Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-22T00:20:09.978Z Has data issue: false hasContentIssue false
  • English
  • Français

Climate change, parasitism and the structure of intertidal ecosystems

Published online by Cambridge University Press:  12 April 2024

R. Poulin  and
K.N. Mouritsen
R. Poulin*
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand:
K.N. Mouritsen
Affiliation:
Department of Marine Ecology, Institute of Biological Sciences, University of Aarhus, Finlandsgade 14, DK-8200 Aarhus N, Denmark
*
*Fax: +64-3-479-7584 E-mail: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Evidence is accumulating rapidly showing that temperature and other climatic variables are driving many ecological processes. At the same time, recent research has highlighted the role of parasitism in the dynamics of animal populations and the structure of animal communities. Here, the likely interactions between climate change and parasitism are discussed in the context of intertidal ecosystems. Firstly, using the soft-sediment intertidal communities of Otago Harbour, New Zealand, as a case study, parasites are shown to be ubiquitous components of intertidal communities, found in practically all major animal species in the system. With the help of specific examples from Otago Harbour, it is demonstrated that parasites can regulate host population density, influence the diversity of the entire benthic community, and affect the structure of the intertidal food web. Secondly, we document the extreme sensitivity of cercarial production in parasitic trematodes to increases in temperature, and discuss how global warming could lead to enhanced trematode infections. Thirdly, the results of a simulation model are used to argue that parasite-mediated local extinctions of intertidal animals are a likely outcome of global warming. Specifically, the model predicts that following a temperature increase of less than 4°C, populations of the amphipod Corophium volutator, a hugely abundant tube-building amphipod on the mudflats of the Danish Wadden Sea, are likely to crash repeatedly due to mortality induced by microphallid trematodes. The available evidence indicates that climate-mediated changes in local parasite abundance will have significant repercussions for intertidal ecosystems. On the bright side, the marked effects of even slight increases in temperature on cercarial production in trematodes could form the basis for monitoring programmes, with these sensitive parasites providing early warning signals of the environmental impacts of global warming.

Type
Research Article
Information
Journal of Helminthology , Volume 80 , Issue 2 , June 2006 , pp. 183 - 191
Copyright
Copyright © Cambridge University Press 2006

References

Albon, S.D., Stien, A., Irvine, R.J., Langvatn, R., Ropstad, E. & Halvorsen, O. (2002) The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society of London B 269, 1625–1632.CrossRefGoogle ScholarPubMed
Babirat, C., Mouritsen, K.N. & Poulin, R. (2004) Equal partnership: two trematode species, not one, manipulate the burrowing behaviour of the New Zealand cockle, Austrovenus stutchburyi. Journal of Helminthology 78, 195–199.CrossRefGoogle Scholar
Beukema, J.J. & Dekker, R. (2005) Decline of recruitment success in cockles and other bivalves in the Wadden Sea: possible role of climate change, predation on postlarvae and fisheries. Marine Ecology Progress Series 287, 149–167.CrossRefGoogle Scholar
Cattadori, I.M., Haydon, D.T. & Hudson, P.J. (2005) Parasites and climate synchronize red grouse populations. Nature 433, 737–741.CrossRefGoogle ScholarPubMed
Christensen, O.B., Christensen, J.H., Machenhauer, B. & Botzet, M. (1998) Very high-resolution regional climate simulations over Scandinavia–present climate. Journal of Climate 11, 3204–3229.2.0.CO;2>CrossRefGoogle Scholar
Christensen, J.H., Raisanen, J., Iversen, T., Bjorge, D., Christensen, O.B. & Rummukainen, M. (2001) A synthesis of regional climate change simulations–a Scandinavian perspective. Geophysical Research Letters 28, 1003–1006.CrossRefGoogle Scholar
