Acute exposure to sublethal doses of neonicotinoid insecticides increases heat tolerance in honey bees

Abstract

The European honey bee, Apis mellifera L., is the single most valuable managed pollinator in the world. Poor colony health or unusually high colony losses of managed honey bees result from a myriad of stressors, which are more harmful in combination. Climate change is expected to accentuate the effects of these stressors, but the physiological and behavioral responses of honey bees to elevated temperatures while under simultaneous influence of one or more stressors remain largely unknown. Here we test the hypothesis that exposure to acute, sublethal doses of neonicotinoid insecticides reduce thermal tolerance in honey bees. We administered to bees oral doses of imidacloprid and acetamiprid at 1/5, 1/20, and 1/100 of LD50 and measured their heat tolerance 4 h post-feeding, using both dynamic and static protocols. Contrary to our expectations, acute exposure to sublethal doses of both insecticides resulted in higher thermal tolerance and greater survival rates of bees. Bees that ingested the higher doses of insecticides displayed a critical thermal maximum from 2 ˚C to 5 ˚C greater than that of the control group, and 67%–87% reduction in mortality. Our study suggests a resilience of honey bees to high temperatures when other stressors are present, which is consistent with studies in other insects. We discuss the implications of these results and hypothesize that this compensatory effect is likely due to induction of heat shock proteins by the insecticides, which provides temporary protection from elevated temperatures.

Sublethal doses of insecticide reduce thermal tolerance of a stingless bee and are not avoided in a resource choice test

“…The survival of the temperature ramp control bees indicates that mortality in the temperature ramp experiment was due to the combination of insecticide exposure and thermal stress, and not just insecticide exposure alone. Our findings contrast with a recent study in which sublethal doses of imidacloprid increased thermal tolerance in A. mellifera [53]. The thermal tolerance of A. mellifera that received doses ranging from 0.18 ng to 3.6 ng of imidacloprid were on average 2.6°C to 4.3°C greater than the control group.…”

“…There is evidence from A. mellifera that the combined effect of insecticide exposure and heat stress could result in higher heat tolerance or synergize and cause higher mortality. For example, acute oral exposure to the neonicotinoids imidacloprid and acetamiprid increased thermal tolerance of A. mellifera by as much as 4.3°C [53]. Conversely, A. mellifera fed three concentrations (0 ppb, 5 ppb and 20 ppb) of imidacloprid and maintained at temperatures (26°C (below optimal) and 38°C (above optimal)) were more susceptible to imidacloprid, with significantly higher mortality compared to the control (32°C) and showed altered gene regulation [54].…”

High thermal tolerance in high‐elevation species and laboratory‐reared colonies of tropical bumble bees

“…Thermal limits are physiological traits measured under controlled conditions in the laboratory when organisms are exposed to constant (static protocols) or increasing or decreasing temperatures (dynamic protocols), and they help to explain their potential response to extreme temperature changes (Gonzalez, Oyen, et al, 2022 ; Roeder et al, 2021 ). However, these estimates may vary in response to a myriad of factors including life history traits (Baudier et al, 2018 ; Hamblin et al, 2017 ), abiotic conditions (Bujan et al, 2020 ; Roeder et al, 2021 ), environmental stressors (Gonzalez, Hranitz, et al, 2022 ; González‐Tokman et al, 2021 ), and experimental conditions (Gonzalez, Oyen, et al, 2022 ; Terblanche et al, 2007 ). For example, some studies indicate that heat tolerance may decrease with increasing elevation (García‐Robledo et al, 2016 ; Gonzalez et al, 2020 ), increase with increasing body size (Baudier et al, 2018 ; Oyen et al, 2016 ), and decrease with increasing age and length of starvation (Chidawanyika et al, 2017 ; Nyamukondiwa & Terblanche, 2009 ).…”

Neotropical stingless bees display a strong response in cold tolerance with changes in elevation

“…For example, in some insects including bees, CT Max decreases with increasing elevation (García-Robledo et al, 2016;Oyen et al, 2016;Gonzalez et al, 2020) and with age and starvation (Nyamukondiwa and Terblanche, 2009;Chidawanyika et al, 2017). How-ever, CT Max may increase with increasing body size (Baudier et al, 2018) and with acute exposure to pesticides (Gonzalez et al, 2022b). These responses may vary depending on the species, community or taxonomic group, as elevation, age, starvation or body size does not influence estimates of CT Max in some ants (Bishop et al, 2017) and bees (Hamblin et al, 2017;Oyen and Dillon, 2018;Gonzalez et al, 2020Gonzalez et al, , 2022aGonzalez et al, , 2022c.…”