Hostname: page-component-848d4c4894-xm8r8 Total loading time: 0 Render date: 2024-07-03T14:14:12.925Z Has data issue: false hasContentIssue false
  • English
  • Français

Consistent differences in macroparasite community composition among populations of three-spined sticklebacks, Gasterosteus aculeatus L.

Published online by Cambridge University Press:  19 July 2012

JOB DE ROIJ  and
ANDREW D. C. MacCOLL
JOB DE ROIJ*
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Ashworth Laboratories, Edinburgh EH9 3JT, UK
ANDREW D. C. MacCOLL
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
*
*Corresponding author: Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Ashworth Laboratories, Edinburgh EH9 3JT, UK. Tel: +0131 650 8682. E-mail: job.deroij@ed.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Parasite ecologists are often interested in the repeatability of patterns in parasite communities in space and/or time, because of implications for the dynamics of host-parasite interactions. Field studies usually examine temporal and spatial variation in isolation or limit themselves to a small number of host populations. Here, we studied the macroparasite communities of 12 populations of three-spined stickleback, Gasterosteus aculeatus L., on North Uist, Scotland, separated by small geographical distances, during the breeding season in 2 consecutive years (2007 and 2008) to determine: (1) the extent of spatial variation in macroparasite communities, (2) whether this variation is consistent across years, and (3) whether habitat characteristics can explain differences in macroparasite community composition among populations. We found substantial variation in parasite communities among populations. Generally, measures of parasite community composition were higher in 2008 than in 2007, but this effect of year was consistent across populations, such that the relative differences in these measures among populations changed little between years. These data suggest that there is short-term stability in the spatial variation in macroparasite communities of North Uist sticklebacks. However, none of the 5 habitat characteristics measured explained spatial variation in any measure of parasite community composition.

