Abstract
Intraguild predation (IGP)–the predation of a natural enemy species upon another one sharing a prey species–is relatively frequent in both natural and agroecosystems. This may reduce pest control and the establishment of predator populations during mass release of biological control agents or in multi-predator systems due to increased mortality of predators. IGP is exacerbated in isolated and space-limited systems such as greenhouses, due to reduced food resources and movement. Therefore, adding food resources as an alternative to the main prey, such as floral resources, could reduce IGP between natural enemies in these systems. In the present study we investigated the role of supplemental floral resources to help reduce intra- and interspecific IGP involving Harmonia axyridis and Propylea japonica (Coleoptera: Coccinellidae) in laboratory conditions, and we tested its application in a greenhouse setup. We found a significant reduction in intra- and interspecific IGP in laboratory conditions when floral resources were abundant. At a greenhouse scale, abundances of both ladybird species increased when floral resources were abundant, potentially through a combination of enhanced fertility and reduced IGP. This resulted in reduced abundances of aphid pest populations on tomato crops. Our study demonstrates that companion plants in greenhouses can improve pest control in systems with multi-species biological control agent releases.
Similar content being viewed by others
6. References
Albajes R, Ghullino ML, van Lenteren JC, Elad Y (2000) Integrated pest and disease management in greenhouse crops. Luwer Academic Publishers, Dordrecht, Netherlands
Albrecht M, Kleijn D, Williams NM, Tschumi M, Blaauw BR, Bommarco R, Campbell AJ, Dainese M, Drummond FA, Entling MH, Ganser D, Arjen de Groot G, Goulson D, Grab H, Hamilton H, Herzog F, Isaacs R, Jacot K, Jeanneret P, Jonsson M, Knop E, Kremen C, Landis DA, Loeb GM, Marini L, McKerchar M, Morandin L, Pfister SC, Potts SG, Rundlöf M, Sardiñas H, Sciligo A, Thies C, Tscharntke T, Venturini E, Veromann E, Vollhardt IM, Wäckers F, Ward K, Wilby A, Woltz M, Wratten S, Sutter L (2020) The effectiveness of flower strips and hedgerows on pest control, pollination services and crop yield: a quantitative synthesis. Ecol Lett 23:1488–1498
Amarasekare P (2008) Coexistence of intraguild predators and prey in resource-rich environments. Ecology 89:2786–2797
Aparicio Y, Gabarra R, Arno J (2020) Interactions among Myzus persicae, predators and parasitoids may hamper biological control in Mediterranean peach orchards. Entomol Gen 40:217–228
Balzan MV, Bocci G, Moonen AC (2016) Utilization of plant functional diversity in wildflower stripes for the delivery of multiple agroecosystem service. Entomol Exp Appl 158:304–319
Barbosa PA (1998) Conservation biological control. Academic Press
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Stat Comput 67:1–48
Berkvens N, Landuyt C, Deforce K, Berkvens D, Tirry L, Clercq P (2010) Alternative foods for the multicoloured asian lady beetle Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 107:189–195
Biondi A, Zappalà L, Di Mauro A, Garzia GT, Russo A, Desneux N, Siscaro G (2016) Can alternative host plant and prey affect phytophagy and biological control by the zoophytophagous mirid Nesidiocoris tenuis. BioControl 61:79–90
Bommarco R, Ekborm B (2000) Landscape management and resident generalist predators in annual crop systems. In: Ekbom B, Irwin ME, Robert Y (eds) Interchanges of insects between agricultural and surrounding landscapes. Springer, Netherlands
Burgio G, Santi F, Maini S (2002) On intra-guild predation and cannibalism in Harmonia axyridis (Pallas) and Adalia bipunctata L. (Coleoptera: Coccinellidae). Biol Control 24:10–116
Cai ZP, Ouyang F, Su JW, Zhang XR, Liu CL, Xiao YL, Zhang JP, Ge F (2020) Attraction of adult Harmonia axyridis to volatiles of the insectary plant Cnidium monnieri. Biol Control 143:104189
