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Annual Review of Ecology, Evolution, and Systematics

Volume 48, 2017

Attached Algae: The Cryptic Base of Inverted Trophic Pyramids in Freshwaters

Abstract

It seems improbable that a thin veneer of attached algae coating submerged surfaces in lakes and rivers could be the foundation of many freshwater food webs, but increasing evidence from chemical tracers supports this view. Attached algae grow on any submerged surface that receives enough light for photosynthesis, but animals often graze attached algae down to thin, barely perceptible biofilms. Algae in general are more nutritious and digestible than terrestrial plants or detritus, and attached algae are particularly harvestable, being concentrated on surfaces. Diatoms, a major component of attached algal assemblages, are especially nutritious and tolerant of heavy grazing. Algivores can track attached algal productivity over a range of spatial scales and consume a high proportion of new attached algal growth in high-light, low-nutrient ecosystems. The subsequent efficient conversion of the algae into consumer production in freshwater food webs can lead to low-producer, high-consumer biomass, patterns that Elton (1927) described as inverted trophic pyramids. Human perturbations of nutrient, sediment, and carbon loading into freshwaters and of thermal and hydrologic regimes can weaken consumer control of algae and promote nuisance attached algal blooms.

Keyword(s): Cladophora, cyanobacteria, diatoms, grazers, lakes, microphytobenthos, periphyton, primary consumer, primary producer, rivers
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2017-11-02
2024-04-26
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Literature Cited

  1. Abe S-I, Uchida K, Nagumo T, Tanaka J. 2007. Alterations in the biomass-specific productivity of periphyton assemblages mediated by fish grazing. Freshw. Biol. 52:1486–93 [Google Scholar]
  2. Andre ER, Hecky RE, Duthie HC. 2003. Nitrogen and phosphorus regeneration by cichlids in the littoral zone of Lake Malawi, Africa. J. Gt. Lakes Res. 29:Suppl. 2190–201 [Google Scholar]
  3. Barka A, Blecker C. 2016. Microalgae as a potential source of single cell proteins. A review. Biotechnol. Agron. Soc. Environ. 20:427–36 [Google Scholar]
  4. Begon M, Townsend CR, Harper JL. 2006. Ecology: From Individuals to Ecosystems Oxford, UK: Blackwell. , 4th ed..
  5. Bein AM. 2012. Consumer-resource coupling stabilizes and enhances productivity in a fluctuating environment Master's Thesis, McGill Univ Montreal, Quebec, Canada:
  6. Benda L, Dunne T. 1997. Stochastic forcing of sediment routing and storage in channel networks. Water Resourc. Res. 33:2865–80 [Google Scholar]
  7. Benke AC, Henry RLI, Gillespie DM, Hunter RJ. 1985. Importance of snag habitat for animal production in southeastern streams. Fisheries 10:8–13 [Google Scholar]
  8. Benstead BP, Hood JM, Whelan NV, Kendrick MR, Nelson D. et al. 2014. Coupling of dietary phosphorus and growth across diverse fish taxa: a meta-analysis of experimental aquaculture studies. Ecology 95:2768–77 [Google Scholar]
  9. Bode CA, Limm MP, Power ME, Finlay JC. 2014. Subcanopy solar radiation model: predicting solar radiation across a heavily vegetated landscape using LiDAR and GIS solar radiation models. Remote Sens. Environ. 154:387–97 https://doi.org/10.1016/j.rse.2014.01.028 [Crossref] [Google Scholar]
  10. Borchardt MA. 1996. Nutrients. Algal Ecology: Freshwater Benthic Ecosystems RJ Stevenson, ML Bothwell, RL Lowe 183–227 San Diego: Academic [Google Scholar]
  11. Bothwell ML, Taylor BW, Kilroy C. 2014. The Didymo story: the role of low dissolved phosphorus in the formation of Didymosphenia geminata blooms. Diatom Res 29:229–36 https://doi.org/10.1080/0269249X.2014.889041 [Crossref] [Google Scholar]
  12. Bowen SH. 1979. A nutritional constraint in detritivory by fishes: the stunted population of Sarotherodon mossambicus in Lake Sibaya, South Africa. Ecol. Monogr. 49:17–31 [Google Scholar]
  13. Bowen SH, Lutz EV, Ahlgren MO. 1995. Dietary protein and energy as determinants of food quality: trophic strategies compared. Ecology 76:899–907 [Google Scholar]
  14. Brett MT, Bunn SE, Chandra S, Galloway AWE, Fuo F. et al. 2017. How important are terrestrial organic carbon inputs for secondary production in freshwater ecosystems. Freshw. Biol. 62:833–53 [Google Scholar]
  15. Brett MT, Kainz MJ, Taipale SJ, Seshan H. 2009. Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production. PNAS 50:21197–201 [Google Scholar]
  16. Brett MT, Müller-Navarra DC. 1997. The role of essential fatty acids in aquatic food web processes. Freshw. Biol. 38:483–99 [Google Scholar]
