Immune-cognitive system connectivity reduces bumblebee foraging success in complex multisensory floral environments

Melissa W Mobley,Robert J Gegear

doi:10.1038/s41598-018-24372-5

Melissa W Mobley, Robert J Gegear

Open Access

https://doi.org/10.1038/s41598-018-24372-5

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Journal: Scientific Reports	Publication Date: Apr 13, 2018
Citations: 8	License type: open-access

Affiliation: Worcester Polytechnic Institute

Abstract

Bumblebees are declining at alarming rate worldwide, posing a significant threat to the function and diversity of temperate ecosystems. These declines have been attributed, in part, to the direct effect of specific pathogens on bumblebee survival. However, pathogens may also have a negative impact on host populations indirectly through immune-induced cognitive deficits in infected individuals. To gain greater insight into mechanisms and potential conservation implications of such ‘immune-brain crosstalk’ in bumblebees, we non-pathogenetically activated humoral and cellular immune pathways in individuals and then tested for long-term reductions in cognitive performance and foraging proficiency. We show that chronic activation of humoral, but not a cellular, immune pathways and effectors in foragers significantly reduces their ability to flexibly and efficiently harvest resources in multi-sensory floral environments for at least 7 days post-treatment. Humoral defense responses thus have the potential to confer significant foraging costs to bumblebee foragers over timeframes that would negatively impact colony growth and reproductive output under natural conditions. Our findings indicate that fitness effects of immune-brain crosstalk should be considered before attributing wild bumblebee decline to a particular pathogen species.

Highlights

Bumblebees are declining in abundance, species richness, and geographic distribution at an unprecedented rate worldwide[1,2,3,4]
Our study demonstrates that humoral defense responses in bumblebee foragers can produce long-term impairments to ‘higher order’ brain functions needed for the flexible and adaptive exploitation of multiple floral resources in complex sensory environments
Bees injected with lipopolysaccharide from Escherichia coli (LPS), a non-pathogenic elicitor of humoral immune defense response, showed substantial reductions in performance on simple color and odor discrimination learning tasks compared to Ringer control bees

Summary

Introduction

Bumblebees are declining in abundance, species richness, and geographic distribution at an unprecedented rate worldwide[1,2,3,4]. Past studies have shown that infection by some pathogens can impair cognitive processes (i.e. brain functions involved in the acquisition, storage, manipulation of information13) needed for bumblebee foragers to adaptively exploit floral resources[14,15] Because these pathogens do not make contact with the central nervous system, destroy neurons, or have the metabolic capacity to secrete neuromodulators, Gegear et al.[15] proposed that cognitive deficits associated with infection were mediated by some form of communication between the immune system and the brain of host bees rather than by the direct action of the pathogen itself, as has been demonstrated previously in vertebrate systems[16,17,18,19]. Recent genetic studies have shown that AMPs have the capacity to alter neuroactivity, cause neurodegeneration, and reduce memory capacity in Drosophila[37,38,39,40]

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