The Moon cycle exposes nocturnal life to variation in environmental light. However, whether moonlight shapes the fitness of nocturnal species with distinct colour variants remains unknown. Combining data from long-term monitoring, high-resolution global positioning system tracking and experiments using prey, we show that barn owls (Tyto alba) with distinct plumage colourations are differently affected by moonlight. The reddest owls are less successful at hunting and providing food to their offspring during moonlit nights, which associates with lower body mass and lower survival of the youngest nestlings and with female mates starting to lay eggs at low moonlight levels. Although moonlight should make white owls more conspicuous to prey, it either positively affects or does not affect the hunting and fitness of the whitest owls. We experimentally show that, under full-moon conditions, white plumage triggers longer freezing times in prey, which should facilitate prey catchability. We propose that the barn owl’s white plumage, a rare trait among nocturnal predators, exploits the known aversion of rodents to bright light, explaining why, counterintuitively, moonlight has a lesser impact on the whitest owls. Our study provides evidence for the long-suspected influence of the Moon on the evolution of colouration in nocturnal species, highlighting the importance of colour in nocturnal ecosystems.
Subscribe to Journal
Get full journal access for 1 year
only $8.67 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Cuthill, I. C. et al. The biology of color. Science 357, eaan0221 (2017).
Endler, J. A. On the measurement and classification of color in studies of animal color patterns. Biol. J. Linn. Soc. 41, 315–352 (1990).
Endler, J. A. & Mappes, J. The current and future state of animal coloration research. Phil. Trans. R. Soc. Lond. B 372, 20160352 (2017).
Terai, Y. et al. Divergent selection on opsins drives incipient speciation in lake victoria cichlids. PLoS Biol. 4, 2244–2251 (2006).
Seehausen, O. et al. Speciation through sensory drive in cichlid fish. Nature 455, 620–627 (2008).
Tate, G. J., Bishop, J. M. & Amar, A. Differential foraging success across a light level spectrum explains the maintenance and spatial structure of colour morphs in a polymorphic bird. Ecol. Lett. 19, 679–686 (2016).
Gomez, D. & Théry, M. Influence of ambient light on the evolution of colour signals: comparative analysis of a neotropical rainforest bird community. Ecol. Lett. 7, 279–284 (2004).
Avilés, J. M., Pérez‐Contreras, T., Navarro, C. & Soler, J. J. Dark nests and conspicuousness in color patterns of nestlings of altricial birds. Am. Nat. 171, 327–338 (2008).
Penteriani, V., Delgado, M. & del, M. Living in the dark does not mean a blind life: bird and mammal visual communication in dim light. Phil. Trans. R. Soc. B 372, 20160064 (2017).
Kronfeld-Schor, N. et al. Chronobiology by moonlight. Proc. R. Soc. B 280, 20123088 (2013).
Skov, M. W. et al. Marching to a different drummer: crabs synchronize reproduction to a 14-month lunar-tidal cycle. Ecology 86, 1164–1171 (2005).
Grant, R. A., Chadwick, E. A. & Halliday, T. The lunar cycle: a cue for amphibian reproductive phenology? Anim. Behav. 78, 349–357 (2009).
Grau, E., Dickhoff, W., Nishioka, R., Bern, H. & Folmar, L. Lunar phasing of the thyroxine surge preparatory to seaward migration of salmonid fish. Science 211, 607–609 (1981).
Dacke, M., Byrne, M. J., Scholtz, C. H. & Warrant, E. J. Lunar orientation in a beetle. Proc. R. Soc. B 271, 361–365 (2004).
Eads, Da, Jachowski, D. S., Millspaugh, J. J. & Biggins, D. E. Importance of lunar and temporal conditions for spotlight surveys of adult black-footed ferrets. West. N. Am. Nat. 72, 179–190 (2012).
Kotler, B. P., Brown, J., Mukherjee, S., Berger-Tal, O. & Bouskila, A. Moonlight avoidance in gerbils reveals a sophisticated interplay among time allocation, vigilance and state-dependent foraging. Proc. R. Soc. B 277, 1469–1474 (2010).
Watanuki, Y. Moonlight avoidance behavior in leach’ s storm-petrels as a defense against slaty-backed gulls. Auk 103, 14–22 (1986).
