@article{ThammSchollReimetal.2017, author = {Thamm, Markus and Scholl, Christina and Reim, Tina and Gruebel, Kornelia and Moeller, Karin and Rossler, Wolfgang and Scheiner, Ricarda}, title = {Neuronal distribution of tyramine and the tyramine receptor AmTAR1 in the honeybee brain}, series = {The journal of comparative neurology}, volume = {525}, journal = {The journal of comparative neurology}, publisher = {Wiley}, address = {Hoboken}, issn = {0021-9967}, doi = {10.1002/cne.24228}, pages = {2615 -- 2631}, year = {2017}, abstract = {Tyramine is an important neurotransmitter, neuromodulator, and neurohormone in insects. In honeybees, it is assumed to have functions in modulating sensory responsiveness and controlling motor behavior. Tyramine can bind to two characterized receptors in honeybees, both of which are coupled to intracellular cAMP pathways. How tyramine acts on neuronal, cellular and circuit levels is unclear. We investigated the spatial brain expression of the tyramine receptor AmTAR1 using a specific antibody. This antibody detects a membrane protein of the expected molecular weight in western blot analysis. In honeybee brains, it labels different structures which process sensory information. Labeling along the antennal nerve, in projections of the dorsal lobe and in the gnathal ganglion suggest that tyramine receptors are involved in modulating gustatory and tactile perception. Furthermore, the ellipsoid body of the central complex and giant synapses in the lateral complex show AmTAR1-like immunoreactivity (AmTAR1-IR), suggesting a role of this receptor in modulating sky-compass information and/or higher sensor-motor control. Additionally, intense signals derive from the mushroom bodies, higher-order integration centers for olfactory, visual, gustatory and tactile information. To investigate whether AmTAR1-expressing brain structures are in vicinity to tyramine releasing sites, a specific tyramine antibody was applied. Tyramine-like labeling was observed in AmTAR1-IR positive structures, although it was sometimes weak and we did not always find a direct match of ligand and receptor. Moreover, tyramine-like immunoreactivity was also found in brain regions without AmTAR1-IR (optic lobes, antennal lobes), indicating that other tyramine-specific receptors may be expressed there.}, language = {en} } @misc{ScheinerBaumannBlenau2006, author = {Scheiner, Ricarda and Baumann, Arnd and Blenau, Wolfgang}, title = {Aminergic control and modulation of honeybee behaviour}, url = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus-46106}, year = {2006}, abstract = {Biogenic amines are important messenger substances in the central nervous system and in peripheral organs of vertebrates and of invertebrates. The honeybee, Apis mellifera, is excellently suited to uncover the functions of biogenic amines in behaviour, because it has an extensive behavioural repertoire, with a number of biogenic amine receptors characterised in this insect. In the honeybee, the biogenic amines dopamine, octopamine, serotonin and tyramine modulate neuronal functions in various ways. Dopamine and serotonin are present in high concentrations in the bee brain, whereas octopamine and tyramine are less abundant. Octopamine is a key molecule for the control of honeybee behaviour. It generally has an arousing effect and leads to higher sensitivity for sensory inputs, better learning performance and increased foraging behaviour. Tyramine has been suggested to act antagonistically to octopamine, but only few experimental data are available for this amine. Dopamine and serotonin often have antagonistic or inhibitory effects as compared to octopamine. Biogenic amines bind to membrane receptors that primarily belong to the large gene-family of GTP-binding (G) protein coupled receptors. Receptor activation leads to transient changes in concentrations of intracellular second messengers such as cAMP, IP3 and/or Ca2+. Although several biogenic amine receptors from the honeybee have been cloned and characterised more recently, many genes still remain to be identified. The availability of the completely sequenced genome of Apis mellifera will contribute substantially to closing this gap. In this review, we will discuss the present knowledge on how biogenic amines and their receptor-mediated cellular responses modulate different behaviours of honeybees including learning processes and division of labour.