The Asian hornet is an invasive predator of honey bees in Western Europe. The Asian hornet-related risk of bee colony mortality has motivated the development of biological and physical control methods over the past years. Although the technical cost–benefit ratio has been established for most of these control methods, it is still unclear whether such methods can reduce the detrimental effects of the Asian hornet on European honey bees. In this study, we investigated the potential benefits of a biodiversity-friendly control method, the beehive muzzle. We observed the flight activity of bees and the predation behaviour of the Asian hornets at the beehive entrance of 22 pairs of honey bee colonies, each with one muzzle-equipped colony and one control colony without muzzle, in France. We measured HF (bee homing failure due to hornet predation of bees) and FP (foraging paralysis: the stop of flight activity in beehives due to hovering hornets), and estimated the mortality probability of the colonies using a mechanistic modelling approach. The beehive muzzle did not reduce the hornet-related HF, but drastically reduced FP. Moreover, the muzzle increased the survival probability of hornet-stressed colonies up to 51% in context of high abundance of Asian hornets based on theoretical simulations. These results suggest that installing beehive muzzles can mitigate the detrimental effect of the Asian hornet on European honey bees. This low-cost technique does not lead to any environmental impacts and could therefore be recommended to beekeepers as an effective biodiversity-friendly method of Asian hornet control.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Arca M, Mougel F, Guillemaud T, Dupas S, Rome Q, Perrard A et al (2015) Reconstructing the invasion and the demographic history of the yellow-legged hornet, Vespa velutina, in Europe. Biol Invasions 17:2357–2371
Becher MA, Grimm V, Thorbek P, Horn J, Kennedy PJ, Osborne JL (2014) BEEHAVE: a systems model of honeybee colony dynamics and foraging to explore multifactorial causes of colony failure. J Appl Ecol 51:470–482
Beggs JR, Brockerhoff EG, Corley JC, Kenis M, Masciocchi M, Muller F et al (2011) Ecological effects and management of invasive alien Vespidae. Biocontrol 56:505–526
Bellard C, Rysman JF, Leroy B, Claud C, Mace GM (2017) A global picture of biological invasion threat on islands. Nat Ecol Evol 1:1862–1869
Bertolino S, Lioy S, Laurino D, Manino A, Porporato M (2016) Spread of the invasive yellow-legged hornet Vespa velutina (Hymenoptera: Vespidae) in Italy. Appl Entomol Zool 51:589–597
Bradshaw CJA, Leroy B, Bellard C, Albert C, Roiz D, Barbet-Massin M et al (2016) Massive yet grossly underestimated global costs of invasive insects. Nat Commun 4:12986
Brook BW, Sodhi NS, Bradshaw CJ (2008) Synergies among extinction drivers under global change. Trends Ecol Evol 23:453–460
Cheng Y, Wen P, Dong S, Tan K, Nieh JC (2017) Poison and alarm: the Asian hornet Vespa velutina uses sting venom volatiles as an alarm pheromone. J Exp Biol 220:645–651
Couto A, Monceau K, Bonnard O, Thiéry D, Sandoz JC (2014) Olfactory attraction of the hornet Vespa velutina to honeybee colony odors and pheromones. PLoS ONE 9:e115943
EFSA (2015) Statement on the suitability of the BEEHAVE model for its potential use in a regulatory context and for the risk assessment of multiple stressors in honeybees at the landscape level. EFSA J 13:91
Garibaldi LA, Requier F, Rollin O, Andersson GKS (2017) Towards an integrated species and habitat management of crop pollination. Curr Opin Insect Sci 21:1–10
Garigliany M, Taminiau B, El Agrebi N, Cadar D, Gilliaux G, Hue M et al (2017) Moku virus in invasive Asian Hornets, Belgium, 2016. Emerg Infect Dis 23:2109–2112
Gévar J, Bagnères AG, Christidès JP, Darrouzet E (2017) Chemical heterogeneity in inbred European population of the invasive hornet Vespa velutina nigrithorax. J Chem Ecol 43:763–777
Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957
Gray A, Brodschneider R, Adjlane N, Ballis A, Brusbardis V, Charrière JD et al (2019) Loss rates of honey bee colonies during winter 2017/18 in 36 countries participating in the COLOSS survey, including effects of forage sources. J Apic Res. https://doi.org/10.1080/00218839.2019.1615661
Grosso-Silva JM, Maia M (2012) Vespa velutina Lepeletier, 1836 (hymenoptera, Vespidae), new species for Portugal. Arq Entomol 6:53–54
Haxaire J, Bouguet JP, Tamisier JP (2006) Vespa velutina Lepeletier, 1836, une redoutable nouveauté pour la faune de France (Hym., Vespidae). Bull Soc Entomol Fr 111:194
Huang KJ, Kingston JM, Albrecht M, Holway DA, Kohn JR (2018) The worldwide importance of honey bees as pollinators in natural habitats. Proc R Soc B 285:20172140
Keeling MJ, Franklin DN, Datta S, Brown MA, Budge GE (2017) Predicting the spread of the Asian hornet (Vespa velutina) following its incursion into Great Britain. Sci Rep 7:6240
Kennedy PJ, Ford SM, Poidatz J, Thiéry D, Osborne JL (2018) Searching for nests of the invasive Asian hornet (Vespa velutina) using radio-telemetry. Commun Biol 1:1–8
Kulhanek K, Steinhauer N, Rennich K, Caron DM, Sagili RR, Pettis JS et al (2017) A national survey of managed honey bee 2015–2016 annual colony losses in the USA. J Apic Res 56:328–340
Leza M, Herrera C, Marques A, Roca P, Sastre-Serra J, Pons DG (2019) The impact of the invasive species Vespa velutina on honeybees: a new approach based on oxidative stress. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2019.06.511
Liu Z, Chen C, Niu Q, Qi W, Yuan C, Su S et al (2016) Survey results of honey bee (Apis mellifera) colony losses in China (2010–2013). J Apic Res 55:29–37
López S, González M, Goldarazena A (2011) Vespa velutina Lepeletier, 1836 (Hymenoptera: Vespidae): first records in Iberian Peninsula. EPPO Bull 41:439–441
Mazza G, Tricarico E, Genovesi P, Gherardi F (2014) Biological invaders are threat to human health: an overview. Ethol Ecol Evol 26:112–129
Milanesio D, Saccani M, Maggiora R, Laurino D, Porporato M (2016) Design of an harmonic radar for the tracking of the Asian yellow-legged hornet. Ecol Evol 6:2170–2178
Monceau K, Arca M, Leprêtre L, Mougel F, Bonnard O, Silvain JF et al (2013) 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
Monceau K, Bonnard O, Thiéry D (2014) Vespa velutina: a new invasive predator of honeybees in Europe. J Pest Sci 87:1–16
Monceau K, Arca M, Leprêtre L, Bonnard O, Arnold G, Thiéry D (2018) How Apis mellifera behaves with its invasive hornet predator Vespa velutina? J Insect Behav 31:1–11
Neumann P, Carreck NL (2010) Honey bee colony losses. J Apic Res 49:1–6
Pirk CWW, Human H, Crewe RM, van Engelsdorp D (2014) A survey of managed honey bee colony losses in the Republic of South Africa—2009 to 2011. J Apic Res 53:35–42
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353
Potts SG, Imperatriz-Fonseca V, Ngo HT, Aizen MA, Biesmeijer JC, Breeze TD et al (2016) Safeguarding pollinators and their values to human well-being. Nature 540:220–229
Prado A, Pioz M, Vidau C, Requier F, Brunet JL, Jury M et al (2019) Exposure to pollen-bound pesticide mixtures induces longer-lived but less efficient honey bees. Sci Total Environ 650:1250–1260
R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Requier F, Odoux JF, Henry M, Bretagnolle V (2017) The carry-over effects of pollen shortage decrease the survival of honeybee colonies in farmlands. J Appl Ecol 54:1161–1170
Requier F, Antúnez K, Morales CL, Aldea Sánchez P, Castilhos D, Garrido M et al (2018) Trends in beekeeping and honey bee colony losses in Latin America. J Apic Res 57:657–662
Requier F, Rome Q, Chiron G, Decante D, Marion S, Ménard M et al (2019) Predation of the invasive Asian hornet-induced risk on honeybee colony collapse affects foraging activity and survival probability of honey bees in Western Europe. J Pest Sci 92:567–578
