The association between the deformed wing virus and the parasitic mite Varroa destructor has been identified as a major cause of worldwide honeybee colony losses. The mite acts as a vector of the viral pathogen and can trigger its replication in infected bees. However, the mechanistic details underlying this tripartite interaction are still poorly defined, and, particularly, the causes of viral proliferation in mite-infested bees. Here, we develop and test a novel hypothesis that mite feeding destabilizes viral immune control through the removal of both virus and immune effectors, triggering uncontrolled viral replication. Our hypothesis is grounded on the predator–prey theory developed by Volterra, which predicts prey proliferation when both predators and preys are constantly removed from the system. Consistent with this hypothesis, we show that the experimental removal of increasing volumes of haemolymph from individual bees results in increasing viral densities. By contrast, we do not find consistent support for alternative proposed mechanisms of viral expansion via mite immune suppression or within-host viral evolution. Our results suggest that haemolymph removal plays an important role in the enhanced pathogen virulence observed in the presence of feeding Varroa mites. Overall, these results provide a new model for the mechanisms driving pathogen–parasite interactions in bees, which ultimately underpin honeybee health decline and colony losses.

The neonicotinoid Clothianidin has a negative impact on NF-κB signaling and on immune responses controlled by this transcription factor, which can boost the proliferation of honey bee parasites and pathogens. This effect has been well documented for the replication of deformed wing virus (DWV) induced by Clothianidin in honey bees bearing an asymptomatic infection. Here, we conduct infestation experiments of treated bees to show that the immune-suppression exerted by Clothianidin is associated with an enhanced fertility of the parasitic mite Varroa destructor, as a possible consequence of a higher feeding efficiency. A conceptual model is proposed to describe the synergistic interactions among different stress agents acting on honey bees.

Food shortage, along with biotic stressors, contributes to winter honey bee colony losses. In autumn, to support honey bee colonies and prepare them for the winter season, beekeepers can supply homemade syrups which could contain compounds with possible negative side effects. In this study, we investigated the toxicity of one of those compounds (e.g., hydroxymethylfurfural, HMF) at doses consistent with literature data both to healthy bees and bees challenged with their most important parasite (i.e., Varroa destructor ). To strengthen available data on HMF concentration in sugar syrups, we also investigated HMF formation in homemade 2:1 inverted sugar syrup, considering, in particular, the influence of temperature or boiling time on different homemade sugar syrups according to their acidity. Finally, we studied the effects of the acidity of sugar syrups on honeybee survival, and tested whether or not sucrose inversion through acidification is really necessary. We show that doses of HMF similar to those reported as sublethal in the literature appear to be non-toxic even to mite infested bees. However, the amount of HMF that can be found in homemade syrups, which increases with temperature and acidity, can be much higher and can cause significant bee mortality. Moreover, we highlighted the detrimental effect of syrups acidity on honeybee survival, suggesting that the addition of lemon or any other acidifying substance to invert the sucrose could be harmful and not necessary. Our results suggest a responsible approach to homemade colony nutrition. honey bee / hydroxymethylfurfural / nutrition / sugar syrup acidity

Honeybees use propolis collected from plants for coating the inner walls of their nest. This substance is also used as a natural antibiotic against microbial pathogens, similarly to many other animals exploiting natural products for self-medication. We carried out chemical analyses and laboratory bioassays to test if honeybees use propolis for social medication against their major ectoparasite: Varroa destructor . We found that propolis is applied to brood cells where it can affect the reproducing parasites, with a positive effect on honeybees and a potential impact on Varroa population. We conclude that propolis can be regarded as a natural pesticide used by the honeybee to limit a dangerous parasite. These findings significantly enlarge our understanding of behavioural immunity in animals and may have important implications for the management of the most important threat to honeybees worldwide.

Global insect decline and, in particular, honey bee colony losses are related to multiple stress factors, including landscape deterioration, pollution, parasites and climate change. However, the implications of the interaction among different stress factors for insect health are still poorly understood; in particular, little is known on how challenging environmental conditions can influence the impact of parasites. Here we exploited the honey bee as a model system to approach this problem and carried out extensive lab and field work aiming at assessing how suboptimal temperatures and parasitic challenges can alter the homeostatic balance of individual bees and the whole colony, leading to individual death and colony collapse. We found that mite infestation further than increasing the mortality of bees, induces an anorexia that in turn reduces the capacity of bees to thermoregulate, thus exposing them to the detrimental effect of lower temperatures. This, in turn, has dramatic implications for the colony as a whole. The results highlight the important role that abiotic factors can have in shaping the effect of parasitic challenges on honey bees. Furthermore, the multilevel and holistic approach adopted here can represent a useful template for similar studies on other insect species, which are particularly urgent in view of climate change and the continuous pressure of natural and exotic parasites on insect populations.