اثرات نماتد Steinernema carpocapsae روی شته معمولی گندم Schizaphis graminum (Hemiptera: Aphididae)

نوع مقاله : علمی پژوهشی-فارسی


1 استاد گروه گیاه‌پزشکی، دانشکده کشاورزی و منابع طبیعی، دانشگاه محقق اردبیلی، اردبیل، ایران

2 دانش آموخته دکتری حشره شناسی کشاورزی، گروه گیاه‌پزشکی، دانشکده کشاورزی و منابع طبیعی، دانشگاه محقق اردبیلی، اردبیل، ایران

3 دانشجوی دکتری حشره شناسی کشاورزی، گروه گیاه‌پزشکی، دانشکده کشاورزی و منابع طبیعی، دانشگاه محقق اردبیلی، اردبیل، ایران

4 استادیار موسسه تحقیقات گیاه‌پزشکی کشور، تهران، ایران


شته معمولی گندم Schizaphis graminum (Hemiptera: Aphididae) ، یکی از مهمترین آفات غلات است که هر ساله خسارت زیادی به مزارع گندم کشور وارد می سازد. هدف تحقیق حاضر، بررسی تأثیر کشندگی و زیرکشندگی نماتد Steinernema carpocapsae بر فراسنجه های جدول زندگی و فعالیت آنزیم فنل اکسیداز شته معمولی گندم با استفاده از سوبسترای (L-dihydroxyphenylalanin) L-DOPA در اتاقک رشد با شرایط دمایی 2±25 درجه‏ی سلسیوس، رطوبت نسبی 5±60 درصد و دوره‏ی نوری 16 ساعت روشنایی و 8 ساعت تاریکی بود. آنزیم فنل اکسیداز نقش کلیدی در سیستم ایمنی ذاتی حشرات دارد. مقدار LC50 نماتد مورد مطالعه روی شته‌های ماده بالغ S. graminum، 136 لارو سن سوم بر حشره به دست آمد. طبق نتایج، این نماتد تاثیر کشندگی بالایی روی مراحل بالغ شته‌ها دارد. نتایج آزمایش تأثیر زیرکشندگی (LC30) این نماتد نشان داد که میزان پوره زایی در تیمار نماتد (07/19پوره/به ازای هر شته کامل) به طور معنی داری کمتر از شاهد (16/39 پوره/ به ازای هر شته کامل) بود. هم چنین، نماتد مورد مطالعه به‌طور معنی-داری باعث کاهش ویژگی‌های دموگرافی شته معمولی گندم شدند. مقدار نرخ ذاتی افزایش جمعیت (r) شته ها در تیمار نماتد و شاهد به‌ترتیب 300/0 و 421/0 بر روز بود. در این بررسی، میزان فعالیت آنزیم فنل اکسیداز، براساس میکرومول بر دقیقه بر میلی گرم پروتئین شته های تیمار شده تفاوت معنی داری با شاهد داشت. نتایج نشان داد که نماتد S. carpocapsae اثر کشندگی و زیرکشندگی قابل ملاحظه‌ای روی شته معمولی گندم دارد و بعد از مطالعات مزرعه ای، می تواند در کنترل بیولوژیک و برنامه های مدیریت تلفیقی آفت مذکور مورد استفاده قرار گیرد.



عنوان مقاله [English]

Effects of Entomopathogenic nematode, Steinernema carpocapsae against Schizaphis graminum (Hemiptera: Aphididae)

نویسندگان [English]

  • H. Rafiee Dastjerdi 1
  • M. Taleh 2
  • R. Ahmadpoor 3
  • L. Ebrahimi 4
1 Professor of Agricultural Entomology, Department of Plant Protection, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran
2 Ph.D. Graduate of Agricultural Entomology, Department of Plant Protection, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran
3 Ph.D. student of Agricultural Entomology, Department of Plant Protection, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran
4 Assistant Professor of Agricultural Entomology, Iranian Research Institute of Plant Protection, Tehran, Iran
چکیده [English]

