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Protistology 13 (2), 71-78 (2019)
Protistology
Ruminal ciliate diversity of domestic cattle in Antalya, Turkey, with special emphasis on morphology of Entodinium rostratum (Entodiniomorphida, Ophryoscolecidae)
Gözde Gürelli and Nuray Yürücüoglu
Department of Biology, Faculty of Sciences and Arts, Kastamonu University, Kastamonu, Turkey
| Submitted March 14, 2019 | Accepted May 05, 2019 | Summary
The ruminal ciliate diversity of domestic cattle living in Antalya, Turkey was investigated and 29 species and 9 morphotypes belonging to 10 genera were detected. The average density (±SD) ofciliates in the ruminal contents of15 individuals ofdomestic cattle (Bos taurus taurus) was 100.0 (±74.4)* 104 cells ml-1. For individual cattle, the total number of species per animal ranged from 7.0 to 17.0 with an average of11.4±3.2 (SD). Of the ciliate species found, Isotricha prostoma and Entodinium simulans were the most abundant occurring in all cattle, each with a prevalence of 100%, whereas Diplodinium rangiferi, E. rectangulatum, Ostracodinium clipeolum, O. gracile and O. trivesiculatum were detected in only one animal (6.7% prevalence). Morphology of Entodinium rostratum (Entodiniomorphida, Ophryoscolecidae) was researched, and the infraciliary band pattern of this ciliate was described for the first time. The buccal infraciliary band pattern of E. rostratum is composed of two polybrachykineties, paralabial kineties, and vestibular fibrils. The adoral polybrachykinety is characteristic of other Entodinium species but vestibular polybrachykinety differs from other Entodinium species. Vestibular polybrachykinety of E. rostratum is straight and contains transverse, parallel, and short vestibular fibrils. Because of these features, the E. rostratum-type infraciliary band pattern is considered as more primitive than the Entodinium-type and could be ancestral in the family Ophryoscolecidae.
Key words: ciliate, domestic cattle, Entodinium rostratum, infraciliary band, rumen, Ophryoscolecidae, Turkey
Introduction
Cattle is one of the economically important domestic herbivores characterized by the presence of a rumen, which is inhabited by highly diverse microbiota consisting of fungi, viruses, bacteria,
archaea, and protozoa (Ogimoto and Imai, 1981; Williams and Coleman, 1992; Regensbogenova et al., 2004; Moon-van der Staay et al., 2014). Most of these protozoa are ciliates first described by Gruby and Delafond (1843). Endocommensal ciliates of the rumen are classified into two orders
doi:10.21685/1680-0826-2019-13-2-5 © 2019 The Author(s)
Protistology © 2019 Protozoological Society Affiliated with RAS
in the subclass Trichostomatia: Entodiniomorphida and Vestibuliferida. Entodiniomorphid ciliates are divided into three families, Ophryoscolecidae in the suborder Entodiniomorphina, Buetschliidae in the suborder Archistomatina, and Blepharocorythidae in the suborder Blepharocorythina (Lynn, 2008). Ophryoscolecid ciliates constitute the most predominant population in the rumen (Imai, 1988), and are divided into three subfamilies, Ophryoscoleci-nae, Diplodiniinae, and Entodiniinae (Lubinsky, 1957). The subfamily Entodiniinae contains only one genus, Entodinium, which is defined by having a single ciliary zone (retractable adoral ciliary zone), micronucleus situated ventrally to the macronuc-leus, and a contractile vacuole (Lubinsky, 1957; Lynn, 2008). In ophryoscolecid ciliates, buccal infraciliary band patterns reflect the evolutionary relationships between the species (Gurelli and Akman, 2017; Gurelli, 2018; Ito and Imai, 2003).
The objectives of this investigation were to assess the ruminal ciliate diversity in domestic cattle (Bos taurus taurus) living in Antalya, Turkey, describe the morphology of Entodinium rostratum (Entodiniomorphida, Ophryoscolecidae) with the special emphasis on the infraciliary band pattern, and discuss the evolution of Entodinium species.
