ABSTRACT
The interaction between insects and the flowers they pollinate has driven the evolutionary diversity of both insects and flowering plants, two groups with the most numerous species on Earth. Insects use vision and olfaction to localize host plants, but we know relatively little about how they find the tiny nectary opening in the flower, which can be well beyond their visual resolution. Especially when vision is limited, touch becomes crucial in successful insect-plant pollination interactions. Here, we studied the remarkable feeding behavior of crepuscular hawkmoths Manduca sexta, which use their long, actively controlled, proboscis to expertly explore flower-like surfaces. Using machine vision and 3D-printed artificial flower-like feeders, we revealed a novel behavior that shows moths actively probe surfaces, sweeping their proboscis from the feeder edge to its center repeatedly until they locate the nectary opening. Moreover, naive moths rapidly learn to exploit these flowers, and they adopt a tactile search strategy to more directly locate the nectary opening in as few as three to five consecutive visits. Our results highlight the proboscis as a unique active sensory structure and emphasize the central role of touch in nectar foraging insect-plant pollinator interactions.
Subject(s)
Manduca , Touch , Animals , Flowers , Plant Nectar , Plants , PollinationABSTRACT
Nocturnal insects like moths are essential for pollination, providing resilience to the diurnal pollination networks. Moths use both vision and mechanosensation to locate the nectary opening in the flowers with their proboscis. However, increased light levels due to artificial light at night (ALAN) pose a serious threat to nocturnal insects. Here, we examined how light levels influence the efficacy by which the crepuscular hawkmoth Manduca sexta locates the nectary. We used three-dimensional-printed artificial flowers fitted with motion sensors in the nectary and machine vision to track the motion of hovering moths under two light levels: 0.1 lux (moonlight) and 50 lux (dawn/dusk). We found that moths in higher light conditions took significantly longer to find the nectary, even with repeated visits to the same flower. In addition to taking longer, moths in higher light conditions hovered further from the flower during feeding. Increased light levels adversely affect learning and motor control in these animals.
Subject(s)
Manduca , Moths , Animals , Flowers , Learning , PollinationABSTRACT
The spectacular success and diversification of insects rests critically on two major evolutionary adaptations. First, the evolution of flight, which enhanced the ability of insects to colonize novel ecological habitats, evade predators, or hunt prey; and second, the miniaturization of their body size, which profoundly influenced all aspects of their biology from development to behavior. However, miniaturization imposes steep demands on the flight system because smaller insects must flap their wings at higher frequencies to generate sufficient aerodynamic forces to stay aloft; it also poses challenges to the sensorimotor system because precise control of wing kinematics and body trajectories requires fast sensory feedback. These tradeoffs are best studied in Dipteran flies in which rapid mechanosensory feedback to wing motor system is provided by halteres, reduced hind wings that evolved into gyroscopic sensors. Halteres oscillate at the same frequency as and precisely antiphase to the wings; they detect body rotations during flight, thus providing feedback that is essential for controlling wing motion during aerial maneuvers. Although tight phase synchrony between halteres and wings is essential for providing proper timing cues, the mechanisms underlying this coordination are not well understood. Here, we identify specific mechanical linkages within the thorax that passively mediate both wing-wing and wing-haltere phase synchronization. We demonstrate that the wing hinge must possess a clutch system that enables flies to independently engage or disengage each wing from the mechanically linked thorax. In concert with a previously described gearbox located within the wing hinge, the clutch system enables independent control of each wing. These biomechanical features are essential for flight control in flies.
