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Genetic improvement of Orius laevigatus for better fitness feeding on pollen

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Abstract

In many protected crops, augmentative biological control heavily relies on generalist predators, which continuous presence on the crop allows an early response to pest immigration and outbreaks. Persistence is possible by their ability to feed on alternative food, such as pollen, plant-provided or artificially supplemented. However, fitness is decreased when feeding on alternative foods, hindering performance. We present a new approach to face this challenge: genetic improvement for better fitness feeding on suboptimal food. Orius laevigatus is one of the main biological control agents used in greenhouse vegetable crops. A breeding process was carried out on the basis of a broad intraspecific variability exploration for 10-day fecundity feeding on pollen (14.2–37.9 eggs/female for 30 wild and commercial populations). Life history traits were finally compared between our two selected strains and three commercial, wild and acclimated-to-pollen unselected populations, both on rich (Ephestia eggs) and suboptimal (dry honeybee pollen) diets. Selected lines showed considerably improved values for longevity (1.5-fold), early (1.3-fold) and lifetime fecundity (1.9-fold), nymphal survival (3.5-fold), intrinsic rate of natural increase (rm) (7.3-fold) and net reproductive rate (R0) (6.7-fold) as compared to reference unselected strains when they were fed on pollen, although still lower than on the optimal diet. Selection feeding on plant material resulted in no trade-offs when feeding on the factitious prey. This improvement was due to genetic gain rather than to phenotypic plasticity to tolerate nutritious restriction. Finally, some potential contributions of these improved lines not only for augmentative biocontrol but also for artificial rearing are provided.

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The datasets generated and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Aragón-Sánchez M, Román-Fernández LR, Martínez-García H et al (2018) Rate of consumption, biological parameters, and population growth capacity of Orius laevigatus fed on Spodoptera exigua. Biocontrol 63:785–794

    Google Scholar 

  • Arijs Y, De Clercq P (2004) Liver-based artificial diets for the production of Orius laevigatus. Biocontrol 49:505–516

    Google Scholar 

  • Balanza V, Mendoza JE, Bielza P (2019) Variation in susceptibility and selection for resistance to imidacloprid and thiamethoxam in Mediterranean populations of Orius laevigatus. Entomol Exp Appl 167:626–635

    CAS  Google Scholar 

  • Bernardo AMG, de Oliveira CM, Oliveira RA, Vacacela HE, Venzon M, Pallini A, Janssen A (2017) Performance of Orius insidiosus on alternative foods. J Appl Entomol 141:702–707

    CAS  Google Scholar 

  • Bielza P, Balanza V, Cifuentes D, Mendoza JE (2020) Challenges facing arthropod biological control: Identifying traits for genetic improvement of predators in protected crops. Pest Manag Sci. https://doi.org/10.1002/ps.5857

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Bonte M, De Clercq P (2008) Developmental and reproductive fitness of Orius laevigatus (Hemiptera: Anthocoridae) reared on factitious and artificial diets. J Econ Entomol 101:1127–1133

    CAS  PubMed  Google Scholar 

  • Bonte M, De Clercq P (2010) Influence of diet on the predation rate of Orius laevigatus on Frankliniella occidentalis. Biocontrol 55:625–629

    Google Scholar 

  • Bonte M, De Clercq P (2011) Influence of predator density, diet and living substrate on developmental fitness of Orius laevigatus. J Appl Entomol 135:343–350

    Google Scholar 

  • Bonte J, Vangansbeke D, Maes S, Bonte M, Conlong D, De Clercq P (2012) Moisture source and diet affect development and reproduction of Orius thripoborus and Orius naivashae, two predatory anthocorids from Southern Africa. J Insect Sci 12:1

    PubMed  PubMed Central  Google Scholar 

  • Brenard N, Sluydts V, Christianen E, Bosmans L, De Bruyn L, Moerkens R, Leirs H (2019) Biweekly supplementation with Artemia spp. cysts allows efficient population establishment by Macrolophus pygmaeus in sweet pepper. Entomol Experi Appli 167:406–414

