Honey bees respond to multimodal stimuli following the principle of inverse effectiveness

Abstract

Multisensory integration is assumed to entail benefits for receivers across multiple ecological contexts. However, signal integration effectiveness is constrained by features of the spatiotemporal and intensity domains. How sensory modalities are integrated during tasks facilitated by learning and memory, such as pollination, remains unsolved. Honey bees use olfactory and visual cues during foraging, making them a good model to study the use of multimodal signals. Here, we examined the effect of stimulus intensity on both learning and memory performance of bees trained using unimodal or bimodal stimuli. We measured the performance and the latency response across planned discrete levels of stimulus intensity. We employed the conditioning of the proboscis extension response protocol in honey bees using an electromechanical setup allowing us to control simultaneously and precisely olfactory and visual stimuli at different intensities. Our results show that the bimodal enhancement during learning and memory was higher as the intensity decreased when the separate individual components were least effective. Still, this effect was not detectable for the latency of response. Remarkably, these results support the principle of inverse effectiveness, traditionally studied in vertebrates, predicting that multisensory stimuli are more effectively integrated when the best unisensory response is relatively weak. Thus, we argue that the performance of the bees while using a bimodal stimulus depends on the interaction and intensity of its individual components. We further hold that the inclusion of findings across all levels of analysis enriches the traditional understanding of the mechanics and reliance of complex signals in honey bees. © 2022. Published by The Company of Biologists Ltd.