Birgit Greiner

Nocturnal Vision and Landmark Orientation in a Tropical Halictid Bee

BACKGROUND Some bees and wasps have evolved nocturnal behavior, presumably to exploit night-flowering plants or avoid predators. Like their day-active relatives, they have apposition compound eyes, a design usually found in diurnal insects. The insensitive optics of apposition eyes are not well suited for nocturnal vision. How well then do nocturnal bees and wasps see? What optical and neural adaptations have they evolved for nocturnal vision? RESULTS We studied female tropical nocturnal sweat bees (Megalopta genalis) and discovered that they are able to learn landmarks around their nest entrance prior to nocturnal foraging trips and to use them to locate the nest upon return. The morphology and optics of the eye, and the physiological properties of the photoreceptors, have evolved to give Megaloptas eyes almost 30 times greater sensitivity to light than the eyes of diurnal worker honeybees, but this alone does not explain their nocturnal visual behavior. This implies that sensitivity is improved by a strategy of photon summation in time and in space, the latter of which requires the presence of specialized cells that laterally connect ommatidia into groups. First-order interneurons, with significantly wider lateral branching than those found in diurnal bees, have been identified in the first optic ganglion (the lamina ganglionaris) of Megaloptas optic lobe. We believe that these cells have the potential to mediate spatial summation. CONCLUSIONS Despite the scarcity of photons, Megalopta is able to visually orient to landmarks at night in a dark forest understory, an ability permitted by unusually sensitive apposition eyes and neural photon summation.

Celestial polarization patterns during twilight

Scattering of sunlight produces patterns of partially linearly polarized light in the sky throughout the day, and similar patterns appear at night when the Moon is bright. We studied celestial polarization patterns during the period of twilight, when the Sun is below the horizon, determining the degree and orientation of the polarized-light field and its changes before sunrise and after sunset. During twilight, celestial polarized light occurs in a wide band stretching perpendicular to the location of the hidden Sun and reaching typical degrees of polarization near 80% at wavelengths >600 nm. In the tropics, this pattern appears approximately 1 h before local sunrise or disappears approximately 1 h after local sunset (within 10 min. after the onset of astronomical twilight at dawn, or before its end at dusk) and extends with little change through the entire twilight period.

Visual summation in night-flying sweat bees: A theoretical study

Bees are predominantly diurnal; only a few groups fly at night. An evolutionary limitation that bees must overcome to inhabit dim environments is their eye type: bees possess apposition compound eyes, which are poorly suited to vision in dim light. Here, we theoretically examine how nocturnal bees Megalopta genalis fly at light levels usually reserved for insects bearing more sensitive superposition eyes. We find that neural summation should greatly increase M. genaliss visual reliability. Predicted spatial summation closely matches the morphology of laminal neurons believed to mediate such summation. Improved reliability costs acuity, but dark adapted bees already suffer optical blurring, and summation further degrades vision only slightly.

Neural organisation in the first optic ganglion of the nocturnal bee Megalopta genalis

Each neural unit (cartridge) in the first optic ganglion (lamina) of the nocturnal bee Megalopta genalis contains nine receptor cell axons (6 short and 3 long visual fibres), and four different types of first-order interneurons, also known as L-fibres (L1 to L4) or lamina monopolar cells. The short visual fibres terminate within the lamina as three different types (svf 1, 2, 3). The three long visual fibres pass through the lamina without forming characteristic branching patterns and terminate in the second optic ganglion, the medulla. The lateral branching pattern of svf 2 into adjacent cartridges is unique for hymenopterans. In addition, all four types of L-fibres show dorso-ventrally arranged, wide, lateral branching in this nocturnal bee. This is in contrast to the diurnal bees Apis mellifera and Lasioglossum leucozonium, where only two out of four L-fibre types (L2 and L4) reach neighbouring cartridges. In M. genalis, L1 forms two sub-types, viz. L1-a and L1-b; L1-b in particular has the potential to contact several neighbouring cartridges. L2 and L4 in the nocturnal bee are similar to L2 and L4 in the diurnal bees but have dorso-ventral arborisations that are twice as wide. A new type of laterally spreading L3 has been discovered in the nocturnal bee. The extensive neural branching pattern of L-fibres in M. genalis indicates a potential role for these neurons in the spatial summation of photons from large groups of ommatidia. This specific adaptation in the nocturnal bee could significantly improve reliability of vision in dim light.

A neural network to improve dim-light vision? Dendritic fields of first-order interneurons in the nocturnal bee Megalopta genalis

Using the combined Golgi-electron microscopy technique, we have determined the three-dimensional dendritic fields of the short visual fibres (svf 1–3) and first-order interneurons or L-fibres (L1-4) within the first optic ganglion (lamina) of the nocturnal bee Megalopta genalis. Serial cross sections have revealed that the svf type 2 branches into one adjacent neural unit (cartridge) in layer A, the most distal of the three lamina layers A, B and C. All L-fibres, except L1-a, exhibit wide lateral branching into several neighbouring cartridges. L1-b shows a dendritic field of seven cartridges in layers A and C, dendrites of L2 target 13 cartridges in layer A, L3 branches over a total of 12 cartridges in layer A and three in layer C and L4 has the largest dendritic field size of 18 cartridges in layer C. The number of cartridges reached by the respective L-fibres is distinctly greater in the nocturnal bee than in the worker honeybee and is larger than could be estimated from our previous Golgi-light microscopy study. The extreme dorso-ventrally oriented dendritic field of L4 in M. genalis may, in addition to its potential role in spatial summation, be involved in edge detection. Thus, we have shown that the amount of lateral spreading present in the lamina provides the anatomical basis for the required spatial summation. Theoretical and future physiological work should further elucidate the roles that this lateral spreading plays to improve dim-light vision in nocturnal insects.

