Research Article
BibTex RIS Cite

The effect of prolonged cold storage period on total lipid content and adult cannibalism of Tenebrio molitor

Year 2023, Volume: 8 Issue: 1, 62 - 68, 31.03.2023

Evrim Sönmez Necati Alp Erilli

https://doi.org/10.35229/jaes.1215263

Abstract

With the discovery that the larvae of Tenebrio molitor (Coleoptera: Tenebrionidae) have a high protein and lipid content in recent years, they are grown in mass as additive feed or live feed. However, one of the most common problems faced by producers in production facilities is cannibalism, which occurs as a result of population density. For this reason, especially when the population is very dense, producers separate the insects that are in the pupa or larvae stage from the culture and keep them in coolers such as refrigerators. Then, when needed, they take the insects out of the refrigerator and use them. However, because insects are ectotherm organisms, their life cycles are extremely dependent on temperature. Although the cold storage method extends the shelf life of insects, exposing them to low temperatures for long periods can both damage their life cycle and significantly affect their lipid and protein content. In this study, the effects of cold storage on total lipid content, total lipid percentage and cannibalism rate of T. molitor larvae, pupae and adults were evaluated. In first stage of the study, the larvae were fed until they weighed 100-190 mg (larval stages 12-17). Afterwards, they were randomly selected and exposed to cold for 10, 20 and 30 days. In the second stage of the study, the larvae were exposed to cold for 10, 20 and 30 days after pupation. Then, they were put under normal laboratory conditions and their development was expected to be completed, and lipid analyzes were made and cannibalism rates were checked. As a result, as the duration of exposure to cold increased, the total lipid content and percentages decreased in the larvae of the unfed control group, while it increased or remained constant in the unfed and cold-exposed group. In addition, cannibalism was observed in T. molitor adults when they werent fed, that is, in cases of hunger and thirst.