Cai Z, Fang O, Chen J, Yang QF, Desneux N, Xiao YL, Zhang J, Ge F (2021) Biological control of Aphis spiraecola in apples using an insectary plant that attracts and sustains predators. Biol Control 155:104532
Chailleux A, Bearez P, Pizzol J, Amiens-Desneux E, Ramirez-Romero R, Desneux N (2013) Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest Tuta absoluta. J Pest Sci 86:533–541
Chailleux A, Stirnemann A, Leyes J, Deletre E (2019) Manipulating natural enemy behavior to improve biological control: attractants and repellents of a weaver ant. Entomol Gen 38:191–210
Damien M, Le Lann C, Desneux N, Alford L, Al Hassan D, Georges R, Van Baaren J (2017) Flowering cover crops in winter increase pest control but not trophic link diversity. Agr Ecosyst Environ 247:418–425
Damien M, Llopis S, Desneux N, van Baaren J, Lann C (2020) How does floral nectar quality affect life history strategies in parasitic wasps? Entomol Gen 40:147–156
Desneux N, Decourtye A, Delpeuch J (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106
Eitzinger B, Abrego N, Gravel D, Huotari T, Vesterinen EJ, Roslin T (2019) Assessing changes in arthropod predator-prey interactions through DNA-based gut content analysis-variable environment, stable diet. Mol Ecol 28:266–280
El-Kareim A, Rashed AA, Marouf AE, Fouda SR (2019) Attractiveness and effects of some flowering plants on the longevity and foraging behavior of certain predatory insects. J Plant Protect Pathol 10:537–541
Fedriani JM, Fuller TK, Sauvajot RM, York EC (2000) Competition and intraguild predation among three sympatric carnivores. Oecologia 125:258–270
Foti MC, Peri E, Wajnberg E, Colazza S, Rostás M (2019) Contrasting olfactory responses of two egg parasitoids to buckwheat floral scent are reflected in field parasitism rates. J Pest Sci 92:747–756
Gagnon AÈ, Heimpel GE, Brodeur J (2015) The ubiquity of intraguild predation among predatory arthropods. PLoS ONE 6:e28061
Gao XY, Shi J, Qiao ZH, Lv DL, Wu HC (2016) Study on the synergistic predation effects of Harmonia axyridis and Propylea japonica on Aphis gossypii. Agric Technol 36:19–20
Gardarin A, Plantegenest M, Bischoff A, Valantin-Morison M (2018) Understanding plant-arthropod interactions in multitrophic communities to improve conservation biological control: useful traits and metrics. J Pest Sci 91:943–955
Gontijo LM (2018) Engineering natural enemy shelter to enhance conservation biological control in field crops. Biol Control 130:155–163
Gurr GM, Wratten SD, Landis DA, You M (2017) Habitat management to suppress pest populations: progress and prospects. Annu Rev Entomol 62:91–109
Hartig F (2019) DHARMa: Residual Diagnostics for Hierarchical (Multi–Level / Mixed) Regression Models. R package version 0.2.4. https://CRAN.R-project.org/package=DHARMa
Hatt S, Osawa N (2019) The role of Perilla frutescens flowers on fitness traits of the ladybird beetle Harmonia axyridis. BioControl 64:381–390
Hatt S, Xu Q, Francis F, Osawa N (2019) Aromatic plants of East Asia to enhance natural enemies towards biological control of insect pests. Entomol Gen 38:275–315
Hironori Y, Katsuhiro S (1997) Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga 42:153–163
Hodek I, Michaud JP (2008) Why is Coccinella septempunctata so successful? (A point-of-view). Eur J Entomol 105:1–12
Hodek I, van Emden HF, Honěk A (2012) Ecology and behaviour of the ladybird beetles (Coccinellidae). Wiley
Jaworski CC, Xiao D, Xu QX, Ramirez-Romero R, Guo XJ, Wang S, Desneux N (2019) Varying the spatial arrangement of synthetic herbivore-induced plant volatiles and companion plants to improve conservation biological control. J Appl Ecol 56:1176–1188
Jonsson M, Kaartinen R, Straub CS (2017) Relationships between natural enemy diversity and biological control. Curr Opin Insect Sci 20:1–6
