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. 2025 Aug 23;101(9):fiaf080.
doi: 10.1093/femsec/fiaf080.

Friend or foe? Concentration of a commensal microbe induces distinct responses in developing honey bees exposed to field-realistic pesticide concentrations

Monika Yordanova  1   2 , Xiao Zhang  1   2 , Carlota B Torres  1 , Sophie E F Evison  3 , Richard J Gill  1 , Peter Graystock  1
Affiliations

Friend or foe? Concentration of a commensal microbe induces distinct responses in developing honey bees exposed to field-realistic pesticide concentrations

Monika Yordanova et al. FEMS Microbiol Ecol. .

Abstract

Commensal microbes play important roles in modulating host health through varied mechanisms. Enterococcus faecalis, a Gram-positive commensal bacterium found across a wide range of hosts, has the potential to benefit its host through probiotic, antimicrobial and detoxification properties. However, it can also cause adverse effects, disrupting the host's healthy microbial communities and responses to co-stressors. Its context-dependent impact on the health of the agriculturally important pollinator - Apis mellifera - has been sparsely explored. Here, we examined the effects on honey bee brood survivorship and development when exposed at different concentrations and when co-exposed with chemical stressors (acetamiprid, thymol, glyphosate, and a mixture of the three). We found high doses of E. faecalis significantly reduced larval survivorship and size of brood at multiple developmental stages. Conversely, we found that low doses of E. faecalis increased larval size when individuals were co-exposed to the pesticide mixture. We also found that glyphosate alone and the pesticide mixture reduced the mass of brown-eyed pupae. These results are the first to show the dual role of E. faecalis in honey bee health is dependent on the concentration of the microbe and the co-stressors that brood are exposed to.

Keywords: Enterococcus; commensalism; honey bee; larvae; pesticides.

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Conflict of interest statement

None declared.

Figures

Figure 1.
Figure 1.
Exposure of honey bee larvae to E. faecalis. The bacterium is represented using blue bacterial icon. A) It is a commensal microbe found in a broad range of species. B) The excrement of some of these species can act as a nutrient-rich fertilizer, which may contain the bacterium. C) As the fertilizer is used on crops, bees can become exposed to E. faecalis through feeding on the pollen and nectar of these crops. D) Adult bees can introduce E. faecalis to larvae in their hives by contaminating their food (31–37). Icons by Icon8.com
Figure 2.
Figure 2.
Measurements collected during larval development observed over 4 weeks. The day of Defecation events (DE), the appearance of brown-eyed pupa (BEP), and adult emergence (AE) were recorded. Daily images were taken to calculate larval growth. Weight was measured on day 12 (D12), when each individual became a brown-eyed pupa (BEP) and when they emerged as an adult bee (AE).
Figure 3.
Figure 3.
Independent effects of both treatment groups. Larval feed was spiked with E. faecalis on day 1 of the experiment, and pesticides were supplemented into feed throughout development. A) Effects of different doses of E. faecalis on larval survivorship over time. The survival rate over time in larvae unexposed to E. faecalis is shown in blue (n = 36); the survival rate of those exposed to low doses of E. faecalis (8.5 × 106 CFUs per larvae) is shown in purple (n = 40); and the survival rate of those exposed to high doses of E. faecalis (4.2 × 107 CFUs per larvae) is shown in red (n = 44). High doses of E. faecalis significantly reduced survival. B) Effects of pesticides on larval survivorship over time in larvae unexposed to E. faecalis (n = 36 per treatment). The treatments included a pesticide-free control in yellow; acetamiprid in orange; glyphosate in pink; thymol in purple and the trimix which contained acetamiprid; glyphosate and thymol in green. Acetamiprid, thymol, and trimix all significantly reduced larval survival.Treatments per line are also annotated on day 8 for clarity.
Figure 4.
Figure 4.
Sublethal effects of exposure to varying levels of E. faecalis on brood size and rate of development. A) Increase in area covered by larvae between day 1 and day 3 (n = 555), between day 3 and day 6 (n = 334) and between day 1 and day 6 (n = 334). B) Increase in mass in larvae measured upon death (n = 275), at day 12 of development (n = 241), when individuals become brown-eyed pupae (BEP) (n = 79), and when individuals emerge as adults (n = 66). C) Rate of reaching key stages of development depending on E. faecalis exposure, including defecation (n = 246), becoming a BEP (n = 79) and emerging as an adult (n = 66). Significant differences relative to controls have been indicated by asterisk * P <0.05, ** P <0.01,*** P <0.001.
Figure 5.
Figure 5.
Sublethal effects of pesticide exposure on brood size and rate of development. A) Increase in area covered by larvae between day 1 and day 3 (n = 555), between day 3 and day 6 (n = 334) and between day 1 and day 6 (n = 334). B) Increase in weight at day 12 of development (n = 241), when individuals become brown-eyed pupae (n = 79), when individuals emerge as adults (n = 66). C) Rate of reaching key stages of development depending on pesticide exposure, including defecation (n = 246), becoming a brown-eyed pupa (n = 79) and emerging as an adult (n = 66). Significant differences relative to controls have been indicated by asterisk * P <0.05, ** P <0.01,*** P <0.001.
Figure 6.
Figure 6.
Effects of E. faecalis dose and pesticide treatment on the growth (mm2) of larvae as determined by the 2D area covered by larvae between day 1 and day 6 (n = 334). These were calculated from images using the image analysis software ImageJ (Schneider et al. 2012). Significant differences relative to controls have been indicated by asterisk * P <0.05, ** P <0.01,*** P <0.001.
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