Export of macroinvertebrate prey from tidal freshwater wetlands provides a significant energy subsidy for outmigrating juvenile salmon

Roegner, G. Curtis; Johnson, Gary E.

doi:10.1371/journal.pone.0282655

Export of macroinvertebrate prey from tidal freshwater wetlands provides a significant energy subsidy for outmigrating juvenile salmon

Journal Article · Fri Mar 17 00:00:00 EDT 2023 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0282655· OSTI ID:2471578

^[1]; Johnson, Gary E. ^[2]

National Oceanic and Atmospheric Administration (NOAA), Hammond, OR (United States). Point Adams Research Station
Pacific Northwest National Laboratory (PNNL), Portland, OR (United States). Coastal Sciences Division

Tidal freshwater wetlands linking terrestrial, riverine, and saline habitats are critical areas for material processing and exchange. Once historically widespread, herbaceous marsh and forested tidal freshwater wetlands especially are now highly degraded worldwide. Additionally, quantitative assessments of hydrology and material exchange from these systems are lacking compared to lotic and estuarine (saltmarsh) habitats. Here we investigate macroinvertebrate and energy export from tidal marsh and forested wetlands and consider potential benefits from this ecological process to endangered Pacific salmon in a large tidal freshwater system, the Columbia River (USA). Macroinvertebrate (salmon prey) concentration, water velocity, and discharge were measured at several wetland habitat types (forested swamp, emergent marsh, and restored marsh). We used these data to compute prey flux and transport metrics. Then, applying literature values to calculate prey energy equivalents and juvenile salmon metabolic requirements, we estimated the potential energy subsidy available to juvenile salmon. Numerically, larval stages of aquatic insects were the predominant type of prey exported from the wetlands, with Diptera chironomid fly abundance exceeding other groups. Energetically, however, non-chironomid dipterans and hemipteran prey comprised most of energy transport due to their higher energetic content (energy density × mean weight). We determined the prey energy transported from the sampled tidal channels was sufficient to meet energetic needs of tens to thousands of juvenile salmon per day, depending on prey production and hydrography. The prey taxonomic composition differed among organisms exiting forested swamp, emergent marsh, and restored marsh habitats with corresponding differences in energy transport, but all habitat types supported similar numbers of juvenile salmon. We conclude that macroinvertebrate prey exported from varied tidal freshwater wetlands likely provide significant benefits to juvenile salmon over a larger ecological footprint than the wetland area would suggest.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 2471578

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 3 Vol. 18; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (68)

