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A Study on the Rumen Fermentation Characteristics and Rumen Ciliates of Fattened Cattle and Sheep Slaughtered in Van Province

Year 2025, Volume: 30 Issue: 1, 354 - 362, 29.04.2025

Muhammed Fatih Ceyhan , Sibel Erdoğan

https://doi.org/10.53433/yyufbed.1600490

Abstract

This study aimed to determine the occurrence percentages, total counts per milliliter, and rumen fermentation characteristics of rumen ciliates in the rumen of fattened cattle and lambs brought to a slaughterhouse in Van province. Accordingly, 10 fattened cattle with an average age of 24 months and 10 lambs with an average age of 8 months were used as animal material. During the postmortem examination of the selected animals, the abdominal region was opened, and the entire fore-stomachs were removed immediately. After separating the omasum and abomasum with a knife, rumen contents and rumen fluid samples were collected. Rumen NH₃-N concentrations were significantly higher in male lambs (P<0.05). The rumen acetate concentration was 67.72 mmol/L in fattened cattle and 61.12 mmol/L in male lambs (P<0.05). While the rumen propionate concentrations were similar in both species, the rumen butyrate concentration was higher in the rumen fluid of male lambs (P<0.05). Analyzing the numerical density of ciliates (x 10⁴ mL⁻¹) in the rumens of fattened cattle and lambs and the statistical results obtained through the Mann-Whitney U test, lambs exhibited lower ciliate density, whereas cattle demonstrated a significant advantage in this regard (P<0.005). In conclusion, based on the information gathered from interviews with animal owners, it was determined that the rumen fermentation characteristics rumen NH₃-N, acetic acid, and butyric acid concentrations were influenced by the composition of the ration in fattened lambs and cattle. The high proportion of grains in the fattening rations led to a higher prevalence of Entodinium sp., a member of the Entodiniomorphida family, in both cattle and lamb rumen.