Clarke, J. A., Chopko, J. T. & Mackessy, S. P. The effect of moonlight on activity patterns of adult and juvenile prairie rattlesnakes (Crotalus viridis viridis). J. Herpetol. 30, 192–197 (1996).
Cozzi, G. et al. Fear of the dark or dinner by moonlight? reduced temporal partitioning among africa’s large carnivores. Ecology 93, 2590–2599 (2012).
Daly, M., Behrends, P. R., Wilson, M. I. & Jacobs, L. F. Behavioural modulation of predation risk: moonlight avoidance and crepuscular compensation in a nocturnal desert rodent, Dipodomys merriami. Anim. Behav. 44, 1–9 (1992).
Mougeot, F. & Bretagnolle, V. Predation risk and moonlight avoidance in nocturnal seabirds. J. Avian Biol. 31, 376–386 (2000).
Orsdol, K. G. V. Foraging behaviour and hunting success of lions in queen elizabeth national park, uganda. Afr. J. Ecol. 22, 79–99 (1984).
O’Carroll, D. C. & Warrant, E. J. Vision in dim light: highlights and challenges. Phil. Trans. R. Soc. B 372, 20160062 (2017).
Verril, A. E. Nocturnal protective coloration of mammals, birds, fishes, insects, etc. Am. Nat. 31, 99–103 (1897).
Hanlon, R. T. et al. Adaptable night camouflage by cuttlefish. Am. Nat. 169, 543–551 (2007).
Warrant, E. Vision in the dimmest habitats on earth. J. Comp. Physiol. A 190, 765–789 (2004).
Merilaita, S. & Tullberg, B. S. Constrained camouflage facilitates the evolution of conspicuous warning coloration. Evolution 59, 38–45 (2005).
Kelber, A., Yovanovich, C. & Olsson, P. Thresholds and noise limitations of colour vision in dim light. Phil. Trans. R. Soc. B 372, 20160065 (2017).
Parejo, D., Avilés, J. M. & Rodríguez, J. Visual cues and parental favouritism in a nocturnal bird. Biol. Lett. 6, 171–173 (2010).
Warrant, E. J. Visual ecology: hiding in the dark. Curr. Biol. 17, 209–211 (2007).
Penteriani, V., Delgado, MdelM., Alonso-Alvarez, C. & Sergio, F. The importance of visual cues for nocturnal species: eagle owls signal by badge brightness. Behav. Ecol. 18, 143–147 (2007).
Penteriani, V., Delgado, MdelM., Campioni, L. & Lourenço, R. Moonlight makes owls more chatty. PLoS ONE 5, e8696 (2010).
Passarotto, A., Parejo, D., Penteriani, V. & Avilés, J. M. Colour polymorphism in owls is linked to light variability. Oecologia 187, 61–73 (2018).
Roulin, A. & Jensen, H. Sex-linked inheritance, genetic correlations and sexual dimorphism in three melanin-based color traits in the barn owl. J. Evol. Biol. 28, 655–666 (2015).
San-Jose, L. M., Ducret, V., Ducrest, A. L., Simon, C. & Roulin, A. Beyond mean allelic effects: a locus at the major color gene MC1R associates also with differing levels of phenotypic and genetic (co)variance for coloration in barn owls. Evolution 71, 2469–2483 (2017).
Antoniazza, S., Burri, R., Fumagalli, L., Goudet, J. & Roulin, A. Local adaptation maintains clinal variation in melanin-based coloration of european barn owls (Tyto alba). Evolution 64, 1944–1954 (2010).
Antoniazza, S. et al. Natural selection in a post-glacial range expansion: the case of the colour cline in the European barn owl. Mol. Ecol. 23, 5508–5523 (2014).
Roulin, A. Covariation between plumage colour polymorphism and diet in the barn owl Tyto alba. Ibis 146, 509–517 (2004).
Charter, M., Peleg, O., Leshem, Y. & Roulin, A. Similar patterns of local barn owl adaptation in the middle east and europe with respect to melanic coloration. Biol. J. Linn. Soc. 106, 447–454 (2012).
