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      Finding flowers in the dark: nectar-feeding bats integrate olfaction and echolocation while foraging for nectar

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          Abstract

          Nectar-feeding bats depend mainly on floral nectar to fulfil their energetic requirements. Chiropterophilous flowers generally present strong floral scents and provide conspicuous acoustic echoes to attract bats. While floral scents are assumed to attract bats over long distances, acoustic properties of flower structures may provide detailed information, thus supporting the localization of a flower at close ranges. So far, to our knowledge, there is no study trying to understand the relative importance as well as the combination of these generally coupled cues for detection (presence) and localization (exact position) of open flowers in nature. For a better comprehension of the significance of olfaction and echolocation in the foraging behaviour of nectar-feeding bats, we conducted two-choice experiments with Leptonycteris yerbabuenae. We tested the bats' behaviour in three experimental scenarios with different cues: (i) olfaction versus echolocation, (ii) echolocation versus echolocation and olfaction, and (iii) olfaction versus echolocation and olfaction. We used the floral scent of the bat-pollinated cactus Pachycereus pringlei as olfactory cue and an acrylic paraboloid as acoustic cue. Additionally, we recorded the echolocation behaviour of the bats and analysed the floral scent of P. pringlei. When decoupled cues were offered, bats displayed no preference in choice for any of the two cues. However, bats reacted first to and chose more often the coupled cues. All bats echolocated continuously and broadcast a long terminal group before a successful visit. The floral scent bouquet of P. pringlei is composed of 20 compounds, some of which (e.g. methyl benzoate) were already reported from chiropterophilous plants. Our investigation demonstrates for the first time to our knowledge, that nectar-feeding bats integrate over different sensory modes for detection and precise localization of open flowers. The combined information from olfactory and acoustic cues allows bats to forage more efficiently.

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          Most cited references21

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          Flowers as sensory billboards: progress towards an integrated understanding of floral advertisement.

          This paper explores the landscape of integrated sensory signals that are produced by flowers, and the contextual information that modulates pollinator responses to such signals. Chiloglottis orchids are pollinated by mimicking the pheromone and posture of female thynnine wasps, but floral height provides the context within which male wasps respond to these signals. The odor and appearance of carrion attract blowflies to Helicodiceros inflorescences, but flies are more likely to enter the floral chamber when heat is present as a contextual cue. Finally, fragrance, UV-visual cues and echo fingerprints are redundant signals that Glossophaga bats can use to find flowers, depending on prior experience and the photic environment.
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            Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb.

            We explored the spatio-temporal dynamics of odor-evoked activity in the rat and mouse main olfactory bulb (MOB) using voltage-sensitive dye imaging (VSDI) with a new probe. The high temporal resolution of VSDI revealed odor-specific sequences of glomerular activation. Increasing odor concentrations reduced response latencies, increased response amplitudes, and recruited new glomerular units. However, the sequence of glomerular activation was maintained. Furthermore, we found distributed MOB activity locked to the nasal respiration cycle. The spatial distribution of its amplitude and phase was heterogeneous and changed by sensory input in an odor-specific manner. Our data show that in the mammalian olfactory bulb, odor identity and concentration are represented by spatio-temporal patterns, rather than spatial patterns alone.
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              A Physiologically-Inspired Model of Numerical Classification Based on Graded Stimulus Coding

              In most natural decision contexts, the process of selecting among competing actions takes place in the presence of informative, but potentially ambiguous, stimuli. Decisions about magnitudes – quantities like time, length, and brightness that are linearly ordered – constitute an important subclass of such decisions. It has long been known that perceptual judgments about such quantities obey Weber's Law, wherein the just-noticeable difference in a magnitude is proportional to the magnitude itself. Current physiologically inspired models of numerical classification assume discriminations are made via a labeled line code of neurons selectively tuned for numerosity, a pattern observed in the firing rates of neurons in the ventral intraparietal area (VIP) of the macaque. By contrast, neurons in the contiguous lateral intraparietal area (LIP) signal numerosity in a graded fashion, suggesting the possibility that numerical classification could be achieved in the absence of neurons tuned for number. Here, we consider the performance of a decision model based on this analog coding scheme in a paradigmatic discrimination task – numerosity bisection. We demonstrate that a basic two-neuron classifier model, derived from experimentally measured monotonic responses of LIP neurons, is sufficient to reproduce the numerosity bisection behavior of monkeys, and that the threshold of the classifier can be set by reward maximization via a simple learning rule. In addition, our model predicts deviations from Weber Law scaling of choice behavior at high numerosity. Together, these results suggest both a generic neuronal framework for magnitude-based decisions and a role for reward contingency in the classification of such stimuli.
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                Author and article information

                Journal
                R Soc Open Sci
                R Soc Open Sci
                RSOS
                royopensci
                Royal Society Open Science
                The Royal Society
                2054-5703
                August 2016
                10 August 2016
                10 August 2016
                : 3
                : 8
                : 160199
                Affiliations
                [1 ]Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm , Albert-Einstein Allee 11, 89069 Ulm, Germany
                [2 ]Smithsonian Tropical Research Institute , Balboa, Panamá, República de Panamá
                Author notes
                Author for correspondence: Tania P. Gonzalez-Terrazas e-mail: tania.gonzalez@ 123456uni-ulm.de
                [†]

                Present address: Department of Fundamental Chemistry, Federal University of Pernambuco, Recife, Brazil.

                Article
                rsos160199
                10.1098/rsos.160199
                5108945
                27853595
                45418e0a-11a4-41a5-a134-4a229810e5a8
                © 2016 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 19 March 2016
                : 5 July 2016
                Funding
                Funded by: University of Ulm
                Award ID: CONACYT-DAAD
                Categories
                1001
                14
                Biology (Whole Organism)
                Research Article
                Custom metadata
                August, 2016

                acoustic cues,bat pollination,chiropterophily,columnar cactus,floral scent

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