اثرات پایین به بالای کودهای مختلف بر تغییرات جدول زندگی دو جنسی کفشدوزک دو نقطه‌ای، Adalia bipunctata L.

نوع مقاله : علمی پژوهشی-فارسی

نویسندگان

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

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

چکیده

کفشدوزک شکارگرAdalia bipunctata L. گونه‌ی چند‌خوار است که عمدتاً از شته‌ها از جمله شته سبز هلو،Myzus persicae (Sulzer) ، تغذیه می‌کند. شته سبز هلو حشره‌ای چندخوار می‌باشد که در گلخانه و مزارع به تعداد زیادی از محصولات خسارت می‌زند. در پژوهش حاضر، تاثیر محلول‌پاشی سولفات روی بر گیاه و افزودن کود آلی ورمی‌کمپوست 30 درصد و کودهای زیستی Bacillus subtilis، Pseudomonas fluorescens، Glomus intraradices، G. intraradices× B. subtilis و G. intraradices×P. fluorescens به بستر بذری گیاه فلفل دلمه‌ای مورد بررسی قرار گرفت. فراسنجه‌های دموگرافی شکارگر در شرایط آزمایشگاهی با دمای 2±25 درجه سلسیوس، رطوبت نسبی 5±65 درصد و دوره‌ی نوری 16 ساعت روشنایی و 8 ساعت تاریکی مورد بررسی قرار گرفت. کوتاه‌ترین دوره تخم‌ریزی در تیمارهای ورمی‌کمپوست 30 درصد (18/27 روز)، سولفات روی (36/28 روز) و شاهد (73/28 روز) و طولانی‌ترین دوره در تیمارB. subtilis (91/34 روز) ثبت گردید. بیشترین و کمترین امید زندگی شکارگر به ترتیب روی تیمارهای B. subtilis(10/47 روز) و ورمی‌کمپوست 30 درصد (63/38 روز) مشاهده شد. همچنین، بیشترین و کمترین مقدار فراسنجه نرخ خالص تولید مثل (R0)کفشدوزک A. bipunctata به ترتیب در B. subtilis (65/131 نتاج) و ورمی‌کمپوست 30 درصد (22/71 نتاج) به دست آمد. کمترین مقدار فراسنجه نرخ ذاتی افزایش جمعیت (r)کفشدوزک A. bipunctataدر ورمی‌کمپوست 30 درصد (1179/0 بر روز) و بیشترین مقادیر آن به ترتیب در تیمارهای B. subtilis، سولفات روی، G. intraradices× B. subtilis و P. fluorescens (به ترتیب 1444/0، 1426/0، 1425/0 و 1408/0 بر روز) مشاهده شد. بنابراین، تیمارکردن بذر با کودهای زیستی (P. fluorescens و B. subtilis) روی فراسنجه‌های مورد بررسی شکارگر تاثیر مثبت و معنی‌داری داشته و می‌توان در کنترل بیولوژیک شته سبز هلو از آنها استفاده نمود.

کلیدواژه‌ها

موضوعات


عنوان مقاله [English]

Bottom-up effects of different fertilizer on changes in the two sex life table of the ladybug beetle Adalia bipunctata L.

نویسندگان [English]

  • M. Mardani-Talaee 1
  • J. Razmjou 2
  • G. Nouri - Ganbalani 2
  • M. Hassanpour 2
  • B. Naseri 2
1 Ph.D. in Agricultural Entomology, Department of Plant Protection, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran
2 Professor, Department of Plant Protection, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran
چکیده [English]

