A semiochemical from brood cells infested by <i>Varroa destructor</i> triggers hygienic behaviour in <i>Apis mellifera</i>

Nazzi, Francesco; Vedova, Giorgio Della; D'Agaro, M.

doi:10.1051/apido:2003065

Cited by 61 publications

(68 citation statements)

References 11 publications

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“…It was suggested that reproduction of the parasitising mother mite in the capped cell influences the probability of detection and subsequent removal of infested brood (Harbo and Harris, 2005) but results of more recent studies do not support this notion Ibrahim et al, 2007). Moreover, studies on the source and nature of the cues used by adult worker bees to detect cells with parasitised brood yielded contradictory results (Aumeier and Rosenkranz, 2001;Martin et al, 2001;Nazzi et al, 2004). In summary, it is still controversially discussed (1) whether the bees recognise and remove mite-infested brood in general or only such brood conspicuously affected by mite parasitism (e.g.…”

Section: Discussionmentioning

confidence: 99%

Evidence for damage-dependent hygienic behaviour towards Varroa destructor-parasitised brood in the western honey bee, Apis mellifera

Schöning

Gisder

Geiselhardt

et al. 2012

Journal of Experimental Biology

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SUMMARYThe ectoparasitic mite Varroa destructor and honey bee pathogenic viruses have been implicated in the recent demise of honey bee colonies. Several studies have shown that the combination of V. destructor and deformed wing virus (DWV) poses an especially serious threat to honey bee health. Mites transmitting virulent forms of DWV may cause fatal DWV infections in the developing bee, while pupae parasitised by mites not inducing or activating overt DWV infections may develop normally. Adult bees respond to brood diseases by removing affected brood. This hygienic behaviour is an essential part of the beesʼ immune response repertoire and is also shown towards mite-parasitised brood. However, it is still unclear whether the bees react towards the mite in the brood cell or rather towards the damage done to the brood. We hypothesised that the extent of mite-associated damage rather than the mere presence of parasitising mites triggers hygienic behaviour. Hygienic behaviour assays performed with mites differing in their potential to transmit overt DWV infections revealed that brood parasitised by ʻvirulentʼ mites (i.e. mites with a high potential to induce fatal DWV infections in parasitised pupae) were removed significantly more often than brood parasitised by ʻless virulentʼ mites (i.e. mites with a very low potential to induce overt DWV infections) or non-parasitised brood. Chemical analyses of brood odour profiles suggested that the bees recognise severely affected brood by olfactory cues. Our results suggest that bees show selective, damage-dependent hygienic behaviour, which may be an economic way for colonies to cope with mite infestation. Supplementary material available online at

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Section: Discussionmentioning

confidence: 99%

Evidence for damage-dependent hygienic behaviour towards Varroa destructor-parasitised brood in the western honey bee, Apis mellifera

Schöning

Gisder

Geiselhardt

et al. 2012

Journal of Experimental Biology

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“…Cuticular hydrocarbons of pupae change in the presence of varroa mites, and these changes may signal ill health to hygienic bees (Salvy et al 2001, Martin et al 2002. Alternatively, behavioral stress responses by infested pupae or diseases vectored to them by mites may induce their hygienic removal (Boecking and Spivak 1999, Boot et al 1999, Vandame et al 2002, Nazzi et al 2004.…”

Section: Discussionmentioning

confidence: 99%

Honey Bees (Hymenoptera: Apidae) with the Trait of Varroa Sensitive Hygiene Remove Brood with All Reproductive Stages of Varroa Mites (Mesostigmata: Varroidae)

