, Volume 176, Issue 3, pp 729–737 | Cite as

The ecology of host immune responses to chronic avian haemosporidian infection

  • Vincenzo A. Ellis
  • Melanie R. Kunkel
  • Robert E. Ricklefs
Physiological ecology - Original research


Host responses to parasitism in the wild are often studied in the context of single host–parasite systems, which provide little insight into the ecological dynamics of host–parasite interactions within a community. Here we characterized immune system responses to mostly low-intensity, chronic infection by haemosporidian parasites in a sample of 424 individuals of 22 avian host species from the same local assemblage in the Missouri Ozarks. Two types of white blood cells (heterophils and lymphocytes) were elevated in infected individuals across species, as was the acute-phase protein haptoglobin, which is associated with inflammatory immune responses. Linear discriminant analysis indicated that individuals infected by haemosporidians occupied a subset of the overall white blood cell multivariate space that was also occupied by uninfected individuals, suggesting that these latter individuals might have harbored other pathogens or that parasites more readily infect individuals with a specific white blood cell profile. DNA sequence-defined lineages of haemosporidian parasites were sparsely distributed across the assemblage of hosts. In one well-sampled host species, the red-eyed vireo (Vireo olivaceus), heterophils were significantly elevated in individuals infected with one but not another of two common parasite lineages. Another well-sampled host, the yellow-breasted chat (Icteria virens), exhibited no differences in immune response to different haemosporidian lineages. Our results indicate that while immune responses to infection may be generalized across host species, parasite-specific immune responses may also occur.


Avian malaria Ecoimmunology Haemosporida Haptoglobin Leukocytes 



Alicia Burke, Kristen Bird, Elyse Coffey, Linlin Meng, and William Burke assisted with fieldwork and Eloisa Sari provided advice regarding lab procedures and insightful comments on an earlier version of the manuscript; Iris Levin, Matthew Medeiros, Eliot Miller, Michael Collins, Alix Matthews, Alison Hanson, Jackson Roberts and an anonymous reviewer also provided helpful comments. The Whitney Harris World Ecology Center at UMSL funded this project through the Leo and Kay Drey Scholarship (V. A. E.). The Missouri Department of Conservation provided housing and logistical support. Logistics were also facilitated by John Faaborg. Laboratory funds were provided by the Curators of the University of Missouri (R. E. R.). All sampling occurred under appropriate federal and state permits and in accordance with the UMSL IACUC.

Supplementary material

442_2014_3048_MOESM1_ESM.doc (314 kb)
Supplementary material 1 (DOC 314 kb)


