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Diet-mediated modulation on the development and phenoloxidase activity in the Alder leaf beetle larvae, Agelastica alni (L., 1758) (Coleoptera: Chrysomelidae)

Year 2020, Volume: 44 Issue: 2, 193 - 202, 01.06.2020
https://doi.org/10.16970/entoted.600893

Abstract

Food-induced changes in the phenoloxidase activity and development of Agelastica alni (L.,1758) (Coleoptera: Chrysomelidae) larvae reared on unbalanced artificial diets were examined. The study was conducted between 2015- 2016. Food quality had an impact on the phenoloxidase activity and growth performance of alder leaf beetle. The maximum pupal mass was recorded in the 0.5:1 P:C (protein:carbohydrate) diet and the minimum pupal mass was recorded from the larvae fed on the 3:1 P:C diet. The amount of carbohydrate consumed affected the pupal mass positively, whereas the amount of protein consumed negatively affected the pupal mass. The highest amount of pupal lipid was found in the 0.5:1 P:C diet and the lowest pupal lipid amount in the 1:3 P:C diet. Also, imbalance diets affected phenoloxidase activity. There was a positive relationship between P ratio of the diet and phenoloxidase activity. Phenoloxidase activity decreases as the amount of carbohydrate consumed by larvae increases. As a result, unbalanced diet affects the immune system of larvae. Carbohydrate also has a significant effect on immune defenses as much as protein. In addition, larvae increase their body size with excessive consumption of carbohydrate.

Thanks

We are grateful to Ender Altun from Ondokuz Mayıs University for helpful suggestion on the manuscript. This study was conducted as a master thesis at Recep Tayyip Erdoğan University. Furthermore, it was presented as a poster presentation at the Ecology Symposium 2017, Kayseri, Turkey.