Keywords

Cattle Rumen ciliates Rumen fermentation Sheep

Project Number

11270

References

  • Beal, A. M. (1974). A chronic re-entrant parotid duct cannula for long-term salivary collection and replacement in the sheep. Journal of Physiology, 242, 22-24
  • Church, D. C. (1993). The ruminant animal: Digestive physiology and nutrition. Prentice Hall.
  • Cao, Z., Yi, M., Zhou, J., Zhang, Z., Liu, Z., Yang, C., Sun, S., Wang, L., Ling, Y., Zhang, Z., & Cao, H. (2024). Multi-omics analysis on the mechanism of the effect of Isatis leaf on the growth performance of fattening sheep. Frontiers in Veterinary Science, 11, 1332457. https://doi.org/10.3389/fvets.2024.1332457
  • Coleman, G. S. (1992). The rate of uptake and metabolism of starch grains and cellulose particles by Entodinium species, Eudiplodinium maggii, some other entodiniomorphid protozoa and natural protozoal populations taken from the ovine rumen. Journal of Applied Bacteriology, 73(6), 507–513. https://doi.org/10.1111/j.1365-2672.1992.tb05013.x
  • Fluharty, F. L., & Dehority, B. A. (1996). Effects of sugar beet pulp and corn as energy supplements for cattle fed forage diets on diet digestibility and ruminal microorganisms. Special Circular-Ohio Agricultural Research and Development Center.
  • Gabler, M. T., & Heinrichs, A. J. (2003). Effects of increasing dietary protein on nutrient utilization in heifers. Journal of Dairy Science, 86(6), 2170-2177. https://doi.org/10.3168/jds.S0022-0302(03)73807-7
  • Göçmen, B., & Öktem, N. (1996). New rumen ciliates from Turkish domestic cattle (Bos taurus L.): I - The presence of Entodinium dalli Dehority, 1974 with a new forma, E. dalli f. rudidorsospinatum n.f. and comparisons with Entodinium williamsi n.sp. European Journal of Protistology, 32(4), 513-522. https://doi.org/10.1016/S0932-4739(96)80010-1
  • Harfoot, C. G., & Hazlewood, G. P. (1997). Lipid metabolism in the rumen. In P. N. Hobson & C. S. Stewart (Eds.), The rumen microbial ecosystem (2nd ed., pp. 140–197). Chapman & Hall.
  • Holder, V. B., El-Kadi, S. W., Tricarico, J. M., Vanzant, E. S., McLeod, K. R., & Harmon, D. L. (2013). The effects of crude protein concentration and slow release urea on nitrogen metabolism in Holstein steers. Archives of Animal Nutrition, 67(2), 93-103. https://doi.org/10.1080/1745039X.2013.773647
  • Imai, S. (1998). Phylogenetic taxonomy of rumen ciliate protozoa based on their morphology and distribution. Journal of Applied Animal Research, 13, 17–36. https://doi.org/10.1080/09712119.1998.9706670
  • Ismartoyo, I., Islamiyati, R., & Rusdy, M. (2023). Rumen fermentation of local grasses feed to native goat. Hasanuddin Journal of Animal Science (HAJAS), 5(1), 28-35. https://doi.org/10.20956/hajas.v5i1.24777
  • 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(3), 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
  • Jenkins, T. C., Wallace, R. J., Moate, P. J., & Mosley, E. E. (2008). Recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem. Journal of Animal Science, 86, 397-412. https://doi.org/10.2527/jas.2007-0588
  • Kamra, D. N. (2005). Rumen microbial ecosystem. Current Science, 89, 124-135.
  • Kaya, I., Unal, Y., Sahin, T., & Elmali, D. (2009). Effect of different protein levels on fattening performance, digestibility and rumen parameters in finishing lambs. J Anim Vet Adv, 8, 309-312.
  • Kiessling, K.-H., Pettersson, H., Sandholm, K., & Olsen, M. (1984). Metabolism of aflatoxin, ochratoxin, zeralenone, and three trichothecenes by intact rumen fluid, rumen protozoa, and rumen bacteria. Applied and Environmental Microbiology, 47, 1070-1073. https://doi.org/10.1128/aem.47.5.1070-1073.1984
  • Kreikemeier, K. K., Harmon, D. L., Brandt Jr, R. T., Nagaraja, T. G., & Cochran, R. C. (1990). Steam-rolled wheat diets for finishing cattle: Effects of dietary roughage and feed intake on finishing steer performance and ruminal metabolism. Journal of Animal Science, 68(7), 2130-2141.