Koch RL (2003) The multicolored Asian lady beetle, Harmonia axyridis: A review of its biology, uses in biological control, and non-target impacts. J Insect Sci. https://doi.org/10.1093/jis/3.1.32
Koch RL, Galvan TL (2008) Bad side of a good beetle: the north American experience with Harmonia axyridis. BioControl 53:23–25
Kuroda T, Miura K (2003) Comparison of the effectiveness of two methods for releasing Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) against Aphis gossypii Glover (Homoptera: Aphididae) on cucumbers in a greenhouse. Appl Entomol Zool 38:271–274
Lamichhane JR, Barzman M, Booij K, Boonekamp P, Desneux N, Huber L, Kudsk P, Langrell SRH, Ratnadass A, Ricci P, Sarah J-L, Messéan A (2015) Robust cropping systems to tackle pests under climate change. Agron Sustain Dev 35:443–459
Landis DA, Wratten SD, Gurr GM (2000) Habitat manipulation to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201
Lanzoni A, Accinelli G, Bazzocchi GG, Burgio G (2004) Biological traits and life table of the exotic Harmonia axyridis compared with Hippodamia variegata, and Adalia bipunctata (Col., Coccinellidae). J Appl Entomol 128:298–306
Lei ZL, Zong LB, Yang GJ, Xiao C (1988) The influence of temperature on development and predation to larvae of Propylea japonica (Thunberg). Zool Res 9:50
Lenth R (2019) emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.3.5. https://CRAN.R-project.org/package=emmeans
Li MT (2013) Biological characteristics and control method of Myzus persicae (Sulzer). J Agric Catastrophol 3:1–4
Li S, Tan XL, Desneux N, Benelli G, Zhao J, Li XH, Zhang F, Gao XW, Wang S (2015) Innate positive chemotaxis to pollen from crops and banker plants in predaceous biological control agents: towards new field lures? Sci Rep 5:12729
Li S, Jaworski CC, Hatt S, Zhang F, Desneux N, Wang S (2021a) Flower strips adjacent to greenhouses help reduce pest populations and insecticide applications inside organic commercial greenhouses. J Pest Sci 94:679–689
Li H, Li B, Lövei GL, Kring TJ, Obrycki JJ (2021b) Interactions among native and non-native predatory Coccinellidae influence biological control and biodiversity. Ann Entomol Soc Am. https://doi.org/10.1093/aesa/saaa047
Liu YJ, Yu JX, Zhou G, Dai LX, Yang ZQ, Zhang LN (2012) Evaluation of biological control of Monochamus alternatus by releasing Scleroderma sichuanensis and Dastarus helophoroides. Hunan For Sci Technol 39:20–23
Lu YH, Wu KM, Jiang YY, Guo YY, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362–365
Lu ZX, Zhu PY, Gurr GM, Zheng XS, Read DME, Heong KL, Yang YJ, Xu HX (2014) Mechanisms for flowering plants to benefit arthropod natural enemies of insect pests: prospects for enhanced use in agriculture. Insect Sci 21:1–12
Ma YY, Zhang F, Wang S, Di N (2019) Synergistic effect of functional plant Calendula officinalis (Asterales: Asteraceae) to the colonization of Coccinella septempunctata (Coleoptera: Coccinellidae) in greenhouse. J Environ Entomol 41:276–282
Mathews CR, Brown MW, Wäckers FL (2016) Comparison of peach cultivars for provision of extrafloral nectar resources to Harmonia axyridis (Coleoptera: Coccinellidae). Environ Entomol 45:649–658
Michaud JP (2010) A comparative study of larval cannibalism in three species of ladybird. Ecol Entomol 28:92–101
Mirande L, Desneux N, Haramboure M, Schneider MI (2015) Intraguild predation between an exotic and a native coccinellid in Argentina: the role of prey density. J Pest Sci 88:155–162
Mohammadpour M, Hosseini M, Michaud JP, Karimi J, Hosseininaveh V (2020) The life history of Nabis pseudoferus feeding on Tuta absoluta eggs is mediated by egg age and parasitism status. Biol Control 151:104401. https://doi.org/10.1016/j.biocontrol.2020.104401
Ortiz-Martínez S, Staudacher K, Baumgartner V, Traugott M, Lavandero B (2020) Intraguild predation is independent of landscape context and does not affect the temporal dynamics of aphids in cereal fields. J Pest Sci 93:235–249