}, language = {en} } @misc{BlenauScheinerPlueckhahnetal.2002, author = {Blenau, Wolfgang and Scheiner, Ricarda and Pl{\"u}ckhahn, Stephanie and Oney, Bahar and Erber, Joachim}, title = {Behavioural pharmacology of octopamine, tyramine and dopamine in honey bees}, url = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus-44308}, year = {2002}, abstract = {In the honey bee, responsiveness to sucrose correlates with many behavioural parameters such as age of first foraging, foraging role and learning. Sucrose responsiveness can be measured using the proboscis extension response (PER) by applying sucrose solutions of increasing concentrations to the antenna of a bee. We tested whether the biogenic amines octopamine, tyramine and dopamine, and the dopamine receptor agonist 2-amino-6,7-dihydroxy-1,2,3,4-tetrahydronaphthalene (6,7-ADTN) can modulate sucrose responsiveness. The compounds were either injected into the thorax or fed in sucrose solution to compare different methods of application. Injection and feeding of tyramine or octopamine significantly increased sucrose responsiveness. Dopamine decreased sucrose responsiveness when injected into the thorax. Feeding of dopamine had no effect. Injection of 6,7-ADTN into the thorax and feeding of 6,7-ADTN reduced sucrose responsiveness significantly. These data demonstrate that sucrose responsiveness in honey bees can be modulated by biogenic amines, which has far reaching consequences for other types of behaviour in this insect. (C) 2002 Elsevier Science B.V. All rights reserved.}, language = {en} } @misc{ScheinerAbramsonBrodschneideretal.2013, author = {Scheiner, Ricarda and Abramson, Charles I. and Brodschneider, Robert and Crailsheim, Karl and Farina, Walter M. and Fuchs, Stefan and Gr{\"u}newald, Bernd and Hahshold, Sybille and Karrer, Marlene and Koeniger, Gudrun and K{\"o}niger, Niko and Menzel, Randolf and Mujagic, Samir and Radspieler, Gerald and Schmickl, Thomas and Schneider, Christof and Siegel, Adam J. and Szopek, Martina and Thenius, Ronald}, title = {Standard methods for behavioural studies of Apis mellifera}, series = {Journal of apicultural research}, volume = {52}, journal = {Journal of apicultural research}, number = {4}, publisher = {International Bee Research Association}, address = {Cardiff}, issn = {0021-8839}, doi = {10.3896/IBRA.1.52.4.04}, pages = {58}, year = {2013}, abstract = {In this BEEBOOK paper we present a set of established methods for quantifying honey bee behaviour. We start with general methods for preparing bees for behavioural assays. Then we introduce assays for quantifying sensory responsiveness to gustatory, visual and olfactory stimuli. Presentation of more complex behaviours like appetitive and aversive learning under controlled laboratory conditions and learning paradigms under free-flying conditions will allow the reader to investigate a large range of cognitive skills in honey bees. Honey bees are very sensitive to changing temperatures. We therefore present experiments which aim at analysing honey bee locomotion in temperature gradients. The complex flight behaviour of honey bees can be investigated under controlled conditions in the laboratory or with sophisticated technologies like harmonic radar or RFID in the field. These methods will be explained in detail in different sections. Honey bees are model organisms in behavioural biology for their complex yet plastic division of labour. To observe the daily behaviour of individual bees in a colony, classical observation hives are very useful. The setting up and use of typical observation hives will be the focus of another section. The honey bee dance language has important characteristics of a real language and has been the focus of numerous studies. We here discuss the background of the honey bee dance language and describe how it can be studied. Finally, the mating of a honey bee queen with drones is essential to survival of the entire colony. We here give detailed and structured information how the mating behaviour of drones and queens can be observed and experimentally manipulated. The ultimate goal of this chapter is to provide the reader with a comprehensive set of experimental protocols for detailed studies on all aspects of honey bee behaviour including investigation of pesticide and insecticide effects.}, language = {en} } @article{ReimThammRolkeetal.2013, author = {Reim, Tina and Thamm, Markus and Rolke, Daniel and Blenau, Wolfgang and Scheiner, Ricarda}, title = {Suitability of three common reference genes for quantitative real-time PCR in honey bees}, series = {Apidologie : a quality journal in bee science}, volume = {44}, journal = {Apidologie : a quality journal in bee science}, number = {3}, publisher = {Springer}, address = {Paris}, issn = {0044-8435}, doi = {10.1007/s13592-012-0184-3}, pages = {342 -- 350}, year = {2013}, abstract = {Honey bees are important model organisms for neurobiology, because they display a large array of behaviors. To link behavior with individual gene function, quantitative polymerase chain reaction is frequently used. Comparing gene expression of different individuals requires data normalization using adequate reference genes. These should ideally be expressed stably throughout lifetime. Unfortunately, this is frequently not the case. We studied how well three commonly used reference genes are suited for this purpose and measured gene expression in the brains of honey bees differing in age and social role. Although rpl32 is used most frequently, it only remains stable in expression between newly emerged bees, nurse-aged bees, and pollen foragers but shows a peak at the age of 12 days. The genes gapdh and ef1 alpha-f1, in contrast, are expressed stably in the brain throughout all age groups except newly emerged bees. According to stability software, gapdh was expressed most stably, followed by rpl32 and ef1 alpha-f1.