  17. Bruggemann JH, Begeman J, Bosma EM, Verburg P, Breeman AM. 1994. Foraging by the stoplight parrotfish Sparisoma viride. II. Intake and assimilation of food, protein and energy. Mar. Ecol. Prog. Ser. 106:57–71 [Google Scholar]
  18. Calow P. 1975. Defaecation strategies of two freshwater gastropods, Ancylusfluviatilis Müll. and Planorbis contortus Linn. (Pulmonata) with a comparison of field and laboratory estimates of food absorption rate. Oecologia 20:51–63 [Google Scholar]
  19. Camacho FA, Thacker RW. 2006. Amphipod herbivory on the freshwater cyanobacterium Lyngbya wollei: chemical stimulants and morphological defenses. Limnol. Oceanogr. 51:1870–75 [Google Scholar]
  20. Capps KA, Flecker AS. 2015. High impact of low-trophic-position invaders: nonnative grazers alter the quality and quantity of basal food resources. Freshw. Sci. 34:784–96 [Google Scholar]
  21. Carpenter SR, Ludwig D, Brock WA. 1999. Management of eutrophication for lakes subject to potentially irreversible change. Ecol. Appl. 9:751–71 [Google Scholar]
  22. Carreira BM, Segurado P, Orizaola G, Gon´çalves N, Pinto V. et al. 2016. Warm vegetarians? Heat waves and diet shifts in tadpoles. Ecology 97:2964–74 [Google Scholar]
  23. Cattaneo A, Mousseau B. 1995. Empirical analysis of the removal rate of periphyton by grazers. Oecologia 103:249–54 [Google Scholar]
  24. Cebrian J. 1999. Patterns in the fate of production in plant communities. Am. Nat. 154:449–68 [Google Scholar]
  25. Cebrian J, Shurin JB, Borer ET, Cardinale BJ, Ngai JT, Smith MD. 2009. Producer nutritional quality controls ecosystem trophic structure. PLOS ONE 4:e4929 [Google Scholar]
  26. Cohen AS, Bills R, Cocquyt CZ, Caljon AG. 1993. The impact of sediment pollution on biodiversity in Lake Tanganyika. Conserv. Biol. 7:667–77 [Google Scholar]
  27. Cole JJ, Carpenter SR, Kitchell JL, Pace ML, Solomon CT, Weidel B. 2011. Strong evidence for terrestrial support of zooplankton in small lakes based on stable isotopes of carbon, nitrogen, and hydrogen. PNAS 108:1975–80 [Google Scholar]
  28. DeNicola DM, McIntire CD. 1991. Effects of hydraulic refuge and irradiance on grazer-periphyton interactions in laboratory streams. J. North Am. Benthol. Soc. 10:251–62 [Google Scholar]
  29. Devlin SP, Vander Zanden MJ, Vadeboncoeur Y. 2013. Depth-specific variation in carbon isotopes demonstrates resource partitioning among the littoral zoobenthos. Freshw. Biol. 11:2389–400 [Google Scholar]
  30. Dietrich WE, Smith JD, Dunne T. 1979. Flow and sediment transport in a sand bedded meander. J. Geol. 87:305–15 [Google Scholar]
  31. Dodds WK. 1991. Community interactions between the filamentous alga Cladophora glomerata (L.) Kuetzing, its epiphytes, and epiphyte grazers. Oecologia 85:572–80 [Google Scholar]
  32. Dodds WK. 2007. Trophic state, eutrophication and nutrient criteria in streams. Trends Ecol. Evol. 22:669–76 [Google Scholar]
  33. Dodds WK, Biggs BJF, Lowe RL. 1999. Photosynthesis-irradiance patterns in benthic microalgae: variations as a function of assemblage thickness and community structure. J. Phycol. 35:42–53 [Google Scholar]
  34. Dodds WK, Gudder DA. 1992. The ecology of Cladophora. J. Phycol. 28:415–27 [Google Scholar]
  35. Dudley TL. 1992. Beneficial effects of herbivores on stream macroalgae via epiphyte removal. Oikos 65:121–27 [Google Scholar]
  36. Dudley TL, D'Antonio CM. 1991. The effects of substrate texture, grazing and disturbance on macroalgal establishment in streams. Ecology 72:297–309 [Google Scholar]
  37. Elton CS. 1927. Animal Ecology London: Sidgwick and Jackson
  38. Engle DL, Melack JM. 1993. Consequences of riverine flooding for seston and the periphyton of floating meadows in Amazon floodplain lakes. Limnol. Oceanogr. 38:1500–20 [Google Scholar]
  39. Evans-White MA, Lamberti GA. 2006. Stoichiometry of consumer driven nutrient recycling across nutrient regimes in streams. Ecol. Lett. 9:1186–97 [Google Scholar]
  40. Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA. et al. 2004. The evolution of modern eukaryotic phytoplankton. Science 305:354–60 [Google Scholar]
  41. Fialkowska E, Pajdak-Stós A. 1997. Inducible defence against a ciliate grazer Pseudomicrothorax dubius, in two strains of Phormidium (cyanobacteria). Proc. R. Soc. B 264:937–41 [Google Scholar]
  42. Finlay JC. 2001. Stable carbon isotope ratios of river biota: implications for energy flow in lotic food webs. Ecology 82:1052–64 [Google Scholar]
  43. Finlay JC, Khandwala S, Power ME. 2002. Spatial scales of carbon flow in a river food web. Ecology 83:1845–59 [Google Scholar]
  44. Flecker AS, Taylor BW. 2004. Tropical fishes as biological bulldozers: density effects on resource heterogeneity and species diversity. Ecology 85:2267–78 [Google Scholar]
