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Spatial Variability in Light Yields Colimitation of Primary Production by Both Light and Nutrients in a Forested Stream Ecosystem

Abstract

Colimitation of primary production is increasingly recognized as a dominant process across aquatic and terrestrial ecosystems. In streams, both nutrient availability and light availability have been shown to independently limit primary production, but colimitation by both light and nutrients is rarely considered. We used a series of nutrient-diffusing substrates (NDS) bioassays deployed across a range of light availability conditions in a single-study stream over two summers to determine the light level at which the limiting factor for benthic periphyton accrual transitioned from light to nutrients. Stream periphyton accrual was nutrient-limited in high-light patches, and light-limited in low-light patches, with the transition from being predominantly light-limited to being predominantly nutrient-limited occurring when daily light fluxes exceeded 3.5 mol m−2 day−1. We quantified light at each NDS bioassay location and at 5 m intervals throughout our two adjacent 160 m study reaches—one in structurally complex old-growth riparian forest and one bordered by more uniform second-growth forest. Although both reaches were colimited overall, the resource (light or nutrients) dominating limitation differed between the two riparian forest age/structure conditions. In the old-growth section, about three quarters of the reach was predominantly nutrient-limited, whereas in the second-growth reach only about a quarter of the streambed was nutrient-limited. In this stream, colimitation of benthic periphyton accrual by light and nutrients at the reach scale was an emergent property of the ecosystem that manifested as a result of high heterogeneity in riparian forest structure.

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References

  • Ambrose HE, Wilzbach MA, Cummins KW. 2004. Periphyton response to increased light and salmon carcass introduction in northern California streams. J N Am Benthol Soc 23:701–12.

    Article  Google Scholar 

  • Bechtold HA, Marcarelli AM, Baxter CV, Inouye RS. 2012. Effects of N, P, and organic carbon on stream biofilm nutrient limitation and uptake in a semi-arid watershed. Limnol Oceanogr 57:1544–54.

    CAS  Article  Google Scholar 

  • Bernhardt ES, Likens GE. 2004. Controls on periphyton biomass in heterotrophic streams. Freshw Biol 49:14–27.

    Article  Google Scholar 

  • Bernhardt ES, Likens GE, Driscoll CT, Buso DC. 2003. In-stream uptake dampens effects of major forest disturbance on watershed nitrogen export. Proc Natl Acad Sci USA 100:10304–8.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Bernot MJ, Sobota DJ, Hall RO, Mulholland PJ, Dodds WK, Webster JR, Tank JL, Ashkenas LR, Cooper LW, Dahm CN, Gregory SV, Grimm NB, Hamilton SK, Johnson SL, Mcdowell WH, Meyer JL, Peterson B, Poole GC, Valett HM, Arango C, Beaulieu JJ, Burgin AJ, Crenshaw C, Helton AM, Johnson L, Merriam J, Niederlehner BR, O’Brien JM, Potter JD, Sheibley RW, Thomas SM, Wilson K. 2010. Inter-regional comparison of land-use effects on stream metabolism. Freshw Biol 55:1874–90.

    Article  Google Scholar 

  • Bilby RE, Bisson PA. 1992. Allochthonous versus autochthonous organic-matter contributions to the trophic support of fish populations in clear-cut and old-growth forested streams. Can J Fish Aquat Sci 49:540–51.

    Article  Google Scholar 

  • Bothwell ML. 1985. Phosphorus limitation of lotic periphyton growth-rates—an intersite comparison using continuous-flow troughs (Thompson River System, British-Columbia). Limnol Oceanogr 30:527–42.

    Article  Google Scholar 

  • Bothwell ML. 1989. Phosphorous limited growth dynamics of lotic periphytic diatom communities—areal biomass and cellular growth-rate responses. Can J Fish Aquat Sci 46:1293–301.

    Article  Google Scholar 

  • Capps KA, Booth MT, Collins SM, Davison MA, Moslemi JM, El-Sabaawi RW, Simonis JL, Flecker AS. 2011. Nutrient diffusing substrata: a field comparison of commonly used methods to assess nutrient limitation. J N Am Benthol Soc 30:522–32.

    Article  Google Scholar 

  • Carey RO, Vellidis G, Lowrance R, Pringle CM. 2007. Do nutrients limit algal periphyton in small blackwater coastal plain streams? J Am Water Resour Assoc 43:1183–93.

