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Rumen Ciliate (Ciliophora, Trichostomatia) Fauna of Goats and Sheep in Antalya, and Phylogeny of Rumen Ciliates

Year 2024, Volume: 29 Issue: 2, 429 - 437, 31.08.2024
https://doi.org/10.53433/yyufbed.1458622

Abstract

In this study, the rumen ciliate fauna of goats (Capra aegagrus hircus) and sheep (Ovis aries) in Antalya was detected, and phylogenetic analyses were performed using 18S rDNA gene sequences of 68 rumen ciliates obtained from GenBank. The average ciliate density in the rumen of 6 goats and 11 sheep in Antalya was 124.0 × 104 cells mL–1 and 46.3 × 104 cells mL–1, respectively. Eight genera, 15 species, and 6 morphotypes have been identified in goats, and 8 genera, 19 species, and 7 morphotypes in sheep. Entodinium simulans was observed in all goats with a prevalence of 100%, while Metadinium affine and Entodinium bursa were identified in a single goat with a prevalence of 16.7%. Entodinium simulans in sheep had a prevalence of 81.8%, and in 10 of the 11 sheep examined, Enoploplastron triloricatum, Entodinium dilobum, E. longinucleatum, E. rectangulatum, E. simplex, and E. simulans m. lobosospinosum were detected in a single sheep with a prevalence of 9.1%. The rumen ciliate fauna of goats and sheep generally consists of Entodinium spp. (the average relative abundance for goats is 88.7%, and the average relative abundance for sheep is 52.2%). According to phylogenetic analyses, the Ophryoscolecinae, Entodiniinae, and Diplodininae subfamilies within the family Ophryoscolecidae have a monophyletic origin. The genera Isotricha, Dasytricha, Ophryoscolex, Epidinium, Entodinium, Diplodinium, and Ostracodinium are also monophyletic.

