Abstract
Few walking insects possess simple eyes known as the ocelli. The role of the ocelli in walking insects such as ants has been less explored. Physiological and behavioural evidence in the desert ant, Cataglyphis bicolor, indicates that ocellar receptors are polarisation sensitive and are used to derive compass information from the pattern of polarised skylight. The ability to detect polarised skylight can also be inferred from the structure and the organisation of the ocellar retina. However, the functional anatomy of the desert ant ocelli has not been investigated. Here we characterised the anatomical organisation of the ocelli in three species of desert ants. The two congeneric species of Cataglyphis we studied had a fused rhabdom, but differed in their organisation of the retina. In Cataglyphis bicolor, each retinula cell contributed microvilli in one orientation enabling them to compare e-vector intensities. In Cataglyphis fortis, some retinula cells contributed microvilli in more than one orientation, indicating that not all cells are polarisation sensitive. The desert ant Melophorus bagoti had an unusual ocellar retina with a hexagonal or pentagonal rhabdomere arrangement forming an open rhabdom. Each retinula cell contributed microvilli in more than one orientation, making them unlikely to be polarisation detectors.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Berry RP, Wcislo WT, Warrant EJ (2011) Ocellar adaptations for dim light vision in a nocturnal bee. J Exp Biol 214:1283–1293
Dreyer D, Frost B, Mouritsen H et al (2018) The Earth’s magnetic field and visual landmarks steer migratory flight behavior in the nocturnal Australian Bogong moth. Curr Biol 28:1–7
Fent K (1986) Polarized skylight orientation in the desert ant Cataglyphis. J Comp Physiol A 158:145–150
Fent K, Wehner R (1985) Ocelli: a celestial compass in the desert ant Cataglyphis. Science 228:192–194
Geiser FX, Labhart T (1982) Electrophysiological investigation on the ocellar retina of the honeybee (Apis mellifera). Verhandlungen der Dtsch Zool Gesellschaft 75:307
Graham P, Fauria K, Collett TS (2003) The influence of beacon-aiming on the routes of wood ants. J Exp Biol 206:535–541
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 12:163–178
Honkanen A, Adden A, da Silva Freitas J, Heinze S (2019) The insect central complex and the neural basis of navigational strategies. J Exp Biol 222:jeb188854. https://doi.org/10.1242/jeb.188854
Labhart T (1986) The electrophysiology of photoreceptors in different eye regions of the desert ant, Cataglyphis bicolor. J Comp Physiol A 158:1–7. https://doi.org/10.1007/BF00614514
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
Mote M, Wehner R (1980) Functional characteristics of photoreceptors in the compound eye and ocellus of the desert ant, Cataglyphis bicolor. J Comp Physiol A 137:63–71
Narendra A, Ribi WA (2017) Ocellar structure is driven by the mode of locomotion and activity time in Myrmecia ants. J Exp Biol 220:4383–4390. https://doi.org/10.1242/jeb.159392
Narendra A, Reid SF, Greiner B et al (2011) Caste-specific visual adaptations to distinct daily activity schedules in Australian Myrmecia ants. Proc R Soc B 278:1141–1149. https://doi.org/10.1098/rspb.2010.1378
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. https://doi.org/10.1038/srep22331
Ogawa Y, Ribi WA, Zeil J, Hemmi JM (2017) Regional differences in the preferred e-vector orientation of honeybee ocellar photoreceptors. J Exp Biol 220:1701–1708
Ribi WA, 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, Zeil J (2018) Diversity and common themes in the organization of ocelli in Hymenoptera, Odonata and Diptera. J Comp Physiol A 204:505–517. https://doi.org/10.1007/s00359-018-1258-0
Ribi WA, Warrant EJ, Zeil J (2011) The organization of honeybee ocelli: regional specializations and rhabdom arrangements. Arthropod Struct Dev 40:509–520. https://doi.org/10.1016/j.asd.2011.06.004
Rossel S, Wehner RD (1984) Celestial orientation in bees: the use of spectral cues. J Comp Physiol A 155:605–613. https://doi.org/10.1007/BF00610846
Schwarz S, Albert L, Wystrach A, Cheng K (2011a) Ocelli contribute to the encoding of celestial compass information in the Australian desert ant Melophorus bagoti. J Exp Biol 214:901–906. https://doi.org/10.1242/jeb.049262
Schwarz S, Wystrach A, Cheng K (2011b) A new navigational mechanism mediated by ant ocelli. Biol Lett 7:856–858. https://doi.org/10.1098/rsbl.2011.0489
Snodgrass RE (1993) Principles of insect morphology. Cornell University Press, Ithaca
Somanathan H, Kelber A, Borges RM et al (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
Steck K (2012) Just follow your nose: homing by olfactory cues in ants. Curr Opin Neurobiol 22:231–235. https://doi.org/10.1016/j.conb.2011.10.011
Taylor GJ, Ribi WA, Bech M et al (2016) The dual function of Orchid bee ocelli as revealed by X-ray microtomography. Curr Biol 26:1319–1324. https://doi.org/10.1016/j.cub.2016.03.038
Toh Y, Tominaga Y, Kuwabara M (1971) The fine structure of the dorsal ocellus of the Fleshfly. J Electron Microsc 20:56–66
Uehara A, Toh Y, Tateda H (1977) Fine structure of the eyes of orb-weavers Argiope amoena L. Koch (Araneae: Argiopidae) 1. The anteromedial eyes. Cell Tissue Res 182:81–91
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. https://doi.org/10.1085/jgp.200509319
Warrant EJ, Kelber A, Wallén R, Wcislo W (2006) Ocellar optics in nocturnal and diurnal bees and wasps. Arthropod Struct Dev 35:293–305
Wehner R (2009) The architecture of the desert ant’s navigational toolkit. Myrmecol News 12:85–96
Wellington WG (1974) Bumblebee ocelli and navigation at dusk. Science 183:550–551. https://doi.org/10.1126/science.183.4124.550
Wunderer H, Weber G, Seifert P (1988) The fine structure of the dorsal ocelli in the male bibionid fly. Tissue Cell 20:145–155
Zeil J, Ribi WA, Narendra A (2014) Polarisation vision in ants, bees and wasps. In: Horváth G (ed) Polarized light and polarization vision in animal sciences. Springer, Berlin, pp 41–60
Acknowledgements
We are grateful to Wolfgang Rössler for loaning us samples of Cataglyphis ants and to Sebastian Schwarz for providing us samples of Melophorus bagoti. We acknowledge the microscopy facilities at Macquarie University, The Australian National University, and at the MPI of Tübingen. Working with these ants requires no ethics approval in Australia, but we treated them with care. We thank financial support from the ANU endowment fund to Willi Ribi, the Australian Research Council (FT140100221, DP150101172) and the Hermon Slade Foundation (HSF17/08).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Penmetcha, B., Ogawa, Y., Ribi, W.A. et al. Ocellar structure of African and Australian desert ants. J Comp Physiol A 205, 699–706 (2019). https://doi.org/10.1007/s00359-019-01357-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-019-01357-x