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Role of pH on the initiation of sperm motility in rainbow trout (Oncorhynchus mykiss) and Çoruh trout (Salmo coruhensis)

Yıl 2018, Cilt: 20 Sayı: 1, 421 - 429, 25.04.2018
https://doi.org/10.25092/baunfbed.418456

Öz

Experiments were designed to examine effects of pH (range 6.0–9.0) in different
activation solutions on sperm motility of
rainbow trout (Oncorhynchus mykiss) and Çoruh trout (Salmo
coruhensis).
Four activation
solutions were prepared: a) NaCl (52 mM)-AS1, b) NaCl (103 mM), CaCl2
(63 mM), Glucose (4 mM), Tris (10 mM)-AS2, c) NaHCO3 (119
mM)-AS3, d) NaCl (45 mM), KCl (5 mM), Tris (30 mM)-AS4. Sperm
was activated at the dilution ratio of 1:100 with different activation solutions.
Highest motility rate and duration for O.
mykiss were obtained from AS2 at a pH
of 9 while highest motility rate and duration
for S. coruhensis were at
a pH of 8. Data here reported also showed
that non-progressive motility in a range of 6–8 was observed in AS2 for
two species. In conclusion, rainbow trout (O. mykiss) and
Çoruh trout (S.
coruhensis) sperm cells can be motile in a wide range of pH although sperm
motility and duration was negatively influenced
by
low pH values.

