Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-03T00:47:18.778Z Has data issue: false hasContentIssue false
  • English
  • Français

Spatial and temporal variation in macroparasite communities of three-spined stickleback

Published online by Cambridge University Press:  20 October 2016

REBECCA E. YOUNG  and
ANDREW D. C. MACCOLL
REBECCA E. YOUNG*
Affiliation:
School of Life Sciences, University Park, University of Nottingham, Nottingham NG7 2RD, UK
ANDREW D. C. MACCOLL
Affiliation:
School of Life Sciences, University Park, University of Nottingham, Nottingham NG7 2RD, UK
*
*Corresponding author: School of Life Sciences, University Park, University of Nottingham, Nottingham NG7 2RD, UK. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Patterns in parasite community structure are often observed in natural systems and an important question in parasite ecology is whether such patterns are repeatable across time and space. Field studies commonly look at spatial or temporal repeatability of patterns, but they are rarely investigated in conjunction. We use a large dataset on the macroparasites of the three-spined stickleback, Gasterosteus aculeatus L., collected from 14 locations on North Uist, Scotland over an 8-year period to investigate: (1) repeatability of patterns in parasite communities among populations and whether variation is consistent across years, (2) whether variation between years can be explained by climatic variation and progression of the season and (3) whether variation in habitat characteristics explain population differences. Differences in relative abundance and prevalence across populations were observed in a number of parasites investigated indicating a lack of consistency across years in numerous parasite community measures; however, differences between populations in the prevalence and abundance of some parasites were consistent throughout the study. Average temperature did not affect parasite community, and progression of the season was only significant for two of 13 community measures. Two of the six habitat characteristics investigated (pH and calcium concentration) significantly affected parasite presence.

Keywords

sticklebackparasite communityrepeatability
Type
Research Article
Information
Parasitology , Volume 144 , Issue 4 , April 2017 , pp. 436 - 449
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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