Keywords

parasite abundanceparasite prevalencespatial variationtemporal variationhabitat characteristics
Type
Research Article
Information
Parasitology , Volume 139 , Issue 11 , September 2012 , pp. 1478 - 1491
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Andersen, K. I. and Gibson, D. I. (1989). A key to three species of larval Diphyllobothrium Cobbold, 1858 (Cestoda: Pseudophyllidea) occurring in European and North American freshwater fishes. Systematic Parasitology 13, 3–9.CrossRefGoogle Scholar
Arneberg, P., Skorping, A., Grenfell, B. and Read, A. (1998 a). Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London, B 265, 1283.CrossRefGoogle Scholar
Arneberg, P., Skorping, A. and Read, A. F. (1998 b). Parasite abundance, body size, life histories, and the energetic equivalence rule. American Naturalist 151, 497–513.CrossRefGoogle ScholarPubMed
Barber, I. (2007). Host-parasite interactions of the three-spined stickleback. In Biology of the Three-Spined Stickleback (ed. Östlund-Nilsson, S., Mayer, I. and Huntingford, F. A.), pp. 271–317. CRC Press, Boca Raton, FL, USA.Google Scholar
Behnke, J. M. (2008). Structure in parasite component communities in wild rodents: predictability, stability, associations and interactions … or pure randomness? Parasitology 135, 751–766.CrossRefGoogle ScholarPubMed
Behnke, J. M., Bajer, A., Harris, P. D., Newington, L., Pidgeon, E., Rowlands, G., Sheriff, C., Kuliś-Malkowska, K., Sinski, E., Gilbert, F. S. and Barnard, C. J. (2008). Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from NE Poland. 2. The infracommunity level. Parasitology 135, 999–1018. doi: 10.1017/s0031182008004484.CrossRefGoogle ScholarPubMed
Bell, A. S. and Sommerville, C. (2002). Molecular evidence for the synonymy of two species of Apatemon Szidat, 1928, A. gracilis (Rudolphi, 1819) and A. annuligerum (von Nordmann, 1832)(Digenea: Strigeidae) parasitic as metacercariae in British fishes. Journal of Helminthology 76, 193–198.CrossRefGoogle Scholar
Bell, G. and Burt, A. (1991). The comparative biology of parasite species diversity: internal helminths of freshwater fish. Journal of Animal Ecology 60, 1047–1063. doi: 10.2307/5430.CrossRefGoogle Scholar
Benjamini, Y. and Hochberg, Y. (1995). Controlling the false discovery rate - a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, B 57, 289–300.Google Scholar
Blair, D. (1976). Observations on life cycle of Strigeoid trematode, Apatemon (Apatemon) gracilis (Rudolphi, 1819) Szidat, 1928. Journal of Helminthology 50, 125–132.CrossRefGoogle ScholarPubMed
Brouat, C., Kane, M., Diouf, M., Bâ, K., Sall-Dramé, R. and Duplantier, J. M. (2007). Host ecology and variation in helminth community structure in Mastomys rodents from Senegal. Parasitology 134, 437–450. doi: 10.1017/s003118200600151x.CrossRefGoogle ScholarPubMed
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Byers, J. E., Blakeslee, A. M. H., Linder, E., Cooper, A. B. and Maguire, T. J. (2008). Controls of spatial variation in the prevalence of trematode parasites infecting a marine snail. Ecology 89, 439–451.CrossRefGoogle ScholarPubMed
Bykhovskaya-Pavlovskaya, I. E., Gusev, A. V., Dubinina, M. N., Izyumova, N. A., Smirnova, T. S., Sokolovskaya, I. L., Shtein, G. A., Shul'man, S. S. and Epshtein, V. M. (1964). Key to Parasites of Freshwater Fish in the U.S.S.R., Israel Program for Scientific Translations, Jerusalum, Israel.Google Scholar
Cardon, M., Loot, G., Grenouillet, G. and Blanchet, S. (2011). Host characteristics and environmental factors differentially drive the burden and pathogenicity of an ectoparasite: a multilevel causal analysis. Journal of Animal Ecology 80, 657–667.CrossRefGoogle ScholarPubMed
Carney, J. P. and Dick, T. A. (2000). Helminth communities of yellow perch (Perca flavescens (Mitchill)): determinants of pattern. Canadian Journal of Zoology 78, 538–555. doi: 10.1139/cjz-78-4-538.CrossRefGoogle Scholar
Corby-Harris, V. and Promislow, D. E. L. (2008). Host ecology shapes geographical variation for resistance to bacterial infection in Drosophila melanogaster. Journal of Animal Ecology 77, 768–776.CrossRefGoogle ScholarPubMed
Curtis, M. A. and Rau, M. E. (1980). The geographical distribution of Diplostomiasis (Trematoda, Strigeidae) in fishes from Northern Quebec, Canada, in relation to the calcium ion concentrations of lakes. Canadian Journal of Zoology 58, 1390–1394.CrossRefGoogle Scholar
de Roij, J., Harris, P. D. and MacColl, A. D. C. (2011). Divergent resistance to a monogenean flatworm among three-spined stickleback populations. Functional Ecology 25, 217–226. doi: 10.1111/j.1365-2435.2010.01775.x.CrossRefGoogle Scholar
Dove, A. D. M. and Cribb, T. H. (2006). Species accumulation curves and their applications in parasite ecology. Trends in Parasitology 22, 568–574. doi: 10.1016/j.pt.2006.09.008.CrossRefGoogle ScholarPubMed
Ebert, D., Hottinger, J. W. and Pajunen, V. I. (2001). Temporal and spatial dynamics of parasite richness in a Daphnia metapopulation. Ecology 82, 3417–3434.Google Scholar
Esch, G. W. (1971). Impact of ecological succession on parasite fauna in centrarchids from oligotrophic and eutrophic ecosystems. American Midland Naturalist 86, 160–168.CrossRefGoogle Scholar