  45. Flecker AS, Taylor BW, Bernhardt ES, Hood JM, Cornwell WK. et al. 2002. Interactions between herbivorous fishes and limiting nutrients in a tropical stream ecosystem. Ecology 83:1831–44 [Google Scholar]
  46. Forrester GE, Dudley TL, Grimm NB. 1999. Trophic interactions in open systems: effects of predators on nutrients on stream food chains. Limnol. Oceanogr. 44:1187–97 [Google Scholar]
  47. Fowler JF, Taber CA. 1985. Food habits and feeding periodicity in two sympatric stonerollers (Cyprinidae). Am. Midl. Nat. 113:217–24 [Google Scholar]
  48. Fretwell SD, Lucas HL. 1970. On territorial behavior and other factors influencing habitat distribution in birds. I. Theoretical development. Acta Biotheor 19:16–36 [Google Scholar]
  49. Furey P, Lowe R, Power ME, Campbell-Craven A. 2012. Midges, Cladophora, and epiphytes: shifting interactions through succession. Freshw. Sci. 31:93–107 [Google Scholar]
  50. Furey PC, Kupferberg SJ, Lind AJ. 2014. The perils of unpalatable periphyton: Didymosphenia and other mucilaginous stalked diatoms as food for tadpoles. Diatom Res 29:267–80 [Google Scholar]
  51. Gaiser EE, Childers D, Jones R, Richards J, Scinto L, Trexler J. 2006. Periphyton responses to eutrophication in the Florida Everglades: cross-system patterns of structural and compositional change. Limnol. Oceanogr. 51:617–30 [Google Scholar]
  52. Gaiser EE, Trexler JC, Richards JH, Childers DK, Lee D. et al. 2005. Cascading ecological effects of low-level phosphorus enrichment in the Florida Everglades. J. Environ. Q. 34:717–23 [Google Scholar]
  53. Geddes P, Trexler JC. 2003. Uncoupling of omnivore-mediated positive and negative effects on periphyton mats. Oecologia 136:585–95 [Google Scholar]
  54. Gelwick FP, Matthews WJ. 1992. Effects of an algivorous minnow on temperate stream ecosystem properties. Ecology 73:1630–45 [Google Scholar]
  55. Gladyshev MI, Sushchik NN, Anishchenko OV, Makhutova ON, Kolmakov VI. et al. 2011. Efficiency of transfer of essential polyunsaturated fatty acids versus organic carbon from producers to consumers in a eutrophic reservoir. Oecologia 165:521–31 [Google Scholar]
  56. Godwin SC, Jones SE, Weidel BC, Solomon CT. 2014. Dissolved organic carbon concentration controls benthic primary production: results from in situ chambers in north-temperate lakes. Limnol. Oceanogr. 59:2112–20 [Google Scholar]
  57. González-López CV, del Carmen Cerón García M, Acién Fernández FG, Bustos CS, Chisti Y, Fernández Sevilla JM. 2010. Protein measurements of microalgal and cyanobacterial biomass. Bioresource Technol 101:7587–91 [Google Scholar]
  58. Guo F, Kainz MJ, Sheldon F, Bunn SE. 2016a. The importance of high quality algal food sources in stream food webs—current status and future perspectives. Freshw. Biol. 61:815–31 [Google Scholar]
  59. Guo F, Kainz MJ, Valdez D, Sheldon F, Bunn SE. 2016b. The effect of light and nutrients on algal food quality and their consequent effect on grazer growth in subtropical streams. Freshw. Sci. 35:1202–12 [Google Scholar]
  60. Hall RO, Tank JL, Dybdahl MF. 2003. Exotic snails dominate nitrogen and carbon cycling in a highly productive stream. Front. Ecol. Environ. 1:407–11 [Google Scholar]
  61. Halvorson HM, Scott JT, Sanders AJ, Evans-White MA. 2015. A stream insect detritivore violates common assumptions of threshold elemental ratio bioenergetics models. Freshw. Sci. 34:508–18 [Google Scholar]
  62. Harrison SS, Hildrew AG. 2001. Epilithic communities and habitat heterogeneity in a lake littoral. J. Anim. Ecol. 70:692–707 [Google Scholar]
  63. Hart DD. 1981. Foraging and resource patchiness—field experiments with a grazing stream insect. Oikos 37:46–52 [Google Scholar]
  64. Hart DD, Finelli CM. 1999. Physical-biological coupling in streams: the pervasive effects of flow on benthic organisms. Annu. Rev. Ecol. Syst. 30:363–95 [Google Scholar]
  65. Hecky RE, Hesslein RH. 1995. Contributions of benthic algae to lake food webs as revealed by stable isotope analysis. J. North Am. Benthol. Soc. 14:631–53 [Google Scholar]
  66. Herren CM, Webert KC, Drake MD, Vander Zanden MJ, Einarsson A. et al. 2017. Positive feedbacks between chironomids and algae creates net mutualism between benthic primary consumers and producers. Ecology447–55
  67. Higgins SN, Hecky RE, Taylor WD. 2001. Epilithic nitrogen fixation in the rocky littoral zones of Lake Malawi, Africa. Limnol. Oceanogr. 46:976–82 [Google Scholar]
  68. Higgins SN, Malkin SY, Howell ET, Guildford SJ, Campbell L. et al. 2008. An ecological review of Cladophora glomerata (Chlorophyta) in the Laurentian Great Lakes. J. Phycol. 44:839–54 [Google Scholar]
