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How Apis mellifera Behaves with its Invasive Hornet Predator Vespa velutina?

Journal of Insect Behavior volume 31, pages 1–11 (2018)Cite this article

Abstract

Invasive species are now recognized as a major cause of native biodiversity loss worldwide. In the current deleterious context for pollinators, the invasive yellow-legged hornet, Vespa velutina, represents an additional threat to the domestic honeybee, Apis mellifera, in Europe. Therefore, understanding the impact of this predator on honeybee colonies is of major importance. In the present study, we tried to assess the impact of V. velutina on the honeybee foraging and defence behaviour based on the video monitoring of two hives. Balling behaviour is reported here for the first time under natural conditions in A. mellifera against V. velutina in Europe. Although these results are preliminary and should be carefully considered, we found that the number of hornets impacted honeybee foraging and defence behaviours. More defensive behaviours were notified in the hive, which survives slightly longer. This may suggest that selecting for more defensive colonies may provide an interesting perspective.

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References

  • Arca M, Papachristoforou A, Mougel F, Rortais A, Monceau K, Bonnard O, Tardy P, Thiéry D, Silvain J-F, Arnold G (2014) Defensive behaviour of Apis mellifera against Vespa velutina in France: testing whether European honeybees can develop an effective collective defence against a new predator. Behav Process 106:122–129

    Article  Google Scholar 

  • Arca M, Mougel F, Guillemaud T, Dupas S, Rome Q, Perrard A, Muller F, Fossoud A, Capdevielle-Dulac C, Torres-Leguizamon M, Chen XX, Tan JL, Villemant C, Arnold G, Silvain JF (2015) Reconstructing the invasion and the demographic history of the yellow-legged hornet, Vespa velutina, in Europe. Biol Invasions 17:2357–2371

    Article  Google Scholar 

  • Baracchi D, Cusseau G, Pradella D, Turillazzi S (2010) Defence reactions of Apis mellifera ligustica against attacks from the European hornet Vespa crabro. Ethol Ecol 22:281–294

    Article  Google Scholar 

  • Barbet-Massin M, Rome Q, Muller F, Perrard A, Villemant C, Jiguet F (2013) Climate change increases the risk of invasion by the yellow-legged hornet. Biol Conserv 157:4–10

    Article  Google Scholar 

  • Bessa AS, Carvalho J, Gomes A, Santarem F (2016) Climate and land-use drivers of invasion: predicting the expansion of Vespa velutina nigrithorax into the Iberian peninsula. Insect Conserv Divers 9:27–37

    Article  Google Scholar 

  • Breed MD, Rogers KB (1991) The behavioral genetics of colony defense in honeybees: genetic variability for guarding behaviour. Behav Genet 21:295–303

    CAS  Article  PubMed  Google Scholar 

  • Breed MD, Guzmán-Novoa E, Hunt GJ (2004) Defensive behaviour of honey bees: organization, genetics, and comparisons with other bees. Annu Rev Entomol 49:271–298

    CAS  Article  PubMed  Google Scholar 

  • Budge GE, Hodgetts J, Jones EP, Ostoja-tarzewski JC, Hall J, Tomkies V, Semmence N, Brown M, Wakefield M, Stainton K (2017) The invasion, provenance and diversity of Vespa velutina Lepeletier (hymenoptera: Vespidae) in great Britain. PLoS One 12:e0185172

    Article  PubMed  PubMed Central  Google Scholar 

  • Calderone NW (1998) Proximate mechanisms of age polyethism in the honey bee, Apis mellifera L. Apidologie 29:127–158

    Article  Google Scholar 

  • Demichelis S, Manimo A, Porporato M (2013) Trovato il primo nido di Vespa velutina a Vallecrosia (IM). http://wwwvespavelutinaeu/LinkClickaspx?fileticket=NhQAlzPdbcg%3d&tabid=111&portalid=0&mid=534&language=it-IT Accessed 5 April 2017

  • Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, McClean C, Osborne PE, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46

    Article  Google Scholar 

  • Essl F, Bacher S, Blackburn TM, Booy O, Brundu G, Brunel S, Cardoso A-C, Eschen R, Gallardo B, Galil B, Garcia-Berthou E, Genovesi P, Groom Q, Harrower C, Hulme PE, Katsanevakis S, Kenis M, Kühn I, Kumschick S, Martinou AF, Nentwig W, O’Flynn C, Pagad S, Pergl J, Pysek P, Rabitsch W, Richardson DM, Roques A, Roy HE, Scalera R, Schindler S, Seebens H, Vanderhoeven S, Vila M, Wilson JRU, Zenetos A, Jeschke JM (2015) Crossing frontiers in tackling pathways of biological invasions. Bioscience DOI:https://doi.org/10.1093/biosci/biv082

