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Hyalomma marginatum (Koch, 1844) (Acari: İxodidae)’un Ovaryumunun Histolojik Yapısı

Year 2021, , 25 - 34, 24.02.2021
https://doi.org/10.35414/akufemubid.708448

Abstract

Hyalomma marginatum’un ovaryumu ve ovogenez süreci ilk kez bu çalışmada ışık mikroskobu düzeyinde histolojik ve histokimyasal olarak incelenmiştir. Ovaryum nurse ve folikül hücrelerinden yoksundur ve bu nedenle panoistik olarak tanımlanmıştır. İçi boş tübül biçimindeki ovaryumun duvarı tek sıra epitel hücrelerinden ve gelişmekte olan ovositlerden oluşur. Ovositler bir pedisel ile hemosöle bakacak şekilde ovaryum duvarına bağlıdır. Sitoplazmanın görünüşü, germinal vesikülün varlığı, yumurta sarısı granüllerinin bileşimi ve koryonun oluşumuna göre gelişmekte olan ovositler sınıflandırılmış ve dört evre tanımlanmıştır. Olgun ovositler küresele yakın eliptik şekilli olup, en büyük ovosit 315x295 µm çapındadır. Protein ve karbonhidratların varlığını gösteren boyama teknikleri bu kene türünde, yumurta sarısı granüllerinde hem proteinlerin hem de karbonhidratların bulunduğunu, vitellogenezde karbonhidratların proteinlerden önce sentezlendiğini ve koryonda karbonhidratların baskın olduğunu göstermiştir. Çok yaygın olmasa da ovaryumda ovosit yozlaşması gözlenmiştir.

Thanks

Kene örneklerimizi toplayan ve teşhisini yapan bölümümüz öğretim üyesi Doç. Dr. Sırrı Kar’a teşekkür ederiz.