References

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  • Burritt, E., & Frost, R. (2006). Chapter 2: Animal behaviour principles and practices. In: K. L. Launchbaugh, J. W. Walker, & R. J. Daines (Eds), Targeted grazing: A natural approach to vegetation management and landscape enhancement (pp. 10–21). Englewood: American Sheep Industry Association.
  • Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575–583. https://doi.org/10.2307/3284227
  • Cannas, A., & Pulina, G. (2008). Dairy goats feeding and nutrition. CAB International.
  • Cedrola, F., Senra, M. V. X., Fregulia, P., D’Agosto, M., & Dias, R. J. P. (2022). Insights into the systematics of the family Ophryoscolecidae (Ciliophora, Entodiniomorphida). Journal of Eukaryotic Microbiology, 69, e12915. https://doi.org/10.1111/jeu.12915
  • Coleman, G. S., Laurie, J. I., & Bailey, J. E. (1977). The cultivation of the rumen ciliate Entodinium bursa in the presence of Entodinium caudatum. Journal of General Microbiology, 101, 253–258. https://doi.org/10.1099/00221287-101-2-253
  • Dehority, B. A. (1974). Rumen ciliate fauna of Alaskan moose (Alces americana), musk-ox (Ovibos moschatus) and Dall moutain sheep (Ovis dalli). Journal of Protozoology, 21, 26–32. https://doi.org/10.1111/j.1550-7408.1974.tb03612.x
  • Dehority, B. A. (1978). Specificity of rumen ciliate protozoa in cattle and sheep. Journal of Protozoology, 25(4), 509–513. https://doi.org/10.1111/j.1550-7408.1978.tb04177.x
  • Dehority, B. A. (1984). Evaluation of subsampling and fixation procedures used for counting rumen protozoa. Applied and Environmental Microbiology, 48(1), 182–185. https://doi.org/10.1128/aem.48.1.182-185.1984
  • Dehority, B. A. (1986). Protozoa of the digestive tract of herbivorous mammals. Insect Science and Its Application, 7, 279–296. https://doi.org/10.1017/S1742758400009346
  • Dehority, B. A. (1993). Laboratory manual for classification and morphology of rumen ciliate protozoa. CRC Press.
  • Dogiel, V. A. (1927). Monographie der familie Ophryoscolecidae. Archiv für Protistenkunde, 59, 1–288.
  • Dogiel, V. A. (1947). The phylogeny of the stomach infusorians of ruminants in the light of paleontological and parasitological data. Quarterly Journal of Microscopical Science, 88(3), 337–343. https://doi.org/10.1242/jcs.s3-88.3.337
  • Eadie, J. M. (1957). The mid-winter rumen microfauna of the seaweed-eating sheep of North Ronaldshay. Proceedings of the Royal Society of Edinburgh, Section B 66(3), 276–287. https://doi.org/10.1017/S0080455X00010055
  • Eadie, J. M. (1962). The development of rumen microbial populations in lambs and calves under various conditions of management. Journal of General Microbiology, 29, 563–578. https://doi.org/10.1099/00221287-29-4-563
  • Göçmen, B., & Özbel, Y. (2001). İşkembede yaşayan kamçılı (Mastigophora) ve holotriş siliyat (Ciliophora) protozoonlar. Türkiye Parazitoloji Dergisi, 25(4), 405–425.
  • Göçmen, B., Rastgeldi, S., Karaoğlu, A., & Aşkan, H. (2005). Rumen ciliated protozoa of the Turkish domestic goats (Capra hircus L.). Zootaxa, 1091(1), 53–64. https://doi.org/10.11646/zootaxa.1091.1.4
  • Göçmen, B., Torun, S., & Öktem, N. (1999). Türkiye evcil koyun (Ovis ammon aries)’larının işkembe siliyat (Protozoa: Ciliophora) faunası hakkında bir ön çalışma: II- Familya Ophryoscolecidae (Entodiniomorphida). Doğa-Turkish Journal of Zoology, 23, 473–490.
  • Gruby, D., & Delafond, O. (1843). Recherches sur des animalcules su developpant en gland nombre dens I’estomac et les intestins, pendant la digestion des animaux herbivores et carnivores. Comptes Rendus Academy Science Paris, 17, 1304–1308.
  • Gurung, Y. B., Parajuli, N., Miyazaki, Y., Imai, S., & Kobayashi, K. (2002). Rumen ciliate faunae of water buffalo (Bubalus bubalis) and goat (Capra hircus) in Nepal. Journal of Veterinary Medical Science, 64, 265–267. https://doi.org/10.1292/jvms.64.265
  • Gürelli, G. (2014). Rumen ciliate fauna (Ciliophora, Protista) of Turkish domestic goats living in İzmir, Turkey. Turkish Journal of Zoology, 38, 136–143. https://doi.org/10.3906/zoo-1303-21
