Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T23:28:06.012Z Has data issue: false hasContentIssue false
  • English
  • Français

Upstream-downstream gradient in infection levels by fish parasites: a common river pattern?

Published online by Cambridge University Press:  12 October 2012

ISABEL BLASCO-COSTA ,
ANSON V. KOEHLER ,
ALICE MARTIN  and
ROBERT POULIN
ISABEL BLASCO-COSTA*
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic
ANSON V. KOEHLER
Affiliation:
Faculty of Veterinary Science, The University of Melbourne, Parkville, Victoria, Australia
ALICE MARTIN
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand
ROBERT POULIN
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand
*
*Corresponding author: Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic. Tel: +420 387775484. E-mail: Isa.Blasco.Costa@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

Physical habitat structure can influence the distribution and abundance of organisms. In rivers, stream drift, a common process originating from the unidirectional water flow, favours the displacement and downstream dispersion of invertebrates. This process could also generate a gradient in infection levels, leading to decreasing numbers of parasites per host as one moves upstream from the river mouth. We tested this hypothesis using 4 trematode species infecting the fish Gobiomorphus breviceps in the Manuherikia River (New Zealand). We analysed the abundance of each trematode infrapopulation as a function of distance from the river junction and fish size by generalized linear models. Our results supported the existence of a longitudinal gradient in trematode abundance along the river with a decreasing downstream-to-upstream continuum. This applied to 3 out of the 4 trematode species studied, suggesting that this might be a common pattern in river populations. Thus, the unidirectional river flow and a major process like drift in lotic systems, that influences the dynamics and distribution of invertebrate hosts, can also affect trematodes. Host properties like habitat preference, and parasite traits, particularly those related to transmission mode can influence the strength of the observed gradient, as may other environmental and biotic factors.

Keywords

trematode abundanceunidirectional river flowinfection patternsdiseaseRiver Continuum ConceptfreshwaterCoitocaecum parvumTelogaster opisthorchisStegodexamene anguillaeApatemon sp
Type
Research Article
Information
Parasitology , Volume 140 , Issue 2 , February 2013 , pp. 266 - 274
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