Subject(s)
Diptera/physiology , Wings, Animal/physiology , Animals , Biomechanical Phenomena , Microscopy, Electron, ScanningABSTRACT
Flying insects use feedback from various sensory modalities including vision and mechanosensation to navigate through their environment. The rapid speed of mechanosensory information acquisition and processing compensates for the slower processing times associated with vision, particularly under low light conditions. While halteres in dipteran species are well known to provide such information for flight control, less is understood about the mechanosensory roles of their evolutionary antecedent, wings. The features that wing mechanosensory neurons (campaniform sensilla) encode remains relatively unexplored. We hypothesized that the wing campaniform sensilla of the hawkmoth, Manduca sexta, rapidly and selectively extract mechanical stimulus features in a manner similar to halteres. We used electrophysiological and computational techniques to characterize the encoding properties of wing campaniform sensilla. To accomplish this, we developed a novel technique for localizing receptive fields using a focused IR laser that elicits changes in the neural activity of mechanoreceptors. We found that (i) most wing mechanosensors encoded mechanical stimulus features rapidly and precisely, (ii) they are selective for specific stimulus features, and (iii) there is diversity in the encoding properties of wing campaniform sensilla. We found that the encoding properties of wing campaniform sensilla are similar to those for haltere neurons. Therefore, it appears that the neural architecture that underlies the haltere sensory function is present in wings, which lends credence to the notion that wings themselves may serve a similar sensory function. Thus, wings may not only function as the primary actuator of the organism but also as sensors of the inertial dynamics of the animal.
Subject(s)
Flight, Animal/physiology , Manduca/physiology , Mechanoreceptors/physiology , Sensilla/physiology , Wings, Animal/innervation , AnimalsABSTRACT
Insects represent more than 60% of all multicellular life forms, and are easily among the most diverse and abundant organisms on earth. They evolved functional wings and the ability to fly, which enabled them to occupy diverse niches. Insects of the hyper-diverse orders show extreme miniaturization of their body size. The reduced body size, however, imposes steep constraints on flight ability, as their wings must flap faster to generate sufficient forces to stay aloft. Here, we discuss the various physiological and biomechanical adaptations of the thorax in flies which enabled them to overcome the myriad constraints of small body size, while ensuring very precise control of their wing motion. One such adaptation is the evolution of specialized myogenic or asynchronous muscles that power the high-frequency wing motion, in combination with neurogenic or synchronous steering muscles that control higher-order wing kinematic patterns. Additionally, passive cuticular linkages within the thorax coordinate fast and yet precise bilateral wing movement, in combination with an actively controlled clutch and gear system that enables flexible flight patterns. Thus, the study of thoracic biomechanics, along with the underlying sensory-motor processing, is central in understanding how the insect body form is adapted for flight.
Subject(s)
Diptera/physiology , Flight, Animal , Wings, Animal/physiology , Animals , Biomechanical Phenomena , Body Size , Diptera/anatomy & histology , Wings, Animal/anatomy & histologyABSTRACT
Reaching and inspecting objects is an intricate part of human life, which is shared by a diversity of animals across phyla. In addition to appendages like legs and antennae, some insects use their mouthparts to reach and inspect targets. Hawkmoths of the family Sphingidae (Lepidoptera) use their extremely long and straw-like proboscis to drink nectar from flowers. As they approach flowers, hawkmoths uncoil their proboscis and explore the floral surface while hovering to target the proboscis to the nectary hole. Several sensory modalities provide feedback to control and guide these extremely versatile proboscis movements. The control task faced by the hawkmoths' nervous system during such behaviors in not unlike that of an animal guiding limbs or a robotic agent guiding a manipulator to a target. Hawkmoths perform these reaching maneuvers while simultaneously hovering, and hence require rapid and continuous coordination between the proboscis, neck and and flight motor systems, thereby providing a unique invertebrate model for studying appendage guidance and reaching. Here, we review what is known about how hawkmoths use their proboscis for floral inspection and nectar discovery, as well as the role of various sensors in proboscis guidance. We give a brief overview of the morphology and muscular apparatus of the hawkmoth proboscis, and discuss how multimodal sensory feedback might be turned into motor action for appendage guidance.
