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Appetite is correlated with octopamine and hemolymph sugar levels in forager honeybees

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Abstract

Insects have rapidly changing energy demands, so they primarily rely on hemolymph and other carbohydrates to carry out life activities. However, how gustatory responsiveness and hemolymph sugar levels coordinate with one another to maintain energetic homeostasis in insects remains largely unknown for the highly social honeybee that goes through large physiological and behavioral changes. The potential role of biogenic amines and neuropeptides in the connection between the regulation of appetite and fluctuating sugar levels in the hemolymph, due to starvation, as the bee ages, was investigated. The largest appetite increase due to the starvation treatment was within the forager age class and this corresponded with an increase in octopamine levels in the brain along with a decline in hemolymph sugar levels. Adipokinetic hormone (AKH) was found in very small quantities in the brain and there were no significant changes in response to starvation treatment. Our findings suggest that the particularly dynamic levels of hemolymph sugar levels may serve as a monitor of the forager honeybee energetic state. Therefore, there may be a pathway in forager bees via octopamine responsible for their precise precipitous regulation of appetite, but to determine cause and effect relationships further investigation is needed.

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Abbreviations

AKH:

Adipokinetic hormone

GC–MS:

Gas chromatography–mass spectrometry

GLM:

Generalized linear model

GRS:

Gustatory response score

HPLC:

High-performance liquid chromatography

MANOVA:

Multivariate analysis of variance

PER assay:

Proboscis extension response assay

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Acknowledgements

We thank Mariann Pü, Brian Shields, Rebecca Zhou, Victor Le, and Elizabeth Eppley for assistance with hemolymph extractions, brain dissections, and data collection. The authors would also like to thank Dr. Kathleen Howard for providing access to her lyophilizer and assisting with its use. This work was supported by an Alexander von Humboldt Foundation Fellowship award to CM, a Swarthmore College Surdna Summer Research Fellowship to KC, and a Howard Hughes Medical Institute Fellowship to NP.

Data availability

The datasets generated during the current study are available in the Open Science Framework repository, https://osf.io/h4c6e/.

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Authors and Affiliations

  1. Institute for Biology/General Zoology, Martin-Luther-University Halle-Wittenberg, 06120, Halle (Saale), Germany

    Christopher Mayack

  2. Department of Biology, Swarthmore College, Swarthmore, PA, 19081, USA

    Christopher Mayack, Nicole Phalen & Kathleen Carmichael

  3. Molecular Biology, Genetics, and Bioengineering, Faculty of Engineering and Natural Sciences, Sabancı University, 34956, Istanbul, Turkey

    Christopher Mayack

  4. Department of Chemistry, Haverford College, Haverford, PA, 19041, USA

    Helen K. White

  5. Institute of Agricultural and Nutritional Sciences, Martin-Luther-University Halle-Wittenberg, 06120, Halle (Saale), Germany

    Frank Hirche & Gabriele I. Stangl

  6. School of Life Sciences, Arizona State University, Tempe, AZ, 85287, USA

    Ying Wang & Gro V. Amdam

  7. Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, 1432, Ås, Norway

    Gro V. Amdam

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  1. Christopher Mayack
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Correspondence to Christopher Mayack.

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All honeybees were handled humanely in accordance with current ethical standards. Special ethical approval is not required to carry out this study.

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Mayack, C., Phalen, N., Carmichael, K. et al. Appetite is correlated with octopamine and hemolymph sugar levels in forager honeybees. J Comp Physiol A 205, 609–617 (2019). https://doi.org/10.1007/s00359-019-01352-2

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