  • Markham, P. (1942). A steam distillation apparatus suitable for micro-Kjeldahl analyses. Journal of Biochemistry, 36, 790-797. https://doi.org/10.1042/bj0360790
  • Nagaraja, T. G. (2016). Microbiology of the rumen. In Rumenology (pp. 39-61). Springer. https://doi.org/10.1007/978-3-319-30533-2_2
  • Newbold, C. J., de la Fuente, G., Belanche, A., Ramos-Morales, E., & McEwan, N. R. (2015). The role of ciliate protozoa in the rumen. Frontiers in Microbiology, 6, 1313. https://doi.org/10.3389/fmicb.2015.01313
  • Ogimoto, K., & Imai, S. (1981). Atlas of rumen microbiology. Japan Scientific Societies Press.
  • Park, T., Ma, L., Ma, Y., Zhou, X., Bu, D., & Yu, Z. (2020). Dietary energy sources and levels shift the multi-kingdom microbiota and functions in the rumen of lactating dairy cows. Journal of Animal Science and Biotechnology, 11, 1-16.
  • Patel, S., & Ambalam, P. (2018). Role of rumen protozoa: Metabolic and fibrolytic. Advances in Biotechnology & Microbiology, 10(4), 2474-7637.
  • Patterson, J. A. (1992). Rumen microbiology. In J. Lederberg (Ed.), Encyclopedia of microbiology (Vol. 3, pp. 623–542). Academic Press.
  • SAS Institute Inc. (2020). SAS/STAT software: Hangan and enhanced (Version 9.4). SAS Institute Inc.
  • Ushida, K., Jouany, J. P., Kayouli, C., & Demeyer, D. I. (1988). Effect of defaunation on fibre digestion in sheep fed ammonia-treated straw-based diets. In J. V. Nolaan, R. A. Leng, & D. I. Demeyer (Eds.), The role of protozoa and fungi in ruminant digestion (pp. 307–308). Penambul Books.
  • Ushida, K., Kayouli, C., De Smet, S., & Jouany, J. P. (1990). Effect of defaunation on protein and fibre digestion in sheep fed on ammonia-treated straw-based diets with or without maize. British Journal of Nutrition, 64(3), 765-775. https://doi.org/10.1079/BJN19900078
  • Ünay, E., Yaman, S., & Karakaş, V. (2008). Ruminantlarda selülozun sindirimi. Journal of Lalahan Livestock Research Institute, 48(2), 93-99.
  • Vargas, J. A. C., de Araújo, T. C., & Mezzomo, R. (2020). Extraction, identification, and quantification of volatile fatty acids (VFA) in rumen fluid samples using reverse phase high-performance liquid chromatography with diode array detector (RP HPLC-DAD). Research Square. https://doi.org/10.21203/rs.3.pex-1121/v1
  • Veira, D. M. (1986). The role of ciliate protozoa in nutrition of the ruminant. Journal of Animal Science, 63(5), 1547-1560. https://doi.org/10.2527/jas1986.6351547x
  • Xia, C., Rahman, M. A. U., Yang, H., Shao, T., Qiu, Q., Su, H., & Cao, B. (2018). Effect of increased dietary crude protein levels on production performance, nitrogen utilisation, blood metabolites and ruminal fermentation of Holstein bulls. Asian-Australasian Journal of Animal Sciences, 31(10), 1643. https://doi.org/10.5713/ajas.18.0125
  • Xie, F., Xu, L., Wang, Y., & Mao, S. (2021). Metagenomic sequencing reveals that high-grain feeding alters the composition and metabolism of cecal microbiota and induces cecal mucosal injury in sheep. Msystems, 6(5), e00915-21. https://doi.org/10.1128/msystems.00915-21
  • Xu, Y., Li, Z., Moraes, L. E., Shen, J., Yu, Z., & Zhu, W. (2019). Effects of incremental urea supplementation on rumen fermentation, nutrient digestion, plasma metabolites, and growth performance in fattening lambs. Animals, 9(9), 652. https://doi.org/10.3390/ani9090652
  • Wang, Y., Wang, Q., Dai, C., Li, J., Huang, P., Li, Y., Ding, X., Huang, J., Hussain, T., & Yang, H. (2020). Effects of dietary energy on growth performance, carcass characteristics, serum biochemical index, and meat quality of female Hu lambs. Animal Nutrition, 6(4), 499-506. https://doi.org/10.1016/j.aninu.2020.05.008
  • Williams, A. G., Coleman, G. S., Williams, A. G., & Coleman, G. S. (1992). Role of protozoa in the rumen. In The rumen protozoa (pp. 317–347). Brock/Springer.
  • Yoshida, J., Nakamura, Y., & Nakamura, R. (1982). Effects of protozoal fraction and lactate on nitrate metabolism of microorganisms in sheep rumen. Nihon Chikusan Gakkaiho, 53, 677-685.

