Ants of the Australian genus Myrmecia partition their foraging niche temporally, allowing them to be sympatric with overlapping foraging requirements. We used histological techniques to study the light and dark adaptation mechanisms in the compound eyes of diurnal (Myrmecia croslandi), crepuscular (M. tarsata, M. nigriceps) and nocturnal ants (M. pyriformis). We found that, except in the day-active species, all ants have a variable primary pigment cell pupil that constricts the crystalline cone in bright light to control for light flux. We show for the nocturnal M. pyriformis that the constriction of the crystalline cone by the primary pigment cells is light dependent whereas the opening of the aperture is regulated by an endogenous rhythm. In addition, in the light-adapted eyes of all species, the retinular cell pigment granules radially migrate towards the rhabdom, a process that in both the day-active M. croslandi and the night-active M. pyriformis is driven by ambient light intensity. Visual system properties thus do not restrict crepuscular and night-active ants to their temporal foraging niche, while day-active ants require high light intensities to operate. We discuss the ecological significance of these adaptation mechanisms and their role in temporal niche partitioning.

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.

Male moths use sex pheromones to find their mating partners. In the moth, Agrotis ipsilon, the behavioral response and the neuron sensitivity within the primary olfactory centre, the antennal lobe (AL), to sex pheromone increase with age and juvenile hormone (JH) biosynthesis. By manipulating the JH level, we previously showed that JH controls this age-dependent neuronal plasticity, and that its effects are slow (within 2 days). We hypothesized that the hormonal effect might be indirect, and one neuromodulator candidate, which might serve as a mediator, is octopamine (OA). Here, we studied the effects of OA and an OA receptor antagonist, mianserin, on behavioral and AL neuron responses of mature and immature males during stimulation with sex pheromone. Our results indicate that, although OA injections enhanced the behavioral pheromone response in mature males, OA had no significant effect on behavior in immature males. However, mianserin injections decreased the behavioral response in mature males. AL neuron sensitivity increased after OA treatment in immature males, and decreased after mianserin treatment in mature males. Determination of OA levels in ALs of immature and mature males did not reveal any difference. To study the possible interactive effects of JH and OA, the behavioral pheromone response was analyzed in JH-deprived mature males injected with OA, and in immature males injected with fenoxycarb, a JH agonist, and mianserin. Results show that both JH and OA are necessary to elicit a behavioral response of A. ipsilon males to sex pheromone.

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.

The presence of a specialised dorsal rim area with an ability to detect the e-vector orientation of polarised light is shown for the first time in a nocturnal hymenopteran. The dorsal rim area of the halictid bee Megalopta genalis features a number of characteristic anatomical specialisations including an increased rhabdom diameter and a lack of primary screening pigments. Optically, these specialisations result in wide spatial receptive fields (Delta rho = 14 degrees), a common adaptation found in the dorsal rim areas of insects used to filter out interfering effects (i.e. clouds) from the sky. In this specialised eye region all nine photoreceptors contribute their microvilli to the entire length of the ommatidia. These orthogonally directed microvilli are anatomically arranged in an almost linear, anterior-posterior orientation. Intracellular recordings within the dorsal rim area show very high polarisation sensitivity and a sensitivity peak within the ultraviolet part of the spectrum.

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.

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. genalis's 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.

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.

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 mum, 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.

Although natural light sources produce depolarized light, patterns of partially linearly polarized light appear in the sky due to scattering from air molecules, dust, and aerosols. Many animals, including bees and ants, orient themselves to patterns of polarization that are present in daytime skies, when the intensity is high and skylight polarization is strong and predictable. The halicitid bee Megalopta genalis inhabits rainforests in Central America. Unlike typical bees, it forages before sunrise and after sunset, when light intensities under the forest canopy are very low, and must find its way to food sources and return to its nest in visually challenging circumstances. An important cue for the orientation could be patterns of polarization in the twilight sky. Therefore, we used a calibrated digital camera to image skylight polarization in an overhead patch of sky, 87.6° across, before dawn on Barro Colorado Island in Panama, where the bees are found. We simultaneously measured the spectral properties of polarized light in a cloudless patch of sky 15° across centered on the zenith. We also performed full-sky imaging of polarization before dawn and after dusk on Lizard Island in Australia, another tropical island. 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. This pattern appears about 45 minutes before local sunrise or disappears 45 minutes after local sunset (about 20 minutes after the onset of astronomical twilight at dawn, or before its end at dusk) and extends with little change through the entire twilight period. Such a strong and reliable orientation cue could be used for flight orientation by any animal with polarization sensitivity that navigates during twilight.

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.

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.

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 Megalopta's 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 Megalopta's 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.

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. © 2004 Wiley‐Liss, Inc.

The apposition compound eye of a nocturnal bee, the halictid Megalopta genalis, is described for the first time. Compared to the compound eye of the worker honeybee Apis mellifera and the diurnal halictid bee Lasioglossum leucozonium, the eye of M. genalis shows specific retinal and optical adaptations for vision in dim light. The major anatomical adaptations within the eye of the nocturnal bee are (1) nearly twofold larger ommatidial facets and (2) a 4-5 times wider rhabdom diameter than found in the diurnal bees studied. Optically, the apposition eye of M. genalis is 27 times more sensitive to light than the eyes of the diurnal bees. This increased optical sensitivity represents a clear optical adaptation to low light intensities. Although this unique nocturnal apposition eye has a greatly improved ability to catch light, a 27-fold increase in sensitivity alone cannot account for nocturnal vision at light intensities that are 8 log units dimmer than during daytime. New evidence suggests that additional neuronal spatial summation within the first optic ganglion, the lamina, is involved.

Male moths rely on female sex pheromones to find their mating partner and on plant volatiles for the detection of food sources. In the noctuid moth, Agrotis ipsilon, plasticity of central sex pheromone processing has been shown previously in the antennal lobe. The sensitivity of antennal lobe interneurons increases with age and juvenile hormone level. Here we investigated whether age affects not only central sex pheromone processing, but also central processing of plant volatiles in A. ipsilon males. Intracellular recordings of antennal lobe interneurons were made in males of different ages after stimulation of the antennae with seven different plant volatiles. The sensitivity and specificity of the antennal lobe interneurons for any of the plant volatiles tested did not change with age. From these results we conclude that the sensitivity of the antennal lobe interneurons involved in central plant volatile processing is age-independent and that the action of juvenile hormone is specific for central sex pheromone processing in A. ipsilon males.