Temporal variation in the importance of a dominant consumer to stream nutrient cycling
Abstract
Animal excretion can be a significant nutrient flux within ecosystems, where it supports primary production and facilitates microbial decomposition of organic matter. The effects of excretory products on nutrient cycling have been documented for various species and ecosystems, but temporal variation in these processes is poorly understood. We examined variation in excretion rates of a dominant grazing snail, Elimia clavaeformis, and its contribution to nutrient cycling, over the course of 14 months in a well-studied, low-nutrient stream (Walker Branch, east Tennessee, USA). Biomass-specific excretion rates of ammonium varied over twofold during the study, coinciding with seasonal changes in food availability (measured as gross primary production) and water temperature (multiple linear regression, R2 = 0.57, P = 0.053). The contribution of ammonium excretion to nutrient cycling varied with seasonal changes in both biological (that is, nutrient uptake rate) and physical (that is, stream flow) variables. On average, ammonium excretion accounted for 58% of stream water ammonium concentrations, 26% of whole-stream nitrogen demand, and 66% of autotrophic nitrogen uptake. Phosphorus excretion by Elimia was contrastingly low throughout the year, supplying only 1% of total dissolved phosphorus concentrations. The high average N:P ratio (89:1) of snail excretion likely exacerbated phosphorus limitation in Walkermore »
- Authors:
-
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Univ. of Illinois at Urbana-Champaign, IL (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge National Environmental Research Park
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1159990
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Ecosystems
- Additional Journal Information:
- Journal Volume: 17; Journal Issue: 7; Journal ID: ISSN 1432-9840
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES
Citation Formats
Griffiths, Natalie A., and Hill, Walter. Temporal variation in the importance of a dominant consumer to stream nutrient cycling. United States: N. p., 2014.
Web. doi:10.1007/s10021-014-9785-1.
Griffiths, Natalie A., & Hill, Walter. Temporal variation in the importance of a dominant consumer to stream nutrient cycling. United States. https://doi.org/10.1007/s10021-014-9785-1
Griffiths, Natalie A., and Hill, Walter. Thu .
"Temporal variation in the importance of a dominant consumer to stream nutrient cycling". United States. https://doi.org/10.1007/s10021-014-9785-1. https://www.osti.gov/servlets/purl/1159990.
@article{osti_1159990,
title = {Temporal variation in the importance of a dominant consumer to stream nutrient cycling},
author = {Griffiths, Natalie A. and Hill, Walter},
abstractNote = {Animal excretion can be a significant nutrient flux within ecosystems, where it supports primary production and facilitates microbial decomposition of organic matter. The effects of excretory products on nutrient cycling have been documented for various species and ecosystems, but temporal variation in these processes is poorly understood. We examined variation in excretion rates of a dominant grazing snail, Elimia clavaeformis, and its contribution to nutrient cycling, over the course of 14 months in a well-studied, low-nutrient stream (Walker Branch, east Tennessee, USA). Biomass-specific excretion rates of ammonium varied over twofold during the study, coinciding with seasonal changes in food availability (measured as gross primary production) and water temperature (multiple linear regression, R2 = 0.57, P = 0.053). The contribution of ammonium excretion to nutrient cycling varied with seasonal changes in both biological (that is, nutrient uptake rate) and physical (that is, stream flow) variables. On average, ammonium excretion accounted for 58% of stream water ammonium concentrations, 26% of whole-stream nitrogen demand, and 66% of autotrophic nitrogen uptake. Phosphorus excretion by Elimia was contrastingly low throughout the year, supplying only 1% of total dissolved phosphorus concentrations. The high average N:P ratio (89:1) of snail excretion likely exacerbated phosphorus limitation in Walker Branch. To fully characterize animal excretion rates and effects on ecosystem processes, multiple measurements through time are necessary, especially in ecosystems that experience strong seasonality.},
doi = {10.1007/s10021-014-9785-1},
journal = {Ecosystems},
number = 7,
volume = 17,
place = {United States},
year = {Thu Jun 19 00:00:00 EDT 2014},
month = {Thu Jun 19 00:00:00 EDT 2014}
}
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Works referenced in this record:
Can ungulates foraging in a multiple-use landscape alter forest nitrogen budgets?
journal, October 2003
- Seagle, Steven W.
