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Succession in Stream Biofilms is an Environmentally Driven Gradient of Stress Tolerance

  • Microbiology of Aquatic Systems
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Abstract

The century-long research on succession has bestowed us with a number of theories, but little agreement on what causes species replacements through time. The majority of studies has explored the temporal trends of individual species in plant and much less so in microbial communities, arguing that interspecific interactions, especially competition, play a key role in community organization throughout succession. In this experimental investigation of periphytic succession in re-circulating laboratory streams, we examined the density and the relative abundance of diatoms and soft algae for 35 days across gradients of low to high nutrient supply (nitrogen + phosphorus) and low to intermediate current velocity (10 vs. 30 cm·s−1). All algal species were classified into trophic groups and morphological guilds, both of which responded more strongly to nutrient than current velocity manipulations, as shown by regression analyses. We concluded that within the manipulated environmental ranges: (1) Succession was a gradient of stress tolerance, driven primarily by nutrient supply and secondarily, by current velocity. Nutrient supply had a qualitative effect in determining whether the contribution of species tolerant vs. sensitive to nutrient limitation would increase through time, while current velocity had a quantitative influence and affected only the rate of this increase. (2) The mechanism of algal succession at a functional level was a neutral coexistence, whereby the tolerant low profile guild maintained high density when overgrown by sensitive species, while sensitive species, constituting mostly the motile and high profile guilds, were neither facilitated nor inhibited by tolerant species but controlled by the environment. It is suggested that the mechanism of succession may depend on the level of biological organization with interspecific interactions giving way to neutral coexistence along the hierarchy from species to functional groups. Considering that the functional makeup is strictly environmentally defined, while species composition reflects local and regional species pools that may exhibit substantial geographic variability, succession is deterministic at a functional level but stochastic at a species level.

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References

  1. Airoldi L (2000) Effects of disturbance, life histories, and overgrowth on coexistence of algal crusts and turfs. Ecology 81:798–814

    Article  Google Scholar 

  2. Biggs BJF, Goring DG, Nikora VI (1998) Subsidy and stress responses of stream periphyton to gradients in water velocity as a function of community growth form. J Phycol 34:598–607

    Article  Google Scholar 

  3. Biggs BJF, Hickey CW (1994) Periphyton responses to a hydraulic gradient in a regulated river in New Zealand. Freshw Biol 32:49–59

    Article  Google Scholar 

  4. Biggs BJF, Stevenson RJ, Lowe RL (1998) A habitat matrix conceptual model for stream periphyton. Arch Hydrobiol 143:21–56

    Google Scholar 

  5. Cermeño P, Falkowski PG (2009) Controls on diatom biogeography in the ocean. Science 325:1539–1541

    Article  PubMed  Google Scholar 

  6. Clements FE (1916) Plant succession. Carnegie Institute of Washington, Washington

    Google Scholar 

  7. Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1144

    Article  Google Scholar 

  8. DeNicola D, de Eyto E, Wemaere A, Irvine K (2006) Periphyton response to nutrient addition in 3 lakes of different benthic productivity. J N Am Benthol Soc 25:616–631

    Article  Google Scholar 

  9. Dodds WK, Smith VH, Lohman K (2002) Nitrogen and phosphorus relationships to benthic algal biomass in temperate streams. Can J Fish Aquat Sci 59:865–874

    Article  Google Scholar 

  10. Donar C, Stoermer EF, Brenner M (2009) The Holocene paleolimnology of Lake Apopka, Florida. Nova Hedwigia 135:57–70

    Google Scholar 

  11. Drury WH, Nisbet ICT (1973) Succession. J Arnold Arbor 54:331–368

    Google Scholar 

  12. Earl SR, Valett HM, Webster JR (2006) Nitrogen saturation in stream ecosystems. Ecology 87:3140–3151

    Article  PubMed  Google Scholar 

  13. Fisher SG (1990) Recovery process in lotic ecosystems: limits of successional theory. Environ Manage 14:725–736

    Article  Google Scholar 

  14. Gleason HA (1917) The structure and development of the plant association. Bull Torrey Bot Club 44:463–481

    Article  Google Scholar 

  15. Grimm NB (1994) Disturbance, succession and ecosystem processes in streams: a case study from the desert. In: Giller PS, Hildrew AG, Raffaelli DG (eds) Aquatic ecology: scale, pattern and process. Blackwell Science Ltd, London, pp 93–112

    Google Scholar 

  16. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chantey MH (eds) Culture of marine invertebrate animals. Plenum Publishers, New York, pp 29–60

    Google Scholar 

  17. Hill W (1996) Effects of light. In: Stevenson RJ, Bothwell ML, Lowe RL (eds) Algal ecology: freshwater benthic ecosystems. Academic, San Diego, pp 121–148

    Google Scholar 

  18. Hill WR, Fanta SE (2008) Phosphorus and light colimit periphyton growth at subsaturating irradiances. Freshw Biol 53:215–225

    CAS  Google Scholar 

  19. Hillebrand H, Gruner DS, Borer ET, Bracken MES, Cleland EE, Elser JJ, Harpole WS, Ngai JT, Seabloom EW, Shurin JB et al (2007) Consumer versus resource control of producer diversity depends on ecosystem type and producer community structure. Proc Natl Acad Sci USA 104:10904–10909

    Article  PubMed  CAS  Google Scholar 

  20. Hoagland KD, Roemer SC, Rosowski JR (1982) Colonization and community structure of two periphyton assemblages, with emphasis on the diatoms (Bacillariophyceae). Am J Bot 69:188–213

