Journal of Ornithology

, Volume 147, Issue 1, pp 107–111

Do night-active birds lack daily melatonin rhythms? A case study comparing a diurnal and a nocturnal-foraging gull species

  • Martin Wikelski
  • Elisa M. Tarlow
  • Corine M. Eising
  • Ton G.G. Groothuis
  • Ebo Gwinner
Original Article

Abstract

Plasma melatonin concentrations in most animals investigated so far increase at night regardless of whether individuals are day or night active. Nevertheless, daily melatonin amplitudes are often seasonally adjusted to ecological conditions, with birds that breed at high latitudes and migrate during the night showing lower daily amplitudes. Here we investigate whether nocturnal seabirds, gulls that feed at night, also show a low melatonin amplitude because they have to be active predominantly during the night but also intermittently during the day. We sampled free-living nocturnal-foraging swallow-tailed gulls (Creagrus furcatus) on two Galapagos islands every ~4 h and compared their plasma melatonin concentrations with those of related black-headed gulls (Larus ridibundus) sampled in the Netherlands. Like most seabirds, the black-headed gulls showed generally low melatonin concentrations, but clear diel cycles. The swallow-tailed gulls, on the other hand, had similarly low absolute melatonin concentrations, but no detectable diel changes. Despite problems inherent in comparisons between two species and field/lab setups, our data lend support to the hypothesis that the lack of a diel melatonin rhythm allows animals to be active at any time.

Keywords

Swallow-tailed gull Creagrus furcatus Black-headed gull Larus ridibundus Melatonin Daily rhythm Nocturnal Diurnal Galápagos Seabird Hormones Activity 

