Differences in within-plant oviposition preferences and immature survival between Orius predators and the importance of spatial availability of prey

Abstract

Oviposition preferences of plant-feeding predators remain a complex topic, as such omnivores choose oviposition sites by assessing both plant characteristics and the quality and quantity of nearby animal food sources. Orius predators are omnivores that oviposit endophytically, thus plant characteristics play an important role in their oviposition choices. In this study, we assessed the oviposition and foraging preferences of O. laevigatus and O. majusculus on vegetative and flowering chrysanthemum plants, and assessed the survival of their offspring on differently aged tissues. Our results show a preference of O. laevigatus for young and tender chrysanthemum tissues, where the survival of the nymphs was longer on a plant diet. In contrast, O. majusculus selected older plant parts when laying its eggs, and nymphs did not survive long on any of the plant tissues offered. The foraging activity of Orius females for animal prey (Ephestia kuehniella eggs) did not reveal any specific pattern for either of the two predators. Furthermore, we tested the plasticity of the within-plant oviposition preferences of O. laevigatus, by offering sentinel prey (E. kuehniella eggs) on distinct plant parts. We found that more eggs were laid in older plant tissue when animal prey was offered lower on the plant. Overall, our findings show that oviposition choices of Orius predators are based on a dynamic interplay between plant characteristics, presence of animal and/or floral food sources among other factors, and that differences may well occur between closely related species based on the importance of plant resources in their diet.

Keywords

biological control / omnivore / Orius laevigatus / Orius majusculus / oviposition / preference-performance

References

[1] Armer, C.A. Wiedenmann, R.N. and Bush, D.R. (1998) Plant feeding site selection on soybean by the facultatively phytophagous predator Orius insidiosus. Entomologia Experimentalis et Applicata, 86, 109-118.

[2] Armer, C.A. Wiedenmann, R.N. and Irwin, M.E. (1999) Effects of soybean mosaic virus on the facultative phytophagous predator Orius insidiosus (Heteroptera: Anthocoridae). Environmental Entomology, 28, 1036-1043.

[3] Bekendam, A. Knapp, M. Suttie, R. van Leeuwen, C. de Fockert, S. Sikken, O. et al. (2023) Reduced pruning and supplementary feeding in sweet pepper have a positive effect on the population development of Orius laevigatus. IOBC/WPRS Bulletin, 167, 207-208.

[4] Castañe, C. and Zalom, F.G. (1994) Artificial oviposition substrate for rearing Orius insidiosus (Hemiptera: Anthocoridae). Biological Control, 4, 88-91.

[5] Chambers, R.J. Long, S. and Helyer, N.L. (1993) Effectiveness of Orius laevigatus (Hem.: Anthocoridae) for the control of Frankliniella occidentalis on cucumber and pepper in the UK. Biocontrol Science and Technology, 3, 295-307.

[6] Cocuzza, G.E. De Clercq, P. Van de Veire, M. De Cock, A. Degheele, D. and Vacante, V. (1997) Reproduction of Orius laevigatus and Orius albidipennis on pollen and Ephestia kuehniella eggs. Entomologia Experimentalis et Applicata, 82, 101-104.

[7] Coll, M. and Guershon, M. (2002) Omnivory in terrestrial arthropods: mixing plant and prey diets. Annual Review of Entomology, 47, 267-297.

[8] Coll, M. and Izraylevich, S. (1997) When predators also feed on plants: Effects of competition and plant quality on omnivore-prey population dynamics. Annals of the Entomological Society of America, 90, 155-161.

[9] Coll, M. Smith, L.A. and Ridgway, R.L. (1997) Effect of plants on the searching efficiency of a generalist predator: The importance of predator-prey spatial association. Entomologia Experimentalis et Applicata, 83, 1-10.

[10] Constant, B. Grenier, S. Febvay, G. and Bonnot, G. (1996) Host plant hardness in oviposition of Macrolophus caliginosus (Hemiptera: Miridae). Journal of Economic Entomology, 89, 1446-1452.

