Physiological basis of phototaxis to near-infrared light in Nephotettix cincticeps

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 200, Issue 6, 2014, Pages 527-536

  Wakakuwa, Motohiro ^a   Stewart, Finlay ^a   Matsumoto, Yukiko ^b   Matsunaga, Shigeru ^c   Arikawa, Kentaro ^a  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^c CENTRAL RESEARCH LABORATORY   (Japan)

Author keywords

Hemipteran insect; Ommatidia; Photoreceptor; Phototaxis; Spectral sensitivity; Visual pigment

Indexed keywords

MESSENGER RNA; OPSIN;

ANIMAL; BUTTERFLY; CLASSIFICATION; COLOR; COLOR VISION; GENETICS; MALE; MAZE TEST; METABOLISM; PHOTORECEPTOR CELL; PHOTOSTIMULATION; PHYSIOLOGY; PROCEDURES; RADIATION RESPONSE; ULTRAVIOLET RADIATION;

ANIMALS; BUTTERFLIES; COLOR; COLOR PERCEPTION; DOSE-RESPONSE RELATIONSHIP, RADIATION; MALE; MAZE LEARNING; OPSINS; PHOTIC STIMULATION; PHOTORECEPTOR CELLS, INVERTEBRATE; RNA, MESSENGER; ULTRAVIOLET RAYS;

EID: 84901687289     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-014-0892-4     Document Type: Article

References (62)

