Main Article Content
Abstract
This study was conducted to investigate the effect of Rue (RE), a medicinal herb having anti-androgenic characteristic on the sexuality of guppy males. In total, 120 males were selected randomly, acclimated and divided equally into four groups that received the RE ethanolic extract at 0, 1, 10 and 100 mg.kg-1, respectively for 30 days. The findings revealed that 100 mg.kg-1 had significantly lower whole-body testosterone levels than control. Furthermore, males administered RE at all doses had a significantly lower gonopodial index than the control group. Whereas, administration of RE at 10 and 100 mg.kg-1 causes a lowering in sperm counts than the control group. Regarding with histopathological examination, the testes of control males were well-differentiated with an increase in spermatozeugmata proportion at all spermatogenesis stages with a significant proportion of cystic structures containing spermatozoa. On the other hand, RE-fed animals showed a dose-dependent decrease in spermatozeugmata and an increase in spermatocytes' number of ducts, indicating the role of RE in reducing the development of guppy’s spermatogenesis. In conclusion, Rue can impact the sexual parameters of adult guppy males by confirming the anti-androgenic properties of RE.
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References
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- https://doi.org/10.1016/j.ygcen.2015.05.011
- Asgarpanah, J., & Khoshkam, R., (2012). Phytochemistry and pharmacological properties of Ruta graveolens L. Journal of Medicinal Plants Research, 6, 3942-3949.
- https://academicjournals.org/journal/JMPR/article-abstract/F4B478423256
- Baatrup, E., & Junge, M. (2001). Antiandrogenic pesticides disrupt sexual characteristics in the adult male guppy (Poecilia reticulata). Environmental Health Perspectives, 109, 1063–1070.
- https://doi.org/10.1289/ehp.011091063
- Bayley, M., Junge, M., & Baatrup, E., (2002). Exposure of juvenile guppies to three antiandrogens causes demasculinization and a reduced sperm count in adult males. Aquatic Toxicology, 56(4), 227-239.
- https://doi.org/10.1016/S0166-445X(01)00210-7
- Blair, B. D., Crago, J. P., Hedman, C. J., & Klaper, R. D. (2013). Pharmaceuticals and personal care products found in the Great Lakes above concentrations of environmental concern. Chemosphere, 93, 2116–2123.
- https://doi.org/10.1016/j.chemosphere.2013.07.057
- Cheshenko, K., Pakdel, F., Segner, H., Kah, O., & Eggen, R. I. (2008). Interference of endocrine disrupting chemicals with aromatase CYP19 expression or activity and consequences for reproduction of teleost fish. General and Comparative Endocrinology, 155, 31-62.
- https://doi.org/10.1016/j.ygcen.2007.03.005
- Chiu, K. W., & Fung, A. Y. (1997). The cardiovascular effects of green beans (Phaseolus aureus), common rue (Ruta graveolens) and kelp (Laminaria japonica) in rats. General Pharmacology, 29, 859-862.
- https://doi.org/10.1016/S0306-3623(97)00001-3
- Froese, R., & Pauly, D. [Editors]. (2024). FishBase. World Wide Web electronic publication. www.fishbase.org, version (02/2024).
- Crago, J., & Klaper, R. (2012). A mixture of an environmentally realistic concentration of a phthalate and herbicide reduces testosterone in male fathead minnow (Pimephales promelas) through a novel mechanism of action. Aquatic Toxicology, 111, 74-83.
- https://doi.org/10.1016/j.aquatox.2011.12.021
- De Gendt, K., Swinnen, J. V., Saunders, P. T., Schoonjans, L., Dewerchin, M., Devos, A., Tan, K., Atanassova, N., Claessens, F., Lécureuil, C., Heyns, W., Carmeliet, P., Guillou, F., Sharpe, R. M., & Verhoeven, G. (2004). A sertoli cell-selective knockout of the androgen receptorcauses spermatogenic arrest in meiosis. Proceedings of the National Academy of Sciences of the United States of America, 101(5), 1327–1332.
- https://doi.org/10.1073/pnas.0308114100
- Forsatkar, M. N., HedayatiRad, M., & Luchiari A. C. (2018). “Not tonight zebrafish”: the effects of Rutagraveolens on reproduction. Pharmaceutical Biology, 56, 60-66.