    CAS  Article  Google Scholar 

  • Collins SM, Sparks JP, Thomas SA, Wheatley SA, Flecker AS. 2016. Increased light availability reduces the importance of bacterial carbon in headwater stream food webs. Ecosystems 19(3):396–410.

    CAS  Article  Google Scholar 

  • Cross WF, Benstead JP, Frost PC, Thomas SA. 2005. Ecological stoichiometry in freshwater benthic systems: recent progress and perspectives. Freshw Biol 50:1895–912.

    CAS  Article  Google Scholar 

  • Curzon MT, Keeton WS. 2010. Spatial characteristics of canopy disturbances in riparian old-growth hemlock—northern hardwood forests, Adirondack Mountains, New York, USA. Can J For Res-Revue Canadienne De Recherche Forestiere 40:13–25.

    Article  Google Scholar 

  • D’Amato AW, Orwig DA, Foster DR. 2009. Understory vegetation in old-growth and second-growth Tsuga canadensis forests in western Massachusetts. For Ecol Manage 257:1043–52.

    Article  Google Scholar 

  • Danger M, Daufresne T, Lucas F, Pissard S, Lacroix G. 2008. Does Liebig’s law of the minimum scale up from species to communities? Oikos 117:1741–51.

    Article  Google Scholar 

  • Delong MD, Thorp JH. 2006. Significance of instream autotrophs in trophic dynamics of the Upper Mississippi River. Oecologia 147:76–85.

    Article  PubMed  Google Scholar 

  • Denicola DM, Hoagland KD, Roemer SC. 1992. Influences of canopy cover on spectral irradiance and periphyton assemblages in a prairie stream. J N Am Benthol Soc 11:391–404.

    Article  Google Scholar 

  • Elsaholi M, Hannigan E, Kelly-Quinn M. 2011. Nutrient and light limitation of periphyton in selected streams in Ireland. Inland Waters 1:74–80.

    Article  Google Scholar 

  • Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–42.

    Article  PubMed  Google Scholar 

  • Fay PA, Prober SM, Harpole WS, Knops JMH, Bakker JD, Borer ET, Lind EM, MacDougall AS, Seabloom EW, Wragg PD, Adler PB, Blumenthal DM, Buckley Y, Chu CJ, Cleland EE, Collins SL, Davies KF, Du GZ, Feng XH, Firn J, Gruner DS, Hagenah N, Hautier Y, Heckman RW, Jin VL, Kirkman KP, Klein J, Ladwig LM, Li Q, McCulley RL, Melbourne BA, Mitchell CE, Moore JL, Morgan JW, Risch AC, Schutz M, Stevens CJ, Wedin DA, Yang LH. 2015. Grassland productivity limited by multiple nutrients. Nat Plants 1:15080. doi:10.1038/nplants.2015.80.

  • Finlay JC, Hood JM, Limm MP, Power ME, Schade JD, Welter JR. 2011. Light-mediated thresholds in stream-water nutrient composition in a river network. Ecology 92:140–50.

    Article  PubMed  Google Scholar 

  • Fisher SG, Gray LJ, Grimm NB, Busch DE. 1982. Temporal succession in a desert stream ecosystem following flash flooding. Ecol Monogr 52:93–110.

    CAS  Article  Google Scholar 

  • Flecker AS, Townsend CR. 1994. Community-wide consequences of trout introduction in new-zealand streams. Ecol Appl 4:798–807.

    Article  Google Scholar 

  • Foster DR, Motzkin G, Slater B. 1998. Land-use history as long-term broad-scale disturbance: regional forest dynamics in central New England. Ecosystems 1:96–119.

    Article  Google Scholar 

  • Franklin JF, Spies TA, Van Pelt R, Carey AB, Thornburgh DA, Berg DR, Lindenmayer DB, Harmon ME, Keeton WS, Shaw DC, Bible K, Chen JQ. 2002. Disturbances and structural development of natural forest ecosystems with silvicultural implications, using Douglas-fir forests as an example. For Ecol Manag 155:399–423.

    Article  Google Scholar 

  • Goodale CL, Aber JD, McDowell WH. 2000. The long-term effects of disturbance on organic and inorganic nitrogen export in the White Mountains, New Hampshire. Ecosystems 3:433–50.

    Article  Google Scholar 

  • Greene S, Taylor D, McElarney YR, Foy RH, Jordan P. 2011. An evaluation of catchment-scale phosphorus mitigation using load apportionment modelling. Sci Total Environ 409:2211–21.

