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PLOS ONE  2011 

Celestial Moderation of Tropical Seabird Behavior

DOI: 10.1371/journal.pone.0027663

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Abstract:

Most animals, including birds, have cyclic life histories and numerous studies generally conducted on captive animals have shown that photoperiod is the main factor influencing this periodicity. Moon cycles can also affect periodic behavior of birds. Few studies have investigated the influence of these environmental cues in natural settings, and particularly in tropical areas where the change in photoperiod is slight and some bird species keep cyclic behaviors. Using miniaturized light sensors, we simultaneously investigated under natural conditions the influence of photoperiod and moon phases on the migration dates and at-sea activity of a tropical seabird species, the Barau's petrel, throughout its annual cycle. Firstly, we found that birds consistently started their pre- and post-breeding migrations at precise dates corresponding in both cases to a day-duration of 12.5 hours, suggesting a strong influence of the photoperiod in the regulation of migration behavior. We also found that mean population arrival dates to the colony changed from year to year and they were influenced by moon phases. Returns at their colonies occurred around the last full moon of the austral winter, suggesting that moon cycle is used by birds to synchronize their arrival. Secondly, variations of day-time activity were sinusoidal and correlated to seasonal changes of daylength. We thus hypothesize that the photoperiod could directly affect the behavior of the birds at sea. Night-time at-sea activity exhibited a clear cycle of 29.2 days, suggesting that nocturnal foraging was highly regulated by moon phase, particularly during the non-breeding season. To our knowledge, this is the first study to document a mixed regulation of the behavior of a wild bird by photoperiod and moon phases throughout its annual cycle.

