Title: TROPHIC CASCADES, NUTRIENTS, AND LAKE PRODUCTIVITY: WHOLE-LAKE EXPERIMENTS
Abstract: Ecological MonographsVolume 71, Issue 2 p. 163-186 Article TROPHIC CASCADES, NUTRIENTS, AND LAKE PRODUCTIVITY: WHOLE-LAKE EXPERIMENTS Stephen R. Carpenter, Stephen R. Carpenter Center for Limnology, University of Wisconsin, Madison, Wisconsin 53706 USA Corresponding author. E-mail: [email protected]Search for more papers by this authorJonathan J. Cole, Jonathan J. Cole Institute of Ecosystem Studies, Millbrook, New York 12545 USASearch for more papers by this authorJames R. Hodgson, James R. Hodgson Department of Biology, Saint Norbert College, DePere, Wisconsin 54115 USASearch for more papers by this authorJames F. Kitchell, James F. Kitchell Center for Limnology, University of Wisconsin, Madison, Wisconsin 53706 USASearch for more papers by this authorMichael L. Pace, Michael L. Pace Institute of Ecosystem Studies, Millbrook, New York 12545 USASearch for more papers by this authorDarren Bade, Darren Bade Center for Limnology, University of Wisconsin, Madison, Wisconsin 53706 USASearch for more papers by this authorKathryn L. Cottingham, Kathryn L. Cottingham Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755 USASearch for more papers by this authorTimothy E. Essington, Timothy E. Essington Center for Limnology, University of Wisconsin, Madison, Wisconsin 53706 USASearch for more papers by this authorJeffrey N. Houser, Jeffrey N. Houser Center for Limnology, University of Wisconsin, Madison, Wisconsin 53706 USASearch for more papers by this authorDaniel E. Schindler, Daniel E. Schindler Department of Zoology, University of Washington, Seattle, Washington 98195 USASearch for more papers by this author Stephen R. Carpenter, Stephen R. Carpenter Center for Limnology, University of Wisconsin, Madison, Wisconsin 53706 USA Corresponding author. E-mail: [email protected]Search for more papers by this authorJonathan J. Cole, Jonathan J. Cole Institute of Ecosystem Studies, Millbrook, New York 12545 USASearch for more papers by this authorJames R. Hodgson, James R. Hodgson Department of Biology, Saint Norbert College, DePere, Wisconsin 54115 USASearch for more papers by this authorJames F. Kitchell, James F. Kitchell Center for Limnology, University of Wisconsin, Madison, Wisconsin 53706 USASearch for more papers by this authorMichael L. Pace, Michael L. Pace Institute of Ecosystem Studies, Millbrook, New York 12545 USASearch for more papers by this authorDarren Bade, Darren Bade Center for Limnology, University of Wisconsin, Madison, Wisconsin 53706 USASearch for more papers by this authorKathryn L. Cottingham, Kathryn L. Cottingham Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755 USASearch for more papers by this authorTimothy E. Essington, Timothy E. Essington Center for Limnology, University of Wisconsin, Madison, Wisconsin 53706 USASearch for more papers by this authorJeffrey N. Houser, Jeffrey N. Houser Center for Limnology, University of Wisconsin, Madison, Wisconsin 53706 USASearch for more papers by this authorDaniel E. Schindler, Daniel E. Schindler Department of Zoology, University of Washington, Seattle, Washington 98195 USASearch for more papers by this author First published: 01 May 2001 https://doi.org/10.1890/0012-9615(2001)071[0163:TCNALP]2.0.CO;2Citations: 366 Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract Responses of zooplankton, pelagic primary producers, planktonic bacteria, and CO2 exchange with the atmosphere were measured in four lakes with contrasting food webs under a range of nutrient enrichments during a seven-year period. Prior to enrichment, food webs were manipulated