[11] De Puysseleyr, V. Höfte, M. and De Clercq, P. (2011) Ovipositing Orius laevigatus increase tomato resistance against Frankliniella occidentalis feeding by inducing the wound response. Arthropod-Plant Interactions, 5, 71-80.

[12] Evans, H.F. (1976) The effect of prey density and host plant characteristics on oviposition and fertility in Anthocoris confusus (Reuter). Ecological Entomology, 1, 157-161.

[13] Funderburk, J. Stavisky, J. and Olson, S. (2000) Predation of Frankliniella occidentalis (Thysanoptera: Thripidae) in field peppers by Orius insidiosus (Hemiptera: Anthocoridae). Environmental Entomology, 29, 376-382.

[14] Gripenberg, S. Mayhew, P.J. Parnell, M. and Roslin, T. (2010) A meta-analysis of preference-performance relationships in phytophagous insects. Ecology Letters, 13, 383-393.

[15] Groenteman, R. Guershon, M. and Coll, M. (2006) Effects of leaf nitrogen content on oviposition site selection, offspring performance, and intraspecific interactions in an omnivorous bug. Ecological Entomology, 31, 155-161.

[16] Hardin, J. and Hilbe, J. (2018) Generalized Linera Models and Extensions, 4th edn. Stata Press.

[17] Isenhour, D. and Yeargan, K. (1982) Oviposition sites of Orius insidiosus (Say) and Nabis spp. in soybean (Hemiptera: Anthocoridae and Nabidae). Journal of the Kansas Entomological Society, 55, 65-72.

[18] Jacobson, R.J. (1995) Egg laying sites of Orius majusculus, a thrips predator, on cucumber. In Thrips Biology and Management (eds. B.L. Parker, M. Skinner & T. Lewis), pp. 241-244. Springer, Boston.

[19] Jaenike, J. (1978) On optimal oviposition behavior in phytophagous insects. Theoretical Population Biology, 14, 350-356.

[20] Kielkiewicz, M. and van de Vrie, M. (1990) Within-leaf differences in nutritive value and defence mechanism in chrysanthemum to the two-spotted spider mite (Tetranychus urticae). Experimental & Applied Acarology, 10, 33-43.

[21] Lambret, P. Besnard, A. and Matushkina, N. (2015) Plant preference during oviposition in the endangered dragonfly Lestes macrostigma (Odonata: Zygoptera) and consequences for its conservation. Journal of Insect Conservation, 19, 741-752.

[22] Lattin, J.D. (1999) Bionomics of the Anthocoridae. Annual Review of Entomology, 44, 207-231.

[23] Lundgren, J.G. (2009) Relationships of Natural Enemies and Non-prey Foods. Springer, New York.

[24] Lundgren, J.G. (2011) Reproductive ecology of predaceous Heteroptera. Biological Control, 59, 37-52.

[25] Lundgren, J.G. and Fergen, J.K. (2006) The oviposition behavior of the predator Orius insidiosus: acceptability and preference for different plants. BioControl, 51, 217-227.

[26] Lundgren, J.G. Fergen, J.K. and Riedell, W.E. (2008) The influence of plant anatomy on oviposition and reproductive success of the omnivorous bug Orius insidiosus. Animal Behaviour, 75, 1495-1502.

[27] Lundgren, J.G. Wyckhuys, K.A.G. and Desneux, N. (2009) Population responses by Orius insidiosus to vegetational diversity. BioControl, 54, 135-142.

[28] Martínez, G. Soler, R. and Dicke, M. (2013) Behavioral ecology of oviposition-site selection in herbivorous true bugs. Advances in the Study of Behavior, 45, 175-207.

[29] Montserrat, M. Albajes, R. and Castañé, C. (2000) Functional response of four Heteropteran predators preying on greenhouse whitefly (Homoptera: Aleyrodidae) and western flower thrips (Thysanoptera: Thripidae). Environmental Entomology, 29, 1075-1082.

[30] Mouratidis, A. Van Der Heide, H. Le Hesran, S. Dicke, M. and Messelink, G.J. (2023a) Complementarity among Orius species enhances pest control of foliar and flower pests. IOBC/WPRS Bulletin, 167, 128-129.

