Female hawkmoths, Manduca sexta, use olfactory cues to locate nectar sources and oviposition sites. We investigated if the behavioral significance of odorants is represented already in the antennal lobe, the first olfactory neuropil of the insect's brain. Using in vivo calcium imaging, we first established a functional map of the dorsal surface of the antennal lobe by stimulating the moths with 80 ecologically relevant and chemically diverse monomolecular odorants. We were able to address 23 olfactory glomeruli, functional subunits of the antennal lobe, in each individual female. Next, we studied the relevance of the same odorants with two-choice experiments (odorant versus solvent) in a wind tunnel. Depending on odorant identity, naive moths made attempts to feed or to oviposit at the scented targets. A correlation of wind tunnel results with glomerular activation patterns revealed that feeding and oviposition behaviors are encoded in the moth's antennal lobe by the activation of distinct groups of glomeruli.
Flying animals need continual sensory feedback about their body position and orientation for flight control. The visual system provides essential but slow feedback. In contrast, mechanosensory channels can provide feedback at much shorter timescales. How the contributions from these two senses are integrated remains an open question in most insect groups. In Diptera, fast mechanosensory feedback is provided by organs called halteres and is crucial for the control of rapid flight manoeuvres, while vision controls manoeuvres in lower temporal frequency bands. Here, we have investigated the visual-mechanosensory integration in the hawkmoth Macroglossum stellatarum. They represent a large group of insects that use Johnston’s organs in their antennae to provide mechanosensory feedback on perturbations in body position. Our experiments show that antennal mechanosensory feedback specifically mediates fast flight manoeuvres, but not slow ones. Moreover, we did not observe compensatory interactions between antennal and visual feedback.
Flying animals need constant sensory feedback about their body position and orientation for flight control. The visual system provides valuable but slow feedback. In contrast, mechanosensory channels can provide feedback at much shorter response times. How the contributions from the two senses are integrated is still an open question in most insect groups. In Diptera, fast mechanosensory feedback is provided by organs called halteres, and is crucial for the control of rapid flight manoeuvres, while vision controls manoeuvres in lower temporal frequency bands. Here we have investigated the visualmechanosensory integration in an insect which lacks halteres: the hawkmoth Macroglossum stellatarum. It is representative for a large group of insects that use mechanoreceptive Johnston's organs in their antennae to provide gyroscopic feedback on perturbations in body position. Highspeed videos of freely-flying hawkmoths hovering at stationary or oscillating artificial flowers show that positional fidelity during flight was reduced in antennectomised animals, but was rescued after antennal re-attachment. Our experiments show that antennal mechanosensory feedback specifically supports fast flight manoeuvres (flower oscillations between 2-6 Hz), but not slow ones. Differences in the reliability of visual feedback (in different light intensities) affected all antennal conditions equally, suggesting there was no compensatory interaction between antennal and visual feedback under the conditions tested. These results establish the importance of antennal mechanosensors in providing rapid mechanosensory feedback for finer control of flight manoeuvres, acting in parallel to visual feedback.not peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission.The copyright holder for this preprint (which was . http://dx.doi.org/10.1101/222448 doi: bioRxiv preprint first posted online Feb. 4, 2018; IntroductionThe impressive aerobatic manoeuvres of insects provide an insightful model for the neural control of flight and for the development of flying robots [Fuller et al. 2014]. Insect flight requires constant sensory feedback, both on body position relative to the environment, as well as on perturbations to body position. Visual feedback provides key information about flight parameters including ground speed, distance to obstacles and targets, and aerial displacements (for a review see [Srinivasan et al. 1999]). However, visual estimation of self-motion [Fuller et al. 2014, Hung et al. 2013] is limited by its temporal resolution and substantial latency to flight muscle activation [Sherman & Dickinson 2004, Suver et al. 2016. This is too slow to control very fast aerial manoeuvres, which require rapid sensory feedback before perturbations become too large and thus energetically costly to the animals [Bender & Dickinson 2006].Avoiding the temporal limitations set by the visual system, insects use mechanosensors to sense their own motion, as these can transduce perturbations on much faster time scales [Y...
Previous studies have considered floral humidity to be an inadvertent consequence of nectar evaporation, which could be exploited as a cue by nectar-seeking pollinators. By contrast, our interdisciplinary study of a night-blooming flower, Datura wrightii, and its hawkmoth pollinator, Manduca sexta, reveals that floral relative humidity acts as a mutually beneficial signal in this system. The distinction between cue- and signal-based functions is illustrated by three experimental findings. First, floral humidity gradients in Datura are nearly ten-fold greater than those reported for other species, and result from active (stomatal conductance) rather than passive (nectar evaporation) processes. These humidity gradients are sustained in the face of wind and are reconstituted within seconds of moth visitation, implying substantial physiological costs to these desert plants. Second, the water balance costs in Datura are compensated through increased visitation by Manduca moths, with concomitant increases in pollen export. We show that moths are innately attracted to humid flowers, even when floral humidity and nectar rewards are experimentally decoupled. Moreover, moths can track minute changes in humidity via antennal hygrosensory sensilla but fail to do so when these sensilla are experimentally occluded. Third, their preference for humid flowers benefits hawkmoths by reducing the energetic costs of flower handling during nectar foraging. Taken together, these findings suggest that floral humidity may function as a signal mediating the final stages of floral choice by hawkmoths, complementing the attractive functions of visual and olfactory signals beyond the floral threshold in this nocturnal plant-pollinator system.
Concern for pollinator health often focuses on social bees and their agricultural importance at the expense of other pollinators and their ecosystem services. When pollinating herbivores use the same plants as nectar sources and larval hosts, ecological conflicts emerge for both parties, as the pollinator's services are mitigated by herbivory and its larvae are harmed by plant defences. We tracked individual-level metrics of pollinator health—growth, survivorship, fecundity—across the life cycle of a pollinating herbivore, the common hawkmoth, Hyles lineata , interacting with a rare plant, Oenothera harringtonii , that is polymorphic for the common floral volatile ( R )-(−)-linalool. Linalool had no impact on floral attraction, but its experimental addition suppressed oviposition on plants lacking linalool. Plants showed robust resistance against herbivory from leaf-disc to whole-plant scales, through poor larval growth and survivorship. Higher larval performance on other Oenothera species indicates that constitutive herbivore resistance by O. harringtonii is not a genus-wide trait. Leaf volatiles differed among populations of O. harringtonii but were not induced by larval herbivory. Similarly, elagitannins and other phenolics varied among plant tissues but were not herbivore-induced. Our findings highlight asymmetric plant–pollinator interactions and the importance of third parties, including alternative larval host plants, in maintaining pollinator health. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.
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