Skip to main content

Advertisement

Log in

The importance of nutrient supply by fish excretion and watershed streams to a eutrophic lake varies with temporal scale over 19 years

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

Animals transform and translocate nutrients at ecologically relevant rates, contributing to eutrophication in aquatic ecosystems by mobilizing otherwise unavailable nutrients. Yet we know little about how animal-mediated nutrient cycling compares with external abiotic nutrient sources over long periods (years–decades) and at multiple timescales. To address this, we conducted a 19-year study in a eutrophic reservoir examining nitrogen (N) and phosphorus (P) inputs from watershed streams versus excretion by an abundant fish (gizzard shad, Dorosoma cepedianum) at weekly, monthly and seasonal timescales. Over the entire time period, watershed N and P loading was 33- and 3-fold greater than fish N and P excretion, respectively. However, fish N excretion exceeded watershed nutrient loading in 36% of weeks and 43% of months, and fish P excretion in 68% of weeks and 58% of months during the growing season. Fish excretion had lower temporal variability in both supply rate and N:P ratio than watershed loading. Fish excretion also supplied nutrients at a much lower molar N:P ratio than the watershed (mean of daily N:P supply ratios were 15 and 723, respectively). In eutrophic lakes with high fish biomass, fish excretion can strongly influence algal biomass and community composition. Eutrophication management efforts should consider removal of benthivorous fish, like gizzard shad, in addition to other watershed management practices to improve water quality. Future climate change will modulate the interplay between fish- and watershed-mediated nutrient dynamics by altering the geographic distribution of detritivorous fish and the frequency and severity of storm and drought events.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Alberts EE, Schuman GE, Burwell RE (1978) Seasonal runoff losses of nitrogen and phosphorus from Missouri Valley Loess watersheds. J Environ Qual 7:203–208

    Article  Google Scholar 

  • Allgeier JE, Layman CA, Mumby PJ, Rosemond AD (2014) Consistent nutrient storage and supply mediated by diverse fish communities in coral reef ecosystems. Glob Change Biol 20:2459–2472

    Article  Google Scholar 

  • Arend, KK (2002) Do vertical gradients affect larval fish depth distribution and prey electivity among reservoirs that vary in productivity? MS Thesis, Ohio State University

  • Atkinson CL, Capps KA, Rugenski AT, Vanni MJ (2016) Consumer-driven nutrient dynamics in freshwater ecosystems: from individuals to ecosystems. Biol Rev 92:2003–2023

    Article  Google Scholar 

  • Auer NA (1982) Identification of larval fishes of the Great Lakes Basin with emphasis on the Lake Michigan Drainage. Great Lakes Fishery Commission 82-3

  • Bartoń K (2018) MuMIn: Multi-Model Inference. R Package version 1.40.4. https://CRAN.R-project.org/package=MuMIn

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects model using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Bayer JM, Counihan TD (2001) Length changes in white sturgeon larvae preserved in ethanol or formaldehyde. Collect Forum 15:57–64

    Google Scholar 

  • Brabrand Å, Faafeng BA, Nilssen JPM (1990) Relative importance of phosphorus supply to phytoplankton production: fish excretion verses external loading. Can J of Fish Aquat Sci 47:364–372

    Article  Google Scholar 

  • Bremigan MT, Stein RA (2001) Variable gizzard shad recruitment with reservoir productivity: causes and implications for classifying systems. Ecol Appl 11:1425–1437

    Article  Google Scholar 

  • Canty A, Ripley B (2016) boot: Bootstrap R (S-Plus) Functions. R package version 1.3-18

  • Carpenter SR, Armbrust EV, Arzberger PW, Chapin FS III, Elser JJ, Hackett EJ, Ives AR, Kareiva PM, Leibold MA, Lundberg P, Mangel M, Merchant N, Murdoch WW, Palmer MA, Peters DPC, Pickett STA, Smith KK, Wall DH, Zimmerman AS (2009) Accelerate synthesis in ecology and environmental sciences. Bioscience 59:699–701

    Article  Google Scholar 

  • Castaldi S (2000) Responses of nitrous oxide, dinitrogen and carbon dioxide production and oxygen consumption to temperature in forest and agricultural light-textured soils determined by model experiment. Biol Fertil of Soils 32:67–72

    Article  Google Scholar 

  • Catalano MJ, Allen MS, Schaus MH, Buck DG, Beaver JR (2010) Evaluating the short-term effects of omnivorous fish removal on water quality and zooplankton at a subtropical lake. Hydrobiologia 655:159–169