[31] Mouratidis, A. Hemming, J. Messelink, G.J. and van Marrewijk, B. (2023b) Automated identification and counting of predated Ephestia kuehniella (Zeller) eggs using deep learning image analysis. Biological Control, 186, 105345.

[32] Mouratidis, A. de Lima, A.P. Dicke, M. and Messelink, G.J. (2022) Predator-prey interactions and life history of Orius laevigatus and O. majusculus feeding on flower and leaf-inhabiting thrips. Biological Control, 172, 104954.

[33] Oveja, M.F. Arnó, J. and Gabarra, R. (2012) Effect of supplemental food on the fitness of four omnivorous predator species. IOBC/WPRS Bulletin, 80, 97-101.

[34] Pascua, M.S. Rocca, M. De Clercq, P. and Greco, N.M. (2019) Host plant use for oviposition by the insidious flower bug (Hemiptera: Anthocoridae). Journal of Economic Entomology, 112, 219-225.

[35] Péricart, J. (1972) Hémiptères: Anthocoridae, Cimicidae et Microphysidae: de l'ouest-paléarctique. Paris: Masson et Cié.

[36] Perring, T.M. Farrar, C.A. and Royalty, R.N. (1987) Intraplant distribution and sampling of spider mites (Acari: Tetranychidae) on cantaloupe. Journal of Economic Entomology, 80, 96-101.

[37] Pijnakker, J. Vangansbeke, D. Duarte, M. Moerkens, R. and Wäckers, F.L. (2020) Predators and parasitoids-in-first: from inundative releases to preventative biological control in greenhouse crops. Frontiers in Sustainable Food Systems, 4, 595630.

[38] Pumariño, L. and Alomar, O. (2012) The role of omnivory in the conservation of predators: Orius majusculus (Heteroptera: Anthocoridae) on sweet alyssum. Biological Control, 62, 24-28.

[39] Pumariño, L. Alomar, O. and Lundgren, J.G. (2012) Effects of floral and extrafloral resource diversity on the fitness of an omnivorous bug, Orius insidiosus. Entomologia Experimentalis et Applicata, 145, 181-190.

[40] Pyke, G.H. Pulliam, H.R. and Charnov, E.L. (1977) Optimal foraging: a selective review of theory and tests. The Quarterly Review of Biology, 51, 3-47.

[41] R. Core Team (2021) R: A language and environment for statistical computing, R Foundation for Statistical Computing. https://www.r-project.org/.

[42] Rademacher, W. (2000) Growth retardants: Effects on gibberellin biosynthesis and other metabolic pathways. Annual Review of Plant Physiology and Plant Molecular Biology, 51, 501-531.

[43] Ramakers, P.M.J. and O'Neill, T.M. (1999) Cucurbits. In Integrated Pest and Disease Maangement in Greehouse Crops (eds. M. Gullino, R. Albajes & P. Nicot), pp. 435-453. Kluwer Academic Publishers, Boston.

[44] Richards, P.C. and Schmidt, J.M. (1996) The suitability of some natural and artificial substrates as oviposition sites for the insidious flower bug, Orius insidiosus. Entomologia Experimentalis et Applicata, 80, 325-333.

[45] Rutledge, C.E. and O'Neil, R.J. (2005) Orius insidiosus (Say) as a predator of the soybean aphid, Aphis glycines Matsumura. Biological Control, 33, 56-64.

[46] Sánchez, J.A. Gillespie, D.R. and McGregor, R.R. (2004) Plant preference in relation to life history traits in the zoophytophagous predator Dicyphus hesperus. Entomologia Experimentalis et Applicata, 112, 7-19.

[47] Scheirs, J. and De Bruyn, L. (2002) Integrating optimal foraging and optimal oviposition theory in plant-insect research. Oikos, 96, 187-191.

[48] Schellhorn, N.A. and Andow, D.A. (1999) Cannibalism and interspecific predation: role of oviposition behavior. Ecological Applications, 9, 418-428.

[49] Schuldiner-Harpaz, T. and Coll, M. (2022) Considering the geographic diversity of natural enemy traits in biological control: a quantitative approach using Orius predators as an example. Diversity, 14, 963.

