Artificial light at night desynchronizes strictly seasonal reproduction in a wild mammal

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1816, 2015, Pages

  Robert, Kylie A ^a   Lesku, John A ^a   Partecke, Jesko ^b,c   Chambers, Brian ^d  

^a LA TROBE UNIVERSITY   (Australia)

^b MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^c UNIVERSITY OF KONSTANZ   (Germany)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Anthropogenic disturbance; Circadian disruption; Light pollution; Macropus eugenii; Melatonin; Trophic mismatch

Indexed keywords

ANTHROPOGENIC SOURCE; BREEDING POPULATION; ENVIRONMENTAL CONDITIONS; LIGHT POLLUTION; MARSUPIAL; REPRODUCTION; SEASONAL VARIATION; WILD POPULATION;

ANIMALIA; MACROPUS EUGENII; MAMMALIA; METATHERIA;

MELATONIN;

ADVERSE EFFECTS; ANIMAL; CITY; KANGAROO; LIGHT; PHYSIOLOGY; RADIATION RESPONSE; REPRODUCTION; WESTERN AUSTRALIA;

ANIMALS; CITIES; LIGHT; MACROPODIDAE; MELATONIN; REPRODUCTION; WESTERN AUSTRALIA;

EID: 84943147771     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2015.1745     Document Type: Article

References (57)