}, language = {en} } @article{ScheinerSteinbachClassenetal.2014, author = {Scheiner, Ricarda and Steinbach, Anne and Classen, Gerbera and Strudthoff, Nicole and Scholz, Henrike}, title = {Octopamine indirectly affects proboscis extension response habituation in Drosophila melanogaster by controlling sucrose responsiveness}, series = {Journal of insect physiology}, volume = {69}, journal = {Journal of insect physiology}, publisher = {Elsevier}, address = {Oxford}, issn = {0022-1910}, doi = {10.1016/j.jinsphys.2014.03.011}, pages = {107 -- 117}, year = {2014}, abstract = {Octopamine is an important neurotransmitter in insects with multiple functions. Here, we investigated the role of this amine in a simple form of learning (habituation) in the fruit fly Drosophila melanogaster. Specifically, we asked if octopamine is necessary for normal habituation of a proboscis extension response (PER) to different sucrose concentrations. In addition, we analyzed the relationship between responsiveness to sucrose solutions applied to the tarsus and habituation of the proboscis extension response in the same individual. The Tyramine-beta-hydroxylase (T beta h) mutant lacks the enzyme catalyzing the final step of octopamine synthesis. This mutant was significantly less responsive to sucrose than controls. The reduced responsiveness directly led to faster habituation. Systemic application of octopamine or induction of octopamine synthesis by T beta h expression in a cluster of octopaminergic neurons within the suboesophageal ganglion restored sucrose responsiveness and habituation of octopamine mutants to control level. Further analyses imply that the reduced sucrose responsiveness of T beta h mutants is related to a lower sucrose preference, probably due to a changed carbohydrate metabolism, since T beta h mutants survived significantly longer under starved conditions. These findings suggest a pivotal role for octopamine in regulating sucrose responsiveness in fruit flies. Further, octopamine indirectly influences non-associative learning and possibly associative appetitive learning by regulating the evaluation of the sweet component of a sucrose reward. (C) 2014 Elsevier Ltd. All rights reserved.}, language = {en} } @article{BehrendsScheiner2012, author = {Behrends, Andreas and Scheiner, Ricarda}, title = {Octopamine improves learning in newly emerged bees but not in old foragers}, series = {JOURNAL OF EXPERIMENTAL BIOLOGY}, volume = {215}, journal = {JOURNAL OF EXPERIMENTAL BIOLOGY}, number = {7}, publisher = {COMPANY OF BIOLOGISTS LTD}, address = {CAMBRIDGE}, issn = {0022-0949}, doi = {10.1242/jeb.063297}, pages = {1076 -- 1083}, year = {2012}, abstract = {Honey bees (Apis mellifera) are well known for their excellent learning abilities. Although most age groups learn quickly to associate an odor with a sucrose reward, newly emerged bees and old foragers often perform poorly. For a long time, the reason for the poor learning performance of these age groups was unclear. We show that reduced sensitivity for sucrose is the cause for poor associative learning in newly emerged bees but not in old foragers. By increasing the sensitivity for sucrose through octopamine, we selectively improved the learning performance of insensitive newly emerged bees. Interestingly, the learning performance of foragers experiencing the same treatment remained low, despite the observed increase in sensitivity for the reward. We thus demonstrate that increasing sensitivity for the reward can improve the associative learning performance of bees when they are young but not when they had foraged for a long time. Importantly, octopamine can have very different effects on bees, depending on their initial sensory sensitivity. These differential effects of octopamine have important consequences for interpreting the action of biogenic amines on insect behavior.}, language = {en} } @article{ReimScheiner2014, author = {Reim, Tina and Scheiner, Ricarda}, title = {Division of labour in honey bees: age- and task-related changes in the expression of octopamine receptor genes}, series = {Insect molecular biology}, volume = {23}, journal = {Insect molecular biology}, number = {6}, publisher = {Wiley-Blackwell}, address = {Hoboken}, issn = {0962-1075}, doi = {10.1111/imb.12130}, pages = {833 -- 841}, year = {2014}, abstract = {The honey bee (Apis melliferaL.) has developed into an important ethological model organism for social behaviour and behavioural plasticity. Bees perform a complex age-dependent division of labour with the most pronounced behavioural differences occurring between in-hive bees and foragers. Whereas nurse