References

  • Anderson, J.F. ve Magnarelli, L.A. 2008. Biology of ticks. Infectious Disease Clinics of North America, 22, 195-215.
  • Bakırcı, S., Sarali, H., Aydın, L., Latif, A., Eren, H. ve Karagenç, T. 2011. Hyalomma rufipes (Koch, 1844) infesting cattle in the West Aegean region of Turkey. Turkish Journal of Veterinary and Animal Sciences, 35(5), 359-363.
  • Bancroft, J.D. ve Gamble, M. 2001. Theory and practice of histological techniques, 5th ed., Churchill Livingstone, 800 sayfa.
  • de Oliveira, P.R., Bechara, G.H., Denardi, S.E., Nunes, E.T. ve Camargo Mathias, M.I. 2005. Morphological characterization of the ovary and oocytes vitellogenesis of the tick Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae). Experimental Parasitology, 110(2), 146-156.
  • de Oliveira, P.R., Camargo Mathias, M.I. ve Bechara, G.H. 2006. Amblyomma triste (Koch, 1844) (Acari: Ixodidae): Morphological description of the ovary and of vitellogenesis. Experimental Parasitology, 113, 179-185.
  • de Oliveira, P.R., Bechara, G.H. ve Camargo Mathias, M.I. 2007. Amblyomma triste (Koch, 1844) (Acari: Ixodidae) ovaries: An ultrastructural analysis. Experimental Parasitology, 116, 407-413.
  • de Oliveira, P.R., Anholeto, L.A., Ferreira Rodrigues, R.A., Arnosti, A., Bechara, G.H., de Carvalho Castro, K.N. ve Camargo-Mathias, M.I. 2019. Cytotoxic effects of extract of Acmella oleracea in the ovaries and midgut of Rhipicephalus sanguineus Latreille, 1806 (Acari: Ixodidae) female ticks. Journal of Microscopy and Ultrastructure, 7(1), 28-43.
  • Denardi, S.E., Bechara, G.H., Oliveira, P.R., Nunes, E.T., Saito, K.C. ve Mathias, M.I. 2004. Morphological characterization of the ovary and vitellogenesis dynamics in the tick Amblyomma cajennense (Acari: Ixodidae). Veterinary Parasitology, 125, 379-395.
  • Diehl, P.A., Aeschlimann, A. ve Obenchain, F.D. 1982. Chapter 9: Tick reproduction: oogenesis and oviposition, Physiology of Ticks, (Current Themes in Tropical Science, Volume 1), Ed: F.D. Obenchain, R. Galun, Pergamon Press, Oxford, 277-350.
  • Edwards, K.T., Goddard, J. ve Varela-Stokes, A.S. 2009. Examination of the internal morphology of the ixodid tick, Amblyomma maculatum Koch, (Acari: Ixodidae); a “How-to” Pictorial Dissection Guide. Midsouth Entomologist, 2, 28-39.
  • Ergonul, O. 2006. Crimean-Congo haemorrhagic fever. Lancet Infectious Diseases, 6, 203-214.
  • Estrada-Peña, A. ve Jongejan, F. 1999. Ticks feeding on humans: A review of records on human-biting Ixodoidea with special reference to pathogen transmission. Experimental and Applied Acarology, 23, 685-715.
  • Gargılı, A., Kar, S., Yılmazer, N., Cerit, Ç., Sönmez, G., Şahin, F., Günseli Alp, H. ve Vatansever, Z. 2010. Evaluation of ticks biting humans in Thrace province, Turkey. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 16(Suppl-A), 141-146.
  • Gargili, A., Thangamani, S. ve Bente, D. 2013. Influence of laboratory animal hosts on the life cycle of Hyalomma marginatum and implications for an in vivo transmission model for Crimean-Congo hemorrhagic fever virus. Frontiers in Cellular and Infection Microbiology, Volume 3, Article 39.
  • Ghosh, S., Azhahianambi, P. ve Yadav, M.P. 2007. Upcoming and future strategies of tick control: a rewiew. Journal of Vector Borne Diseases, 44, 79-89.
  • Gullan, P.J. ve Cranston, P.S. 2005. The insects: An outline of entomology, 4th Edition, Blackwell Publishing Ltd, USA, 505 sayfa.
  • Güler, S. 1982. Ankara ve civarındaki koyun ve keçilerde kış ixodidaeleri üzerine araştırmalar. Uludağ Üniversitesi Veteriner Fakültesi Dergisi, 1, 45-54.
  • Güler, S., Özer, E., Erdoğmuş, S.Z., Köroğlu, E. ve Bektaş, İ. 1993. Malatya ve bazı Güneydoğu Anadolu illerinde sığır, koyun ve keçilerde bulunan kene (Ixodidea) türleri. Doğa Turkish Journal of Veterinary and Animal Sciences, 17, 229-231.
  • Jameson, L.J., Morgan, P.J., Medlock, J.M., Watola, G. ve Vauxa, A.G. 2012. Importation of Hyalomma marginatum, vector of Crimean-Congo haemorrhagic fever virus, into the United Kingdom by migratory birds. Ticks and Tick-borne Diseases, 3, 95-99.
