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Extracting individual characteristics from population data reveals a negative social effect during honeybee defence

Tatjana Petrov, Matej Hajnal, Julia Klein, David Šafránek and Morgane Nouvian

PLOS Computational Biology, 2022, vol. 18, issue 9, 1-20

Abstract: Honeybees protect their colony against vertebrates by mass stinging and they coordinate their actions during this crucial event thanks to an alarm pheromone carried directly on the stinger, which is therefore released upon stinging. The pheromone then recruits nearby bees so that more and more bees participate in the defence. However, a quantitative understanding of how an individual bee adapts its stinging response during the course of an attack is still a challenge: Typically, only the group behaviour is effectively measurable in experiment; Further, linking the observed group behaviour with individual responses requires a probabilistic model enumerating a combinatorial number of possible group contexts during the defence; Finally, extracting the individual characteristics from group observations requires novel methods for parameter inference.We first experimentally observed the behaviour of groups of bees confronted with a fake predator inside an arena and quantified their defensive reaction by counting the number of stingers embedded in the dummy at the end of a trial. We propose a biologically plausible model of this phenomenon, which transparently links the choice of each individual bee to sting or not, to its group context at the time of the decision. Then, we propose an efficient method for inferring the parameters of the model from the experimental data. Finally, we use this methodology to investigate the effect of group size on stinging initiation and alarm pheromone recruitment.Our findings shed light on how the social context influences stinging behaviour, by quantifying how the alarm pheromone concentration level affects the decision of each bee to sting or not in a given group size. We show that recruitment is curbed as group size grows, thus suggesting that the presence of nestmates is integrated as a negative cue by individual bees. Moreover, the unique integration of exact and statistical methods provides a quantitative characterisation of uncertainty associated to each of the inferred parameters.Author summary: In this paper, our interdisciplinary team has significantly improved the understanding of how honeybees coordinate their actions during defence. Our first step was to measure the output behaviour of groups of bees under controlled experimental conditions. We then developed a model and methodology that allow us to quantify how the responsiveness to the alarm pheromone evolves during a defensive event, for a given group size. We show that recruitment becomes less effective as group size increases, thus revealing the existence of a negative social effect that acts on top of alarm pheromone communication. Our contribution is thus two-fold: on the computational side, we provide new tools to extract individual characteristics from population data, which is a challenging issue in the study of collective behaviour. On the biological side, we provide evidence that bees weight in their social context when making the decision to sting. We hypothesize that this may be an important mechanism to prevent recruitment from spinning out of control, ultimately preserving the colony from workforce depletion.

Date: 2022
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Persistent link: https://EconPapers.repec.org/RePEc:plo:pcbi00:1010305

DOI: 10.1371/journal.pcbi.1010305

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