References

  • Adamo, S. A., 2004. Estimating disease resistance in insects: phenoloxidase and lysozyme-like activity and disease resistance in the Cricket Gryllus texensis. Journal of Insect Physiology, 50: 209-216.
  • Adamo, S. A., J. L. Roberts, R. H. Easy & N. W. Ross, 2008. Competition between immune function and lipid transport for the protein apolipophorin III leads to stress-induced immunosuppression in crickets. Journal of Experimental Biology, 211: 531-538.
  • Amar, S., Q. Zhou, Y. Shaik-Dasthagirisaheb & S. Leeman, 2007. Diet-induced obesity in mice causes changes in immune responses and bone loss manifested by bacterial challenge. Proceedings of National Academy of Sciences of the United States of America, 104 (51): 20466-20471.
  • Bernays, E. A., 1998. Evolution of feeding behaviour in insect herbivores. Bioscience, 48: 35-45.
  • Bernays, E. A., R. F. Chapman & M. S. Singer, 2004. Changes in taste receptor cell sensitivity in a polyphagous caterpillar reflect carbohydrate but not protein imbalance. Journal of Comparative Physiology A, 190 (1): 39-48.
  • 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: 248-254.
  • Cerenius, L. & K. Soderhall, 2004. The prophenoloxidase-activating system in invertebrates. Immunological Review, 198: 116-126.
  • Cotter, S. C., S. J. Simpson, D. Raubenheimer & K. Wilson, 2011. Macronutrient balance mediates trade-offs between immune function and life history traits. Functional Ecology, 25: 186-198.
  • Firidin, B. & C. Mutlu, 2009. Nitrogen utilization pattern and degradation capability of some plant secondary metabolites by Agelastica alni L. (Coleoptera: Chrysomelidae). Journal of Entomological Research Society, 11 (2): 1-15.
  • Garrad, R., D. T. Booth & M. J. Furlong, 2016. The effect of rearing temperature on development, body size, energetics and fecundity of the diamondback moth. Bulletin of Entomological Research, 106: 175-181.
  • González-Santoyo, I. & A. Córdoba-Aguilar, 2012. Phenoloxidase: a key component of the insect immune system. Entomologia Experimentalis et Applicata, 142: 1-16.
  • Honek, A., 1993. Intraspecific variation in body size and fecundity in insects-a general relationship. Oikos, 66: 483-492.
  • Joern, A. & S. T. Behmer, 1997. Importance of dietary nitrogen and carbohydrates to survival, growth, and reproduction in adults of the Grasshopper Ageneotettix deorum (Orthoptera: Acrididae). Oecologia, 112: 201-208.
  • Juma, G., M. Thiongo, L. Dutaur, K. Rharrabe, F. Marion-Poll, R. B. Lee, G. Magoma, J. B. Silvain & P. A. Calatayud, 2013. Two sugar isomers influence host plant acceptance by a cereal caterpillar pest. Bulletin of Entomological Research, 103: 20-28.
  • Kangassalo, K., T. M. Valtonen, J. Sorvari, S. Kecko, M. Pölkki, I. Krams, T. Krama & M. J. Rantala, 2018. Independent and interactive effects of immune activation and larval diet on adult immune function, growth and development in the greater wax moth (Galleria mellonella). Journal of Evolutionary Biology, 10: 1485-1497.
  • Klemola, N., T. Klemola, M. J. Rantala & T. Ruuhola, 2007. Natural host-plant quality affects immune defence of an insect herbivore. Entomologia Experimentalis et Applicata, 123: 167-176.
  • Lee, K. P., S. T. Behmer, S. J. Simpson & D. Raubenheimer, 2002. A geometric analysis of nutrient regulation in the generalist caterpillar Spodoptera littoralis (Boisduval). Journal of Insect Physiology, 48: 655-665.
  • Lee, K. P., S. J. Simpson & K. Wilson, 2008. Dietary protein-quality influences melanization and immune function in an insect. Functional Ecology, 22: 1052-1061.
  • Loveridge, J. P., 1973. Age and the changes in water and fat content of adult laboratory-reared Locusta migratoria migratorioides. Rhodesian Journal of Agricultural Research (ZDB), 11: 131-143.
  • Nigam, Y., I. Maudlin, S. Welburn & N. A. Ratcliffe, 1997. Detection of phenoloxidase activity in the hemolymph of tsetse flies, refractory and susceptible to infection with Trypanosoma brucei rhodesiense. Journal of Invertebrate Pathology, 69: 279-281.
  • Oonincx, D. G. A. B., S. V. Broekhoven, A. V. Huis, J. A. Joop & V. Loon, 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.
  • Ponton, F., K. Wilson, S. C. Cotter, D. Raubenheimer & S. J. Simpson, 2011. Nutritional immunology: a multi-dimensional approach. PLOS Pathogens, 7 (12): e1002223.
  • Ponton, F., K. Wilson, A. J. Holmes, S. Cotter & D. Raubenheimer, 2013. Integrating nutrition and immunology: A new frontier. Journal of Insect Physiology, 59: 130-137.
  • Prasad, A. K. & A. Mukhopadhyay, 2015. Fitness traits of the tea defoliator, Hyposidra talaca (Walker 1860) (Lepidoptera: Geometridae) on natural and artificial diets in relation to gut enzymes and nutritional efficiencies. Paris: La Société (N.S.), 51 (2): 145-152.
  • Raubenheimer, D. & S. A. Jones, 2003. Nutritional imbalance in an extreme generalist omnivore: tolerance and recovery through complementary food selection. Animal Behaviour, 71: 1253-1262.
  • Ravenscraft, A. & L. Boggs, 2016. Nutrient acquisition across a dietary shift: fruit feeding butterflies crave amino acids, nectivores seek salt. Oecologia, 181: 1-12.
  • Rho, M. S. & K. P. Lee, 2015. Nutrient-specific food selection buffers the effect of nutritional imbalance in the mealworm beetle, Tenebrio molitor (Coleoptera: Tenebrionidae). European Journal of Entomology, 112 (2): 251-258.
  • Rios, R. S., C. Salgado-Ruarte, G. C. Stotz & E. Gianoli, 2016. Co-occurrence of host plants associated with plant quality determines performance patterns of the specialist butterfly, Battus polydamas archidamas (Lepidoptera: Papilionidae: Troidini). European Journal of Entomology, 113: 150-157.
  • Santoyo, I. G. & A. C. Aguilar, 2011. Phenoloxidase: a key component of the insect immune system. Entomologia Experimentalis et Appliata, 142 (1): 1-16.
  • Schroeder, L. A., 1986. Protein limitation of a tree leaf feeding Lepidopteran. Entomologia Experimentalis et Appliata, 41: 115-120.
  • Simpson, S. J. & D. Raubenheimer, 2001. The Geometric analysis of nutrient allelochemical interactions: a case study using locusts. Ecology, 82: 422-439.
  • Singer, M. S., P. A. Mason & A. M. Smilanich, 2014. Ecological immunology mediated by diet in herbivorous insects. Integrative and Comparative Biology, 54 (5): 913-921.
  • Siva-Jothy, M. & J. J. W. Thompson, 2002. Short term nutrient deprivation affects immune function. Physiological Entomology, 27: 206-212.
  • Srygley, R. B., 2017. Mormon crickets maximize nutrient intake at the expense of immunity. Physiological Entomology, 42: 1-9.
  • Srygley, R. B., P. D. Lorch, S. J. Simpson & G. A. Sword, 2009. Immediate protein dietary effects on movement and the generalised immunocompetence of migrating mormon crickets Anabrus simplex (Orthoptera: Tettigoniidae). Ecological Entomology, 34: 663-668.
  • Togashi, K. & H. Yamashita, 2017. Effects of female body size on lifetime fecundity of Monochamus urussovii (Coleoptera: Cerambycidae). Applied Entomology and Zoology, 52: 79-87.
  • Trier, T. M. & W. J. Mattson, 2003. Diet-induced thermogenesis in insects: a developing concept in nutritional ecology. Environmental Entomology. 32 (1): 1-8.
  • Vogelweith, F., D. Thiery, Y. Moret & J. Memoreau, 2015. Food-mediated modulation of immunity in a phytophagous insect: An effect of nutrition rather than parasitic contamination. Journal of Insect Physiology, 77: 55-61.
  • Waldbauer, G. P. & S. Friedman, 1991. Self- Selection of optimal diets by insects. Annual Review of Entomology, 36: 43-63.
  • Warbrick-Smith, J., S. T. Behmer, K. P. Lee, D. Raubenheimer & S. J. Simpson, 2006. Evolving resistance to obesity in an insect. Proceedings of the National Academy of Sciences of the United States of America, 103 (38): 14045-14049.
  • Yamamoto, R. T., 1969. Mass rearing of Tobacco hornworm. II. Larval rearing and pupation. Journal of Economic Entomology, 62 (6): 1427-1431.
  • Yang, Y. & A. Joern, 1994. Gut Size Changes in Relation to Variable food Quality and Body Size in Grasshoppers. Functional Ecology, 8: 36-45.
  • Yi, L., C. M. M. Lakemonda, L. M. C. Sagisb, V. Eisner-Schadlerc, A. van Huisd & M. A. J. S. van Boekela, 2013. Extraction and characterization of protein fractions from five insect species. Food Chemistry, 141: 3341-3348.
  • Zdybicka-Barabas, A. & M. Cytrynska, 2010. Phenoloxidase activity in hemolymph of Galleria mellonella larvae challenged with Aspergillus oryzae. Annales Universitatis Mariae Curie Sklodowska, Sectio C-Biologia, 515 (2): 49-57.

