Journal of Ornithology

, Volume 156, Issue 2, pp 429–440 | Cite as

The relationship between parasites and spleen and bursa mass in the Icelandic Rock Ptarmigan Lagopus muta

  • Ute Stenkewitz
  • Ólafur K. Nielsen
  • Karl Skírnisson
  • Gunnar Stefánsson
Original Article

Abstract

The spleen and bursa of Fabricius in birds are organs that play an important role in fighting parasite infections. The size of these organs can be used by ecologists as a measure of immune investment, with larger size implying greater investment. The bursa only occurs in juvenile birds during the development of the B cell repertoire, whereas the spleen, which is the main site of lymphocyte differentiation and proliferation, is present in both juveniles and adults. We investigated spleen and bursa mass in relation to parasite measures for 541 Rock Ptarmigan Lagopus muta collected in northeast Iceland during October from 2007 to 2012. Of these 541birds, 540 carried at least one parasite species. Juveniles had heavier spleens than adults, and adult females had heavier spleens than adult males, but there were no sex differences in juveniles. Spleen mass increased from 2007 to 2009, then decreased up to 2011, before slightly increasing again in 2012. Spleen and bursa mass in juveniles increased with improved body condition, but decreased in adults, and this effect differed significantly among years. Spleen mass in juveniles was positively associated with parasite species richness and abundance, in particular endoparasite abundance, with coccidian parasites being the main predictors. Bursa mass was negatively associated with elevated ectoparasite abundance, with two chewing lice being the main predictors. These two immune defense organs appeared to relate to different stimuli. Mean annual spleen mass of juveniles changed in synchrony with Ptarmigan body condition and population density over the years of this study. The only parasite measure that showed any relation to density was coccidian prevalence in juvenile birds, with an approximately 2-year time-lag, suggesting that factors other than parasites are probably more important in triggering changes in spleen mass.

Keywords

Bursa of Fabricius Iceland Parasites Population density Rock Ptarmigan Spleen 

Zusammenfassung

Der Zusammenhang zwischen Parasiten und Milz- und Bursamasse beim isländischen Alpenschneehuhn Lagopus muta

Die Milz und Bursa Fabricii in Vögeln sind wichtige Organe, die eine Rolle in der Abwehr von Parasiteninfektionen spielen. Die Größe dieser Organe wird von Ökologen gelegentlich als Richtwert von Immuninvestition genutzt, wobei zunehmende Größe mit stärkerer Investition verbunden wird. Die Bursa existiert nur in Jungvögeln während der Entwicklung des B-Zellen Repertoires, aber die Milz, welche der Hauptsitz der Lymphozytenabgrenzung und–vermehrung ist, kommt in Vögeln jeglichen Alters vor. Wir untersuchten Milz-und Bursamasse im Verhältnis zu Parasiten von 541 Alpenschneehühnern Lagopus muta, die in Nordost-Island im Oktober von 2007 bis 2012 gesammelt wurden. Von diesen trugen 540 Vögel wenigstens eine Parasitenart. Jungvögel hatten schwerere Milzen als ausgewachsene Vögel und ausgewachsene Weibchen hatten schwerere Milzen als ausgewachsene Männchen, aber es gab keine Geschlechtsunterschiede bei den Jungvögeln. Milzmassen nahmen von 2007 bis 2009 zu, fielen dann bis 2011, bevor sie in 2012 leicht anstiegen. In Jungvögeln nahmen Milz-und Bursamasse mit verbessertem Körperzustand zu, aber in ausgewachsenen Vögeln verschlechterte er sich, und dieser Effekt war signifikant über die Jahre. Milzmasse in Jungvögeln stand in positivem Zusammenhang mit Parasitenartenfülle und-häufigkeit, besonders Endoparasitenhäufigkeit, wobei Coccidien den größten Einfluss ausübten. Bursamasse stand in negativem Zusammenhang mit erhöhter Ektoparasitenhäufigkeit, wobei zwei Kieferlausarten den größten Einfluss hatten. Die zwei Immunabwehrorgane schienen mit verschiedenen Stimuli in Zusammenhang zu stehen. Die mittlere jährliche Milzmasse von Jungvögeln veränderte sich synchron mit dem Körperzustand und der Populationsdichte der Schneehühner während den Jahren dieser Untersuchung. Die einzige Parasiteneinheit, die in Zusammenhang mit der Populationsdichte stand, war Coccidienprevalänz in Jungvögeln, welche den Verlauf mit einer etwa 2-Jahre zeitlichen Verzögerung folgte. Dies gibt zu erkennen, dass andere Faktoren als Parasiten wahrscheinlich gewichtiger sind, Veränderungen in der Milzmasse hervorzurufen.

Notes

Acknowledgments

This project was financially supported by the Icelandic Research Fund (Grant Number 090207021), Icelandic Hunter’s Fund, Landsvirkjun Energy Fund, Institute of Experimental Pathology (KELDUR) at University of Iceland, and Icelandic Institute of Natural History. Logistical help was provided by the Icelandic Institute of Natural History, Mývatn Research Station, and Northeast Iceland Nature Center. For help in the field and the laboratory we thank S.S. Árnason, M. le Barh, A. Bjarnasson, Þ.Þ. Björnsson, I. Blazquez de Paz, M. Donofrio, P.C. Garcia Galindo, J. Geiger, A.F. Guðmundsson, G.A. Guðmundsson, G. Halldórsson, H. Haraldsson, M. Holzapfel, E. Igersheim, F.L. Jóhannsson, F. Jónasson, F. Karlsson, D. Lange, V. Mader, K.P. Magnússon, K. Pelletier, N. de Pelsmaeker, K. Ries, A. Schlaich, I. Schwenkmeier, Ó.G. Sigurðardóttir, A.Ö. Snæþórsson, H.W. Stefánsson, S. Thirgood, D. Zeugler, S.Þ. Þórarinsdóttir, Þ.L. Þórarinsson, and V. Moos. We thank S. Þorsteinsdóttir, A.P. Møller, and two anonymous reviewers for their valuable comments on this manuscript, and A. Galkin, A.V. Bochkov, R.L. Palma, R.E. Lewis, R. Stensvold, S.V. Mironov for describing or confirming identifications of parasites. This study complies with the current laws of Iceland.

Conflict of interest

None.

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Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2014

Authors and Affiliations

  • Ute Stenkewitz
    • 1
    • 2
    • 3
  • Ólafur K. Nielsen
    • 2
  • Karl Skírnisson
    • 3
  • Gunnar Stefánsson
    • 4
  1. 1.Faculty of Life and Environmental SciencesUniversity of IcelandReykjavíkIceland
  2. 2.Icelandic Institute of Natural HistoryGarðabærIceland
  3. 3.Institute for Experimental PathologyUniversity of Iceland, KeldurReykjavíkIceland
  4. 4.Science InstituteUniversity of IcelandReykjavíkIceland

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