  69. Hill WR. 1996. Effects of light. Algal Ecology: Freshwater Benthic Ecosystems RJ Stevenson, ML Bothwell, RL Lowe 121–49 San Diego: Academic [Google Scholar]
  70. Hill WR, Fanta SE. 2008. Phosphorus and light co-limit periphyton growth at subsaturating irradiances. Freshw. Biol. 53:215–25 [Google Scholar]
  71. Hill WR, Mulholland PJ, Marzolf ER. 2001. Stream ecosystem responses to forest leaf emergence in spring. Ecology 82:2306–19 [Google Scholar]
  72. Hill WR, Rinchard J, Czesny S. 2011. Light, nutrients and the fatty acid composition of stream periphyton. Freshw. Biol. 56:1825–36 [Google Scholar]
  73. Hill WR, Ryon MG, Schilling EM. 1995. Light limitation in a stream ecosystem: responses by primary producers and consumers. Ecology 76:1297–309 [Google Scholar]
  74. Hill WR, Smith JG, Stewart AJ. 2010. Light, nutrients and herbivore growth in oligotrophic streams. Ecology 91:518–27 [Google Scholar]
  75. Hillebrand H. 2008. Grazing regulates the spatial variability of periphyton biomass. Ecology 89:165–73 [Google Scholar]
  76. Hillebrand H. 2009. Meta-analysis of grazer control of periphyton biomass across aquatic ecosystems. J. Phycol. 45:798–806 [Google Scholar]
  77. Hillebrand H, Sommer U. 1999. The nutrient stoichiometry of benthic microalgal growth: Redfield proportions are optimal. Limnol. Oceanogr. 44:440–46 [Google Scholar]
  78. Hori M, Yamaoka K, Takamura K. 1983. Abundance and micro-distribution of Cichlid fishes on a rocky shore of Lake Tanganyika. Afr. Study Monogr. 3:25–38 [Google Scholar]
  79. Humphreys WF. 1979. Production and respiration in animal populations. J. Anim. Ecol. 48:427–53 [Google Scholar]
  80. Ings NE, Hildrew AG, Grey J. 2010. Gardening by the psychomyiid caddisfly Tinodes waeneri: evidence from stable isotopes. Oecologia 163:127–39 [Google Scholar]
  81. Izagirre O, Serra A, Guasch H, Elosegi A. 2009. Effects of sediment deposition on periphytic biomass, photosynthetic activity and algal community structure. Sci. Total Environ. 407:5694–700 [Google Scholar]
  82. John DM. 2003. Filamentous and plantlike green algae. Freshwater Algae of North America JD Wehr, RG Sheath 311–52 New York: Academic [Google Scholar]
  83. Junk WJ, Bayley PB, Sparks RE. 1989. The flood pulse concept in river-floodplain systems. Proceeding of the International Large River Symposium DP Dodge 110–27 Ottawa, Can: Can. Spec. Publ. Fish. Aquat. Sci. [Google Scholar]
  84. Karasov WH, Martínez del Rio C. 2007. Physiological Ecology: How Animals Process Energy, Nutrients, and Toxins Princeton, NJ: Princeton Univ. Press
  85. Karlsson J, Byström P, Ask J, Ask P, Persson L, Jansson M. 2009. Light limitation of nutrient-poor lake ecosystems. Natur 460:506–9 [Google Scholar]
  86. Kelly PT, Solomon CT, Weidel BC, Jones SE. 2014. Terrestrial carbon is a resource, but not a subsidy, for lake zooplankton. Ecology 95:1236–42 [Google Scholar]
  87. Koehl M, Strickler J. 1981. Copepod feeding currents—food capture at low Reynolds-number. Limnol. Oceanogr. 26:1062–73 [Google Scholar]
  88. Kohler SL. 1984. Search mechanism of a stream grazer in patchy environments: the role of food abundance. Oecologia 62:209–18 [Google Scholar]
  89. Komárek J, Kling H, Komárková J. 2003. Filamentous cyanobacteria. Freshwater Algae of North America Wehr JD, Sheath RG 117–96 New York: Academic [Google Scholar]
  90. Krause-Jensen D, Sand-Jensen K. 1998. Light attenuation and photosynthesis of aquatic plant communities. Limnol. Oceanogr. 43:396–407 [Google Scholar]
  91. Krienitz L, Ballot A, Kotut K, Wiegand C, Putz S. et al. 2003. Contribution of hot spring cyanobacteria to the mysterious deaths of Lesser Flamingos at Lake Bogoria, Kenya. FEMS Microbiol. Ecol. 43:141–48 [Google Scholar]
  92. Kupferberg SJ, Marks JC, Power ME. 1994. Variation in natural algal and detrital diets affects Larval Anuran (Hyla regilla) life history traits. Copeia 1994:446–57 [Google Scholar]
  93. Lamberti GA. 1996. The role of periphyton in benthic food webs. Algal Ecology: Freshwater Benthic Ecosystems RJ Stevenson, ML Bothwell, RL Lowe 533–73 San Diego: Academic [Google Scholar]
  94. Lau DC, Leung KMY, Dudgeon D. 2009. Are autochthonous foods more important than allochthonous resources to benthic consumers in tropical headwater streams. J. North Am. Benthol. Soc. 28:426–39 [Google Scholar]
  95. Lau DC, Sundh I, Vrede T, Pickova J, Goedkoop W. 2014. Autochthonous resources are the main driver of consumer production in dystrophic boreal lakes. Ecology 95:1506–19 [Google Scholar]
  96. Lee DS, Gilbert SCR, Hocutt CH, Jenkins RE, McAllister DE, Stauffer JR. 1980. Atlas of North American Freshwater Fishes Raleigh, NC: N.C. State Mus. Nat. Hist.