Material and methods
Rumen samples were gathered from 15 domestic cattle (B. taurus taurus) at the slaughterhouses near Antalya, Turkey between January 2017 and July 2017. After slaughter, the rumen was cut open with a knife and fresh rumen contents were fixed with an equal volume of18.5% formalin as soon as possible to avoid the destruction of ciliates (Dehority, 1984). In the laboratory, they were filtered and stained with methyl green formalin saline solution to get differential and total cell counts (Ogimoto and Imai, 1981). The solution of 2% Lugol's iodine was added to samples to reveal the skeletal plates, and methyl green formalin saline solution was used to indicate nuclei (Gurelli, 2016a). The infraciliary band was impregnated using the method of pyridinated silver carbonate. The term polybrachykinety was used for infraciliary band consisting of numerous short and parallel kineties (Fernandez-Galiano et al., 1985; Ito and Imai, 1998, 2003, 2006).
For the orientation of the ciliates, the rule of Dogiel (1927) was approved. The side closest to the macronucleus was named the dorsal side, and
the opposite side was named the ventral side, thus defining the left and right sides.
Ciliate densities were calculated using the hemocytometer counting chamber. The relative abundance of each species and genus was estimated from smear slides (Gürelli and Akman, 2017).
The identification and classification of the species were primarily in accordance with the descriptions published by Dehority (1993), Dogiel (1927), Lubinsky (1957), Lynn (2008), and Ogimoto and Imai (1981).
The specimens of E. rostratum were examined in detail using a FEG 250 scanning electron microscope (SEM) (FEI-Quanta, Hillsboro, OR, USA) following the method of Imai et al. (1992).
Results
Ruminal ciliate diversity in domestic cattle
The average density (±SD) of ciliates in the ruminal contents of 15 domestic cattle (B. taurus taurus) was 100.0 (±74.4)x104 cells ml-1. Values ranged from 28.5 to 260.0 x 104 cells ml-1. Twenty-nine species and 9 morphotypes belonging to 10 genera were detected. Of the ciliate species found, Isotricha prostoma and Entodinium simulans were the most abundant occurring in all cattle, each with a prevalence of 100%, whereas Diplodinium rangiferi, E. rectangulatum, Ostracodinium clipeolum, O. gracile, and O. trivesiculatum were detected in only one animal (6.7% prevalence). Ordinarily, the ruminal ciliate fauna of cattle in Antalya, Turkey was mostly composed of Entodinium species (mean: 72.9%; range: 15.4-98.0%) (Table 1). For individual cattle, the total number of species per animal ranged from 7.0 to 17.0 with an average of11.4±3.2.
Infraciliary band pattern of Entodinium rostratum (Entodiniomorphida, Ophryoscolecidae)
The buccal infraciliary band pattern of E. rostratum is composed of two polybrachykineties, paralabial kineties, and vestibular fibrils. The adoral polybrachykinety encircles the ventral, right and dorsal edges of the circumference of the vestibular opening. The left ventral part ofthe adoral polybrachykinety is shorter and directs toward the postero-dorsal side. Paralabial kineties are at the right ventral side ofthe adoral polybrachykinety; they are composed of short transverse or slightly oblique
Table 1. Prevalence and relative abundance of ruminal ciliates in the rumen contents of 15 domestic cattle
living in Antalya, Turkey.