References

  1. 1.
    Aschoff J (1981) Freerunning and entrained circadian rhythms In: Aschoff J (ed) Handbook of behavioral neurobiology. Plenum, New York, pp 81–93Google Scholar
  2. 2.
    Pittendrigh CS (1981) Circadian systems: general perspective. In: Aschoff J (ed) Handbook of behavioral neurobiology. Plenum, New York, pp 57–80Google Scholar
  3. 3.
    Rattenborg NC, Mandt BH, Obermeyer WH, Winsauer P, Huber R, Wikelski W, Benca RM (2004) Migratory sleeplessness in the white-crowned sparrow (Zonotrichia leucophrys gambelii). Publ Lib Sci 2:0924–0936Google Scholar
  4. 4.
    Palmgren P (1935) Über den Tagesrhythmus der Vögel im arktischen Sommer. Ornis Fennica 12:107–121Google Scholar
  5. 5.
    Underwood H (1984) The pineal and circadian rhythms. In: Reiter RJ (ed) The pineal gland. Raven, New York, pp 221–252Google Scholar
  6. 6.
    Binkley S (1993) Structures and molecules involved in generation and regulation of biological rhythms in vertebrates and invertebrates. Experientia 49:648–653CrossRefPubMedGoogle Scholar
  7. 7.
    Gwinner E, Hau M, Heigel S (1994) Phasic and tonic effects of melatonin on avian circadian systems. In: Hiroshige T, Honma KI (eds) Circadian clocks and evolution. Hokkaido University Press, Sapporo, pp 127–137Google Scholar
  8. 8.
    Gwinner E, Hau M, Heigel S (1997) Melatonin: generation and modulation of avian circadian rhythms. Brain Res Bull 44:439–444CrossRefPubMedGoogle Scholar
  9. 9.
    Gwinner E, Hau M (2000) Pineal gland, circadian rhythms and photoperiodism. In: Whittow CG (ed) Sturkie’s avian physiology. Academic, San Diego, pp 557–658Google Scholar
  10. 10.
    Cassone VM, Warren WS, Brooks DS, Lu J (1993) Melatonin, the pineal gland, and circadian rhythms. J Biol Rhythms 8:573–581Google Scholar
  11. 11.
    Van’t Hof TJ, Gwinner E (1998) A highly rudimentary circadian melatonin profile in a nocturnal bird, the barn owl (Tyto alba). Naturwissenschaften 85:4002–4004Google Scholar
  12. 12.
    Hau M, Gwinner E (1994) Melatonin facilitates synchronization of sparrow circadian-rhythms to light. J Comp Physiol A 175:343–347CrossRefGoogle Scholar
  13. 13.
    Hau M, Gwinner E (1995) Continuous melatonin accelerates resynchronization following phase shifts of a light-dark cycle. Physiol Behav 58:89–95CrossRefPubMedGoogle Scholar
  14. 14.
    Abraham U, Gwinner E, Van’t Hof JJ (2000) Exogenous melatonin reduces the resynchronization time after phase shifts of a nonphotic zeitgeber in the house sparrow (Passer domesticus). J Biol Rhythms 15:48–56PubMedCrossRefGoogle Scholar
  15. 15.
    Gwinner E, Brandstatter R (2001) Complex bird clocks. Phil Trans R Soc Lond B 356:1801–1810CrossRefGoogle Scholar
  16. 16.
    Hailman JP (1964) The Galapagos swallow-tailed gull is nocturnal. Wilson Bull 76:347–354Google Scholar
  17. 17.
    Snow BK, Snow DW (1968) The behaviour of the swallow-tailed gull of the Galápagos. Condor 70:210–214CrossRefGoogle Scholar
  18. 18.
    Burtt EH (1993) Cliff-facing behavior of the swallow-tailed gull Creagrus furcatus. Ibis 135:459–462Google Scholar
  19. 19.
    Jackson MH (1995) Galápagos: a natural history. University of Calgary Press, Calgary, pp 155–158Google Scholar
  20. 20.
    Chandler RJ (1983) Feeding-behavior of black-headed gull. Br Birds 76:85–87Google Scholar
  21. 21.
    Garland TJ, Adolph SC (1994) Why not to do two-species comparative studies: limitations on inferring adaptation. Physiol Zool 67:797–828Google Scholar
  22. 22.
    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 Endocrinol 133:297–304CrossRefPubMedGoogle Scholar
  23. 23.
    Fraser S, Cowen P, Franklin M, Franey C, Arendt J (1983) Direct radioimmunoassay for melatonin in plasma. Clin Chem 29:396–397PubMedGoogle Scholar
  24. 24.
    Hau M, Romero MR, Brawn JD, van’t Hof TJ (2002) Effect of polar day on plasma profiles of melatonin, testosterone and estradiol in high-Arctic Lapland longspurs. Gen Comp Endocrinol 126:101–112CrossRefPubMedGoogle Scholar
  25. 25.
    Nisbet ICT, Finch CE, Thompson N, Russek-Cohen E, Proudman JA, Ottinger MA (1999) Endocrine patterns during aging in the common tern (Sterna hirundo). Gen Comp Endocrinol 114:279–789CrossRefPubMedGoogle Scholar
  26. 26.