  97. Lewis WM Jr., Hamilton SK, Rodríguez MA, Saunders JF III, Lasi MA. 2001. Foodweb analysis of the Orinoco floodplain based on production estimates and stable isotope data. 2001. J. North Am. Benthol. Soc. 20:241–54 [Google Scholar]
  98. Liess A, Hillebrand H. 2004. Invited review: direct and indirect effects in herbivore–periphyton interactions. Arch. Hydrobiol. 159:4433–53 [Google Scholar]
  99. Lindeman RL. 1942. The trophic-dynamic aspect of ecology. Ecology 23:399–418 [Google Scholar]
  100. Liras V, Lindberg N, Nystom P, Annadotter H, Lawton LA, Graf B. 1998. Can ingested cyanobacteria be harmful to the signal crayfish (Pacifastacus leniusculus). Freshw. Biol. 39:233–42 [Google Scholar]
  101. Lorenz RC, Herdendorf CE. 1982. Growth dynamics of Cladophora glomerata in Western Lake Erie in relation to some environmental factors. J. Gt. Lakes Res. 8:42–53 [Google Scholar]
  102. Lowe RL. 1996. Periphyton patterns in lakes. Algal Ecology: Freshwater Benthic Ecosystems RJ Stevenson, ML Bothwell, RL Lowe 57–77 San Diego: Academic [Google Scholar]
  103. Lowe RL, Hunter RD. 1988. Effect of grazing by Physa integra on periphyton community structure. J. North Am. Benthol. Soc. 7:29–36 [Google Scholar]
  104. Makhutova ON, Shulepina SP, Sharapova TA, Dubovskaya OP, Sushchik NN. et al. 2016. Content of polyunsaturated fatty acids essential for fish nutrition in zoobenthos species. Freshw. Sci. 35:1222–34 [Google Scholar]
  105. Malkin SY, Bocaniov SA, Smith RE, Guildford SJ, Hecky RE. 2010. In situ measurements confirm the seasonal dominance of benthic algae over phytoplankton in nearshore primary production of a large lake. Fresh. Biol. 55:2468–83 [Google Scholar]
  106. Marks JC, Lowe RL. 1993. Interactive effects of nutrient availability and light levels on the periphyton composition of a large oligotrophic lake. Can. J. Fish. Aquat. Sci. 50:1270–78 [Google Scholar]
  107. Marks JC, Power ME, Parker MS. 2000. Flood disturbance, algal productivity, and interannual variation in food chain length. Oikos 90:20–27 [Google Scholar]
  108. Matthews WJ, Stewart AM, Power ME. 1987. Grazing fishes as components of North American stream ecosystems: effects of Campostomaanomalum. Community and Evolutionary Ecology of North American Stream Fishes WJ Matthews, DC Heins 128–35 Norman, OK: Univ. Okla. Press [Google Scholar]
  109. Mayer MS, Likens GE. 1987. The importance of algae in a shaded headwater stream as food source for an abundant caddisfly (Trichoptera). J. North Am. Benthol. Soc. 6:262–69 [Google Scholar]
  110. McAllister TG, Wood SA, Hawes I. 2016. The rise of toxic benthic Phormidium proliferations: a review of their taxonomy, distribution, toxin content and factors regulating prevalence and increased severity. Harmful Algae 55:282–94 [Google Scholar]
  111. McCollum EW, Crowder LB, McCollum SA. 1998. Complex interactions of fish, snails, and littoral zone periphyton. Ecology 79:1980–94 [Google Scholar]
  112. McCullough DA, Minshall GW, Cushing CE. 1979a. Bioenergetics of a stream “collector” organism, Tricorythodes minutus (Insecta: Ephemeroptera). Limnol. Oceanogr. 24:45–58 [Google Scholar]
  113. McCullough DA, Minshall GW, Cushing CE. 1979b. Bioenergetics of lotic filter-feeding insects Simulium spp. (diptera) and Hydropsyche occidentalis (Trichoptera) and their function in controlling organic transport in streams. Ecology 60:585–96 [Google Scholar]
  114. McIntyre PB, Flecker AS, Vanni MJ, Hood JM, Taylor BW, Thomas SA. 2008. Fish distributions and nutrient cycling in streams: Can fish create biogeochemical hotspots. Ecology 89:2335–46 [Google Scholar]
  115. Moore JW. 1977. Some factors effecting algal consumption in subarctic Ephemeroptera, Plecoptera and Simuliidae. Oecologia 27:261–73 [Google Scholar]
  116. Moriarty DJW. 1973. The physiology of digestion of bluegreen algae in the cichlid fish. Tilapia nilotica. J. Zool. Lond. 171:25–39 [Google Scholar]
  117. Moss B. 2015. Mammals, freshwater reference states, and the mitigation of climate change. Freshw. Biol. 60:1964–76 [Google Scholar]
  118. Mulholland. 1996. Role of nutrient cycling in streams. Algal Ecology: Freshwater Benthic Ecosystems RJ Stevenson, ML Bothwell, RL Lowe 609–40 San Diego: Academic [Google Scholar]