  • Gürelli, G. (2016). Rumen ciliates of domestic cattle (Bos taurus taurus) in Kastamonu, Turkey with the description of a new species. European Journal of Protistology, 56, 51–59. https://doi.org/10.1016/j.ejop.2016.07.002
  • Gürelli, G. (2017). Rumen ciliate fauna of domestic sheep (Ovis aries) in İzmir, Turkey and scanning electron microscopic observations. Zootaxa, 4286(4), 545–554. https://doi.org/10.11646/zootaxa.4286.4.7
  • Gürelli, G., Canbulat, S., Aldayarov, N., & Dehority, B.A. (2016). Rumen ciliate protozoa of domestic sheep (Ovis aries) and goat (Capra aegagrus hircus) in Kyrgyzstan. FEMS Microbiology Letters, 363, fnw028. https://doi.org/10.1093/femsle/fnw028
  • Gürelli, G., & Mohamed, A. R. A. (2021). Comparative study of rumen ciliate fauna of goat and sheep in Libya. Türkiye Parazitoloji Dergisi, 45(4), 274–279. https://doi.org/10.4274/tpd.galenos.2021.39974
  • Hoang, D. T., Chernomor, O., Von Haeseler A., Minh, B. Q., & Vinh, L. S. (2018). UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 3, 518–522. https://doi.org/10.1093/molbev/msx281
  • Hungate, R. E. (1996). The rumen and its microbes. Academic Press.
  • Imai, S. (1988). Ciliate protozoa in the rumen of Kenyan zebu cattle, Bos taurus indicus, with the description of four new species. Journal of Protozoology, 35, 130–136. https://doi.org/10.1111/j.1550-7408.1988.tb04092.x
  • Imai, S., Han, S. S., Cheng, K. J., & Kudo, H. (1989). Composition of the rumen ciliate population in experimental herds of cattle and sheep in Lethbridge, Alberta, Western Canada. Canadian Journal of Microbiology, 35, 686–90. https://doi.org/10.1139/m89-112
  • Imai, S., Katsuno, M., & Ogimoto, K. (1978). Distribution of rumen ciliate protozoa in cattle, sheep and goat and experimental transfaunation of them. Japanese Journal of Zootechnical Science, 49(7), 494–505. https://doi.org/10.2508/chikusan.49.494
  • Imai, S., Katsuno, M., & Ogimoto, K. (1979). Type of the pattern of the rumen ciliate composition of the domestic ruminants and the predator-prey interaction of ciliates. Japanese Journal of Zootechnical Science, 50(2), 79–87. https://doi.org/10.2508/chikusan.50.79
  • Ito, A., & Imai, S. (1990). Ciliated protozoa in the rumen of Holstein–Friesian cattle (Bos taurus taurus) in Hokkaido, Japan, with the description of two new species. Zoological Science, 7, 449–458.
  • Ito, A., Imai, S., Manda, M., & Ogimoto, K. (1995). Rumen ciliates of Tokara native goat in Kagoshima, Japan. Journal of Veterinary Medical Science, 57, 355–357. https://doi.org/10.1292/jvms.57.355
  • Ito, A., Imai, S., & Ogimoto, K. (1993). Rumen ciliates of ezo deer (Cervus nippon yesoensis) with the morphological comparison with those of cattle. The Journal of Veterinary Medical Science, 55, 93–98. https://doi.org/10.1292/jvms.55.93
  • Kalyaanamoorthy, S., Minh, B. Q., Wong, T. F. K., & Von Haeseler, A. (2017). ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285
  • Kumar, S., Stecher, G., & Tamura, K., (2016). MEGA 7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874. https://doi.org/10.1093/molbev/msw054
  • Kurihara, Y., Takechi, T., & Shibata, F. (1978). Relationship between bacteria and ciliate protozoa in the rumen of sheep fed on a purified diet. The Journal of Agricultural Science, 90, 373–381. https://doi.org/10.1017/S0021859600055489
  • Lubinsky, G. (1957). Studies on the evolution of the Ophryoscolecidae III. Phylogeny of the Ophryoscolecidae based on their comparative morphology. Canadian Journal of Zoology, 35, 141–159. https://doi.org/10.1139/z57-009
  • Lynn, D. H. (2008). The ciliated protozoa: Characterization, classification and guide to the literature (3rd ed.). Springer.
  • Moon-van der Staay, S. Y., van der Staay, G. W. M., Michalowski, T., Jauany, J.-P., Pristas, P., Javorský, P., … & Hackstein, J. H. P. (2014). The symbiotic intestinal ciliates and the evolution of their hosts. European Journal of Protistology, 50, 166–173. https://doi.org/10.1016/j.ejop.2014.01.004
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Antalya’daki Keçi ve Koyunların İşkembe Siliyat (Ciliophora, Trichostomatia) Faunası ve İşkembe Siliyatlarının Filogenisi