- https://doi.org/10.1080/13880209.2017.1421234
- Forsatkar, M. N., Nematollahi, M. A., & Brown, C. (2016). The toxicological effect of Ruta graveolens extract in Siamese fighting fish: A behavioral and histopathological approach. Ecotoxicology, 25, 824-834. https://doi.org/10.1007/s10646-016-1639-5
- Gharban, H. A. J., & Yousif, A. A. (2021). First isolation and molecular phylogenetic analysis of Coxiella burnetii in lactating cows, Iraq. Bulgarian Journal of Veterinary Medicine, 24(4), 508-519. http://tru.uni-sz.bg/bjvm/summary%20vol.24-4-06.htm+
- Hale, A. L., Meepagala, K. M., Oliva, A., Aliotta, G., & Duke, S. O. (2004). Phytotoxins from the leaves of Ruta graveolens. Journal of agricultural and food Chemistry, 52(11), 3345–3349.
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- Halvaei, I., Roodsari, H. R., & Harat, Z. N. (2012). Acute Effects of Ruta graveolens L. on sperm parameters and DNA integrity in rats. Journal of Reproduction & Infertility, 13(1), 33–38. http://www.ncbi.nlm.nih.gov/pmc/articles/pmc3719372/
- Haubruge, E., Petit, F., & Gage, M. J. G. (2000). Reduced sperm counts in guppies (Poecilia reticulata) following exposure to low levels of tributyltin and bisphenol A. Proceedings Biological Sciences, 267(1459), 2333-2337.
- https://doi.org/10.1098/rspb.2000.1288
- Hewitson, T. D., & Darby, I. A. (2010). Histology Protocols. Humana Totowa N. J. 229pp.
- https://doi.org/10.1007/978-1-60327-345-9
- Hoopfer, E. D., Penton, A., Watts, R. J., & Luo, L. (2008). Genomic analysis of Drosophila neuronal remodeling: a role for the RNA-binding protein Boule as a negative regulator of axon pruning. Journal of Neuroscience, 28, 6092–6103.
- https://doi.org/10.1523/jneurosci.0677-08.2008
- Houde, A. E. (1997). Sex, color and mate choice in guppies. Princeton University Press. Princeton, N.J. 226pp. https://doi.org/10.2307/j.ctvs32rtk
- Ikeuchi, T., Todo, T., Kobayashi, T., & Nagahama, Y. (2001). Two subtypes of androgen and progestogen receptors in fish testes. Comparative Biochemistry & Physiology Part B: Biochemical and Molecular Biology, 129B, 449-455.
- https://doi.org/10.1016/S1096-4959(01)00375-X
- Ivanova, A., Mikhova, B., Najdenski, H., Tsvetkova, I., & Kostova, I. (2005). Antimicrobial and cytotoxic activity of Rutagraveolens. Fitoterapia, 76, 344–347. https://doi.org/10.1016/j.fitote.2005.02.008
- Jensen K. M., Kahl, M. D., Makynen, E. A., Korte J. J., Leino, R. L., Butterworth, B. C., & Ankley G. T. (2004). Characterization of responses to the antiandrogen flutamide in a short-term reproduction assay with the fathead minnow. Aquatic Toxicology, 70, 99-110. https://doi.org/10.1016/j.aquatox.2004.06.012
- Kadhim, A. H., Yesser, A. T., & Al-Niaeem, K. S. (2023). Effect of Marjoram Origanum majorana L. Extract on Growth Performance and Some Haematological Parameters of Common Carp Cyprinus carpio L. Basrah Journal of Agricultural Sciences, 36(1), 29-38.
- https://doi.org/10.37077/25200860.2023.36.1.03
- Khouri, N. A., & El-Akawi Z. (2005). Antiandrogenic activity of Ruta graveolens L in male Albino rats with emphasis on sexual and aggressive behavior. Neuro Endocrinology Letters, 26, 823-829.
- https://pubmed.ncbi.nlm.nih.gov/16380694/#:~:text=PMID%3A-,16380694,-Abstract
- Kinnberg, K., & Toft, G. (2003). Effects of estrogenic and antiandrogenic compounds on the testis structure of the adult guppy (Poecilia reticulata). Ecotoxicology and Environmental Safety, 54, 16-24.