  119. Munubi RN. 2015. Algal quality controls the distribution, behavior and growth of algivorous cichlids in Lake Tanganyika PhD Dissertation. Wright State University, Dayton, OH
  120. Nagarkar S, Williams GA, Subramanian G, Saha SK. 2004. Cyanobacteria-dominated biofilms: a high quality food resource for intertidal grazers. Hydrobiologia 512:89–95 [Google Scholar]
  121. Ogdahl ME, Lougheed VL, Stevenson RJ, Steinman AD. 2010. Influences of multi-scale habitat on metabolism in a coastal Great Lakes watershed. Ecosystems 11:222–38 [Google Scholar]
  122. Oksanen T, Power ME, Oksanen L. 1995. Ideal free habitat selection and consumer-resource dynamics. Am. Nat. 146:565–85 [Google Scholar]
  123. O'Reilly CM. 2006. Seasonal dynamics of periphyton in a large tropical lake. Hydrobiologia 553:293–301 [Google Scholar]
  124. Paerl HW, Otten TG, Joiner AR. 2016. Moving towards adaptive management of cyanotoxin-impaired water bodies. Microb. Biotechnol. 9:641–51 [Google Scholar]
  125. Peters RH, Downing JA. 1984. Empirical analysis of zooplankton filtering and feeding rates. Limnol. Oceanogr. 29:763–84 [Google Scholar]
  126. Peterson CG, Grimm NB. 1992. Temporal variation in enrichment effects during periphyton succession in a nitrogen-limited desert stream ecosystem. J. North Am. Benthol. Soc. 11:20–36 [Google Scholar]
  127. Power ME. 1983. Grazing responses of tropical freshwater fishes to different scales of variation in their food. Environ. Biol. Fishes 9:103–15 [Google Scholar]
  128. Power ME. 1984a. Habitat quality and the distribution of algae-grazing catfish in a Panamanian stream. J. Anim. Ecol. 53:357–74 [Google Scholar]
  129. Power ME. 1984b. Depth-distribution of armored catfish: predator-induced resource avoidance. Ecology 65:523–28 [Google Scholar]
  130. Power ME. 1990a. Resource enhancement by indirect effects of grazers: armored catfish, algae, and sediment. Ecology 71:897–904 [Google Scholar]
  131. Power ME. 1990b. Effects of fish in river food webs. Science 250:811–14 [Google Scholar]
  132. Power ME. 1991. Shifts in the effects of tuft-weaving midges on filamentous algae. Am. Midl. Nat. 125:275–85 [Google Scholar]
  133. Power ME. 1992. Hydrologic and trophic controls of seasonal algal blooms in northern California rivers. Arch. Hydrobiol. 125:384–410 [Google Scholar]
  134. Power ME, Bouma-Gregson K, Higgins P, Carlson SM. 2015. The thirsty Eel: summer and winter flow thresholds that tilt the Eel River of northwestern California from salmon-supporting to cyanobacterially degraded states. Copeia 103:200–11 [Google Scholar]
  135. Power ME, Dudley TL, Cooper SD. 1989. Grazing catfish, fishing birds, and attached algae in a Panamanian stream. Environ. Biol. Fishes 26:285–94 [Google Scholar]
  136. Power ME, Lowe R, Furey P, Welter J, Limm M. et al. 2009. Algal mats and insect emergence in rivers under Mediterranean climates: towards photogrammetric surveillance. Freshw. Biol. 54:2101–15 [Google Scholar]
  137. Power ME, Matthews WJ. 1983. Algae-grazing minnows (Campostoma anomalum), piscivorous bass (Micropterus spp.) and the distribution of attached algae in a small prairie-margin stream. Oecologia 60:328–32 [Google Scholar]
  138. Power ME, Matthews WJ, Stewart AJ. 1985. Grazing minnows, piscivorous bass, and stream algae: dynamics of a strong interaction. Ecology 66:1448–56 [Google Scholar]
  139. Power ME, Parker MS, Dietrich WE. 2008. Seasonal reassembly of a river food web: floods, droughts, and impacts of fish. Ecol. Monogr. 78:263–82 [Google Scholar]
  140. Power ME, Stewart AJ, Matthews WJ. 1988. Grazer control of algae in an Ozark Mountain stream: effects of short-term exclusion. Ecology 69:1894–98 [Google Scholar]
  141. Puschner B, Hoff B, Tor ER. 2008. Diagnosis of anatoxin-a poisoning in dogs from North America. J. Vet. Diagn. Investig. 20:89–92 [Google Scholar]
  142. Rautio M, Vincent WF. 2006. Benthic and pelagic food resources for zooplankton in shallow high-latitude lakes. Freshw. Biol. 51:1038–52 [Google Scholar]
