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Seasonal changes in aphid hyperparasitoid occurrence in sweet pepper and raspberry in Belgium

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Abstract

By attacking primary parasitoids, hyperparasitoids represent a major threat to biological pest control, especially in the context of aphid control which relies to a large extent on parasitoids. Despite their importance still little is known about when hyperparasitoids arrive in the crop, their diversity, how hyperparasitoid communities change throughout the growth season and whether these changes are similar across different crop species. Here, we used banker plants with aphids parasitized by the commonly applied biocontrol agent Aphidius ervi to detect and identify hyperparasitoids in five sweet pepper and five raspberry farms in Flanders, Belgium. Surveys started early in the growth season (March) and lasted until October. Throughout the survey, hyperparasitoid species from six different genera were found. Hyperparasitoids were observed from the start of the survey until September in sweet pepper and until October in raspberry. However, the overall observed rate of hyperparasitism within the banker plants was higher in sweet pepper (42%) than in raspberry (10%). The most commonly identified genus differed between the two crops. Dendrocerus was the most frequently identified hyperparasitoid in raspberry throughout the entire season. Conversely, while Dendrocerus was the only hyperparasitoid genus found in March and April in sweet pepper, it became replaced by individuals of the genera Alloxysta, Pachyneuron and Phaenoglyphis later in the growth season. The presence of multiple species of hyperparasitoids in a single crop reinforces their potential to disrupt biocontrol programs. Therefore, future efforts should focus on the development of effective management strategies to control hyperparasitoids.

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References

  • Acheampong S, Gillespie DR, Quiring D (2012) Survey of parasitoids and hyperparasitoids (Hymenoptera) of the green peach aphid, Myzus persicae and the foxglove aphid, Aulacorthum solani (Hemiptera: Aphididae) in British Columbia. J Entomol Soc b c 109:12–22

    Google Scholar 

  • Alfaro-Tapia A, Alvarez-Baca JK, Tougeron K, van Baaren J, Lavandero B, Le Lann C (2022) Composition and structure of winter aphid-parasitoid food webs along a latitudinal gradient in Chile. Oecologia 200:425–440

    Article  PubMed  Google Scholar 

  • Boivin G, Hance T, Brodeur J (2012) Aphid parasitoids in biological control. Can J Plant Sci 92:1–12

    Article  Google Scholar 

  • Bloemhard CMJ, Wielen M, Messelink GJ (2014) Seasonal abundance of aphid hyperparasitoids in organic greenhouse crops in the Netherlands. IOBC/WPRS Bull 102:15–19

    Google Scholar 

  • Brodeur J, McNeil JN (1994) Life history of the aphid hyperparasitoid Asaphes vulgaris Walker (Pteromalidae): Possible consequences on the efficacy of the primary parasitoid Aphidius nigripes Ashmead (Aphidiidae). Can Entomol 126:1493–1497

    Article  Google Scholar 

  • Buitenhuis R, Boivin G, Vet LEM, Brodeur J (2004) Preference and performance of the hyperparasitoid Syrphophagus aphidivorus (Hymenoptera: Encyrtidae): fitness consequences of selecting hosts in live aphids or aphid mummies. Ecol Entomol 29:648–656

    Article  Google Scholar 

  • Chaianunporn T, Hovestadt T (2019) Dispersal evolution in metacommunities of tri-trophic systems. Ecol Model 395:28–38

    Article  Google Scholar 

  • Chomnunti P, Hongsanan S, Aguirre-Hudson B, Tian Q, Peršoh D, Dhami MK, Alias AS, Xu J, Liu X, Stadler M, Hyde KD (2014) The sooty moulds. Fungal Divers 66:1–36

    Article  Google Scholar 

  • Cusumano A, Harvey JA, Bourne ME, Poelman EH, de Boer JG (2020) Exploiting chemical ecology to manage hyperparasitoids in biological control of arthropod pests. Pest Manag Sci 76:432–443

    Article  CAS  PubMed  Google Scholar 

  • de Boer JG, Salis L, Tollenaar W, van Heumen LJM, Costaz TPM, Harvey JA, Kos M, Vet LEM (2019) Effects of temperature and food source reproduction and longevity of aphid hyperparsaitoids of the genera Dendrocerus and Asaphes. BioControl 64:277–290

    Article  Google Scholar 

  • Edwards OR, Hoy MA (1993) Polymorphism in two parasitoids detected using random amplified polymorphic DNA polymerase chain reaction. Biol Control 3:243–257

    Article  Google Scholar 

  • Fergusson NDM (1980) Revision of the British species of Dendrocerus Ratzeburg (Hymenoptera: Ceraphronoidea) with a review of their biology as aphid hyperparasites. Bull Br Mus Nat Hist Entomol 41:255–314

