Compound and Dose-Dependent Effects of Two Neonicotinoid Pesticides on Honey Bee (Apis mellifera) Metabolic Physiology

Abstract

Use of neonicotinoid pesticides is now ubiquitous, and consequently non-targeted arthropods are exposed to their residues at sub-lethal doses. Exposure to these neurotoxins may be a major contributor to poor honey bee colony health. Few studies have explored how sub lethal exposure to neonicotinoids affects honey bee metabolic physiology, including nutritional and energetic homeostasis, both of which are important for maintaining colony health. Reported here are results from a study of chronic oral exposure of honey bees to two sub lethal concentrations of clothianidin and imidacloprid. Neonicotinoids altered important aspects of honey bee nutritional and metabolic physiology in a compound and dose-dependent manner; both compounds at low doses reduced honey bee body weight. Low-dose clothianidin exposure resulted in bees having protein, lipids, carbohydrates, and glycogen levels similar to newly emerged bees. High-dose clothianidin exposure lowered lipids and glycogen content of bees. High-dose imidacloprid exposure resulted in bees having depressed metabolic rate. Low-dose imidacloprid exposure resulted in bees consuming low and high levels of protein and carbohydrate rich foods, respectively. Results suggest neonicotinoids interfere with honey bee endocrine neurophysiological pathways. Compound and dose-dependent effects might represent respective chemical structural differences determining an observed effect, and thresholds of compound effects on honey bee physiology.

Keywords: carbon dioxide; glucose; glycogen; lipids; neurophysiology; protein; respiration.

Figure 1

Mean (±s.e.m) total pollen patty (A) and sucrose (B) from sugar syrup consumed by caged honey bees over two weeks. Black bar = Control treatment; Dark grey bars = Clothianidin Low (CLLO) and High (CLHI) dose treatments; Light grey bars = Imidacloprid Low (IMLO) and High (IMHI) dose treatments. Letters above bars represent significant differences across treatments from Student’s post hoc tests.

Figure 2

Mean (±s.e.m) weight of individual newly emerged honey bees and those from pesticide treatment groups after two weeks. White bar = Newly Emerged Treatment; Black bar = Control treatment; Dark grey bars = Clothianidin Low (CLLO) and High (CLHI) dose treatments; Light grey bars = Imidacloprid Low (IMLO) and High (IMHI) dose treatments. Letters above bars represent significant differences across treatments from Student’s post hoc tests.

Figure 3

Mean (±s.e.m) relative quantity (mg/g) of soluble proteins (A) and median (±quartiles) lipids (B), from spectrophotometric assays of homogenized tissues of individual newly emerged honey bees, and those from pesticide treatment groups after two weeks. (A) White bar = Newly emerged bees; Black bar = Control treatment; Dark grey bars = Clothianidin Low (CLLO) and High (CLHI) dose treatments; Light grey bars = Imidacloprid Low (IMLO) and High (IMHI) dose treatments. Single point in (B) represents outlying data point. Letters above bars represent significant differences across treatments from Student’s (A) or multiple comparison Wilcoxon (B) post hoc tests.

Figure 4

Mean (±s.e.m) log₁₀-transformed quantity of glucose (A) and glycogen (B), measured by spectrophotometric assays of homogenized tissues of individual newly emerged honey bees, and those from pesticide treatment groups after two weeks. White bar = Newly emerged bees; Black bar = Control treatment; Dark grey bars = Clothianidin Low (CLLO) and High (CLHI) dose treatments; Light grey bars = Imidacloprid Low (IMLO) and High (IMHI) dose treatments. Letters above bars represent significant differences across treatments from Student’s post hoc tests.

Figure 5

Median (±quartiles) volume of carbon dioxide (μL/min) emitted over 10 min by individual newly emerged honey bees, and by honey bees after two weeks exposure to two neonicotinoids. Treatment groups = Clothianidin Low (CLLO) and High (CLHI) dose treatments; Imidacloprid Low (IMLO) and High (IMHI) dose treatments. Letters above bars represent significant differences across treatments from multiple comparison Wilcoxon post hoc tests.