Abu-Madi, M. A., Behnke, J. M., Lewis, J. W. and Gilbert, F. (1998). Descriptive epidemiology of Heligmosomoides polygyrus in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 72, 93–100.Google Scholar
Andersen, K. and Valtonen, E. (1990). On the infracommunity structure of adult cestodes in freshwater fishes. Parasitology 101, 257–264.Google Scholar
Anderson, R. M. and May, R. M. (1987). Regulation and stability of host-parasite population interactions: I. Regulatory processes. Journal of Animal Ecology 47, 219–247.Google Scholar
Appleby, C. and Mo, T. A. (1997). Population dynamics of Gyrodactylus salaris (Monogenea) infecting Atlantic salmon, Salmo salar, parr in the River Batnfjordselva, Norway. Journal of Parasitology 83, 23–30.CrossRefGoogle ScholarPubMed
Arneberg, P. (2002). Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25, 88–94.Google Scholar
Arneberg, P., Skorping, A. and Read, A. F. (1998). Parasite abundance, body size, life histories, and the energetic equivalence rule. American Naturalist 151, 497–513.CrossRefGoogle ScholarPubMed
Bagamian, K., Heins, D. and Baker, J. (2004). Body condition and reproductive capacity of three-spined stickleback infected with the cestode Schistocephalus solidus . Journal of Fish Biology 64, 1568–1576.CrossRefGoogle Scholar
Behnke, J. (2008). Structure in parasite component communities in wild rodents: predictability, stability, associations and interactions…. or pure randomness? Parasitology 135, 751–766.Google Scholar
Behnke, J., Bajer, A., Sinski, E. and Wakelin, D. (2001). Interactions involving intestinal nematodes of rodents: experimental and field studies. Parasitology 122, S39–S49.Google Scholar
Behnke, J., Gilbert, F., Abu-Madi, M. and Lewis, J. (2005). Do the helminth parasites of wood mice interact? Journal of Animal Ecology 74, 982–993.Google Scholar
Behnke, J., Bajer, A., Harris, P., Newington, L., Pidgeon, E., Rowlands, G., Sheriff, C., Kuliś-Malkowska, K., Siński, E. and Gilbert, F. (2008 a). Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from NE Poland. 1. Regional fauna and component community levels. Parasitology 135, 985–997.CrossRefGoogle ScholarPubMed
Behnke, J., Bajer, A., Harris, P., Newington, L., Pidgeon, E., Rowlands, G., Sheriff, C., Kuliś-Malkowska, K., Siński, E. and Gilbert, F. (2008 b). Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from NE Poland. 2. The infracommunity level. Parasitology 135, 999–1018.Google Scholar
Blanchet, S., Rey, O., Berthier, P., Lek, S. and Loot, G. (2009). Evidence of parasite-mediated disruptive selection on genetic diversity in a wild fish population. Molecular Ecology 18, 1112–1123.Google Scholar
Bolek, M. G. and Coggins, J. R. (2000). Seasonal occurrence and community structure of helminth parasites from the eastern American toad, Bufo americanus americanus, from southeastern Wisconsin, USA. Comparative Parasitology 67, 202–209.Google Scholar
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.Google Scholar
Bykhovskaya-Pavloskaya, 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
Calvete, C., Blanco-Aguiar, J., Virgós, E., Cabezas-Díaz, S. and Villafuerte, R. (2004). Spatial variation in helminth community structure in the red-legged partridge (Alectoris rufa L.): effects of definitive host density. Parasitology 129, 101–113.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.Google Scholar
Carney, J. and Dick, T. (2000). Helminth communities of yellow perch (Perca flavescens (Mitchill)): determinants of pattern. Canadian Journal of Zoology 78, 538–555.Google Scholar
Chappell, L. (1969). Competitive exclusion between two intestinal parasites of the three-spined stickleback, Gasterosteus aculeatus L. Journal of Parasitology 55, 775–778.Google Scholar
Connor, E. F. and McCoy, E. D. (1979). The statistics and biology of the species-area relationship. American Naturalist 113, 791–833.Google Scholar
Cribb, T. H., Bray, R. A., Olson, P. D., Timothy, D. and Littlewood, J. (2003). Life cycle evolution in the Digenea: a new perspective from phylogeny. Advances in Parasitology 54, 197–254.Google Scholar
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.Google Scholar
Dartnall, H. J. G. (1973). Parasites of the nine-spined stickleback Pungitius pungitius (L). Journal of Fish Biology 5, 505–509.Google Scholar
de Roij, J. and MacColl, A. D.C. (2012). Consistent differences in macroparasite community composition among populations of three-spined sticklebacks, Gasterosteus aculeatus L. Parasitology 139, 1478–1491.Google Scholar
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
Folstad, I. and Karter, A. J. (1992). Parasites, bright males, and the immunocompetence handicap. American Naturalist 139, 603–622.Google Scholar
Folstad, I., Hope, A. M., Karter, A. and Skorping, A. (1994). Sexually selected color in male sticklebacks: a signal of both parasite exposure and parasite resistance? Oikos 69, 511–515.Google Scholar
Fryer, G. (1980). Acidity and species diversity in freshwater crustacean faunas. Freshwater Biology 10, 41–45.Google Scholar
