Interactions between Herbivorous Fishes and Limiting Nutrients in a Tropical Stream Ecosystem
2002; Wiley; Volume: 83; Issue: 7 Linguagem: Inglês
10.2307/3071768
ISSN1939-9170
AutoresAlexander S. Flecker, Brad W. Taylor, Emily S. Bernhardt, James M. Hood, William K. Cornwell, Shawn R. Cassatt, Michael J. Vanni, Naomi Altman,
Tópico(s)Fish Ecology and Management Studies
ResumoEcologyVolume 83, Issue 7 p. 1831-1844 Article INTERACTIONS BETWEEN HERBIVOROUS FISHES AND LIMITING NUTRIENTS IN A TROPICAL STREAM ECOSYSTEM Alexander S. Flecker, Alexander S. Flecker Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, New York 14853 USA E-mail: [email protected]Search for more papers by this authorBrad W. Taylor, Brad W. Taylor Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, New York 14853 USA Present address: Department of Zoology and Physiology, University of Wyoming, Laramie, Wyoming 82071 USASearch for more papers by this authorEmily S. Bernhardt, Emily S. Bernhardt Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, New York 14853 USA. Institute of Ecosystem Studies, Box AB 44A, Millbrook, New York 12545 USA Present address: Nicholas School of the Environment and Earth Sciences, Duke University, Durham, North Carolina 27708 USASearch for more papers by this authorJames M. Hood, James M. Hood Department of Zoology, Miami University, Oxford, Ohio 45056 USASearch for more papers by this authorWilliam K. Cornwell, William K. Cornwell Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, New York 14853 USA Present address: Department of Biological Sciences, Stanford University, Stanford, California 94305 USASearch for more papers by this authorShawn R. Cassatt, Shawn R. Cassatt Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, New York 14853 USASearch for more papers by this authorMichael J. Vanni, Michael J. Vanni Department of Zoology, Miami University, Oxford, Ohio 45056 USASearch for more papers by this authorNaomi S. Altman, Naomi S. Altman Department of Biometrics, Warren Hall, Cornell University, Ithaca, New York 14853 USA Present address: Department of Statistics, Pennsylvania State University, University Park, Pennsylvania 16802 USASearch for more papers by this author Alexander S. Flecker, Alexander S. Flecker Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, New York 14853 USA E-mail: [email protected]Search for more papers by this authorBrad W. Taylor, Brad W. Taylor Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, New York 14853 USA Present address: Department of Zoology and Physiology, University of Wyoming, Laramie, Wyoming 82071 USASearch for more papers by this authorEmily S. Bernhardt, Emily S. Bernhardt Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, New York 14853 USA. Institute of Ecosystem Studies, Box AB 44A, Millbrook, New York 12545 USA Present address: Nicholas School of the Environment and Earth Sciences, Duke University, Durham, North Carolina 27708 USASearch for more papers by this authorJames M. Hood, James M. Hood Department of Zoology, Miami University, Oxford, Ohio 45056 USASearch for more papers by this authorWilliam K. Cornwell, William K. Cornwell Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, New York 14853 USA Present address: Department of Biological Sciences, Stanford University, Stanford, California 94305 USASearch for more papers by this authorShawn R. Cassatt, Shawn R. Cassatt Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, New York 14853 USASearch for more papers by this authorMichael J. Vanni, Michael J. Vanni Department of Zoology, Miami University, Oxford, Ohio 45056 USASearch for more papers by this authorNaomi S. Altman, Naomi S. Altman Department of Biometrics, Warren Hall, Cornell University, Ithaca, New York 14853 USA Present address: Department of Statistics, Pennsylvania State University, University Park, Pennsylvania 16802 USASearch for more papers by this author First published: 01 July 2002 