- Oikos, Vol. 103, Issue 1
Seasonal patterns in streamwater nutrient and dissolved organic carbon concentrations: Separating catchment flow path and in-stream effects
journal, June 1997
- Mulholland, Patrick J.; Hill, Walter R.
- Water Resources Research, Vol. 33, Issue 6
Can ungulates foraging in a multiple-use landscape alter forest nitrogen budgets?
journal, October 2003
- Seagle, Steven W.
- Oikos, Vol. 103, Issue 1
Fish Distributions and Nutrient Cycling in Streams: can fish Create Biogeochemical Hotspots
journal, August 2008
- McIntyre, Peter B.; Flecker, Alexander S.; Vanni, Michael J.
- Ecology, Vol. 89, Issue 8
Impacts of an Invasive Snail (Tarebia granifera) on Nutrient Cycling in Tropical Streams: The Role of Riparian Deforestation in Trinidad, West Indies
journal, June 2012
- Moslemi, Jennifer M.; Snider, Sunny B.; MacNeill, Keeley
- PLoS ONE, Vol. 7, Issue 6
Physiological responses to stoichiometric constraints: nutrient limitation and compensatory feeding in a freshwater snail
journal, June 2006
- Fink, Patrick; Von Elert, Eric
- Oikos, Vol. 115, Issue 3
Phosphorus Dynamics in a Woodland Stream Ecosystem: A Study of Nutrient Spiralling
journal, October 1983
- Newbold, J. D.; Elwood, J. W.; O'Neill, R. V.
- Ecology, Vol. 64, Issue 5
Stoichiometry of nutrient recycling by vertebrates in a tropical stream: linking species identity and ecosystem processes
journal, March 2002
- Vanni, Michael J.; Flecker, Alexander S.; Hood, James M.
- Ecology Letters, Vol. 5, Issue 2
Nutrient release and ecological stoichiometry of freshwater mussels (Mollusca:Unionidae) in 2 small, regionally distinct streams
journal, June 2008
- Christian, Alan D.; Crump, Betty G.; Berg, David J.
- Journal of the North American Benthological Society, Vol. 27, Issue 2
Mollusca: Gastropoda
book, January 2001
- Brown, Kenneth M.
- Ecology and Classification of North American Freshwater Invertebrates
Release of Phosphorus by Certain Benthic Invertebrates
journal, August 1981
- Gardner, Wayne S.; Nalepa, Thomas F.; Quigley, Michael A.
- Canadian Journal of Fisheries and Aquatic Sciences, Vol. 38, Issue 8
Land use controls nutrient excretion by stream invertebrates along a gradient of agriculture
journal, September 2007
- James, Leah A. H.; Xenopoulos, Marguerite A.; Wilson, Henry F.
- Journal of the North American Benthological Society, Vol. 26, Issue 3
Interactions between sediment-feeders and microalgae on coral reefs: grazing losses versus production enhancement
journal, January 2001
- Uthicke, S.
- Marine Ecology Progress Series, Vol. 210
Phosphorus Spiralling in a Woodland Stream: Seasonal Variations
journal, June 1985
- Mulholland, Patrick J.; Newbold, J. Denis; Elwood, Jerry W.
- Ecology, Vol. 66, Issue 3
Streams in Mediterranean Climate Regions: Abiotic Influences and Biotic Responses to Predictable Seasonal Events
journal, November 1999
- Gasith, Avital; Resh, Vincent H.
- Annual Review of Ecology and Systematics, Vol. 30, Issue 1
Release of Phosphorus by Certain Benthic Invertebrates
journal, August 1981
- Gardner, Wayne S.; Nalepa, Thomas F.; Quigley, Michael A.
- Canadian Journal of Fisheries and Aquatic Sciences, Vol. 38, Issue 8
Role of the fish Astyanax aeneus (Characidae) as a keystone nutrient recycler in low-nutrient Neotropical streams
journal, February 2011
- Small, Gaston E.; Pringle, Catherine M.; Pyron, Mark
- Ecology, Vol. 92, Issue 2
Ammonium excretion by a symbiotic sponge supplies the nitrogen requirements of its rhodophyte partner
journal, November 2002
- Davy, Simon K.; Trautman, Donelle A.; Borowitzka, Michael A.
