Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-19T22:10:26.651Z Has data issue: false hasContentIssue false

Impacts of agriculture on the parasite communities of northern leopard frogs (Rana pipiens) in southern Quebec, Canada

Published online by Cambridge University Press:  03 August 2007

K. C. KING*
Affiliation:
Department of Biology, Concordia University, Montreal, Quebec, Canada H3G 1M8
J. D. McLAUGHLIN
Affiliation:
Department of Biology, Concordia University, Montreal, Quebec, Canada H3G 1M8
A. D. GENDRON
Affiliation:
Fluvial Ecosystem Research Section, Aquatic Ecosystem Protection Research Division, Water Science and Technology Directorate, Science and Technology Branch, St. Lawrence Centre, Environment Canada, 105 rue McGill, Montreal, Quebec, Canada H2Y 2E7
B. D. PAULI
Affiliation:
Canadian Wildlife Service, National Wildlife Research Centre, Carleton University, Ottawa, Ontario, Canada K1A 0H3
I. GIROUX
Affiliation:
Ministère du Développement durable, de l'Environnement et des Parcs, Direction du suivi de l'état de l'environnement, Service de l'information sur les milieux aquatiques, 675 boul. René-Lévesque Est, Montreal, Quebec, Canada G1R 5V7
B. RONDEAU
Affiliation:
Quebec Water Quality Monitoring and Surveillance Section, Water Quality Monitoring and Surveillance Science and Technology Branch, Environment Canada, 105 McGill, 7th floor, Montreal, Quebec, Canada H2Y 2E7
M. BOILY
Affiliation:
Centre TOXEN, Université du Quèbec á Montréal, 141 ave. Président Kennedy, Montreal, Quebec, Canada H2X 3Y7
P. JUNEAU
Affiliation:
Department of Biological Sciences-TOXEN, Université du Quèbec à Montréal, C.P. 8888, Succ. Centre-ville, Montreal, Quebec, Canada H3C 3PB
D. J. MARCOGLIESE
Affiliation:
Fluvial Ecosystem Research Section, Aquatic Ecosystem Protection Research Division, Water Science and Technology Directorate, Science and Technology Branch, St. Lawrence Centre, Environment Canada, 105 rue McGill, Montreal, Quebec, Canada H2Y 2E7
*
*Corresponding author: Present address, Department of Biology, Indiana University, Jordan Hall 142, 1001 East Third Street, Bloomington, Indiana 47405, USA. Tel: +812 855 3282. E-mail: [email protected]

Summary

Given that numerous amphibians are suffering population declines, it is becoming increasingly important to examine the relationship between disease and environmental disturbance. Indeed, while many studies relate anthropogenic activity to changes in the parasitism of snails and fishes, little is known of the impact on the parasites of amphibians, particularly from agriculture. For 2 years, the parasite communities of metamorphic northern leopard frogs from 7 agricultural wetlands were compared with those from 2 reference wetlands to study differences in parasite community diversity and abundance of various species under pristine conditions and 3 categories of disturbance: only agricultural landscape, only pesticides, and agricultural landscape with pesticides. Agricultural (and urban) area was negatively related to species richness, and associated with the near absence of adult parasites and species that infect birds or mammals. We suggest that agriculture and urbanization may hinder parasite transmission to frogs by limiting access of other vertebrate hosts of their parasites to wetlands. The only parasite found at all localities was an unidentified echinostome infecting the kidneys. This parasite dominated communities in localities surrounded by the most agricultural land, suggesting generalist parasites may persist in disrupted habitats. Community composition was associated with dissolved organic carbon and conductivity, but few links were found with pesticides. Pollution effects may be masked by a strong impact of land use on parasite transmission.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2007