https://doi.org/10.1890/0012-9658(2002)083[1831:IBHFAL]2.0.CO;2Citations: 111 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 Ecologists have long been interested in understanding the strengths of consumer and resource limitation in influencing communities. Here we ask three questions concerning the relative importance of nutrients and grazing fishes to primary producers of a tropical Andean stream: (1) Are stream algae nutrient limited? (2) Are top-down and bottom-up forces of dual importance in limiting primary producers? (3) Do grazing fishes modulate the degree of resource limitation? We obtained several lines of evidence suggesting that Andean stream algae are nitrogen limited. Addition of nitrogen in flow-through channels resulted in major increases in algal standing crop, whereas there were no measurable effects of phosphorus enrichment. Interestingly, the N2-fixing cyanobacteria Anabaena was one of the taxa that responded most dramatically to the addition of nitrogen. Moreover, nutrient uptake rates were significantly higher for inorganic nitrogen (NO3-N and NH4-N) compared to phosphorus (PO4-P). Nutrients and the presence of grazing fishes were manipulated simultaneously in a series of experiments by using nutrient-diffusing substrates in fish exclusions vs. open cages accessible to the natural fish assemblage. We observed strong effects of both nitrogen addition and consumers on algal standing crop, although consumer limitation was found to be of considerably greater magnitude than resource limitation in influencing algal biomass and composition. Finally, the degree of resource limitation varied as a consequence of grazing fishes. Experiments examining nutrient limitation in the presence and absence of fishes showed that the response to nitrogen enrichment was significantly greater on substrates accessible to natural fish assemblages compared to substrates where grazing fishes were excluded. These experiments demonstrate simultaneous and interactive effects of top-down and bottom-up factors in limiting primary producers of tropical Andean streams. Whereas other studies have shown that consumers affect nutrient supply in ecosystems, our findings suggest that consumers can play an important role in influencing nutrient demand. Literature Cited Berlow, E. L., S. A. Navarrete, C. J. Briggs, M. E. Power, and B. A. Menge . 1999. Quantifying variation in the strengths of species interactions. Ecology 80: 2206–2224. 10.1890/0012-9658(1999)080[2206:QVITSO]2.0.CO;2 Web of Science®Google Scholar Borchardt, M. A. 1996. Nutrients. Pages 183–227 in R. J. Stevenson, M. L. Bothwell, and R. L. Lowe, editors. Algal ecology: freshwater benthic ecosystems. Academic Press, San Diego, California, USA. Google Scholar Brett, M. T., and C. R. Goldman . 1997. Consumer versus resource control in freshwater pelagic food webs. Science 275: 384–386. 10.1126/science.275.5298.384 CASPubMedWeb of Science®Google Scholar Carpenter, S. R., J. J. Cole, J. F. Kitchell, and M. L. Pace . 1998. Impact of dissolved organic carbon, phosphorus, and grazing on phytoplankton biomass and production in experimental lakes. Limnology and Oceanography 43: 73–80. 10.4319/lo.1998.43.1.0073 CASPubMedWeb of Science®Google Scholar 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. 10.2307/1939878 CASPubMedWeb of Science®Google Scholar DeAngelis, D. L. 1992. Dynamics of nutrient cycling and food webs. Chapman and Hall, London, UK. Google Scholar Downing, J. A. et al. 1999a.. The impact of accelerating land-use change on the N-cycle of tropical aquatic ecosystems: current conditions and projected changes. Biogeochemistry 46: 109–148. 10.1007/BF01007576 Web of Science®Google Scholar Downing, J. A., C. W. Osenberg, and O. Sarnelle . 1999b.. Meta-analysis of marine nutrient enrichments experiments: variation in the magnitude of nutrient limitation. Ecology 80: 1157–1167. 