    Cassone V (1990) Effects of melatonin on vertebrate circadian systems. Trends Neurosci 13:57–464CrossRefGoogle Scholar
  27. 27.
    Horning M, Trillmich F (1999) Lunar cycles in diel prey migrations exert a stronger effect on the diving of juveniles than adult Galapagos fur seals. Proc R Soc Lond B 266:1127–1132CrossRefGoogle Scholar
  28. 28.
    Breuner CW, Wingfield JC, Romero LM (1999) Diel rhythms of basal and stress-induced corticosterone in a wild, seasonal vertebrate, Gambel’s white-crowned sparrow. J Exp Zool 284:334–342CrossRefPubMedGoogle Scholar
  29. 29.
    Erkert HG, Nagel B, Stephani I (1986) Light and social effects on the free-running circadian activity rhythm in common marmosets (Callithrix jacchus; Primates) social masking, pseudo-splitting, and relative coordination. Behav Ecol Sociobiol 18:443 452CrossRefGoogle Scholar
  30. 30.
    Meyer WE, Millam JR (1991) Plasma melatonin levels in Japanese quail exposed to dim light are determined by subjective interpretation of day and night, not light intensity. Gen Comp Endocrinol 82:377–385CrossRefPubMedGoogle Scholar
  31. 31.
    John TM, George JC, Yie SM, Brown GM (1993) Flight-induced increase in circulating levels of melatonin in the homing pigeon. Comp Biochem Physiol 106A:645–648CrossRefGoogle Scholar
  32. 32.
    Fernandez de M, Arechiga H (1994) Circadian locomotor activity and its entrainment by food in the crayfish, Procambarus darki. J Exp Biol 190:9–21PubMedGoogle Scholar
  33. 33.
    Kumar V, Gwinner E, Van’t Hof TJ (2000) Circadian rhythms of melatonin in European starlings exposed to different lighting conditions: relationship with locomotor and feeding rhythms. J Comp Physiol A 186:205–215CrossRefPubMedGoogle Scholar
  34. 34.
    Jessop TS, Limpus CJ, Whittier JM (2002) Nocturnal activity in the green sea turtle alters daily profiles of melatonin and corticosterone. Horm Behav 41:357–365CrossRefPubMedGoogle Scholar
  35. 35.
    Cockrem JF (1991a) Plasma melatonin in the Adelie penguin (Pygoscelis adeliae) under continuous daylight in Antactica. J Pineal Res 10:2–8PubMedCrossRefGoogle Scholar
  36. 36.
    Cockrem JF (1991b) Circadian rhythms of plasma melatonin in the Adelie penguin (Pygoscelis adeliae) in constant dim light and artificial photoperiods. J Pineal Res 11:63–69PubMedCrossRefGoogle Scholar
  37. 37.
    Miché F, Vivien-Roels B, Pévet P, Spehner C, Robin JP, Le Maho Y (1991) Daily pattern of melatonin secretion in an Antarctic bird, the emperor penguin Aptenodytes forsteri: seasonal variations, effect of constant illumination and of administration of isoproterenol or propranolol. Gen Comp Endocrinol 84:249–263CrossRefPubMedGoogle Scholar
  38. 38.
    Reierth E, Van’t Hof TJ, Stokkan KA (1999) Seasonal and daily variations in plasma melatonin in the high-Arctic Svalbard ptarmigan (Lagopus mutus hyperboreus). J Biol Rhythms 14:314–319CrossRefPubMedGoogle Scholar
  39. 39.
    Fusani L, Gwinner E (2004) Simulation of migratory flight and stopover affects night levels of melatonin in a nocturnal migrant. Proc R Soc Lond B 271:205–211CrossRefGoogle Scholar
  40. 40.
    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 Endocrinol 90:119–124CrossRefPubMedGoogle Scholar
  41. 41.
    Guchhait P, Haldar C (1999) Circadian rhythms of melatonin and sex steroids in a nocturnal bird, Indian spotted owlet Athene brama during reproductively active and inactive phases. Biol Rhythm Res 30:508–516CrossRefGoogle Scholar
  42. 42.
    Taniguchi M, Murakami N, Nakamura H, Nasu T, Shinohara S, Etoh T (1993) Melatonin release from pineal cells of diurnal and nocturnal birds. Brain Res 620:297–300CrossRefPubMedGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2005

Authors and Affiliations

  • Martin Wikelski
    • 1
  • Elisa M. Tarlow
    • 1
  • Corine M. Eising
    • 2
    • 3
  • Ton G.G. Groothuis
    • 2
  • Ebo Gwinner
    • 4
  1. 1.Department of Ecology and Evolutionary BiologyPrinceton UniversityPrincetonUSA
  2. 2.Department of Animal BehaviorUniversity of GroningenAA HarenThe Netherlands
  3. 3.Percy FitzPatrick Institute of African OrnithologyCape TownSouth Africa
  4. 4.Max Planck Research Center for OrnithologyAndechsGermany

Personalised recommendations