    Article  Google Scholar 

  • Chamberlain SA, Bronstein JL, Rudgers JA (2014) How context dependent are species interactions? Ecol Lett 14:881–890

    Article  Google Scholar 

  • Chapman DW (1966) Food and space as regulators of salmonid populations in streams. Am Nat 100:345–357

    Article  Google Scholar 

  • Davis TW, Berry DL, Boyer GL, Gobler CJ (2009) The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8:715–725

    Article  Google Scholar 

  • Dettmers JM, Stein RA (1992) Food consumption by larval gizzard shad: zooplankton effects and implication for reservoir communities. Trans Am Fish Soc 121:494–507

    Article  Google Scholar 

  • Devine JA, Vanni MJ (2002) Spatial and seasonal variation in nutrient excretion by benthic invertebrates in a eutrophic reservoir. Freshw Biol 47:1107–1121

    Article  Google Scholar 

  • DeVries DR, Frie RV (1996) Determination of age and growth. In: Murphy BR, Willis D (eds) Fisheries techniques, 2nd edn. American Fisheries Society, Bethesda, pp 483–512

    Google Scholar 

  • Domine LM, Vanni MJ, Renwick WH (2010) New and regenerated primary production in a productive reservoir ecosystem. Can J of Fish Aquat Sci 67:278–287

    Article  Google Scholar 

  • Dugdale RC, Goering JJ (1967) Uptake of new and regenerated forms of nitrogen in primary productivity. Limnol Oceanogr 12:196–206

    Article  Google Scholar 

  • El-Sabaawi RW, Bassar RD, Rakowski C, Marshall MC, Bryan BL, Thomas SN, Pringle C, Reznick DN, Flecker AS (2015) Intraspecific phenotypic differences in fish affect ecosystem processes as much as bottom-up factors. Oikos 124:1181–1191

    Article  Google Scholar 

  • Elser JJ, Urabe J (1999) The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80:735–751

    Article  Google Scholar 

  • Evens-White MA, Lamberti GA (2005) Grazer species effects on epilithon nutrient composition. Freshw Biol 50:1853–1863

    Article  Google Scholar 

  • Fetzer WW, Brooking TE, Jackson JR, Rudstam LG (2011) Overwinter mortality of gizzard shad: evaluation of starvation and cold temperature stress. Trans Am Fish Soc 140:1460–1471

    Article  Google Scholar 

  • Frost PC, Kinsman LE, Johnston CA, Larson JH (2009) Watershed discharge modulates relationships between landscape components and nutrient ratios in stream seston. Ecology 90:1631–1640

    Article  Google Scholar 

  • Godwin W, Coveney M, Lowe E, Battoe L (2011) Improvements in water quality following biomanipulation of gizzard shad (Dorosoma cepedianum) in Lake Denham, Florida. Lake Reserv Manag 24:287–297

    Article  Google Scholar 

  • Grover JP (1991) Resource competition in a variable environment: phytoplankton growing according to the variable-internal-stores model. Am Nat 138:811–835

    Article  Google Scholar 

  • Guildford SJ, Hecky RE (2000) Total nitrogen, total phosphorus, and nutrient limitation in lakes and oceans: is there common relationship? Limnol Oceanogr 45:1213–1223

    Article  Google Scholar 

  • Hale RS, Degan DJ, Renwick WH, Vanni MJ, Stein RA (2008) Assessing fish biomass and prey availability in Ohio reservoirs. Am Fish Soc Symp 62:517–541

    Google Scholar 

  • Harper JE (1971) Seasonal nutrient uptake and accumulation patterns in soybeans. Crop Sci 11:347–350

    Article  Google Scholar 

  • Hayes NM, Vanni MJ, Horgan MJ, Renwick WH (2015) Climate and land use interactively affect lake phytoplankton nutrient limitation status. Ecology 96:392–402

    Article  Google Scholar 

  • Higgins KA, Vanni MJ, González MJ (2006) Detritivory and the stoichiometry of nutrient cycling by a dominant fish species in lakes of varying productivity. Oikos 114:419–430

    Article  Google Scholar 

  • Huusko A, Hyvärinen P (2005) A high harvest rate induces a tendency to generation cycling in a freshwater fish population. J Anim Ecol 74:525–531

    Article  Google Scholar 

  • Jeppesen E, Søndergaard M, Peder Jensen J, Havens KE, Anneville O, Carvalho L, Coveney MF, Deneke R, Dokulil MT, Foy B, Gerdeaux D, Hampton SE, Hilt S, Kangur K, Köhler J, Lammens EHHR, Lauridsen TL, Manca M, Miracle MR, Moss B, Nõges P, Persson G, Phillips G, Portielje R, Romo S, Schelske CL, Straile D, Tatrai I, Willén E, Winder M (2005) Lake responses to reduced nutrient loading—an analysis of contemporary long-term data from 35 case studies. Freshw Biol 50:1747–1771