References

[1]  Perrins CM (1970) The timing of birds' breeding seasons. Ibis 112: 242–255. doi:10.1111/j.1474-919X.1970.tb00096.x.
[2]  Nussey DH, Postma E, Gienapp P, Visser ME (2005) Selection on heritable phenotypic plasticity in a wild bird population. Science 310: 304–306. doi:10.1126/science.1117004.
[3]  van Asch M, Visser ME (2007) Phenology of forest caterpillars and their host trees: the importance of synchrony. Annu Rev Entomol 52: 37–55. doi:10.1146/annurev.ento.52.110405.091418.
[4]  Wikelski M, Martin LB, Scheuerlein A, Robinson MT, Robinson ND, et al. (2008) Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control. Philos Trans R Soc Lond B Biol Sci 363: 411–423. doi:10.1098/rstb.2007.2147.
[5]  Farner DS (1985) Annual rhythms. Annu Rev Physiol 47: 65–82. doi:10.1146/annurev.ph.47.030185.000433.
[6]  Murton R, Westwood N (1977) Avian breeding cycles. Oxford: Carendon Press.
[7]  Dawson A, King VM, Bentley GE, Ball GF (2001) Photoperiodic control of seasonality in birds. J Biol Rhythms 16: 365–380. doi:10.1177/074873001129002079.
[8]  Leitner S, Van't Hof TJ, Gahr M (2003) Flexible reproduction in wild canaries is independent of photoperiod. Gen Comp End 130: 102–108.
[9]  Visser ME, Holleman LJM, Caro SP (2009) Temperature has a causal effect on avian timing of reproduction. Proc Roy Soc Lon B 276: 2323–2331. doi:10.1098/rspb.2009.0213.
[10]  Dawson A (2008) Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability. Philos Trans R Soc Lond B 363: 1621–1633. doi:10.1098/rstb.2007.0004.
[11]  Chapin J, Wing L (1959) The wideawake calendar, 1953 to 1958. The Auk 76: 153–158.
[12]  Rahman M, Takemura A, Takano K (2001) Lunar synchronization of testicular development and steroidogenesis in rabbitfish. Comp Biochem Physiol B 129: 367–373.
[13]  Sábato MAL, de Melo LFB, Magni EMV, Young RJ, Coelho CM (2006) A note on the effect of the full moon on the activity of wild maned wolves, Chrysocyon brachyurus. Behav Processes 73: 228–230. doi:10.1016/j.beproc.2006.05.012.
[14]  Penteriani V, Delgado MDM, Campioni L, Louren?o R (2010) Moonlight makes owls more chatty. PLoS ONE 5: e8696. doi:10.1371/journal.pone.0008696.
[15]  Yamamoto T, Takahashi A, Yoda K, Katsumata N, Watanabe S, et al. (2008) The lunar cycle affects at-sea behaviour in a pelagic seabird, the streaked shearwater, Calonectris leucomelas. Anim Behav 76: 1647–1652.
[16]  Hau M, Wikelski M, Wingfield JC (1998) A neotropical forest bird can measure the slight changes in tropical photoperiod. Proc Roy Soc Lon B 265: 89–95. doi:10.1098/rspb.1998.0268.
[17]  Gwinner E, Scheuerlein A (1998) Seasonal changes in day-light intensity as a potential zeitgeber of circannual rhythms in equatorial Stonechats. Journal of Ornithology 139: 407–412.
[18]  Jaquemet S, Le Corre M, Quartly G (2007) Ocean control of the breeding regime of the sooty tern in the southwest Indian Ocean. Deep-Sea Research Part I 54: 130–142.
[19]  Cooke SJ, Hinch SG, Wikelski M, Andrews RD, Kuchel LJ, et al. (2004) Biotelemetry: a mechanistic approach to ecology. Trends Ecol Evol 19: 334–343. doi:10.1016/j.tree.2004.04.003.
[20]  Péron C, Delord K, Phillips RA, Charbonnier Y, Marteau C, et al. (2010) Seasonal variation in oceanographic habitat and behaviour of white-chinned petrels Procellaria aequinoctialis from Kerguelen Island. Mar Ecol Prog Ser 416: 267–288. doi:10.3354/meps08785.
[21]  Croxall JP, Silk JRD, Phillips RA, Afanasyev V, Briggs DR (2005) Global Circumnavigations: Tracking Year-Round Ranges of Nonbreeding Albatrosses. Science 307: 249–250. doi:10.1126/science.1106042.
[22]  Phillips R, Silk J, Croxall JP (2005) Foraging and provisioning strategies of the light-mantled sooty albatross at South Georgia: competition and co-existence with sympatric pelagic predators. Mar Ecol Prog Ser 285: 259–270.
[23]  Wilson R, Ducamp J, Rees G, Niekamp K (1992) Estimation of location: global coverage using light intensity. In: Ellis Horward , Chichester , editors. Wildlife telemetry: remote monitoring and tracking of animals. Priede IMSS. pp. 131–134.
[24]  Hill R (1994) Theory of geolocation by light levels. In: Le Boeuf B, Laws R, editors. Elephant seals, population ecology, behavior, and physiology. University of California Press. pp. 227–236.
[25]  Bretagnolle V, Attié C (1991) Status of Barau's Petrel (Pterodroma baraui): Colony Sites, Breeding Population and Taxonomic Affinities. Colon Waterbirds 14: 25–33.
[26]  Le Corre M, Ollivier A, Ribes S, Jouventin P (2002) Light-induced mortality of petrels: a 4-year study from Reunion Island (Indian Ocean). Biol Conserv 105: 93–102.
[27]  Pinet P, Jaquemet S, Pinaud D, Weimerskirch H, Phillips R, et al. (2011) Migration, wintering distribution and habitat use of an endangered tropical seabird, the Barau's Petrel Pterodroma baraui. Mar Ecol Prog Ser 423: 291–302.
[28]  Pinet P, Salamolard M, Probst J, Russell J, Jaquemet S, et al. (2009) Barau's Petrel (Pterodroma baraui): History, Biology and Conservation of an Endangered Endemic Petrel. Mar Ornithol 37: 107–113.
[29]  González-Solís J, Croxall JP, Oro D, Ruiz X (2007) Trans-equatorial migration and mixing in the wintering areas of a pelagic seabird. Front Ecol Environ 5: 297–301.
[30]  Guilford T, Meade J, Willis J, Phillips R, Boyle D, et al. (2009) Migration and stopover in a small pelagic seabird, the Manx shearwater Puffinus puffinus: insights from machine learning. Proc Roy Soc Lon B 276: 1215.
[31]  Phillips R, Xavier J, Croxall JP (2003) Effects of satellite transmitters on albatrosses and petrels. The Auk 120: 1082–1090.