bees, for example, stay inside the hive and provide the larvae with food, foragers leave the hive to collect pollen and nectar for the entire colony. The biogenic amine octopamine appears to play a major role in division of labour but the molecular mechanisms involved are unknown. We here investigated the role of two characterized octopamine receptors in honey bee division of labour. AmOctR1 codes for a Ca2+-linked octopamine receptor. AmOctR3/4 codes for a cyclic adenosine monophosphate-coupled octopamine receptor. Messenger RNA expression of AmOctR1 in different brain neuropils correlates with social task, whereas expression of AmOctR3/4 changes with age rather than with social role per se. Our results for the first time link the regulatory role of octopamine in division of labour to specific receptors and brain regions. They are an important step forward in our understanding of complex behavioural organization in social groups.}, language = {en} } @article{Scheiner2012, author = {Scheiner, Ricarda}, title = {Birth weight and sucrose responsiveness predict cognitive skills of honeybee foragers}, series = {Animal behaviour}, volume = {84}, journal = {Animal behaviour}, number = {2}, publisher = {Elsevier}, address = {London}, issn = {0003-3472}, doi = {10.1016/j.anbehav.2012.05.011}, pages = {305 -- 308}, year = {2012}, abstract = {Honeybees, Apis mellifera, can differ considerably in their birth weights but the consequences of these weight differences for behaviour are unknown. I investigated how these birth weight differences affected their cognitive skills when the bees reached foraging age. Individual sucrose responsiveness measured by the proboscis extension response is a strong determinant of appetitive olfactory learning performance in honeybees. Most of the observed learning differences between individuals or between genetic bee strains correlate with differences in their sucrose responsiveness. My second aim was therefore to investigate whether the sucrose responsiveness of newly emerged bees could predict the learning behaviour of the bees 3 weeks later. Both birth weight and sucrose responsiveness measured at emergence could predict olfactory learning scores as demonstrated by significant positive correlations. Heavy bees and bees with high sucrose responsiveness later learned better than lighter individuals or bees with lower responsiveness to sucrose at emergence. These results demonstrate for the first time a fundamental relationship between sensory responsiveness and morphology at emergence and later cognitive skills in insects. Because sensory responsiveness is closely linked to division of labour in honeybees, differences in weight and sucrose responsiveness at emergence might be involved in regulating division of labour.}, language = {en} } @article{ScheinerKulikovskajaThamm2014, author = {Scheiner, Ricarda and Kulikovskaja, Leonora and Thamm, Markus}, title = {The honey bee tyramine receptor AmTYR1 and division of foraging labour}, series = {The journal of experimental biology}, volume = {217}, journal = {The journal of experimental biology}, number = {8}, publisher = {Company of Biologists Limited}, address = {Cambridge}, issn = {0022-0949}, doi = {10.1242/jeb.098475}, pages = {1215 -- 1217}, year = {2014}, abstract = {Honey bees display a fascinating division of labour among foragers. While some bees solely collect pollen, others only collect nectar. It is assumed that individual differences in sensory response thresholds are at the basis of this division of labour. Biogenic amines and their receptors are important candidates for regulating the division of labour, because they can modulate sensory response thresholds. Here, we investigated the role of the honey bee tyramine receptor AmTYR1 in regulating the division of foraging labour. We report differential splicing of the Amtyr1 gene and show differential gene expression of one isoform in the suboesophageal ganglion of pollen and nectar foragers. This ganglion mediates gustatory inputs. These findings imply a role for the honey bee tyramine receptor in regulating the division of foraging labour, possibly through the suboesophageal ganglion.}, language = {en} } @article{ScheinerTotevaReimetal.2014, author = {Scheiner, Ricarda and Toteva, Anna and Reim, Tina and Sovik, Eirik and Barron, Andrew B.}, title = {Differences in the phototaxis of pollen and nectar foraging honey bees are related to their octopamine brain titers}, series = {Frontiers in physiology}, volume = {5}, journal = {Frontiers in physiology}, publisher = {Frontiers Research Foundation}, address = {Lausanne}, issn = {1664-042X}, doi = {10.3389/fphys.2014.00116}, pages = {8}, year = {2014}, abstract = {The biogenic amine octopamine is an important neuromodulator, neurohormone and neurotransmitter in insects. We here investigate the role of octopamine signaling in honey bee phototaxis. Our results show that groups of bees differ naturally in their phototaxis. Pollen forgers display a lower light responsiveness than nectar foragers. The lower phototaxis of pollen foragers coincides with higher octopamine titers in the optic lobes but is independent of octopamine receptor gene expression. Increasing octopamine brain titers reduces responsiveness to light, while tyramine application enhances phototaxis. These findings suggest an involvement of octopamine signaling in honey bee phototaxis and possibly division of labor, which is hypothesized to be based on individual differences in sensory responsiveness.