Parasitology Research

, Volume 114, Issue 10, pp 3637–3643 | Cite as

Spatial covariation of local abundance among different parasite species: the effect of shared hosts

  • C. Lagrue
  • R. Poulin
Original Paper


Within any parasite species, abundance varies spatially, reaching higher values in certain localities than in others, presumably reflecting the local availability of host resources or the local suitability of habitat characteristics for free-living stages. In the absence of strong interactions between two species of helminths with complex life cycles, we might predict that the degree to which their abundances covary spatially is determined by their common resource requirements, i.e. how many host species they share throughout their life cycles. We test this prediction using five trematode species, all with a typical three-host cycle, from multiple lake sampling sites in New Zealand’s South Island: Stegodexamene anguillae, Telogaster opisthorchis, Coitocaecum parvum, Maritrema poulini, and an Apatemon sp. Pairs of species from this set of five share the same host species at either one, two, or all three life cycle stages. Our results show that when two trematode species share the same host species at all three life stages, they show positive spatial covariation in abundance (of metacercarial and adult stages) across localities. When they share hosts at two life stages, they show positive spatial covariation in abundance in some cases but not others. Finally, if two trematode species share only one host species, at a single life stage, their abundances do not covary spatially. These findings indicate that the extent of resource sharing between parasite species can drive the spatial match-mismatch between their abundances, and thus influence their coevolutionary dynamics and the degree to which host populations suffer from additive or synergistic effects of multiple infections.


Complex life cycles Trematodes New Zealand Local abundance Spatial covariation 



We thank Anne Besson, Isa Blasco-Costa, Manna Warburton, and Kim Garrett for assistance with field collection and laboratory processing of samples. We also thank an anonymous reviewer for constructive comments on an earlier version of the manuscript. This study was funded by a grant from the Marsden Fund (New Zealand) to RP.

Compliance statement

Animal collections and the protocol for this study were approved by Otago University’s Animal Ethic Committee (permit 10/12), New Zealand’s Department of Conservation (permit OT-34204-RES), and by Fish and Game New Zealand.


