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

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.

Antimicrobial Activity against Paenibacillus larvae and Functional Properties of Lactiplantibacillus plantarum Strains: Potential Benefits for Honeybee Health

“…This gram-positive, flagellated, spore-forming bacterium is highly adapted to honeybee larvae [1,2]. The honeybee gut is the site of P. larvae infection, as well as of pathogens such as Ascosphaera apis, Nosema ceranae, and probably many of the honeybee viruses [3]. Following ingestion, through spore-contaminated food, the spores germinate in the larval midgut lumen, where the vegetative bacteria massively proliferate before eventually breaching the midgut epithelium and invading the hemocoel, causing the death of the larvae, which during their decay releases a large number of spores.…”

Phages in Therapy and Prophylaxis of American Foulbrood – Recent Implications From Practical Applications

“…This glue-colloid dries down and adheres to the cell wall forming a kind of hard scale consisting of billions of spores, and are highly infectious (Bailey and Ball, 1991;Gregorc and Bowen, 1998). According to Stephan et al (2020), there is a relationship between spore count and disease and colony development.…”

Novel TaqMan PCR Assay for the Quantification of Paenibacillus larvae Spores in Bee-Related Samples

“…Apparently healthy honeybee colonies can harbor P. larvae spores [9][10][11]. Spore counts in honey, hive debris, and adult bees correlate with the severity of symptoms in the clinical stage of AFB and may be useful in identifying colonies in the pre-clinical stage of the disease [10][11][12][13][14][15][16][17]. Thus, quantification of P. larvae spores offers a promising prognostic tool for early detection of at-risk apiaries based on increased spore counts in the colonies, which should then undergo thorough clinical examination.…”

“…Two main approaches for the quantification of P. larvae spores in bee-related samples are culture-and PCR-based methods. To date, the detection and quantification of P. larvae in honey and hive debris have mostly relied on culture-based methods [9,11,17,18]. However, these suffer from certain limitations.…”