Osawa N (2015) Sex-dependent effects of sibling cannibalism on life history traits of the ladybird beetle Harmonia axyridis. Biol J Lin Soc 76:349–360
Ovchinnikov AN, Belyakova NA, Ovchinnikova AA, Reznik SY (2019) Factors determining larval cannibalistic behavior in invasive and native populations of the multicolored Asian ladybird, Harmonia axyridis. Entomol Gen 38:243–254
Parolin P, Bresch C, Poncet C, Desneux N (2012) Functional characteristics of secondary plants for increased pest management. Int J Pest Manag 58:369–377
Pell JK, Baverstock J, Roy HE, Ware RL, Majerus MEN (2008) Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl 53:147–168
Pervez A, Gupta AK (2010) Role of surface chemicals in egg cannibalism and intraguild predation by neonates of two aphidophagous ladybirds, Propylea dissecta and Coccinella transversalis. J Appl Entomol 128:691–695
Perovic DJ, Gámez-Virués S, Landis DA et al (2018) Managing biological control services through multi-trophic trait interactions: review and guidelines for implementation at local and landscape scales. Biol Rev 93:306–321
Polis GA, Myers CA (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330
Polis GA, Holt RD (1992) Intraguild predation: the dynamics of complex trophic interactions. Trends Ecol Evol 7:151–154
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, https://www.R-project.org/.
Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N (2011) Ecology and management of the soybean aphid in North America. Ann Rev Entomol 56:375–399
Riahi E, Fathipour Y, Talebi AA, Mehrabadi M (2016) Pollen quality and predator viability: life table of Typhlodromus bagdasarjani on seven different plant pollens and two-spotted spider mite. Syst Appl Acarol 21:1399–1412
Rosenheim JA, Wilhoit LR, Armer CA (1993) Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population. Oecologia 96:439–449
Rosenheim JA, Kaya HK, Ehler LE, Marois JJ, Jaffee BA (1995) Intraguild predation among biological-control agents: theory and evidence. Biol Control 5:303–335
Sanchez-Hernandez CV, Desneux N, Bao-Fundora L, Ramirez-Romero R (2021) Alternative extraguild prey modifies focal extraguild prey consumption and parasitism but not intraguild predation intensity. Biol Control 153:104475
Sato S, Dixon AFG, Yasuda H (2003) Effect of emigration on cannibalism and intraguild predation in aphidophagous ladybirds. Ecol Entomol 28:628–633
Snyder WE, Evans EW (2006) Ecological effects of invasive arthropod generalist predators. Annu Rev Ecol Evol Syst 37:95–122
Snyder WE (2019) Give predators a complement: Conserving natural enemy biodiversity to improve biocontrol. Biol Control 135:73–82
Song BZ, Zhang J, Wiggins NL, Yao YC, Tan GB, Sang XS (2012) Intercropping with aromatic plants decrease herbivore abundance species richness, and shifts arthropod community trophic structure. Environ Entomol 4:872–879
Straub CS, Finke DL, Snyder WE (2008) Are the conservation of natural enemy biodiversity and biological control compatible goals? Biol Control 45:225–237
Sun H, Song Y (2019) Establishment of a wheat banker plant system for the parasitoid Aphidius gifuensis against Myzus persicae in greenhouse chili pepper. Appl Entomol Zool 54:1–9
Tan XL, Zhao J, Wang S, Zhang F (2015) Optimization and evaluation of microencapsulated artificial diet for mass rearing the predatory ladybird Propylea japonica (Coleoptera: Coccinellidae). Insect Sci 22:111–120
Tan XL, Hu NN, Zhang F, Ramirez-Romero R, Desneux N, Wang S, Ge F (2016) Mixed release of two parasitoids and a polyphagous ladybird as a potential strategy to control the tobacco whitefly Bemisia tabaci. Sci Rep 6:28245
Thomine E, Rusch A, Supplisson C, Monticelli LS, Amiens-Desneux E, Lavoir AV, Desneux N (2020) Highly diversified crop systems can promote the dispersal and foraging activity of the generalist predator Harmonia axyridis. Entomol Gen 40:133–145