- Journal of Experimental Biology, Vol. 205, Issue 22
Fish Distributions and Nutrient Cycling in Streams: can fish Create Biogeochemical Hotspots
journal, August 2008
- McIntyre, Peter B.; Flecker, Alexander S.; Vanni, Michael J.
- Ecology, Vol. 89, Issue 8
Physiological responses to stoichiometric constraints: nutrient limitation and compensatory feeding in a freshwater snail
journal, June 2006
- Fink, Patrick; Von Elert, Eric
- Oikos, Vol. 115, Issue 3
Light, nutrients, and herbivore growth in oligotrophic streams
journal, February 2010
- Hill, Walter R.; Smith, John G.; Stewart, Arthur J.
- Ecology, Vol. 91, Issue 2
Secondary Production of Two Lotic Snails (Pleuroceridae:Elimia)
journal, September 1988
- Richardson, Terry D.; Scheiring, Joseph F.; Brown, Kenneth M.
- Journal of the North American Benthological Society, Vol. 7, Issue 3
The Ratio of Nitrogen to Phosphorus Resupplied by Herbivores: Zooplankton and the Algal Competitive Arena
journal, August 1990
- Sterner, Robert W.
- The American Naturalist, Vol. 136, Issue 2
The Limiting Role of Phosphorus in a Woodland Stream Ecosystem: Effects of P Enrichment on Leaf Decomposition and Primary Producers
journal, February 1981
- Elwood, Jerry W.; Newbold, J. Denis; Trimble, Ann F.
- Ecology, Vol. 62, Issue 1
Light Limitation in a Stream Ecosystem: Responses by Primary Producers and Consumers
journal, June 1995
- Hill, Walter R.; Ryon, Michael G.; Schilling, Elizabeth M.
- Ecology, Vol. 76, Issue 4
Long-term data reveal patterns and controls on stream water chemistry in a forested stream: Walker Branch, Tennessee
journal, August 2012
- Lutz, Brian D.; Mulholland, Patrick J.; Bernhardt, Emily S.
- Ecological Monographs, Vol. 82, Issue 3
Effect of a leaf-shredding invertebrate on organic matter dynamics and phosphorus spiralling in heterotrophic laboratory streams
journal, May 1985
- Mulholland, P. J.; Elwood, J. W.; Newbold, J. D.
- Oecologia, Vol. 66, Issue 2
Evidence that hyporheic zones increase heterotrophic metabolism and phosphorus uptake in forest streams
journal, May 1997
- Mulholland, Patrick J.; Marzolf, Erich R.; Webster, Jackson R.
- Limnology and Oceanography, Vol. 42, Issue 3
Exotic snails dominate nitrogen and carbon cycling in a highly productive stream
journal, October 2003
- Hall, Robert O.; Tank, Jennifer L.; Dybdahl, Mark F.
- Frontiers in Ecology and the Environment, Vol. 1, Issue 8
Periphyton Response to Longitudinal Nutrient Depletion in a Woodland Stream: Evidence of Upstream-Downstream Linkage
journal, December 1992
- Mulholland, Patrick J.; Rosemond, Amy D.
- Journal of the North American Benthological Society, Vol. 11, Issue 4
Seasonally shifting limitation of stream periphyton: response of algal populations and assemblage biomass and productivity to variation in light, nutrients, and herbivores
journal, January 2000
- Rosemond, Amy D.; Mulholland, Patrick J.; Brawley, Susan H.
- Canadian Journal of Fisheries and Aquatic Sciences, Vol. 57, Issue 1
Multiple Scales of Temporal Variability in Ecosystem Metabolism Rates: Results from 2 Years of Continuous Monitoring in a Forested Headwater Stream
journal, May 2007
- Roberts, Brian J.; Mulholland, Patrick J.; Hill, Walter R.
- Ecosystems, Vol. 10, Issue 4
Stoichiometry and population dynamics: Stoichiometry and population dynamics
journal, August 2004
- Andersen, Tom; Elser, James J.; Hessen, Dag O.
