Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Published:
Journal of Ornithology Aims and scope Submit manuscript

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.

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Acquarone C, Cucco M, Malacarne G (2002) Annual variation of immune condition in the Hooded Crow (Corvus corone cornix). J Ornithol 143:351–355

    Article  Google Scholar 

  • Akbar Z, Qureshi AS, Rahman S (2012) Effects of seasonal variation in different reproductive phases on the cellular response of bursa and testes in Japanese Quail (Coturnix japonica). Pak Vet J 32:525–529

    Google Scholar 

  • Anderson RM, May RM (1979) Biology of infectious diseases: part I. Nature 280:361–367

    Article  CAS  PubMed  Google Scholar 

  • Baumel JJ (1979) Nomina anatomica avium. Academic Press, London

    Google Scholar 

  • Blanco G, de la Puente J, Corroto M, Baz A, Colás J (2001) Condition-dependent immune defense in the Magpie: how important is ectoparasitism? Biol J Linn Soc 72:279–286

    Article  Google Scholar 

  • Boehm T, Hess I, Swann JB (2012) Evolution of lymphoid tissue. Trends Immunol 33:315–321

    Article  CAS  PubMed  Google Scholar 

  • Brown CR, Brown MB (2002) Spleen volume varies with colony size and parasite load in a colonial bird. Proc R Soc Lond B7(269):1367–1373

    Article  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

    Article  CAS  PubMed  Google Scholar 

  • Bush AO, Fernández JC, Esch GW, Seed JR (2001) Parasitism: the diversity and ecology of animal parasites. Cambridge University Press, Cambridge

    Google Scholar 

  • Cary JR, Keith LB (1979) Reproductive change in the 10-year cycle of Snowshoe Hares. Can J Zool 57:375–390

    Article  Google Scholar 

  • Clayton DH, Adams RJ, Bush SE (2008) Phthiraptera: the chewing lice. In: Atkinson CT, Thomas NJ, Hunter DB (eds) Parasitic diseases of wild birds. Wiley, Ames, pp 515–526

    Google Scholar 

  • Clayton DH, Koop JAH, Harbison CW, Moyer BR, Bush SE (2010) How birds combat ectoparasites. Open Ornithol J 3:41–71

    Article  Google Scholar 

  • Cooper MD, Peterson RDA, South MA, Good RA (1966) The functions of the thymus system and the bursa system in the chicken. J Exp Med 123:75–102

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cowan KM, Shutler D, Herman TB, Stewart DT (2009) Splenic mass of Masked Shrew Sorex cinereus in relation to body mass, sex, age, day of year and bladder nematode Liniscus (=Capillaria) maseri infection. J Parasitol 95:228–230

    Article  PubMed  Google Scholar 

  • Derting TL, Compton S (2003) Immune response not immune maintenance is energetically costly in wild White-footed Mice Peromyscus leucopus. Physiol Biochem Zool 76:744–752

    Article  PubMed  Google Scholar 

  • Forbes MR, Alisauskas RT, McLaughlin JD, Cuddington KM (1999) Explaining co-occurrence among helminth species of Lesser Snow Geese Chen caerulescens during their winter and spring migration. Oecologia 120:613–620

    Article  Google Scholar 

  • Garðarsson A (1988) Cyclic population changes and some related events in Rock Ptarmigan in Iceland. In: Bergerud AT, Gratson MW (eds) Adaptive strategies and population ecology of northern grouse. University of Minnesota, Minneapolis, pp 300–329

    Google Scholar 

  • Glick B (1956) Normal growth of the bursa of Fabricius in chickens. Poult Sci 35:843–851

    Article  Google Scholar 

  • Glick B (1994) The bursa of Fabricius: the evolution of a discovery. Poult Sci 73:979–983

    Article  CAS  PubMed  Google Scholar 

  • Glick B, Chang TS, Jaap RG (1956) The bursa of Fabricius and antibody production. Poult Sci 35:224–225

    Article  Google Scholar 

  • Grenfell BT, Chappell LH (1995) Ecology of wildlife host–parasite interactions. Cambridge University Press, Cambridge