Allan, B. F., Keesing, F. and Ostfeld, R. S. (2003). Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17, 267–272.CrossRefGoogle Scholar
Allan, J. D. (2007). Stream Ecology. Springer, London/New York.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interactions. 1. Regulatory processes. Journal of Animal Ecology 47, 219–247.CrossRefGoogle Scholar
Arneberg, P. (2001). An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence. Ecography 24, 352–358.CrossRefGoogle Scholar
Arneberg, P., Skorping, A., Grenfell, B. and Read, A. F. (1998). Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London, B, 265, 1283–1289.CrossRefGoogle Scholar
Atkinson, N. K. and Joy, M. K. (2009). Longitudinal size distributions of bluegill bullies (Gobiomorphus hubbsi) and torrentfish (Cheimarrichthys fosteri) in two large New Zealand rivers. New Zealand Journal of Marine and Freshwater Research 43, 643–651.CrossRefGoogle Scholar
Barger, M. A. (2006). Spatial heterogeneity in the parasite communities of creek chub (Semotilus atromaculatus) in southeastern Nebraska. Journal of Parasitology 92, 230–235.CrossRefGoogle ScholarPubMed
Barger, M. A. and Esch, G. W. (2001). Downstream changes in the composition of the parasite community of fishes in an Appalachian stream. Journal of Parasitology 87, 250–255.CrossRefGoogle Scholar
Barker, D. E., Marcogliese, D. J. and Cone, D. K. (1996). On the distribution and abundance of eel parasites in Nova Scotia: Local versus regional patterns. Journal of Parasitology 82, 697–701.CrossRefGoogle ScholarPubMed
Basu, B. K., Kalff, J. and Pinel-Alloul, B. (2000). Midsummer plankton development along a large temperate river: the St. Lawrence River. Canadian Journal of Fisheries and Aquatic Sciences 57, 7–15.CrossRefGoogle Scholar
Benda, L. and Dunne, T. (1997). Stochastic forcing of sediment supply to channel networks from landsliding and debris flow. Water Resources Research 33, 2849–2863.CrossRefGoogle Scholar
Benda, L., Poff, N. L., Miller, D., Dunne, T., Reeves, G., Pess, G. and Pollock, M. (2004). The network dynamics hypothesis: How channel networks structure riverine habitats. Bioscience 54, 413–427.CrossRefGoogle Scholar
Blanar, C. A., Marcogliese, D. J. and Couillard, C. M. (2011). Natural and anthropogenic factors shape metazoan parasite community structure in mummichog (Fundulus heteroclitus) from two estuaries in New Brunswick, Canada. Folia Parasitologica 58, 240–248.CrossRefGoogle ScholarPubMed
Blasco-Costa, I., Waters, J. M. and Poulin, R. (2012). Swimming against the current: Genetic structure, host mobility and the drift paradox in trematode parasites. Molecular Ecology 21, 207–217.CrossRefGoogle ScholarPubMed
Blouin, M. S., Yowell, C. A., Courtney, C. H. and Dame, J. B. (1995). Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141, 1007–1014.CrossRefGoogle ScholarPubMed
Campbell Grant, E. H., Lowe, W. H. and Fagan, W. F. (2007). Living in the branches: population dynamics and ecological processes in dendritic networks. Ecology Letters 10, 165–175.CrossRefGoogle ScholarPubMed
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
Carrara, F., Altermatt, F., Rodriguez-Iturbe, I. and Rinaldo, A. (2012). Dendritic connectivity controls biodiversity patterns in experimental metacommunities. Proceedings of the National Academy of Sciences, USA 109, 5761–5766.CrossRefGoogle ScholarPubMed
Criscione, C. D. and Blouin, M. S. (2004). Life cycles shape parasite evolution: Comparative population genetics of salmon trematodes. Evolution 58, 198–202.Google ScholarPubMed
de Montaudouin, X. and Lanceleur, L. (2011). Distribution of parasites in their second intermediate host, the cockle cerastoderma edule: Community heterogeneity and spatial scale. Marine Ecology Progress Series 428, 187–199.CrossRefGoogle Scholar
Dezfuli, B. S., Rossetti, E., Bellettato, C. M. and Maynard, B. J. (1999). Pomphorhynchus laevis in its intermediate host Echinogammarus stammeri in the River Brenta, Italy. Journal of Helminthology 73, 95–102, 130.CrossRefGoogle Scholar
Elliott, J. M. (2003). A comparative study of the dispersal of 10 species of stream invertebrates. Freshwater Biology 48, 1652–1668.CrossRefGoogle Scholar
Gomi, T., Sidle, R. C. and Richardson, J. S. (2002). Understanding processes and downstream linkages of headwater systems. Bioscience 52, 905–916.CrossRefGoogle Scholar
Greenberg, A. E. (1964). Plankton of the Sacramento River. Ecology 45, 40–49.CrossRefGoogle Scholar
Hall, S. R., Smyth, R., Becker, C. R., Duffy, M. A., Knight, C. J., MacIntyre, S., Tessier, A. J. and Cceres, C. E. (2010). Why are daphnia in some lakes sicker? disease ecology, habitat structure, and the plankton. Bioscience 60, 363–375.CrossRefGoogle Scholar