Storm-driven particulate organic matter flux connects a tidal tributary floodplain wetland, mainstem river, and estuary Thom, Ronald M.; Breithaupt, Stephen A.; Diefenderfer, Heida L. Ecological Applications, Vol. 28, Issue 6 https://doi.org/10.1002/eap.1759	journal	July 2018
Evidence‐based evaluation of the cumulative effects of ecosystem restoration Diefenderfer, Heida L.; Johnson, Gary E.; Thom, Ronald M. Ecosphere, Vol. 7, Issue 3 https://doi.org/10.1002/ecs2.1242	journal	March 2016
Ecohydrology of wetland plant communities along an estuarine to tidal river gradient Borde, Amy B.; Diefenderfer, Heida L.; Cullinan, Valerie I. Ecosphere, Vol. 11, Issue 9 https://doi.org/10.1002/ecs2.3185	journal	September 2020
Inferring tidal wetland stability from channel sediment fluxes: Observations and a conceptual model Ganju, Neil K.; Nidzieko, Nicholas J.; Kirwan, Matthew L. Journal of Geophysical Research: Earth Surface, Vol. 118, Issue 4 https://doi.org/10.1002/jgrf.20143	journal	October 2013
Comparison of experimental and computational methods for discharge measurements from tidal wetlands Harding, Samuel F.; Coleman, André M.; Roegner, G. Curtis River Research and Applications, Vol. 36, Issue 9 https://doi.org/10.1002/rra.3709	journal	September 2020
Effects of Extreme Hydrologic Regimes on Juvenile Chinook Salmon Prey Resources and Diet Composition in a Large River Floodplain Goertler, Pascale; Jones, Kristopher; Cordell, Jeffery Transactions of the American Fisheries Society, Vol. 147, Issue 2 https://doi.org/10.1002/tafs.10028	journal	February 2018
Seasonal Variation, Export Dynamics and Consumption of Freshwater Invertebrates in an Estuarine Environment Williams, D. D.; Williams, N. E. Estuarine, Coastal and Shelf Science, Vol. 46, Issue 3 https://doi.org/10.1006/ecss.1997.0280	journal	March 1998
Hydrodynamic Control of the Supply of Suspended Chlorophyllato Infaunal Estuarine Bivalves Roegner, G. C. Estuarine, Coastal and Shelf Science, Vol. 47, Issue 3 https://doi.org/10.1006/ecss.1998.0351	journal	September 1998
Between Coastal Marshes and Coastal Waters — A Review of Twenty Years of Speculation and Research on the Role of Salt Marshes in Estuarine Productivity and Water Chemistry Nixon, Scott W. Estuarine and Wetland Processes https://doi.org/10.1007/978-1-4757-5177-2_20	book	January 1980
Size-dependent drift responses of mayflies to experimental hydrologic variation: active predator avoidance or passive hydrodynamic displacement? Poff, N. LeRoy; DeCino, R. D.; Ward, J. V. Oecologia, Vol. 88, Issue 4 https://doi.org/10.1007/BF00317723	journal	December 1991
Effects of trout on the diel periodicity of drifting in baetid mayflies Douglas, Paul L.; Forrester, Graham E.; Cooper, Scott D. Oecologia, Vol. 98, Issue 1 https://doi.org/10.1007/BF00326089	journal	June 1994
Estuarine influence on survival rates of coho (Oncorhynchus kisutch) and chinook salmon (Oncorhynchus tshawytscha) released from hatcheries on the U.S. Pacific coast Magnusson, A.; Hilborn, R. Estuaries, Vol. 26, Issue 4 https://doi.org/10.1007/BF02803366	journal	August 2003
Movements and food habits of striped bass ( Morone saxatilis ) in Delaware Bay (USA) salt marshes: comparison of a restored and a reference marsh Tupper, M.; Able, K. W. Marine Biology, Vol. 137, Issue 5-6 https://doi.org/10.1007/s002270000421	journal	December 2000
Movement patterns and feeding behavior of juvenile salmon (Oncorhynchus spp.) along armored and unarmored estuarine shorelines Heerhartz, Sarah M.; Toft, Jason D. Environmental Biology of Fishes, Vol. 98, Issue 6 https://doi.org/10.1007/s10641-015-0377-5	journal	January 2015