[50] Seagraves, M.P. (2009) Lady beetle oviposition behavior in response to the trophic environment. Biological Control, 51, 313-322.

[51] Seagraves, M.P. and Lundgren, J.G. (2010) Oviposition response by Orius insidiosus (Hemiptera: Anthocoridae) to plant quality and prey availability. Biological Control, 55, 174-177.

[52] Shapiro, J.P. and Ferkovich, S.M. (2006) Oviposition and isolation of viable eggs from Orius insidiosus in a parafilm and water substrate: Comparison with green beans and use in enzyme-linked immunosorbent assay. Annals of the Entomological Society of America, 99, 586-591.

[53] Stavrinides, M.C. and Skirvin, D.J. (2003) The effect of chrysanthemum leaf trichome density and prey spatial distribution on predation of Tetranychus urticae (Acari: Tetranychidae) by Phytoseiulus persimilis (Acari: Phytoseiidae). Bulletin of Entomological Research, 93, 343-350.

[54] Tawfik, M. and Ata, A. (1973) The life-history of Orius albidipennis (Reut.) (Hemiptera-Heteroptera:Anthocoridae). Bulletin de la Societe Entomologique D'egypte, 57, 117-126.

[55] Tommasini, M.G. Van Lenteren, J.C. and Burgio, G. (2004) Biological traits and predation capacity of four Orius species on two prey species. Bulletin of Insectology, 57, 79-93.

[56] Vacante, V. Cocuzza, G.E. De Clercq, P. Van De Veire, M. and Tirry, L. (1997) Development and survival of Orius albidipennis and O. laevigatus (Het.: Anthocoridae) on various diets. Entomophaga, 42, 493-498.

[57] van den Meiracker, R.A.F. and Ramakers, P.M.J. (1991) Biological control of the western flower thrips Frankliniella occidentalis in sweet pepper, with the anthocorid predator Orius insidiosus. Mededelingen Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen Universiteit Gent, 56, 241-249.

[58] van den Meiracker, R.A.F. and Sabelis, M.W. (1993) Oviposition sites of Orius insidiosus in sweet pepper. IOBC/WPRS Bulletin, 16, 109-112.

[59] van Schelt, J. Hoogerbrugge, H. van Houten, Y.M. and Bolckmans, K. (2002) Biological control and survival of Echinothrips americanus in pepper. IOBC/WPRS Bulletin, 25, 285-288.

[60] Venzon, M. Janssen, A. and Sabelis, M.W. (2002) Prey preference and reproductive success of the generalist predator Orius laevigatus. Oikos, 97, 116-124.

[61] Waite, M.O. Scott-Dupree, C.D. Brownbridge, M. Buitenhuis, R. and Murphy, G. (2014) Evaluation of seven plant species/cultivars for their suitability as banker plants for Orius insidiosus (Say). BioControl, 59, 79-87.

[62] Walzer, A. Moder, K. and Schausberger, P. (2009) Spatiotemporal within-plant distribution of the spider mite Tetranychus urticae and associated specialist and generalist predators. Bulletin of Entomological Research, 99, 457-466.

[63] Yokoyama, V.Y. (1978) Relation of seasonal changes in extrafloral nectar and foliar protein and arthropod populations in cotton. Environmental Entomology, 7, 799-802.

[64] Yu, C. Huang, J. Ren, X. Fernández-Grandon, G.M. Li, X. Hafeez, M. et al. (2021) The predatory bug Orius strigicollis shows a preference for egg-laying sites based on plant topography. PeerJ, 9, e11818.

[65] Zeng, F. and Cohen, A.C. (2000) Demonstration of amylase from the zoophytophagous anthocorid Orius insidiosus. Archives of Insect Biochemistry and Physiology, 44, 136-139.

[66] Zhang, L. Qin, Z. Liu, P. Yin, Y. Felton, G.W. and Shi, W. (2021) Influence of plant physical and anatomical characteristics on the ovipositional preference of Orius sauteri (Hemiptera: Anthocoridae). Insects, 12, 326.

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