Kaynakça

  • Kocabas, M., Kayim, M., Can, E., Ateş, M., Kutluyer, F., Aksu, Ö., Spotting pattern features in the brown trout (Salmo trutta macrostigma, T., 1954) population, Scientific Research and Essays, 6, 5021-5024, (2011).
  • Kuru, M., The last systematic status of inland fish in Turkey, Gazi University Journal of Faculty Education, 24(3), 1-21, (2004).
  • Kottelat, M., Freyhof, J., Handbook of European freshwater fishes. Kottelat, Cornol, Switzerland and Freyhof, Berlin, Germany pp. 646, (2007).
  • Turan, D., Kottelat, M., Engin, S., Two new species of trouts, resident and migratory, sympatric in streams of northern Anatolia (Salmoniformes: Salmonidae). Ichthyological Exploration of Freshwaters, 20(4), 333-364, (2009).
  • Kocabaş, M., Bascinar, N., The effect of salinity on spotting features of Salmo trutta abanticus, S. trutta fario and S. trutta labrax of cultured, Iranian Journal of Fisheries Science, 12, 723-732, (2013).
  • Costedoat, C., Pech, N., Chappaz, R., Gilles, A., Novelties in hybrid zones: crossroads between population genomic and ecological approaches. PLoS One, 2:e357, (2007).
  • Roberts, D.G., Gray, C.A., West, R.J., Ayre, D.J., Evolutionary impacts of hybridization and interspecific gene flow on an obligatory estuarine fish, Journal of Evolutionary Biology, 22, 27–35, (2009).
  • Crego-Prieto, V., Martinez, J.L., Roca, A., Garcia-Vazquez, E., Interspecific hybridization increased in congeneric flatfishes after the Prestige oil spill, PLoS One, 7, e34485, (2012).
  • Šimková, A., Vojtek, L., Halačka, K., Hyršl, P., Vetešník, L., The effect of hybridization on fish physiology, immunity and blood biochemistry: A case study in hybridizing Cyprinus carpio and Carassius gibelio (Cyprinidae), Aquaculture, 435, 381–389, (2015).
  • Öğretmen, F., Inanan, B.E., Kutluyer, F., Combined effects of physicochemical variables (pH and salinity) on sperm motility: characterization of sperm motility in European sea bass Dicentrarchus labrax, Marine and Freshwater Behaviour and Physiology, 49(3), 217-222, (2016).
  • Ingermann, R.L., Bencic, D.C., Gloud, J.G., Low seminal plasma buffering capacity corresponds to high pH sensitivity of sperm motility in salmonids, Fish Physiology and Biochemistry, 24, 299–307, ( 2002).
  • Dzyuba, B., Boryshpolets, S., Rodina, M., Gela D, Linhart O. Spontaneous activation of spermatozoa motility by routine freeze-thawing in different fish species, Journal of Applied Ichthyology, 26, 720–72, (2010).
  • Marian, T., Krasznai, Z., Balkay, L., Role of ex-tra-and intracellular pH in the sperm motility. Hyperosmosis modifies regulation of the Na+/H+ exchanger in the carp sperm, Cytometry, 27, 374–382, (1997).
  • Le, M.H., Pham, H.Q., Sperm motilities in waigieu seaperch, Psammoperca waigiensis: Effects of various dilutions, ph, temperature, osmolality, and cations, Journal of the World Aquaculture Society, doi: 10.1111/jwas.12357, (2016).
  • Hines, R., Yashouv, A., Some environmental factors influencing the activity of spermatozoa of Mugil capito Cuvier, a grey mullet, Journal of Fish Biology, 3, 123–127, (1971).
  • Billard, R., Effects of coelomic and seminal fluids and various saline diluents on the fertilizing ability of spermatozoa in the rainbow trout, Salmo gairdneri. Journal of Reproduction and Fertilization, 68, 77–84, (1983).
  • Billard, R., Cosson, M.P., Sperm motility in rainbow trout Parasalmo mykiss: effect of pH and temperature. In: Breton, B., Zohar, Y. (Eds.), Reproduction in Fish Basic and Applied Aspect in Endocrinology and Genetics, INRA, Paris, pp. 161–167, (1988).
  • Gatti, J.L., Billard, R., Christen, R., Ionic regulation of the plasma membrane potential of rainbow trout (Salmo gairdneri) sperm: role in the initiation of motility, Journal of Cell Physiology, 143, 546–544, (1990).
  • Billard, R., Cosson, J., Crim, L.W., Motility and survival of halibut sperm during short term storage, Aquatic Living Resources, 6, 67–75, (1993).
  • Billard, R., Prolongation de la durée de la mobilité et du pouvoir fécondant des spermatozoids de truite arc-en-ciel par addition de théophilline au milieu de dilution. Compte Rendus Academie Science Paris Serie D, 291, 649–652. (1980).
  • Chambeyron, F., Zohar, Y., A diluent for sperm cryopreservation of gilthead sea bream, Sparus aurataus, Aquaculture, 90, 345–352, (1990).
  • Cosson, J., The ionic and osmotic factors controlling motility of fish spermatozoa. Aquaculture International, 12, 69–85, (2004).
  • Linhart, O., Mims, S.D., Shelton, W.L., Motility of spermatozoa from Shovelnose sturgeon, Scaphirhynchus platorynchus, and Paddlefish, Polyodon spathula. Journal of Fish Biology, 47, 902-909, (1995).