    Article  Google Scholar 

  • Kelly PT, González MJ, Renwick WH, Vanni MJ (2018a) Increased light availability and nutrient cycling by fish provide resilience against reversing eutrophication in an agriculturally impacted reservoir. Limnol Oceanogr 00:1–14

    Google Scholar 

  • Kelly PT, Vanni MJ, Renwick WH (2018b) Assessing uncertainty in annual nitrogen, phosphorus, and suspended sediment load estimates in three agricultural streams using a 21-year dataset. Environ Monit Assess 190:91

    Article  Google Scholar 

  • Kinter BT, Ludsin SA (2012) Nutrient inputs versus piscivore biomass as the primary driver of reservoir food webs. Can J Fish Aquat Sci 70:367–380

    Article  Google Scholar 

  • Knoll LB, Vanni MJ, Renwick WH, Dittman EK, Gelphart JA (2013) Temperate reservoirs are large carbon sinks and small CO2 sources: results from high-resolution carbon budgets. Glob Biogeochem Cycles 27:52–64

    Article  Google Scholar 

  • Knoll LB, Morgan A, Vanni MJ, Leach TH, Williamson TJ, Brentrup JA (2016) Quantifying pelagic phosphorus regeneration using three methods in lakes of varying productivity. Inland Waters 6:509–522

    Article  Google Scholar 

  • Kremer CT, Williams AK, Finiguerra M, Fong AA, Kellerman A, Paver SF, Tolar B, Toscano BJ (2017) Realizing the potential of trait-based aquatic ecology: new tools and collaborative approaches. Limnol Oceanogr 62:253–271

    Article  Google Scholar 

  • Kristoffersen JB, Gro Vea Salvanes A (1998) Effects of formaldehyde and ethanol preservative on body and otoliths of Maurolicus muelleri and Benthosema glaciale. Sarsia 83:95–102

    Article  Google Scholar 

  • Kunsch HR (1989) The jackknife and the bootstrap for general stationary observations. Ann Stat 17:1217–1241

    Article  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26

    Article  Google Scholar 

  • Lean DRS, Pick FR (1981) Photosynthetic response of lake plankton to nutrient enrichment: a test for nutrient limitation. Limnol Oceanogr 26:1001–1019

    Article  Google Scholar 

  • Leibold MA (1999) Biodiversity and nutrient enrichment in pond plankton communities. Evol Ecol Res 1:73–95

    Google Scholar 

  • Litchman E, Klausmeier CA, Schofield OM, Falkowski PG (2007) The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem levels. Ecol Lett 10:1170–1181

    Article  Google Scholar 

  • McCrackin ML, Jones HP, Jones PC, Moreno-Mateos D (2016) Recovery of lakes and coastal marine ecosystems from eutrophication: a global meta-analysis. Limnol Oceanogr 62:507–518

    Article  Google Scholar 

  • McIntyre PB, Flecker AS (2010) Ecological stoichiometry as an integrative framework in stream fish ecology. Am Fish Soc Symp 73:539–558

    Google Scholar 

  • 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 89:2335–2346

    Article  Google Scholar 

  • Michaletz PH (2010) Overwinter survival of age-0 gizzard shad in Missouri reservoirs spanning a productivity gradient: roles of body size and winter severity. Trans Am Fish Soc 139:241–256

    Article  Google Scholar 

  • Miller RR (1960) Systematics and biology of the gizzard shad (Dorosoma cepedianum) and related fishes. Fish Bull Fish Wildlife Serv 173:371–392

    Google Scholar 

  • Moody EK, Corman JR, Elser JJ, Sabo JL (2015) Diet composition affects the rate of N: P ratio of fish excretion. Freshw Biol 60:456–465

    Article  Google Scholar 

  • Mulholland PJ, Hill WR (1997) Seasonal patterns in streamwater nutrient and dissolved organic carbon concentrations: separating catchment flow path and instream effects. Water Resour Res 33:1297–1306

    Article  Google Scholar 

  • Ottersen G, Loeng H (2000) Covariabililty in early growth and year-class strength of Barents Sea cod, haddock, and herring: the environmental link. J Mar Sci 57:339–348

    Google Scholar 

  • Pastor J, Dewey B, Naiman RJ, McInnes PF, Cohen Y (1993) Moose browsing and soil fertility in the boreal forests of Isle Royal National Park. Ecology 74:467–480