Background and Objectives
The wheat aphid, Schizaphis graminum, is deemed one of the most significant grain pests, causing substantial damage to the country's wheat farms. Consequently, various biological, agronomic, and chemical methods are used to control wheat aphids, where chemical spraying is the most common method. The increasing use of chemical insecticides has resulted in several issues, including the emergence of insect resistance to pesticides, adverse effects on the environment, beneficial organisms, and humans, and the development of insecticide-resistant pests. In this regard, insect pathogens like nematodes may be preferable to chemical insecticides. This study aimed to evaluate the lethal and sublethal effects of entomopathogenic nematode Steinernema carpocapsae on the life history parameters and phenoloxidase enzyme activity of S. graminum by L-DOPA (L-dihydroxyphenylalanine) substrate. This enzyme activity is essential to the insect's innate immune response.
Materials and Methods
S. graminum was cultivated on a wheat host in a growth chamber maintained at 25 ± 2 °C, 60 ± 5% relative humidity (RH), and 16:8 light/day (L:D) hour photoperiods. Daily observations and recordings were used to track the development period and survival rate. In addition, for breeding the wheat aphid S. graminum, populations from the plant protection department's laboratory were utilized and transferred to wheat plants in a growth chamber.
Aphids infested the plants once they had reached their optimal size. Age-stage and two-sex life table analyses were used to analyze the raw data. TWOSEX-MSChart was used to evaluate the raw data based on the age stage and two-sex life table. In addition, blood cell phenol oxidase and hemolymph testing were performed. Samples of the enzyme were preincubated with phosphate buffer at 30 °C for 30 min, then 50 µl of 10 mM L dihydroxyphenylalanine (L-DOPA) substrate was added and incubated at 25 and 30 °C for 5 min. The phenol oxidase activity was measured using a 492 nm enzyme-linked immunosorbent assay (ELISA) reader device.
The bioassays indicated that the lethal concentration (LC50) of nematode treatment against the adults of S. graminum was 136 larvae/insect. The current study revealed that S. carpocapsae had a higher adult mortality rate than S. graminum. Results of the sublethal effects experiment showed that the pest's fecundity in S. carpocapsae treatment (19.07 offspring/female) was lower than the control (39.16 offspring/female). Furthermore, the studied nematode significantly reduced the population growth parameters of S. graminum. The intrinsic rate of increase for treated and control nematodes was 0.300 and 0.421, respectively, per day. Based on the results, the nematode increased the phenol oxidase enzyme's activity at 25 and 30 °C relative to the control.
Considering that chemical insecticides are accompanied by problems such as resistance and residual toxins in agricultural products, it is preferable to use entomopathogenic nematodes, which have a higher immunity to environment and natural enemies. The lethal concentration (LC50) study of the examined nematode showed that the nematode S. carpocapsae exhibited good disease-causing power on the adult female aphids of S. graminum.
The investigation into the effect of experimental nematode sublethal concentration on the growth parameters of the wheat aphid population revealed that in the nematode S. carpocapsae, the characteristics of the aphid population, particularly the intrinsic rate of population increase parameter value, decreased significantly. Sublethal concentrations of the studied nematode can slow or even stop the population growth of wheat aphids and significantly impact aphid fertility, survival, and life expectancy.
In this study, the phenol oxidase enzyme's activity significantly differed between treated and untreated aphids. It appears that the insect uses phenol oxidase enzymes to counteract the nematode's effect, and this enzyme plays a role in the wheat aphid's body when dealing with S. carpocapsae. The overall results revealed that S. carpocapsae exhibited high lethal and sublethal effects on S. graminum. After additional field studies, it can be recommended for use in biological control and an integrated pest management (IPM) program for this pest.

کلیدواژه‌ها [English]