  1. Apanius V, Yorinks N, Bermingham E, Ricklefs RE (2000) Island and taxon effects in parasitism and resistance of lesser Antillean birds. Ecology 81:1959–1969CrossRefGoogle Scholar
  2. Atkinson CT, Dusek RJ, Woods KL, Iko WM (2000) Pathogenicity of avian malaria in experimentally-infected Hawaii amakihi. J Wildl Dis 36:197–204PubMedCrossRefGoogle Scholar
  3. Atkinson CT, Dusek RJ, Lease JK (2001) Serological responses and immunity to superinfection with avian malaria in experimentally-infected Hawaii amakihi. J Wildl Dis 37:20–27PubMedCrossRefGoogle Scholar
  4. Bensch S, Hellgren O, Perez-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9:1353–1358PubMedCrossRefGoogle Scholar
  5. Booth CE, Elliott PF (2003) Hematological responses to hematozoa in North American and Neotropical songbirds. Comp Physiol Biochem Part A 133:451–467CrossRefGoogle Scholar
  6. Buckland ST, Burnham KP, Augustin NH (1997) Model selection: an integral part of inference. Biometrics 53:603–618CrossRefGoogle Scholar
  7. Calcagno V (2012) glmulti: model selection and multimodel inference made easy. R package version 1.0.6.
  8. Cellier-Holzem E, Esparza-Salas R, Garnier S, Sorci G (2010) Effect of repeated exposure to Plasmodium relictum (lineage SGS1) on infection dynamics in domestic canaries. Int J Parasitol 40:1447–1453PubMedCrossRefGoogle Scholar
  9. Clark P, Boardman W, Raidal S (2009) Atlas of clinical avian hematology. Blackwell, OxfordGoogle Scholar
  10. Dale S, Kruszewicz A, Slagsvold T (1996) Effects of blood parasites on sexual and natural selection in the pied flycatcher. J Zool 238:373–393CrossRefGoogle Scholar
  11. Day FP, Monk CD (1974) Vegetation patterns on a southern Appalachian watershed. Ecology 55:1064–1074CrossRefGoogle Scholar
  12. Dunbar MR, Tornquist S, Giordano MR (2003) Blood parasites in sage-grouse from Nevada and Oregon. J Wildl Dis 39:203–208PubMedCrossRefGoogle Scholar
  13. Fallon SM, Ricklefs RE (2008) Parasitemia in PCR-detected Plasmodium and Haemoproteus infections in birds. J Avian Biol 39:514–522CrossRefGoogle Scholar
  14. Fecchio A, Lima MR, Svensson-Coelho M, Marini MA, Ricklefs RE (2013) Structure and organization of an avian haemosporidian assemblage in a Neotropical savanna in Brazil. Parasitology 140:181–192PubMedCrossRefGoogle Scholar
  15. Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121CrossRefGoogle Scholar
  16. Garvin MC, Homer BL, Greiner EC (2003) Pathogenicity of Haemoproteus danilewskyi, Kruse, 1890, in blue jays (Cyanocitta cristata). J Wildl Dis 39:161–169PubMedCrossRefGoogle Scholar
  17. Horrocks NPC, Tieleman BI, Matson KD (2011) A simple assay for measurement of ovotransferrin—a marker of inflammation and infection in birds. Methods Ecol Evol 2:518–526CrossRefGoogle Scholar
  18. Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258PubMedCrossRefGoogle Scholar
  19. Jarra W, Brown KN (1985) Protective immunity to malaria: studies with cloned lines of Plasmodium chabaudi and P. berghei in CBA/Ca mice. I. The effectiveness and inter- and intra-species specificity of immunity induced by infection. Parasite Immunol 7:595–606PubMedCrossRefGoogle Scholar
  20. Knowles SCL, Palinauskas V, Sheldon BC (2010) Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. J Evol Biol 23:557–569PubMedCrossRefGoogle Scholar
  21. Kogut MH, Iqbal M, He H, Philbin V, Kaiser P, Smith A (2005) Expression and function of Toll-like receptors in chicken heterophils. Dev Comp Immunol 29:791–807PubMedCrossRefGoogle Scholar
  22. Lafferty KD, Kuris AM (2009) Parasitic castration: the evolution and ecology of body snatchers. Trends Parasitol 25:564–572PubMedCrossRefGoogle Scholar
  23. Legendre P, Legendre L (2012) Numerical ecology, 3rd English edn. Elsevier, OxfordGoogle Scholar
  24. Longmire JL, Maltbie M, Baker RJ (1997) Use of “lysis buffer” in DNA isolation and its implication for museum collections. Occas Pap Mus Texas Tech Univ 163:1–4Google Scholar
  25. Marzal A, de Lope F, Navarro C, Moller AP (2005) Malaria parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142:541–545PubMedCrossRefGoogle Scholar
  26. Matson KD, Cohen AA, Klasing KC, Ricklefs RE, Scheuerlein A (2006) No simple answers for ecological immunology: relationships among immune indices at the individual level break down at the species level in waterfowl. Proc R Soc Lond B 273:815–822CrossRefGoogle Scholar
  27. Merino S, Moreno J, Sanz JJ, Arriero E (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proc R Soc Lond B 267:2507–2510CrossRefGoogle Scholar
  28. Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19–26CrossRefGoogle Scholar
  29. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2012) Vegan: community ecology package. R package version 2.0-4.
  30. Ots I, Murumagi A, Horak P (1998) Haematological health state indices of reproducing great tits: methodology and sources of natural variation. Funct Ecol 12:700–707CrossRefGoogle Scholar
  31. Palinauskas V, Valkiūnas G, Bolshakov CV, Bensch S (2008) Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Exp Parasitol 120:372–380PubMedCrossRefGoogle Scholar
  32. Palinauskas V, Valkiūnas G, Krizanauskiene A, Bensch S, Bolshakov CV (2009) Plasmodium relictum (lineage P-SGS1): further observation of effects on experimentally infected passeriform birds, with remarks on treatment with Malarone. Exp Parasitol 123:134–139PubMedCrossRefGoogle Scholar
  33. Palinauskas V, Valkiūnas G, Bolshakov CV, Bensch S (2011) Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): the effects of the co-infection on experimentally infected passerine birds. Exp Parasitol 127:527–533PubMedCrossRefGoogle Scholar
  34. Pyle P (1997) Identification guide to North American birds. Part I. Slate Creek Press, BolinasGoogle Scholar
  35. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0.
  36. Raj GD, Jones RC (1997) Infectious bronchitis virus: immunopathogenesis of infection in the chicken. Avian Pathol 26:677–706PubMedCrossRefGoogle Scholar
  37. Ricklefs RE, Sheldon KS (2007) Malaria prevalence and white-blood-cell response to infection in a tropical and in a temperate thrush. Auk 124:1254–1266CrossRefGoogle Scholar
  38. Ricklefs RE, Swanson BL, Fallon SM, Martinez-Abrain A, Scheuerlein A, Gray J, Latta SC (2005) Community relationships of avian malaria parasites in southern Missouri. Ecol Monogr 75:543–559CrossRefGoogle Scholar
  39. Schall JJ, Vogt SP (1993) Distribution of malaria in Anolis lizards of the Luquillo Forest, Puerto Rico: implications for host community ecology. Biotropica 25:229–235CrossRefGoogle Scholar
  40. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 75:758–771CrossRefGoogle Scholar
  41. Suarez DL, Schultz-Cherry S (2000) Immunology of avian influenza virus: a review. Dev Comp Immunol 24:269–283PubMedCrossRefGoogle Scholar
  42. Svensson LME, Ricklefs RE (2009) Low diversity and high intra-island variation in prevalence of avian Haemoproteus parasites on Barbados, Lesser Antilles. Parasitology 136:1121–1131PubMedCrossRefGoogle Scholar
  43. Szymanski MM, Lovette IJ (2005) High lineage diversity and host sharing of malarial parasites in a local avian assemblage. J Parasitol 91:768–774PubMedCrossRefGoogle Scholar
  44. Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC, Boca RatonGoogle Scholar
  45. van Riper CIII, van Riper SG, Goff ML, Laird M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr 56:327–344CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Vincenzo A. Ellis
    • 1
  • Melanie R. Kunkel
    • 1
  • Robert E. Ricklefs
    • 1
  1. 1.Department of BiologyUniversity of Missouri-St LouisSt LouisUSA

Personalised recommendations