Light and dark adaptation mechanisms in the compound eyes of Myrmecia ants that occupy discrete temporal niches

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

Techniques for investigating the anatomy of the ant visual system

This article outlines a suite of techniques in light microscopy (LM) and electron microscopy (EM) which can be used to study the internal and external eye anatomy of insects. These include traditional histological techniques optimized for work on ant eyes and adapted to work in concert with other techniques such as transmission electron microscopy (TEM) and scanning electron microscopy (SEM). These techniques, although vastly useful, can be difficult for the novice microscopist, so great emphasis has been placed in this article on troubleshooting and optimization for different specimens. We provide information on imaging techniques for the entire specimen (photo-microscopy and SEM) and discuss their advantages and disadvantages. We highlight the technique used in determining lens diameters for the entire eye and discuss new techniques for improvement. Lastly, we discuss techniques involved in preparing samples for LM and TEM, sectioning, staining, and imaging these samples. We discuss the hurdles that one might come across when preparing samples and how best to navigate around them.This work was supported by a graduate scholarship to FRE and grants from the Australian Research Council (DE120100019, FT140100221, DP150101172)

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

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 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 nm 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 Green receptors (2.1±0.6, N=60). Interestingly, most receptors with receptive fields below 35° elevation were sensitive to vertically polarized light while the receptors with visual fields above 35° 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.This study was supported by a Japan Society for the Promotion of Science (JSPS) Postdoctoral Fellowship for Research Abroad to Y.O. and an Australian Research Council grant (FT110100528) to J.M.H

Diversity and common themes in the organization of ocelli in Hymenoptera, Odonata and Diptera

We show in a comparative analysis that distinct retinal specializations in insect ocelli are much more common than previously realized and that the rhabdom organization of ocellar photoreceptors is extremely diverse. Hymenoptera, Odonata and Diptera show prominent equatorial fovea-like indentations of the ocellar retinae, where distal receptor endings are furthest removed from the lens surface and receptor densities are highest. In contrast, rhabdomere arrangements are very diverse across insect groups: in Hymenoptera, with some exceptions, pairs of ocellar retinular cells form sheet-like rhabdoms that form elongated rectangular shapes in cross-section, with highly aligned microvilli directions perpendicular to the long axis of cross-sections. This arrangement makes most ocellar retinular cells in Hymenoptera sensitive to the direction of polarized light. In dragonflies, triplets of retinular cells form a y-shaped fused rhabdom with microvilli directions oriented at 60° to each other. In Dipteran ocellar retinular cells microvilli directions are randomised, which destroys polarization sensitivity. We suggest that the differences in ocellar organization between insect groups may reflect the different head attitude control systems that have evolved in these insect groups, but possibly also differences in the mode of locomotion and in the need for celestial compass information

The visual system of the Australian 'Redeye' cicada (Psaltoda moerens)

We investigated the functional anatomy of the visual system in the Australian 'Redeye' cicada Psaltoda moerens, including compound eyes and ocelli. The compound eyes have large visual fields, about 7500 ommatidia per eye and binocular overlaps of 10-15° in the frontal and of 50-60° in the dorsal visual field. The diameters of corneal facet lenses range between 22 and 34μm and the lenses are unusually long with up to 100μm in some eye regions. In the posterior part of the eyes, the hexagonal facet array changes to a square lattice. The compound eyes are of the eucone apposition type with 8 retinular cells contributing to a fused rhabdom in each ommatidium. The red eye colour is due to the pigment granules in the secondary pigment cells. We found a small Dorsal Rim Area (DRA), in which rhabdom cross-sections are rectangular rather than round. The cross-sections of DRA rhabdoms do not systematically change orientation along the length of the rhabdom, indicating that microvilli directions do not twist, which would make retinular cells in the DRA polarization sensitive. The three ocelli have unusual lenses with a champagne-cork shape in longitudinal sections. Retinular cells are short in the dorsal and ventral part of the retinae, and long in their equatorial part. Ocellar rhabdoms are short (<10μm), positioned close to the corneagenous layer and are formed by pairs of retinular cells. In cross-section, the rhabdomeres are 2-5μm long and straight. The red colour of ocelli is produced by screening pigments that form an iris around the base of the ocellar lens and by screening pigments between the ocellar retinular cells. We discuss the organization of the compound eye rhabdom, the organization of the ocelli and the presence of a DRA in the light of what is known about Hemipteran compound eyes. We note in particular that cicadas are the only Hemipteran group with fused rhabdoms, thus making Hemiptera an interesting case to study the evolution of open rhabdoms and neural superposition