- Ecology Letters, Vol. 7, Issue 9
Controls on spatial and temporal variation of nutrient uptake in three Michigan headwater streams
journal, September 2007
- Hoellein, Timothy J.; Tank, Jennifer L.; Rosi-Marshall, Emma J.
- Limnology and Oceanography, Vol. 52, Issue 5
Role of the fish Astyanax aeneus (Characidae) as a keystone nutrient recycler in low-nutrient Neotropical streams
journal, February 2011
- Small, Gaston E.; Pringle, Catherine M.; Pyron, Mark
- Ecology, Vol. 92, Issue 2
Nutrient recycling by fish in streams along a gradient of agricultural land use: LAND USE AND NUTRIENT RECYCLING BY FISH
journal, December 2010
- Wilson, Henry F.; Xenopoulos, Marguerite A.
- Global Change Biology, Vol. 17, Issue 1
Respiration, calcification, and excretion of the invasive slipper limpet, Crepidula fornicata L.: Implications for carbon, carbonate, and nitrogen fluxes in affected areas
journal, September 2006
- Martin, Sophie; Thouzeau, Gérard; Chauvaud, Laurent
- Limnology and Oceanography, Vol. 51, Issue 5
Concepts and Methods for Assessing Solute Dynamics in Stream Ecosystems
journal, June 1990
- Workshop, Stream Solute
- Journal of the North American Benthological Society, Vol. 9, Issue 2
Are Snails Important Competitors in Stream Ecosystems?
journal, June 1987
- Hawkins, Charles P.; Furnish, Joseph K.
- Oikos, Vol. 49, Issue 2
Top-Down and Bottom-Up Control of Stream Periphyton: Effects of Nutrients and Herbivores
journal, June 1993
- Rosemond, Amy D.; Mulholland, Patrick J.; Elwood, Jerry W.
- Ecology, Vol. 74, Issue 4
Streams in Mediterranean Climate Regions: Abiotic Influences and Biotic Responses to Predictable Seasonal Events
journal, November 1999
- Gasith, Avital; Resh, Vincent H.
- Annual Review of Ecology and Systematics, Vol. 30, Issue 1
Biotic and abiotic controls on the ecosystem significance of consumer excretion in two contrasting tropical streams: N and P excretion by stream consumers
journal, June 2010
- Benstead, Jonathan P.; Cross, Wyatt F.; March, James G.
- Freshwater Biology, Vol. 55, Issue 10
Spatial and seasonal variation in nutrient excretion by benthic invertebrates in a eutrophic reservoir: Nutrient excretion by benthic invertebrates
journal, May 2002
- Devine, Jennifer A.; Vanni, Michael J.
- Freshwater Biology, Vol. 47, Issue 6
Multiple Sources and Forms of Nitrogen Sustain Year-Round Kelp Growth on the Inner Continental Shelf of the Santa Barbara Channel
journal, September 2013
- Brzezinksi, Mark; Reed, Daniel; Harrer, Shannon
- Oceanography, Vol. 26, Issue 3
Promotion of the Cycling of Diet-Enhancing Nutrients by African Grazers
journal, December 1997
- McNaughton, S. J.; Banyikwa, F. F.; McNaughton, M. M.
- Science, Vol. 278, Issue 5344
Agricultural land use alters the seasonality and magnitude of stream metabolism
journal, July 2013
- Griffiths, Natalie A.; Tank, Jennifer L.; Royer, Todd V.
- Limnology and Oceanography, Vol. 58, Issue 4
Does diet influence consumer nutrient cycling? Macroinvertebrate and fish excretion in streams
journal, March 2011
- McManamay, Ryan A.; Webster, Jackson R.; Valett, H. Maurice
- Journal of the North American Benthological Society, Vol. 30, Issue 1
Reconciling the temperature dependence of respiration across timescales and ecosystem types
journal, June 2012
- Yvon-Durocher, Gabriel; Caffrey, Jane M.; Cescatti, Alessandro
- Nature, Vol. 487, Issue 7408
Agricultural land use alters the seasonality and magnitude of stream metabolism
journal, July 2013
- Griffiths, Natalie A.; Tank, Jennifer L.; Royer, Todd V.