Kızılağaç yaprak böceği, Agelastica alni (L., 1758) (Coleoptera: Chrysomelidae) larvalarının fenoloksidaz aktivitesi ve gelişiminde diyet etkenli değişiklikler

Year 2020, Volume: 44 Issue: 2, 193 - 202, 01.06.2020
https://doi.org/10.16970/entoted.600893

Abstract

Bu çalışmada gıda bakımından dengesiz diyetlerle beslenen Agelastica alni (L.,1758) (Coleoptera: Chrysomelidae) larvalarının fenoloksidaz aktivitesi ve gelişiminde meydana gelen besin kaynaklı değişiklikler araştırılmıştır. Çalışma 2015-2016 yılları arasında gerçekleştirilmiştir. Besin kalitesi kızılağaç yaprak böceğinin gelişim performansında ve fenoloksidaz aktivitesinde önemli bir etkiye sahiptir. En fazla pupa kütlesi 0.5:1 P:C (protein:karbonhidrat) besininde ve en az pupa kütlesi ise 3:1 P:C besininde beslenen larvalarda kaydedilmiştir. Tüketilen karbonhidrat miktarı pupa kütlesini pozitif olarak etkilerken, tüketilen protein miktarı pupa kütlesini negatif olarak etkilemektedir. Pupa lipid miktarı diyetler arasında farklılık göstermektedir. En fazla pupa lipid miktarı 0.5:1 P:C diyetinde kaydedilirken, en az lipid miktarı 1:3 P:C diyetinde kaydedilmiştir. Dengesiz diyetler fenoloksidaz aktivitesini de etkilemiştir. Besinin protein oranıyla fenoloksidaz aktivitesi arasında pozitif bir ilişki vardır. Fenoloksidaz aktivitesi larvaların tüketmiş olduğu karbonhidrat miktarının artışıyla azalmaktadır. Sonuç olarak, dengesiz diyetler larvaların fenoloksidaz aktivitesini etkilemektedir. Karbonhidrat savunma sistemi üzerinde protein kadar önemli bir etkiye sahiptir. Ek olarak, larvaların vücut büyüklüğü aşırı karbonhidrat tüketimiyle artmaktadır.