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

Amezaga, J. M., Santamaría, L. and Green, A. J. (2002). Biotic wetland connectivity – supporting a new approach for wetland policy. Acta Oecologica 23, 213222.CrossRefGoogle Scholar
Beasley, V. R., Faeh, S. A., Wikoff, B., Staehle, C., Eisold, J., Nichols, D., Cole, R., Schotthoefer, A. M., Greenwell, M. and Brown, L. E. (2005). Risk factors and declines in northern cricket frogs (Acris crepitans). In Declining Amphibians: a United States Response to the Global Phenomenon (ed. Lannoo, M. J.), pp. 7586. University of California Press, Berkeley, USA.CrossRefGoogle Scholar
Beaven, L., Sadler, J. and Pinder, C. (2001). The invertebrate fauna of a physically modified urban river. Hydrobiologia 445, 97108.CrossRefGoogle Scholar
Bradley, C. A. and Altizer, S. (2006). Urbanization and the ecology of wildlife diseases. Trends in Ecology and Evolution 22, 95102.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, 575583.CrossRefGoogle Scholar
Canadian Council of Ministers of the Environment. (2001). Canadian Water Quality Guidelines (CWQG) for the Protection of Aquatic Life. Environment Canada, Ottawa.Google Scholar
Carey, C., Bradford, D. F., Brunner, J. L., Collins, J. P., Davidson, E. W., Longcore, J. E., Ouellet, M., Pessier, A. P. and Schock, D. M. (2003). Biotic factors in amphibian population declines. In Amphibian Decline: An Integrated Analysis of Multiple Stressor Effects (ed. Linder, G. L., Krest, S. and Sparling, D.), pp. 153208. Society of Environmental Toxicology and Chemistry (SETAC), Pensacola, FL, USA.Google Scholar
Carey, C. and Bryant, C. J. (1995). Possible interrelations among environmental toxicants, amphibian development, and decline of amphibian populations. Environmental Health Perspectives 103 (Suppl.), S13S17.Google ScholarPubMed
Carpenter, S. R., Caraco, N. F., Correll, D. L., Howarth, R. W., Sharpley, A. N. and Smith, V. H. (1998). Non-point pollution of surface waters with phosphorus and nitrogen. Ecological Applications 8, 559568.CrossRefGoogle Scholar
Carrier, S. (2001). National Laboratory for Environmental Testing, 2001–02 Sample Collection Summary. Environment Canada, National Water Research Institute, Burlington/Saskatoon.Google Scholar
Christin, M. S., Gendron, A. D., Brousseau, P., Menard, L., Marcogliese, D. J., Cyr, D., Ruby, S. and Fournier, M. (2003). Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environmental Toxicology and Chemistry 22, 11271133.CrossRefGoogle ScholarPubMed
Christin, M. S., Ménard, L., Gendron, A. D., Ruby, S., Cyr, D., Marcogliese, D. J., Rollins-Smith, L. and Fournier, M. (2004). Effects of agricultural pesticides on the immune system of Xenopus laevis and Rana pipiens. Aquatic Toxicology 67, 3343.CrossRefGoogle ScholarPubMed
Clarke, A. H. (1981). The Freshwater Molluscs of Canada. National Museums of Canada, Ottawa.CrossRefGoogle Scholar
Cone, D. K., Marcogliese, D. J. and Watt, W. D. (1993). Metazoan parasite communities of yellow eels (Anguilla rostrata) in acidic and limed rivers of Nova Scotia. Canadian Journal of Zoology 71, 177184.CrossRefGoogle Scholar
Conover, W. J. and Iman, R. L. (1981). Rank transformations as a bridge between parametric and nonparametric statistics. American Statistician 35, 124136.Google Scholar
Czech, H. A. and Parsons, K. C. (2002). Agricultural wetlands and waterbirds: a review. Waterbirds 25 (Special Publication 2), 2541.Google Scholar
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2003). Infectious disease and amphibian population declines. Diversity and Distributions 9, 141150.CrossRefGoogle Scholar