10.1890/0012-9658(1999)080[1157:MAOMNE]2.0.CO;2 Web of Science®Google Scholar Elser, J. J. 1992. Phytoplankton dynamics and the role of grazers in Castle Lake, California. Ecology 73: 887–902. 10.2307/1940166 Web of Science®Google Scholar Fairchild, G. W., R. L. Lowe, and W. B. Richardson . 1985. Algal periphyton growth on nutrient-diffusing substrates: an in-situ bioassay. Ecology 66: 465–472. 10.2307/1940395 CASWeb of Science®Google Scholar Flecker, A. S. 1992. Fish trophic guilds and the structure of a tropical stream: weak direct versus strong indirect effects. Ecology 73: 927–940. 10.2307/1940169 Web of Science®Google Scholar Flecker, A. S. 1996. Ecosystem engineering by a dominant detritivore in a diverse tropical ecosystem. Ecology 77: 1845–1854. 10.2307/2265788 Web of Science®Google Scholar Forkner, R. E., and M. D. Hunter . 2000. What goes up must come down? Nutrient addition and predation pressure on oak herbivores. Ecology 81: 1588–1600. 10.1890/0012-9658(2000)081[1588:WGUMCD]2.0.CO;2 Web of Science®Google Scholar Forrester, G. E., T. L. Dudley, and N. B. Grimm . 1999. Trophic interactions in open systems: effects of predators and nutrients on stream food webs. Limnology and Oceanography 44: 1187–1197. 10.4319/lo.1999.44.5.1187 Web of Science®Google Scholar Fretwell, S. D. 1977. The regulation of plant communities by food chains exploiting them. Perspectives in Biology and Medicine 20: 169–185. 10.1353/pbm.1977.0087 Web of Science®Google Scholar Fretwell, S. D. 1987. Food chain dynamics: the central theory of ecology? Oikos 50: 291–301. 10.2307/3565489 Web of Science®Google Scholar Gregory, S. V. 1980. Effects of light, nutrients, and grazing on periphyton communities in streams. Dissertation. Oregon State University, Corvallis, Oregon, USA. Google Scholar Grimm, N. B. 1988. Feeding dynamics, nitrogen budgets, and ecosystem role of a desert stream omnivore, Agosia chrysogaster (Pisces: Cyprinidae). Environmental Biology of Fishes 21: 143–152. 10.1007/BF00004849 Web of Science®Google Scholar Grimm, N. B., and S. G. Fisher . 1986. Nitrogen limitation in a Sonoran desert stream. Journal of the North American Benthological Society 5: 2–15. 10.2307/1467743 Google Scholar Hairston, N. G., Jr., and N. G. Hairston, Sr . 1993. Cause–effect relationships in energy flow, trophic structure, and interspecific interactions. American Naturalist 142: 379–411. 10.1086/285546 Web of Science®Google Scholar Hairston, N. G., F. E. Smith, and L. B. Slobodkin . 1960. Community structure, population control, and competition. American Naturalist 94: 421–425. 10.1086/282146 Web of Science®Google Scholar Hill, W. R., H. L. Boston, and A. D. Steinman . 1992. Grazers and nutrients simultaneously limit lotic primary productivity. Canadian Journal of Fisheries and Aquatic Sciences 49: 504–512. 10.1139/f92-059 Web of Science®Google Scholar Hill, W. R., and A. W. Knight . 1988. Nutrient and light limitation of algae in two northern California streams. Journal of Phycology 24: 125–132. 10.1111/j.1529-8817.1988.tb04225.x Web of Science®Google Scholar Hood, J. M. 2000. The potential importance of nutrient regeneration by fish in a Neotropical stream. Thesis. Miami University, Oxford, Ohio, USA. Google Scholar Howarth, R. W., R. Marino, J. Lane, and J. J. Cole . 1988. Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 1. Rates and importance. Limnology and Oceanography 33: 669–687. 10.4319/lo.1988.33.4part2.0669 CASWeb of Science®Google Scholar Hunter, M. D., and P. W. Price . 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73: 724–732. 10.2307/1940152 Web of Science®Google Scholar Jackson, J. K., and B. W. Sweeney . 1995. Present status and future directions of tropical stream research. Journal of the North American Benthological Society 14: 5–11. 10.2307/1467720 Web of Science®Google Scholar Kenward, M. G., and J. H. Roger . 1997. Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53: 983–997. 