- https://doi.org/10.1016/S0147-6513(02)00010-6
- Kuzovkina, I., Al’terman, I., & Schneider, B. (2004). Specific accumulation and revised structures of acridone alkaloid glucosides in the tips of transformed roots of Ruta graveolens. Phytochemistry, 65, 1095-100.
- https://doi.org/10.1016/j.phytochem.2004.03.003
- Li, X., Wang, J., Yu, M., Zhang, X., Wang, W., Tian, H., & Ru, S. (2019). 2,2′-Dithiobis-pyridine induced reproductive toxicity in male guppy (Poecilia reticulata). Ecotoxicology and Environmental Safety, 169, 778–785.
- https://doi.org/10.1016/j.ecoenv.2018.11.076
- Manibusan, M. K., & Touart, L. W. (2017). A comprehensive review of regulatory test methods for endocrine adverse health effects. Critical Reviews in Toxicology, 47, 433-481. doi.org/10.1080/10408444.2016.1272095
- Matthiessen, P., Wheeler J. R., & Weltje, L. (2018). A review of the evidence for endocrine disrupting effects of current-use chemicals on wildlife populations. Critical Reviews in Toxicology, 48, 195-216.
- https://doi.org/10.1080/10408444.2017.1397099
- Maurya, R., Srivastava, S., Kulshreshta, D. K., & Gupta, C. M. (2004). Traditional remedies for fertility regulation. Current Medicinal Chemistry, 11, 1431–1450. http://doi.org/10.2174/0929867043365215
- Meepagala, K. M., Schrader, K. K., Wedge, D. E., & Duke, S. O. (2005). Algicidal and antifungal compounds from the roots of Ruta graveolens and synthesis of their analogs. Phytochemistry, 66(22), 2689-2695.
- https://doi.org/10.1016/j.phytochem.2005.09.019
- Miguel, E. S. (2003). Rue in traditional Spain: frequency and distribution of its medicinal and symbolic applications. Economic Botany, 57, 231-244.
- https://www.jstor.org/stable/4256681
- Oliva, A., Meepagala, K. M., Wedge, D. E., Harries, D., Hale, A. L., Aliotta, G., & Duke, S. O. (2003). Natural fungicides from Ruta graveolens L. leaves, including a new quinolone alkaloid. Journal of Agricultural and Food Chemistry, 51, 890-896.
- https://doi.org/10.1021/jf0259361
- Pathak, S., Multani, A. S., Banerji, P., & Banerji, P. (2003). Ruta selectively induces cell death in brain cancer cells but proliferation in normal peripheral blood lymphocytes: a novel treatment for human brain cancer. International Journal of Oncology, 23, 975-982. http://doi.org/10.3892/ijo.23.4.975
- Preethi, K. C., Kuttan, G., & Kuttan, R. (2006). Anti-tumour activity of Ruta graveolens extract. Asian Pacific Journal of Cancer Prevention, 7, 439-443.
- https://pubmed.ncbi.nlm.nih.gov/17059340/#:~:text=Abstract,lifespan%20of%20tumour%20bearing%20animals
- Raghav, S. K., Gupta, B., Agrawal, C., Goswami, K., & Das, H. R. (2006). Anti-inflammatory effect of Ruta graveolens L. in murine macrophage cells. Journal of Ethnopharmacology, 104(1-2), 234-239.
- https://doi.org/10.1016/j.jep.2005.09.008
- Rodriguez, C. M. (1997). Phylogenetic analysis of the tribe Poeciliini (Cyprinodontiformes: Poeciliidae). Copeia, 1997(4), 663-679.
- https://doi.org/10.2307/1447285
- Sailani, M. R., & Moeini, H. (2007). Effect of Ruta graveolens and Cannabis sativa alcoholic extract on spermatogenesis in the adult wistar male rats. Indian Journal of Urology, 23, 257-60.
- https://doi.org/10.4103%2F0970-1591.33720
- Tian, H., Fotidis, I. A., Mancini, E., & Angelidaki, I. (2017). Different cultivation methods to acclimatise ammonia-tolerant methanogenic consortia. Bioresource Technology, 232, 1-9.
- https://doi.org/10.1016/j.biortech.2017.02.034
- Toft, G., & Baatrup, E. (2001). Sexual characteristics are altered by 4-tert-octylphenol and 17β-estradiol in the adult male guppy (Poecilia reticulata). Ecotoxicology and environmental safety, 48(1), 76-84. https://doi.org/10.1006/eesa.2000.1985
- Walker, W. H. (2009). Molecular mechanisms of testosterone action in spermatogenesis. Steroids, 74(2), 602–607.
