How stressors disrupt honey bee biological traits and overwintering mechanisms

Abstract

High winter mortality of honey bees (Apis mellifera) has been observed in temperate regions over the past 30 years. Several biotic and abiotic stressors associated with winter colony losses have been identified, but the mechanisms and interactions underlying their effects remain unclear. We reviewed the effects of stressors on key overwintering biological traits, distinguishing between individual and colony traits. We found that disturbances at the level of individual traits can be amplified when transmitted to colony traits. By analyzing these cascading effects, we propose a concept of a feedback loop mechanism of winter mortality. We found that population size, social thermoregulation and honey reserve are integrative traits and can predict overwintering failure. Furthermore, we identified social thermoregulation as a good candidate for an early warning indicator. We therefore discuss existing tools for monitoring hive temperature to help mitigate the current high winter mortality of honey bees and support the sustainability of beekeeping.

Keywords: Apis mellifera; Feedback loop mechanism; Honey bee; Stressors; Winter ecology; Winter mortality.

Graphical abstract

Fig. 1

Overwintering of honey bees. Evolution of colony component individuals, population size [56], and cluster size [54] depending on time and external temperature. Winter bees (in blue) emerge at the end of autumn and survive until early spring to restart the colony. They differ from summer bees (in orange) in physiology, morphology, and lifespan (average 130 days against 30 days for summer bees). When the temperature drops below 18 °C, they perform social thermoregulation by forming a cluster in the hive. The mantle of the cluster (10–15 °C) is shown in yellow, the core (18–29 °C) in orange, and the center (27–35 °C) in red. The energy needed for this behavior is obtained by consuming the honey reserves made during the year. In spring, the surviving winter bees forage and rear the new summer bee brood. (

Fig. 2

Causal links between key biological traits in honey bee colonies undergoing overwintering stress. The width of the links and the size of the biological traits are proportional to the number of studies concerned. We show horizontal arrows indicating the direction of reading of causal links using the package networkD3 in R [149]. The position of the traits is determined by calculating the number of causal effects of which it is the precursor relative to the number of causal effects it has received.

Fig. 3

Concept of the feedback loop mechanism of winter colony mortality in honey bees. The premature mortality of winter bees reduces the population size, negatively affecting the size and cohesion of the cluster. The distorted bee cluster (e.g., a misshaped cluster and/or loss of heat per bee) affects social thermoregulation, resulting in over-consumption of honey reserves. Starvation due to decreased honey reserves weakens winter bees. Social thermoregulation is a good candidate as early warning indicator of winter colony mortality, as it is an integrative trait that can be accurately monitored by in-hive temperature sensors.