References

  • Adamo, S. A., 2004. Estimating disease resistance in insects: phenoloxidase and lysozyme-like activity and disease resistance in the Cricket Gryllus texensis. Journal of Insect Physiology, 50: 209-216.
  • Adamo, S. A., J. L. Roberts, R. H. Easy & N. W. Ross, 2008. Competition between immune function and lipid transport for the protein apolipophorin III leads to stress-induced immunosuppression in crickets. Journal of Experimental Biology, 211: 531-538.
  • Amar, S., Q. Zhou, Y. Shaik-Dasthagirisaheb & S. Leeman, 2007. Diet-induced obesity in mice causes changes in immune responses and bone loss manifested by bacterial challenge. Proceedings of National Academy of Sciences of the United States of America, 104 (51): 20466-20471.
  • Bernays, E. A., 1998. Evolution of feeding behaviour in insect herbivores. Bioscience, 48: 35-45.
  • Bernays, E. A., R. F. Chapman & M. S. Singer, 2004. Changes in taste receptor cell sensitivity in a polyphagous caterpillar reflect carbohydrate but not protein imbalance. Journal of Comparative Physiology A, 190 (1): 39-48.
  • 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: 248-254.
  • Cerenius, L. & K. Soderhall, 2004. The prophenoloxidase-activating system in invertebrates. Immunological Review, 198: 116-126.
  • Cotter, S. C., S. J. Simpson, D. Raubenheimer & K. Wilson, 2011. Macronutrient balance mediates trade-offs between immune function and life history traits. Functional Ecology, 25: 186-198.
  • Firidin, B. & C. Mutlu, 2009. Nitrogen utilization pattern and degradation capability of some plant secondary metabolites by Agelastica alni L. (Coleoptera: Chrysomelidae). Journal of Entomological Research Society, 11 (2): 1-15.
  • Garrad, R., D. T. Booth & M. J. Furlong, 2016. The effect of rearing temperature on development, body size, energetics and fecundity of the diamondback moth. Bulletin of Entomological Research, 106: 175-181.
  • González-Santoyo, I. & A. Córdoba-Aguilar, 2012. Phenoloxidase: a key component of the insect immune system. Entomologia Experimentalis et Applicata, 142: 1-16.
  • Honek, A., 1993. Intraspecific variation in body size and fecundity in insects-a general relationship. Oikos, 66: 483-492.
  • Joern, A. & S. T. Behmer, 1997. Importance of dietary nitrogen and carbohydrates to survival, growth, and reproduction in adults of the Grasshopper Ageneotettix deorum (Orthoptera: Acrididae). Oecologia, 112: 201-208.
  • Juma, G., M. Thiongo, L. Dutaur, K. Rharrabe, F. Marion-Poll, R. B. Lee, G. Magoma, J. B. Silvain & P. A. Calatayud, 2013. Two sugar isomers influence host plant acceptance by a cereal caterpillar pest. Bulletin of Entomological Research, 103: 20-28.
  • Kangassalo, K., T. M. Valtonen, J. Sorvari, S. Kecko, M. Pölkki, I. Krams, T. Krama & M. J. Rantala, 2018. Independent and interactive effects of immune activation and larval diet on adult immune function, growth and development in the greater wax moth (Galleria mellonella). Journal of Evolutionary Biology, 10: 1485-1497.
  • Klemola, N., T. Klemola, M. J. Rantala & T. Ruuhola, 2007. Natural host-plant quality affects immune defence of an insect herbivore. Entomologia Experimentalis et Applicata, 123: 167-176.
  • Lee, K. P., S. T. Behmer, S. J. Simpson & D. Raubenheimer, 2002. A geometric analysis of nutrient regulation in the generalist caterpillar Spodoptera littoralis (Boisduval). Journal of Insect Physiology, 48: 655-665.
  • Lee, K. P., S. J. Simpson & K. Wilson, 2008. Dietary protein-quality influences melanization and immune function in an insect. Functional Ecology, 22: 1052-1061.
  • Loveridge, J. P., 1973. Age and the changes in water and fat content of adult laboratory-reared Locusta migratoria migratorioides. Rhodesian Journal of Agricultural Research (ZDB), 11: 131-143.
  • Nigam, Y., I. Maudlin, S. Welburn & N. A. Ratcliffe, 1997. Detection of phenoloxidase activity in the hemolymph of tsetse flies, refractory and susceptible to infection with Trypanosoma brucei rhodesiense. Journal of Invertebrate Pathology, 69: 279-281.
  • Oonincx, D. G. A. B., S. V. Broekhoven, A. V. Huis, J. A. Joop & V. Loon, 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.
  • Ponton, F., K. Wilson, S. C. Cotter, D. Raubenheimer & S. J. Simpson, 2011. Nutritional immunology: a multi-dimensional approach. PLOS Pathogens, 7 (12): e1002223.
