, Volume 136, Issue 4, pp 585–595 | Cite as

Uncoupling of omnivore-mediated positive and negative effects on periphyton mats

  • Pamela GeddesEmail author
  • Joel C. Trexler
Community Ecology


The riverine grass shrimp (Palaemonetes paludosus) and eastern mosquitofish (Gambusia holbrooki) consume periphyton and small invertebrates, potentially affecting periphyton through negative effects (i.e., consumption) and/or positive effects such as nutrient regeneration, physical stimulation, and trophic cascades. We performed field experiments in the Everglades in which omnivores and periphyton were maintained in cages, with a fraction of the periphyton held in omnivore-exclusion bags that allowed passage of nutrients but prevented its consumption or physical disturbance. In some instances, periphyton growth rate increased with increasing omnivore biomass. Omnivores probably stimulated periphyton growth through nutrient regeneration, possibly subsidizing periphyton with nutrients derived from ingested animal prey. The net balance of omnivore-mediated negative and positive effects varied among experiments because of seasonal and spatial differences in periphyton characteristics. Consumption of periphyton mats might have been reduced by the arrangement of palatable algae (green algae and diatoms) within a matrix of unpalatable ones (CaCO3-encrusting filamentous cyanobacteria). In a laboratory feeding experiment, mosquitofish consumed more green algae and diatoms in treatments with disrupted mat structure than in those with intact mats. No difference in diet was observed for shrimp. Our study underscores the complexity of consumer-periphyton interactions in which periphyton edibility affects herbivory and consumers influence periphyton through multiple routes that cannot be fully appreciated in experiments that only investigate net effects.


Florida Everglades Grazing Omnivory Periphyton Positive and negative effects 



We thank Ron Jones and the Southeastern Environmental Research Center (SERC) for processing nutrient samples, and Sue Perry for assistance and support. Thanks to the 23 people who helped with fieldwork, making this project possible. We thank J.H. Chick who provided help with several conceptual areas of this project. We also greatly appreciate the comments of C. Osenberg, which improved this manuscript considerably. This work was funded by cooperative agreement number CA5280-8-9002 between Everglades National Park and Florida International University, and a fellowship to P. Geddes from the FIU Tropical Biology Program. This is SERC contribution 199 and 61 of the FIU Tropical Biology Program.


