Abstract
Omnivorous insects make foraging decisions between plant and prey resources depending on their accessibility, availability, and nutritional value. This shapes the stability and complexity of food webs, but also pest control services in agroecosystems. The mirid bug Lygus pratensis is a common cotton pest in China, but it also feeds on a variety of prey species. However, little is known about how different types of available resources affect its fitness and foraging behaviour. In laboratory experiments, we measured the fitness (survival, longevity and fecundity) of L. pratensis fed with bean pod only, bean and Aphis gossypii nymphs, or bean and Helicoverpa armigera eggs, and we also conducted focal observations of its foraging behaviour when provided the latter two. Adding H. armigera to its diet increased its fitness (both survival and fecundity), while adding A. gossypii was marginally detrimental. The different diets did not affect the time spent walking (searching for food resources) or preying, but significantly affected the time spent sapping bean tissue depending on L. pratensis life stage. Nymphs spent more time sapping plant when provided with H. armigera than A. gossypii (possibly through higher efficiency of handling prey). In addition, adults spent less time sapping plant than did nymphs (possibly through good efficiency of handling A. gossypii mobile prey and due to higher protein requirements). This special case of life-history omnivory highlights the complexity of natural food webs, where a major crop pest at the juvenile stage may become a biological control agent at the adult stage.
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References
Alvarado, P., Baltà, O., & Alomar, O. (1997). Efficiency of four heteroptera as predators of Aphis gossypii and Macrosiphum euphorbiae (Hom.: Aphididae). Entomophaga, 42, 215–226. https://doi.org/10.1007/BF02769899.
Barrett, E. L., Hunt, J., Moore, A. J., & Moore, P. J. (2009). Separate and combined effects of nutrition during juvenile and sexual development on female life-history trajectories: The thrifty phenotype in a cockroach. Proceedings of the Royal Society b: Biological Sciences, 276, 3257–3264. https://doi.org/10.1098/rspb.2009.0725
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B, 57, 289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
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. Journal of Pest Science, 86, 533–541. https://doi.org/10.1007/s10340-013-0498-6
Coll, M., & Guershon, M. (2002). Omnivory in terrestrial arthropods: Mixing plant and prey diets. Annual Review of Entomology, 47, 267–297. https://doi.org/10.1146/annurev.ento.47.091201.145209
Desneux, N., & O’Neil, R. J. (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. Bulletin of Entomological Research, 98, 631–639. https://doi.org/10.1017/S0007485308006238
Desneux, N., Barta, R. J., Hoelmer, K. A., Hopper, K. R., & Heimpel, G. E. (2009). Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia, 160, 387–398. https://doi.org/10.1007/s00442-009-1289-x
Eubanks, M. D., & Denno, R. F. (2000). Health food versus fast food: The effects of prey quality and mobility on prey selection by a generalist predator and indirect interactions among prey species. Ecological Entomology, 25, 140–146. https://doi.org/10.1046/j.1365-2311.2000.00243.x
Han, P., Dong, Y., Lavoir, A. V., Adamowicz, S., Bearez, P., Wajnberg, E., & Desneux, N. (2015a). Effect of plant nitrogen and water status on the foraging behavior and fitness of an omnivorous arthropod. Ecology and Evolution, 5, 5468–5477. https://doi.org/10.1002/ece3.1788
Han, P., Bearez, P., Adamowicz, S., Adamowicz, S., Lavoir, A.-V., Amiens-Desneux, E., & Desneux, N. (2015b). Nitrogen and water limitations in tomato plants trigger negative bottom-up effects on the omnivorous predator Macrolophus pygmaeus. Journal of Pest Science, 88, 685–691. https://doi.org/10.1007/s10340-015-0662-2
Han, Z., Tan, X., Wang, Y., Xu, Q., Zhang, Y., Harwood, J. D., & Chen, J. (2019). Effects of simulated climate warming on the population dynamics of Sitobion avenae (Fabricius) and its parasitoids in wheat fields. Pest Management Science, 75, 3252–3259. https://doi.org/10.1002/ps.5447
Han, P., Becker, C., Le Bot, J., Larbat, R., Lavoir, A.-V., & Desneux, N. (2020). Plant nutrient supply alters the magnitude of indirect interactions between insect herbivores: From foliar chemistry to community dynamics. Journal of Ecology, 108, 1497–1510. https://doi.org/10.1111/1365-2745.13342
Hartig, F. (2022). DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression. Models. R package version 0.4.5. https://CRAN.R-project.org/package=DHARMa.