1. Arikawa K, Inokuma K, Eguchi E (1987a) Pentachromatic visual system in a butterfly. Naturwissenschaften 74: 297-298.
2. Arikawa K, Kawamata K, Suzuki T, Eguchi E (1987b) Daily changes of structure, function and rhodopsin content in the compound eye of the crab Hemigrapsus sanguineus. J Comp Physiol A 161: 161-174.
3. Arikawa K, Scholten DGW, Kinoshita M, Stavenga DG (1999) Tuning of photoreceptor spectral sensitivities by red and yellow pigments in the butterfly Papilio xuthus. Zool Sci 16: 17-24.
4. Arikawa K, Pirih P, Stavenga DG (2009) Rhabdom constriction enhances filtering by the red screening pigment in the eye of the Eastern Pale Clouded yellow butterfly, Colias erate (Pieridae). J Exp Biol 212: 2057-2064.
5. Armett-Kibel C, Meinertzhagen IA, Dowling JE (1977) Cellular and synaptic organization in the lamina of the dragon-fly Sympetrum rubicundulum. Proc R Soc B 196: 385-413.
6. Autrum H (1968) Colour vision in man and animals. Naturwissenschaften 55: 10-18.
7. Autrum H, von Zwehl V (1964) Die spektrale Empfindlichkeit einzelner Sehzellen des Bienenauges. Z Vergl Physiol 48: 357-384.
8. Bernard GD (1979) Red-absorbing visual pigment of butterflies. Science 203: 1125-1127.
9. Bernard GD, Miller WH (1970) What does antenna engineering have to do with insect eyes? IEEE Student J 8: 2-8.
10. Bertholf LM (1931a) The distribution of stimulative efficiency in the ultraviolet spectrum for the honeybee. J Agric Res 43: 703-713.
11. Bertholf LM (1931b) Reactions of the honeybee to light. J Agric Res 42: 379-419.
12. Bertholf LM (1932) The extent of the spectrum for Drosophila and the distribution of stimulative efficiency in it. Z Vergl Physiol 18: 32-64.
13. Briscoe AD (2000) Six opsins from the butterfly Papilio glaucus: molecular phylogenetic evidence for paralogous origins of red-sensitive visual pigments in insects. J Mol Evol 51: 110-121.
14. Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46: 471-510.
15. Briscoe AD, Bernard GD, Szeto AS, Nagy LM, White RH (2003) Not all butterfly eyes are created equal: rhodopsin absorption spectra, molecular identification and localization of UV- blue- and green-sensitive rhodopsin encoding mRNA in the retina of Vanessa cardui. J Comp Neurol 458: 334-349.
16. Bruckmoser P (1968) Die spektrale Empfindlichkeit einzelner Sehzellen des Rückenschwimmers Notonecta glauca L. (Heteroptera). Z vergl Physiol 59: 187-204.
17. Eguchi E, Watanabe K, Hariyama T, Yamamoto K (1982) A comparison of electrophysiologically determined spectral responses in 35 species of lepidoptera. J Insect Physiol 28: 675-682.
18. Franceschini N, Kirschfeld K, Minke B (1981) Fluorescence of photoreceptor cells observed in vivo. Science 213: 1264-1267.
19. Friedrich M, Wood EJ, Wu M (2011) Developmental evolution of the insect retina: insights from standardized numbering of homologous photoreceptors. J Exp Zool B 316: 484-499.
20. Frisch KV (1914) Der Farbensinn und Formensinn der Biene. Zool Jb Physiol 37: 1-238.
21. Goldsmith TH (1961) The color vision of insects. In: McElroy WD, Glass B (eds) A symposium on light and life. The Johns Hopkins Press, Baltimore, pp 771-794.
22. Goldsmith TH (1965) Do flies have a red receptor? J Gen Physiol 49: 265-287.
23. Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Vis Neurosci 17: 509-528.
24. Green CH (1985) A comparison of phototactic responses to red and green light in Glossina morsitans morsitans and Musca domestica. Physiol Entomol 10: 165-172.
25. Griffin DR, Hubbard R, Wald G (1947) The sensitivity of the human eye to infra-red radiation. J Opt Soc Am 37: 546-553.
26. Hardie RC (1985) Functional organization of the fly retina. In: Ottoson D (ed) Progress in sensory physiology, vol 5. Springer, Berlin Heidelberg, New York, Toronto, pp 1-79.
27. Henze M, Lind O, Kohler M, Kelber A (2013) Seeing and (not) being seen: sensory ecology of the blue-tailed damselfly Ishnura elegans. In: front physiol conference abstract: International Conference on invertebrate vision, Bäkaskog Castle, Sweden, 2013, p 90. doi: 10. 3389/conf. fphys. 2013. 25. 00068.
28. Hollingsworth JP, Wright RL, Lindquist DA (1964) Spectral response characteristics of the boll weevil. J Econ Entomol 57: 38-41.
29. Horridge G, Barnard P (1965) Movement of palisade in locust retinula cells when illuminated. Q J Microsc Sci 3: 131-136.
30. Hu K, Stark W (1977) Specific receptor input into spectral preference in Drosophila. J Comp Physiol 121: 241-252.
31. Ilse D (1928) Über den Farbensinn der Tagfalter. Z vergl Physiol 8: 658-691.
32. Ilse D (1937) New observations on responses to colours in egg-laying butterflies. Nature 140: 544-545.
33. Kelber A (2006) Invertebrate colour vision. In: Warrant E, Nilsson DE (eds) Invertebrate vision. Cambridge University Press, Cambridge, pp 250-290.
34. Kelber A, Henze Miriam J (2013) Colour vision: parallel pathways intersect in Drosophila. Curr Biol 23: R1043-R1045.