Background and Objectives

The widespread use of chemical pesticides and fertilizers remains essential in modern agriculture; however, their excessive application poses significant environmental and human health risks. Consequently, alternative pest management strategies, such as host plant resistance and biological control, have gained increasing attention. One promising avenue of research explores the role of plant growth-promoting rhizobacteria (PGPR) fertilizers in integrated pest management (IPM). PGPR fertilizers improve plant quality by improving nutrient availability, facilitating nitrogen fixation, and regulating key signaling pathways. Rhizobacteria contribute to plant defense against herbivorous insects through two primary mechanisms: direct defense, involving the release of insect-deterring proteins, and indirect defense, wherein dilute volatile compounds attract natural enemies of insect pests. Induced systemic resistance (ISR) has been shown to significantly reduce pest populations, reinforcing the role of plant resistance in IPM strategies. Beyond host plant resistance, biological control is widely regarded as a crucial component of IPM programs. Predatory coccinellids have garnered global interest among biological control agents due to their potential in managing diverse populations of sap-sucking pests. The predatory ladybird beetle, Adalia bipunctata L., is a polyphagous species that primarily prey on aphids, with a particular preference for the green peach aphid, Myzus persicae (Sulzer), a highly polyphagous pest responsible for significant damage to numerous field and greenhouse crops. This study aims to assess the demographic parameters of A. bipunctata, a natural predator of M. persicae when reared on bell pepper plants and treated with different plant growth stimulants. The findings could provide valuable insights into the effectiveness of biological control agents as a sustainable strategy for reducing M. persicae populations and mitigating crop damage.

Materials and Methods

In this study, the effects of zinc sulfate foliar application and the incorporation of organic fertilizer (30% vermicompost) and biological fertilizers (Bacillus subtilis, Pseudomonas fluorescens, Glomus intraradices, G. intraradices × B. subtilis, and G. intraradices × P. fluorescens) into the growth medium of bell pepper plants were investigated. The demographic parameters of the predatory ladybird beetle, Adalia bipunctata, were examined under controlled laboratory conditions at 25 ± 2°C, 65 ± 5% relative humidity, and a 16L:8D photoperiod. The experiment followed a completely randomized design (CRD) with seven treatments and a control. Pairs of male and female A. bipunctata were selected, and 100 eggs were incubated in plastic Petri dishes. The larvae were fed on Myzus persicae and subjected to the respective treatments, with results compared against the control. The developmental parameters of immature stages, including molting, larval growth, pupation, and survival rates, were recorded. After adulthood, beetles were transferred to fresh containers with host plant leaves and aphid prey. Key reproductive and population parameters were analyzed, including oviposition rate, age-specific fecundity, survival rate, life expectancy, and demographic indices. Data were processed using the age-stage, two-sex life table approach. Treatment means were compared using the paired bootstrap test, with statistical analyses performed using TWOSEX-MSChart software.
Results

The results indicate that the shortest oviposition period was observed in the vermicompost (30%), zinc sulfate, and control treatments, whereas the longest was recorded in the B. subtilis treatment. Life expectancy was highest in the B. subtilis treatment and lowest in the vermicompost (30%) treatment. Similarly, the net reproductive rate (R0) of A. bipunctata reached its highest value in the B. subtilis treatment and its lowest in the vermicompost (30%) treatment. The intrinsic rate of increase (r) was lowest in the vermicompost (30%) treatment, while the highest values were recorded in the B. subtilis, zinc sulfate, G. intraradices × B. subtilis, and P. fluorescens treatments.
Discussion

The B. subtilis and P. fluorescens treatments were the most beneficial for the two-spotted ladybird beetle, Adalia bipunctata, suggesting enhanced nutritional quality. These PGPRs interact with insects through multiple mechanisms, such as inducing resistance against herbivores or attracting natural predators. Our analysis demonstrated that different fertilizer treatments significantly impacted the population growth parameters and the biological traits of A. bipunctata. Notably, soil treatment with biological fertilizers (B. subtilis and P. fluorescens) positively and significantly affected the population dynamics of the predatory insects. These findings suggest that biological fertilizers could be integrated with biological control agents in IPM programs to improve green peach aphid (Myzus persicae) management in greenhouse environments.