Harris

Danka

Villa

2010

Annals of the Entomological Society of America

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Varroa sensitive hygiene (VSH) is a trait of honey bees, Apis mellifera L. (Hymenoptera: Apidae), which supports resistance to Varroa destructor Anderson & Trueman. VSH is the hygienic removal of mite-infested pupa. Bees selectively bred for VSH produce colonies in which the fertility of mites decreases over time. In addition, mite fertility decreases after infested brood is exposed to VSH bees for 1 wk. The purpose of this study was to decide whether the reduction in mite fertility is caused by selective removal of mites that produce offspring. Initially, we monitored changes in a small patch of capped brood during exposure to VSH bees at 2-h intervals through 60 h, which provided a reference for the subsequent experiment. The first test showed that VSH bees uncapped, recapped, and began to remove many pupae in ≈2 h. The approach in the second experiment was to compare the percentage of fertile mites from brood exposed to VSH bees for a 3-h period to the percentage of fertile mites in brood that was protected from hygiene by a screen. There were no significant differences in fertility between mites on pupae that were being removed by the bees and mites on protected pupae. These results suggest that neither egg-laying by foundress mites nor mite offspring are the stimuli that trigger hygienic removal of mite-infested pupae by VSH bees. It may be that hygienic activities such as the uncapping of brood cells inhibits or disrupts reproduction by varroa mites.

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“…Previous studies confirmed that the profiles of volatile chemicals differ between the Varroainfested and noninfested worker brood. These profiles vary with respect to some of the low molecular weight compounds (Nazzi et al 2004;Schöning et al 2012). Schöning et al (2012) reported that brood parasitized by virulent Varroa mites (mites with a high chance of transmitting overt or fatal infections of deformed wing virus (DWV) in the infested brood) contain compounds like acetoin, 2-and 3-methylbutanoic acid in higher proportions in their volatile chemical profiles compared to the volatile profiles of broods infected with the less virulent mites (mites with low potential to vector an overt infection of DWV in parasitized brood).…”

Section: Discussionmentioning

confidence: 99%

“…Nazzi et al 2004 found multiple unsaturated hydrocarbons such as Z-(6) and Z-(7) isomers of pentadecenes and heptadecenes expressed in quantitatively higher amounts in the headspace volatile profiles of the intact Varroa -infested brood cells (Nazzi et al 2004). Healthy brood treated with pure Z-(6) pentadecene in a bioassay were removed significantly more than brood treated with the pure solvent.…”

Section: Introductionmentioning

confidence: 98%

Odor learning and odor discrimination of bees selected for enhanced hygienic behavior

2015

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-Odor learning and odor discrimination were tested in a line of honeybees selected for increased hygienic behavior (HB) against the Varroa mite and compared with control bees (CB). Olfactory proboscis extension conditioning was used to quantify learning, discrimination, and generalization. Retention tests were performed after 1 h and after 1 day to probe the stability of memory. HB and CB did not differ in their learning, discriminating, generalizing, and remembering behavior when pairs of floral odors and pairs of sting pheromone and floral odor were tested. Colony odor used as a background odor during learning and discrimination reduced the performance in both groups, possibly due to an adaptation effect. This effect was found to be particularly strong in CB. In both groups of test bees, no learning was found if wax caps of Varroa -infected and Varroa -uninfected cells were used as test stimuli, possibly because of the common odors. Volatile odors from Varroa -infected and noninfected pupae, however, were learned and discriminated indicating that the volatile signals are strong enough to override the similar cues of pupae. HB performed somewhat better than CB when infected pupae were used as the rewarded stimulus, but the difference between the two groups of test bees was small. Taken together, we conclude that odor learning and discrimination do not differ between HB and CB as long as general odors are involved, but when specific odor profiles from infected pupae are used as the reinforced signal, then a slightly better performance is seen in HB.Varroa destructor / hygienic behavior / PER conditioning / odor discrimination

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A semiochemical from brood cells infested by Varroa destructor triggers hygienic behaviour in Apis mellifera

Cited by 61 publications

References 11 publications

Evidence for damage-dependent hygienic behaviour towards Varroa destructor-parasitised brood in the western honey bee, Apis mellifera

Evidence for damage-dependent hygienic behaviour towards Varroa destructor-parasitised brood in the western honey bee, Apis mellifera

Honey Bees (Hymenoptera: Apidae) with the Trait of Varroa Sensitive Hygiene Remove Brood with All Reproductive Stages of Varroa Mites (Mesostigmata: Varroidae)

Odor learning and odor discrimination of bees selected for enhanced hygienic behavior

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