    Article  Google Scholar 

  • Peel MC, McMahon TA, Finlayson BL, Watson FGR (2002) Implications of the relationship between vegetation type and the variability of annual runoff. Hydrol Process 16:2995–3002

    Article  Google Scholar 

  • Piehler MF, Twomey LJ, Hall NS, Paerl HW (2004) Impacts of inorganic nutrient enrichment on phytoplankton community structure and function in Pamlico Sound, NC, USA. Estuar Coast Shelf Sci 64:197–209

    Article  Google Scholar 

  • Pilati A, Vanni MJ (2007) Ontogeny, diet shifts, and nutrient stoichiometry in fish. Okios 116:1663–1674

    Article  Google Scholar 

  • Pionke HB, Gburek WJ, Schnabel RR, Sharpley AN, Elwinger GF (1999) Seasonal flow, nutrient concentration and loading patterns in stream flow draining an agricultural hill-land watershed. J Hydrol 220:62–73

    Article  Google Scholar 

  • Ptacnik R, Andersen T, Tamminen T (2010) Performance of the Redfield Ratio and a family of nutrient limitation indicators as thresholds for phytoplankton N vs P limitation. Ecosystems 13:1201–1214

    Article  Google Scholar 

  • R Core Team 2016. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  • Redfield AC (1958) The biological control of chemical factors in the environment. Am Nat 46:205–221

    Google Scholar 

  • Renwick WH, Vanni MJ, Zhang Q, Patton J (2008) Water quality trends and changing agricultural practices in a Midwest U.S. watershed 1994–2006. J Environ Qual 37:1862–1874

    Article  Google Scholar 

  • Richards RP, Baker DB, Crumrine JP (2009) Improved water quality in Ohio tributaries to Lake Erie: a consequence of conservation practices. J Soil Water Conserv 64:200–211

    Article  Google Scholar 

  • Sabo JL, Post DM (2008) Quantifying periodic, stochastic, and catastrophic environmental variation. Ecol Monogr 78:19–40

    Article  Google Scholar 

  • Sadro SS, Melack JM (2012) The effect of an extreme rain event on the biogeochemistry and ecosystem metabolism of an oligotrophic high-elevation lake. Arct Antarct Alp Res 44:222–231

    Article  Google Scholar 

  • Salvatore SR, Mundahl ND, Wissing TE (1987) Effect of water temperature on food evacuation rate and feeding activity of age-0 gizzard shad. Trans Am Fish Soc 116:67–70

    Article  Google Scholar 

  • Schaus MH, Vanni MJ, Wissing TE, Bremigan MT, Garvey JE, Stein RA (1997) Nitrogen and phosphorus excretion by detritivorous gizzard shad in a reservoir ecosystem. Limnol Oceanogr 42:1386–1397

    Article  Google Scholar 

  • Schaus MH, Godwin W, Battoe L, Coveney M, Lowe E, Roth R, Hawkins C, Vindigni M, Weinberg C, Zimmerman A (2010) Impact of the removal of gizzard shad (Dorosoma cepedianum) on nutrient cycles in Lake Apopka, Florida. Freshw Biol 55:2401–2413

    Article  Google Scholar 

  • Schindler DE, Kitchell JF, He X, Carpenter SR, Hodgson JR, Cottingham KL (1993) Food web structure and phosphorus cycling in lakes. Trans Am Fish Soc 122:756–772

    Article  Google Scholar 

  • Sharpley AN, Kleinman PJA, Heathwaite AL, Gburek WJ, Folmar GJ, Schmidt JP (2008) Phosphorus loss from an agricultural watershed as a function of storm size. J Environ Qual 37:362–368

    Article  Google Scholar 

  • Shostell J, Bukaveckas PA (2004) Seasonal and interannual variation in nutrient fluxes from tributary inputs, consumer recycling and algal growth in a eutrophic river impoundment. Aquat Ecol 38:359–373

    Article  Google Scholar 

  • Sitters J, Atkinson CL, Guelzow N, Kelly P, Sullivan LL (2015) Spatial stoichiometry: cross-ecosystem material flows and their impacts on recipient ecosystems and organisms. Oikos 124:920–930

    Article  Google Scholar 

  • Sommer U (1984) The paradox of the plankton: fluctuations of phosphorus availability maintain diversity of phytoplankton in flow-through cultures. Limnol Oceanogr 29:633–636

    Article  Google Scholar 

  • Spiess A-N (2017) propagate: Propagation of Uncertainty. R package version 1.0-5. https://CRAN.R-project.org/package=propagate