Goater, C., Baldwin, R. and Scrimgeour, G. (2005). Physico-chemical determinants of helminth component community structure in whitefish (Coregonus clupeaformes) from adjacent lakes in Northern Alberta, Canada. Parasitology 131, 713–722.Google Scholar
González, M. 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.Google Scholar
Halmetoja, A., Valtonen, E. T. and Koskenniemi, E. (2000). Perch (Perca fluviatilis L.) parasites reflect ecosystem conditions: a comparison of a natural lake and two acidic reservoirs in Finland. International Journal for Parasitology 30, 1437–1444.CrossRefGoogle ScholarPubMed
Hopkins, C. (1959). Seasonal variations in the incidence and development of the cestode Proteocephalus filicollis (Rud. 1810) in Gasterosteus aculeatus (L. 1766). Parasitology 49, 529–542.Google Scholar
Kennedy, C. R. (1993). The dynamics of intestinal helminth communities in eels Anguilla anguilla in a small stream: long-term changes in richness and structure. Parasitology 107, 71–78.CrossRefGoogle Scholar
Kennedy, C. R. (1997). Long-term and seasonal changes in composition and richness of intestinal helminth communities in eels Anguilla anguilla of an isolated English river. Folia Parasitologica 44, 267–273.Google Scholar
Kennedy, C. R. (2009). The ecology of parasites of freshwater fishes: the search for patterns. Parasitology 136, 1653–1662.Google Scholar
Kennedy, C. R., Shears, P. and Shears, J. (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.Google Scholar
Lawton, J. H. (1999). Are there general laws in ecology? Oikos 84, 177–192.CrossRefGoogle Scholar
Lester, R. (1971). The influence of Schistocephalus plerocercoids on the respiration of Gasterosteus and a possible resulting effect on the behavior of the fish. Canadian Journal of Zoology 49, 361–366.Google Scholar
Lively, C. M., de Roode, J. C., Duffy, M. A., Graham, A. L. and Koskella, B. (2014). Interesting open questions in disease ecology and evolution. American Naturalist 184, S1–S8.Google Scholar
MacColl, A. D.C. (2009). Parasite burdens differ between sympatris three-spined sticklebacks. Ecography 32, 153–160.CrossRefGoogle Scholar
MacColl, A. D.C., Nagar, A. E. and de Roij, J. (2013). The evolutionary ecology of dwarfism in three-spined sticklebacks. Journal of Animal Ecology 82, 642–652.Google Scholar
Magurran, A. E. (2004). Measuring Biological Diversity, 2nd Edn. Blackwell Science Ltd, Oxford, UK.Google Scholar
Marcogliese, D. J. and Cone, D. K. (1991). Importance of lake characteristics in structuring parasite communities of salmonids from insular Newfoundland. Canadian Journal of Zoology 69, 2962–2967.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
Meggitt, F. J. (1914). The structure and life history of a tapeworm (Ichthyotaenia filicollis Rud.) parasitic in the stickleback. Proceedings of the Zoological Society of London 1, 113–138.Google Scholar
Ostlund-Nilsson, S., Mayer, I. and Huntingford, F. A. (2010). Biology of the Three-spined Stickleback. CRC Press: Taylor & Francis Group, Florida, USA.Google Scholar
Pennycuick, L. (1971). Seasonal variations in the parasite infections in a population of three-spined sticklebacks, Gasterosteus aculeatus L. Parasitology 63, 373–388.Google Scholar
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. (1997). Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics 28, 341–358.Google Scholar
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.Google Scholar
Poulin, R. (2007). Are there general laws in parasite ecology? Parasitology 134, 763–776.Google Scholar
Pressley, P. H. (1981). Parental effort and the evolution of nest-guarding tactics in the three-spined stickleback Gasterosteus aculeatus L. Evolution 35, 282–295.CrossRefGoogle Scholar
Scholz, T. (1999). Life cycles of species of Proteocephalus parasites of fishes in the Palearctic Region: a review. Journal of Helmintholog 73, 1–19.Google Scholar
Soleng, A., Jansen, P. A. and Bakke, T. A. (1999). Transmission of the monogenean Gyrodactylus salaris . Folia Parasitologica 46, 179–184.Google Scholar
Vidal-Martínez, V. and Poulin, R. (2003). Spatial and temporal repeatability in parasite community structure of tropical fish hosts. Parasitology 127, 387–398.Google Scholar
Waterston, A. R., Holden, A. V., Campbell, R. N. and Maitland, P. S. (1979). The inland waters of the Outer Hebrides. Proceedings of the Royal Society of Edinburgh Section B: Biological Sciences 77B, 329–351.Google Scholar
Wilson, K., Bjørnstad, O., Dobson, A., Merler, S., Poglayen, G., Randolph, S., Read, A. and Skorping, A. (2002). Heterogeneities in macroparasite infections: patterns and processes. The Ecology of Wildlife Diseases 44, 6–44.Google Scholar
Zander, C. D. (2007). Parasite diversity of sticklebacks from the Baltic Sea. Parasitology Research 100, 287–297.CrossRefGoogle ScholarPubMed
Supplementary material: File

Young and MacColl supplementary material

Table S1

Download Young and MacColl supplementary material(File)
File 19.8 KB
Supplementary material: File

Young and MacColl supplementary material

Table S2

Download Young and MacColl supplementary material(File)
File 17.3 KB