Spectral properties of identified polarized-light sensitive interneurons in the brain of the desert locust Schistocerca gregaria

Many migrating animals employ a celestial compass mechanism for spatial navigation. Behavioral experimentsin bees and ants have shown that sun compass navigation may rely on the spectral gradient in the sky as well as onthe pattern of sky polarization. While polarized-light sensitive interneurons (POL neurons) have been identifiedin the brain of several insect species, there are at present no data on the neural basis of coding the spectral gradientof the sky. In the present study we have analyzed the chromatic properties of two identified POL neurons in thebrain of the desert locust. Both neurons, termed TuTu1 and LoTu1, arborize in the anterior optic tubercle andrespond to unpolarized light as well as to polarized light. We show here that the polarized-light response of both types of neuron relies on blue-sensitive photoreceptors. Responses to unpolarized light depended on stimulus position and wavelength. Dorsal unpolarized blue light inhibited the neurons, while stimulation from the ipsilateral side resulted in opponent responses to UV light and green light. While LoTu1 was inhibited by UV light and was excited by green light, one subtype of TuTu1 was excited by UV and inhibited by green light. In LoTu1 the sensitivity to polarized light was at least 2 log units higher than the response to unpolarized light stimuli. Taken together, the spatial and chromatic properties of the neurons may be suited to signal azimuthal directions based on a combination of the spectral gradient and thepolarization pattern of the sky

Multimodal interactions in insect navigation

Animals travelling through the world receive input from multiple sensory modalities that could be important for the guidance of their journeys. Given the availability of a rich array of cues, from idiothetic information to input from sky compasses and visual information through to olfactory and other cues (e.g. gustatory, magnetic, anemotactic or thermal) it is no surprise to see multimodality in most aspects of navigation. In this review, we present the current knowledge of multimodal cue use during orientation and navigation in insects. Multimodal cue use is adapted to a species’ sensory ecology and shapes navigation behaviour both during the learning of environmental cues and when performing complex foraging journeys. The simultaneous use of multiple cues is beneficial because it provides redundant navigational information, and in general, multimodality increases robustness, accuracy and overall foraging success. We use examples from sensorimotor behaviours in mosquitoes and flies as well as from large scale navigation in ants, bees and insects that migrate seasonally over large distances, asking at each stage how multiple cues are combined behaviourally and what insects gain from using different modalities

Natural History Note Differential Response To Circularly Polarized Light By The Jewel Scarab Beetle Chrysina Gloriosa

Circularly polarized light is rare in the terrestrial environment, and cuticular reflections from scarab beetles are one of the few natural sources. Chrysina gloriosa LeConte 1854, a scarab beetle found in montane juniper forests of the extreme southwestern United States and northern Mexico, are camouflaged in juniper foliage; however, when viewed with right circularly polarizing filters, the beetles exhibit a stark black contrast. Given the polarization-specific changes in the appearance of C. gloriosa, we hypothesized that C. gloriosa can detect circularly polarized light. We tested for phototactic response and differential flight orientation of C. gloriosa toward different light stimuli. Chrysina gloriosa exhibited (a) positive phototaxis, (b) differential flight orientation between linear and circularly polarized light stimuli of equal intensities, and (c) discrimination between circularly polarized and unpolarized lights of different intensities consistent with a model of circular polarization sensitivity based on a quarter-wave plate. These results demonstrate that C. gloriosa beetles respond differentially to circularly polarized light. In contrast, Chrysina woodi Horn 1885, a close relative with reduced circularly polarized reflection, exhibited no phototactic discrimination between linear and circularly polarized light. Circularly polarized sensitivity may allow C. gloriosa to perceive and communicate with conspecifics that remain cryptic to predators, reducing indirect costs of communication.Integrative Biolog

Celestial navigation in Drosophila

Many casual observers typecast Drosophila melanogaster as a stationary pest that lurks around fruit and wine. However, the omnipresent fruit fly, which thrives even in desert habitats, likely established and maintained its cosmopolitan status via migration over large spatial scales. To perform long-distance dispersal, flies must actively maintain a straight compass heading through the use of external orientation cues, such as those derived from the sky. In this Review, we address how D. melanogaster accomplishes long-distance navigation using celestial cues. We focus on behavioral and physiological studies indicating that fruit flies can navigate both to a pattern of linearly polarized light and to the position of the sun – the same cues utilized by more heralded insect navigators such as monarch butterflies and desert ants. In both cases, fruit flies perform menotaxis, selecting seemingly arbitrary headings that they then maintain over time. We discuss how the fly's nervous system detects and processes this sensory information to direct the steering maneuvers that underlie navigation. In particular, we highlight recent findings that compass neurons in the central complex, a set of midline neuropils, are essential for navigation. Taken together, these results suggest that fruit flies share an ancient, latent capacity for celestial navigation with other insects. Furthermore, they illustrate the potential of D. melanogaster to help us to elucidate both the cellular basis of navigation and mechanisms of directed dispersal on a landscape scale

The quantitative description of heading choices of flying Drosophila under changing angles of polarized light