Davies, P. E. and Nelson, M. (1994). Relationships between riparian buffer widths and the effects of logging on stream habitat, invertebrate community composition and fish abundance. Australian Journal of Marine and Freshwater Research 45, 12891305.CrossRefGoogle Scholar
Desroches, J. F. and Rodrigue, D. (2004). Amphibiens et reptiles du Québec et des maritimes. Éditions Michel Quintin, Waterloo.Google Scholar
Gendron, A. D., Marcogliese, D. J., Barbeau, S., Christin, M. S., Brousseau, P., Ruby, S., Cyr, D. and Fournier, M. (2003). Exposure of leopard frogs to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae. Oecologia 135, 469476.CrossRefGoogle ScholarPubMed
Gibbs, J. P. (2000). Wetland loss and biodiversity conservation. Conservation Biology 14, 314317.CrossRefGoogle Scholar
Gilbertson, M. K., Haffner, G. D., Drouillard, K. G., Albert, A. and Dixon, B. (2003). Immunosuppression in the northern leopard frog (Rana pipiens) induced by pesticide exposure. Environmental Toxicology and Chemistry 22, 101110.Google Scholar
Gillilland, M. G. III and Muzzall, P. M. (1999). Helminths infecting froglets of the northern leopard frog (Rana pipiens) from Foggy Bottom Marsh, Michigan. Journal of the Helminthological Society of Washington 66, 7377.Google Scholar
Giroux, I. (1999). Contamination de l'eau par les Pesticides dans les Régions de Culture de Maïs et de Soya au Québec. Direction des écosystèmes aquatiques, Ministère de l'Environnement, Quebec.Google Scholar
Giroux, I. (2002). Contamination de l'eau par les Pesticides dans les Régions de Culture de Maïs et de Soya au Québec. Direction des écosystèmes aquatiques, Ministère de l'Environnement, Quebec.Google Scholar
Goater, T. M. and Goater, C. P. (2001). Ecological monitoring and assessment network: Protocols for measuring biodiversity: Parasites of amphibians and reptiles. http://www.eman-rese.ca/eman/ecotools/protocols/terrestrial/herp_parasites/intro.htmlGoogle Scholar
Green, D. M. (2005). The biology of amphibian declines. In Declining Amphibians: a United States Response to the Global Phenomenon (ed. Lannoo, M. J.), pp. 5872. University of California Press, Berkeley, USA.Google Scholar
Hamann, M. I., Kehr, A. I. and González, C. E. (2006). Species affinity and infracommunity ordination of helminths of Leptodactylus chaqensis (Anura: Letpdactylidae) in two contrasting environments from northeastern Argentina. Journal of Parasitology 92, 11711179.CrossRefGoogle ScholarPubMed
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, 10591066.Google ScholarPubMed
Hernandez, A. D., Bunnel, J. F. and Sukhdeo, M. V. K. (2007). Composition and diversity patterns in metazoan parasite communities and anthropogenic disturbance in stream ecosystems. Parasitology 134, 91102.CrossRefGoogle ScholarPubMed
Heyer, R. A., Donnelly, M. A., McDiarmid, R. W., Hayek, L.-A. C. and Foster, M. S. (1994). Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians. Smithsonian Institution Press, Washington.Google Scholar
Houlahan, J. E. and Findlay, C. S. (2003). The effects of adjacent land use on wetland amphibian species richness and community composition. Canadian Journal of Fisheries and Aquatic Sciences 60, 10781094.CrossRefGoogle Scholar
Hudson, P. J., Dobson, A. P. and Lafferty, K. D. (2006). Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 7, 381385.CrossRefGoogle Scholar
Hudson, P. J., Dobson, A. P. and Newborn, D. (1998). Prevention of population cycles by parasite removal. Science 282, 22562258.Google Scholar
Huspeni, T. C. and Lafferty, K. D. (2004). Using larval trematodes that parasitize snails to evaluate a saltmarsh restoration project. Ecological Applications 14, 795804.Google Scholar