    Google Scholar 

  • Ferrer-Suay M, Selfa J, Equihua-Martínez A, Estrada-Venegas E, Lomeli-Flores R, Martínez RP, Pujade-Villar J (2013) Charipinae (Hymenoptera: Cynipoidea: Figitidae) from Mexico with description of three new species. Ann Entomol 106:26–41

    Google Scholar 

  • Goelen T, Sobhy IS, Vanderaa C, Boer JG, Delvigne F, Francis F, Wäckers FL, Rediers H, Verstrepen KJ, Wenseleers T, Jacquemyn H, Lievens B (2020) Volatiles of bacteria associated with parasitoid habitats elicit distinct olfactory responses in an aphid parasitoid and its hyperparasitoid. Funct Ecol 34:507–520

    Article  Google Scholar 

  • Gómez-Marco F, Urbaneja A, Jaques JA, Rugman-Jones PF, Stouthamer R, Tena A (2015) Untangling the aphid-parasitoid food web in citrus: can hyperparasitoids disrupt biological control? Biol Control 81:111–121

    Article  Google Scholar 

  • Gordon SC, Woodford JAT, Birch ANE (1997) Arthropod pests of Rubus in Europe: pest status, current and future control strategies. J Hortic Sci 72:831–862

    Article  Google Scholar 

  • de Graham MWR, V. (1969) The Pteromalidae of Northwestern Europe (Hymenoptera: Chalcidoidea). Bull Br Mus Nat Hist Entomol 16:1–908

    Google Scholar 

  • Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. PNAS 101:14812–14817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hodge S, Powell G (2010) Conditional facilitation of an aphid vector, Acyrthosiphon pisum, by the plant pathogen pea enation mosaic virus. J Insect Sci 10:155

    Article  PubMed  PubMed Central  Google Scholar 

  • Höller C, Borgemeister C, Haardt H, Powell W (1993) The relationship between primary parasitoids and hyperparasitoids of cereal aphids: an analysis of field data. J Anim Ecol 62:12–21

    Article  Google Scholar 

  • Janssen A, Montserrat M, Hillerislambers R, de Roos AM, Pallini A, Sabelis MW (2006) Intraguild predation usually does not disrupt biological control. In: Brodeur J, Boivin G (eds) Trophic and guild in biological interactions control. Progress in Biological control, vol 3. Springer, Dordrecht, pp 21–44

    Chapter  Google Scholar 

  • Jeavons E, van Baaren J, Le Ralec A, Buchard C, Duval F, Llopis S, Postic E, Le Lann C (2021) Third and fourth trophic level composition shift in an aphid-parasitoid-hyperparasitoid food web limits aphid control in an intercropping system. J Appl Ecol 59:300–313

    Article  Google Scholar 

  • Kos K, Petrović-Obradović O, Žikić V, Petrović A, Trdan S, Tomanović Ž (2012) Review of interactions between host plants, aphids, primary parasitoids and hyperparasitoids in vegetable and cereal ecosystems in Slovenia. J Entomol Res Soc 14(3):67–78

    Google Scholar 

  • Luan Y, Zhang Y, Yue Q, Pang J, Xie R, Yin W (2003) Ribosomal DNA gene and phylogenetic relationships of Diplura and lower Hexapods. Sci China Life Sci 46:67–76

    Article  CAS  Google Scholar 

  • Messelink GJ, Bloemhard CMJ, Cortes JA, Sabelis MW, Janssen A (2011) Hyperpredation by generalist predatory mites disrupts biological control of aphids by the aphidophagous gall midge Aphidoletes aphidimyza. Biol Control 57:246–252

    Article  Google Scholar 

  • Nagasaka K, Takahasi N, Okabayashi T (2010) Impact of secondary parasitism on Aphidius colemani in the banker plant system on aphid control in comercial greenhouses in Kochi Japan. Appl Entomol Zool 45:541–550

    Article  Google Scholar 

  • Nematollahi MR, Fathipour Y, Talebi AA, Karimzadeh J, Zalucki MP (2014) Parasitoid- and hyperparasitoid-mediated seasonal dynamics of the cabbage aphid (Hemiptera: Aphididae). Environ Entomol 43:1542–1551

    Article  PubMed  Google Scholar 

  • Nenzén HK, Martel V, Gravel D (2018) Can hyperparasitoids cause large-scale outbreaks of insect herbivores? Oikos 127:1344–1354

    Article  Google Scholar 

  • Poelman EH, Cusumano A, de Boer JG (2022) The ecology of hyperparasitoids. Annu Rev Entomol 67:143–161

    Article  CAS  PubMed  Google Scholar 

  • Pons X, Lumbierres B, Antoni R, Starý P (2011) Parasitoid complex of alfalfa aphids in an IPM intensive crop system in northern Catalonia. J Pest Sci 84:437–445