[32]  Igual J, Forero M, Tavecchia G, Gonzalez-Solis J, Martínez-Abraín A, et al. (2005) Short-term effects of data-loggers on Cory's shearwater (Calonectris diomedea). Mar Biol 146: 619–624.
[33]  Phillips R, Silk J, Croxall JP, Afanasyev V, Briggs D (2004) Accuracy of geolocation estimates for flying seabirds. Mar Ecol Prog Ser 266: 265–272.
[34]  Weimerskirch H, Wilson R, Lys P (1997) Activity pattern of foraging in the wandering albatross: a marine predator with two modes of prey searching. Mar Ecol Prog Ser 151: 245–254.
[35]  Phillips R, Catry P, Silk J, Bearhop S, McGill R, et al. (2007) Movements, winter distribution and activity patterns of Falkland and brown skuas: insights from loggers and isotopes. Mar Ecol Prog Ser 345: 281–291.
[36]  Mackley EK, Phillips RA, Silk JRD, Wakefield ED, Afanasyev V, et al. (2011) At-sea activity patterns of breeding and nonbreeding white-chinned petrels Procellaria aequinoctialis from South Georgia. Mar Biol 158: 429–438. doi:10.1007/s00227-010-1570-x.
[37]  Cazelles B, Chavez M, Berteaux D, Ménard F, Vik J, et al. (2008) Wavelet analysis of ecological time series. Oecologia 156: 287–304.
[38]  Bovet P, Benhamou S (1988) Spatial analysis of animals' movements using a correlated random walk model. J Theor Biol 131: 419–433.
[39]  Girard C, Benhamou S, Dagorn L (2004) FAD: Fish Aggregating Device or Fish Attracting Device? A new analysis of yellowfin tuna movements around floating objects. Anim Behav 67: 319–326.
[40]  Kumar V, Wingfield JC, Dawson A, Ramenofsky M, Rani S, et al. (2010) Biological clocks and regulation of seasonal reproduction and migration in birds. Physiol Biochem Zool 83: 827–835. doi:10.1086/652243.
[41]  Brandst?tter R, Kumar V, Abraham U, Gwinner E (2000) Photoperiodic information acquired and stored in vivo is retained in vitro by a circadian oscillator, the avian pineal gland. Proc Natl Acad Sci 97: 12324–12328. doi:10.1073/pnas.200354997.
[42]  Brandst?tter R, Kumar V, Van't Hof TJ, Gwinner E (2001) Seasonal variations of in vivo and in vitro melatonin production in a passeriform bird, the house sparrow (Passer domesticus). J Pineal Res 31: 120–126.
[43]  Kumar V, Follett BK (1993) The circadian nature of melatonin secretion in Japanese quail (Coturnix coturnix japonica). J Pineal Res 14: 192–200.
[44]  Gwinner E (1996) Circadian and circannual programmes in avian migration. J Exp Biol 199: 39.
[45]  Gwinner E, Schwabl-Benzinger I, Schwabl H, Dittami J (1993) Twenty-four hour melatonin profiles in a nocturnally migrating bird during and between migratory seasons. Gen Comp End 90: 119–124. doi:10.1006/gcen.1993.1066.
[46]  Wolfson A (1952) Day length, migration, and breeding cycles in birds. The Scientific Monthly 74: 191–200.
[47]  Buehler DM, Koolhaas A, Van't Hof TJ, Schwabl I, Dekinga A, et al. (2009) No evidence for melatonin-linked immunoenhancement over the annual cycle of an avian species. J Comp. Physiol 195: 445–451. doi:10.1007/s00359-009-0422-y.
[48]  Dawson A (2007) Seasonality in a temperate zone bird can be entrained by near equatorial photoperiods. Proc Roy Soc Lon B 274: 721–725. doi:10.1098/rspb.2006.0067.
[49]  Dawson A, King V (1994) Thyroidectomy does not affect the daily or free-running rhythms of plasma melatonin in European starlings. J Biol Rhythms 9: 137–144.
[50]  Coverdill AJ, Bentley GE, Ramenofsky M (2008) Circadian and Masking Control of Migratory Restlessness in Gambel's White-Crowned Sparrow (Zonotrichia leucophrys gambelii). J Biol Rhythms 23: 59–68. doi:10.1177/0748730407311456.
[51]  Phalan B, Phillips R, Silk J, Afanasyev V (2007) Foraging behaviour of four albatross species by night and day. Mar Ecol Prog Ser 340: 271–286.
[52]  Brothers N, Gales R, Reid T (1999) The influence of environmental variables and mitigation measures on seabird catch rates in the Japanese tuna longline fishery within the Australian Fishing Zone, 1991–1995. Biol Conserv 88: 85–101.
[53]  Clarke JA (1983) Moonlight's influence on predator/prey interactions between short-eared owls (Asio flammeus) and deermice (Peromyscus maniculatus). Behav Ecol Sociobiol 13: 205–209. doi:10.1007/BF00299924.
[54]  Martin G (1990) Birds by night. London: T&AD Poyser.
[55]  Neumann D (1981) Tidal and lunar rhythms. In: Aschoff J, editor. Handbook of behavioral neurobiology. Plenum. pp. 351–380.
[56]  Taylor M (1984) Lunar synchronization of fish reproduction. Transactions of the American Fisheries Society 113: 484–493.
[57]  Parrish J (1999) Using behavior and ecology to exploit schooling fishes. Environmental Biology of Fishes 55: 157–181.
[58]  Tarling G, Buchholz F, Matthews J (1999) The effect of lunar eclipse on the vertical migration behaviour of Meganyctiphanes norvegica (Crustacea: Euphausiacea) in the Ligurian Sea. Journal of Plankton Research 21: 1475–1488.
[59]  Benoit-Bird K, Au W, Wisdoma D (2009) Nocturnal light and lunar cycle effects on diel migration of micronekton. Limnol Oceanogr 54: 1789–1800.
[60]  Tarlow EM, Hau M, Anderson DJ, Wikelski M (2003) Diel changes in plasma melatonin and corticosterone concentrations in tropical Nazca boobies (Sula granti) in relation to moon phase and age. Gen Comp End 133: 297–304.
[61]  Warham J (1990) The petrels: their ecology and breeding systems. London: Academic press.
[62]  Gwinner E (2003) Circannual rhythms in birds. Curr Opin Neurobiol 13: 770–778.
[63]  Stahl J, Bartle J (1991) Distribution, abundance and aspects of the pelagic ecology of Barau's Petrel (Pterodroma baraui) in the south-west Indian Ocean. Notornis 38: 211–225.
[64]  Pocklington R (1979) An oceanographic interpretation of seabird distributions in the Indian Ocean. Mar Biol 51: 9–21.

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