Kelber, A. & Roth, L. S. Nocturnal colour vision - not as rare as we might think. J. Exp. Biol. 209, 781–788 (2006).
Osorio, D. & Vorobyev, M. Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and colour vision. Proc. R. Soc. B 272, 1745–1752 (2005).
Jacobs, G. H. Evolution of colour vision in mammals. Phil. Trans. R. Soc. B 364, 2957–2967 (2009).
Eilam, D. Die hard: a blend of freezing and fleeing as a dynamic defense—implications for the control of defensive behavior. Neurosci. Biobehav. Rev. 29, 1181–1191 (2005).
Ilany, A. & Eilam, D. Wait before running for your life: defensive tactics of spiny mice (Acomys cahirinus) in evading barn owl (Tyto alba) attack. Behav. Ecol. Sociobiol. 62, 923–933 (2008).
Durant, J. M., Gendner, J.-P. & Handrich, Y. Behavioural and body mass changes before egg laying in the barn owl: cues for clutch size determination? J. Ornithol. 151, 11–17 (2010).
Roulin, A. Effects of hatching asynchrony on sibling negotiation, begging, jostling for position and within-brood food allocation in the barn owl, Tyto alba. Evol. Ecol. Res. 6, 1083–1098 (2004).
Navarro-Castilla, Á. & Barja, I. Does predation risk, through moon phase and predator cues, modulate food intake, antipredatory and physiological responses in wood mice (Apodemus sylvaticus)? Behav. Ecol. Sociobiol. 68, 1505–1512 (2014).
Schmidt, K. A., Manson, R. & Lewis, D. Voles competing with mice: differentiating exploitative, interference and apparent competition using patch use theory. Evol. Ecol. Res. 7, 273–286 (2005).
Halle, S. Effect of extrinsic factors on activity of root voles, Microtus oeconomus. J. Mammal. 76, 88–99 (1995).
Barker, D. et al. Brief light as a practical aversive stimulus for the albino rat. Behav. Brain Res. 214, 402–408 (2010).
Lockard, R. B. Some effects of light upon the behavior of rodents. Psychol. Bull. 60, 509–529 (1963).
Bourin, M., Petit-Demoulière, B., Nic Dhonnchadha, B. & Hascöet, M. Animal models of anxiety in mice. Fundam. Clin. Pharmacol. 21, 567–574 (2007).
Trullas, R. & Skolnick, P. Differences in fear motivated behaviors among inbred mouse strains. Psychopharmacology 111, 323–331 (1993).
Campbell, B. A. & Messing, R. B. Aversion thresholds and aversion difference limens for white light in albino and hooded rats. J. Exp. Psychol. 82, 353–359 (1969).
Sousa, N., Almeida, O. F. X. & Wotjak, C. T. A hitchhiker’s guide to behavioral analysis in laboratory rodents. Genes Brain Behav. 5, 5–24 (2006).
Ryan, M. Sexual selection, receiver biases, and the evolution of sex differences. Science 281, 1999–2003 (1998).
Ducret, V., Gaigher, A., Simon, C., Goudet, J. & Roulin, A. Sex-specific allelic transmission bias suggests sexual conflict at MC1R. Mol. Ecol. 41, 4551–4563 (2016).
Roulin, A., Altwegg, R., Jensen, H., Steinsland, I. & Schaub, M. Sex-dependent selection on an autosomal melanic female ornament promotes the evolution of sex ratio bias. Ecol. Lett. 13, 616–626 (2010).
Romano, A., Séchaud, R., Hirzel, A. H. & Roulin, A. Climate-driven convergent evolution of plumage colour in a cosmopolitan bird. Glob. Ecol. Biogeogr. 28, 496–507 (2019).
San-Jose, L. M. et al. Effect of the MC1R gene on sexual dimorphism in melanin-based colorations. Mol. Ecol. 24, 2794–2808 (2015).
Dreiss, A. & Roulin, A. Age‐related change in melanin‐based coloration of barn owls (Tyto alba): females that become more female‐like and males that become more male‐like perform better. Biol. J. Linn. Soc. 101, 689–704 (2010).
Altwegg, R., Schaub, M. & Roulin, A. Age-specific fitness components and their temporal variation in the barn owl. Am. Nat. 169, 47–61 (2007).