  • Cosson, J., Linhart, O., Paddlefish, Polyodon spathula, spermatozoa: Effects of potassium and pH on motility, Folia Zoologica, 45, 361-370, (1996).
  • Chauvaud, L., Cosson, J., Suquet, M., Billard, R., Sperm motility in turbot, Scophthalmus maximus, initiation of movement and changes with time of swimming characteristics, Environmental Biology of Fishes, 43, 341–349, (1995).
  • Gallis, J.L., Fedrigo, E., Jatteau, P., Bonpunt, E., Billard, R., Siberian sturgeon spermatozoa: effects of dilution, pH, osmotic pressure, sodium and potassium ions on motility. In: Williot P. (Eds), Acipenser. Bordeaux: Cemagref. pp. 143-151, (1991).
  • Le, M.H., Lim, H.K., Min, B.H., Park, M.S., Son, M.H., Lee, J.U., Chang, Y.J., Effects of varying dilutions, pH, temperature and cations on spermatozoa motility in fish Larimichthys polyactis, Journal of Environmental Biology, 32, 271-276, (2011).
  • Öğretmen, F., Gölbaşı, S., İnanan, B.E., Inhibitory effect of K+ and Ca2+ concentrations, pH, and osmolality of activation solution on motility of shabut (Barbus grypus Heckel 1843) spermatozoa. Turkish Journal of Veterinary & Animal Sciences, 38, 245-252. (2014).
  • Effer, B., Figueroa, E., Augsburger, A., Valdebenito, I., Sperm biology of Merluccius australis: Sperm structure, semen characteristics and effects of pH, temperature and osmolality on sperm motility, Aquaculture, 408–409, 147–151, (2013).
  • Gallego, V., Martínez-Pastor, F., Mazzeo, I., Peñaranda, D.S., Herráez, M.P., Asturianoa, J.F., Pérez, L., Intracellular changes in Ca2+, K+ and pH after sperm motility activation in the European eel (Anguilla anguilla): Preliminary results, Aquaculture, 418–419, 155–158, (2014).
  • Ingermann, R.L., Holcomb, M., Zuccarelli, M.D., Kanuga, M.K., Cloud, J.G., Initiation of motility by steelhead (Oncorhynchus mykiss) sperm: Membrane ion exchangers and pH sensitivity, Comparative Biochemistry and Physiology Part A, 151, 651–656, (2008).
  • Ciereszko, A., Dietrich, G.J., Dietrich, M.A., Nynca, J., Kuzminski, H., Dobosz, S., Grudniewska, J., Effects of pH on sperm motility in several Salmoniformes species: Oncorhynchus mykiss, Salvelinus fontinalis, Salmo trutta, Salmo salar and Thymallus thymallus. Journal of Applied Ichthyology, 26, 665–667, (2010).
  • Alavi, S.M.H., Cosson, J., Sperm motility in fishes. (II) Effects of ions and osmolality: a review, Cell Biology International, 30(1), 1-14, (2006).
  • Lee, H.C., Jonson, C., Epel, D., 1983. Changes in internal pH associated with initiation of motility and acrosome reaction of sea urchin sperm, Developmental Biology, 95, 31–45, (1983).
  • Babcock, D., Rufo, G.A., Lardy, H.A., Potassium-dependent increases in cytosolic pH stimulate metabolism and motility of mammalian sperm, Proceedings of the National Academy of Sciences USA, 80, 1327–1331, (1983).
  • Wong, P.Y.D., Lee, W.M., Tsang, A.Y.F., The effects of extracellular sodium on acid release and motility initiation in rat caudal epididymal spermatozoa in vitro. Experimental Cell Research, 131, 97–104, (1981).
  • Morisawa, M., Adaptation and strategy for fertilization in the sperm of teleost fish, Journal of Applied Ichthyology, 24, 362–370, (2008).
  • Morisawa, M., Suzuki, K., Osmolality and potassium ion: their roles in initiation of sperm motility in teleosts. Science, 210, 1145–1147, (1980).
  • Oda, S., Morisawa, M., Rises of intracellular Ca2+ and pH mediate the initiation of sperm motility by hyperosmolality in marine teleosts. Cell Motility and the Cytoskeleton, 25, 171–178, (1993).
  • Zilli, L., Schiavone, R., Chauvigne, F., Cerda, J., Storelli, C., Vilella, S., Evidence for the involvement of aquaporins in sperm motility activation of the teleost gilthead sea bream (Sparus aurata), Biology of Reproduction, 81, 880–888, (2009).
  • Kocabas, M., Kayim, M., Aksu, Ö., Can, E., Kızak, V., Kutluyer, F., Serdar, O., Demirtaş N., Seasonal variation in food preference of the brown trout Salmo trutta macrostigma (T., 1954) from Uzungöl Stream, Turkey. African Journal of Agricultural Research, 7(13), 1982-1987, (2012).
  • Kocabas, M., Kayim, M., Can, E., Kutluyer, F., Aksu, Ö., The reproduction traits of native brown trout (Salmo trutta macrostigma T., 1954), Turkey. Journal of Animal and Veterinary Advances, 10(13), 1632-1637, (2011).
  • Kocabas, M., Basçinar, N., Kutluyer, F., Aksu Ö., Ülkemizde yayılım gösteren Salmo trutta macrostigma ekotipi gerçekten yok oluyormu.. Turkish Journal of Scientific Reviews, 6(1), 132-138, (2012).