  • Jongejan, F. ve Uilenberg, G. 2004. The global importance of ticks. Parasitolology, 129, 3-14.
  • Kanapadinchareveetil, S., Chandrasekhar, L., Gopi, J., Lenka, D.R., Vasu, A., KGopalan, A.K., Nair, S.N., Ravindran, R., Juliet, S. ve Ghosh, S. 2015. Histoarchitecture of the ovary of Rhipicephalus (Boophilus) annulatus during pre- and postengorgement period. The Scientific World Journal, 126584.
  • Kanapadinchareveetil S, Chandrasekhar L, Pious A, Kartha HS, Ravindran R, Juliet S, Nair SN, Ajithkumar KG, Ghosh S. 2019. Molecular, histological and ultrastructural characterization of cytotoxic effects of amitraz on the ovaries of engorged females of Rhipicephalus (Boophilus) annulatus. Experimental Parasitology, 204, 107732.
  • Koniga, I.F.M., Gonçalves, R.R.P., Oliveira, M.V.S., Silva, C.M., Thomasi, S.S., Peconick, A.P. ve Remedio, R.N. 2019. Sublethal concentrations of acetylcarvacrol strongly impact oocyte development of engorged female cattle ticks Rhipicephalus microplus (Canestrini, 1888) (Acari: Ixodidae). Ticks and Tick-borne Diseases, 10, 766-774.
  • Labuda, M. ve Nuttall, P.A. 2004. Tick-borne viruses. Parasitology, 129, 221-245.
  • Mihara, R., Umemiya-Shirafuji, R., Abe, Y., Matsuo, T., Horiuchi, N., Kawano, S., Fujisaki, K. ve Suzuki, H. 2018. The development of oocytes in the ovary of a parthenogenetic tick, Haemaphysalis longicornis. Parasitology International, 67(4), 465-471.
  • Pearse, A.G.E. 1985. Histochemistry theoretical and applied. Livingstone, Churchill, 123-214.
  • Ricardo, A.J., de Oliveira, P.R., Bechara, G.H. ve Mathias, M.I. 2007. Ultrastructural detection of proteins, lipids and carbohydrates in oocytes of Amblyomma triste (Koch, 1844) (Acari; Ixodidae) during the vitellogenesis process. Tissue and Cell, 39, 203-215.
  • Rymaszewska, A. 2007. Symbiotic bacteria in oocyte and ovarian cell mitochondria of the tick Ixodes ricinus: biology and phylogenetic position. Parasitology Research, 100, 917-920.
  • Saito, K.C., Bechara, G.H., Nunes, E.T., de Oliveira, P.R., Denardi, S.E. ve Camargo Mathias, M.I. 2005. Morphological, histological, and ultrastructural studies of the ovary of the cattle-tick Boophilus microplus (Canestrini, 1887) (Acari: Ixodidae). Veterinary Parasitology, 129, 299-311.
  • Sanches, G.S., Bechara, G.H. ve Camargo Mathias, M.I. 2010. Ovary and oocyte maturation of the tick Amblyomma brasiliense Aragão, 1908 (Acari: Ixodidae). Micron, 41, 84-89.
  • Sanches, G.S., Araujo, A.M., Martins, T.F., Bechara, G.H., Labruna, M.B., Camargo Mathias, M.I. 2012. Morphological records of oocyte maturation in the parthenogenetic tick Amblyomma rotundatum Koch, 1844 (Acari: Ixodidae). Ticks and Tick-borne Diseases, 3, 59-64.
  • Sonenshine, D.E. ve Roe, R.M. 2014. Biology of ticks, Volume 1, Second Edition. Oxford University Press, New York, 560 sayfa.
  • Sreelekha, K.P., Chandrasekhar, L., Jyothimol, G., Lenka, D.R., Aswathi, V., Adarshkrishna, T.P., Ajithkumar, K.G., Nair, S.N., Ravindran, R., Juliet, S. ve Ghosh, S. 2015. Histoarchitecture of ovary of Haemaphysalis bispinosa during engorgement period. Tropical Biomedicine, 32(3), 497-503.
  • Wourms, J.P. 1987. Oogenesis. Reproduction of marine invertebrates. Vol. IX. General aspects: seeking unity in diversity, Ed: A.C. Giese, J.S. Pearse, V.B. Pearse, Blackwell Scientific Publications, the Boxwood Press, 50-157.
  • Yaman, E. 2014. Hyalomma marginatum (Koch, 1844) (Acari: İxodidae)’un ovaryumunun histolojik yapısı. Yüksek lisans tezi, Fen Bilimleri Enstitüsü, Tekirdağ Namık Kemal Üniversitesi, 57 sayfa.
  • Yılmazer, N. 2018. The genome size of some species of Hyalomma ticks from Turkish Thrace. Systematic and Applied Acarology, 23(11), 2122-2128.
  • Yukarı, B.A., Nalbantoğlu, S., Karaer, Z., İnci, A., Eren, H. ve Sayın, F. 2011. Laboratuvarda Hyalomma marginatum’un bazı biyolojik özellikleri. Türkiye Parazitoloji Dergisi, 35, 40-42.