  • Ponton, F., K. Wilson, A. J. Holmes, S. Cotter & D. Raubenheimer, 2013. Integrating nutrition and immunology: A new frontier. Journal of Insect Physiology, 59: 130-137.
  • Prasad, A. K. & A. Mukhopadhyay, 2015. Fitness traits of the tea defoliator, Hyposidra talaca (Walker 1860) (Lepidoptera: Geometridae) on natural and artificial diets in relation to gut enzymes and nutritional efficiencies. Paris: La Société (N.S.), 51 (2): 145-152.
  • Raubenheimer, D. & S. A. Jones, 2003. Nutritional imbalance in an extreme generalist omnivore: tolerance and recovery through complementary food selection. Animal Behaviour, 71: 1253-1262.
  • Ravenscraft, A. & L. Boggs, 2016. Nutrient acquisition across a dietary shift: fruit feeding butterflies crave amino acids, nectivores seek salt. Oecologia, 181: 1-12.
  • Rho, M. S. & K. P. Lee, 2015. Nutrient-specific food selection buffers the effect of nutritional imbalance in the mealworm beetle, Tenebrio molitor (Coleoptera: Tenebrionidae). European Journal of Entomology, 112 (2): 251-258.
  • Rios, R. S., C. Salgado-Ruarte, G. C. Stotz & E. Gianoli, 2016. Co-occurrence of host plants associated with plant quality determines performance patterns of the specialist butterfly, Battus polydamas archidamas (Lepidoptera: Papilionidae: Troidini). European Journal of Entomology, 113: 150-157.
  • Santoyo, I. G. & A. C. Aguilar, 2011. Phenoloxidase: a key component of the insect immune system. Entomologia Experimentalis et Appliata, 142 (1): 1-16.
  • Schroeder, L. A., 1986. Protein limitation of a tree leaf feeding Lepidopteran. Entomologia Experimentalis et Appliata, 41: 115-120.
  • Simpson, S. J. & D. Raubenheimer, 2001. The Geometric analysis of nutrient allelochemical interactions: a case study using locusts. Ecology, 82: 422-439.
  • Singer, M. S., P. A. Mason & A. M. Smilanich, 2014. Ecological immunology mediated by diet in herbivorous insects. Integrative and Comparative Biology, 54 (5): 913-921.
  • Siva-Jothy, M. & J. J. W. Thompson, 2002. Short term nutrient deprivation affects immune function. Physiological Entomology, 27: 206-212.
  • Srygley, R. B., 2017. Mormon crickets maximize nutrient intake at the expense of immunity. Physiological Entomology, 42: 1-9.
  • Srygley, R. B., P. D. Lorch, S. J. Simpson & G. A. Sword, 2009. Immediate protein dietary effects on movement and the generalised immunocompetence of migrating mormon crickets Anabrus simplex (Orthoptera: Tettigoniidae). Ecological Entomology, 34: 663-668.
  • Togashi, K. & H. Yamashita, 2017. Effects of female body size on lifetime fecundity of Monochamus urussovii (Coleoptera: Cerambycidae). Applied Entomology and Zoology, 52: 79-87.
  • Trier, T. M. & W. J. Mattson, 2003. Diet-induced thermogenesis in insects: a developing concept in nutritional ecology. Environmental Entomology. 32 (1): 1-8.
  • Vogelweith, F., D. Thiery, Y. Moret & J. Memoreau, 2015. Food-mediated modulation of immunity in a phytophagous insect: An effect of nutrition rather than parasitic contamination. Journal of Insect Physiology, 77: 55-61.
  • Waldbauer, G. P. & S. Friedman, 1991. Self- Selection of optimal diets by insects. Annual Review of Entomology, 36: 43-63.
  • Warbrick-Smith, J., S. T. Behmer, K. P. Lee, D. Raubenheimer & S. J. Simpson, 2006. Evolving resistance to obesity in an insect. Proceedings of the National Academy of Sciences of the United States of America, 103 (38): 14045-14049.
  • Yamamoto, R. T., 1969. Mass rearing of Tobacco hornworm. II. Larval rearing and pupation. Journal of Economic Entomology, 62 (6): 1427-1431.
  • Yang, Y. & A. Joern, 1994. Gut Size Changes in Relation to Variable food Quality and Body Size in Grasshoppers. Functional Ecology, 8: 36-45.
  • Yi, L., C. M. M. Lakemonda, L. M. C. Sagisb, V. Eisner-Schadlerc, A. van Huisd & M. A. J. S. van Boekela, 2013. Extraction and characterization of protein fractions from five insect species. Food Chemistry, 141: 3341-3348.
  • Zdybicka-Barabas, A. & M. Cytrynska, 2010. Phenoloxidase activity in hemolymph of Galleria mellonella larvae challenged with Aspergillus oryzae. Annales Universitatis Mariae Curie Sklodowska, Sectio C-Biologia, 515 (2): 49-57.
There are 44 citations in total.