Hallett, S. L. and Bartholomew, J. L. (2008). Effects of water flow on the infection dynamics of Myxobolus cerebralis. Parasitology 135, 371–384.CrossRefGoogle ScholarPubMed
Hansen, E. K. and Poulin, R. (2006). Spatial covariation between infection levels and intermediate host densities in two trematode species. Journal of Helminthology 80, 255–259.Google ScholarPubMed
Hildrew, A. G. and Townsend, C. R. (1980). Aggregation, interference and foraging by larvae of Plectrocnemia conspersa (Trichoptera: Polycentropodidae). Animal Behaviour 28, 553–560.CrossRefGoogle Scholar
Hopkins, C. L. (1970). Some aspects of the bionomics in a brown trout nursery stream. New Zealand Marine Department of Fisheries Research Bulletin 4, 38.Google Scholar
Hynes, H. B. N. (1970). The Ecology of Running Waters, 1st Edn.Liverpool University Press, Liverpool, UK.Google Scholar
Jakobsen, P. J. and Wedekind, C. (1998). Copepod reaction to odor stimuli influenced by cestode infection. Behavioral Ecology 9, 414–418.CrossRefGoogle Scholar
Kelly, D. W., Paterson, R. A., Townsend, C. R., Poulin, R. and Tompkins, D. M. (2009). Has the introduction of brown trout altered disease patterns in native New Zealand fish? Freshwater Biology 54, 1805–1818.CrossRefGoogle Scholar
Kennedy, C. R. (1990). Helminth communities in freshwater fish: structured communities or stochastic assemblages? In Parasite Communities: Patterns and Processes (ed. Esch, G. W., Bush, A. O. and Aho, J. M.), pp. 131–156. Chapman and Hall, London, UK.CrossRefGoogle Scholar
Kennedy, C. R. (2001). Metapopulation and community dynamics of helminth parasites of eels Anguilla anguilla in the River Exe system. Parasitology 122, 689–698.CrossRefGoogle ScholarPubMed
Krause, R. J., McLaughlin, J. D. and Marcogliese, D. J. (2010). Parasite fauna of Etheostoma nigrum (Percidae: Etheostomatinae) in localities of varying pollution stress in the St. Lawrence River, Quebec, Canada. Parasitology Research 107, 285–294.CrossRefGoogle Scholar
Krkosek, M. (2010). Host density thresholds and disease control for fisheries and aquaculture. Aquaculture Environment Interactions 1, 21–32.CrossRefGoogle Scholar
Krueger, R. C., Kerans, B. L., Vincent, E. R. and Rasmussen, C. (2006). Risk of Myxobolus cerebralis infection to rainbow trout in the Madison River, Montana, USA. Ecological Applications 16, 770–783.CrossRefGoogle ScholarPubMed
Lagrue, C., Kaldonski, N., Motreuil, S., Lefèvre, T., Blatter, O., Giraud, P. and Bollache, L. (2011). Interspecific differences in drift behaviour between the native Gammarus pulex and the exotic Gammarus roeseli and possible implications for the invader's success. Biological Invasions 13, 1409–1421.CrossRefGoogle Scholar
Loot, G., Reyjol, Y., Poulet, N., Simkova, A., Blanchet, S. and Lek, S. (2007). Effects of small weirs on fish parasite communities. Parasitology Research 101, 1265–1276.CrossRefGoogle ScholarPubMed
Louhi, K.-R., Karvonen, A., Rellstab, C. and Jokela, J. (2010). Is the population genetic structure of complex life cycle parasites determined by the geographic range of the most motile host? Infection Genetics and Evolution 10, 1271–1277.CrossRefGoogle ScholarPubMed
Marcogliese, D. J., Compagna, S., Bergeron, E. and McLaughlin, J. D. (2001). Population biology of eyeflukes in fish from a large fluvial ecosystem: the importance of gulls and habitat characteristics. Canadian Journal of Zoology-Revue Canadienne De Zoologie 79, 1102–1113.CrossRefGoogle Scholar
Marcogliese, D. J., Gendron, A. D. and Cone, D. K. (2009). Impact of municipal effluents and hydrological regime on myxozoan parasite communities of fish. International Journal for Parasitology 39, 1345–1351.CrossRefGoogle ScholarPubMed
May, R. M. and Anderson, R. M. (1978). Regulation and stability of host-parasite populations interactions. 2. Destabilizing processes. Journal of Animal Ecology 47, 249–267.CrossRefGoogle Scholar
Maynard, B. J., Wellnitz, T. A., Zanini, N., Wright, W. G. and Dezfuli, B. S. (1998). Parasite-altered behavior in a crustacean intermediate host: Field and laboratory studies. Journal of Parasitology 84, 1102–1106.CrossRefGoogle Scholar
McCahon, C. P., Maund, S. J. and Poulton, M. J. (1991). The effect of the acanthocephalan parasite (Pomphorhynchus laevis) on the drift of its intermediate host (Gammarus pulex). Freshwater Biology 25, 507–513.CrossRefGoogle Scholar
McDowall, R. M. (1990). New Zealand Freshwater Fishes: A Natural History and Guide. 2nd Edn. Heinemann Reed and Maf Publishing Group, Auckland, New Zealand.Google Scholar