Heil, M., & Ton, J. (2008). Long-distance signalling in plant defence. Trends in Plant Science, 13(6), 264–272. https://doi.org/10.1016/j.tplants.2008.03.005
Huang, F. L. (2020). MANOVA: A Procedure Whose Time Has Passed? Gifted Child Quarterly, 64, 56–60. https://doi.org/10.1177/0016986219887200
Jaworski, C. C., Bompard, A., Genies, L., Amiens-Desneux, E., & Desneux, N. (2013).Preference and Prey Switching in a Generalist Predator Attacking Local and Invasive Alien Pests. PLoS ONE 8, e82231. https://doi.org/10.1371/journal.pone.0082231.
Jaworski, C. C., Chailleux, A., Bearez, P., & Desneux, N. (2015). Apparent competition between major pests reduces pest population densities on tomato crop, but not yield loss. Journal of Pest Science, 88, 793–803. https://link.springer.com/article/10.1007/s10340-015-0698-3.
Kaplan, I., & Thaler, J. S. (2011). Do plant defenses enhance or diminish prey suppression by omnivorous Heteroptera? Biological Control, 59, 53–60. https://doi.org/10.1016/j.biocontrol.2010.12.005
Kassambara, A., Kosinski, M., & Biecek, P. (2021). survminer: Drawing Survival Curves using 'ggplot2'. R package version 0.4.9. https://CRAN.R-project.org/package=survminer.
Kratina, P., Lecraw, R. M., Ingram, T., & Anholt, B. R. (2012). Stability and persistence of food webs with omnivory: Is there a general pattern? Ecosphere, 3, 1–18. https://doi.org/10.1890/ES12-00121.1
Lenth, R. V. (2022). emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.7.3. https://CRAN.R-project.org/package=emmeans.
Li, W., Wang, L., Jaworski, C. C., Yang, F., Liu, B., Jiang, Y., Lu, Y., Wu, K., & Desneux, N. (2020). The outbreaks of nontarget mirid bugs promote arthropod pest suppression in Bt cotton agroecosystems. Plant Biotechnology Journal, 18, 322–324. https://doi.org/10.1111/pbi.13233
Liang, H. J., Li, Y., Cun, C. Y., Feng, L. K., Wang, P. L., & Lu, Y. H. (2013). The predation of Lygus pratensis to Aphis gossypii Glover. Journal of Environmental Entomology, 35, 317–321.