  143. Rier ST, Kuehn KA, Francoeur SN. 2007. Algal regulation of extracellular enzyme activity in stream microbial communities associated with inert substrata and detritus. J. North Am. Benthol. Soc. 26:439–49 [Google Scholar]
  144. Rosemond AD, Mulholland PJ, Elwood JW. 1993. Top-down and bottom-up control of stream periphyton: effects of nutrients and herbivores. Ecology 74:1264–80 [Google Scholar]
  145. Royama T. 1971. Evolutionary significance of predators’ response to local differences in prey density: a theoretical study. Proceeding of the Advanced Study Institute on Dynamics of Numbers in Populations344–57 Wageningen, Neth.: Cent. Agric. Pub. Doc. [Google Scholar]
  146. Smith JL, Haney JF. 2006. Foodweb transfer, accumulation, and depuration of microcystins, a cyanobacterial toxin, in pumpkinseed sunfish (Lepomis gibbosus). Toxicon 48:580–89 [Google Scholar]
  147. Smucker NJ, Drerup SA, Vis ML. 2014. Roles of benthic algae in the structure, function, and assessment of stream ecosystems affected by acid mine drainage. J. Phycol. 50:425–36 [Google Scholar]
  148. Sousa WP. 1984. The role of disturbance in natural communities. Annu. Rev. Ecol. Syst. 15:353–91 [Google Scholar]
  149. Steinman AD. 1996. Effects of grazers on freshwater benthic algae. Algal Ecology: Freshwater Benthic Ecosystems RJ Stevenson, ML Bothwell, RL Lowe 341–73 San Diego: Academic [Google Scholar]
  150. Sterner RW, Elser JJ. 2002. Ecological stoichiometry: the biology of elements from molecules to the biosphere Princeton, NJ: Princeton Univ. Press
  151. Stevenson RJ, Bothwell ML, Lowe RL. 1996. Algal Ecology: Freshwater Benthic Ecosystems San Diego: Academic
  152. Stevenson RJ, Stoermer EF. 1982. Seasonal abundance patterns of diatoms on Cladophora in Lake Huron. J. Gt. Lakes Res. 8:169–83 [Google Scholar]
  153. Stoddard JL, Larsen DP, Hawkins CP, Johnson RK, Norris RH. 2006. Setting expectations for the ecological condition of streams: the concept of reference condition. Ecol. Appl. 16:1267–76 [Google Scholar]
  154. Strandberg U, Taipale SJ, Hiltunen M, Galloway AWE, Brett MT, Kankaala P. 2015. Inferring phytoplankton community composition with a fatty acid mixing model. Ecosphere 6:11–18 https://doi.org/10.1890/ES14-00382.1 [Crossref] [Google Scholar]
  155. Sturmbauer C, Dallinger R. 1995. Diurnal variation of spacing and foraging behavior in Tropheus moorii (Cichlidae) in Lake Tanganyika, eastern Africa. Neth. J. Zool. 45:386–401 [Google Scholar]
  156. Sturt MM, Jansen MAK, Harrison SSC. 2011. Invertebrate grazing and riparian shade as controllers of nuisance algae in a eutrophic river. Freshw. Biol. 56:2580–93 [Google Scholar]
  157. Takamura K. 1984. Interspecific relationships of aufwuchs-eating fishes in Lake Tanganyika. Environ. Biol. Fishes 10:225–41 [Google Scholar]
  158. Takeuchi Y, Ochi H, Kohda M, Sinyinza D, Hori M. 2010. A 20-year census of a rocky littoral fish community in Lake Tanganyika. Ecol. Freshw. Fish 19:239–48 [Google Scholar]
  159. Tall L, Cloutier L, Cattaneo A. 2006. Grazer–diatom size relationships in an epiphytic community. Limnol. Oceanogr. 51:1211–16 [Google Scholar]
  160. Talling JF, Rzoska J. 1967. The development of plankton in relation to hydrological regime in the Blue Nile. J. Ecol. 55:637–62 [Google Scholar]
  161. Thorp JH, Delong MD. 2002. Dominance of autochthonous autotrophic carbon in food webs of heterotrophic rivers. Oikos 96:543–50 [Google Scholar]
  162. Tibbetts SM, Milley JE, Lall SP. 2015. Chemical composition and nutritional properties of freshwater and marine microalgal biomass cultured in photobioreactors. J. Appl. Phycol. 27:1109–19 [Google Scholar]
  163. Torres-Ruiz M, Wehr JD, Perrone AA. 2007. Trophic relations in a stream food web: importance of fatty acids for macroinvertebrate consumers. J. North Am. Benthol. Soc. 26:509–22 [Google Scholar]
  164. Trexler JC, Gaiser EE, Kominoski JS, Sanchez J. 2015. The role of periphyton mats in consumer community structure and function in calcareous wetlands: lessons from the Everglades. Microbiology of the Everglades Ecosystem JA Entry, AD Gottlieb, K Jayachandrahan, A Ogram 155–79 Boca Raton, FL: CRC Press [Google Scholar]