Faltýnková, A., Valtonen, E. and Karvonen, A. (2008). Spatial and temporal structure of the trematode component community in Valvata macrostoma (Gastropoda, Prosobranchia). Parasitology 135, 1691–1699.CrossRefGoogle ScholarPubMed
Gibson, D. I., Jones, A. and Bray, R. A. (2002). Keys to the Trematoda, Vol. 1, CABI International, Wallingford, UK.CrossRefGoogle Scholar
Giles, N. (1983). The possible role of environmental calcium levels during the evolution of phenotypic diversity in Outer Hebridean populations of the 3-spined stickleback, Gasterosteus aculeatus. Journal of Zoology 199, 535–544.CrossRefGoogle Scholar
Goater, C. P., Baldwin, R. E. and Scrimgeour, G. J. (2005). Physico-chemical determinants of helminth component community structure in whitefish (Coregonus clupeaformes) from adjacent lakes in Northern Alberta, Canada. Parasitology 131, 713–722.CrossRefGoogle ScholarPubMed
González, M. T. and Poulin, R. (2005). Spatial and temporal predictability of the parasite community structure of a benthic marine fish along its distributional range. International Journal for Parasitology 35, 1369–1377. doi: 10.1016/j.ijpara.2005.07.016.CrossRefGoogle ScholarPubMed
Gregory, R. D. (1990). Parasites and host geographic range as illustrated by waterfowl. Functional Ecology 645–654.CrossRefGoogle Scholar
Guégan, J. F. and Kennedy, C. R. (1993). Maximum local helminth parasite community richness in British freshwater fish: a test of the colonization time hypothesis. Parasitology 106, 91–100.CrossRefGoogle Scholar
Guégan, J. F. and Kennedy, C. R. (1996). Parasite richness/sampling effort/host range: The fancy three-piece jigsaw puzzle. Parasitology Today 12, 367–369. doi: 10.1016/0169-4758(96)10054-5.CrossRefGoogle ScholarPubMed
Guégan, J. F., Morand, S. and Poulin, R. (2005). Are there general laws in parasite community ecology? The emergence of spatial parasitology and epidemiology. In Parasitism and Ecosystems (ed. Thomas, F., Renaud, F. and Guégan, J. F.), pp. 22–42. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Hartvigsen, R. and Halvorsen, O. (1994). Spatial patterns in the abundance and distribution of parasites of freshwater fish. Parasitology Today 10, 28–31.CrossRefGoogle ScholarPubMed
Hasu, T., Benesh, D. P. and Valtonen, E. T. (2009). Differences in parasite susceptibility and costs of resistance between naturally exposed and unexposed host populations. Journal of Evolutionary Biology 22, 699–707. doi: 10.1111/j.1420-101.2009.01704.x.CrossRefGoogle ScholarPubMed
Hayward, A. D., Wilson, A. J., Pilkington, J. G., Pemberton, J. M. and Kruuk, L. E. B. (2009). Ageing in a variable habitat: environmental stress affects senescence in parasite resistance in St Kilda Soay sheep. Proceedings of the Royal Society of London, B 276, 3477–3485. doi: 10.1098/rspb.2009.0906.Google Scholar
Hechinger, R. F. and Lafferty, K. D. (2005). Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society of London, B 272, 1059–1066. doi: 10.1098/rspb.2005.3070.Google ScholarPubMed
Heins, D. C., Birden, E. L. and Baker, J. A. (2010). Host mortality and variability in epizootics of Schistocephalus solidus infecting the threespine stickleback, Gasterosteus aculeatus. Parasitology 137, 1681–1686. doi: 10.1017/s003118201000048x.CrossRefGoogle ScholarPubMed
Hernandez, A. D., Bunnell, J. F. and Sukhdeo, M. V. K. (2007). Composition and diversity patterns in metazoan parasite communities and anthropogenic disturbance in stream ecosystems. Parasitology 134, 91–102. doi: 10.1017/s0031182006001247.CrossRefGoogle ScholarPubMed
Kalbe, M., Wegner, K. M. and Reusch, T. B. H. (2002). Dispersion patterns of parasites in 0 + year three-spined sticklebacks: a cross population comparison. Journal of Fish Biology 60, 1529–1542. doi: 10.1006/jfbi.2002.2013.Google Scholar
Kennedy, C. R. (1978). Analysis of metazoan parasitocoenoses of brown trout, Salmo trutta, from British lakes. Journal of Fish Biology 13, 255–263.CrossRefGoogle Scholar
Kennedy, C. R. (2009). The ecology of parasites of freshwater fishes: the search for patterns. Parasitology 136, 1653–1662. doi: 10.1017/s0031182009005794.CrossRefGoogle ScholarPubMed
Kennedy, C. R. and Bush, A. O. (1994). The relationship between pattern and scale in parasite communities: a stranger in a strange land. Parasitology 109, 187–196.CrossRefGoogle Scholar
Kennedy, C. R., Shears, P. C. and Shears, J. A. (2001). Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus: a study of three epizootic cycles over thirty-one years. Parasitology 123, 257–269.CrossRefGoogle ScholarPubMed
King, K. C., McLaughlin, J. D., Gendron, A. D., Pauli, B. D., Giroux, I., Rondeau, B., Boily, M., Juneau, P. and Marcogliese, D. J. (2007). Impacts of agriculture on the parasite communities of northern leopard frogs (Rana pipiens) in southern Quebec, Canada. Parasitology 134, 2063–2080. doi: 10.1017/s0031182007003277.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Shenbrot, G. I., Medvedev, S. G., Vatschenok, V. S. and Khokhlova, I. S. (1997). Host-habitat relations as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev desert. Parasitology 114, 159–173. doi: 10.1017/s0031182096008347.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Shenbrot, G. I., Mouillot, D., Khokhlova, I. S. and Poulin, R. (2005). Spatial variation in species diversity and composition of flea assemblages in small mammalian hosts: geographical distance or faunal similarity? Journal of Biogeography 32, 633–644. doi: 10.1111/j.1365-2699.2004.01206.x.CrossRefGoogle Scholar
