Nocturnal light environments and species ecology: Implications for nocturnal color vision in forests

Journal of Experimental Biology

Volumn 215, Issue 23, 2012, Pages 4085-4096

  Veilleux, Carrie C ^a   Cummings, Molly E ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Dry forest; Lunar irradiance; Photoreceptor spectral tuning; Rainforest; Visual ecology

Indexed keywords

VISUAL PIGMENT;

ANIMAL; ARTICLE; BIRD; COLOR VISION; DIET; ECOSYSTEM; ILLUMINATION; LIZARD; MADAGASCAR; MAMMAL; PHOTOPERIODICITY; PHOTORECEPTOR CELL; PHYSIOLOGY; SEASON; SPECIES DIFFERENCE; STATISTICAL MODEL;

ANIMALS; BIRDS; COLOR VISION; DIET; ECOSYSTEM; LIGHTING; LINEAR MODELS; LIZARDS; MADAGASCAR; MAMMALS; PHOTOPERIOD; PHOTORECEPTOR CELLS, VERTEBRATE; RETINAL PIGMENTS; SEASONS; SPECIES SPECIFICITY;

MAMMALIA;

EID: 84869148737     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.071415     Document Type: Article

References (88)

1. Ahnelt, P. K. and Kolb, H. (2000). The mammalian photoreceptor mosaic-adaptive design. Prog. Retin. Eye Res. 19, 711-777.
2. Balko, E. A. and Underwood, H. B. (2005). Effects of forest structure and composition on food availability for Varecia variegata at Ranomafana National Park, Madagascar. Am. J. Primatol. 66, 45-70.
3. Barlow, H. B., Levick, W. R. and Yoon, M. (1971). Responses to single quanta of light in retinal ganglion cells of the cat. Vision Res. 11 Suppl. 3, 87-101.
4. Bates, D., Maechler, M. and Bolker, B. (2012). lme4: Linear mixed-effects models using S4 classes. R package version 0. 999375-37. http://cran. r-project.org/web/packages/lme4
5. Bidlingmayer, W. L. (1964). The effect of moonlight on the flight activity of mosquitoes. Ecology 45, 87-94.
6. Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L. and Purvis, A. (2007). The delayed rise of present-day mammals. Nature 446, 507-512.
7. Bowmaker, J. K., Govardovskii, V. I., Shukolyukov, S. A., Zueva, L. V., Hunt, D. M., Sideleva, V. G. and Smirnova, O. G. (1994). Visual pigments and the photic environment: the cottoid fish of Lake Baikal. Vision Res. 34, 591-605.
8. Burgess, N. D., D'Amico Hales, J., Underwood, E. C., Dinerstein, E., Olson, D., Itoua, I., Schipper, J., Rickets, T. H. and Newman, K. (2004). Terrestrial Ecoregions of Africa and Madagascar: A Conservation Assessment. Washington, DC: Island Press.
9. Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference, 2nd edn. New York: Springer.
10. Burnham, K. P. and Anderson, D. R. (2004). Multimodel inference: understanding AIC and BIC in model selection. Sociol. Methods Res. 33, 261-304.
11. Burnham, K. P., Anderson, D. R. and Huyvaert, K. P. (2011). AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav. Ecol. Sociobiol. 65, 23-35.
12. Chiao, C. C., Vorobyev, M., Cronin, T. W. and Osorio, D. (2000). Spectral tuning of dichromats to natural scenes. Vision Res. 40, 3257-3271.
13. Condit, H. R. and Grum, F. (1964). Spectral energy distribution of daylight. J. Opt. Soc. Am. 54, 937-940.
14. Cowing, J. A., Arrese, C. A., Davies, W. L., Beazley, L. D. and Hunt, D. M. (2008). Cone visual pigments in two marsupial species: the fat-tailed dunnart (Sminthopsis crassicaudata) and the honey possum (Tarsipes rostratus). Proc. R. Soc. B 275, 1491-1499.
15. Cummings, M. E. (2004). Modelling divergence in luminance and chromatic detection performance across measured divergence in surfperch (Embiotocidae) habitats. Vision Res. 44, 1127-1145.
16. Cummings, M. E. (2007). Sensory trade-offs predict signal divergence in surfperch. Evolution 61, 530-545.
17. Cummings, M. E. and Partridge, J. C. (2001). Visual pigments and optical habitats of surfperch (Embiotocidae) in the California kelp forest. J. Comp. Physiol. A 187, 875-889.
18. Cummings, M. E., Bernal, X. E., Reynaga, R., Rand, A. S. and Ryan, M. J. (2008). Visual sensitivity to a conspicuous male cue varies by reproductive state in Physalaemus pustulosus females. J. Exp. Biol. 211, 1203-1210.