Gökkuşağı alabalığı (Oncorhynchus mykiss) ve Çoruh alabalığı (Salmo coruhensis) sperm motilitesinin başlamasında pH’ın rolü

Yıl 2018, Cilt: 20 Sayı: 1, 421 - 429, 25.04.2018
https://doi.org/10.25092/baunfbed.418456

Öz

Çoruh alabalığı (Salmo coruhensis) ve gökkuşağı alabalığının (Oncorhynchus mykiss) sperm motilitesi üzerinde farklı aktivasyon solusyonlarının pH (6.0–9.0)’ının etkilerini belirlemek için denemeler dizayn edilmiştir. Dört aktivasyon solusyonu hazırlanmıştır: a) NaCl (52 mM)-AS1, b) NaCl (103 mM), CaCl2 (63 mM), Glikoz (4 mM), Tris (10 mM)-AS2, c) NaHCO3 (119 mM)-AS3, d) NaCl (45 mM), KCl (5 mM), Tris (30 mM)-AS4. Sperm farklı aktivasyon solusyonlarıyla 1:100 sulandırma oranıyla aktive edilmiştir. S. coruhensis türünde en yüksek motilite oranı ve süresi pH 8’den elde edilirken O. mykiss türünde en yüksek motilite oranı ve süresi AS2 solusyonu pH 9’da elde edilmiştir. Veriler, iki tür için AS2’de ph 6-8 aralığında non-progresif motilite olduğunu göstermiştir. Sonuç olarak, sperm motilitesi ve süresi düşük pH değerlerinden olumsuz etkilemesine rağmen, Çoruh alabalığı S. coruhensis ve gökkuşağı alabalığının O. mykiss spermi geniş pH aralıklarında motil olabilir.

