Temporal changes in volatile profiles of Varroa destructor‐infested brood may trigger hygienic behavior in Apis mellifera

Abstract

Varroa destructor Anderson & Trueman (Acari: Varroidae) is one of the major contributors to the significant losses of western honey bee, Apis mellifera L. (Hymenoptera: Apidae), colonies worldwide. Hygienic behavior, in which individual workers detect, uncap, and remove unhealthy brood, is a type of social immunity that reduces pathogen and parasite loads in the colony. Previous evidence suggests that hygienic worker bees identify diseased brood through olfactory cues. The aims of the present work were (1) to study the hygienic behavior of worker bees toward V. destructor-infested cells at different stages of brood development, (2) to explore changes in brood volatile profiles associated with the progression of mite infestation, and (3) to analyze the role of specific volatile compounds in triggering the hygienic behavior. Results showed that the removal rate of infested brood changed along its development and the progression of mite reproduction. Two compounds, ethyl hexanoate and a-pinene, were present in volatile collections from mite-infested pupae but absent from uninfested pupae. Field bioassays showed that these volatiles are relevant to elicit the hygienic behavior. A third compound, b-ocimene, was present in infested and uninfested brood but its abundance pattern varied according to the infestation status throughout brood development. Specifically, for uninfested brood, the abundance of b-ocimene showed a reduction in black-eyed pupae, whereas for infested brood, its abundance decreased drastically in light-pink-eyed pupae and remained constant in blackeyed pupae. Our results revealed that olfactory signals associated with V. destructor infestation change as the reproductive cycle of V. destructor progresses inside the cell. These changes can be mimicked to some extent by adding specific volatile compounds to the cell to induce hygienic removal. These findings shed light on the chemical basis of hygienic behavior against V. destructor and could facilitate the development of improved hygienic selection tools to breed mite-resistant honey bee colonies.

Detailed chemical analysis of honey bee (Apis mellifera) worker brood volatile profile from egg to emergence

“…The hygienic behaviour is then triggered by the emission of phenethyl acetate, 2-phenylethanol, and benzyl alcohol [ 14 ]. A variant of hygienic behaviour, VSH ( Varroa Sensitive Hygiene ) behaviour, targets brood cells parasitized by the varroa mite and is triggered by compounds emitted by parasitized brood cells ((Z)-6-pentadecene, (Z)-10-tritriacontene, 6 VPS ( Varroa-Parasitization-Specific : tricosan-2-one, pentacosan-2-one, tetracosyl acetate, heptacosan-2-one, hexacosyl acetate and nonacosan-2-one), α-pinene and ethyl hexanoate) [ 15 – 18 ]. Stressed or diseased brood emit other compounds but potential behavioural responses of workers have not been assayed.…”

Honey bees (Apis mellifera) preselected for Varroa sensitive hygiene discriminate between live and dead Varroa destructor and inanimate objects

“…Cues from brood that trigger removal behaviour have been previously shown for factors such as brood damages caused by virulent virus infections vectored by mites, which trigger a a higher removal rate than uninfected brood 29 or chemical cues linking V. destructor and Deformed wing virus 43 . Different chemical cues originating from the brood or changed brood movements could also trigger removal behaviour 44 . Interestingly, we saw high recapping rates in all treatment groups indicating that a foreign object may trigger cell inspection, but upon viewing the cell contents, the workers recap the cell without removing the pupa.…”

Volatile Organic Compounds from Offspring of Stingless Bee Sacrificed in Hygienic Behavior Test

“…It relies on the detection of conspecific volatile organic compounds exhaled by unhealthy offspring, [5] thereby ensuring the health and survival of the colonies. [6][7][8] Although the wax cells of the brood comb are sealed, volatile organic compounds (VOCs) from dead or sick offspring are able to permeate the wax cell lid (operculum), thus dispersing into the environment, and being recognized by the olfactory chemoreception system of the brood cells workers bees. [8][9] To date, there is information that compounds such as cuticular hydrocarbons, terpenes and carboxylic acid mediate hygienic behavior of bees.…”

“…This behavior is linked to chemical signals that enable workers to promptly discern sick or deceased larvae and pupae among healthy offspring. It relies on the detection of conspecific volatile organic compounds exhaled by unhealthy offspring, [5] thereby ensuring the health and survival of the colonies [6–8] …”