10.2307/2533558 CASPubMedWeb of Science®Google Scholar Knapp, A. K., J. M. Blair, J. M. Briggs, S. L. Collins, D. C. Hartnett, L. C. Johnson, and E. G. Towne . 1999. The keystone role of bison in North American tallgrass prairie—Bison increase habitat heterogeneity and alter a broad array of plant, community, and ecosystem processes. Bioscience 49: 39–50. 10.2307/1313492 Web of Science®Google Scholar Kraft, C. E. 1992. Estimates of phosphorus and nitrogen cycling by fish using a bioenergetics approach. Canadian Journal of Fisheries and Aquatic Sciences 49: 2596–2604. 10.1139/f92-287 CASWeb of Science®Google Scholar Lamberti, G. A. 1996. The role of periphyton in benthic food webs. Pages 533–572 in R. J. Stevenson, M. L. Bothwell, and R. L. Lowe, editors. Algal ecology: freshwater benthic ecosystems. Academic Press, San Diego, California, USA. Google Scholar Lamberti, G. A., L. R. Ashkenas, S. V. Gregory, and A. D. Steinman . 1987. Effects of three herbivores on periphyton communities in laboratory streams. Journal of the North American Benthological Society 6: 92–104. 10.2307/1467219 Google Scholar Lewis, W. M., Jr., S. K. Hamilton, and J. F. Saunders III . 1995. Rivers of northern South America. Pages 219–256 in C. E. Cushing, K. W. Cummins, and G. W. Minshall, editors. Ecosystems of the world 22. Rivers and stream ecosystems. Elsevier, Amsterdam, The Netherlands. Google Scholar Lohman, K., J. R. Jones, and C. Baysinger-Daniel . 1991. Experimental evidence for nitrogen limitation in a northern Ozark stream. Journal of the North American Benthological Society 19: 14–23. 10.2307/1467760 Web of Science®Google Scholar Lowe, R. L., and G. D. LaLiberte . 1996. Benthic stream algae: distribution and structure. Pages 269–293 in F. R. Hauer and G. A. Lamberti, editors. Methods in stream ecology. Academic Press, San Diego, California, USA. Google Scholar Lowe-McConnell, R. H. 1987. Ecological studies in tropical fish communities. Cambridge University Press, Cambridge, UK. Google Scholar Martí, E., N. B. Grimm, and S. G. Fisher . 1997. Pre- and post-flood retention efficiency in a Sonoran Desert stream. Journal of the North American Benthological Society 16: 805–819. 10.2307/1468173 Web of Science®Google Scholar Martí, E., and F. Sabater . 1996. High variability in temporal and spatial nutrient retention in Mediterranean streams. Ecology 77: 854–869. 10.2307/2265506 Web of Science®Google Scholar McCormick, P. V., and R. J. Stevenson . 1989. Effects of snail grazing on benthic community structure in different nutrient environments. Journal of the North American Benthological Society 8: 162–172. 10.2307/1467634 Web of Science®Google Scholar McCormick, P. V., and R. J. Stevenson . 1991. Grazer control of nutrient availability in the periphyton. Oecologia 86: 287–291. 10.1007/BF00317542 PubMedWeb of Science®Google Scholar McNaughton, S. J., R. W. Ruess, and S. W. Seagle . 1988. Large mammals and process dynamics in African ecosystems. Bioscience 38: 794–800. 10.2307/1310789 Web of Science®Google Scholar Menge, B. A., and J. P. Sutherland . 1987. Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. American Naturalist 130: 730–757. 10.1086/284741 Web of Science®Google Scholar Miller, M. W., M. E. Hay, S. L. Miller, D. Malone, E. E. Sotka, and A. M. Szmant . 1999. Effects of nutrients versus herbivores on reef algae: a new method for manipulating nutrients on coral reefs. Limnology and Oceanography 44: 1847–1861. 10.4319/lo.1999.44.8.1847 Web of Science®Google Scholar Mulholland, P. J., A. D. Steinman, and J. W. Elwood . 1990. Measurement of phosphorus uptake length in streams: comparison of radiotracer and stable PO4 releases. Canadian Journal of Fisheries and Aquatic Science 47: 2351–2357. 10.1139/f90-261 CASWeb of Science®Google Scholar Mulholland, P. J., A. D. Steinman, A. V. Palumbo, J. W. Elwood, and D. B. Kirschtel . 1991. Role of nutrient cycling and herbivory in regulating periphyton communities in laboratory streams. Ecology 72: 966–982. 