Van ilinde Kesilen Besi Sığırları ile Koyunların Rumen Fermentasyon Özellikleri ve Rumen Siliyatları Üzerine Bir Çalışma

Year 2025, Volume: 30 Issue: 1, 354 - 362, 29.04.2025

Muhammed Fatih Ceyhan , Sibel Erdoğan

https://doi.org/10.53433/yyufbed.1600490

Abstract

Bu çalışma, Van ilindeki bir kesimhaneye getirilen besi sığırları ve tokluların rumenlerinde yaşayan rumen siliyatlarının bulunuş yüzdelerini, mililitre başına toplam sayılarını ve rumen fermentasyon özelliklerini belirlemek amacıyla gerçekleştirilmiştir. Bu doğrultuda, 10 baş ortalama 24 aylık besi sığırı ile 10 baş ortalama 8 aylık toklu hayvan materyal olarak kullanılmıştır. Seçilen hayvanların postmortem muayenesi sırasında abdominal bölge açıldıktan hemen sonra ön mideler tamamen çıkarılmış; omasum ve abomasum bıçak yardımıyla ayrıldıktan sonra rumen içeriği ve rumen sıvısı örnekleri alınmıştır. Rumen NH₃-N konsantrasyonları, erkek kuzularda anlamlı derecede daha yüksek bulunmuştur (P<0.05). Rumen asetat konsantrasyonu, besi sığırlarında 67.72 mmol/L iken, erkek kuzularda 61.12 mmol/L olarak saptanmıştır (P<0.05). Her iki türde rumen propiyonat konsantrasyonu benzerlik gösterirken, rumen bütirat konsantrasyonu erkek kuzuların rumen sıvısında daha yüksek tespit edilmiştir (P<0.05). Besi sığırları ve erkek kuzuların rumenlerinde bulunan siliyatların sayısal yoğunluğu (x 10⁴ mL⁻¹) ve Mann-Whitney U testi ile elde edilen istatistiksel sonuçlar incelendiğinde, kuzuların daha düşük siliyat yoğunluğuna sahip olduğu, sığırların ise bu konuda belirgin bir üstünlük sergilediği ortaya konulmuştur (P<0.005). Sonuç olarak, hayvan sahipleriyle yapılan görüşmeler sonucunda elde edilen bilgilere dayanarak, besi yapılan kuzu ve sığırların rumen fermentasyon özelliklerinden NH₃-N konsantrasyonu, asetik asit ve bütirik asit konsantrasyonlarının rasyon bileşimlerinden etkilendiği belirlenmiştir. Besi rasyonlarında dane yem oranının yüksek olması hem sığırlarda hem de kuzularda Entodiniomorphida familyasından Entodinium sp.'nin yoğun olarak bulunmasına neden olmuştur.

Keywords

Koyun Rumen fermentasyonu Rumen siliyatları Sığır

Ethical Statement

Proje Van İli kesimhanesinde kesilen ve ölmüş hayvanlarda yapıldığı için etik kurul gerekmemektedir.

Supporting Institution

TÜBİTAK 2209-A

Project Number

11270

Thanks

Bu araştırma makalesi TUBİTAK 2209- A Üniversite Öğrencileri Araştırma Projeleri Destekleme Programı 2022/2 kapsamında 11270 nolu proje ile desteklenmiş olup finansal destek için TÜBİTAK’a teşekkür ederiz.

