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Olfactory Cues and Vespula Wasp Recognition by Honey Bee Guards Matthew Wood, Francis Ratnieks

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Olfactory Cues and Vespula Wasp Recognition by Honey Bee Guards Matthew Wood, Francis Ratnieks Olfactory cues and Vespula wasp recognition by honey bee guards Matthew Wood, Francis Ratnieks To cite this version: Matthew Wood, Francis Ratnieks. Olfactory cues and Vespula wasp recognition by honey bee guards. Apidologie, Springer Verlag, 2004, 35 (5), pp.461-468. 10.1051/apido:2004040. hal-00891847 HAL Id: hal-00891847 https://hal.archives-ouvertes.fr/hal-00891847 Submitted on 1 Jan 2004 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie 35 (2004) 461–468 © INRA/DIB-AGIB/ EDP Sciences, 2004 461 DOI: 10.1051/apido:2004040 Original article Olfactory cues and Vespula wasp recognition by honey bee guards Matthew J. WOOD*, Francis L.W. RATNIEKS Laboratory of Apiculture and Social Insects, Evolution and Behaviour Group, Department of Animal and Plant Sciences, The University of Sheffield, Sheffield S10 2TN, UK (Received 12 June 2003; revised 12 December 2003; accepted 29 December 2003) Abstract – Guard honey bees patrol the entrance to the nest and are thought to recognise nestmates by cuticular hydrocarbons. We aimed to determine whether honey bee guards can recognise predatory common wasps Vespula vulgaris and nestmates by olfactory cues. Odours were transferred between both honey bees and wasps and the responses of guards to controlled introductions monitored. When controlling for the species of introduced insect, the transferred odour was a predictor of aggressive attacks on both bees and wasps. Carriers of incongruous, allospecific odours were antennated by more guards than carriers of conspecific odours. Olfactory cues were, therefore, transferred and guards responded not only to odour per se but also odour incongruity. Olfactory cues may therefore be important in predator recognition by honey bee guards. Apis mellifera / guard behaviour / olfactory cue / predator recognition / common wasp Vespula vulgaris 1. INTRODUCTION and have been seen to enter hives to steal both brood and honey (N.S. Badcock, pers. comm.). Guard honey bees Apis mellifera (L.) patrol Allospecific intruders could be recognised the nest entrance and prevent entry by intruders by a variety of potential cues. Honey bees have (Butler and Free, 1952; Free, 1954). Conspe- well developed vision (Giurfa et al., 1995; cific intruders – bees from other colonies – steal Lunau and Maier, 1995) and can discriminate honey and this robbing can result in the total between complex textures and patterns loss of honey stores and the death of the plun- (Maddess et al., 1999). Honey bees also have dered colony (Winston, 1987). Many other spe- excellent olfaction (von Frisch 1967), which is cies also attack honey bee colonies. Hornets important in nestmate discrimination based on Vespa spp. are large enough to kill adult genotype-specific cues (Getz and Smith, 1983; honeybees and may enter the colony to carry off but see Downs and Ratnieks, 1999), comb wax developing larvae and pupae (Futuyama, 1986; hydrocarbons (Breed et al., 1988a; Breed et al., de Jong, 1990). Similarly, yellow-jacket wasps 1995) and floral oil odours (Bowden et al., Vespula spp. frequently kill adult honey bees at 1998; but see Downs et al., 2000; Downs et al., the entrance and also steal honey from the col- 2001). ony, a particular problem in late summer and Common wasps and honey bees are sympat- early autumn when the annual wasp colony ric in Europe (Spradbery, 1973; Winston, reaches its peak population (Spradbery, 1973; 1987). There exists, therefore, the potential for de Jong, 1990). In Sheffield, common wasps coevolution between predator and prey Vespula vulgaris (L.) can become abundant (Futuyama, 1986). In Japan, for example, the * Corresponding author: [email protected] Present address: Edward Grey Institute, Department of Zoology, University of Oxford, Oxford OX1 3PS, UK. 462 M.J. Wood, F.L.W. Ratnieks Asian honey bee Apis cerana japonica wasps. Returning honey bee foragers from each of (Radoszkowsky) recognises the aggregation the three discriminator colonies, and foraging wasps pheromone of a sympatric predator, the giant returning to laboratory study nests were collected. hornet Vespa mandarinia (Smith), forming a Captured insects were separated into odour recipi- ball around the intruder until the temperature ents and odour donors. Recipients were chilled in a refrigerator at 5 °C for 20 min to anaesthetise them becomes high enough to kill the hornet, but not and prevent fighting. Donors were killed by placing the bees. By contrast, European honeybees A. them in a freezer at –19 °C for 20 min and then kept mellifera introduced to Japan do not respond at 5 °C until used for odour transfers within one