MacColl, A. D. C. (2009). Parasite burdens differ between sympatric three-spined stickleback species. Ecography 32, 153–160. doi: 10.1111/j.1600-0587.2008.05486.x.CrossRefGoogle Scholar
MacColl, A. D. C. and Chapman, S. M. (2010). Parasites can cause selection against migrants following dispersal between environments. Functional Ecology 24, 847–856.CrossRefGoogle Scholar
Magurran, A. E. (2003). Measuring Biological Diversity, Wiley Blackwell, Oxford, UK.Google Scholar
Manly, B. F. J. (1997). Randomization, Bootstrap and Monte Carlo Methods in Biology, 2nd Edn., Chapman and Hall, London, UK.Google Scholar
Marcogliese, D. J. and Cone, D. K. (1996). On the distribution and abundance of eel parasites in Nova Scotia: Influence of pH. Journal of Parasitology 82, 389–399.CrossRefGoogle ScholarPubMed
Norton, J., Lewis, J. W. and Rollinson, D. (2004). Temporal and spatial patterns of nestedness in eel macroparasite communities. Parasitology 129, 203–211. doi: 10.1017/s0031182004005517.CrossRefGoogle ScholarPubMed
Nunn, C. L., Altizer, S., Jones, K. E. and Sechrest, W. (2003). Comparative tests of parasite species richness in primates. The American Naturalist 162, 597–614.CrossRefGoogle ScholarPubMed
Pacala, S. W. and Dobson, A. P. (1988). The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96, 197–210.CrossRefGoogle ScholarPubMed
Pietrock, M. and Marcogliese, D. J. (2003). Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293–299.CrossRefGoogle ScholarPubMed
Poulin, R. (2000). Variation in the intraspecific relationship between fish length and intensity of parasitic infection: biological and statistical causes. Journal of Fish Biology 56, 123–137.CrossRefGoogle Scholar
Poulin, R. (2003). The decay of similarity with geographical distance in parasite communities of vertebrate hosts. Journal of Biogeography 30, 1609–1615.CrossRefGoogle Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites, Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Poulin, R., Blanar, C. A., Thieltges, D. W. and Marcogliese, D. J. (2011). The biogeography of parasitism in sticklebacks: distance, habitat differences and the similarity in parasite occurrence and abundance. Ecography 34, 540–551. doi: 10.1111/j.1600-0587.2010.06826.x.CrossRefGoogle Scholar
Poulin, R., Mouillot, D. and George-Nascimento, M. (2003). The relationship between species richness and productivity in metazoan parasite communities. Oecologia 137, 277–285. doi: 10.1007/s00442-003-1343-z.CrossRefGoogle ScholarPubMed
Poulin, R. and Valtonen, E. (2002). The predictability of helminth community structure in space: a comparison of fish populations from adjacent lakes. International Journal for Parasitology 32, 1235–1243.CrossRefGoogle ScholarPubMed
Randhawa, H. S. and Poulin, R. (2010). Determinants of tapeworm species richness in elasmobranch fishes: untangling environmental and phylogenetic influences. Ecography 33, 866–877.CrossRefGoogle Scholar
Schluter, D. (1995). Adaptive radiation in sticklebacks: trade-offs in feeding performance and growth. Ecology 76, 82–90.CrossRefGoogle Scholar
Sousa, W. P. and Grosholz, E. D. (1991). The influence of habitat structure on the transmission of parasites. In Habitat Structure: The Physical Arrangement of Objects in Space (ed. Bell, S. S., McCoy, E. D. and Mushinsky, H. R.), pp. 300–324. Chapman and Hall, London, UK.CrossRefGoogle Scholar
Thieltges, D. W., Fredensborg, B. L. and Poulin, R. (2009). Geographical variation in metacercarial infection levels in marine invertebrate hosts: parasite species character versus local factors. Marine Biology 156, 983–990. doi: 10.1007/s00227-009-1142-0.CrossRefGoogle Scholar
Thompson, J. N. (2005). The Geographic Mosaic of Coevolution, University of Chicago Press, Chicago, IL, USA.CrossRefGoogle Scholar
Vidal-Martínez, V. M. and Poulin, R. (2003). Spatial and temporal repeatability in parasite community structure of tropical fish hosts. Parasitology 127, 387–398. doi: 10.1017/s0031182003003792.CrossRefGoogle ScholarPubMed
Voutilainen, A., van Ooik, T., Puurtinen, M., Kortet, R. and Taskinen, J. (2009). Relationship between prevalence of trematode parasite Diplostomum sp. and population density of its snail host Lymnaea stagnalis in lakes and ponds in Finland. Aquatic Ecology 43, 351–357. doi: 10.1007/s10452-008-9203-x.CrossRefGoogle Scholar
Walther, B. A., Cotgreave, P., Price, R. D., Gregory, R. D. and Clayton, D. H. (1995). Sampling effort and parasite species richness. Parasitology Today 11, 306–310. doi: 10.1016/0169-4758(95)80047-6.CrossRefGoogle ScholarPubMed
Wetzel, R. G. (2001). Limnology: Lake and River Ecosystems. Academic Press San Diego, CA, USA.Google Scholar
Wootton, R. J. (1976). The Biology of the Sticklebacks. Academic Press, London, UK.Google Scholar
Supplementary material: File

de Roij supplementary material

de Roij supplementary material

Download de Roij supplementary material(File)
File 155.6 KB