Skip to main content

Advertisement

SpringerLink
Log in

Parasite biodiversity and host defenses: chewing lice and immune response of their avian hosts

  • Ecophysiology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Antagonistic host-parasite interactions lead to coevolution of host defenses and parasite virulence. Such adaptation by parasites to host defenses may occur to the detriment of the ability of parasites to exploit alternative hosts, causing parasite specialization and speciation. We investigated the relationship between level of anti-parasite defense in hosts and taxonomic richness of two chewing louse suborders (Phthiraptera: Amblycera, Ischnocera) on birds. While Amblyceran lice tend to occur in contact with host skin, feed on host skin and chew emerging tips of developing feathers to obtain blood, Ischnoceran lice live on feathers and feed on the non-living keratin of feather barbules. We hypothesized that Amblyceran abundance and richness would have evolved in response to interaction with the immune system of the host, while Ischnoceran taxonomic richness would have evolved independently of immunological constraints. In an interspecific comparison, the abundance of Ischnocerans was positively related to host body size, while host body mass and Ischnoceran taxonomic richness accounted for the abundance of Amblycerans. Amblyceran taxonomic richness was predicted by the intensity of T-cell mediated immune response of nestling hosts, while the T-cell response of adults had no significant effect. In contrast, Ischnoceran taxonomic richness was not predicted by host T-cell responses. These results suggest that the taxonomic richness of different parasite taxa is influenced by different host defenses, and they are consistent with the hypothesis that increasing host allocation to immune defense increases Amblyceran biodiversity.

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

  • Abbas AK, Lichtman AH, Pober JS (1994) Cellular and molecular immunology. Saunders, Philadelphia

    Google Scholar 

  • Badyaev AV (1997) Altitudinal variation in sexual dimorphism: a new pattern and alternative hypotheses. Behav Ecol 8:675–690

    Google Scholar 

  • Balát F (1966) Federlinge tschechoslowakischer Ufernschwalben. Ang Parasitol 7:244–248

    Google Scholar 

  • Barbosa A, Merino S, de Lope F, Møller AP (2002) Effects of feather lice on flight behavior of male barn swallows (Hirundo rustica). Auk 119:213–216

    Google Scholar 

  • Barker FK, Barrowclough GF, Groth JG (2001) A phylogenetic hypothesis for passerine birds: taxonomic and biogeographic implications of an analysis of nuclear DNA sequence data. Proc R Soc Lond B 269:295–308

    Article  Google Scholar 

  • Barker SC, Whiting M, Johnson KP, Murrell A (2002) Phylogeny of the lice (Insecta: Phthiraptera) inferred from small subunit rRNA. Zool Scripta (in press)

  • Barlett CM (1993) Lice (Amblycera and Ischnocera) as vectors of Eulimdana spp. (Nematoda: Filarioidea) in Charadriiform birds and the necessity of short reproductive periods in adult worms. J Parasitol 79:85–91

    Google Scholar 

  • Blagoveshchensky DI (1951) Mallophaga of Tadzhikistan. Parazit Sbornyk 13:272–327

    Google Scholar 

  • Blondel J, Catzeflis F, Perret P (1996) Molecular phylogeny and the historical biogeography of the warblers of the genus Sylvia (Aves). J evol Biol 9:871–891

    Google Scholar 

  • Blount JD, Houston DC, Møller AP, Wright J (2003) Multiple measures reveal complex patterns in immune defence: a comparative case study of scavenging and non-scavenging birds. Oikos 102:340–350

    Article  Google Scholar 

  • Booth DT, Clayton DH, Block BA (1993) Experimental demonstration of the energetic cost of parasitism in free-ranging hosts. Proc R Soc Lond B 253:125–129

    Google Scholar 

  • Brown CR, Brown MB, Rannala B (1995) Ectoparasites reduce long-term survivorship of their avian host. Proc R Soc Lond B 262:313–319

    Google Scholar 

  • Burley N, Tidemann SC, Halupka K (1991) Bill colour and parasite levels of zebra finches. In: Loye JE, Zuk M (eds) Bird–parasite interactions. Oxford University Press, Oxford, pp 359–376

    Google Scholar 

  • Casto JM, Nolan V Jr, Ketterson ED (2001) Steroid hormones and immune function: Experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). Am Nat 157:408–420