Lu, Y. H., Qiu, F., Feng, H. Q., Li, H. B., Yang, Z. C., Wyckhuys, K. A. G., & Wu, K. M. (2008). Species composition and seasonal abundance of pestiferous plant bugs (Hemiptera: Miridae) on Bt cotton in China. Crop Protection, 27, 465–472. https://doi.org/10.1016/j.cropro.2007.07.017
Lu, Y., Wu, K., Jiang, Y., Xia, B., Li, P., Feng, H., Wyckhuys, K. A. G., & Guo, Y. (2010). Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science, 328, 1151–1154. https://doi.org/10.1126/science.1187881
Lu, Y., & Wu, K. (2011). Mirid bugs in China: Pest status and management strategies. Outlooks on Pest Management, 22, 248–252. https://doi.org/10.1564/22dec02
Lu, Y., Wu, K., Jiang, Y., Guo, Y., & Desneux, N. (2012). Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature, 487, 362–365. https://doi.org/10.1038/nature11153
Lu, Z. Z., Hou, X. J., Liu, X. X., Yang, C. H., Downes, S., Parry, H., & Zalucki, M. P. (2022). Quo vadis Bt cotton: A dead-end trap crop in the post Bt era in China? Entomologia Generalis, 42(4), 649–654. https://doi.org/10.1127/entomologia/2021/1355
Lumbierres, B., Madeira, F., Roca, M., & Pons, X. (2021). Effects of temperature and diet on the development and reproduction of the ladybird Oenopia conglobata. Entomologia Generalis, 41, 197–208. https://doi.org/10.1127/entomologia/2020/1077
Lundgren, J. G., Wyckhuys, K. A. G., & Desneux, N. (2009). Population responses by Orius insidiosus to vegetational diversity. BioControl, 54, 135–142. https://doi.org/10.1007/s10526-008-9165-x
Luo, C., Chai, R., Liu, X., Dong, Y,; Desneux, N., Feng, Y., & Hu, Z. (2022). The facultative symbiont Regiella insecticola modulates non-consumptive and consumptive effects of Harmonia axyridis on host aphids. Entomologia Generalis, 42(5), 733–741. https://doi.org/10.1127/entomologia/2022/1368.
Maselou, D. A., Perdikis, D. C., & Fantinou, A. A. (2018). Prey-mediated changes in the selectivity of the predator Macrolophus pygmaeus (Heteroptera: Miridae). Entomological Science, 21, 260–269. https://doi.org/10.1111/ens.12305
Pappas, M. L., Tavlaki, G., Triantafyllou, A., & Broufas, G. (2018). Omnivore-herbivore interactions: Thrips and whiteflies compete via the shared host plant. Scientific Reports, 8, 3996. https://doi.org/10.1038/s41598-018-22353-2
Pérez-Hedo, M., Alonso-Valiente, M., Vacas, S., Gallego, C., Rambla, J. L., Navarro-Llopis, V., Granell, A., & Urbaneja, A. (2021). Eliciting tomato plant defenses by exposure to herbivore induced plant volatiles. Entomologia Generalis, 41, 209–218. https://doi.org/10.1127/entomologia/2021/1196
R Core Team (2022). R: a language and environment for statistical computing. R foundation for statistical computing. https://www.R-project.org/.
Ren, X. Y., Huang, J., Li, X. W., Zhang, J. M., Zhang, Z. J., Chen, L. M., Hafeez, M., Zhou, S. X., & Lu, Y. B. (2022). Frozen lepidopteran larvae as promising alternative factitious prey for rearing of Orius species. Entomologia Generalis, 42(6), 959–966. https://doi.org/10.1127/entomologia/2022/1579
Rosenheim, J. A., Goeriz, R. E., & Thacher, E. F. (2004). Omnivore or herbivore? Field observations of foraging by Lygus hesperus (Hemiptera: Miridae). Environmental Entomology, 33, 1362–1370. https://doi.org/10.1603/0046-225X-33.5.1362
Schone, H. (2014). Spatial orientation. Princeton University Press.
Siddique, A. B., & Chapman, R. B. (1987). Effect of prey type and quantity on the reproduction, development, and survival of Pacific damsel bug, Nabis kinbergii Reuter (Hemiptera: Nabidae). New Zealand Journal of Zoology, 14, 343–349. https://doi.org/10.1080/03014223.1987.10423004
Sinia, A., Roitberg, B., McGregor, R. R., & Gillespie, D. R. (2004). Prey feeding increases water stress in the omnivorous predator Dicyphus hesperus. Entomologia Experimentalis Et Applicata, 110, 243–248. https://doi.org/10.1111/j.0013-8703.2004.00145.x
Therneau, T. (2022). A Package for Survival Analysis in R. R package version 3.3–1. https://CRAN.R-project.org/package=survival.