Combes, C. (1996) Parasites, biodiversity and ecosystem stability. Biodiversity and Conservation 5, 953–962.CrossRefGoogle Scholar
Donald, K.M., Kennedy, M., Poulin, R. & Spencer, H.G. (2004) Host specificity and molecular phylogeny of larval Digenea isolated from New Zealand and Australian topshells (Gastropoda: Trochidae). International Journal for Parasitology 34, 557–568.CrossRefGoogle ScholarPubMed
Evans, N.A. (1985) The influence of environmental temperature upon transmission of the cercariae of Echinostoma liei (Digenea: Echinostomatidae). Parasitology 90, 269–275.CrossRefGoogle Scholar
Fredensborg, B.L., Latham, A.D.M. & Poulin, R. (2004a) New records of gastrointestinal helminths from the red-billed gull (Larus novaehollandiae scopulinus). New Zealand Journal of Zoology 31, 75–80.CrossRefGoogle Scholar
Fredensborg, B.L., Mouritsen, K.N. & Poulin, R. (2004b) Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. Journal of Experimental Marine Biology and Ecology 311, 253–265.CrossRefGoogle Scholar
Fredensborg, B.L., Mouritsen, K.N. & Poulin, R. (2005) Impact of trematodes on host survival and population density in the intertidal gastropod Zeacumantus subcarinatus. Marine Ecology Progress Series 290, 109–117.CrossRefGoogle Scholar
Harvell, C.D., Kim, K., Burkholder, J.M., Colwell, R.R., Epstein, P.R., Grimes, D.J., Hofmann, E.E., Lipp, E.K., Osterhaus, A.D.M.E., Overstreet, R.M., Porter, J.W., Smith, G.W. & Vasta, G.R. (1999) Emerging marine diseases: climate links and anthropogenic factors. Science 285, 1505–1510.CrossRefGoogle ScholarPubMed
Harvell, C.D., Mitchell, C.E., Ward, J.R., Altizer, S., Dobson, A.P., Ostfeld, R.S. & Samuel, M.D. (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162.CrossRefGoogle ScholarPubMed
Holmgren, M., Scheffer, M., Ezcurra, E., Gutierrez, J.R. & Mohren, G.M.J. (2001) El Niño effects on the dynamics of terrestrial ecosystems. Trends in Ecology and Evolution 16, 89–94.CrossRefGoogle ScholarPubMed
Hudson, P.J., Dobson, A.P. & Newborn, D. (1998) Prevention of population cycles by parasite removal. Science 282, 2256–2258.CrossRefGoogle ScholarPubMed
Huxham, M., Raffaelli, D. & Pike, A. (1995) Parasites and food web patterns. Journal of Animal Ecology 64, 168–176.CrossRefGoogle Scholar
Jensen, K.T., Latama, G. & Mouritsen, K.N. (1996) The effect of larval trematodes on the survival rates of two species of mud snails (Hydrobiidae) experimentally exposed to desiccation, freezing and anoxia. Helgoländer Meeresuntersuchungen 50, 327–335.CrossRefGoogle Scholar
Jensen, K.T. & 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. & Mouritsen, K.N. (1998) The influence of the trematode Microphallus claviformis on two congeneric intermediate host species (Corophium): infection characteristics and host survival. Journal of Experimental Marine Biology and Ecology 227, 35–48.CrossRefGoogle Scholar
Lafferty, K.D. (1997) Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitology Today 13, 251–255.CrossRefGoogle ScholarPubMed
Lafferty, K.D., Porter, J.W. & Ford, S.E. (2004) Are diseases increasing in the ocean? Annual Review of Ecology, Evolution and Systematics 35, 31–54.CrossRefGoogle Scholar
Latham, A.D.M. & Poulin, R. (2002a) New records of gastrointestinal helminths from the southern black-backed gull (Larus dominicanus) in New Zealand. New Zealand Journal of Zoology 29, 253–257.CrossRefGoogle Scholar
Latham, A.D.M. & Poulin, R. (2002b) Field evidence of the impact of two acanthocephalan parasites on the mortality of three species of New Zealand shore crabs (Brachyura). Marine Biology 141, 1131–1139.Google Scholar
Lauckner, G. (1987) Ecological effects of larval trematode infestations on littoral marine invertebrate populations. International Journal for Parasitology 17, 391–398.CrossRefGoogle Scholar
