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Influence of dietary indole-3-acetic acid on phenoloxidase and hemolytic activities in Pimpla turionellae L., 1758 (Hymenoptera: Ichneumonidae) and Galleria mellonella L., 1758 (Lepidoptera: Pyralidae) in a host-parasitoid system

Year 2022, Volume: 46 Issue: 2, 149 - 158, 01.06.2022
https://doi.org/10.16970/entoted.1039327

Abstract

The continuity of food demand has caused modern agriculture to be heavily dependent on chemical inputs. Plant growth regulators (PGRs) are naturally occurring or synthetic compounds that have the potential to control pest insects through their chemosterilant activity. Along with pests, non-target organisms such as parasitoids in agroecological systems are likely to be influenced by indirect contact via their hosts or direct contact with hosts and plants at the tritrophic level. This study demonstrated the dietary effects of PGR indole-3-acetic acid (IAA) on hemolytic activity and phenoloxidase activity in stored product pest Galleria mellonella L., 1758 (Lepidoptera: Pyralidae) and parasitoid Pimpla turionellae L., 1758 (Hymenoptera: Ichneumonidae). The significant increase in hemolytic activity in G. mellonella and P. turionellae hemolymph were observed in 500, 5,000 and 10,000 ppm IAA-treated groups. Phenoloxidase activity in G. mellonella hemolymph significantly decreased with all IAA doses compared to control, however, the reductions in phenoloxidase activity in P. turionellae hemolymph were significant between 500 and 10,000 ppm. Since IAA interacts with both host and parasitoid immunity, it should be used with caution in agricultural areas with high host-parasitoid population.

Supporting Institution

Kocaeli University, Scientific Research Coordination Unit, Türkiye

Project Number

Grant Project No: 2014/068.

