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

Abstract

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.

Improved color constancy in honey bees enabled by parallel visual projections from dorsal ocelli

“…processes (25), ocelli provide underfocused images (26), have large apertures or field of view, and possess two spectrally different photoreceptor classes containing AmUVop and AmLop2 opsins (27), with peak absorption at 335-360 and 499-500 nm, respectively (28,29), in their skyward-facing ventral retinas (26). Interestingly, the ocellar long-wavelength opsin differs from the corresponding opsin present in the compound eye (AmLop) (27).…”

Three‐dimensional visualization of ocellar interneurons of the orchid bee Euglossa imperialis using micro X‐ray computed tomography

“…In the light of growing evidence that ocelli serve at least two distinct functions, namely providing a fast pathway for the attitude control of the head and providing celestial compass information, we note the following relevant aspects of our present findings: (a) The large ocellar L‐neurons integrate the signals from many photoreceptors, but in most cases separately from the dorsal and the ventral ocellar retinae. In orchid bees with their highly aligned rhabdoms (Taylor et al, ), this means that these large L‐neurons are likely to be polarization sensitive (Ogawa et al, ; Ribi et al, ). We note that this is unlikely to be the case in other insects where ocellar photoreceptors are either not polarization sensitive or if they are, their selectivity to different directions of polarization is likely to be averaged out by the extensive dendritic catchment of large L‐neurons.…”

“…The three simple lens eyes that are carried dorsally or frontally on the head between the compound eyes have been shown to supply information for the control of roll and pitch orientation of the head in dragonflies, locusts, and flies (e.g., Hengstenberg, ; Stange, ; Stange & Howard, ; Taylor, ; Wilson, ), but also celestial compass information in ants (Fent & Wehner, ; Schwarz, Albert, Wystrach, & Cheng, ). Ocellar photoreceptors are UV and green sensitive (in dragonflies: van Kleef, James, & Stange, ) and in addition polarization sensitive, at least in hymenopteran insects (honeybees: Geiser & Labhart, ; Ogawa, Ribi, Zeil, & Hemmi, ; reviewed in Zeil, Ribi, & Narendra, ). In the case of orchid bees, ocellar photoreceptors have distinctly aligned rhabdom cross‐sections in the lateral and the median ocelli (Taylor et al, ).…”

“…Recent comparative work of ocellar systems has sparked a renewed interest in their functional design: (a) Although ocelli are generally not focused, in some cases, such as in the ocelli of dragonflies (Berry, Stange, Olberg, & Kleef, ; Berry, Stange, & Warrant, ; Berry, van Kleef, & Stange, ; Stange, Stowe, Chahl, & Massro, ; van Kleef et al, ) and in the equatorial region of the honeybee ocelli, ocellar retinae appear to be close to the focal plane of the lens (Hung & Ibbotson, ; Ribi, Warrant, & Zeil, ); (b) Ocellar retinae are very diverse, in particular with respect to the arrangement and shape of rhabdoms (e.g., Zeil et al, ); (c) The retinae of most ocellar systems are divided into a dorsal and a ventral part which differ in their distance from the ocellar lens surface, in the sizes and arrangements of rhabdoms and in the properties of screening pigments (e.g., Ribi et al, ; Zeil et al, ); (d) The organization of rhabdoms in many hymenopteran ocellar retinae suggests that ocellar photoreceptors are polarization sensitive (Geiser & Labhart, ; Ribi et al, ; Taylor et al, ; Zeil et al, ) as shown by electrophysiological recordings (Geiser and Labhart, ; Ogawa et al, ); (e) In insects that are active at low light, ocellar optics and rhabdoms are enlarged, compared to diurnal insects and thus show the usual adaptations to dim‐light vision (e.g., Berry, Wcislo, & Warrant, ; Greiner, ; Narendra et al, ; Somanathan, Kelber, Borges, Wallen, & Warrant, ; Streinzer, Brockmann, Nagaraja, & Spaethe, ; Warrant, Kelber, Wallen, & Wcislo, ); (f) In ants, ocellar systems also depend on the mode of locomotion, being larger in flying, compared to walking castes (Narendra, Ramirez‐Esquivel, & Ribi, ).…”

Taking Inspiration from Flying Insects to Navigate inside Buildings

“…The "8" orientation is highly correlated to the azimuthal orientation of a nectar source [1]. In flight, honeybees use a kind of "solar compass" based on polarized ultraviolet light [7][8][9] instead of a "magnetic compass" to maintain their heading toward the nectar source or their hive. Karl von Frisch therefore concluded that bees "recruited" by this dance used the information encoded in it to guide them directly to the remote food source.…”