Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-22T23:15:37.052Z Has data issue: false hasContentIssue false

Keeping the clock set under the midnight sun: diurnal periodicity and synchrony of avian Isospora parasites cycle in the High Arctic

Published online by Cambridge University Press:  15 July 2011

OLGA V. DOLNIK*
Affiliation:
Institute for Polar Ecology, Wischhofstrasse, 1-3 Geb. 12, D-24148 Kiel, Germany
BENJAMIN J. METZGER
Affiliation:
Institute of Avian Research ‘Vogelwarte Helgoland’, An der Vogelwarte 21, 26386 Wilhelmshaven, Germany
MAARTEN J. J. E. LOONEN
Affiliation:
Arctic Centre University of Groningen, Aweg 30, 9718 CW Groningen, The Netherlands
*
*Corresponding author: Institute for Polar Ecology, Wischhofstrasse, 1-3 Geb. 12, D-24148 Kiel, Germany. Tel: ++49(0)431 8860842. Fax: ++49(0)431 6001210. E-mail: [email protected]

Summary

For Isospora (Protozoa: Eimeriidae) parasites of passerine birds, diurnal periodicity of oocyst output is a well-described phenomenon. From the temporal zone to the tropics, oocyst production is correlated with the light-dark cycle, peaking in the afternoon hours. However, nothing is known about the existence of diurnal periodicity of these parasites in the birds of High Arctic environments, under permanent light during summer. We sampled free-ranging Snow Bunting (Aves: Passeriformes), on Svalbard in summer and tested oocysts output of Isospora plectrophenaxia. Here we show that under the permanent light conditions of Arctic summer in the wild, Isospora plectrophenaxia, a parasite of the Snow Bunting, still keeps the 24-h rhythm of oocyst output with the peak in the post-meridiem hours, despite the absence of diurnal periodicity in host's activity. Our findings prove the ability of avian Isospora to invoke alternative cues for synchronizing the circadian rhythms. Possible cues and adaptive significance of diurnal periodicity of parasite output in High Arctic are discussed. The maintenance of synchronization and timing of the parasite life-cycle stages is under positive selection pressure even in permanent daylight in the Arctic.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Asio, S. M., Simonsen, P. E. and Onapa, A. W. (2009). Analysis of the 24-h microfilarial periodicity of Mansonella perstans. Parasitology Research 104, 945948. doi: 10.1007/s00436-008-1312-x.CrossRefGoogle ScholarPubMed
Barré, N. and Troncy, P. M. (1974). Note on a coccidian of some Ploceidae in Chad: Isospora xerophila n. sp. Zeitschrift für Parasitenkunde 44, 139147.Google Scholar
Belli, S. I., Smith, N. C. and Ferguson, D. J. P. (2006). The coccidian oocyst: a tough nut to crack! Trends in Parasitology 22, 416423. doi: 10.1016/j.pt.2006.07.004.CrossRefGoogle ScholarPubMed
Boughton, D. C. (1933). Diurnal gametic periodicity in avian Isospora. American Journal of Hygiene 33, 161184.Google Scholar
Brandlmeier, H. (2006). Die circadiane Ausscheidung von Kokzidienoozysten beim Haussperling (Passer domesticus) unter Veränderung des Melatoninspiegels: Experimentelle Untersuchungen am Modell eines Wirt-Parasit-Systems. Ph.D. thesis, University of Munich, Munich.Google Scholar
Bünning, E. (1973). The Physiological Clock. Springer-Verlag, New York, USA.Google Scholar
Bush, A. O., Fernandez, J. W., Esch, G. W. and Seed, J. R. (2001). Perspectives in Parasitology: The Ecology and Diversity of Parasites. Cambridge University Press, Cambridge, UK.Google Scholar
Calisi, R. M. and Bentley, G. E. (2009). Lab and field experiments: are they the same animal? Hormones and Behavior 56, 110. doi:10.1016/j.yhbeh.2009.02.010.CrossRefGoogle ScholarPubMed
Cockrem, J. F. (1991). Plasma melatonin in the Adelie penguin (Pygoscelis adeliae) under continuous daylight in Antarctica. Journal of Pineal Research 10, 28. doi: 10.1111/j.1600-079X.1991.tb00002.x.CrossRefGoogle ScholarPubMed
Combes, C. (2001). Parasitism. The Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago, IL, USA.Google Scholar
Cramp, S. and Perrins, C. (eds.) (1994). Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic: Buntings and New World Warblers Vol. IX. Oxford University Press, Oxford, UK.Google Scholar
Dolnik, O. V. (1999). Diurnal periodicity in appearance of Isospora (Protozoa: Coccidea) oocysts from some passerine birds. Proceedings of the Zoological Institute RAS 281, 113118.Google Scholar
Dolnik, O. (2002). Some aspects of the biology and host-parasite interactions of Isospora spp. (Protozoa: Coccidiida) of passerine birds. Ph.D. thesis, University of Oldenburg, Oldenburg, Germany.Google Scholar