References

  • Abdellaoui, K., M. B. Halima-Kamel, N. Soltani, N. Aribi & M. H. B. Hamouda, 2013. Biochemical and histological effects of gibberellic acid on Locusta migratoria fifth instar larvae. Pesticide Biochemistry & Physiology, 107 (1): 32-37.
  • Ahmad, F., I. Ahmad & M. S. Khan, 2005. Indole acetic acid production by the indigenous isolates of azotobacter and fluorescent Pseudomonas in the presence and absence of tryptophan. Turkish Journal of Biology, 29 (1): 29-34.
  • Altuntaş, H., 2015. Determination of gibberellic acid (GA3)-induced oxidative stress in a model organism Galleria mellonella L. (Lepidoptera: Pyralidae). Environmental Entomology, 44 (1): 100-105.
  • Altuntaş, H., R. Gwokyalya & N. Bayram, 2021. Immunotoxic effects of force-fed ethephon on model organism Galleria mellonella (Lepidoptera: Pyralidae). Drug and Chemical Toxicology, 18: 1-8.
  • An, C., M. Zhang, Y. Chu & Z. Zhao, 2013. Serine protease MP2 activates prophenoloxidase in the melanization immune response of Drosophila melanogaster. PloS One, 8 (11): e79533.
  • Bradford, M. M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72 (1): 248-254.
  • Bronskill, J. F., 1961. A cage to simplify the rearing of the greater wax moth, Galleria mellonella (Pyralidae). Journal of the Lepidopterists' Society, 15 (1): 102-104.
  • Brzozowski, L. & M. Mazourek, 2018. A sustainable agricultural future relies on the transition to organic agroecological pest management. Sustainability, 10 (6): 2023.
  • Çelik, D., R. Özbek & F. Uçkan, 2017. Effects of indole-3-acetic acid on hemocytes of Achoria grisella Fabr. (Lepidoptera: Pyralidae). Journal of the Entomological Research Society, 19 (2): 83-93.
  • Eleftherianos, I. & C. Revenis, 2011. Role and importance of phenoloxidase in insect hemostasis. Journal of Innate Immunity, 3 (1): 28-33.
  • Er, A. & M. Keskin, 2016. Influence of abscisic acid on the biology and hemocytes of the model insect Galleria mellonella (Lepidoptera: Pyralidae). Annals of the Entomological Society of America, 109 (2): 244-251.
  • Ghoneim, K., 2018. Role of plant growth regulators in the insect pest control: a quick outlook. Environmental Analyses & Ecological Studies, 4 (1): 1-2.
  • Gillespie, J. P., M. R. Kanost & T. Trenczek, 1997. Biological mediators of insect immunity. Annual Review of Entomology, 42 (1): 611-643.
  • Greco, I., N. Molchanova & E. Holmedal, 2020. Correlation between hemolytic activity, cytotoxicity and systemic in vivo toxicity of synthetic antimicrobial peptides. Scientific Reports, 10 (1): 13206.
  • Guzman, M. A., J. L. Ochoa & F. Vargas-Albores, 1993. Hemolytic activity in the brown shrimp (Penaeus californiensis Holmes) haemolymph. Comparative Biochemistry & Physiology, 106A (2): 271-275.
  • James, R. R. & J. Xu, 2012. Mechanisms by which pesticides affect insect immunity. Journal of Invertebrate Pathology, 109 (2):175-182.
  • Kaya, S., G. Akkuş, S. Türkdoğan & B. Gündüz, 2021a. Influence of Helichrysum arenarium on hemocyte-mediated immune responses and phenoloxidase enzyme activity of model organism Galleria mellonella (L.). International Journal of Tropical Insect Science, 41 (4): 2521-2528.
  • Kaya, S., F. Uçkan & A. Er, 2021b. Influence of Indole-3-Acetic Acid on Cellular Immune Responses of Galleria mellonella L. (Lepidoptera: Pyralidae) and Pimpla turionellae L. (Hymenoptera: Ichneumonidae) in a host-parasitoid system. International Journal of Tropical Insect Science, 41 (1): 169-179.
  • Kefford, B. J., L. Zalizniak, M. S. J. Warne & D. Nugegoda, 2008. Is the integration of hormesis and essentiality into ecotoxicology now opening Pandora’s box? Environmental Pollution, 151 (3): 516-523.
  • Lee, W., J. Lee, R. Kulkarni, M.-A. Kim, J. S. Hwang M. K. Na & J.-S. Bae, 2016. Antithrombotic and antiplatelet activities of small-molecule alkaloids from Scolopendra subspinipes mutilans. Scientific Reports, 6: 21956 (12pp).
  • Lins, P. G., C. R. Valle, S. M. P. Pugine, D. L. Oliveira, M. S. L. Ferreira, E. J. X. Costa & M. P. De Melo, 2006. Effect of indole acetic acid administration on the neutrophil functions and oxidative stress from neutrophil, mesenteric lymph node and liver. Life Sciences, 78 (6): 564-570.
