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Research article - Peer-reviewed, 2020

American foulbrood in a honeybee colony: spore-symptom relationship and feedbacks between disease and colony development

Stephan, Jörg; Rodrigues De Miranda, Joachim; Forsgren, Eva

Abstract

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.

Keywords

Apis mellifera; Paenibacillus larvae; Group size; Enzootic disease; Host-pathogen dynamics; Social immunity; MCMC; Detection; SIR-model; Diagnosis; Host density

Published in

BMC Ecology
2020, volume: 20, number: 1, article number: 15

Authors' information

Swedish University of Agricultural Sciences, Department of Ecology
Swedish University of Agricultural Sciences, Swedish Species Information Centre
Swedish University of Agricultural Sciences, Department of Ecology
Swedish University of Agricultural Sciences, Department of Ecology

UKÄ Subject classification

Agricultural Science
Ecology

Publication Identifiers

DOI: https://doi.org/10.1186/s12898-020-00283-w

URI (permanent link to this page)

https://res.slu.se/id/publ/104877