    Article  Google Scholar 

  • Cerny V (1970) Die parasitischen Arthropoden der synanthropen Taubenvögel einer Großstadt. Angew Parasitol 11:244–248

    Google Scholar 

  • Cibois A, Pasquet E (1999) Molecular analysis of the phylogeny of 11 genera of the Corvidae. Ibis 141:297–306

    Google Scholar 

  • Clay T (1964) Geographical distribution of the Mallophaga (Insecta). Bull Br Ornithol Cl 84:14–16

    Google Scholar 

  • Clayton DH (1990) Mate choice in experimentally parasitized rock doves, lousy males lose. Am Zool 30:251–262

    Google Scholar 

  • Clayton DH (1991) Coevolution of avian grooming and ectoparasite avoidance. In: Loye JE, Zuk M (eds) Bird–parasite interactions. Oxford University Press, Oxford, pp 258–289

    Google Scholar 

  • Clayton DH, Tompkins DM (1994) Ectoparasite virulence is linked to mode of transmission. Proc R Soc Lond B 256:211–217

    CAS  PubMed  Google Scholar 

  • Clayton DH, Tompkins DM (1995) Comparative effects of mites and lice on the reproductive success of rock doves (Columba livia). Parasitology 110:195–206

    PubMed  Google Scholar 

  • Clayton DH, Walther BA (2001) Influence of host ecology and morphology on the diversity of Neotropical bird lice. Oikos 94:455–467

    Google Scholar 

  • Clayton DH, Gregory RD, Price RD (1992) Comparative ecology of Neotropical bird lice (Insecta: Phthiraptera). J Anim Ecol 61:781–795

    Google Scholar 

  • Clayton DH, Lee PLM, Tompkins DM, Brodie ED (1999) Reciprocal natural selection on host-parasite phenotypes. Am Nat 154:261–270

    Article  PubMed  Google Scholar 

  • Cohen S, Greenwood MT, Fowler JA (1991) The louse Trinoton anserinum (Amblycera: Phthiraptera), an intermediate host of Sarconema eurycerca (Filarioidea: Nematoda), a heartworm of swans. Med Vet Entomol 5:101–110

    CAS  PubMed  Google Scholar 

  • Dietert RR, Golemboski KA, Kwak H, Ha R, Miller TE (1996) Environment-immunity interactions. In: Davison TF, Morris TR, Payne LN (eds) Poultry immunology. Carfax, Abingdon, pp 343–356

    Google Scholar 

  • Dritschilo W, Connell H, Nafus D, O’Connor B (1975) Insular biogeography, of mice and mites. Science 190:467–469

    CAS  PubMed  Google Scholar 

  • Dunning JB (1993) CRC handbook of avian body masses. CRC Press, Boca Raton

    Google Scholar 

  • Ebert D, Hottinger JW, Pujanen VI (2001) Temporal and spatial dynamics of parasite richness in a Daphnia metapopulation. Ecology 82:2417–2424

    Google Scholar 

  • Ewenson EL, Zann RA, Flannery GR (2001) Body condition and immune response in wild zebra finches: effects of capture, confinement and captive-rearing. Naturwissenschaften 88:391–394

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Fowler JA, Williams LR (1985) Population dynamics of Mallophaga and Acari on reed buntings occupying a communal winter roost. Ecol Entomol 10:377–383

    Google Scholar 

  • Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Am Nat 141:18–32

    Google Scholar 

  • Goto N, Kodama H, Okada K, Fujimoto Y (1978) Suppression of phytohaemagglutinin skin response in thymectomized chickens. Poult Sci 52:246–250

    Google Scholar 

  • Gregory RD (1990) Parasites and host geographic range, patterns and artefacts. Funct Ecol 4:645–654

    Google Scholar 

  • Gregory RD (1997) Comparative studies of host-parasite communities. In: Clayton DH, Moore J (eds) Host–parasite evolution: general principles and avian models. Oxford University Press, Oxford, pp 198–211

    Google Scholar 

  • Hackmann W (1994) Mallofager (Phthiraptera, Mallophaga) som parasiterar pa Finlands fågelarter. Mem Soc Fauna Flora Fenn 70:35–70

    Google Scholar 

  • Hart BJ (1990) Behavioral adaptations to pathogens and parasites: five strategies. Neurosci Biobehav Rev 14:273–294