  • Mu, J., T. Uehara & T. Furuno, 2003. Effect of bamboo vinegar on regulation of germination and radicle growth of seed plants. Journal of Wood Science, 49 (3): 262-270.
  • Nasr, H. M., M. E. I. Badawy & E. Rabea, 2010. Toxicity and biochemical study of two insect growth regulators, buprofezin and pyriproxyfen, on cotton leafworm Spodoptera littoralis. Pesticide Biochemistry & Physiology, 98 (2): 198-205.
  • Özyılmaz, D., R. Özbek, H. Altuntaş & F. Uçkan, 2019. Indole-3-Acetic Acid induced oxidative stress in model host Galleria mellonella L. (Lepidoptera: Pyralidae) and its endoparasitoid Pimpla turionellae (L.) (Hymenoptera: Ichneumonidae). Invertebrate Survival Journal, 16 (1): 184-188.
  • Pech, L. L. & M. R. Strand, 2000. Plasmatocytes from the moth Pseudoplusia includens induce apoptosis of granular cells. Journal of Insect Physiology, 46 (12): 1565-1573.
  • Phipps, D. J., J. S. Chadwick, R. G. Leeder & W. P. Aston, 1989. The hemolytic activity of Galleria mellonella hemolymph. Developmental and Comparative Immunology, 13 (2): 103-111.
  • Prado, S. G. & S. D. Frank, 2013. Tritrophic effects of plant growth regulators in an aphid-parasitoid system. Biological Control, 66 (1): 72-76.
  • Santoyo, I. G. & A. C. Aguilar, 2011. Phenoloxidase: a key component of the insect immune system. Entomologia Experimentalis et Applicata, 142 (1): 1-16.
  • Sasaki, T., T. Hiraoka & M. Kobayashi, 2010. Hemolytic activity is mediated by the endogenous lectin in the mosquito hemolymph serum. Journal of Insect Physiology, 56 (9): 1032-1039.
  • SPSS, 2018. IBM SPSS Statistics for Windows, Version 20. Armonk, NY.
  • Şeker, D. A., A. Yanıkoğlu, 1999. Pimpla turionellae L. (Hymenoptera: Ichneumonidae)’nın açlık, beslenme, parazitleme ve yaşlılık durumlarında glikojen seviyesindeki değişmeler. Turkish Journal of Zoology, 23 (1): 289-296 (in Turkish with abstract in English).
  • Strand, M. D., 2008. The insect cellular immune response. Insect Science, 15 (1): 1-14.
  • Uçkan, F., İ. Haftacı & E. Ergin, 2011a. Effects of indol-3-acetic acid on biological parameters of the larval endoparasitoid Apanteles galleriae (Hymenoptera: Braconidae). Annals of the Entomological Society of America, 104 (1): 77-82.
  • Uçkan, F., R. Özbek & E. Ergin, 2015. Effects of Indol-3-Acetic Acid on the biology of Galleria mellonella and its endoparasitoid Pimpla turionellae. Belgian Journal of Zoology, 145 (1): 49-58.
  • Uçkan, F., Z. Öztürk, H. Altuntaş & E. Ergin, 2011b. Effects of gibberellic acid (GA3) on biological parameters and hemolymph metabolites of the pupal endoparasitoid Pimpla turionellae (Hymenoptera: Ichneumonidae) and its host Galleria mellonella (Lepidoptera: Pyralidae). Journal of the Entomological Research Society, 13 (3): 1-14.
  • Uçkan, F., H. K. Soydabaş & R. Özbek, 2014. Effect of indol-3-acetic acid on the biochemical parameters of Achoria grisella hemolymph and Apanteles galleriae larva. Pakistan Journal of Biotechnology, 11 (2): 163-171.
  • Uçkan, F., A. Tüven, A. Er & E. Ergin, 2008. Effects of gibberellic acid on biological parameters of the larval endoparasitoid Apanteles galleriae (Hymenoptera: Braconidae). Annals of the Entomological Society of America, 101 (3): 593-597.
  • Wang, X. Y., S. F. Bai, X. Li, X. M. Yin & X. C. Li, 2015. The endoparasitoid Campoletis chlorideae induces a hemolytic factor in the herbivorous insect Helicoverpa armigera. Archives of Insect Biochemistry and Physiology, 90 (1): 14-27.
  • Wang, Z. Z., Y. Q. Liu, M. Shi, J. H. Huang & X. X. Chen, (2019). Parasitoid wasps as effective biological control agents. Journal of Integrative Agriculture, 18 (4): 705-715.
  • Wojda, I., 2017. Immunity of the greater wax moth Galleria mellonella. Insect Science, 24 (3): 342-357.
  • Zhao, H., H. H. Cao & M. Z. Pan, 2017. The role of plant growth regulators in a plant-aphid-parasitoid tritrophic system. Journal of Plant Growth Regulation, 36 (4): 868-876.
  • Zibaee, A. & A. R. Bandani, 2010. Effects of Artemisia annua L. (Asteracea) on the digestive enzymatic profiles and the cellular immune reactions of the sunn pest, Eurygaster integriceps (Heteroptera: Scutellaridae), against Beauveria bassiana. Bulletin of Entomological Research,100 (2): 185-196.

