Abstract
The efficiency of natural enemies may be affected by different agricultural practices. We investigated the functional response of the seven-spot ladybird, Coccinella septempunctata L. adults to different densities of the cabbage aphid, Brevicoryne brassicae L., reared on four treated canola plants including: control, humic acid (HA), salicylic acid (SA), and a mixed application of humic acid and salicylic acid (HA + SA). Based on logistic regression analysis, C. septempunctata adults exhibited a type II functional response in all treatments. The higher attack rate (a) and shorter handling time (Th) of adult males were significantly obtained in SA. The handling time of adult females on different treatments were not significant, but their attack rates were significantly higher in HA + SA and SA. Based on the results, more aphids were consumed in SA and HA + SA. Based on the results, the amount of total flavonoid contents (TFC) and phenolic contents (TPC) in canola leaves was not significant, but the levels of total Glucosinolates (GLS) were significantly high in HA + SA and SA. The results of this study revealed that SA and HA + SA can positively affect the functional response of C. septempunctata to B. brassicae.
Similar content being viewed by others
References
Aljalaly SAS, Al-Mentafji HN, Al-Arzawazi AL (2018) The effect of salicylic acid, fertilizer NPKZn and water stress on the pepper plant, Capsicum annuum L. J Pharm Sci Res 14:705–712
Aqueel MA, Leather SR (2012) Nitrogen fertilizer affects the functional response and prey consumption of Harmonia axyridis (Coleoptera: Coccinellidae) feeding on cereal aphids. Ann Appl Biol 160:6–15
Aqueel MA, Raza AM, Balal RM, Shahid MA, Mustafa I, Javaid MM, Leather SR (2015) Tritrophic interactions between parasitoids and cereal aphids are mediated by nitrogen fertilizer. Insect Sci 22:813–820
Arancon NQ, Lee S, Edwards CA, Atiyeh RM (2003) Effects of humic acids derived from cattle, food and paper-waste vermicomposts on growth of greenhouse plants. Pedobiologia. 47:741–744
Arancon NQ, Edwards CA, Lee S, Byrne R (2006) Effects of humic acids from vermicomposts on plant growth. Eur J Soil Biol 42:65–69
Asiimwe P, Naranjo S, Ellsworth PC (2013) Relative influence of plant quality and natural enemies on the seasonal dynamics of Bemisia tabaci (Hemiptera: Aleyrodidae) in cotton. J Econ Entomol 106:1260–1273
Blackman RL, Eastop VF (2000) Aphids on the world’s crops: an identification and information guide. Wiley, London, 467p
Chaplin-Kramer R, Kliebenstein D, Chiem A, Morrill E, Mills NJ, Kremen C (2011) Chemically mediated tritrophic interactions: opposing effects of glucosinolates on a specialist herbivore and its predators. J Appl Ecol 48:880–887
Cheeke PR (1989) Toxicants of plant origin. Volume IV, Phenolics. Boca Raton CRC Press, Boca Raton
Chen Y, Ruberson JR, Olson DM (2008) Nitrogen fertilization rate affects feeding, larval performance, and oviposition preference of the beet armyworm, Spodoptera exigua, on cotton. Entomol Exp Appl 126:244–255
Cipollini D, Stevenson R, Enright S, Eyles A, Bonello P (2008) Phenolic metabolites in leaves of the invasive shrub, Lonicera maackii, and their potential phytotoxic and anti-herbivore effects. J Chem Ecol 34:144–152
Clarke DB (2010) Glucosinolates, structures and analysis in food. Anal Methods 2:310–325
Desneux N, Ramirez-Romero R (2009) Plant characteristics mediated by growing conditions can impact parasitoid’s ability to attack host aphids in winter canola. J Pest Sci 82:335–342
Dixon AFG (2000) Insect predator-prey dynamics: ladybird beetles and biological control. Cambridge University Press, Cambridge
Elhamahmy MAM, Mahmoud MF, Bayoumi TY (2016) The effect of applying exogenous salicylic acid on aphid infection and its influence on histo-physiological traits and thermal imaging of canola. Cercetări Agronomice în Moldova 49:67–85
Fuenzalida T (2015) Plant natural defense against insects: role of secondary metabolites. Sntiago. 1-24
Fürstenberg-Hägg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. Int J Mol Sci 14:10242–10297
Garratt MPD, Leather SR, Wright DJ (2010) Tritrophic effects of organic and conventional fertilisers on a cereal–aphid–parasitoid system. Entomol Exp Appl 134:211–219