  • Giray T, Guzmán-Novoa E, Aron CW, Zelinsky B, Fahrbach SE, Robinson GE (2000) Genetic variation in worker temporal polyethism and colony defensiveness in the honey bee, Apis mellifera. Behav Ecol 11:44–55

    Article  Google Scholar 

  • Goulson D, Nicholls E, Botias C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1435–1444

    CAS  Article  Google Scholar 

  • Grosso-Silva JM, Maia M (2012) Vespa velutina Lepeletier, 1836 (Hymenoptera, Vespidae), new species for Portugal. Arquiv Entomol 6:53–54

    Google Scholar 

  • Hölldobler B, Wilson EO (2008) The superorganism. Norton WW & Company, New York, In

    Google Scholar 

  • Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18

    Article  Google Scholar 

  • Ibáñez-Justicia A, Loomans AJM (2011) Mapping the potential occurrence of an invasive species by using CLIMEX: case of the Asian hornet (Vespa velutina nigrithorax) in The Netherlands. Proc Neth Entomol Soc Meet 22:39–46

    Google Scholar 

  • Johnson BR (2010) Division of labor in honeybees: form, function, and proximate mechanisms. Behav Ecol Sociobiol 64:305–316

    Article  PubMed  Google Scholar 

  • Kastberger G, Thenius G, Stabentheiner A, Hepburn R (2009) Aggressive and docile colony defence patterns in Apis mellifera. A retreater–releaser concept. J Insect Behav 22:65–85

    Article  Google Scholar 

  • Ken T, Hepburn HR, Radloff SE, Yusheng Y, Yiqiu L, Danyin Z, Neumann P (2005) Heat-balling wasps by honeybees. Naturwissenschaften 92:492–495

    Article  PubMed  Google Scholar 

  • López S, Gonzáles M, Goldarazena A (2011) Vespa velutina Lepeletier, 1836 (hymenoptera: Vespidae): first records in Iberian peninsula. Bull. OEPP/EPPO Bull 41:439–441

    Article  Google Scholar 

  • Monceau K, Thiéry D (2017) Vespa velutina nest distribution at a local scale: an 8-year survey of the invasive honeybee predator. Insect Sci 24:663–674

    Article  PubMed  Google Scholar 

  • Monceau K, Arca M, Leprêtre L, Mougel F, Bonnard O, Silvain J-F, Maher N, Arnold G, Thiéry D (2013a) Native prey and invasive predator patterns of foraging activity: the case of the yellow-legged hornet predation at European honeybee hives. PLoS One 8:e66492

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Monceau K, Maher N, Bonnard O, Thiéry D (2013b) Predation dynamics study of the recently introduced honeybee killer Vespa velutina: learning from the enemy. Apidologie 44:209–221

    Article  Google Scholar 

  • Monceau K, Bonnard O, Thiéry D (2014a) Vespa velutina: a new invasive predator of honeybees in Europe. J Pest Sci 87:1–16

    Article  Google Scholar 

  • Monceau K, Bonnard O, Moreau J, Thiéry D (2014b) Spatial distribution of Vespa velutina individuals hunting at domestic honeybee hives: heterogeneity at a local scale. Insect Sci 21:765–774

    Article  PubMed  Google Scholar 

  • Nouvian M, Reinhard J, Giurfa M (2016) The defensive response of the honeybee Apis mellifera. J Exp Biol 219:3505–3517

    Article  PubMed  Google Scholar 

  • Page RE, Robinson GE, Fondrk MK, Nasr ME (1995) Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.) Behav Ecol Sociobiol 36:387–396

    Article  Google Scholar 

  • Papachristoforou A, Rortais A, Zafeiridou G (2007) Smothered to death: hornets asphyxiated by honeybees. Curr Biol 1:795–796

    Article  Google Scholar 

  • Papachristoforou A, Rortais A, Sueur J, Arnold G (2011) Attack or retreat: contrasted defensive tactics used by Cyprian honeybee colonies under attack from hornets. Behav Process 86:236–241

    Article  Google Scholar 

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria URL https://wwwR-projectorg/Accessed 5 April 2017

  • Rittschof CC, Robinson GE (2013) Manipulation of colony environment modulates honey bee aggression and brain gene expression. Genes Brain Behav 12:802–811

    CAS  Article  PubMed  Google Scholar 

  • Robinet C, Suppo C, Darrouzet E (2017) Rapid spread of the invasive yellow-legged hornet in France: the role of human-mediated dispersal and the effects of control measures. J Appl Ecol 54:205–215

    Article  Google Scholar 

  • Seeley TD (1985) Honeybee ecology a study of adaptation in social life. Princeton University Press, Princeton