Habitat change in the lower Columbia River estuary, 1870–2009 Marcoe, Keith; Pilson, Stephen Journal of Coastal Conservation, Vol. 21, Issue 4 https://doi.org/10.1007/s11852-017-0523-7	journal	June 2017
Estuarine Habitat and Demographic Factors Affect Juvenile Chinook (Oncorhynchus tshawytscha) Growth Variability in a Large Freshwater Tidal Estuary Goertler, Pascale A. L.; Simenstad, Charles A.; Bottom, Daniel L. Estuaries and Coasts, Vol. 39, Issue 2 https://doi.org/10.1007/s12237-015-0002-z	journal	June 2015
Diel Behaviors of Zooplankton Interact with Tidal Patterns to Drive Spatial Subsidies in the Northern San Francisco Estuary Yelton, Rowan; Slaughter, Anne M.; Kimmerer, Wim J. Estuaries and Coasts, Vol. 45, Issue 6 https://doi.org/10.1007/s12237-021-01036-8	journal	February 2022
Effect of frequency of feeding on nitrogen and energy balance in rainbow trout under maintenance conditions Kaushik, Sadasivam J.; Gomes, Emidio F. Aquaculture, Vol. 73, Issue 1-4 https://doi.org/10.1016/0044-8486(88)90055-5	journal	October 1988
Nutrient partitioning in rainbow trout at different feeding rates Storebakken, T.; Hung, S. S. O.; Calvert, C. C. Aquaculture, Vol. 96, Issue 2 https://doi.org/10.1016/0044-8486(91)90149-2	journal	August 1991
Energy requirements, utilization and dietary supply to salmonids Kaushik, S. J.; Médale, F. Aquaculture, Vol. 124, Issue 1-4 https://doi.org/10.1016/0044-8486(94)90364-6	journal	July 1994
A geohydrologic continuum theory for the spatial and temporal evolution of marsh-estuarine ecosystems Dame, R.; Childers, D.; Koepfler, E. Netherlands Journal of Sea Research, Vol. 30 https://doi.org/10.1016/0077-7579(92)90046-H	journal	December 1992
Species composition, distribution, and invertebrate prey of fish assemblages in the Columbia River Estuary Bottom, Daniel L.; Jones, Kim K. Progress in Oceanography, Vol. 25, Issue 1-4 https://doi.org/10.1016/0079-6611(90)90009-Q	journal	January 1990
Between estuaries and the sea Dame, R. F.; Allen, D. M. Journal of Experimental Marine Biology and Ecology, Vol. 200, Issue 1-2 https://doi.org/10.1016/S0022-0981(96)02642-1	journal	November 1996
The tidal exchange of Callianassa californiensis (Crustacea, Decapoda) larvae between the ocean and the Salmon River estuary, Oregon Johnson, Gary E.; Gonor, J. J. Estuarine, Coastal and Shelf Science, Vol. 14, Issue 5 https://doi.org/10.1016/S0302-3524(82)80073-X	journal	May 1982
Ecological assessment criteria for restoring anadromous salmonid habitat in Pacific Northwest estuaries Simenstad, Charles A.; Cordell, Jeffery R. Ecological Engineering, Vol. 15, Issue 3-4 https://doi.org/10.1016/S0925-8574(00)00082-3	journal	July 2000
Temporal variability of hydrodynamics, sediment concentration and sediment settling velocity in a tidal creek Voulgaris, George; Meyers, Samuel T. Continental Shelf Research, Vol. 24, Issue 15 https://doi.org/10.1016/j.csr.2004.05.006	journal	October 2004
Restoration ecology: Ecological fidelity, restoration metrics, and a systems perspective Weinstein, Michael P.; Litvin, Steven Y.; Krebs, Justin M. Ecological Engineering, Vol. 65 https://doi.org/10.1016/j.ecoleng.2013.03.001	journal	April 2014
A spatially based area–time inundation index model developed to assess habitat opportunity in tidal–fluvial wetlands and restoration sites Coleman, André M.; Diefenderfer, Heida L.; Ward, Duane L. Ecological Engineering, Vol. 82 https://doi.org/10.1016/j.ecoleng.2015.05.006	journal	September 2015
Indexing habitat opportunity for juvenile anadromous fishes in tidal-fluvial wetland systems Curtis Roegner, G.; Johnson, Gary E.; Coleman, André M. Ecological Indicators, Vol. 124 https://doi.org/10.1016/j.ecolind.2021.107422	journal	May 2021
