The role of nutrients and parasitoid on the interaction between the cotton aphid and the parasitoid wasp Aphidius matricariae

Document Type : Research Paper

Authors

1 Department of Plant Protection, University Campus, University of Guilan, Rasht, Iran

2 Department of Plant Protection, Isfahan Research and Education Center for Agriculture and Natural Resources, AREEO, Isfahan, Iran

3 Department of Plant Protection, Faculty of Agricultural Sciences, University of Guilan, Rasht, Iran

Abstract

To have a better understanding of sustainable management strategies of Aphis gossypii Glover (Hemiptera: Aphididae), it is necessary to determine the role of bottom-up vs. top-down forces on its population dynamics. The present study examined the effect of fertilization (bottom-up force) and parasitoid release (top-down force) on population fluctuations of A. gossypii and its parasitoid (Aphidius matricariae Haliday (Hymenoptera: Braconidae)). A factorial experiment was carried out with two factors: fertilization (0, 0.5 and 1.0 g per plant per time with a fertilizer consisted of macro- and microelements) and initial parasitoid release (0, 2 and 10 1-day-old mated females of A. matricariae per cage). The experiment was started with a 5-week-old cucumber and 10 newly emerged A. gossypii adults. After one generation of A. gossypii, A. matricariae females were introduced into cages. The treatments replicated four times in a randomized complete block design, and maintained under a standard constant environment. The number of live A. gossypii and A. matricariae adults was weekly recorded until two generations of the parasitoid had been completed. The results indicated that an increase of nutrition increased aphid density and its percentage parasitism but did not affect the parasitoid population size. In addition, parasitoid release resulted in higher parasitoid density and percentage parasitism but a reduction of aphid population size. The interaction between factors influenced the aphid population only. These findings indicated that bottom-up and top-down forces play an important role in population regulation of A. gossypii, and hence, must be considered in the pest management.

