Defensive behaviour of Apis mellifera against Vespa velutina in France: Testing whether European honeybees can develop an effective collective defence against a new predator

Behavioural Processes

Volumn 106, Issue , 2014, Pages 122-129

  Arca, Mariangela ^a,b   Papachristoforou, Alexandros ^a,b,c,f   Mougel, Florence ^a,b   Rortais, Agnès ^a,b,g   Monceau, Karine ^d   Bonnard, Olivier ^d   Tardy, Pascal ^e   Thiéry, Denis ^d   Silvain, Jean François ^a   Arnold, Gérard ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^d BORDEAUX SCIENCES AGRO   (France)

^e UNIVERSITÉ BORDEAUX 1   (France)

^f France and University of Paris Sud   (France)

^g EUROPEAN FOOD SAFETY AUTHORITY   (Italy)

Author keywords

Apis mellifera; Defensive behaviour; Invasive species; Predation; Vespa velutina

Indexed keywords

COLONY FOUNDING; DEFENSE BEHAVIOR; HONEYBEE; INTERSPECIFIC COMPETITION; PREDATOR-PREY INTERACTION;

APIS MELLIFERA; ARTICLE; BALLING BEHAVIOR; BODY TEMPERATURE; DEFENSIVE BEHAVIOR; EUROPE; FRANCE; HONEY; LARVA; POLLEN; PREDATOR PREY INTERACTION; PUPA (LIFE CYCLE STAGE); QUALITATIVE ANALYSIS; SIMULATION; VESPA; VESPA VELUTINA; ANIMAL; BEE; INTRODUCED SPECIES; PHYSIOLOGY; PREDATION; SOCIAL BEHAVIOR; WASP;

FRANCE;

ANIMALS; BEES; FRANCE; INTRODUCED SPECIES; PREDATORY BEHAVIOR; SOCIAL BEHAVIOR; WASPS;

EID: 84902130412     PISSN: 03766357     EISSN: 18728308     Source Type: Journal    
DOI: 10.1016/j.beproc.2014.05.002     Document Type: Article

References (46)