    CAS  PubMed  Google Scholar 

  • Hart BJ (1997) Behavioural defence. In: Clayton DH, Moore J (eds) Host–parasite evolution: general principles and avian models. Oxford University Press, Oxford, pp 59–77

    Google Scholar 

  • Hoi-Leitner M, Romero-Pujante M, Hoi H, Pavlova A (2001) Food availability and imune capacity in serin (Serinus serinus) nestlings. Behav Ecol Sociobiol 49:333–339

    Article  Google Scholar 

  • Johnsen A, Andersen V, Sunding C, Lifjeld JT (2000) Female blue throats enhance offspring immunocompetence through extra-pair copulations. Nature 406:296–299

    Article  CAS  PubMed  Google Scholar 

  • Johnson KP, Clayton DH (2003) The biology, ecology, and evolution of chewing lice. In: Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton DH (eds) The chewing lice: World checklist and biological overview. INHS Special Publication 24. Illinois Natural History Survey, Illinois

  • Johnson KP, Whiting MF (2002) Multiple genes and monophyly of Ischnocera (Insecta: Phthiraptera). Mol Phylogenet Evol 22:101–110

    Article  CAS  PubMed  Google Scholar 

  • Klein J (1990) Immunology. Oxford University Press, Oxford

    Google Scholar 

  • Kose M, Møller AP (1999) Sexual selection, feather breakage and parasites: the importance of white spots in the tail of the barn swallow. Behav Ecol Sociobiol 45:430–436

    Article  Google Scholar 

  • Kose M, Mänd R, Møller AP (1999) Sexual selection for white tail spots in the barn swallow in relation to habitat choice by feather lice. Anim Behav 58:1201–1205

    Article  PubMed  Google Scholar 

  • Lee PLM, Clayton DH (1995) Population biology of swift (Apus apus) ectoparasites in relation to host reproductive success. Ecol Entomol 20:43–50

    Google Scholar 

  • Leisler B, Heidrich P, Schulze-Hagen K, Wink W (1997) Taxonomy and phylogeny of reed warblers (genus Acrocephalus) based on mtDNA sequences and morphology. J Orn 138:469–496

    Google Scholar 

  • Martin TE, Clobert J (1996) Nest predation and avian life history evolution in Europe versus North America: a possible role for humans? Am Nat 147:1028–1046

    Article  Google Scholar 

  • Martin TE, Møller AP, Merino S, Clobert J (2001) Does clutch size evolve in response to parasites and immunocompetence? Proc Natl Acad Sci U S A 98:2071–2076

    Article  CAS  PubMed  Google Scholar 

  • McCorkle F Jr, Olah I, Glick B (1980) The morphology of the phytohemagglutinin-induced cell response in the chicken wattle. Poult Sci 59:616–623

    Google Scholar 

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

    Article  Google Scholar 

  • Møller AP, Merino S, Brown CR, Robertson RJ (2001) Immune defense and host sociality: a comparative study of swallows and martins. Am Nat 158:136–145

    Article  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 

  • National Research Council (1992) Biologic markers in immunotoxicology. National Academy Press, Washington

  • Parmentier HK, Schrama JW, Meijer F, Nieuwland MGB (1993) Cutaneous hypersensitivity responses in chickens divergently selected for antibody responses to sheep red blood cells. Poult Sci 72:1679–1692

    CAS  PubMed  Google Scholar 

  • Parmentier HK, de Vries Reilingh G, Nieuwland MGB (1998) Kinetic immunohistochemical characteristic of mitogen-induced cutaneous hypersensitivity responses in chickens divergently selected for antibody responsiveness. Vet Immunol Immunopathol 66:367–376

    Article  CAS  PubMed  Google Scholar 

  • Paterson AM, Palma RL, Gray ER (1999) How frequently do avian lice missing the boat? Implications for coevolutionary studies. Syst Biol 48:214–223

    Article  Google Scholar 

  • Price PV (1980) Evolutionary biology of parasites. Princeton University Press, Princeton

    Google Scholar 

  • Price PD, Hellenthal RA, Palma RL (2003) World checklist of chewing lice with host associations and keys to families and genera. In: Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton DH (eds) The chewing lice: World checklist and biological overview. INHS Special publication 24. Illinois Natural History Survey, IL

  • Purvis A, Rambaut A (1995) Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analyzing comparative data. Comp Appl Biosci 11:247–251