    CAS  Google Scholar 

  • Calvo FJ, Bolckmans K, Belda JE (2012a) Biological control based IPM in sweet pepper greenhouses using Amblyseius swirskii (Acari: Phytoseiidae). Biocontrol Sci Technol 22:1398–1416

    Google Scholar 

  • Calvo FJ, Bolckmans K, Belda JE (2012b) Release rate for a pre-plant application of Nesidiocoris tenuis for Bemisia tabaci control in tomato. Biocontrol 57:809–817

    Google Scholar 

  • Calixto A, Bueno V, Montes F, Silva A, van Lenteren J (2013) Effect of different diets on reproduction, longevity and predation capacity of Orius insidiosus (Say) (Hemiptera: Anthocoridae). Biocontrol Sci Techn 23:1245–1255

    Google Scholar 

  • Castañé C, Bueno VH, Carvalho LM, van Lenteren JC (2014) Effects of founder population size on the performance of Orius laevigatus (Hemiptera: Anthocoridae) colonies. Biol Control 69:107–112

    Google Scholar 

  • Cocuzza GE, De Clercq P, van de Veire M, de Cock A, Degheele D, Vacante V (1997) Reproduction of Orius laevigatus and Orius albidipennis on pollen and Ephestia kuehniella eggs. Entomol Exp Appl 82(1):101–104

    Google Scholar 

  • Davis RB, Javoiš J, Kaasik A, Õunap E, Tammaru T (2016) An ordination of life histories using morphological proxies: capital versus income breeding in insects. Ecology 97:2112–2124

    PubMed  Google Scholar 

  • Dumont F, Aubry O, Lucas E (2018) From evolutionary aspects of zoophytophagy to biological control. Front Ecol Evol 6:221

    Google Scholar 

  • Dumont F, Lucas E, Reale D (2016) Evidence of genetic basis of zoophagy and nymphal developmental time in isogroup lines of the zoophytophagous mullein bug, Campylomma verbasci. Biocontrol 61:425–435

    Google Scholar 

  • Dumont F, Lucas E, Reale D (2017) Coexistence of zoophytophagous and phytozoophagous strategies linked to genotypic diet specialization in plant bug. PLoS ONE 12:e0176369

    PubMed  PubMed Central  Google Scholar 

  • Dumont F, Reale D, Lucas E (2019) Can isogroup selection of highly zoophagous lines of a zoophytophagous bug improve biocontrol of spider mites in apple orchards? Insects 10:303

    PubMed Central  Google Scholar 

  • Hughes KA, Reynolds RM (2005) Evolutionary and mechanistic theories of aging. Annu Rev Entomol 50:421–445

    CAS  PubMed  Google Scholar 

  • Ingegno BL, Pansa MG, Tavella L (2011) Plant preference in the zoophytophagous generalist predator Macrolophus pygmaeus (Heteroptera: Miridae). Biol Control 58:174–181

    Google Scholar 

  • Janssen A, Sabelis MW (2015) Alternative food and biological control by generalist predatory mites: the case of Amblyseius swirskii. Exp Appl Acarol 65:413–418

    PubMed  Google Scholar 

  • Kirkwood TB, Rose MR (1991) Evolution of senescence: late survival sacrificed for reproduction. Philos T Roy Soc B 332(1262):15–24

    CAS  Google Scholar 

  • Kruitwagen A, Beukeboom LW, Wertheim B (2018) Optimization of native biocontrol agents, with parasitoids of the invasive pest D. suzukii as an example. Evol Appl 11:1473–1497

    PubMed  PubMed Central  Google Scholar 

  • Leman A, Messelink GJ (2015) Supplemental food that supports both predator and pest: a risk for biological control? Experi Appli Acar 65:511–524