- https://doi.org/10.1016/j.steroids.2008.11.017
- Yilmaz, E., & Ergün, S. (2015). Influence of carvacrol on the growth performance, haematological, non-specific immune and serum biochemistry parameters in rainbow trout (Oncorhynchus mykiss). Food and Nutrition Sciences, 6(5), 523.
- https://doi.org/10.4236/fns.2015.65054
References
Ahmadivand, S., Farahmand, H., Teimoori-Toolabi, L., Mirvaghefi, A., Eagderi, S., Geerinckx, T., Shokrpoor, S., & Rahmati-Holasoo, H. (2016). Boule gene expression underpins the meiotic arrest in spermatogenesis in male rainbow trout (Oncorhynchus mykiss) exposed to DEHP and butachlor. General and Comparative Endocrinology, 225, 235–241.
https://doi.org/10.1016/j.ygcen.2015.05.011
Asgarpanah, J., & Khoshkam, R., (2012). Phytochemistry and pharmacological properties of Ruta graveolens L. Journal of Medicinal Plants Research, 6, 3942-3949.
https://academicjournals.org/journal/JMPR/article-abstract/F4B478423256
Baatrup, E., & Junge, M. (2001). Antiandrogenic pesticides disrupt sexual characteristics in the adult male guppy (Poecilia reticulata). Environmental Health Perspectives, 109, 1063–1070.
https://doi.org/10.1289/ehp.011091063
Bayley, M., Junge, M., & Baatrup, E., (2002). Exposure of juvenile guppies to three antiandrogens causes demasculinization and a reduced sperm count in adult males. Aquatic Toxicology, 56(4), 227-239.
https://doi.org/10.1016/S0166-445X(01)00210-7
Blair, B. D., Crago, J. P., Hedman, C. J., & Klaper, R. D. (2013). Pharmaceuticals and personal care products found in the Great Lakes above concentrations of environmental concern. Chemosphere, 93, 2116–2123.
https://doi.org/10.1016/j.chemosphere.2013.07.057
Cheshenko, K., Pakdel, F., Segner, H., Kah, O., & Eggen, R. I. (2008). Interference of endocrine disrupting chemicals with aromatase CYP19 expression or activity and consequences for reproduction of teleost fish. General and Comparative Endocrinology, 155, 31-62.
https://doi.org/10.1016/j.ygcen.2007.03.005
Chiu, K. W., & Fung, A. Y. (1997). The cardiovascular effects of green beans (Phaseolus aureus), common rue (Ruta graveolens) and kelp (Laminaria japonica) in rats. General Pharmacology, 29, 859-862.
https://doi.org/10.1016/S0306-3623(97)00001-3
Froese, R., & Pauly, D. [Editors]. (2024). FishBase. World Wide Web electronic publication. www.fishbase.org, version (02/2024).
Crago, J., & Klaper, R. (2012). A mixture of an environmentally realistic concentration of a phthalate and herbicide reduces testosterone in male fathead minnow (Pimephales promelas) through a novel mechanism of action. Aquatic Toxicology, 111, 74-83.
https://doi.org/10.1016/j.aquatox.2011.12.021
De Gendt, K., Swinnen, J. V., Saunders, P. T., Schoonjans, L., Dewerchin, M., Devos, A., Tan, K., Atanassova, N., Claessens, F., Lécureuil, C., Heyns, W., Carmeliet, P., Guillou, F., Sharpe, R. M., & Verhoeven, G. (2004). A sertoli cell-selective knockout of the androgen receptorcauses spermatogenic arrest in meiosis. Proceedings of the National Academy of Sciences of the United States of America, 101(5), 1327–1332.
https://doi.org/10.1073/pnas.0308114100
Forsatkar, M. N., HedayatiRad, M., & Luchiari A. C. (2018). “Not tonight zebrafish”: the effects of Rutagraveolens on reproduction. Pharmaceutical Biology, 56, 60-66.