1. Hölker F, Wolter C, Perkin EK, Tockner K. 2010 Light pollution as a biodiversity threat. Trends Ecol. Evol. 25, 681-682. (doi:10.1016/j.tree.2010.09.007)
2. Downs NC, Beaton V, Guest J, Polanski J, Robinson SL, Racey PA. 2003 The effects of illuminating the roost entrance on the emergence behaviour of Pipistrellus pygmaeus. Biol. Conserv. 111, 247-252. (doi:10.1016/S0006-3207(02)00298-7)
3. Stone E, Jones G, Harris S. 2009 Street lighting disturbs commuting bats. Curr. Biol. 19, 1123-1127. (doi:10.1016/j.cub.2009.05.058)
4. Bird BL, Branch LC, Miller DL. 2004 Effects of coastal lighting on foraging behaviour on beach mice. Conserv. Biol. 18, 1435-1439. (doi:10.1111/j.1523-1739.2004.00349.x)
5. Krams I. 2001 Communication in crested tits and the risk of predation. Anim. Behav. 61, 1065-1068. (doi:10.1006/anbe.2001.1702)
6. Miller MW. 2006 Apparent effects of light pollution on singing behavior of American robins. Condor 108, 130-139. (doi:10.1650/0010-5422(2006)108[0130:AEOLPO]2.0.CO;2)
7. Longcore T. 2010 Sensory ecology: night lights alter reproductive behavior of blue tits. Curr. Biol. 20, 893-895. (doi:10.1016/j.cub.2010.09.011)
8. Kempenaers B, Borgström P, Loës P, Schlicht E, Valcu M. 2010 Artificial night lighting affects dawn song, extra-pair siring success, and lay date in songbirds. Curr. Biol. 20, 1735-1739. (doi:10.1016/j.cub.2010.08.028)
9. Dominoni D, Quetting M, Partecke J. 2013 Artificial light at night advances avian reproductive physiology. Proc. R. Soc. B 280, 20123017. (doi:10.1098/rspb.2012.3017)
10. LeTallec T, Théry M, Perret M. 2015 Effects of light pollution on seasonal estrus and daily rhythms in a nocturnal primate. J. Mammal. 96, 438-445. (doi:10.1093/jmammal/gyv047)
11. Bedrosian TA, Fonken LK, Walton JC, Nelson RJ. 2011 Chronic exposure to dim light at night suppresses immune responses in Siberian hamsters. Biol. Lett. 7, 468-471. (doi:10.1098/rsbl.2010.1108)
12. Bedrosian TA, Aubrecht TG, Kaugars KE, Weil ZM, Nelson RJ. 2013 Artificial light at night alters delayedtype hypersensitivity reaction in response to acute stress in Siberian hamsters. Brain Behav. Immunol. 34, 39-42. (doi:10.1016/j.bbi.2013.05.009)
13. Fonken LF, Kitsmiller E, Smale L, Nelson RJ. 2012 Dim nighttime light impairs cognition and provokes depressive-like responses in a diurnal rodent. J. Biol. Rhythms 27, 319-327. (doi:10.1177/0748730412448324)
14. Beier P. 2006 Effects of artificial night lighting on terrestrial mammals. In Ecological consequences of artificial night lighting (eds C Rich, T Longcore), pp. 19-42. Washington, DC: Island Press.
15. Dibner C, Schibler U, Albrecht U. 2010 The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 72, 517-549. (doi:10.1146/annurev-physiol-021909-135821)
16. Prendergast BJ, Nelson RJ, Zucker I. 2002 Mammalian seasonal rhythms: behavior and neuroendocrine substrates. In Hormones, brain and behavior (eds DW Pfaff, A Arnold, A Etgen, S Fahrbach, R Rubin), pp. 93-156. San Diego, CA: Academic Press.
17. Malpaux B, Thiéry JC, Chemineau P. 1999 Melatonin and the seasonal control of reproduction. Reprod. Nutr. Dev. 39, 355-366. (doi:10.1051/rnd:19990308)
18. Arendt J. 1998 Melatonin and the pineal gland: influence on mammalian seasonal and circadian physiology. Rev. Reprod. 3, 13-22. (doi:10.1530/ror.0.0030013)
19. Bronson FH. 1985 Mammalian reproduction, an ecological perspective. Biol. Reprod. 32, 1-26. (doi:10.1095/biolreprod32.1.1)
20. Cork SJ, Dove H. 1989 Lactation in the tammar wallaby (Macropus eugenii). II. Intake of milk components and maternal allocation of energy. J. Zool. 219, 399-409. (doi:10.1111/j.1469-7998.1989.tb02588.x)
21. Yamada H, Oshima I, Sato K, Ebihara S. 1988 Loss of the circadian rhythms of locomotor activity, food intake, and plasma melatonin concentration induced by constant bright light in the pigeon (Columba livia). J. Comp. Physiol. A 163, 459-463. (doi:10.1007/BF00604900)
22. Dominoni DM, Goymann W, Helm B, Partecke J. 2013 Urban-like night illumination reduces melatonin release in European blackbirds (Turdus merula): implications of city life for biological timekeeping of songbirds. Front. Zool. 10, 60. (doi:10.1186/1742-9994-10-60)
23. Lewy AJ, Wehr TA, Goodwin FK, Newsome DA, Markey P. 1980 Light suppresses melatonin secretion in humans. Science 210, 1267-1269. (doi:10.1126/science.7434030)
24. Kurvers RHJM, Hölker F. 2015 Bright nights and social interactions: a neglected issue. Behav. Ecol. 26, 334-339. (doi:10.1093/beheco/aru223)
25. Tyndale-Biscoe H, Renfree M. 1987 Reproductive physiology of marsupials. Cambridge, UK: Cambridge University Press.
26. Tyndale-Biscoe H. 2005 Life of marsupials. Collingwood, Australia: CSIRO Publishing.
27. Chambers BK. 2009 Human disturbance affects the ecology and population dynamics of the tammar wallaby, Macropus eugenii, on Garden Island, Western Australia. Dissertation, University of Western Australia, Australia.
28. Chambers BK, Bencini R. 2010 Impact of human disturbance on the population dynamics and ecology of tammar wallabies on Garden Island, Western Australia. In Macropods: the biology of kangaroos, wallabies and rat-kangaroos (eds G Coulson, M Eldridge), pp. 211-218. Collingwood, Australia: CSIRO Publishing.
29. Berger PJ. 1966 Eleven-month ‘embryonic diapause’ in a marsupial. Nature 211, 435-436. (doi:10.1038/211435a0)