    CAS  Google Scholar 

  • Leung K, Ras E, Ferguson K, Ariëns S, Babendreier D, Bijma P, Bourtzis K, Brodeur J, Bruins M, Centurión A, Chattington S, Chinchilla-Ramírez M, Dicke M, Fatouros N, González Cabrera J, Groot T, Haye T, Knapp M, Koskinioti P, Le Hesran S, Lirakis M, Paspati A, Pérez-Hedo M, Plouvier W, Schlötterer C, Stahl J, Thiel A, Urbaneja A, van de Zande L, Verhulst E, Vet L, Visser S, Werren J, Xia S, Zwaan B, Magalhães S, Beukeboom L, Pannebakker B (2020) Next Generation Biological Control: The Need for Integrating Genetics and Evolution. Preprints 2019:2019110300. https://doi.org/10.20944/preprints201911.0300.v1)

    Article  Google Scholar 

  • Lommen ST, Jong PW, Pannebakker BA (2017) It is time to bridge the gap between exploring and exploiting: prospects for utilizing intraspecific genetic variation to optimize arthropods for augmentative pest control-a review. Entomol Exp Appl 162(2):108–123

    Google Scholar 

  • Lundgren JG (2009) Relationships of natural enemies and non-prey foods progress in biological control. Springer Science, Dordrecht

    Google Scholar 

  • Messelink GJ, Bennison J, Alomar O, Ingegno BL, Tavella L, Shipp L et al (2014) Approaches to conserving natural enemy populations in greenhouse crops: current methods and future prospects. Biocontrol 59:377–393

    Google Scholar 

  • Montoro M, De Clercq P, Overgaard J, Sigsgaard L (2020) Fitness consequences of artificial diets with different macronutrient composition for the predatory bug Orius majusculus. Entomol Exp Appl. https://doi.org/10.1111/eea.12881

    Article  Google Scholar 

  • Mendoza JE, Balanza V, Cifuentes D, Bielza P (2020) Selection for larger body size in Orius laevigatus: intraspecific variability and effects on reproductive parameters. Biol Control. https://doi.org/10.1016/j.biocontrol.2020.104310

    Article  Google Scholar 

  • Nunney L, Leppla NC, Bloem KA, Luck RF (2002) The population genetics of mass-rearing. In: quality control for mass-reared arthropods. Proceedings of the eighth and ninth workshops of the IOBC working group on quality control of mass-reared arthropods, 9–12 Oct 1995, Santa Barbara, CA and 2–4 Mar 1998, Cali, Colombia, pp 43–49

  • Oveja MF, Arnó J, Gabarra R (2012) Effect of supplemental food on the fitness of four omnivorous predator species. IOBC/WPRS Bull 80:97–101

    Google Scholar 

  • Oveja MF, Riudavets J, Arnó J, Gabarra R (2016) Does a supplemental food improve the effectiveness of predatory bugs on cucumber? Biocontrol 61:47–56

    Google Scholar 

  • Parra JRP (2008) Mass rearing of natural enemies. In: Capinera JL (ed) Encyclopedia of entomology. Springer, Dordrecht

    Google Scholar 

  • Rasmussen LB, Jensen K, Sørensen JG, Sverrisdóttir E, Nielsen KL, Overgaard J, Holmstrup M, Kristensen TN (2018) Are commercial stocks of biological control agents genetically depauperate?—A case study on the pirate bug Orius majusculus Reuter. Biol Control 127:31–38

    Google Scholar 

  • Richards PC, Schmidt JM (1996) The effects of selected dietary supplements on survival and reproduction of Orius insidiosus (Say) (Hemiptera: Anthocoridae). Can Entomol 128:171–176

    Google Scholar 

  • Sanchez JA, Alcazar A, Lacasa A, Llamas A, Bielza P (2000) Integrated pest management strategies in sweet pepper plastic houses in the Southeast of Spain. IOBC/WPRS Bull 23:21–30

    Google Scholar 

  • Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594

    CAS  PubMed  Google Scholar 

  • Taberner A, Castañera P, Silvestre E, Bopazo J (1993) Estimation of the intrinsic rate of natural increase and its error by both algebraic and resampling approaches. Comput Appl Biosci 9:535–540

    CAS  PubMed  Google Scholar 

  • Tommasini MG, van Lenteren JC, Burgio G (2004) Biological traits and predation capacity of four Orius species on two prey species. Bull Insectol 57:79–93