Year 2024, Volume: 29 Issue: 2, 429 - 437, 31.08.2024
https://doi.org/10.53433/yyufbed.1458622

Abstract

Bu çalışmada Antalya’daki keçi (Capra aegagrus hircus) ve koyunların (Ovis aries) işkembe siliyat faunası tespit edilmiş ve GenBank’tan elde edilen 68 işkembe siliyatına ait 18S rDNA gen dizileri kullanılarak filogenetik analizler yapılmıştır. Antalya’daki 6 keçi ve 11 koyunun işkembesindeki ortalama siliyat yoğunluğu sırasıyla, 124.0 × 104 hücre mL–1 ve 46.3 × 104 hücre mL–1’dir. Keçide 8 cins, 15 tür ve 6 morfotip, koyunda 8 cins, 19 tür ve 7 morfotip teşhis edilmiştir. Entodinium simulans %100 yaygınlıkla tüm keçilerde, Metadinium affine ve Entodinium bursa ise %16.7 yaygınlıkla tek bir keçiden gözlemlenmiştir. Koyunlarda Entodinium simulans %81.8 yaygınlıkla incelenen 11 koyunun 10’unda, Enoploplastron triloricatum, Entodinium dilobum, E. longinucleatum, E. rectangulatum, E. simplex, E. simulans m. lobosospinosum ise %9.1 yaygınlıkla tek bir koyundan tespit edilmiştir. Keçi ve koyunların işkembe siliyat faunası genelde Entodinium spp.’den meydana gelmektedir (keçiler için ortalama nispi bolluk %88.7, koyunlar için ortalama nispi bolluk %52.2). Filogenetik analizlere göre Ophryoscolecidae ailesi içinde Ophryoscolecinae, Entodiniinae ve Diplodininae alt-aileleri monofiletik orijine sahiptirler. Isotricha, Dasytricha, Ophryoscolex, Epidinium, Entodinium, Diplodinium ve Ostracodinium cinsleri de monofiletik kökenlidir.

