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Contrasting olfactory responses of two egg parasitoids to buckwheat floral scent are reflected in field parasitism rates

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Abstract

Conservation biological control programs advocate the planting of flower strips alongside crops to improve the survival and effectiveness of parasitoids. Ideally, the provided food plants are highly attractive and benefit the targeted biocontrol agents without promoting pests or intraguild competition. Previous laboratory studies showed that Trissolcus basalis, an egg parasitoid of the stink bug Nezara viridula, is highly attracted to floral odors of buckwheat and that its nectar increases the wasp’s fecundity. In the field, T. basalis competes with the co-occurring parasitoid Ooencyrtus telenomicida for host eggs. Therefore, in the present study, we explored whether O. telenomicida shows similar attraction to buckwheat volatiles. We then carried out a 2-year field experiment to assess whether the laboratory-observed olfactory behaviors of both species are reflected in changed parasitism rates of stink bug eggs. Parasitism by naturally occurring egg parasitoids was measured in tomato plots with and without a margin of flowering buckwheat. Our results showed that, unlike T. basalis, O. telenomicida was repelled by the odor of buckwheat flowers. In both years, T. basalis found more egg batches and parasitized more stinkbug eggs when flower margins were present. Egg parasitism correlated positively with proximity to the buckwheat margin. In accordance with our prediction, egg parasitism by O. telenomicida occurred almost exclusively in the control plots and for a shorter period during the season. We conclude that buckwheat strips can influence intraguild competition and hypothesize that the effect was mediated by floral volatiles.

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References

  • Belz E, Kölliker M, Balmer O (2013) Olfactory attractiveness of flowering plants to the parasitoid Microplitis mediator: potential implications for biological control. Biocontrol 58:163–173

    Article  Google Scholar 

  • Bianchi FJJA, Wäckers FL (2008) Effects of flower attractiveness and nectar availability in field margins on biological control by parasitoids. Biol Control 46:400–408

    Article  Google Scholar 

  • Bianchi FJJA, Schellhorn NA, Cunningham SA (2013) Habitat functionality for the ecosystem service of pest control: reproduction and feeding sites of pests and natural enemies. Agric For Entomol 15:12–23

    Article  Google Scholar 

  • Bin F, Vinson SB (1991) Efficacy assessment in egg parasitoids (Hymenoptera): proposal for a unified terminology. In: Wajnberg E, Vinson SB (eds) Trichogramma and Other Egg Parasitoids. INRA, vol 56, pp 175–180

  • Blumstein DT, Daniel JC (2007) Quantifying behavior the JWatcher way. Sinauer Associates, Sunderland, p 198

    Google Scholar 

  • Burger H, Dötterl S, Häberlein C, Schulz S, Ayasse M (2012) An arthropod deterrent attracts specialised bees to their host plants. Oecologia 168:727–736

    Article  PubMed  Google Scholar 

  • Colazza S, Salerno G, Wajnberg E (1999) Volatile and contact chemicals released by Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Biol Control 16:310–317

    Article  Google Scholar 

  • Colazza S, Lo Bue M, Lo Giudice D, Peri E (2009) The response of Trissolcus basalis to footprint contact kairomones from Nezara viridula females is mediated by leaf epicuticular waxes. Naturwissenschaften 96:975–981

    Article  CAS  PubMed  Google Scholar 

  • Colazza S, Peri E, Guarino S (2017) Plant and stink bug interactions at different trophic levels. In: Cokl A, Borges M (eds) Biorational control based on communication processes. CRC Press, Boca Raton, pp 18–199

    Google Scholar 

  • Cusumano A, Peri E, Vinson SB, Colazza S (2011) Intraguild interactions between two egg parasitoids exploring host patches. Biocontrol 56:173–184

    Article  Google Scholar 

  • Cusumano A, Peri E, Vinson SB, Colazza S (2012) The ovipositing female of Ooencyrtus telenomicida relies on physiological mechanisms to mediate intrinsic competition with Trissolcus basalis. Entomol Exp Appl 143:155–163

    Article  Google Scholar 

  • Cusumano A, Peri E, Boivin G, Colazza S (2015) Fitness costs of intrinsic competition in two egg parasitoids of a true bug. J Insect Physiol 81:52–59