Marshes as sources or sinks of an estuarine mysid: demographic patterns and tidal flux of Neomysis kadiakensis at China Camp marsh, San Francisco estuary Dean, Amy F.; Bollens, Stephen M.; Simenstad, Charles Estuarine, Coastal and Shelf Science, Vol. 63, Issue 1-2 https://doi.org/10.1016/j.ecss.2004.08.019	journal	April 2005
Hydrodynamic modelling of tidal-fluvial flows in a large river estuary Sandbach, S. D.; Nicholas, A. P.; Ashworth, P. J. Estuarine, Coastal and Shelf Science, Vol. 212 https://doi.org/10.1016/j.ecss.2018.06.023	journal	November 2018
An expert panel process to evaluate habitat restoration actions in the Columbia River estuary Krueger, Kirk L.; Bottom, Daniel L.; Hood, W. Gregory Journal of Environmental Management, Vol. 188 https://doi.org/10.1016/j.jenvman.2016.11.028	journal	March 2017
Density of red alder (Alnus rubra) in headwaters influences invertebrate and detritus subsidies to downstream fish habitats in Alaska Wipfli, Mark S.; Musslewhite, Jake Hydrobiologia, Vol. 520, Issue 1-3 https://doi.org/10.1023/B:HYDR.0000027734.95586.24	journal	June 2004
Impacts of Columbia River discharge on salmonid habitat: 2. Changes in shallow-water habitat Kukulka, Tobias Journal of Geophysical Research, Vol. 108, Issue C9 https://doi.org/10.1029/2003JC001829	journal	January 2003
The Role of the Upper Tidal Estuary in Wetland Blue Carbon Storage and Flux Krauss, Ken W.; Noe, Gregory B.; Duberstein, Jamie A. Global Biogeochemical Cycles, Vol. 32, Issue 5 https://doi.org/10.1029/2018GB005897	journal	May 2018
Floodplain Wetland Channel Planform, Cross‐Sectional Morphology, and Sediment Characteristics Along an Estuarine to Tidal River Gradient Diefenderfer, Heida L.; Borde, Amy B.; Cullinan, Valerie I. Journal of Geophysical Research: Earth Surface, Vol. 126, Issue 5 https://doi.org/10.1029/2019JF005391	journal	May 2021
A Comprehensive Estuarine Dissolved Organic Carbon Budget Using an Enhanced Biogeochemical Model Clark, J. B.; Long, W.; Hood, R. R. Journal of Geophysical Research: Biogeosciences, Vol. 125, Issue 5 https://doi.org/10.1029/2019JG005442	journal	May 2020
Export of invertebrates and detritus from fishless headwater streams in southeastern Alaska: implications for downstream salmonid production Wipfli, Mark S.; Gregovich, David P. Freshwater Biology, Vol. 47, Issue 5 https://doi.org/10.1046/j.1365-2427.2002.00826.x	journal	May 2002
Quantifying macrodetritus fluxes from a small temperate estuary Gladstone-Gallagher, Rebecca V.; Sandwell, Dean R.; Lohrer, Andrew M. Marine and Freshwater Research, Vol. 68, Issue 12 https://doi.org/10.1071/MF16408	journal	January 2017
Reciprocal subsidies: Dynamic interdependence between terrestrial and aquatic food webs Nakano, S.; Murakami, M. Proceedings of the National Academy of Sciences, Vol. 98, Issue 1 https://doi.org/10.1073/pnas.98.1.166	journal	January 2001
Density and Condition of Subyearling Chinook Salmon in the Lower Columbia River and Estuary in Relation to Water Temperature and Genetic Stock of Origin Roegner, G. Curtis; Teel, David J. Transactions of the American Fisheries Society, Vol. 143, Issue 5 https://doi.org/10.1080/00028487.2014.918055	journal	July 2014
Foraging and Growth Potential of Juvenile Chinook Salmon after Tidal Restoration of a Large River Delta David, Aaron T.; Ellings, Christopher S.; Woo, Isa Transactions of the American Fisheries Society, Vol. 143, Issue 6 https://doi.org/10.1080/00028487.2014.945663	journal	September 2014
Tidal exchange of larvae ofSesarma catenata(Decapoda, Brachyura) in the Swartkops estuary, South Africa Pereyra Lago, R. South African Journal of Zoology, Vol. 28, Issue 4 https://doi.org/10.1080/02541858.1993.11448316	journal	January 1993