to create contrasts between piscivore dominance and planktivore dominance. Nutrient enrichments of inorganic nitrogen and phosphorus exhibited ratios of N:P > 17:1, by atoms, to maintain P limitation. An unmanipulated reference lake, Paul Lake, revealed baseline variability but showed no trends that could confound the interpretation of changes in the nearby manipulated lakes. Herbivorous zooplankton of West Long Lake (piscivorous fishes) were large-bodied Daphnia spp., in contrast to the small-bodied grazers that predominated in Peter Lake (planktivorous fishes). At comparable levels of nutrient enrichment, Peter Lake's areal chlorophyll and areal primary production rates exceeded those of West Long Lake by factors of approximately three and six, respectively. Grazers suppressed pelagic primary producers in West Long Lake, relative to Peter Lake, even when nutrient input rates were so high that soluble reactive phosphorus accumulated in the epilimnions of both lakes during summer. Peter Lake also had higher bacterial production (but not biomass) than West Long Lake. Hydrologic changes that accompanied manipulation of East Long Lake caused concentrations of colored dissolved organic carbon to increase, leading to considerable variability in fish and zooplankton populations. Both trophic cascades and water color appeared to inhibit the response of primary producers to nutrients in East Long Lake. Carbon dioxide was discharged to the atmosphere by Paul Lake in all years and by the other lakes prior to nutrient addition. During nutrient addition, only Peter Lake consistently absorbed CO2 from the atmosphere, due to high rates of carbon fixation by primary producers. In contrast, CO2 concentrations of West Long Lake shifted to near-atmospheric levels, and net fluxes were near zero, while East Long Lake continued to discharge CO2 to the atmosphere. Literature Cited Aiken, L. S., and S. G. West . 1991. Multiple regression: testing and interpreting interactions. Sage Publications, Newbury Park, California, USA. Bade, D., J. Houser, and S. Scanga . 1998. Methods of the Cascading Trophic Interactions Project. Fifth edition. Center for Limnology, University of Wisconsin–Madison, Wisconsin, USA. Benndorf, J. 1987. Food web manipulation without nutrient control: a useful strategy in lake restoration? Schweizerische Zeitschrift für Hydrologie 49: 237–248. Benndorf, J. 1995. Possibilities and limits for controlling eutrophication by biomanipulation. Internationale Revue der gesampten Hydrobiologie 80: 519–534. Box, G. E. P., W. G. Hunter, and J. S. Hunter . 1978. Statistics for experimenters. Wiley, New York, New York, USA. Brooks, J. L., and S. I. Dodson . 1965. Body size and composition of plankton. Science 150: 28–35. Carpenter, S. R. 1988. Transmission of variance through lake food webs. Pages 119–138 in S. R. Carpenter, editor. Complex interactions in lake communities. Springer-Verlag, New York, New York, USA. Carpenter, S. R. 1999. Role of microcosm experiments in aquatic ecology: reply. Ecology 80: 1085–1088. Carpenter, S. R., D. L. Christensen, J. J. Cole, K. L. Cottingham, X. He, J. R. Hodgson, J. F. Kitchell, S. E. Knight, M. L. Pace, D. M. Post, D. E. Schindler, and N. Voichick . 1995. Biological control of eutrophication in lakes. Environmental Science and Technology 29: 784–786. Carpenter, S. R., J. J. Cole, T. E. Essington, J. R. Hodgson, J. N. Houser, J. F. Kitchell, and M. L. Pace . 1998a. Evaluating alternative explanations in ecosystem experiments. Ecosystems 1: 335–344. Carpenter, S. R., J. J. Cole, J. F. Kitchell, and M. L. Pace . 