Abstract
Nectar mediates complex interactions between plants and animals. Recent research has focused on nectar secondary compounds that may play a role in regulating some of these interactions. These compounds may affect the behavior of nectar feeders by interacting with their neurobiology. Non-protein amino acids (NPAAs) can constitute a large portion of the amino acid content of floral nectar, but their ecological function has, to date, not been investigated. In this study, we tested the effects of diets with low and high concentrations of γ-amino butyric acid (GABA) and β-alanine on the survival and behavior of Bombus terrestris and Apis mellifera. The most apparent effect on longevity was observed for B. terrestris workers that fed on high concentration of GABA, with longevity increased. By contrast, neither of the two NPAAs (at either concentration) had an affect on A. mellifera longevity. At the low NPAA concentration, only B. terrestris workers showed a difference in consumption, consuming more β-alanine solution than the other two solutions. By contrast, at the high NPAA concentration, only A. mellifera workers showed a difference in consumption, consuming more β-alanine solution. The effects of the NPAAs on behavior differed between the two species, with B. terrestris appearing more sensitive to the NPAAs than A. mellifera. After consuming NPAAs, B. terrestris showed changes in three (walking, flying, stationary) of the four behaviors recorded, although the effects varied with concentration and compound. In contrast, honey bees only showed a change in feeding behavior, with consumption of both NPAAs (at low concentrations) resulting in a decrease. Thus, pollinator intake of NPAAs may have important behavioral/ecological implications.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adler LS (2000) The ecological significance of toxic nectar. Oikos 91:409–420. https://doi.org/10.1034/j.1600-0706.2000.910301.x
Archer CR, Pirk CW, Wright GA, Nicolson SW (2014) Nutrition affects survival in African honeybees exposed to interacting stressors. Funct Ecol 28:913–923. https://doi.org/10.1111/1365-2435.12226
Baker HG, Baker I (1977) Intraspecific constancy of floral nectar amino acid complements. Bot Gaz 138:183–191. https://doi.org/10.1086/336914
Baker HG, Baker I (1983) A brief historical review of the chemistry of floral nectar. In: Bentley B, Elias T (eds) The biology of nectaries. Columbia Univ Press, New York, pp 126–152
Bertazzini M, Medrzycki P, Bortolotti L, Maistrello L, Forlani G (2010) Amino acid content and nectar choice by forager honeybees (Apis mellifera L.). Amino Acids 39:315–318. https://doi.org/10.1007/s00726-010-0474-x
Bogo G (2016) Exploring plant-pollinator interactions: critical studies for the safeguard of wild Apoidea and spontaneous plant populations. In: PhD dissertation, Department of Biological, geological and environmental sciences. University of Bologna, Bologna
Bown AW, MacGregor KB, Shelp BJ (2006) Gamma-aminobutyrate: defense against invertebrate pests? Trends Plant Sci 11:424–427. https://doi.org/10.1016/j.tplants.2006.07.002
Breer H, Heilgenberg H (1985) Neurochemistry of GABAergic activities in the central nervous system of Locusta migratoria. J Comp Physiol A 157:343–354. https://doi.org/10.1007/BF00618124
Cook SC, Eubanks MD, Gold RE, Behmer ST (2010) Colony-level macronutrient regulation in ants: mechanisms, hoarding and associated costs. Anim Behav 79:429–437. https://doi.org/10.1016/j.anbehav.2009.11.022
Dussutour A, Simpson SJ (2009) Communal nutrition in ants. Curr Biol 19:740–744. https://doi.org/10.1016/j.cub.2009.03.015
