The Dual Function of Orchid Bee Ocelli as Revealed by X-Ray Microtomography

Taylor, Gavin J.; Ribi, Willi A.; Bech, Martin; Bodey, Andrew J.; Rau, Christoph; Steuwer, A.; Warrant, Eric J.; Baird, Emily

doi:10.1016/j.cub.2016.03.038

Cited by 55 publications

(71 citation statements)

References 39 publications

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“…3B,C). The visual systems of other tropical insects also have prominent dorsal visual fields (17), suggesting that extending the dorsal visual field is a common visual specialization for the densest forests where the sky can be completely occluded by the thick canopy (18). Another difference between the tropical and temperate species is that the lens diameters of the tropical species are larger (Fig.…”

Section: Discussionmentioning

confidence: 99%

Imaging the evolution of visual specializations in fungus gnats

Taylor

Hall

Gren

et al. 2018

Preprint

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Abstract:Many insects use vision to inform their behavior, but visual information differs between habitats and the sensory demands vary with each species' ecology. The small size of insects' eyes constrains their optical performance, and so it is unsurprising that they have evolved specializations for optimizing the information they obtain from their habitat. Unraveling how behavioral, environmental, and phylogenetic factors influence the evolution of such specializations is difficult, however, because existing techniques to analyze insect eyes require specimens to be preserved beforehand. To facilitate broad comparative studies on insect eyes and the evolution of complex visual behavior, we developed a novel analysis technique that uses x-ray micro-computed tomography to quantify and recreate the visual world of insects. We use our methodology to investigate the eyes of fungus gnats (Orfeliini), a tribe of diminutive Dipterans, to identify the visual specializations they evolved for surviving in different forest habitats and to explore how this changed over 30 million years of evolutionary history. The specimens we studied were preserved in different ways (in ethanol, air dried, and as an endocast in amber), demonstrating that our method provides a new opportunity to quantitatively study and compare the vision of a wide range insects held in museum collections. Our analysis indicates that different visual specializations have evolved between fungus gnat species living in different forest types and that the eyes of gnats from a similar geographic location have evolved to match the changing environmental conditions. Despite the small size of fungus gnats, evolution has evidentially been able to exploit sensory specializations to meet the differing sensory demands of species from a variety of forest habitats.Significance statement: Do insects have visual specializations that evolve with changes in their environment? To answer this question, a novel analysis technique is described that uses 3D imaging and simulations to compare the vision of ancient amber-embedded insects to those of their extant relatives. This study investigated the vision of fungus gnats to understand how tiny insects use vision to negotiate forests, some of the world's most visually complex environments. Despite being amongst the smallest of any flying insect, the gnats' miniature eyes have evolved visual specializations specifically adapted for different forest types, allowing different species to meet their visual demands of their specific habitats.Introduction: Vision provides essential information to meet the sensory demands of flying insects and is utilized to orchestrate both movement through, and interactions with, their environment (1). To fly safely and efficiently and to avoid collisions with obstacles, an insect must control its speed and orientation. To forage successfully, it must locate and recognize food objects from the wing, before safely approaching and landing upon them. The visual requirements of both sets of tasks depend up...

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Section: Discussionmentioning

confidence: 99%

Imaging the evolution of visual specializations in fungus gnats

Taylor

Hall

Gren

et al. 2018

Preprint

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“…In conclusion, the distribution of polarization sensitivities across the visual fields of honeybee ocelli suggests that ocelli serve two functions, one is contrast enhancement of the visual horizon for head attitude control and the other is support for the celestial compass system (reviewed in Ribi et al, 2011;Zeil et al, 2014;Taylor et al, 2015). It will thus be interesting in future to study the polarization sensitivities of ocellar interneurons, depending on their dendritic catchment and their size.…”