Many insect visual systems are comprised of dedicated neuronal circuits that allow for perceiving, processing, and integrating different modalities of light in order to orient or even navigate within visually complex environments. In addition to intensity or chromatic cues, many insects can utilize the linear polarization of light as a separate modality (Labhart, 2016) for orientation. For instance, polarized reflections can signal specific surface properties, aiding in the detection of water bodies, finding oviposition sites, or localizing prey. Additionally, due to scattering of sunlight in the atmosphere, a celestial polarization pattern is created that can be used by many insects as a reference for both orientation and navigation. Here in this thesis, Manuscript I provides an overview over polarization vision in insects, by summarizing the current knowledge (as of 2017) on anatomical and physiological adaptions of insect visual systems and their behavioral implications in different species (Mathejczyk & Wernet, 2017). To experimentally study visual orientation and navigation in insects, I designed affordable and highly modular behavioral assays, which are described in Manuscript II (Mathejczyk & Wernet, 2020). These assays provide a quantitative behavioral readout in response to panoramic intensity and chromatic patterns or to polychromatic linearly polarized light presented dorsally, when insects are either walking on a spherical treadmill or flying in a magneto-tether. This publication provides 3D model data and building instructions for those modular assays, including an easy-to-build tethering station and a low-cost temperature and humidity control. All code for tracking and data analysis was also made available online to aid the scientific community in establishing and modifying the presented assays in the spirit of open science. In this publication, I further demonstrate the setup’s functionality and versatility by describing opto-motor responses of walking and flying flies to rotating panoramic intensity patterns as well as behavioral responses to rapid e-vector switches of polarized light presented dorsally in flying Drosophila melanogaster. Using the setup described in Manuscript II, I assessed polarotactic responses in flying Drosophila in response to a constantly rotating e-vector presented dorsally, under open-loop conditions (Mathejczyk & Wernet, 2019). I found that flying flies align their body axis in response to linearly polarized UV, but not under polarized green or depolarized UV light. Every fly chose an arbitrary preferred heading relative to a celestial e-vector and most flies were able the keep those headings at least over the course of several minutes. Taken together, these findings confirm that Drosophila can utilize wavelength-specific skylight polarization for orientation and suggest that in Drosophila celestial polarization vision might serve an underlying dispersal strategy, optimizing chances of survival and reproduction on a population level

Heading choices of flying Drosophila under changing angles of polarized light

Many navigating insects include the celestial polarization pattern as an additional visual cue to orient their travels. Spontaneous orientation responses of both walking and flying fruit flies (Drosophila melanogaster) to linearly polarized light have previously been demonstrated. Using newly designed modular flight arenas consisting entirely of off-the-shelf parts and 3D-printed components we present individual flying flies with a slow and continuous rotational change in the incident angle of linear polarization. Under such open-loop conditions, single flies choose arbitrary headings with respect to the angle of polarized light and show a clear tendency to maintain those chosen headings for several minutes, thereby adjusting their course to the slow rotation of the incident stimulus. Importantly, flies show the tendency to maintain a chosen heading even when two individual test periods under a linearly polarized stimulus are interrupted by an epoch of unpolarized light lasting several minutes. Finally, we show that these behavioral responses are wavelength-specific, existing under polarized UV stimulus while being absent under polarized green light. Taken together, these findings provide further evidence supporting Drosophila’s abilities to use celestial cues for visually guided navigation and course correction

The Role of Landscapes and Landmarks in Bee Navigation: A Review.

The ability of animals to explore landmarks in their environment is essential to their fitness. Landmarks are widely recognized to play a key role in navigation by providing information in multiple sensory modalities. However, what is a landmark? We propose that animals use a hierarchy of information based upon its utility and salience when an animal is in a given motivational state. Focusing on honeybees, we suggest that foragers choose landmarks based upon their relative uniqueness, conspicuousness, stability, and context. We also propose that it is useful to distinguish between landmarks that provide sensory input that changes ("near") or does not change ("far") as the receiver uses these landmarks to navigate. However, we recognize that this distinction occurs on a continuum and is not a clear-cut dichotomy. We review the rich literature on landmarks, focusing on recent studies that have illuminated our understanding of the kinds of information that bees use, how they use it, potential mechanisms, and future research directions

Processing of sky compass cues and wide-field motion in the central complex of the desert locust (Schistocerca gregaria)

1. Polarization-sensitive neurons of the locust central complex show azimuthdependent responses to unpolarized light spots. This suggests that direct sunlight supports the sky polarization compass in this brain area. / 2. In the brain of the desert locust, neurons sensitive to the plane of celestial polarization are arranged like a compass in the slices of the central complex. These neurons, in addition, code for the horizontal direction of an unpolarized light cue possibly representing the sun. We show here that horizontal directions are, in addition to E-vector orientations from dorsal direction, represented in a compass-like manner across the slices of the central complex. However, both compasses are not linked to each other but seem to interact in a cell specific nonlinear way. Our study confirms the role of the central complex in signaling heading directions signaling and shows that different cues are employed for this task. / 3. Visual cues are essential for animal navigation and spatial orientation. Many insects rely on celestial cues for spatial orientation, including the sky polarization pattern. In desert locusts neurons encoding the plane of polarized light (E-vector) are located in the central complex (CX), a group of midline-spanning neuropils. Several types of CX neuron signalling heading direction represent zenithal Evectors in a topographic manner across the slices of the CX and, likely, act as an internal sky compass. Because animals experience optic flow stimulation during flight, we asked whether progressive wide-field motion affects the responses of CX neurons to polarized light. In most neurons, progressive motion disadapted the response to the preferred E-vector (i.e. the E-vector eliciting strongest firing), whereas the response to the anti-preferred E-vector remained comparatively unaffected. This suggests context-dependent gain modulation in sky compass signalling. Three types of compass neuron were responsive to motion simulating body rotation around the yaw axis. Depending on arborization domains in the CX and rotation direction these neurons were strongly excited or inhibited. As proposed for Drosophila, they may be involved in shifting compass signal activity across the slices of the CX as the animal turns enabling it to keep track of its heading