Abstract
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.
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References
Berry RP, Warrant EJ, Stange G (2007a) Form vision in the insect dorsal ocelli: an anatomical and optical analysis of the locust ocelli. Vis Res 47:1382–1393
Berry RP, Warrant EJ, Stange G (2007b) Form vision in the insect dorsal ocelli: an anatomical and optical analysis of the dragonfly median ocellus. Vis Res 47:1394–1409
Berry RP, Wcislo WT, Warrant EJ (2011) Ocellar adaptations for dim light vision in a nocturnal bee. J Exp Biol 214:1283–1293
Chahl J, Mizutani A (2012) Biomimetic attitude and orientation sensors. IEEE Sens J 12(2):289–297
Dickens JC, Eaton JL (1974) Fine structure of ocelli in sphinx moths. Tissue Cell 6:463–470
Dow MA, Eaton JL (1976) Fine structure of the ocellus of the cabbage looper moth (Trichoplusia ni). Cell Tissue Res 171:523–533
Fent K, Wehner R (1985) Ocelli—a celestial compass in the desert ant Cataglyphis. Science 228:192–194
Fuller SB, Karpelson M, Censi A, Ma KY, Wood RJ (2014) Controlling free flight of a robotic fly using an onboard vision sensor inspired by insect ocelli. J R Soc Interface 11:20140281
Futahashi R, Kawahara-Miki R, Kinoshita M, Yoshitake K, Yajima S, Arikawa K, Fukatsu T (2015) Extraordinary diversity of visual opsin genes in dragonflies. Proc Nat Acad Sci 112:E1247-E1256
Geiser FX, Labhart T (1982) Electrophysiological investigation on the ocellar retina of the honeybee (Apis mellifera). Verh Dtsch Zool Gesellschaft 75:307
Goldsmith TH, Ruck PR (1958) The spectral sensitivities of the dorsal ocelli of cockroaches and honeybees. J Gen Physiol 41:1171–1185
Gremillion G, Humbert JS, Krapp HG (2014) Bio-inspired modeling and implementation of the ocelli visual system of flying insects. Biol Cybern 108:735–746
Grünewald B, Wunderer H (1996) The ocelli of arctiid moths: ultrastructure of the retina during light and dark adaptation. Tissue Cell 28:267–277
Hallberg E, Hagberg M (1986) Ocellar fine structure in Caenis robusta (Ephemeroptera), Trichostegia minor, Agrypnia varia, and Limnephilus flavicornis (Trichoptera). Protoplasma 135:12–18
Henze MJ, Dannenhauer K, Kohler M, Labhart T, Gesemann M (2012) Opsin evolution and expression in arthropod compound eyes and ocelli: insights from the cricket Gryllus bimaculatus. BMC Evol Biol 12:163
Hertweck H (1931) Anatomie und Variabilität des Nervensystems und der Sinnesorgane von Drosophila melanogaster (Meigen). Z Wiss Zool 139:559–663
Honkanen A, Saari P, Takalo J, Heimonen K, Weckström M (2017) The role of ocelli in cockroach optomotor performance. J Comp Physiol A 204:231–243
Hung Y-S, Ibbotson MR (2014) Ocellar structure and neural innervation in the honeybee. Front Neuroanat 8:1–11
Insausti TC, Lazzari CR (2002) The fine structure of the ocelli of Triatoma infestans (Hemiptera: Reduviidae). Tissue Cell 34(6):437–449
Kerfoot WB (1967a) Correlation between ocellar size and the foraging activities of bees (Hymenoptera; Apoidea). Am Nat 101:65–70
Kerfoot WB (1967b) Dorsal light receptors. Nature 215:305–307
Kral K (1978) The orientation of the rhabdoms in the ocelli of Apis mellifera carnia Pollm. and of Vespa vulgaris L. Zool Jahrb Physiol 82:263–271
Krapp HG (2009) Ocelli. Curr Biol 19:R435–R437
Labhart T, Meyer EP (1999) Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc Res Tech 47:368–379
Lazzari CR, Fischbein D, Insausti TC (2011) Differential control of light–dark adaptation in the ocelli and compound eyes of Triatoma infestans. J Insect Physiol 57:1545–1552
Meyer-Rochow VB (1980) Electrophysiologically determined spectral efficiencies of the compound eye and median ocellus in the Bumblebee Bombus hortorum tarhakimalainen (Hymenoptera, Insecta). J Comp Physiol 139:261–266
Mizunami M (1994) Information processing in the insect ocellar system: comparative approaches to the evolution of visual processing and neural circuits. Adv Insect Physiol 25:151–265
Mizunami M (1995) Functional diversity of neural organization in insect ocellar systems. Vis Res 35:443–452
Müller H (1875) Function of the ocelli of hymenopterous insects. Nature 15:167–168
Narendra A, Ribi W (2017) Ocellar structure is driven by the mode of locomotion and activity time in Myrmecia ants. J Exp Biol 220:4383–4390
Narendra A, Ramirez-Esquivel F, Ribi WA (2016) Compound eye and ocellar structure for walking and flying modes of locomotion in the Australian ant, Camponotus consobrinus. Sci Rep 6:22331
Ogawa Y, Ribi W, Zeil J, Hemmi JM (2017) Regional differences in the preferred e-vector orientation of honeybee ocellar photoreceptors. J Exp Biol 220:1701–1708
