Flight restriction prevents associative learning deficits but not changes in brain protein-adduct formation during honeybee ageing

Abstract

SUMMARYHoneybees (Apis mellifera) senesce within 2weeks after they discontinue nest tasks in favour of foraging. Foraging involves metabolically demanding flight, which in houseflies (Musca domestica) and fruit flies (Drosophila melanogaster) is associated with markers of ageing such as increased mortality and accumulation of oxidative damage. The role of flight in honeybee ageing is incompletely understood. We assessed relationships between honeybee flight activity and ageing by simulating rain that confined foragers to their colonies most of the day. After 15days on average, flight-restricted foragers were compared with bees with normal (free) flight: one group that foraged for ~15days and two additional control groups, for flight duration and chronological age, that foraged for ~5days. Free flight over 15days on average resulted in impaired associative learning ability. In contrast, flight-restricted foragers did as well in learning as bees that foraged for 5days on average. This negative effect of flight activity was not influenced by chronological age or gustatory responsiveness, a measure of the bees' motivation to learn. Contrasting their intact learning ability, flight-restricted bees accrued the most oxidative brain damage as indicated by malondialdehyde protein adduct levels in crude cytosolic fractions. Concentrations of mono-and poly-ubiquitinated brain proteins were equal between the groups, whereas differences in total protein amounts suggested changes in brain protein metabolism connected to forager age, but not flight. We propose that intense flight is causal to brain deficits in aged bees, and that oxidative protein damage is unlikely to be the underlying mechanism.Supplementary material available online at

Aging and its modulation in a long-lived worker caste of the honey bee

“…Rather, declined learning performance could be due to changes in the central brain, as shown earlier for synaptic protein levels (Wolschin et al, 2009). Further, the performance decline 14days after foraging was initiated in the flight room (Fig.2) is in accord with previous work on bees under natural summer conditions (Behrends et al, 2007;Scheiner and Amdam, 2009;Tolfsen et al, 2011). Significant decline after approximately 2weeks of foraging both in summer and in post-winter bees makes it unlikely that a recent history of being in a winter state confers additional survival benefits over summer workers.…”

“…between comparably young summer and old post-winter foragers. However, the time point at which senescence becomes detectable after foraging had been initiated is not static, but can be delayed by restricting the daily foraging time (Tolfsen et al, 2011). It is therefore plausible that lowered flight activity can partly explain the lack of behavioral senescence in foragers from post-winter colonies that were made broodless (Fig.3).…”

“…Further studies focused on systems including metabolism, as well as insulin signaling, and identified age-related abundance changes for molecules involved in neuronal signaling and growth (Ament et al, 2008;Roberts and Elekonich, 2005;Wolschin and Amdam, 2007;Wolschin et al, 2009). In contrast, little is known about biomarkers of cellular senescence, which often can provide a more direct indication of deterioration than protein expression (Hsieh and Hsu, 2011;Seehuus et al, 2006a;Tolfsen et al, 2011).…”

“…The behavioral decline of foragers is paralleled by a sharp mortality increase after approximately 10days of foraging (Dukas, 2008). Experimental restriction of daily flight periods further suggests that metabolically demanding flight activity is causally linked to a shortened lifespan (Neukirch, 1982), and to the agerelated decline of learning function in foragers (Tolfsen et al, 2011). Few studies so far have explored the aging dynamics of winter bees (Behrends and Scheiner, 2010;Lindauer, 1963;Seehuus et al, 2006a), but the results suggest that organismal integrity, learning and memory are not compromised despite high chronological age.…”

Octopamine improves learning in newly emerged bees but not in old foragers

“…This decreases their sensitivity for sucrose (Page et al, 1998) and reduces their learning performance in appetitive learning (Ben-Shahar and Robinson, 2001;Friedrich et al, 2004). Another is to test age groups of bees with poor learning performance (Behrends et al, 2007;Scheiner and Amdam, 2009;Tolfsen et al, 2011). Obviously, the mechanisms underlying the poor learning performance of these groups must be different.…”