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Behavioral Responses of Honey Bees, Apis Cerana and Apis Mellifera , to Vespa Mandarinia Marking and Alarm Pheromones

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Behavioral Responses of Honey Bees, Apis Cerana and Apis Mellifera , to Vespa Mandarinia Marking and Alarm Pheromones See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/327870759 Behavioral responses of honey bees, Apis cerana and Apis mellifera , to Vespa mandarinia marking and alarm pheromones Article in Journal of Apicultural Research · September 2018 DOI: 10.1080/00218839.2018.1494917 CITATIONS READS 0 320 9 authors, including: Beverly McClenaghan Gard Otis Centre for Environmental Genomics Applications (CEGA) University of Guelph 9 PUBLICATIONS 39 CITATIONS 104 PUBLICATIONS 2,004 CITATIONS SEE PROFILE SEE PROFILE All content following this page was uploaded by Beverly McClenaghan on 05 October 2018. The user has requested enhancement of the downloaded file. Journal of Apicultural Research ISSN: 0021-8839 (Print) 2078-6913 (Online) Journal homepage: http://www.tandfonline.com/loi/tjar20 Behavioral responses of honey bees, Apis cerana and Apis mellifera, to Vespa mandarinia marking and alarm pheromones Beverly McClenaghan, Marcel Schlaf, Megan Geddes, Joshua Mazza, Grace Pitman, Kaileigh McCallum, Samuel Rawluk, Karen Hand & Gard W. Otis To cite this article: Beverly McClenaghan, Marcel Schlaf, Megan Geddes, Joshua Mazza, Grace Pitman, Kaileigh McCallum, Samuel Rawluk, Karen Hand & Gard W. Otis (2018): Behavioral responses of honey bees, Apiscerana and Apismellifera, to Vespamandarinia marking and alarm pheromones, Journal of Apicultural Research, DOI: 10.1080/00218839.2018.1494917 To link to this article: https://doi.org/10.1080/00218839.2018.1494917 View supplementary material Published online: 25 Sep 2018. Submit your article to this journal View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tjar20 Journal of Apicultural Research, 2018 https://doi.org/10.1080/00218839.2018.1494917 ORIGINAL RESEARCH ARTICLE Behavioral responses of honey bees, Apis cerana and Apis mellifera,toVespa mandarinia marking and alarm pheromones à Beverly McClenaghana , Marcel Schlafb, Megan Geddesa, Joshua Mazzaa, Grace Pitmana, Kaileigh McCalluma, Samuel Rawluka, Karen Handc and Gard W. Otisa aSchool of Environmental Sciences, University of Guelph, Guelph, Canada; bDepartment of Chemistry, University of Guelph, Guelph, Canada; cStrategic Solutions Group, Puslinch, Canada (Received 3 October 2017; accepted 24 May 2018) The giant hornet, Vespa mandarinia is a predator of honey bees throughout its range in eastern Asia. The hornets’ behaviors are coordinated through pheromones; a marking pheromone is used to mark honey bee nests as a food source, and an alarm pheromone, comprised of three chemical components of their venom, is released when a hornet is attacked by honey bees. The Asian honey bee Apis cerana evolved in sympatry with the giant hornet. In contrast, the European honey bee, Apis mellifera and V. mandarinia evolved in allopatry, although A. mellifera colonies have been intro- duced within the hornet’s range. We investigated the responses of these two honey bee species to the V. mandarinia marking pheromone, two alarm pheromone chemicals individually, and the three alarm pheromone chemicals together. We applied these substances above hive entrances and photographically monitored pre- and post-treatment numbers of bees on the exterior of the hive near the entrance. A. cerana colonies responded to the marking pheromone by quickly retreating into the hive, causing the numbers of bees near the hive entrance to decrease quickly. The bees responded to the other two alarm pheromone components and the 3-compound alarm pheromone treatment by exiting their hive and increasing their activity at the entrance. A. mellifera colonies did not respond to any of the hornet chemical treat- ments. The marked differences in responses of the two honey bee species suggest that Asian honey bees are able to alter their behavior in response to one of their major predators while honey bees that are not exposed to this preda- tor do not. Respuestas del comportamiento de las abejas melıferas, Apis cerana y Apis mellifera, a las feromonas de marcacion y de alarma de Vespa mandarinia El avispon gigante, Vespa mandarinia, es un depredador de las abejas melıferas en toda su area de distribucion en Asia oriental. El comportamiento de los avispones se coordina a traves de las feromonas: una feromona de marcacion se uti- liza para marcar los nidos de las abejas melıferas como fuente de alimento y una feromona de alarma, compuesta de tres componentes quımicos de su veneno, se libera cuando un avispon es atacado por las abejas melıferas. La abeja asia- tica, Apis cerana, evoluciono en simpatrıa con el avispon gigante. En contraste, la abeja europea Apis mellifera y V. man- darinia evolucionaron en alopatrıa, aunque se han introducido colonias de A. mellifera en el area de distribucion del avispon. Investigamos las respuestas de estas dos especies de abejas melıferas a la feromona de V. mandarinia, dos