Compound Eye Adaptations for Diurnal and Nocturnal Lifestyle in the Intertidal Ant, Polyrhachis sokolova

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.

[1]  R. Wehner.  Himmelsnavigation bei Insekten : Neurophysiologie und Verhalten , 1982 .

[2]  Eric J. Warrant,et al.  Visual summation in night-flying sweat bees: A theoretical study , 2006, Vision Research.

[3]  G. Horridge.  The Compound eye and vision of insects , 1975 .

[4]  T S Collett,et al.  Novel landmark-guided routes in ants , 2007, Journal of Experimental Biology.

[5]  G. D. Bernard,et al.  Insect pupil mechanisms , 1979, Journal of Comparative Physiology A.

[6]  Invertebrate photoreceptor optics , .

[7]  R. Menzel,et al.  Functional organisation of an insect ommatidium with fused rhabdom , 1975 .

[8]  Norm Johnson,et al.  Nomenclatural changes and new Australian records in the ant genus Polyrhachis Fr. Smith (Hymenoptera: Formicidae: Formicinae). , 1988 .

[9]  R. Peters,et al.  Caste-specific visual adaptations to distinct daily activity schedules in Australian Myrmecia ants , 2011, Proceedings of the Royal Society B: Biological Sciences.

[10]  Eric J. Warrant,et al.  Vision and visual navigation in nocturnal insects. , 2011, Annual review of entomology.

[11]  Almut Kelber,et al.  Visual ecology of Indian carpenter bees II: adaptations of eyes and ocelli to nocturnal and diurnal lifestyles , 2009, Journal of Comparative Physiology A.

[12]  Eric J. Warrant,et al.  Lunar orientation in a beetle , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[13]  J. H. van Hateren,et al.  Three modes of spatiotemporal preprocessing by eyes , 1993, Journal of Comparative Physiology A.

[14]  R. Wehner,et al.  Fine structure of light‐ and dark‐adapted eyes of desert ants, Cataglyphis bicolor (Formicidae, Hymenoptera) , 1973, Journal of morphology.

[15]  R. Wehner,et al.  Visual navigation in insects: coupling of egocentric and geocentric information , 1996, The Journal of experimental biology.

[16]  S. Robson,et al.  A review of the nesting habits and socioecology of the ant genus Polyrhachis Fr. Smith , 2007 .

[17]  Eric J. Warrant,et al.  Absorption of white light in photoreceptors , 1998, Vision Research.

[18]  Ajay Narendra,et al.  Homing strategies of the Australian desert ant Melophorus bagoti II. Interaction of the path integrator with visual cue information , 2007, Journal of Experimental Biology.

[19]  J. Zeil,et al.  The properties of the visual system in the Australian desert ant Melophorus bagoti. , 2011, Arthropod structure & development.

[20]  J. Zeil.  Visual homing: an insect perspective , 2012, Current Opinion in Neurobiology.

[21]  Esch,et al.  Distance estimation by foraging honeybees , 1996, The Journal of experimental biology.

[22]  Stanley Heinze.  Polarization Vision , 2014, Encyclopedia of Computational Neuroscience.

[23]  Colin R. Trainor,et al.  Biogeography of Timor and Surrounding Wallacean Islands: Endemism in Ants of the Genus Polyrhachis Fr. Smith , 2013 .

[24]  Eye structure correlates with distinct foraging-bout timing in primitive ants , 2007, Current Biology.

[25]  Rüdiger Wehner,et al.  Neurobiology of polarization vision , 1989, Trends in Neurosciences.

[26]  E. Warrant.  Seeing better at night: life style, eye design and the optimum strategy of spatial and temporal summation , 1999, Vision Research.

[27]  Structural specializations of the cornea and retina at the dorsal rim of the compound eye in hymenopteran insects , 2004, Cell and Tissue Research.

[28]  M. Land.  Visual acuity in insects. , 1997, Annual review of entomology.

[29]  P. Graham,et al.  Ants use the panoramic skyline as a visual cue during navigation , 2009, Current Biology.

[30]  J. Zeil,et al.  Polarised skylight and the landmark panorama provide night-active bull ants with compass information during route following , 2011, Journal of Experimental Biology.

[31]  D. Stavenga.  Angular and spectral sensitivity of fly photoreceptors. I. Integrated facet lens and rhabdomere optics , 2002, Journal of Comparative Physiology A.

[32]  J. Spaethe,et al.  Sex and Caste-Specific Variation in Compound Eye Morphology of Five Honeybee Species , 2013, PloS one.

[33]  Fukushi,et al.  Optical scaling in conspecific Cataglyphis ants , 1995, The Journal of experimental biology.

[34]  Eric J. Warrant,et al.  A neural network to improve dim-light vision? Dendritic fields of first-order interneurons in the nocturnal bee Megalopta genalis , 2005, Cell and Tissue Research.

[35]  Birgit Greiner.  Visual adaptations in the night‐active wasp Apoica pallens , 2006, The Journal of comparative neurology.

[36]  Eric J. Warrant,et al.  Retinal and optical adaptations for nocturnal vision in the halictid bee Megalopta genalis , 2004, Cell and Tissue Research.

[37]  Rüdiger Wehner,et al.  The significance of direct sunlight and polarized skylight in the ant’s celestial system of navigation , 2006, Proceedings of the National Academy of Sciences.

[38]  R. Wehner,et al.  Visual spatial memory in desert ants,Cataglyphis bicolor (Hymenoptera: Formicidae) , 1979, Experientia.

[39]  Life in the dark : vision and navigation in a nocturnal bull ant , 2010 .

[40]  Ursula Menzi,et al.  Visual adaptation in nocturnal and diurnal ants , 2004, Journal of Comparative Physiology A.

[41]  D. Stavenga,et al.  Insect pupil mechanisms , 2004, Journal of comparative physiology.

[42]  A. Narendra,et al.  Navigational Efficiency of Nocturnal Myrmecia Ants Suffers at Low Light Levels , 2013, PloS one.

[43]  Jay M. Enoch,et al.  Vertebrate photoreceptor optics , 1981 .

[44]  R. Morse.  The Dance Language and Orientation of Bees , 1994 .

[45]  J. Zeil,et al.  Mapping the navigational knowledge of individually foraging ants, Myrmecia croslandi , 2013, Proceedings of the Royal Society B: Biological Sciences.

[46]  Michael F. Land,et al.  Optics and Vision in Invertebrates , 1981 .

[47]  E. Warrant,et al.  The visual ecology of pupillary action in superposition eyes , 2004, Journal of Comparative Physiology A.

[48]  D. Stavenga,et al.  Insect pupil mechanisms , 2004, Journal of comparative physiology.

[49]  D. Stavenga.  Angular and spectral sensitivity of fly photoreceptors. II. Dependence on facet lens F-number and rhabdomere type in Drosophila , 2003, Journal of Comparative Physiology A.

[50]  R. Menzel.  The Fine Structure of the Compound Eye of Formica polyctena — Functional Morphology of a Hymenopterean Eye , 1972 .

[51]  U. Homberg,et al.  Behavioral analysis of polarization vision in tethered flying locusts , 2003, Journal of Comparative Physiology A.

[52]  B. WALCOTT,et al.  Movement of Retinula Cells in Insect Eyes on Light Adaptation , 1969, Nature.

[53]  Sex and Caste Specific Eye Structures in Stingless Bees and Honey Bees (Hymenoptera: Trigonidae, Apidae) , 1989 .

[54]  T. Labhart,et al.  Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye , 1999, Microscopy research and technique.