Eye structure correlates with distinct foraging-bout timing in primitive ants

Summary Social insects have evolved remarkable physiological adaptations and behavioural strategies that enable them to access new temporal foraging niches (for example [1]). Here we report striking correlations between the timing of foraging bouts and the modification of eye structure in four species of ants belonging to the primitive genus Myrmecia . Most noteworthy, photoreceptor diameters progressively increase from 1.3 μm in strictly day-active species, to 5.9 μm in predominantly night-active species.

Caste-specific visual adaptations to distinct daily activity schedules in Australian Myrmecia ants

Animals are active at different times of the day and their activity schedules are shaped by competition, time-limited food resources and predators. Different temporal niches provide different light conditions, which affect the quality of visual information available to animals, in particular for navigation. We analysed caste-specific differences in compound eyes and ocelli in four congeneric sympatric species of Myrmecia ants, with emphasis on within-species adaptive flexibility and daily activity rhythms. Each caste has its own lifestyle: workers are exclusively pedestrian; alate females lead a brief life on the wing before becoming pedestrian; alate males lead a life exclusively on the wing. While workers of the four species range from diurnal, diurnal-crepuscular, crepuscular-nocturnal to nocturnal, the activity times of conspecific alates do not match in all cases. Even within a single species, we found eye area, facet numbers, facet sizes, rhabdom diameters and ocelli size to be tuned to the distinct temporal niche each caste occupies. We discuss these visual adaptations in relation to ambient light levels, visual tasks and mode of locomotion.

Visual adaptations in the night-active wasp Apoica pallens

The apposition compound eye of the nocturnal polistine wasp Apoica pallens shows, in comparison to the closely related diurnal wasp Polistes occidentalis, specific adaptations to vision at low light intensities. When considering recent work on nocturnal and diurnal bees, general principles for dim‐light vision in hymenopterans become evident: The rhabdom diameters in nocturnal bees and wasps are 4 times wider compared to their diurnal relatives, leading to wide receptive fields, which in turn account for a 25‐fold higher optical sensitivity. Interestingly, the rhabdom diameters in both nocturnal bees and wasps measure 8 μm, which may represent the maximum width for nocturnal hymenopteran apposition eyes. A ratio of 1.8 times larger eyes is present in the nocturnal bees and wasps, which in A. pallens is achieved by increasing the facet number, instead of enlarging the facets, as in nocturnal bees. Although this initially indicates spatial resolution to be important for the nocturnal wasp, the wide receptive fields of the rhabdoms will reduce its potentially high acuity. As the optical sensitivity alone cannot account for the 8 log units intensity difference between day and night, a possible role of neural summation within the first optic ganglion (lamina) of nocturnal hymenopterans is discussed. J. Comp. Neurol. 495:255–262, 2006.

Three-dimensional antennal lobe atlas of the male moth, Agrotis ipsilon: A tool to study structure-function correlation

The glomerular structure of the primary olfactory neuropil has long been thought to play an important role in odour coding. In insects, the number of glomeruli in the antennal lobe is limited in most species to fewer than 100 compared with more than 1,000 in vertebrates, making it possible to identify individual glomeruli. A complete three‐dimensional atlas of the glomeruli within the antennal lobe of the male noctuid moth Agrotis ipsilon was constructed. All 66 glomeruli were singly identifiable in both antennal lobes of the three brains investigated. Further, six antennal lobes containing intracellularly stained projection neurones were reconstructed. By using the atlas, the respective target glomerulus of each projection neurone could be identified. The importance of the glomerular atlas as a tool to study central olfactory processing and its plasticity is discussed. J. Comp. Neurol. 475:202–210, 2004.

Adaptations for nocturnal vision in insect apposition eyes.

Due to our own preference for bright light, we tend to forget that many insects are active in very dim light. Nocturnal insects possess in general superposition compound eyes. This eye design is truly optimized for dim light as photons can be gathered through large apertures comprised of hundreds of lenses. In apposition eyes, on the other hand, the aperture consists of a single lens resulting in a poor photon catch and unreliable vision in dim light. Apposition eyes are therefore typically found in day-active insects. Some nocturnal insects have nevertheless managed the transition to a strictly nocturnal lifestyle while retaining their highly unsuitable apposition eye design. Large lenses and wide photoreceptors enhance the sensitivity of nocturnal apposition eyes. However, as the gain of these optical adaptations is limited and not sufficient for vision in dim light, additional neural adaptations in the form of spatial and temporal summation are necessary.