Details

Primary Language English
Journal Section Articles
Authors

Rukiye Sivrikaya This is me 0000-0003-3387-4778

Nurver Altun 0000-0002-2657-9263

Özlem Faiz This is me 0000-0003-2447-0763

Publication Date June 1, 2020
Submission Date August 2, 2019
Acceptance Date January 22, 2020
Published in Issue Year 2020 Volume: 44 Issue: 2

Cite

APA Sivrikaya, R., Altun, N., & Faiz, Ö. (2020). Diet-mediated modulation on the development and phenoloxidase activity in the Alder leaf beetle larvae, Agelastica alni (L., 1758) (Coleoptera: Chrysomelidae). Turkish Journal of Entomology, 44(2), 193-202. https://doi.org/10.16970/entoted.600893
AMA Sivrikaya R, Altun N, Faiz Ö. Diet-mediated modulation on the development and phenoloxidase activity in the Alder leaf beetle larvae, Agelastica alni (L., 1758) (Coleoptera: Chrysomelidae). TED. June 2020;44(2):193-202. doi:10.16970/entoted.600893
Chicago Sivrikaya, Rukiye, Nurver Altun, and Özlem Faiz. “Diet-Mediated Modulation on the Development and Phenoloxidase Activity in the Alder Leaf Beetle Larvae, Agelastica Alni (L., 1758) (Coleoptera: Chrysomelidae)”. Turkish Journal of Entomology 44, no. 2 (June 2020): 193-202. https://doi.org/10.16970/entoted.600893.
EndNote Sivrikaya R, Altun N, Faiz Ö (June 1, 2020) Diet-mediated modulation on the development and phenoloxidase activity in the Alder leaf beetle larvae, Agelastica alni (L., 1758) (Coleoptera: Chrysomelidae). Turkish Journal of Entomology 44 2 193–202.
IEEE R. Sivrikaya, N. Altun, and Ö. Faiz, “Diet-mediated modulation on the development and phenoloxidase activity in the Alder leaf beetle larvae, Agelastica alni (L., 1758) (Coleoptera: Chrysomelidae)”, TED, vol. 44, no. 2, pp. 193–202, 2020, doi: 10.16970/entoted.600893.
ISNAD Sivrikaya, Rukiye et al. “Diet-Mediated Modulation on the Development and Phenoloxidase Activity in the Alder Leaf Beetle Larvae, Agelastica Alni (L., 1758) (Coleoptera: Chrysomelidae)”. Turkish Journal of Entomology 44/2 (June 2020), 193-202. https://doi.org/10.16970/entoted.600893.
JAMA Sivrikaya R, Altun N, Faiz Ö. Diet-mediated modulation on the development and phenoloxidase activity in the Alder leaf beetle larvae, Agelastica alni (L., 1758) (Coleoptera: Chrysomelidae). TED. 2020;44:193–202.
MLA Sivrikaya, Rukiye et al. “Diet-Mediated Modulation on the Development and Phenoloxidase Activity in the Alder Leaf Beetle Larvae, Agelastica Alni (L., 1758) (Coleoptera: Chrysomelidae)”. Turkish Journal of Entomology, vol. 44, no. 2, 2020, pp. 193-02, doi:10.16970/entoted.600893.
Vancouver Sivrikaya R, Altun N, Faiz Ö. Diet-mediated modulation on the development and phenoloxidase activity in the Alder leaf beetle larvae, Agelastica alni (L., 1758) (Coleoptera: Chrysomelidae). TED. 2020;44(2):193-202.