hour. (Matsuura and Sakagami, 1973; Ono et al., For each odour treatment group, three recipients 1995). were place in a sealed, sterile 20 mL plastic Univer- In view of the sympatry of honey bees and sal tube containing four donors and lightly shaken common wasps and the potential ubiquity of for five minutes. The recipients were then separated, cuticular hydrocarbons in insect recognition, placed in individual 2 mL Eppendorf tubes, and labelled such that introductions were blind with the aim of this study was to examine the impor- respect to odour treatment. Recipients were kept in tance of olfactory cues in the recognition of an ice-box to await introduction to a discriminator Vespula vulgaris (L.) by honey bee guards, a colony within 30 min. sympatric wasp predator. We transferred All honey bees were introduced to their own col- odours between honey bees and wasps and onies and, where appropriate, received nestmate observed their treatment by honey bee guards honey bee odour. This avoided the complicating at the colony entrance. While guards always factor of non-nestmate honey bee olfactory cues. behaved more aggressively to wasps than bees, Similarly, introductions to a discriminator colony they were more aggressive to bees with wasp involving wasps or wasp odour transfer were con- versus nestmate bee odour, and less aggressive ducted using wasps from the same nest. The four to wasps with nestmate bee versus wasp odour. treatment groups were arranged thus, shown as Incongruous, allospecific odours (i.e. bee with ‘recipient insect (odour transferred)’: bee (bee), bee wasp odour or wasp with bee odour) resulted (wasp), wasp (bee), wasp (wasp). in increased guard antennation. 2.3. Guarding assay 2. METHODS The behaviour of guard honey bees was observed using a standard bioassay adapted from Breed 2.1. Study species (1983) (see Downs and Ratnieks, 1999, 2000; Downs et al., 2000, 2001) in which the cooled intro- Three discriminator honey bee A. m. mellifera duced bees and wasps were allowed to warm up colonies were studied at the apiary of the Laboratory enough to walk but not to fly away. Using forceps, of Apiculture and Social Insects. Colonies were the introduced insect was placed on the centre of the situated 2 m apart to minimise drifting between entrance platform, taking care not to disturb the colonies, were queenright with approximately guard bees. To minimise the observer’s disturbance 20 000 workers and brood and were housed in stand- of the colony, each introduction was filmed (Sony ard two-deep Langstroth hive bodies. Each colony Hi8 digital camcorder). had a 3.5 cm diameter entrance hole in the lower box From video footage, each introduced insect was immediately above a 15 cm by 20 cm wooden plat- classified as rejected (when it was either bitten, held, form to facilitate both introductions and observa- carried away or stung by guards) or accepted (when tions. Introduced bees or wasps were placed on the no such aggressive approach was made for two min- centre of this platform to be contacted by guards utes following introduction). In addition, we also patrolling the platform and entrance. noted evictions – when the introduced insect was Nests of the common wasp V. vulgaris were physically removed from the colony entrance by collected during pest control visits to houses in guards and thrown from the platform. Eviction, Sheffield, and relocated to the laboratory where they therefore, is a more violent and aggressive sub-cat- were housed in 30 × 30 × 30 cm polystyrene boxes egory of rejection. At least five minutes was allowed with one 5 cm diameter entrance hole. between introductions, for the number of guards to return to normal. We also determined from the video 2.2. Odour transfer the number of approaches by guards to each intro- duced insect. These were classified as either aggres- The following procedure was used to transfer sive or non-aggressive (guard merely antennated the odour within and among groups of honey bees and introduced insect before moving away). Guard Olfactory cues and honey bee predator recognition 463 100% 100% 100 Rejected 80 Evicted 74% 59% 60 52% 40 20 11% 7% 0% Figure 1. The percentage of introduced 0 insects in each category rejected or evicted bee (bee) bee (wasp) wasp (bee) wasp (wasp) by honey bee guards is presented. Each Introduced insect (odour transferred) category, n = 27. approach behaviour was not considered if the insect wise elimination of non-significant variables. Guard was evicted or entered the colony in less than 10 s, approach behaviour was analysed using a backward due to the difficulties in observing guard behaviour stepwise general linear model. In the starting model, in such a short time Thereafter, the behavioural all predictor variables and their two-way interactions observations over a maximum of two minutes were were entered.
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