Lo, C.-T. Lee, K.-M. (1996) Pattern of emergence and the effects of temperature and light on the emergence and survival of heterophyid cercariae (Centrocestus formosanus and Haplorchis pumilio). Journal of Parasitology 82, 347–350.CrossRefGoogle ScholarPubMed
Marcogliese, D.J. (2001) Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 1331–1352.CrossRefGoogle Scholar
McCarthy, A.M. (1999) The influence of temperature on the survival and infectivity of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 118, 383–388.CrossRefGoogle ScholarPubMed
Meissner, K. & Bick, A. (1997) Population dynamics and ecoparasitological surveys of Corophium volutator in coastal waters in the Bay of Mecklenburg (southern Baltic Sea). Diseases of Aquatic Organisms 29, 169–179.CrossRefGoogle Scholar
Meissner, K. & Bick, A. (1999) Mortality of Corophium volutator (Amphipoda) caused by infestation with Maritrema subdolum (Digenea, Microphallidae): laboratory studies. Diseases of Aquatic Organisms 35, 47–52.CrossRefGoogle Scholar
Minchella, D.J. & Scott, M.E. (1991) Parasitism: a cryptic determinant of animal community structure. Trends in Ecology and Evolution 6, 250–254.CrossRefGoogle ScholarPubMed
Moravec, F., Fredensborg, B.L., Latham, A.D.M. & Poulin, R. (2003) Larval Spirurida (Nematoda) from the crab Macrophthalmus hirtipes in New Zealand. Folia Parasitologica 50, 109–114.CrossRefGoogle ScholarPubMed
Mouritsen, K.N. (2002a) The parasite-induced surfacing behaviour in the cockle Austrovenus stutchburyi: a test of an alternative hypothesis and identification of potential mechanisms. Parasitology 124, 521–528.CrossRefGoogle ScholarPubMed
Mouritsen, K.N. (2002b) 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.CrossRefGoogle ScholarPubMed
Mouritsen, K.N. & Jensen, K.T. (1994) The enigma of gigantism: effect of larval trematodes on growth, fecundity, egestion and locomotion in Hydrobia ulvae (Pennant) (Gastropoda: Prosobranchia). Journal of Experimental Marine Biology and Ecology 181, 53–66.CrossRefGoogle Scholar
Mouritsen, K.N. & 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. & Poulin, R. (2002a) Parasitism, climate oscillations and the structure of natural communities. Oikos 97, 462–468.CrossRefGoogle Scholar
Mouritsen, K.N. & Poulin, R. (2002b) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124, S101–S117.CrossRefGoogle ScholarPubMed
Mouritsen, K.N. & Poulin, R. (2005a) Parasites boost biodiversity and change animal community structure by trait-mediated indirect effects. Oikos 108, 344–350.CrossRefGoogle Scholar
Mouritsen, K.N. & Poulin, R. (2005b) Parasitism can influence the intertidal zonation of non-host organisms. Marine Biology 148, 1–11.CrossRefGoogle Scholar
Mouritsen, K.N., Mouritsen, L.T. & Jensen, K.T. (1998) Changes 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 UK 78, 1167–1180.CrossRefGoogle Scholar
Mouritsen, K.N., McKechnie, S., Meenken, E., Toynbee, J.L. & 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 UK 83, 307–310.CrossRefGoogle Scholar
Mouritsen, K.N., Tompkins, D.M. & Poulin, R. (2005) Climate warming may cause a parasite-induced collapse in coastal amphipod populations. Oecologia 146, 476–483.CrossRefGoogle Scholar
Mysterud, A., Stenseth, N.C., Yoccoz, N.G., Langvatn, R. & Steinheim, G. (2001) Nonlinear effects of large-scale climatic variability on wild and domestic herbivores. Nature 410, 1096–1099.CrossRefGoogle ScholarPubMed
Ottersen, G., Planque, B., Belgrano, A., Post, E., Reid, P.C. & Stenseth, N.C. (2001) Ecological effects of the North Atlantic Oscillation. Oecologia 128, 1–14.CrossRefGoogle ScholarPubMed
Patz, J.A., Graczyk, T.K., Geller, N. & Vittor, A.Y. (2000) Effect of environmental change on emerging parasitic diseases. International Journal for Parasitology 30, 1395–1405.CrossRefGoogle ScholarPubMed
Pearson, E.J. & Cheng, T.C. (1985) Studies on parasitic castration: occurrence of a gametogenesis-inhibiting factor in extract of Zoogonus lasius (Trematoda). Journal of Invertebrate Pathology 46, 239–246.CrossRefGoogle Scholar
