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      Limitations of learning in the proboscis reflex of the flower visiting syrphid fly Eristalis tenax

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          Abstract

          Flower visiting Eristalis hoverflies feed on nectar and pollen and are known to rely on innate colour preferences. In addition to a preference for visiting yellow flowers, the flies possess an innate proboscis reflex elicited by chemical as well as yellow colour stimuli. In this study we show that the flies’ proboscis reflex is only triggered by yellow colour stimuli and not altered by conditioning to other colours. Neither in absolute nor in differential conditioning experiments the flies learned to associate other colours than yellow with reward. Even flies that experienced only blue nutrients during the first four days after hatching could not be trained to extend the proboscis towards other colours than yellow. The natural targets of the visually elicited proboscis reflex are yellow pollen and yellow anthers. One consequence of our findings is that flowers might advertise nectar and pollen rewards for Eristalis hoverflies by a yellow colour hue of nectar guides, nectaries, stamens or pollen. Alternatively, flowers might protect their pollen against Eristalis by displaying other pollen colours than yellow or direct flies by yellow pollen-mimicking floral guides towards nectar resources. Testing the proboscis extension of various hoverfly species in the field showed that only Eristalis hoverflies possess the proboscis reflex elicited by yellow colour hues.

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          Most cited references54

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          Flower Constancy, Insect Psychology, and Plant Evolution

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            Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees.

            The honeybee Apis mellifera has emerged as a robust and influential model for the study of classical conditioning, thanks to the existence of a powerful Pavlovian conditioning protocol, the olfactory conditioning of the proboscis extension response (PER). In 2011, the olfactory PER conditioning protocol celebrates 50 years since it was first introduced by Kimihisa Takeda in 1961. Here, we review its origins, developments, and perspectives in order to define future research avenues and necessary methodological and conceptual evolutions. We show that olfactory PER conditioning has become a versatile tool for the study of questions in extremely diverse fields in addition to the study of learning and memory and that it has allowed behavioral characterizations, not only of honeybees, but also of other insect species, for which the protocol was adapted. We celebrate, therefore, Takeda's original work and prompt colleagues to conceive and establish further robust behavioral tools for an accurate characterization of insect learning and memory at multiple levels of analysis.
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              Evolutionary biology of insect learning.

              Learning and memory, defined as the acquisition and retention of neuronal representations of new information, are ubiquitous among insects. Recent research indicates that a variety of insects rely extensively on learning for all major life activities including feeding, predator avoidance, aggression, social interactions, and sexual behavior. There is good evidence that individuals within an insect species exhibit genetically based variation in learning abilities and indirect evidence linking insect learning to fitness. Although insects rely on innate behavior to successfully manage many types of variation and unpredictability, learning may be superior to innate behavior when dealing with features unique to time, place, or individuals. Among insects, social learning , which can promote the rapid spread of novel behaviors, is currently known only from a few well-studied examples in social Hymenoptera. The prevalence and importance of social learning in insects are still unknown. Similarly, we know little about ecological factors that may have promoted enhanced learning abilities in insects, and whether learning has significantly contributed to speciation in insects.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: SupervisionRole: Writing – original draft
                Role: InvestigationRole: Writing – review & editing
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                20 March 2018
                2018
                : 13
                : 3
                : e0194167
                Affiliations
                [1 ] Institute of Sensory Ecology, Biology Department, Heinrich-Heine-University, Düsseldorf, Germany
                [2 ] College of Plant Protection, Hebei Agricultural University, Baoding, China
                University of Sussex, UNITED KINGDOM
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-5184-4201
                Article
                PONE-D-17-41852
                10.1371/journal.pone.0194167
                5860702
                29558491
                131d890c-4019-4fa7-b351-e5c45f6a3499
                © 2018 Lunau et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 28 November 2017
                : 26 February 2018
                Page count
                Figures: 10, Tables: 0, Pages: 20
                Funding
                The authors received no specific funding for this work.
                Categories
                Research Article
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Flowers
                Biology and Life Sciences
                Neuroscience
                Reflexes
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Pollen
                Biology and Life Sciences
                Behavior
                Behavioral Conditioning
                Biology and Life Sciences
                Behavior
                Conditioned Response
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Hymenoptera
                Bees
                Honey Bees
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Biology and Life Sciences
                Neuroscience
                Cognitive Science
                Cognitive Psychology
                Learning
                Biology and Life Sciences
                Psychology
                Cognitive Psychology
                Learning
                Social Sciences
                Psychology
                Cognitive Psychology
                Learning
                Biology and Life Sciences
                Neuroscience
                Learning and Memory
                Learning
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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