کلیدواژه‌ها [English]

  • Myzus persicae
  • two-spotted ladybug
  • population growth parameters
  • bio- and organic-fertilizers
  • bell pepper
References
Akca, I., Ayvaz, T., Yazici, E., Smith, C. L., & Chi, H. (2015). Demography and population projection of Aphis fabae (Hemiptera: Aphididae): with additional comments on life table research criteria. Journal of Economic Entomology, 108(4), 1466-1478. https://doi.org/10.1093/jee/tov187.  
Alizamani, T., Razmjou, J., Naseri, B., Hassanpour, M., Asadi, A., & Kerr, C. (2017). Effect of vermicompost on life history of Hippodamia variegata preying on Aphis gossypii Glover. Journal of the Entomological Research Society, 19, 51-60.
Alizamani, T., Shakarami, J., Mardani Talaee, M., & Zibaee, A. (2022). Effect of Micronutrient Fertilizers on Digestive Enzymes Activity of Hippodamia variegata (Goeze) Fed on Myzus persicae (Sulzer). Journal of Iranian Plant Protection Research, 36(2), 213-225. https://doi.org/10.22067/JPP.2022.74291.1070.
Alizamani, T., Shakarami, J., Mardani-Talaee, M., Zibaee, A. & Serrao, J. E. (2020). Direct interaction between micronutrients and bell pepper (Capsicum annum L.), to affect fitness of Myzus persicae (Sulzer). Journal of Plant Protection Research, 60(3), 253–262. https://doi.org/10.24425/jppr.2020.133319.
Aqueel, M. A., & Leather, S. R. (2012). Nitrogen fertiliser affects the functional response and prey consumption of Harmonia axyridis (Coleoptera: Coccinellidae) feeding on cereal aphids. Annals of Applied Biology, 160(1), 6-15. https://doi.org/10.1111/j.1744-7348.2011.00514.x.
Baidoo, P. K., & Mochiah, M. B. (2011). The influence of nutrient application on the pests and natural enemies of pests of okra Abelmoschus esculentus (L.) (Moench.). Journal of Applied Biosciences, 41, 2765- 2771.
Bala, K., Sood, A. K., Pathania, V. S., & Thakur, S. (2018). Effect of plant nutrition in insect pest management: A review. Journal of Pharmacognosy and Phytochemistry, 7(4), 2737–2742. 
Bashan, Y., & Levanony, H. (1990). Current status of Azospirillum inoculation technology: Azospirillum as achallenge for agriculture. Candian Journal of. Microbiology, 36(9), 591- 608. https://doi.org/10.1139/m90-105.
Bernays, E. A., & Chapman, R. F. (1994). Host- plant selection by phytophagous insects. Chapman and Hall, New York. https://doi.org/10.1007/b102508.
Bigirimana, J., & Hofte, M. (2002). “Induction of systemic resistance to Colletotrichum lindemuthianum in bean by a benzothiadiazole derivative and Rhizobacteria. Phytoparasitica, 30, 159-168. https://doi.org/10.1111/J.1364-3703.2004.00276.X.
Birch, A. N. E., Geoghegan, I. E., Majerus, M. E., McNicol, J. W., Hackett, C. A., Gatehouse, A. M., & Gatehouse, J. A. (1999). Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Molecular Breeding, 5, 75-83. https://doi.org/10.1023/A:1009659316170.
Carey, J. R. (2001). Insect biodemography. Annual Review of Entomology, 46(1): 79- 110. https://doi.org/10.1146/annurev.ento.46.1.79.
Chavez-Mendoza, C., Sanchez, C., Munoz Marquez, E., Sida Arreola, J. P., & Flores Cordova, M. A. (2015). Bioactive compounds and antioxidant activity in different grafted varieties of bell pepper. Antioxidants, 4(2), 427-446. https://doi.org/ 10.3390/antiox4020427.
Chi, H. (2024). CONSUME-MSChart: a computer program for the age-stage, two-sex consumption rate analysis. National Chung Hsing University in Taiwan. (http://140.120.197.173/ Ecology/prod02.htm).
Chi, H., & Su, H. Y. (2006). Age-stage, two-sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate. Environmental entomology, 35(1), 10-21. https://doi.org/10.1603/0046-225X-35.1.10.