    CAS  Article  PubMed  Google Scholar 

  • Greenwood JL, Rosemond AD. 2005. Periphyton response to long-term nutrient enrichment in a shaded headwater stream. Can J Fish Aquat Sci 62:2033–45.

    CAS  Article  Google Scholar 

  • Grimm NB, Chapin FS, Bierwagen B, Gonzalez P, Groffman PM, Luo YQ, Melton F, Nadelhoffer K, Pairis A, Raymond PA, Schimel J, Williamson CE. 2013. The impacts of climate change on ecosystem structure and function. Front Ecol Environ 11:474–82.

    Article  Google Scholar 

  • Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE. 2011. Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–62.

    Article  PubMed  Google Scholar 

  • Hill WR, Fanta SE. 2008. Phosphorus and light colimit periphyton growth at subsaturating irradiances. Freshw Biol 53:215–25.

    CAS  Google Scholar 

  • Hill WR, Fanta SE, Roberts BJ. 2009. Quantifying phosphorus and light effects in stream algae. Limnol Oceanogr 54:368–80.

    CAS  Article  Google Scholar 

  • Hill WR, Roberts BJ, Francoeur SN, Fanta SE. 2011. Resource synergy in stream periphyton communities. J Ecol 99:454–63.

    Google Scholar 

  • Hill WR, Ryon MG, Schilling EM. 1995. Light limitation in a stream ecosystem—responses by primary producers and consumers. Ecology 76:1297–309.

    Article  Google Scholar 

  • Johnson LT, Tank JL, Dodds WK. 2009. The influence of land use on stream biofilm nutrient limitation across eight North American ecoregions. Can J Fish Aquat Sci 66:1081–94.

    CAS  Article  Google Scholar 

  • Julian JP, Seegert SZ, Powers SM, Stanley EH, Doyle MW. 2011. Light as a first-order control on ecosystem structure in a temperate stream. Ecohydrology 4:422–32.

    Article  Google Scholar 

  • Keck F, Lepori F. 2012. Can we predict nutrient limitation in streams and rivers? Freshw Biol 57:1410–21.

    CAS  Article  Google Scholar 

  • Keeton WS, Kraft CE, Warren DR. 2007. Mature and old-growth riparian forests: structure, dynamics, and effects on adirondack stream habitats. Ecol Appl 17:852–68.

    Article  PubMed  Google Scholar 

  • Kiffney PM. 2008. Response of lotic producer and consumer trophic levels to gradients of resource supply and predation pressure. Oikos 117:1428–40.

    Article  Google Scholar 

  • Larned ST. 2010. A prospectus for periphyton: recent and future ecological research. J N Am Benthol Soc 29:182–206.

    Article  Google Scholar 

  • Lau DCP, Leung KMY, Dudgeon D. 2009a. Are autochthonous foods more important than allochthonous resources to benthic consumers in tropical headwater streams? J N Am Benthol Soc 28:426–39.

    Article  Google Scholar 

  • Lau DCP, Leung KMY, Dudgeon D. 2009b. What does stable isotope analysis reveal about trophic relationships and the relative importance of allochthonous and autochthonous resources in tropical streams? A synthetic study from Hong Kong. Freshw Biol 54:127–41.

    CAS  Article  Google Scholar 

  • Marcarelli AM, Wurtsbaugh WA. 2007. Effects of upstream lakes and nutrient limitation on periphytic biomass and nitrogen fixation in oligotrophic, subalpine streams. Freshw Biol 52:2211–25.

    CAS  Article  Google Scholar 

  • Matheson FE, Quinn JM, Martin ML. 2012. Effects of irradiance on diel and seasonal patterns of nutrient uptake by stream periphyton. Freshw Biol 57:1617–30.

    CAS  Article  Google Scholar 

  • McClain ME, Boyer EW, Dent CL, Gergel SE, Grimm NB, Groffman PM, Hart SC, Harvey JW, Johnston CA, Mayorga E, McDowell WH, Pinay G. 2003. Biogeochemical hot spots and hot moments at the interface of terrestrial and aquatic ecosystems. Ecosystems 6:301–12.

    CAS  Article  Google Scholar 

  • McCutchan JH, Lewis WM. 2002. Relative importance of carbon sources for macroinvertebrates in a Rocky Mountain stream. Limnol Oceanogr 47:742–52.