References

  • Beal, A. M. (1974). A chronic re-entrant parotid duct cannula for long-term salivary collection and replacement in the sheep. Journal of Physiology, 242, 22-24
  • Church, D. C. (1993). The ruminant animal: Digestive physiology and nutrition. Prentice Hall.
  • Cao, Z., Yi, M., Zhou, J., Zhang, Z., Liu, Z., Yang, C., Sun, S., Wang, L., Ling, Y., Zhang, Z., & Cao, H. (2024). Multi-omics analysis on the mechanism of the effect of Isatis leaf on the growth performance of fattening sheep. Frontiers in Veterinary Science, 11, 1332457. https://doi.org/10.3389/fvets.2024.1332457
  • Coleman, G. S. (1992). The rate of uptake and metabolism of starch grains and cellulose particles by Entodinium species, Eudiplodinium maggii, some other entodiniomorphid protozoa and natural protozoal populations taken from the ovine rumen. Journal of Applied Bacteriology, 73(6), 507–513. https://doi.org/10.1111/j.1365-2672.1992.tb05013.x
  • Fluharty, F. L., & Dehority, B. A. (1996). Effects of sugar beet pulp and corn as energy supplements for cattle fed forage diets on diet digestibility and ruminal microorganisms. Special Circular-Ohio Agricultural Research and Development Center.
  • Gabler, M. T., & Heinrichs, A. J. (2003). Effects of increasing dietary protein on nutrient utilization in heifers. Journal of Dairy Science, 86(6), 2170-2177. https://doi.org/10.3168/jds.S0022-0302(03)73807-7
  • Göçmen, B., & Öktem, N. (1996). New rumen ciliates from Turkish domestic cattle (Bos taurus L.): I - The presence of Entodinium dalli Dehority, 1974 with a new forma, E. dalli f. rudidorsospinatum n.f. and comparisons with Entodinium williamsi n.sp. European Journal of Protistology, 32(4), 513-522. https://doi.org/10.1016/S0932-4739(96)80010-1
  • Harfoot, C. G., & Hazlewood, G. P. (1997). Lipid metabolism in the rumen. In P. N. Hobson & C. S. Stewart (Eds.), The rumen microbial ecosystem (2nd ed., pp. 140–197). Chapman & Hall.
  • Holder, V. B., El-Kadi, S. W., Tricarico, J. M., Vanzant, E. S., McLeod, K. R., & Harmon, D. L. (2013). The effects of crude protein concentration and slow release urea on nitrogen metabolism in Holstein steers. Archives of Animal Nutrition, 67(2), 93-103. https://doi.org/10.1080/1745039X.2013.773647
  • Imai, S. (1998). Phylogenetic taxonomy of rumen ciliate protozoa based on their morphology and distribution. Journal of Applied Animal Research, 13, 17–36. https://doi.org/10.1080/09712119.1998.9706670
  • Ismartoyo, I., Islamiyati, R., & Rusdy, M. (2023). Rumen fermentation of local grasses feed to native goat. Hasanuddin Journal of Animal Science (HAJAS), 5(1), 28-35. https://doi.org/10.20956/hajas.v5i1.24777
  • 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(3), 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
  • Jenkins, T. C., Wallace, R. J., Moate, P. J., & Mosley, E. E. (2008). Recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem. Journal of Animal Science, 86, 397-412. https://doi.org/10.2527/jas.2007-0588
  • Kamra, D. N. (2005). Rumen microbial ecosystem. Current Science, 89, 124-135.
  • Kaya, I., Unal, Y., Sahin, T., & Elmali, D. (2009). Effect of different protein levels on fattening performance, digestibility and rumen parameters in finishing lambs. J Anim Vet Adv, 8, 309-312.
  • Kiessling, K.-H., Pettersson, H., Sandholm, K., & Olsen, M. (1984). Metabolism of aflatoxin, ochratoxin, zeralenone, and three trichothecenes by intact rumen fluid, rumen protozoa, and rumen bacteria. Applied and Environmental Microbiology, 47, 1070-1073. https://doi.org/10.1128/aem.47.5.1070-1073.1984
  • Kreikemeier, K. K., Harmon, D. L., Brandt Jr, R. T., Nagaraja, T. G., & Cochran, R. C. (1990). Steam-rolled wheat diets for finishing cattle: Effects of dietary roughage and feed intake on finishing steer performance and ruminal metabolism. Journal of Animal Science, 68(7), 2130-2141.
  • Markham, P. (1942). A steam distillation apparatus suitable for micro-Kjeldahl analyses. Journal of Biochemistry, 36, 790-797. https://doi.org/10.1042/bj0360790
  • Nagaraja, T. G. (2016). Microbiology of the rumen. In Rumenology (pp. 39-61). Springer. https://doi.org/10.1007/978-3-319-30533-2_2
  • Newbold, C. J., de la Fuente, G., Belanche, A., Ramos-Morales, E., & McEwan, N. R. (2015). The role of ciliate protozoa in the rumen. Frontiers in Microbiology, 6, 1313. https://doi.org/10.3389/fmicb.2015.01313
