The dorsal eye of the dragonfly Sympetrum: specializations for prey detection against the blue sky

Dragonflies of the genus Sympetrum have compound eyes conspicuously divided into dorsal and ventral regions. Using anatomical, optical, electrophysiological, in-vivo photochemical and microspectrophotometrical methods, we have investigated the design and physiology of the dorsal part which is characterized by a pale yellow-orange screening pigment and extremely large facets. The upper part of the yellow dorsal region is a pronounced fovea with interommatidial angles approaching 0.3°, contrasting to the much larger values of 1.5°–2° in the rest of the eye. The dorsal eye part is exclusively sensitive to short wavelengths (below 520 nm). It contains predominantly blue-receptors with a sensitivity maximum at 420 nm, and a smaller amount of UV-receptors. The metarhodopsin of the blue-receptors absorbs maximally at 535 nm. The yellow screening pigment transmits longwavelength light (cut-on 580 nm), which increases the conversion rate from metarhodopsin to rhodopsin (see Fig. 11a). We demonstrate that because of the yellow pigment screen nearly all of the photopigment is in the rhodopsin state under natural conditions, thus maximizing sensitivity. Theoretical considerations show that the extremely long rhabdoms (1.1 mm) in the dorsal fovea are motivated for absorption reasons alone. A surprising consequence of the long rhabdoms is that the sensitivity gain, caused by pumping photopigment into the rhodopsin state, is small. To explain this puzzling fact we present arguments for a mechanism producing a gradient of rhodopsin concentration along the rhabdom, which would minimize saturation of transduction units, and hence improve the signal-to-noise ratio at high intensities. The latter is of special importance for the short integration time and high contrast sensitivity these animals need for spotting small prey at long distances.

[1]  Philip Ruck,et al.  A comparison of the electrical responses of compound eyes and dorsal ocelli in four insect species , 1958 .

[2]  S. T. Henderson,et al.  The spectral energy distribution of daylight , 1963 .

[3]  P. Ruck The Components of the Visual System of a Dragonfly , 1965, The Journal of general physiology.

[4]  K. Hamdorf,et al.  Photoregeneration and Sensitivity Control of Photoreceptors of Invertebrates , 1973 .

[5]  Kuno Kirschfeld,et al.  The Absolute Sensitivity of Lens and Compound Eyes , 1974, Zeitschrift fur Naturforschung. Section C, Biosciences.

[6]  G A Horridge,et al.  The ommatidium of the dorsal eye of Cloeon as a specialization for photoreisomerization , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[7]  The dorsal compound eye of simuliid flies: an eye specialized for the detection of small, rapidly moving objects. , 1976, Zeitschrift fur Naturforschung. Section C, Biosciences.

[8]  Barry Honig,et al.  New wavelength dependent visual pigment nomograms , 1977, Vision Research.

[9]  George Adrian Horridge,et al.  The dorsal eye of the mayfly Atalophlebia (Ephemeroptera) , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[10]  Doekele G. Stavenga,et al.  Pseudopupils of Compound Eyes , 1979 .

[11]  A. Snyder Physics of Vision in Compound Eyes , 1979 .

[12]  K. Hamdorf The Physiology of Invertebrate Visual Pigments , 1979 .

[13]  Pigment transformation and electrical responses in retinula cells of drone, Apis mellifera male. , 1979, The Journal of physiology.

[14]  R. Wehner Spatial Vision in Arthropods , 1981 .

[15]  S B Laughlin,et al.  Single photon signals in fly photoreceptors and first order interneurones at behavioral threshold. , 1981, The Journal of physiology.

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

[17]  G. Horridge,et al.  Light guides in the dorsal eye of the male mayfly , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[18]  A. Snyder,et al.  Transduction as a limitation on compound eye function and design , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[19]  Bleaching of Rhabdoms in Eyes of Intact Butterflies , 1983, Science.

[20]  Doekele G. Stavenga,et al.  Visual Pigments of Invertebrates , 1984 .

[21]  S B Laughlin,et al.  Synaptic limitations to contrast coding in the retina of the blowfly Calliphora , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[22]  Barbara Blakeslee,et al.  The intracellular pupil mechanism and photoreceptor signal: noise ratios in the fly Lucilia cuprina , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[23]  D. Stavenga Pigments in Compound Eyes , 1989 .