19. Endler, J. A. (1990). On the measurement and classification of color in studies of animal color patterns. Biol. J. Linn. Soc. Lond. 41, 315-352.
20. Endler, J. A. (1991). Variation in the appearance of guppy color patterns to guppies and their predators under different visual conditions. Vision Res. 31, 587-608.
21. Endler, J. A. (1993). The color of light in forests and its implications. Ecol. Monogr. 63, 1-27.
22. Endler, J. A. and Théry, M. (1996). Interacting effects of lek placement, display behaviour, ambient light, and color patterns in three Neotropical forest-dwelling birds. Am. Nat. 148, 421-452.
23. Fietz, J. and Ganzhorn, J. U. (1999). Feeding ecology of the hibernating primate Cheirogaleus medius: how does it get so fat? Oecologia 121, 157-164.
24. Fleishman, L. J., Bowman, M., Saunders, D., Miller, W. E., Rury, M. J. and Loew, E. R. (1997). The visual ecology of Puerto Rican anoline lizards: habitat light and spectral sensitivity. J. Comp. Physiol. A 181, 446-460.
25. Frazer, G. W., Canham, C. D. and Lertzman, K. P. (1999). Gap Light Analyzer (GLA), Version 2.0: Imaging software to extract canopy structure and gap light transmission indices from true-color fisheye photographs, users manual and program documentation. Simon Fraser University, Burnaby, BC, and the Institute of Ecosystem Studies, Millbrook, NY.
26. Garland, T., Jr and Ives, A. R. (2000). Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am. Nat. 155, 346-364.
27. Gomez, D., Richardson, C., Lengagne, T., Plenet, S., Joly, P., Léna, J.-P. and Théry, M. (2009). The role of nocturnal vision in mate choice: females prefer conspicuous males in the European tree frog (Hyla arborea). Proc. R. Soc. B 276, 2351-2358.
28. Gomez, D., Richardson, C., Lengagne, T., Derex, M., Plenet, S., Joly, P., Léna, J.-P. and Théry, M. (2010). Support for a role of colour vision in mate choice in the nocturnal European treefrog (Hyla arborea). Behaviour 147, 1753-1768.
29. Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E. and Challenger, W. (2008). GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129-131.
30. Hunt, D. M., Carvalho, L. S., Cowing, J. A. and Davies, W. L. (2009). Evolution and spectral tuning of visual pigments in birds and mammals. Philos. Trans R. Soc. Lond. B 364, 2941-2955.
31. Jacobs, G. H. (2009). Evolution of colour vision in mammals. Philos. Trans. R. Soc. Lond. B 364, 2957-2967.
32. Jacobs, G. H. and Rowe, M. P. (2004). Evolution of vertebrate colour vision. Clin. Exp. Optom. 87, 206-216.
33. Johnsen, S. (2012). The Optics of Life: A Biologist's Guide to Light in Nature. Princeton, NJ: Princeton University Press.
34. Johnsen, S., Kelber, A., Warrant, E., Sweeney, A. M., Widder, E. A., Lee, R. L., Jr and Hernández-Andrés, J. (2006). Crepuscular and nocturnal illumination and its effects on color perception by the nocturnal hawkmoth Deilephila elpenor. J. Exp. Biol. 209, 789-800.
35. Kamilar, J. M., Muldoon, K. M., Lehman, S. M. and Herrera, J. P. (2012). Testing Bergmann's rule and the resource seasonality hypothesis in Malagasy primates using GIS-based climate data. Am. J. Phys. Anthropol. 147, 401-408.
36. Kawamura, S. and Kubotera, N. (2004). Ancestral loss of short wave-sensitive cone visual pigment in lorisiform prosimians, contrasting with its strict conservation in other prosimians. J. Mol. Evol. 58, 314-321.
37. Kelber, A. and Lind, O. (2010). Limits of colour vision in dim light. Ophthalmic Physiol. Opt. 30, 454-459.
38. Kelber, A. and Osorio, D. (2010). From spectral information to animal color vision: experiments and concepts. Proc. R. Soc. B 277, 1617-1625.
39. Kelber, A. and Roth, L. S. V. (2006). Nocturnal colour vision - not as rare as we might think. J. Exp. Biol. 209, 781-788.