  1. Atsatt PR, O'Dowd DJ (1976) Plant defense guilds. Science 193:24–29Google Scholar
  2. Beck JT, Cowell BC (1976) Life history and ecology of the freshwater caridean shrimp, Palaemonetes paludosus (Gibbes). Am Midl Nat 96:52–65Google Scholar
  3. Bouchard SS, Bjorndal KA (2000) Sea turtles as biological transporters of nutrients and energy from marine to terrestrial ecosystems. Ecology 81:2305–2313Google Scholar
  4. Brabrand A, Faafeng BA, Moritz Nilssen JP (1990) Relative importance of phosphorus supply to phytoplankton production: Fish excretion versus external loading. Can J Fish Aquat Sci 47:364–372Google Scholar
  5. Carpenter SR, Cottingham KL, Schindler DE (1992) Biotic feedbacks in lake phosphorus cycles. Trends Ecol Evol 7:332–336Google Scholar
  6. Cattaneo A, Mousseau B (1995) Empirical analysis of the removal rate of periphyton by grazers. Oecologia 103:249–254Google Scholar
  7. Cuker BE (1983) Grazing and nutrient interactions in controlling the activity and composition of the epilithic algal community of an arctic lake. Limnol Oceanogr 28:133–141Google Scholar
  8. DeAngelis DL (1992) Dynamics of nutrient cycling and food webs, 1st edn. Chapman & Hall, New YorkGoogle Scholar
  9. Deegan LA (1993) Nutrient and energy transport between estuaries and coastal marine ecosystems by fish migration. Can J Fish Aquat Sci 50:74–49Google Scholar
  10. Diehl S (1993) Relative consumer sizes and the strengths of direct and indirect interactions in omnivorous feeding relationships. Oikos 68:151–157Google Scholar
  11. Drenner RW, Smith JD, Threlkeld ST (1996) Lake trophic state and the limnological effect of omnivorous fish. Hydrobiologia 319:213–223Google Scholar
  12. Eaton AD, Clesceri LS, Greenberg AE (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association, Washington, DCGoogle Scholar
  13. Elser JJ, Goldman CR (1990) Experimental separation of the direct and indirect effects of herbivorous zooplankton on phytoplankton in a subalpine lake. Verh Int Verein Limnol 24:493–498Google Scholar
  14. Feminella JW, Hawkins CP (1995) Interactions between stream herbivores and periphyton: a quantitative analysis of past experiments. J North Am Benthol Soc 14:465–509Google Scholar
  15. Geddes P (1999) Omnivory and periphyton mats: uncoupling and quantifying consumer effects in the Florida Everglades. Master's Thesis. Florida International University, Miami, Fla.Google Scholar
  16. Gresens SE (1995) Grazer diversity, competition and the response of the periphyton community. Oikos 73:336–346Google Scholar
  17. Hay ME, Kappel QE, Fenical W (1994) Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality. Ecology 75:1714–1726Google Scholar
  18. Hillebrand H, Kahlert M (2001) Effect of grazing and nutrient supply on periphyton biomass and nutrient stoichiometry in habitats of different productivity. Limnol Oceanogr 46:1881–1898Google Scholar
  19. Hudson JJ, Taylor WD, Schindler DW (1999) Planktonic nutrient regeneration and cycling efficiency in temperate lakes. Nature 400:659–661CrossRefGoogle Scholar
  20. Hunt BP (1952) Food relationships between Florida spotted gar and other organisms in the Tamiami Canal, Dade County, Florida. Trans Am Fish Soc 82:13–33Google Scholar
  21. Huntly N (1991) Herbivores and the dynamics of communities and ecosystems. Annu Rev Ecol Syst 22:477–503CrossRefGoogle Scholar
  22. Jones JI, Moss B, Young JO (1998) Interactions between periphyton, nonmolluscan invertebrates, and fish in standing freshwaters. In: Jeppesen E, Sondergaard M, Sondergaard M, Christoffersen K (eds) The structuring role of submerged macrophytes in lakes, 1st edn. Springer, Berlin Heidelberg New York, pp 69–90Google Scholar
  23. Kitchell JF, O'Neill RV, Webb D, Gallepp GW, Bartell SM, Koonce JF, Ausmus BS (1979) Consumer regulation on nutrient cycling. BioScience 29:28–34Google Scholar
  24. Krause PR, Bray RN (1994) Transport of cadmium and zinc to rocky reef communities in feces of the blacksmith (Chromis punctipinnis), a planktivorous fish. Mar Env Res 38:33–42Google Scholar
  25. Kupferberg S (1997) Facilitation of periphyton production by tadpole grazing: functional differences between species. Freshw Biol 37:427–439Google Scholar
  26. Kushlan JA, Voorhees SA, Loftus WF, Frohring PC (1986) Length, mass, and calorific relationships of Everglades animals. Fla Sci 49:65–79Google Scholar
  27. Lamarra VA (1975) Digestive activities of carp as a major contributor to the nutrient loading of lakes. Verh Int Verein Limnol 19:2461–2468Google Scholar
  28. Lamberti GA (1996) The role of periphyton in benthic food webs. In: Stevenson RJ, Bothwell ML, Lowe RL (eds) Algal ecology, 1st edn. Academic Press, San Diego, pp 533–564Google Scholar
  29. Leibold MA (1989) Resource edibility and the effects of predators and productivity on the outcome of trophic interactions. Am Nat 134:922–949CrossRefGoogle Scholar
  30. Loftus WF (2000) Accumulation and fate of mercury in an everglades aquatic food web. PhD dissertation, Florida International University, Miami, Fla.Google Scholar
  31. Loftus WF, Eklund A (1994) Long-term dynamics of an Everglades small-fish assemblage. In: Davis SM, Ogden JC (eds) Everglades: the ecosystem and its restoration, 1st edn. St. Lucie Press, Delray Beach, pp 461–484Google Scholar
  32. Loreau M (1995) Consumers as maximizers of matter and energy flow in ecosystems. Am Nat 145:22–42CrossRefGoogle Scholar