Gols R (2014) Direct and indirect chemical defences against insects in a multitrophic framework. Plant Cell Environ 37:1741–1752
Guo B, Liu C, Liang Y, Li N, Fu Q (2019) Salicylic acid signals plant defence against cadmium toxicity. Int J Mol Sci 20:2960. https://doi.org/10.3390/ijms20-122960
Gupta RK, Pervez A, Guroo MA, Srivastava K (2012) Stage-specific functional response of an aphidophagous ladybird, Coccinella septempunctata (Coleoptera: Coccinellidae), to two aphid species. Int J Trop Insect Sci 32:136–141
Halkier BA (1999) Glucosinolates. In: Ikan R (ed) Naturally occurring glycosides: chemistry distribution and biological properties. John Wiley and Sons, pp 193–223
Hassell M (2000) The spatial and temporal dynamics of host parasitoid interactions. Oxford University Press, Oxford
Hodek I, Honek A (1996) Ecology of Coccinellidae. Kluwer Academic, Dordrecht, Boston, London, 464 pp
Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398
Hosseini A, Hosseini M, Michaud JP, Modarres Awal M, Ghadamyari H (2018) Nitrogen fertilization increases the nutritional quality of Aphis gossypii (Hemiptera: Aphididae) as prey for Hippodamia variegata (Coleoptera: Coccinellidae) and alters predator foraging behavior. J Econ Entomol 111:2059–2068
Ishida M, Kakizaki T, Ohara T, Morimitsu Y (2011) Development of a simple and rapid extraction method of glucosinolates from radish roots. Breed Sci 61:208–211
Jervis MA, Kidd NAC (1996) Insect natural enemies: practical approaches to their study and evaluation. Chapman and Hall, London, 491 pp
Juliano SA (2001) Non-linear curve fitting: predation and functional response curves. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman and Hall, New York, pp 178–196
Karami A, Fathipour Y, Talebi AA, Reddy GVP (2018) Parasitism capacity and searching efficiency of Diaeretiella rapae parasitizing Brevicoryne brassicae on susceptible and resistant canola cultivars. J Asia Pac Entomol 21:1095–1101
Khaled H, Fawy HA (2011) Effect of different levels of humic acids on the nutrient content, plant growth, and soil properties under conditions of salinity. Soil Water Res 61:21–29
Kibrom G, Kebede K, Weldehaweria G, Dejen G, Mekonen S, Gebreegziabher E, Nagappan R (2012) Field evaluation of aqueous extract of Melia azedarach Linn. seeds against cabbage aphid, Brevicoryne brassicae Linn. (Homoptera: Aphididae), and its predator Coccinella septempunctata Linn. (Coleoptera: Coccinellidae). Arch Phytopathology Plant Protect 45:1273–1279
Kos M, Houshyani B, Achhami BB, Rafal Wietsma R, Gols R, Weldegergis BT, Kabouw P, Bouwmeester HJ, LEM V, Dicke M, Van Loon JJA (2012) Herbivore-mediated effects of glucosinolates on different natural enemies of a specialist aphid. Chem Ecol 38:100–115
Krizek DT, Brita SJ, Mirecki RM (1998) Inhibitory effects of ambient level of solar UV-A and UV-B on growth of cv. New Red Fire lettuce Physiol Plant 103:1–7
Lill JT, Marquis RJ (2001) The effects of leaf quality on herbivore performance and attack from natural enemies. Oecologia. 126:418–428
Lu ZX, Yu XP, Heong KL, Hu C (2007) Effect of nitrogen fertilizer on herbivores and its stimulation to major insect pests in rice. Rice Sci 14:56–66
Luck RF (1985) Principles of arthropod predation. In: Huffaker CB, Rabb RL (eds) Ecological entomology. Wiley, New York, pp 497–530
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). Neotrop Entomol 46:678–684. https://doi.org/10.1007/s13744-017-0536-9
Møller P, Ploger A, Sørensen H (1985) Quantitative analysis of total glucosinolate content in concentrated extracts from double low rapeseed by the Pd-glucosinolate complex method. In: Sørensen H (ed) Advances in the production and utilization of cruciferous crop. Martinus Nijhoff/DR W. Junk Publishers, Dordrecht, pp 97–110
Mottaghinia L, Hassanpour M, Razmjou J, Hosseini M, Chamani E (2015) Functional response of Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae) to Aphis gossypii glover (Hemiptera: Aphididae): effects of vermicompost and host plant cultivar. Neotrop Entomol. 45:88–95. https://doi.org/10.1007/s13744-015-0343-0