Keywords

References

Aqueel, M. A., Collins, C. M., Raza, A. M., Shehbaz, M., Tariq, M. and Leather, S. R. 2014. Effect of plant nutrition on aphid size, prey consumption and life history characteristics of green lacewing. Rice Science 21(1): 74–82.
Arancon, N. Q., Edwards, C. A., Yardim, E. N., Oliver, T., Byrnem, R. J. and Keeney, G. 2006. Suppression of two-spotted spidermite (Tetranychus urticae), mealy bugs (Pseudococcus sp.) and aphid (Myzus persicae) populations and damage by vermicomposts. Crop Protection 26: 29-39.
Aslam, M., Razaq, M. and Maalik, A. 2004. Effect of nitrogen fertilizer application on population of mustard aphid (Lipaphis erysimi Kalt.) on different canola varieties. Pakistan Journal of Entomology 26: 115–11.
Bernays, E. and Graham, M. 1988. On the evolution of host specificity in phytophagous arthropods. Ecology 69: 886–892.
Bethke, J. A., Redak, R. A. and Schuch, U. K. 1998. Melon aphid performance on chrysanthemum as mediated by cultivar, and differential levels of fertilization and irrigation. Entomologia Experimentalis et Applicata 88: 41-47.
Blazhevski, S., Kalaitzaki, A. P. and Tsagkarakis, A. E. 2018. Impact of nitrogen and potassium fertilization regimes on the biology of the tomato leaf miner Tuta absoluta. Entomologia Generalis 37(2): 157–174
Blua, M. J. and Toscano, K. 1994. Bemisia argentifolii development and honeydew production as a function of cotton nitrogen status. Environmental Entomology 23: 316-321.
Bouchet, A. S., Laperche, A., Bissuel-Belaygue, C., Snowdon, R., Nesi, N. and Stahl, A. 2016. Nitrogen use efficiency in rapeseed. A review. Agronomy for Sustainable Development 36: 18–38.
Casey, C. A. and Raupp, M. J. 1999. Supplemental nitrogen fertilization of containerized azalea does not affect performance of Azalea lace bug. Environmental Entomology 28: 998-1003.  
Chen, Y., Olson, D. M. and Ruberson, J. R. 2010. Effects of nitrogen fertilization on tritrophic interactions. Arthropod-Plant Interactions 4: 81–94.
Choudhary, A. K., Ramesh, L. and Sharma, V. 2001. Incidence of mustard aphid (Lipaphis erysimi Kalt and Myzus persicae Sulzer) in Brassica species at varying fertility levels in the mid-hill zone of Himachal Pradesh. Insect Environment 7(2): 58–59.
Clancy, K. M. and Price, P. W. 1987. Rapid herbivore growth enhances enemy attack: sublethal plant defenses remain a paradox. Ecology 68: 733-737.
Crawley, M. J. 2013. The R book. Chichester: Wiley.
Cuevas-Reyes, P., Quesada, M., Hanson, P. and Oyama, K. 2007. Interactions among three trophic levels and diversity of parasitoids: a case of top-down processes in Mexican tropical dry forest. Environmental Entomology 36: 792–800.
Cusumano A., Zhu, F., Volkoff, A. N., Verbaarschot, P., Bloem, J., Vogel, H., Dicke, M. and Poelman, E. H. 2018. Parasitic wasp-associated symbiont affects plant-mediated species interactions between herbivores. Ecology Letters 21(7): 957-967.
Daugherty, M. P. 2011. Host plant quality, spatial heterogeneity, and the stability of mite predator–prey dynamics. Experimental and Applied Acarology 53: 311–322.
Daugherty, M. P., Briggs, C. J. and Welter, S. C. 2007. Bottom-up and top-down control of pear psylla (Cacopsylla pyricola): fertilization, plant quality, and the efficacy of the predator Anthocoris nemoralis. Biological Control 43: 257–264.
Fallahpour, F., Ghorbani, R., Nassiri‑Mahallati, M. and Hosseini, M. 2019. Plant fertilization helps plants to compensate for aphid damage, positively affects predator efficiency and improves canola yield. Journal of Pest Science 93: 251–260.
Fernández, C. and Nentwig, W. 1997. Quality control of the parasitoid Aphidius colemani (Hym.: Aphidiidae) used for biological control in greenhouses. Journal of Applied Entomology 121: 447–456.