Section: Regional Distribution Of Preferred E-vector Orientationsmentioning

confidence: 94%

“…This arrangement and the fact that the rhabdom sheets do not twist along their length indicates that they are likely to be polarization sensitive (Kral, 1978;Ribi et al, 2011;Zeil et al, 2014). A recent study of the particular alignment of elongated rhabdoms in the three ocelli of orchid bees has provided further evidence for the possible involvement of ocelli in the detection of polarized skylight (Taylor et al, 2015). In contrast, the cross-sections of ocellar rhabdoms in the nocturnal bee Megalopta are not straight (Ribi et al, 2011) and the ocellar photoreceptors have indeed been found not to be polarization sensitive (Berry et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

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Regional differences in the preferred e-vector orientation of honeybee ocellar photoreceptors

Ogawa

Ribi

Zeil

et al. 2017

Journal of Experimental Biology

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In addition to compound eyes, honeybees (Apis mellifera) possess three single-lens eyes called ocelli located on the top of the head. Ocelli are involved in head-attitude control and in some insects have been shown to provide celestial compass information. Anatomical and early electrophysiological studies have suggested that UV and blue-green photoreceptors in ocelli are polarization sensitive. However, their retinal distribution and receptor characteristics have not been documented. Here, we used intracellular electrophysiology to determine the relationship between the spectral and polarization sensitivity of the photoreceptors and their position within the visual field of the ocelli. We first determined a photoreceptor's spectral response through a series of monochromatic flashes (340-600 nm). We found UV and green receptors, with peak sensitivities at 360 and 500 nm, respectively. We subsequently measured polarization sensitivity at the photoreceptor's peak sensitivity wavelength by rotating a polarizer with monochromatic flashes. Polarization sensitivity (PS) values were significantly higher in UV receptors (3.8± 1.5, N=61) than in green receptors (2.1±0.6, N=60). Interestingly, most receptors with receptive fields below 35 deg elevation were sensitive to vertically polarized light while the receptors with visual fields above 35 deg were sensitive to a wide range of polarization angles. These results agree well with anatomical measurements showing differences in rhabdom orientations between dorsal and ventral retinae. We discuss the functional significance of the distribution of polarization sensitivities across the visual field of ocelli by highlighting the information the ocelli are able to extract from the bee's visual environment.

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“…Due to the low refractive power of the cornea, ocelli typically cannot form images on the photo receptor layers, although some exceptions have been reported. [388] As a consequence of the large aperture and the resulting low f-number of the lens, ocelli can detect lower light levels and have a faster response time than compound eyes. Ocelli are typically found on the dorsal (top) surface of the head of many insects and coexist with compound eyes (Figure 17).…”

Section: Simple Eyes-ocelli As Light Detectorsmentioning

confidence: 99%

It's Not a Bug, It's a Feature: Functional Materials in Insects

2018

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Over the course of their wildly successful proliferation across the earth, the insects as a taxon have evolved enviable adaptations to their diverse habitats, which include adhesives, locomotor systems, hydrophobic surfaces, and sensors and actuators that transduce mechanical, acoustic, optical, thermal, and chemical signals. Insect‐inspired designs currently appear in a range of contexts, including antireflective coatings, optical displays, and computing algorithms. However, as over one million distinct and highly specialized species of insects have colonized nearly all habitable regions on the planet, they still provide a largely untapped pool of unique problem‐solving strategies. With the intent of providing materials scientists and engineers with a muse for the next generation of bioinspired materials, here, a selection of some of the most spectacular adaptations that insects have evolved is assembled and organized by function. The insects presented display dazzling optical properties as a result of natural photonic crystals, precise hierarchical patterns that span length scales from nanometers to millimeters, and formidable defense mechanisms that deploy an arsenal of chemical weaponry. Successful mimicry of these adaptations may facilitate technological solutions to as wide a range of problems as they solve in the insects that originated them.

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The Dual Function of Orchid Bee Ocelli as Revealed by X-Ray Microtomography

Cited by 55 publications

References 39 publications

Imaging the evolution of visual specializations in fungus gnats

Imaging the evolution of visual specializations in fungus gnats

Regional differences in the preferred e-vector orientation of honeybee ocellar photoreceptors

It's Not a Bug, It's a Feature: Functional Materials in Insects

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