Histological Structure of the Ovary of Hyalomma marginatum (Koch, 1844) (Acari: Ixodidae)

Year 2021, , 25 - 34, 24.02.2021
https://doi.org/10.35414/akufemubid.708448

Abstract

With this study, the ovary and oogenesis in Hyalomma marginatum were histologically and histochemically examined at light microscope level for the first time. The ovary lacks nurse and follicular cells, thus defined as panoistic type. Wall of the ovary, a hollow tubular structure, is composed of a layer of epithelial cells and developing oocytes. Facing hemocoel, oocytes are attached to the ovarian wall through a pedicel. The developing oocytes were classified according to cytoplasm appearance, presence of germinal vesicle, constitution of yolk granules, and formation of chorion, and accordingly four developmental stages were described. Mature oocytes were oval to rounded in shape, the largest one being 315x295 µm in diameter. Staining techniques revealing the presence of proteins and carbohydrates indicate in this tick species that yolk granules contain both proteins and carbohydrates, that carbohydrates are first to be synthesized prior to proteins during vitellogenesis, and that carbohydrates predominate in chorion. Oocyte degeneration was observed although it was not so common in the ovary.

References

  • Anderson, J.F. ve Magnarelli, L.A. 2008. Biology of ticks. Infectious Disease Clinics of North America, 22, 195-215.
  • Bakırcı, S., Sarali, H., Aydın, L., Latif, A., Eren, H. ve Karagenç, T. 2011. Hyalomma rufipes (Koch, 1844) infesting cattle in the West Aegean region of Turkey. Turkish Journal of Veterinary and Animal Sciences, 35(5), 359-363.
  • Bancroft, J.D. ve Gamble, M. 2001. Theory and practice of histological techniques, 5th ed., Churchill Livingstone, 800 sayfa.
  • de Oliveira, P.R., Bechara, G.H., Denardi, S.E., Nunes, E.T. ve Camargo Mathias, M.I. 2005. Morphological characterization of the ovary and oocytes vitellogenesis of the tick Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae). Experimental Parasitology, 110(2), 146-156.
  • de Oliveira, P.R., Camargo Mathias, M.I. ve Bechara, G.H. 2006. Amblyomma triste (Koch, 1844) (Acari: Ixodidae): Morphological description of the ovary and of vitellogenesis. Experimental Parasitology, 113, 179-185.
  • de Oliveira, P.R., Bechara, G.H. ve Camargo Mathias, M.I. 2007. Amblyomma triste (Koch, 1844) (Acari: Ixodidae) ovaries: An ultrastructural analysis. Experimental Parasitology, 116, 407-413.
  • de Oliveira, P.R., Anholeto, L.A., Ferreira Rodrigues, R.A., Arnosti, A., Bechara, G.H., de Carvalho Castro, K.N. ve Camargo-Mathias, M.I. 2019. Cytotoxic effects of extract of Acmella oleracea in the ovaries and midgut of Rhipicephalus sanguineus Latreille, 1806 (Acari: Ixodidae) female ticks. Journal of Microscopy and Ultrastructure, 7(1), 28-43.
  • Denardi, S.E., Bechara, G.H., Oliveira, P.R., Nunes, E.T., Saito, K.C. ve Mathias, M.I. 2004. Morphological characterization of the ovary and vitellogenesis dynamics in the tick Amblyomma cajennense (Acari: Ixodidae). Veterinary Parasitology, 125, 379-395.
  • Diehl, P.A., Aeschlimann, A. ve Obenchain, F.D. 1982. Chapter 9: Tick reproduction: oogenesis and oviposition, Physiology of Ticks, (Current Themes in Tropical Science, Volume 1), Ed: F.D. Obenchain, R. Galun, Pergamon Press, Oxford, 277-350.
  • Edwards, K.T., Goddard, J. ve Varela-Stokes, A.S. 2009. Examination of the internal morphology of the ixodid tick, Amblyomma maculatum Koch, (Acari: Ixodidae); a “How-to” Pictorial Dissection Guide. Midsouth Entomologist, 2, 28-39.
  • Ergonul, O. 2006. Crimean-Congo haemorrhagic fever. Lancet Infectious Diseases, 6, 203-214.
  • Estrada-Peña, A. ve Jongejan, F. 1999. Ticks feeding on humans: A review of records on human-biting Ixodoidea with special reference to pathogen transmission. Experimental and Applied Acarology, 23, 685-715.
  • Gargılı, A., Kar, S., Yılmazer, N., Cerit, Ç., Sönmez, G., Şahin, F., Günseli Alp, H. ve Vatansever, Z. 2010. Evaluation of ticks biting humans in Thrace province, Turkey. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 16(Suppl-A), 141-146.
  • Gargili, A., Thangamani, S. ve Bente, D. 2013. Influence of laboratory animal hosts on the life cycle of Hyalomma marginatum and implications for an in vivo transmission model for Crimean-Congo hemorrhagic fever virus. Frontiers in Cellular and Infection Microbiology, Volume 3, Article 39.
  • Ghosh, S., Azhahianambi, P. ve Yadav, M.P. 2007. Upcoming and future strategies of tick control: a rewiew. Journal of Vector Borne Diseases, 44, 79-89.