  • Stein RA, DeVries DR, Dettmers JM (1995) Food-web regulation by a planktivore: exploring the generality of the trophic cascade hypothesis. Can J Fish Aquat Sci 52:2518–2526

    Article  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from the molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Suttle CA, Stockner JG, Harrison PJ (1987) Effects of nutrient pulses on community structure and cell size of a freshwater phytoplankton assemblage in culture. Can J of Fish Aquat Sci 44:1768–1774

    Article  Google Scholar 

  • Taylor JM, Vanni MJ, Flecker AS (2015) Top-down and bottom-up interactions in freshwater ecosystems: emerging complexities. In: Hanley TC, La Pierre KJ (eds) Trophic ecology: bottom-up and top-down interactions across aquatic and terrestrial systems. Cambridge University Press, Cambridge, pp 55–85

    Chapter  Google Scholar 

  • Tronstad LM, Hall RO Jr, Koel TM (2015) Introduced lake trout alter nitrogen cycling beyond Yellowstone Lake. Ecosphere 6:1–24

    Article  Google Scholar 

  • Vanni MJ (2002) Nutrient cycling by animals in freshwater ecosystems. Annu Rev Ecol Syst 33:341–370

    Article  Google Scholar 

  • Vanni MJ, McIntyre PB (2016) Predicting nutrient excretion of aquatic animals with metabolic ecology and ecological stoichiometry: a global synthesis. Ecology 97:3460–3471

    Article  Google Scholar 

  • Vanni MJ, Renwick WH, Headworth JF, Auch JD, Schaus MH (2001) Dissolved and particulate nutrient flux from three adjacent agricultural watersheds: a five-year study. Biogeochemistry 54:85–114

    Article  Google Scholar 

  • Vanni MJ, Arend KK, Bremigan MT, Bunnell DB, Garvey JE, González MJ, Renwick WH, Soranno PA, Stein RA (2005) Linking landscapes and food webs: effects of omnivorous fish and watershed on reservoir ecosystems. Bioscience 55:155–167

    Article  Google Scholar 

  • Vanni MJ, Andrews JS, Renwick WH, González MJ, Nobel SJ (2006a) Nutrient and light limitation of reservoir phytoplankton in relation to storm-mediated pulses in stream discharge. Arch Hydrobiol 167:421–445

    Article  Google Scholar 

  • Vanni MJ, Bowling AM, Dickman EM, Hale RS, Higgens KA, Horgan MJ, Knoll LB, Renwick WH, Stein RA (2006b) Nutrient cycling by fish supports relatively more primary production as lake productivity increases. Ecology 87:1696–1709

    Article  Google Scholar 

  • Vanni MJ, Renwick WH, Bowling AM, Horgan MJ, Christian AD (2011) Nutrient stoichiometry of linked catchment-lake systems along a gradient of land use. Freshw Biol 56:791–811

    Article  Google Scholar 

  • Vanni MJ, Boros G, McIntyre PB (2013) When are fish sources vs. sinks of nutrients in lake ecosystems? Ecology 94:2195–2206

    Article  Google Scholar 

  • Weathers KC, Groffman PM, Dolah EV, Bernhardt E, Grimm NB, McMahon K, Schimel J, Paolisso M, Maranger R, Baer S, Brauman K, Hinckley E (2016) Frontiers in ecosystem ecology from a community perspective: the future is boundless and bright. Ecosystems 19:753–770

    Article  Google Scholar 

Download references

Acknowledgements

This research was supported mainly by National Science Foundation awards 9318452, 9726877, 0235755, 0743192, and 1255159, and the Federal Aid in Sport Fish Restoration Program (F-69-P, Fish Management in Ohio) administered jointly by the U.S. Fish and Wildlife Service and the Ohio Department of Natural Resources-Division of Wildlife. We also thank Hueston Woods State Park staff for their cooperation throughout the study. We thank P. Kelly and A. Rock for their insightful feedback on earlier drafts of this manuscript. We are especially indebted to Miami University students and staff, especially A. Bowling, P. Levi, J. Headworth, B. Mette, J. Duncan and T. Ratliff, for assistance with field and lab work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tanner J. Williamson.

Additional information

Responsible Editor: R. Kelman Wieder.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 8685 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Williamson, T.J., Vanni, M.J., González, M.J. et al. The importance of nutrient supply by fish excretion and watershed streams to a eutrophic lake varies with temporal scale over 19 years. Biogeochemistry 140, 233–253 (2018). https://doi.org/10.1007/s10533-018-0490-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-018-0490-6

Keywords

Navigation