Parsons MM, Krapp HG, Laughlin SB (2006) A motion-sensitive neurone responds to signals from the two visual systems of the blowfly, the compound eyes and ocelli. J Exp Biol 209:4464–4474
Parsons MM, Krapp HG, Laughlin SB (2010) Sensor fusion in identified visual interneurons. Curr Biol 20:624–628
Ribi WA, Zeil J (2015) The visual system of the Australian ‘Redeye’ Cicada (Psaltoda moerens). Arthropod Struct Dev 44:574–586
Ribi W, Zeil J (2017) Three-dimensional visualization of ocellar interneurons of the Orchid bee Euglossa imperialis using micro X-ray Computed Tomography. J Comp Neurol 525:3581–3595
Ribi WA, Warrant EJ, Zeil J (2011) The organization of honeybee ocelli: regional specialization and rhabdom arrangements. Arthropod Struct Dev 40:509–520
Ruck P, Edwards GA (1964) The structure of the insect dorsal ocellus. I. General organization of the ocellus in dragonflies. J Morphol 115:1–26
Schwarz S, Albert L, Wystrach A, Cheng K (2011) Ocelli contribute to the encoding of celestial compass information in the Australian desert ant Melophorus bagoti. J Exp Biol 214:901–906
Somanathan H, Kelber A, Borges RM, Wallén R, Warrant EJ (2009) Visual ecology of Indian carpenter bees II: adaptations of eyes and ocelli to nocturnal and diurnal lifestyles. J Comp Physiol A 195:571–583
Stange G (1981) The ocellar component of flight equilibrium control in dragonflies. J Comp Physiol A 141:335–347
Stange G, Howard J (1979) An ocellar dorsal light response in a dragonfly. J Exp Biol 83:351–355
Stange GS, Stowe JS, Chahl JS, Massro A (2002) Anisotropic imaging in the dragonfly median ocellus: a matched filter for horizon detection. J Comp Physiol A 188:455–467
Taylor GJ, Ribi W, Bech M, Bodey AJ, Rau C, Steuwer A, Warrant EJ, Baird E (2016) The dual function of orchid bee ocelli as revealed by X-ray microtomography. Curr Biol 26:1319–1324
Toh Y, Kuwabara M (1974) Fine structure of the dorsal ocellus of the worker honeybee. J Morphol 143:285–306
Toh Y, Kuwabara M (1975) Synaptic organization of the fleshfly ocellus. J Neurocytol 4:271–287
Toh Y, Sagara H (1984) Dorsal ocellar system of the American cockroach. I. Structure of the ocellus and ocellar nerve. J Ultrastruct Res 86:119–134
Toh Y, Tominaga Y, Kuwabara M (1971) The fine structure of the dorsal ocellus of the fleshfly. J Electronmicrosc 20:56–56
van Kleef J, James AC, Stange G (2005) A spatiotemporal white noise analysis of photoreceptor responses to UV and green light in the dragonfly median ocellus. J Gen Physiol 126:481–497
Warrant EJ, Kelber A, Walle´n R, Wcislo W (2006) Ocellar optics in diurnal and nocturnal bees and wasps. Arthropod Struct Dev 35:293–305
Weber G, Renner M (1976) The ocellus of the cockroach, Periplaneta americana (Blattariae). Receptro area. Cell Tissue Res 168:209–222
Wei Y, Hua B (2011) Ultrastructural comparison of the ocelli of Sinopanorpa tincta and Bittacus planus (Mecoptera). Microsc Res Tech 74:502–511
Wellington WG (1974) Bumblebee ocelli and navigation at dusk. Science 183:550–551
Wheeler W (1936) Binary anterior ocelli in ants. Biol Bull 70:185–192
Wilson M (1978) The functional organization of locust ocelli. J Comp Physiol 124:297–316
Wunderlich H (1988) The fine structure of the dorsal ocelli in the male bibionid fly. Tissue Cell 20:145–155
Yoon C-S, Hirosawa K, Suzuki E (1996) Studies on the structure of ocellar photoreceptor cells of Drosophila melanogaster with special reference to subrhabdomeric cisternae. Cell Tissue Res 284:77–85
Zeil J, Ribi W, Narendra A (2014) Polarisation vision in ants, bees and wasps. In: Horvath G (ed) Polarized light and polarization vision in animal sciences. Springer, Heidelberg, pp 41–60
Acknowledgements
We thank the ANU Centre of Advanced Microscopy (CAM) for the use of their facilities, CSIRO Entomology for identification of some insects and Michael Batley, Australian Museum, Sydney, for the identification of Amegilla. The work was made possible by financial support from the ANU endowment fund. We thank Joanne Lee (CAM), Rainer Foelix (Aarau), Hua Chun (CAM) for their help with SEM scanning, and Ladina Ribi, Sara Wood and Sharyn Wragg for preparing the drawings.
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Ribi, W., Zeil, J. Diversity and common themes in the organization of ocelli in Hymenoptera, Odonata and Diptera. J Comp Physiol A 204, 505–517 (2018). https://doi.org/10.1007/s00359-018-1258-0
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DOI: https://doi.org/10.1007/s00359-018-1258-0