1. Abrol D. Ecology, behaviour and management of social wasp, Vespa velutina Smith (Hymenoptera: Vespidae), attacking honeybee colonies. Kor. J. Apic. 1994, 9:5-10.
2. Abrol D. Defensive behaviour of Apis cerana F. against predatory wasps. J. Apic. Sci. 2006, 50:39-46.
3. Baracchi D., Cusseau G., Pradella D., Turillazzi S. Defence reactions of Apis mellifera ligustica against attacks from the European hornet Vespa crabro. Ethol. Ecol. Evol. 2010, 22:281-294.
4. Breed M.D.M., Guzmán-Novoa E., Hunt G.J. Defensive behavior of honey bees: organization, genetics, and comparisons with other bees. Annu. Rev. Entomol. 2004, 49:271-298.
5. Butler C.G. The World of the Honeybee 1954, Collins, London, 226.
6. Castro L., Pagola-Carte S. Vespa velutina Lepeletier, 1836 (Hymenoptera: Vespidae), recolectada en la Península Ibérica. Heteropterus Revista de Entomología 2010.
7. Collins A.M. Effect of age on the response to alarm pheromones by caged honey bees. Ann. Entomol. Soc. Am. 1980, 73:307-309.
8. Collins A.M., Rinderer T., Tucker K. Colony defense of two honeybee types and their hybrid. 1. Naturally mated queens. J. Apic Res. 1988, 27:137-140.
9. DeGrandi-Hoffman G., Collins A.M., Martin J.H., Schmidt J.O., Spangler H.G. Nest defence behavior in colonies from crosses between Africanized and European honey bees (Apis mellifera L.) (Hymenoptera: Apidae). J. Insect Behav. 1998, 11:37-45.
10. Demichelis S., Manimo A., Porporato M. Trovato il primo nido di Vespa velutina a Vallecrosia (IM). Communicato Stampa 2013, Universita Degli Studi di Torino, Turin, http://www.apilandia.it/capt/doc/Vespa%20velutina%202013.pdf (accessed 09.03.14).
11. Grosso-silva J.M., Maia M. Vespa velutina Lepeletier, 1836 (Hymenoptera, Vespidae), new species for Portugal. Eppo Bull. 2012, 1836:53-54.
12. Guzmán-Novoa E., Page R. Backrossing Africanized honey bee queens to European drones reduces colony defensive behavior. Ann. Entomol. Soc. Am. 1993, 86:352-355.
13. Hunt J.G., Amdam V.G., Schlipalius D., Emore C., Sardesai N., Williams E.C., Rueppell O., Guzman-Novoa E., Arechavaleta-Velasco M., Chandra S., Fondrk K.M., Beye M., Page E.R. Behavioral genomics of honeybee foraging and nest defence. Naturwissenschaften 2007, 94:247-267.
14. Kastberger G., Sharma D. The predator-prey interaction between blue-bearded bee eaters (Nyctyornis athertoni Jardine and Selby 1830) and giant honeybees (Apis dorsata Fabricius 1798). Apidologie 2000, 31:727-736.
15. Kastberger G., Schmelzer E., Kranner I. Social waves in giant honeybees repel hornets. PLoS ONE 2008, 3:e3141.
16. Kastberger G., Thenius R. Aggressive and docile colony defence patterns in Apis mellifera. A retreater-releaser concept. J. Insect Behav. 2009, 22:65-85.
17. Ken T., Radloff H.R.H.S.E., Hepburn H.R., Radloff S.E., Yusheng Y., Yiqiu L., Danyin Z., Neumann P. Heat-balling wasps by honeybees. Die Naturwissenschaften 2005, 92:492-495.
18. López S., González M., Goldarazena A. Vespa velutina Lepeletier, 1836 (Hymenoptera: Vespidae): first records in Iberian Peninsula. EPPO Bull. 2011.
19. Matsuura M., Yamane S. Biology of the Vespine Wasps 1990, Springer-Verlag, Berlin.
20. Mishra R., Kumar J., Gupta J. A new approach to the control of predatory wasps (Vespa sp) of the honey bee. Apis mellifera. Indian J. Apic. Res. 1989, 28:126-131.
21. Monceau K., Maher N., Bonnard O., Thiéry D.a. Predation dynamics study of the recently introduced honeybee killer Vespa velutina: learning from the enemy. Apidologie 2013, 44:209-221.
22. Monceau K., Arca M., Leprêtre L., Mougel F., Bonnard O., Silvain J.-F., Maher N., Arnold G., Thiéry D. Native prey and invasive predator patterns of foraging activity: the case of the yellow-legged hornet predation at European honeybee hives. PLoS ONE 2013, 8:e66492.
23. Monceau, K., Bonnard, O., Moreau, J., Thiéry, D. (in press). Spatial distribution of Vespa velutina individuals hunting at domestic honeybee hives: heterogeneity at a local scale. Insect Science, doi 10.1111/1744-7917.12090.
