Rapid behavioral maturation accelerates failure of stressed honey bee colonies

Abstract

Many complex factors have been linked to the recent marked increase in honey bee colony failure, including pests and pathogens, agrochemicals, and nutritional stressors. It remains unclear, however, why colonies frequently react to stressors by losing almost their entire adult bee population in a short time, resulting in a colony population collapse. Here we examine the social dynamics underlying such dramatic colony failure. Bees respond to many stressors by foraging earlier in life. We manipulated the demography of experimental colonies to induce precocious foraging in bees and used radio tag tracking to examine the consequences of precocious foraging for their performance. Precocious foragers completed far fewer foraging trips in their life, and had a higher risk of death in their first flights. We constructed a demographic model to explore how this individual reaction of bees to stress might impact colony performance. In the model, when forager death rates were chronically elevated, an increasingly younger forager force caused a positive feedback that dramatically accelerated terminal population decline in the colony. This resulted in a breakdown in division of labor and loss of the adult population, leaving only brood, food, and few adults in the hive. This study explains the social processes that drive rapid depopulation of a colony, and we explore possible strategies to prevent colony failure. Understanding the process of colony failure helps identify the most effective strategies to improve colony resilience.

Weight of evidence evaluation of a network of adverse outcome pathways linking activation of the nicotinic acetylcholine receptor in honey bees to colony death

“…For example, high Vtg levels suppress JH, delaying onset of foraging behavior, whereas high JH suppresses Vtg, causing a decrease in nursing behavior (Page et al, 2012). Studies exploring drivers of precocious foraging, using both treatment with a JH analog and social manipulation of a single-cohort colony of 1 d old bees in the absence of older foragers, induced precocious foraging, demonstrating that both hormonal and social interactions play a role (Chang et al, 2015;Perry et al, 2015). Active foragers produce a pheromone, ethyl oleate, which is transferred to the hive bees during trophallaxis or oral food exchange, delaying the rate at which bees transition to foraging.…”

“…Consequences of precocious foraging may include shorter worker lifespans, less efficient foraging due to maladapted flight muscles, and higher mortality due to inexperience of young foragers that may lead to weaker colonies (Perry et al, 2015;Vance et al, 2009). However, in addition to early onset of foraging, honey bee colonies have a repertoire of compensatory responses to overcome foraging deficiencies.…”

“…Colony population dynamics modeling has provided some valuable insights in this regard (Khoury et al, 2011;Perry et al, 2015;Bryden et al, 2013), but corresponding field studies testing model predictions are lacking. Therefore, although there is both strong biological plausibility and supporting empirical evidence for the KER linking abnormal foraging activity and behavior to abnormal role change within the caste, the WoE for the KER was designated 'moderate' due to the uncertainties associated with how survival strategies are selected and employed by the colony.…”

“…In addition to impacts on lifespan, studies evaluating performance of precociously-foraging bees have demonstrated poor hovering flight capacity, reduced flight span (distance and time), reduced number and duration of successful flights performed in the bee's lifetime, impaired olfactory reversal-learning, and a preference toward nectar (as opposed to pollen) foraging compared to bees that had completed a more normal, prolonged progression of behavioral development (Chang et al, 2015;Page et al, 2012;Perry et al, 2015). Bees that follow typical behavioral development proceed through dramatic physiological and biochemical changes (Vance et al, 2009).…”

“…A reduction in hive bees could also contribute to a weakened colony, as the brood cannot be adequately fed, and optimal rearing temperatures cannot be maintained (Perry et al, 2015). The number of hive bees available to care for developing brood is another factor that dictates whether larvae receive adequate nutrition.…”