[24]  Michael F. Land,et al.  Variations in the Structure and Design of Compound Eyes , 1989 .

[25]  Simon Laughlin,et al.  The reliability of single neurons and circuit design: a case study , 1989 .

[26]  K. Hamdorf,et al.  Microvillar components of light adaptation in blowflies , 1990, The Journal of general physiology.

[27]  R. B. Pinter,et al.  Changes of Acuity during Light and Dark Adaptation in the Dragonfly Compound Eye , 1990 .

[28]  A method for estimating the minimum visual stimulus that evokes a behavioural response in the drone, apis mellifera ♂ , 1991, Vision Research.

[29]  D. Stavenga,et al.  Functional morphology of the divided compound eye of the honeybee drone (Apis mellifera). , 1991, Tissue & cell.

[30]  D. Stavenga Eye regionalization and spectral tuning of retinal pigments in insects , 1992, Trends in Neurosciences.

[31]  J. Schwemer Visual pigment renewal and the cycle of the chromophore in the compound eye of the blowfly , 1993 .

[32]  D. Stavenga,et al.  Simple exponential functions describing the absorbance bands of visual pigment spectra , 1993, Vision Research.

[33]  R. Barlow,et al.  On the molecular origin of photoreceptor noise , 1993, Nature.

[34]  Modlin,et al.  A MYSID SHRIMP CARRYING A PAIR OF BINOCULARS , 1994, The Journal of experimental biology.

[35]  Christian Kleinewächter,et al.  On identification , 2005, Electron. Notes Discret. Math..

[36]  P.,et al.  Microvillar Components of Light Adaptation in Blowflies , 2003 .

[37]  P. Streck Der Einfluß des Schirmpigmentes auf das Sehfeld einzelner Sehzellen der Fliege Calliphora erythrocephala Meig. , 1972, Zeitschrift für vergleichende Physiologie.

[38]  K. Hamdorf,et al.  Beschleunigung der „Dunkeladaptation“ eines UV-Rezeptors durch sichtbare Strahlung , 1971, Zeitschrift für vergleichende Physiologie.

[39]  R. Menzel,et al.  The identification of spectral receptor types in the retina and lamina of the dragonflySympetrum rubicundulum , 1983, Journal of comparative physiology.

[40]  T. Goldsmith,et al.  The visual pigment and visual cycle of the lobster,Homarus , 2004, Journal of comparative physiology.

[41]  M. Gogala Die spektrale Empfindlichkeit der Doppelaugen von Ascalaphus macaronius Scop. (Neuroptera, Ascalaphidae) , 1967, Zeitschrift für vergleichende Physiologie.

[42]  S. Laughlin,et al.  The structures of dorsal and ventral regions of a dragonfly retina , 1978, Cell and Tissue Research.

[43]  G. Horridge Unit studies on the retina of dragonflies , 1969, Zeitschrift für vergleichende Physiologie.

[44]  I. Meinertzhagen,et al.  Structural organization of the ommatidium in the ventral compound eye of the dragonflySympetrum , 1983, Journal of comparative physiology.

[45]  T. Labhart,et al.  Morphological specializations of dorsal rim ommatidia in the compound eye of dragonflies and damselfies (Odonata) , 1993, Cell and Tissue Research.

[46]  Allan W. Snyder,et al.  Acuity of compound eyes: Physical limitations and design , 2004, Journal of comparative physiology.

[47]  K. Hamdorf,et al.  UV-Sehfarbstoff bei Insekten , 1970, Zeitschrift für vergleichende Physiologie.

[48]  D. Burkhardt,et al.  Das Sehfeld einzelner Sehzellen: Eine Richtigstellung , 1965, Zeitschrift für vergleichende Physiologie.

[49]  J. Howard,et al.  Intensity and polarization of the eyeshine in butterflies , 1989, Journal of Comparative Physiology A.

[50]  J. H. Hateren,et al.  Waveguide theory applied to optically measured angular sensitivities of fly photoreceptors , 1984, Journal of Comparative Physiology A.

[51]  N. Franceschini,et al.  Les phénomènes de pseudopupille dans l'œil composé deDrosophila , 1971, Kybernetik.