Varroa destructor is an ectoparasitic pest of honeybees, and a threat to the survival of the apiculture industry. Several studies have shown that unlike European honeybees, African honeybee populations appear to be minimally affected when attacked by this mite. However, little is known about the underlying drivers contributing to survival of African honeybee populations against the mite. We hypothesized that resistant behavioral defenses are responsible for the survival of African honeybees against the ectoparasite. We tested this hypothesis by comparing grooming and hygienic behaviors in the African savannah honeybee Apis mellifera scutellata in Kenya and A. mellifera hybrids of European origin in Florida, USA against the mite. Grooming behavior was assessed by determining adult mite infestation levels, daily mite fall per colony and percentage mite damage (as an indicator of adult grooming rate), while hygienic behavior was assessed by determining the brood removal rate after freeze killing a section of the brood. Our results identified two additional undescribed damaged mite categories along with the six previously known damage categories associated with the grooming behavior of both honeybee subspecies. Adult mite infestation level was approximately three-fold higher in A. mellifera hybrids of European origin than in A. m. scutellata, however, brood removal rate, adult grooming rate and daily natural mite fall were similar in both honeybee subspecies. Unlike A. mellifera hybrids of European origin, adult grooming rate and brood removal rate did not correlate with mite infestation levels on adult worker honeybee of A. m. scutellata though they were more aggressive towards the mites than their European counterparts. Our results provide valuable insights into the tolerance mechanisms that contribute to the survival of A. m. scutellata against the mite.

Although Varroa destructor is the most serious ecto-parasite to the honeybee, Apis mellifera L., some honeybee populations such as Apis mellifera scutellata in Kenya can survive mite infestations without treatment. Previously, we reported that grooming behaviour could be a potential tolerant mechanism expressed by this honeybee subspecies towards mite infestation. However, both hygienic and grooming behaviours could not explain the lower mite-infestation levels recorded in these colonies. Here, we investigated the involvement of other potential resistant mechanisms including suppression of mite reproduction in worker brood cells of A. m. scutellata to explain the low mite numbers in their colonies. High infertility rates (26-27%) and percentages of unmated female offspring (39-58%) as well as low fecundity (1.7-2.2, average offspring produced) were identified as key parameters that seem to interact with one another during different seasons to suppress mite reproduction in A. m. scutellata colonies. We also identified offspring mortality in both sexes and absence of male offspring as key factors accounting for the low numbers of mated daughter mites produced in A. m. scutellata colonies. These results suggest that reduced mite reproductive success could explain the slow mite population growth in A. m. scutellata colonies.

Olfaction as well as gustation, are essential for animal survival, allowing behavioral modulation according to environmental input. We focused our study on an obligate ecto-parasitic mite of honey bees, the Varroa destructor Anderson and Trueman (Parasitiformes, Mesostigmata, Varroidae). By mechanically blocking the main olfactory organ on Varroa forelegs by varnishing with nail polish, we were able to show that other sensory organs cannot significantly compensate chemosensory abilities required for mite’s host selection, identification as well as reproduction. In fact, we found that mites with blocked forelegs had a significantly lower ability to reach a host bee than those with varnished idiosoma and unvarnished control. Furthermore, fewer foreleg blocked mites were feeding on the nurse bees and their reproduction in the brood cells was significantly impaired. The inhibition of reproduction was also reflected in altered expression levels of vitellogenin and vitellogenin receptor genes in foreleg-blocked mites.