Genus/species/morphotype Prevalence (%) Relative abundance (%)
Mean ± SD Range
Dasytricha 80 2.5±2.4 0-9.2
D. ruminantium Schuberg, 1888 80 2.5±2.4 0-9.2
Diplodinium 20 1.0±2.9 0-11.2
D. dentatum (Stein, 1858) 13.3 0.8±2.9 0-11.2
D. rangiferi Dogiel, 1925 6.7 0.2±0.7 0-2.7
Entodinium 100 72.9±21.6 15.4-98.0
E. bifidum Dogiel, 1927 20 4.2 ± 10.0 0-33.1
E. bifidum m. bifidum Dogiel, 1927 20 4.2 ± 10.0 0-33.1
E. bursa Stein, 1858 13.3 0.2 ± 0.5 0-1.9
E. dilobum (Dogiel, 1927) 73.3 1.4 ± 2.0 0-7.6
E. dubardi Buisson, 1923 13.3 0.7 ± 1.9 0-6.8
E. ellipsoideum (Kofoid and MacLennan, 1930) 53.3 5.0 ± 8.7 0-32.4
E. exiguum Dogiel, 1925 40 2.0 ± 3.4 0-8.6
E. longinucleatum Dogiel, 1925 86.7 2.8 ± 4.0 0-15.1
E. minimum Schuberg, 1888 53.3 7.1 ± 9.4 0-29.6
E. nanellum Dogiel, 1923 80 23.6 ± 23.5 0-69.8
E. rectangulatum Kofoid and MacLennan, 1930 6.7 0.1 ± 0.5 0-1.9
E. rectangulatum m. rectangulatum Kofoid and MacLennan, 1930 6.7 0.1 ± 0.5 0-1.9
E. rostratum Fiorentini, 1889 13.3 0.2 ± 0.5 0-1.5
E. simplex (Dogiel, 1925) 73.3 5.6 ± 6.0 0-15.8
E. simulans Lubinsky, 1957 100 16.1 ± 11.8 3.7-41.7
E. simulans m. dubardi Lubinsky, 1957 40 4.1 ± 8.9 0-34.4
E. simulans m. lobosospinosum Lubinsky, 1957 33.3 0.5 ± 1.0 0-3.2
E. simulans m. caudatum Lubinsky, 1957 86.7 11.5 ± 11.0 0-41.6
E. triacum Dogiel, 1927 26.7 3.6 ± 8.7 0-29.9
E. triacum m. triacum Dogiel, 1927 26.7 3.6 ± 8.7 0-29.9
Epidinium 53.3 7.3 ± 10.0 0-33.6
E. ecaudatum (Fiorentini, 1889) 53.3 7.3 ± 10.0 0-33.6
E. ecaudatum m. ecaudatum (Fiorentini, 1889) 20 0.4 ± 1.5 0-5.7
E. ecaudatum m. caudatum (Fiorentini, 1889) 53.3 6.8 ± 9.6 0-33.0
Eudiplodinium 46.7 2.4 ± 4.1 0-14.0
E. bovis (Dogiel, 1927) 13.3 0.5 ± 1.5 0-5.5
E. maggii (Fiorentini, 1889) 26.7 0.6 ± 1.0 0-2.9
E. rostratum (Fiorentini, 1889) 20 1.3 ± 3.2 0-11.2
Isotricha 100.0 6.6 ± 11.5 0.6-46.5
I. intestinalis Stein, 1858 40.0 0.4 ± 0.9 0-3.1
I. prostoma Stein, 1858 100.0 6.2 ± 11.2 0.4-45.0
Metadinium 26.7 0.4 ± 1.1 0-3.9
M. affine (Dogiel and Fedorowa, 1925) 26.7 0.4 ± 1.1 0-3.9
Ostracodinium 20 0.5 ±1.5 0-5.8
O. clipeolum Kofoid and MacLennan, 1932 6.7 <0.1 ± <0.1 0-0.3
O. gracile (Dogiel, 1925) 6.7 0.4 ± 1.5 0-5.8
O. trivesiculatum Kofoid and MacLennan, 1932 6.7 0.1 ± 0.5 0-1.8
Ophryoscolex 20 0.7 ± 2.2 0-9.2
O. purkynjei Stein, 1858 20 0.7 ± 2.2 0-9.2
O. purkynjei m. purkynjei Stein, 1858 20 0.7 ± 2.2 0-9.2
Polyplastron 40 0.6 ± 1.1 0-3.5
P. multivesiculatum (Dogiel and Fedorowa, 1923) 40 0.6 ± 1.1 0-3.5
Notes. Total species, morphotypes, and genera number: 29, 9, and 10, accordingly.
kineties. Kinetids of paralabial kineties are slightly larger than those of the other polybrachykineties. The vestibular polybrachkinety is straight and begins from the dorsal part ofthe adoral polybrachykinety, extends along the dorsal wall of the vestibulum, and ends near the micronucleus. Vestibular fibrils are transverse, parallel, and short and arise from the dorsal wall of the vestibulum. When the adoral ciliary zone is protruded, both ends of the adoral polybrachykinety come close to each other and paralabial kineties change their direction from the right ventral side to the ventral side. When the adoral ciliary zone is strongly retracted, the inner edge of the adoral polybrachykinety is further posterior than the outher edge. The widths of the adoral and vestibular polybrachykineties are equal (Figs 1, 2).