1998b. Impact of dissolved organic carbon, phosphorus and grazing on phytoplankton biomass and production in experimental lakes. Limnology and Oceanography 43: 73–80. Carpenter, S. R., T. M. Frost, J. F. Kitchell, T. K. Kratz, D. W. Schindler, J. Shearer, W. G. Sprules, M. J. Vanni, and A. P. Zimmerman . 1991. Patterns of primary production and herbivory in 25 North American lake ecosystems. Pages 67–96 in J. Cole, G. Lovett, and S. Findlay, editors. Comparative analyses of ecosystems. Springer-Verlag, New York, New York, USA. Carpenter, S. R., and J. F. Kitchell . 1988. Consumer control of lake productivity. BioScience 38: 764–769. Carpenter, S. R., and J. F. Kitchell . 1993. The trophic cascade in lakes. Cambridge University Press, Cambridge, UK. Carpenter, S. R., J. F. Kitchell, J. J. Cole, and M. L. Pace . 1999. Predicting responses of chlorophyll and primary production to changes in phosphorus, grazing and dissolved organic carbon. Limnology and Oceanography 44: 1179–1182. Carpenter, S. R., J. F. Kitchell, K. L. Cottingham, D. E. Schindler, D. L. Christensen, D. M. Post, and N. Voichick . 1996. Chlorophyll variability, nutrient input and grazing: evidence from whole-lake experiments. Ecology 77: 725–735. Carpenter, S. R., J. F. Kitchell, J. R. Hodgson, P. A. Cochran, J. J. Elser, M. M. Elser, D. M. Lodge, D. Kretchmer, X. He, and C. N. von Ende . 1987. Regulation of lake primary productivity by food web structure. Ecology 68: 1863–1876. Christensen, D. L., S. R. Carpenter, K. L. Cottingham, S. E. Knight, J. P. LeBouton, D. E. Schindler, N. Voichick, J. J. Cole, and M. L. Pace . 1996. Pelagic responses to changes in dissolved organic carbon following division of a seepage lake. Limnology and Oceanography 41: 553–559. Cole, J. J., and N. F. Caraco . 1998. Atmospheric exchange of carbon dioxide in a low-wind oligotrophic lake measured by the addition of SF6. Limnology and Oceanography 43: 647–656. Cole, J. J., N. F. Caraco, G. W. Kling, and T. K. Kratz . 1994. Carbon dioxide supersaturation in the surface waters of lakes. Science 265: 1568–1570. Cole, J. J., S. Findlay, and M. L. Pace . 1988. Bacterial production in fresh and saltwater ecosystems: a cross-system overview. Marine Ecology Progress Series 43: 1–10. Cole, J. J., and M. L. Pace . 1998. Hydrologic variability of small, northern Michigan lakes measured by the addition of tracers. Ecosystems 1: 310–320. Cottingham, K. L. 1999. Nutrients and zooplankton as multiple stressors of phytoplankton communities: evidence from size structure. Limnology and Oceanography 44: 810–827. Cottingham, K. L., and S. R. Carpenter . 1998. Population, community, and ecosystem variates as ecological indicators: phytoplankton responses to whole-lake enrichment. Ecological Applications 8: 508–530. Cottingham, K. L., S. R. Carpenter, and A. L. St. Amand . 1998. Responses of epilimnetic phytoplankton to experimental nutrient enrichment in three small seepage lakes. Journal of Plankton Research 20: 1889–1914. Currie, D. J., P. Dilworth-Christie, and F. Chapleau . 1999. Assessing the strength of top-down influences on plankton abundance in unmanipulated lakes. Canadian Journal of Fisheries and Aquatic Sciences 56: 427–436. Downing, J., and F. H. Rigler . 1984. Secondary productivity in fresh waters. Blackwell, New York, New York, USA. Elser, J. J., T. H. Chrzanowski, R. W. Sterner, and K. H. Mills . 1998. Stoichiometric constraints on food-web dynamics: a whole-lake experiment on the Canadian shield. Ecosystems 1: 120–136. Elser, J. J., D. R. Dobberfuhl, N. A. MacKay, and J. H. Schampel . 1996. Organism size, life history, and N:P stoichiometry. BioScience 46: 674–684. Essington, T. E., and J. F. Kitchell . 