https://doi.org/10.1080/13880209.2017.1421234
Forsatkar, M. N., Nematollahi, M. A., & Brown, C. (2016). The toxicological effect of Ruta graveolens extract in Siamese fighting fish: A behavioral and histopathological approach. Ecotoxicology, 25, 824-834. https://doi.org/10.1007/s10646-016-1639-5
Gharban, H. A. J., & Yousif, A. A. (2021). First isolation and molecular phylogenetic analysis of Coxiella burnetii in lactating cows, Iraq. Bulgarian Journal of Veterinary Medicine, 24(4), 508-519. http://tru.uni-sz.bg/bjvm/summary%20vol.24-4-06.htm+
Hale, A. L., Meepagala, K. M., Oliva, A., Aliotta, G., & Duke, S. O. (2004). Phytotoxins from the leaves of Ruta graveolens. Journal of agricultural and food Chemistry, 52(11), 3345–3349.
https://doi.org/10.1021/jf0497298
Halvaei, I., Roodsari, H. R., & Harat, Z. N. (2012). Acute Effects of Ruta graveolens L. on sperm parameters and DNA integrity in rats. Journal of Reproduction & Infertility, 13(1), 33–38. http://www.ncbi.nlm.nih.gov/pmc/articles/pmc3719372/
Haubruge, E., Petit, F., & Gage, M. J. G. (2000). Reduced sperm counts in guppies (Poecilia reticulata) following exposure to low levels of tributyltin and bisphenol A. Proceedings Biological Sciences, 267(1459), 2333-2337.
https://doi.org/10.1098/rspb.2000.1288
Hewitson, T. D., & Darby, I. A. (2010). Histology Protocols. Humana Totowa N. J. 229pp.
https://doi.org/10.1007/978-1-60327-345-9
Hoopfer, E. D., Penton, A., Watts, R. J., & Luo, L. (2008). Genomic analysis of Drosophila neuronal remodeling: a role for the RNA-binding protein Boule as a negative regulator of axon pruning. Journal of Neuroscience, 28, 6092–6103.
https://doi.org/10.1523/jneurosci.0677-08.2008
Houde, A. E. (1997). Sex, color and mate choice in guppies. Princeton University Press. Princeton, N.J. 226pp. https://doi.org/10.2307/j.ctvs32rtk
Ikeuchi, T., Todo, T., Kobayashi, T., & Nagahama, Y. (2001). Two subtypes of androgen and progestogen receptors in fish testes. Comparative Biochemistry & Physiology Part B: Biochemical and Molecular Biology, 129B, 449-455.
https://doi.org/10.1016/S1096-4959(01)00375-X
Ivanova, A., Mikhova, B., Najdenski, H., Tsvetkova, I., & Kostova, I. (2005). Antimicrobial and cytotoxic activity of Rutagraveolens. Fitoterapia, 76, 344–347. https://doi.org/10.1016/j.fitote.2005.02.008
Jensen K. M., Kahl, M. D., Makynen, E. A., Korte J. J., Leino, R. L., Butterworth, B. C., & Ankley G. T. (2004). Characterization of responses to the antiandrogen flutamide in a short-term reproduction assay with the fathead minnow. Aquatic Toxicology, 70, 99-110. https://doi.org/10.1016/j.aquatox.2004.06.012
Kadhim, A. H., Yesser, A. T., & Al-Niaeem, K. S. (2023). Effect of Marjoram Origanum majorana L. Extract on Growth Performance and Some Haematological Parameters of Common Carp Cyprinus carpio L. Basrah Journal of Agricultural Sciences, 36(1), 29-38.
https://doi.org/10.37077/25200860.2023.36.1.03
Khouri, N. A., & El-Akawi Z. (2005). Antiandrogenic activity of Ruta graveolens L in male Albino rats with emphasis on sexual and aggressive behavior. Neuro Endocrinology Letters, 26, 823-829.
https://pubmed.ncbi.nlm.nih.gov/16380694/#:~:text=PMID%3A-,16380694,-Abstract
Kinnberg, K., & Toft, G. (2003). Effects of estrogenic and antiandrogenic compounds on the testis structure of the adult guppy (Poecilia reticulata). Ecotoxicology and Environmental Safety, 54, 16-24.
https://doi.org/10.1016/S0147-6513(02)00010-6
Kuzovkina, I., Al’terman, I., & Schneider, B. (2004). Specific accumulation and revised structures of acridone alkaloid glucosides in the tips of transformed roots of Ruta graveolens. Phytochemistry, 65, 1095-100.