  • Ogimoto, K., & Imai, S. (1981). Atlas of rumen microbiology. Japan Scientific Societies Press.
  • Park, T., Ma, L., Ma, Y., Zhou, X., Bu, D., & Yu, Z. (2020). Dietary energy sources and levels shift the multi-kingdom microbiota and functions in the rumen of lactating dairy cows. Journal of Animal Science and Biotechnology, 11, 1-16.
  • Patel, S., & Ambalam, P. (2018). Role of rumen protozoa: Metabolic and fibrolytic. Advances in Biotechnology & Microbiology, 10(4), 2474-7637.
  • Patterson, J. A. (1992). Rumen microbiology. In J. Lederberg (Ed.), Encyclopedia of microbiology (Vol. 3, pp. 623–542). Academic Press.
  • SAS Institute Inc. (2020). SAS/STAT software: Hangan and enhanced (Version 9.4). SAS Institute Inc.
  • Ushida, K., Jouany, J. P., Kayouli, C., & Demeyer, D. I. (1988). Effect of defaunation on fibre digestion in sheep fed ammonia-treated straw-based diets. In J. V. Nolaan, R. A. Leng, & D. I. Demeyer (Eds.), The role of protozoa and fungi in ruminant digestion (pp. 307–308). Penambul Books.
  • Ushida, K., Kayouli, C., De Smet, S., & Jouany, J. P. (1990). Effect of defaunation on protein and fibre digestion in sheep fed on ammonia-treated straw-based diets with or without maize. British Journal of Nutrition, 64(3), 765-775. https://doi.org/10.1079/BJN19900078
  • Ünay, E., Yaman, S., & Karakaş, V. (2008). Ruminantlarda selülozun sindirimi. Journal of Lalahan Livestock Research Institute, 48(2), 93-99.
  • Vargas, J. A. C., de Araújo, T. C., & Mezzomo, R. (2020). Extraction, identification, and quantification of volatile fatty acids (VFA) in rumen fluid samples using reverse phase high-performance liquid chromatography with diode array detector (RP HPLC-DAD). Research Square. https://doi.org/10.21203/rs.3.pex-1121/v1
  • Veira, D. M. (1986). The role of ciliate protozoa in nutrition of the ruminant. Journal of Animal Science, 63(5), 1547-1560. https://doi.org/10.2527/jas1986.6351547x
  • Xia, C., Rahman, M. A. U., Yang, H., Shao, T., Qiu, Q., Su, H., & Cao, B. (2018). Effect of increased dietary crude protein levels on production performance, nitrogen utilisation, blood metabolites and ruminal fermentation of Holstein bulls. Asian-Australasian Journal of Animal Sciences, 31(10), 1643. https://doi.org/10.5713/ajas.18.0125
  • Xie, F., Xu, L., Wang, Y., & Mao, S. (2021). Metagenomic sequencing reveals that high-grain feeding alters the composition and metabolism of cecal microbiota and induces cecal mucosal injury in sheep. Msystems, 6(5), e00915-21. https://doi.org/10.1128/msystems.00915-21
  • Xu, Y., Li, Z., Moraes, L. E., Shen, J., Yu, Z., & Zhu, W. (2019). Effects of incremental urea supplementation on rumen fermentation, nutrient digestion, plasma metabolites, and growth performance in fattening lambs. Animals, 9(9), 652. https://doi.org/10.3390/ani9090652
  • Wang, Y., Wang, Q., Dai, C., Li, J., Huang, P., Li, Y., Ding, X., Huang, J., Hussain, T., & Yang, H. (2020). Effects of dietary energy on growth performance, carcass characteristics, serum biochemical index, and meat quality of female Hu lambs. Animal Nutrition, 6(4), 499-506. https://doi.org/10.1016/j.aninu.2020.05.008
  • Williams, A. G., Coleman, G. S., Williams, A. G., & Coleman, G. S. (1992). Role of protozoa in the rumen. In The rumen protozoa (pp. 317–347). Brock/Springer.
  • Yoshida, J., Nakamura, Y., & Nakamura, R. (1982). Effects of protozoal fraction and lactate on nitrate metabolism of microorganisms in sheep rumen. Nihon Chikusan Gakkaiho, 53, 677-685.
There are 37 citations in total.

Details

Primary Language Turkish
Subjects Animal Feeding
Journal Section Agriculture / Zirai Bilimler
Authors

Muhammed Fatih Ceyhan 0009-0005-1951-4487

Sibel Erdoğan 0000-0003-2640-3871

Project Number 11270
Publication Date April 29, 2025
Submission Date December 12, 2024
Acceptance Date February 20, 2025
Published in Issue Year 2025 Volume: 30 Issue: 1

Cite

APA Ceyhan, M. F., & Erdoğan, S. (2025). Van ilinde Kesilen Besi Sığırları ile Koyunların Rumen Fermentasyon Özellikleri ve Rumen Siliyatları Üzerine Bir Çalışma. Yüzüncü Yıl Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 30(1), 354-362. https://doi.org/10.53433/yyufbed.1600490
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