1999. New perspectives in the analysis of fish distributions: a case study on the spatial distribution of largemouth bass. Canadian Journal of Fisheries and Aquatic Sciences 56: (Supplement 1) 52–60. Gulati, R. D., and W. R. DeMott . 1997. The role of food quality for zooplankton: remarks on the state of the art, perspectives and priorities. Freshwater Biology 38: 753–768. Hambright, K. D. 1994. Morphological constraints on the piscivore–planktivore interaction—implications for the trophic cascade hypothesis. Limnology and Oceanography 39: 897–912. Hansson, L. A., H. Annadotter, E. Bergman, S. F. Hamrin, E. Jeppesen, T. Kairesalo, E. Luokkanen, P. A. Nilsson, M. Søndergaard, and J. Strand . 1998. Biomanipulation as an application of food-chain theory: constraints, synthesis, and recommendations for temperate lakes. Ecosystems 1: 558–574. He, X., J. R. Hodgson, J. F. Kitchell, and R. A. Wright . 1994. Growth and diet composition of largemouth bass in four experimental lakes. Internationale Vereinigung fur Theoreticsche und Angewandte Limnologie 25: 766–772. Hobbie, J. E., R. J. Daley, and S. Jasper . 1977. Use of nuclepore filters for counting bacteria by fluorescent microscopy. Applied and Environmental Microbiology 33: 1225–1228. Hodgson, J. R., X. He, D. E. Schindler, and J. F. Kitchell . 1997. Diet overlap in a piscivore community. Ecology of Freshwater Fish 6: 144–149. Hodgson, J. Y., and J. R. Hodgson . 2001. Exploring optimal foraging by largemouth bass (Micropterus salmoides) from three experimental lakes. Internationale Vereinigung fur Theoreticsche und Angewandte Limnologie, In press. Hoover, T. E., and D. C. Berkshire . 1969. Effects of hydration on carbon dioxide exchange across an air–water interface. Journal of Geophysical Research 74: 456–464. Houser, J. N., S. R. Carpenter, and J. J. Cole . 2000. Food web structure and nutrient enrichment: effects on sediment phosphorus retention in whole-lake experiments. Canadian Journal of Fisheries and Aquatic Sciences 57: 1524–1533. Hrbácek, J. M., V. Dvoraková, V. Korinek, and L. Procházková . 1961. Demonstration of the effect of the fish stock on the species composition of zooplankton and the intensity of the metabolism of the whole plankton association. Internationale Vereinigung für Theoretische und Angewandte Limnologie 14: 192–195. Hurlbert, S. H., J. Zedler, and D. Fairbanks . 1972. Ecosystem alteration by mosquitofish (Gambusia affinis) predation. Science 175: 639–641. Jeppesen, E., Ma. Søndergaard, Mo. Søndergaard, and K. Christoffersen . editors 1998. The structuring role of submerged macrophytes in lakes. Springer-Verlag, Berlin, Germany. Kitchell, J. F., E. A. Eby, X. He, D. E. Schindler, and R. A. Wright . 1994. Predator–prey dynamics in an ecosystem context. Journal of Fish Biology 45: 1–18. Kling, G. W., G. W. Kipphut, and M. C. Miller . 1991. Arctic lakes and streams as gas conduits to the atmosphere—implications for tundra carbon budgets. Science 251: 298–301. Lodge, D. M., S. C. Blumenshine, and Y. Vadeboncoeur . 1998. Insights and applications of large scale, long term ecological observations and experiments. Pages 202–235 in W. R. Resetarits and J. Bernardo, editors. Experimental ecology: issues and perspectives. Oxford University Press, Cambridge, UK. Marker, A. F. H., C. A. Crowther, and R. J. M. Gunn . 1980. Methanol and acetone as solvents for estimating chlorophyll and pheopigments by spectrophotometry. Ergebnisse der Limnologie 14: 52–69. Mazumder, A. 1994. Phosphorus–chlorophyll relationships under contrasting herbivory and thermal stratification: predictions and patterns. Canadian Journal of Fisheries and Aquatic Sciences 51: 401–407. Meijer, M.