10.2307/1940597 CASWeb of Science®Google Scholar Munn, N. L., and J. L. Meyer . 1990. Habitat-specific solute retention in two small streams: an intersite comparison. Ecology 71: 2069–2082. 10.2307/1938621 Web of Science®Google Scholar Newbold, J. D., J. W. Elwood, R. V. O'Neill, and W. Van Winkle . 1981. Measuring nutrient spiralling in streams. Canadian Journal of Fisheries and Aquatic Sciences 38: 860–863. 10.1139/f81-114 Web of Science®Google Scholar Nusch, E. A. 1980. Comparison of different methods for chlorophyll and phaeopigment determination. In H. Ria, editor. The measurement of photosynthetic pigments in fresh waters and the standardization of methods Archiv für Hydrobiologie, Ergebnisse der Limnologie 14: 14–36. CASGoogle Scholar Oksanen, L. 1988. Ecosystem organization: mutualism and cybernetics or plain Darwinian struggle for existence? American Naturalist 131: 424–444. 10.1086/284799 Web of Science®Google Scholar Oksanen, L., S. D. Fretwell, J. Arruda, and P. Niemela . 1981. Exploitation ecosystems in gradients of primary productivity. American Naturalist 118: 240–261. 10.1086/283817 Web of Science®Google Scholar Osenberg, C. W., and G. G. Mittelbach . 1996. The relative importance of resource limitation and predator limitation in food chains. Pages 134–149 in G. Polis and K. Winemiller, editors. Food webs: integration patterns and dynamics. Chapman and Hall, New York, New York, USA. Google Scholar Osenberg, C. W., O. Sarnelle, S. D. Cooper, and R. D. Holt . 1999. Resolving ecological questions through meta-analysis: goals, metrics, and models. Ecology 80: 1105–1117. 10.1890/0012-9658(1999)080[1105:REQTMA]2.0.CO;2 Web of Science®Google Scholar Paaby-Hansen, P. 1988. Light and nutrient limitation in a Costa Rican lowland stream. Dissertation. University of California-Davis, California, USA. Google Scholar 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. 10.1016/S0169-5347(99)01723-1 CASPubMedWeb of Science®Google Scholar Pastor, J., R. J. Naiman, B. Dewey, and P. McInnes . 1988. Moose, microbes, and the boreal forest. Bioscience 38: 770–777. 10.2307/1310786 Web of Science®Google Scholar Persson, L., J. Bengtsson, B. A. Menge, and M. E. Power . 1996. Productivity and consumer regulation—concepts, patterns, and mechanisms. Pages 396–434 in G. A. Polis and K. O. Winemiller, editors. Food webs: integration of patterns and dynamics. Chapman and Hall, New York, New York, USA. Google Scholar Peterson, B. J. et al. 1993. Biological responses of a tundra river to fertilization. Ecology 74: 653–672. 10.2307/1940794 CASWeb of Science®Google Scholar Peterson, B. J., J. E. Hobbie, T. L. Corliss, and K. Kriet . 1983. A continuous flow periphyton bioassay: tests of nutrient limitation in a tundra stream. Limnology and Oceanography 28: 583–591. 10.4319/lo.1983.28.3.0583 CASWeb of Science®Google Scholar Peterson, C. G., and N. B. Grimm . 1992. Temporal variation in enrichment effects during periphyton succession in a nitrogen-limited desert stream ecosystem. Journal of the North American Benthological Society 11: 20–36. 10.2307/1467879 Web of Science®Google Scholar Polis, G. A., and D. R. Strong . 1996. Food web complexity and community dynamics. American Naturalist 147: 813–846. 10.1086/285880 Web of Science®Google Scholar Post, D. M., M. L. Pace, and N. G. Hairston . 2000. Ecosystem size determines food-chain length in lakes. Nature 405: 1047–1049. 10.1038/35016565 CASPubMedWeb of Science®Google Scholar Power, M. E. 1983. Grazing responses of tropical freshwater fishes to different scales of variation in their food. Environmental Biology of Fishes 9: 103–115. 10.1007/BF00690856 Web of Science®Google Scholar Power, M. E. 1984. The importance of sediment in the grazing ecology and size class interactions of an armored catfish, Ancistrus spinosus. Environmental Biology of Fishes 10: 173–181. 10.1007/BF00001124 Web of Science®Google Scholar Power, M. E. 1990. Resource enhancement by indirect effects of grazers: armored catfish, algae, and sediment. Ecology 71: 897–904. 