Kaynakça

  • Kocabas, M., Kayim, M., Can, E., Ateş, M., Kutluyer, F., Aksu, Ö., Spotting pattern features in the brown trout (Salmo trutta macrostigma, T., 1954) population, Scientific Research and Essays, 6, 5021-5024, (2011).
  • Kuru, M., The last systematic status of inland fish in Turkey, Gazi University Journal of Faculty Education, 24(3), 1-21, (2004).
  • Kottelat, M., Freyhof, J., Handbook of European freshwater fishes. Kottelat, Cornol, Switzerland and Freyhof, Berlin, Germany pp. 646, (2007).
  • Turan, D., Kottelat, M., Engin, S., Two new species of trouts, resident and migratory, sympatric in streams of northern Anatolia (Salmoniformes: Salmonidae). Ichthyological Exploration of Freshwaters, 20(4), 333-364, (2009).
  • Kocabaş, M., Bascinar, N., The effect of salinity on spotting features of Salmo trutta abanticus, S. trutta fario and S. trutta labrax of cultured, Iranian Journal of Fisheries Science, 12, 723-732, (2013).
  • Costedoat, C., Pech, N., Chappaz, R., Gilles, A., Novelties in hybrid zones: crossroads between population genomic and ecological approaches. PLoS One, 2:e357, (2007).
  • Roberts, D.G., Gray, C.A., West, R.J., Ayre, D.J., Evolutionary impacts of hybridization and interspecific gene flow on an obligatory estuarine fish, Journal of Evolutionary Biology, 22, 27–35, (2009).
  • Crego-Prieto, V., Martinez, J.L., Roca, A., Garcia-Vazquez, E., Interspecific hybridization increased in congeneric flatfishes after the Prestige oil spill, PLoS One, 7, e34485, (2012).
  • Šimková, A., Vojtek, L., Halačka, K., Hyršl, P., Vetešník, L., The effect of hybridization on fish physiology, immunity and blood biochemistry: A case study in hybridizing Cyprinus carpio and Carassius gibelio (Cyprinidae), Aquaculture, 435, 381–389, (2015).
  • Öğretmen, F., Inanan, B.E., Kutluyer, F., Combined effects of physicochemical variables (pH and salinity) on sperm motility: characterization of sperm motility in European sea bass Dicentrarchus labrax, Marine and Freshwater Behaviour and Physiology, 49(3), 217-222, (2016).
  • Ingermann, R.L., Bencic, D.C., Gloud, J.G., Low seminal plasma buffering capacity corresponds to high pH sensitivity of sperm motility in salmonids, Fish Physiology and Biochemistry, 24, 299–307, ( 2002).
  • Dzyuba, B., Boryshpolets, S., Rodina, M., Gela D, Linhart O. Spontaneous activation of spermatozoa motility by routine freeze-thawing in different fish species, Journal of Applied Ichthyology, 26, 720–72, (2010).
  • Marian, T., Krasznai, Z., Balkay, L., Role of ex-tra-and intracellular pH in the sperm motility. Hyperosmosis modifies regulation of the Na+/H+ exchanger in the carp sperm, Cytometry, 27, 374–382, (1997).
  • Le, M.H., Pham, H.Q., Sperm motilities in waigieu seaperch, Psammoperca waigiensis: Effects of various dilutions, ph, temperature, osmolality, and cations, Journal of the World Aquaculture Society, doi: 10.1111/jwas.12357, (2016).
  • Hines, R., Yashouv, A., Some environmental factors influencing the activity of spermatozoa of Mugil capito Cuvier, a grey mullet, Journal of Fish Biology, 3, 123–127, (1971).
  • Billard, R., Effects of coelomic and seminal fluids and various saline diluents on the fertilizing ability of spermatozoa in the rainbow trout, Salmo gairdneri. Journal of Reproduction and Fertilization, 68, 77–84, (1983).
  • Billard, R., Cosson, M.P., Sperm motility in rainbow trout Parasalmo mykiss: effect of pH and temperature. In: Breton, B., Zohar, Y. (Eds.), Reproduction in Fish Basic and Applied Aspect in Endocrinology and Genetics, INRA, Paris, pp. 161–167, (1988).
  • Gatti, J.L., Billard, R., Christen, R., Ionic regulation of the plasma membrane potential of rainbow trout (Salmo gairdneri) sperm: role in the initiation of motility, Journal of Cell Physiology, 143, 546–544, (1990).
  • Billard, R., Cosson, J., Crim, L.W., Motility and survival of halibut sperm during short term storage, Aquatic Living Resources, 6, 67–75, (1993).
  • Billard, R., Prolongation de la durée de la mobilité et du pouvoir fécondant des spermatozoids de truite arc-en-ciel par addition de théophilline au milieu de dilution. Compte Rendus Academie Science Paris Serie D, 291, 649–652. (1980).
  • Chambeyron, F., Zohar, Y., A diluent for sperm cryopreservation of gilthead sea bream, Sparus aurataus, Aquaculture, 90, 345–352, (1990).
  • Cosson, J., The ionic and osmotic factors controlling motility of fish spermatozoa. Aquaculture International, 12, 69–85, (2004).
  • Linhart, O., Mims, S.D., Shelton, W.L., Motility of spermatozoa from Shovelnose sturgeon, Scaphirhynchus platorynchus, and Paddlefish, Polyodon spathula. Journal of Fish Biology, 47, 902-909, (1995).