  165. Vadeboncoeur Y, Devlin SP, McIntyre PB, Vander Zanden MJ. 2014. Is there light after depth? Distribution of periphyton chlorophyll and productivity in lake littoral zones. Freshw. Sci. 33:524–36 [Google Scholar]
  166. Vadeboncoeur Y, Jeppesen E, Vander Zanden MJ, Schierup H-H, Christoffersen K, Lodge DM. 2003. From Greenland to green lakes: cultural eutrophication and the loss of benthic energy pathways in lakes. Limnol. Oceanogr. 48:1408–18 [Google Scholar]
  167. Vadeboncoeur Y, Lodge DM, Carpenter SR. 2001. Whole-lake fertilization effects on the distribution of primary production between benthic and pelagic habitats. Ecology 82:1065–77 [Google Scholar]
  168. Vadeboncoeur Y, McCann KS, Vander Zanden MJ, Rasmussen JB. 2005. Effects of multi-chain omnivory on the strength and stability of trophic control in lakes. Ecosystems 8:682–93 [Google Scholar]
  169. Vadeboncoeur Y, McIntyre PB, Vander Zanden MJ. 2011. Borders of biodiversity: life at the edge of the world's large lakes. BioScience 61:526–37 [Google Scholar]
  170. Vadeboncoeur Y, Peterson G, Vander Zanden MJ, Kalff J. 2008. Benthic algal production across lake-size gradients: interactions among morphometry, nutrients and light. Ecology 89:2542–52 [Google Scholar]
  171. Vadeboncoeur Y, Vander Zanden MJ, Lodge DM. 2002. Putting the lake back together: reintegrating benthic pathways into lake food web models. BioScience 52:44–55 [Google Scholar]
  172. Vander Zanden MJ, Chandra S, Park S-K, Vadeboncoeur Y, Goldman CR. 2006. Efficiencies of benthic and pelagic trophic pathways in a subalpine lake. Can. J. Fish. Aquat. Sci. 63:2608–20 [Google Scholar]
  173. Vander Zanden MJ, Rasmussen JB. 1999. Primary consumer δ13C and δ15N and the trophic position of aquatic consumers. Ecology 80:1395–404 [Google Scholar]
  174. Vander Zanden MJ, Vadeboncoeur Y. 2002. Fishes as integrators of benthic and pelagic food webs in lakes. Ecology 83:2152–61 [Google Scholar]
  175. Vander Zanden MJ, Vadeboncoeur Y, Chandra S. 2011. Fish reliance on littoral–benthic resources and the distribution of primary production in lakes. Ecosystems 14:894–903 [Google Scholar]
  176. Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE. 1980. The river continuum concept. Can. J. Fish. Aquat. Sci. 37:130–37 [Google Scholar]
  177. Wagenhoff A, Lange K, Townsend CR, Matthaei CD. 2013. Patterns of benthic algae and cyanobacteria along twin-stressor gradients of nutrients and fine sediment: a stream mesocosm experiment. Freshw. Biol. 58:1849–63 [Google Scholar]
  178. Wagner CE, McIntyre PB, Buels KS, Gilbert DM, Michel E. 2009. Diet predicts intestine length in Lake Tanganyika's cichlid fishes. Funct. Morphol. 23:1122–31 [Google Scholar]
  179. Wagner ND, Hillebrand H, Whacker A, Frost PC. 2013. Nutritional indicators and their uses in ecology. Ecol. Lett. 16:535–44 [Google Scholar]
  180. Wetzel RG. 2001. Limnology: Lake and River Ecosystems San Diego: Academic. , 3rd ed..
  181. Whitton BA. 1970. Biology of Cladophora in freshwaters. Water Res 4:457–76 [Google Scholar]
  182. Whitton BA, Mateo P. 2013. Rivulariaceae. Ecology of Cyanobacteria II: Their Diversity in Space and Time BA Whitton 561–91 Dordrecht, Neth.: Springer [Google Scholar]
  183. Wood SA, Kuhajek JM, de Winton M, Phillips NR. 2011. Species composition and cyanotoxin production in periphyton mats from three lakes of varying trophic status. FEMS Microbiol. Ecol. 79:312–26 [Google Scholar]
  184. Wood SA, Phillips NR, de Winton M, Gibbs M. 2012. Consumption of benthic cyanobacterial mats and nodularin-R accumulation in freshwater crayfish (Paranephrops planifrons) in Lake Tikitapu (Rotorua, New Zealand). Harmful Algae 20:175–79 [Google Scholar]
  185. Wootton JT, Parker MS, Power ME. 1996. Effects of disturbance on river food webs. Science 273:1558–60 [Google Scholar]
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Attached Algae: The Cryptic Base of Inverted Trophic Pyramids in Freshwaters
Annual Review of Ecology, Evolution, and Systematics 48, 255 (2017); https://doi.org/10.1146/annurev-ecolsys-121415-032340
/content/journals/10.1146/annurev-ecolsys-121415-032340
/content/journals/10.1146/annurev-ecolsys-121415-032340
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