References

  • Berber, B., & Gürelli, G. (2019). Rumen ciliate fauna of domestic sheep in Kastamonu, Turkey and infraciliature of Diplodinium quinquespinosum, Metadinium affine, and M. tauricum (Entodiniomorphida, Ophryoscolecidae). Zootaxa, 4695(6), 550–558. https://doi.org/10.11646/zootaxa.4695.6.5
  • Burritt, E., & Frost, R. (2006). Chapter 2: Animal behaviour principles and practices. In: K. L. Launchbaugh, J. W. Walker, & R. J. Daines (Eds), Targeted grazing: A natural approach to vegetation management and landscape enhancement (pp. 10–21). Englewood: American Sheep Industry Association.
  • Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575–583. https://doi.org/10.2307/3284227
  • Cannas, A., & Pulina, G. (2008). Dairy goats feeding and nutrition. CAB International.
  • Cedrola, F., Senra, M. V. X., Fregulia, P., D’Agosto, M., & Dias, R. J. P. (2022). Insights into the systematics of the family Ophryoscolecidae (Ciliophora, Entodiniomorphida). Journal of Eukaryotic Microbiology, 69, e12915. https://doi.org/10.1111/jeu.12915
  • Coleman, G. S., Laurie, J. I., & Bailey, J. E. (1977). The cultivation of the rumen ciliate Entodinium bursa in the presence of Entodinium caudatum. Journal of General Microbiology, 101, 253–258. https://doi.org/10.1099/00221287-101-2-253
  • Dehority, B. A. (1974). Rumen ciliate fauna of Alaskan moose (Alces americana), musk-ox (Ovibos moschatus) and Dall moutain sheep (Ovis dalli). Journal of Protozoology, 21, 26–32. https://doi.org/10.1111/j.1550-7408.1974.tb03612.x
  • Dehority, B. A. (1978). Specificity of rumen ciliate protozoa in cattle and sheep. Journal of Protozoology, 25(4), 509–513. https://doi.org/10.1111/j.1550-7408.1978.tb04177.x
  • Dehority, B. A. (1984). Evaluation of subsampling and fixation procedures used for counting rumen protozoa. Applied and Environmental Microbiology, 48(1), 182–185. https://doi.org/10.1128/aem.48.1.182-185.1984
  • Dehority, B. A. (1986). Protozoa of the digestive tract of herbivorous mammals. Insect Science and Its Application, 7, 279–296. https://doi.org/10.1017/S1742758400009346
  • Dehority, B. A. (1993). Laboratory manual for classification and morphology of rumen ciliate protozoa. CRC Press.
  • Dogiel, V. A. (1927). Monographie der familie Ophryoscolecidae. Archiv für Protistenkunde, 59, 1–288.
  • Dogiel, V. A. (1947). The phylogeny of the stomach infusorians of ruminants in the light of paleontological and parasitological data. Quarterly Journal of Microscopical Science, 88(3), 337–343. https://doi.org/10.1242/jcs.s3-88.3.337
  • Eadie, J. M. (1957). The mid-winter rumen microfauna of the seaweed-eating sheep of North Ronaldshay. Proceedings of the Royal Society of Edinburgh, Section B 66(3), 276–287. https://doi.org/10.1017/S0080455X00010055
  • Eadie, J. M. (1962). The development of rumen microbial populations in lambs and calves under various conditions of management. Journal of General Microbiology, 29, 563–578. https://doi.org/10.1099/00221287-29-4-563
  • Göçmen, B., & Özbel, Y. (2001). İşkembede yaşayan kamçılı (Mastigophora) ve holotriş siliyat (Ciliophora) protozoonlar. Türkiye Parazitoloji Dergisi, 25(4), 405–425.
  • Göçmen, B., Rastgeldi, S., Karaoğlu, A., & Aşkan, H. (2005). Rumen ciliated protozoa of the Turkish domestic goats (Capra hircus L.). Zootaxa, 1091(1), 53–64. https://doi.org/10.11646/zootaxa.1091.1.4
  • Göçmen, B., Torun, S., & Öktem, N. (1999). Türkiye evcil koyun (Ovis ammon aries)’larının işkembe siliyat (Protozoa: Ciliophora) faunası hakkında bir ön çalışma: II- Familya Ophryoscolecidae (Entodiniomorphida). Doğa-Turkish Journal of Zoology, 23, 473–490.
  • Gruby, D., & Delafond, O. (1843). Recherches sur des animalcules su developpant en gland nombre dens I’estomac et les intestins, pendant la digestion des animaux herbivores et carnivores. Comptes Rendus Academy Science Paris, 17, 1304–1308.
  • Gurung, Y. B., Parajuli, N., Miyazaki, Y., Imai, S., & Kobayashi, K. (2002). Rumen ciliate faunae of water buffalo (Bubalus bubalis) and goat (Capra hircus) in Nepal. Journal of Veterinary Medical Science, 64, 265–267. https://doi.org/10.1292/jvms.64.265
  • Gürelli, G. (2014). Rumen ciliate fauna (Ciliophora, Protista) of Turkish domestic goats living in İzmir, Turkey. Turkish Journal of Zoology, 38, 136–143. https://doi.org/10.3906/zoo-1303-21
  • Gürelli, G. (2016). Rumen ciliates of domestic cattle (Bos taurus taurus) in Kastamonu, Turkey with the description of a new species. European Journal of Protistology, 56, 51–59. https://doi.org/10.1016/j.ejop.2016.07.002