  • Gullan, P.J. ve Cranston, P.S. 2005. The insects: An outline of entomology, 4th Edition, Blackwell Publishing Ltd, USA, 505 sayfa.
  • Güler, S. 1982. Ankara ve civarındaki koyun ve keçilerde kış ixodidaeleri üzerine araştırmalar. Uludağ Üniversitesi Veteriner Fakültesi Dergisi, 1, 45-54.
  • Güler, S., Özer, E., Erdoğmuş, S.Z., Köroğlu, E. ve Bektaş, İ. 1993. Malatya ve bazı Güneydoğu Anadolu illerinde sığır, koyun ve keçilerde bulunan kene (Ixodidea) türleri. Doğa Turkish Journal of Veterinary and Animal Sciences, 17, 229-231.
  • Jameson, L.J., Morgan, P.J., Medlock, J.M., Watola, G. ve Vauxa, A.G. 2012. Importation of Hyalomma marginatum, vector of Crimean-Congo haemorrhagic fever virus, into the United Kingdom by migratory birds. Ticks and Tick-borne Diseases, 3, 95-99.
  • Jongejan, F. ve Uilenberg, G. 2004. The global importance of ticks. Parasitolology, 129, 3-14.
  • Kanapadinchareveetil, S., Chandrasekhar, L., Gopi, J., Lenka, D.R., Vasu, A., KGopalan, A.K., Nair, S.N., Ravindran, R., Juliet, S. ve Ghosh, S. 2015. Histoarchitecture of the ovary of Rhipicephalus (Boophilus) annulatus during pre- and postengorgement period. The Scientific World Journal, 126584.
  • Kanapadinchareveetil S, Chandrasekhar L, Pious A, Kartha HS, Ravindran R, Juliet S, Nair SN, Ajithkumar KG, Ghosh S. 2019. Molecular, histological and ultrastructural characterization of cytotoxic effects of amitraz on the ovaries of engorged females of Rhipicephalus (Boophilus) annulatus. Experimental Parasitology, 204, 107732.
  • Koniga, I.F.M., Gonçalves, R.R.P., Oliveira, M.V.S., Silva, C.M., Thomasi, S.S., Peconick, A.P. ve Remedio, R.N. 2019. Sublethal concentrations of acetylcarvacrol strongly impact oocyte development of engorged female cattle ticks Rhipicephalus microplus (Canestrini, 1888) (Acari: Ixodidae). Ticks and Tick-borne Diseases, 10, 766-774.
  • Labuda, M. ve Nuttall, P.A. 2004. Tick-borne viruses. Parasitology, 129, 221-245.
  • Mihara, R., Umemiya-Shirafuji, R., Abe, Y., Matsuo, T., Horiuchi, N., Kawano, S., Fujisaki, K. ve Suzuki, H. 2018. The development of oocytes in the ovary of a parthenogenetic tick, Haemaphysalis longicornis. Parasitology International, 67(4), 465-471.
  • Pearse, A.G.E. 1985. Histochemistry theoretical and applied. Livingstone, Churchill, 123-214.
  • Ricardo, A.J., de Oliveira, P.R., Bechara, G.H. ve Mathias, M.I. 2007. Ultrastructural detection of proteins, lipids and carbohydrates in oocytes of Amblyomma triste (Koch, 1844) (Acari; Ixodidae) during the vitellogenesis process. Tissue and Cell, 39, 203-215.
  • Rymaszewska, A. 2007. Symbiotic bacteria in oocyte and ovarian cell mitochondria of the tick Ixodes ricinus: biology and phylogenetic position. Parasitology Research, 100, 917-920.
  • Saito, K.C., Bechara, G.H., Nunes, E.T., de Oliveira, P.R., Denardi, S.E. ve Camargo Mathias, M.I. 2005. Morphological, histological, and ultrastructural studies of the ovary of the cattle-tick Boophilus microplus (Canestrini, 1887) (Acari: Ixodidae). Veterinary Parasitology, 129, 299-311.
  • Sanches, G.S., Bechara, G.H. ve Camargo Mathias, M.I. 2010. Ovary and oocyte maturation of the tick Amblyomma brasiliense Aragão, 1908 (Acari: Ixodidae). Micron, 41, 84-89.
  • Sanches, G.S., Araujo, A.M., Martins, T.F., Bechara, G.H., Labruna, M.B., Camargo Mathias, M.I. 2012. Morphological records of oocyte maturation in the parthenogenetic tick Amblyomma rotundatum Koch, 1844 (Acari: Ixodidae). Ticks and Tick-borne Diseases, 3, 59-64.
  • Sonenshine, D.E. ve Roe, R.M. 2014. Biology of ticks, Volume 1, Second Edition. Oxford University Press, New York, 560 sayfa.
  • Sreelekha, K.P., Chandrasekhar, L., Jyothimol, G., Lenka, D.R., Aswathi, V., Adarshkrishna, T.P., Ajithkumar, K.G., Nair, S.N., Ravindran, R., Juliet, S. ve Ghosh, S. 2015. Histoarchitecture of ovary of Haemaphysalis bispinosa during engorgement period. Tropical Biomedicine, 32(3), 497-503.
  • Wourms, J.P. 1987. Oogenesis. Reproduction of marine invertebrates. Vol. IX. General aspects: seeking unity in diversity, Ed: A.C. Giese, J.S. Pearse, V.B. Pearse, Blackwell Scientific Publications, the Boxwood Press, 50-157.
  • Yaman, E. 2014. Hyalomma marginatum (Koch, 1844) (Acari: İxodidae)’un ovaryumunun histolojik yapısı. Yüksek lisans tezi, Fen Bilimleri Enstitüsü, Tekirdağ Namık Kemal Üniversitesi, 57 sayfa.
  • Yılmazer, N. 2018. The genome size of some species of Hyalomma ticks from Turkish Thrace. Systematic and Applied Acarology, 23(11), 2122-2128.
  • Yukarı, B.A., Nalbantoğlu, S., Karaer, Z., İnci, A., Eren, H. ve Sayın, F. 2011. Laboratuvarda Hyalomma marginatum’un bazı biyolojik özellikleri. Türkiye Parazitoloji Dergisi, 35, 40-42.
There are 37 citations in total.