ABSTRACT
Flight control requires active sensory feedback, and insects have many sensors that help them estimate their current locomotor state, including campaniform sensilla, which are mechanoreceptors that sense strain resulting from deformation of the cuticle. Campaniform sensilla on the wing detect bending and torsional forces encountered during flight, providing input to the flight feedback control system. During flight, wings experience complex spatio-temporal strain patterns. Because campaniform sensilla detect only local strain, their placement on the wing is presumably critical for determining the overall representation of wing deformation; however, how these sensilla are distributed across wings is largely unknown. Here, we test the hypothesis that campaniform sensilla are found in stereotyped locations across individuals of Manduca sexta, a hawkmoth. We found that although campaniform sensilla are consistently found on the same veins or in the same regions of the wings, their total number and distribution can vary extensively. This suggests that there is some robustness to variation in sensory feedback in the insect flight control system. The regions where campaniform sensilla are consistently found provide clues to their functional roles, although some patterns might be reflective of developmental processes. Collectively, our results on intraspecific variation in campaniform sensilla placement on insect wings will help reshape our thinking on the utility of mechanosensory feedback for insect flight control and guide further experimental and comparative studies.
ABSTRACT
Research on insect flight control has focused primarily on the role of wings. Yet abdominal deflections during flight can potentially influence the dynamics of flight. This paper assesses the role of airframe deformations in flight, and asks to what extent the abdomen contributes to flight maneuverability. To address this, we use a combination of both a Model Predictive Control (MPC)-inspired computational inertial dynamics model, and free flight experiments in the hawkmoth, Manduca sexta. We explored both underactuated (i.e., number of outputs are greater than the number of inputs) and fully actuated (equal number of outputs and inputs) systems. Using metrics such as the non-dimensionalized tracking error and cost of transport to evaluate flight performance of the inertial dynamics model, we show that fully actuated simulations minimized the tracking error and cost of transport. Additionally, we tested the effect of restricted abdomen movement on free flight in live hawkmoths by fixing a carbon fiber rod over the thoracic-abdomen joint. Moths with a restricted abdomen performed worse than sham treatment moths. This study finds that abdominal motions contribute to flight control and maneuverability. Such motions of non-aerodynamic structures, found in all flying taxa, can inform the development of multi-actuated micro air vehicles.
ABSTRACT
The mechanics of Dipteran thorax is dictated by a network of exoskeletal linkages that, when deformed by the flight muscles, generate coordinated wing movements. In Diptera, the forewings power flight, whereas the hindwings have evolved into specialized structures called halteres, which provide rapid mechanosensory feedback for flight stabilization. Although actuated by independent muscles, wing and haltere motion is precisely phase-coordinated at high frequencies. Because wingbeat frequency is a product of wing-thorax resonance, any wear-and-tear of wings or thorax should impair flight ability. How robust is the Dipteran flight system against such perturbations? Here, we show that wings and halteres are independently driven, coupled oscillators. We systematically reduced the wing length in flies and observed how wing-haltere synchronization was affected. The wing-wing system is a strongly coupled oscillator, whereas the wing-haltere system is weakly coupled through mechanical linkages that synchronize phase and frequency. Wing-haltere link acts in a unidirectional manner; altering wingbeat frequency affects haltere frequency, but not vice versa. Exoskeletal linkages are thus key morphological features of the Dipteran thorax that ensure wing-haltere synchrony, despite severe wing damage.
Subject(s)
Diptera/physiology , Flight, Animal/physiology , Wings, Animal/physiology , Animals , Diptera/anatomy & histology , Wings, Animal/anatomy & histologyABSTRACT
Insect wings serve two crucial functions in flight: propulsion and sensing. During flapping flight, complex spatiotemporal patterns of strain on the wing reflect mechanics, kinematics, and external perturbations; sensing wing deformation provides feedback necessary for flight control. Campaniform sensilla distributed across the wing transduce local strain fluctuations into neural signals, so their placement on the wing determines sensory information available to the insect. Thus, understanding the significance of these sensor locations will also reveal how sensing and wing movement are coupled. Here, we identify trends in wing campaniform sensilla placement across flying insects from the literature. We then discuss how these patterns can influence sensory encoding by wing mechanosensors. Finally, we propose combining a comparative approach on model insect clades with computational modeling, leveraging the spectacular natural diversity in wings to uncover biological principles of mechanosensory feedback in flight control.