×104 cells mL−1 )
Total no.
of genera
Total no.
of species
Total no.
of morphotypes
References
15
10
8
1
15
1
43.9
11.6
33.2
13.4
94.3
37.0
5
8
12
7
7
8
11
21
39
19
19
12
3
12
35
–
10
4
Ito et al. (1995)
Gurung et al. (2002)
Göçmen et al. (2005)
Baraka (2012)
Gürelli (2014a)
Present study
on rumen protozoa of herbivores living in various countries are
needed to obtain more information on the distribution of species
among different hosts.
ACKNOWLEDGEMENTS
We would like to express our appreciation to Prof. Dr AndréDenis G. Wright (School of Animal and Comparative Biomedical Sciences, The University of Arizona, USA) for his kind help
checking the manuscript, and to Fatih Çelik for his kind help receiving of samples from customs.
FUNDING
We would like to express our appreciation to the Kastamonu
University Scientific Research Project Commission, which supported this study (KUBAP-01/2014-22), to the Kyrgyz Turkish
Manas University Scientific Research Project Commission,
which supported this study (KTMUBAP 2013-FBE-05).
Conflict of interest. None declared.
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