Colonies of the red harvester ant, Pogonomyrmex barbatus, regulate foraging activity based on food availability and local conditions. Colony variation in foraging behavior is thought to be linked to biogenic amine signaling and metabolism. Measurements of differences in neurotransmitters have not been made among ant colonies in a natural environment. Here, for the first time, we quantified tissue content of 4 biogenic amines (dopamine, serotonin, octopamine, and tyramine) in single forager brains from 9 red harvester ant colonies collected in the field. Capillary electrophoresis coupled with fast-scan cyclic voltammetry (CE-FSCV) was used to separate and detect the amines in individual ant brains. Low levels of biogenic amines were detected using field-amplified sample stacking by preparing a single brain tissue sample in acetonitrile and perchloric acid. The method provides low detection limits: 1 nM for dopamine, 2 nM for serotonin, 5 nM for octopamine, and 4 nM for tyramine. Overall, the content of dopamine (47 ± 9 pg/brain) was highest, followed by octopamine (36 ± 10 pg/brain), serotonin (20 ± 4 pg/brain), and tyramine (14 ± 3 pg/brain). Relative standard deviations were high, but there was less variation within a colony than among colonies, so the neurotransmitter content of each colony might change with environmental conditions. This study demonstrates that CE-FSCV is a useful method for investigating natural variation in neurotransmitter content in single ant brains and could be useful for future studies correlating tissue content with colony behavior such as foraging.
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The data supports the finding of this study are available in figshare [DOI: https://doi.org/10.6084/m9.figshare.10023080].
Barron AB, Søvik E, Cornish JL. The roles of dopamine and related compounds in reward-seeking behavior across animal phyla. Front Behav Neurosci. 2010;4:163.
Gordon DM. The rewards of restraint in the collective regulation of foraging by harvester ant colonies. Nature. 2013;498(7452):91–3.
Jandt J, Gordon D. The behavioral ecology of variation in social insects. Curr Opin Insect Sci. 2016;15:40–4.
Friedman DA, Pilko A, Skowronska-Krawczyk D, Krasinska K, Parker JW, Hirsh J, et al. The role of dopamine in the collective regulation of foraging in harvester ants. iScience. 2018;8:283–94.
Friedman DA, Gordon DM. Ant genetics: reproductive physiology, worker morphology, and behavior. Annu Rev Neurosci. 2016;39(1):41–56.
Kamhi JF, Traniello JFA. Biogenic amines and collective organization in a superorganism: neuromodulation of social behavior in ants. Brain Behav Evol. 2013;82(4):220–36.
Kamhi JF, Arganda S, Moreau CS, Traniello JFA. Origins of aminergic regulation of behavior in complex insect social systems. Front Syst Neurosci. 2017;11:74.
Szczuka A, Korczyńska J, Wnuk A, Symonowicz B, Gonzalez Szwacka A, Mazurkiewicz P, Kostowski W, Godzinska. The effects of serotonin, dopamine, octopamine and tyramine on behavior of workers of the ant Formica polyctena during dyadic aggression tests. Acta Neurobiol Exp 2013;73(4):495–520.
Entler BV, Cannon JT, Seid MA. Morphine addiction in ants: a new model for self-administration and neurochemical analysis. J Exp Biol. 2016;219(Pt 18):2865–9.
Wada-Katsumata A, Yamaoka R, Aonuma H. Social interactions influence dopamine and octopamine homeostasis in the brain of the ant Formica japonica. J Exp Biol. 2011;214(10):1707–13.
Cuvillier-Hot Alain Lenoir V. Biogenic amine levels, reproduction and social dominance in the queenless ant Streblognathus peetersi. Naturwissenschaften. 2006;93:149–53.
Okada Y, Sasaki K, Miyazaki S, Shimoji H, Tsuji K, Miura T. Social dominance and reproductive differentiation mediated by dopaminergic signaling in a queenless ant. J Exp Biol. 2015;218(Pt 7):1091–8.
Fang H, Pajski ML, Ross AE, Venton BJ. Quantitation of dopamine, serotonin and adenosine content in a tissue punch from a brain slice using capillary electrophoresis with fast-scan cyclic voltammetry detection. Anal Methods. 2013;5(11):2704–11.
Fang H, Vickrey TL, Venton BJ. Analysis of biogenic amines in a single Drosophila larva brain by capillary electrophoresis with fast-scan cyclic voltammetry detection. Anal Chem. 2011;83(6).
Denno ME, Privman E, Borman RP, Wolin DC, Venton BJ. Quantification of histamine and carcinine in Drosophila melanogaster tissues. ACS Chem Neurosci. 2016;7(3):407–14.
Denno ME, Privman E, Venton BJ. Analysis of neurotransmitter tissue content of drosophila melanogaster in different life stages. ACS Chem Neurosci. 2015;6(1):117–23.
Berglund EC, Kuklinski NJ, Karagunduz E, Ucar K, Hanrieder J, Ewing AG. Freeze-drying as sample preparation for micellar electrokinetic capillary chromatography-electrochemical separations of neurochemicals in Drosophila brains. Anal Chem. 2013;85(5):2841–6.