Thomine, E., Jeavons, E., Rusch, A., Bearez, P., & Desneux, N. (2020). Effect of crop diversity on predation activity and population dynamics of the mirid predator Nesidiocoris tenuis. Journal of Pest Science, 93, 1255–1265. https://doi.org/10.1007/s10340-020-01222-w
Thompson, R. M., Hemberg, M., Starzomski, B. M., & Shurin, J. B. (2007). Trophic levels and trophic tangles: The prevalence of omnivory in real food webs. Ecology, 88, 612–617. https://doi.org/10.1890/05-1454
Urbaneja, A., Tapia, G., & Stansly, P. (2005). Influence of host plant and prey availability on developmental time and survivorship of Nesidiocoris tenius (Heteroptera: Miridae). Biocontrol Science and Technology, 15, 513–518. https://doi.org/10.1080/09583150500088777
Vankosky, M. A., & VanLaerhoven, S. L. (2015). Plant and prey quality interact to influence the foraging behaviour of an omnivorous insect, Dicyphus hesperus. Animal Behaviour, 108, 109–116. https://doi.org/10.1016/j.anbehav.2015.07.019
Venables, W. N., & Ripley, B. D. (2002). Modern Applied Statistics with S. Fourth Edition. Springer. ISBN 0–387–95457–0. https://www.stats.ox.ac.uk/pub/MASS4/.
Wang, J. R. (1996). The management of mirid bugs in early spring. Xinjiang Agriculture, 4, 163–164.
Woodward, G., & Hildrew, A. G. (2002). Body-size determinants of niche overlap and intraguild predation within a complex food web. Journal of Animal Ecology, 71, 1063–1074. https://doi.org/10.1046/j.1365-2656.2002.00669.x
Wu, K., Lin, K., Miao, J., & Zhang, Y. (2005). Field abundances of insect predators and insect pests on δ-endotoxin-producing transgenic cotton in Northern China. In: Hoddle MS, editor. Second International Symposium on Biological Control of Arthropods. Riverside, California: University of California. pp. 362–368.
Yang, X., Jin, B. F., Meng, J. W., & Zhu, B. (2004). Outbreaks of Lygus pratensis in southern Xinjiang in 2003. China Cotton, 31, 43.
Yao, Y. S., Han, P., Niu, C. Y., Dong, Y. C., Gao, X. W., Cui, J. J., & Desneux, N. (2016). Transgenic Bt cotton does not disrupt the top-down forces regulating the cotton aphid in central China. PLoS ONE, 11, e0166771. https://doi.org/10.1371/journal.pone.0166771.
Zhang, Q., Liu, Y. Q., Wyckhuys, K. A. G., Liang, H. S., Desneux, N. , & Lu, Y. H. (2021). Lethal and sublethal effects of chlorantraniliprole on Helicoverpa armigera adults enhance the potential for use in "attract-and”-kill" control strategies. Entomologia Generalis 41(1), 111–120. https://doi.org/10.1127/entomologia/2020/1104
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We thank undergraduate students for their assistance during the experiments.
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This work was supported by a grant to Pei-ling Wang, Ruo-han Ma, Jia-min Gu and Xue-ling Li from The National Key Research and Development Program of China (2017YFD0201904), and a grant to Ruo-han Ma and Zhen-xuan Xue from The Xinjiang Uygur Autonomous Region Postgraduate Research and Innovation Project (XJ2019G125).
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Pei-ling Wang and Ruo-han Ma secured the funding; Pei-ling Wang, Peng Han and Nicolas Desneux designed the study; Ruo-han Ma, Jia-min Gu, Zheng-xuan Xue and Xue-ling Li acquired the data; Ruo-han Ma and Coline C. Jaworski performed the data analysis; Ruo-han Ma, Coline C. Jaworski, Peng Han and Nicolas Desneux wrote the manuscript. All authors agreed to the publication.
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Ma, Rh., Gu, Jm., Jaworski, C.C. et al. Life stage affects prey use with fitness consequences in a zoophytophagous mirid bug. Phytoparasitica 51, 503–511 (2023). https://doi.org/10.1007/s12600-023-01061-2
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DOI: https://doi.org/10.1007/s12600-023-01061-2