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INTRODUCTION
Recent discoveries of functional color vision at low light levels among
nocturnal geckos, tree frogs, bees and hawkmoths (Kelber et al., 2002;
Roth and Kelber, 2004; Somanathan et al., 2008; Gomez et al., 2010)
have prompted a re-evaluation of the importance of color vision for
nocturnal animals. Traditionally, the low light intensities available in
nocturnal environments were believed to preclude color discrimination
(Walls, 1942; Ahnelt and Kolb, 2000). Recent studies, however,
suggest that nocturnal color vision may be both selectively
advantageous for some species and more widespread than previously
believed (Kelber and Roth, 2006; Gomez et al., 2009; Müller et al.,
2009). Color discrimination at nocturnal light levels may even be
adaptive for some mammals. Studies of opsin genes in nocturnal
primates and bats, for example, have revealed evidence of selection
acting to maintain functional dichromacy in several lineages, possibly
for nocturnal color discrimination (Kawamura and Kubotera, 2004;
Perry et al., 2007; Zhao et al., 2009a; Zhao et al., 2009b). Further,
recent work suggests that cone thresholds in some nocturnal mammals
may extend down to dim moonlight or starlight levels (Umino et al.,
2008). Because the appearance of visual targets (such as conspecifics,
food or predators) depends upon the spectral quality of ambient light
as well as the target’s reflective properties (Endler, 1990; Endler,
1993), an understanding of the light environments available to
nocturnal animals may be instrumental in studying nocturnal color
vision (Johnsen et al., 2006).
Endler’s (Endler, 1993) seminal work ‘The color of light in forests
and its implications’ offered a detailed study of variation in diurnal
light environments, forming the basis for most subsequent work on
diurnal visual ecology. In contrast, variation in nocturnal light
environments has not been as extensively studied. By ‘nocturnal
light environments’, we are referring strictly to the nocturnal period
after the conclusion of twilight [for twilight environments, see Munz
and McFarland among others (Munz and McFarland, 1973; Munz
and McFarland, 1977; Martin, 1990; Endler, 1991; Endler, 1993;
Lee and Hernández-Andrés, 2003; Johnsen et al., 2006; Sweeney
et al. 2011)]. Much of the published research on nocturnal light
environments has focused on variation in light intensity. These
studies reveal that light intensity at night can vary dramatically,
differing by as much as eight orders of magnitude due to lunar phase,
lunar altitude (height of the moon in the sky), weather, foliage
density, seasonality and latitude (United States Navy, 1952; Lythgoe,
1979; Pariente, 1980; Martin, 1990; Cummings et al., 2008; Warrant,
2008; Johnsen, 2012).
However, few data are currently available on spectral variation
in light environments at night. Munz and McFarland (Munz and
McFarland, 1973; Munz and McFarland, 1977) and Lythgoe
(Lythgoe, 1972; Lythgoe, 1979) identified spectral differences
between moonlight and starlight. Although the spectral quality of
moonlight resembles sunlight, starlight is ‘red-shifted’, with
maximum irradiance displaced to longer wavelengths (Lythgoe,
SUMMARY
Although variation in the color of light in terrestrial diurnal and twilight environments has been well documented, relatively little
work has examined the color of light in nocturnal habitats. Understanding the range and sources of variation in nocturnal light
environments has important implications for nocturnal vision, particularly following recent discoveries of nocturnal color vision.
In this study, we measured nocturnal irradiance in a dry forest/woodland and a rainforest in Madagascar over 34 nights. We found
that a simple linear model including the additive effects of lunar altitude, lunar phase and canopy openness successfully
predicted total irradiance flux measurements across 242 clear sky measurements (r0.85, P<0.0001). However, the relationship
between these variables and spectral irradiance was more complex, as interactions between lunar altitude, lunar phase and
canopy openness were also important predictors of spectral variation. Further, in contrast to diurnal conditions, nocturnal forests
and woodlands share a yellow-green-dominant light environment with peak flux at 560 nm. To explore how nocturnal light
environments influence nocturnal vision, we compared photoreceptor spectral tuning, habitat preference and diet in 32 nocturnal
mammals. In many species, long-wavelength-sensitive cone spectral sensitivity matched the peak flux present in nocturnal
forests and woodlands, suggesting a possible adaptation to maximize photon absorption at night. Further, controlling for
phylogeny, we found that fruit/flower consumption significantly predicted short-wavelength-sensitive cone spectral tuning in
nocturnal mammals (P0.002). These results suggest that variation in nocturnal light environments and species ecology together
influence cone spectral tuning and color vision in nocturnal mammals.
Supplementary material available online at http://jeb.biologists.org/cgi/content/full/215/23/4085/DC1
Key words: visual ecology, lunar irradiance, photoreceptor spectral tuning, rainforest, dry forest.
Received 16 February 2012; Accepted 30 July 2012
The Journal of Experimental Biology 215, 4085-4096
© 2012. Published by The Company of Biologists Ltd
doi:10.1242/jeb.071415
RESEARCH ARTICLE
Nocturnal light environments and species ecology: implications for nocturnal color
vision in forests
Carrie C. Veilleux
1,
* and Molly E. Cummings
2
1
Department of Anthropology and
2
Section of Integrative Biology, University of Texas at Austin, Austin, TX 78712, USA
*Author for correspondence (carrie.veilleux@utexas.edu)
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