    Article  Google Scholar 

  21. Hondzo M, Wang H (2002) Effects of turbulence on growth and metabolism of periphyton in a laboratory flume. Water Resour Res 38:1277–1286

    Article  Google Scholar 

  22. Horner RR, Welch EB, Seeley MR, Jacoby JM (1990) Responses of periphyton to changes in current velocity, suspended sediment and phosphorus concentration. Freshw Biol 24:215–232

    Article  Google Scholar 

  23. Huston M, Smith T (1987) Plant succession: life history and competition. Am Nat 130:168–198

    Article  Google Scholar 

  24. Keithan ED, Lowe RL (1985) Primary productivity and spatial structure of phytolithic growth in streams in the Great Smoky Mountains National Park, Tennessee. Hydrobiologia 123:59–67

    Article  Google Scholar 

  25. McCormick PV, Stevenson RJ (1991) Mechanisms of benthic algal succession in lotic environments. Ecology 72:1835–1848

    Article  Google Scholar 

  26. Munk WH, Riley GA (1952) Absorption of nutrients by aquatic plants. J Mar Res 11:215–240

    Google Scholar 

  27. Odum EP (1969) Strategy of ecosystem development. Science 164:262–270

    Article  PubMed  CAS  Google Scholar 

  28. Passy SI (2001) Spatial paradigms of lotic diatom distribution: a landscape ecology perspective. J Phycol 37:370–378

    Article  Google Scholar 

  29. Passy SI (2007) Diatom ecological guilds display distinct and predictable behavior along nutrient and disturbance gradients in running waters. Aquat Bot 86:171–178

    Article  Google Scholar 

  30. Passy SI (2008) Continental diatom biodiversity in stream benthos declines as more nutrients become limiting. Proc Natl Acad Sci USA 105:9663–9667

    Article  PubMed  CAS  Google Scholar 

  31. Passy SI (2010) A distinct latitudinal gradient of diatom diversity is linked to resource supply. Ecology 91:36–41

    Article  PubMed  Google Scholar 

  32. Peterson CG, Grimm NB (1992) Temporal variation in enrichment effects during periphyton succession in a nitrogen-limited desert stream ecosystem. J N Am Benthol Soc 11:20–36

    Article  Google Scholar 

  33. Pickett STA, Cadenasso ML, Meiners SJ (2009) Ever since Clements: from succession to vegetation dynamics and understanding to intervention. Appl Veg Sci 12:9–21

    Article  Google Scholar 

  34. Pickett STA, Collins SL, Armesto JJ (1987) Models, mechanisms and pathways of succession. Bot Rev 53:335–371

    Article  Google Scholar 

  35. Pringle CM (1990) Nutrient spatial heterogeneity: effects on community structure, physiognomy, and diversity of stream algae. Ecology 71:905–920

    Article  Google Scholar 

  36. Rinke K, Robinson CT, Uehlinger U (2001) A note on abiotic factors that constrain periphyton growth in alpine glacier streams. Int Rev Hydrobiol 86:361–366

    Article  CAS  Google Scholar 

  37. Steinman AD, McIntire CD (1986) Effects of current velocity and light energy on the structure of periphyton assemblages in laboratory streams. J Phycol 22:352–361

    Article  Google Scholar 

  38. Stevenson RJ (1996) The stimulation and drag of current. In: Stevenson RJ, Bothwell ML, Lowe RL (eds) Algal ecology: freshwater benthic ecosystems. Academic, San Diego, pp 321–340

    Google Scholar 

  39. Stevenson RJ, Glover R (1993) Effects of algal density and current on ion transport through periphyton communities. Limnol Oceanogr 38:1276–1281

    CAS  Google Scholar 

  40. Tilman D (1985) The resource-ratio hypothesis of plant succession. Am Nat 125:827–852

    Article  Google Scholar 

  41. Van Hulst R (1979) On the dynamics of vegetation: Markov chains as models of succession. Vegetatio 40:3–14

    Article  Google Scholar 

  42. Walker LR, Chapin FS (1987) Interactions among processes controlling successional change. Oikos 50:131–135

    Article  Google Scholar 

  43. Whitford LA, Schumacher GJ (1961) Effect of current on mineral uptake and respiration by a freshwater alga. Limnol Oceanogr 6:423–425

    Article  Google Scholar 

  44. Yallop M, Hirst H, Kelly M, Juggins S, Jamieson J, Guthrie R (2009) Validation of ecological status concepts in UK rivers using historic diatom samples. Aquat Bot 90:289–295

    Article  Google Scholar 

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Acknowledgments

We gratefully acknowledge the financial support from UT Arlington Research Enhancement Grant No. 14-7487-30 and Norman Hackerman Advanced Research Program Grant No. 003656-0054-2009 to SP and Environmental Protection Agency GRO Fellowship for Graduate Environmental Study No. F6E61489 to CL. We thank an anonymous reviewer for the helpful suggestions that improved the clarity of the manuscript.

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  1. Department of Biology, University of Texas at Arlington, Box 19498, Arlington, TX, 76019-0498, USA

    Sophia I. Passy & Chad A. Larson

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  1. Sophia I. Passy
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  2. Chad A. Larson
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Correspondence to Sophia I. Passy.

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Passy, S.I., Larson, C.A. Succession in Stream Biofilms is an Environmentally Driven Gradient of Stress Tolerance. Microb Ecol 62, 414–424 (2011). https://doi.org/10.1007/s00248-011-9879-7

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