https://doi.org/10.1016/j.phytochem.2004.03.003
Li, X., Wang, J., Yu, M., Zhang, X., Wang, W., Tian, H., & Ru, S. (2019). 2,2′-Dithiobis-pyridine induced reproductive toxicity in male guppy (Poecilia reticulata). Ecotoxicology and Environmental Safety, 169, 778–785.
https://doi.org/10.1016/j.ecoenv.2018.11.076
Manibusan, M. K., & Touart, L. W. (2017). A comprehensive review of regulatory test methods for endocrine adverse health effects. Critical Reviews in Toxicology, 47, 433-481. doi.org/10.1080/10408444.2016.1272095
Matthiessen, P., Wheeler J. R., & Weltje, L. (2018). A review of the evidence for endocrine disrupting effects of current-use chemicals on wildlife populations. Critical Reviews in Toxicology, 48, 195-216.
https://doi.org/10.1080/10408444.2017.1397099
Maurya, R., Srivastava, S., Kulshreshta, D. K., & Gupta, C. M. (2004). Traditional remedies for fertility regulation. Current Medicinal Chemistry, 11, 1431–1450. http://doi.org/10.2174/0929867043365215
Meepagala, K. M., Schrader, K. K., Wedge, D. E., & Duke, S. O. (2005). Algicidal and antifungal compounds from the roots of Ruta graveolens and synthesis of their analogs. Phytochemistry, 66(22), 2689-2695.
https://doi.org/10.1016/j.phytochem.2005.09.019
Miguel, E. S. (2003). Rue in traditional Spain: frequency and distribution of its medicinal and symbolic applications. Economic Botany, 57, 231-244.
https://www.jstor.org/stable/4256681
Oliva, A., Meepagala, K. M., Wedge, D. E., Harries, D., Hale, A. L., Aliotta, G., & Duke, S. O. (2003). Natural fungicides from Ruta graveolens L. leaves, including a new quinolone alkaloid. Journal of Agricultural and Food Chemistry, 51, 890-896.
https://doi.org/10.1021/jf0259361
Pathak, S., Multani, A. S., Banerji, P., & Banerji, P. (2003). Ruta selectively induces cell death in brain cancer cells but proliferation in normal peripheral blood lymphocytes: a novel treatment for human brain cancer. International Journal of Oncology, 23, 975-982. http://doi.org/10.3892/ijo.23.4.975
Preethi, K. C., Kuttan, G., & Kuttan, R. (2006). Anti-tumour activity of Ruta graveolens extract. Asian Pacific Journal of Cancer Prevention, 7, 439-443.
Raghav, S. K., Gupta, B., Agrawal, C., Goswami, K., & Das, H. R. (2006). Anti-inflammatory effect of Ruta graveolens L. in murine macrophage cells. Journal of Ethnopharmacology, 104(1-2), 234-239.
https://doi.org/10.1016/j.jep.2005.09.008
Rodriguez, C. M. (1997). Phylogenetic analysis of the tribe Poeciliini (Cyprinodontiformes: Poeciliidae). Copeia, 1997(4), 663-679.
https://doi.org/10.2307/1447285
Sailani, M. R., & Moeini, H. (2007). Effect of Ruta graveolens and Cannabis sativa alcoholic extract on spermatogenesis in the adult wistar male rats. Indian Journal of Urology, 23, 257-60.
https://doi.org/10.4103%2F0970-1591.33720
Tian, H., Fotidis, I. A., Mancini, E., & Angelidaki, I. (2017). Different cultivation methods to acclimatise ammonia-tolerant methanogenic consortia. Bioresource Technology, 232, 1-9.
https://doi.org/10.1016/j.biortech.2017.02.034
Toft, G., & Baatrup, E. (2001). Sexual characteristics are altered by 4-tert-octylphenol and 17β-estradiol in the adult male guppy (Poecilia reticulata). Ecotoxicology and environmental safety, 48(1), 76-84. https://doi.org/10.1006/eesa.2000.1985
Walker, W. H. (2009). Molecular mechanisms of testosterone action in spermatogenesis. Steroids, 74(2), 602–607.
https://doi.org/10.1016/j.steroids.2008.11.017
Yilmaz, E., & Ergün, S. (2015). Influence of carvacrol on the growth performance, haematological, non-specific immune and serum biochemistry parameters in rainbow trout (Oncorhynchus mykiss). Food and Nutrition Sciences, 6(5), 523.