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The relationship between specialization and local abundance: the case of helminth parasites of birds

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Abstract

Positive relationships are commonly observed between the abundance of a species in a locality and the frequency of its occurrence among localities on a larger scale. This pattern may not hold for parasitic organisms when the average abundance of a parasite among its hosts is related to the number of host species in which it occurs, because of the additive investment in specific adaptations to counter host immune responses required for each host species in a parasite’s repertoire. For a rigorous test of the hypothesis that there is a trade-off between the number of host species that can be successfully exploited and the average abundance of parasites in those hosts, one needs to take into account the phylogenetic (or taxonomic) distances among the host species used by a parasite. Differences in immune responses are likely to increase with increasing phylogenetic distances. The trade-off hypothesis was tested in a comparative analysis of 393 species of trematodes, cestodes and nematodes parasitic in birds surveyed from the same geographical area, using an index of host specificity that measures the average taxonomic distances between a parasite’s known host species. After correcting for the influences of parasite phylogeny and other potential confounding variables, mean abundance was negatively correlated with the average taxonomic distance among host species for nematodes, and with the variance in taxonomic distances among hosts for cestodes. In the case of trematodes, these variables covaried positively. The trade-off between average infection success and how taxonomically distant a parasite’s host species are from each other was only found in two of the three groups of helminths investigated, possibly because of compensating features in trematodes, such as their ability to multiply asexually in intermediate hosts. These results provide empirical evidence consistent with the hypothesis that specialization allows greater local adaptation and therefore greater local population abundance, supporting key predictions regarding the evolution of ecological specialization.

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References

  • Adamson ML, Caira JN (1994) Evolutionary factors influencing the nature of parasite specificity. Parasitology 109:S85–S95

    PubMed  Google Scholar 

  • Anderson RC (2000) Nematode parasites of vertebrates: their development and transmission. CABI, Wallingford

    Google Scholar 

  • Barger MA, Esch GW (2002) Host specificity and the distribution—abundance relationship in a community of parasites infecting fishes in streams of North Carolina. J Parasitol 88:446–453

    PubMed  Google Scholar 

  • Berenbaum M (1983) Coumarins and caterpillars: a case for coevolution. Evolution 37:163–179

    CAS  Google Scholar 

  • Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, Vierstraete A, Vanfleteren JR, Mackey LY, Dorris M, Frisse LM, Vida JT, Thomas WK (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392:71–75

    Article  CAS  PubMed  Google Scholar 

  • Brown JH (1984) On the relationship between abundance and distribution of species. Am Nat 124:255–279

    Article  Google Scholar 

  • Cornell HV, Hawkins BA (2003) Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory. Am Nat 161:507–522

    Article  PubMed  Google Scholar 

  • Desdevises Y, Morand S, Legendre P (2002) Evolution and determinants of host specificity in the genus Lamellodiscus (Monogenea). Biol J Linn Soc 77:431–443

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233

    Article  Google Scholar 

  • Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32

    Google Scholar 

  • Gaston KJ (1996) The multiple forms of the interspecific abundance-distribution relationship. Oikos 76:211–220

    Google Scholar 

  • Gaston KJ, Blackburn TM (2000) Pattern and process in macroecology. Blackwell, Oxford

  • Gaston KJ, Lawton JH (1990) Effects of scale and habitat on the relationship between regional distribution and local abundance. Oikos 58:329–335

    Google Scholar 

  • Gaston KJ, Blackburn TM, Lawton JH (1997) Interspecific abundance range size relationships: an appraisal of mechanisms. J Anim Ecol 66:579–601

    Google Scholar 

  • Gibson DI, Jones A, Bray RA (2002) Keys to the Trematoda, vol 1. CABI, Wallingford

  • Gregory RD, Blackburn TM (1991) Parasite prevalence and host sample size. Parasitol Today 7:316–318

    Article  Google Scholar 

  • Gregory RD, Woolhouse MEJ (1993) Quantification of parasite aggregation: a simulation study. Acta Trop 54:131–139