  33. Matveev V, Matveeva L, Jones GJ (1994) Phytoplankton stimulation by mosquitofish in the presence of large Daphnia. Verh Int Verein Limnol 25:2193–2197Google Scholar
  34. de Mazancourt C, Loreau M, Abbadie L (1998) Grazing optimization and nutrient cycling: when do herbivores enhance plant production? Ecology 79:2242–2252Google Scholar
  35. McCormick PV (1994) Evaluating the multiple mechanisms underlying herbivore-algal interactions in streams. Hydrobiologia 291:47–59Google Scholar
  36. McCormick PV, O'Dell MB (1996) Quantifying periphyton responses to phosphorus in the Florida Everglades: a synoptic-experimental approach. J North Am Benthol Soc 15:450-468Google Scholar
  37. McCormick PV, Stevenson RJ (1991) Grazer control of nutrient availability in the periphyton. Oecologia 86:287–291Google Scholar
  38. McCormick PV, Rawlik PS, Lurding K, Smith EP, Sklar FH (1996) Periphyton-water relationships along a nutrient gradient in the northern Florida Everglades. J North Am Benthol Soc 15:433–449Google Scholar
  39. McNaughton SJ (1978) Serengeti ungulates: feeding selectivity influences the effectiveness of plant defense guilds. Science 199:806–807Google Scholar
  40. Merz MUE (1992) The biology of carbonate precipitation by cyanobacteria. Facies 26:81–102Google Scholar
  41. Meyer JL, Schultz ET, Helfman GS (1983) Fish schools: an asset to corals. Science 220:1047-1049Google Scholar
  42. Newman JA, Bergelson J, Grafen A (1997) Blocking factors and hypothesis testing in ecology: is your statistics text wrong? Ecology 78:1312–1320Google Scholar
  43. Pennings SC, Paul VJ (1992) Effect of plant toughness, calcification, and chemistry on herbivory by Dolabella auricularia. Ecology 73:1606–1619Google Scholar
  44. Pfister CA, Hay ME (1988) Associational plant refuges: convergent patterns in marine and terrestrial communities result from differing mechanisms. Oecologia 77:118–129Google Scholar
  45. Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–846CrossRefGoogle Scholar
  46. Porter KG (1976) Enhancement of algal growth and productivity by grazing zooplankton. Science 192:1332–1334Google Scholar
  47. Porter KG (1977) The plant-animal interface in freshwater ecosystems. Am Sci 65:159–170Google Scholar
  48. Power ME (1990) Resource enhancement by indirect effects of grazers: Armored catfish, algae, and sediment. Ecology 71:897–904Google Scholar
  49. Pringle CM, Blake GA, Covich AP, Buzby KM, Finley A (1993) Effects of omnivorous shrimp in a montane tropical stream: sediment removal, disturbance of sessile invertebrates and enhancement of understory algal biomass. Oecologia 93:1–11Google Scholar
  50. Schaus MH, Vanni MJ (2000) Effects of gizzard shad on phytoplankton and nutrient dynamics: role of sediment feeding and fish size. Ecology 81:1701–1719Google Scholar
  51. Schindler DE, Scheuerell MD (2002) Habitat coupling in lake ecosystems. Oikos 98:177–189CrossRefGoogle Scholar
  52. Schindler DE, Carpenter SR, Cottingham KL, He X, Hodgson JR, Kitchell JF, Soranno PA (1996) Food web structure and littoral zone coupling to pelagic trophic cascades. In: Polis GA, Winemiller KO (eds) Food webs: integration of patterns and dynamics, 1st edn. Chapman & Hall, New York, pp 96–105Google Scholar
  53. Steinman AD (1996) Effects of grazers on freshwater benthic algae. In: Stevenson RJ, Bothwell ML, Lowe RL (eds) Algal ecology, 1st edn. Academic Press, San Diego, pp 341–373Google Scholar
  54. Sterner RW (1986) Herbivores' direct and indirect effects on algal populations. Science 231:605–607Google Scholar
  55. Taylor RC, Trexler JC, Loftus WF (2001) Separating the effects of intra- and interspecific age-structured interactions in an experimental fish assemblage. Oecologia 127:143–152CrossRefGoogle Scholar
  56. Trexler JC, Loftus WF, Jordan CF, Chick J, Kandl KL, McElroy TC, Bass OL (2001) Ecological scale and its implications for freshwater fishes in the Florida Everglades. In: Porter JW, Porter KG (eds) The Everglades, Florida Bay, and coral reefs of the Florida Keys: an ecosystem sourcebook, 1st edn. CRC, Boca Raton, pp 153–181Google Scholar
  57. Turner AM, Trexler JC, Jordan CF, Slack SJ, Geddes P, Chick JH, Loftus WF (1999) Targeting ecosystem features for conservation: Standing crops in the Florida Everglades. Conserv Biol 13:898–911CrossRefGoogle Scholar
  58. Van Meter-Kasanof N (1973) Ecology of the microalgae of the Florida Everglades. Part I. Environment and some aspects of freshwater periphyton. Nova Hedwigia 24:619–664Google Scholar
  59. Vanni MJ (1996) Nutrient transport and recycling by consumers in lake food webs: implications for algal communities. In: Polis GA, Winemiller KO (eds) Food webs: integration of patterns and dynamics, 1st edn. Chapman & Hall, New York, pp 81–95Google Scholar
  60. Vanni MJ, Findlay DL (1990) Trophic cascades and phytoplankton community structure. Ecology 71:921–937Google Scholar
  61. Vanni MJ, Layne CD (1997) Nutrient recycling and herbivory as mechanisms in the "top-down" effect of fish on algae in lakes. Ecology 78:21–40Google Scholar
  62. Wahl M, Hay ME (1995) Associational resistance and shared doom: effects of epibiosis on herbivory. Oecologia 102:329–340Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Department of Biological ScienceFlorida International UniversityMiamiUSA
  2. 2.Department of Ecology and EvolutionUniversity of ChicagoChicagoUSA

Personalised recommendations