Emran S, Yang M, He X, Zandveld J, Piper MD (2014) Target of rapamycin signalling mediates the lifespan-extending effects of dietary restriction by essential amino acid alteration. Aging 6:390–398. https://doi.org/10.18632/aging.100665
EPPO (2010) PP 1/170 (4): side-effects on honey bees. EPPO Bulletin 40:313–319
Faegri K, van der Pijl L (1979) The principles of pollination ecology. Pergamon Press, Oxford
Felicioli A, Sagona S, Galloni M, Bortolotti L, Bogo G, Guarnieri M, Nepi M (2018) Effects of non-protein amino acids on survival and locomotion of Osmia bicornis. Insect Mol Biol 27:556–563. https://doi.org/10.1111/imb.12496
González-Teuber M, Heil M (2009) Nectar chemistry is tailored for both attraction of mutualists and protection from exploiters. Plant Signal Behav 4:809–813. https://doi.org/10.4161/psb.4.9.9393
Gottsberger G, Arnold T, Linskens HF (1990) Variation in floral nectar amino acids with aging of flowers, pollen contamination, and flower damage. Israel J Bot 39:167–176. https://doi.org/10.1080/0021213X.1990.10677141
Grandison RC, Piper MD, Partridge L (2009) Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 462:1061–1064. https://doi.org/10.1038/nature08619
Grønli J, Fiske E, Murison R, Bjorvatn B, Sørensen E, Ursin R, Portas CM (2007) Extracellular levels of serotonin and GABA in the hippocampus after chronic mild stress in rats. A microdialysis study in an animal model of depression. Behav Brain Res 181:42–51. https://doi.org/10.1016/j.bbr.2007.03.018
Hamilton RL, Cooper RA, Schal C (1990) The influence of nymphal and adult dietary protein on food intake and reproduction in female brown-banded cockroaches. Entomol Exp Appl 55:23–31. https://doi.org/10.1111/j.1570-7458.1990.tb01344.x
Hosmer Jr DW, Lemeshow S (1999) Applied Survival Analysis: Time-to-Event, Wiley-Interscience publication. Wiley
Huang T, Jander G, de Vos M (2011) Non-protein amino acids in plant defense against insect herbivores: representative cases and opportunities for further functional analysis. Phytochemistry 72:1531–1537. https://doi.org/10.1016/j.phytochem.2011.03.019
Kessler D, Baldwin IT (2007) Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant J 49:840–854. https://doi.org/10.1111/j.1365-313X.2006.02995.x
Lee KP, Simpson SJ, Clissold FJ, Brooks R, Ballard JWO, Taylor PW, Soran N, Raubenheimer D (2008) Lifespan and reproduction in Drosophila: new insights from nutritional geometry. P Natl Acad Sci USA 105:2498–2503. https://doi.org/10.1073/pnas.0710787105
Maklakov AA, Simpson SJ, Zajitschek F, Hall MD, Dessmann J, Clissold F, Raubenheimer D, Bonduriansky R, Brooks RC (2008) Sex-specific fitness effects of nutrient intake on reproduction and lifespan. Curr Biol 18:1062–1066. https://doi.org/10.1016/j.cub.2008.06.059
Medrzycki P (2013) Funnel trap – a tool for selective collection of exiting forager bees for tests. J Apicult Res 52:122–123. https://doi.org/10.3896/IBRA.1.52.3.02
Min KJ, Tatar M (2006) Restriction of amino acids extends lifespan in Drosophila melanogaster. Mech Ageing Dev 127:643–646. https://doi.org/10.1016/j.mad.2006.02.005
Nepi M (2014) Beyond nectar sweetness: the hidden ecological role of non-protein amino acids in nectar. J Ecol 102:108–115. https://doi.org/10.1111/1365-2745.12170
Nicolson SW (2007) Nectar consumers. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Dordrecht, pp 289–342
Nicolson SW, Thornburg RW (2007) Nectar chemistry. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Dordrecht, pp 215–264. https://doi.org/10.1007/978-1-4020-5937-7_5
OECD (1998) OECD guideline for testing of chemicals. Test No 213: Honey bees, acute oral toxicity test
Paoli PP, Wakeling LA, Wright GA, Ford D (2014) The dietary proportion of essential amino acids and Sir2 influence lifespan in the honeybee. AGE 36:1239–1247. https://doi.org/10.1007/s11357-014-9649-9