35. Kitamoto J, Sakamoto K, Ozaki K, Mishina Y, Arikawa K (1998) Two visual pigments in a single photoreceptor cell: identification and histological localization of three mRNAs encoding visual pigment opsins in the retina of the butterfly Papilio xuthus. J Exp Biol 201: 1255-1261.
36. Lamb T (1995) Photoreceptor spectral sensitivities: common shape in the long-wavelength region. Vision Res 35: 3083-3091.
37. Langer H, Hamann B, Meinecke CC (1979) Tetrachromatic visual system in the moth Spodoptera exempta (Insecta: Noctuidae). J Comp Physiol A 129: 235-239.
38. Martinez-Harms J, Vorobyev M, Schorn J, Shmida A, Keasar T, Homberg U, Schmeling F, Menzel R (2012) Evidence of red sensitive photoreceptors in Pygopleurus israelitus (Glaphyridae: Coleoptera) and its implications for beetle pollination in the southeast Mediterranean. J Comp Physiol A 198: 451-463.
39. Matic T (1983) Electrical inhibition in the retina of the butterfly Papilio. I. Four spectral types of photoreceptors. J Comp Physiol A 152: 169-182.
40. Matsumoto Y, Wakakuwa M, Yukuhiro F, Arikawa K, Noda H (2014) The attraction to different wavelength light emitting diodes (LEDs), the compound eye structure and opsin genes in Nilaparvata lugens. Jpn J Appl Entomol Zool (in press).
41. Matsushita M, Awata H, Wakakuwa M, Takemura S, Arikawa K (2012) Rhabdom evolution in butterflies: insights from the uniquely tiered and heterogeneous ommatidia of the Glacial Apollo butterfly, Parnassius glacialis. Proc R Soc B 279: 3482-3490.
42. Menzel R (1979) Spectral sensitivity and color vision in invertebrates. In: Autrum H (ed) Invertebrate photoreceptors. Handbook of sensory physiology, vol VII/6A. Springer, Berlin Heidelberg, New York, pp 503-580.
43. Nilsson D-E, Land MF, Howard J (1988) Optics of the butterfly eye. J Comp Physiol A 162: 341-366.
44. Nowel M, Shelton PJ (1981) A Golgi-electron-microscopical study of the structure and development of the lamina ganglionaris of the locust optic lobe. Cell Tissue Res 216: 377-401.
45. Ogawa Y, Kinoshita M, Stavenga DG, Arikawa K (2013) Sex-specific retinal pigmentation results in sexually dimorphic long-wavelength-sensitive photoreceptors in the Eastern Pale Clouded Yellow butterfly, Colias erate. J Exp Biol 216: 1916-1923.
46. Peitsch D, Fietz A, Hertel H, Desouza J, Ventura DF, Menzel R (1992) The spectral input systems of hymenopteran insects and their receptor-based colour vision. J Comp Physiol A 170: 23-40.
47. Reisenman CE, Lazzari C (2006) Spectral sensitivity of the photonegative reaction of the blood-sucking bug Triatoma infestans (Heteroptera: Reduviidae). J Comp Physiol A 192: 39-44.
48. Ribi WA (1978) A unique hymenopteran compound eye. The retina fine structure of the digger wasp Sphex cognatus Smith (Hymenoptera, Sphecidae). Zool Jb Anat Bd 100: 299-342.
49. Schnaitmann C, Garbers C, Wachtler T, Tanimoto H (2013) Color discrimination with broadband photoreceptors. Curr Biol 23: 2375-2382.
50. Schümperli RA (1973) Evidence for colour vision in Drosophila melanogaster through spontaneous phototactic choice behaviour. J Comp Physiol 86: 77-94.
51. Schwind R, Schlecht P, Langer H (1984) Microspectrophotometric characterization and localization of three visual pigments in the compound eye of Notonecta glauca L. (Heteroptera). J Comp Physiol A 116: 183-207.
52. Shimohigashi M, Tominaga Y (1991) Identification of UV, green and red receptors, and their projection to lamina in the cabbage butterfly, Pieris rapae. Cell Tissue Res 263: 49-59.
53. Stavenga DG (2002) Reflections on colourful ommatidia of butterfly eyes. J Exp Biol 205: 1077-1085.
54. Stavenga DG, Arikawa K (2011) Photoreceptor spectral sensitivities of the Small White butterfly Pieris rapae crucivora interpreted with optical modeling. J Comp Physiol A 197: 373-385.
55. Strausfeld NJ, Lee J-K (1991) Neuronal basis for parallel visual processing in the fly. Vis Neurosci 7: 13-33.
56. Swihart SL, Gordon WC (1971) Red photoreceptor in butterflies. Nature 231: 126-127.
57. Takemura S, Kinoshita M, Arikawa K (2005) Photoreceptor projection reveals heterogeneity of lamina cartridges in the visual system of the Japanese yellow swallowtail butterfly, Papilio xuthus. J Comp Neurol 483: 341-350.
58. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4. 0. Mol Biol Evol 24: 1596-1599.
59. Wakakuwa M, Stavenga DG, Kurasawa M, Arikawa K (2004) A unique visual pigment expressed in green, red and deep-red receptors in the eye of the Small White butterfly, Pieris rapae crucivora. J Exp Biol 207: 2803-2810.
60. Wakakuwa M, Kurasawa M, Giurfa M, Arikawa K (2005) Spectral heterogeneity of honeybee ommatidia. Naturwissenschaften 92: 464-467.
61. Williams D (1982) Ommatidial structure in relation to turnover of photoreceptor membrane in the locust. Cell Tissue Res 225: 595-617.
62. Yang EC, Osorio D (1991) Spectral sensitivities of photoreceptors and lamina monopolar cells in the dragonfly, Hemicordulia tau. J Comp Physiol A 169: 663-669.