Dolnik, O. V. (2006). The relative stability of chronic Isospora sylvianthina (Protozoa: Apicomplexa) infection in blackcaps (Sylvia atricapilla): evaluation of a simplified method of estimating isosporan infection intensity in passerine birds. Parasitology Research 100, 155160. doi: 10.1007/s00436-006-0253-5.CrossRefGoogle ScholarPubMed
Dolnik, O. V., Dolnik, V. R. and Bairlein, F. (2010). The effect of host foraging ecology on the prevalence and intensity of coccidian infection in wild passerine birds. Ardea 98, 97103.Google Scholar
Dolnik, O. V. and Loonen, M. J. J. E. (2007). Isospora plectrophenaxia n. sp (Apicomplexa: Eimeriidae), a new coccidian parasite found in Snow Bunting (Plectrophenax nivalis) nestlings on Spitsbergen. Parasitology Research 101, 16171619. doi: 10.1007/s00436-007-0703-8.Google Scholar
Erikstad, K. E. (1989). The diel activity of Carabid Beetles (Coleoptera) North of the Arctic Circle, with particular reference to Patrobus assimilis Chaud. and Notiophilus aquaticus L. Polar Biology 9, 319323. doi: 10.1007/BF00287430.Google Scholar
Grulet, O., Landau, I., Millet, P. and Baccam, D. (1986). Les Isospora du moineau II – Etudes sur la biologie. Annales de Parasitologie Humaine et Comparée 61, 161192.CrossRefGoogle Scholar
Gwinner, E., Hau, M. and Heigl, S. (1997). Melatonin: generation and modulation of avian circadian rhythms. Brain Research Bulletin 44, 439444. doi: 10.1016/S0361-9230(97)00224-4.CrossRefGoogle ScholarPubMed
Haarhaus, D. (1968). Zum Tagesrhythmus des Staren (Sturnus vulgaris) und der Schneeammer (Plectrophenax nivalis). Oecologia 1, 176218.Google Scholar
Hau, M., Romero, L. M., Brawn, J. D. and Van't Hof, T. J. (2002). Effect of Polar Day on plasma profiles of melatonin, testosterone, and estradiol in High-Arctic Lapland Longspurs. General and Comparative Endocrinology 126, 101112. doi:10.1006/gcen.2002.7776.CrossRefGoogle ScholarPubMed
Krüll, F., Demmelmeyer, H. and Remmert, H. (1985). On the circadian rhythm of animals in high Polar latitudes. Naturwissenschaften 72, 197203.CrossRefGoogle Scholar
Kumar, V., Singh, B. P. and Rani, S. (2004). The bird clock: A complex, multi-oscillatory and highly diversified system. Biological Rhythms Research 35, 121144. doi: 10.1080/09291010412331313287.CrossRefGoogle Scholar
Lindström, K. M., Dolnik, O., Yabsley, M., Hellgren, O., O'Connor, B., Pärn, H. and Foufopoulos, J. (2009). Feather mites and internal parasites in small ground finches (Geospiza fuliginosa, Emberizidae) from the Galapagos Islands (Equador). Journal of Parasitology 95, 3945. doi: 10.1645/GE-1655.1.Google Scholar
Long, P. L. (1982). The Biology of the Coccidia. University Park Press, Baltimore, MD, USA.Google Scholar
Martinaud, G., Billaudelle, M. and Moreau, J. (2009). Circadian variation in shedding of the oocysts of Isospora turdi (Apicomplexa) in blackbirds (Turdus merula): an adaptative trait against desiccation and ultraviolet radiation. International Journal for Parasitology 39, 735739. doi: 10.1016/j.ijpara.2008.11.006.CrossRefGoogle ScholarPubMed
Reierth, E., Van't Hof, T. J. and Stokkan, K. A. (1999). Seasonal and daily variations in plasma melatonin in the High Arctic Svalbard ptarmigan (Lagopus mutus hyperboreus). Journal of Biological Rhythms 14, 314319. doi: 10.1177/074873099129000731.CrossRefGoogle ScholarPubMed
Schwalbach, G. (1959). Untersuchungen und Beobachtungen an Coccidien der Gattungen Eimeria, Isospora und Caryospora bei Vögeln mit einer Beschreibung von sechzehn neuen Arten. Archiv für Protistenkunde 104, 431491.Google Scholar
Schwalbach, G. (1960). Die Coccidiose der Singvoegel. I. Der Ausscheidungsrhythmus der Isospora-Oocysten beim Haussperling (Passer domesticus). Zentralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene 178, 263276.Google Scholar
Sharma, V. K. (2003). Adaptive significance of circadian clocks. Chronobiology International 20, 901919. doi: 10.1081/CBI-120026099.CrossRefGoogle ScholarPubMed
Svobodová, M. (1994). Isospora, Caryospora and Eimeria (Apicomplexa: Eimeriidae) in passeriform birds from Czech Republic. Acta Protozoologica 33, 101108.Google Scholar
Wild, C. (2003). Experimentelle Untersuchung zur Chronobiologie einer Wirt-Parasit-Beziehung am Beispiel der Coccidiose (Isospora lacazei) des Haussperling (Passer domesticus). Ph.D. thesis, University of Munich, Munich, Germany.Google Scholar
Willmer, P., Stone, G. and Johnston, I. A. (2005). Environmental Physiology of Animals. Blackwell Science, Oxford, UK.Google Scholar