Indole-3 asetik asit’in Pimpla turionellae L., 1758 (Hymenoptera: Ichneumonidae) ve Galleria mellonella L., 1758 (Lepidoptera: Pyralidae)’nın konukçu-parazitoit sisteminde fenoloksidaz ve hemolitik aktivitelerine beslenme yoluyla etkileri

Year 2022, Volume: 46 Issue: 2, 149 - 158, 01.06.2022
https://doi.org/10.16970/entoted.1039327

Abstract

Gıda ihtiyacının sürekliliği, modern tarımın büyük ölçüde kimyasal girdilere bağımlı hale gelmesine neden olmuştur. Bitki büyüme düzenleyicileri, kemosterilant aktiviteye sahip doğal olarak oluşan veya sentetik bitki kaynaklı kimyasallardır ve zararlı böcekleri baskılama potansiyeline sahiptir. Zararlılarla birlikte, agroekolojik sistemlerdeki parazitoitler gibi hedef olmayan organizmaların, konukçuları aracılığıyla dolaylı temastan veya konukçu ve bitkilerle tritrofik etkileşim yoluyla doğrudan temastan etkilenmesi muhtemeldir. Bu çalışma bitki büyüme düzenleyicisi indol-3-asetik asidin (IAA) depolanmış ürün zararlısı Galleria mellonella L., 1758 (Lepidoptera: Pyralidae) ve parazitoit Pimpla turionellae L., 1758 (Hymenoptera: Ichneumonidae)’nın hemolitik aktivitesi ve fenoloksidaz aktivitesi üzerindeki besinsel etkilerini göstermektedir. Galleria mellonella ve P. turionellae hemolenfinin hemolitik aktivitelerinde istatistiksel olarak önemli artışlar 500, 5000 ve 10000 ppm IAA dozları tatbik edilen gruplarda gözlenmiştir. Galleria mellonella hemolenfinin fenoloksidaz aktivitesi, kontrole kıyasla tüm IAA uygulanan dozlarda önemli ölçüde azalırken, P. turionellae hemolenf fenoloksidaz aktivitesindeki azalmalar 500 ve 10000 ppm arasında anlamlı bulundu. IAA, hem konukçu hem de parazitoit bağışıklığı ile etkileşime girdiğinden, konukçu-parazitoit popülasyonu yüksek olan tarım alanlarında dikkatle kullanılmalıdır.

Project Number

Grant Project No: 2014/068.