  • Cosson, J., Linhart, O., Paddlefish, Polyodon spathula, spermatozoa: Effects of potassium and pH on motility, Folia Zoologica, 45, 361-370, (1996).
  • Chauvaud, L., Cosson, J., Suquet, M., Billard, R., Sperm motility in turbot, Scophthalmus maximus, initiation of movement and changes with time of swimming characteristics, Environmental Biology of Fishes, 43, 341–349, (1995).
  • Gallis, J.L., Fedrigo, E., Jatteau, P., Bonpunt, E., Billard, R., Siberian sturgeon spermatozoa: effects of dilution, pH, osmotic pressure, sodium and potassium ions on motility. In: Williot P. (Eds), Acipenser. Bordeaux: Cemagref. pp. 143-151, (1991).
  • Le, M.H., Lim, H.K., Min, B.H., Park, M.S., Son, M.H., Lee, J.U., Chang, Y.J., Effects of varying dilutions, pH, temperature and cations on spermatozoa motility in fish Larimichthys polyactis, Journal of Environmental Biology, 32, 271-276, (2011).
  • Öğretmen, F., Gölbaşı, S., İnanan, B.E., Inhibitory effect of K+ and Ca2+ concentrations, pH, and osmolality of activation solution on motility of shabut (Barbus grypus Heckel 1843) spermatozoa. Turkish Journal of Veterinary & Animal Sciences, 38, 245-252. (2014).
  • Effer, B., Figueroa, E., Augsburger, A., Valdebenito, I., Sperm biology of Merluccius australis: Sperm structure, semen characteristics and effects of pH, temperature and osmolality on sperm motility, Aquaculture, 408–409, 147–151, (2013).
  • Gallego, V., Martínez-Pastor, F., Mazzeo, I., Peñaranda, D.S., Herráez, M.P., Asturianoa, J.F., Pérez, L., Intracellular changes in Ca2+, K+ and pH after sperm motility activation in the European eel (Anguilla anguilla): Preliminary results, Aquaculture, 418–419, 155–158, (2014).
  • Ingermann, R.L., Holcomb, M., Zuccarelli, M.D., Kanuga, M.K., Cloud, J.G., Initiation of motility by steelhead (Oncorhynchus mykiss) sperm: Membrane ion exchangers and pH sensitivity, Comparative Biochemistry and Physiology Part A, 151, 651–656, (2008).
  • Ciereszko, A., Dietrich, G.J., Dietrich, M.A., Nynca, J., Kuzminski, H., Dobosz, S., Grudniewska, J., Effects of pH on sperm motility in several Salmoniformes species: Oncorhynchus mykiss, Salvelinus fontinalis, Salmo trutta, Salmo salar and Thymallus thymallus. Journal of Applied Ichthyology, 26, 665–667, (2010).
  • Alavi, S.M.H., Cosson, J., Sperm motility in fishes. (II) Effects of ions and osmolality: a review, Cell Biology International, 30(1), 1-14, (2006).
  • Lee, H.C., Jonson, C., Epel, D., 1983. Changes in internal pH associated with initiation of motility and acrosome reaction of sea urchin sperm, Developmental Biology, 95, 31–45, (1983).
  • Babcock, D., Rufo, G.A., Lardy, H.A., Potassium-dependent increases in cytosolic pH stimulate metabolism and motility of mammalian sperm, Proceedings of the National Academy of Sciences USA, 80, 1327–1331, (1983).
  • Wong, P.Y.D., Lee, W.M., Tsang, A.Y.F., The effects of extracellular sodium on acid release and motility initiation in rat caudal epididymal spermatozoa in vitro. Experimental Cell Research, 131, 97–104, (1981).
  • Morisawa, M., Adaptation and strategy for fertilization in the sperm of teleost fish, Journal of Applied Ichthyology, 24, 362–370, (2008).
  • Morisawa, M., Suzuki, K., Osmolality and potassium ion: their roles in initiation of sperm motility in teleosts. Science, 210, 1145–1147, (1980).
  • Oda, S., Morisawa, M., Rises of intracellular Ca2+ and pH mediate the initiation of sperm motility by hyperosmolality in marine teleosts. Cell Motility and the Cytoskeleton, 25, 171–178, (1993).
  • Zilli, L., Schiavone, R., Chauvigne, F., Cerda, J., Storelli, C., Vilella, S., Evidence for the involvement of aquaporins in sperm motility activation of the teleost gilthead sea bream (Sparus aurata), Biology of Reproduction, 81, 880–888, (2009).
  • Kocabas, M., Kayim, M., Aksu, Ö., Can, E., Kızak, V., Kutluyer, F., Serdar, O., Demirtaş N., Seasonal variation in food preference of the brown trout Salmo trutta macrostigma (T., 1954) from Uzungöl Stream, Turkey. African Journal of Agricultural Research, 7(13), 1982-1987, (2012).
  • Kocabas, M., Kayim, M., Can, E., Kutluyer, F., Aksu, Ö., The reproduction traits of native brown trout (Salmo trutta macrostigma T., 1954), Turkey. Journal of Animal and Veterinary Advances, 10(13), 1632-1637, (2011).
  • Kocabas, M., Basçinar, N., Kutluyer, F., Aksu Ö., Ülkemizde yayılım gösteren Salmo trutta macrostigma ekotipi gerçekten yok oluyormu.. Turkish Journal of Scientific Reviews, 6(1), 132-138, (2012).
Toplam 43 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Bölüm Araştırma Makalesi
Yazarlar

