Sublethal pesticide doses negatively affect survival and the cellular responses in American foulbrood-infected honeybee larvae

Abstract

Disclosing interactions between pesticides and bee infections is of most interest to understand challenges that pollinators are facing and to which extent bee health is compromised. Here, we address the individual and combined effect that three different pesticides (dimethoate, clothianidin and fluvalinate) and an American foulbrood (AFB) infection have on mortality and the cellular immune response of honeybee larvae. We demonstrate for the first time a synergistic interaction when larvae are exposed to sublethal doses of dimethoate or clothianidin in combination with Paenibacillus larvae, the causative agent of AFB. A significantly higher mortality than the expected sum of the effects of each individual stressor was observed in co-exposed larvae, which was in parallel with a drastic reduction of the total and differential hemocyte counts. Our results underline that characterizing the cellular response of larvae to individual and combined stressors allows unmasking previously undetected sublethal effects of pesticides in colony health.

Detrimental interactions of neonicotinoid pesticide exposure and bumblebee immunity

“…The results demonstrated here in bumblebees are congruent with the outcomes of prior studies investigating interactions between neonicotinoid exposure and immunity in honeybees (Alaux et al., ; Di Prisco et al., ; Brandt et al., ; López et al., ). This is not a trivial extension, as honeybees and bumblebees, while both highly susceptible, have been suggested to differ in their detoxification of neonicotinoids (Cresswell, Robert, Florance, & Smirnoff, ), and neonicotinoid exposure and parasite stress has been shown to have differential effects in the two groups of bees (Piiroinen & Goulson, ).…”

“…It has been shown that neonicotinoid exposure increases pathogen spore load and mortality in honeybees infected with the microsporidian Nosema ceranae (Alaux et al., ; Vidau et al., ; Pettis, van Engelsdorp, Johnson, & Dively, ; Retschnig, Neumann, & Williams, ). Similar results have been shown for honeybee viral (Di Prisco et al., ; Doublet, Labarussias, de Miranda, Moritz, & Paxton, ) and bacterial infection (López et al., ). In bumblebees, exposure to clothianidin and thiomethoxam and a trypanosome parasite reduce mother queen longevity in a greater than additive manner (Fauser‐Misslin et al., ), although effects on overwintering were less than additive, with strong early pesticide exposure effects masking later parasite effects (Fauser et al., ).…”

“…An obvious candidate linking neonicotinoid exposure to heightened susceptibility to infection and the consequences of infection is the immune system, with neonicotinoid exposure having the potential to compromise the immune system via a number of routes. In honeybees, exposure to neonicotinoids has been associated with decreased cellular responses on bacterial infection (López et al, 2017), reduced hemocyte numbers, encapsulation, and antibacterial responses (Brandt, Gorenflo, Siede, Meixner, & Büchler, 2016;Siede et al, 2017), and reduced activity of an enzyme involved in social immune sterilization of food (Alaux et al, 2010). NF-B signaling, with a central role in immunity, has also been shown to be inhibited by neonicotinoid exposure in honeybees (Di Prisco et al, 2013).…”

Morphological and functional characterization of honey bee, Apis mellifera, hemocyte cell communities

“…However, a second larval cell type, resembling those described as L5-2 by Negri et al (2014b), were also observed though they were not encountered during cytospin transect counting, indicating that they are either rare or not easily distinguished using the methods described here. It is possible that the cytospin method we employed resulted in the loss or degradation of cell types observed in other works (e.g., López et al 2014López et al , 2017. Alternatively, additional cell types may be inducible upon infection or wounding.…”

Acute and chronic toxicity of acetamiprid, carbaryl, cypermethrin and deltamethrin to Apis mellifera larvae reared in vitro

“…There is clear evidence that bee larvae reared in treatment combs containing insecticide residues experience delayed development . Reduced survival and weight loss are the main indicators of the effects of insecticides on bee larvae in the literature . Several studies have even confirmed that insecticide toxicity occurs at lower exposure rates to larvae compared to adult bees …”