Abstract

Visually guided flight control in the rainforest is arguably one of the most complex insect behaviors: illumination varies dramatically depending on location [1Endler J.A. The color of light in forests and its implications.Ecol. Monogr. 1993; 63: 2-27Crossref Scopus (858) Google Scholar], and the densely cluttered environment blocks out most of the sky [2Gonsamo A. D'odorico P. Pellikka P. Measuring fractional forest canopy element cover and openness–definitions and methodologies revisited.Oikos. 2013; 122: 1283-1291Crossref Scopus (38) Google Scholar]. What visual information do insects sample for flight control in this habitat? To begin answering this question, we determined the visual fields of the ocelli—thought to play a role in attitude stabilization of some flying insects [3Stange G. The ocellar component of flight equilibrium control in dragonflies.J. Comp. Physiol. 1981; 141: 335-347Crossref Scopus (87) Google Scholar, 4Taylor C.P. Contribution of compound eyes and ocelli to steering of locusts in flight: I. Behavioural analysis.J. Exp. Biol. 1981; 93: 1-18Google Scholar, 5Parsons M.M. Krapp H.G. Laughlin S.B. Sensor fusion in identified visual interneurons.Curr. Biol. 2010; 20: 624-628Abstract Full Text Full Text PDF PubMed Scopus (43) Google Scholar]—of an orchid bee, Euglossa imperialis. High-resolution 3D models of the ocellar system from X-ray microtomography were used for optical ray tracing simulations. Surprisingly, these showed that each ocellus possesses two distinct visual fields—a focused monocular visual field suitable for detecting features elevated above the horizon and therefore assisting with flight stabilization [3Stange G. The ocellar component of flight equilibrium control in dragonflies.J. Comp. Physiol. 1981; 141: 335-347Crossref Scopus (87) Google Scholar, 4Taylor C.P. Contribution of compound eyes and ocelli to steering of locusts in flight: I. Behavioural analysis.J. Exp. Biol. 1981; 93: 1-18Google Scholar, 5Parsons M.M. Krapp H.G. Laughlin S.B. Sensor fusion in identified visual interneurons.Curr. Biol. 2010; 20: 624-628Abstract Full Text Full Text PDF PubMed Scopus (43) Google Scholar] and, unlike other ocelli investigated to date [4Taylor C.P. Contribution of compound eyes and ocelli to steering of locusts in flight: I. Behavioural analysis.J. Exp. Biol. 1981; 93: 1-18Google Scholar, 6Berry R. van Kleef J. Stange G. The mapping of visual space by dragonfly lateral ocelli.J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2007; 193: 495-513Crossref PubMed Scopus (33) Google Scholar, 7Ribi W. Warrant E. Zeil J. The organization of honeybee ocelli: Regional specializations and rhabdom arrangements.Arthropod Struct. Dev. 2011; 40: 509-520Crossref PubMed Scopus (26) Google Scholar], a large trinocular fronto-dorsal visual field shared by all ocelli. Histological analyses show that photoreceptors have similar orientations within each ocellus and are likely to be sensitive to polarized light, as in some other hymenopterans [7Ribi W. Warrant E. Zeil J. The organization of honeybee ocelli: Regional specializations and rhabdom arrangements.Arthropod Struct. Dev. 2011; 40: 509-520Crossref PubMed Scopus (26) Google Scholar, 8Zeil J. Ribi W.A. Narendra A. Polarisation vision in ants, bees and wasps.in: Horváth G. Polarized Light and Polarization Vision in Animal Sciences. Springer, 2014: 41-60Crossref Scopus (42) Google Scholar]. We also found that the average receptor orientation is offset between the ocelli, each having different axes of polarization sensitivity relative to the head. Unlike the eyes of any other insect described to date, this ocellar system meets the requirements of a true polarization analyzer [9Kirschfeld K. Die notwendige Anzahl von Rezeptoren zur Bestimmung der Richtung des elektrischen Vektors linear polarisierten Lichtes.Z. Naturforsch., B. J. Chem. Sci. 1972; 27c: 578-579Google Scholar, 10Wehner R. Labhart T. Polarization vision.in: Warrant E.J. Nilsson D.-E. Invertebrate Vision. Cambridge University Press, 2006: 291-348Google Scholar]. The ocelli of E. imperialis could provide sensitive compass information for navigation in the rainforest and, additionally, provide cues for visual discrimination or flight control.