Details

Primary Language Turkish
Subjects Engineering
Journal Section Articles
Authors

Elif Yaman

Nadim Yılmazer 0000-0002-9935-9608

Publication Date February 24, 2021
Submission Date March 25, 2020
Published in Issue Year 2021

Cite

APA Yaman, E., & Yılmazer, N. (2021). Hyalomma marginatum (Koch, 1844) (Acari: İxodidae)’un Ovaryumunun Histolojik Yapısı. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi, 21(1), 25-34. https://doi.org/10.35414/akufemubid.708448
AMA Yaman E, Yılmazer N. Hyalomma marginatum (Koch, 1844) (Acari: İxodidae)’un Ovaryumunun Histolojik Yapısı. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi. February 2021;21(1):25-34. doi:10.35414/akufemubid.708448
Chicago Yaman, Elif, and Nadim Yılmazer. “Hyalomma Marginatum (Koch, 1844) (Acari: İxodidae)’un Ovaryumunun Histolojik Yapısı”. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi 21, no. 1 (February 2021): 25-34. https://doi.org/10.35414/akufemubid.708448.
EndNote Yaman E, Yılmazer N (February 1, 2021) Hyalomma marginatum (Koch, 1844) (Acari: İxodidae)’un Ovaryumunun Histolojik Yapısı. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi 21 1 25–34.
IEEE E. Yaman and N. Yılmazer, “Hyalomma marginatum (Koch, 1844) (Acari: İxodidae)’un Ovaryumunun Histolojik Yapısı”, Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi, vol. 21, no. 1, pp. 25–34, 2021, doi: 10.35414/akufemubid.708448.
ISNAD Yaman, Elif - Yılmazer, Nadim. “Hyalomma Marginatum (Koch, 1844) (Acari: İxodidae)’un Ovaryumunun Histolojik Yapısı”. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi 21/1 (February 2021), 25-34. https://doi.org/10.35414/akufemubid.708448.
JAMA Yaman E, Yılmazer N. Hyalomma marginatum (Koch, 1844) (Acari: İxodidae)’un Ovaryumunun Histolojik Yapısı. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi. 2021;21:25–34.
MLA Yaman, Elif and Nadim Yılmazer. “Hyalomma Marginatum (Koch, 1844) (Acari: İxodidae)’un Ovaryumunun Histolojik Yapısı”. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi, vol. 21, no. 1, 2021, pp. 25-34, doi:10.35414/akufemubid.708448.
Vancouver Yaman E, Yılmazer N. Hyalomma marginatum (Koch, 1844) (Acari: İxodidae)’un Ovaryumunun Histolojik Yapısı. Afyon Kocatepe Üniversitesi Fen Ve Mühendislik Bilimleri Dergisi. 2021;21(1):25-34.


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