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

Abstract

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

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

“…Previously, it was shown that honeybees parasitized by Varroa mites carrying the virulent strain of the deformed wing virus (DWV) sustained higher virus titers and showed more severe morphological deformities than bees infected with mites harboring low virus titers and possibly nonvirulent DWV strains (Bowen-Walker et al 1999). In agreement with Bowen-Walker's study, Schöning and colleagues found that hygienic bees detected and preferentially removed the severely damaged broods, which had been artificially infested with virulent mites harboring the replicating DWV causing an overt or fatal form of infection in infested broods, than broods parasitized by less virulent mites which transmitted a covert form of DWV infection (Schöning et al 2012). These authors reported the expression of compounds such as 2-and 3-butanediol or 2-and 3-methylbutanoic acid in higher proportions in the volatile chemical profiles of broods carrying an overt DWV infection compared to the broods with covert DWV infection.…”

“…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). The authors also found that bees in their hygienic behavior assays detected and then preferentially removed the severely damaged brood infested with the virulent mites.…”

Changes in Infestation, Cell Cap Condition, and Reproductive Status of Varroa destructor (Mesostigmata: Varroidae) in Brood Exposed to Honey Bees with Varroa Sensitive Hygiene

“…Odors triggering hygienic removal of Varroa-infested brood have not been fully described, but odors related to stress of infested pupae, pathogens, and resultant diseases vectored to host pupae, or to the mites and their offspring have been suggested as probable cues (Boecking and Spivak 1999, Aumeier and Rosenkranz 2001, Salvy et al 2001, Martin et al 2002, Vandame et al 2002, Nazzi et al 2004, Schö ning et al 2012. The biased removal of fertile mites in this study suggests that some stimuli triggering VSH behavior are related to the presence of offspring within the brood cell.…”

Hygienic Behavior in Honey Bees (Hymenoptera: Apidae): Effects of Brood, Food, and Time of the Year

“…When sufÞcient workers in a colony perform hygienic behavior, it confers colonylevel resistance (WilsonÐRich et al 2009) against diseases that affect honey bee brood such as American foulbrood (Spivak andReuter 1998b, 2001), chalkbrood (Gilliam et al 1983, Spivak andReuter 1998a), and varroa mites (Spivak 1996(Spivak , 1998aRinderer et al 2010;Schö ning et al 2012), which breed in brood cells although the adult female mites are also phoretic on adult honey bees.…”