    Article  Google Scholar 

  • Mosisch TD, Bunn SE, Davies PM, Marshall CJ. 1999. Effects of shade and nutrient manipulation on periphyton growth in a subtropical stream. Aquat Bot 64:167–77.

    Article  Google Scholar 

  • Moslemi JM, Snider SB, MacNeill K, Gilliam JF, Flecker AS. 2012. Impacts of an invasive snail (Tarebia granifera) on nutrient cycling in tropical streams: the role of riparian deforestation in Trinidad, West Indies. PloS One 7:e38806.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Noel DS, Martin CW, Federer CA. 1986. Effects of forest clearcutting in New England, USA on stream macroinvertebrates and periphyton. Environ Manag 10:661–70.

    Article  Google Scholar 

  • Pan Y, Chen JM, Birdsey R, McCullough K, He L, Deng F. 2011. Age structure and disturbance legacy of North American forests. Biogeosciences 8:715–32.

    Article  Google Scholar 

  • Peterson BJ, Wollheim WM, Mulholland PJ, Webster JR, Meyer JL, Tank JL, Marti E, Bowden WB, Valett HM, Hershey AE, McDowell WH, Dodds WK, Hamilton SK, Gregory S, Morrall DD. 2001. Control of nitrogen export from watersheds by headwater streams. Science 292:86–90.

    CAS  Article  PubMed  Google Scholar 

  • R Core Team. 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.

  • Renwick WH, Vanni MJ, Zhang Q, Patton J. 2008. Water quality trends and changing agricultural practices in a Midwest US watershed, 1994–2006. J Environ Qual 37:1862–74.

    CAS  Article  PubMed  Google Scholar 

  • Rier ST, Shirvinski JM, Kinek KC. 2014. In situ light and phosphorus manipulations reveal potential role of biofilm algae in enhancing enzyme-mediated decomposition of organic matter in streams. Freshw Biol 59:1039–51.

    CAS  Article  Google Scholar 

  • Roberts BJ, Mulholland PJ. 2007. In-stream biotic control on nutrient biogeochemistry in a forested stream, West Fork of Walker Branch. J Geophys Res 112:G04002. doi:10.1029/2007JG000422.

  • Rosemond AD. 1993. Interactions among irradiance, nutrients, and herbivores constrain a stream algal community. Oecologia 94:585–94.

    Article  Google Scholar 

  • Rosemond AD, Benstead JP, Bumpers PM, Gulis V, Kominoski JS, Manning DWP, Suberkropp K, Wallace JB. 2015. Experimental nutrient additions accelerate terrestrial carbon loss from stream ecosystems. Science 347:1142–5.

    CAS  Article  PubMed  Google Scholar 

  • Rosemond AD, Mulholland PJ, Brawley SH. 2000. Seasonally shifting limitation of stream periphyton: response of algal populations and assemblage biomass and productivity to variation in light, nutrients, and herbivores. Can J Fish Aquat Sci 57:66–75.

    Article  Google Scholar 

  • Sabater F, Butturini A, Marti E, Munoz I, Romani A, Wray J, Sabater S. 2000. Effects of riparian vegetation removal on nutrient retention in a Mediterranean stream. J N Am Benthol Soc 19:609–20.

    Article  Google Scholar 

  • Sanderson BL, Coe HJ, Tran CD, Macneale KH, Harstad DL, Goodwin AB. 2009. Nutrient limitation of periphyton in Idaho streams: results from nutrient diffusing substrate experiments. J N Am Benthol Soc 28:832–45.

    Article  Google Scholar 

  • Sperfeld E, Martin-Creuzburg D, Wacker A. 2012. Multiple resource limitation theory applied to herbivorous consumers: Liebig’s minimum rule vs. interactive co-limitation. Ecol Lett 15:142–50.

    Article  PubMed  Google Scholar 

  • Stelzer RS, Lamberti GA. 2001. Effects of N: P ratio and total nutrient concentration on stream periphyton community structure, biomass, and elemental composition. Limnol Oceanogr 46:356–67.

    Article  Google Scholar 

  • Stone MK, Wallace JB. 1998. Long-term recovery of a mountain stream from clearcut logging: the effects of forest succession on benthic invertebrate community structure. Freshw Biol 39:151–69.

    Article  Google Scholar 

  • Stovall JP, Keeton WS, Kraft CE. 2009. Late-successional riparian forest structure results in heterogeneous periphyton distributions in low-order streams. Can J For Res-Revue Canadienne De Recherche Forestiere 39:2343–54.