- Limnology and Oceanography, Vol. 58, Issue 4
Promotion of the Cycling of Diet-Enhancing Nutrients by African Grazers
journal, December 1997
- McNaughton, S. J.; Banyikwa, F. F.; McNaughton, M. M.
- Science, Vol. 278, Issue 5344
The effects of grazing by the snail, Lymnaea elodes, on benthic N2 fixation and primary production in oligotrophic, arctic lakes
journal, November 2007
- Gettel, Gretchen M.; Giblin, Anne E.; Howarth, Robert W.
- Limnology and Oceanography, Vol. 52, Issue 6
Role of brown bears ( Ursus arctos ) in the flow of marine nitrogen into a terrestrial ecosystem
journal, December 1999
- Hilderbrand, G. V.; Hanley, Thomas A.; Robbins, Charles T.
- Oecologia, Vol. 121, Issue 4
Stream ecosystem responses to the 2007 spring freeze in the southeastern United States: unexpected effects of climate change
journal, July 2009
- Mulholland, Patrick J.; Roberts, Brian J.; Hill, Walter R.
- Global Change Biology, Vol. 15, Issue 7
Stream Ecosystem Responses to Forest leaf Emergence in Spring
journal, August 2001
- Hill, Walter R.; Mulholland, Patrick J.; Marzolf, Erich R.
- Ecology, Vol. 82, Issue 8
The effect of grazing intensity on phosphorus spiralling in autotropic streams
journal, June 1983
- Mulholland, Patrick J.; Newbold, J. Denis; Elwood, Jerry W.
- Oecologia, Vol. 58, Issue 3
Nutrient recycling by two phosphorus-rich grazing catfish: the potential for phosphorus-limitation of fish growth
journal, August 2005
- Hood, James M.; Vanni, Michael J.; Flecker, Alexander S.
- Oecologia, Vol. 146, Issue 2
Nutrient Cycling by Animals in Freshwater Ecosystems
journal, November 2002
- Vanni, Michael J.
- Annual Review of Ecology and Systematics, Vol. 33, Issue 1
Stream ecosystem properties and processes along a temperature gradient
journal, January 2011
- Rasmussen, Jes Jessen; Baattrup-Pedersen, Annette; Riis, Tenna
- Aquatic Ecology, Vol. 45, Issue 2
Fish extinctions alter nutrient recycling in tropical freshwaters
journal, February 2007
- McIntyre, P. B.; Jones, L. E.; Flecker, A. S.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 11
Phosphorus-limited Daphnia: Intraspecific facilitation instead of competition
journal, July 1992
- Sommer, Ulrich
- Limnology and Oceanography, Vol. 37, Issue 5
Periphyton Response to Longitudinal Nutrient Depletion in a Woodland Stream: Evidence of Upstream-Downstream Linkage
journal, December 1992
- Mulholland, Patrick J.; Rosemond, Amy D.
- Journal of the North American Benthological Society, Vol. 11, Issue 4
Estimating autotrophic respiration in streams using daily metabolism data
journal, June 2013
- Hall, Robert O.; Beaulieu, Jake J.
- Freshwater Science, Vol. 32, Issue 2
The Stoichiometry of Consumer-Driven Nutrient Recycling: Theory, Observations, and Consequences
journal, April 1999
- Elser, James J.; Urabe, Jotaro
- Ecology, Vol. 80, Issue 3
Primary Production in Flowing Waters1
journal, April 1956
- Odum, Howard T.
- Limnology and Oceanography, Vol. 1, Issue 2
Effects of periphyton stoichiometry on mayfly excretion rates and nutrient ratios
journal, September 2008
- Rothlisberger, John D.; Baker, Michelle A.; Frost, Paul C.
- Journal of the North American Benthological Society, Vol. 27, Issue 3
Light Limitation in a Stream Ecosystem: Responses by Primary Producers and Consumers
journal, June 1995
- Hill, Walter R.; Ryon, Michael G.; Schilling, Elizabeth M.