Petanidou T (2007) Ecological and evolutionary aspects of floral nectars in Mediterranean habitats. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Dordrecht, pp 343–375. https://doi.org/10.1007/978-1-4020-5937-7_8
Petanidou T, Smets E (1996) Does temperature stress induce nectar secretion in Mediterranean plants? New Phytol 133:513–518. https://doi.org/10.1111/j.1469-8137.1996.tb01919.x
Petanidou T, Van Laere A, Ellis WN, Smets E (2006) What shapes amino acid and sugar composition in Mediterranean floral nectars? Oikos 115:155–169. https://doi.org/10.1111/j.2006.0030-1299.14487.x
Pirk CWW, Boodhoo C, Human H, Nicolson SW (2010) The importance of protein type and protein to carbohydrate ratio for survival and ovarian activation of caged honeybees (Apis mellifera scutellata). Apidologie 41:62–72. https://doi.org/10.1051/apido/2009055
Rossi M, Fisogni A, Nepi M, Quaranta M, Galloni M (2014) Bouncy versus idles: on the different role of pollinators in the generalist Gentiana lutea L. Flora 209:164–171
Schoonhoven LM, van Loon B, van Loon JJA, Dicke M (2005) Insect–plant biology. Oxford University Press, Oxford
Sgolastra F, Medrzycki P, Bortolotti L, Renzi MT, Tosi S, Bogo G, Teper D, Porrini C, Molowny-Horas R, Bosch J (2017) Synergistic mortality between a neonicotinoid insecticide and an ergosterol-biosynthesis-inhibiting fungicide in three bee species. Pest Manag Sci 73:1236–1243. https://doi.org/10.1002/ps.4449
Stabler D, Paoli PP, Nicolson SW, Wright GA (2015) Nutrient balancing of the adult worker bumblebee (Bombus terrestris) depends on the dietary source of essential amino acids. J Exp Biol 218:793–802. https://doi.org/10.1242/jeb.114249
Stevenson PA (1999) Colocalisation of taurine- with transmitter-immunoreactivities in the nervous system of the migratory locust. J Comp Neurol 404:86–96. https://doi.org/10.1002/(SICI)1096-9861(19990201)404:1<86::AID-CNE7>3.0.CO;2-8
Stevenson PC, Nicolson SW, Wright GA (2017) Plant secondary metabolites in nectar: impacts on pollinators and ecological functions. Funct Ecol 31:65–75. https://doi.org/10.1111/1365-2435.12761
Straub L, Williams GR, Pettis J, Fries I, Neumann P (2015) Superorganism resilience: eusociality and susceptibility of ecosystem service providing insects to stressors. Curr Opin Insect Sci 12:109–112. https://doi.org/10.1016/j.cois.2015.10.010
Vranova V, Rejsek K, Skene KR, Formanek P (2011) Non-protein amino acids: plant, soil and ecosystem interactions. Plant Soil 342:31–48. https://doi.org/10.1007/s11104-010-0673-y
Vrzal EM, Allan SA, Hahn DA (2010) Amino acids in nectar enhance longevity of female Culex quinquefasciatus mosquitoes. J Insect Physiol 56:1659–1664. https://doi.org/10.1016/j.jinsphys.2010.06.011
Acknowledgements
We thank Joan Rabassa Juvanteny and Mariachiara Zanichelli for laboratory assistance. Dr. Bogo was supported by a research fellowship from the University of Bologna and Council for Agricultural Research and Economics - Research Centre for Agriculture and Environment (CREA-AA).
Author information
Authors and Affiliations
Contributions
MN, MG, LB and AF conceived the ideas; GB, LB, AF and SS designed the methodology; GB, LB, MB and MG collected the data; GB, LB and MN analysed the data; GB, LB, MN, AF, SS, MB and MG led writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
ESM 1
(DOC 447 kb)
Rights and permissions
About this article
Cite this article
Bogo, G., Bortolotti, L., Sagona, S. et al. Effects of Non-Protein Amino Acids in Nectar on Bee Survival and Behavior. J Chem Ecol 45, 278–285 (2019). https://doi.org/10.1007/s10886-018-01044-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-018-01044-2