    Article  Google Scholar 

  • Tank JL, Bernot MJ, Rosi-Marshall EJ. 2007. Nitrogen limitation and uptake. In: Hauer FR, Lamberti GA, Eds. Methods in stream ecology. 2nd edn. Burlington: Elsevier.

    Google Scholar 

  • Tank JL, Dodds WK. 2003. Nutrient limitation of epilithic and epixylic biofilms in ten North American streams. Freshw Biol 48:1031–49.

    CAS  Article  Google Scholar 

  • Thorp JH, Delong AD. 2002. Dominance of autochthonous autotrophic carbon in food webs of heterotrophic rivers. Oikos 96:543–50.

    Article  Google Scholar 

  • Townsend CR, Doledec S, Scarsbrook MR. 1997. Species traits in relation to temporal and spatial heterogeneity in streams: a test of habitat templet theory. Freshw Biol 37:367–87.

    Article  Google Scholar 

  • Valett HM, Crenshaw CL, Wagner PF. 2002. Stream nutrient uptake, forest succession, and biogeochemical theory. Ecology 83:2888–901.

    Article  Google Scholar 

  • Van Pelt R, Franklin JF. 2000. Influence of canopy structure on the understory environment in tall, old-growth, conifer forests. Can J For Res-Revue Canadienne De Recherche Forestiere 30:1231–45.

    Article  Google Scholar 

  • Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman D. 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–50.

    Google Scholar 

  • Vitousek PM, Reiners WA. 1975. Ecosystem succession and nutrient retention—hypothesis. Bioscience 25:376–81.

    CAS  Article  Google Scholar 

  • Von Schiller D, Marti E, Riera JL, Sabater F. 2007. Effects of nutrients and light on periphyton biomass and nitrogen uptake in Mediterranean streams with contrasting land uses. Freshw Biol 52:891–906.

    Article  Google Scholar 

  • Warren DR, Bernhardt ES, Hall ROJ, Likens GE. 2007. Forest age, wood, and nutrient dynamics in headwater streams of the Hubbard Brook Experimental Forest, NH. Earth Surf Proc Land 32:1154–63.

    CAS  Article  Google Scholar 

  • Warren DR, Keeton WS, Bechtold HA, Rosi-Marshall EJ. 2013. Comparing streambed light availability and canopy cover in streams with old-growth versus early-mature riparian forests in western Oregon. Aquat Sci 75:547–58.

    Article  Google Scholar 

  • Winemiller KO, Flecker AS, Hoeinghaus DJ. 2010. Patch dynamics and environmental heterogeneity in lotic ecosystems. J N Am Benthol Soc 29:84–99.

    Article  Google Scholar 

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Acknowledgements

We thank Brian VerWey, Emily Heaston, Katherine Pospisil, and Chris Kopet for help in the field and in the lab. We thank Brian VerWey and Lindsey Thurman for feedback on early drafts of the manuscript. Summer 2015 fieldwork was supported by NSF DEB 1547628 awarded to DRW. SMC was supported by an NSF Postdoctoral Research Fellowship in Biology (DBI 1401954). Funding for author EMP was provided through the HJ Andrews Research Experience for Undergraduates (REU) program, and facilities were provided by the HJ Andrews Experimental Forest research program—both funded by the National Science Foundation’s Long-Term Ecological Research Program (DEB 1440409), US Forest Service Pacific Northwest Research Station, and Oregon State University.

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Correspondence to Dana R. Warren.

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DR Warren contributed to initial study idea, contributed to fieldwork, and wrote the majority of the paper. SM Collins contributed to writing, to framing of ideas and to study design, and conducted loess analysis. EM Purvis performed research in the first year of the study (2014) and provided significant input on study design and implementation. MJ Kaylor contributed to initial study idea, contributed to fieldwork in year one (2014), performed research in year two (2015), and edited the paper. HA Bechtold contributed to initial study idea, helped design the study, and edited the paper.

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Warren, D.R., Collins, S.M., Purvis, E.M. et al. Spatial Variability in Light Yields Colimitation of Primary Production by Both Light and Nutrients in a Forested Stream Ecosystem. Ecosystems 20, 198–210 (2017). https://doi.org/10.1007/s10021-016-0024-9

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Keywords

  • nutrient-diffusing substrate
  • nitrogen limitation
  • light limitation
  • colimitation
  • benthic primary production
  • HJ Andrews
  • riparian forest
  • stream light
  • habitat heterogeneity