Keywords

developmental stage feeding flour worm temperature total lipid

References

  • Adámková, A., Adámek, M., Mlček, J., Borkovcová, M., Bednářová, M., Kouřimská, L., Skácel, J. & Vítová, E. (2017). Welfare of the mealworm (Tenebrio molitor) breeding with regard to nutrition value and food safety. Potravinarstvo Slovak Journal of Food Sciences, 11(1), 460-465. DOI: 10.5219/779.
  • Adámková, A., Mlček, J., Adámek, M., Borkovcová, M., Bednářová, M., Hlobilová, V., Knížková, I. & Juríková, T. (2020). Tenebrio molitor (Coleoptera: Tenebrionidae) optimization of rearing conditions to obtain desired nutritional values. Journal of Insect Science, 20, 1-10. DOI: 10.1093/jisesa/ieaa100.
  • Arbab, A. (2019). Effect of temperature on pupal development in meal worm Tenebrio molitor L. Indian Journal of Entomology, 81(4), 640-646. DOI: 10.5958/0974-8172.2019.00138.X.
  • Aguila, J.R., Suszko, J., Gibbs, A.G. & Hoshizaki, D.K. (2007). The role of larval fat cells in adult Drosophila melanogaster. Journal of Experimantal Biology, 210(6), 956-963. DOI: 10.1242/jeb.001586.
  • Costa, S., Pedro, S., Lourenço, H., Batista, I., Teixeira, B., Bandarra, N.M., Murta, D., Nunes, R. & Pires, C. (2020). Evaluation of Tenebrio molitor larvae as an alternative food source. NFS Journal, 21, 57-64. DOI: 10.1016/j.nfs.2020.10.001.
  • Deruytter, D., Coudron, C.L. & Teerlinck, S. (2019). Influence of crate size, oviposition time, number of adults and cannibalism on the reproduction of Tenebrio molitor. Journal of Insects as Food and Feed, 5(4), 1-10. DOI: 10.3920/JIFF2019.0018.
  • Dreassi, E., Cito, A., Zanfini, A., Materozzi, L., Botta, M. & Francardi, V. (2017). Dietary fatty acids influence the growth and fatty acid composition of the yellow mealworm Tenebrio molitor (Coleoptera: Tenebrionidae). Lipids, 52(3), 285-294. DOI: 10.1007/s11745-016-4220-3.
  • Errico, S., Spagnoletta, A., Verardi, A., Moliterni, S., Dimatteo, S. & Sangiorgio, P. (2021). Tenebrio molitor as a source of interesting natural compounds, their recovery processes, biological effects, and safety aspects. Comprehensive Reviwes in Food Science and Food Safety, 21,148-197. DOI: 10.1111/1541-4337.12863.
  • Finkel, A.J. (1948). The lipid composition of Tenebrio molitor larvae. Physiological Zoology, 21(2), 111- 133.
  • Folch, J., Lees, M. & Stanley, S.G.H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226(1), 497-509. DOI: 10.1016/s0021- 9258(18)64849-5.
  • Halloran, A., Muenke, C., Vantomme, P. & Van Huis, A. (2014). Insects in the human food chain: global status and opportunities. Food Chain, 4(2), 103-118. DOI: 10.3362/2046-1887.2014.011.
  • Ichikawa, T. & Kurauchi, T. (2009). Larval cannibalism and pupal defense against cannibalism in two species of Tenebrionid beetles. Zoological Science, 26(8), 525- 529. DOI: 10.2108/zsj.26.525.
  • Irwin, J.T. & Lee, R.E.Jr. (2003). Cold winter microenvironments conserve energy and improve overwintering survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis. Oikos, 100(1), 71-78. DOI: 10.1034/j.1600- 0706.2003.11738.x.
  • Jones, L.D., Cooper, R.W. & Harding, R.S. (1972). Composition of mealworm Tenebrio molitor larvae. The Journal of Zoo Animal Medicine, 3(4), 34-41.
  • Liu, C., Masri, J., Perez, V., Maya, C. & Zhao, J. (2020). Growth performance and nutrient composition of mealworms (Tenebrio molitor) fed on fresh plant materials-supplemented diets. Foods, 9(2), 151. DOI: 10.3390/foods9020151.
  • Levie, A., Vernon, P. & Hance, T. (2005). Consequences of acclimation on survival and reproductive capacities of coldstored mummies of Aphidius rhopalosiphi (Hymenoptera: Aphidiinae). Journal of Economical Entomology, 98(3), 704-708.
  • Marshall, K.E. & Sinclair, B.J. (2012). Threshold temperatures mediate the impact of reduced snow cover on overwintering freeze-tolerant caterpillars. Naturwissenschaften, 99, 33-41.
  • Mirzaeva, D.A., Khujamshukurov, N.A., Zokirov, B., Soxibov, B.O. & Kuchkarova, DKh. (2020). Influence of temperature and humidity on the development of Tenebrio molitor L. International Journal of Current Microbiology and Applied Sciences, 9(4), 3544-3559. DOI: 10.20546/ijcmas.2020.905.422.