Johnson, P. T. J. and Chase, J. M. (2004). Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecology Letters 7, 521526.Google Scholar
Jones, J. J., Lortie, J. P. and Pierce, U. D. (1988). The Identification and Management of Significant Fish and Wildlife Resources in Southern Coastal Maine. Maine Department of Inland Fisheries and Wildlife, Augusta,, USA.Google Scholar
Jones, E. B. D., Helfman, G. S., Harper, J. O. and Bolstad, P. V. (1999). Effects of riparian forest removal on fish assemblages in southern Appalachian streams. Conservation Biology 13, 14541465.Google Scholar
Keas, B. and Blankespoor, H. D. (1997). The prevalence of cercariae from Stagnicola emarginata over 50 years in Northern Michigan. Journal of Parasitology 83, 536540.CrossRefGoogle ScholarPubMed
Kennedy, C. R. (1997). Freshwater fish parasites and environmental quality: an overview and caution. Parassitologia 39, 249254.Google Scholar
Khan, R. A. and Thulin, J. (1991). Influence of pollution on parasites of aquatic animals. Advances in Parasitology 30, 201238.CrossRefGoogle ScholarPubMed
Kiesecker, J. M. (2002). Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proceedings of the National Academy of Sciences, USA 99, 99009904.CrossRefGoogle ScholarPubMed
Kiesecker, J. M., Belden, L. K., Katriona, S. and Rubbo, M. J. (2004). Amphibian decline and emerging disease: What can sick frogs teach us about new and resurgent diseases in human populations and other species of wildlife? American Scientist 92, 139147.Google Scholar
Kiesecker, J. M., Blaustein, A. R. and Belden, L. K. (2001). Complex causes of amphibian population declines. Nature, London 410, 681684.Google Scholar
Koprivnikar, J., Forbes, M. R. and Baker, R. L. (2006 a). Environmental factors influencing trematode prevalence in the grey tree frog (Hyla versicolor) tadpoles in southern Ontario. Journal of Parasitology 92, 9971001.CrossRefGoogle ScholarPubMed
Koprivnikar, J., Forbes, M. R. and Baker, R. L. (2006 b). Effects of atrazine on cercarial longevity, activity, and infectivity. Journal of Parasitology 92, 306311.CrossRefGoogle ScholarPubMed
Kostadinova, A. and Gibson, D. I. (2000). The systematics of the echinostomes. In Echinostomes as Experimental Models for Biological Research (ed. Fried, B. and Graczyk, T. K.), pp. 3157. Kluwer, Dordrecht, The Netherlands.CrossRefGoogle Scholar
Kuris, A. M. and Lafferty, K. D. (1994). Community structure: larval trematodes in snail hosts. Annual Review of Ecology and Systematics 25, 189217.Google Scholar
Laboratoire du Centre Saint-Laurent. (1994). Manuel des Méthodes d'Analyse: Partie 1 (Analyses Physico-Chimiques). Partie 2 (Analyse des Paramètres Inorganiques). Environnement Canada, Conservation de l'environnement, Centre Saint-Laurent, Montreal.Google Scholar
Lafferty, K. D. (1997). Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitology Today 13, 251255.Google Scholar
Lafferty, K. D. and Holt, R. D. (2003). How should environmental stress affect the population dynamics of disease? Ecology Letters 6, 654664.CrossRefGoogle Scholar
Lafferty, K. D. and Kuris, A. M. (1999). How environmental stress affects the impacts of parasites. Limnology and Oceanography 44, 925931.CrossRefGoogle Scholar
Lafferty, K. D. and Kuris, A. M. (2005). Parasitism and environmental disturbances. In Parasitism and Ecosystems (ed. Thomas, F, Guégan, J. F. and Renaud, F.), pp. 113123. Oxford University Press, London.CrossRefGoogle Scholar
Laurila, A., Pakkasmaa, S., Crochet, P. A. and Merilä, J. (2002). Predator-induced plasticity in early life-history and morphology in two anuran amphibians. Oecologia 132, 524530.CrossRefGoogle ScholarPubMed
Laurila, A., Pakkasmaa, S. and Merilä, J. (2001). Influence of seasonal time constraints on growth and development of common frog tadpoles: a photoperiod experiment. Oikos 95, 451460.Google Scholar