Chi, H., Kavousi, A., Gharekhani, G., Atlihan, R., Salih Özgökçe, M., Güncan, A., Gökçe, A., Smith, C.L., Benelli, G., Guedes, R.N.C., & Amir Maafi, M. (2023). Advances in theory, data analysis, and application of the age-stage, two-sex life table for demographic research, biological control, and pest management. Entomologia Generalis, 43(4), 705–732.
Chi, H., You, M., Atlıhan, R., Smith, C.L., Kavousi, A., Özgökçe, M.S., Güncan, A., Tuan, S.J., Fu, ‎J.W., Xu, Y.Y., & Zheng, F.Q. (2020). Age-Stage, two-sex life table: an introduction to theory, data ‎analysis, and application. Entomologia Generalis, 40(2).‎‏
De Clercq, P., Bonte, M., Van Speybroeck, K., Bolckmans, K., & Deforce, K. (2005). Development and reproduction of Adalia bipunctata (Col., Coccinellidae) on eggs of Ephestia kuehniella (Lep.: Phycitidae) and pollen. Pest Management Science, 61(11), 1129- 1132. https://doi.org/10.1002/ps.1111.
Fenton, B., Kasprowicz, L., Malloch, G., & Pickup, J. (2010). Reproductive performance of asexual clones of the peach-potato aphid, Myzus persicae, (Homoptera: Aphididae), colonising Scotland in relation to host plant and field ecology. Bulletin of Entomological Research, 100(4), 451–460. https://doi.org/10.1017/S0007485309990447.
Frel, A. G. H., Cardona, C., & Dorn, S. (2003). Antixenosis and antibiosis of common beans to Thrips palmi. Journal of Economic Entomology, 93, 1577- 1584.
Gadhave, K. R., Finch, P., Gibson, T. M., & Gange, A. C. (2016). Plant growthpromoting Bacillus suppress Brevicoryne brassicae field infestation and trigger density- dependent and density- independent natural enemy responses. Journal of Pest Science, 89(4), 985–992. https://doi.org/10.1007/s10340-015-0721-8
Hagbardsland, K. J. F. (2018). Multitrophic effects of the relationship between a plant growth-promoting rhizobacteria (Bacillus amyloliquefaciens) and arugula (Eruca sativa) on the predator Doru luteipes, using Plutella xlyostella and Spodoptera frugiperda (Master's thesis, Norwegian University of Life Sciences, Ås). http://hdl.handle.net/11250/2588237.
Hajek, A. E., & Eilenberg, J. (2018). Natural enemies: an introduction to biological control. Cambridge University Press. https://doi.org/10.1017/9781107280267.
Harun-or-Rashid, M., Khan, A., Hossain, M. T., & Chung, Y. R. (2017). Induction of Systemic Resistance against Aphid by Endophytic Bacillus velezensis YC7010 via Expressing Phytoalexin Deficient4 in Arabidopsis”. Frontiers in Physiology, 8, 211. https://doi.org/10.3389/fpls.2017.00211.
Harun-or-Rashid, M., Kim, H. J., Yeom, S. I., Yu, H. A., Manir, M. M., Moon, S. S., Kang, Y, J., & Chung, Y. R. (2019). Bacillus velezensis YC7010 enhances plant defenses against brown planthopper through transcriptomic and metabolic changes in rice. Frontiers in Plant Science, 9, 1904. https://doi.org/10.3389/fpls.2018.01904.
Hodek, I., & Honek, A. (1996) Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht. http://dx.doi.org/10.1007/978-94-017-1349-8.
Hodek, I., & Honêk, A. (2013). Ecology of coccinellidae (Vol. 54). Springer Science & Business Media. https://doi.org/10.1007/978-94-017-1349-8.
Hosseini, A., Hosseini, M., & Schausberger, P. (2022). Plant growth-promoting rhizobacteria enhance defense of strawberry plants against spider mites. Frontiers in Plant Science, 12, 783578. https://doi.org/10.3389/fpls.2021.783578.
Huang, H. W., Chi, H., & Smith, C. L. (2018). Linking demography and consumption of Henosepilachna vigintioctopunctata (Coleoptera: Coccinellidae) fed on Solanum photeinocarpum (Solanales: Solanaceae): with a new method to project the uncertainty of population growth and consumption. Journal of Economic Entomology, 111, 1–9. https://doi.org/10.1093/jee/ tox330.
