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Climate influences parasite-mediated competitive release

Published online by Cambridge University Press:  03 August 2011

MARTIN H. LARSEN ,
K. THOMAS JENSEN  and
KIM N. MOURITSEN
MARTIN H. LARSEN
Affiliation:
Department of Bioscience, Marine Ecology, University of Aarhus, Ole Worms Allé 1, DK-8000 Aarhus C, Denmark
K. THOMAS JENSEN
Affiliation:
Department of Bioscience, Marine Ecology, University of Aarhus, Ole Worms Allé 1, DK-8000 Aarhus C, Denmark
KIM N. MOURITSEN*
Affiliation:
Department of Bioscience, Marine Ecology, University of Aarhus, Ole Worms Allé 1, DK-8000 Aarhus C, Denmark
*
*Corresponding author: Tel: +45 89424386. Fax: +45 89424387. E-mail: kim.mouritsen@biology.au.dk
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Summary

Parasitism is believed to play an important role in maintaining species diversity, for instance by facilitating coexistence between competing host species. However, the possibility that environmental factors may govern the outcome of parasite-mediated competition has rarely been considered. The closely related amphipods Corophium volutator and Corophium arenarium both serve as second intermediate host for detrimental trematodes. Corophium volutator is the superior competitor of the two, but also suffers from higher mortality when exposed to infective trematode stages. Here, we report parasite-mediated competitive release of C. arenarium in an intertidal habitat, in part triggered by unusually high temperatures linked to the North Atlantic climate oscillation (NAO). The elevated temperatures accelerated the transmission of cercariae from sympatric first intermediate hosts (mud snails) to amphipods, causing a local collapse of the parasite-sensitive C. volutator population and concordant increase in the abundance of the competitively inferior C. arenarium.