Reynaud L, Guérin-Lassous I (2016) Design of a force-based controlled mobility on aerial vehicles for pest management. Ad Hoc Netw 53:41–52
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
Rodríguez-Flores MS, Seijo-Rodríguez A, Escuredo O, del Carmen Seijo-Coello M (2019) Spreading of Vespa velutina in northwestern Spain: influence of elevation and meteorological factors and effect of bait trapping on target and non-target living organisms. J Pest Sci 92:557–565
Rojas-Nossa SV, Novoa N, Serrano A, Calvino-Cancela M (2018) Performance of baited traps used as control tools for the invasive hornet Vespa velutina and their impact on non-target insects. Apidologie 49:872–885
Rome Q, Villemant C (2018) Le Frelon asiatique Vespa velutina. In: INPN—MNHN. http://frelonasiatique.mnhn.fr/home. Accessed Nov 2018
Rome Q, Perrard A, Muller F, Villemant C (2011) Monitoring and control modalities of a honeybee predator, the yellow-legged hornet Vespa velutina nigrithorax (Hymenoptera: Vespidae). Aliens Invasive Species 31:7–15
Schindler S, Staska B, Adam M, Rabitsch W, Essl F (2015) Alien species and public health impacts in Europe: a literature review. NeoBiota 27:1–23
Simone-Finstrom M, Borba RS, Wilson M, Spivak M (2017) Propolis counteracts some threats to honey bee health. Rev Insects 8:46
Sokal RR, Rohlf FJ (1994) Biometry: the principles and practice of statistics in biological research, 3rd revised edition. W.H. Freeman & Co Ltd, New York
Steinhauer N, Kulhanek K, Antúnez K, Human H, Chantawannakul P, Chauzat MP, vanEngelsdorp D (2018) Drivers of colony losses. Curr Opin Insect Sci 26:142–148
Turchi L, Derijard B (2018) Options for the biological and physical control of Vespa velutina nigrithorax (Hym.: Vespidae) in Europe: a review. J Appl Entomol 142:553–562
van der Zee R, Pisa P, Andonov S, Brodschneider R, Charrière JD, Chlebo R et al (2012) Managed honey bee colony losses in Canada, China, Europe, Israel and Turkey, for the winters of 2008–9 and 2009–10. J Apic Res 51:100–114
Wen P, Cheng YN, Dong SH, Wang ZW, Tan K, Nieh JC (2017) The sex pheromone of a globally invasive honey bee predator, the Asian eusocial hornet, Vespa velutina. Sci Rep 7:12956
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
Special thanks go to A. Lavignotte for conception of the Muzzle setup and constructive discussions. We are grateful to F. Nürnberger for his constructive comments at the first stages of the manuscript. We also thank F. Muller and the beekeepers for help in the field, especially S. Mignot-Gasparoux, A. Lavignotte, the M.J.C. Berlioz, A. Richard, O. Coulon, Y. Ducourt, S. Berthomé, B. Devaure, H. Marques de Brito, Association entre l’herbe et le vent, P. Nikiel, P. Fert, O. Bessonnet, J.F. Serra, M. Deux, L. Gouverneur, L. Jezequel, and Y. Le Dantec. Finally, we thank the four anonymous reviewers for their constructive comments on the manuscript.
This study was supported by grants from the European Community Program (797/2004) for French beekeeping (RISQAPI project), the French Ministry of Ecology and the French Ministry of Agriculture.
Conflict of interest
No conflict of interest was reported by the authors.
Human and animals rights
All applicable international, national and/or, institutional guidelines for the care and use of animals were followed.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Communicated by M. Traugott.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Requier, F., Rome, Q., Villemant, C. et al. A biodiversity-friendly method to mitigate the invasive Asian hornet’s impact on European honey bees. J Pest Sci 93, 1–9 (2020). https://doi.org/10.1007/s10340-019-01159-9
- Apis mellifera
- Biological invasion
- Control methods
- Predator–prey interaction
- Yellow-legged hornet