    Article  CAS  PubMed  Google Scholar 

  • Hanski I, Kouki J, Halkka A (1993) Three explanations of the positive relationship between distribution and abundance of species. In: Ricklefs RE, Schluter D (eds) Species diversity in ecological communities: historical and geographical perspectives. University of Chicago Press, Chicago, pp 108–116

  • Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

  • Hoberg EP, Jones A, Bray RA (1999) Phylogenetic analysis among the families of the Cyclophyllidea (Eucestoda) based on comparative morphology, with new hypotheses for co-evolution in vertebrates. Syst Parasitol 42:51–73

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • John JL (1995) Parasites and the avian spleen: helminths. Biol J Linn Soc 54:87–106

    Google Scholar 

  • Kearn GC (1998) Parasitism and the platyhelminths. Chapman and Hall, London

  • Khalil LF, Jones A, Bray RA (1994) Keys to the cestode parasites of vertebrates. CABI, Wallingford

  • Kostadinova A (2004) Family Echinostomatidae Looss, 1899. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI, Wallingford (in press)

  • Mariaux J (1998) A molecular phylogeny of the Eucestoda. J Parasitol 84:114–124

    CAS  PubMed  Google Scholar 

  • 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 

  • Nickisch-Rosenegk M von, Lucius R, Loos-Frank B (1999) Contributions to the phylogeny of the Cyclophyllidea (Cestoda) inferred from mitochondrial 12S rDNA. J Mol Evol 48:586–596

    PubMed  Google Scholar 

  • Olson PD, Littlewood DTJ, Bray RA, Mariaux J (2001) Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Mol Phylogenet Evol 19:443–467

    CAS  PubMed  Google Scholar 

  • Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33:733–755

    Article  CAS  PubMed  Google Scholar 

  • Poulin R (1992) Determinants of host-specificity in parasites of freshwater fishes. Int J Parasitol 22:753–758

    Article  CAS  PubMed  Google Scholar 

  • Poulin R (1998) Large-scale patterns of host use by parasites of freshwater fishes. Ecol Lett 1:118–128

    Article  Google Scholar 

  • Poulin R (1999) The intra- and interspecific relationships between abundance and distribution in helminth parasites of birds. J Anim Ecol 68:719–725

    Article  Google Scholar 

  • Poulin R, Mouillot D (2003) Parasite specialization from a phylogenetic perspective: a new index of host specificity. Parasitology 126:473–480

    Article  CAS  PubMed  Google Scholar 

  • Purvis A, Rambaut A (1994) Comparative analysis by independent contrasts (CAIC), version 2.0. Oxford University, Oxford

  • Sasal P, Trouvé S, Muller-Graf C, Morand S (1999) Specificity and host predictability: a comparative analysis among monogenean parasites of fish. J Anim Ecol 68:437–444

    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 

  • Sibley CG, Ahlquist JE (1991) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New Haven

    Google Scholar 

  • Sibley CG, Monroe BL Jr (1990) Distribution and taxonomy of birds of the world. Yale University Press, New Haven

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

  • Toivanen P, Toivanen A (1987) Avian immunology. CRC Press, Boca Raton

  • Vaidova SM (1978) Helminths of the birds of Azerbaidzhan (in Russian). Akademy Nauk Azerbaidzhan SSR, Elm, Baku

  • Ward SA (1992) Assessing functional explanations of host-specificity. Am Nat 139:883–891

    Article  Google Scholar 

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Acknowledgements

We thank Amy Armstrong for assistance with data compilation. R. Poulin is supported by a James Cook Research Fellowship from the Royal Society of New Zealand.

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Authors and Affiliations

  1. Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand

    Robert Poulin

  2. UMR CNRS-UMII 5119 ECOLAG, Université Montpellier II, CC 093, 34095, Montpellier Cedex 5, France

    David Mouillot

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  1. Robert Poulin
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  2. David Mouillot
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Correspondence to Robert Poulin.

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Poulin, R., Mouillot, D. The relationship between specialization and local abundance: the case of helminth parasites of birds. Oecologia 140, 372–378 (2004). https://doi.org/10.1007/s00442-004-1593-4

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  • DOI: https://doi.org/10.1007/s00442-004-1593-4

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