40. Kelber, A., Balkenius, A. and Warrant, E. J. (2002). Scotopic colour vision in nocturnal hawkmoths. Nature 419, 922-925.
41. Kelber, A., Balkenius, A. and Warrant, E. J. (2003). Colour vision in diurnal and nocturnal hawkmoths. Integr. Comp. Biol. 43, 571-579.
42. Kieffer, H. H. and Stone, T. C. (2005). The spectral irradiance of the moon. Astron. J. 129, 2887-2901.
43. Lane, A. P. and Irvine, W. M. (1973). Monochromatic phase curves and albedos for the lunar disk. Astron. J. 78, 267-277.
44. Leal, M. and Fleishman, L. J. (2002). Evidence for habitat partitioning based on adaptation to environmental light in a pair of sympatric lizard species. Proc. R. Soc. Lond. B 269, 351-359.
45. Lee, R. L., Jr and Hernández-Andrés, J. (2003). Measuring and modeling twilight's purple light. Appl. Opt. 42, 445-457.
46. Levine, J. S. and MacNichol, E. F., Jr (1979). Visual pigments in teleost fishes: effects of habitat, microhabitat, and behavior on visual system evolution. Sens. Processes 3, 95-131.
47. Lewis, R. J. and Bannar-Martin, K. H. (2012). The impact of cyclone Fanele on a tropical dry forest in Madagascar. Biotropica 44, 135-140.
48. Lillywhite, P. G. (1977). Single photon signals and transduction in an insect eye. J. Comp. Physiol. A 122, 189-200.
49. Lukáts, A., Dkhissi-Benyahya, O., Szepessy, Z., Röhlich, P., Vígh, B., Bennett, N. C., Cooper, H. M. and Szél, A. (2002). Visual pigment coexpression in all cones of two rodents, the Siberian hamster, and the pouched mouse. Invest. Ophthalmol. Vis. Sci. 43, 2468-2473.
50. Lythgoe, J. N. (1972). The adaptation of visual pigments to the photic environment. In Handbook of Sensory Physiology Vol. VII/1: Photochemistry of Vision (ed. H. J. A. Dartnall), pp. 566-603. New York: Springer-Verlag.
51. Lythgoe, J. N. (1979). The Ecology of Vision. Oxford: Clarendon Press.
52. Lythgoe, J. N. (1984). Visual pigments and environmental light. Vision Res. 24, 1539-1550.
53. Martin, G. (1990). Birds By Night. London: Poyser.
54. McFarland, W. N. and Munz, F. W. (1975). Part III: The evolution of photopic visual pigments in fishes. Vision Res. 15, 1071-1080.
55. Melin, A. D., Moritze, G. L., Fosbury, R. A. E., Kawamura, S. and Dominy, N. J. (2012). Why aye-ayes see blue. Am. J. Primatol. 74, 185-192.
56. Miller, S. D. and Turner, R. E. (2009). A dynamic lunar spectral irradiance data set for NPOESS/VIIRS day/night band nighttime environmental applications. IEEE Trans. Geosci. Remote Sens. 47, 2316-2329.
57. Mollon, J. D. (1989). "Tho-she kneel-d in that place where they grew..." The uses and origins of primate colour vision. J. Exp. Biol. 146, 21-38.
58. Müller, B., Glösmann, M., Peichl, L., Knop, G. C., Hagemann, C. and Ammermüller, J. (2009). Bat eyes have ultraviolet-sensitive cone photoreceptors. PLoS ONE 4, e6390.
59. Munz, F. W. and McFarland, W. N. (1973). The significance of spectral position in the rhodopsins of tropical marine fishes. Vision Res. 13, 1829-1874.
60. Munz, F. W. and McFarland, W. N. (1977). Evolutionary adaptations of fishes to the photic environment. In The Visual System of Vertebrates (ed. F. Crescitelli), pp. 194-274. New York: Springer-Verlag.
61. Orme, D., Freckleton, R., Thomas, G., Petzoldt, T., Fritz, S. and Isaac, N. (2010). caper: comparative analyses of phylogenetics and evolution in R. R package version 0.4/r71.
62. Osorio, D. and Vorobyev, M. (2005). Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and colour vision. Proc. R. Soc. B 272, 1745-1752.
63. Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature 401, 877-884.
64. Paradis, E., Claude, J. and Strimmer, K. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290.
65. Pariente, G. F. (1980). Quantitative and qualitative study of the light available in the natural biotope of Malagasy prosimians. In Nocturnal Malagasy Primates: Ecology, Physiology, and Behaviour (ed. P. Charles-Dominique, H. M. Cooper, A. Hladik, C. M. Hladik, G. F. Pariente, A. Petter-Rousseaux and A. Schilling), pp. 117-134. New York: Academic Press.
