Abstract
The Asian hornet (Vespa velutina) is a keen predator of honeybees and other insects. Its success as invasive species threatens the stability of ecosystem services provided by them, such as pollination of wild plants and crops. In this study we analyse their impact as hunters of flower visitors on plant pollination, by studying the hunting behaviour of V. velutina in flower surroundings, the effect of V. velutina hunting on the floral visiting behaviour by insects and its impact on the amount of conspecific pollen deposited on the stigmas of Mentha suaveolens, a native and common herb to southern and western Europe. We made observations and video-recordings in blooming patches with and without the presence of V. velutina and quantified the deposition of conspecific pollen on stigmas in those same patches. Asian hornets were frequent and successful hunters of flower visitors of Mentha suaveolens, inducing changes in the foraging behaviour of several groups of pollinators. The patch visitation rate of European honeybees (Apis mellifera), the flower visitation rate of small hymenopterans and the flower visitation time of bumblebees (Bombus sp.) and syrphids was significantly reduced in patches with presence of the predator. As a consequence, the quantity of conspecific pollen on stigmas of the studied native plant decreased in patches with V. velutina. In this study we demonstrate the negative impact of the invasive hornet V. velutina on pollination services in invaded areas as a consequence of their hunting of pollinators in flower patches.
This is a preview of subscription content, access via your institution.


References
Abbott KR (2006) Bumblebees avoid flowers containing evidence of past predation events. Can J Zool 84:1240–1247
Abbott KR, Dukas R (2009) Honeybees consider flower danger in their waggle dance. Anim Behav 78:633–635
Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS biol 6:e31
Arca M, Papachristoforou A, Mougel F et al (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
Barbosa P, Castellanos I (2005) Ecology of predator-prey interactions. Oxford University Press, Oxford
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Beggs JR, Brockerhoff EG, Corley JC et al (2011) Ecological effects and management of invasive alien Vespidae. Biocontrol 56:505–526
Brechbühl R, Kropf C, Bacher S (2010) Impact of flower-dwelling crab spiders on plant-pollinator mutualisms. Basic Appl Ecol 11:76–82
Budge GE, Hodgetts J, Jones EP et al (2017) The invasion, provenance and diversity of Vespa velutina Lepeletier (Hymenoptera: Vespidae) in Great Britain. PLoS ONE 12:e0185172
Carvalheiro LG, Kunin WE, Keil P et al (2013) Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol Lett 16:870–878
Choi MB, Martin SJ, Lee JW (2012) Distribution, spread, and impact of the invasive hornet Vespa velutina in South Korea. J Asia Pac Entomol 15:473–477
Cini A, Cappa F, Petrocelli I, Pepiciello I, Bortolotti L, Cervo R (2018) Competition between the native and the introduced hornets Vespa crabro and Vespa velutina: a comparison of potentially relevant life-history traits. Ecol Entomol 43:351–362
De Jong D (1990) Insects: Hymenoptera (ants, wasps, and bees). In: Morse RA, Nowogrodzki R (eds) Honey bee pests, predators, and diseases. Cornell University Press, Ithaca, pp 135–155
Dukas R (2005) Bumble bee predators reduce pollinator density and plant fitness. Ecology 86:1401–1406
Elliott NB, Elliott WM (1994) Recognition and avoidance of the predator Phymata americana Melin on Solidago odora Ait. by late season floral visitors. Am Midl Nat 131:378–380
EU Regulation 1143/2014. https://ec.europa.eu/environment/nature/invasivealien/list/index_en.htm
Fox J, Friendly M, Weisberg S (2013) Hypothesis tests for multivariate linear models using the car package. R J 5:39–52
Haxaire J, Bouguet J-P, Tamisier J-P (2006) Vespa velutina Lepeletier, 1836, une redoutable nouveauté pour la faune de France (Hym, Vespidae). Bull Soc Entomol Fr 111:194
Holm S (1979) A simple sequential rejective multiple test procedure. Scan J Stat 6:65–70
INPN (Inventaire National du Patrimoine Naturel) (2018) Le Frelon asiatique Vespa velutina. https://frelonasiatique.mnhn.fr/home/. Accessed 27 June 2019.