  1. Anderson RM, May RM (1978) Regulation and stability of host-parasite population interactions. I Regulatory processes. J Anim Ecol 47:219–247CrossRefGoogle Scholar
  2. Anderson RM, May RM (1979) Population biology of infectious diseases: part I. Nature 280:361–367CrossRefPubMedGoogle Scholar
  3. Arneberg P (2001) An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence. Ecography 24:352–358CrossRefGoogle Scholar
  4. Arneberg P, Skorping A, Grenfell BT, Read AF (1998) Host densities as determinants of abundance in parasite communities. Proc R Soc B 265:1283–1289CrossRefPubMedCentralGoogle Scholar
  5. Blasco-Costa I, Poulin R (2013) Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology 140:1316–1322CrossRefPubMedGoogle Scholar
  6. Blasco-Costa I, Rouco C, Poulin R (2015) Biogeography of parasitism in freshwater fish: spatial patterns in hot spots of infection. Ecography 38:301–310CrossRefGoogle Scholar
  7. Brown JH, Mehlman DW, Stevens GC (1995) Spatial variation in abundance. Ecology 76:2028–2043CrossRefGoogle Scholar
  8. Bush AO, Holmes JC (1986) Intestinal helminths of lesser scaup ducks: patterns of association. Can J Zool 64:132–141CrossRefGoogle Scholar
  9. Criscione CD, Blouin MS (2004) Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58:198–202CrossRefPubMedGoogle Scholar
  10. Dezfuli BS, Giari L, De Biaggi S, Poulin R (2001) Associations and interactions among intestinal helminths of the brown trout, Salmo trutta, in northern Italy. J Helminthol 75:331–336PubMedGoogle Scholar
  11. Diekmann O, Heesterbeek JAP (2000) Mathematical epidemiology of infectious diseases. Wiley, New YorkGoogle Scholar
  12. Dobson AP (1985) The population dynamics of competition between parasites. Parasitology 91:317–347CrossRefPubMedGoogle Scholar
  13. Dobson AP, Roberts M (1994) The population dynamics of parasitic helminth communities. Parasitology 109:S97–S108CrossRefPubMedGoogle Scholar
  14. Esch GW, Kennedy CR, Bush AO, Aho JM (1988) Patterns in helminth communities in freshwater fish in Great Britain: alternative strategies for colonization. Parasitology 96:519–532CrossRefPubMedGoogle Scholar
  15. Ferguson KI, Stiling P (1996) Non-additive effects of multiple natural enemies on aphid populations. Oecologia 108:375–379CrossRefGoogle Scholar
  16. Haukisalmi V, Henttonen H (1993) Coexistence in helminths of the bank vole. Clethrionomys glareolus. I. Patterns of co-occurrence. J Anim Ecol 62:221–229CrossRefGoogle Scholar
  17. Hechinger RF, Lafferty KD, Kuris AM (2008) Trematodes indicate animal biodiversity in the Chilean intertidal and Lake Tanganyika. J Parasitol 94:966–968CrossRefPubMedGoogle Scholar
  18. Herrmann KK, Poulin R (2011) Encystment site affects the reproductive strategy of a progenetic trematode in its fish intermediate host: is host spawning an exit for parasite eggs? Parasitology 138:1183–1192CrossRefPubMedGoogle Scholar
  19. Holmstad PR, Skorping A (1998) Covariation of parasite intensities in willow ptarmigan, Lagopus lagopus L. Can J Zool 76:1581–1588CrossRefGoogle Scholar
  20. Kennedy CR, Bush AO, Aho JM (1986) Patterns in helminth communities: why are birds and fish so different? Parasitology 93:205–215CrossRefPubMedGoogle Scholar
  21. Lagrue C, Poulin R (2015) Bottom-up regulation of parasite population densities in freshwater ecosystems. Oikos. doi: 10.1111/oik.02164 Google Scholar
  22. Lagrue C, Poulin R, Cohen JE (2015) Parasitism alters three power laws of scaling in a metazoan community: Taylor’s law, density-mass allometry, and variance-mass allometry. Proc Natl Acad Sci U S A 112:1791–1796CrossRefPubMedCentralPubMedGoogle Scholar
  23. Lotz JM, Font WF (1991) The role of positive and negative interspecific associations in the organization of communities of intestinal helminths of bats. Parasitology 103:127–138CrossRefPubMedGoogle Scholar
  24. May RM, Anderson RM (1979) Population biology of infectious diseases: part II. Nature 280:455–461CrossRefPubMedGoogle Scholar
  25. Perez-del-Olmo A, Morand S, Raga JA, Kostadinova A (2011) Abundance-variance and abundance-occupancy relationships in a marine host-parasite system: the importance of taxonomy and ecology of transmission. Int J Parasitol 41:11361–1370CrossRefGoogle Scholar
  26. Poulin R (2001) Interactions between species and the structure of helminth communities. Parasitology 122:S3–S11CrossRefPubMedGoogle Scholar
  27. Poulin R (2006) Variation in infection parameters among populations within parasite species: intrinsic properties versus local factors. Int J Parasitol 36:877–885CrossRefPubMedGoogle Scholar
  28. Poulin R, Dick TA (2007) Spatial variation in population density across the geographical range in helminth parasites of yellow perch Perca flavescens. Ecography 30:629–636CrossRefGoogle Scholar
  29. Rauque CA, Paterson RA, Poulin R, Tompkins DM (2011) Do different parasite species interact in their effects on host fitness? A case study on parasites of the amphipod Paracalliope fluviatilis. Parasitology 138:1176–1182CrossRefPubMedGoogle Scholar
  30. Sonnenholzner JI, Lafferty KD, Ladah LB (2011) Food webs and fishing affect parasitism of the sea urchin Eucidaris galapagensis in the Galápagos. Ecology 92:2276–2284CrossRefPubMedGoogle Scholar
  31. Thieltges DW, Hof C, Borregaard MK, Dehling DM, Brändle M, Brandl R, Poulin R (2011) Range size patterns in European freshwater trematodes. Ecography 34:982–989CrossRefGoogle Scholar
  32. Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, ChicagoGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of ZoologyUniversity of OtagoDunedinNew Zealand

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