pro- ductos quımicos de feromonas de alarma individualmente y los tres productos quımicos de feromonas de alarma juntos. Aplicamos estas sustancias sobre las entradas de las colmenas y monitoreamos fotograficamente el numero de abejas antes y despues del tratamiento en el exterior de la colmena cerca de la entrada. Las colonias de A. cerana respon- dieron a la feromona de marcado retirandose rapidamente a la colmena, causando que el numero de abejas cerca de la entrada de la colmena disminuyera rapidamente. Las abejas respondieron a los otros dos componentes de la feromona de alarma y al tratamiento de feromonas de alarma de 3 compuestos saliendo de su colmena y aumentando su actividad en la entrada. Las colonias de A. mellifera no respondieron a ninguno de los tratamientos quımicos del avispon. Las marcadas diferencias en las respuestas de las dos especies de abejas melıferas sugieren que las abejas melıferas asiaticas son capaces de alterar su comportamiento en respuesta a uno de sus principales depredadores, mientras que las abejas melıferas que no estan expuestas a este depredador no lo hacen. Keywords: Alarm pheromone; Apis; chemical synthesis; coevolution; honey bee; kairomone; marking pheromone; Vespa Introduction Turillazzi, 2010). In addition to feeding on individual for- The giant hornet, Vespa mandarinia is a major honey agers as they return to their nests, the hornets also bee predator that occurs over much of eastern Asia launch mass attacks on entire bee colonies that are (Lien & Carpenter, 2002). These hornets live in large coordinated with pheromones (Ono, Igarashi, Ohno, & colonies with correspondingly large food demands. Sasaki, 1995). After locating a nest of bees, scout hor- Honey bees, with their large colonies, represent a food nets mark it with a pheromone produced by the van bonanza for hornets (Baracchi, Cusseau, Pradella, & der Vecht gland on the last abdominal sternite (Ono à Corresponding author. Email: [email protected] ß 2018 International Bee Research Association 2 B. McClenaghan et al. et al., 1995). Their nestmates, recruited to the vicinity their marking pheromone, 1-methylbutyl 3-methylbuta- of the nest, orient to the marking pheromone, locate noate (1-M-3-MB; Ono et al., 2003), on the exterior sur- the bee nest, and gradually increase in numbers (Abrol, face of the bees’ nest. It serves as a signal that enables 2013; Ono et al., 1995). If the hornets gain access to other members of the hornet colony to find the food the nest, the bees’ defenses become overwhelmed and (i.e., bees and their brood and honey; Abrol, 2013;Ono the bee colony is killed (A. mellifera; Matsuura & et al., 1995). Ono et al. (1995) demonstrated that A. Sakagami, 1973) or it absconds (A. cerana; Ono et al., cerana responds to the marking pheromone of V. mandar- 1995), in both cases leaving behind a large quantity of inia by increasing the number of bees just inside the hive brood and honey (0.25–0.75 kg for A. cerana; Fuchs & entrance. Additionally, when a V. mandarinia hornet is Tautz, 2011) that the hornets forage upon for several attacked or disturbed it releases an alarm pheromone days afterwards. blend consisting of three chemicals contained within its Apis cerana, the Asian honey bee, has evolved many venom: 2-pentanol (2-P), 3-methyl-1-butanol (3-M-1-B), remarkable defenses to several species of wasp preda- and 1-M-3-MB, the marking pheromone (Ono et al., tors. Bees at the nest entrance “shimmer” in unison in 2003). The hornets may release this alarm pheromone in response to the visual stimulus of a wasp, especially V. response to being heat-balled by honey bees. Additionally, 3-M-1-B is found in honey bee alarm phero- velutina and V. simillima (Fuchs & Tautz, 2011; Oldroyd & mones (Wang et al., 2016b;Wenetal.,2017). Wongsiri, 2006). Shimmering involves a coordinated Hornet pheromones may become enemy-avoidance rapid shaking of the bees’ abdomens that is repeated at kairomones (Ono et al. 2003; Ruther, Meiners, & Steidle, approximately one-second intervals (Tan, Wang, Chen, 2002) if detected and acted upon by the bees. In many Hu, & Oldroyd, 2013). This “Iseeyou” display informs predator-prey systems, prey species have evolved incoming forager bees of the presence of the wasp, and responses to pheromones of their predators. For may inform the wasp that it has been detected (Tan example, Daphnia, after detecting chemicals emitted by et al., 2012). In response to a wasp, some of the bees predatory midge larvae, move to greater depths and are emit vibrational “stop signals” that are tuned to the stimulated to grow antipredator “neckteeth” (Lampert, severity of the threat (i.e., the species of wasp; Tan Tollrian, & Stibor, 1994; Tollrian & Dodson, 1999). et al., 2016). Bees can detect the odor of live wasps Stingless bees, Trigona (Tetragonisca) angustula, detect cit- while foraging, and it reduces their ability to learn floral ral secreted by attacking Lestrimelitta limao bees and odors (Wang et al., 2016a). Furthermore, when V. man- respond by increasing the number of aerial defenders near darinia hornets arrive at a colony of A.
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