  • Gürelli, G. (2017). Rumen ciliate fauna of domestic sheep (Ovis aries) in İzmir, Turkey and scanning electron microscopic observations. Zootaxa, 4286(4), 545–554. https://doi.org/10.11646/zootaxa.4286.4.7
  • Gürelli, G., Canbulat, S., Aldayarov, N., & Dehority, B.A. (2016). Rumen ciliate protozoa of domestic sheep (Ovis aries) and goat (Capra aegagrus hircus) in Kyrgyzstan. FEMS Microbiology Letters, 363, fnw028. https://doi.org/10.1093/femsle/fnw028
  • Gürelli, G., & Mohamed, A. R. A. (2021). Comparative study of rumen ciliate fauna of goat and sheep in Libya. Türkiye Parazitoloji Dergisi, 45(4), 274–279. https://doi.org/10.4274/tpd.galenos.2021.39974
  • Hoang, D. T., Chernomor, O., Von Haeseler A., Minh, B. Q., & Vinh, L. S. (2018). UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 3, 518–522. https://doi.org/10.1093/molbev/msx281
  • Hungate, R. E. (1996). The rumen and its microbes. Academic Press.
  • Imai, S. (1988). Ciliate protozoa in the rumen of Kenyan zebu cattle, Bos taurus indicus, with the description of four new species. Journal of Protozoology, 35, 130–136. https://doi.org/10.1111/j.1550-7408.1988.tb04092.x
  • Imai, S., Han, S. S., Cheng, K. J., & Kudo, H. (1989). Composition of the rumen ciliate population in experimental herds of cattle and sheep in Lethbridge, Alberta, Western Canada. Canadian Journal of Microbiology, 35, 686–90. https://doi.org/10.1139/m89-112
  • Imai, S., Katsuno, M., & Ogimoto, K. (1978). Distribution of rumen ciliate protozoa in cattle, sheep and goat and experimental transfaunation of them. Japanese Journal of Zootechnical Science, 49(7), 494–505. https://doi.org/10.2508/chikusan.49.494
  • Imai, S., Katsuno, M., & Ogimoto, K. (1979). Type of the pattern of the rumen ciliate composition of the domestic ruminants and the predator-prey interaction of ciliates. Japanese Journal of Zootechnical Science, 50(2), 79–87. https://doi.org/10.2508/chikusan.50.79
  • Ito, A., & Imai, S. (1990). Ciliated protozoa in the rumen of Holstein–Friesian cattle (Bos taurus taurus) in Hokkaido, Japan, with the description of two new species. Zoological Science, 7, 449–458.
  • Ito, A., Imai, S., Manda, M., & Ogimoto, K. (1995). Rumen ciliates of Tokara native goat in Kagoshima, Japan. Journal of Veterinary Medical Science, 57, 355–357. https://doi.org/10.1292/jvms.57.355
  • Ito, A., Imai, S., & Ogimoto, K. (1993). Rumen ciliates of ezo deer (Cervus nippon yesoensis) with the morphological comparison with those of cattle. The Journal of Veterinary Medical Science, 55, 93–98. https://doi.org/10.1292/jvms.55.93
  • Kalyaanamoorthy, S., Minh, B. Q., Wong, T. F. K., & Von Haeseler, A. (2017). ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285
  • Kumar, S., Stecher, G., & Tamura, K., (2016). MEGA 7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874. https://doi.org/10.1093/molbev/msw054
  • Kurihara, Y., Takechi, T., & Shibata, F. (1978). Relationship between bacteria and ciliate protozoa in the rumen of sheep fed on a purified diet. The Journal of Agricultural Science, 90, 373–381. https://doi.org/10.1017/S0021859600055489
  • Lubinsky, G. (1957). Studies on the evolution of the Ophryoscolecidae III. Phylogeny of the Ophryoscolecidae based on their comparative morphology. Canadian Journal of Zoology, 35, 141–159. https://doi.org/10.1139/z57-009
  • Lynn, D. H. (2008). The ciliated protozoa: Characterization, classification and guide to the literature (3rd ed.). Springer.
  • Moon-van der Staay, S. Y., van der Staay, G. W. M., Michalowski, T., Jauany, J.-P., Pristas, P., Javorský, P., … & Hackstein, J. H. P. (2014). The symbiotic intestinal ciliates and the evolution of their hosts. European Journal of Protistology, 50, 166–173. https://doi.org/10.1016/j.ejop.2014.01.004
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There are 49 citations in total.

Details

Primary Language Turkish
Subjects Phylogeny and Comparative Analysis, Animal Systematics and Taxonomy
Journal Section Natural Sciences and Mathematics / Fen Bilimleri ve Matematik
Authors

Gözde Gürelli 0000-0001-7233-9060

Nuray Yürücüoğlu This is me 0009-0002-5530-6659

Publication Date August 31, 2024
Submission Date March 25, 2024
Acceptance Date June 7, 2024
Published in Issue Year 2024 Volume: 29 Issue: 2

Cite

APA Gürelli, G., & Yürücüoğlu, N. (2024). Antalya’daki Keçi ve Koyunların İşkembe Siliyat (Ciliophora, Trichostomatia) Faunası ve İşkembe Siliyatlarının Filogenisi. Yüzüncü Yıl Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 29(2), 429-437. https://doi.org/10.53433/yyufbed.1458622