  • Mlček, J., Adámková, A., Adámek, M., Borkovcová, M., Bednářová, M. & Knížková, I. (2019). Fat from Tenebrionidae bugs – sterols content, fatty acid profiles, and cardiovascular risk indexes. Polish Journan of Food and Nutrition Sciences, 69(3), 247- 254. DOI: 10.31883/pjfns/109666.
  • Morales-Ramos, J.A., Rojas, M.G., Kay, S., Shapiro-lIan, D.I. & Tedders, W.L. (2012). Impact of adult weight, density, and age on reproduction of Tenebrio molitor (Coleoptera: Tenebrionidae). Journal of Entomological Science, 47(3), 208-220. DOI: 10.18474/0749-8004-47.3.208.
  • Morales-Ramos, J.A., Rojas, M.G, Shelby, K.S. & Coudron, T.A. (2015). Nutritional value of pupae versus larvae of Tenebrio molitor (Coleoptera: Tenebrionidae) as food for rearing Podisus maculiventris (Heteroptera: Pentatomidae). Journal of Economical Entomology, 109(2), 564-571. DOI: 10.1093/jee/tov338.
  • Nevesa, R.C.S., Torresa, J.B. & Zanunciob, J.C. (2010). Production and storage of mealworm beetle as prey for predatory stinkbug. Biocontrol Science and Technology, 20(10), 1013-1025. DOI: 10.1080/09583157.2010.500718.
  • Ochieng-Odero, J.P.R. (1992). The effect of three constant temperatures on larval critical weight, latent feding period, larval maximal weight and fecundity of Cnephasia jactatana (Walker) (Lepidoptera: Tortricidae). Journal of Insect Physiology, 38(2), 127-130. DOI: 10.1016/0022-1910(92)90041-B.
  • Oonincx, D.G.A.B., Van Broekhoven, S., Van Huis, A. & Van Loon J.J.A. (2015). Feed conversion, survival and development, and composition of four insect species on diets composed of food by-products. Plos One, 10(12), 1-20. DOI: 10.1371/journal.pone.0144601.
  • Ravzanaadii, N., Kim, S., Choi, W.H., Hong, S. & Kim, N.J. (2012). Nutritional value of mealworm, Tenebrio molitor as food source. International Journal of Industrial Entomology, 25(1), 93-98. DOI: 10.7852/ijie.2012.25.1.093.
  • Sasmita, H.I., Tu, W., Bong, L. & Neoh, K. (2019). Effects of larval diets and temperature regimes on life history traits, energy reserves and temperature tolerance of male Aedes aegypti (Diptera: Culicidae): optimizing rearing techniques for the sterile insect programmes. Vectors, 12, 2-16. DOI: 10.1186/s13071-019-3830-z.
  • Sinclair, B.J. & Marshall, K.E. (2018). The many roles of fats in overwintering insects. Journal of Experimental Biology, 7(221), 1-9. DOI: 10.1242/jeb.161836.
  • Sørensen, J.G., Addison M.F. & Terblanche J.S. (2012). Mass-rearing of insects for pest management: Challenges, synergies and advancesfrom evolutionary physiology. Crop Protection, 38, 87- 94. DOI: 10.1016/j.cropro.2012.03.023.
  • Sönmez, E. (2021). The effect of different cold storage period on total lipid amount of Tenebrio molitor (Coleoptera: Tenebrionidae) larvae. Journal of Anatolian Environmental and Animal Sciences, 6(3), 449-455. DOI: 10.35229/jaes.970307.
  • Stanley-Samuelson, D.W., Jurenka, R.A., Cripps, C., Blomquist, G.J. & Renobales, M. (1988). Fatty acids in insects: composition, metabolism, and biological significance. Archive of Insect Biochemistry and Physiology, 9(1), 1-33. DOI: 10.1002/arch.940090102.
  • Van Broekhoven, S., Oonincx, D.G., Van Huis, A. & Van Loon, J.J. (2015). Growth performance and feed conversion efficiency of three edible mealworm species (Coleoptera: Tenebrionidae) on diets composed of organic by-products. Journal of Insect Physiology, 73, 1-10. DOI: 10.1016/j.jinsphys.2014.12.005.
  • Via, S. (1999). Cannibalism facilitates the use of a novel environment in the flour beetle, Tribolium castaneum. Heredity, 82(3), 267-275. DOI: 10.1038/sj.hdy.6884820.
  • Weaver, D.K. & McFarlane, J.E. (1990). The effect of larval density on growth and development of Tenebrio molitor. Journal of Insect Physiology, 36(7), 531- 536. DOI: 10.1016/0022-1910(90)90105-O.
  • Zaelor, J. & Kitthawee, S. (2018). Growth response to population density in larval stage of darkling beetles (Coleoptera; Tenebrionidae) Tenebrio molitor and Zophobas atratus. Agriculture and Natural Resources, 52(6), 603-606. DOI: 10.1016/j.anres.2018.11.004.