  • bioassay
  • life history
  • nematode
  • phenol oxidase
  • Wheat aphid
Abbott, W. S. (1925). A method of computing the effectiveness of an insecticide. Journal of Economic Entomology,18, 265-267.
Abdollahi, M. (2009). A survey on entomopathogenic nematodes in Kohgiluyeh and Boyerahmad province. Final report of research project, Yasouj University, Yasouj, Iran. 116pp.
Andalo, V., Faria, L. S., Carvalho, F. J., Assis, G. A., Santos, V., Mendes, S. M. & Gonring, A. H. R. (2020). Entomopathogenic nematodes for the control of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) pupae. Arquivos do Instituto Biológico, 88,1-8. e007.
Azambuja, P., Garcia, E. S. & Ratcliffe, N. A. (1991). Aspects of classification of Hemiptera hemocytes from six triatomine species. Memórias do Instituto Oswaldo Cruz, 86, 1-10.
Batalla-Carrera, L., Morton, A. & Garcia, D. P. (2010). Efficacy of entomopathogenic nematodes against the tomato leafminer Tuta absoluta in laboratory and greenhouse conditions. BioControl, 55, 523-530.
Baur, M. E. & Kaya, H. K. (2001). Persistence of entomopathogenic nematodes. LSUAg Center. (Acquired December, 2008). Available: http:// www.Lsuagcenter.com/s265/baur.htm.
Berkvens N., Van Vaerenbergh, J., Maes, M., Belien, T.  & Viaene, N. (2013). Entomopathogenic nematodes fail to parasitize the woolly apple aphid Eriosoma lanigerum as their symbiotic bacteria are suppressed. Journal of Applied Entomology, 138, 644-655.
Blackman, R.L., & Eastop, V.F. (2006). Aphids on the world’s herbaceous plants and shrubs. John Wiley.
Brivio, M. F., Pagani, M. & Restelli, S. (2002). Immune suppression of Galleria mellonella
(Insecta, Lepidoptera) humoral defenses induced by Steinernema feltiae (Nematoda, Rhabditida): involvement of the parasite cuticle. Experimental Parasitology,101, 149-156.   
Caccia, M. G., Del Valle, E., Doucet, M. E. & Lax, P. (2014). Susceptibility of Spodoptera frugiperda and Helicoverpa gelotopoeon (Lepidoptera: Noctuidae) to the entomopathogenic nematode Steinernema diaprepesi (Rhabditida: Steinernematidae) under laboratory conditions. Chilean Journal of Agricultural Research, 74(1), 123-126.
Cerenius, L. & Soderhall, K. (2004). The prophenoloxidase-activating system in invertebrates. Immunological Reviews, 198, 116-126.
Chi, H. (2020). TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis.
Chi, H. (1988). Life-table analysis incorporating both sexes and variable development rates among individuals. Environmental Entomology, 17, 26-34.
Chi, H. & Liu, H. (1985). Two new methods for the study of insect population ecology. Bulletin of the Institute of Zoology, Academia Sinica, 24, 225-240.
Chi, H. & Yang, T. (2003). Two-sex life table and predation rate of Propylaea japonica Thunberg (Coleoptera: Coccinellidae) fed on Myzus persicae (Sulzer) (Homoptera: Aphididae). Environmental Entomology, 32, 327-333.
Cuthbertson, A. G. S., Mathers, J. J., Northing, P. H., Luo, W. & Walters, K. F. A. (2007). Establishing effect of commonly used insecticides for aphid control on the infectivity of the entomopathogenic nematode, Steinernema feltiae using a streamlined screening method.  Estudos de Biologia, 29(66),17-21.
Desneux, N., Denoyelle, R. & Kaiser, L. (2006). A multi- step bioassay to assess the effect of the deltamethrin on the parasitic wasps, Aphidiuservi. Chemosphere. 62: 1697-1706.
Devi G. 2020. Entomopathogenic nematode against foliar pests. International Journal of Agriculture, Environment and Bioresearch, 5(03), 252-275.
Ebrahimi, L., Niknam, G. & Lewis, E. E. (2011). Lethal and sublethal effects of Iranian isolates of Steinernema feltiae and Heterorhabditis bacteriophora on the Colorado potato beetle, Leptinotarsa decemlineata. BioControl, 56, 781-788.
Ebrahimi L., Shiri, Sh. & Dunphy, G. B. (2018). Effect of entomopathogenic nematode,
Steinernema feltiae, on survival and plasma phenoloxidase activity of Helicoverpa
(Hb) (Lepidoptera: Noctuidae) in laboratory conditions. Egyptian Journal of Biological Pest Control, 28, 12.
Fattah-Alhoseini, S., Allahyari, H., Azemayesh-Fard, P., & Heydari, S. (2011). Effects of host plant on development and reproduction of green wheat Aphid Schizaphis graminum (Rondani) (Hem.: Aphididae). Iranian Journal of Plant Protection Science, 4(2), 233-242.
Ferreira, T. & Malan, A. P. (2014). Xenorhabdus and Photorhabdus, bacterial symbionts of the entomopathogenic nematodes Steinernema and Heterorhabditis and their in vitro liquid mass culture: a review. African Entomology, 22,1-14.