24. Monceau K., Bonnard O., Thiéry D. Vespa velutina: a new invasive predator of honeybees in Europe. J. Pest Sci. 2014, 87:1-16.
25. Moritz Robin F.A., Southwick Edward E., Breh M. A metabolic test for the quantitative analysis of alarm behavior of honeybees (Apis mellifera L.). J. Exp. Zool. 1985, 235:1-5.
26. Morse R. Honey Bee Pests, Predators, and Diseases 1990, Cornell University Press, Ithaca, NY, USA, 430.
27. Ono M., Okada I., Sasaki M. Heat production by balling in the Japanese honeybee, Apis cerana japonica as a defensive behavior against the hornet, Vespa simillima xanthoptera (Hymenoptera: Vespidae). Experientia 1987, 43:1031-1034.
28. Ono M., Igarashi T., Ohno E., Sasaki M. Unusual thermal defence by a honeybee against mass attack by hornets. Nature 1995, 377:334-336.
29. Papachristoforou A., Rortais A.s., Zafeiridou G., Theophilidis G., Garnery L., Thrasyvoulou A., Arnold G. Smothered to death: hornets asphyxiated by honeybees. Curr. Biol. 2007, 17:R795-R796.
30. Papachristoforou A., Sueur J., Rortais A., Angelopoulos S., Thrasyvoulou A., Arnold G. High frequency sounds produced by Cyprian honeybees Apis mellifera cypria when confronting their predator, the Oriental hornet Vespa orientalis. Apidologie 2008, 39:468-474.
31. Papachristoforou A., Rortais A., Sueur J., Arnold G. Attack or retreat: contrasted defensive tactics used by Cyprian honeybee colonies under attack from hornets. Behav. Process. 2011, 86:236-241.
32. Rome Q., Dambrine L., Onate C., Muller F., Villemant C., García-Pérez A.L., Maia M., Carvalho Esteves P., Bruneau E. Spread of the invasive hornet Vespa velutina Lepeletier, 1836, in Europe in 2012 (Hym., Vespidae). B. Soc. Entomol. Fr. 2013, 118:21-22.
33. Rortais A., Arnold G., Garnery L. Introgressions and structure of the genetic diversity of the black honeybee in France. Proceedings of the Second European Conference of Apidology Eurbee 2007, 59. Bee Research Institute Dol, Prague, Czech Republic.
34. R Development Core Team R: A Language and Environment for Statistical Computing 2010, R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org.
35. Rothenbuhler W. A technique for studying genetics of colony behavior in honey bees. Am. Bee J. 1960, 100:176-198.
36. Ruttner F. Biogeography and Taxonomy of Honeybees 1988, Springer, Berlin, Germany, 284.
37. Sakagami S., Akahira Y. Studies on the Japanese honeybee, Apis cerana cerana Fabricisu. VIII. Two opposing adaptations in the post-stinging behavior of honeybees. Evolution 1960, 14:29-40.
38. Shah F., Shah T. Vespa velutina, a serious pest of honey bees in Kashmir. Bee World 1991, 72:161-164.
39. Stort A. Genetic study of aggressiveness of two subspecies of Apis mellifera in Brazil. I. Some tests to measure aggressiveness. J. Apic. Res. 1974, 13:33-38.
40. Sugahara M., Sakamoto F. Heat and carbon dioxide generated by honeybees jointly act to kill hornets. Naturwissenschaften 2009, 96:1133-1136.
41. Sugahara M., Nishimura Y., Sakamoto F. Differences in heat sensitivity between Japanese honeybees and hornets under high carbon dioxide and humidity conditions inside bee balls. Zool. Sci. 2012, 29:30-36.
42. Tan K., Radloff S., Li J.J., Hepburn H. Bee-hawking by the wasp, Vespa velutina, on the honeybees Apis cerana and A. mellifera. Naturwissenschaften 2007, 94:469-472.
43. Tan K., Wang Z., Li H., Yang S.H., Kastberger Z., Oldroyd G.B.P. An "I see you" prey-predator signal between the Asian honeybee, Apis cerana, and the hornet, Vespa velutina. Anim. Behav. 2012, 83:879-882.
44. Tan K., Wang Z., Chen W., Hu Z., Oldroyd B.P. The 'I see you' prey-predator signal of Apis cerana is innate. Naturwissenschaften 2013, 100:245-248.
45. Ugajin A., Kiya T., Kunieda T., Ono Masato, Yoshida T., Kubo T. Detection of neural activity in the brains of Japanese honeybee workers during the formation of a "hot defensive bee ball". PLoS ONE 2012, 7:e32902.
46. Villemant C., Haxaire J., Streito J. Premier bilan de l'invasion de Vespa velutina Lepeletier en France (Hymenoptera, Vespidae). B. Soc. Entomol. Fr. 2006, 111:535.