    Article  CAS  PubMed  Google Scholar 

  • Cusumano A, Peri E, Colazza S (2016) Interspecific competition/facilitation among insect parasitoids. Curr Opin Insect Sci 14:12–16

    Article  Google Scholar 

  • Fiedler AK, Landis DA, Wratten SD (2008) Maximizing ecosystem services from conservation biological control: the role of habitat management. Biol Control 45:254–271

    Article  Google Scholar 

  • Foti MC, Rostás M, Peri E, Park KC, Slimani T, Wratten SD, Colazza S (2017) Chemical ecology meets conservation biological control: identifying plant volatiles as predictors of floral resource suitability for an egg parasitoid of stink bugs. J Pest Sci 90:299–310

    Article  Google Scholar 

  • Géneau CE, Wäckers FL, Luka H, Balmer O (2013) Effects of extrafloral and floral nectar of Centaurea cyanus on the parasitoid wasp Microplitis mediator: olfactory attractiveness and parasitization rates. Biol Control 66:16–20

    Article  Google Scholar 

  • Gurr GM, Wratten SD, Barbosa P (2000) Success in conservation biological control of arthropods. In: Gurr G, Wratten S (eds) In biological control: measures of success. Springer, Netherlands, pp 105–132

    Chapter  Google Scholar 

  • Gurr GM, Wratten SD, Landis DA, You M (2017) Habitat management to suppress pest populations: progress and prospects. Annu Rev Entomol 62:91–109

    Article  CAS  PubMed  Google Scholar 

  • Hassemer MJ, Sant’ana J, De Oliveira MW, Borges M, Laumann RA, Caumo M, Blassioli-Moraes MC (2015) Chemical composition of Alphitobius diaperinus (Coleoptera: Tenebrionidae) abdominal glands and the influence of 1,4-benzoquinones on its behavior. J Econ Entomol 108:2107–2116

    Article  CAS  PubMed  Google Scholar 

  • Incrocci L, Pardossi A, Campiotti CA, Balducchi R, Giunchi L (2002) Energy, water and fertilizer requirements of a closed loop soilless culture of greenhouse cherry tomato in Sicily. In: VI international symposium on protected cultivation in mild winter climate: product and process innovation vol 614, pp 189–192

  • Jacometti M, Jørgensen N, Wratten S (2010) Enhancing biological control by an omnivorous lacewing: floral resources reduce aphid numbers at low aphid densities. Biol Control 55:159–165

    Article  Google Scholar 

  • Kugimiya S, Uefune M, Shimoda T, Takabayashi J (2010) Orientation of the parasitic wasp, Cotesia vestalis (Haliday) (Hymenoptera: Braconidae), to visual and olfactory cues of field mustard flowers, Brassica rapa L. (Brassicaceae), to exploit food sources. Appl Entomol Zool 45:369–375

    Article  Google Scholar 

  • Lucchetta P, Bernstein C, Thery M, Lazzari C, Desouhant E (2008) Foraging and associative learning of visual signals in a parasitic wasp. Anim Cogn 11:525–533

    Article  PubMed  Google Scholar 

  • Ohnishi O, Matsuoka Y (1996) Search for the wild ancestor of buckwheat II. Taxonomy of Fagopyrum (Polygonaceae) species based on morphology, isozymes and cpDNA variability. Genes Genet Syst 71:383–390

    Article  Google Scholar 

  • Peri E, Cusumano A, Agrò A, Colazza S (2011) Behavioral response of the egg parasitoid Ooencyrtus telenomicida to host-related chemical cues in a tritrophic perspective. Biocontrol 56:163–171

    Article  Google Scholar 

  • Peri E, Cusumano A, Amodeo V, Wajnberg E, Colazza S (2014) Intraguild interactions between two egg parasitoids of a true bug in semi-field and field conditions. PLoS ONE 9(6):e99876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahat S, Gurr GM, Wratten SD, Mo J, Neeson R (2005) Effect of plant nectars on adult longevity of the stinkbug parasitoid, Trissolcus basalis. Int J Pest Manag 51:321–324