10.2307/1937361 Web of Science®Google Scholar Power, M. E. 1992. Top-down and bottom-up forces in food webs—do plants have primacy? Ecology 73: 733–746. 10.2307/1940153 Web of Science®Google Scholar Pringle, C. M., and G. A. Blake . 1994. Quantitative effects of atyid shrimp (Decapoda: Atyidae) on the depositional environment in a tropical stream: use of electricity for experimental exclusion. Canadian Journal of Fisheries and Aquatic Sciences 51: 1443–1450. 10.1139/f94-144 Web of Science®Google Scholar Pringle, C. M., and T. Hamazaki . 1997. Effects of fishes on algal response to storms in a tropical stream. Ecology 78: 2432–2442. 10.1890/0012-9658(1997)078[2432:EOFOAR]2.0.CO;2 Web of Science®Google Scholar Pringle, C. M., and T. Hamazaki . 1998. The role of omnivory in a neotropical stream: separating diurnal and nocturnal effects. Ecology 79: 269–280. 10.1890/0012-9658(1998)079[0269:TROOIA]2.0.CO;2 Web of Science®Google Scholar Pringle, C. M., P. Paaby-Hansen, P. D. Vaux, and C. R. Goldman . 1986. In situ nutrient assays of periphyton growth in a lowland Costa Rican stream. Hydrobiologia 134: 207–213. 10.1007/BF00008489 CASWeb of Science®Google Scholar Pringle, C. M., and F. J. Triska . 1991. Effects of geothermal groundwater on nutrient dynamics of a lowland Costa Rican stream. Ecology 72: 951–965. 10.2307/1940596 CASWeb of Science®Google Scholar Pringle, C. M., and F. J. Triska . 1996. Effects of nutrient enrichment on periphyton. Pages 607–623 in F. R. Hauer and G. A. Lamberti, editors. Methods in stream ecology. Academic Press, San Diego, California, USA. Google Scholar Rosemond, A. D. 1993. Interactions among irradiance, nutrients, and herbivores constrain a stream algal community. Oecologia 94: 585–594. 10.1007/BF00566976 CASPubMedWeb of Science®Google Scholar Rosemond, A. D., P. J. Mulholland, and S. H. Brawley . 2000. Seasonally shifting limitation of stream periphyton: response of algal populations and assemblage biomass and productivity to variation in light, nutrients, and herbivores. Canadian Journal of Fisheries and Aquatic Sciences 57: 66–75. Web of Science®Google Scholar Rosemond, A. D., P. J. Mulholland, and J. W. Elwood . 1993. Top-down and bottom-up control of stream periphyton effects of nutrients and herbivore. Ecology 74: 1264–1280. 10.2307/1940495 Web of Science®Google Scholar SAS Institute. 1989. SAS/STAT user's guide, version 6. Fourth edition. Volume 2. SAS Institute, Cary, North Carolina, USA. Google Scholar SAS Institute. 1999. SAS/STAT user's guide, version 8. SAS Institute, Cary, North Carolina, USA. Google Scholar Schindler, D. E., S. R. Carpenter, K. L. Cottingham, X. He, J. R. Hodgson, J. F. Kitchell, and P. A. Soranno . 1996. Food web structure and littoral zone coupling to pelagic trophic cascades. Pages 96–105 in G. A. Polis and K. O. Winemiller, editors. Food webs: integration of pattern and process. Chapman and Hall, New York, New York, USA. Google Scholar Scrimgeour, G. J., and P. A. Chambers . 1997. Development and application of a nutrient-diffusing bioassay for large rivers. Freshwater Biology 38: 221–231. 10.1046/j.1365-2427.1997.00198.x Web of Science®Google Scholar Solorzano, L. 1969. Determination of ammonia in natural waters by the phenolhypochlorite method. Limnology and Oceanography 14: 799–801. 10.4319/lo.1969.14.5.0799 CASWeb of Science®Google Scholar Steinman, A. D. 1996. Effects of grazers on freshwater benthic algae. Pages 341–373 in R. J. Stevenson, M. L. Bothwell, and R. L. Lowe, editors. Algal ecology: freshwater benthic ecosystems. Academic Press, San Diego, California, USA. Google Scholar Steinman, A. D., and G. A. Lamberti . 1996. Biomass and pigments of benthic algae. Pages 295–313 in F. R. Hauer and G. A. Lamberti, editors. Methods in stream ecology. Academic Press. San Diego, California, USA. Google Scholar Steinman, A. D., P. J. Mulholland, and J. J. Beauchamp . 