Parasitic and immune-modulation of flight activity in honey bees tracked with optical counters

Abstract

Host-parasite interactions are often characterized by changes in the host behaviour, which are beneficial to either the parasite or the host, or are a non-adaptive byproduct of parasitism. These interactions are further complicated in animal society because individual fitness is associated with group performance. However, a better understanding of host-parasite interaction in animal society first requires the identification of individual host behavioural modification. Therefore, we challenged honey bee (Apis mellifera) workers with the parasite Nosema ceranae or an immune stimulation and tracked their flight activity over their lifetime with an optic counter. We found that bees responded differently to each stress: both Nosema-infected and immune-challenged bees performed a lower number of daily flights compared with control bees, but the duration of their flights increased and decreased over time, respectively. Overall, parasitized bees spent more time in the field each day than control bees, and the inverse was true for immune-challenged bees. Despite the stress of immune challenge, bees had a survival similar to that of control bees likely because of their restricted activity. We discuss how those different behavioural modifications could be adaptive phenotypes. This study provides new insights into how biological stress can affect the behaviour of individuals living in society and how host responses have evolved.

Nosema spp. infections cause no energetic stress in tolerant honeybees

“…This behavioural alteration of infected honeybees might also reduce the parasite transmission and ultimately limit the damage at the colony level. However, changes in the foraging behaviour of infected individuals is also likely to negatively affect the life-history traits of the colony (Alaux et al, 2014;Naug, 2014;Wolf et al, 2014) and lower its overall fitness as a whole in the long run.…”

“…Although N. ceranae infection does not appear to alter the navigation and orientation of the honeybees while foraging, increased foraging duration and decreased flight frequencies have been reported in infected honeybees (Alaux et al, 2014;Dussaubat et al, 2013;Naug, 2014;Wolf et al, 2014). This decline in foraging efficiency is likely to be a result of imposed nutritional and energetic stress from infection (Aliferis et al, 2012;Martín-Hernández et al, 2011;Mayack & Naug, 2009;Mayack & Naug, 2010;Moffett & Lawson, 1975).…”

Modulation of pesticide response in honeybees

“…However, in their natural environment, honeybees rarely face such optimal conditions but are exposed to a large variability of environmental conditions from suboptimal to severe. For example, bees reared under optimal conditions in the laboratory clearly live longer than bees reared in colonies in the field (Alaux et al 2014). The observed effects of potential stressors (parasitism and immune stimulation) on bee longevity under natural conditions are also reduced (parasitism) or not detected (immune stimulation) compared to laboratory conditions which is likely due to the fact that control bees have a reduced longevity in nonoptimal field conditions (Alaux et al 2014).…”

“…For example, bees reared under optimal conditions in the laboratory clearly live longer than bees reared in colonies in the field (Alaux et al 2014). The observed effects of potential stressors (parasitism and immune stimulation) on bee longevity under natural conditions are also reduced (parasitism) or not detected (immune stimulation) compared to laboratory conditions which is likely due to the fact that control bees have a reduced longevity in nonoptimal field conditions (Alaux et al 2014). It is therefore recommended to perform pesticide bioassays under a range of test conditions that reflect the range of variability in conditions experienced by bees in the field (Holmstrup et al 2010).…”

“…Exposure to Nosema and thiacloprid at the colony level did not produce the synergistic interaction (Retschnig et al 2015) observed in laboratory conditions (Vidau et al 2011;Retschnig et al 2014). It is likely that the colony environment has a buffering effect on stress exposure and/or that control bees die faster in their natural environment than in laboratory conditions leading to no effect of treatments (Alaux et al 2014). In addition, the type of interaction between pathogens and pesticides may be dose-dependent.…”