- Ecology, Vol. 76, Issue 4
Nutrient recycling by two phosphorus-rich grazing catfish: the potential for phosphorus-limitation of fish growth
journal, August 2005
- Hood, James M.; Vanni, Michael J.; Flecker, Alexander S.
- Oecologia, Vol. 146, Issue 2
Seasonally shifting limitation of stream periphyton: response of algal populations and assemblage biomass and productivity to variation in light, nutrients, and herbivores
journal, January 2000
- Rosemond, Amy D.; Mulholland, Patrick J.; Brawley, Susan H.
- Canadian Journal of Fisheries and Aquatic Sciences, Vol. 57, Issue 1
Interactions between sediment-feeders and microalgae on coral reefs: grazing losses versus production enhancement
journal, January 2001
- Uthicke, S.
- Marine Ecology Progress Series, Vol. 210
Grazing and nutrient interactions in controlling the activity and composition of the epilithic algal community of an arctic lake1: Nutrients, snails, and algae
journal, January 1983
- Cuker, Benjamin E.
- Limnology and Oceanography, Vol. 28, Issue 1
Consumer-resource stoichiometry in detritus-based streams
journal, August 2003
- Cross, Wyatt F.; Benstead, Jonathan P.; Rosemond, Amy D.
- Ecology Letters, Vol. 6, Issue 8
Reconciling the temperature dependence of respiration across timescales and ecosystem types
journal, June 2012
- Yvon-Durocher, Gabriel; Caffrey, Jane M.; Cescatti, Alessandro
- Nature, Vol. 487, Issue 7408
Secondary Production of Two Lotic Snails (Pleuroceridae:Elimia)
journal, September 1988
- Richardson, Terry D.; Scheiring, Joseph F.; Brown, Kenneth M.
- Journal of the North American Benthological Society, Vol. 7, Issue 3
Importance of Terrestrial Arthropods as Subsidies in Lowland Neotropical Rain Forest Stream Ecosystems
journal, July 2012
- Small, Gaston E.; Torres, Pedro J.; Schweizer, Lauren M.
- Biotropica, Vol. 45, Issue 1
Role of Macroinvertebrates in Nitrogen Dynamics of a Desert Stream
journal, December 1988
- Grimm, Nancy B.
- Ecology, Vol. 69, Issue 6
Ammonium excretion by a symbiotic sponge supplies the nitrogen requirements of its rhodophyte partner
journal, November 2002
- Davy, Simon K.; Trautman, Donelle A.; Borowitzka, Michael A.
- Journal of Experimental Biology, Vol. 205, Issue 22
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A stream classification system to explore the physical habitat diversity and anthropogenic impacts in riverscapes of the eastern United States
journal, June 2018
- McManamay, Ryan A.; Troia, Matthew J.; DeRolph, Christopher R.
- PLOS ONE, Vol. 13, Issue 6
Egestion Versus Excretion: A Meta-Analysis Examining Nutrient Release Rates and Ratios across Freshwater Fauna
journal, October 2019
- Halvorson, Halvor M.; Atkinson, Carla L.
- Diversity, Vol. 11, Issue 10
Stream metabolism increases with drainage area and peaks asynchronously across a stream network
journal, December 2018
- Mejia, Francine H.; Fremier, Alexander K.; Benjamin, Joseph R.
- Aquatic Sciences, Vol. 81, Issue 1
Consumer-driven nutrient dynamics in freshwater ecosystems: from individuals to ecosystems: Consumer-driven nutrient dynamics in freshwater ecosystems
journal, December 2016
- Atkinson, Carla L.; Capps, Krista A.; Rugenski, Amanda T.
- Biological Reviews, Vol. 92, Issue 4
Contributions of freshwater mussels (Unionidae) to nutrient cycling in an urban river: filtration, recycling, storage, and removal
journal, September 2017
- Hoellein, Timothy J.; Zarnoch, Chester B.; Bruesewitz, Denise A.
- Biogeochemistry, Vol. 135, Issue 3
Biomass distribution of fishes and mussels mediates spatial and temporal heterogeneity in nutrient cycling in streams
journal, October 2018
- Hopper, Garrett W.; Gido, Keith B.; Vaughn, Caryn C.
- Oecologia, Vol. 188, Issue 4