Ge, F., Liu, X., Li, H., Men, X. and Su, J. 2003. Effect of nitrogen fertilizer on pest population and cotton production. Chinese Journal of Applied Ecology 14(10): 1735-8.
Gols, R., Wagenaar, R., Poelman, E. H., Kruidhof, H. M., van Loon, J. J. A. and Harvey, J. A. 2015. Fitness consequences of indirect plant defence in the annual weed, Sinapis arvensis. Functional Ecology 29(8): 1019-1025.
Gonzaga, J. V., Ramalho, F. S. and Santos, J. W. 1991. Distribuicao de Aphis gossypii no algodoeiro nos sistemas de plantio solteiro e consorciado. Pesquisa Agropecuaria Brasileira 26: 1839–1844.
Hairston, N. G., Smith, F. E.  and Slobodkin, L. B. 1960. Community structure, population control, and competition. American Naturalist 94: 421–425.
Han, P., Niu C. Y. and Desneux, N. 2014. Identification of top-down forces regulating cotton aphid population growth in transgenic bt cotton in central China. Plos One 9(8): e102980.
Heidary, M. and Karimzadeh, J. 2014. Relative influences of plant type and parasitoid initial density on host–parasitoid relationships in a tritrophic system. Archive of Phytopathology and Plant Protection 47(19): 2392–2399.
Hoballah M. E. F. and Turlings, T. C. J. 2001. Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids. Evolutionary Ecology Research 3: 553-565.
Hosseini, A., Hosseini, M., Michaud, J. P., Awal, M. M. and Ghadamyari, M. 2019. Life history responses of Hippodamia variegata (Coleoptera: Coccinellidae) to changes in the nutritional content of its prey, Aphis gossypii (Hemiptera: Aphididae), mediated by nitrogen fertilization. Biological Control 130: 27-33.
Hosseini, M., Ashouri, A., Enkegaard, A., Weisser, W. W., Goldansaz, S. H., Nasiri Mahalati, M. and Sarraf Moayeri, H. R. 2010. Plant quality effects on intraguild predation between Orius laevigatus and Aphidoletes aphidimyza. Entomologia Experimentalis et Applicata 135: 208–216.
Hullé, M., Chaubet, B., Turpeau, E. and Simon, J. 2020. Encyclop’ Aphid: a website on aphids and their natural enemies. Entomologia Generalis 40, 97–101.
Jafari, Kh., Fathipour, Y., Bagheri, A. and Talebi, A. A. 2020. Tritrophic interactions in a wheat (Triticum aestivum), aphid (Rhopalosiphum padi) and parasitoid (Aphidius matricariae) system. Crop Protection 130: 105076.
Jansson, R. K., Leibee, G. L., Sanchez, C. A. and Lecrone, S. H. 1991. Effects of nitrogen and foliar biomass on population parameters of cabbage insects. Entomologia Experimentalis et Applicata 61: 7–16.
Kalule, T. and Wright, D. J. 2002. Tritrophic interactions between cabbage cultivars with different resistance and fertilizer levels, cruciferous aphids and parasitoids under field conditions. Bulletin of Entomological Research 92: 61–69.
Karimzadeh, J. and Besharatnejad, M. H. 2019. Ecological control of Plutella xylostella (Lepidoptera, Plutellidae) using trap cropping and Bt applications. Archives of Phytopathology and Plant Protection 52(19-20): 1326-1347.
Karimzadeh, J. and Wright, D. J. 2008. Bottom-up cascading effects in a tritrophic system: interactions between plant quality and host-parasitoid immune responses. Ecological Entomology 33: 45-52.
Karimzadeh, J., Bonsall, M. B. and Wright, D. J. 2004. Bottom-up and top-down effects in a tritrophic system: the population dynamics of Plutella xylostella (L.)-Cotesia plutellae (Kurdjumov) on different host plants. Ecological Entomology 29: 285-293.
Karimzadeh, J., Hardie, J. and Wright, D. J. 2013. Plant resistance affects the olfactory response and parasitism success of Cotesia vestalis. Journal of Insect Behavior 26: 35–50.
Kersting, U., Satar, S. and Uygun, N. 1999. Effect of temperature on development rate and fecundity of apterous Aphis gossypii Glover (Homoptera: Aphididae) reared on Gossypium hirsutum L. Journal of Applied Entomology 123: 23-27.
