Ocellar adaptations for dim light vision in a nocturnal bee

Abstract

SUMMARYGrowing evidence indicates that insect ocelli are strongly adapted to meet the specific functional requirements in the environment in which that insect lives. We investigated how the ocelli of the nocturnal bee Megalopta genalis are adapted to life in the dim understory of a tropical rainforest. Using a combination of light microscopy and three-dimensional reconstruction, we found that the retinae contain bar-shaped rhabdoms loosely arranged in a radial pattern around multi-layered lenses, and that both lenses and retinae form complex non-spherical shapes reminiscent of those described in other ocelli. Intracellular electrophysiology revealed that the photoreceptors have high absolute sensitivity, but that the threshold location varied widely between 10 9 and 10 11 photonscm -2 s -1 . Higher sensitivity and greater visual reliability may be obtained at the expense of temporal resolution: the corner frequencies of dark-adapted ocellar photoreceptors were just 4-11Hz. Spectral sensitivity profiles consistently peaked at 500nm. Unlike the ocelli of other flying insects, we did not detect UV-sensitive visual pigments in M. genalis, which may be attributable to a scarcity of UV photons under the rainforest canopy at night. In contrast to earlier predictions based on anatomy, the photoreceptors are not sensitive to the e-vector of polarised light. Megalopta genalis ocellar photoreceptors possess a number of unusual properties, including inherently high response variability and the ability to produce spike-like potentials. These properties bear similarities to photoreceptors in the compound eye of the cockroach, and we suggest that the two insects share physiological characteristics optimised for vision in dim light. Supplementary material available online at

Ocellar structure and neural innervation in the honeybee

“…Berry et al (2011) found that the ocellar lenses of a nocturnal bee ( Megalopta genalis ) consist of at least three structurally distinct components, named the outer, middle and inner layer. The outer layer is stained lightly with Toluidine Blue; the middle layer is similarly composed of tightly layered tissue and stained more densely with Toluidine Blue; and the inner layer stains with the highest density of Toluidine Blue.…”

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

“…If a photoreceptor contains microvilli of a constant orientation, the receptor would have a strong e-vector preference, because incident light is absorbed maximally when its e-vector orientation is parallel to the long axis of microvilli (Moody and Parriss, 1961). The cross-sections of ocellar rhabdoms in honeybees are much straighter than those in the nocturnal bee Megalopta (Ribi et al, 2011), in which ocellar photoreceptors have been found not to be polarization sensitive (Berry et al, 2011). The maximum predicted PS value that is achievable from perfectly aligned microvilli but with randomly oriented opsin molecules within microvilli falls between 1.6 and 2.0 (Snyder and Laughlin, 1975).…”

“…Stange et al, 2002;Berry et al, 2006Berry et al, , 2007a. They are particularly important at low light levels (Wellington, 1974;Berry et al, 2011). Ocelli have also been shown to be involved in providing compass information by sensing the pattern of polarized skylight (Wellington, 1974;Fent and Wehner, 1985).…”

“…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). The polarization sensitivity in ocelli has been suggested not only to provide celestial compass information but also to improve segmentation of the horizon line by enhancing contrast for the control of head attitude, particularly around roll and pitch axes (Zeil et al, 2014).…”

Visual ecology and potassium conductances of insect photoreceptors

“…This is accomplished by adaptations both at the visual system periphery by optical (e.g., by superposition-type eyes) and/or physiological means (temporal integration in photoreceptors; Warrant and Dacke 2011) and at the level of optic lobes (e.g., high degree of spatial summation in the lamina; Greiner 2006;Stöckl et al 2015). Photoreceptors of nocturnal insects usually demonstrate high gain of phototransduction, with a concomitant increase in bump latency and decrease in corner frequency (Berry et al 2011;Fain et al 2010;Laughlin 1981). Thus, due to evolutionary design principles, visual systems of crepuscular/nocturnal insects generally facilitate neither high temporal resolution nor visual acuity.…”