Jha, R. K., Chi, H., & Tang, L. C. (2012). A comparison of artificial diet and hybrid sweet corn for the rearing of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) based on life table characteristics. Environmental Entomology, 41, 30-39. https://doi.org/10.1603/EN11206.
Kalushkov, P., & Hodek, I. (2004). The effects of thirteen species of aphids on some life history parameters of the ladybird Coccinella septempunctata. BioControl, 49, 21-32. https://doi.org/10.1023/B:BICO.0000009385.90333.b4.
Kindlmann, P., & Dixon, A. F. (1999). Generation time ratios—determinants of prey abundance in insect predator–prey interactions. Biological Control, 16, 133-138. https://doi.org/10.2307/2680210.
Lewontin, R. C. (1965). Selection for colonizing ability, pp. 77–94. In H. G. Baker and G. L. Stebbins (eds.), The genetics of colonizing species. Academic Press, San Diego, CA.
Liu, Z., Li, D., Gong, P., & Wu, K. (2004). Life table studies of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), on different host plants. Environmental entomology, 33, 1570-1576. https://doi.org/10.1603/0046-225X-33.6.1570.
Lucy, M., Reed, E., & Glick, B. R. (2004). Applications of free living plant growth-promoting rhizobacteria. Antonie van leeuwenhoek, 86, 1-25. https://doi.org/10.1023/B:ANTO.0000024903.10757.6e.
Mardani-Talaee, M., Nouri-Ganblani, G., Razmjou, J., Hassanpour, M., Naseri, B., & Asgharzadeh, A. (2016). Effects of chemical, organic and bio-fertilizers on some secondary metabolites in the leaves of bell pepper (Capsicum annuum) and their impact on life table parameters of Myzus persicae (Hemiptera: Aphididae). Journal of Economic Entomology, 109(3), 1231-1240. https://doi.org/10.1093/jee/tov389.
Mardani‐Talaee, M., Nouri‐Ganblani, G., Razmjou, J., Hassanpour, M., Vivekanandhan, P., & Naseri, B. (2024). Bottom‐Up Effects of Various Plant Growth Promoting Treatments on Fitness Parameters of Hippodamia variegata. Journal of Basic Microbiology, p.e2400486. https://doi.org/10.1002/jobm.202400486.
Mardani-Talaee, M., Nouri-Ganblani, G., Zibaee, A., Razmjou, J., Hassanpour, M., & Naseri, B. (2022). Effect of nutritional interaction between plant growth stimulants and peach green aphid (Myzus persicae Sulzer) on physiological processes of two-spotted ladybird (Adalia bipunctata L.). Plant Protection (Scientific Journal of Agriculture), 45, 65-82. https://doi.org/10.22055/PPR.2022.17365.
Mardani-Talaee, M., Razmjou, J., Nouri-Ganblani, G., Hassanpour, M., & Naseri, B. (2017). Impact of Chemical, Organic and Bio-Fertilizers Application on Bell Pepper, Capsicum annuum L. and Biological Parameters of Myzus persicae (Sulzer) (Hem.: Aphididae). Neotropical Entomology, 46, 578–586. https://doi.org/10.1007/s13744-017-0494-2.
Mardani-Talaee, M., Zibaee, A., Nouri-Ganblani, G., & Razmjou, J. (2016). Chemical and organic fertilizers affect physiological performance and antioxidant activities in Myzus persicae (Hemiptera: Aphididae). Invertebrate Survival Journal, 13, 122-133. https://doi.org/10.25431/1824-307X/isj.v13i1.122-133.
Marshall, S. (2014, 15 January). Lady Beetles of Ontario. http://www.uoguelph.ca/debu/lady/lady-beetles.htm.
Megali, L., Schlau, B., & Rasmann, S. (2015). Soil microbial inoculation increases corn yield and insect attack. Agronomy for Sustainable Development, 35, 1511-1519. https://doi.org/10.1007/s13593-015-0323-0.