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

We used contrast-optimized micro X-ray computed tomography (mCT) to trace the profiles of the full complement of large ocellar L-neurons in the male orchid bee Euglossa imperialis. We find that most L-neurons collect information from either the dorsal or the ventral retinae in both median and lateral ocelli, with only three neurons associated with the median ocellus having dendritic branches in both dorsal and ventral retina. In the median ocellus, we find also L-neurons that either collect information from the left or the right half of the ocellar plexus and two neurons that have a split dendritic tree in both halves. Fourteen large L-neurons collect information from the median ocellus and six to seven L-neurons from each of the lateral ocelli. The only L-neurons that project to the contralateral protocerebrum are those that have their dendritic branches in the ventral plexi of both median and lateral ocelli. The target areas of dorsal L-neurons from the lateral ocelli include a tract of mechanosensory fibers originating in the antennae. We compare our findings with what is known from the ocellar systems of other insects, make a number of functional inferences and discuss the advantages and disadvantages of mCT scans for the purpose of tracing large neuron profiles.We acknowledge financial support from the ANU Endowment Fund

The organization of honeybee ocelli: Regional specializations and rhabdom arrangements

We have re-investigated the organization of ocelli in honeybee workers and drones. Ocellar lenses are divided into a dorsal and a ventral part by a cusp-shaped indentation. The retina is also divided, with a ventral retina looking skywards and a dorsal retina looking at the horizon. The focal plane of lenses lies behind the retina in lateral ocelli, but within the dorsal retina in the median ocellus of both workers and drones. Ventral retinula cells are ca. 25μm long with dense screening pigments. Dorsal retinula cells are ca. 60μm long with sparse pigmentation mainly restricted to their proximal parts. Pairs of retinula cells form flat, non-twisting rhabdom sheets with elongated, straight, rectangular cross-sections, on average 8.7μm long and 1μm wide. Honeybee ocellar rhabdoms have shorter and straighter cross-sections than those recently described in the night-active bee Megalopta genalis. Across the retina, rhabdoms form a fan-shaped pattern of orientations. In each ocellus, ventral and dorsal retinula cell axons project into two separate neuropils, converging on few large neurons in the dorsal, and on many small neurons in the ventral neuropil. The divided nature of the ocelli, together with the particular construction and arrangement of rhabdoms, suggest that ocelli are not only involved in attitude control, but might also provide skylight polarization compass information

Compound eye and ocellar structure for walking and flying modes of locomotion in the Australian ant, Camponotus consobrinus

Ants are unusual among insects in that individuals of the same species within a single colony have different modes of locomotion and tasks. We know from walking ants that vision plays a significant role in guiding this behaviour, but we know surprisingly little about the potential contribution of visual sensory structures for a flying mode of locomotion. Here we investigate the structure of the compound eye and ocelli in pedestrian workers, alate females and alate males of an Australian ant, Camponotus consobrinus, and discuss the trade-offs involved in optical sensitivity and spatial resolution. Male ants have more but smaller ommatidia and the smallest interommatidial angles, which is most likely an adaptation to visually track individual flying females. Both walking and flying forms of ants have a similar proportion of specialized receptors sensitive to polarized skylight, but the absolute number of these receptors varies, being greatest in males. Ocelli are present only in the flying forms. Each ocellus consists of a bipartite retina with a horizon-facing dorsal retina, which contains retinula cells with long rhabdoms, and a sky-facing ventral retina with shorter rhabdoms. We discuss the implications of these and their potential for sensing the pattern of polarized skylight.10 page(s