Comparative Use of Shallow and Deepwater Habitats by Juvenile Pacific Salmon in the Columbia River Estuary Prior to Ocean Entry Roegner, G. Curtis; Weitkamp, Laurie A.; Teel, David J. Marine and Coastal Fisheries, Vol. 8, Issue 1 https://doi.org/10.1080/19425120.2016.1227889	journal	January 2016
Transport of molluscan larvae through a shallow estuary Roegner, G. C. Journal of Plankton Research, Vol. 22, Issue 9 https://doi.org/10.1093/plankt/22.9.1779	journal	September 2000
Distribution and feeding of juvenile Pacific salmon in freshwater tidal creeks of the lower Fraser River, British Columbia Levings, C. D.; Boyle, D. E.; Whitehouse, T. R. Fisheries Management and Ecology, Vol. 2, Issue 4 https://doi.org/10.1111/j.1365-2400.1995.tb00121.x	journal	December 1995
Determination of the energy requirements of fish with particular reference to salmonids Cho, C. Young; Bureau, D. P. Journal of Applied Ichthyology, Vol. 11, Issue 3-4 https://doi.org/10.1111/j.1439-0426.1995.tb00015.x	journal	December 1995
Ecological Linkages Between Headwaters and Downstream Ecosystems: Transport of Organic Matter, Invertebrates, and Wood Down Headwater Channels1: Ecological Linkages Between Headwaters and Downstream Ecosystems Wipfli, Mark S.; Richardson, John S.; Naiman, Robert J. JAWRA Journal of the American Water Resources Association, Vol. 43, Issue 1 https://doi.org/10.1111/j.1752-1688.2007.00007.x	journal	January 2007
Metabolic rate in fishes: definitions, methods and significance for conservation physiology Chabot, D.; McKenzie, D. J.; Craig, J. F. Journal of Fish Biology, Vol. 88, Issue 1 https://doi.org/10.1111/jfb.12873	journal	January 2016
Estimation of salmonid habitat growth potential through measurements of invertebrate food abundance and temperature Weber, Nicholas; Bouwes, Nicolaas; Jordan, Chris E. Canadian Journal of Fisheries and Aquatic Sciences, Vol. 71, Issue 8 https://doi.org/10.1139/cjfas-2013-0390	journal	August 2014
Causes and consequences of invertebrate drift in running waters: from individuals to populations and trophic fluxes Naman, Sean M.; Rosenfeld, Jordan S.; Richardson, John S. Canadian Journal of Fisheries and Aquatic Sciences, Vol. 73, Issue 8 https://doi.org/10.1139/cjfas-2015-0363	journal	August 2016
Hot eats and cool creeks: juvenile Pacific salmonids use mainstem prey while in thermal refuges Brewitt, Kimberly S.; Danner, Eric M.; Moore, Jonathan W. Canadian Journal of Fisheries and Aquatic Sciences, Vol. 74, Issue 10 https://doi.org/10.1139/cjfas-2016-0395	journal	October 2017
Floodplain rearing of juvenile chinook salmon: evidence of enhanced growth and survival Sommer, T. R.; Nobriga, M. L.; Harrell, W. C. Canadian Journal of Fisheries and Aquatic Sciences, Vol. 58, Issue 2 https://doi.org/10.1139/f00-245	journal	February 2001
Influence of streamside vegetation on inputs of terrestrial invertebrates to salmonid food webs Allan, J. David; Wipfli, Mark S.; Caouette, John P. Canadian Journal of Fisheries and Aquatic Sciences, Vol. 60, Issue 3 https://doi.org/10.1139/f03-019	journal	March 2003
Scope for Metabolism and Growth of Sockeye Salmon, Oncorhynchus nerka, and Some Related Energetics Brett, J. R. Journal of the Fisheries Research Board of Canada, Vol. 33, Issue 2 https://doi.org/10.1139/f76-046	journal	February 1976
Invertebrate drift and longitudinal transport processes in streams Lancaster, J.; Hildrew, A. G.; Gjerlov, C. Canadian Journal of Fisheries and Aquatic Sciences, Vol. 53, Issue 3 https://doi.org/10.1139/f95-217	journal	March 1996
Terrestrial invertebrates as salmonid prey and nitrogen sources in streams: contrasting old-growth and young-growth riparian forests in southeastern Alaska, U.S.A. Wipfli, Mark S. Canadian Journal of Fisheries and Aquatic Sciences, Vol. 54, Issue 6 https://doi.org/10.1139/f97-034	journal	June 1997