Mirab-Balou, M., & Alizamani, T. (2021). The effect of nutritional interaction between micronutrient fertilizers and Capsicum annuum L. on the population growth of Aphidoletes aphidimyza Rondani as predator of green peach aphid. Journal of Iranian Plant Protection Research, 35, 481-494. https://doi.org/10.22067/JPP.2021.70745.1028.
Mirhosseini, M. A., Hosseini, M. R., & Jalali, M. A. (2015). Effects of diet on development and reproductive fitness of two predatory coccinellids (Coleoptera: Coccinellidae). European Journal of Entomology, 112, 446. https://doi.org/10.14411/eje.2015.051.
Mohamadi, P., Razmjou, J., Naseri, B., & Hassanpour, M. (2017). Humic fertilizer and vermicompost applied to the soil can positively affect population growth parameters of Trichogramma brassicae (hymenoptera: Trichogrammatidae) on eggs of Tuta absoluta (lepidoptera: Gelechiidae). Neotropical Entomology, 46, 678–684. https://doi.org/10.1007/s13744-017-0536-9.
Moradi, R., Shakarami, J., & Mardani-Talaee, M. (2021). Investigation of induced resistance in wheat to Sitobion avenae (Hemiptera: Aphididae) under greenhouse conditions. Journal of Agricultural Science and Technology, 23, 1057-1072.
Naeem, M., Aslam, Z., Khaliq, A., Ahmed, J. N., Nawaz, A., & Hussain, M. (2018). Plant growth promoting rhizobacteria reduce aphid population and enhance the productivity of bread wheat. Brazilian Journal of Microbiology, 49, 9–14. https://doi.org/10.1016/j.bjm.2017.10.005.
Obrycki, J. J., & Kring, T. J. (1998). Predaceous coccinellidae in biological control. Annual Review of Entomology, 43, 295-321. https://doi.org/10.1146/annurev.ento.43.1.295.
Özgökçe, M. S., Chi, H., Atlıhan, R., & Kara, H. (2018). Demography and population projection of Myzus persicae (Sulzer.) (Hemiptera: Aphididae) on five pepper (Capsicum annuum L.) cultivars. Phytoparasitica, 46, 153–167. https://doi.org/10.1007/s12600-018-0651-0.
Pervez, M. N., Stylios, G. K., Liang, Y., Ouyang, F., & Cai, Y. (2020). Low-temperature synthesis of novel polyvinylalcohol (PVA) nanofibrous membranes for catalytic dye degradation. Journal of Cleaner Production, 262, 121301. https://doi.org/10.1016/j.jclepro.2020.121301.
Pineda, A., Zheng, S. J., van Loon, J. J., Pieterse, C. M., & Dicke, M. (2010). Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends in plant science, 15, 507-514. https://doi.org/10.1016/j.tplants.2010.05.007.
Pourya, M., Shakarami, J., Mardani-Talaee, M., Sadeghi, A., & Serrao, J. E. (2021). Bio-fertilizers and micronutrients affect the digestibility, detoxification, and intermediary metabolisms of English grain aphid, Sitobion avenae, in greenhouse. Journal of Asia-Pacific Entomology, 24, 704-710. https://doi.org/10.1016/j.aspen.2021.06.003.
Pourya, M., Shakarami, J., Mardani-Talaee, M., Sadeghi, A., & Serrão, J.E. (2020). Induced resistance in wheat Triticum aestivum L. by chemical-and bio-fertilizers against English aphid, Sitobion avenae (Fabricius) (Hemiptera: Aphididae) in greenhouse. International Journal of Tropical Insect Science, 40, 1043-1052. https://doi.org/10.1007/s42690-020-00164-1.
Pourya, M., Shakarami, J., Mardani-Talaee, M., Sadeghi, A., & Serrao, J. E. (2021). Bio-fertilizers and micronutrients affect the digestibility, detoxification, and intermediary metabolisms of English grain aphid, Sitobion avenae, in greenhouse. Journal of Asia-Pacific Entomology, 24(3), 704-710. https://doi.org/10.1016/j.aspen.2021.06.003.
Price, P. W. (1997). Insect ecology. John Wiley & Sons.
Puech, C., Baudry, J., Joannon, A., Poggi, S., & Aviron, S. (2014). Organic vs. conventional farming dichotomy: does it make sense for natural enemies?. Agriculture, Ecosystems & Environment, 194, 48-57. https://doi.org/10.1016/j.agee.2014.05.002.
