The effects of age and behavioral development on honey bee (Apis mellifera) flight performance

Abstract

SUMMARYA critical but seldom-studied component of life history theory is how behavior and age affect whole-organism performance. To address this issue we compared the flight performance of honey bees (whose behavioral development and age can be assessed independently via simple manipulations of colony demographics) between distinct behavioral castes (in-hive nurse bees vs outof-hive foragers) and across lifespan. Variable-density gases and high-speed video were used to determine the maximum hovering flight capacity and wing kinematics of age-matched nurse bees and foragers sampled from a single-cohort colony over a period of 34 days. The transition from hive work to foraging was accompanied by a 42% decrease in body mass and a proportional increase in flight capacity (defined as the minimum gas density allowing hovering flight). The lower flight capacity of hive bees was primarily due to the fact that in air they were functioning at a near-maximal wing angular velocity due to their high body masses. Foragers were lighter and when hovering in air required a much lower wing angular velocity, which they were able to increase by 32% during maximal flight performance. Flight performance of hive bees was independent of age, but in foragers the maximal wingbeat frequency and maximal average angular velocity were lowest in precocious (7-14 day old) foragers, highest in normal-aged (15-28 day old) foragers and intermediate in foragers older than 29 days. This pattern coincides with previously described age-dependent biochemical and metabolic properties of honey bee flight muscle.

Changes in mitochondrial energy utilization in young and old worker honeybees (Apis mellifera)

“…The decline in mitochondrial energy utilization in the trophocytes and fat cells of workers most likely reflect the accumulation of oxidative damages. This hypothesis is consistent with previous studies, showing that flight behavior accelerated oxidative damages in house flies (Musca domestica) (Vance et al 2009). Conversely, stopping flight decreases oxidative damages and increases longevity (Yan and Sohal 2000).…”

“…Conversely, stopping flight decreases oxidative damages and increases longevity (Yan and Sohal 2000). In addition, honeybee foragers have higher flight metabolic rate in flight muscles and result in 43 % body mass loss compared to hive bees (Vance et al 2009;Schippers et al 2010). Likewise, orchid bee foragers also have higher flight metabolic rate in flight muscles (Suarez et al 2005).…”

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

“…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.…”

“…The unique adaptations observed in foraging bees, including, for example, decreased body mass, increased 10A troponin T isoforms (important muscle structural component), and increased metabolic flux capacity in the glycolytic pathway, could be targeted in future research comparing precociously foraging bees to normally developed foragers (Vance et al, 2009;Schippers et al, 2010;Schippers et al, 2006). These comparisons would provide a more thorough understanding of whether the expedited behavioral transition causes the poor flight performance and shortened lifespan observed in precocious foragers.…”

“…Bees that follow typical behavioral development proceed through dramatic physiological and biochemical changes (Vance et al, 2009). For example, accompanying the transition to foraging, bees undergo a 42% reduction in body mass, particularly in abdominal tissue (Vance et al, 2009).…”