WETLAND RESOURCES: Status, Trends, Ecosystem Services, and Restorability Zedler, Joy B.; Kercher, Suzanne Annual Review of Environment and Resources, Vol. 30, Issue 1 https://doi.org/10.1146/annurev.energy.30.050504.144248	journal	November 2005
Fluxes of water, sediments, and biogeochemical compounds in salt marshes Fagherazzi, Sergio; Wiberg, Patricia L.; Temmerman, Stijn Ecological Processes, Vol. 2, Issue 1 https://doi.org/10.1186/2192-1709-2-3	journal	February 2013
Insights into estuary habitat loss in the western United States using a new method for mapping maximum extent of tidal wetlands Brophy, Laura S.; Greene, Correigh M.; Hare, Van C. PLOS ONE, Vol. 14, Issue 8 https://doi.org/10.1371/journal.pone.0218558	journal	August 2019
Zooplankton Dynamics in the Cache Slough Complex of the Upper San Francisco Estuary No authors listed San Francisco Estuary and Watershed Science, Vol. 16, Issue 3 https://doi.org/10.15447/sfews.2018v16iss3art4	journal	October 2018
Linking Ecosystems, Food Webs, and Fish Production: Subsidies in Salmonid Watersheds Wipfli, Mark S.; Baxter, Colden V. Fisheries, Vol. 35, Issue 8 https://doi.org/10.1577/1548-8446-35.8.373	journal	August 2010
Juvenile Salmonid Use of Reconnected Tidal Freshwater Wetlands in Grays River, Lower Columbia River Basin Roegner, G. Curtis; Dawley, Earl W.; Russell, Micah Transactions of the American Fisheries Society, Vol. 139, Issue 4 https://doi.org/10.1577/T09-082.1	journal	July 2010
The Network Dynamics Hypothesis: How Channel Networks Structure Riverine Habitats Benda, Lee; Poff, N. Leroy; Miller, Daniel BioScience, Vol. 54, Issue 5 https://doi.org/10.1641/0006-3568(2004)054[0413:TNDHHC]2.0.CO;2	journal	January 2004
Mechanistic effects of low-flow hydrology on riverine ecosystems: ecological principles and consequences of alteration Rolls, Robert J.; Leigh, Catherine; Sheldon, Fran Freshwater Science, Vol. 31, Issue 4 https://doi.org/10.1899/12-002.1	journal	December 2012
The Ecological Role of Zooplankton in a Long Island Salt Marsh Carlson, Douglas M. Estuaries, Vol. 1, Issue 2 https://doi.org/10.2307/1351596	journal	June 1978
Foraging and Growth Potential of Juvenile Chinook Salmon after Tidal Restoration of a Large River Delta Takekawa, John Y.; David, Aaron T.; Ellings, Christopher S. Figshare https://doi.org/10.6084/m9.figshare.c.2018291.v1	collection	January 2015
How effective are created or restored freshwater wetlands for nitrogen and phosphorus removal? A systematic review Land, Magnus; Granéli, Wilhelm; Grimvall, Anders figshare https://doi.org/10.6084/m9.figshare.c.3628610.v1	collection	January 2016

Similar Records

Indexing habitat opportunity for juvenile anadromous fishes in tidal-fluvial wetland systems

Journal Article · Sat May 01 00:00:00 EDT 2021 · Ecological Indicators · OSTI ID:1763357

An Ecosystem-Based Approach to Habitat Restoration Projects with Emphasis on Salmonids in the Columbia River Estuary, 2003 Technical Report.

Technical Report · Fri Oct 31 23:00:00 EST 2003 · OSTI ID:962127

Salmon Life Histories, Habitat, and Food Webs in the Columbia River Estuary: An Overview of Research Results, 2002-2006.

Technical Report · Fri Aug 01 00:00:00 EDT 2008 · OSTI ID:941582

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
aquatic insects
bioenergetics
insects
marshes
rivers
salmon
tides
wetlands

Export of macroinvertebrate prey from tidal freshwater wetlands provides a significant energy subsidy for outmigrating juvenile salmon

Citation Formats

References (68)

Similar Records

Related Subjects