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

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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.

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References

  1. Aschoff J (1981) Freerunning and entrained circadian rhythms In: Aschoff J (ed) Handbook of behavioral neurobiology. Plenum, New York, pp 81–93

    Google Scholar 

  2. Pittendrigh CS (1981) Circadian systems: general perspective. In: Aschoff J (ed) Handbook of behavioral neurobiology. Plenum, New York, pp 57–80

    Google Scholar 

  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 2:0924–0936

    CAS  Google Scholar 

  4. Palmgren P (1935) Über den Tagesrhythmus der Vögel im arktischen Sommer. Ornis Fennica 12:107–121

    Google Scholar 

  5. Underwood H (1984) The pineal and circadian rhythms. In: Reiter RJ (ed) The pineal gland. Raven, New York, pp 221–252

    Google Scholar 

  6. Binkley S (1993) Structures and molecules involved in generation and regulation of biological rhythms in vertebrates and invertebrates. Experientia 49:648–653

    Article  CAS  PubMed  Google Scholar 

  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 127–137

    Google Scholar 

  8. Gwinner E, Hau M, Heigel S (1997) Melatonin: generation and modulation of avian circadian rhythms. Brain Res Bull 44:439–444

    Article  CAS  PubMed  Google Scholar 

  9. Gwinner E, Hau M (2000) Pineal gland, circadian rhythms and photoperiodism. In: Whittow CG (ed) Sturkie’s avian physiology. Academic, San Diego, pp 557–658

    Chapter  Google Scholar 

  10. Cassone VM, Warren WS, Brooks DS, Lu J (1993) Melatonin, the pineal gland, and circadian rhythms. J Biol Rhythms 8:573–581

    Google Scholar 

  11. Van’t Hof TJ, Gwinner E (1998) A highly rudimentary circadian melatonin profile in a nocturnal bird, the barn owl (Tyto alba). Naturwissenschaften 85:4002–4004

    Google Scholar 

  12. Hau M, Gwinner E (1994) Melatonin facilitates synchronization of sparrow circadian-rhythms to light. J Comp Physiol A 175:343–347

    Article  CAS  Google Scholar 

  13. Hau M, Gwinner E (1995) Continuous melatonin accelerates resynchronization following phase shifts of a light-dark cycle. Physiol Behav 58:89–95

    Article  CAS  PubMed  Google Scholar 

  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 15:48–56

    Article  CAS  PubMed  Google Scholar 

  15. Gwinner E, Brandstatter R (2001) Complex bird clocks. Phil Trans R Soc Lond B 356:1801–1810

    Article  CAS  Google Scholar 

  16. Hailman JP (1964) The Galapagos swallow-tailed gull is nocturnal. Wilson Bull 76:347–354

    Google Scholar 

  17. Snow BK, Snow DW (1968) The behaviour of the swallow-tailed gull of the Galápagos. Condor 70:210–214

    Article  Google Scholar 

  18. Burtt EH (1993) Cliff-facing behavior of the swallow-tailed gull Creagrus furcatus. Ibis 135:459–462

    Article  Google Scholar 

  19. Jackson MH (1995) Galápagos: a natural history. University of Calgary Press, Calgary, pp 155–158

    Google Scholar 

  20. Chandler RJ (1983) Feeding-behavior of black-headed gull. Br Birds 76:85–87

    Google Scholar 

  21. Garland TJ, Adolph SC (1994) Why not to do two-species comparative studies: limitations on inferring adaptation. Physiol Zool 67:797–828

    Article  Google Scholar 

  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 133:297–304

    Article  CAS  PubMed  Google Scholar 

  23. Fraser S, Cowen P, Franklin M, Franey C, Arendt J (1983) Direct radioimmunoassay for melatonin in plasma. Clin Chem 29:396–397

    Article  CAS  PubMed  Google Scholar 

  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 126:101–112

    Article  CAS  PubMed  Google Scholar 

  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 114:279–789

    Article  CAS  PubMed  Google Scholar 

  26. Cassone V (1990) Effects of melatonin on vertebrate circadian systems. Trends Neurosci 13:57–464

    Article  Google Scholar 

  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 266:1127–1132

    Article  CAS  Google Scholar 

  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 284:334–342

    Article  CAS  PubMed  Google Scholar 

  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 18:443 452

    Article  Google Scholar 

  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 82:377–385

    Article  CAS  PubMed  Google Scholar 

  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:645–648

    Article  CAS  Google Scholar 

  32. Fernandez de M, Arechiga H (1994) Circadian locomotor activity and its entrainment by food in the crayfish, Procambarus darki. J Exp Biol 190:9–21

    Article  Google Scholar 

  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 186:205–215

    Article  CAS  PubMed  Google Scholar 

  34. Jessop TS, Limpus CJ, Whittier JM (2002) Nocturnal activity in the green sea turtle alters daily profiles of melatonin and corticosterone. Horm Behav 41:357–365

    Article  CAS  PubMed  Google Scholar 

  35. Cockrem JF (1991a) Plasma melatonin in the Adelie penguin (Pygoscelis adeliae) under continuous daylight in Antactica. J Pineal Res 10:2–8

    Article  CAS  PubMed  Google Scholar 

  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 11:63–69

    Article  CAS  PubMed  Google Scholar 

  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 84:249–263

    Article  PubMed  Google Scholar 

  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 14:314–319

    Article  CAS  PubMed  Google Scholar 

  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 271:205–211

    Article  CAS  Google Scholar 

  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 90:119–124

    Article  CAS  PubMed  Google Scholar 

  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 30:508–516

    Article  CAS  Google Scholar 

  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 620:297–300

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Franz Kümmeth for assistance in the field, Michaela Hau for discussions and use of her laboratory, and David Anderson for use of his field site. We also thank the Galápagos National Park Service, the Charles Darwin Research Station, and TAME Airline for enabling this work. This is a contribution of the Charles-Darwin-Foundation and was supported by the National Science Foundation, Princeton University and the Max Planck Society.

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Correspondence to Martin Wikelski.

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Communicated by F. Bairlein

Ebo Gwinner was involved in the planning stage, the experimental realization and the writing of a manusript draft of this project. Unfortunately he deceased before the manuscript was completed. Thus, he was thus not involved in the finalization of the manuscript.

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Wikelski, M., Tarlow, E.M., Eising, C.M. et al. Do night-active birds lack daily melatonin rhythms? A case study comparing a diurnal and a nocturnal-foraging gull species. J Ornithol 147, 107–111 (2006). https://doi.org/10.1007/s10336-005-0018-4

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  • DOI: https://doi.org/10.1007/s10336-005-0018-4

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