-L., I. De Boos, M. Scheffer, R. Portielje, and H. Hosper . 1999. Biomanipulation in shallow lakes in the Netherlands: an evaluation of 18 case studies. Hydrobiologia 408/409: 13–30. Meijer, M.-L., E. Jeppesen, E. van Donk, B. Moss, M. Scheffer, E. Lammens, E. van Nes, J. A. van Berkum, G. J. de Jong, B. A. Faafeng, and J. P. Jensen . 1994. Long-term responses to fish-stock reduction in small shallow lakes: interpretation of five-year results of four biomanipulation cases in The Netherlands and Denmark. Hydrobiologia 275/276: 457–466. Micheli, F. 1999. Eutrophication, fisheries and consumer–resource dynamics in marine pelagic ecosystems. Science 285: 1396–1398. Mills, E. L., and A. Schiavone . 1982. Evaluation of fish communities through assessment of zooplankton populations and measures of lake productivities. North American Journal of Fisheries Management 2: 14–27. Mittelbach, G. G., A. M. Turner, D. J. Hall, J. E. Rettig, and C. W. Osenberg . 1995. Perturbation and resilience in an aquatic community: a long-term study of the extinction and reintroduction of a top predator. Ecology 76: 2347–2360. Murdoch, W. W., R. M. Nisbet, E. McCauley, A. M. de Roos, and W. S. C. Gurney . 1998. Plankton abundance and dynamics across nutrient levels: tests of hypotheses. Ecology 79: 1339–1356. Nürnberg, G. K. 1999. Determining trophic state in experimental lakes. Limnology and Oceanography 44: 1176–1179. Pace, M. L. 1984. Zooplankton community structure, but not biomass, influences the phosphorus–chlorophyll a relationship. Canadian Journal of Fisheries and Aquatic Sciences 41: 1089–1096. Pace, M. L. 2001. Getting it right and wrong: extrapolations across experimental scales. Pages 161–181 in R. Gardner, M. Kemp, V. Kennedy, and J. Peterson, editors. Scaling relations in experimental ecology. Columbia University Press, New York, New York, USA. Pace, M. L., and J. J. Cole . 1994. Primary and bacterial production: are they coupled over depth? Journal of Plankton Research 16: 661–672. Pace, M. L., and J. J. Cole . 1996. Regulation of bacterial by resources and predation tested in whole-lake experiments. Limnology and Oceanography 41: 1448–1460. Pace, M. L., J. J. Cole, and S. R. Carpenter . 1998. Trophic cascades and compensation: differential responses of microzooplankton in whole-lake experiments. Ecology 79: 138–152. Pace, M. L., J. J. Cole, S. R. Carpenter, and J. F. Kitchell . 1999. Trophic cascades revealed in diverse ecosystems. Trends in Ecology and Evolution 14: 483–488. Paine, R. T. 1980. Food webs: linkage, interaction strength and community infrastructure. Journal of Animal Ecology 49: 667–685. Persson, L. 1999. Trophic cascades: abiding heterogeneity and the trophic level concept at the end of the road. Oikos 85: 385–397. Persson, L., S. Diehl, L. Johansson, G. Andersson, and S. F. Hamrin . 1992. Trophic interactions in temperate lake ecosystems: a test of food chain theory. The American Naturalist 140: 59–84. Peters, R. H., and J. Downing . 1984. Empirical analysis of zooplankton filtering and feeding rates. Limnology and Oceanography 29: 763–784. Polis, G. A. 1999. Why are parts of the world green? Multiple factors control productivity and the distribution of biomass. Oikos 86: 3–15. Post, D. M., S. R. Carpenter, D. L. Christensen, K. L. Cottingham, J. R. Hodgson, J. F. Kitchell, and D. E. Schindler . 