Keywords

climate changecommunity structurecompetitionCorophiumhost–parasite interactionstrematodes
Type
Research Article
Information
Parasitology , Volume 138 , Issue 11 , September 2011 , pp. 1436 - 1441
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Bates, A. E., Poulin, R. and Lamare, M. D. (2010). Spatial variation in parasite-induced mortality in an amphipod: shore height versus exposure history. Oecologia 163, 651–659. doi: 10.1007/s00442-010-1593-5.CrossRefGoogle Scholar
Bonsall, M. B. and Hassell, M. P. (1997). Apparent competition structures ecological assemblages. Nature, London 388, 371–373.CrossRefGoogle Scholar
Brockhurst, M. A., Fenton, A., Roulston, B. and Rainey, P. B. (2006). The impact of phages on interspecific competition in experimental populations of bacteria. BMC Ecology 6, 19–25. doi: 10.1186/1472-6785-6-19.CrossRefGoogle ScholarPubMed
Cappelen, J. and Jørgensen, B. V. (2009). Dansk vejr siden 1874 – måned for måned med temperatur, nedbør og soltimer samt beskrivelser af vejret. Technical report, Danish Meteorological Institute. http://www.dmi.dk/dmi/tr08-02.pdf (in Danish).Google Scholar
Deblock, S. (1980). Inventaire des trématodes larvaires parasites des mollusques Hydrobia (Prosobranches) des côtes de France. Parassitologia 22, 1–105 (in French).Google Scholar
Fenton, A. and Brockhurst, M. A. (2008). The role of specialist parasites in structuring host communities. Ecological Research 23, 795–804. doi: 10.1007/s11284-007-0440-6.CrossRefGoogle Scholar
Field, L. C. and Irwin, S. W. B. (1999). Digenean larvae in Hydrobia ulvae from Belfast Lough (Northern Ireland) and the Ythan Estuary (north-east Scotland). Journal of the Marine Biological Association of the United Kingdom 79, 431–435.CrossRefGoogle Scholar
Flach, E. C. (1993). The distribution of the amphipod Corophium arenarium in the Dutch Wadden Sea: relationships with sediment composition and the presence of cockles and lungworms. Netherlands Journal of Sea Research 31, 281–290.CrossRefGoogle Scholar
Fleury, F., Ris, N., Allemand, R., Fouillet, P., Carton, Y. and Boulétreau, M. (2004). Ecological and genetic interactions in Drosophila–parasitoids communities: a case study with D. melanogaster, D. simulans and their common Leptopilina parasitoids in south-eastern France. Genetica 120, 181–194.CrossRefGoogle ScholarPubMed
Hatcher, M. J., Dick, J. T. A. and Dunn, A. M. (2006). How parasites affect interactions between competitors and predators. Ecology Letters 9, 1253–1271. doi: 10.1111/j.1461-0248.2006.00964.x.CrossRefGoogle ScholarPubMed
Hoenicke, R. (1984). The effects of a fungal infection of Diaptomus novamexicanus eggs on the zooplankton community structure of Castle Lake, California. Verhandlungen der Internationale Vereinigung für Theoretische und Angewandte Limnologie 22, 573–577.Google Scholar
Holt, R. D. and Lawton, J. H. (1994). The ecological consequences of shared natural enemies. Annual Review of Ecology and Systematics 25, 495–520.CrossRefGoogle Scholar
Hudson, P. J. and Greenman, J. V. (1998). Competition mediated by parasites: biological and theoretical progress. Trends in Ecology and Evolution 13, 387–390.CrossRefGoogle ScholarPubMed
Hurrell, J. W. (1995). Decadal trends in the North Atlantic Oscillation: regional temperatures and precipitation. Science 269, 676–679.CrossRefGoogle ScholarPubMed
IPCC (2007). Climate change 2007: synthesis report. Fourth Assessment Report. Intergovernmental Panel on Climate Change, Geneva, Switzerland.Google Scholar
Jensen, K. T. and Kristensen, L. D. (1990). A field experiment on competition between Corophium volutator (Pallas) and Corophium arenarium Crawford (Crustacea: Amphipoda): effects on survival, reproduction and recruitment. Journal of Experimental Marine Biology and Ecology 137, 1–24.CrossRefGoogle Scholar
Jensen, K. T. and Mouritsen, K. N. (1992). Mass mortality in two common soft-bottom invertebrates, Hydrobia ulvae and Corophium volutator – the possible role of trematodes. Helgoländer Meeresuntersuchungen 46, 329–339.CrossRefGoogle Scholar
Jensen, T., Jensen, K. T. and Mouritsen, K. N. (1998). The influence of the trematode Microphallus claviformis on two congeneric intermediate host species (Corophium): infection characteristicts and host survival. Journal of Experimental Marine Biology and Ecology 227, 35–48.CrossRefGoogle Scholar
Koehler, A. V. and Poulin, R. (2010). Host partitioning by parasites in an intertidal crustacean community. Journal of Parasitology 96, 862–868. doi: 10.1645/GE-2460.1.CrossRefGoogle Scholar
Kube, S., Kube, J. and Bick, A. (2002). Component community of larval trematodes in the mudsnail Hydrobia ventrosa: temporal variations in prevalence in relation to host life history. Journal of Parasitology 88, 730–737.CrossRefGoogle ScholarPubMed
Laursen, K. and Frikke, J. (1984). The Danish Wadden Sea. In Coastal Waders and Wildfowl in Winter (ed. Evans, P. R., Goss-Custard, J. D. and Hale, W. G.), pp. 214–223. Cambridge University Press, Cambridge, UK.Google Scholar