The division is by transverse binary fission and begins when the primordium of the adoral polybrachykinety (ventral primordium) and the primordium of the vestibular polybrachykinety (left primordium) appear on the ventral and left sides at the same axial level. The primordium of paralabial kineties is composed of the right ventral side ofthe ventral primordium. The left primordium tilts obliquely relative to the longitudinal axis of the body and then the ventral extremity of the left primordium turns toward the posterior end and develops into the vestibular polybrachykinety. The ventral primordium develops into the adoral polybrachykinety. The buccal polybrachykineties of the opisthe arise with no relationship to the buccal polybrachykineties of the proter (Fig. 3).
Discussion
In this investigation, 29 ciliate species and 9 morphotypes belonging to 10 genera were detected in the ruminal contents of15 individuals of domestic cattle living in Antalya, Turkey; morphology of Entodinium rostratum (Entodiniomorphida, Oph-ryoscolecidae) was researched and its infraciliary band pattern was described for the first time. E. rostratum was reported for the first time by Fiorentini (1889). The body of E. rostratum is asymmetric in shape. The right side of the body is strongly convex, and the ventral side is flattened or concave. The anterior end of the body is flattened, a heavy spine is at the postero-ventral end of the body and directs to the dorsal side. The adoral ciliary zone is retractable and lies at the anterior end of the body. The vestibulum is funnel-shaped and straight. The macronucleus is rod-shaped and has
Fig. 1. Schematic figure of infraciliary band pattern of Entodinium rostratum from the right side, after pyridinated silver carbonate impregnation. Abbreviations: ap — adoral polybrachykinety, cp — cytoproct, cv — contractile vacuole, ma — macronucleus, mi — micronucleus, pk — paralabial kineties, s — spine, vf — vestibular fibrils, vp — vestibular polybrachykinety. Scale bar: 10 ^m.
the same thickness of any part. The micronucleus is spherical in shape and adheres to the ventral side of the macronucleus. A contractile vacuole is at the anterior end ofthe macronucleus. The cytoproct is at the posterior end ofthe body and near the ventral side (Dogiel, 1927; Ogimoto and Imai, 1981; Dehority 1993) (Figs 1, 2). In addition, the morphological features of E. rostratum were examined with SEM in this investigation showing that the lateral groove extends along the right dorsal surface from the anterior end to the cytoproct. Ectosymbiotic rumen bacteria inhabit between the lateral groove and the dorsal side of the body (Fig. 4).
E. rostratum possesses a different buccal infra-ciliary band pattern from that of other Entodinium species. Despite the shape ofthe adoral polybrachykinety and location of paralabial kineties are similar in all Entodinium species, the shape ofthe vestibular polybrachykinety is different. The vestibulum of E. rostratum is funnel-shaped and straight, whereas the vestibulum of other Entodinium species is funnel-shaped and curved. The vestibular polybrachykinety of E. rostratum contains the transverse, parallel and short vestibular fibrils, which arise from the dorsal wall of the vestibulum. Up to now, vestibular fibrils
Fig. 2. Photomicrographs of E. rostratum, after pyridinated silver carbonate impregnation. A — From the right side; B, C, D — from the left side; E — from the right side, when the adoral ciliary zone protruded; F — from the right side, when the adoral ciliary zone strongly retracted. Abbreviations: ap — adoral polybrachykinety, cp — cytoproct, cv — contractile vacuole, ma — macronucleus, mi — micronucleus, pk — paralabial kineties, s — spine, vf — vestibular fibrils, vp — vestibular polybrachykinety. Scale bars: 10 ^m.
