The interaction between a parasite and sub-optimal temperatures contributes to honey bee decline

Abstract

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.

The Beneficial Effect of Pollen on Varroa Infested Bees Depends on Its Influence on Behavioral Maturation Genes

“…In conclusion, we confirm that pollen has a beneficial effect on bees challenged with Varroa mite. Varroa infestation at the pupal stage influences the nutritional status of the honey bee ( 23 , 24 ); this compromises the natural maturation by influencing the relationship between two core physiological factors, Vitellogenin and JH ( 27 ). This leads to an accelerated transition to foraging and thus an anticipated death since this transition determines the overall lifespan of the bee ( 25 ).…”

“…Indeed, mite parasitized bees have a lower weight at the emergence, lower protein content and elevated free amino acids levels, suggesting that protein synthesis and growth are disrupted by Varroa ( 23 ). Varroa also influences the food intake of adult honey bees parasitized at the pupal stage (i.e., parasite induced anorexia), likely due to an interaction with the insulin pathway ( 24 ). Varroa can additionally modulate the honey bee's age-dependent behavioral maturation.…”

Field Application of an Innovative Approach to Assess Honeybee Health and Nutritional Status

“…This last finding suggests a reduced storage capacity and a reduced immune response in infested bees, mainly due to the lower concentration of vitellogenin, the most abundant protein in honeybee haemolymph, which is also involved in immunity. Accordingly, it has been reported that Varroa infestation affects the nutritional status of honeybees [43,44] and compromises their normal polyethism by altering the interaction between vitellogenin and juvenile hormone, two essential physiological components [45]. In addition, parasitisation reduces the life expectancy and impairs immune system function, increasing the risk of viral infections.…”

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“…In conclusion, we confirm that pollen has a beneficial effect on bees challenged with Varroa mite. Varroa infestation at the pupal stage influences the nutritional status of the honey bee (23,24); this compromises the natural maturation by influencing the relationship between two core physiological factors, Vitellogenin and JH (27). This leads to an accelerated transition to foraging and thus an anticipated death since this transition determines the overall lifespan of the bee (25).…”