techniques-for-investigating-the-anatomy-of-the-ant-visual-system

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 ...

Australian National University

Lateralization of function is a well-known phenomenon in humans. The two hemispheres of the human brain are functionally specialized such that certain cognitive skills, such as language or musical ability, conspecific recognition, and even emotional responses, are mediated by one hemisphere more than the other [1, 2]. Studies over the past 30 years suggest that lateralization occurs in other vertebrate species as well [3-11]. In general, lateralization is observed in different sensory modalities in humans as well as vertebrates, and there are interesting parallels (reviewed in [12]). However, little is known about functional asymmetry in invertebrates [13, 14] and there is only one investigation in insects [15]. Here we show, for the first time, that the honeybee Apis mellifera displays a clear laterality in responding to learned odors. By training honeybees on two different versions of the well-known proboscis extension reflex (PER) paradigm [16, 17], we demonstrate that bees respond to odors better when they are trained through their right antenna. To our knowledge, this is the first demonstration of asymmetrical learning performance in an insect.

Lateralization of olfaction in the honeybee Apis mellifera.

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.

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

The Australian intertidal ant, Polyrhachis sokolova lives in mudflat habitats and nests at the base of mangroves. They are solitary foraging ants that rely on visual cues. The ants are active during low tides at both day and night and thus experience a wide range of light intensities. We here ask the extent to which the compound eyes of P. sokolova reflect the fact that they operate during both day and night. The ants have typical apposition compound eyes with 596 ommatidia per eye and an interommatidial angle of 6.0°. We find the ants have developed large lenses (33 µm in diameter) and wide rhabdoms (5 µm in diameter) to make their eyes highly sensitive to low light conditions. To be active at bright light conditions, the ants have developed an extreme pupillary mechanism during which the primary pigment cells constrict the crystalline cone to form a narrow tract of 0.5 µm wide and 16 µm long. This pupillary mechanism protects the photoreceptors from bright light, making the eyes less sensitive during the day. The dorsal rim area of their compound eye has specialised photoreceptors that could aid in detecting the orientation of the pattern of polarised skylight, which would assist the animals to determine compass directions required while navigating between nest and food sources.

Compound eye adaptations for diurnal and nocturnal lifestyle in the intertidal ant, Polyrhachis sokolova.

Animals use vision over a wide range of light intensities, from dim starlight to bright sunshine. For animals active in very dim light the visual system is challenged by several sources of visual noise. Adaptations in the eyes, as well as in the neural circuitry, have evolved to suppress the noise and enhance the visual signal, thereby improving vision in dim light. Among neural adaptations, spatial summation of visual signals from neighboring processing units is suggested to increase the reliability of signal detection and thus visual sensitivity. In insects, the likely neural candidates for carrying out spatial summation are the lamina monopolar cells (LMCs) of the first visual processing area of the insect brain (the lamina). We have classified LMCs in three species of hawkmoths with considerably different activity periods but very similar ecology-the diurnal Macroglossum stellatarum, the nocturnal Deilephila elpenor and the crepuscular-nocturnal Manduca sexta. Using this classification, we investigated the anatomical adaptations of hawkmoth LMCs suited for spatial summation. We found that specific types of LMCs have dendrites extending to significantly more neighboring cartridges in the two nocturnal and crepuscular species than in the diurnal species, making these LMC types strong candidates for spatial summation. Moreover, while the absolute number of cartridges visited by the LMCs differed between the two dim-light species, their dendritic extents were very similar in terms of visual angle, possibly indicating a limiting spatial acuity. The overall size of the lamina neuropil did not correlate with the size of its LMCs.

Adaptations for nocturnal and diurnal vision in the hawkmoth lamina.

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 34 μm and the lenses are unusually long with up to 100 μm 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 (<10 μm), positioned close to the corneagenous layer and are formed by pairs of retinular cells. In cross-section, the rhabdomeres are 2-5 μm 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.

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

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.

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

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.

Article	Year
Lateralization of olfaction in the honeybee Apis mellifera. Current biology : CB\| PubMed ID: 16860748	2006
Caste-specific visual adaptations to distinct daily activity schedules in Australian Myrmecia ants. Proceedings. Biological sciences\| PubMed ID: 20926444	2011
Compound eye adaptations for diurnal and nocturnal lifestyle in the intertidal ant, Polyrhachis sokolova. PloS one\| PubMed ID: 24155883	2013
Adaptations for nocturnal and diurnal vision in the hawkmoth lamina. The Journal of comparative neurology\| PubMed ID: 26100612	2016
The visual system of the Australian 'Redeye' cicada (Psaltoda moerens). Arthropod structure & development\| PubMed ID: 26335848	2015
Compound eye and ocellar structure for walking and flying modes of locomotion in the Australian ant, Camponotus consobrinus. Scientific reports\| PubMed ID: 26975481	2016
Light and dark adaptation mechanisms in the compound eyes of Myrmecia ants that occupy discrete temporal niches. The Journal of experimental biology\| PubMed ID: 27535985	2016

Willi A. Ribi

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