Tate, G., Sumasgutner, P., Koeslag, A. & Amar, A. Pair complementarity influences reproductive output in the polymorphic black sparrowhawk Accipiter melanoleucus. J. Avian Biol. 48, 387–398 (2017).
Brommer, J. E., Karell, P., Aaltonen, E., Ahola, K. & Karstinen, T. Dissecting direct and indirect parental effects on reproduction in a wild bird of prey: dad affects when but not how much. Behav. Ecol. Sociobiol. 69, 293–302 (2015).
Galeotti, P., Rubolini, D., Dunn, P. O. & Fasola, M. Colour polymorphism in birds: causes and functions. J. Evol. Biol. 16, 635–646 (2003).
Orlowski, J., Harmening, W. & Wagner, H. Night vision in barn owls: visual acuity and contrast sensitivity under dark adaptation. J. Vis. 12, 1–8 (2012).
Roulin, A. & Dijkstra, C. Female- and male-specific signals of quality in the barn owl. J. Evol. Biol. 14, 255–266 (2001).
Garriga, J., Palmer, J. R. B., Oltra, A. & Bartumeus, F. Expectation-maximization binary clustering for behavioural annotation. PLoS ONE 11, e0151984 (2016).
Chakraborti, S. Verification of the Rayleigh scattering cross section. Am. J. Phys. 75, 824–826 (2007).
Aubé, M., Roby, J. & Kocifaj, M. Evaluating potential spectral impacts of various artificial lights on melatonin suppression, photosynthesis, and star visibility. PLoS ONE 8, e67798 (2013).
Foster, R. G. & Roenneberg, T. Human responses to the geophysical daily, annual and lunar cycles. Curr. Biol. 18, 784–794 (2008).
Bates, D., Mächler, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed-effects models using lme4. Preprint at https://arxiv.org/abs/1406.5823 (2014).
Béziers, P., Ducrest, A.-L., Simon, C. & Roulin, A. Circulating testosterone and feather-gene expression of receptors and metabolic enzymes in relation to melanin-based colouration in the barn owl. Gen. Comp. Endocrinol. 250, 36–45 (2017).
Roulin, A. Linkage disequilibrium between a melanin-based colour polymorphism and tail length in the barn owl. Biol. J. Linn. Soc. 88, 475–488 (2006).
Almasi, B. & Roulin, A. Signalling value of maternal and paternal melanism in the barn owl: implication for the resolution of the lek paradox. Biol. J. Linn. Soc. 115, 376–390 (2015).
Béziers, P. & Roulin, A. Double brooding and offspring desertion in the barn owl Tyto alba. J. Avian Biol. 47, 235–244 (2016).
Quinn, G. P. & Keough, M. J. Experimental Design and Data Analysis for Biologists (Cambridge Univ. Press, 2002).
Grueber, C. E., Nakagawa, S., Laws, R. J. & Jamieson, I. G. Multimodel inference in ecology and evolution: challenges and solutions. J. Evol. Biol. 24, 699–711 (2011).
We thank P. Ducouret for setting the video system to record the voles’ behaviour, J. Buser for his guidance and help in housing the voles in the animal facilities, I. H. Dufresnes for her help with the long-term barn owl database and for providing the picture in Fig. 1, P. Guillemin for helping prepare the data on adult food provisioning, P. Christe for giving us access to the Longworth live traps, K. Safi for helping us with the analysis of the GPS data and the people that have been involved in monitoring our barn-owl population over the last 20 years. We thank L. Keller, B. Milá and J. Delhaye for providing comments on early versions of the manuscript. We acknowledge funding from the Swiss National Science Foundation, ref. 173178, to A.R.
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
San-Jose, L.M., Séchaud, R., Schalcher, K. et al. Differential fitness effects of moonlight on plumage colour morphs in barn owls. Nat Ecol Evol 3, 1331–1340 (2019). https://doi.org/10.1038/s41559-019-0967-2
Nature Ecology & Evolution (2020)
Nature Ecology & Evolution (2020)
Gray plumage color is more cryptic than brown in snowy landscapes in a resident color polymorphic bird
Ecology and Evolution (2020)
Nature Ecology & Evolution (2019)