Pechenik, J.A. & Fried, B. (1995) Effect of temperature on survival and infectivity of Echinostoma trivolvis cercariae: a test of the energy limitation hypothesis. Parasitology 111, 373–378.CrossRefGoogle Scholar
Pechenik, J.A., Fried, B. & Simpkins, H.L. (2001) Crepidula fornicata is not a first intermediate host for trematodes: who is? Journal of Experimental Marine Biology and Ecology 261, 211–224.CrossRefGoogle Scholar
Phoenix, G.K. & Lee, J.A. (2004) Predicting impacts of Arctic climate change: past lessons and future challenges. Ecological Research 19, 65–74.CrossRefGoogle Scholar
Poulin, R. (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143–151.CrossRefGoogle ScholarPubMed
Poulin, R. & Mouritsen, K.N. (2003) Large-scale determinants of trematode infections in intertidal gastropods. Marine Ecology Progress Series 254, 187–198.CrossRefGoogle Scholar
Poulin, R., Nichol, K. & Latham, A.D.M. (2003) Host sharing and host manipulation by larval helminths in shore crabs: cooperation or conflict? International Journal for Parasitology 33, 425–433.CrossRefGoogle ScholarPubMed
Poulin, R., Steeper, M.J. & Miller, A.A. (2000) Non-random patterns of host use by the different parasite species exploiting a cockle population. Parasitology 121, 289–295.CrossRefGoogle ScholarPubMed
Schmidt-Nielsen, K. (1997) Animal physiology: adaptation and environment. 5th edn. Cambridge, Cambridge University Press.CrossRefGoogle Scholar
Scott, M.E. (1987) Regulation of mouse colony abundance by Heligmosomoides polygyrus. Parasitology 95, 111–124.CrossRefGoogle ScholarPubMed
Sousa, W.P. (1983) Host life history and the effect of parasitic castration on growth: a field study of Cerithidea californica Haldemann (Gastropoda: Prosobranchia) and its trematode parasites. Journal of Experimental Marine Biology and Ecology 73, 273–296.CrossRefGoogle Scholar
Sousa, W.P. (1991) Can models of soft-sediment community structure be complete without parasites? American Zoologist 31, 821–830.CrossRefGoogle Scholar
Stenseth, N.C., Mysterud, A., Ottersen, G., Hurrell, J.W., Chan, K.-S. Lima, M. (2002) Ecological effects of climate fluctuations. Science 297, 1292–1296.CrossRefGoogle ScholarPubMed
Stenseth, N.C., Ottersen, G., Hurrell, J.W., Mysterud, A., Lima, M., Chan, K.-S. Yoccoz, N.G. & Adlandsvik, B. (2003) Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, El Niño Southern Oscillation and beyond. Proceedings of the Royal Society of London B 270, 2087–2096.CrossRefGoogle ScholarPubMed
Thomas, F. & Poulin, R. (1998) Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance? Parasitology 116, 431–436.CrossRefGoogle ScholarPubMed
Thomas, F., Renaud, F., de Meeûs, T. Poulin, R. (1998) Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone? Proceedings of the Royal Society of London B 265, 1091–1096.CrossRefGoogle Scholar
Thomas, F., Renaud, F. & Guégan, J.-F. (2005) Parasitism and ecosystems. Oxford, Oxford University Press.CrossRefGoogle Scholar
Thompson, R.M., Mouritsen, K.N. & Poulin, R. (2005) Importance of parasites and their life cycle characteristics in determining the structure of a large marine food web. Journal of Animal Ecology 74, 77–85.CrossRefGoogle Scholar
Umadevi, K. & Madhavi, R. (1997) Effects of light and temperature on the emergence of Haplorchis pumilio cercariae from the snail host, Thiara tuberculata. Acta Parasitologica 42, 12–16.Google Scholar
Vaughan, D.G., Marshall, G.J., Connolley, W.M., Parkinson, C., Mulvaney, R., Hodgson, D.A., King, J.C., Pudsey, C.J. & Turner, J. (2003) Recent rapid regional climate warming on the Antarctic Peninsula. Climatic Change 60, 243–274.CrossRefGoogle Scholar
Walther, G.-R. Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C., Fromentin, J.-M., Hoegh-Guldberg, O. & Bairlein, F. (2002) Ecological responses to recent climate change. Nature 416, 389–395.CrossRefGoogle ScholarPubMed
Willmer, P., Stone, G. & Johnston, I. (2000) Environmental physiology of animals. Oxford, Blackwell Science.Google Scholar