    Google Scholar 

  • Hahn DC, Smith GW (2011) Life history trade-offs between longevity and immunity in the parasitic brown-headed cowbird? Open Evol J 5:8–13

    Article  Google Scholar 

  • Holder K, Montgomerie R (1993) Rock Ptarmigan Lagopus mutus. In: Poole A, Gill F (eds) The birds of North America No 51. Academy of Natural Sciences Philadelphia and American Ornithologists’ Union, Washington DC

    Google Scholar 

  • Holmstad PR, Hudson PJ, Skorping A (2005) The influence of a parasite community on the dynamics of a host population: a longitudinal study on Willow Ptarmigan and their parasites. Oikos 111:337–391

    Article  Google Scholar 

  • Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258

    Article  CAS  PubMed  Google Scholar 

  • Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (2001) The ecology of wildlife diseases. Oxford University Press, New York

    Google Scholar 

  • John JL (1994) The avian spleen: a neglected organ. Q Rev Biol 69:327–351

    Article  CAS  PubMed  Google Scholar 

  • Klein SL (2004) Hormonal and immunological differences mediating sex differences in parasite infection. Parasite Immunol 26:247–264

    Article  CAS  PubMed  Google Scholar 

  • Krebs CJ (1962) The Lemming cycle at Baker Lake N.W.T. during 1959–61. PhD thesis. University of British Columbia, Vancouver

  • Magnússon KG, Brynjarsdóttir J, Nielsen ÓK (2004) Population cycles in Rock Ptarmigan Lagopus muta: modelling and parameter estimation. Technical report RH-19-2004. Science Institute University of Iceland, Reykjavík

  • Margolis L, Esch GW, Holmes JC, Kuris AM, Schad GA (1982) The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). J Parasitol 68:131–133

    Article  Google Scholar 

  • May RM, Anderson RM (1979) Biology of infectious diseases: part II. Nature 280:455–461

    Article  CAS  PubMed  Google Scholar 

  • Møller AP, Erritzøe J (1996) Parasite virulence and host immune defense: host immune reponse is related to nest reuse in birds. Evolution 50:2066–2072

    Article  Google Scholar 

  • Møller AP, Rózsa L (2005) Parasite biodiversity and host defenses: chewing lice and immune response of their avian hosts. Oecologia 142:169–176

    Article  PubMed  Google Scholar 

  • Møller AP, Saino N (2004) Immune response and survival. Oikos 104:299–304

    Article  Google Scholar 

  • Møller AP, Kimball RT, Erritzøe J (1996) Sexual ornamentation condition and immune defense in the House Sparrow Passer domesticus. Behav Ecol Sociobiol 39:317–322

    Article  Google Scholar 

  • Møller AP, Christe P, Erritzøe J, Mavarez J (1998a) Condition disease and immune defense. Oikos 83:301–306

    Article  Google Scholar 

  • Møller AP, Sorci G, Erritzøe J (1998b) Sexual dimorphism in immune defense. Am Nat 152:605–619

    Article  PubMed  Google Scholar 

  • Møller AP, Erritzøe J, Saino N (2003) Seasonal changes in immune response and parasite impact on hosts. Am Nat 161:657–671

    Article  PubMed  Google Scholar 

  • Montgomerie R, Holder K (2008) Rock Ptarmigan Lagopus muta. In: Poole A (ed) The birds of North America. Online Cornell Laboratory of Ornithology, Ithaca. Available at: http://bna.birds.cornell.edu.bnaproxy.birds.cornell.edu/bna/species/051

  • Morand S, Poulin R (2000) Nematode parasite species richness and the evolution of spleen size in birds. Can J Zool 78:1356–1360

    Article  Google Scholar 

  • Mougeot F, Redpath SM (2004) Sexual ornamentation relates to immune function in male Red Grouse Lagopus lagopus scoticus. J Avian Biol 35:425–433

    Article  Google Scholar 

  • Moyer BR, Rock A, Clayton DH (2003) Experimental test of the importance of preen oil in Rock Doves (Columbia livia). Auk 120:490–496

    Article  Google Scholar 

  • Nielsen ÓK (1996) Rock Ptarmigan censuses in northeast Iceland (In Icelandic with English summary). Náttúrufræðingurinn 65:137–151