Leclair, R. and Castanet, J. (1987). Skeletochronological assessment of age and growth in the frog Rana pipiens Schreber (Amphibia, Anura) from Southwestern Quebec. Copeia 2, 361369.CrossRefGoogle Scholar
Legendre, P. and Legendre, L. (1998). Numerical Ecology, 2nd Edn. Elsevier, Oxford.Google Scholar
Lemieux, C., Quémerais, B. and Lum, K. R. (1995). Seasonal patterns of atrazine loading for the St. Lawrence River (Canada) and its tributaries. Water Research 29, 14911504.CrossRefGoogle Scholar
Loman, J. and Lardner, B. (2006). Does pond quality limit frogs Rana arvalis and Rana temporaria in agricultural landscapes? A field experiment. Journal of Applied Ecology 43, 690700.Google Scholar
MacKenzie, K., Williams, H. H., Williams, B., McVicar, A. H. and Siddall, R. (1995). Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Advances in Parasitology 35, 85114.CrossRefGoogle ScholarPubMed
MacKenzie, K. (1999). Parasites as pollution indicators in marine ecosystems: a proposed early warning system. Marine Pollution Bulletin 38, 955959.CrossRefGoogle Scholar
Magurran, A. E. (1988). Ecological Diversity and Its Measurement. Princeton University Press, Princeton, USA.CrossRefGoogle Scholar
Marcogliese, D. J. (2003). Food webs and biodiversity: are parasites the missing link? Journal of Parasitology (Suppl.) 89, S106S113.Google Scholar
Marcogliese, D. J. (2004). Parasites: small players with crucial roles in the ecological theatre. Ecohealth 1, 151164.Google Scholar
Marcogliese, D. J. (2005). Parasites of the superorganism: are they indicators of ecosystem health? International Journal for Parasitology 35, 705716.CrossRefGoogle ScholarPubMed
Marcogliese, D. J., Ball, M. and Lankester, M. W. (2001). Potential impacts of clearcutting on parasites of minnows in small boreal lakes. Folia Parasitologica 48, 269274.Google Scholar
Marcogliese, D. J. and Cone, D. K. (1997). Parasite communities as indicators of ecosystem stress. Parassitologia 39, 227232.Google Scholar
Marcogliese, D. J., Gagnon Brambilla, L., Gagné, F. and Gendron, A. D. (2005). Joint effects of parasitism and pollution on biomarkers of oxidative stress in yellow perch (Perca flavescens). Diseases of Aquatic Organisms 63, 7784.Google Scholar
Marcogliese, D. J., Gendron, A. D., Plante, C., Fournier, M. and Cyr, D. (2006). Parasites of spottail shiners (Notropis hudsonius) in the St. Lawrence River: effects of municipal effluents and habitat. Canadian Journal of Zoology 84, 14611481.CrossRefGoogle Scholar
Matson, P. A., Parton, W. J., Power, A. G. and Swift, M. J. (1997). Agricultural intensification and ecosystem properties. Science 277, 504509.CrossRefGoogle ScholarPubMed
McAlpine, D. F. and Burt, M. D. B. (1998). Helminths of bullfrogs (Rana catesbeiana), green frogs (Rana clamitans), and leopard frogs (Rana pipiens) in New Brunswick. Canadian Field-Naturalist 112, 5068.CrossRefGoogle Scholar
McDonald, M. E. (1969). Annotated Bibliography of Helminths of Waterfowl (Anatidae). Bureau of Sport Fisheries and Wildlife Special Scientific Report No. 125, Washington.Google Scholar
McKenzie, V. J. (2007). Human land use and patterns of parasitism in tropical amphibian hosts. Biological Conservation 137, 102116.Google Scholar
McMahon, R. F. and Bogan, A. E. (2001). Mollusca: Bivalvia. In Ecology and Classification of North American Freshwater Invertebrates, 2nd Edn (ed. Thorp, J. H. and Covich, A. P.), pp. 297325. Academic Press, San Diego, USA.Google Scholar
Moore, A. A. and Palmer, M. A. (2005). Invertebrate biodiversity in agricultural and urban headwater streams: implications for conservation and management. Ecological Applications 15, 11691177.CrossRefGoogle Scholar