    Google Scholar 

  • Urbaneja A, Tapia G, Stansly P (2005) Influence of host plant and prey availability on developmental time and surviorship of Nesidiocoris tenius (Het.: Miridae). Biocontrol Sci Tech 15:513–518

    Google Scholar 

  • Urbaneja-Bernat P, Alonso M, Tena A et al (2013) Sugar as nutritional supplement for the zoophytophagous predator Nesidiocoris tenuis. Biocontrol 58:57–64

    CAS  Google Scholar 

  • Urbaneja-Bernat P, Mollá O, Alonso M et al (2015) Sugars as complementary alternative food for the establishment of Nesidiocoris tenuis in greenhouse tomato. J Appl Entomol 139:161–167

    CAS  Google Scholar 

  • Vacante V, Cocuzza GE, De Clercq P, Van de Veire M, Tirry L (1997) Development and survival of Orius albidipennis and O. laevigatus (Het.: Anthocoridae) on various diets. Entomophaga 42:493

    Google Scholar 

  • van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. Biocontrol 57(1):1–20

    Google Scholar 

  • van Lenteren JC, Alomar O, Ravensberg WJ, Urbaneja A (2020) Integrated pest and disease management in greenhouse crops. In: Gullino ML, Albajes R, Nicot PC (eds) Integrated pest and disease management in greenhouse crops, plant pathology in the 21st Century 9. Springer International Publishing, Cham, pp 409–439

    Google Scholar 

  • Vandekerkhove B, De Clercq P (2010) Pollen as an alternative or supplementary food for the mirid predator Macrolophus pygmaeus. Biol Control 53:238–242

    Google Scholar 

  • Vangansbeke D, Duarte MV, Gobin B, Tirry L, Wäckers F, De Clercq P (2019) Cold-born killers: exploiting temperature-size rule enhances predation capacity of a predatory mite. Pest Manag Sci. https://doi.org/10.1002/ps.5713

    Article  PubMed  Google Scholar 

  • Venkatesan T, Jalali SK, Srinivasamurthy K, Bhaskaran TV (2008) Development, survival and reproduction of an anthocorid predator (Orius tantillus) on artificial and natural diets. Indian J Agr Sci 78:102–105

    Google Scholar 

  • Yano E, Watanabe K, Yara K (2002) Life history parameters of Orius sauteri (Poppius) (Heteroptera: Anthocoridae) reared on Ephestia kuehniella eggs and the minimum amount of the diet for rearing individuals. J Appl Entomol 126:389–394

    Google Scholar 

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Aknowledgements

This research was supported by the Spanish Ministry of Science, Innovation and Universities and by the European FEDER funds (AGL2017-89600-R). José Enrique Mendoza holds a grant from the MSIU (FPU14/02932).

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Authors and Affiliations

  1. Departamento de Ingeniería Agronómica, Universidad Politécnica de Cartagena, Cartagena, Spain

    José Enrique Mendoza, Virginia Balanza, Dina Cifuentes & Pablo Bielza

  2. Instituto de Biotecnología Vegetal, Universidad Politécnica de Cartagena, Cartagena, Spain

    Dina Cifuentes & Pablo Bielza

Authors
  1. José Enrique Mendoza
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  2. Virginia Balanza
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  3. Dina Cifuentes
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  4. Pablo Bielza
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Contributions

PB conceived research. JEM, VB and PB designed experiments. PB, JEM, VB and DC collected and prepared material. JEM and VB conducted experiments and collected data. PB supervised experiments. JEM and PB analysed data. JEM and PB wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to José Enrique Mendoza or Pablo Bielza.

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Communicated by Antonio Biondi.

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Mendoza, J.E., Balanza, V., Cifuentes, D. et al. Genetic improvement of Orius laevigatus for better fitness feeding on pollen. J Pest Sci 94, 729–742 (2021). https://doi.org/10.1007/s10340-020-01291-x

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  • DOI: https://doi.org/10.1007/s10340-020-01291-x

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