    Article  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org/. ISBN 3-900051-07-0

  • Rush A, Bommarco R, Ekbom E (2017) Conservation biological control in agricultural landscapes. In: Sauvion N, Calatayud PA, Thiéry D (eds) Insect-plant interactions in a crop protection perspective. Academic Press, New York, pp 333–360

    Chapter  Google Scholar 

  • Sasaki H, Wagatsuma T (2007) Bumblebees (Apidae: Hymenoptera) are the main pollinators of common buckwheat, Fagopyrum esculentum, in Hokkaido, Japan. Appl Entomol Zool 42:659–661

    Article  Google Scholar 

  • Steidle JLM, Schöller M (1997) Olfactory host location and learning in the granary weevil parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae). J Insect Behav 10:331–342

    Article  Google Scholar 

  • Stevenson PC, Nicolson SW, Wright GA (2017) Plant secondary metabolites in nectar: impacts on pollinators and ecological functions. Funct Ecol 31:65–75

    Article  Google Scholar 

  • Tscharntke T, Karp DS, Chaplin-Kramer R et al (2016) When natural habitat fails to enhance biological pest control—five hypotheses. Biol Conserv 204:449–458

    Article  Google Scholar 

  • Tschumi M, Albrecht M, Entling MH, Jacot K (2015) High effectiveness of tailored flower strips in reducing pests and crop plant damage. Proc R Soc B 282(1814):20151369

    Article  Google Scholar 

  • Wäckers FL (2005) Suitability of (extra-) floral nectar, pollen, and honeydew as insect food sources. In: Wäckers FL, van Rijn PCJ, Bruin J (eds) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge, pp 17–74

    Chapter  Google Scholar 

  • Wakil W, Brust GE, Perring T (eds) (2017) Sustainable management of arthropod pests of tomato. Academic Press, New York

    Google Scholar 

Download references

Author Contributions

MCF, EP, SC, and MR contributed to the design and implementation of the research; MCF acquired field data; MCF and EW analyzed the results. All authors discussed the results and wrote the final manuscript.

Acknowledgements

The authors thank Edgardo Foti for providing fields and for assistance in the management of the crop and flowering plants. We thank Janine Johnson for copyediting the manuscript. This research was partially supported by the Marie Skłodowska-Curie Research and Innovation Staff Exchange (RISE) H2020-MSCA-RISE-2015 of the European Union with the project Impact of invasive alien true bug species in native trophic webs—INVASIoN (GA 690952).

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Authors and Affiliations

  1. University of Palermo, Department of Agricultural, Food and Forest Sciences, Viale delle scienze, 90128, Palermo, Italy

    Maria Cristina Foti, Ezio Peri & Stefano Colazza

  2. Bio-Protection Research Centre, Lincoln University, PO Box 85084, Lincoln, 7647, New Zealand

    Michael Rostás

  3. INRA, 400 Route des Chappes, 06410, Sophia Antipolis Cedex, France

    Eric Wajnberg

  4. INRIA, Sophia Antipolis, Projet Hephaistos, 2004 Route des Lucioles, BP 93, 06902, Sophia Antipolis Cedex, France

    Eric Wajnberg

  5. Fondazione Angelo e Salvatore Lima Mancuso, Piazza Marina 61, 90100, Palermo, Italy

    Maria Cristina Foti

Authors
  1. Maria Cristina Foti
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  2. Ezio Peri
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  3. Eric Wajnberg
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  4. Stefano Colazza
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  5. Michael Rostás
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Correspondence to Maria Cristina Foti.

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The authors declare that they have no conflict of interests regarding this research.

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Informed consent was obtained from all individual participants included in the study.

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This article does not contain any studies with human participants or animals (vertebrates) performed by any of the authors.

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Communicated by S. Macfadyen.

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Foti, M.C., Peri, E., Wajnberg, E. et al. Contrasting olfactory responses of two egg parasitoids to buckwheat floral scent are reflected in field parasitism rates. J Pest Sci 92, 747–756 (2019). https://doi.org/10.1007/s10340-018-1045-2

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  • DOI: https://doi.org/10.1007/s10340-018-1045-2

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