Muzzall, P. M. (2005). Parasites of Amphibians and Reptiles from Michigan: A Review of the Literature 1916–2003. Fisheries Research Report No. 2077. State of Michigan Department of Natural Resources, Ann Arbor, USA.Google Scholar
Environment Canada. (2005). A Literature Review of Risks and Benefits of Agriculture to Biodiversity and Biodiversity to Agriculture. National Agri-Environmental Standards Initiative Technical Series Report 1–15, Gatineau,, Canada.Google Scholar
Olsen, O. W. (1974). Animal Parasites: Their Life Cycles and Ecology, 3rd Edn. University Park Press, Baltimore, USA.Google Scholar
Overstreet, R. M. and Howse, H. D. (1977). Some parasites and diseases of estuarine fishes in polluted habitats of Mississippi. Annals of the New York Academy of Sciences 298, 437462.CrossRefGoogle Scholar
Pietrock, M. and Marcogliese, D. J. (2003). Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293298.CrossRefGoogle ScholarPubMed
Poulin, R. (1992). Toxic pollution and parasitism in freshwater fish. Parasitology Today 8, 5861.Google Scholar
Prudhoe, S. and Bray, R. A. (1982). Platyhelminth Parasites of the Amphibia. Oxford University Press, London.Google Scholar
Rau, M. E., Doyle, J. and Gordon, D. (1978). Les parasites des animaux sauvages du Québec. 2. Les parasites des grenouilles et des serpents de la région de l'Île Perrot. Le Naturaliste Canadien 105, 5657.Google Scholar
Relyea, R. A. (2004). Growth and survival of five amphibian species exposed to combinations of pesticides. Environmental Toxicology and Chemistry 23, 17371742.CrossRefGoogle ScholarPubMed
Schotthoefer, A. M., Cole, R. A. and Beasley, V. R. (2003). Relationship of tadpole stage to location of echinostome cercariae encystment and the consequences for tadpole survival. Journal of Parasitology 89, 475482.Google Scholar
Scott, D. E. (1990). Effect of larval density of Ambystoma opacum: an experiment in large-scale field enclosures. Ecology 71, 296306.CrossRefGoogle Scholar
Seburn, C. N. L. and Seburn, D. C. (1998). Status Report: Northern Leopard Frog Rana pipiens (Western Population). Committee on the Status of Endangered Wildlife in Canada, Ottawa.Google Scholar
Semlitsch, R. D. and Bodie, J. R. (2003). Biological criteria for buffer zones around wetlands and riparian habitats for amphibians and reptiles. Conservation Biology 17, 12191228.CrossRefGoogle Scholar
Semlitsch, R. D., Scott, D. E. and Pechmann, J. H. K. (1988). Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69, 184192.CrossRefGoogle Scholar
Shirley, S. M. and Smith, J. N. M. (2005). Bird community structure across riparian buffer strips of varying width in a coastal temperature forest. Biological Conservation 125, 475489.CrossRefGoogle Scholar
Skelly, D. K., Bolden, S. R., Holland, M. P., Freidenburg, L. K., Freidenfelds, N. A. and Malcolm, T. R. (2005). Urbanization and disease in amphibians. In Disease Ecology: Community Structure and Pathogen Dynamics (ed. Collinge, S. K. and Ray, C.), pp. 153167. Oxford University Press, Oxford.Google Scholar
Smith, N. F. (2001). Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts. Oecologia 127, 115122.Google Scholar
Ter Braak, C. J. F. and Šmilauer, P. (1998). CANOCO Reference Manual and User's Guide to Canoco for Windows: Software for Canonical Community Ordination (Version 4.0). Centre for Biometry, Wageningen, The Netherlands.Google Scholar
Wetzel, R. G. (2001). Limnology. Saunders College Publishing, Philadelphia, USA.Google Scholar
Wissel, B., Boeing, W. J. and Ramcharan, C. W. (2003). Effects of water color on predation regimes and zooplankton assemblages in freshwater lakes. Limnology and Oceanography 48, 19651976.CrossRefGoogle Scholar