Filiz Kutluyer

Yayımlanma Tarihi 25 Nisan 2018
Gönderilme Tarihi 6 Nisan 2018
Yayımlandığı Sayı Yıl 2018 Cilt: 20 Sayı: 1

Kaynak Göster

APA Kutluyer, F. (2018). Role of pH on the initiation of sperm motility in rainbow trout (Oncorhynchus mykiss) and Çoruh trout (Salmo coruhensis). Balıkesir Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 20(1), 421-429. https://doi.org/10.25092/baunfbed.418456
AMA Kutluyer F. Role of pH on the initiation of sperm motility in rainbow trout (Oncorhynchus mykiss) and Çoruh trout (Salmo coruhensis). BAUN Fen. Bil. Enst. Dergisi. Temmuz 2018;20(1):421-429. doi:10.25092/baunfbed.418456
Chicago Kutluyer, Filiz. “Role of PH on the Initiation of Sperm Motility in Rainbow Trout (Oncorhynchus Mykiss) and Çoruh Trout (Salmo Coruhensis)”. Balıkesir Üniversitesi Fen Bilimleri Enstitüsü Dergisi 20, sy. 1 (Temmuz 2018): 421-29. https://doi.org/10.25092/baunfbed.418456.
EndNote Kutluyer F (01 Temmuz 2018) Role of pH on the initiation of sperm motility in rainbow trout (Oncorhynchus mykiss) and Çoruh trout (Salmo coruhensis). Balıkesir Üniversitesi Fen Bilimleri Enstitüsü Dergisi 20 1 421–429.
IEEE F. Kutluyer, “Role of pH on the initiation of sperm motility in rainbow trout (Oncorhynchus mykiss) and Çoruh trout (Salmo coruhensis)”, BAUN Fen. Bil. Enst. Dergisi, c. 20, sy. 1, ss. 421–429, 2018, doi: 10.25092/baunfbed.418456.
ISNAD Kutluyer, Filiz. “Role of PH on the Initiation of Sperm Motility in Rainbow Trout (Oncorhynchus Mykiss) and Çoruh Trout (Salmo Coruhensis)”. Balıkesir Üniversitesi Fen Bilimleri Enstitüsü Dergisi 20/1 (Temmuz 2018), 421-429. https://doi.org/10.25092/baunfbed.418456.
JAMA Kutluyer F. Role of pH on the initiation of sperm motility in rainbow trout (Oncorhynchus mykiss) and Çoruh trout (Salmo coruhensis). BAUN Fen. Bil. Enst. Dergisi. 2018;20:421–429.
MLA Kutluyer, Filiz. “Role of PH on the Initiation of Sperm Motility in Rainbow Trout (Oncorhynchus Mykiss) and Çoruh Trout (Salmo Coruhensis)”. Balıkesir Üniversitesi Fen Bilimleri Enstitüsü Dergisi, c. 20, sy. 1, 2018, ss. 421-9, doi:10.25092/baunfbed.418456.
Vancouver Kutluyer F. Role of pH on the initiation of sperm motility in rainbow trout (Oncorhynchus mykiss) and Çoruh trout (Salmo coruhensis). BAUN Fen. Bil. Enst. Dergisi. 2018;20(1):421-9.