    CAS  PubMed  Google Scholar 

  • Rothschild M, Clay T (1952) Fleas, flukes and cuckoos. A study of bird parasites. Collins, London

    Google Scholar 

  • Rózsa L (1990) The ectoparasite fauna of feral pigeon populations in Hungary. Parasitol Hung 23:115–119

    Google Scholar 

  • Rózsa L (1993a) Speciation patterns of ectoparasites and “straggling” lice. Int J Parasitol 23:859–864

    Article  PubMed  Google Scholar 

  • Rózsa L (1993b) An experimental test of the site-specificity of preening to control lice in feral pigeons. J Parasitol 79:968–970

    PubMed  Google Scholar 

  • Rózsa L, Rékási J, Rieczigel J (1996) Relationship of host coloniality to the population ecology of avian lice (Insecta: Phthiraptera). J Anim Ecol 65:242–248

    Google Scholar 

  • Rózsa L, Reiczigel J, Majoros G (2000) Quantifying parasites in samples of hosts. J Parasitol 86:228–232

    PubMed  Google Scholar 

  • Seibold I, Helbig AJ (1995) Evolutionary history of New and Old World vultures inferred from nucleotide sequences of the mitochondrial cytochrome b gene. Phil Trans R Soc Lond B 350:163–178

    CAS  Google Scholar 

  • Sheldon FH, Winkler DW (1993) Intergeneric phylogenetic relationships of swallows estimated by DNA–DNA hybridization. Auk 110:798–824

    Google Scholar 

  • Shumilo RP, Lunkashu MI (1972) Mallophaga from wild terrestrial birds of the Dnester-Prut region. Moldavian Academy of Sciences, Kishinau

    Google Scholar 

  • Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds. Yale University Press, New Haven

    Google Scholar 

  • Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572

    Article  Google Scholar 

  • Soler JJ, Møller AP, Soler M, Martínez JG (1999) Interactions between a brood parasite and its host in relation to parasitism and immune defence. Evol Ecol Res 1:189–210

    Google Scholar 

  • Strong DR, McCoy ED, Rey R (1977) Time and the number of herbivore species, the pests of sugarcane. Ecology 58:167–175

    Google Scholar 

  • Tella JL, Botolotti GR, Dawson RD, Forero MG (2000) The T-cell mediated immune response and return rate of fledgling American kestrels are positively correlated with parental clutch size. Proc R Soc Lond B 267:891–895

    Article  CAS  PubMed  Google Scholar 

  • Tella JL, Scheuerlein A, Ricklefs RE (2002) Is cell-mediated immunity related to the evolution of life-history strategies in birds? Proc R Soc Lond B 269:1059–1066

    Article  PubMed  Google Scholar 

  • Thompson JN (1994) The coevolutionary process. University of Chicago Press, Chicago

    Google Scholar 

  • Wakelin D (1996) Immunology to parasites. Cambridge University Press, Cambridge

    Google Scholar 

  • Walther BA, Cotgreave P, Price RD, Gregory RD, Clayton DH (1995) Sampling effort and parasite species richness. Parasitol Today 11:306–310

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

E. Flensted-Jensen and W. C. Aarestrup kindly helped to find nests. We received unpublished information from Ph. Christe, J. Fair, H. Hoi, M. Martín-Vivaldi, K. McCoy, S. Schjørring and M. Soler. Without their support we would not have been able to conduct this study. This study was supported by a grant to LR from the Hungarian Scientific Research Fund (Grant No. T 035150).

Author information

Authors and Affiliations

  1. Laboratoire de Parasitologie Evolutive, CNRS UMR 7103, Université Pierre et Marie Curie, Bât. A, 7ème étage, 7 quai St. Bernard, Case 237, 75252, Paris Cedex 05, France

    Anders Pape Møller

  2. Animal Ecology Research Group, Hungarian Academy of Sciences, Hungarian Natural History Museum, Budapest, Ludovika t. 2, 1083, Hungary

    Lajos Rózsa

Authors
  1. Anders Pape Møller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lajos Rózsa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anders Pape Møller.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Møller, A.P., Rózsa, L. Parasite biodiversity and host defenses: chewing lice and immune response of their avian hosts. Oecologia 142, 169–176 (2005). https://doi.org/10.1007/s00442-004-1735-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-004-1735-8

Keywords

Search

Navigation