Jeanne R (1980) Evolution of social behaviour in the Vespidae. Ann Rev Entomol 25:371–396
Jones EI, Dornhaus A (2011) Predation risk makes bees reject rewarding flowers and reduce foraging activity. Behav Ecol Sociobiol 65:1505–1511
Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Boulder
Korner-Nievergelt F, Roth T, von Felten S et al (2015) Blmeco: data files and functions accompanying the book “Bayesian Data Analysis in Ecology Using R, BUGS and Stan”. Elsevier, New York
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 689:709–715
Llandres AL, Gonzálvez FG, Rodríguez-Gironés MA (2013) Social but not solitary bees reject dangerous flowers where a conspecific has recently been attacked. Anim Behav 85:97–102
Matsuura M, Yamane S (1990) Biology of vespine wasps. Springer-Verlag, Berlin
Monceau K, Arca M, Leprêtre L 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, Maher N, Bonnard O, Thiéry D (2015) Evaluation of competition between a native and an invasive hornet species: do seasonal phenologies overlap? Bull Entomol Res 105:462–469
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
Muñoz AA, Arroyo MT (2004) Negative impacts of a vertebrate predator on insect pollinator visitation and seed output in Chuquiraga oppositifolia, a high Andean shrub. Oecologia 138:66–73
Nieh JC (2010) A negative feedback signal that is triggered by peril curbs honey bee recruitment. Curr Biol 20:310–315
Ohashi K, Yahara T (2001) Behavioral responses of pollinators to variation in floral display size and their influences on the evolution of floral traits. In: Chittka L, Thomson J (eds) Cognitive ecology of pollination. Cambridge University Press, Cambridge, pp 274–296
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326
Perrard A, Haxaire J, Rortais A, Villemant C (2009) Observations on the colony activity of the Asian hornet Vespa velutina Lepeletier 1836 (Hymenoptera: Vespidae: Vespinae) in France. Ann Soc Entomol Fr 45:119–127
Poidatz J, Monceau K, Bonnard O, Thiéry D (2018) Activity rhythm and action range of workers of the invasive hornet predator of honeybees Vespa velutina, measured by radio frequency identification tags. Ecol Evol 8:7588–7598
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
Pyšek P, Jarošík V, Hulme PE et al (2012) A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species' traits and environment. Glob Chang Biol 18:1725–1737
Rader R, Bartomeus I, Garibaldi LA et al (2016) Non-bee insects are important contributors to global crop pollination. Proc Natl Acad Sci 113:146–151
Requier F, Rome Q, Chiron G et al (2019) Predation of the invasive Asian hornet affects foraging activity and survival probability of honey bees in Western Europe. J Pest Sci 92:567–578
Richter MR (2000) Social wasp (Hymenoptera: Vespidae) foraging behavior. Annu Rev Entomol 45:121–150
Rojas-Nossa SV, Novoa N, Serrano A, Calviño-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, Muller FJ, Touret-Alby A, Darrouzet E, Perrard A, Villemant C (2015) Caste differentiation and seasonal changes in Vespa velutina (Hym: Vespidae) colonies in its introduced range. J Appl Entomol 139:771–782
Romero GQ, Koricheva J (2011) Contrasting cascade effects of carnivores on plant fitness: a meta-analysis. J Anim Ecol 80:696–704
Romero GQ, Antiqueira PA, Koricheva J (2011) A meta-analysis of predation risk effects on pollinator behaviour. PLoS ONE 6:e20689
Russo L, Memmott J, Montoya D, Shea K, Buckley YM (2014) Patterns of introduced species interactions affect multiple aspects of network structure in plant–pollinator communities. Ecology 95:2953–2963
Schweiger O, Biesmeijer JC, Bommarco R et al (2010) Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination. Biol Rev 85:777–795
Suttle KB (2003) Pollinators as mediators of top-down effects on plants. Ecol Lett 6:688–694
Tan K, Hu Z, Chen W, Wang Z, Wang Y, Nieh JC (2013) Fearful foragers: honey bees tune colony and individual foraging to multi-predator presence and food quality. PLoS ONE 8:e75841
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
Tan K, Radloff SE, Li JJ et al (2007) Bee-hawking by the wasp, Vespa velutina, on the honeybees Apis cerana and A. mellifera. Naturwissenschaften 94:469–472
Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216
Ueno T (2014) Establishment of the invasive hornet Vespa velutina (Hymenoptera : Vespidae) in Japan. Int J Chem Environ Biol Sci 2:220–222
Vanbergen AJ, Espíndola A, Aizen MA (2018) Risks to pollinators and pollination from invasive alien species. Nat Ecol Evol 2:16
Villemant C, Muller F, Haubois S, Perrard A, Darrouzet E, Rome Q (2011) Bilan des travaux (MNHN et IRBI) sur l’invasion en France de Vespa velutina, le frelon asiatique prédateur d’abeilles. In: Barbançon J-M, L’Hostis M (eds) Proc J Scient Apicole. ONIRIS-FNOSAD, Nantes, pp 3–12
Wilson EE, Mullen LM, Holway DA (2009) Life history plasticity magnifies the ecological effects of a social wasp invasion. Proc Nat Acad Sci 106:12809–12813
Xunta de Galicia (2016) Protocolo de vixilancia e control fronte a avespa asiática (Vespa velutina). https://boqueixon.gal/contido/subidas/2017/03/Protocolo_vixilancia_e_control_vespa_velutina_Galicia_Rev_2016.pdf. Accessed 09 May 2020
Acknowledgements
This work was supported by Xunta de Galicia through the collaboration agreement between Consellería de Medio Ambiente e Ordenación do Territorio, University of Vigo and University of Santiago de Compostela for the Study of behaviour, habitat and impact on ecosystems of Vespa velutina, and improvement of control methods (2017). L. O. Aguado helped with identification of insects. We also thank two anonymous reviewers for the valuable comments on an earlier draft of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Rojas-Nossa, S.V., Calviño-Cancela, M. The invasive hornet Vespa velutina affects pollination of a wild plant through changes in abundance and behaviour of floral visitors. Biol Invasions 22, 2609–2618 (2020). https://doi.org/10.1007/s10530-020-02275-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-020-02275-9