    Article  Google Scholar 

  • Quicke DLJ (1997) Parasitic wasps. Chapman & Hall Ltd., London

    Google Scholar 

  • R Core team (2023) R: a language and environment for statistical computing. R Foundation for Statistical computing. Vienna, Austria. https://www.r-project.org/

  • Sanchez JA, La-Spina M, Michelena JM, Lacasa A, Hermoso de Mendoza A (2010) Ecology of the aphid pests of protected pepper crops and their parasitoids. Biocontrol Sci 21:171–188

    Article  Google Scholar 

  • Schellhorn NA, Kuhman TR, Olson AC, Ives AR (2002) Competition between native and introduced parasitoids of aphids: Nontarget effects and biological control. Ecology 83:2745–2757

    Article  Google Scholar 

  • Schooler SS, Ives AR, Harmon J (1996) Hyperparasitoid aggregation in response to variation in Aphidius ervi host density at three spatial scales. Ecol Entomol 21:249–258

    Article  Google Scholar 

  • Schooler SS, De Barro P, Ives AR (2011) The potential for hyperparasitism to compromise biological control: Why don’t hyperparasitoids drive their primary parasitoid hosts extinct? Biol Control 58:167–173

    Article  Google Scholar 

  • Starý P (1988) Parasites: Aphidiidae. In: Minks AK, Harrewijn P (eds) Aphids: their biology, natural enemies and control. Elsevier, Amsterdam, pp 171–184

    Google Scholar 

  • Stephens AEA, Srivastava DS, Myers JH (2013) Strength in numbers? Effects of multiple natural enemy species on plant performance. Proc R Soc B 280:20122756

    Article  PubMed  PubMed Central  Google Scholar 

  • Sullivan DJ (1987) Insect hyperparasitism. Annu Rev Entomol 32:49–70

    Article  Google Scholar 

  • Sullivan DJ, Völkl W (1999) Hyperparasitism: multitrophic ecology and behavior. Annu Rev Entomol 44:291–315

    Article  CAS  PubMed  Google Scholar 

  • Tougeron K, Damien M, Le Lann C, Brodeur J, van Baaren J (2018) Rapid responses of winter aphid-parasitoid communities to climate warming. Front Ecol Evol 6:173

    Article  Google Scholar 

  • van Baaren J, Wist T, Soroka J, Tougeron K (2020) Host-parasitoid network in extreme conditions: the case of cereal aphids in wheat crops in Saskatchewan. Canada Entomol Gen 40:63–77

    Google Scholar 

  • van Emden HF, Harrington R (2007) Aphids as crop pests. CABI Publishing, Wallingford

    Book  Google Scholar 

  • van Neerbos FAC, Dewitte P, Wäckers F, Wenseleers T, Jacquemyn H, Lievens B (2023) Bacterial volatiles elicit differential olfactory responses in insect species from the same and different trophic levels. Insect Sci 30:1464–1480

    Article  PubMed  Google Scholar 

  • Yang F, Xu L, Wu YK, Wang Q, Yao ZW, Žikic V, Tomanović Ž, Ferrer-Suay M, Selfa J, Pujade-Villar J, Traugott M, Desneux M, Lu Y-H, Guo YY (2017) Species composition and seasonal dynamics of aphid parasitoids and hyperparasitoids in wheat fields in northern China. Sci Rep 7:13989

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We are grateful to VLAIO (Flanders Innovation and Entrepeneurship) for financial support of this research [project HBC.2018.2202]. Furthermore, we would like to thank all growers involved in this study.

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Authors and Affiliations

  1. CMPG Laboratory for Process Microbial Ecology and Bioinspirational Management (PME & BIM). Department Microbial and Molecular Systems (M2S), KU Leuven, Willem De Croylaan 46 Box 2458, 3001, Leuven, Belgium

    Francine A. C. van Neerbos & B. Lievens

  2. Leuven Plant Institute (LPI), KU Leuven, 3001, Leuven, Belgium

    Francine A. C. van Neerbos, H. Jacquemyn & B. Lievens

  3. Zoology Department, Research Centre for Fruit Growing, 3800, Sint-Truiden, Belgium

    A. Alhmedi & T. Beliën

  4. Research Station for Vegetable Production, 2860, Sint-Katelijne-Waver, Belgium

    L. Van Herck, E. Van Erkel, R. M. J. De Vis & R. Clymans

  5. Laboratory of Plant Conservation and Population Biology, Biology Department, KU Leuven, 3001, Leuven, Belgium

    H. Jacquemyn

Authors
  1. Francine A. C. van Neerbos
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  2. A. Alhmedi
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  4. E. Van Erkel
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  7. T. Beliën
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  9. B. Lievens
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Correspondence to B. Lievens.

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van Neerbos, F.A.C., Alhmedi, A., Van Herck, L. et al. Seasonal changes in aphid hyperparasitoid occurrence in sweet pepper and raspberry in Belgium. BioControl (2024). https://doi.org/10.1007/s10526-024-10248-3

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