Kuklinski NJ, Berglund EC, Engelbrektsson J, Ewing AG. Biogenic amines in microdissected brain regions of Drosophila melanogaster measured with micellar electrokinetic capillary chromatography-electrochemical detection. Anal Chem. 2010;82(18):7729–35.
Omiatek DM, Santillo MF, Heien ML, Ewing AG. Hybrid capillary-microfluidic device for the separation, lysis, and electrochemical detection of vesicles. Anal Chem. 2009;81(6):2294–302.
Ream PJ, Suljak SW, Ewing AG, Han K-A. Micellar electrokinetic capillary chromatography- electrochemical detection for analysis of biogenic amines in Drosophila melanogaster. Anal Chem. 2003;75(16):3972–8.
Pyakurel P, Shin M, Venton BJ. Nicotinic acetylcholine receptor (nAChR) mediated dopamine release in larval Drosophila melanogaster. Neurochem Int. 2018;114:33–41.
Shin M, Field TM, Stucky CS, Furgurson MN, Johnson MA. Ex vivo measurement of electrically evoked dopamine release in zebrafish whole brain. ACS Chem Neurosci. 2017;8(9):1880–8.
Shin M, Copeland JM, Venton BJ. Drosophila as a model system for neurotransmitter measurements. ACS Chem Neurosci. 2018;9(8):1872–83.
Shin M, Venton BJ. Electrochemical measurements of acetylcholine-stimulated dopamine release in adult Drosophila melanogaster brains. Anal Chem. 2018;90(17):10318–25.
Cao Q, Puthongkham P, Venton BJ. Review: new insights into optimizing chemical and 3D surface structures of carbon electrodes for neurotransmitter detection. Anal Methods. 2019;11(3):247–61.
Ganesana M, Lee ST, Wang Y, Venton BJ. Analytical techniques in neuroscience: recent advances in imaging, separation, and electrochemical methods. Anal Chem. 2017;89(1):314–41.
Shin M, Wang Y, Borgus JR, Venton BJ. Electrochemistry at the synapse. Annu Rev Anal Chem. 2019 12;12(1):297–321.
Ingram KK, Pilko A, Heer J, Gordon DM. Colony life history and lifetime reproductive success of red harvester ant colonies. Coulson T, editor. J Anim Ecol 2013;82(3):540–550.
Cooper SE, Venton BJ. Fast-scan cyclic voltammetry for the detection of tyramine and octopamine. Anal Bioanal Chem. 2009;394(1):329–36.
Jackson BP, Dietz SM, Wightman RM. Fast-scan cyclic voltammetry of 5-hydroxytryptamine. Anal Chem. 1995;67(6):1115–20.
Hashemi P, Dankoski EC, Petrovic J, Keithley RB, Wightman RM. Voltammetric detection of 5-hydroxytryptamine release in the rat brain. Anal Chem. 2009;81(22):9462–71.
Hardie SL, Hirsh J. An improved method for the separation and detection of biogenic amines in adult Drosophila brain extracts by high performance liquid chromatography. J Neurosci Methods. 2006;153(2):243–9.
Aonuma H, Watanabe T. Changes in the content of brain biogenic amine associated with early colony establishment in the queen of the ant, Formica japonica. Gronenberg W, editor. PLoS One. 2012;7(8):e43377.
Mannino G, Abdi G, Emilio Maffei M, Barbero F. Origanum vulgare terpenoids modulate Myrmica scabrinodis brain biogenic amines and ant behaviour. PLoS One. 2018;13(12):e0211749.
Cook CN, Brent CS, Breed MD. Octopamine and tyramine modulate the thermoregulatory fanning response in honey bees (Apis mellifera). J Exp Biol. 2017;220(10):1925–30.
Brenes JC, Fornaguera J. The effect of chronic fluoxetine on social isolation-induced changes on sucrose consumption, immobility behavior, and on serotonin and dopamine function in hippocampus and ventral striatum. Behav Brain Res. 2009;198(1):199–205.
Meiser J, Weindl D, Hiller K. Complexity of dopamine metabolism. Cell Commun Signal. 2013;11(1):34.
Bauknecht P, Jékely G. Ancient coexistence of norepinephrine, tyramine, and octopamine signaling in bilaterians. BMC Biol. 2017;15(1):6.
Sloley B. Metabolism of monoamines in invertebrates: the relative importance of monoamine oxidase in different phyla. Neurotoxicology. 2004;25(1–2):175–83.
Yamamoto S, Seto ES. Dopamine dynamics and signaling in Drosophila: an overview of genes, drugs and behavioral paradigms. Exp Anim. 2014;63(2):107–19.
This research was funded by NIH R01MH085159 to the Venton Lab and a grant from the Stanford Neurosciences Institute to the Gordon lab.
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Published in the topical collection featuring Female Role Models in Analytical Chemistry.
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Shin, M., Friedman, D.A., Gordon, D.M. et al. Measurement of natural variation of neurotransmitter tissue content in red harvester ant brains among different colonies. Anal Bioanal Chem 412, 6167–6175 (2020). https://doi.org/10.1007/s00216-019-02355-3
- Neurotransmitters tissue content
- Pogonomyrmex barbatus/red harvester ants
- Capillary electrophoresis/electrophoresis
- Fast-scan cyclic voltammetry
- Carbon-Fiber microelectrode