Khodayari, S. and Abedini, F. 2019. Effect of Fosfalim-k foliar spray in cucumber on some characteristics of host plant and life table parameters of two-spotted spider mite. Plant Pest Research 9(2): 1-13. (in Farsi)
Leite, M. V., dos Santos, T. M., Souza, B., Calixto, A. M. and Carvalho, C. F. 2006. Biologia de Aphis gossypii Glover, 1877 (Hemiptera: Aphididae) em abobrinha cultivar Caserta (Cucurbita pepo L.) em diferentes temperaturas. Ciencia e Agrotecnologia 32: 1394–1401.
Luna, J. M. 1988. Influence of soil fertility practices on agricultural pests. In: Proceedings of the Sixth International Science Conference of IFOAM on Global Perspectives on Agroecology and Sustainable Agricultural Systems, Santa Cruz, CA, pp. 589-600.
Mardani-Talaee, M., Zibaee, A., Nouri-Ganblani, G. and Razmjou, J. 2016. Chemical and organic fertilizers affect physiological performance and antioxidant activities in Myzus persicae (Hemiptera: Aphididae). Invertebrate Survival Journal 13: 122-133.
Moon, D. C., Rossi, A. M. and Stiling, P. 2000. The effects of a biotical induced changes in host plant quality (and morphology) on a salt marsh plant hopper and its parasitoid. Ecological Entomology 25: 325–331.
Mooney, K. A., Pratt, R. T. and Singer, M. S. 2012. The tri-trophic interactions hypothesis: interactive effects of host plant quality, diet breadth and natural enemies on herbivores. PLoS ONE 7(4): e34403.
Oltean, I., Covaci, A. A., Florian, T. and Matei, C. 2012. Frankliniella occidentalis (Thysanoptera: Thripidae) population dynamics on cucumber crop. Bulletin of the University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca 69(1): 77-80.
Pinto, Z. V., Rezende, J. A. M., Yuki, V. A. and Piedade, S. M. S. 2008. Ability of Aphis gossypii and Myzus persicae to transmit Cucumber mosaic virus in single and mixed infection with two Potyviruses to zucchini squash. Summa Phytopathologica 34(2): 183–185.
Poelman E. H., Zheng, S. J., Zhang, Z., Heenskerk, N. M., Cortesero, A. M. and Dicke, M. 2011. Parasitoid-specific induction of plant responses to parasitized herbivores affects colonization by subsequent herbivores. Proceedings of the National Academy of Science of the United State of America 108(49): 19647-19652. 
Price, P. W., Bouton, C. E., Gross, P., Mc Pheron, B. A. N., Thompson, J. N. and Weis, A. E. 1980. Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology, Evolution, and Systematics 11: 41–65.
Rezaei, M., Talebi, A. A., Fathipour, Y., Karimzadeh, J. and Mehrabadi, M. 2019. Foraging behavior of Aphidius matricariae (Hymenoptera: Braconidae) on tobacco aphid, Myzus persicae nicotianae (Hemiptera: Aphididae). Bulletin of Entomological Research 109(6): 840-848.
Rossi, A. M., Brodbeck, B. V. and Strong, D. R. 1996. Response of xylem-feeding leafhopper to host plant species and plant quality. Journal of Chemical Ecology 22(4): 653-671.
Rouhani, M., Samih, M. A. and Esmaeilizadeh, M. 2012. Evaluation of effects of two spring applications of micronutrients on the population density of common pistachio psylla (Agonoscena pistaciae) in pistachio orchards. Journal of Plant Protection Research 52(3): 314-318.
Sarfraz, M., Dosdall, L. M. and Keddie, B. A. 2009. Host plant nutritional quality affects the performance of the parasitoid Diadegma insulare. Biological Control 51: 34–41.
Sarwar, M. 2011. Effects of Zinc fertilizer application on the incidence of rice stem borers (Scirpophaga species) (Lepidoptera: Pyralidae) in rice (Oryza sativa L.) crop. Journal of Cereals Oilseeds 2(5): 61-65.
Shobana, S., Krishnaswamy, K., Sudha, V., Malleshi, N. G., Anjana, R. M., Palaniappan, L. and Mohan, V. 2013. Finger millet (Ragi, Eleusine coracana L.). A review of its nutritional properties, processing, and plausible health benefits. Advances in Food and Nutrition Research 69: 1–39. 