References

  • Abdellaoui, K., M. B. Halima-Kamel, N. Soltani, N. Aribi & M. H. B. Hamouda, 2013. Biochemical and histological effects of gibberellic acid on Locusta migratoria fifth instar larvae. Pesticide Biochemistry & Physiology, 107 (1): 32-37.
  • Ahmad, F., I. Ahmad & M. S. Khan, 2005. Indole acetic acid production by the indigenous isolates of azotobacter and fluorescent Pseudomonas in the presence and absence of tryptophan. Turkish Journal of Biology, 29 (1): 29-34.
  • Altuntaş, H., 2015. Determination of gibberellic acid (GA3)-induced oxidative stress in a model organism Galleria mellonella L. (Lepidoptera: Pyralidae). Environmental Entomology, 44 (1): 100-105.
  • Altuntaş, H., R. Gwokyalya & N. Bayram, 2021. Immunotoxic effects of force-fed ethephon on model organism Galleria mellonella (Lepidoptera: Pyralidae). Drug and Chemical Toxicology, 18: 1-8.
  • An, C., M. Zhang, Y. Chu & Z. Zhao, 2013. Serine protease MP2 activates prophenoloxidase in the melanization immune response of Drosophila melanogaster. PloS One, 8 (11): e79533.
  • Bradford, M. M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72 (1): 248-254.
  • Bronskill, J. F., 1961. A cage to simplify the rearing of the greater wax moth, Galleria mellonella (Pyralidae). Journal of the Lepidopterists' Society, 15 (1): 102-104.
  • Brzozowski, L. & M. Mazourek, 2018. A sustainable agricultural future relies on the transition to organic agroecological pest management. Sustainability, 10 (6): 2023.
  • Çelik, D., R. Özbek & F. Uçkan, 2017. Effects of indole-3-acetic acid on hemocytes of Achoria grisella Fabr. (Lepidoptera: Pyralidae). Journal of the Entomological Research Society, 19 (2): 83-93.
  • Eleftherianos, I. & C. Revenis, 2011. Role and importance of phenoloxidase in insect hemostasis. Journal of Innate Immunity, 3 (1): 28-33.
  • Er, A. & M. Keskin, 2016. Influence of abscisic acid on the biology and hemocytes of the model insect Galleria mellonella (Lepidoptera: Pyralidae). Annals of the Entomological Society of America, 109 (2): 244-251.
  • Ghoneim, K., 2018. Role of plant growth regulators in the insect pest control: a quick outlook. Environmental Analyses & Ecological Studies, 4 (1): 1-2.
  • Gillespie, J. P., M. R. Kanost & T. Trenczek, 1997. Biological mediators of insect immunity. Annual Review of Entomology, 42 (1): 611-643.
  • Greco, I., N. Molchanova & E. Holmedal, 2020. Correlation between hemolytic activity, cytotoxicity and systemic in vivo toxicity of synthetic antimicrobial peptides. Scientific Reports, 10 (1): 13206.
  • Guzman, M. A., J. L. Ochoa & F. Vargas-Albores, 1993. Hemolytic activity in the brown shrimp (Penaeus californiensis Holmes) haemolymph. Comparative Biochemistry & Physiology, 106A (2): 271-275.
  • James, R. R. & J. Xu, 2012. Mechanisms by which pesticides affect insect immunity. Journal of Invertebrate Pathology, 109 (2):175-182.
  • Kaya, S., G. Akkuş, S. Türkdoğan & B. Gündüz, 2021a. Influence of Helichrysum arenarium on hemocyte-mediated immune responses and phenoloxidase enzyme activity of model organism Galleria mellonella (L.). International Journal of Tropical Insect Science, 41 (4): 2521-2528.
  • Kaya, S., F. Uçkan & A. Er, 2021b. Influence of Indole-3-Acetic Acid on Cellular Immune Responses of Galleria mellonella L. (Lepidoptera: Pyralidae) and Pimpla turionellae L. (Hymenoptera: Ichneumonidae) in a host-parasitoid system. International Journal of Tropical Insect Science, 41 (1): 169-179.
  • Kefford, B. J., L. Zalizniak, M. S. J. Warne & D. Nugegoda, 2008. Is the integration of hormesis and essentiality into ecotoxicology now opening Pandora’s box? Environmental Pollution, 151 (3): 516-523.
  • Lee, W., J. Lee, R. Kulkarni, M.-A. Kim, J. S. Hwang M. K. Na & J.-S. Bae, 2016. Antithrombotic and antiplatelet activities of small-molecule alkaloids from Scolopendra subspinipes mutilans. Scientific Reports, 6: 21956 (12pp).
  • Lins, P. G., C. R. Valle, S. M. P. Pugine, D. L. Oliveira, M. S. L. Ferreira, E. J. X. Costa & M. P. De Melo, 2006. Effect of indole acetic acid administration on the neutrophil functions and oxidative stress from neutrophil, mesenteric lymph node and liver. Life Sciences, 78 (6): 564-570.