    Book  Google Scholar 

  • Tan K, Radloff SE, Li JJ, Hepburn HR, Yang MX, Zhang LJ, Neumann P (2007) Bee-hawking by the wasp, Vespa velutina, on the honeybees Apis cerana and A. mellifera. Naturwissenschaften 94:469–472

    CAS  Article  PubMed  Google Scholar 

  • Tan K, Li H, Yang MX, Hepburn HR, Radloff SE (2010) Wasp hawking induces endothermic heat production in guard bees. J Insect Sci 10:142 http://jinsectscience.oxfordjournals.org/content/10/1/142 Accessed 5 April 2017

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Tan K, Wang Z, Li H, Yang S, Hu Z, Kastberger G, Oldroyd BP (2012) An ‘I see you’ prey–predator signal between the Asian honeybee, Apis cerana, and the hornet, Vespa velutina. Anim Behav 83:879–882

    Article  Google Scholar 

  • Tan K, Wang Z, Chen W, Hu Z, Oldroyd BP (2013) The ‘I see you’ prey–predator signal of Apis cerana is innate. Naturwissenschaften 100:245–248

    CAS  Article  PubMed  Google Scholar 

  • Villemant C, Barbet-Massin M, Perrard A, Muller F, Gargominy O, Jiguet F, Rome Q (2011) Predicting the invasion risk by the alien bee-hawking yellow-legged hornet Vespa velutina nigrithorax across Europe and other continents with niche models. Biol Conserv 144:2150–2152

    Article  Google Scholar 

  • Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499

    CAS  Article  Google Scholar 

  • Witt R (2015) Erstfund eines Nestes der Asiatischen Hornisse Vespa velutina Lepeletier, 1838 in Deutschland und Details zum Nestbau (Hymenoptera, Vespinae). Ampulex 7:42–53

    Google Scholar 

  • Wray MK, Mattila HR, Seeley TD (2011) Collective personalities in honeybee colonies are linked to colony fitness. Anim Behav 81:559–568

    Article  Google Scholar 

  • Yang G-H (2005) Harm of introducing the western honeybee Apis mellifera L to the Chinese honeybee Apis cerana F and its ecological impact. Acta Entomol Sin 48:401–406 (in Chinese)

    Google Scholar 

Download references

Acknowledgements

This research project was funded by a FranceAgriMer [grant #797/2007–2010]. Second author was also supported by a grant from the Fondation pour la Recherche sur la Biodiversité [Wasprey project]. Financial support was also provided by CNRS, IRD and INRA SPE department core budgets. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Conceived and designed the experiments: MA, GA. Performed the experiments: KM, MA, LL, OB, GA. Analyzed the data: KM, LL, DT. Contributed reagents/materials/analysis tools: KM, MA, OB, GA, DT. Wrote the paper: KM, DT.

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Authors and Affiliations

  1. UMR CNRS 7372 Centre d’Etudes Biologiques de Chizé, Université de la Rochelle, 79360, Villiers-en-bois, France

    Karine Monceau

  2. CNRS, Laboratoire Evolution, Génomes, Comportement, Ecologie, 91198, Gif-sur-Yvette, France

    Mariangela Arca & Gérard Arnold

  3. Université Paris-Sud 11, Orsay, France

    Mariangela Arca

  4. Unité de Recherche IRD 072, Laboratoire Evolution, Génomes, Comportement, Ecologie CNRS, 91198, Gif-sur-Yvette, France

    Mariangela Arca

  5. UMR INRA 1065 Santé et Agroécologie du Vignoble, ISVV, BSA, F-33883, Villenave d’Ornon, France

    Lisa Leprêtre, Olivier Bonnard & Denis Thiéry

Authors
  1. Karine Monceau
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  2. Mariangela Arca
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  3. Lisa Leprêtre
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  4. Olivier Bonnard
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  5. Gérard Arnold
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  6. Denis Thiéry
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Corresponding author

Correspondence to Denis Thiéry.

Electronic supplementary material

Online Resource 1

Variation of the number of flying Apis mellifera during the season (DOCX 182 kb)

Online Resource 2

Apis mellifera mellifera balling behavior against Vespa velutina. (MP4 421,501 kb)

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Monceau, K., Arca, M., Leprêtre, L. et al. How Apis mellifera Behaves with its Invasive Hornet Predator Vespa velutina?. J Insect Behav 31, 1–11 (2018). https://doi.org/10.1007/s10905-017-9658-5

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  • DOI: https://doi.org/10.1007/s10905-017-9658-5

Keywords

  • Balling behaviour
  • Defence behaviour
  • Domestic honeybee
  • Foraging
  • Yellow-legged hornet