30. Sharman GB, Berger PJ. 1969 Embryonic diapause in marsupials. Adv. Reprod. Physiol. 4, 211-240.
31. Renfree MB, Tyndale-Biscoe CH. 1973 Intra-uterine development after diapause in the marsupial Macropus eugenii. Dev. Biol. 32, 28-40. (doi:10.1016/0012-1606(73)90217-0)
32. Sadleir R, Tyndale-Biscoe H. 1977 Photoperiod and the termination of embryonic diapause in the marsupial Macropus eugenii. Biol. Reprod. 16, 605-608. (doi:10.1095/biolreprod16.5.605)
33. Hinds LA, Tyndale-Biscoe CH. 1985 Seasonal and circadian patterns of circulating prolactin during lactation and seasonal quiescence in the tammar, Macropus eugenii. J. Reprod. Fertil. 74, 173-183. (doi:10.1530/jrf.0.0740173)
34. Renfree MB, Lincoln DW, Almeida OFX, Short RV. 1981 Abolition of seasonal embryonic diapause in a wallaby by pineal denervation. Nature 293, 138-139. (doi:10.1038/293138a0)
35. McConnell SJ, Tyndale-Biscoe CH. 1985 Response in peripheral plasma melatonin to photoperiod change and the effects of exogenous melatonin on seasonal quiescence in the tammar, Macropus eugenii. J. Reprod. Fertil. 75, 529-538. (doi:10.1530/jrf.0.0730529)
36. McConnell SJ, Tyndale-Biscoe CH, Hinds LA. 1986 Change in duration of elevated concentrations of melatonin is the factor in photoperiod response of the tammar, Macropus eugenii. J. Reprod. Fertil. 77, 623-632. (doi:10.1530/jrf.0.0770623)
37. Inns RW. 1982 Age determination in the Kangaroo Island wallaby, Macropus eugenii (Desmarest). Aust. Wild. Res. 9, 213-220. (doi:10.1071/WR9820213)
38. Poole WE, Simms NG, Wood JT, Luboloa M. 1991 Tables for age determination of the Kangaroo Island tammar wallaby (Macropus eugenii), from body measurements. Technical Memorandum no. 32. Canberra, Australia: CSIRO (Division of Wildlife and Ecology).
39. Dominoni DM, Carmona-Wagner EO, Hofmann M, Kranstauber B, Partecke J. 2013 Individual-based measurements of light intensity provide new insights into the effects of artificial light at night on daily rhythms of urban-dwelling songbirds. J. Anim. Ecol. 83, 681-692. (doi:10.1111/1365-2656.12150)
40. Bates D, Maechler M, Bolker B, Walker S. 2014 lme4: linear mixed-effects models using Eigen and S4. R package v. 1.1-7. http://cran.r-project.org/package=lme4.
41. R Development Core Team. 2014 R: a language and environment for statistical computing, v. 3.0.1. Vienna, Austria: R Foundation for Statistical Computing.
42. Lenth RV. 2014 Least-squares means. R package v. 2.17. http://cran.r-project.org/package= lsmeans.
43. Lyons A, Turner W, Getz W. 2013 Home range plus: a space-time characterization of movement over real landscapes. BMC Mov. Ecol. 1, 2. (doi:10.1186/2051-3933-1-2)
44. Getz WM, Fortmann-Roe S, Cross PC, Lyons AJ, Ryan SJ, Wilmers CC. 2007 LoCoH: nonparameteric kernel methods for constructing home ranges and utilization distributions. PLoS ONE 2, e207. (doi:10.1371/journal.pone.0000207)
45. McConnell S. 1986 Seasonal changes in the circadian plasma melatonin profile of the Tammar, Macropus eugenii. J. Pineal. Res. 3, 119-125. (doi:10.1111/j.1600-079X.1986.tb00734.x)
46. Collie A. 1830 On some particulars connected with the natural history of the kangaroo. Zool. J. 5, 238-241.
47. Rich C, Longcore T. 2006 Ecological consequences of artificial night lighting. Washington, DC: Island Press.
48. Inns RW. 1980 Ecology of the Kangaroo Island wallaby (Macropus eugenii) in the Flinders Chase National Park. Dissertation, University of Adelaide, Australia.
49. Zerbe P, Clauss M, Codron D. 2012 Reproductive seasonality in captive wild ruminants: implications for biogeographical adaptation, photoperiodic control, and life history. Biol. Rev. 87, 965-990. (doi:10.1111/j.1469-185X.2012.00238.x)
50. Post E, Forchhammer MC. 2008 Climate change reduces reproductive success of an arctic herbivore through trophic mismatch. Phil. Trans. R. Soc. B 363, 2369-2375. (doi:10.1098/rstb.2007.2207)
51. Both C, Bouwhuis S, Lessells CM, Visser ME. 2006 Climate change and population declines in a longdistance migratory bird. Nature 441, 81-83. (doi:10.1038/nature04539)
52. McMillan A, Coupland G, Chambers BK, Mills HR, Bencini R. 2010 Determining the diet of tammar wallabies on Garden island, Western Australia, using stable isotope analysis. In Macropods: the biology of kangaroos, wallabies and rat-kangaroos (eds G Coulson, M Eldridge), pp. 171-177. Collingwood, Australia: CSIRO Publishing.
53. Schwanz LE, Robert KA. 2012 Reproductive ecology of wild tammar wallabies in natural and developed habitats on Garden Island, Western Australia. Aust. J. Zool. 60, 111-119. (doi:10.1071/ZO12024)
54. Mottier P. 2009 LED for lighting applications. Hoboken, NJ: John Wiley and Sons.
55. Stone E, Jones G, Harris S. 2012 Conserving energy at a cost to biodiversity? Impacts of LED lighting on bats. Glob. Change Biol. 18, 2458-2465. (doi:10.1111/j.1365-2486.2012.02705.x)
56. Falchi F, Cinzano P, Elvidge CD, Keith DM, Haim A. 2011 Limiting the impact of light pollution on human health, environment and stellar visibility. J. Environ. Manage. 92, 2714-2722. (doi:10.1016/j.jenvman.2011.06.029)
57. Aubé M, Roby J, Kocifaj M. 2013 Evaluating potential spectral impacts of various artificial lights on melatonin suppression, photosynthesis, and star visibility. PLoS ONE 8, e67798. (doi:10.1371/journal.pone.0067798)