Fig. 3. Photomicrographs of E. rostratum in binary fission, after pyridinated silver carbonate impregnation. A — From the right side; B — from the left side. Abbreviations: ap — adoral polybrachykinety, lpr — left primordium, pk — paralabial kineties, ppk — primordium of PK, vf — vestibular fibrils, vp — vestibular polybrachykinety, vpr — ventral primordium. Scale bars: 10 ^m.
Fig. 4. SEM images of E. rostratum. A — From the left side; B — from the right side. Abbreviations: acz — adoral ciliary zone, b — bacteria, lg — lateral groove, p — pore of contractile vacuole. Scale bars: A - 10 ^m; B - 20 ^m.
were not observed in other Entodinium species as well as in other ophryoscolecid ciliates (Noirot-Timothee, 1960; Ito et al., 1997, 2001; Ito and Imai, 1998, 2003, 2005, 2006; Mishima et al., 2009; Gurelli and Akman, 2017; Gurelli, 2018; Ito and Tokiwa, 2018; Cedrola et al., 2018). Transverse, short, and parallel dorsal vestibular fibrils were detected in the hindgut ciliate species Charonina elephanti, which was classified in the family Blepharocorythidae, suborder Blepharocorythina (Gurelli, 2019). Transverse, short, and parallel vestibular fibrils with different locations also exist in Charonina ventricula, which is living in the rumen of ruminants (Wolska, 1967). Because of transverse vestibular fibrils, and funnel-shaped straight vestibulum, the evolutionary relationship could be suggested between Charonina species and E. rostratum.
According to our results, two different infra-ciliary band patterns occur in Entodinium species, Entodinium rostratum-type, and Entodinium-type. E. bursa, E. biconcavum, E. bovis, E. bimastus, E. exiguum, E. ovinum, E. longinucleatum, E. minimum, E. parvum, E. nanellum, E. simplex, E. caudatum, E. triacum, and E. simulans have Entodinium-type infraciliary band pattern (Ito and Imai, 2006; Gurelli, 2016b). The vestibular polybrachykinety is curved shaped in the Entodinium-type infraciliary band pattern, because ofthe curved vestibulum (Fig. 5). It is considered that Entodinium rostratum-type infraciliary band pattern is more primitive compared to Entodinium-type and thus could be the ancestral type in the family Ophryoscolecidae. In the course of evolution, the funnel-shaped, straight vestibulum of E. rostratum most likely has changed to the funnel-shaped, curved vestibulum of other
Entodinium species. Such an evolutionary change of the vestibulum must have had an effect on the pattern of infraciliary bands in the buccal region (Ito and Imai, 2006). Along with the changing ofthe vestibulum, vestibular fibrils could have disappeared.
The average ciliate density in the ruminal contents of domestic cattle living in Antalya (100.0 ±74.4* 104 cells ml-1) was higher than that of domestic cattle in Istanbul (Gurelli and Akman, 2017), domestic cattle in Kastamonu (Gurelli, 2016b) and domestic cattle in Izmir (Gormen et al., 2003). The host's different geographical locations, their respective diets, the number ofhosts examined, or combination ofthese factors are important drivers responsible for this variation (Imai et al., 1989; Ito and Imai, 1990; Gurelli, 2016b; Gurelli and Akman, 2017).
The ruminal ciliate fauna of domestic cattle in Antalya was mostly composed of Entodinium species because the host is fed a concentrate-rich ration, Entodinium species grow fast, and their relative abundance increases (Hungate, 1966).
In conclusion, further investigations on endo-symbiotic ciliate diversity of herbivores and infra-ciliary band patterns of ciliates will help to unveil evolutionary relationships among them.
Acknowledgements
We would like to express our appreciation to the Kastamonu University Scientific Research Project Commission, which supported this investigation (KU-BAP-01/2017-3), and to the Research and Application Center of Kastamonu University for SEM images.
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Address for correspondence: Gözde Gürelli. Department of Biology, Faculty of Sciences and Arts, Kastamonu University, Kastamonu, Turkey; e-mail: [email protected], [email protected]