Soğukta bekletme süresinin uzamanasının Tenebrio molitor’un toplam lipid miktarına ve ergin yamyamlığına etkisi

Year 2023, Volume: 8 Issue: 1, 62 - 68, 31.03.2023

Evrim Sönmez Necati Alp Erilli

https://doi.org/10.35229/jaes.1215263

Abstract

Tenebrio molitor (Coleoptera: Tenebrionidae) larvalarının son yıllarda protein ve lipit içeriğinin yüksek olduğunun keşfedilmesi ile katkı yemi veya canlı yem olarak kitlesel olarak yetiştirilmektedir. Fakat üretim tesislerinde üreticilerin en sık karşılaştığı sorunlardan biri popülasyon yoğunluğu sonucu ortaya çıkan kanibalizmdir. Bu nedenle özellikle popülasyon çok yoğun olduğu dönemlerde üreticiler pupa aşamasında olan böcekleri kültürden ayırarak ya başka kaplarda ya da larva ve pupaları buzdolabı gibi soğutucularda bekletmektedirler. Daha sonra ihtiyaç olduğunda böcekleri buzdolabından çıkarıp kullanmaktadırlar. Fakat böcekler ektoterm canlılar olduklarından yaşam döngüleri aşırı derecede sıcaklığa bağımlıdır. Soğukta depolama yöntemi böceklerin raf ömrünü uzatmakla birlikte uzun süreler düşük sıcaklığa maruz bırakmak onların yaşam döngülerine hem zarar verebilir hem de içerdikleri yağ ve protein oranını önemli derecede etkileyebilir. Bu çalışmada soğukta depolamanın T. molitor larva, pupa ve erginlerinin toplam yağ miktarı, toplam yağ yüzdesi ve kanibalizm oranına etkileri değerlendirildi. Çalışmanın ilk aşamasında larvalar 100-190 mg (12-17. larval aşamadakiler) ağırlığa gelene kadar beslendi ve sonrasında rastgele seçilerek 10, 20 ve 30 gün boyunca soğuğa maruz bırakıldı. Çalışmanın ikinci aşamasında larvalar pupa olduktan sonra 10, 20 ve 30 gün boyunca soğuğa maruz bırakıldı. Sonra normal laboratuvar şartlarına alınarak gelişimlerinin tamamlanması beklendi ve yağ analizleri yapılarak, kanibalizm oranlarına bakıldı. Sonuç olarak soğuğa maruz kalma süresi uzadıkça beslenmemiş kontrol grubu larvalarda toplam yağ miktarı ve yüzdeleri düşmüş, beslenmemiş ve soğuğa maruz kalmış grubun ise artmış veya sabit kalmıştır. Ayrıca T. molitor erginlerinde beslenmedikleri zaman yani açlık ve susuzluk durumlarında kanibalizm görülmüştür.