Milner, A. M., Taylor, R. C. and Winterbourn, M. J. (2001). Longitudinal distribution of macroinvertebrates in two glacier-fed New Zealand rivers. Freshwater Biology 46, 1765–1775.CrossRefGoogle Scholar
Molyneaux, D. H. (2002). Vector-borne infections and health related to landscape changes. In Conservation medicine: Ecological Health in Practice (ed. Aguirre, A. A., Ostfeld, R. S., Tabor, G. M., House, C. and Pearl, M. C.), pp. 194–206. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Morand, S. and Poulin, R. (1998). Density, body mass and parasite species richness of terrestrial mammals. Evolutionary Ecology 12, 717–727.CrossRefGoogle Scholar
Müller, K. (1954). Investigations on the organic drift in North Swedish streams. Report of the Institute of freshwater research Drottningholm 35, 133–148.Google Scholar
Murray, D. L. (1975). Regional hydrology of the Clutha River. Journal of Hydrology (N.Z.) 14, 83–98.Google Scholar
O'Farrell, I. (1993). Phytoplankton ecology and limnology of the Salado River (Buenos Aires, Argentina). Hydrobiologia 271, 169–178.CrossRefGoogle Scholar
Ostfeld, R. S., Glass, G. E. and Keesing, F. (2005). Spatial epidemiology: an emerging (or re-emerging) discipline. Trends in Ecology & Evolution 20, 328–336.CrossRefGoogle ScholarPubMed
Otago Regional Council (2011). Water Quality and Ecosystem Health in the Manuherikia Catchment. Otago Regional Council Technical Report. Otago Regional Council, Dunedin, New Zealand.Google Scholar
Perry, J. A. and Schaeffer, D. J. (1987). The longitudinal distribution of riverine benthos: A river dis-continuum? Hydrobiologia 148, 257–268.CrossRefGoogle 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.CrossRefGoogle Scholar
Poulin, R., Paterson, R. A., Townsend, C. R., Tompkins, D. M. and Kelly, D. W. (2011). Biological invasions and the dynamics of endemic diseases in freshwater ecosystems. Freshwater Biology 56, 676–688.CrossRefGoogle Scholar
Pounds, J. A., Bustamante, M. R., Coloma, L. A., Consuegra, J. A., Fogden, M. P. L., Foster, P. N., La Marca, E., Masters, K. L., Merino-Viteri, A., Puschendorf, R., Ron, S. R., Sánchez-Azofeifa, G. A., Still, C. J. and Young, B. E. (2006). Widespread amphibian extinctions from epidemic disease driven by global warming. Nature, London 439, 161–167.CrossRefGoogle ScholarPubMed
Prugnolle, F., Liu, H., De Meeûs, T. and Balloux, F. (2005). Population genetics of complex life-cycle parasites: An illustration with trematodes. International Journal for Parasitology 35, 255–263.CrossRefGoogle ScholarPubMed
R Development Core Team (2010). R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Roberts, M. G., Dobson, A. P., Arneberg, P., de Leo, G. A., Krecek, R. C., Manfredi, M. T., Lanfranchi, P. and Zaffaroni, E. (2002). Parasite community ecology and biodiversity. In The Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 63–82. Oxford University Press, New York, USA.CrossRefGoogle Scholar
Sousa, W. P. and Grosholz, E. D. (1990). 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.Google Scholar
Sures, B. and Streit, B. (2001). Eel parasite diversity and intermediate host abundance in the River Rhine, Germany. Parasitology 123, 185–191.CrossRefGoogle ScholarPubMed
Thrush, M. A., Murray, A. G., Brun, E., Wallace, S. and Peeler, E. J. (2011). The application of risk and disease modelling to emerging freshwater diseases in wild aquatic animals. Freshwater Biology 56, 658–675.CrossRefGoogle Scholar
Townsend, C. R. (1989). The patch dynamics concept of stream community ecology. Journal of the North American Benthological Society 8, 36–50.CrossRefGoogle Scholar
Townsend, C. R. and Hildrew, A. G. (1976). Field experiments on the drifting, colonization and continuous redistribution of stream benthos. Journal of Animal Ecology 45, 759–772.CrossRefGoogle Scholar
Vannote, R. L., Minshall, G. W., Cummins, K. W., Sedell, J. R. and Cushing, C. E. (1980). The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences 37, 130–137.CrossRefGoogle Scholar
Walton, O. E. (1980). Invertebrate drift from predator-prey associations. Ecology 61, 1486–1497.CrossRefGoogle Scholar
Waters, T. F. (1961). Standing crop and drift of stream bottom organisms. Ecology 42, 532–537.CrossRefGoogle Scholar
Weichman, M. A. and Janovy, J. Jr (2000). Parasite community structure in Pimephales promelas (Pisces: Cyprinidae) from two converging streams. Journal of Parasitology 86, 654–656.CrossRefGoogle ScholarPubMed
Wellnitz, T., Giari, L., Maynard, B. and Dezfuli, B. S. (2003). A parasite spatially structures its host population. Oikos 100, 263–268.CrossRefGoogle Scholar
Wooster, D. E. (1998). Amphipod (Gammarus minus) responses to predators and predator impact on amphipod density. Oecologia 115, 253–259.CrossRefGoogle ScholarPubMed