Nuessly GS, Scully BT, Hentz MG, Beiriger R, Snook ME, Widstrom NW (2007) Resistance to Spodoptera frugiperda (Lepidoptera: Noctuidae) and Euxesta stigmatias (Diptera: Ulidiidae) in sweet corn derived from exogenous and endogenous genetic systems. J Econ Entomol 100:1887–1895
Oberdorster E, Clay MA, Cottam DM, Wilmot FA, Mclachlan JA, Milner MJ (2001) Common phytochemicals are ecdysteroid agonists and antagonists: a possible evolutionary link between vertebrate and invertebrate steroid hormones. J Steroid Biochem Mol Biol 77:229–238
Omkar O, Srivastava S (2003) Functional response of the sevenspotted lady beetle, Coccinella septempunctata Linnaeus on the mustard aphid, Lipaphis erysimi (Kaltenbach). Int J Trop Insect Sci 23:149–152
Otieno BA (2005) A study of the factors influencing aphids as vectors of viral diseases of Brassica oleracea (kale and cabbage) in Kenya. MSc thesis in zoology (agricultural entomology), Department of Zoology, University of Nairobi
Painter RH (1951) Insect resistance in crop plants. Macmillan, New York, 520 pp
Pervez A, Omkar O (2005) Functional responses of coccinellid predators: an illustration of a logistic approach. J Insect Sci 5:1–6
Pratt C, Pope TW, Powell G, Rossiter JT (2008) Accumulation of glucosinolates by the cabbage aphid Brevicoryne brassicae as a defense against two Coccinellid species. J Chem Ecol 34:323–329
Rogers DJ (1972) Random search and insect population models. J Anim Ecol 41:369–383
Ronald SF, Laima SK (1999) Phenolics and cold tolerance of Brassica napus. Ontario, Department of Plant Agriculture
Sabelis MW (1992) Predatory arthropods. In: Crawley MJ (ed) Natural enemies: the population biology of predators, parasites and diseases. Blackwell, Oxford, pp 225–264
Sattari Nasab R, Pahlavan Yali M, Bozorg-Amirkalaee M (2018) Effect s of humic acid and plant growth-promoting rhizobacteria (PGPR) on induced resistance of canola to Brevicoryne brassicae L. Bull Entomol Res. https://doi.org/10.1017/S00074853180-00779
Shivaji R, Camas A, Ankala A, Engelberth J, Tumlinson JH, Williams WP, Wilkinson JR, Luthe DS (2010) Plants on constant alert: elevated levels of jasmonic acid and jasmonate-induced transcripts in caterpillar-resistant maize. J Chem Ecol 36:179–191
Simmonds MSJ (2001) Importance of flavonoids in insect-plant interactions: feeding and oviposition. Phytochemistry. 56:245–252
SPSS (2015) SPSS 22.0 for Windows. SPSS Inc, Chicago
Thakur T, Sangha MK, Arora R, Javed M (2016) Effect of foliar spray of elicitors on status of defense proteins in relation to mustard aphid infestation in crop Brassica cultivars. J Appl Nat Sci 8:2242–2248
Veeravel R, Baskaran P (1997) Searching behaviour of two coccinellid predators, Coccinella transversalis Fab. and Cheilomenes sexmaculatus Fab., on eggplant infested with Aphis gossypii Glov. Int J Trop Insect Sci 17:363–368
War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320
Watt KEF (1959) A mathematical model for the effect of densities of attacked and attacking species on the number attacked. Can Entomol 91:129–144
Wink M (2018) Plant secondary metabolites modulate insect behavior-steps toward addiction? Front Physiol 9. https://doi.org/10.3389/fphys.2018.00364
Yang M, Zheng C, Zhou Q, Liu C, Li W, Huang F (2014) Influence of microwaves treatment of rapeseed on phenolic compounds and canola content. J Agric Food Chem 62:1956–1963
Yildirim EM, Unay A (2011) Effects of different fertilizations on Liriomyza trifolii (Burgess) (Diptera: Agromyzidae) in tomato. Afr J Agric Res 6:4104–4107
Zhang Q, Xiao S (2015) Lipids in salicylic acid mediated defense in plants: focusing on the roles of phosphatidic acid and phosphatidylinositol 4-phosphate. Front Plant Sci 6:387. https://doi.org/10.3389/fpls.2015.00387
Funding
This work was funded by Shahid Bahonar University of Kerman, Iran.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
No potential conflict of interest was reported by the authors.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Yali, M.P., Sattari_Nassab, R. Evaluating the biological control capability of Coccinella septempunctata on canola plants treated with humic acid and salicylic acid via functional response experiments. Int J Trop Insect Sci 40, 1031–1041 (2020). https://doi.org/10.1007/s42690-020-00162-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42690-020-00162-3