Abstract
This work puts forward a dynamical population model to qualitatively reproduce the phenomena of apparent competition and apparent mutualism found in an experiment with two arthropods being attacked by a predator in a context of pest biological control in greenhouse crops. The two agricultural pests consist of one species of thrips (Frankliniella occidentalis (Pergande 1895)) and one species of whiteflies (Trialeurodes vaporariorum Westwood, 1956), and the shared predator is a predatory mite (Amblyseius swirskii Athias-Herriot, 1962). The predatory mite is the biocontrol agent employed in order to achieve the biological control. The proposed model successfully reproduces this density mediated indirect interactions between pests when their carrying capacities are increased. Moreover, the pests’ final population levels may depend on their initial densities and those of their predator. With these results, the proposed model may have the potential to assess whether these indirect pest interactions disrupt or enhance biological control. Additionally, it can also be used as an ancillary tool to theoretically assess the effects of pest biocontrol strategies in the referred experimental setup.



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14 June 2021
A Correction to this paper has been published: https://doi.org/10.1007/s13744-021-00879-x
References
Abrams PA, Roth J (1994) The responses of unstable food chains to enrichment. Evol Ecol 8(2):150–171. https://doi.org/10.1007/BF01238247
Abrams PA, Holt RD, Roth JD (1998) Apparent competition or apparent mutualism? Shared predation when populations cycle. Ecology 79(1):201–212. https://doi.org/10.2307/176875
Bompard A, Jaworski CC, Bearez P, Desneux N (2013) Sharing a predator: can an invasive alien pest affect the predation on a local pest? Popul Ecol 55(3):33–440. https://doi.org/10.1007/s10144-013-0371-8
Case TJ (1999) An illustrated guide to theoretical ecology. Oxford University Press, New York
Chailleux A, Mohl EK, Teixeira Alves M, Messelink GJ, Desneux N (2014) Natural enemy-mediated indirect interactions among prey species: potential for enhancing biocontrol services in agroecosystems. Pest Manag Sci 70(12):1769–1779. https://doi.org/10.1002/ps.3916
Croft BA, Blackwood JS, McMurtry JA (2004) Classifying life-style types of phytoseiid mites: diagnostic traits. Exp Appl Acarol 33(4):247–260. https://doi.org/10.1023/B:APPA.0000038622.26584.82
Desneux N, O'Neil RJ (2008) Potential of an alternative prey to disrupt predation of the generalist predator, Orius insidiosus, on the pest aphid, Aphis glycines, via short-term indirect interactions. Bull Entomol Res 98(6):631–639. https://doi.org/10.1017/S0007485308006238
Edwards AM, Yool A (2000) The role of higher predation in plankton population models. J Plankton Res 22(6):1085–1112. https://doi.org/10.1093/plankt/22.6.1085
Enkegaard A, Brødsgaard HF (2006) Biocontrol in protected crops: is lack of biodiversity a limiting factor? In: Eilenberg J, Hokkanen HM (eds) An ecological and societal approach to biological control, vol 2. Dordrecht: Springer, pp 91–112
Ermentrout B (2002) Simulating, analyzing, and animating dynamical systems: a guide to XPPAUT for researchers and students, vol 14. Society for Industrial and Applied Mathematics, Philadelphia
Faria LDB, Costa MIS (2009) The interplay between predator's prey preference and environmental heterogeneity in food web long-term stability. J Theor Biol 258(3):339–343. https://doi.org/10.1016/j.jtbi.2008.06.010
Gao Y, Reitz SR (2017) Emerging themes in our understanding of species displacements. Annu Rev Entomol 62:165–183. https://doi.org/10.1146/annurev-ento-031616-035425
Giovanelli A, Vieira MV, Silva CLPAC (2003) Apparent competition through facilitation between Melanoides tuberculata and Biomphalaria glabrata and the control of schistosomiasis. Mem Inst Oswaldo Cruz 98(3):429–431. https://doi.org/10.1590/S0074-02762003000300025
Han P, Becker C, Le Bot J, Larbat R, Lavoir AV, Desneux N (2020) Plant nutrient supply alters the magnitude of indirect interactions between insect herbivores: from foliar chemistry to community dynamics. J Ecol 2020:1–14. https://doi.org/10.1111/1365-2745.13342
Hardin G (1960) The competitive exclusion principle. Science 131(3409):1292–1297. https://doi.org/10.1126/science.131.3409.1292
Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12(2):197–229. https://doi.org/10.1016/0040-5809(77)90042-9
Holt RD (1997) Community modules. In: Brown VK (ed) Gange AC. Multitrophic interactions in terrestrial systems, Blackwell Science Oxford, pp 333–339
Jaworski CC, Chailleux A, Bearez P, Desneux N (2015) Apparent competition between major pests reduces pest population densities on tomato crop, but not yield loss. J Pest Sci 88(4):793–803. https://doi.org/10.1007/s10340-015-0698-3
Leman A, Messelink GJ (2015) Supplemental food that supports both predator and pest: a risk for biological control? Exp Appl Acarol 65(4):511–524. https://doi.org/10.1007/s10493-014-9859-y
Lima ID, Olson DB, Doney SC (2002) Intrinsic dynamics and stability properties of size-structured pelagic ecosystem models. J Plankton Res 24(6):533–556. https://doi.org/10.1093/plankt/24.6.533
Messelink GJ, van Maanen R, van Steenpaal SE, Janssen A (2008) Biological control of thrips and whiteflies by a shared predator: two pests are better than one. Biol Control 44(3):372–379. https://doi.org/10.1016/j.biocontrol.2007.10.017
Messelink GJ (2012) Positive and negative indirect interactions between prey sharing a predator population (Chapter 4). In: Generalist predators, food web complexities and biological pest control in greenhouse crops. PhD thesis, University of Amsterdam, The Netherlands
Messelink GJ, Janssen A (2014) Increased control of thrips and aphids in greenhouses with two species of generalist predatory bugs involved in intraguild predation. Biol Control 79:1–7. https://doi.org/10.1016/j.biocontrol.2014.07.009
Rasmy AH, Abou-El-Ella GM, Hussein HE (2004) Cannibalism and interspecific predation of the phytoseiid mite, Amblyseius swirskii. J Pest Sci 77(1):23–25. https://doi.org/10.1007/s10340-003-0022-5
Acknowledgments
The authors acknowledge the helpful comments and suggestions made by the reviewers on an earlier version of this work. Lucas dos Anjos was supported by a fellowship from the Institutional Training Program (PCI) from the Ministry of Science, Technology, Innovation and Communication (MCTIC) (Grant Number: 301327/2020-3).
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All authors contributed to the study conception and design. MISC did the conceptualization, the creation of the studied model, and the preparation of the manuscript. LA performed the analyses, discussed the results, and reviewed the original text.
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Costa, M.I.S., Anjos, L. The Occurrence of Apparent Competition and Apparent Mutualism in a Modeled Greenhouse System with Two Non-competing Pests and a Shared Biocontrol Agent. Neotrop Entomol 49, 874–881 (2020). https://doi.org/10.1007/s13744-020-00820-8
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DOI: https://doi.org/10.1007/s13744-020-00820-8