}, language = {en} } @article{ThammScheiner2014, author = {Thamm, Markus and Scheiner, Ricarda}, title = {PKG in honey bees: spatial expression, amfor gene expression, sucrose responsiveness, and division of labor}, series = {The journal of comparative neurology}, volume = {522}, journal = {The journal of comparative neurology}, number = {8}, publisher = {Wiley-Blackwell}, address = {Hoboken}, issn = {0021-9967}, doi = {10.1002/cne.23500}, pages = {1786 -- 1799}, year = {2014}, abstract = {Division of labor is a hallmark of social insects. In honey bees, division of labor involves transition of female workers from one task to the next. The most distinct tasks are nursing (providing food for the brood) and foraging (collecting pollen and nectar). The brain mechanisms regulating this form of behavioral plasticity have largely remained elusive. Recently, it was suggested that division of labor is based on nutrition-associated signaling pathways. One highly conserved gene associated with food-related behavior across species is the foraging gene, which encodes a cyclic guanosine monophosphate (cGMP)-dependent protein kinase (PKG). Our analysis of this gene reveals the presence of alternative splicing in the honey bee. One isoform is expressed in the brain. Expression of this isoform is most pronounced in the mushroom bodies, the subesophageal ganglion, and the corpora allata. Division of labor and sucrose responsiveness in honey bees correlate significantly with foraging gene expression in distinct brain regions. Activating PKG selectively increases sucrose responsiveness in nurse bees to the level of foragers, whereas the same treatment does not affect responsiveness to light. These findings demonstrate a direct link between PKG signaling in distinct brain areas and division of labor. Furthermore, they demonstrate that the difference in sensory responsiveness between nurse bees and foragers can be compensated for by activating PKG. Our findings on the function of PKG in regulating specific sensory responsiveness and social organization offer valuable indications for the function of the cGMP/PKG pathway in many other insects and vertebrates. J. Comp. Neurol. 522:1786-1799, 2014. (c) 2013 Wiley Periodicals, Inc.}, language = {en} } @article{ScheinerReimSoviketal.2017, author = {Scheiner, Ricarda and Reim, Tina and Sovik, Eirik and Entler, Brian V. and Barron, Andrew B. and Thamm, Markus}, title = {Learning, gustatory responsiveness and tyramine differences across nurse and forager honeybees}, series = {The journal of experimental biology}, volume = {220}, journal = {The journal of experimental biology}, publisher = {Company of Biologists Limited}, address = {Cambridge}, issn = {0022-0949}, doi = {10.1242/jeb.152496}, pages = {1443 -- 1450}, year = {2017}, abstract = {Honeybees are well known for their complex division of labor. Each bee sequentially performs a series of social tasks during its life. The changes in social task performance are linked to gross differences in behavior and physiology. We tested whether honeybees performing different social tasks (nursing versus foraging) would differ in their gustatory responsiveness and associative learning behavior in addition to their daily tasks in the colony. Further, we investigated the role of the biogenic amine tyramine and its receptors in the behavior of nurse bees and foragers. Tyramine is an important insect neurotransmitter, which has long been neglected in behavioral studies as it was believed to only act as the metabolic precursor of the better-known amine octopamine. With the increasing number of characterized tyramine receptors in diverse insects, we need to understand the functions of tyramine on its own account. Our findings suggest an important role for tyramine and its two receptors in regulating honeybee gustatory responsiveness, social organization and learning behavior. Foragers, which were more responsive to gustatory stimuli than nurse bees and performed better in appetitive learning, also differed from nurse bees in their tyramine brain titers and in the mRNA expression of a tyramine receptor in the brain. Pharmacological activation of tyramine receptors increased gustatory responsiveness of nurse bees and foragers and improved appetitive learning in nurse bees. These data suggest that a large part of the behavioral differences between honeybees may be directly linked to tyramine signaling in the brain.}, language = {en} }