  • Mu, J., T. Uehara & T. Furuno, 2003. Effect of bamboo vinegar on regulation of germination and radicle growth of seed plants. Journal of Wood Science, 49 (3): 262-270.
  • Nasr, H. M., M. E. I. Badawy & E. Rabea, 2010. Toxicity and biochemical study of two insect growth regulators, buprofezin and pyriproxyfen, on cotton leafworm Spodoptera littoralis. Pesticide Biochemistry & Physiology, 98 (2): 198-205.
  • Özyılmaz, D., R. Özbek, H. Altuntaş & F. Uçkan, 2019. Indole-3-Acetic Acid induced oxidative stress in model host Galleria mellonella L. (Lepidoptera: Pyralidae) and its endoparasitoid Pimpla turionellae (L.) (Hymenoptera: Ichneumonidae). Invertebrate Survival Journal, 16 (1): 184-188.
  • Pech, L. L. & M. R. Strand, 2000. Plasmatocytes from the moth Pseudoplusia includens induce apoptosis of granular cells. Journal of Insect Physiology, 46 (12): 1565-1573.
  • Phipps, D. J., J. S. Chadwick, R. G. Leeder & W. P. Aston, 1989. The hemolytic activity of Galleria mellonella hemolymph. Developmental and Comparative Immunology, 13 (2): 103-111.
  • Prado, S. G. & S. D. Frank, 2013. Tritrophic effects of plant growth regulators in an aphid-parasitoid system. Biological Control, 66 (1): 72-76.
  • Santoyo, I. G. & A. C. Aguilar, 2011. Phenoloxidase: a key component of the insect immune system. Entomologia Experimentalis et Applicata, 142 (1): 1-16.
  • Sasaki, T., T. Hiraoka & M. Kobayashi, 2010. Hemolytic activity is mediated by the endogenous lectin in the mosquito hemolymph serum. Journal of Insect Physiology, 56 (9): 1032-1039.
  • SPSS, 2018. IBM SPSS Statistics for Windows, Version 20. Armonk, NY.
  • Şeker, D. A., A. Yanıkoğlu, 1999. Pimpla turionellae L. (Hymenoptera: Ichneumonidae)’nın açlık, beslenme, parazitleme ve yaşlılık durumlarında glikojen seviyesindeki değişmeler. Turkish Journal of Zoology, 23 (1): 289-296 (in Turkish with abstract in English).
  • Strand, M. D., 2008. The insect cellular immune response. Insect Science, 15 (1): 1-14.
  • Uçkan, F., İ. Haftacı & E. Ergin, 2011a. Effects of indol-3-acetic acid on biological parameters of the larval endoparasitoid Apanteles galleriae (Hymenoptera: Braconidae). Annals of the Entomological Society of America, 104 (1): 77-82.
  • Uçkan, F., R. Özbek & E. Ergin, 2015. Effects of Indol-3-Acetic Acid on the biology of Galleria mellonella and its endoparasitoid Pimpla turionellae. Belgian Journal of Zoology, 145 (1): 49-58.
  • Uçkan, F., Z. Öztürk, H. Altuntaş & E. Ergin, 2011b. Effects of gibberellic acid (GA3) on biological parameters and hemolymph metabolites of the pupal endoparasitoid Pimpla turionellae (Hymenoptera: Ichneumonidae) and its host Galleria mellonella (Lepidoptera: Pyralidae). Journal of the Entomological Research Society, 13 (3): 1-14.
  • Uçkan, F., H. K. Soydabaş & R. Özbek, 2014. Effect of indol-3-acetic acid on the biochemical parameters of Achoria grisella hemolymph and Apanteles galleriae larva. Pakistan Journal of Biotechnology, 11 (2): 163-171.
  • Uçkan, F., A. Tüven, A. Er & E. Ergin, 2008. Effects of gibberellic acid on biological parameters of the larval endoparasitoid Apanteles galleriae (Hymenoptera: Braconidae). Annals of the Entomological Society of America, 101 (3): 593-597.
  • Wang, X. Y., S. F. Bai, X. Li, X. M. Yin & X. C. Li, 2015. The endoparasitoid Campoletis chlorideae induces a hemolytic factor in the herbivorous insect Helicoverpa armigera. Archives of Insect Biochemistry and Physiology, 90 (1): 14-27.
  • Wang, Z. Z., Y. Q. Liu, M. Shi, J. H. Huang & X. X. Chen, (2019). Parasitoid wasps as effective biological control agents. Journal of Integrative Agriculture, 18 (4): 705-715.
  • Wojda, I., 2017. Immunity of the greater wax moth Galleria mellonella. Insect Science, 24 (3): 342-357.
  • Zhao, H., H. H. Cao & M. Z. Pan, 2017. The role of plant growth regulators in a plant-aphid-parasitoid tritrophic system. Journal of Plant Growth Regulation, 36 (4): 868-876.
  • Zibaee, A. & A. R. Bandani, 2010. Effects of Artemisia annua L. (Asteracea) on the digestive enzymatic profiles and the cellular immune reactions of the sunn pest, Eurygaster integriceps (Heteroptera: Scutellaridae), against Beauveria bassiana. Bulletin of Entomological Research,100 (2): 185-196.
There are 42 citations in total.