1995. Effects of biomass, light, and grazing on phosphorus cycling in stream periphyton communities. Journal of the North American Benthological Society 14: 371–381. 10.2307/1467203 Web of Science®Google Scholar Sterner, R. W. 1986. Herbivores' direct and indirect effects on algal populations. Science 231: 605–607. 10.1126/science.231.4738.605 CASPubMedWeb of Science®Google Scholar Sterner, R. W. 1990. The ratio of nitrogen to phosphorus resupplied by herbivores: zooplankton and the algal competitive arena. American Naturalist 136: 209–229. 10.1086/285092 Web of Science®Google Scholar Sterner, R. W., J. J. Elser, T. H. Chrzanowski, J. H. Schampel, and N. B. George . 1996. Biogeochemistry and trophic ecology: a new food web diagram. Pages 72–80 in G. A. Polis and K. O. Winemiller, editors. Food webs: integration of pattern and process. Chapman and Hall, New York, New York, USA. Google Scholar Sterner, R. W., and N. B. George . 2000. Carbon, nitrogen, and phosphorus stoichiometry of cyprinid fishes. Ecology 81: 127–140. 10.1890/0012-9658(2000)081[0127:CNAPSO]2.0.CO;2 Web of Science®Google Scholar Sterner, R. W., and D. O. Hessen . 1994. Algal nutrient limitation and nutrition of aquatic herbivores. Annual Review of Ecology and Systematics 25: 1–29. 10.1146/annurev.es.25.110194.000245 Web of Science®Google Scholar Stewart, A. J. 1987. Responses of stream algae to grazing minnows and nutrients: a field test for interactions. Oecologia 72: 1–7. 10.1007/BF00385036 CASPubMedWeb of Science®Google Scholar Stiling, P., and A. M. Rossi . 1997. Experimental manipulations of top-down and bottom-up factors in a tri-trophic system. Ecology 78: 1602–1606. 10.1890/0012-9658(1997)078[1602:EMOTDA]2.0.CO;2 Web of Science®Google Scholar Tate, C. M. 1990. Patterns and controls of nitrogen in tallgrass prairie streams. Ecology 71: 2007–2018. 10.2307/1937609 Web of Science®Google Scholar Tilman, D., S. S. Kilham, and P. Kilham . 1982. Phytoplankton ecology: the role of limiting nutrients. Annual Review of Ecology and Systematics 13: 349–373. 10.1146/annurev.es.13.110182.002025 Google Scholar Vanni, M. J. 1987. Effects of nutrients and zooplankton size on the structure of a phytoplankton community. Ecology 68: 624–635. 10.2307/1938467 Web of Science®Google Scholar Vanni, M. J. 1996. Nutrient transport and recycling by consumers in lake food webs: implications for algal communities. Pages 81–91 in G. A. Polis and K. O. Winemiller, editors. Food webs: integration of pattern and process. Chapman and Hall, New York, New York, USA. Google Scholar Vanni, M. J., and D. L. Findlay . 1990. Trophic cascades and phytoplankton community structure. Ecology 71: 921–937. 10.2307/1937363 Web of Science®Google Scholar Webster, J. R., and T. P. Ehrman . 1996. Solute dynamics. Pages 145–160 in F. R. Hauer and G. A. Lamberti, editors. Methods in stream ecology. Academic Press, San Diego, California, USA. Google Scholar Winemiller, K. O. 1990. Spatial and temporal variation in tropical fish trophic networks. Ecological Monographs 60: 331–367. 10.2307/1943061 Web of Science®Google Scholar Wootton, J. T. 1997. Estimates and test of per capita interaction strength: diet, abundance, and impact of intertidally foraging birds. Ecological Monographs 67: 45–64. 10.1890/0012-9615(1997)067[0045:EATOPC]2.0.CO;2 Web of Science®Google Scholar Wootton, J. T., and M. P. Oemke . 1992. Latitudinal differences in fish community trophic structure, and the role of fish herbivory in a Costa Rican stream. Environmental Biology of Fishes 35: 311–319. 10.1007/BF00001899 Web of Science®Google Scholar Wootton, J. T., and M. E. Power . 1993. Productivity, consumers, and the structure of a river food chain. Proceedings of the National Academy of Sciences USA 90: 1384–1387. 10.1073/pnas.90.4.1384 CASPubMedGoogle Scholar Citing Literature Volume83, Issue7July 2002Pages 1831-1844 ReferencesRelatedInformation
Referência(s)