Filgueiras, C. C. & Willett, D. S. (2021). Non-lethal effects of entomopathogenic nematode infection. scientific reports, 11, 17090.
Hein, G. L., Kalisch, J. & Thomas, A. J. (1996). Identification and general discussion of the cereal aphid species most commonly found in Nebraeska small grain, corn, sorghum and millet. University of Nebraeska, Lincoln/NE.
Kavallieratos, N. G., Arthanassiou, C. G., Michalaki, M. P., Batta, Y. A., Rigatos H. A.,
& et al. (2006). Effect of combined use of Metarhizium anisopliae (Metschinkoff) Sorokin and diatomaeus earth for the control of three stored product beetle species. Crop Protection, 25, 1087-1094.
Khodabandeh, N. (2000). The Cultivation of Crops. Tehran University Press.
Lalitha, K., Venkatesan, S., Balamuralikrishnan, B. & Subramanian, M. (2022). Isolation and biocontrol efficacy of entomopathogenic nematodes Steinernema carpocapsae, Steinernema monticolum and Rhabditis blumi on lepidopteran pest Spodoptera litura. Biocatalysis and Agricultural Biotechnology, 39, 102291.
Leonard, C., Kenneth, S. & Ratcliffe, N. A. (1985). Studies on prophenoloxidase and protease activity of Blaberus craniifer haemocytes. Insect Biochemistry, 15, 803-810. 
Michels, G. J. & Behle, R. W. (1989). Influence of temperature on reproduction, development and intrinsic rate of increase of Russian wheat aphid, greenbug, and bird cherry-oat aphid (Homoptera: Aphididae). Journal of Economic Entomology, 82, 439-444.
Papanikolaou, N. E., Kalaitzaki, A., Karamaouna, F., Michaelakis, A., Papadimitriou, V., Dourtoglou, V. & Papachristos, D. P. (2017). Nano-formulation enhances insecticidal activity of natural pyrethrins against Aphis gossypii (Hemiptera: Aphididae) and retains their harmless effect to non-target predators. Environmental Science and Pollution Research. 1-7. 5(11), 10243-10249.
Papp, M., & Mesterhazy, A. (1993). Resistance to bird cherry oat-aphid Rhopalosiphum padi (L.) in winter wheat varieties. Euphytica, 67(1), 49-57.
Poinar, G. O. J. (1990). Taxonomy and biology of Steinernematidae and Heterorhabditidae, p. 23–61. In: Gaugler, R. & Kaya, H. K. (eds) Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, p 365.
Sevgi, T. & Galip, K. (2016). Determination of the efficacy of some entomopathogenic nematodes against Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) under laboratory conditions. Turkish Journal of Entomology, 40(2), 175-183.
Souza, L. M., Moino Junior, A., Mertz, N. R., Silva, M.A.T., Soarez, F. M. & Bonete, F. R. Z. (2012). Nematoides entomopatogênicos e compatibilidade com imidaclopridevisandoaocontrole de Spodoptera frugiperda em viveiro florestal. Nematologia Brasileira, Piracicaba, 36(1-2), 32-41.
SPSS Inc. 2007. SPSS base 16.0 user’s guide. SPSS Incorporation, Chicago.
Stark, J. D. & Banks, J. E. (2003). Population-level effects of pesticides and other toxicant on arthropods. Annals of Review Entomology, 48,505-519.
Stark, J. D., Sugayama, R. I., & Kovaleski, A. (2007). Why demographic and modeling approaches should be adopted for estimating the effects of pesticides on biocontrol agents. Biocontrol, 52, 365-374.
Taleh, M., Saadati, M., Farshbaf, R. & Khakvar, R. (2014). Partial characterization of phenoloxidas enzyme in the hemocytes of Helicoverpaarmigera Hubner (Lepidoptera: Noctuidae). Journal of King Saud University Science, 26, 285-289.
Vakhide, N. & Safavi, S. A. (2014). Lethal and sublethal effects of direct exposure to acetamiprid on reproduction and survival of the greenbug, Schizaphis graminum (Hemiptera: Aphididae). Archives of Phytopathology and Plant Protection, 47(3), 339-348.
Wilde, G. E., Shufran, R. A., Kindler, S. D., Brooks, H. L., & Sloderbeck, P. E. (2001). Distribution and abundance of insecticide resistant greenbugs (Homoptera: Aphididae) and validation of a bioassay to assess resistance. Journal of Economic Entomology, 94(2), 547-551.
Yan, X., Shahid Arain, M., Lin, Y., Gu, X., Zhang, L., Li, J. & Han, R. (2020). Effcacy of entomopathogenic nematodes against the tobacco cutworm, Spodoptera litura (Lepidoptera: Noctuidae). Journal of Economic Entomology, 113, 64-72.
Zibaee, A., Bandani, A. R. & Malagoli, D. (2011). Purification and characterization of phenoloxidase from the hemocytes of Eurygaster integriceps. Comparative Biochemistry and Physiology. Part B, 158, 117-123.
 © 2023 by the authors. Licensee SCU, Ahvaz, Iran. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0 license) (http://creativecommons.org/licenses/by-nc/4.0/.