66. Partridge, J. C. and Cummings, M. E. (1999). Adaptation of visual pigments to the aquatic environment. In Adaptive Mechanisms in the Ecology of Vision (ed. S. N. Archer, M. B. A. Djamgoz, E. R. Loew, J. C. Partridge and S. Vallerga), pp. 251-283. Boston, MA: Kluwer Academic Publishers.
67. Perry, G. H., Martin, R. D. and Verrelli, B. C. (2007). Signatures of functional constraint at aye-aye opsin genes: the potential of adaptive color vision in a nocturnal primate. Mol. Biol. Evol. 24, 1963-1970.
68. R Development Core Team (2011). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, Vienna, Austria.
69. Roth, L. S. V., Balkenius, A. and Kelber, A. (2008). The absolute threshold of colour vision in the horse. PLoS One 3, e3711.
70. Roth, L. S. V. and Kelber, A. (2004). Nocturnal colour vision in geckos. Proc. R. Soc. Lond. B 271 Suppl. 6, S485-S487.
71. Shaw, J. A. (2005). The digital blue sky at night. Opt. Photonics News 16, 18-23.
72. Somanathan, H., Borges, R. M., Warrant, E. J. and Kelber, A. (2008). Nocturnal bees learn landmark colours in starlight. Curr. Biol. 18, R996-R997.
73. Sorg, J.-P. and Rohner, U. (1996). Climate and tree phenology of the dry deciduous forest of the Kirindy Forest. Primate Report 46-1, 57-80.
74. Sumner, P. and Mollon, J. D. (2000). Catarrhine photopigments are optimized for detecting targets against a foliage background. J. Exp. Biol. 203, 1963-1986.
75. Sweeney, A. M., Boch, C. A., Johnsen, S. and Morse, D. E. (2011). Twilight spectral dynamics and the coral reef invertebrate spawning response. J. Exp. Biol. 214, 770-777.
76. Symonds, M. R. E. and Moussalli, A. (2011). A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion. Behav. Ecol. Sociobiol. 65, 13-21.
77. Théry, M. (2001). Forest light and its influence on habitat selection. Plant Ecol. 153, 251-261.
78. Umino, Y., Solessio, E. and Barlow, R. B. (2008). Speed, spatial, and temporal tuning of rod and cone vision in mouse. J. Neurosci. 28, 189-198.
79. United States Naval Observatory (2011). Complete sun and moon data for one day. Astronomical Applications Department, United States Navy. http://aa.usno. navy.mil/data/docs/RS-OneDay.php
80. United States Navy (1952). Natural illumination charts. United States Navy Research and Development Project NS 714-100. Report No. 374-1 (September). Washington, DC: Dept. of the Navy, Bureau of Ships.
81. Walls, G. L. (1942). The Vertebrate Eye and Its Adaptive Radiation. Bloomfield Hills, MI: The Cranbrook Press.
82. Wang, D., Oakley, T., Mower, J., Shimmin, L. C., Yim, S., Honeycutt, R. L., Tsao, H. and Li, W.-H. (2004). Molecular evolution of bat color vision genes. Mol. Biol. Evol. 21, 295-302.
83. Warrant, E. J. (2004). Vision in the dimmest habitats on earth. J. Comp. Physiol. A 190, 765-789.
84. Warrant, E. J. (2008). Nocturnal vision. In The Senses: A Comprehensive Reference Vol. 2: Vision II (ed. T. Albright and R. H. Masland), pp. 53-86. Oxford: Academic Press.
85. Wright, P. C. (1992). Primate ecology, rainforest conservation, and economic development: building a national park in Madagascar. Evol. Anthropol. 1, 25-33.
86. Young, R. E. and Mencher, F. M. (1980). Bioluminescence in mesopelagic squid: diel color change during counterillumination. Science 208, 1286-1288.
87. Zhao, H., Rossiter, S. J., Teeling, E. C., Li, C., Cotton, J. A. and Zhang, S. (2009a). The evolution of color vision in nocturnal mammals. Proc. Natl. Acad. Sci. USA 106, 8980-8985.
88. Zhao, H., Xu, D., Zhou, Y., Flanders, J. and Zhang, S. (2009b). Evolution of opsin genes reveals a functional role of vision in the echolocating little brown bat (Myotis lucifugus). Biochem. Syst. Ecol. 37, 154-161.