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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.

SUBMITTER: Lopez JH

PROVIDER: S-EPMC5286422 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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

López Javier Hernández JH Krainer Sophie S Engert Antonia A Schuehly Wolfgang W Riessberger-Gallé Ulrike U Crailsheim Karl K

Scientific reports 20170201

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 ex ...[more]

PMID: 28145462

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Project description:Paenibacillus larvae, the causative agent of American foulbrood (AFB), is the primary bacterial pathogen affecting honeybees and beekeeping. The main methods for controlling AFB are incineration of diseased colonies or prophylactic antibiotic treatment (e.g., with tylosin), neither of which is fully satisfactory. The search for superior means for controlling AFB has led to an increased interest in the natural relationships between the honeybee-pathogenic and mutualistic microorganisms and, in particular, the antagonistic effects of honeybee-specific lactic acid bacteria (hbs-LAB) against P. larvae These effects have been demonstrated only on individual larvae in controlled laboratory bioassays. Here we investigated whether supplemental administration of hbs-LAB had a similar beneficial effect on P. larvae infection at colony level. We compared experimentally AFB-infected colonies treated with hbs-LAB supplements to untreated and tylosin-treated colonies and recorded AFB symptoms, bacterial spore levels, and two measures of colony health. To account for the complexity of a bee colony, we focused on (Bayesian) probabilities and magnitudes of effect sizes. Tylosin reduced AFB disease symptoms but also had a negative effect on colony strength. The tylosin treatment did not, however, affect P. larvae spore levels and might therefore "mask" the potential for disease. hbs-LAB tended to reduce brood size in the short term but was unlikely to affect AFB symptoms or spores. These results do not contradict demonstrated antagonistic effects of hbs-LAB against P. larvae at the individual bee level but rather suggest that supplementary administration of hbs-LAB may not be the most effective way to harness these beneficial effects at the colony level.IMPORTANCE The previously demonstrated antagonistic effects of honeybee-derived bacterial microbiota on the infectivity and pathogenicity of P. larvae in laboratory bioassays have identified a possible new approach to AFB control. However, honeybee colonies are complex superorganisms where social immune defenses play a major role in resistance against disease at the colony level. Few studies have investigated the effect of beneficial microorganisms on bee diseases at the colony level. Effects observed at the individual bee level do not necessarily translate into similar effects at the colony level. This study partially fills this gap by showing that, unlike at the individual level, hbs-LAB supplements did not affect AFB symptoms at the colony level. The inference is that the mechanisms regulating the honeybee microbial dynamics within a colony are too strong to manipulate positively through supplemental feeding of live hbs-LAB and that new potential remedies identified through laboratory research have to be tested thoroughly in situ, in colonies.

Project description:BACKGROUND:The most severe bacterial disease of honeybees is American foulbrood (AFB). The epidemiology of AFB is driven by the extreme spore resilience, the difficulty of bees to remove these spores, and the considerable incidence of undetected spore-producing colonies. The honeybee collective defence mechanisms and their feedback on colony development, which involves a division of labour at multiple levels of colony organization, are difficult to model. To better predict disease outbreaks we need to understand the feedback between colony development and disease progression within the colony. We therefore developed Bayesian models with data from forty AFB-diseased colonies monitored over an entire foraging season to (i) investigate the relationship between spore production and symptoms, (ii) disentangle the feedback loops between AFB epidemiology and natural colony development, and (iii) discuss whether larger insect societies promote or limit within-colony disease transmission. RESULTS:Rather than identifying a fixed spore count threshold for clinical symptoms, we estimated the probabilities around the relationship between spore counts and symptoms, taking into account modulators such as brood amount/number of bees and time post infection. We identified a decrease over time in the bees-to-brood ratio related to disease development, which should ultimately induce colony collapse. Lastly, two contrasting theories predict that larger colonies could promote either higher (classical epidemiological SIR-model) or lower (increasing spatial nest segregation and more effective pathogen removal) disease prevalence. CONCLUSIONS:AFB followed the predictions of the SIR-model, partly because disease prevalence and brood removal are decoupled, with worker bees acting more as disease vectors, infecting new brood, than as agents of social immunity, by removing infected brood. We therefore established a direct link between disease prevalence and social group size for a eusocial insect. We furthermore provide a probabilistic description of the relationship between AFB spore counts and symptoms, and how disease development and colony strength over a season modulate this relationship. These results help to better understand disease development within honeybee colonies, provide important estimates for further epidemiological modelling, and gained important insights into the optimal sampling strategy for practical beekeeping and honeybee research.

Dataset Information

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

Publications

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

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