Details

Primary Language English
Journal Section Articles
Authors

Gülşah Becerikli Aksan This is me 0000-0003-0512-3117

Fevzi Uçkan 0000-0001-9304-4296

Aylin Er 0000-0002-8108-8950

Project Number Grant Project No: 2014/068.
Early Pub Date May 14, 2022
Publication Date June 1, 2022
Submission Date December 29, 2021
Acceptance Date May 24, 2022
Published in Issue Year 2022 Volume: 46 Issue: 2

Cite

APA Becerikli Aksan, G., Uçkan, F., & Er, A. (2022). Influence of dietary indole-3-acetic acid on phenoloxidase and hemolytic activities in Pimpla turionellae L., 1758 (Hymenoptera: Ichneumonidae) and Galleria mellonella L., 1758 (Lepidoptera: Pyralidae) in a host-parasitoid system. Turkish Journal of Entomology, 46(2), 149-158. https://doi.org/10.16970/entoted.1039327
AMA Becerikli Aksan G, Uçkan F, Er A. Influence of dietary indole-3-acetic acid on phenoloxidase and hemolytic activities in Pimpla turionellae L., 1758 (Hymenoptera: Ichneumonidae) and Galleria mellonella L., 1758 (Lepidoptera: Pyralidae) in a host-parasitoid system. TED. June 2022;46(2):149-158. doi:10.16970/entoted.1039327
Chicago Becerikli Aksan, Gülşah, Fevzi Uçkan, and Aylin Er. “Influence of Dietary Indole-3-Acetic Acid on Phenoloxidase and Hemolytic Activities in Pimpla Turionellae L., 1758 (Hymenoptera: Ichneumonidae) and Galleria Mellonella L., 1758 (Lepidoptera: Pyralidae) in a Host-Parasitoid System”. Turkish Journal of Entomology 46, no. 2 (June 2022): 149-58. https://doi.org/10.16970/entoted.1039327.
EndNote Becerikli Aksan G, Uçkan F, Er A (June 1, 2022) Influence of dietary indole-3-acetic acid on phenoloxidase and hemolytic activities in Pimpla turionellae L., 1758 (Hymenoptera: Ichneumonidae) and Galleria mellonella L., 1758 (Lepidoptera: Pyralidae) in a host-parasitoid system. Turkish Journal of Entomology 46 2 149–158.
IEEE G. Becerikli Aksan, F. Uçkan, and A. Er, “Influence of dietary indole-3-acetic acid on phenoloxidase and hemolytic activities in Pimpla turionellae L., 1758 (Hymenoptera: Ichneumonidae) and Galleria mellonella L., 1758 (Lepidoptera: Pyralidae) in a host-parasitoid system”, TED, vol. 46, no. 2, pp. 149–158, 2022, doi: 10.16970/entoted.1039327.
ISNAD Becerikli Aksan, Gülşah et al. “Influence of Dietary Indole-3-Acetic Acid on Phenoloxidase and Hemolytic Activities in Pimpla Turionellae L., 1758 (Hymenoptera: Ichneumonidae) and Galleria Mellonella L., 1758 (Lepidoptera: Pyralidae) in a Host-Parasitoid System”. Turkish Journal of Entomology 46/2 (June 2022), 149-158. https://doi.org/10.16970/entoted.1039327.
JAMA Becerikli Aksan G, Uçkan F, Er A. Influence of dietary indole-3-acetic acid on phenoloxidase and hemolytic activities in Pimpla turionellae L., 1758 (Hymenoptera: Ichneumonidae) and Galleria mellonella L., 1758 (Lepidoptera: Pyralidae) in a host-parasitoid system. TED. 2022;46:149–158.
MLA Becerikli Aksan, Gülşah et al. “Influence of Dietary Indole-3-Acetic Acid on Phenoloxidase and Hemolytic Activities in Pimpla Turionellae L., 1758 (Hymenoptera: Ichneumonidae) and Galleria Mellonella L., 1758 (Lepidoptera: Pyralidae) in a Host-Parasitoid System”. Turkish Journal of Entomology, vol. 46, no. 2, 2022, pp. 149-58, doi:10.16970/entoted.1039327.
Vancouver Becerikli Aksan G, Uçkan F, Er A. Influence of dietary indole-3-acetic acid on phenoloxidase and hemolytic activities in Pimpla turionellae L., 1758 (Hymenoptera: Ichneumonidae) and Galleria mellonella L., 1758 (Lepidoptera: Pyralidae) in a host-parasitoid system. TED. 2022;46(2):149-58.