Sial, M. U., Zhao, Z., Zhang, L., Zhang, Y., Mao, L. and Jiang, H. 2018. Evaluation of insecticides induced hormesis on the demographic parameters of Myzus persicae and expression changes of metabolic resistance detoxification genes. Sci. Rep. UK 8, 16601.
Sinha, R., Singh, B., Rai, P. K., Kumar, A., Jamwal, S. and Sinha, B. K. 2018. Soil fertility management and its impact on mustard aphid, Lipaphis erysimi (Kaltenbach) (Hemiptera: Aphididae). Food Science and Technology 4: 1450941.
Staley, J. T., Girling, R. D., Stewart-Jones, A., Poppy, G. M., Leather, S. R. and Wright, D. J. 2011. Organic and conventional fertilizer effects on a tritrophic interaction: parasitism, performance and preference of Cotesia vestalis. Journal of Applied Entomology 135: 658–665.
Tan, C. W., Peiffer, M. L., Ali J. G., Luthe, D. S. and Gray, W. 2020. Top-down effects from parasitoids may mediate plant defense and plant fitness. Functional Ecology 34(9): 1767-1778.
Tan, C. W., Peiffer, M., Hoover, K., Rosa, C. and Felton, G. W. 2019. Parasitic wasp mediates plant perception of insect herbivores. Journal of Chemical Ecology 45: 972-981.
Tan, C. W., Peiffer, M., Hoover, K., Rosa, C., Acevedo, F. E. and Felton, G. W. 2018. Symbiotic polydnavirus of a parasite manipulates caterpillar and plant immunity.  Proceedings of the National Academy of Science of the United State of America 115(20): 5199-5204.
Tazerouni, Z., Talebi, A. A. and Rezaei, M. 2019. Functional response of parasitoids: its impact on biological control. In: Donnelly, E.(Ed.) Parasitoids: Biology, behavior, and ecology, Nova Science Publishers. pp 35-58.
Tazerouni, Z., Talebi, A. A., Fathipour, Y. and Soufbaf, M. 2017. Age-specific functional response of Aphidius matricariae and Praon volucre (Hym.: Braconida) on Aphis gossypii (Hem.: Aphididae). Journal of Entomological Society of Iran 36(4): 239–248.
Ulber, B., Eickermann, M. and Mennerich, D. 2006. The parasitism of ceutorhynchid stem weevils onBrassica host plants. Proceedings Symposium on Integrated Pest Management in Oilseed Rape, 3–5 April 2006, Göttingen, Germany.
Vidal, M. C. and Murphy, S. M. 2018. Bottom-up vs. top-down effects on terrestrial insect herbivores: A meta-analysis. Ecology Letters 21(1): 138–150.
Walters, K. F. A., Young, J. E. B., Kromp, B. and Cox, P. D. 2003. Management of oilseed rape pests. In: Alford, D. V. (Ed) Biocontrol of oilseed rape pests. Blackwell Science Ltd., Oxford, pp 43–71.
White, T. C. R. 1978. The importance of a relative shortage of food in animal ecology. Oecologia 33: 71–86.
Yuan, H.B., Li, J.H., Liu, Y.Q., Cui, L., Lu, Y.H., Xu, X.Y., Li, Z., Wu, K.M. and Desneux, N. 2017. Lethal, sublethal and transgenerational effects of the novel chiral neonicotinoid pesticide cycloxaprid on demographic and behavioral traits of Aphis gossypii (Hemiptera: Aphididae). Insect Science 24: 743–752.
Zaller, J. G., Moser, D., Drapela, T., Schmöger, C. and Frank, T. 2009. Parasitism of stem weevils and pollen beetles in winter oilseed rape is differentially affected by crop management and landscape characteristics. Biological Control 54: 505–514.
Zhong-Xian, L. U., Xiao-Ping, Y. U., Kong-Luen, H. and Cui, H. U. 2007. Effect of nitrogen fertilizer on herbivores and its stimulation to major insect pests in rice. Rice Science 14(1): 56–66.
Zhu F., Broekgaarden, C., Weldegergis, B. T., Harvey, J. A., Vosman, B., Dicke, M. and Poelman, E. H. 2015. Parasitism overrides herbivore identity allowing hyperparasitoids to locate their parasitoid host using herbivore-induced plant volatiles. Molecular Ecology 24(11): 2886-2899.
Plant Pest Research
Volume 12, Issue 1
June 2022
Pages 27-41

Files

History

  • Receive Date: 13 June 2022
  • Accept Date: 13 June 2022

Share

How to cite

Statistics