Discovery of octopamine and tyramine in nectar and their effects on bumblebee behavior

Muth, Felicity; Philbin, Casey S.; Jeffrey, Christopher S.; Leonard, Anne S.

doi:10.1016/j.isci.2022.104765

Cited by 18 publications

(20 citation statements)

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“…Although these results have intriguing implications for understanding how nectar chemistry might activate octopaminergic pathways (Muth et al, 2022), this experiment was not designed to identify the mechanism behind shifts in floral choice. Indeed, understanding how OA (or other biogenic amines) influences foraging behavior in diverse bee taxa will require standardized and replicable behavioral assays.…”

Section: Discussionmentioning

confidence: 99%

Octopamine affects gustatory responsiveness and associative learning performance in bumble bees

Muth

Breslow

Leonard

2022

Preprint

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Octopamine has broad roles within invertebrate nervous systems as a neurohormone, neurotransmitter and neuromodulator. It orchestrates foraging behavior in many insect taxa via effects on feeding, gustatory responsiveness and appetitive learning. Knowledge of how this biogenic amine regulates bee physiology and behavior is based largely on study of a single species, the honey bee, Apis mellifera. Until recently, its role in the foraging ecology and social organization of diverse bee taxa had been unexplored. Bumble bees (Bombus spp.) are a model for the study of foraging and learning, and its neural basis, but whether octopamine similarly affects sensory and cognitive performance in this genus is not known. To address this gap, we explored the effects of octopamine on sucrose response thresholds and associative learning in Bombus impatiens via conditioning of the Proboscis Extension Reflex (PER) using a visual (color) cue. We found that octopamine had similar effects on bumble bee behavior as honey bees, however, higher doses were required to induce these effects. At this higher dose, octopamine lowered bees’ sucrose response thresholds and appeared to enhance associative learning performance. Adding to recent studies on stingless bees (Meliponini), these findings support the idea that octopamine’s role in reward processing and learning is broadly conserved across Apidae, while pointing towards some differences across systems worth exploring further.

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Section: Discussionmentioning

confidence: 99%

Octopamine affects gustatory responsiveness and associative learning performance in bumble bees

Muth

Breslow

Leonard

2022

Preprint

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“…Here, we propose some potential avenues of exploration which we think would be of particular interest: Focusing on olfactory learning, which is thought to take place in the acetylcholine receptor-rich antennal lobes and mushroom bodies. Using lower sucrose concentrations would reduce motivation, in theory decreasing learning speed or quality, which could help studying subtle effects induced by the chemicals – especially in the face of ceiling effects caused by excellent olfactory learning. Using different, more complex tasks, such as reversal learning or navigation in an open field (Galante et al In prep.) would require more neural pathways to be activated and therefore could help expose effects induced by the chemicals. Testing learning, but also its extinction, could provide insights into how these chemicals impact long-term memory formation, consolidation, and retention. Using different concentrations and combinations of various nectar secondary metabolites seems to be promising – for example combining caffeine with arginine or octopamine and tyramine (Marchi, Palottini & Farina, 2021; Muth et al, 2022). β-alanine is a promising chemical for further testing, as it caused a small but significant reduction in return time to the nest. …”

Section: Discussionmentioning

confidence: 99%

“…Using different concentrations and combinations of various nectar secondary metabolites seems to be promising – for example combining caffeine with arginine or octopamine and tyramine (Marchi, Palottini & Farina, 2021; Muth et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

“…Honeybees fed 0.05μmol ml −1 or 0.16μmol ml −1 of caffeine showed improved learning performance, but no change in memory retention unless caffeine was mixed with arginine (Marchi, Palottini & Farina, 2021). Moreover, octopamine and tyramine mixed with caffeine altered bumblebee behaviour, but not when present individually (Muth et al ., 2022). However, considering the infinite possible combinations of chemicals at different concentrations, it seems that using neuroactive chemicals to artificially manipulate ant behaviour might not be straightforward.…”

Section: Discussionmentioning

confidence: 99%

“…• Testing learning, but also its extinction, could provide insights into how these chemicals impact long-term memory formation, consolidation, and retention. • Using different concentrations and combinations of various nectar secondary metabolites seems to be promising -for example combining caffeine with arginine or octopamine and tyramine (Marchi, Palottini & Farina, 2021;Muth et al, 2022). • β-alanine is a promising chemical for further testing, as it caused a small but significant reduction in return time to the nest.…”

