Mite not make it home: Tracheal mites reduce the safety margin for oxygen delivery of flying honeybees

Many physiological systems appear to have safety margins, with excess capacity relative to normal functional needs, but the significance of such excess capacity remains controversial. In this study, we investigate the effects of parasitic tracheal mites (Acarapis woodi) on the safety margin for oxygen delivery and flight performance of honeybees. Tracheal mites did not affect the flight metabolic rate of honeybees in normoxic (21% oxygen) or hyperoxic (40% oxygen) air, but did reduce their metabolic rate relative to uninfected bees when flying in hypoxic air (5 or 10% oxygen), demonstrating that mites reduced the safety margin for tracheal oxygen delivery. The negative effects of mites on flight metabolic rate in hypoxic atmospheres were graded with the number of mites per trachea. For example, in 10% oxygen atmospheres, flight metabolic rate was reduced by 20% by moderate mite infection and by 40% by severe mite infection. Thus, the safety margin for oxygen delivery in honeybees allows them to retain normal flight metabolic rate and behavior despite tracheal mite infection under most conditions. However, the reduction in tracheal gas-exchange capacity may constrain activities requiring the highest metabolic rates, such as flying in cool weather. In support of this hypothesis, bees that were unable to return to the hive during late-winter flights showed significantly higher levels of mite infection than bees that returned safely.