Behavioral alteration in the honeybee due to parasite-induced energetic stress

Abstract

Parasites are dependent on their hosts for energy and honeybee foragers with their high metabolic demand due to flight are especially prone to an energetic stress when they are infected. The microsporidian gut parasite Nosema ceranae is relatively new to the honeybee, Apis mellifera and because it is less co-evolved with its new host the virulence from infection can be particularly high. Using a series of feeding and survival experiments, I found that bees infected with N. ceranae have a higher appetite and hunger level, and the survival of infected bees is compromised when they are fed with a limited amount of food. However, if fed ad libitum the survival of infected individuals is not different from that of uninfected bees, demonstrating that energetic stress is the primary cause of the shortened lifespan observed in infected bees. I then developed a high throughput colorimetric assay to analyze hemolymph sugar levels of individual bees to demonstrate that the parasite mediated energetic stress is expressed as lower trehalose levels in free-flying bees, which suggests that infected bees are not only likely to have a reduced flight capacity but they are also unable to compensate for their lower energetic state. One of the ways in which the changing energetic state of an individual is predicted to impact its behavior is its sensitivity to risk although this has never been convincingly demonstrated. According to the energy budget rule of Risk Sensitivity Theory, it is adaptive for an animal to be risk averse when it is on a positive energy budget and be risk prone when it is on a negative budget because the utility of a potential large reward is much higher in the latter case. By constructing an empirical utility curve and conducting choice tests using a Proboscis Extension Response assay in bees that have been variously manipulated with respect to their energy budgets, I comprehensively demonstrated that bees shift between risk averse to risk prone behavior in accordance with the energy budge rule. Even more importantly, I showed that this shift is contingent upon a change in the energy budget as bees maintained on constant high or low energy budgets were found to be risk indifferent. Given that Nosema infected bees have been seen to forage precociously and inclement weather, my results suggest that such risky foraging might be a consequence of the lower energetic state of infected foragers. As these previous results suggest that parasitism, by lowering their energetic state could have a significant influence on how infected bees forage, I decided to test if the energetic state of an individual can regulate its foraging independent of the colony level regulation of foraging. I uncoupled the energetic state of the individual from that of the colony by feeding individual bees with the non-metabolizable sugar sorbose, thereby creating hungry bees in a satiated colony. I found that these energy depleted bees initially compensate for their lower energetic state by being less active within the colony and taking fewer foraging trips, but not by feeding more within the colony. However, with further depletion in their energetic state, these bees increase their foraging frequency showing that foraging is still partly regulated at the individual level even in a eusocial animal such as the honeybee. My research therefore shows that the energetic stress from a parasite could be a general mechanism that leads to significant behavioral alterations in infected individuals. Since the energetic state of an animal is a fundamental driver of its behavior, such a mechanism underlying behavioral alterations could have a significant impact on the life history of the host and transmission dynamics of a disease. More specifically, these results also suggest that a parasitic infection leading to energy depleted bees going out to forage in a risky manner also provides a plausible mechanism that explains the recent observations of bees disappearing from their colonies.