Ramamoorthy, V., Viswanathan, R., Raguchander, T., Prakasam, V., & Samiyappan, R. (2001). Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Protection, 20, 1-11. https://doi.org/10.1016/S0261-2194(00)00056-9.
Razmjou, J., Mohammadi, M., & Hassanpour, M. (2011). Effect of vermicompost and cucumber cultivar on population growth attributes of the melon aphid (Hemiptera: Aphididae). Journal of Economic Entomology, 104, 1379-1383. https://doi.org/10.1603/ec10120.
Schausberger, P., Peneder, S., Jürschik, S., & Hoffmann, D. (2012). Mycorrhiza changes plant volatiles to attract spider mite enemies. Functional Ecology, 26, 441-449.
Shannag, H. K., & Obeidat, W. M. (2008). Interaction between plant resistance and predation of Aphis fabae (Homoptera: Aphididae) by Coccinella septempunctata (Coleoptera: Coccinellidae). Annals of Applied Biology, 152(3), 331-337. https://doi.org/10.1111/j.1744-7348.2008.00220.x.
Southwood, R., & Henderson, P. A. (2000). Ecological Methods. Third edition, Blackwell Science, Oxford, USA.
Stella de Freitas, T. F., Stout, M. J., & Sant'Ana, J. (2019). Effects of exogenous methyl jasmonate and salicylic acid on rice resistance to Oebalus pugnax. Pest management science, 75(3), 744-752. https://doi.org/10.1002/ps.5174.
Tripathi, R. N., & Singh, R. (1990). Fecundity, reproductive rate, longevity and intrinsic rate of increase of an aphidiid parasitoid Lysiphlebia mirzai. Entomophaga, 35, 601- 610. https://doi.org/10.1007/BF02375094.
Valenzuela-Soto, J. H., Estrada-Hernández, M. G., Ibarra-Laclette, E., & Délano-Frier, J. P. (2010). Inoculation of tomato plants (Solanum lycopersicum) with growth-promoting Bacillus subtilis retards whitefly Bemisia tabaci development. Planta, 231(2), 397-410. https://doi.org/10.1007/s00425-009-1061-9.
van Lenteren, J. C., Alomar, O., Ravensberg, W. J., & Urbaneja, A. (2020). Biological Control Agents for Control of Pests in Greenhouses. In: Gullino, M., Albajes, R., & Nicot, P. (eds) Integrated Pest and Disease Management in Greenhouse Crops (pp. 409-439). https://doi.org/10.1007/978-3-030-22304-5-14.
Vargas, G., Michaud, J. P., & Nechols, J. R. (2012). Larval food supply constrains female reproductive schedules in Hippodamia convergens (Coleoptera: Coccinellidae). Annals of the Entomological Society of America, 105(6), 832-839. https://doi.org/10.1111/een.12065.
Vet, L. E., Van Lenteren, J. C., & Woets, J. 1980. The parasite‐host relationship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae) IX. A review of the biological control of the greenhouse whitefly with suggestions for future research. Zeitschrift für angewandte Entomologie, 90(1‐5), 26-51. https://doi.org/10.1017/S0007485300052214.
Wu, X. H., Zhou, X. R., & Pang, B. P. (2010). Influence of five host plants of Aphis gossypii Glover on some population parameters of Hippodamia variegata (Goeze). Journal of Pest Science, 83, 77-83.
Wyss, E., Villiger, M., Hemptinne, J. L., & Müller- Schärer, H. (1999). Effects of augmentative releases of eggs and larvae of the two- spot ladybird beetle, Adalia bipunctata, on the abundance of the rosy apple aphid, Disaphis plantaginea, in organic apple orchards. Entomologia Experimentalis et Applicata, 90(2), 167- 173. https://doi.org/10.1046/j.1570-7458.1999.00435.x.
Zúñiga, E., Suzuki, H., & Vargas, R. (1986). Control biológico de los áfidos (Homoptera: Aphididae) de los cereales en Chile. III. Multiplicación y producción masiva de depredadores y parasitoides introducidos. Agriculture Equipment and Technology, 46, 489- 494. https://doi.org/10.3989/graellsia.2016.v72.167
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