van Veen FJF, Morris RJ, Godfray HCJ (2006) Apparent competition, quantitative food webs, and structure of phytophagous insect communities. Annu Rev Entomol 51:187–208
Vuong PT, Kim J, Song Y (2001) The seasonal occurrence of the two aphid species, Myzus persicae and Aphis gossypii, and their natural enemies on vegetable crops in Chinju, Korea. J Asia-Pacific Entomol 4:41–44
Wäckers FL, van Rijn PCJ (2012) Pick and mix: selecting flowering plants to meet the requirements of target biological control insects. In: Gurr G, Wratten S, Snyder W, Read D (eds) Biodiversity and insect pests. Wiley
Wang S, Tan XL, Xu HX, Zhang F (2012) Interspecific competition among three predacious ladybirds (Coleoptera: Coccinellidae). Scientia Agricultura Sinica 45:3980–3987
Wang YS, Yao FL, Soares MA, Basiri SE, Amiens-Desneux E, Campos MR, Lavoir AV, Desneux N (2020) Effects of four non-crop plants on life history traits of the lady beetle Harmonia axyridis. Entomol Gen 40:243–252
Ware RL, Majerus MEN (2008) Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl 53:169–188
Wolf S, Romeis J, Collatz J (2018) Utilization of plant-derived food sources from annual flower strips by the invasive harlequin ladybird Harmonia axyridis. Biol Control 122:118–126
Xiu CL, Pan HS, Ali A, Lu YH (2017) Extrafloral nectar of Hibiscus cannabinus promotes adult populations of Harmonia axyridis. Biocontrol Sci Tech 27:1009–1013
Xu Q, Wang S, Li S, Hatt S (2020) Conservation Biological Control in Organic Greenhouse Vegetables. In: Gao Y, Hokkanen H, Menzler-Hokkanen I (eds) Integrative Biological Control. Progress in Biological Control, vol 20. Springer, Cham
Yang NW, Zang LS, Wang S, Guo JY, Xu HX, Zhang F, Wan FH (2014) Biological pest management by predators and parasitoids in the greenhouse vegetables in China. Biol Control 68:92–102
Zhang SZ, Li JJ, Shan HW, Zhang F, Liu TX (2012) Influence of five aphid species on development and reproduction of Propylaea japonica (Coleoptera: Coccinellidae). Biol Control 62:135–139
Zhang ZQ, Zhou C, Xu YY, Huang XQ, Zhang LX, Mu W (2016) Effects of intercropping tea with aromatic plants on population dynamics of arthropods in Chinese tea plantations. J Pest Sci 90:227–237
Zhao J, Guo XJ, Tan XL, Desneux N, Zappala L, Zhang F, Wang S (2017) Using Calendula officinalis as a floral resource to enhance aphid and thrips suppression by the flower bug Orius sauteri (Hemiptera: Anthocoridae). Pest Manag Sci 73:515–520
Acknowledgements
The study was funded by the project 32072479 supported by the National Natural Science Foundation of China, the National Key Research and Development Program of China (2017YFD0201000; 2017YFD0200400), the Beijing Key Laboratory of Environment Friendly Management on Fruit Diseases and Pests in North China (BZ0432) and the Key Research and Development Program of Jiangxi Province (20202BBF62006).
Author information
Authors and Affiliations
Contributions
SW, CCJ, YL and XG designed the study; CX and JW performed the experiments; CX, HDJ and CCJ analyzed the data; YL, CX, CCJ and SW wrote the manuscript. All authors read and approved the manuscript for submission.
Corresponding authors
Ethics declarations
Conflict of interest
Authors declare they have no competing interests. SW is a Subject Editor of Journal of Pest Science and was not involved in the journal’s review of, or decision related to, this manuscript.
Additional information
Communicated by Antonio Biondi.
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
Liang, Y., Chen, X., Dai, H. et al. Flower provision reduces intraguild predation between predators and increases aphid biocontrol in tomato. J Pest Sci 95, 461–472 (2022). https://doi.org/10.1007/s10340-021-01396-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-021-01396-x