Keywords

beslenme gelişim aşamaları sıcaklık unkurdu toplam lipid

References

  • Adámková, A., Adámek, M., Mlček, J., Borkovcová, M., Bednářová, M., Kouřimská, L., Skácel, J. & Vítová, E. (2017). Welfare of the mealworm (Tenebrio molitor) breeding with regard to nutrition value and food safety. Potravinarstvo Slovak Journal of Food Sciences, 11(1), 460-465. DOI: 10.5219/779.
  • Adámková, A., Mlček, J., Adámek, M., Borkovcová, M., Bednářová, M., Hlobilová, V., Knížková, I. & Juríková, T. (2020). Tenebrio molitor (Coleoptera: Tenebrionidae) optimization of rearing conditions to obtain desired nutritional values. Journal of Insect Science, 20, 1-10. DOI: 10.1093/jisesa/ieaa100.
  • Arbab, A. (2019). Effect of temperature on pupal development in meal worm Tenebrio molitor L. Indian Journal of Entomology, 81(4), 640-646. DOI: 10.5958/0974-8172.2019.00138.X.
  • Aguila, J.R., Suszko, J., Gibbs, A.G. & Hoshizaki, D.K. (2007). The role of larval fat cells in adult Drosophila melanogaster. Journal of Experimantal Biology, 210(6), 956-963. DOI: 10.1242/jeb.001586.
  • Costa, S., Pedro, S., Lourenço, H., Batista, I., Teixeira, B., Bandarra, N.M., Murta, D., Nunes, R. & Pires, C. (2020). Evaluation of Tenebrio molitor larvae as an alternative food source. NFS Journal, 21, 57-64. DOI: 10.1016/j.nfs.2020.10.001.
  • Deruytter, D., Coudron, C.L. & Teerlinck, S. (2019). Influence of crate size, oviposition time, number of adults and cannibalism on the reproduction of Tenebrio molitor. Journal of Insects as Food and Feed, 5(4), 1-10. DOI: 10.3920/JIFF2019.0018.
  • Dreassi, E., Cito, A., Zanfini, A., Materozzi, L., Botta, M. & Francardi, V. (2017). Dietary fatty acids influence the growth and fatty acid composition of the yellow mealworm Tenebrio molitor (Coleoptera: Tenebrionidae). Lipids, 52(3), 285-294. DOI: 10.1007/s11745-016-4220-3.
  • Errico, S., Spagnoletta, A., Verardi, A., Moliterni, S., Dimatteo, S. & Sangiorgio, P. (2021). Tenebrio molitor as a source of interesting natural compounds, their recovery processes, biological effects, and safety aspects. Comprehensive Reviwes in Food Science and Food Safety, 21,148-197. DOI: 10.1111/1541-4337.12863.
  • Finkel, A.J. (1948). The lipid composition of Tenebrio molitor larvae. Physiological Zoology, 21(2), 111- 133.
  • Folch, J., Lees, M. & Stanley, S.G.H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226(1), 497-509. DOI: 10.1016/s0021- 9258(18)64849-5.
  • Halloran, A., Muenke, C., Vantomme, P. & Van Huis, A. (2014). Insects in the human food chain: global status and opportunities. Food Chain, 4(2), 103-118. DOI: 10.3362/2046-1887.2014.011.
  • Ichikawa, T. & Kurauchi, T. (2009). Larval cannibalism and pupal defense against cannibalism in two species of Tenebrionid beetles. Zoological Science, 26(8), 525- 529. DOI: 10.2108/zsj.26.525.
  • Irwin, J.T. & Lee, R.E.Jr. (2003). Cold winter microenvironments conserve energy and improve overwintering survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis. Oikos, 100(1), 71-78. DOI: 10.1034/j.1600- 0706.2003.11738.x.
  • Jones, L.D., Cooper, R.W. & Harding, R.S. (1972). Composition of mealworm Tenebrio molitor larvae. The Journal of Zoo Animal Medicine, 3(4), 34-41.
  • Liu, C., Masri, J., Perez, V., Maya, C. & Zhao, J. (2020). Growth performance and nutrient composition of mealworms (Tenebrio molitor) fed on fresh plant materials-supplemented diets. Foods, 9(2), 151. DOI: 10.3390/foods9020151.
  • Levie, A., Vernon, P. & Hance, T. (2005). Consequences of acclimation on survival and reproductive capacities of coldstored mummies of Aphidius rhopalosiphi (Hymenoptera: Aphidiinae). Journal of Economical Entomology, 98(3), 704-708.
  • Marshall, K.E. & Sinclair, B.J. (2012). Threshold temperatures mediate the impact of reduced snow cover on overwintering freeze-tolerant caterpillars. Naturwissenschaften, 99, 33-41.
  • Mirzaeva, D.A., Khujamshukurov, N.A., Zokirov, B., Soxibov, B.O. & Kuchkarova, DKh. (2020). Influence of temperature and humidity on the development of Tenebrio molitor L. International Journal of Current Microbiology and Applied Sciences, 9(4), 3544-3559. DOI: 10.20546/ijcmas.2020.905.422.
  • Mlček, J., Adámková, A., Adámek, M., Borkovcová, M., Bednářová, M. & Knížková, I. (2019). Fat from Tenebrionidae bugs – sterols content, fatty acid profiles, and cardiovascular risk indexes. Polish Journan of Food and Nutrition Sciences, 69(3), 247- 254. DOI: 10.31883/pjfns/109666.
  • Morales-Ramos, J.A., Rojas, M.G., Kay, S., Shapiro-lIan, D.I. & Tedders, W.L. (2012). Impact of adult weight, density, and age on reproduction of Tenebrio molitor (Coleoptera: Tenebrionidae). Journal of Entomological Science, 47(3), 208-220. DOI: 10.18474/0749-8004-47.3.208.