    Google Scholar 

  • Nielsen ÓK, Pétursson G (1995) Population fluctuations of Gyrfalcon and Rock Ptarmigan: analysis of export figures from Iceland. Wildl Biol 1:65–71

    Google Scholar 

  • Ottinger MA, Lavoie E (2007) Neuroendocrine and immune characteristics of aging in avian species. Cytogenet Genome Res 117:352–357

    Article  CAS  PubMed  Google Scholar 

  • Powers LV (2000a) The avian spleen: anatomy physiology and diagnosis. Comp Cont Educ Pract 22:838–843

    Google Scholar 

  • Powers LV (2000b) Diseases of the avian spleen. Comp Cont Educ Pract 22:925–933

    Google Scholar 

  • Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton HD (2003) The chewing lice: world checklist and biological overview. Illinois Natural History Survey Special Publication 24. Illinois Natural History Survey, Champaign

    Google Scholar 

  • R Core Team (2011) R: a language and environment for statistical computing r foundation for statistical computing. Available at: http://www.R-project.org

  • Schulte-Hostedde AI, Elsasser SC (2011) Spleen mass body condition and parasite load in male American Mink Neovison vison. J Mammal 92:221–226

    Article  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  CAS  PubMed  Google Scholar 

  • Shutler D, Alisauskas RT, McLaughlin JD (1999) Mass dynamics of the spleen and other organs in geese: measures of immune relationships to helminths? Can J Zool 77:351–359

    Article  Google Scholar 

  • Skírnisson K, Þórarinsdóttir ST, Nielsen ÓK (2012) The parasite fauna of Rock Ptarmigan Lagopus muta in Iceland: prevalence intensity and distribution within the host population. Comp Parasitol 79:44–55

    Article  Google Scholar 

  • Sturkie PD, Whittow GC (1999) Sturkie’s Avian Physiology, 5th edn. Academic Press, London

    Google Scholar 

  • Þórarinsdóttir ST, Skírnisson K, Nielsen ÓK (2010) Seasonal changes in endoparasites of Rock Ptarmigan (In Icelandic with English summary). Náttúrufræðingurinn 80:33–40

    Google Scholar 

  • Vicente J, Pérez-Rodríguez L, Gortazar C (2007) Sex age spleen size and kidney fat of Red Deer relative to infection intensities of the lungworm Elaphostrongylus cervi. Naturwissenschaften 94:581–587

    Article  CAS  PubMed  Google Scholar 

  • Watson A, Moss R (2008) Grouse. Collins, London

    Google Scholar 

  • Weeden RB, Watson A (1967) Determining the age of Rock Ptarmigan in Alaska and Scotland. J Wildl Manage 31:825–826

    Article  Google Scholar 

  • Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1024

    Article  CAS  PubMed  Google Scholar 

  • Zuk M, Stoehr AM (2002) Immune defense and host life history. Am Nat 160[Suppl 4]:S9–S22

    Article  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Faculty of Life and Environmental Sciences, University of Iceland, Sturlugata 7, Askja Building, 101, Reykjavík, Iceland

    Ute Stenkewitz

  2. Icelandic Institute of Natural History, Urriðaholtsstræti 6-8, 210, Garðabær, Iceland

    Ute Stenkewitz & Ólafur K. Nielsen

  3. Institute for Experimental Pathology, University of Iceland, Keldur, Keldnavegur 3, 112, Reykjavík, Iceland

    Ute Stenkewitz & Karl Skírnisson

  4. Science Institute, University of Iceland, Dunhaga 5, 107, Reykjavík, Iceland

    Gunnar Stefánsson

Authors
  1. Ute Stenkewitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ólafur K. Nielsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karl Skírnisson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gunnar Stefánsson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ute Stenkewitz.

Additional information

Communicated by K. C. Klasing.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stenkewitz, U., Nielsen, Ó.K., Skírnisson, K. et al. The relationship between parasites and spleen and bursa mass in the Icelandic Rock Ptarmigan Lagopus muta . J Ornithol 156, 429–440 (2015). https://doi.org/10.1007/s10336-014-1141-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10336-014-1141-x

Keywords

Search

Navigation