1997. Seasonal effects of variable recruitment of a dominant piscivore on pelagic food web structure. Limnology and Oceanography 42: 722–729. Quiros, R. 1990a. Empirical relationships between nutrients, phyto- and zooplankton and relative fish biomass in lakes and reservoirs of Argentina. Internationale Vereinigung fur theoretische und angewandte Limnologie 24: 1198–1206. Quiros, R. 1990b. Factors related to variance of residuals in chlorophyll–total phosphorus regressions in lakes and reservoirs of Argentina. Hydrobiologia 200/201: 343–355. Quiros, R. 1998. Fish effects on trophic relationships in the pelagic zone of lakes. Hydrobiologia 361: 101–111. Reynolds, C. S. 1994. The ecological basis for the successful biomanipulation of aquatic communities. Archiv für Hydrobiologie 130: 1–33. Sarnelle, O. 1992. Nutrient enrichment and grazer effects on phytoplankton in lakes. Ecology 73: 551–560. Scheffer, M. 1997. Ecology of shallow lakes. Chapman and Hall, New York, New York, USA. Schindler, D. E., S. R. Carpenter, J. J. Cole, J. F. Kitchell, and M. L. Pace . 1997a. Food web structure alters carbon exchange between lakes and the atmosphere. Science 277: 248–251. Schindler, D. E., J. R. Hodgson, and J. F. Kitchell . 1997b. Density-dependent changes in individual foraging specialization of largemouth bass. Oecologia 110: 592–600. Schindler, D. E., J. F. Kitchell, X. He, S. R. Carpenter, J. R. Hodgson, and K. L. Cottingham . 1993. Food web structure and phosphorus cycling in lakes. Transactions of the American Fisheries Society 122: 756–772. Schindler, D. W. 1998. Replication versus realism: the necessity for ecosystem-scale experiments, replicated or not. Ecosystems 1: 323–334. Schindler, D. W., E. J. Fee, and T. Ruszczynski . 1978. Phosphorus input and its consequences for phytoplankton standing crop and production in the Experimental Lakes Area and in similar lakes. Journal of the Fisheries Research Board of Canada 35: 190–196. Shapiro, J. 1990. Biomanipulation: the next phase—making it stable. Hydrobiologia 200/201: 13–27. Shapiro, J., V. Lamarra, and M. Lynch . 1975. Biomanipulation: an ecosystem approach to lake restoration. Pages 85–96 in P. L. Brezonik and J. L. Fox, editors. Water quality management through biological control. University of Florida, Gainesville, Florida, USA. Shiomoto, A., K. Tadokoro, K. Nagasawa, and Y. Ishida . 1997. Trophic relations in the subarctic North Pacific ecosystem: possible feeding effect from pink salmon. Marine Ecology Progress Series 150: 75–85. Stainton, M. P. 1973. A syringe gas-stripping procedure for gas-chromatographic determination of dissolved inorganic and organic carbon in freshwater and carbonates in sediments. Journal of the Fisheries Research Board of Canada 30: 1441–1445. Strong, D. R. 1992. Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73: 747–754. Vadeboncoeur, Y., D. M. Lodge, and S. R. Carpenter . 2001. Whole-lake fertilization effects on distribution of primary production between benthic and pelagic habitats. Ecology 82: 1065–1077. Vollenweider, R. A. 1976. Advances in defining critical loading levels for P in lake eutrophication. Memorie dell'Istituto Italiano di Idrobiologia 33: 53–83. Walters, C. J. 1986. Adaptive management of renewable resources. MacMillan, New York, New York, USA. Weiss, R. F. 1974. Carbon dioxide in water and seawater: the solubility of a non-ideal gas. Marine Chemistry 2: 203–215. White, P. A., J. Kalff, J. B. Rasmussen, and J. M. Gasol . 1991. The effect of temperature and algal biomass on bacterial production and specific growth rate in freshwater and marine habitats. Microbial Ecology 21: 99–118. Citing Literature Volume71, Issue2May 2001Pages 163-186 ReferencesRelatedInformation
Publication Year: 2001
Publication Date: 2001-05-01
Language: en
Type: article
Indexed In: ['crossref']
Access and Citation
Cited By Count: 499
AI Researcher Chatbot
Get quick answers to your questions about the article from our AI researcher chatbot