Section: Box 1 -Future Directionsmentioning

confidence: 99%

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Invasive ant learning is not affected by seven potential neuroactive chemicals

Galante

Czaczkes

2022

Preprint

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Nectar-feeding insects are often the victims of psychoactive manipulation, with plants lacing their nectar with secondary metabolites such as alkaloids and non-protein amino acids which often boost learning, foraging, or recruitment. However, the effect of neuroactive chemicals has seldomly been explored in ants. Argentine ants (Linepithema humile) are one of the most damaging invasive alien species worldwide. Enhancing or disrupting cognitive abilities, such as learning, has the potential to improve management efforts, for example by increasing preference for a bait, or improving ants' ability to learn its characteristics or location. Here, we test the effects of seven potential neuroactive chemicals - two alkaloids: caffeine and nicotine; two biogenic amines: dopamine and octopamine, and three non-protein amino acids: β-alanine, GABA and taurine - on the cognitive abilities of invasiveL. humileusing bifurcation mazes. Our results confirm that these ants are strong associative learners, requiring as little as one experience to develop an association. However, we show no short-term effect of any of the chemicals tested on spatial learning, and in addition no effect of caffeine on short-term olfactory learning. This lack of effect is surprising, given the extensive reports of the tested chemicals affecting learning and foraging in bees. This mismatch could be due to the heavy bias towards bees in the literature, a positive result publication bias, or differences in methodology.

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Field agrochemical exposure impacts locomotor activity in wild bumblebees

Strang,

Rondeau,

Baert

et al. 2024

Ecology

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Agricultural intensification has been identified as one of the key causes of global insect biodiversity losses. These losses have been further linked to the widespread use of agrochemicals associated with modern agricultural practices. Many of these chemicals are known to have negative sublethal effects on commercial pollinators, such as managed honeybees and bumblebees, but less is known about the impacts on wild bees. Laboratory‐based studies with commercial pollinators have consistently shown that pesticide exposure can impact bee behavior, with cascading effects on foraging performance, reproductive success, and pollination services. However, these studies typically assess only one chemical, neglecting the complexity of real‐world exposure to multiple agrochemicals and other stressors. In the summer of 2020, we collected wild‐foraging workers of the common eastern bumblebee, Bombus impatiens, from five squash (Cucurbita) agricultural sites (organic and conventional farms), selected to represent a range of agrochemical, including neonicotinoid insecticide, use. For each bee, we measured two behaviors relevant to foraging success and previously shown to be impacted by pesticide exposure: sucrose responsiveness and locomotor activity. Following behavioral testing, we used liquid chromatography–tandem mass spectrometry (LC–MS/MS) chemical analysis to detect and quantify the presence of 92 agrochemicals in each bumblebee. Bees collected from our sites did not vary in pesticide exposure as expected. While we found a limited occurrence of neonicotinoids, two fungicides (azoxystrobin and difenoconazole) were detected at all sites, and the pesticide synergist piperonyl butoxide (PBO) was present in all 123 bees. We found that bumblebees that contained higher levels of PBO were less active, and this effect was stronger for larger bumblebee workers. While PBO is unlikely to be the direct cause of the reduction in bee activity, it could be an indicator of exposure to pyrethroids and/or other insecticides that we were unable to directly quantify, but which PBO is frequently tank‐mixed with during pesticide applications on crops. We did not find a relationship between agrochemical exposure and bumblebee sucrose responsiveness. To our knowledge, this is the first evidence of a sublethal behavioral impact of agrochemical exposure on wild‐foraging bees.

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Discovery of octopamine and tyramine in nectar and their effects on bumblebee behavior

Cited by 18 publications

References 68 publications

Octopamine affects gustatory responsiveness and associative learning performance in bumble bees

Octopamine affects gustatory responsiveness and associative learning performance in bumble bees

Invasive ant learning is not affected by seven potential neuroactive chemicals

Field agrochemical exposure impacts locomotor activity in wild bumblebees

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