  • Morales-Ramos, J.A., Rojas, M.G, Shelby, K.S. & Coudron, T.A. (2015). Nutritional value of pupae versus larvae of Tenebrio molitor (Coleoptera: Tenebrionidae) as food for rearing Podisus maculiventris (Heteroptera: Pentatomidae). Journal of Economical Entomology, 109(2), 564-571. DOI: 10.1093/jee/tov338.
  • Nevesa, R.C.S., Torresa, J.B. & Zanunciob, J.C. (2010). Production and storage of mealworm beetle as prey for predatory stinkbug. Biocontrol Science and Technology, 20(10), 1013-1025. DOI: 10.1080/09583157.2010.500718.
  • Ochieng-Odero, J.P.R. (1992). The effect of three constant temperatures on larval critical weight, latent feding period, larval maximal weight and fecundity of Cnephasia jactatana (Walker) (Lepidoptera: Tortricidae). Journal of Insect Physiology, 38(2), 127-130. DOI: 10.1016/0022-1910(92)90041-B.
  • Oonincx, D.G.A.B., Van Broekhoven, S., Van Huis, A. & Van Loon J.J.A. (2015). Feed conversion, survival and development, and composition of four insect species on diets composed of food by-products. Plos One, 10(12), 1-20. DOI: 10.1371/journal.pone.0144601.
  • Ravzanaadii, N., Kim, S., Choi, W.H., Hong, S. & Kim, N.J. (2012). Nutritional value of mealworm, Tenebrio molitor as food source. International Journal of Industrial Entomology, 25(1), 93-98. DOI: 10.7852/ijie.2012.25.1.093.
  • Sasmita, H.I., Tu, W., Bong, L. & Neoh, K. (2019). Effects of larval diets and temperature regimes on life history traits, energy reserves and temperature tolerance of male Aedes aegypti (Diptera: Culicidae): optimizing rearing techniques for the sterile insect programmes. Vectors, 12, 2-16. DOI: 10.1186/s13071-019-3830-z.
  • Sinclair, B.J. & Marshall, K.E. (2018). The many roles of fats in overwintering insects. Journal of Experimental Biology, 7(221), 1-9. DOI: 10.1242/jeb.161836.
  • Sørensen, J.G., Addison M.F. & Terblanche J.S. (2012). Mass-rearing of insects for pest management: Challenges, synergies and advancesfrom evolutionary physiology. Crop Protection, 38, 87- 94. DOI: 10.1016/j.cropro.2012.03.023.
  • Sönmez, E. (2021). The effect of different cold storage period on total lipid amount of Tenebrio molitor (Coleoptera: Tenebrionidae) larvae. Journal of Anatolian Environmental and Animal Sciences, 6(3), 449-455. DOI: 10.35229/jaes.970307.
  • Stanley-Samuelson, D.W., Jurenka, R.A., Cripps, C., Blomquist, G.J. & Renobales, M. (1988). Fatty acids in insects: composition, metabolism, and biological significance. Archive of Insect Biochemistry and Physiology, 9(1), 1-33. DOI: 10.1002/arch.940090102.
  • Van Broekhoven, S., Oonincx, D.G., Van Huis, A. & Van Loon, J.J. (2015). Growth performance and feed conversion efficiency of three edible mealworm species (Coleoptera: Tenebrionidae) on diets composed of organic by-products. Journal of Insect Physiology, 73, 1-10. DOI: 10.1016/j.jinsphys.2014.12.005.
  • Via, S. (1999). Cannibalism facilitates the use of a novel environment in the flour beetle, Tribolium castaneum. Heredity, 82(3), 267-275. DOI: 10.1038/sj.hdy.6884820.
  • Weaver, D.K. & McFarlane, J.E. (1990). The effect of larval density on growth and development of Tenebrio molitor. Journal of Insect Physiology, 36(7), 531- 536. DOI: 10.1016/0022-1910(90)90105-O.
  • Zaelor, J. & Kitthawee, S. (2018). Growth response to population density in larval stage of darkling beetles (Coleoptera; Tenebrionidae) Tenebrio molitor and Zophobas atratus. Agriculture and Natural Resources, 52(6), 603-606. DOI: 10.1016/j.anres.2018.11.004.
There are 34 citations in total.

Details

Primary Language English
Journal Section Articles
Authors

Evrim Sönmez 0000-0002-5412-5728

Necati Alp Erilli 0000-0001-6948-0880

Publication Date March 31, 2023
Submission Date December 6, 2022
Acceptance Date February 8, 2023
Published in Issue Year 2023 Volume: 8 Issue: 1

Cite

APA Sönmez, E., & Erilli, N. A. (2023). The effect of prolonged cold storage period on total lipid content and adult cannibalism of Tenebrio molitor. Journal of Anatolian Environmental and Animal Sciences, 8(1), 62-68. https://doi.org/10.35229/jaes.1215263
 Download Cover Image


13221            13345           13349              13352              13353              13354          13355    13356   13358   13359   13361     13363   13364                crossref1.png            
         Paperity.org                                  13369                                         EBSCOHost                                                        Scilit                                                    CABI   
JAES/AAS-Journal of Anatolian Environmental and Animal Sciences/Anatolian Academic Sciences&Anadolu Çevre ve Hayvancılık Dergisi/Anadolu Akademik Bilimler-AÇEH/AAS