Laursen, K., Hounisen, J. P., Rasmussen, L. M., Frikke, J., Pihl, S., Kahlert, J., Bak, M. and Amstrup, O. (2009). Rastende vandfugle i Margrethe Kog og på forlandet vest for Tøndermarsken, 1984–2007. Technical Report, National Environmental Research Institution, Aarhus University, 78 pp. http://www.dmu.dk/Pub/FR702.pdf (in Danish).Google Scholar
Lincoln, R. J. (1979). British Marine Amphipoda: Gammaridea. British Museum (Natural History), London, UK.Google Scholar
Marcogliese, D. J. (2001). Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 1331–1352. doi: 10.1139/cjz-79-8-1331.CrossRefGoogle Scholar
Meissner, K. and Bick, A. (1999 a). Laboratory studies of parasite transmission aspects between Hydrobia spp. (Gastropoda) and Corophium volutator (Amphipoda). International Review of Hydrobiology 84, 61–72.CrossRefGoogle Scholar
Meissner, K. and Bick, A. (1999 b). Mortality of Corophium volutator (Amphipoda) caused by infestation with Maritrema subdolum (Digenea, Microphallidae)–laboratory studies. Diseases of Aquatic Organisms 35, 47–52.CrossRefGoogle Scholar
Mouritsen, K. N. (1994). Day and night feeding in dunlins Calidris alpina: choice of habitat, foraging technique and prey. Journal of Avian Biology 25, 55–62.CrossRefGoogle Scholar
Mouritsen, K. N. (2002). The Hydrobia ulvae–Maritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity. Journal of Helminthology 76, 341–347. doi: 10.1079/JOH2002137.CrossRefGoogle ScholarPubMed
Mouritsen, K. N. and Jensen, K. T. (1997). Parasite transmission between soft-bottom invertebrates: temperature mediated infection rates and mortality in Corophium volutator. Marine Ecology Progress Series 151, 123–134.CrossRefGoogle Scholar
Mouritsen, K. N., Jensen, T. and Jensen, K. T. (1997). Parasites on an intertidal Corophium-bed: factors determining the phenology of microphallid trematodes in the intermediate host populations of the mud-snail Hydrobia ulvae and the amphipod Corophium volutator. Hydrobiologia 355, 61–70.CrossRefGoogle Scholar
Mouritsen, K. N., McKechnie, S., Meenken, E., Toynbee, J. L. and Poulin, R. (2003). Spatial heterogeneity in parasite loads in the New Zealand cockle: the importance of host condition and density. Journal of the Marine Biological Association of the United Kingdom 83, 307–310.CrossRefGoogle Scholar
Mouritsen, K. N., Mouritsen, L. T. and Jensen, K. T. (1998). Change of topography and sediment characteristics on an intertidal mud-flat following mass-mortality of the amphipod Corophium volutator. Journal of the Marine Biological Association of the United Kingdom 78, 1167–1180.CrossRefGoogle Scholar
Mouritsen, K. N. and Poulin, R. (2002). Parasitism, climate oscillations and the structure of natural communities. Oikos 97, 462–468.CrossRefGoogle Scholar
Mouritsen, K. N., Tompkins, D. M. and Poulin, R. (2005). Climate warming may cause a parasite-induced collapse in coastal amphipod populations. Oecologia 146, 476–483. doi: 10.1007/s00442-005-0223-0.CrossRefGoogle Scholar
Möller, P. and Rosenberg, R. (1982). Production and abundance of the amphipod Corophium volutator on the west coast of Sweden. Netherlands Journal of Sea Research 16, 127–140.CrossRefGoogle Scholar
Park, T. (1948). Experimental studies of interspecies competition. I. Competition between populations of the flour beetles, Tribolium confusum Duval and Tribolium castaneum Herbst. Ecological Monographs 18, 265–308.CrossRefGoogle Scholar
Pietrock, M. and Marcogliese, D. J. (2003). Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293–299. doi: 10.1016/S1471-4922(03)00117-X.CrossRefGoogle ScholarPubMed
Pohley, W. J. (1976). Relationships among three species of Littorina and their larval Digenea. Marine Biology 37, 179–186.CrossRefGoogle Scholar
Poulin, R. (2006). Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143–151. doi: 10.1017/S0031182005008693.CrossRefGoogle ScholarPubMed
Stenseth, N. C., Ottersen, G., Hurrell, J. W., Mysterud, A., Lima, M., Chan, K-S., Yoccoz, N. G. and Ådlandsvik, B. (2003). Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, El Niño Sourthern Oscillation and beyond. Proceedings of the Royal Society of London, B 270, 2087–2096. doi: 10.1098/rspb.2003.2415.CrossRefGoogle Scholar
Studer, A., Thieltges, D. W. and Poulin, R. (2010). Parasites and global warming: net effects of temperature on an intertidal host – parasite system. Marine Ecology Progress Series 415, 11–22. doi: 10.3354/meps08742.CrossRefGoogle Scholar
Thieltges, D. W. and Reise, K. (2007). Spatial heterogeneity in parasite infections at different spatial scales in an intertidal bivalve. Oecologia 150, 569–581. doi: 10.1007/s00442-006-0557-2.CrossRefGoogle Scholar
Thieltges, D. W. and Rick, J. (2006). Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae). Diseases of Aquatic Organisms 73, 63–68.Google ScholarPubMed
Tompkins, D. M., White, A. R. and Boots, M. (2003). Ecological replacement of native red squirrels by invasive greys driven by disease. Ecology Letters 6, 189–196.CrossRefGoogle Scholar
Watkin, E. E. (1941). The yearly life cycle of the amphipod, Corophium volutator. Journal of Animal Ecology 10, 77–93.CrossRefGoogle Scholar